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Neotropical Primates A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group Conservation International 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA ISSN 1413-4703 Abbreviation: Neotrop. Primates Editors Erwin Palacios, Conservacin Internacional Colombia, Bogot DC, Colombia Liliana Corts Ortiz, Museum of Zoology, University of Michigan, Ann Arbor, MI, USA Jlio Csar Bicca-Marques, Pontifcia Universidade Catlica do Rio Grande do Sul, Porto Alegre, Brasil Eckhard Heymann, Deutsches Primatenzentrum, Gttingen, Germany Jessica Lynch Alfaro, Institute for Society and Genetics, University of California-Los Angeles, Los Angeles, CA, USA Liza Veiga, Museu Paraense Emlio Goeldi, Belm, Brazil New s and Books Reviews Brenda Solrzano, Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mxico Ernesto Rodrguez-Luna, Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mxico Founding Editors Anthony B. Rylands, Center for Applied Biodiversity Science Conservation International, Arlington VA, USA Ernesto Rodrguez-Luna, Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mxico Editorial Board Bruna Bezerra, University of Louisville, Louisville, KY, USA Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK Adelmar F. Coimbra-Filho, Academia Brasileira de Cincias, Rio de Janeiro, Brazil Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA Stephen F. Ferrari, Universidade Federal do Sergipe, Aracaj, Brazil Russell A. Mittermeier, Conservation International, Arlington, VA, USA Marta D. Mudry, Universidad de Buenos Aires, Argentina Anthony Rylands, Conservation International, Arlington, VA, USA Horcio Schneider, Universidade Federal do Par, Campus Universitrio de Bragana, Brazil Karen B. Strier, University of Wisconsin, Madison, WI, USA Maria Emlia Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil Primate Specialist Group Chairman, Russell A. Mittermeier Deputy Chair, Anthony B. Rylands Coordinator, Special Section on Great Apes, Liz Williamson Regional Coordinators Neotropics Mesoamerica, Liliana Corts -Ortiz Andean Countries, Erwin Palacios and Eckhard W. Heymann Brazil and the Guianas, M. Ceclia M. Kierul, Mauricio Talebi and Fabiano R. de Melo Regional Coordinators Africa West Africa John F. Oates East Africa, David Mbora Regional Coordinator Madagascar Jrg U. Ganzhorn Regional Coordinators Asia China, Long Yongcheng Southeast Asia, Jatna Supriatna and Christian Roos South Asia, Sally Walker Layout: Kim Meek, Washington, DC
1 A THE ECOLOGY OF TRUNK-TO-TRUNK LEAPING IN SAGUINUS FUSCICOLLI S : IMPLICATIONS FOR UNDERSTANDING LOCOMOTOR DIVERSITY IN CALLITRICHINES P. A. Garber 1,4 A. C. McKenney 2 and E. K. Mallott 1 1 Department of Anthropology, University of Illinois, Urbana, Illinois 61801 USA 2 Academic Professional, Department of Anthropology, University of Illinois 3 Editorial Assistant, American Journal of Primatology, Urbana, Illinois 61891 4 Corresponding Author: Paul A. Garber, Department of Anthropology, University of Illinois, Urbana, Illinois 61801, email@example.com, (217) 333-3616 (phone), (217) 244-3490 (FAX) Abstract Several species of callitrichines (tamarins, marmosets, and callimicos) are reported to frequently leap between vertical sup ports when foraging and traveling in the forest understory. In the present study, we examine trunk-to-trunk leaping in a wild group of four habituated adult saddleback tamarins ( Saguinus fuscicollis weddelli ) in northern Bolivia. From June through July, 2011 we analyzed 200 leaps in which the tamarins moved between vertical supports. On average, takeo height was 4.1 m (.3 m, range 1-7.5 m). During the airborne phase of travel the monkeys lost an average of 0.5 m (.5 m) at contact with the landing support, and the mean distance leapt was 1.4 m ( 0.7 m). We found no correlation between the diameter at breast height (DBH) of landing and takeo supports, and either the distance leapt or height gained/lost during leaping. Across callitrichine taxa, it appears that ecological distinctions in diet, patterns of habitat utilization, and predator avoidance strategies have played an important role in understanding the frequency and context of trunk-to-trunk leaping behavior. Keywords : Tamarins, marmosets, positional behavior, vertical clinging and leaping, habitat utilization Resumen Muchas especies de callitrichinos (tamarinos, tits, y callimicos) se caracterizan por saltar frecuentemente entre substratos verticales durante el forrajeo y los desplazamientos en el sotobosque. En este estudio, examinamos los saltos de tronco a tronco en un grupo habituado de cuatro tamarinos de cabeza amarilla silvestres ( Saguinus fuscicollis weddelli ) en el norte de Bolivia. Durante junio y julio 2011 analizamos 200 saltos de los tamarinos entre substratos verticales. El promedio de la altura de despegue fue 4.1 m (.3 m, rango 1-7.5 m). En la fase area del salto, los individuos perdieron un promedio 0.5 m (.5 m) de altura al llegar al rea de aterrizaje y la distancia promedio saltada fue 1.4 m ( 0.7 m). No encontramos ninguna correlacin entre el dimetro a la altura del pecho (DAP) de los substratos de despegue y aterrizaje, y la distancia saltada o la altura ganada/perdida durante el salto. Las diferencias ecolgicas en la dieta, los patrones de uso de hbitat y las estrategias para evitar la depredacin, parecen haber jugado un papel importante para entender la frecuencia y el contexto del comportamiento de salto de tronco a tronco en los diferentes taxa de callitrichinos. Palabras clave : Tamarinos, tits, comportamiento postural, salto desde y abrazarse a soportes verticales, utilizacin del hbitat Introduction Several species of primates including strepsirhines, tarsiers, Pithecia pithecia, and callitrichines are commonly report ed to leap between vertical and/or sharply inclined sup ports when foraging and traveling in the forest understory (Garber 1991; Demes et al., 1995, 1999; Walker 1998; Youlatos, 1999, 2009; Garber and Leigh, 2001, Cromp ton et al., 2010). Traditionally, researchers have described this pattern of positional behavior as vertical clinging and leaping (Napier and Walker, 1967; Kinzey et al., 1975; Gebo, 2011). From a functional perspective, vertical cling ing and leaping is composed of two component behaviors: vertical clinging in which an individual adopts a relatively stable upright posture on a trunk or other vertical support, either by grasping the support with their hands and feet or by embedding their claw-like nails into the bark, and leaping between vertical supports which requires power ful and rapid hindlimb extension and propulsion during takeo, orientation of the body at a subvertical or inclined
2 angle (45 represents the ballistic optimum, Crompton et al., 2010), and an ability to absorb large compressive forces when landing on a noncompliant substrate (Demes et al., 1995; Garber et al., 2009). Given that clinging to a verti cal support and leaping between vertical supports represent two distinct modes of positional behavior, we refer to leap ing between vertical supports as trunk-to-trunk leaping. In this paper we present data on trunk-to-trunk leaping in Weddells saddleback tamarin, Saguinus fusciciollis weddelli in northwestern Bolivia. Field studies indicate that between 20-89% of leaping in S. fuscicollis involves movement to and from vertical supports (Table 1). Saddleback tamarins are the smallest tamarin species, are characterized by fore limb elongation, in particular the distal segments, and pos sess the highest intermembral index (IMI or the ratio of forelimb length to hindlimb length) among members of the genus Saguinus (Falsetti and Cole, 1992; Garber and Leigh, 2001; Davis, 2002). Among callitrichines, trunk-to-trunk leaping is reported to be a major component of the locomo tor repertoire in Callimico goeldii (callimicos) (Garber and Leigh, 2001; Garber and Porter, 2009), Cebuella pygmaea (pygmy marmosets) (Kinzey et al., 1976; Youlatos (1999, 2009), S. fuscicollis (saddleback tamarins) (Garber, 1991; Garber and Leigh, 2001; Nyakatura and Heymann 2010) and Saguinus tripartitus (golden-mantled tamarins) (You latos, 1999) (Table 1). Given dierences among these taxa in body mass (adult female body mass: C. goeldii 468gm, S fuscicollis 358gm, C. pygmaea 122gm, body mass data for wild S. tripartitus are not available; Smith and Jungars (1997), foreand hindlimb proportions (IMI in C. goel dii :70.6, S. fuscicolli s : 77.1, C. pygmaea : 82.3, no data are available for S. tripartitus ; Davis, 2002), patterns of habitat utilization, and feeding ecology (e.g., bamboo fungi are a dietary staple for C. goeldii trunk exudates are a dietary staple for C. pygmaea and insects, ripe fruits, exudates, and oral nectar are critical components of the diet of S. fus cicollis and S. tripartitus reviewed in Digby et al. 2011), we anticipate signicant dierences in the frequency and context of trunk-to-trunk leaping and the use of trunks as a foraging substrate (Garber et al. 2009). Table 1. Frequency of trunk-to-trunk leaping during travel in callitrichine primates. Species Trunk-to trunk leaps (% of locomotor samples) Trunk-to-trunk leaps (% of all leaps) Reference Saguinus fuscicollis nigrifrons 1 38.4 89.2 Nyakatura and Heymann 2010 Saguinus fuscicollis nigrifrons 24.0 54.5 Norconk 1986 Saguinus fuscicollis nigrifrons 20.8 39.7 Castro 1991 Saguinus fuscicollis nigrifrons 6.1 20.7 Garber 1991 Saguinus fuscicollis weddelli 11.1 67.5 Porter 2004 Saguinus fuscicollis weddelli 6.7 20.0 Garber and Leigh 2001 Saguinus tripartitus 5.8 17.5 Youlatos 1999 Saguinus georoyi 1.6 3.8 Garber 1991 Saguinus midas 1.9 7.3 Youlatos unpub. data Saguinus mystax 2 8.2 58.9 Nyakatura and Heymann 2010 Saguinus mystax 2.7 8.8 Garber 1991 Saguinus labiatus 2.8 8.4 Garber and Leigh 2001 Saguinus labiatus 2.3 10.9 Porter 2004 Leontopithecus rosalia 3 2.8 8.9 Staord et al. 1996 Callimico goeldii 23.1 55.1 Garber and Leigh 2001 Callimico goeldii 47.4 88.6 Porter 2004 Callithrix jacchus 4 0.6 2.9 Youlatos unpub. data Cebuella pygmaea 12.9 35.1 Youlatos 1999 Cebuella pygmaea 15.3 36.7 Youlatos 2009 1 Data from this study of S. fuscicollis nigrifrons were extrapolated based on Table 1 and Figure 1 from Nyakatura and Heymann (2010). ese authors do not provide quantitative data on both takeo and landing platform orientation during leaping but state almost all leaps were associated with vertical clinging and leaping behavior (page 246). 2 Data from this study of S. mystax were extrapolated based on Table 1 and Figure 1 from Nyakatura and Heymann (2010). ese authors do not provide quantitative data on both takeo and landing platform orientation during leaping but state Leaps occurred mostly on vertical inclines from trunk to trunk (vertical clinging and leaping behavior), but were also observed on other inclines, often connecting terminal branches of dierent trees. S. mystax displayed much less vertical clinging and leaping than S. fuscicollis (page 246). 3 Data for wild Leonopitheucs rosalia were extrapolated from data presented in Figure 4 and Table 5 from Staord et al. (1996) and include leaps in which trunks were used either as landing or takeo platforms. 4 -Data for Callithrix jacchus based on preliminary observations of a semi-natural group inhabiting the Botanical Gardens, Rio de Janeiro, Brazil.
3 Methods During June and July, 2011, we collected behavioral and ecological data on a group of four adult saddleback tama rins ( S. fuscicollis weddelli three adult males and one adult female) inhabiting a mixture of primary forest, matur ing secondary forest, bamboo forest, disturbed secondary forest, and stream edge forest in the Department of the Pando in northern Bolivia (Camp Callimico, 11'S, 69'W). is area of the Amazon Basin experiences pro nounced dry and rainy seasons (with rainfall averaging ap proximately 2,000 mm per year, Porter, 2001). On 7 of 22 full-day follows, we opportunistically recorded a total of 200 trunk-to-trunk leaps. Our study group of saddleback tamarins was fully habituated to the presence of observers, and had been the focus of previous studies in 2008 and 2009 (Porter and Garber, 2011). To ensure that our presence had a negligible eect on tamarin locomotor behavior or the distance leapt, we followed the monkeys daily for a period of two weeks prior to collecting data on leaping. For each leap the following information was col lected: takeo and landing height, the horizontal distance leapt, support type, height gained or height lost during travel, and diameter at breast height (DBH) of takeo and landing supports. All measurements were taken immedi ately after we observed the tamarin to leap. Takeo height and landing height were estimated by placing a 1.5 m tape on the substrate for scale. Height gain or height loss during a leap was calculated as takeo height minus land ing height. However to be conservative, in our analyses we consider height gains or height losses of .25 m to reect horizontal travel (no eective change in height). DBH was measured using a metric tape. Takeo and landing supports were scored either as tree trunk, liana, or woody bamboo. All vertical supports leapt to and from were considered in our analysis (we did not have a size threshold). e horizontal distance leapt was calculated by measuring the distance between the landing and takeo supports using a metric tape. Finally, a support was considered compliant if we could detect it to move or be displaced during a tamarin leap. We acknowledge that this is a highly qualitative measure of support compliance. In order to examine whether the distribution of substrate type, DBH, and inter-tree distances within the study groups home range inuenced tamarin support preference and leaping behavior, we walked two 100 2 meter tran sects running east-west between marked trails and measured every vertical support with a DBH >2.5 cm and a height of >2.0 m that was present inside the transect (N=406) (West, 2004). At every 20 th support (N=20 target trees), we marked an area that formed a semicircle with a radius of 3 meters with the target tree at the midline of its base. We then counted the number and measured the DBH of vertical lianas, trunks, and bamboo culms that were located within the 9.42 m 2 area (total area sampled for 20 target trees was 188.4 m 2 ). For each vertical support present in the semicircle (total = 71) we also measured the horizontal distance from the midpoint of the base of the semicircle to each tree (distance between focal tree and sample tree). We selected a radius of 3 meters because approximately 94% of trunk-to-trunk leaps in saddleback tamarins were less than 3 meters in horizontal distance (see Results). Given that the data were not normally distributed, com parisons between the DBH of takeo and landing sup ports were made using the nonparametric Mann-Whitney U-test. Comparisons between the DBH of vertical sup ports in our sample transects and the DBH of supports used by the tamarins for leaping also were evaluated using a Mann-Whitney U-test. Variance in the size of takeo and landing supports was compared using an F-Test. e eects of takeo support DBH, landing support DBH, and the distance leapt on height gained/lost during leaping were analyzed using multiple regression analysis, as were the ef fects of the takeo support DBH, landing support DBH, and height lost/gained during leaping on the horizontal distance leapt (SAS v9.3, SAS Institute, 2011). Probability values of p.05 are considered signicant. Results Support type and support diameter Saddleback tamarins commonly foraged and traveled on tree trunks in the forest understory. We did not observe the tamarins to leap between vertical branches in the middle or upper levels of the tree crown. Trunks were used as both takeo and landing supports in approximately 90% of leaps. Areas of bamboo forest were uncommon in the study groups home range and bamboo culms accounted for less than 0.25% of vertical supports present in our sample tran sects. We did not observe the tamarins to leap to or from bamboo culms. Lianas accounted for 14% (57/407) of the vertical supports present in our vegetation transects, how ever, they were used by the tamarins as takeo supports during only 7.5% of leaps (X 2 =6.0, df=1, p<.05) and as landing supports in 10% of leaps (X 2 =2.2 df=1, p>.20). We found that in 7 of 15 leaps in which lianas served as takeo supports, the liana moved or was displaced by the leaping tamarin. In each case the liana had a DBH of 5 cm. In 7 of 20 leaps in which lianas served as a landing support, the liana also was compliant. In each of these cases the liana had a DBH of 5 cm (however, there were two instances in which the tamarins landed on a liana with a DBH 5 cm and the support was judged not to be compliant. Tree trunks were rarely compliant; 1.0% of takeo and 2.7% of landing supports). Overall, lianas were signicantly smaller in diameter than were tree trunks (lianas =5.48 2.8 cm DBH; range 2.5-16.2 cm vs. tree trunks =11.3 12.6 cm DBH; range 2.5-103.5 cm; Mann-Whitney U-test, Z=5.57, p<.0001), and this may have aected the tamarins use of lianas as leaping supports. As indicated in Fig. 1, tamarins used vertical supports of less than 5 cm DBH as either take o (X 2 =30.0, df=1, p<.001) or landing supports (X 2 =25.3, df=1, p<.001) less frequently than expected based on their
4 availability. In contrast, the monkeys exhibited a prefer ence for leaping to and from supports of between 10-20 cm DBH (X 2 =26.4, df=1, p<.001 for takeo support; X 2 =19.9, df=1, p<.001 for landing support). Overall, we found no signicant dierence between the mean DBH of takeo (15.7 cm 16.3) and landing supports (15.2 cm 17.8; Mann-Whitney U-test, Z= 1.21, p=0.22) selected by the tamarins. Height gained/height lost During 200 trunk-to-trunk leaps, the height of the tama rins takeo support ranged from 7.5m to 1m above the ground. Mean takeo height was 4.1 m (.3 m). During 30% of takeos the tamarins were positioned at a height of between 4-5m and during 30% of the landings the tamarins were positioned at a height of between 3-4 m. (Table 2). During their airborne phase of travel, the mon keys experienced a loss in height during 121 leaps (60.5%), retained a relatively horizontal trajectory during 70 leaps (35%), and gained height during only 9 leaps (4.5%). e greatest vertical distance lost during a leap was 2.2 m and the greatest gained was 0.7 m. On average, the saddleback tamarins lost 0.5 m (.5 m) in height when leaping be tween vertical supports. During all trunk-to-trunk leaps, saddleback tamarins landed forelimbs rst, a behavioral pattern which is consistent across callitrichines. Distance leapt e average horizontal distance leapt by the tamarins was 1.4 m ( 0.7), with the greatest number of leaps spanning a distance of 1-2m (51.5%) (Table 3). In our sample, 9.5% of leaps were <0.5m in distance and 2.0% spanned a dis tance of greater than 3 meters (Table 3). Given that our measure of horizontal distance leapt was identical to the way we measured the spatial distribution of vertical sup ports in our sample plots, we compared these data sets to determine whether the tamarins selected nearer or further vertical supports for leaping. We found that the horizontal distance leapt by the tamarins between vertical supports diered signicantly from the spatial distribution of these supports in our focal transects (1.90 0.84 m; N=71; Mann-Whitney U-test, Z=4.17, p<.0001). ese data sug gest that given the option of leaping between nearer or more distant vertical supports, especially those separated by a distance of approximately 2 meters, saddleback tamarins preferred to jump to and from nearer supports. Finally, using multiple regression we examined the eects of support DBH and height gained or lost on distance leapt. e multiple regression analysis for height lost during leap ing (R 2 =0.3802) showed a signicant eect with increas ing distance (t=10.921, p<0.0001). As indicated in Table 3, in 68.8% (42/61) of leaps of less than 1 meter, the tama rins either maintained (60.6.%) or gained (8.2%) height, whereas in 67% of leaps (69/103) between 1 meters, 90.6% of leaps (29/32) between 2 m, and 100% (4/4) of leaps > 3 meters, the tamarins lost height. In contrast, take o support DBH (t=0.542, p=0.5888) and landing support DBH (t=0.959, p=0.3387) did not signicantly predict height loss/gain during leaping. Saddleback tamarins did not select landing supports of smaller (and potentially more compliant) DBH during longer leaps nor did they select more larger and more stable landing supports with an in crease in leaping distance (Mann-Whitney U-test, Z= 0.39, p=.696; Table 4). Similarly, a multiple regression examin ing the eects of takeo support DBH (t=1.34, p=0.1813) and landing support DBH (t=0.68, p=0.4961) did not sig nicantly predict distance leapt. us, the DBH of takeo and landing supports did not appear to be a critical factor inuencing trunk-to-trunk leaping in saddleback tamarins. Table 2. Takeo and landing height during trunk-to-trunk leap ing in Saguinus fuscicollis weddelli (N=200 leaps) Height (meters) Takeo Platform (%) Landing Platform (%) <1 0.5 0.5 <2 2.5 7.0 <3 13.0 21.5 <4 21.5 30.0 <5 30.5 25.0 <6 21.0 10.5 <7 9.5 5.0 1.5 0.5 Table 3. Distance leaped and height gain/loss in Saguinus fuscicol lis weddelli during trunk-to-trunk leaping Distance leaped (m) Height change (cm) Sample size % Leaps with height loss 1 % Leaps with height gain 1 -22 43 61 31.1 8.2 >1 -49 44 103 67.0 3.8 >2 -104 55 32 90.6 0.0 >3 -150 46 4 100.0 0.0 1in our analyses we consider height gains or height losses of .25 m to reect horizontal travel (no eective change in height) Figure 1. Diameter at breast height (DBH) of the pattern of verti cal support use by saddleback tamarins compared to the availabil ity of vertical supports in their home range. **: p<.001
5 Discussion Leaping is a dominant form of travel in all species of tama rins, marmosets, and callimicos, and in general, three types of leaping behavior have been described for these smallbodied primates (Garber, 1991; Youlatos, 1999, 2009; Garber and Leigh, 2001; Nyakatura and Heymann, 2010). ese are acrobatic leaps (also called terminal leaps by You latos, 2009) which begin and end on thin terminal supports in the periphery of the tree crown and between the crowns of adjacent trees, bounding leaps which are an outgrowth of rapid quadrupedal travel and occur principally on mod erate and large diameter horizontal and oblique supports, and trunk-to-trunk leaps which occur on small, moderate, or large sized vertical or sharply inclined supports in the forest understory. However, there exists marked variability among callitrichine species in body mass, limb and body proportions, and the frequency of dierent forms of posi tional behavior (Table 1). An understanding of these dif ferences oers critical insight into patterns of habitat uti lization, feeding ecology, and locomotor anatomy in this primate radiation. Among callitrichines, C. goeldii C. pygmaea and S. fuscicol lis are the most frequent trunk-to-trunk leapers (Table 1). In the case of callimico, the exploitation of resources (fungi) present both in bamboo forest (which is dominated by ver tical supports) and on decaying logs and fallen trunks, a behavioral pattern of crypticity and rapid escape, and ana tomical adaptations associated with hindlimb elongation and ankle stability during dorsoexion (Davis, 1996), help to explain the high frequency of long trunk-to-trunk leaps reported in this species (Garber and Porter, 2009; Porter and Garber, 2010). In contrast, the diet of pygmy marmo sets is dominated by the consumption of plant exudates that are found in inundated forests along stream margins and in dense liana forest (Rylands, 1996; Youlatos, 2009). Youlatos (2009) reports that during feeding, 84.2% of lo comotor behavior (principally claw climbing) and 85.7% of postural behavior (principally claw clinging) in Cebuella involved the exploitation of vertical trunks. In contrast to callimicos, the majority of trunk-to-trunk leaps in wild pygmy marmosets spanned a horizontal distance of less than 0.5 meters, with only 3% greater than 1 m (Youla tos pers. comm, Youlatos, 2009). is may reect the fact that pygmy marmosets are characterized by extremely short hindlimbs, even when adjusted for body size (Davis, 2002). Moreover given that peak leaping forces scale to body mass (-1/3) and increase with distance leapt, smaller bodied primates are expected to engage in a series of shorter leaps in order to reduce mechanical stresses on their musculo skeletal system (Demes et al., 1999). In the present study we analyzed 200 trunk-to-trunk leaps in Weddells saddleback tamarins ( S. fuscicollis weddelli ). Relative to other tamarin species, S. fuscicollis (and possibly S. tripartitus and Saguinus nigricollis ; all three of these taxa are members of the S. nigricollis group; Matauschek et al., 2011) travel and feed more commonly in the forest under story and use trunks as a perch to scan the ground for insect and small vertebrate prey, and to explore tree holes and bark crevices (Garber, 1992, Porter, 2001). In addition, exudates are reported to account for between 7.6-30.3% of saddleback tamarin feeding time (Table 7.2 in Digby et al., 2011). During exudate feeding, saddleback tamarins commonly cling to vertical trunks in the forest understory (Garber, 1993). We found that saddleback tamarins leapt to and from vertical supports that varied in DBH from 2.8 cm to over 110 cm, with 64% of takeo supports and 66% of landing supports >5 cm DBH. e majority Table 4. Support diameter, horizontal distance leapt and height gain/loss during trunk-to-trunk leaping in Saguinus fuscicollis weddelli. Takeo Platform DBH N Distance leapt Range Height Gain/Loss Range cm 28 1.18.71 0.20-2.60 -0.40.59 -2.25-0.5 >5 62 1.47..74 0.48-3.37 -0.46.56 -1.75-0.75 >10 66 1.48.61 0.36-3.37 -0.60.58 -2.0-0.5 >20 34 1.61.81 0.38-3.68 -0.60.45 -1.5-0.5 >40 7 0.98.40 0.43-1.75 -0.46.24 -0.75-0.0 >80 3 0.77.26 0.49-1.02 -0.08.14 -0.25-0 Landing Platform DBH N Distance leapt Range Height Gain/Loss Range cm 32 1.41.72 0.20-2.86 -0.46.49 -1.5-0.25 >5 70 1.38.77 0.23-3.68 -0.47.61 -2.25-0.75 >10 62 1.49.66 0.33-3.37 -0.56.54 -2.0-0.5 >20 24 1.52.69 0.42-2.84 -0.61.56 -1.75-0.5 >40 6 1.11.39 0.55-1.75 -0.55.17 -0.75-(-0.25) >80 5 1.36.54 0.81-1.90 -0.55.41 -1.0-(-0.25)
6 of leaps occurred in the under canopy (at a height between 1 and 5m), with 30% spanning a horizontal distance of m, 51.5% <2m, and 18% m. As distance leapt increased, the tamarins lost a greater amount of height (Table 3). Few of the takeo or landing supports used by saddleback tamarins were compliant, and support DBH was not correlated with distance leapt or height gained or lost during leaping. is same pattern has been reported in wild C. pygmaea (Youlatos, 2009) and wild C goeldii (Garber and Porter, 2009). us, it appears that among both smaller bodied and larger bodied callitrichines sup port DBH is not a critical factor inuencing trunk-totrunk leaping. is may reect the mechanical advantage claw-like nails provide in maintaining support on vertical branches that otherwise are too large to be grasped by their relatively small hands and feet (Garber, 1992). In the present study, wild saddleback tamarins were found to leap relatively longer distances between vertical supports than do wild pygmy marmosets and relatively shorter dis tances than wild callimicos (Youlatos, 2009, Garber and Porter, 2009). Approximately 18% of the leaps we recorded in wild saddleback tamarins spanned a horizontal distance of >2 m. However, during these longer leaps tamarins ex perienced considerable height loss (average height loss of >1m when leaping a horizontal distance of greater than 2m, Table 3, compared to a height loss of 17.5 cm in cal limicos leaping a distance of 2m), which is expected to result in an increase in compressive forces acting on their forelimbs during landing. is is supported by the fact that during trunk-to-trunk leaping, height loss in callitrichines is negatively correlated with takeo velocity and positively correlated with landing velocity (Garber et al., 2009). In this regard, Garber and Leigh (2001:28) have suggested that forelimb elongation in saddleback tamarins (relative to other Saguinus species) may function to increase[ing] the braking distance available for decelerating the body when landing on a rigid support and more eectively dissipate the high forces generated on impact. In conclusion, although all species of callitrichines cling to and travel on relatively large vertical supports using their claw-like nails, only a small number of taxa, most nota bly C. goeldii, S. fuscicollis and C. pygmaea are reported to commonly leap between vertical supports in the forest understory. ese three species dier markedly in diet, body mass, limb proportions, and the kinematics of leap ing. Detailed studies of positional behavior are needed on marmosets of the genera Mico Callithrix and Callibella and in other Saguinus species, to better understand the functional and ecological implications of callitrichine post cranial anatomy on vertical clinging, patterns of leaping, and species dierences in habitat utilization. Acknowledgments We thank the Ministerio de Medio Ambiente, Coleccin Boliviana de Fauna, Bolivia for granting us permission to conduct research at the eld site. is study complied with the guidelines governing nonhuman primate research at the University of Illinois and the laws of Bolivia. Funds to conduct this research were provided by the Center for Latin American and Caribbean Studies at the University of Illi nois. We wish to thank Leila Porter, Edilio Nacimento, and Ruth Cuadiay for assistance in Bolivia in habituating and monitoring the saddleback tamarins. We also thank Dioni sios Youlatos for allowing us to cite his unpublished data on positional behavior in Saguinus midas and Callithrix jacchus and Michelle Bezanson for providing comments on an ear lier draft of this manuscript. Nicoletta Righini translated the abstract into Spanish. Finally, without the love and support of Sara and Jenni none of this would be possible. References Castro, N.R. 1991. Behavioral ecology of two coexisting tamarin species ( Saguinus fuscicollis nigrifrons and Sagui nus mystax mystax Callitrichidae, Primates) in Amazo nian Peru. Doctoral thesis. Washington University, St. Louis, MO. Crompton, R.H., Blanchard, M.L., Coward, S., McNeill Alexander, R. and orpe, S.K. 2010. Vertical clinging and leaping revisited: Locomotion and habitat use in the Western Tarsier, Tarsius bancanus explored via loglinear modeling. Int. J. Primatol 31: 958979. Davis LC. 1996. Functional and phylogenetic implications of ankle morphology in Goeldis monkey ( Callimico goel dii ). In: Adaptive Radiations of Neotropical Primates M. Norconk, A.L.Rosenberger, and P.A. Garber (eds.), pp. 133156. Plenum Press, New York. Davis, L.C. 2002. Functional morphology of the fore limb and long bones in the Callitrichidae (Platyrrhini, Primates). Doctoral thesis, Southern Illinois University, Carbondale, Illinois. Demes, B., Jungers, W.L., Gross, T.S. and Fleagle, J.G. 1995. Kinetics of leaping primates: inuence of substrate orientation and compliance. Am. J. Phys. Anthropol 96: 419429. Demes, B., Fleagle, J.G. and Jungers, W.L. 1999. Takeo and landing forces of leaping strepsirhine primates. J. Hum. Evol 37: 279292. Digby, L.J., Ferrari, S.F. and Saltzman, W. 2011: Callitri chines: the role of competition in cooperatively breed ing species. In: Primates in Perspective. 2nd Edition C.J. Campbell, A. Fuentes, K.M. MacKinnon, S.K. Bearder and R.M. Stumpf, (eds.), pp. 91107. Oxford University Press, Oxford, UK. Falsetti, A.G. and Cole III, T.M. 1992. Relative growth of postcranial skeleton in callitrichines. J. Hum. Evol 23:7992.
7 Garber, P.A. 1991. A comparative study of positional be havior in three species of tamarin monkeys. Primates 32: 219230. Garber, P.A. 1992 Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae. Am. J. Phys. Anthropol 88: 469482. Garber, P.A. 1993. Feeding ecology and behaviour of the genus Saguinus In: Marmosets and Tamarins: Systematics, Ecology and Behaviour A.B. Rylands (ed.), pp. 273295. Oxford University Press. Oxford, UK. Garber, P.A and Leigh, S.L. 2001. Patterns of positional behavior in mixed-species troops of Callimico goeldii, Sa guinus labiatus and Saguinus fuscicollis in northwestern Brazil. Am. J. Primatol 54: 1731. Garber, P.A, Sallanave, A., Blomquist, G. and Anzenberger, G. 2009. A comparative study of the kinematics of leap ing in Callimico goeldii Callithrix jacchus and Cebuella pygmaea In: e Smallest Anthropoids: e Marmoset/Cal limico Radiation S.M. Ford, L.M. Porter, and L.C. Davis (eds.), pp. 259278. Springer Press, New York. Garber, P.A. and Porter, L.M. 2009. Trunk-to-trunk leap ing in wild Callimico goeldii in northern Bolivia. Neotrop. Primates 16: 914. Gebo, D.L. 2011. Vertical clinging and leaping revisited: Vertical support use as the Ancestral Condition of Strep shirrhine primates. Am. J. Phys. Anthropol 146: 323335 Kinzey, W.G., Rosenberger, A.L. and Ramirez, M. 1975. Vertical clinging and leaping in a neotropical primate. Nature 255: 327328. Matauschek, C., Roos, C. and Heymann, E.W. 2011. Mitochondrial phylogeny of tamarins ( Saguinus Ho mannsegg 1807) with taxonomic and biogeographic im plications for the S. nigricollis species group. Am. J. Phys. Anthropol 144: 564574. Napier, J.R. and Walker, A.C. 1967. Vertical clinging and leaping, a newly recognised category of locomotor behav iour among Primates. Folia Primatol 6: 204219. Norconk, M.A. 1986. Interactions between primate species in a neotropical forest: mixed-species troops of Saguinus mystax and S. fuscicollis (Callitrichidae). Doctoral thesis, University of California, Los Angeles. California. Nyakatura, J.A. and Heymann, E.W. 2010. Eects of sup port size and orientation on symmetric gaits in free-rang ing tamarins of Amazonian Peru: Implications for the functional signicance of primate gait sequence patterns. J. Hum. Evol 58: 242251. Porter, L.M. 2001. Dietary dierences among sympat ric Callitrichinae in northern Bolivia: Callimico goeldii ,Saguinus fuscicollis and S. labiatus Int. J. Primatol. 22: 961992. Porter, L.M. 2004. Forest use and activity patterns of Cal limico goeldii in comparison to two sympatric tamarins, Saguinus fuscicollis and Saguinus labiatus Am. J. Phys. An thropol 124: 139153. Porter, L.M. and Garber, P.A. 2010. Mycophagy and its in uence on habitat use and ranging patterns in Callimico goeldii Am. J. Phys. Anthropol 142: 468475 Porter, L.M. and Garber, P.A. 2011. Foraging and spatial memory in saddleback tamarins (Saguinus fuscicollis ). Am. J. Phys. Anthropol 144 (Supplement 52): 242 Rylands, A.B. 1996. Habitat and the evolution of social and reproductive behavior in Callitrichidae Am. J. Pri matol 38: 518. Smith, R.J. and Jungers, W.L. 1997. Body mass in com parative primatology. J. Hum. Evol 32: 523559. Staord, B.J., Rosenberger, A.L., Baker, A.J., Beck, B., Dietz, J. and Kleiman, D.G. 1996. Locomotion of golden lion tamarins ( Leontopithecus rosalia ): the eects of forag ing adaptations and substrate characteristics on locomo tor behavior. In: Adaptive Radiations of Neotropical Pri mates M. Norconk, A.L. Rosenberger, and P.A. Garber (eds.), pp. 111132. Plenum Press, New York. Walker, S.E. 1998. Fine-grained dierences within posi tional categories: a case study of Pithecia and Chiropotes In: Primate Locomotion E. Strasser, J. Fleagle, A. Rosen berger, and H. McHenry (eds.), pp. 3143. Plenum Press, New York. West, P.W. 2004. Tree and Forest Measurement Springer Press, Berlin. Youlatos, D. 1999. Positional behavior of Cebuella pygmaea in Yasuni National Park, Ecuador. Primates 40: 543550. Youlatos D. 2009. Locomotion, postures, and habitat use by pygmy marmosets ( Cebuella pygmaea ). In: e Small est Anthropoids: e Marmoset/Callimico Radiation S.M. Ford, L.M. Porter, and L.C. Davis (eds.), pp. 279297. Springer Press, New York.
8 DISTRIBUTION, HABITAT AND STATUS OF THE WHITE-COATED TITI MONKEY ( C ALLICEBUS PALLESCENS ) IN THE CHACO CHIQUITANO FORESTS OF SANTA CRUZ, BOLIVIA Damin I. Rumiz 1,2 1 Museo de Historia Natural Noel Kempff-Mercado 2 Chiquitano Forest Conservation Foundation (FCBC), P.O. Box 5300, Santa Cruz de la Sierra, Bolivia,
9 expanse of dry forest habitats where the presence, absence or identity of titi monkeys is uncertain. In order to review the distribution and status of the Chacoan or white-coated titi monkey in Bolivia, I exam ined the available records of Callicebus new eld obser vations, photos and vegetation types where they occur in southern Santa Cruz. Based on the color pattern of the in dividuals, their geographic location and available ecological data, I characterize the distribution range of C. pallescens propose a range limit with C. donacophilus and identify un certainties on the current knowledge of these species. Study sites and Methods Wildlife surveys conducted mainly by researchers from Wildlife Conservation Society (WCS) and the Museo Noel Kemp Mercado (MNKM) have produced records of titi monkeys within and around the Kaa Iya National Park during the last 15 years. is park is the largest in Bolivia and encompasses 3.5 million hectares of alluvial plains and eroded peneplains (250-450 m a.s.l.), with a few isolated sandstone hills rising 200 m or more above the plains (Cerro Cortado 600 m, Cerro San Miguel 840 m). Two Ramsar sites partially overlap the park, the Parapet River-Isoso Baados (Isoso oodplain or inland delta) in the west, and the Palmar de las Islas-Salinas de San Jos in the east, on the border with Paraguay. Mean temperature is 24-26 across the region but rainfall decreases sharply from 1,000 mm and 3 dry months per year in the NE of the region to 400 mm and 10 dry months in the SW corner of the park (Fig. 1). is results in semi-arid, dry, and sub humid bioclimatic ombrotypes (Navarro and Maldonado, 2002) that aect the vegetation and fauna. Main vegetation types of Kaa Iya park are associated with Chaco landscape systems (Navarro and Ferreira, 2008) such as the alluvial plain dry forests of the Parapet and Grande rivers in the SW, the distinct riverine vegetation complexes along these rivers, and the transitional forests towards the Chiquitano region on alluvial plains to the N and on sandstones to the E. At the eastern border of the park, vegetation types have more anity with the Brazilian Cerrado, and include transitional and distinct Chiquitano dry forests and scrublands that are more mesic (humid) than those of the Chaco. Further E and NE from the park, Chiquitano and Chaco forests continue as riverine strips and patches into the ooded Pantanal. A digital vegetation map of Santa Cruz (scale 1:100,000; Navarro and Ferreira, 2008) and eld descriptions of at least 20 sites were used to dene the forest types associated to the Callicebus records compiled in this study. Figure 1. Callicebus records, protected areas, rainfall isoclines, deforestation and mayor landscape systems in southern Santa Cruz, Bolivia (ecosystems adapted from Navarro and Ferreira, 2008).
10 e range of C. pallescens was assessed by mapping 60 titi monkey localities in southern Santa Cruz and neighbor ing Pantanal, based on previous reviews, verication of original observations with WCS and MNKM research ers, and examination of recent images and sightings (see Table 1 for sources). However, most sources either did not identify the titi monkey species or referred it to as C. moloch. To become capable of identifying these species, I examined skins of C. donacophilus at MNKM and ob served wild individuals around Santa Cruz city. I could not examine museum specimens of C. pallescens because there are none in Bolivia. I followed the descriptions published for these species (Hershkovitz 1990, Anderson 1997, van Roosmalen et al. 2002) and discussed them with observ ers and photographers to assess the identity of new sight ings, photographs and videos. Because no specimens were collected for this study, the most reliable identications of C. pallescens were those records contiguous to the collec tion localities of specimens identied as such by Anderson (1997). Images or sightings from these and other areas that showed C. pallescens with diagnostic features (uniform light color, relatively long pelage and lack of contrasting white ears) were also considered reliable identications for this species Undened titi monkey observations that occurred near others identied as C. pallescens were assumed to be of this species, but those that were both undened and distant from reliable records were labeled as suspected C. palles cens Localities marked as of C. donacophilus reected their sources and were not corroborated except when stated as such in the text. Results and discussion Identification and distribution of Callicebus records Forty out of the 60 titi monkey locality records were mapped in Figure 1 and listed in Table 1 after removing or grouping some points to avoid cluttering. Sources of these records included review papers (Hershkovitz, 1990; An derson, 1997; Martnez and Wallace, 2010), broad wild life surveys (Parker et al. 1993; Cullar and Noss, 1997; Miserendino et al ., 1998; Navarro et al ., 1998; Ayala and Noss, 2000; Arispe and Rumiz, 2002; Brooks et al., 2002; Cullar et al. 2003; Maei, 2005), specic primate studies (Justiniano, 2004; urley, 2009; Pyritz et al. 2010; Ayala 2011), unpublished photos and related personal commu nications (Table 1). e presence of C. pallescens was sup ported by collected specimens in two sites (# 15 and 22) and by new photos and a video in nine sites (# 1, 2, 7, 8, 10, 14, 23, two in 24), while undened observations in 21 sites and local reports in nine other sites completed the assumed and suspected localities for this species. C do nacophilus was assigned to 19 localities based on three col lection sites (two near #32, one in 37), 14 direct observa tions as dened by their authors, and photographs that I reviewed from three sites (near #32 and 33). Sightings assigned to C. pallescens with high reliability in clude Ravelo (#1), Palmar de las Islas (#2), Sol de Mayo, camp Tucavaca and nearby points (#6, 7, 8), and commu nity sites along the Parapet river (#13 through 19). From Ravelo and Palmar there are photos and a video that show the long and uniformly colored pale bu pelage of the in dividuals (Fig. 2), as well as in Sol de Mayo (Fig. 3) and Tucavaca (Fig. 4). e photograph from Paraboca in the Parapet river (Fig. 5) shows the same light color of the in dividuals sighted in nearby riparian communities, includ ing the locality # 15 where three specimens were collected in the 1980s and assigned then to C. donacophilus pallescens by Anderson (1997). Sightings and a photo from the Rio Negro in the Otuquis Pantanal (#24, Vernica Zambrana, pers. comm.) also matched C. pallescens descriptions, as well as the photos available from the nearby Paraguayan Figure 2 C. pallescens at Ravelo (#1), Martin urley. Figure 3 C. pallescens in #8, Rosario Arispe.
11 Table 1. Localities, type of evidence and source of 40 records of titi monkeys from southern Santa Cruz, Bolivia mapped in Figure 1, with the species assigned by this study or its original author in the case of C. donacophilus No. Locality Type of evidence and source Coordinates Assigned species 1 Fortn Ravelo Photos, counts: Justiniano, 2004; urley, 2009 19'S 60'W Callicebus pallescens 2 Palmar de las Islas Obs.: Navarro et al ., 1998; urley, 2009; video, S. Angulo, R. Montao, pers. comm. 19'S 60'W C. pallescens 3 Salina San Jos Obs.: Cullar et al ., 2003 19'S 60'W C. pallescens 4 El Cruce Obs.: Navarro et al ., 1998 18'S 60'W C. pallescens 5 Santa Adriana Obs.: Navarro et al ., 1998 19'S 60'W C. pallescens 6 Camp Tucavaca Photos, counts: Justiniano, 2004; Maei, 2005 18'S 60'W C. pallescens 7 S. Lucia pond Photos: D. Alarcn pers. comm. 18'S 60'W C. pallescens 8 Sol de Mayo Photos, obs.: Arispe pers. comm. 18'S 60'W C. pallescens 9 San Ignacito Obs.: Navarro et al ., 1998 17'S 61'W Suspected C. pallescens 10 Cupes Charata Counts: Miserendino et al ., 1998 Photos: D. Alarcn, pers. comm. 18'S 62'W Assumed C. pallescens 11 La Madre Counts: Cullar and Noss, 1997 18'S 62'W Assumed C. pallescens 12 Curuyuqui Local report: Parker et al ., 1993 18'S 62'W Assumed C. pallescens 13 Kuarirenda Counts: Ayala, 2011 19'S 62'W C. pallescens 14 Paraboca Photos: L. Acosta, pers. comm. 19' S 62'W C. pallescens 15 Guirapembi Specimens: Anderson, 1997 19'S 62'W C. pallescens 16 La Brecha Counts: Ayala, 2011 19'S 62'W C. pallescens 17 Isiporenda Obs.: Noss and Cullar, 2000 19'S 62'W C. pallescens 18 Karapari Counts: Ayala, 2011 19'S 62'W C. pallescens 19 Perforacin Local report: Parker et al ., 1993 19'S 62'W Assumed C. pallescens 20 Cerro Cortado, Cerro Colorado Counts: Ayala and Noss, 2000; Noss and Cullar, 2000 19'S 62'W C. pallescens 21 Tacuaremb, Charagua Obs.: L. Acosta and R. Strem, pers. comm. 19'S 63'W Suspected C. pallescens 22 Rio Grande Specimen: Anderson, 1997 18'S 63'W C. pallescens 23 Laguna Concepcin Photo: A. Mamani and L. Acosta, pers. comm. 2011 17'S 61'W Suspected C. pallescens 24 Rio Negro, Pantanal Photos: V. Zambrana, pers. comm. 2008; Smith, 2012 20'S 58'W C. pallescens 25 Quituquia Loc. rep.: Arispe and Rumiz, 2002 17'S 60'W Suspected C. pallescens 26 Uruc Loc. rep.: Arispe and Rumiz, 2002 18'S 59'W Suspected C. pallescens 27 Quitunuquia Loc. rep.: Arispe and Rumiz, 2002 18'S 59'W Suspected C. pallescens 28 Mutun Local report: Parker et al ., 1993 19'S 57'W Suspected C. pallescens 29 Guayacanes Local report: Parker et al ., 1993 18'S 58'W Suspected C. pallescens 30 Sunsas farm Obs.: L. Acosta, pers. comm. 18'S 58'W Suspected C. pallescens 31 Lag. Cceres Loc. rep.: Arispe and Rumiz, 2002 18'S 57'W Suspected C. pallescens 32 Around Santa Cruz city Specimens, photos, obs.: Anderson, 1997; Pyritz et al ., 2010; K. Dingess, pers. comm. 16 sites near 17'S 63'W Callicebus donacophilus 33 Mineros Photos: D. Alarcon, pers. comm. 17'S 63'W C. donacophilus 34 San Miguelito Counts: Rumiz et al ., 2000 17'S 61'W Assumed C. donacophilus 35 San Juan de Chiquitos Obs.: Brooks et al ., 2002 17'S 59'W Assumed C. donacophilus 36 Candelaria Obs.: Brooks et al ., 2002 16'S 58'W Assumed C. donacophilus 37 Puerto Surez Specimen: Anderson, 1997 18'S 57'W C. donacophilus 38 Corumb Specimens: Hershkovitz, 1990; Auricchio, 2010 19'S 57'W C. pallescens or C. donacophilus 39 Santa Teresa Counts: Tomas et al ., 2010 18'S 57'W C a donacophilus 40 Acurizal Specimen: Hershkovitz, 1990 17'S 57'W C. pallescens
12 Pantanal (Smith, 2012). According to all our photos, the color pattern of C. pallescens individuals agreed with the published descriptions of the species, although their faces were not as white as in the drawing from van Roosmalen et al. (2002). Records from transect censuses east of Ravelo (#4, 5), on the Isoso ood plain (#10, 11) and near the hills of Cerro Cortado and Cerro Colorado (#20) were originally identi ed as Callicebus moloch, but surely correspond to C palles cens according to pictures taken in or near these sites. Recent sightings and pictures of light colored titi monkeys from the riverine forest of Laguna Concepcin (#23, Ana Mamani and Luis Acosta, pers. comm.) are suspected to be this species, as well as undened sightings (# 9, 30) and local reports of titi monkeys (# 25-31) extended further east. An old (1980) collecting site of C. pallescens on the lower slopes of the Andes (# 22; Anderson, 1997) could not be veried with newer data, and its closest recent record was an undened sighting of titi monkeys in the Charagua hills (# 21; Rosa Strem, Luis Acosta, pers. comm.). Square dots near Santa Cruz city (around # 32) included two col lecting sites of C. donacophilus (Anderson, 1997), subse quent reviews (Martnez and Wallace, 2010) and several recent sightings nearby that can be condently assigned to the gray titi monkey (Pyritz et al. 2010; Dingess, un published; Rumiz pers. obs.). C. donacophilus showed a buy or brownish agouti pelage in the upper and outer parts of head, body and limbs, darker than in C. pallescens but with the tail base noticeably paler and ear tus mark edly whitish (Fig. 6 from #32, Fig. 7 from #33). Square dots at # 34 most probably correspond to sightings of the same form (Rumiz et al., 2000) and would represent the easternmost record of the gray titi monkeys (Veiga et al. 2008b; Martinez and Wallace, 2010), unless we accept that this species was also seen on the gas pipeline to Cuiab (#35, 36; Brooks et al. 2002) and may reach the Brazilian Pantanal. In fact, a specimen from Puerto Surez on the eastern Bolivian border (# 37) was considered by Ander son (1997) to be C. d. donacophilus as well as another ve specimens from Corumb (# 38) in western Brazil men tioned as C donacophilus by Auricchio (2010). However, it seems that the same ve specimens from Corumb in the Museum of So Paulo, plus another specimen from Acurizal further N (#40), had been originally examined and assigned to C d. pallescens by Hershkovitz (1990) in Figure 4 C. pallescens in # 7, Daniel Alarcn. Figure 5. C. pallescens Ro Parapeti #13, Luis Acosta Figure 6. C. donacophilus near Santa Cruz city (#32), Daniel Alarcn.
13 his seminal paper. A recent eld transect study conducted nearby (Santa Teresa # 39; Tomas et al ., 2010) identied the titi monkeys as a. donacophilus. Dry forest types and the occurrence of Callicebus pallescens According to the latest classication and mapping of Santa Cruz vegetation (Navarro and Ferreira, 2008), the com piled titi monkey localities included a variety of forest types belonging to the Chaco, Chiquitano and Pantanal biogeographical provinces, belonging to semi-arid, dry, and subhumid bioclimatic ombrotypes (Figure 1). e available data on the occurrence and abundance of white coated titi monkeys were grouped in dierent situations according to climate, sites and forest types (Table 2). From these, three best known areas with titi monkey populations are described below in order of increasing humidity. C palles cens was found living in one of the driest Chaco forests (semiarid ombrotype, <475 mm of rainfall), such as in the foothills of Cerro Cortado and Cerro Colorado (#20), but apparently only in forests patches with large trees and tree-like cacti. Encounter rates along transects run through mixed dry forests were very low since monkeys were absent in shorter stature forest (Cullar and Noss, 1997, Ayala and Noss, 2000; Noss and Cullar, 2000). Several sites in the driest SW corner of Kaa Iya had no titi monkeys (open dots in Fig. 1), and at least one of them had Aotus but not Cal licebus (Justiniano, 2004). It is possible that titi monkeys occur only in the taller/denser patches of these dry Chaco forests and they may be found near other hills to the east within Kaa Iya, but they are absent in the driest Chaco of western Paraguay (Stallings et al. 1989; Brooks, 1996). e Chaco riverine, hydrophytic, and seasonally ooded forests along the Parapet river (# 11-18) harbor abun dant C. pallescens and three other primate species (Ayala and Noss, 2000; Ayala, 2011) despite their upper semi arid ombrotype (475-625 mm of rainfall). e inuence of the river and a shallow water table allow the existence of dense algarrobo ( Prosopis chilensis ; Fabaceae) forests, where titi monkeys were found at densities of 3.5, 6.2 and 10.4 groups/km 2 Riverine habitats extend downstream into less dry ombrotypes allowing the connectivity of Calli cebus populations of northern Kaa Iya and the Chiquitano forests. Outside the park, however, deforestation is intense and threatens this corridor. White coated titi monkeys occur in the transitional ChacoChiquitano forests of Ravelo and Palmar (#1, 2, 3) under a lower-dry ombrotype (625-800 mm of rainfall), and reach a high density of 15.3 groups/km 2 at the tall foothill forest of Cerro San Miguel (urley, 2009). ey are absent or less abundant in low stature forests nearby, but occur fur ther north and east suggesting a continuous distribution in eastern Kaa Iya park. Within the same climate type but in the tall transitional Chiquitano forest, C. pallescens is common and was found at a relatively high abundance (#6; 1.8 groups encountered / 10 km walked; Justiniano, 2004; Maei, 2005). South of Palmar de la Islas, in northern Par aguay, titi monkeys are also present at several sites (Brooks, 1996; Smith 2012) and were abundant in the tall forest of Agua Dulce (Stallings et al. 1989). Further east in Bolivia and Paraguay, extending up to the Pantanal, these forests become more mesic (>800 mm), include more Chiquitano species, and also harbor titi monkeys. e occurrence and abundance of primate species through the dry Chaco seems to depend on the relatively tall and more diverse forest patches that grow associated to well drained and richer soils (Stallings et al. 1989). In Kaa Iya, Callicebus and other monkeys occur mainly in tall Chaco forests around the Parapet river, old river channels, iso lated hills, and in the Chiquitano transitional forest. It is likely that size of the trees, availability of tree holes and other shelters, and water-rich foods (such as succulent leaves, owers and fruits of arboreal cacti) become the key habitat features for C. pallescens (and for Aotus ). In humid Chiquitano forest patches near Santa Cruz city (Pyritz et al. 2010), forest maturity, surrounding forest area and understory density have been identied as factors aect ing diversity and abundance of primates, although only the high understory density seemed to have a signicant and negative eect on the abundance of C. donacophilus Field studies are needed to identify and conserve the main habi tat features that allow these monkeys to survive in these extremely dry forests. Subhumid forests and the range of C. pallescens and C. donacophilus C. pallescens was conrmed to occur in the subhumid om brotype forests (>1,000 mm ) of the Otuquis Pantanal of Bolivia and Paraguay, and it is the suspected form although no good images are available that occurs in the Chiquitano forests north and northeast of Kaa Iya under sub humid and upper-dry (800-1,000 mm) ombrotypes. is area (sites # 9, 23, 25-35) has been considered par tially within the range of C. pallescens (Veiga et al ., 2008a), while further north of it there would be a hiatus in Cal licebus distribution since the range of C. donacophilus (#32, Figure 7. C. donacophilus North of Santa Cruz de La Sierra (#33), Daniel Alarcn.
14 33) had not reached east of the ro Grande (Veiga, et al ., 2008b). Points # 23, 25, 34-36, however, show that titi monkeys are present in these subhumid Chiquitano habi tats, north of the accepted range of C. pallescens and that they are connected westward through forests to the range of C. donacophilus (#32, 33). erefore, this northeastern population may belong to C. pallescens, connected with the Paraguayan Pantanal and Chaco populations (Hershkovitz, 1990; van Roosmalen et al. 2002; Veiga et al. 2008a), or to C. donacophilus according to the labeling of Pantanal specimens from Bolivia (#37: Anderson, 1997) and Brazil (#38: Aurichio, 2010). However, a current habitat con nection between titi monkey populations does not prove a species identity, furthermore if the phenotypes are not well dened and the karyotypes from these locations are unknown. C. pallescens from the dry Chaco looks quite dierent from C. donacophilus from the humid Amazon and Beni forests, but some photographed individuals seem intermediate in their diagnostic color features. To better characterize these phenotypes it is necessary to assess the individual variation of southern C. donacophilus color pat terns, considering age and sex dierences in known groups around Santa Cruz city, and to collect specimens and more photos of potential C. pallescens in the subhumid transition southward into the Chaco. e old collecting site of C. pallescens near the upper Rio Grande (#22) falls on a marked gradient of dry to humid forests on the Andean slopes, and it is only one hundred kilometers from C. donacophilus localities on the same for ested slopes further north. is suggests that both species may come in contact on the sub Andean forests (around 18S, 63W), and also along the humid to dry low land forest gradient of the Beni-Chaco alluvial plains near the Rio Grande, which is currently being lost to agricul ture. It would be important to verify if titi monkey pheno types in these transitions are intermediate or dened for either species. e scarce data available on the karyotype of C. donacophilus (Minezawa and Borda, 1985) and C. palles cens (Dumas, 2005) suggest that dierences in the number of bi-armed and acrocentric chromosomes, although both species have 2n=50, would prevent fertile interbreeding. is can only be veried by collecting geo-referenced ge netic samples of these little known species and by identify ing the phenotypes of the peripheral Chaco populations. Summary and conclusions Callicebus pallescens is the titi monkey species occurring in the Kaa Iya and Otuquis parks of Bolivia, and neighboring areas in Paraguay. It can be identied and distinguished in the eld from C. donacophilus by its longer pelage, light er color and little or no contrasting white ears. However, more images, new specimens and genetic samples should be analyzed to assess its phenotypic variation and relation ships with C. donacophilus White-coated titi monkeys occur in a variety of Chaco and Chiquitano forests, ranging from semiarid Chaco forests (475 mm of rainfall), to dry transitional Chaco and Chiquitano forests (625-800 mm), and up to subhumid Pantanal riverine forests in southeast ern Santa Cruz (>1000 mm). In the subhumid and humid forests north and northwest of the Chaco, C. pallescens is replaced by the gray titi monkey ( C. donacophilus ), but the geographic limit between the two species is not clearly known. Moreover, additional records of titi monkeys in the Chiquitano forests fall outside the known range of both species, and likewise the Pantanal records on the BoliviaBrazil border, their identity needs to be veried. Surveys are needed to assess remnant populations in the threatened forest north of Kaa Iya and Otuquis parks, for which park guards and biologists should be trained with visual aids to recognize the primate species in the eld and to take pic tures, specimens or genetic samples if opportunities arise. Acknowledgments I want to thank the biologists and technicians who collected the original eld data on monkeys and habitats, especially Luis Acosta, Sixto Angulo, Rosario Arispe, Johnny Ayala, Joaqun Barrientos, Erika Cullar, Rosa Leny Cullar, Ciro Justiniano, Leo Maei, Romer Miserendino, Rossy Mon tao, Gonzalo Navarro, Jorge Segundo, Martin urley and Veronica Zambrana, who also provided images and descriptions. Daniel Alarcn kindly contributed his great pictures, while Louise H. Emmons, Leo Maei, Andrew Noss, Rob Wallace and an anonymous reviewer provided useful comments to the manuscript. is study was funded through Wildlife Conservation Society and additional donors such as US Fish and Wildlife, Kaa Iya Founda tion, Shared Earth and Ramsar, under agreements with the Museo Noel Kemp Mercado, Capitana del Alto y Bajo Isoso, Servicio Nacional de Areas Protegidas, and Vicemin isterio de Medio Ambiente y Agua, Bolivia. References Anderson, S. 1997. Mammals of Bolivia, taxonomy and distribution. Bull. Am. Mus. Nat. His. 231: 1652. Arispe, R. and Rumiz, D. I. 2002. Una estimacin del uso de los recursos silvestres en la zona del Bosque Chiqui tano, Cerrado y Pantanal. Rev. Boliv. Ecol. Conserv. 11: 1736. Auricchio, P. 2010. A morphological analysis of some spe cies of Callicebus omas, 1903 (Pithecidae, Callicebi nae). Neotrop. Primates 17: 4758. Ayala, J.M. 2011. Estudio de la comunidad de primates en el Alto y Bajo Isoso (Gran Chaco), Santa Cruz, Bolivia. Masters thesis in Ecology and Conservation. Universidad Mayor de San Andrs, La Paz. Ayala, J. and Noss, A. J. 2000. Censo por transectas en el Chaco Boliviano: limitaciones biolgicas y sociales de la metodologa. In: Manejo de fauna silvestre en Amazona y Latinoamrica, E. Cabrera, C. Mercolli and R. Resquin (eds.), pp. 2936. CITES Paraguay, Fundacin Moises Bertoni, University of Florida. Asuncin, Paraguay.
15 Brooks, D. M. 1996. Some observations of primates in Paraguay. Neotrop. Primates 4: 1519. Brooks, D.M., Tarifa, T., Rojas, J.M., Vargas, R.J. and Ara nibar, H. 2002. A preliminary assessment of the mamma lian fauna of the eastern Bolivian panhandle. Mammalia 65: 509520. Cullar, E. and Noss, A.J. 1997. Conteo de huellas en bre chas barridas: un ndice de abundancia para mamferos. Ecologa en Bolivia 30: 5567. Cullar, E. and Noss, A.J. 2003. Mamferos del Chaco y la Chiquitana Wildlife Conservation Society. Editorial FAN, Santa Cruz, Bolivia. Cullar, E., R. Montao, Hesse, A., Azurduy H., Dosapei, T., and Pea, R. 2003. Biodiversidad de la Salina Ravelo (19 17' 44" S, 60 37' 10" W) Parque Nacional Kaa Iya del Gran Chaco. Unpublished report # 96, CABI/WCS, Santa Cruz, Bolivia. Hershkovitz, P. 1963. A systematic and zoogeographic ac count of the monkeys of the genus Callicebus (Cebidae) of the Amazonas and Orinoco river basins. Mammalia 27: 179. Hershkovitz, P. 1990. Titis, New World monkeys of the genus Callicebus (Cebidae, Platyrrhini): A preliminary taxonomic review. Fieldiana Zool. NS 55: 1109. Justiniano, C. 2004. Los monos en dos zonas del Parque Nacional Kaa-Iya del Gran Chaco. In : II Congreso de in vestigadores en recursos naturales del Parque Nacional KaaIya y zonas de inuencia R.L. Cullar (ed.), pp. 2122. CABI, WCS, Santa Cruz, Bolivia. Maei, L. 2005. Informe nal de los trabajos de investig acin realizados en el campamento de Tucavaca, Gaso ducto Bolivia-Brasil. Unpublished report, CABI/WCS, Santa Cruz, Bolivia. Martinez, J. and Wallace, R. B. 2010. Pithecidae. In: Dis tribucin, ecologa y conservacin de los mamferos medianos y grandes de Bolivia R.B. Wallace, H. Gomez, Z. Porcel and D.I. Rumiz (eds.), pp.307330. Centro de Ecologa Difusin Fundacin Simon I. Patio, Santa Cruz de la Sierra, Bolivia. Miserendino, R., Cullar, E. and Noss, A.J. 1998. Diver sidad de los mamferos en el Izozog y el Area Natural de Manejo Integrado del Gran Chaco, Santa Cruz, Bolivia. Ecologa en Bolivia 31: 1731. Navarro, G., Guerrero, J., Gonzles, L., Hurtado, J.C., Santivaez, J. L., Cullar, E., Rojas J. M. and Fuentes, A. 1998. Tipicacin y caracterizacin de los ecosistemas del Parque Nacional Kaa-Iya del Gran Chaco (Departa mento de Santa Cruz, Bolivia). Documento Tecnico # 38, WCS-CABI, Santa Cruz, Bolivia. Navarro, G. and Maldonado, M. 2002. Geografa ecolgica de Bolivia. Vegetacin y ambientes acuticos Centro de Ecologa Simn I. Patio, Departamento de Difusin. Cochabamba, Bolivia. Navarro, G. and Ferreira, W. 2008. Mapas de vegetacin, potencial forestal ecolgico y proteccin de la vegetacin del departamento de Santa Cruz Gobierno Departa mental Santa Cruz, Santa Cruz de la Sierra.
16 PRIMATES OF THE LOWER URUBAMBA REGION, PERU, WITH COMMENTS ON OTHER MAMMALS Tremaine Gregory 1,2 Farah Carrasco Rueda 1 Jessica L. Deichmann 1 Joseph Kolowski 1 and Alfonso Alonso 1 1 Center for Conservation Education and Sustainability, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, D.C. 20013-7012 2 Corresponding author; e-mail: firstname.lastname@example.org Abstract We present data on encounter rates and group sizes of primates in the Lower Urubamba Region of Peru, an unprotected area little represented in the literature. We censused a total of 467.7km on 10 transects during two seasons and documented nine primate species in the area. Compared to nearby protected areas, group encounter rates were lower and group sizes were smaller for all species except Saguinus fuscicollis and S. imperator Relatively high abundance of S. imperator and low abun dance of larger bodied primates is a possible example of density compensation resulting from hunting pressure. In addition to the primates, 23 other mammal species were observed or photographed by camera traps, including Procyon cancrivorus which was not previously reported in the area. Keywords : Lower Urubamba, Peru, primate densities Resumen Presentamos los datos de tasas de encuentro y tamaos grupales de especies de primates en la Regin del Bajo Urubamba en Per, un rea no protegida poco representada en la literatura. Censamos un total de 467.7km a lo largo de 10 transectos durante dos estaciones y documentamos la presencia de nueve especies de primates en el rea. Comparando nuestros datos con los de reas protegidas cercanas, las tasas de encuentro fueron bajas y los tamaos grupales fueron menores para todas las especies a excepcin de Saguinus fuscicollis y S. imperator La abundancia relativamente alta de S. imperator y la abundancia baja de las especies de mayor tamao corporal podran ser un ejemplo de la compensacin de densidad que resulta de la presin ejercida por la caza. Adicionalmente a los registros de primates, 23 especies de otros mamferos fueron observados o fotograados por cmaras trampa, incluyendo a Procyon cancrivorous el cul no ha sido reportado en el rea previamente. Palabras clave: Bajo Urubamba, Per, densidades de primates Introduction Peru is one of the more active South American countries in primate research ( PrimateLit, 1940-2010: 678 records ), yet the Lower Urubamba Region (LUR, named for the Urubamba River) in the Department of Cuzco is underrep resented in the primate literature ( PrimateLit, 1940-2010: 0 records ). is is likely due to the lack of protected areas in the region and the LURs many oil concession areas ( Finer and Orta-Martnez, 2010 ), which can limit access. Pri mate records therefore come primarily from environmental consulting agencies and are in the form of environmental impact assessments (EIAs; Table 1). Because these reports are often the result of rapid assessments, species lists are produced primarily with indirect evidence (e.g. scat, vo calizations), and data on encounter rates and group sizes are limited. Because the LUR lies at the base of the Andes Mountain Range, it exhibits high precipitation and great variation in elevation and topography ( Alonso et al. 2001 ) promoting oral and faunal diversity ( Gentry, 1988 ; Pacheco et al. 2009 ). ere is much debate regarding the geographic dis tributions, names, and characteristics of the primate species likely to be found in the LUR and surrounding areas ( e.g., for Callicebus spp. see Aquino et al. 2008 ; Deer, 2004 ; Hershkovitz, 1990 ; Heymann et al. 2002 ; van Roosmalen et al. 2002, among many others ). e purpose of this paper is to document the primate species present in the LUR, report their encounter rates and group sizes, and present observations of other large mammal species encountered. Study site Covering approximately 60,000 ha, the LUR is bordered to the west by the Vilcabamba Mountains and to the east
17 Table 1. Summary of primate and mammal census data for the Lower Urubamba Region (LUR), Cordillera Vilcabamba (CV), and Manu National Park (MNP). e total number of mammal species registered in each study, both through direct (sighted or photographed) and indirect observations, are listed, as are the number of primate and other mammal species directly observed. e nal column lists the primate species observed, and bold type indicates species also found at the study site. NR = not reported. Study Area Loc. Date a Habitat Eort b (days, hours, km diurnal monit.) All mammals Primates Primate species c Total no. spp. reg. No. spp. dir. obs. No. spp. dir. obs. Present Study LUR Pagoreni A D,W 1 lowland forest 80d; 370hrs 467.6km 27 27 9 AC, ASA, AN, CB, CAL, CAP, PI, SF, SI Boddicker et al ., 2001 LUR Pagoreni A D 1 and 2 lowland forest 16d; 112 hrs; 80km 24 7 4 AO, APC (Vo), AS, CAL PM LUR San Martn 3 D 1 lowland forest with bamboo 12d; 84hrs; 42km 24 13 6 APC, AS, CAL, CAP, SI SSB LUR Cashiriari 2 D 1 lowland forest 13d; 91hrs; 65km 24 11 5 CAL, CAP, CP, SF, SM LUR Cashiriari 3 W 1 lowland forest 20d; 140hrs; 100km 26 15 8 AO, AS, CAL, CAP, CMB, LL, SI, SSB Emmons et al. 2001 CV Ro Pomureni D Pampas 28d 4 1 0 No Primates CV Ro Poyeni 1 montane forest 7 3 2 ABC (Vo), AO (Vo), CAL, CAP CV Ro Picha D,W Mid-montane cloud forest 25d 10 8 4 ABC (Vo), AO, AS (Vo), CAL, CAP, LL Rodriguez and Amanzo, 2001 CV Llactahuaman D 1 montane forest with bamboo 31d 12 5 0 No Primates CV Wayrapata Cloud forest 12 1 No Primates ERM, 2010 LUR Kinteroni D,W W 1 lowland forest with bamboo 12d; 85.5hrs; 50km 23 14 6 AC AL CA, CAL, CAP PI (Vo), SI LUR Mashira 12d; 87.1hrs; 59km 27 21 8 AC AL AN, CA, CAL, CAP, SB, SI LUR Mapi 12d; 104.9hrs; 55km 21 14 6 AC, AL, AN CA, CAL, LC ERM, 2009 LUR Kinteroni W 1 lowland forest with bamboo 2d; 23.5hrs; 12.4km 20 6 3 AN, AS (Vo), CAP CB, SI ERM, 2006b LUR Yamihua (Coviri Alto) W 6d; 34.5hrs; 37.6km 34 14 7 AN, AS (Vo), CAP, CB, SA, SB, SF SI ERM, 2006a LUR Kinteroni W 5d; 15hrs; 7.5km 13 7 4 AS (Vo), CAL, CAP, CB, SI ERM, 2005 in ERM 2006a LUR Miara (Atalaya) W 1 lowland forest 6d; 33.5hrs; 32.1km 22 6 2 AN, AS (Vo), CAL (Vo), CB (Vo), SI LUR Sabetari (Coviri) W 1 lowland forest 5d; 33hrs; 28.2km 26 10 5 AN, AS (Vo), CAL, CAP (Vo), CB (Vo), SB, SI Leite Pitman et al ., 2003 ; Terborgh et al ., 1984 MNP EBCC D,W ; 1 lowland and ooded forest, grassland 12 yrs 61 NR 14 AP, AS, AT, CAL, CAP, CG, CM, CP, LL, PM, SF, SI, SM, SS Walsh Peru, 2010 LUR Kinteroni, Block 57 D,W 1 lowland forest with bamboo 36d; 403.2hrs; 268.8km 38 NR NR AC, AN, ASA, AV, CA, CAL, CAP, CB, SB, SI a D = Dry season; W = Wet season; b Camera and other trap time not listed; c ABC = Ateles belzebuth chamek AC = Ateles chamek AL = Alouatta sp. AN = Aotus nigriceps AO = Aotus sp ., AP = Ateles paniscus APC = Ateles paniscus chamek AS = Alouatta seniculus ASA = Alouatta sara AT = Aotus trivirgatus AV = Aotus vociferans CA = Callicebus sp., CAL = Cebus albifrons CAP = Cebus apella CB = Callicebus brunneus CG = Callimico goeldii CM = Cal licebus moloch CMB = Callicebus moloch brunneus CP = Cebuella pygmaea CPI = Cebus pithecia LC = Lagothrix cana LL = Lagothrix lagothricha PI = Pithecia irrorata PM = Pithecia monachus SA = Saguinus sp., SB = Saimiri boliviensis SF = Saguinus fuscicollis SI = Saguinus imperator SM = Saguinus mystax SS = Saimiri sciureus, SSB = Saimiri sciureus boliviensis
18 by the Urubamba Mountains. e study site is near the Pagoreni A natural gas well site, east of the conuence of the Camisea and Urubamba Rivers (11' S, 72' W; Fig. 1). ree habitat types terra rme riverine terrace, and mixed uplandhave been described for the area, and Pagoreni A is in terra rme primary forest, dominated by Iriartea deltoidea (Araceae) and Pentagonia parvifolia (Ru biaceae) ( Comiskey et al. 2001 ). In the region, the local Matsigenka people cultivate manioc, maize, plantains, and bananas using swidden agricultural techniques ( Shepard and Chicchn, 2001 ) along the Camisea River, and sub sistence hunting is legally practiced. e study area is in traditional Matsigenka territory, within oil concession lots 56 and 58, controlled by Pluspetrol. Repsol Exploracin Per is building a second pipeline from Pagoreni A to the Malvinas processing plant. We studied a 9.2 km section of the northern part of this proposed pipeline (Fig. 1) under a collaborative agreement with Repsol, and results presented here are part of a larger study on the impacts of pipeline construction on primates. Methods Primates were censused along eight transect trails perpen dicular to the route of the planned pipeline, between 1.2 and 1.5 km in length (opened in March-May 2011) and along two transects on the proposed pipeline route 4.0 and 5.2 km in length (Fig. 1) during the dry (28 May-3 July 2011) and wet (13 October-24 November 2011) seasons. Transects were sampled between 700-1200 and 1300-1700 h. In the dry season, perpendicular transects were walked a total of 8 times each and in the wet season 20 times each. e pipeline trail transects were sampled 20 and 18 times each during the wet season only. A total of 467.6 km (dry season: 84 km; wet season: 383.6 km) were sampled. An additional 668.2 km (dry season: 259.3 km; wet season: 408.9 km) were sampled opportunistically during transit time to, from, and between transects. ere were two eld teams, each consisting of a Matsigenka guide, a primatolo gist (TG or FCR), and a eld nurse. e team members walked transects at approximately 1.25 km per hour and upon encountering a group of primates recorded the fol lowing data: species, group size, sex-age composition of the group, height of the group in the canopy, and the location with a hand-held Garmin Map CSx or Cx GPS unit. When possible, primates were photographed to conrm species identications. Groups that were heard but not seen (par ticularly Alouatta sara and Callicebus brunneus groups) were not included in data analysis because their exact location and group size could not be conrmed. We used group size and composition data, combined with the spatial distribu tion of sightings, to estimate the total number of distinct groups observed (Table 2). Group encounter rates (# seen per 10 km walked) were calculated for each species and compared to adjacent documented localities. Additionally, we placed Reconyx RC55 digital infrared trail cameras (Reconyx Inc., Holmen, Wisconsin, USA) along the pipeline route and perpendicular transects to document the presence of primates and other mammals. During the dry season, there were four cameras in ve locations on the ground (87 camera trap nights) and ve cameras in six lo cations in the canopy (89 nights). During the wet season, we placed six cameras in seven locations on the ground (157 nights). Results and discussion During the dry season, we documented eight species of primates. ese species were also conrmed in the wet season in addition to a single subadult female Ateles chamek (Fig. 2; Table 2). Encounter rates were highest for the two Saguinus spp. and the two Cebus spp. Callicebus brunneus Alouatta sara and Pithecia irrorata were seen relatively in frequently. Aotus nigriceps was only seen on four occasions; however, this low encounter rate is likely a byproduct of strictly diurnal sampling. Group sizes were similar to those reported from other sites for both Saguinus spp, C. brun neus and P irrorata Groups of Cebus spp., however, were small compared to group sizes documented in the literature (Table 2). In either or both of the seasons, infants and/ or juveniles were observed in groups of all species except C brunneus More species of primates were observed during this study than in previous studies in the area (Table 1). However, with the exception of the two Saguinus spp., encounter rates Figure 1. Map of study area. Solid black lines indicate the 9.2 km portion of the proposed pipeline that was monitored and eight perpendicular transects that are at least one kilometer in straightline distance from the proposed pipeline.
19 Figure 2. Images from Pagoreni A the nine species observed: A. Callicebus brunneus (sexes unknown), B. Pithecia irrorata (female?), C. Aotus nigriceps (sex unknown), D. Saguinus imperator (male?), E. Saguinus fuscicollis (sex unknown), F. Cebus apella (sub-adult male) G. Cebus albifrons (juvenile), H. Alouatta sara (male), and I. Ateles chamek (female). Photos: TG: A, B, D, G, H; FCR: E, I; Camera trap (taken 2013): C, F. Table 2. Primates observed during study period both on transect walks and during walks to reach sampling sites (total). Mean group size (with all age classes), range, and estimated number of groups observed are based on total sightings. Encounter rates (ER) are based only on transect walk sightings. References for species identications include names of experts consulted. Group sizes and ER for nearby protected areas Manu National Park (MNP) and Los Amigos Conservation Concession (CICRA) are presented for comparison. Species No. of sightings on transects (total) Mean group size (range) Est. no. of unique groups obs. Group ER/10km MNP, CICRA a References for species identications Mean group size (range) GroupER/ 10km Saguinus fuscicollis 28 (46) 4.8 (2-6) 10 0.60 5 (3-13) 0.43 Aquino and Encarnacin, 1994 Saguinus imperator 34 (52) 6.0 (3-10) 9 0.73 4 (3-5) 0.37 Hershkovitz, 1977 ; 1979 Aotus nigriceps 2 (4) 2.8 (2-4) 4 0.04 4 (2-4) b Fernndez-Duque, 2011 ; Ford, 1994 ; Hershkovitz, 1983 Cebus albifrons 26 (41) 11.0 (8-16) 4 0.56 15 (8-16) 1.22 Silva Jr., 2001 Cebus apella 28 (36) 5.3 (3-8) 3 0.60 10 (4-12) 2.82 Aquino and Encarnacin, 1994 ; Silva Jr., 2001 Callicebus brunneus 5 (7) 2.0 (2) 4 0.11 3 (3-4) c 1.04 c Hershkovitz, 1990; T. Deer, pers. comm. Pithecia irrorata 5 (12) 2.4 (2-4) 9 0.11 4.7 (2-8) Hershkovitz, 1987; L. Marsh and S. Palminteri, pers. comm. Alouatta sara 7 (10) 4.2 (3-5) 6 0.15 6 (4-7) d 1.35 d Corts-Ortiz et al., 2003 ; Groves, 2001 ; 2005; R. Cadenillas, pers. comm. Ateles chamek 0 (1) 0 29.7 (1844) 2.82 Quintana et al., 2009 a References: Gibson, 2012 ; Janson and Terborgh, 1980 ; Palminteri and Peres, 2012 ; Terborgh, 1983 b Aotus trivirgatus c Callicebus moloch d Alouatta seniculus
20 were low compared to nearby protected areas (Table 2). Primate species not observed but considered potential in habitants of the area include: Cebuella pygmaea Saimiri boliviensis and Lagothrix cana Appropriate data were not gathered during this study to determine whether these spe cies are absent for ecological reasons. However, given that sampling intensity was relatively high and data were gath ered during two seasons, it is unlikely they simply went undetected. Low encounter rates and group sizes may be attributable to various causes including ecological factors and human impact. While these factors were not speci cally addressed by this study, human impact is indeed a possibility. Although construction of the original Pluspet rol pipeline from Pagoreni to Malvinas was completed in 2008, maintenance of the pipeline and well requires the continuous presence of personnel along with associated frequent helicopter trac, resulting in a notable human presence in the area. Separate from this disturbance, legal Table 3. Non-primate mammal species registered during the study either through direct observations or photographs from camera traps. Scientic name Common name (English) Common name (Matsigenka) Registration type Camera trap Direct observation Cingulata Dasypodidae Dasypus novemcinctus Nine-banded armadillo tini x Priodontes maximus Giant armadillo Kinterni x Pilosa Myrmecophagidae Tamandua tetradactyla Amazonian tamandua Mntani x Rodentia Sciuridae Microsciurus sp. x Sciurus spadiceus Southern Amazon red squirrel Mguiri x Dasyproctidae Myoprocta pratii Green acouchi Chochori x Cuniculidae Cuniculus paca Lowland paca Samni x Lagomorpha Leporidae Sylvilagus brasiliensis Forest rabbit Tsroni x x Carnivora Felidae Leopardus pardalis Ocelot Matsnsori, maniti x Puma concolor Puma Matsnsori, maniti x Panthera onca Jaguar Matsnsori, maniti x Procyonidae Procyon cancrivorus Crab-eating raccoon Kovntsiri x Potos avus Kinkajou Kutsni x Mustelidae Lontra longicaudis Neotropical otter Parri x Eira barbara Tyra Oti x Perissodactyla Tapiridae Tapirus terrestris Brazilian tapir Kmari x Cetartiodactyla Tayassuidae Pecari tajacu Collared peccary Shntori x x Cervidae Mazama americana Red brocket deer Manro x x
21 subsistence hunting by local communities has been docu mented to have a signicant inuence on abundance and diversity of local primates in the Amazon ( Naughton-Trev es et al. 2003 ) and this could be a factor in the LUR as well. Ateles chamek and Lagothrix cana are the two most pre ferred edible primate species for the Matsigenka people in Manu National Park, followed by Alouatta seniculus ( sara in the present study), Cebus apella and C. albifrons ( da Silva et al. 2005 ; Shepard, 2002 ). In the present study, the ab sence of L. cana and encounter rates of the other species are consistent with this preference pattern of primate con sumption. A. chamek and A. sara were seen infrequently, and while both Cebus spp. were among the four most fre quently sighted, encounter rates and group sizes were lower than other sites, particularly for C. apella In contrast to the larger bodied primates, both Saguinus spp. were relatively abundant and showed higher encounter rates than re ported in Manu National Park (Table 2). Both small body size and high fertility (twinning every six months) likely contribute to this phenomenon. According to da Silva et al ( 2005 ), Matsigenka hunters only take Saguinus Calli cebus and Pithecia spp. on occasion because of their small body size. Abundances of Saguinus spp. may therefore be an example of density compensation, wherein abundances of smaller and medium-bodied species increase given an absence of larger-bodied species, a pattern that has been associated with hunting pressure ( Barrera Zambrano et al. 2008 ; Peres and Dolman, 2000 ). Alternatively, a preference among Saguinus spp. for disturbed and secondary habitat ( Garber, 1993 ; Oliveira and Ferrari, 2008 ), such as that created by the nearby pipeline, may also explain higher numbers of these two species. Low encounter rates of Pithe cia irrorata and Callicebus brunneus may be have to do with lack of habituation and a resulting cryptic anti-predator response ( Gleason and Norconk, 2002 ; Terborgh, 1983 ), which likely reduced detectability for observers. Regarding non-primates, eighteen additional large mammal species were documented in the area (Table 3). Procyon cancrivorus was recorded for the rst time in the area, and both large felids ( Puma concolor and Panthera pardus ) were photographed, along with Leopardus pardalis Other docu mented species of interest include Priodontes maximus and Tapirus terrestris both of which are listed as vulnerable on the IUCN Red List ( Naveda et al. 2008 ; Superina et al. 2010 ). T. terrestris and felid tracks were seen almost daily, and Cuniculus paca Myoprocta pratii Mazama americana and Pecari tajacu were recorded frequently in the camera traps. is potentially high diversity and abundance of ter restrial large mammals, despite the low abundances of large bodied primates, requires further investigation. Acknowledgements We thank F. Dallmeier, M. Costa, G. Joo, S. Castro, and T. Pacheco for their invaluable logistical support, and M. Matas, A. Pearreal, T. Italiano, E. Pascal, L. Yavireri, C. Caya, A. Elias, and R. Quenticuari and other sta for eld support. Funding for this project and logistical sup port were provided by Repsol Exploracin Per. is re search was conducted under Resolucin Directoral N 0221-2011-AG-DGFFS-DGEFFS. is publication is contribution #11 of the Peru Biodiversity Program. References Alonso, A., Dallmeier, F., Campbell, P., and Norgueron, R. 2001. e Lower Urubamba Region, Peru. 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24 S A INDCIOS DE PREDAO DE OVOS DE CAIMAN CROCODILUS (JACAR TINGA) POR SAIMIRI SP. (MACACO DE CHEIRO) Rafael S Leito Barboza Jos Francisco Reis da Costa Alfredo Fonseca Andrade Juarez Carlos de Brito Pezzuti George Henrique Reblo A inundao e a predao de ovos so os principais fato res da perda ou controle populacional de crocodilianos, assim, seus ovos compem a dieta de vrios animais com hbito alimentar oportunista, incluindo rpteis, aves e ma mferos (Larriera and Pia, 2000; Chen et al., 2003). No Novo Mundo j foram descritas predao de ovos de vrias espcies de crocodilianos, porm, a nica espcie de pri mata descrita como predadora de ovos de jacars foi Cebus apella (macaco prego) (Tabela 1). A diferena das espcies de predadores para cada espcie de crocodiliano, descrita na tabela 1, varia de acordo com a ocorrncia de cada espcie em seus habitats. O presente estudo relata, pela primeira vez na literatura, indcios de predao de ovos de jacars por Saimiri sp. (macaco de cheiro). O comportamento do primata foi evidenciado na co munidade Ilha do Carmo durante atividades de pesquisa em campo sobre a ecologia reprodutiva de crocodilianos na vrzea do Baixo Rio Amazonas. A Ilha do Carmo est situada na vrzea do rio Amazonas (S 02'27.6" W 054'43.6"), no municpio de Alenquer PA, e est in serida no Projeto de Assentamento Agroextrativista (PAE) Salvao, prximo ao municpio de Santarm (Figura 1). Um dos objetivos do projeto inclua a captura de lhotes de jacars recm-nascidos para vericao da razo sexual nos ninhos (Allsteadt and Lang, 1995). A estratgia uti lizada para captura dos lhotes foi a construo de uma cerca em volta dos ninhos. No dia 30 de janeiro de 2012 restava apenas um ninho para que seus ovos fossem eclodi dos. Na manh do dia seguinte (08:00 h) foi observado um grupo de Saimiri sp. acima do ninho com comportamento inquieto e muitas vocalizaes. No foi tomado nota sobre a quantidade de indivduos nem a composio do grupo Figura 1. Localizao da comunidade Ilha do Carmo, municpio de Alenquer (PA), Brasil, onde foram registrados os indcios de predao do ninho de C. crocodilus por Saimiri sp.
25 de primatas. Vericamos que havia uma casca vazia com o respectivo lhote neonato de jacar no predado dentro da cerca que rodeava o ninho, e do lado de fora da cerca havia outra casca vazia e seu atinente lhote escondido em baixo de um tronco. O lhote encontrado fora da cerca estava ferido na regio dorsal com uma perfurao, ainda sangrando, semelhante marca de mordidas com caninos. Em uma das estacas da cerca havia indcios da quebra do ovo com marcas de sangue e pequenos fragmentos da casca do ovo, indicando tentativa de quebra do ovo para poste rior consumo (Figura 2). Tabela 1. Crocodilianos e seus predadores de ovos no Novo Mundo. Crocodilianos Predador de Ovos Fonte Alligator mississipiensis (aligator americano) Procyon lotor, Lutra canadensis, Oryzomis palustris, Ursus americanus. Joanen, 1969; Deitz and Hines, 1980; Joanen and McNease, 1989; Howard and Ogden, 1991. Caiman yacare (jacar do pantanal) Nasua nasua, Cerdocyon thous. Crawshaw and Schaller, 1980; Cintra, 1988; Campos, 1993. Caiman crocodilus (jacar tinga) Cebus apella, Tupinambis teguixin, Panthera onca, Homo sapiens, Cerdocyon thous, Caracara plancus. Rivero Blanco, 1974; Staton and Dixon, 1977; Villamarn-Jurado and Surez, 2007; Da Silveira et al., 2010. Caiman latirrostris (jacar do papo amarelo) Sus scrofa, Polyborus plancus, Conepatus chinga. Larriera and Pia, 2000. Crocodilus acutus (crocodilo americano) Procyon lotor, Procyon cancrivorus, Nasua narica. Ogden, 1978; Mazzotti, 1983; orbjarnarson, 1989; Abada, 1996; Platt and orbjarnarson, 2000. Melanosuchus niger (jacar au) Cebus apella, Tupinambis teguixin, Panthera onca, Homo sapiens. Rueil, 2004; Villamarn-Jurado and Surez, 2007; Da Silveira et al., 2010; Villamarn et al., 2011. Figura 2. Imagens do ninho de Caiman crocodilus possivelmente predado por Saimiri sp. na comunidade Ilha do Carmo, Alenquer (PA): a) ninho no dia anterior predao; b), c) ninho com indcios de predao; d) estaca do ninho com marcas de sangue e fragmentos de casca do ovo; e) recuperao de lhote de C. crocodilus aps alguns dias do ferimento.
26 A perfurao no dorso do lhote deve ter ocorrido quando ainda estava no ovo ou aps ecloso. Propem-se duas si tuaes, onde: (1) o primata tentou consumir apenas o ovo, e o lhote fugiu aps ecloso; ou (2) o primata alm de tentar consumir apenas o ovo teria quebrado-o e ten tado consumir o lhote mordendo-o aps quebra do ovo, porm, o lhote escapou. A chegada da equipe (pesquisa dor e comunitrio) pode ter contribudo com a fuga do lhote. A dieta de indivduos do gnero Saimiri inclui folhas, frutos, resinas, sementes, insetos, larvas de lepidpteros e ortpteros, nctar, ores, moluscos terrestres, caranguejos, ovos de aves, e pequenos vertebrados como lagartos, perere cas, morcegos e lhotes de aves (Janson and Boinski, 1992; de oisy et al., 2002; Voguel et al., 2002; Lima and Fer rari, 2003; Reis et al., 2011; Andrade, 2007). Ovos e lho tes de jacars foram caracterizados por ns como possveis componentes da dieta nutricional j citada para o primata, contudo, no h registros do consumo de ovos e lhotes neonatos de jacars por Saimiri sp. Outro predador de ovos de jacars presente em reas de vrzea na Amaznia o Tupinambis teguixin (jacurar, tej ou tei) (Da Silveira et al., 2011). Sobretudo, dicilmente um jacurar conseguiria levar o ovo de jacar para fora da cerca devido altura da mesma (70 cm) e sua manei ra de consumo, na qual o rptil no ingere o ovo inteiro com a casca em sua boca (Magnusson, 1982). E ainda, as marcas de sangue e fragmentos de casca na estaca indi cam a quebra do ovo nesta estrutura, comportamento no identicado no lagarto supracitado. Os ninhos de jacars apresentam forma de pilhas cnicas e so formados por material orgnico presente no local de nidicao como galhos e folhios, assim, podem tornar-se facilmente vis veis para os predadores. Apesar do cuidado parental ofe recido por crocodilianos, nem sempre a me est presente durante o perodo de incubao dos ovos, deixando-os vulnerveis ao ataque de predadores (Wang et al., 2011). Sobretudo, quanto mais tempo o ovo permanece incuban do no ninho, maior possibilidade de predao (Larriera, 1994; Wang et al., 2011). Para obter informaes sobre o ambiente e fauna local, foram realizadas conversas informais e aplicao de en trevistas semiestruturadas em 30 % das famlias, no ano de 2012. Foi utilizada a metodologia do tipo bola de neve, na qual, os prprios entrevistados indicam os informantes chave, que so os moradores reconhecida mente experientes por demonstrar conhecimento deta lhado sobre a regio (Biernacki and Waldorf, 1981; Vier tler, 2002; Davis and Wagner, 2003; Albuquerque and Lucena, 2004; Seixas, 2005). Dessa forma, foi constatado que na Ilha do Carmo h apenas primatas pertencentes ao gnero Saimiri (denominados localmente macaco de cheiro, macaco mo amarela ou xuim) (dados no publi cados). Alm da informao fornecida pelos moradores locais referente espcie de primata existente na ilha, a evidncia da predao de ovos de C. crocodilus por Saimiri sp. foi sugerida pelo pescador Jos da Costa, membro da equipe de pesquisa participativa de jacars, o que refora a relevncia do conhecimento tradicional para a pesquisa cientca (Posey, 2000). Mesmo sem a observao direta da coleta e quebra do ovo pelo(s) primata(s) e tentativa de consumo desse e do lho te, as evidncias apresentadas indicam a tentativa de preda o de ovos e neonatos de Caiman crocodilus por Saimiri sp. Este, apresenta-se como mais um predador de ovos e lho tes de Caiman crocodilus e, possivelmente, os ovos do jacar como uma fonte alimentar alternativa para Saimiri sp. Rafael S Leito Barboza Instituto de Pesquisa Ambiental da Amaznia IPAM. Av. Rui Barbosa, 136. CEP 68005080, Santarm-PA, E-mail:
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28 IDENTIFYING AND PRIORITIZING FOREST PATCHES KEY FOR THE SURVIVAL OF THE GOLDEN-HEADED LION TAMARIN ( LEONTOPITHECUS CHRYSOMELA S ) Sara L. Zeigler Introduction rough habitat loss and fragmentation, species often expe rience a loss in space and resources with associated changes to metapopulation dynamics and gene ow as continuous habitat is divided into small, isolated patches. e result is a decrease in survival and reproduction, ultimately reducing population abundance, range extent, and genetic diversity ( reviewed in Fahrig, 2003 ) and leaving the species vulnera ble to extinction through demographic and environmental stochasticity, genetic drift, inbreeding depression, and Alle eects ( Fischer & Lindenmayer, 2007 ). Brazils Atlantic Forest provides a prime example of how habitat loss and fragmentation can threaten native spe cies. It is one of the worlds most endangered biomes and provides habitat for a disproportionate number of species, many of which are endemic ( Myers et al., 2000 ). Only 11.73% of the original vegetation in the Atlantic Forest re mains, the majority of which is found in small fragments ( < 50 ha; Ribeiro et al., 2009 ). Deforestation has been attrib uted primarily to clear cutting for timber harvest, charcoal production, cattle ranching, and monoculture plantations ( Morellato & Haddad, 2000 ; Pinto & Wey de Brito, 2003 ) and has been linked to widespread extinctions and popula tion declines for a variety of species ( e.g. Chiarello, 1999 ; Pardini et al., 2005 ; Uezu et al., 2005 ). One species af fected by the loss and fragmentation of the Atlantic Forest is the endangered golden-headed lion tamarin (GHLT; Le ontopithecus chrysomelas ), an arboreal primate endemic to a small region of southern Bahia, Brazil (Figure 1). GHLTs preferentially use lowland primary forest, secondary/regen erating forest, and shade-cocoa agroforest ( Oliveira, 2010 ; Pinto and Rylands, 1997 ; Raboy and Dietz, 2004 ) as habi tat. A survey conducted between 1991 and 1993 provides the most recent published population estimate at over 6,000 individuals covering an area of 19,462 km 2 ( Pinto and Rylands, 1997 ). However, recent surveys suggest that the population has declined and that the total range has been reduced by 15% over the last 13 years ( Raboy et al., 2010; Raboy, unpublished data ). Persistence of the GHLTs primary habitat types is uncer tain. e majority of native vegetation throughout Brazil is found on private land where pressure for agricultural ex pansion is highest ( Ferreira et al., 2012 ; Sparovek et al., 2010 ). Between 1987 and 2007, 13% of forest cover was lost within the GHLT range ( Zeigler et al., 2010 ), and recent changes to Brazilian forestry laws are likely to in crease deforestation rates country-wide by reducing levels of enforced protection of certain areas of existing forest ( Calmon et al., 2011 ). In addition, since the early 1990s, the price of cocoa has fallen dramatically and fungal epi demics put entire plantations at risk. us, it is becoming increasingly more protable for farmers to clear cut their land for timber extraction ( Alger and Caldas, 1994 ) or for conversion to other agricultural systems like cattle ranching or management-intensive monoculture plantations that do not provide habitat for endangered species ( Cassano et al., 2009 ; Schroth and Harvey, 2007 ). Given the uncertain future of remaining habitat for GHLTs, determining which habitat patches are most valu able for GHLT populations is a conservation priority. Such knowledge is especially critical for the proactive protection of existing habitat and populations, preventing the severe population declines and limited opportunities for recovery associated with other Atlantic Forest species (e.g. Kierul et al., 2008a ; Kierul et al., 2008b c ). e objective of this paper is to synthesize recent, published results of rangewide landscape analyses of GHLT habitat to prioritize habitat for further study and protection. Methods Between 2010 and 2011, three major studies were pub lished that analyzed the spatial distribution of GHLTs and their habitat over time. Zeigler et al., ( 2010 ) created a binary forest/non-forest map of the species range using supervised classication of Landsat 5TM remotely sensed imagery taken from 2004-2008 (the forest map). ey determined that only 5% of forest patches were greater than 36ha, the smallest recorded territory size for a group of GHLTs in primary and degraded habitat ( Ry lands, 1989 ). e authors also used the population viability analysis (PVA) program Vortex ( Lacy, 2000 ) to calculate the minimum required area of habitat required for viable populations of GHLTs that were of sucient size to be able to recover from threats such as disease epidemics and re. ey then located patches meeting those size requirements on the 2007 map. ey found that 22 patches could sup port a viable population of GHLTs over 100 years (98% probability) under a baseline scenario (i.e. no additional threats), although this number decreased to 20, 9, and 6 habitat patches when they included the additional threats of disease, re, and disease with re, respectively. Only two patches were large enough to support a viable population that could also retain 98% of its genetic heterozygosity under the baseline, disease, and re scenarios, and only one patch could support such a population under the disease with re scenario. In the second study, Zeigler et al. ( 2011 ) used a graph theoretical approach and the 2007 forest map ( Zeigler et al. 2010 ) to determine patterns of habitat connectivity throughout the GHLT range. Assuming that the average GHLT would travel a maximum of 100m in non-forest matrix (J. Mickelberg, unpublished data), 95% of all
29 Figure 1 Priority forest patches for the conservation of golden-headed lion tamarins. Each patch was given a point if it was large enough to sustain a minimum viable population, large enough to support a genetically viable population, important for promoting functional landscape connectivity, or occupied based on positive survey results (Raboy et al., 2010). Patches meeting all of these requirements (patch ranking = 4; shown in black) may be disproportionately important for GHLTs and should be prioritized for further research and protec tion. All patches with at least one point (displayed in darker shades of gray) are designated with a number that corresponds to Table 1, where additional information about each patch is given (some patches are too small to be visible at this resolution).
30 Table 1. Priority forest patches for the conservation of golden-headed lion tamarins (GHLTs). Each patch was given a point if it was large enough to sustain a minimum viable population, large enough to support a genetically viable population, important for promoting func tional landscape connectivity, or occupied based on positive survey results (Raboy et al., 2010). Descriptions of patches meeting at least one of these criteria are listed here (Rank = 1-4), and patches meeting all criteria (Rank = 4) may be especially important for protection and research in the future. See Figure 1 for the locations of these priority forest patches. Patch Number Patch Area (ha) Occupied by GHLTS?* a Genetically Viable Population?* b Viable Population?* c Forest Connectivity?* d Total Rank 1 741973.30 1 1 1 1 4 2 1929.87 0 0 1 0 1 3 1555.83 0 0 1 0 1 4 4.50 1 0 0 0 1 5 1731.06 0 0 1 0 1 6 1467.54 0 0 1 0 1 7 1347.39 0 0 1 0 1 8 109.71 0 0 0 1 1 9 7.92 0 0 0 1 1 10 126.18 0 0 0 1 1 11 1492.02 0 0 1 0 1 12 1985.49 0 0 1 0 1 13 3054.60 1 0 1 0 2 14 1809.45 0 0 1 0 1 15 7149.96 1 0 1 0 2 16 4.50 1 0 0 0 1 17 8004.69 0 0 1 0 1 18 1140.03 0 0 1 0 1 19 432.99 1 0 0 0 1 20 35.64 1 0 0 0 1 21 1.80 1 0 0 0 1 22 9.72 1 0 0 0 1 23 243.72 1 0 0 0 1 24 956.97 1 0 0 0 1 25 477.99 1 0 0 0 1 26 231.84 0 0 0 1 1 27 85.68 0 0 0 1 1 28 2080.71 0 0 1 0 1 29 896.31 1 0 0 1 2 30 532.89 1 0 0 0 1 31 393.75 1 0 0 0 1 32 702.99 0 0 0 1 1 33 2026.44 0 0 1 0 1 34 160.65 0 0 0 1 1 35 806.58 1 0 0 0 1 36 44.55 0 0 0 1 1 37 59.76 1 0 0 0 1 38 4.41 1 0 0 0 1 39 4006.98 1 0 1 0 2 40 2662.92 0 0 1 0 1
31 habitat patches had no neighboring patches within this dis tance, and the median component size (i.e. forested area of a group of patches less than 100m apart) was 80ha. In general, they determined that habitat connectivity for this species was low and that 15 habitat patches were dispropor tionately important for maintaining habitat connectivity in the landscape (Zeigler, unpublished data). Finally, Raboy et al. ( 2010 ) conducted a range-wide survey to establish the location of possible GHLT populations using play-back studies and interviews with local people. By overlaying pos itive points that established the presence of GHLTs from this survey with the 2007 forest map, it was determined that 21 patches in the landscape were probably occupied by GHLTs ( Zeigler et al., 2010 ). Using the results of these three studies, I calculated a simple ranking scheme to prioritize forest patches throughout the range of the species. I created four separate geographical information system (GIS) layers in the program ArcGIS ver. 9.3 (ESRI). In the rst layer, I gave each forest patch a point if it was large enough to support a minimum viable population under baseline conditions according to Zeigler et al. ( 2010; 22 patches ). In the second layer, I gave forest patches a point if they were large enough to support a ge netically viable population under baseline conditions, also according to Zeigler et al. ( 2010; 2 patches ). e third layer contained forest patches, all given a point, if they were con sidered important for maintaining functional connectivity based on the results of Zeigler et al. ( 2011; 15 patches ). Finally, I gave forest patches a point in the fourth layer if they were known to be occupied based on positive survey results according to Raboy et al. ( 2010; 21 patches ). I then added the four GIS layers together in the raster calculator in ArcGIS to produce a single map in which forest patches could have a value ranging from zero (not meeting any of the above conditions) to four (meeting all of the above conditions). Results Within the GHLT historical distribution, only one forest patch had a ranking of while 5 and 48 patches had rank ings of and , respectively (Table 1; Figure 1). All other remaining forest patches were too small to support viable Patch Number Patch Area (ha) Occupied by GHLTS?* a Genetically Viable Population?* b Viable Population?* c Forest Connectivity?* d Total Rank 41 4003.65 0 0 1 0 1 42 13734.72 0 1 1 0 2 43 928.44 0 0 0 1 1 44 1531.08 0 0 1 0 1 45 924.03 1 0 0 0 1 46 1189.35 0 0 1 0 1 47 501.21 0 0 0 1 1 48 21.60 0 0 0 1 1 49 720.18 0 0 0 1 1 50 53.73 0 0 0 1 1 51 497.70 0 0 0 1 1 52 134.28 1 0 0 0 1 53 2621.97 0 0 1 0 1 54 37.44 0 0 0 1 1 In these columns, denotes that the patch met this requirement, and denotes that it did not. a Researchers found evidence of GHLTs in these patches during surveys of the landscape (Raboy et al. 2010). b Patches meeting this requirement are large enough to support a population of GHLTs that has at least a 98% probability of surviving for 100 years and is able to maintain at least 98% of its original genetic heterozygosity (Zeigler et al. 2010). c Patches meeting this requirement are large enough to support a population of GHLTs that has at least a 98% probability of surviving for 100 years under baseline conditions (i.e. no added threats from disease, re, etc; Zeigler et al. 2010). d Patches meeting this requirement were found to be disproportionately more important for maintaining functional habitat connectivity throughout the landscape (Zeigler et al 2011, Zeigler et al unpublished data).
32 or genetically viable populations of GHLTs, were not im portant for maintaining connectivity between patches, and were not occupied by GHLTs according to recent surveys. Discussion e ranking scheme described here oers a simple rst step for prioritizing habitat patches for the conservation of GHLTs. An ideal next step would be to conduct additional surveys on forest patches highlighted here to understand land ownership, likely plans for substantial changes to forest patches by landowners, habitat quality, and the size and condition of any GHLT groups on these patches. ey can then be further prioritized, based on the best available science, for protection or as reintroduction sites. As described in the Introduction, habitat throughout the GHLT range is vulnerable to deforestation for a variety of reasons. Ultimately, the survival of GHLTs and other Atlantic Forest species will depend on the creation of fed erally mandated protected areas, the promotion of private reserves, and the implementation of positive incentives for farmers to continue biodiversity-friendly agroforestry prac tices ( reviews in Alger and Caldas, 1994 ; Cassano et al., 2009 ; Langholz and Lassoie, 2001 ; Rambaldi et al., 2005 ; Tabarelli et al., 2005 ). In addition, it will be critical to protect forested areas throughout the species range in an eort to preserve redundant populations and the species full complement of genetic variability. Currently, protected areas within the GHLT range are exclusively found in the eastern half of the region ( Schroth et al., 2011 ) despite the fact that deforestation has historically been heaviest in the west ( Zeigler et al., 2010 ). Further research and protection of western forest patches highlighted here may be especially pertinent. Forest patches of high quality that meet one or more of the four criteria could also be prioritized as potential re introduction sites for captive-bred GHLT populations. A large and well-managed captive breeding program cur rently exists for GHLTs ( Ballou et al., 2002 ), yet these populations have rarely contributed to wild populations. Reintroductions of captive golden lion tamarins ( Leonto pithecus rosalia ) have signicantly improved the status of the wild population, contributing to the species nearly unprecedented downlisting from Critically Endangered to Endangered in recent years ( Ballou et al., 2002 ; Kierul et al., 2008a ). A similar program for GHLTs, where cap tive individuals are reintroduced into ranked forest patches highlighted in Figure 1 (particularly in the western portion of the species range), could also provide substantial conser vation benets for this species. Finally, only one forest patch (area: 741973 ha), which contains Una Biological Reserve (Figure 1), meets all four criteria in my ranking scheme (Table 1) and, therefore, may be especially important for the long-term survival of GHLTs. Although I do not advocate strict protection of this entire forest patch, eorts to minimize its fragmentation are critical. is patch was primarily composed of shadecocoa agroforests as of 1995 ( Landau et al., 2003 ) and is vulnerable to forest loss and fragmentation as small yields, low cocoa prices, and fungal epidemics make landcover conversion more protable ( Alger and Caldas, 1994 ; Cas sano et al., 2009 ; Schroth and Harvey, 2007 ). Government subsidies, price premiums for shade or fair-trade cocoa production, and other incentives for maintaining biodiver sity-friendly cshade-cocoa/forest mosaics over cattle pas tures and management intensive monoculture plantations will be critical for the persistence of GHLTs (and other At lantic Forest species) and should be encouraged ( Cassano et al., 2009 ; Schroth et al., 2011 ). Such mechanisms would allow farmers to be protable while supporting biodiversity conservation. Acknowledgments Data presented here are the culmination of my disserta tion work at the University of Maryland. I am grateful to Becky Raboy, Leonardo Oliveira, James Dietz, and Jennifer Mickelberg for sharing their survey locations and data on GHLTs. In addition, this manuscript was greatly improved from discussions with and feedback from William Fagan, Ruth DeFries, Maile Neel, Becky Raboy, Ralph Dubayah, and Christopher Justice. Funding was provided by the Smithsonian Institutions Graduate Research Fellowship, the Explorers Club of Washington DCs Exploration and Field Research Grant, the Department of Geography at the University of Maryland, and the University of Marylands Ann G. Wylie Dissertation Fellowship. Sarah Zeigler Department of Geographical Sciences, University of Maryland, College Park MD 20742, email:
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34 CORREO DA DISTRIBUIO GEOGRFICA DO PARAUACU-CINZA ( PITHECIA IRRORATA GRAY 1842) NO LIMITE SUDOESTE DA AMAZNIA BRASILEIRA Ricardo Sampaio Robson Odeli Espndola Hack Kurazo Mateus Okada Aguiar Adriana Akemi Kuniy Jos de Sousa e Silva Jr Introduo Pithecia irrorata (Primates: Pitheciidae) uma espcie de primata amaznico conhecido pelo nome comum de pa rauacu ou macaco-velho. Esta espcie foi descrita por Gray (1842) e, de acordo com Hershkovitz (1987), sua locali dade tipo a margem esquerda do rio Tapajs, no interior do Parque Nacional do Amaznia, Estado do Par, Brasil. A distribuio geogrca de Pithecia irrorata foi atualizada por Hershkovitz (1987). Na Figura 1(p. 390), Hershkovitz (1987) representou a distribuio da espcie em forma de polgono, indicando que esta distribuio estaria restrita regio situada ao sul do rio Solimes-Amazonas, oeste dos rios Tapajs e Juruena, norte dos rios Guapor e Madre de Dios, e leste do rio Juru, nos estados brasileiros do Par, Amazonas, Acre e Rondnia, e tambm no sudoeste do Peru (Departamento de Madre de Dios) e noroeste da Bo lvia (Provncia de Pando). O mapa da Figura 1 de Hers hkovitz (1987) serviu como base para a construo do mais recente polgono de distribuio geogrca de P. irrorata (Patterson et al ., 2007; Veiga, 2009; Fig. 1). Na mesma obra, Hershkovitz (1987) apresentou outro mapa (Figura 2; p. 392), indicando os locais de coleta das amostras utilizadas no trabalho. Comparando-se os dois mapas, foi possvel vericar uma incongruncia entre os mesmos. Duas localidades (stio # 114 [15'S; 59'W] e stio # 117 [14'S; 57'W]) indicadas na Figura 2 esto situadas fora do polgono apresentado na Figura 1. Baseado em fontes bibliogrcas (Miranda Ribeiro, 1914; Wagner, 1848), Hershkovitz (1987) indicou que o espci me oriundo do stio # 114 havia sido obtido por J. Natterer no ano de 1826, nas orestas de Cravari, estado de Mato Grosso (Wagner, 1848), e o espcime proveniente do stio # 117 havia sido coletado por F. Hoehne em Tapirapu, rio Cipotuba, estado de Mato Grosso (Miranda Ribeiro, 1914). O objetivo do presente estudo esclarecer o equvo co ocasionado pela incongruncia observada nas guras de Hershkovitz (1987). A conrmao da presena de P. irro rata na regio em questo reforada por dados de campo, estabelecendo-se novos registros para a espcie. Metodologia Os registros apresentados no presente estudo foram obtidos em dois inventrios independentes de primatas no estado de Mato Grosso (Fig. 1). Nesta regio, a vegetao natural composta por orestas tropicais midas, orestas de tran sio e manchas de cerrado nas pores mais meridionais (RADAMBRASIL, 1978; Daly e Prance, 1989). Contudo, as atividades humanas alteraram signicativamente esta pai sagem nas ltimas dcadas (Fearnside, 2005). O primeiro stio de amostragem est localizado no municpio de Bras norte (Stio # 1: 12'S, 57'W). Dezenove incurses foram realizadas durante todos os nais de semana, no pe rodo de fevereiro a junho de 2009, em trs fragmentos o restais situados em torno da Pequena Central Hidreltrica Bocaiva, com extenses de 306, 450 e 600 hectares. Ca minhadas aleatrias em trilhas j existentes, bem como em bordas de mata e estradas de terra no interior dos fragmentos foram realizadas. O perodo de amostragem de campo/nal de semana foi de 24 horas. O esforo total de amostragem Figura 1 Distribuio geogrca de Pithecia irrorata (em cinza), de acordo com Hershkovitz (1987), Patterson et al ., (2007) e Veiga et al ., (2008). Os crculos (# 114 e # 117) correspondem aos stios apresentados por Hershkovitz (1987). As estrelas rep resentam os novos registros de Pithecia irrorata numerados de acordo com o texto. Figura 2 Indivduo de Pithecia irrorata observado em Chupin guaia-RO. Foto: Kurazo Matheus Okada Aguiar.
35 foi de 456 km. Um chamariz ( playback ) com vocalizaes do txon identicado por Emmons et al (1997) como Pithecia monachus foi utilizado para facilitar as buscas. O segundo stio est localizado entre as cidades de Vila Bela da Santssima Trindade e Pontes e Lacerda (Stio # 2: 59'W, 15'S). Os registros foram feitos em uma tran seco de 5 km atravs da metodologia Rapeld (Magnusson et al ., 2005), em novembro de 2009. O esforo de amos tragem foi de 40 km. As identicaes de Pithecia irrorata foram baseadas na chave de identicao de Hershkovitz (1987). Alm disso, fotograas feitas nos dois stios foram posteriormente utilizadas para conrmao da identi cao dos animais (Fig. 2), por comparao direta com os exemplares de Pithecia irrorata pertencentes ao acervo do Museu Paraense Emlio Goeldi. Resultados No Stio # 1, Pithecia irrorata foi registrada em apenas um fragmento orestal de 306 ha, na margem direita do rio Cra vari, um auente de segunda ordem do rio Juruena. Somente uma observao (dois indivduos adultos) foi realizada. No Stio # 2, os registros foram feitos em um fragmento de o resta sazonal semi-descdua de 400 ha. Neste stio, ocorreram cinco observaes de Pithecia irrorata Na primeira, obser vou-se um grupo composto por trs indivduos. Na segunda, foi possvel visualizar quatro animais. As demais observaes foram de indivduos aparentemente sozinhos. Discusso e concluso Os resultados sugerem que os registros #114 e 117 de Her shkovitz (1987) so dedignos, uma vez que esto situados na mesma regio inventariada no presente estudo. Assim, o limite sudeste da distribuio geogrca de Pithecia irrorata estendido para alm da margem direita do rio Guapor e da margem esquerda do rio Juruena (Figura 1). possvel que o limite natural da distribuio da espcie coincida, nesta regio, com os limites entre a vegetao de oresta e a de cerrado. O renamento deste conhecimento carece de mais investigaes de campo, uma vez que os dados sobre a distribuio de P. irrorata nesta regio ainda so escas sos. De acordo com Sampaio et al (2012), existem grandes fragmentos de oresta situados prximo s reas investiga das no presente estudo. Tais fragmentos so representados por Terras Indgenas (TI), tais como as TI de Enawen Naw, Nambiquara e o complexo de TI Paresi-UtlaritiTlrecatinga (Mato Grosso), e tambm TI menores, tais como as TIs Vale do Rio Guapor, Sarar e Irantxe/Manoki (Mato Grosso), as quais podem abrigar populaes viveis e apresentam um grande valor de conservao para esta es pcie e demais primatas da regio. Agradecimentos DM Construtora de Obras Ltda., que forneceu apoio logstico no Stio # 1. Ricardo Sampaio Coordenao de Pesquisas em Ecologia, Instituto Nacional de Pesquisas da Amaznia (INPA), C.P. 478, 69011-970, Manaus, Amazonas, Brasil e Colees Zoolgicas, Instituto Nacional de Pesquisas da Amaznia (INPA), Manaus, Amazonas, Brasil, e-mail:
36 distribuio geogrca de Callicebus cinerascens (SPIX, 1823). Mastozool. Neotrop. 19(1): 159164. Veiga, L. M. e Marsh, L. 2008. Pithecia irrorata In: IUCN 2010. IUCN Red List of reatened Species. Version 2010.1. website: http://www.iucnredlist.org. Acessada em 26 de abril de 2010. Wagner, J. A. 1948. Beitrge zur kenntniss des sugethiere Amerikas. Dritte Abteilung. Vierte Ordnung. Abhan dlungen der Akademie der Wissenschaften. Munchen 5:405480. PREDATION ATTEMPT ON A ROADKILLED BROWN-EARED WOOLLY OPOSSUM ( CALUROMYS LANATUS ) BY A BLACK-HORNED CAPUCHIN ( SAPAJUS NIGRITUS ) Francesca Belem Lopes Palmeira Camila Camara Pianca Hunting and scavenging of vertebrates by nonhuman pri mates has been recorded widely across the world (Butyn ski, 1982). Researchers have observed predation of small amphibians, reptiles, birds and mammals by several dier ent primate species (Boinski and Timm, 1985; Wrangham and Riss, 1990; Heymann et al., 2000; Poulsen and Clark, 2001; Begotti and Landesmann 2008; Silva et al., 2008). However, capuchins, chimpanzees and baboons are the only non-human primates known to prey systematically upon relatively large vertebrates (Rose, 1997). Capuchin monkeys have consumed a variety of vertebrate prey such as frogs (Izawa, 1978); lizards, birds, bats (Fedigan, 1990; Rose, 1997; Rose et al., 2003); opossums ( Didelphis sp.), rats ( Rattus rattus ) (Resende et al., 2003); mice ( Rhipidomys sp.) (Milano and Monteiro-Filho, 2009); squirrels ( Sciurus aestuans S. variegatoides ) (Galletti, 1990; Cunha et al., 2006); coati pups ( Nasua narica ) (Newcomer and Fancy, 1985; Fedigan, 1990; Perry and Rose, 1994; Rose et al., 2003); anteater juveniles ( Tamandua mexicana ) (Rose et al., 2003); and even other primates, such as titi monkeys, Callicebus moloch (Sampaio and Ferrari, 2005), and owl monkeys Aotus brumbacki (Carretero-Pinzon et al., 2008). Here we describe an opportunistic attack attempt on a road-killed brown-eared woolly opossum ( Caluromys lana tus ) by a black-horned capuchin monkey ( Sapajus nigritus ) during a fortuitous encounter in a disturbed fragment in the Brazilian Atlantic Forest. On November, 30 th 2003, at around 1000 h, we collected ad libitum data on a black-horned capuchin attacking a brown-eared woolly opossum that had been hit by a car, in the Ecological Station of Ribeiro Preto, Mata Santa Tereza (21 S; 47 W), a semi-urban area of 154.16 ha in Ribeiro Preto, in the northeast of So Paulo state, Brazil. Mata Santa Tereza is an isolated forest frag ment and has a large population of these capuchin mon keys (Amaral et al., 2005). Although the group has been well studied (Siemers, 2000; Amaral et al., 2005; Machado et al., 2012), this is the rst report of this particular behav ior. e brown-eared woolly opossum was still alive on the ground, with its organs exposed (Fig. 1a), when an adult male black-horned capuchin monkey, that was standing on the ground (Fig. 1b), approached the fatally injured woolly opossum and started to attack the animal viscera while the rest of the capuchin group watched at the edge of the road. ere was high trac volume on the road that day, and the predation attempt was interrupted by the approach of a car, which caused the capuchin to run away towards the forest adjacent to the road. Perhaps, Mata Santa Tereza does not have enough feeding resources to support this large monkey population and food shortage is a common situation faced by the group. It may also be important that, especially on weekends and holi days, local people feed these capuchins a variety of foods such as bananas, eggs, peanuts, bread and other snacks. In most cases, individuals descend to the ground to get the food from the visitors hands. So, these monkeys may have learned to patrol the road for peoples food and also are aware of other opportunities such as road-killed animals, which could serve as alternative food source available in this area. Siemers (2000) observed that the capuchins of Figure 1. (a) Road-killed Brown-eared woolly opossum ( Caluromys lanatus ) and (b) Black-horned capuchin ( Sapajus nigritus ) in the Eco logical Station of Ribeiro Preto, northeastern of So Paulo state, Brazil (Photos: Camila Camara Pianca).
37 Mata Santa Tereza remained on the forest oor and did not ee to higher strata when humans passed. ey often foraged for food voluntarily or accidentally dropped by humans on the ground. Also, the monkeys predominantly traveled in low forest strata and spent more time close to the ground than in the canopy. In general, predation of mammals or other vertebrates by monkeys is usually performed during a period of food shortage or through intraspecic social learning (Resende et al., 2004). Apparently, seasonality is not an important factor in the occurrence of vertebrate predation by capu chins. Dierent surveys on predation by capuchins have been recorded during the dry season which is also the birth ing season of most prey species (Fedigan, 1990), but also in the wet season (Rose, 1997) or even with the same frequen cy in dry and wet seasons (Ferreira et al., 2002). Appar ently, there is a sex dierence in frequency of predation by capuchins, since adult males tend to catch more prey than females (Fedigan, 1990; Rose, 1997; Ferreira et al., 2002). In addition, capuchins tend to select prey items by size and age; for example, they preferentially search for infants or ju veniles of large mammals, such as for coatis, anteaters and other primates (Rose, 1997; Rose et al., 2003; Sampaio and Ferrari, 2005). However, injured or killed animals could be consumed opportunistically by capuchins regardless of their age or size (Carretero-Pinzn et al., 2008). erefore, further detailed surveys are needed to determine the condi tions under which predation of large mammals by capu chin monkeys can occur. Francesca Belem Lopes Palmeira Postgraduate Program in Forestry Resources, Department of Forestry Sciences, Luiz de Queiroz College of Agriculture, University of So Paulo (ESALQ/USP), Av. Padua Dias 11, CP 9, CEP 13418-900, Piracicaba, SP, Brazil, Email:
38 Resende, B. D., Greco, V. L. G., Ottoni, E. B. and Izar, P. 2003. Some observations on the predation of small mam mals by Tufted capuchin monkeys ( Cebus apella ). Neo trop. Primates 11(2): 103104. Resende, B. D., Mannu, M., Izar, P. and Ottoni, E. B. 2004. Interaction between Capuchins and Coatis: nonagonistic behaviors and lack of predation. Int. J. Primatol. 24(6): 12131224. DOI 10.1023/B:IJOP.0000043959.12073. bc. Rose, L. M. 1997. Vertebrate predation and food-sharing in Cebus and Pan Int. J. Primatol. 18: 727765. Rose, L. M., Perry, S., Panger, M. A., Jack, K., Manson, J. H., Gros-Louis, J., Macknnon, K. C. and Vogel, E. 2003. Interspecic interactions between Cebus capucinus and other species: data from three Costa Rican sites. Int. J. Primatol. 24(4): 759796. Sampaio, D. T. and Ferrari, S. F. 2005. Predation of an infant Titi monkey ( Callicebus moloch ) by a Tufted capu chin ( Cebus apella ). Folia Primatol. 76: 113115. DOI: 10.1159/000083617. Siemers, B. M. 2000. Seasonal variation in food resource and forest strata use by brown capuchin monkeys (Cebus apella) in a disturbed forest fragment. Folia Primatol. 71: 181184. DOI: 10.1159/000021739. Silva, I. O., Alvarenga, A. B. B. and Boere, V. Occasional eld observations of the predation on mice, dove and ants by black-tufted-ear marmosets ( Callithrix penicil lata ). Neotrop. Primates 15(2): 5962. Wrangham, R. W. and Riss, E. Z. B. 1990. Rates of preda tion on mammals by Gombe chimpanzees, 19721975. Primates 31(2): 157170. DOI 10.1007/BF02380938. PARASITOS GASTROINTESTINALES EN EL MONO CHORO COLA AMARILLA ( OREONAX FLAVICAUDA ) Y EL MONO NOCTURNO ANDINO ( AOTUS MICONAX ) EN AMAZONAS, PERU Jssica Snchez Larraaga Sam Shanee Introduccin El parasitismo es un fenmeno ecolgico de asociacin sim bitica donde solo uno de los organismos de dicha asocia cin se benecia y el otro la tolera (Campillo, 1999). Existe as una estrecha relacin entre el parsito y el husped la cual acta como una fuerza para la seleccin natural, afec tando por ende los patrones de densidad y la distribucin de las especies (Stoner et al, 2005; Gillespie et al, 2005). Dentro de los factores que inuyen en el parasitismo de los primates estn la densidad poblacional, factores climticos, comportamientos, factores reproductivos y, lo ms impor tante, su dieta y la fragmentacin del hbitat (Scott, 1988; Serrano, 1998; Stoner et al, 2005). En el bosque de El Toro se puede observar la presencia humana y de animales domsticos por algunas zonas ya que se ha iniciado la fragmentacin del bosque, y esto in uye en el aumento de la carga parasitaria. El mono choro cola amarilla ( Oreonax avicauda ) es endmico del Per (Macedo Ruiz y Mittermeier, 1979; Leo Luna, 1987), habita los bosques nublados de la vertiente nororiental de los Andes a una altitud de 1,500 2,700 msnm, encon trndolos en los departamentos de Amazonas y San Martn (Leo Luna, 1980; Shanee, 2011) as como en pequeas reas de las regiones de Hunuco y La Libertad (Shanee, 2011; Graves y ONeil, 1976). El mono nocturno Andino ( Aotus miconax ) tambin es endmico del Per y comparte mucha de su distribucin con el mono choro cola amarilla (Shanee, 2011). Su extensin es un tanto ms amplia latitu dinalmente, hasta los 3,000 msnm., y llega ms al sur en el departamento de Hunuco. Su distribucin actual no es del todo conocida y falta muchos datos para evaluar su estado de conservacin. El hbitat de ambas especies se caracteriza por ser zonas de empinados desladeros y barrancos. La extensin original del hbitat de Oreonax avicauda se estima en alrededor de 11,000 km (Leo Luna, 1982). Estudios actuales reportan que el hbitat de esta especie ha decrecido quedando entre 6,000 y 7,000 km (Buckingham y Shanee, 2009). Oreonax avicauda se encuentra reportado por la UICN como es pecie en peligro crtico de extincin (lista Roja A4c). Aotus miconax se encuentra en UICN como especie vulnerable a la extincin (Lista Roja A2c). En La Esperanza ambos especies estn presentes en varios tipos de hbitat y niveles de disturbio antropognico. Las densidades poblacionales de las especies son medio altas y se encuentran fcilmente (Shanee y Shanee, 2011; en prensa). El objetivo de la pre sente investigacin fue determinar la presencia de parsitos en estas especies endmicas de primates, ya que ste puede ser uno de los factores que pone en riesgo el bienestar de sus poblaciones. Materiales y mtodos Area de estudio El presente estudio se realiz en La Esperanza, un pueblo situado en la comunidad campesina Yambrasbamba, Pro vincia de Bongar, Regin Amazonas, Per. Las muestras se tomaron en un bosque primario localmente llamado El Toro. La temperatura media en el rea es de entre 15 y 25 C, con precipitacin fuerte durante todo el ao con una pequea sequa entre Mayo y Setiembre. El bosque primario est a una altitud de 1,920 msnm Esta rea se forma al extremo sur de un bosque continuo hasta el Ro Maran en el Norte (~115 km). Recoleccin de muestras y procesamiento Durante los meses de Marzo y Mayo del 2011 se recolect un total de 33 muestras de heces procedentes de Oreonax avicauda y Aotus miconax Las muestras se tomaron me diante una tcnica no invasiva que consisti en la recolec cin manual de estas inmediatamente despus de la defeca cin, la cual se realiz con mayor frecuencia despus de los
39 periodos de descanso y antes de iniciar su desplazamiento, principalmente en el caso de O avicauda Para la reco leccin de las muestras de A. miconax primero se identi caron los nidos, y se tomaron las muestras principalmente antes de que los animales iniciaran su desplazamiento y du rante esta actividad pero en menor proporcin. Se tomaron muestras de dos grupos diferentes de O. avicauda con un tamao de grupo cada uno de 18 y 15 miembros, donde recogieron 12 y 13 muestras individuales respectivamente. En el caso de A. miconax se encontr un solo grupo sin poder determinar el tamao, tomando del mismo nido por 3 das consecutivos un total de 8 muestras. Las muestras se colocaron en un envase plstico con tapa rosca, posteriormente se le adicion formol al 10% y luego fueron refrigeradas para su conservacin hasta el traslado al laboratorio de biologa-microbiologa de la Universidad nacional Toribio Rodrguez de Mendoza en la ciudad de Chachapoyas donde fueron analizadas por los autores. Las muestras de heces fueron procesadas mediante la tcnica de otacin con solucin sobresaturada de cloruro de sodio, solucin shater y la tcnica de sedimentacin. As mismo se procedi a realizar un pool cada 02 o 03 muestras rea lizando sedimentacin en mallas metlicas; y se examin a travs de un microscopio electrnico determinando la pre sencia de trofozoitos o quistes de protozoarios, as como huevos, larvas o adultos de nemtodos gastrointestinales, mediante las caractersticas morfolgicas correspondientes a cada una. Resultados De las 33 muestras estudiadas 21 (64%) resultaron ser po sitivas al menos a una forma parasitaria; en las muestras de Aotus miconax y Oreonax avicauda se pudo hallar infec ciones mltiples de protozoarios y nemtodes. (Tabla 1). Los resultados fueron diferentes para las dos especies en estudio. En el caso de Oreonax avicauda se encontraron dos clases de nemtodos; Strongydoides spp. y Trichuris spp., y protozoarios como Iospora spp Endolimax spp; se encon tr adems un mayor nmero de casos de infeccin por Eimerias spp. En Aotus miconax se encontr un caso de Strongylodes spp. y de protozoarios solo se hall Eimeria spp. (Tabla 2). Discusin Este es el primer estudio parasitolgico realizado en mono choro cola amarilla ( Oreonax avicauda) y mono nocturno Andino (Aotus miconax) Tanto en O. avicauda y A. mico nax se registr la presencia de parsitos. Debe considerar se que las muestras fueron tomadas del mismo bosque, y el primer grupo de individuos muestreados comparten el mismo areal de distribucin con los A. miconax. Se aprecia Tabla 1. Porcentaje de frecuencia de parsitos gastrointestinales en Oreonax avicauda y Aotus miconax Especie Resultados N muestras Nemtodes Protozoarios N N % N % Aotus miconax 8 1 13% 2 25% Oreonax avicauda Grupo N (n:18 individos) 12 3 25% 10 83% Grupo N (n:15 individuos) 13 2 15% 6 46% Total 25 5 20% 16 64% Tabla 2. Porcentaje de grupos de parsitos encontrados en Aotus miconax y Oreonax avicauda de acuerdo a la zona de estudio. Parsitos encontrados A. miconax O. avicauda Nemtodes Muestras positivas % total de muestras Muestras positivas % total de muestras Strongyloides spp 1 13% 3 12% Trichuris spp. 3 12% Protozoos Eimeria spp. 2 25% 12 46% Iospora spp. 5 19% Endolimax spp. 2 8% Total 3 38% 25 100%
40 la relacin existente entre parsito-hospedero ya que fac tores como la composicin de la dieta afecta considerable mente esta relacin. Existen compuestos secundarios pre sentes en algunas plantas que pueden tener efecto adverso en los organismos (Freeland, 1983); cualquiera de los me canismos del husped relacionado con la resistencia gene ral y especcamente el parasitismo tiene una importante relacin con la dieta (Stoner et al, 2005). Estudios demues tran que existen ciertas partes de las plantas, entre ellas los frutos, que tienen efecto antiparasitario y que los animales de forma instintiva pueden usarlas en aquellos momentos que se sienten en mal estado, probablemente por un au mento en su carga parasitaria (Stoner et al, 2005; Human, 1997; Martnez Esquivel, 2010). En investigaciones de Aotus spp. se han reportado con ante rioridad casos de Strongyloides spp. (Perea-Rodriguez et al, 2010; Tantalean y Gonsalo, 1994). En el presente estudio se puede apreciar que existen diferencias en los resultados entre las dos especies de primates, a pesar de que ambas comparten el mismo hbitat. Puede ser que Aotus miconax tiene una alimentacin diversa y/o selectiva en compara cin con O. avicauda ; de igual manera debe considerarse que en el caso de los primates en vida silvestre muchas veces estos hacen inmunidad a los parsitos as como tambin que los parsitos en especial los protozoarios son parte de la compleja biologa de sus hospederos (Campillo, 1999) y necesitan una carga parasitaria elevada para causar signos clnicos. Finalmente, hay que mencionar que pudimos tomar algu nas muestras de A. miconax (t= 03) en un parche cercano al poblado de La Esperanza, donde hallamos que el 100% son positivas a infeccin parasitaria (datos sin publicar). Estos resultados son un punto de partida para futuras investiga ciones, en las cuales se pueda considerar el tomar muestras de otros grupos de O. Flavicauda y A. miconax, tanto en bosques primarios continuos como en parches, y aportar al entendimiento de la dinmica de la parasitosis en estos primates. Agradecimientos Agradecimiento a los guas de la zona y a la Universidad Nacional Toribio Rodrguez de Mendoza-Chachapoyas por brindarnos los equipos e instalaciones para el proce samiento de muestras. Tambin agradecimos el DGFFS del Ministerio de Agricultura por permiso de investigacin (N 384-2010-AG-DGFFS-DGEFFS). Este trabajo fue realizado gracias a nanciamiento de Neotropical Primate Conservation. Jssica Snchez Larraaga Universidad Nacional Jorge Ba sadre Grohmann, Tacna, Per, e-mail:
41 monkeys ( Aotus azarai azarai ) in the Argentinean Chaco. Neotrop. Primates. 17: 711. Scott, M. E. 1988. e impact of infection and disease on animal populations: implication for conservation biol ogy. Conserv. Biol 2:4056 Serrano, M. A. 1998. Incidencia de protozoarios gastroin testinales en primates de zoolgico de Zangano de Ca milaya, Estado de Mxico. Tesis profesional de Mdico Veterinario y Zootecnista. Universidad Autnoma del estado de Mxico. 98pp. Toluca, Mexico. Shanee S. 2011. Distribution survey and threat assessment of the yellow tailed woolly monkey ( Oreonax avicauda ; Humboldt 1812), north eastern Peru. Int. J. Primatol. 32: 691-707. Shanee, S. and Shanee, N. 2011. Observations of Terres trial Behaviour in the Peruvian Night Monkey (Aotus Miconax) in an Anthropogenic Landscape, La Esperanza, Peru. Neotrop. Primates. Stoner, K. E., Gonsalo-di-Pierro, A. M. and MaldonadonLopez, S. 2005. Infecciones de parsitos intestinales de primates: Implicaciones para la conservacin. Rev. virtual Universidad y Ciencia Nmero especial II : 6172. Tantalean, M., Gozalo, A. 1994. Parasites of the Aotus monkey. In: Aotus: e Owl Monkey J. F. Baer, R. E. Weller, and I. Kakoma (eds.), pp 354373. San Diego, Academic Press. TWINS AND INFANTICIDE IN RED HOWLER MONKEYS INHABITING A FRAGMENT IN WESTERN ORINOQUIA Marta L. Beltrn Pablo R. Stevenson Twinning is rare in anthropoid primates, but it occurs in a variety of species, including New World atelid monkeys (Link et al., 2006). is reproductive strategy is common in some small primates (e.g., Callithrichinae), but it does not seem to be appropriate for larger species, for which the cost of simultaneously rising two infants is quite high (Chapman and Chapman, 1986; Link et al., 2006). Simi larly, infanticide (the killing of an infant) is an uncommon primate behavior. is occurs particularly when a mature male wins alpha status and kills unrelated infants. e loss of the infant allows the mother to become receptive sooner and to mate with the new, infanticidal male, likely increas ing his reproductive success (i.e. sexual selection hypoth esis; van Shaik 2000). Infanticide has been documented in several populations of howler monkeys (Crockett, 2003). In this note we report an unusual case of twinning and infanticide in red howler monkeys ( Alouatta seniculus ). e observation took place during a socio-ecological study in Santa Rosa Farm, located in San Martn (Meta, Colom bia) (3.10N, 73.20W, 373 m a.s.l). e study group, composed of two adult males, two adult fe males, one juvenile male, and one infant male, ranged over 12 ha within a forest fragment of 32 ha. Changes in alpha male status were observed three times during a period of six months (February-August 2004). On July 18 th we were following the subordinate adult male (Tamarindo) and the alpha male (Die) was not observed that day. Both males showed injuries and we suspected a recent change in alpha male status, since Die did not rejoin the group. In the morning we noted that one of the adult females (Juana) was giving birth. e infants tail was rst ob served and then its hind limbs. Five minutes later (8:15 h), half of the infants body was outside, but the mother was unable to completely pull it out. e infants head was still inside after 45 minutes of delivery. More than two hours later (11:28 h) the female nally took out the infant, but it was dead. e mother held it for about 10 min. and, then, dropped it at 11:40 h. Our inspection of the infant suggested that it died asphyxiated by the umbilical cord. Surprisingly, there was another infant attached alive to the cord, but about one third the size of the dead one. We placed the second infant on the forest oor closer to the mother. She went down to the ground after hearing the infant screaming, but probably because of its small size and its attachment to the placenta, it was unable to grab the mothers fur. She took the infant and went to the canopy, where the adult male approached her and took the infant. e male quickly bit the infants head and dropped it in the creek, where it died. We suggest that twinning may incur mechanical complica tions during delivery. Although the resident males fought the day before the infanticide (as expected by the sexual selection hypothesis), we do not know which male had sired the infants. erefore, it is not possible to conrm the attack completely ts the sexual selection hypothesis. Acknowledgements We are very grateful to Snchez family, for the logistic sup port and for allowing us to carry out the study in Santa Rosa farm. Marta L. Beltrn and Pablo R. Stevenson Centro de In vestigaciones Ecolgicas La Macarena. Depto. Ciencias Biolgicas, Universidad de Los Andes. Bogot, Colombia; e-mail:
42 Link, A., Palma, A. C., Velez, A. and De Luna, A. G. 2006. Costs of twins in free-ranging white-bellied spider mon keys ( Ateles belzebuth ) at Tinigua National Park, Colom bia. Primates 47:131139. van Schaik, C. 2000. Infanticide by male primates: the sexual selection hypothesis revisited. In: Infanticide by Males and its Implications C. van Schaik and C. H. Janson (eds.), pp. 2760. Cambridge University Press, Cambridge. MORPHOMETRIC DATA FROM A WILD FEMALE TITI MONKEY, CALLICEBUS CUPREUS Eckhard W. Heymann Jenni G. Prez Yamacita Britta Mller Body size and the size of organs and other body structures are intimately related to the life history and ecology of a species (Temerin et al. 1984). Comparative analyses of data from dierent taxa can reveal allometric relationships and the adaptive value of dierent body or organ size (Martin 1990, Terborgh 1983). E.g., Terborgh (1992) showed the Table 1. Morphometric measurements from the Callicebus cupreus female and comparative data from the literature is report Hill 1960 Hershkovitz 1990 Bicca-Marques et al. 2002 Peres 1993 Ferrari & Lopes 1995 External measurements Body mass [g] 720 1106 (1000-1175) 750, 900 860, 970 880 # 1020 Head-body length [mm] 285 325, 310 337 (270-410) 280, 310 302, 358 Tail length [mm] 475 440, 420 439 (405-470) 340, 440 412, 414 Hind foot length [mm] 89 100, 95 92 (85-100) 89, 91 Skull length [mm] 67.7 65 63.9 (60.0-66.8) Zygomatic breadth [mm] 42.2 41.25 39.0 (36.0-42.0) Orbital breadth [mm] 37.2 Braincase width [mm] 39.8 Postorbital restriction [mm] 31.4 Across molars [mm] 19.9 C 1 C 1 [mm] 12.0 13.7 (12.9-15.0) C1 C1 [mm] 8.7 P 2 M 3 [mm] 15.1 15.4 M 1 (right) breadth [mm] 4.4 M 2 (right) breadth [mm] 4.1 M 3 (right) breadth [mm] 3.3 Mandibular height [mm] 35.4 Orbita height [mm] 1.7 Orbita breadth [mm] 1.4 Internal organs Liver mass [g] 25.5 Kidney mass [g], right left 3.5 4.8 Adrenal length [mm], right left 5 7 Spleen mass [g] 3.25 Small intestine length [mm] 950 944 # 1056 Caecum length [mm] 100 Large intestine length [mm] 435 324 # 521 Pluck (lung, heart, trachea, tongue) [g] 9.75 Data for male C. cupreus only; # Callicebus caligatus; Callicebus moloch; Hill (1960) provides a mean of two males and three females; Peres (1993) gives 716 and 770 mm, but this is likely to be head-body-tail length, values listed here are therefore the value given by Peres minus tail length
43 relationship between primate body size and dietary strate gies. Ferrari et al. (1993) compared gut proportions of a specialized and an opportunistic gum feeder and showed the former to have a comparatively larger caecum, as an ad aptation to the fermentation of gums. Morphometric data from skulls and skeletons can be obtained from museum material, but data on fresh body mass and on organ size or mass are generally not available from museum specimen. Given ethical implications and the increasing threat to wild primates, collecting wild primates for the purpose of ob taining organ size data is prohibitive. It is therefore impera tive to exploit opportunities for taking morphometric data without collection, e.g. when a fresh carcass is found. In this paper, we report morphometric data from a wild female red titi monkey, Callicebus cupreus at the Estacin Biolgica Quebrada Blanco (EBQB) in north-eastern Pe ruvian Amazonia. is female was a member of one study group and found in a comatose state below the sleeping tree on early morning of 29 September 2002. It died a few hours later and was subjected to a eld necropsy by the senior author, a trained veterinarian. For a detailed case report and the pathological ndings see Mller et al. (2010). We measured body mass, head-body length, tail length and hind foot length on the fresh carcass with Pesola spring balances and a Vernon calliper, respectively. Skull length was measured before the braincase was opened for brain inspection and removal. After necropsy, skull and skeletal material were buried, to allow for decomposition of esh, and recovered later. Unfortunately, part of the material was taken by scavengers. e remaining material was stored at EBQB and measured with a Mitutoyo CD-20DCX digital calliper by the rst author in October 2012. Each variable was measured three times with and values were averaged. Morphometric data collected before and during necropsy, and from the skull and skeletal material are provided in Table 1, together with data compiled from the literature. For many measurements taken here, actually no compara tive data are available from the literature. Most skeletal and dental measurements are within or close to the range of values reported in the literature. e comparatively low body mass is likely due to the diseased condition. It should be note that data for liver, spleen and adrenal, perhaps also for kidney may also represent pathological conditions (Mller et al. 2010). Acknowledgements e study during which these data were collected was supported by a grant from the Deutsche Forschungsge meinschaft to EWH (DFG He 1870/13-1) and from the Deutsche Akademische Austauschdienst (DAAD) to BM, and carried out under permission from the Instituto Nacio nal de Recursos Naturales (INRENA) in Lima (Peru). We thank Ney Shahuano Tello for eld assistance, and biology students Victor Raygada Guerra and Cristina Lopez Wong from the Universidad Nacional de la Amazona Peruana in Iquitos (Peru) for their help with the eld necropsy. Eckhard W. Heymann Abteilung Verhaltenskologie & Soziobiologie, Deutsches Primatenzentrum, Kellnerweg 4, 37077 Gttingen, Germany, e-mail:
44 ALOUATTA CARAYA : NUEVO SITIO DE ESTUDIO EN ARGENTINA Gabriela Bruno Carola Milozzi Marta D. Mudry Introduccin Dentro de la familia Atelidae, los monos aulladores (gnero Alouatta ) tienen una de las distribuciones geogrcas ms amplias, extendindose desde el sur de Mxico hasta el norte de Argentina (Crockett y Eisenberg, 1987; Zunino et al., 2001). Groves (2001; 2005) reconoce 10 especies para el gnero. De stas especies dos llegan a la Repbli ca Argentina: Alouatta guariba clamitans y Al ouatta caraya Humboldt, 1812 (Cabrera, 1939). Alouatta caraya posee una amplia distribucin en Sudamrica, en Argentina, el lmite sur de su distribucin, se encuentra al Este de For mosa y Chaco, NE de Santa Fe, el centro de Corrientes y Misiones (Brown y Zunino, 1994). A nales del 2008 se realizaron salidas de campo a un nuevo sitio de estudio conocido como: Las Lomas, (27 23' S; 58 22' O), campo privado de 623 ha en la loca lidad de San Cosme, Provincia de Corrientes, Argentina (Fig. 1). La temperatura media anual es 21C y las preci pitaciones medias anuales son de 1,200 mm. All se cons tat la presencia de varias tropas de aulladores. Segn Ca brera (1976) y Carnevali (1994) forma parte del Distrito Oriental Chaqueo, Sub-distritos: Correntino, a su vez dividido en Parque Chaqueo Correntino (sector No roeste). El Chaco Oriental est compuesto por un mosaico de bosques, palmares, pastizales, pajonales y esteros. Las es pecies ms caractersticas de estos bosques los quebrachos ( Schinopsis spp ), el urunday ( Astronium balansae ), y el virar ( Ruprechtia laxiora ). En las zonas ms bajas se desarrollan bosques de algarrobos ( Prosopis spp ) acompaados de talas ( Celtis spinosa ) y palmeras caranday ( Trithrinax sp). En forma de isletas de monte aparecen especies vegetales tpi cas como el alecrn ( Holocalyx balansae ), la palmera pind ( Syagrus romanzoana ), el timb ( Canthormion sp ) y el laurel ( Nectandra spp ) (Burkart et al 1999). Figura 1. Mapa de Ubicacin del Campo Privado Las Lomas, Departamento de San Cosme, Provincia de Corrientes, Republica Argen tina. (Tomada de Bruno, 2011)
45 En este sitio se realizaron registros de reconocimiento de in dividuos y composicin sexo etrea las tropas de aulladores y rea de accin dentro los parches de bosque nativo. Para ello se aplicaron las tcnicas de barrido y registro de todas las acciones (Altmann, 1974; Martin & Batenson, 1991). A partir de este procedimiento se obtuvieron datos para ca racterizar patrn de actividad. Tambin se tomaron mues tras frescas seriadas de materia fecal (n=74) para caracterizar los endoparsitos presentes en esas tropas que eran objeto de observacin. Las muestras se conservaron en formol al 10 % y se analizaron en el CEPAVE-UNLPArgentina, aplicando las tcnicas de Ritchie y de Willis. Resultados Preliminares Se realiz el seguimiento de 2 tropas; una formada por 11 individuos (4 machos adultos, 4 hembras adultas, 2 machos juveniles y 1 hembra juvenil), y otra formada por 12 individuos (1 macho adulto, 3 hembras adultas, 3 machos juveniles, 2 hembras juveniles y 3 infantes). En la gura 2 se muestra el patrn de actividad de estas tropas de aulladores con base en un total de 40,841 registros de com portamiento. De los anlisis parasitolgicos, el 56,75 % de las muestras analizadas mostraron presencia de endopar sitos. La prevalencia de infeccin fue 77,5 %. Las especies ms frecuentemente encontradas fueron: Blastocystis sp., Giardia sp.; y Entamoeba coli. (Milozzi, et al 2010). En el presente ao se continan los anlisis estacionales de com portamiento y de prevalencia de parasitosis. Agradecimientos Queremos agradecer a J. Ezcurra y M. Brusca por permitir nos el acceso al campo privado y facilitarnos la estada en el mismo. Por la lectura crtica del manuscrito a la Lic. E.R. Steinberg. Este trabajo se lleva a cabo con subsidios MDM PIP 112-200801-00744 CONICET y UBACyT X154. Gabriela Bruno Grupo de Investigacin en Biologa Evo lutiva (GIBE). Depto. de Ecologa, Gentica y Evolucin. FCEyN, IEGEBA-UBA. Ciudad Univ. Pabelln II. 4to Piso. Labs. 43-46. (1428EHA). Cdad. Autnoma de Bs. As. Argentina; CONICET, e-mail:
46 A RECORD OF THE VARIEGATED SPIDER MONKEY ( ATELES HYBRIDUS BRUNNEUS ) IN SELVA DE FLORENCIA NATIONAL PARK, COLOMBIA Nstor Roncancio Duque Ateles hybridus brunneus is a subspecies endemic to Colom bia. Its distribution has been estimated at 49,000 km 2 as suming its distribution extends up to 2,000 meters above sea level (Deer, 2010). However, a new model predicts an even smaller potential distribution and habitat avail able, between 5,000 and 13,000 km 2 (Roncancio et al ., in press). Several characteristics of the variegated spider monkey make it extremely vulnerable to the loss, reduc tion and fragmentation of its habitat: these include its low population density, which ranges from 0.24 to 43 ind/km 2 (Roncancio et al ., 2010a, b) and features such as its large body mass (7-9 kg), frugivorous diet (up to 85% of the diet is composed of ripe fruit), long birth intervals (one o spring every 3-4 years), wide-ranging activity patterns (1.53.5 km traveled per day) and large home range (60-350 ha) (Chapman and Onderdonk, 1998; Stevenson et al., 2002; Deer et al., 2003; Link and Di Fiore, 2006; Takahashi, 2008; Urbani et al., 2008; Palacios et al., 2009; Deer, 2010). A. hybridus is categorized as Critically Endangered (CR) (Urbani et al., 2008) and is considered one of the 25 most threatened primates in the world (Mittermeier et al., 2009). In particular, A. h. brunneus is most at risk of extinction be cause in addition to other threats common to all subspecies, the area of distribution for this subspecies is smaller and no national protected area contains a conrmed population of the taxon. Only the recently declared National Natural Park, Selva de Florencia, on the southern limit of the his torical distribution of this subspecies (Deer, 2010), may house a population, but has never been an ocial record of its presence there. e nearest conrmed population is 61 km away from this area (Roncancio et al., 2010a). In order to plan eective strategies for wildlife conserva tion, it is necessary to assess conservation status by mea suring indicators that, compared over time, will enable the evaluation of any implemented interventions. Two of these indicators are species distribution and available habi tat. Following a random sampling design, several points in the historical distribution of A. h. brunneus were visited in order to gather occurrence records to model its current distribution. Additionally, some places that could be im portant conservation areas for the taxon were visited (Ron canio et al, in prep). Selva de Florencia National Natural Park is the only pro tected area in the historical distribution of this taxon. Ten years ago, the presence of this primate was reported near the area of the park (Castao 2001), but the individual recorded was in captivity and its owner said that the pri mate was captured in the parks area. Nevertheless, there was no ocial record of the species in the park. In order to conrm a natural population of the variegated spider monkey in Selva de Florencia National Natural Park, the sta of the park interviewed local inhabitants in the area. In November 2011 an individual living on the western zone of the park provided information about the species pres ence in the protected area. On December 8, this zone was visited by a sta from the park and individuals living in the area, and two indi viduals of A. h. brunneus were recorded. ey were seen moving and foraging at 1,780 meters a.s.l. (5'43"N, -75'56"W). e Selva de Florencia National Natural Park is now conrmed as the only national park that pro tects this taxon and its southernmost population. Another important aspect lies in the fact that this park has an altitu dinal distribution from 850 to 2,200 meters a.s.l. and only a limited area (10% of the park) is below 1,000 m. e fact that this remnant population is at the limit of the distribu tion makes this population more vulnerable. Additionally, Ateles hybridus prefers habitat from 0 to 800 meters a.s.l. (Deer, 2010), and thus suitable habitat available inside the protected area is also relatively small. e lowland sec tion of the park is also highly aected by extractive and productive human activities and some of the lands are still under private ownership. In consequence, this park might only oer marginal habitat to this spider monkey, but, due to the loss of its preferred habitat, is a very important refuge for a population. It is necessary to acquire land adjacent to the park and restore the habitat to generate better quality habitat for this taxon. Acknowledgments To the Selva de Florencia National Natural Park and its sta for their interest and continuous help. To Wildlife Conservation Society and its sta for nancial and tech nical support, and to the United States Fish and Wildlife Service for the nancial support. Nstor Roncancio Duque, Wildlife Conservation Society, Colombian Program, Carrera 25 # 4-39 Cali-Colombia, E-mail:
47 Rabinowitz, D., Cairns, S. and Dillon, T. 1986. Seven forms of rarity and their frequency in the ora of the Brit ish Isles, In: Conservation biology: the science of scarcity and diversity M. E. Soul (ed.), pp. 182204. Sinauer Associ ates, Sunderland MA. Roncancio, N., Garca L. M., and Acosta, A. 2010a. Den sidad poblacional y estructura de un grupo de Ateles hy bridus brunneus (Primates: Atelidae) en un fragmento de bosque aislado en el suroriente de Antioquia, Colombia. Mastozool. Neotropical 17: 385389. Roncancio, N. J., Garca, L. M., Acosta, A., Quiroga, J., Buitrago, C. and Gmez K. 2010b. Densidad Poblacio nal y Estructura de grupo de Ateles hybridus (Primates Atelidae) en la Serrana de San Lucas y el Suroriente de Antioquia. III Congreso Colombiano de Zoologa. Me delln, Colombia. Presentacin Oral. Libro de resmenes pg. 137 Chapman, C. and Oonderdonk, D. 1998. Forests without primates: Primate/Plant codependency. Am. J. Primatol 45: 127141. Deer T. R., Rodrguez-Mahecha, J. V., Hernndez-Cama cho, J. I. 2003. Conservation priorities for Colombian primates. Primate Conserv 19: 1018. Mittermeier, R. A., Wallis, J., Rylands, A. B., Ganzhorn, J. U., Oates, J. F., Williamson, E. A., 2006. Primates in Peril: e Worlds 25 Most Endangered Primates. IUCN/ SSC Primate Specialist Group (PSG), International Pri matological Society (IPS), and Conservation International (CI) 20082010, Arlington. Link, A. and Di Fiore, A. 2006. Seed dispersal by spider monkeys and its importance in the maintenance of Neotropical rain-forest diversity. J. Trop. Ecol 22: 113. Palacios, E., Morales-Jimnez, A. L., and Urbani, B. 2009. Variegated or Brown Spider Monkey, Ateles hybridus I. Georoy, 1829. In: Primates in Peril: e Worlds 25 Most Endangered Primates IUCN/SSC Primate Specialist Group (PSG), International Primatological Society (IPS), and Conservation International (CI) 2008 R. A. Mit termeier, J. Wallis, A. B. Rylands, J. F. Ganzhorn, J. F. Oates, Williamson, E. A. (eds.), pp.7273. Arlington, VA. Stevenson, P. R., Castellanos, M. C., Pizarro, J. C., Gara vito, M. 2002. Eects of seed dispersal by three Ateline monkey species on seed germination at Tinigua National Park, Colombia. Int. J. Primatol 32: 11871204. Takahashi, J. A. 2008. Literature review of the spider monkey, Ateles sp., with special focus on risk for extinc tion. Doctoral thesis. Swedish University of Agricultural Science. Urbani, B., Morales, A. L., Link, A. and Stevenson P. Ateles hybridus In: IUCN 2011. IUCN Red List of reatened Species. Version 2011.2. REGISTROS DE JUVENIS PERDIDOS DE ALOUATTA FUSCA GEOFFROY SAINTHILAIRE, 1812 PRIMATES: ATELIDAE NO PARQUE NACIONAL DA SERRA DOS RGOS Bruna Maia Pedro Henrique dos Santos Dias Dentre os primatas neotropicais, o gnero Alouatta La cpde, 1799 o que apresenta a mais ampla distribuio geogrca, ocorrendo desde o Estado de Vera Cruz, no Mxico, at o Estado do Rio Grande do Sul, no Brasil e Corrientes, na Argentina (Hill, 1962; Gregorin, 2006). Alouatta fusca (Georoy Saint-Hilaire, 1812) uma espcie endmica do Brasil e restrita Mata Atlntica (Gregorin, 2006). Em comparao com outros mamferos, lhotes de primatas necessitam de um longo perodo de cuidado parental e aprendizagem com suas mes (Vochteloo et al. 1993). Em espcies monogmicas, muitas vezes as fmeas recebem alguma espcie de colaborao por parte dos machos, seja ela direta ou indireta (Tardif, 1984; Wright, 1984, 1986; Van Schaik e Dumbar, 1990; Runcie, 2000; Sommer, 2000). No gnero Alouatta a necessidade da me muito grande, e mesmo quando j so capazes de se deslocarem sozin hos (Miranda et al. 2005), juvenis podem passar at 86% do tempo com as mes (Podgaiski e Jardim, 2009), e em muitas das ocasies podem passar longos perodos de tempo sob os cuidados de outros indivduos do grupo, inclusive machos adultos (Bolin, 1981). Alomatria foi registrada para A. caraya (Calegaro-Marques and BiccaMarques, 1993; Bravo e Sallenave, 2003), A. clamitans (Miranda et al. 2005), A. palliata (Clarke et al. 1998) e A. seniculus (Mack, 1979), de tal modo que muito raro o avistamento de indivduos de pequeno porte perdidos do grupo. Os relatos apresentados aqui so referentes a trabal hos de campo realizados em outubro de 2010 no Parque Nacional da Serra dos rgos (PARNASO), municpio de Terespolis, estado do Rio de Janeiro, Brasil. O PARNASO uma Unidade de Conservao que abriga uma rea de 20.024 hectares de Mata Atlntica. Em duas ocasies foram observados indivduos perdidos de seus grupos. Na primeira delas (15 de outubro de 2010), dois juvenis I de sexo indeterminado ( sensu Mendes, 1989) foram observados atravessando de uma rvore para outra (22'22.6"S, 42'49.7"W) s 15:20. Os mesmos per maneceram um curto perodo de tempo na mesma rvore. Durante esse perodo no foi observada a presena de nenhum indivduo adulto nas proximidades. Na segunda ocasio (27 de outubro de 2010) um juvenil II, novamen te sem sexo determinado, foi observado sozinho em uma rvore (22'16.0"S, 43'59.1"W) por volta das 16:40. O mesmo estava bastante agitado, balanando galhos e ras gando bromlias (Bromeliaceae). Aps cerca de 15 minu tos exibindo esse comportamento, o indivduo subiu para
48 o ponto mais elevado da rvore e l permaneceu. Mesmo com a chuva e o anoitecer, no se deslocou e no foram observados indivduos adultos ao redor. O juvenil foi ob servado at aproximadamente s 19:00, e presume-se que tenha passado a noite no local. Todas as observaes foram feitas seguindo o mtodo ad libitum (Altmann, 1974) sem limite de tempo. sabido, sobretudo em primatas neotropicais, que as fmeas com lhotes reduzem suas reas de atividade e tendem concentrar seus esforos nos mesmos. Chapman (1988) demonstrou tal fato para duas espcies de ateldeos ( Alouatta palliata e Ateles georoyi ) e um cebdeo ( C ebus capucinus ), de modo que bastante incomum encontrar juvenis e infantes longe de membros de seu grupo. Apesar do fato de que juvenis perdidos constituam um fenmeno raro, j foram relatados casos em que durante o forrageio, indivduos de um mesmo grupo de bugios apresentavam-se mais dispersos, podendo ocorrer eventualmente uma sepa rao (Steinmetz, 2005). Quando isso acontecia os indiv duos perdidos cavam se deslocando a procura dos outros e em alguns casos vocalizavam. Embora tenha sido levantada a hiptese de ser uma peculiaridade dos grupos estudados, o mesmo foi observado no presente estudo. Os registros descritos no presente estudo corroboram a hi ptese de que indivduos de Alouatta fusca possam even tualmente se perder de seus grupos por longos perodos de tempo, uma vez que o primeiro registro para esta popu lao. A ocorrncia de indivduos perdidos em populaes geogracamente isoladas d indcios de que este comporta mento no uma peculiaridade regional, e sim algo reco rrente nestes animais. Outra informao importante que pode ser extrada de nossas observaes diz respeito s questes demogrcas de Alouatta fusca na Serra dos rgos. Treves (2001) hipote tizou que as fmeas das espcies de Alouatta podem maxi mizar a taxa de sobrevivncia da prole ao se reproduzirem em grupos que apresentam uma alta proporo de machos adultos e subadultos em relao ao nmero de fmeas. Mu danas de dominncia ou subdiviso de grandes grupos em grupos menores podem estar relacionados aos avistamentos de indivduos perdidos, no entanto, maiores concluses no podem ser extradas devido ausncia de estudos po pulacionais com bugios nessa regio. Agradecimentos Dra. Cibele Bonvicino pelo incentivo a publicao deste trabalho e Cecilia Cronemberger (PARNASO) pelo apoio logstico. Agradecemos ao Conselho Nacional de Desen volvimento Cientco e Tecnolgico (CNPq) e Coorde nao de Aperfeioamento de Pessoal de Nvel Superior (CAPES) pelas bolsas concedidas. Tambm gostaramos de agradecer a um revisor annimo pelas sugestes que con triburam signicativamente para o aumento da qualidade deste manuscrito. Bruna Maia Laboratrio de Biologia e Parasitologia de Mamferos Silvestres Reservatrios, IOC/FIOCRUZ, Avenida Brasil, 4365, CEP 21040-900, RJ, Brasil, e-mail:
49 Steinmetz, S. 2005. Vocalizaes de longo alcance como comunicao intra-grupal nos bugios ( Alouatta guariba ). Neotrop. Primates 13(2): 1115. Tardif, S.D. 1994. Relative energetic cost of infant care in small-bodied neotropical primates and its relation to infant-care patterns. Am. J. Primatol. 34:133143. Treves, A. 2001. Reproductive consequences of variation in the composition of howler monkey ( Alouatta spp.) groups. Behav. Ecol. Sociobiol. 50: 6171. Van Schaik, C.P. e Dunbar, R.I.M. 1990. e evolution of monogamy in large primates: a new hypothesis and some crucial tests. Behaviour 115(1-2): 3061. Vochteloo, J.D., Timmermans, P. J. A., Duijghuisen, J. A. H. e Vossen, M. H. 1993. Eects of reducing the mothers radius of action on the development of motherinfant relationship in longtailed macaques. Anim. Behav 45: 603612. Wright, P.C. 1984. Biparental care in Aotus trivirgatus and Callicebus moloch In: Small, M. (ed.). Female primates: studies by women primatologists Alan R. Liss Inc., New York, pp 5975. Wright, P.C. 1986. Ecological correlates of monogamy in Aotus and Callicebus In: Else J.G and Lee P.C. (eds.). Primate ecology and conservation Cambridge University Press, New York, pp 159167. Orf Liza Maria Veiga (1963 2012) Liza Maria Veiga was born on October 31st, 1963, in London, England. She graduated in Business Economics at Cardi University in Wales, in 1994, and took her mas ters in Environment and International Development at the University of East Anglia (UEA), in England, in 1995. In 1996, Liza became a researcher for the Overseas Develop ment Group at UEA, where she developed studies on the traditional knowledge and subsistence systems of rural pop ulations for DFID, the British government body for Interna tional Cooperation and Development. In 1997, as a member of the socio-economic team of the Environment and Natural Resources Program, Liza embarked on her rst research in the tropics; in Tanzania and other African countries. In 1999, Liza was involved in her rst professional activi ties in Brazil, where she participated in a study of human activities in the Amazon estuary, analyzing the evolution of local practices for the management of the environment and natural resourcescontinuing the activities she had begun in Africa some three years previously. is rst Brazilian project was coordinated by Dr. Edna Castro of the Ncleo de Altos Estudos Amaznicos NAEA Environmental ques tions, which Liza had previously considered to be no more than one aspect of the life of rural populations, began to take on an increasingly important role in her approach to this research, and eventually became her principal focus. is shift in focus probably inspired Liza to seek new re search horizons more directly linked to the environment, biodiversity, and a unique group of mammals. Amazonian primates and their conservation began to dominate Lizas in tellectual interests and her professional activities at around this time (2000), rstly as a DTI assistant at NAEA, and then through her graduate research in the Behavior eory and Research Program of the Department of Experimental Psychology at the Federal University of Par (UFPA). Be tween 2001 and 2004, Liza was involved in research proj ects on primate ecology and conservation, as well as sur veys of mammal populations, which had now become her principal study subjects. Her main study during this period was a project entitled Management of the Populations of Chiropotes satanas in the Area of the Tucuru Reservoir, coordinated by Dr. Stephen Ferrari; a project which later became the embryo of her doctoral research. In 2004, as a graduate student at the UFPA Experimental Psychology Department, Liza began to teach undergraduate courses. Her doctorate was supervised by Dr. Stephen Ferrari, and co-supervised by Dr. Olavo Galvo. In 2005, Liza became a scientic consultant to the Center for the Protection of Brazilian Primates (CPB-ICMBio) and a member of the International Committee for the Conservation and Management of Amazonian Primates. is period was marked by the increasing intensication of her involvement in all elds of Primatology. Liza defended her doctoral dissertation, entitled Ecology and Behavior of the Black Cuxi ( Chiropotes satanas ) in the Fragmented Landscape of eastern Amazonia at UFPA
50 in 2006. In her dissertation, Liza demonstrated not only her profound interest in the ecology and behavior of the cuxis, but also her preoccupation with the conservation and protection of these animals, which would become the primary focus of her professional activities in subsequent years. In 2007, Liza became a member of the Primate Specialist Group (PSG) of the Species Survival Commission of the In ternational Union for the Conservation of Nature (IUCN), and played an important role in the Global Mammal As sessment (GMA), participating in the production of the Red List for Neotropical primates (Pitheciidae) as part of the Biodiversity Assessment Initiative of IUCN/SSC and the Center for Applied Biodiversity Science (CABS), based at Conservation International in Washington, DC. She was also a collaborator on the IUCN Species Survival Com mission (SSC), and participated in the development of the Pitheciine Action Group (PAG) of the PSG (Neotropical Section), as well as being active on the subcommittee for the integrated development of research of the International Committee for the Conservation and Management of Am azonian Primates (IBAMA). Liza became a member of the Brazilian Primatological So ciety (SBPr), was part of its executive council, and partici pated in the scientic committee of the Societys 13th con gress. In 2007, she began to intensify her relationship with the Goeldi Museum (MPEG) in Belm, rst by becoming a DTI grantee in the Professional Training Program until the middle of 2008, and then, at the end of the year, by becoming a postdoc in the joint UFPA/MPEG Graduate Program in Zoology (PPGZool). As a postdoc, Liza had a grant from the CAPES National Post-doctoral Program (PNPD), and in 2007 and 2008, she coordinated the proj ect entitled Ecology, Social Organization, and Conserva tion of the Black Cuxi ( Chiropotes satanas ). In 2007, she joined the TEAM (Ecology, Evaluation, and Monitoring of Tropical Forests) project, collaborating with Conserva tion International (Brazil), rst as project manager, then as vice-coordinator, and nally as coordinator, between 2008 and 2010. As a postdoc and an associate researcher at the Goeldi Museum, Liza was a graduate supervisor, and contributed to the teaching of a number of courses, including Behav ioral Ecology, Conservation Biology, Primatology, and Special Topics in Primatology, in which she administered the topic Reproductive Behavior and Ecology. Between 2008 and 2010, Liza participated in a number of surveys of medium-sized and large mammals, and worked as a private environmental consultant. However, it was as a postdoc at the Goeldi Museum that Liza advanced even further as a professional. She participated in the ongoing project Ecol ogy and Conservation of the Endangered Primates of the Brazilian state of Par, coordinated by Dr. Jos de Sousa e Silva Jnior. is project aims to provide a database on the ecology, distribution, and extinction risk of the threatened primates of the Brazilian state of Par ( Cebus kaapori Chi ropotes satanas Chiropotes utahickae and Ateles marginatus ), one of Lizas main concerns. Between 2008 and 2010, she participated in the project Endangered Species and Criti cal Areas for the Biodiversity of the Brazilian state of Par, coordinated by Dr. Teresa Cristina vila Pires, during which she contributed to the development of a database of the information available on the species included in the state list of endangered taxa. Between 2009 and 2011, Liza coordinated the project Conservation of the primates Cebus kaapori and Chi ropotes satanas , during which she conducted eld studies of both species, as well as a population viability analysis of Chiropotes satanas is project sought to develop guide lines for the conservation and management of these spe cies. During the same period, she coordinated the project entitled Survey of Mediumand Large-bodied Mammals and the Use of Camera Traps in the Tucuru Environmen tal Protection Area, and began participating in the project Biodiversity in the state of Par: Development of the rst Atlas of Priority Areas for Conservation coordinated by Dr. Ana Luisa Albernaz, and during which she contributed to the denition of the priority areas for the conservation of the states biodiversity. In 2012, Liza initiated a project entitled Distribution and Conservation of the Remnant Populations of the Kaapor capuchin ( Cebus kaapori ), a Critically Endangered Spe cies, undertaking a survey of the remaining populations of this species in the remaining habitat, with the ultimate aim of capturing and translocating a vulnerable group of these primates in the area surrounding the Tucuru reservoir. is project also involved the National Primate Center and the CPB. In 2009 and 2010, as a member of the IUCN Primate Spe cialist Group (PSG-SSC), Liza participated in the evalu ation of the conservation status of Brazilian primates, an initiative of the CPB and the Brazilian Environment Min istry (MMA), contributing to the production of the lists of Brazilian endangered animal species and the Action Plan for the Mammals of Southeastern Brazil. As a private consultant, Liza also participated in a Rapid Ecological As sessment (RAPELD) in Guyana. In 2011, she joined the Neotropical Section of the PSG, providing the focus for the development of the primate Red List for the Amazon region. As a member of a joint task-force between the Spe cies Survival Commission (SSC) and the World Protected Areas Commission (WPC), Liza contributed to the evalu ation of the impact of protected areas on biodiversity, and the identication of new key areas for conservation. She also became a member of the Strategic Assessment Group of the National Action Plan for the Conservation of En demic Endangered Species of the Middle and Lower Xingu River, an initiative of the Coordination for the Develop ment and Implementation of Action Plans (COPAN), part of the Chico Mendes Biodiversity Institute (ICMBio).
51 Liza was especially active as an educator, and supervised or co-supervised a number of undergraduate projects and dissertations, and masters theses. She co-supervised a study of tufted capuchins, and supervised studies of the ecology and behavior of Chiropotes satanas and Cebus kaapori e thesis on Cebus kaapori is the only systematic study of the ecology and behavior of this Critically Endangered spe cies. Liza accepted three new masters students in 2011 and 2012, developing ecological studies of the primates and fe lines of the region of Alta Floresta (Mato Grosso). She was also supervising a number of undergraduate students who were researching the behavior and ecology of primates in the Tucuru region. Lizas students were always profoundly involved in the research projects that she developed with such dedication. Liza was a member of the editorial board of Neotropical Primates and the Pitheciine Action Group Newsletter and a reviewer for the American Journal of Primatology Folia Primatologica the International Journal of Primatology and the International Zoo Yearbook She attended many scien tic events, such as conferences and workshops, where she presented papers and participated in scientic committees, and was the principal editor of the book Evolutionary Bi ology and Conservation of Titis, Sakis and Uacaris just re cently published by the Cambridge University Press. She published numerous papers, including articles in journals, book chapters, texts in newspapers and magazines, as well as congress abstracts. Liza Maria Veiga passed away prema turely on October 28th, 2012. Jos de Sousa e Silva Jnior, Helder Lima de Queiroz and Maria Aparecida Lopes Museu Paraense Emlio-Goeldi; Universidade Federal do Par Being an editor can be a lonely job, with most of ones time spent alone in front of the computer. It is made much more interesting at Neotropical Primates by the lively inter national e-mail exchanges among the editors, on topics that range from the fate of particular articles, to our opinions on primatological controversies, to more personal conver sations as we have gotten to know each other better and have become friends. e best part is the few occasions, usually at international meetings, when the editors actu ally get to spend time with each other in person. Here, we acknowledge the tremendous loss of one of our editorial team members, Liza Veiga, and make a tribute to her work for the understanding and conservation of primates, and in appreciation of her persistent eorts to improve Neotropical Primates e rst time I met Liza Veiga was at the Congress of the International Primatological Society at Edinburgh, Scot land, in 2008, about a year after I started work at NP I had assumed she was Brazilian until then, and I left the meetings still unsureperfect Brazilian Portuguese, perfect British English, thick black silky hair, Asian eyes, stylish modern blouse, old jeans, Amazonian jewelry. She deed simple categorization. What I noticed about her then was her intensity, her focus, and her seriousness. She was ready with several ideas of how to improve the journal, and after the meetings she was the rst to contact others and imple ment the changes. I saw Liza again briey at the Brazilian Primatology Meet ings in Curitiba, Brazil, in 2011. She spoke as part of a roundtable discussion on Amazonian Primates. She was ill at the meetings, had nearly lost her voice, and she ad mitted she was feeling dizzy and might faint. Nevertheless, Neotropical Primates editorial team, August 2008. IPS meetings in Edinburgh, Scotland. From left to right, Brenda Solrzano, Erwin Pa lacios, Liza Maria Veiga, Liliana Corts-Ortiz, Jessica Lynch Alfaro, Eckhard Heymann, Anthony B. Rylands, Jlio Csar Bicca-Marques.
52 she soldiered on with her presentation. She delivered her words slowly, precisely and quietly. It was, without doubt, the most moving and devastating talk I have ever seen. Up until that moment I had harbored the illusion that the vastness of the Amazon Basin remained relatively safe, rela tively pristine. Liza demonstrated, in careful detail, the arc of deforestation that has denuded most of eastern Par, and she went on to explore other threatsthe impact of hydro electric dams, the new rise in soybean plantations, the everexpanding cattle ranchesthat are devouring the Amazon rainforest from all sides, from the outside in. ere never was such a convincing advocate as Liza for the desperate need for research and conservation work on Amazonian primates. I left that roundtable with a new worldview after hearing Lizas message. e last time I spent time with Liza was in the summer of 2012, at the Assessment Workshop for the Conservation Status of Brazilian Primates, at Iper, So Paulo, Brazil. It was a workshop she had helped to organize, and I was grate ful for the invitation to participate. We ended up as room mates there, and this is where I really got to see the personal side of Liza. She was hilarious, charming and brimming with ideas about everything. She could hold a room en thralled with her stories from the eld. She loved to imitate everyone and everything: the park guards who sat around all day scratching themselves; the Indians around Tucuru who would stick a lower lip out farther and farther to show how truly far away something was; her students circling back to her with more and more questions; the eld guide who fell out of the boat with the motor still running; the bearded saki males huddled together in a greeting; the ca puchin monkey that threatened her from the doorway so she couldnt enter her own house at the eld station... Liza loved to laugh. She lived and breathed Brazil, the Amazon, the animals. She was the Amazons biggest cham pion, with so much determination to solve the gargantuan problem of habitat loss against all odds. She was tireless in her ght. She also embodied a huge wealth of knowledge about Brazilian fauna. A tiny example: We had heard that the lake near the workshop in Iper had capybara, a species Id never seen in the wild. As she was leaving the workshop and we said our goodbyes, Liza told me if I walked up slowly enough, capybaras dont get scared. e next morning at dawn I followed her advice at the lake, creeping nearer until I could sit right next to that giant rodent at the waters edge. What Liza had inside of her was unique, particular, and cant be recreated. She saw things in the forest that no one else has seen, and that perhaps may never be seen again. But also, she desperately wanted to share her experiences. She was so very excited about the upcoming publication of her book on the pitheciines, after ten years of hard work and waiting. Liza was so very alive, so in the middle of things, she had so much that she still wanted to accom plish; but she was also deeply tired from so much desire, so much passion, and so much struggle. I am grateful for the time I had with her, as co-editor, collaborator and friend. We will all miss her terribly at Neotropical Primates and we thank her wholeheartedly for all of her contributions, that have accomplished so much in promoting the research and conservation of Brazilian primates. Jessica Lynch Alfaro, Editor of Neotropical Primates University of California, Los Angeles e 2008 IPS meetings in Edinburgh gave me the oppor tunity to meet Liza Veiga in person for rst time. I only saw her again a few other times, but regularly heard from her due to her enthusiastic and ecient participation in Neotropical Primates and her devoted actions towards the conservation of Amazonian primates. Liza always showed a great passion for research, a strong commitment to share her knowledge with colleagues and students, and a tremen dous devotion to truth in her actions. Liliana Corts-Ortiz Editor of Neotropical Primates University of Michigan I met Liza for the rst and only time at the 2008 IPS meet ings in Edinburgh. From the rst moment on, it was in spiring to talk to Liza, and I appreciated her collegiality and friendliness. Her ambitious and conservationist spirit will be missed. Eckhard W. Heymann, Editor of Neotropical Primates Deutsches Primatenzentrum GmbH (DPZ), LeibnizInstitut fr Primatenforschung Liza was truly a special, a kind and trustworthy person and an excellent researcher, editor and student advisor. Sadly, our great new and growing friendship and colleagueship ended quite prematurely. Brazilian primatology and the Amazonian biodiversity will miss her. Hopefully her war rior spirit will continue inspiring us all. Jlio Csar Bicca-Marques, Editor of Neotropical Primates Pontifcia Universidade Catlica do Rio Grande do Sul Liza was always ready to devote time to give advice, no matter the time of the day or the size of her workload; she was a fantastic friend and teammate. I will miss her. Erwin Palacios, Chief Editor of Neotropical Primates Conservation International Colombia
53 I rst met Liza at the Brazilian Primate Congress in Porto Alegre and immediately appreciated a certain specialness about her. Her calm, elegance, and sweet nature combined with a remarkable courage, energy and determination in her work. Lizas pioneer research on the black saki was out standing, and she rapidly became an important contact and reference for teaching, research and the general business of primate conservation and ecology in Brazil; and most par ticularly for the pitheciines. She played a fundamental role in the IUCN SSC Primate Specialist Group as a member of the Executive Committee, as the PSG liaison with the Brazilian government on the assessment of the conserva tion status of the Brazilian primates, and as a member of the editorial board for the PSG newsletter and journal Neotropical Primates Her distinguished academic achieve ments are well represented in her book, recently published, Evolutionary Biology and Conservation of Titis, Sakis and Uacaris She was dedicated and brilliant, and adored and respected by all her colleagues and those who had the privi lege to work with her. Anthony B. Rylands, Deputy Chair IUCN SSC Primate Specialist Group Liza was a wonderful person, and a very active member of our IUCN/SSC Primate Specialist Group. And of course I followed her work very closely because she studied the pitheciines, probably my favorite primates in the world, and especially Chiropotes a genus to which I have a par ticularly close attachment. She was at the peak of her career, which makes her loss even more tragic. We will all miss her, and remember her outstanding contributions for the rest of our lives. I am especially saddened by the fact that she did not see her book on the evolutionary biology and conserva tion of the pitheciines nally published, but it is a tting memorial to all that she achieved in her career. Russell A. Mittermeier, President Conservation International, and Chair, IUCN SSC Primate Specialist Group Neotropical Primates editorial team, August 2008. IPS meetings in Edinburgh, Scotland. From left to right, Brenda Solrzano, Erwin Palacios, Liza Maria Veiga, Lili ana Corts-Ortiz, Jessica Lynch Alfaro, Eckhard Heymann, Anthony B. Rylands, Jlio Csar Bicca-Marques. Brazilian Primatology owes a lot to scholars who werent born in Brazil, but adopted this country as their own. Many great individuals in our history didnt grow up in Brazil. Liza is proof of this. No one would say that Liza wasnt Brazilian. Her love of primates, of the Amazon, and for all she did in her work is revealed in the articles she wrote. We know much more about the pitheciines now, thanks to Lizas particular dedication to this group. At the time that she left us, Liza was on the directorial board of the Brazilian Primatological Society (SBPr). Her willingness and readi ness to share information was essential to SBPr running smoothly. We will always have Liza as an exampleof love and complete dedication to the study of Brazilian primates. SBPr will never let this example be forgotten. ank you for so very much, Liza. Maria Adlia Borstelmann de Oliveira, President Brazilian Primatological Society Brazilian Primatology has lost an excellent researcher and a wonderful spokesperson, and primatologists have lost a dear friend. e members of the Centro Nacional de Pesquisa e Conservacao de Primatas Brasileiros (CPB/ICMBio) oer their tribute to Liza Maria Veiga with heavy hearts. Lizas work highlighted black bearded saki ( Chiropotes sata nas ) conservation in both Brazilian and international pri matology. She promoted conservation action for the family Pitheciidae in general, and worked in favor of Brazilian pri mate conservation even more broadly, with a focus on the Amazon. Her technical abilities and her great willingness to collaborate are shown through her work as the coordinator of both the IUCN (International Union for the Conserva tion of Nature) Pitheciine Action Group and the IUCN Primate Specialist Group. CPB honors Liza as a valuable researcher and a great friend, and thanks her for the generous help and participation in several Center projects, most recently for her role as Taxon Coordinator in the Evaluation Process for the Conserva tion Status for Brazilian Primates in 2012, where her ef forts were essential in facilitating the interactions with and among the scientic community. As always, she made use of her collaborative nature for which we were so grateful.
54 Our tribute goes beyond just the research accomplishments and professional partnerships; what we most want to cel ebrate is Liza as a dear and special friend. She will always be remembered for her important work ghting for the conservation of Brazilian primates, and for the sum of her intelligent and ethical personality. Centro Nacional de Pesquisa e Conservacao de Primatas Brasileiros (CPB/ICMBio) I rst met Liza Veiga at the Primate Society of Brazils con ference in Belm in 2000. A little lost in a city I didnt know at all, in a language in which I was only half-compe tent, I was ever so impressed when a rather Chinese-look ing person with a very Brazilian name (Liza Maria Veiga, after all) suddenly started speaking to me in uent Eng lishespecially as she had just concluded a conversation in rapid re and apparently perfect Portuguese (she also spoke uent French; languages being one of Lizas many talents). By sheer happenstance, we were both starting PhDs; I was in ooded forests, she was in ood-created islands. And we were both working on one of the least-known of the Neotropical primate groups, the pitheciines; she was study ing Chiropotes, I was studying Cacajao. I remember tea (real tea!) in a garden somewhere in Belm and the conversation evolving into one that decided that something must be done. Fast forward six years and we are in another conference, this time in Entebbe, Uganda, and we are about to see the fruition of about 18 months of hard workthe rst-ever symposium dedicated solely to pitheciines, their ecology and conservation. Like the Pitheciine Action Group and the soon-to-be-published book on Pitheciine ecology and conservation, my initial idea for the symposium was seized upon by Liza with what can only be described as zeal and glee. ings rst expanded and then fell into place, both with a remarkable speed as Lizas training in business logis tics swung into action. at is one of the many remarkable things about Liza Veiga, that for fully three-quarters of her all-to-brief life, she didnt do biology at all. With a degree in Economics and a Mas ters in International Development Studies, Liza only came to monkeys via a strange set of steps that Stephen Ferrari has already described so well. A curious course from which primatology benetted greatly. e Liza I rst met was brisk, charming, funny and breathtakingly ecient. To-do lists had a habit of rapidly vapor izing into nothing in her presence. Finishing her PhD on a Friday in 2006, she had a job by the following Monday possibly a record for post-grad unemployment. And how she networked, and how hard she worked, and how much she helped others. And she took on students and she took on projects with Conservation International and IUCN and the SSC and became member of various committees and commissions and spread herself thinner and thinner so that gradually the phone calls and e-mails stopped being bouncy and full of vim, and slowly depression clouded the life of our dear friend and colleague. And now shes gone, and I still cant quite adapt to the fact. Its not true that Ill never get another e-mail from her, or have another crackly skype call, never see her again at con ferencesjuggling students and presentations, talks to see and committees to attend, all with a smile and a busy busy cell phone. We will publish those papers we were always just about to be going to get round toLizas out in the eld, shell be back A book on pitheciinesher rst and foremost primatologi cal lovewas published in April 2013 by Cambridge Uni versity Press. Its dedicated to her, but I just wish it didnt have to be. I wish it were a celebration of her still-present competency and drive, rather than a memorial of muchmissed abilities. Primatology has lost a great colleague, and a person of remarkable vision, ability and drive. Many students have lost a magnicent and insightful mentor, I have lost a dear friend, and primates in general have lost a small, bustling and much-loved champion. Liza Maria Veiga, remembered-in-primates. Adrian Barnett Roehampton University, London e trajectory of Liza Maria Veiga shows us that a success ful career must be constructed through hard work and ded ication, but also with intense love for the chosen work. e eld of primatology was lucky to have Liza fall in love with it, and Liza dedicated herself not only to the study of pri mates, but also to the mentoring and professional develop ment of several students. She loved to work collaboratively, and she was always sharing her experiences. Liza was a great friend, and she participated in many im portant moments of my professional life, always with much generosity. It was my privilege to have her on my doctoral thesis committee, and I greatly beneted from her rich knowledge of Chiropotes and her experience as some one who had gone through similar diculties during long and arduous eldwork. She was the author of one of the most thorough studies of Chiropotes ever conducted. Her work with the black bearded saki, C. satanas in the Tucuru region in Brazil, caused admiration among primatologists for the seriousness and eort that she put into it. From the beginning of her career as a primatologist, she showed commitment, collaboration and tireless dedication to primate conservation in Brazil. She came to Brazil in 1999 with a dream of exploring new worlds and dedicat ing herself to new causes, both of which happened in her short and intense career. ose with the luck of sharing in her life can give testimony that her genuine happiness and admirable disposition, in addition to her ethics and her
55 commitment, made Liza a captivating researcher. An exam ple was her participation in the symposium Pitheciines: Ecology and Conservation, organized by her and Adrian Barnett for the XXI International Primatological Society Meetings, in 2006 in Uganda. An outcome of this sympo sium was the book Evolutionary Biology and Conservation of Titis, Sakis, and Uakaris that demonstrates the full force of the combined qualities Liza possessed. Liza also acted on her passion for primatology through her collaboration in the evaluation of threatened species for IUCN, as the pri mary person responsible for data collection to support the evaluation of the Pitheciidae in 2008. She also played an important role in the Evaluation Workshop of the Conser vation Status of Brazilian Primates, held by the Centro Na cional de Pesquisa e Conservao de Primatas Brasileiros/ ICMBio in 2012. Liza was remarkable and courageous in her position in the post-doctoral program at the Museu Paraense Emlio Goeldi, where she advised students, lec tured, and collaborated in diverse lines of research. Besides her dedication, her ethics, her eciency, and her joy, Liza Maria Veiga added love in her particular way of acting and living. Her death has transformed her trajec tory into a legacy and has consolidated what I already knew before her untimely departure: everyone loved her, and she deeply deserved our love. Liliam Patricia Pinto Centro Nacional de Pesquisa e Conservao da Biodiversidade Amaznica CEPAM/ICMBio e recent loss of Liza Veiga is a painful fact that saddens us all profoundly... not only is the sudden death shocking in itself, but so is the loss of such a pivotal researcher with a brilliant, awless and aspiring career. We are forced to realize that we cannot turn to her anymore for her muchneeded help in our unending shared ght for a world that takes responsibility in protecting the environment. We have lost a great friend who was loving, caring, attentive, genuine, and extremely fair. It is unnecessary to describe her competence and seriousness, to try to enumerate all the virtues that Liza possessed as a professionalwe all know these and can attest to them. In truth there is no way to express the pain of losing someone as special as her, and all we can do now is try, with our best eorts and sacrice, to make up for, at least partially, her loss... In life she waged an enduring struggle to ght against the imminent threat of extinction for our Brazilian primates... We will continue this mission in her absence, though now it seems even more impossible, and without Liza, more arduous, lonely, and sad! Fabiano Rodrigues de Melo Universidade Federal de Gois University of Wisconsin, Madison Teaching is an extremely rewarding profession, and it is hard not to get involved with ones students, especially at the graduate level, when a somewhat intimate relation ship inevitably arises from the long hours spent together discussing projects and data, and worrying over analyses and deadlines. In Liza Veigas case, the sense of a familial bond was especially strong, for a number of reasons. While I think neither of us felt an especially strong link with our home country, the fact that we were both English was perhaps the most important factor, possibly for no better reason than being able to share the odd moment of typi cally British humor to the blank-faced consternation of the Brazilians around us. It was nice to have someone to chat to in English now and again, although we would more often than not talk to each other in Portuguese. ere were other, minor coincidences. We both had mixed backgroundsLizas father was Chinese and mine was Italianso in some ways, we were both quirky, atypical Britons who shared a slightly distinctive viewpoint on the world. We were both also late starters, following unusual, roundabout paths to nally become primatologists. But Liza beat me hands down for originality, having graduated in Business Economics and taken a masters degree in Inter national Development. In fact, when she walked into my oce at the Federal University of Par, in the Amazon city of Belm, and told me she was an economist, one of the last things I imagined her doing was a doctorate in experimen tal psychology based on a study of primate ecology. But a few short years later, she was defending her thesis, and nobody would ever imagine she had ever been anything but a career primatologist. During the intervening years, Liza taught me, her academic mentor, many important lessons, beginning with the old adage that anything is possible. As far as she was con cerned, in fact, nothing is impossible would have been a more appropriate motto. In addition to her incorrigible en thusiasm and dedication to her work, studies, and research, she was endowed with an impressive ability to organize things, which represented probably the major dierence between us. I would often feel almost embarrassed, in fact, whenever she was in my oce, because Im sure she found the absolute chaos of my typical absent-minded academics workplace at the very least a little annoying, if not totally frustrating or infuriating. She never criticized, although she would sometimes say something like my goodness, this place could do with a good spring cleaning, and all I could do would be to agree wholeheartedly. But she did once clear it all out, repaint the walls, and rearrange everything to her satisfaction, which was nice, even though I subse quently spent weeks trying to nd all my important stu. While she was meticulous in the extremewhich I can only see as being a positive trait in a scientistLiza was far from being a fuddy-duddy, cloistered away in ivory towers. She was always full of energy, always good for a joke and a laugh, and only very rarely would she refuse an invita tion for a happy hour (or two or more) after a long days hard work. In addition to brightening up the laboratory environment with her invariably good humor, Liza was always ready to lend a hand too, whether it was helping
56 me to make a deadline, nding a reference for one of her colleagues, or just chipping in around the department in general. Lizas dedication and attention to detail, not to mention her eagerness to learn, more than compensated for any lack of formal training in biological sciences, and she was an exemplary doctoral student, going to extremes to guarantee the collection of her data. She had her fair share of mishaps in the eld, including a shipwreck, when the boat she was travelling in to her eld site hit a submerged log at a fairly high speed and threw her and the boatman into the water. Liza took this and other minor disasters in her stride, with typically British stoicism, but about halfway through her eldwork, she hit an unexpected barrier. She always took pretty good care of herself, and was a regular in the gym (when she was in town), but she pushed herself to the limit and the long, hard days in the eld nally took their toll on her health. However, the problem was not so much her blistered feet, bad back, and almost clinical exhaustion, but the fact that she was determined not to miss any of her planned eldwork time. She was monitoring two groups of cuxis ( Chiropotes satanas ) simultaneously, and was worried that any interruption of her schedule would jeopardize the quality of her data. I had my work cut out to convince her that she could more than compensate by obtaining com parative data in consecutive years, but in the end, she real ized that her health issues were a little more serious than she wanted to believe, and she took a much-needed two month sabbatical. Liza neednt have worried, because her study was excellent. It bore all the characteristics of her trademark dedication and eciency. Her dissertation transformed her from a novice economist-cum-monkey-watcher into a fullyedged primatologist, more than ready to go on to higher things. Most people tend to relax after nishing their de grees, but Liza wasnt like that. In fact, she seemed to thrive on hard work and new challenges, and almost before the ink had dried on her diploma, she was o managing proj ects, working as an environmental consultant, and then taking up a postdoctoral position at the Goeldi Museum, where she dedicated herself to new research initiatives, and in particular, teaching. I had moved away from Belm by this time, and sadly, we saw each other only very rarely over the past few years, al though we continued to work together on many new proj ects and publications, and would still chat regularly through long e-mails. While Liza had become a procient prima tologist, her administrative skills also showed through, and she was active in many dierent capacities, perhaps most importantly, the IUCN Red List and the Pitheciine Action Group, as well as being an editor of Neotropical Primates My memories of Liza Veiga are as a cheerful, hard-working, and dedicated student, colleague, and friend. I am proud to have been able to help her achieve her dream of study ing the monkeys of the Amazon forest, and even prouder to know that she did so much to share her knowledge and experience with the rest of us, and in particular her stu dents. As a teacher, there are few more satisfying things than seeing an ex-student carrying on the tradition, and while she was with us for such a painfully short time, Lizas contribution to primatology will stand proud for many generations to come. Stephen F. Ferrari Universidade Federal de Sergipe Liza Maria Veiga's publications Articles in journals and newsletters Barnett, A. A., Boyle, S. A., Norconk, M. M., Palminteri, S., Santos, R. R., VEIGA, L. M. Alvim, T. H. G., Bowler, M., Chism, J., Di Fiore, A., Fernandez-Duque, E., Gui mares, A. C. P., Harrison-Levine, A. M. Y., Haugaas en, T., Lehman, S., Mackinnon, K. C., De Melo, F. R., Moreira, L. S., Moura, V. S., Phillips, C. R., Pinto, L. P., Port-Carvalho, M., Setz, E. Z. F., Shaer, C., Da Silva, L. R., Da Silva, S. D. S. B., Soares, R. F., ompson, C. L., Vieira, T. M., Vreedzaam, A., Walker-Pacheco, S. E., Spi ronello, W. R., Maclarnon, A.N. N., Ferrari, S. F. 2012. Terrestrial activity in Pitheciins ( Cacajao Chiropotes and Pithecia ). Am J Primatol 74:11061127 Barnett, A. A ., Pinto, L. P., Bicca-Marques, J. C., Ferra ri, S. F ., Gordo, M., Lopes, M. A., Port-Carvalho, M., Spironello, W. R., VEIGA, L. M. Vieira, T. M., Boyle, S. 2012. Proposal for the common names for species of Chiropotes (Pitheciinae: Primates). Zootaxa 3507:7983 Homann, M., Hilton-Taylor, C., Angulo, A., Bohm, M., Brooks, T. M., VEIGA, L. M. , Smart, J., Stein, B. A., Stuart, S. N. 2010. e impact of conservation on the status of the worlds vertebrates. Science 330:15031509 VEIGA, L. M. Veiga, I. 2009. Galeria bichos ameaa dos: cuxi-preto ( Chiropotes satanas ): procura-se macaco amigo. Cincia Hoje das Crianas 207:13-16 Ferrari, S. F ., VEIGA, L. M. Urbani, B. 2008. Geophagy in New World monkeys (Platyrrhini): ecological and geo graphic patterns. Folia Primatol 79:402415 Schipper, J., Chanson, J. S., Chiozza, F., Cox, N. A., Ho mann, M., ... VEIGA, L. M. Vi, J-C., Williamson, E. A., Wyatt, S. A., Xie, Y., Young, B. E. 2008. e status of the worlds land and marine mammals: diversity, threat, and knowledge. Science 322:225230 Palacios, E., Corts-Ortiz, L., Bicca-Marques, J. C., Hey mann, E. W., Alfaro, J. L., VEIGA, L. M. 2008. Edito rial. Neotrop Primates 15:39 VEIGA, L. M. Ferrari, S. F. 2007. Geophagy at termitaria by bearded sakis ( Chiropotes satanas ) in Southeastern Bra zilian Amazonia. Am J Primatol 69:816820 VEIGA, L. M. Barnett, A. A 2007. Pitheciine Action Group (PAG) Neotrop Primates 14:3738 VEIGA, L. M. Ferrari, S. F. 2006. Predation of arthropods by southern bearded sakis ( Chiropotes satanas ) in eastern Brazilian Amazonia. Am J Primatol 68:209215
57 Ferrari, S. F., Pereira, W. L. A., Santos, R. R., VEIGA, L. M. 2004. Fatal attack of a Boa constrictor on a bearded saki ( Chiropotes satanas utahicki ). Folia Primatol 75:111113 Edited books VEIGA, L. M. Barnett, A. A ., Ferrari, S. F ., Norconk, M. A. 2013. Evolutionary biology and conservation of titis, sakis and uacaris Cambridge, Cambridge University Press Book chapters Boyle, S., VEIGA, L. M. Silva Jr, J. S. (in press). Black bearded saki Chiropotes satanas Homannsegg, 1807. In: Rowe, N., Myers, M. (eds.) All the worlds primates East Hampton, NY, Pogonias Press. Boyle, S., VEIGA, L. M. Silva Jr, J. S. (in press). Uta Hicks bearded saki Chiropotes utahicki Hershkovitz, 1985. In: Rowe N, Myers M (ed.) All the worlds primates East Hampton (NY), Pogonias Press. Silva Jr, J. S., Lopes, M. A., VEIGA, L. M. (in press). Kaapor capuchin Cebus kaapori Queiroz, 1992. In: Rowe N, Myers M (ed.) All the worlds primates East Hampton, NY, Pogonias Press. Pinto, L. P., Barnett, A. A ., Bezerra, B. M., Boubli, J. P., Bowler, M., Cardoso, N. A., Caselli, C. B., Rodriguez, M. J. O., Santos, R. R., Setz, E. Z. F., VEIGA, L. M. 2013. Why we know so little: the challenges of eldwork on the Pitheciids. In: Veiga, L. M., Barnett, A. A ., Fer rari, S. F ., Norconk, M. A. (eds.) Evolutionary biology and conservation of titis, sakis and uacaris Cambridge, Cam bridge University Press, p 145150. VEIGA, L. M. Ferrari, S. F. 2013. Ecology and behavior of bearded sakis (genus Chiropotes ). A review of the ecology of Chiropotes In: Veiga LM, Barnett AA Ferrari SF Nor conk MA (eds.) Evolutionary biology and conservation of titis, sakis and uacaris Cambridge, Cambridge University Press, p 240249. VEIGA, L. M. 2013. Conservation of the Pitheciids. In: Veiga LM, Barnett AA Ferrari SF Norconk MA (eds.) Evolutionary biology and conservation of titis, sakis and uacaris Cambridge, Cambridge University Press, p 309310. Ferrari, S. F ., Boyle, S., Marsh, L. K., Port-Carvalho, M., Santos, R. R., Silva, S. S. B., Vieira, T. M., VEIGA, L. M. 2013. e challenge of living in fragments. In: Veiga, L. M., Barnett, A. A ., Ferrari, S. F ., Norconk, M. A. (eds.). Evolutionary biology and conservation of titis, sakis and uacaris Cambridge, Cambridge University Press, p 350358. Ferrari, S. F., VEIGA, L. M. Pinto, L. P., Marsh, L. K., Mittermeier, R. A. and Rylands, A. B. 2013. Family Pitheciidae (titis, sakis and uacaris). In: Mittermeier, R. A., Rylands, A. B. & Wilson, D. E. (eds.). Handbook of the Mammals of the World. Volume 3 Primates Lynx Edi cions, Barcelona, pp.432457. VEIGA, L. M. Silva Jr, J. S., Lopes, M. A. 2008. Cux i-preto, Chiropotes satanas Homannsegg, 1807. In: Machado ABM, Drummond GM, Paglia AP (ed.). Livro vermelho da fauna brasileira ameaada de extino vol 2 Belo Horizonte (MG), Fundao Biodiversitas, p 776778. Lopes, M. A., Ferrari, S. F ., VEIGA, L. M. Silva Jr, J. S. 2008. Cuxi-de-uta-hick, Chiropotes utahicki Hershkov itz, 1985. In: Machado, A. B. M., Drummond, G. M., Paglia, A. P. (ed.). Livro vermelho da fauna brasileira ame aada de extino vol 2 Belo Horizonte (MG), Fundao Biodiversitas, p 778780. VEIGA, L. M. Pinto, L. P. 2008. Gnero Chiropotes Lesson 1840. In: Reis, N. R., Peracchi, A. L., Andrade, F. R. (eds.). Primatas Brasileiros vol 1 Londrina, Technical Books Editora, p 139146. Escarlate-Tavares, F., VEIGA, L. M. 2011. Callicebus per sonatus (. Georoy, 1812). In: Plano de ao dos mamfe ros do sudeste do Brasil Escarlate-Tavares, F., VEIGA, L. M. 2011. Callicebus melanochir Wied-Neuwied, 1820. In: Plano de ao dos mamferos do sudeste do Brasil Furthermore, Liza Veiga is author or co-author of 38 species accounts in the latest version (2012.2) of the IUCN Red List of reatened Species (see http://www.iucnredlist.org) N 2013 CONSERVATION AWARDS e Conservation Leadership Programme is currently so liciting applications for 2013 Conservation Awards. ese awards are aimed at early-career conservationists (no more than 5 years professional experience in the conservation sector). Awards that will be oered in three categories: 1) Future conservationist, 2) Conservation follow-up, and 3) Conservation leadership. e application deadline for all awards is 9 th November 2012. For more information go to www.conservationleadershipprogramme.org PRIMATE ECOLOGY AND ANIMAL BEHAVIOR e Primate Ecology and Animal Behavior course will be oered in Panama from December 20th, 2012 to January 9th, 2013. e course is given at Bocas del Toro Biologi cal Station is located on the north end of Isla Coln. e purpose of this course is to give the student a foundation in primate ecology, primate behaviour, eld techniques and analytical tools in a tropical setting. e material covered is equivalent to a university upper level course in primate ecology. For more information go to www.itec-edu.org/ info.html#course
58 SOCIEDAD LATINOAMERICANA DE PRIMATOLOGA (SLAPRIM) Durante el XXIV Congreso IPS 2012, llevado a cabo del 12 al 17 de Agosto de 2012 en Cancn, Mxico, nos reunimos un numeroso grupo de primatlogos latinoamericanos con la intencin de revivir a la SLAPrim (Sociedad Latinoamer icana de Primatologa). La SLAP (ahora SLAPrim) tuvo su origen en 1986 durante el XII Congreso IPS en Alemania, y fue alentada principalmente por el Dr. Milton iago de Mello, ilustre primatlogo brasileo quien fungi como su primer presidente. La SLAP sobrevivi hasta los inicios de los aos noventa, siendo su ltimo presidente el Dr. Er nesto Rodrguez Luna, primatlogo de origen mexicano. Desde entonces, a pesar de algunos intentos, no se haba logrado reactivar sta sociedad, que represent por varios aos los esfuerzos por mantener la unidad entre primatlo gos de Latinoamrica. Por esta razn es que, en esta ltima la reunin se decidi dar inicio a una serie de acciones que debern culminar durante el Congreso Brasileo de Pri matologa y Segundo Congreso Latinoamericano de Pri matologa que se llevarn a cabo en Recife, Pernambuco, Brasil, del 4 al 9 de Agosto de 2013. Los puntos que se acordaron fueron: a)Realizar el II Congreso Latinoameri cano de Primatologa dentro del XV Congreso Brasileo de Primatologa; b) Se eligi a Domingo Canales Espinosa (Mxico) como Presidente Honorario, debindose elegir un Presidente formal para la SLAPrim en la Asamblea General de la asociacin durante el Congreso Brasileo de Primatologa; c) Se eligi a Martin Kowalewski como representante de la regin Cono Sur (Argentina, Paraguay, Chile, y Uruguay), Andres Link como representante de la regin Andina (Bolivia, Peru, Ecuador y Colombia), Ber nardo Urbani como representante de la regin Amazonia) Venezuela, Guyanas, Surinam y Caribe), Domingo Canales como representante de la regin Mesoamerica (Mexico y Centroamrica), Leandro Jerusalinsky y Mauricio Talebi como representantes de Brasil; d) El Presidente Honorario deber presentar en Recife la propuesta de estatutos que regirn a la SLAP, as como una propuesta de organizacin para la asociacin; e) Se invitar a participar de SLAPrim a todos los primatlogos que trabajan en hbitats de primates del Nuevo Mundo, sin importar su nacionalidad. Esta es una primera invitacin dirigida a todos los investigadores, estudiantes e interesados en el estudio, manejo y conserva cin de los primates del Nuevo Mundo, a que participen en la SLAPrim. Esperamos con ello, dar la cara a los nuevos paradigmas que debemos enfrentar desde la Primatologa Latinoamericana. Atentamente Domingo Canales Espinosa Presidente Honorario SLAPrim Rn Prn BOOKS Long-Term Field Studies of Primates, edited by Peter M. Kappeler & David P. Watts. 2012. Springer. 479pp. ISBN: 978-3642225130. In this volume, leading eld workers report on the history and infrastructure of their projects in Madagascar, Africa, Asia and South America. ey provide summaries of their long-term research eorts on primate behaviour, ecology and life history, highlighting insights that were only possible because of the long-term nature of the study. Contents: 1. e values and challenges of long-term eld studies Kappeler PM, et.al ; 2. Berenty Reserve, Madagascar: A long time in a small space Jolly A: 3. Beza Mahafaly Special Reserve: Long-term research on lemurs in southwestern Madagascar Sussman RW, et.al ; 4. Long-term lemur research at Center Valbio, Rano mafana National Park, Madagascar Wright PC, et.al; 5. A 15-year perspective on the social organization and life history of sifaka in Kirindy Forest Kappeler PM & Fich tel C; 6. e northern muriqui ( Brachyteles hypoxanthus ): Lessons on behavioral plasticity and population dynamics from critically endangered species Strier KB & Mendes SL; 7. e Lomas Barbudal Monkey Project: Two decades of research on Cebus capucinus Perry S, et.al.; 8. Tracking Neotropical monkeys in Santa Rosa: Lessons from a regen erating Costa Rican dry forest Fedigan LM & Jack KM; 9. e group life cycle and demography of brown capuchin monkeys ( Cebus apella nigritus ) in Iguaz National Park, Argentina Janson C, et.al; 10. Social organization and male residence pattern in Phayres Leaf monkeys Koengi A & Borries C; 11. White handed gibbons of Khao Yai: social exibility, complex reproductive strategies, and slow life history Reichard UH, et.al; 12. e Amboseli baboon research project: 40 years of continuity and change Al berts SC & Atlmann J; 13. e 30 year blues: what we know and dont know about life history, group size, and group ssion of blue monkeys in the Kakamega Forest, Kenya Cords M; 15. Long-term eld studies of chim panzees at Mahale Mountains National Park, Tanzania; 16. Long-term studies of the chimpanzees of Gombe National Park, Tanzania Wilson ML; 17. Long-term research on Grauers gorillas in Kahuzi-Biega National Park, DRC: life history, foraging strategies, and ecological dierentiation from sympatric chimpanzees Yamagiwa J, et.al; 18. Longterm studies on wild bonobos at Wamba, Luo Scientic Reserve, D.R. Congo: towards the understanding of female life history in a male-philopatric species Furuichi T, et.al; 19. Long-term, individual-based eld studies CluttonBrock T. Building Babies: Primate Development in Proximate and Ul timate Perspective, edited by Kathryn B.H. Clancy, Katie Hinde & Julienne N. Rutherford. 2012. Springer. 575pp. ISBN: 978-1461440598. is book features multiand
59 trans-disciplinary research approaches to primate develop mental trajectories. It is organized thematically along the developmental trajectory: conception, pregnancy, lactation, the mother-infant dyad, broader social relationships, and transitions to independence. Contents: 1. Inammation, re production, and the Goldilocks Principle; 2. e primate placenta as an agent of developmental and health trajecto ries across the lifecourse; 3. Placental development, evolu tion, and epigenetics of primate pregnancies; 4. Nutritional ecology and reproductive output in female chimpanzees: variation among and within populations; 5. Prenatal an drogens aect development and behavior in primates; 6. Navigating transitions in HPA function from pregnancy through lactation: implications for maternal health and infant brain development; 7. Genome-environment co ordination in neurobehavioral development; 8. Building marmoset babies: Trade-os and cutting bait; 9. Lactational programming: mothers milk predicts infant behavior and temperament; 10. Do bigger brains mean better milk?; 11. Infant gut microbiota: developmental inuences and health outcomes;12. Maternal inuences on social and neural de velopment in rhesus monkeys; 13. Behavioral response of mothers and infants to variation in maternal condition: adaptation, compensation and resilience; 14. e role of mothers in the development of tool-use in chimpanzees;15. Reproductive strategies and infant care in the Malagasy pri mates; 16. When dads help: male behavioral care during primate infant development; 17. Ontogeny of social behav ior in the genus Cebus and the application of an integrative framework for examining plasticity and complexity in evo lution; 18. Identifying proximate and ultimate causation in the development of primate sex-typed social behavior; 19. Future adults or old children? Integrating life history frameworks for understanding primate positional patterns; 20. Quantitative genetic perspectives female macaque life histories: heritability, plasticity, and trade-os; 21. Cultural evolution and human reproductive behavior; 22. e on togeny of investigating primate ontogeny. Transfrontier Conservation Areas: People Living on the Edge edited by Jens A. Andersson, Michel de GarineWichatitsky, David H.M. Cumming, Vupenyu Dzingirai, & Ken E. Giller. 2012. Routledge. 256pp. ISBN: 9781849712088. is book focuses on the forgotten people displaced by, or living on the edge of protected wildlife areas. It moves beyond the grand enchanting promise of conservation and development across frontiers, and un founded notions of transfrontier conservation areas as in tegrated social-ecological systems. Peoples dependency on natural resources varies enormously along the conservation frontier, as does their reliance on resources on the other side of the conservation boundary. Hence, the studies in this book move from the dream of ecotourism-fuelled develop ment supporting nature conservation and people, towards the local realities facing marginalized people, living adja cent to protected areas in environments often poorly suited to agriculture. Tropical rainforests Compared in a nutshell Review of: Tropical Rain Forests An Ecological and Biogeo graphical Comparison 2nd edition, by Richard T. Corlett and Richard B. Primack, 2011. Chichester: John Wiley. ISBN paperback: 978-1-4443-3255-1, ISBN hardcover: 978-1-4443-3254-4. x+326 pp., numerous colour g ures. Price: US-$ 79.95 (paperback), US-$ 149.95 (hard cover).
60 I enjoyed reading this book and recommend it to every primatologist who wants to look beyond the primatologi cal horizon and update his/her knowledge in comparative tropical ecology and biogeography. Eckhard W. Heymann, Abt. Verhaltenskologie & Sozio biologie, Deutsches Primatenzentrum, Kellnerweg 4, D-37077 Gttingen, e-mail:
61 southern Brazil (Rio Grande do Sul State), 20082009. Am. J. Primatol. 7481): 6876) Behie AM, Pavelka MSM. 2012. Food selection in the black howler monkey following habitat disturbance: im plications for the importance of mature leaves. J. Trop. Ecol. 28(2): 153-160 Behie AMM, Pavelka MSM. 2012. e role of minerals in food selection in a black howler monkey ( Alouatta Pigra ) population in Belize following a major hurricane. Am. J. Primatol. 74(11): 10541063 Bezanson M. 2012. e ontogeny of prehensile-tail use in Cebus capucinus and Alouatta palliata Am. J. Primatol. 74(8) : 770782 Bezerra BM, Souto AS, Jones G. 2012. Propagation of the loud tch call of golden-backed uakaris, Cacajao melanocephalus in the black-swamp forests of the upper Amazon. Primates 53(4): 317-325 Blair ME; Melnick DJ. 2012. Genetic evidence for dispersal by both sexes in the Central American Squirrel Monkey, Saimiri oerstedii citrinellus. Am. J. Primatol. 74(1): 3747 Boubli JP, Rylands AB, Farias IP, Alfaro ME, Lynch J. 2012. Cebus phylogenetic relationships: a preliminary reassess ment of the diversity of the untufted capuchin monkeys. Am. J. Primatol. 74(4): 381393 Bowler M, Knogge C, Heymann EW. 2012. Multilevel societies in New World primates? exibility may charac terize the organization of Peruvian red Uakaris ( Cacajao calvus ucayalii ). Int. J. Primatol 33(5):1110-1124 Bravo SP. 2012. From which Ocotea diospyrifolia trees does Alouatta caraya (Primates, Atelidae) eat fruits? J. Trop. Ecol 28(4): 417-420 Buchwald U, Teupser D, Kuehnel F, Grohmann J, Schmie der N, Beindor N, Schlumbohm C, Fuhrmann H, Ein spanier A. 2012. Prenatal stress programs lipid metabo lism enhancing cardiovascular risk in the female F1, F2, and F3 generation in the primate model common mar moset ( Callithrix jacchus ). J. Med. Prim. 41(4): 231240 Caperos JM, Morcillo A, Pelez F, Fidalgo A, Snchez S. 2012. e eect of infant body mass on carrier travel speed in cotton-top tamarins ( Saguinus oedipus ). Int. J. Primatol. 33(2): 447-459 Csar C, Byrne R, Young RJ, Zuberbhler K. 2012. e alarm call system of wild black-fronted titi monkeys, Cal licebus nigrifrons. Behav. Ecol & Sociobiol. 66(5) Csar C, Byrne RW, Hoppitt W, Young RJ, Zuberbhler K. 2012. Evidence for semantic communication in titi monkey alarm calls. Anim. Behav. 84(2): 405-411 Coles RC, Lee PC, Talebi M. 2012. Fissionfusion dynam ics in southern muriquis ( Brachyteles arachnoides ) in con tinuous Brazilian Atlantic Forest. Int. J. Primatol. 33(1): 93-114 de Melo AL, Mati VLT, Martins WA. Callithrix penicillat as a nonhuman primate model for strongyloidiasis. Primates 53(3): 303-309 de Miranda Fl, Barros Monteiro FO, Cicalise Takeshita RS, Da Silva GA, Faturi C, Correia Palha M, Barros Monteiro MV, Coutinho LN, Kugelmeier T, Gomes de Castro PH. 2012. 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Antrhopol. 147(4):580592 ABSTRACTS Selected abstracts relating with Neotropical primates from the XXIV Congress of the International Primato logical Society, Cancn, Mxico August 12 to 17, 2012 Amato KR, Yeoman CJ, Kent A, Righini N, Estrada A, Stumpf RM, Yildirim S, Torralba M, Gillis M, Wilson BA, Nelson KE, White BA, Leigh SR. Spatial and tempo ral patterns in Mexican black howler ( Alouatta pigra ) gut microbial community composition. Arakaki PR, Carvalho FM, Mendes CM, Visintin JA, As sumpcao MEOA, Castro PHG, Muniz JAPC, Valle RR. Evaluation of sperm DNA fragmentation of semen from Goeldis monkey ( Calimico goeldii ). Aristizabal JF, Perez Torres J. Relationship between ranging patterns and forage patch occupation time: a case study with Alouatta seniculus. Arroyo-Rodriguez V, Gonzalez-Zamora A, Chavez OM, Stoner KE. Diet and activity pattern of spider monkey ( Ateles georoyi ) throughout their range: a review. Arruda MF, Lima AK, Mantilla GR, Yamamoto ME, Araujo A. Reproductive vacancy in Callithrix jacchus : what must we expect? Arruda MF, Lima AK. Care and development of youngsters in Callithrix jacchus and the relation with social and eco logical context. Aureli F, Schaner CM, Asensio N, Lusseau D. What is a subgroup? How to dene it using inter-individual dis tance in spider monkeys. Babb PL, Fernandez-Duque E, Schurr TG. e enigmatic taxonomic status of Aotus among the Platyrrhines: signals from ve genetic loci. Behie AM, Pavelka MS. Taking a multifactoral approach to understanding population changes: the interaction of diet, cortisol and parasites in determining the population density of black howler monkeys ( Alouatta pigra ) follow ing a hurricane. Bello R, Escate W, Timson S, Aguirre M, Rosemberg F, Gongora D. Preliminary results of the reintroduction of a group of spider monkeys Ateles chamek in the South-east of the Peruvian Amazon. Beltrao-Mendes R, Santos Junior EM, Ferrari SF. An eco logical lacuna in the geographic distribution of titi mon keys ( Callicebus spp.) in the Brazilian northeast. Bezerra BM, Vastos M, Reed D, Souto AS, Schiel N, Eason P, Jones G. Using camera traps to investigate aspects of the behavior and ecology of wild blond capuchins, Sapa jus avius (former Cebus avius). Boubli JP, da Silva MN, Farias I, Rohe F, Alfaro JL. Ama zonia river barriers: the primates of the Rio Branco Rio Negro region. Bowler M, Claidiere N. Temporal variation in party size in Peruvian red uakari monkeys. Buckner JL, Alfaro J, Rylands A, Alfaro M. Statistical phy logeography of the marmosets and tamarins. Bueno ML, Deer TR. Karyotypic variation in Aotus speciation. Campbell CJ, Di Fiore A, Link A, Notman H, Pavelka MS, Ramirez S, Santorelli CJ. Spider monkey ( Ateles spp.) sexual behavior: a multiple site and species comparison. Carrara MC. Yanes B. e expectancy violation procedure in a black handed spider monkey. Carretero-Pinzon X, Deer TR, Ruiz-Garcia. Activity budget, home range, daily distances and diet Samiri sciu reus albigena group in fragments at Colombian Llanos. Carvalho FM, Arakaki PR, Nichi M, Mendes CM, As sumpcao ME, Muniz JA, Duarte M, Valle RR. Eect of cryopreservation on lipid peroxidation and DNA frag mentation in Alouatta caraya semen. Csar C, Zuberbhler K, Young RJ, Byrne RW. Blackfronted titi monkeys alarm calls signal predator type and location. Caselli CB, Bicca-Marques JC, Setz EZ. Does fruit avail ability inuence the territorial behavior of Callibecus ni grofrons in a semideciduous Tropical forest in southeast ern Brazil? Caselli CB, Nagy-Reis MB, Gestich CC, Setz EZ. Sleep ing sites use in wild black-fronted titi monkey ( Callicebus nigrifrons ) in Tropical forest of southern Brazil. Champion JE, Hartwell SK, Notman H, Pavelka MSM. e short term eects of hurricane Richard on diet, be havior, and sub-grouping patterns of spider monkeys ( Ateles georoyi ) at Runaway Creek Nature Reserve, Belize. Chaves PB, Cornejo FM, Shanee S, Schmitt CA, CortesOrtiz L, Roos C, Pacheco V, Di Fiore A. Ateline phylo genetics revisited: an assessment of the position of the yellow-tailed woolly monkey based on nuclear DNA se quences and complete mitochondrial genomes. Chism J, Brasington LF, Do Santos A, Kieran T. Presence of two species of saki monkeys ( Phitecia) one possible undescribed, south of the Amazon river in northeast Peru, and preliminary evidence for hybridization of the two species.
65 Claidiere N, McGuigan NM, Messer E, Whiten A. e comparative study of prosociality in capuchin monkeys and human children. Clayton JB, Kim HB, Danzeisen JL, Glander KE, Isaacson RE, Johnson TJ. Characterization and functional analy sis of the fecal metagenome of the wild mantled howling monkey ( Alouatta palliata ). Corewyn LC. Male-male associations in two multi-male groups of mantled howlers ( Alouatta palliata ) at Haci enda La Pacca, Costa Rica. Cornejo FM, Fernandez-Melo F. Four years of primate conservation education in Peru. Cornejo FM, Tello C, Chocce M, Vega N. Use of space and diet of the Andean night monkey Aotus miconax in the private area of conservation Huiquilla, Amazonas, Peru. Cortes-Ortiz L. Reconstructing the evolutionary history of Mesoamerican howler monkeys. Coutinho LN, Brito MB, Andrade RS, Castro PG, Mon teiro FO, Vicente WR. Hemodynamics changes during ovulatory events in owl monkeys. De Luna AG, Garcia Y, Snchez AM, Velez NK, Link A. e role of the endangered silvery-brown tamarin ( Sagui nus leucopus ) as seed dispersers in the maintenance of the inter-Andean Tropical forest of Colombia. De Luna AG, Link A. Interspecic competition and niche partitioning in a forest fragment of the Colombia Mag dalena river valley. Deer TR. A database and catalogue for Colombian pri mate collections: consolidating our knowledge. Deet TR. Using ooded forest: Colombian primates in the Amazon and Llanos Orientales. DeLuycker AM. Sleeping site selection by titi monkeys ( Callicebus oenanthe ) in fragmented forest, northern Peru. Di Fiore A, Botero S, Zarate DA, Stevenson PR. A primer on the phylogeography of Lagothrix lagothricha in north ern south America. Duarte A, Zagal AS, Priston N. Resource and dietary overlap in black howler monkeys ( Alouatta pigra ), blackhanded spider monkeys ( Ateles georoyi ), and humans in the mountain range of Tenosique, Tabasco, Mexico. Dunn JC, Asensio N, Arroyo-Rodriguez V, Schnitzer S, Cristobal-Azkarate J. e ranging costs of a fallback food: liana consumption supplements diet but increases forag ing eort in howler monkeys. Dunn JC, Shedden A, Rodriguez-Luna E, Knapp L. Ge netic diversity and population structure of a critically en dangered primate, the Mexican howler monkey ( Alouatta palliata mexicana ). Emidio RA, Ferreira RG. Anvils to tree distances on capu chins tool use sites at Caatinga. Escorcia-Quintana M. MacSwiney C, Quiroz-Romero H, Cristobal-Azkarate J. e eects of distance from the forest edge on the development of a nematode, Trypan oxyuris minutus, from mantled howler monkey ( Alouatta palliata ) in high tropical forest. Eshchar Y, Visalberghi A, Resende BD, Izar P, Laity KM, Verderane M, Carvalho CE, Fragaszy DM. Nut-cracking in wild bearded capuchin monkeys: community resourc es for learning. Espinosa FC, Gomez S, Canales D, Hernandez LT. Diges tive exibility and lack of selective digesta retention in free ranging howler monkeys ( Alouatta palliata ). Estevez-Noboa M, Peck M. Conservation of the brown headed spider monkey ( Ateles fusciceps ) in NW Ecuador. Estevez-Noboa M. e primate of Los Cedros Reserve: a cloud forest with a small population of the brown headed spider monkey ( Ateles fusciceps ) in Ecuador. Evans S, Wolovich CK. e owl monkeys of the Dumond Conservancy, Miami, USA. A scientic, educational and community asset. Ferrari SF. Functional variation in pelage coloration: a missing piece in the jigsaw of Platyrrine systematic? Finkenwirth C, Burkart JM. Neuroendocrine regulation of prosociality in common marsmosets. Fogaca MD, Tokuda M, Wright BW, de Resende BD, Izar P. Does socially biased learning play a role in pal, preda tion by capuchin monkeys? Franquesa M, Velez del Burgo, Shedden A, Rodriguez-Lu na E. Longitudinal study of a translocated howler group: coping with the impact of environmental and population changes. Freitas DS, Bicca-Marques JC. e impact of yellow fever outbreak on black and gold howler monkeys ( Alouatta caraya ) in a fragmented landscape in southern Brazil. Galvins N, Link A, Montes A, Villanueva B, Cortes FA, Rimbach R. Increased folivory in a population of brown spider monkeys ( Ateles hybridus ) in Colombia. Garber PA, Porter LM. Integrating route-based and coor dinate-based mental maps in wild Bolivian saddleback tamarins ( Saguinus fuscicollis weddelli ). Garcia Villalba J, Jimenez Viasus J, Deer T. Loss and frag mentation of the habitat of Callibecus caquetensis, new species of Colombian primate. Gomez-Espinosa EE, Dias PAD, Rangel-Negrin A, Cha vira R, Canales-Espinosa D. Cortisol levels and agonistic behavior of two groups of free-ranging mantled howler monkeys. Gomez-Posada C, Roncancio-Duque N, Londoo JM, Giraldo-Ch P, Alvarez Z, Hincapie P. Landscape attri butes aecting population status of red howler monkeys in Colombian Andes mountain forest. Gonzalez-Hernandez M, Garcia-Hernandez J, EspinosaGomez FC, Romero-Callejas E, Osorio-Sarabia D, Ca nales-Espinosa D. Changes in gastrointestinal parasite infection in Alouatta palliata mexicana associated with translocation. Gregory T, Carrasco F, Deichmann J, Kolowski J, Alonso A. Natural canopy bridges as a mitigation measure to reduce forest fragmentation eects on primates in Peru Gunhold T, Whiten A, Bugnyar T. Social learning in wild common marmosets ( Callithrix jacchus ): transmission and maintenance of experimental seeded information. Hartwell KS, Notman H, Pavelka MS. Patterns of aggres sion in spider monkeys ( Ateles georoyi yucatanensis ) at Runway Creek Nature Reserve, Belize.
66 Heymann EW, Matauschek C, Roos C. Tamarin ( Sa guinus ) biogeography and diversication determined by major geologic events. Hughes KD, Santos LR. Samll-scale spatial strategies that support large-scale navigation: experimental evidence from capuchins ( Cebus apella ). Izar P, Lynch J, Nakai ES. Fission-fusion dynamics of black tufted capuchin monkeys ( Cebus nigritus ) in the Brazilian Atlantic forest: a comparison across populations Jerusalinsky L, Souza-Alves JP, Beltrao-Mendes R, Printes RC, Hilario RR, Santos ME, Ferrari SF. Biogeography of the Callicebus personatus group: surveys and potential distribution base on the maximum entropy algorithm (Maxent). Juarez CP, Fernandez-Duque E. Eects of a naturally frag mented habitat on two owl monkey ( Aotus azaraik ) pop ulations in the Argentinan Chaco. Kawamura S. Sakurai K, Bergstrom M, Shirasu M. Matsu shita Y, Melin A, Imai H, Touhara K, Oota H, Aureli F, Fedigan L. Assessment of bitter taste receptor gene varia tion and dietary fruit odorants in natural populations of color-vision polymorphic New World monkeys. Leimgruber KL, Ward AF, Benitez ME, Widness J, Norton MI, Olson KR, Gray K, Santos LR. Do capuchin mon keys ( Cebus apella ) pay it forward: the role of social con text in prosocial behavior. Link A, Blazquez I, Londoo CP. Variation in spatial co hesion of red howler monkeys, white faced capuchins and brown spider monkeys in a fragmented forest in Colombia Link A, Di Fiore A. Ranging and grouping patterns of males and female in two populations of spider monkeys inhabiting continuous versus fragmented forest. Lynch J, Boubli JP, Di Fiore A, Rylands A, Farias I, Rohe F, Nguyen MT, Koshkarian G, Alfaro ME. Comparative Cebine biogeography: Cebus, Sapajus and Saimiri. Maldonado AM, Peck M. e use of owl monkeys as ag ship species for enhancing environmental law enforce ment and conservation awareness at the Colombian-Pe ruvian border. Maldonado AM. Primates, Tikunas and protected areas: Lessons and challenges in community resources management. Martin-Solano S. Carrillo-Bilbao GA, Celi W, Benitez W, Huynen M, Losson B. Identifying primate parasites in the Ecuadorian Amazon: a tool for public health and conservation. Matsushita Y, oota H, Welker B, Pavelka M, Kawamura S. possible anomalous trichromacy or color vision by hybrid L7M Opsin genes in wild howler monkeys, Alouatta. Menezes AN, Bovincino CR Seuanez HN. Aotus evolution. Messer EJ, Claidiere N, Hoppitt W, Whiten A. Social learning and the transmission of foraging techniques in squirrel monkeys ( Saimiri sciureus ). Milton K, Giacalone J. Dierential eects of unusual cli matic stress on two sympatric primate species ( Alouatta palliata and Cebus capucinus ) in Panama. Morales A, Disotell T, Di Fiore A. Phylogeny and bio geography of spider monkeys (Genus Ateles ). A new hypothesis. Morales Jimenez A, Di Fiore A. Molecular genetic evidence challenging the current classication of Mesoamerican spider monkeys ( Ateles sp.) Moura AC, Montenegro MM, Lee PC. Ecological con straints on tool use among the capuchin genus. Norconk MA, Conklin-Brittain NL. Is the lean season in food availability and nutrition reversed in sakis compared with ripe fruit specialists? Ottoni EB, Falotico T, Mannu M. Probe tools manufac ture and use by wild bearded capuchin monkeys ( Spajus libidinosus ) in Serra da Capivara National Park, Brazil. Papworth SK, Milner-Gulland EJ, Slocombe K. Can wild woolly monkeys ( Lagothrix lagotricha ) distinguish be tween human hunters and non-hunters? Papworth SK, Milner-Gulland EJ, Slocombe K. Non-le thal eects of human hunters on the morning chorus of dusty titi monkeys ( Callicebus discolor ). Parrish AE, Brosnan SF. Food sharing in capuchin mon keys ( Cebus apella ). Possamai CB, Strier KB. Dispersal strategies of female northern muriquis ( Brachyteles hypoxanthus ). Presotto A, Izar P, Madden M, Fragaszy D. Route-based navigation in wild bearded capuchin moneys ( Sapajus libidinosus ). Quintana-Morales PC, Hernandez-Salazar LT, MoralesMavil J, Rico-Gray V, Rodriguez-Luna E, Lopez-Galindo F. Intergroup dynamics of Alouatta palliata under spatial restriction conditions. Quintana-Morales PC, Morales-Mavil J, Garca-Ordua F, Canales-Espinosa D. Human pressure on the habitat of primates: direct inuence of economic and political fac tors in Los Tuxtlas, Mexico Ramos-Fernandez G, Pinacho-Guendulain B. Ecological correlates of spatial dispersion in spider monkeys ( Ateles georoyi ). Ramos-Fernandez G. Conservation implications of inter and intraspecic trait variability in spider monkeys. Rapaport L. e ins and outs (and back and forth) of food sharing, Tamarin style. Resende BD, Vieria M, Carvalho M, Silva AP. Tolerance and social learning of tool use: comparison between a semi-free and semi-captive group of tufted capuchin monkeys ( Sapajus sp.) Righini N, Garber PA. Does resource mixing explain why howler monkeys leave a feeding patch? Rimbach R, Alfonso F, Montes A, Di Fiore A, Link A. Pat terns of social behavior amongst female spider monkeys ( Ateles hybridus ). Rimbach R, Montes A, Pardo A, Di Fiore A, Link A. In terspecic aggression and infanticide by spider monkeys ( Ateles hybridus ) in a fragmented forest in Colombia. Rodrigues MA, Kitchen DM. Cortisol, estradiol and repro ductive state among wild female spider monkeys. Rodriguez-Luna E, Shedden A, Solorzano-Garcia B. e Mesoamerican primatological tradition.
67 Roncancio Duque N, Acosta Castaeda A, Garcia Loaiza L, Rios C. Current potencial distribution, population density and habitat available of two endangered endemic primates, Ateles hybridus brunneus and Saguinus leucopus of Colombian Andes. Rubin TL, Pokorny JJ, de Waal F. Facial expression dis crimination in captive tufted capuchins ( Cebus apella ). Sampaio I, Carneiro JC, Araujo TS, Barbosa JB, Vallinoto M, Schneider H. Saimiri: molecular phylogeny, taxono my and natural hybridization. Santorelli CJ, Schaner CM, Aureli F. Traditions and dia lects across spider monkey communities: what we can learn from universal behaviors. Scarry CJ, Tiddi B. Male strategies during intergroup en counters among tufted capuchin monkeys. Schaner SM, Murillo E, Di Fiore A, Kawamura S, Aureli F. Male immigration in spider monkeys? Schneider H, Bernardi JR, Cunha DB, Tagliaro CH, Valli noto M, Ferrari SF, Sampaio I. Evolutionary relationships in the Callitrichinae, with emphasis on the position of the dwarf marmoset. Schoof VA, Jack KM. ick and thieves: strength and qual ity of male co-resident social relationships in white faced capuchin. Serio-Silva JC, Hernandez NA, Ronzn-Perez P. Virtual library for theses and dissertations relating to Mexican primatology: a useful tool with online access. Serio-Silva JC, Vidal-Garcia F, Arguello-Sanchez L, Coro na-Callejas N. Environmental education and community attitudes about conservation of Mexican wild primates: compromises and activities on Tabasco state. Shanee A, Shanee N, Horwich R. Protecting Perus en demic primates: conservation contagion in the Tropical Andes. Shimooka Y. Flexibility in female relationship of spider monkeys. Slater KY, Burdekin OJ, Wallis B, Hill RA. e relation ship between group size and 2D versus 3D estimates of home range size in a hyper dense population of mantled howler monkeys ( Alouatta palliata ). Slater KY, Fielder H. Female vigilance in response to male loud calls in a hyper-dense population of mantled howler monkeys ( Alouatta palliata ). Smith-Aguilar SE, Ramos-Fernandez G, Aureli F, Schaner CM, Vick LG. Long term patterns of space use by spider monkeys ( Ateles georoyi ) in Punta Laguna, Yucatan Pen insula, Mexico. Souza-Alves JP, Ferrari SF. Unwanted homecoming: an adult male titi ( Callicebus coimbrai ) retuns to its natal group. Souza-Alves JP, Fontes IP, Ferrari SF. Extreme sleeping site delity in a group of Callicebus coimbrai. Stevenson P, Ramirez MA, Vargas S, Galvis N. Leon J, Cifuentes E. Population densities and behavior of high land woolly monkeys at the Cueva de los Guacharos Na tional Park, Colombia. Strier KB, Mendes SL. Grandmotherhood and the north ern muriqui ( Brachyteles hypoxanthus ) Strier KB, Mendes SL. Long term perspectives on social plasticity in the northern muriqui, Brachyteles ssp. Takimoto A, Fujita K. Nature of prosociality in tufted ca puchin monkeys. Talebi M. Current perspectives and challenges for the future of Brazilian primatology. Talebi M. Fruit phenology of the dietary items of southern muriquis ( Brachyteles arachnoides ) in the last fragment of continuous Brazilian Atlantic forest, Sao Paulo state, Brazil. Teixeira DS, Nobrega Y, Carvalho RM, Castro L, de Carv alho MM, Santos RA, Teruya V, Pratesi R. Assessment of vitamin D levels in primates Callhithrix pennicilata in its natural habitat in Brazil. Teixeira RG, Jardim LL, da Silva LG, Hasui E. Explaining and predicting Callicebus nigrifrons presence and a frag mented landscape. Valencia LM, Link A, Cadena CD, Di Fiore A. Current taxonomic status of the critically endangered brown spider monkey ( Ateles hybridus ). Van Belle S, Estrada A, Garber PA. Spatial and temporal patterns of loud calls in black howler monkeys ( Alouatta pigra ). Van der Heide G, Fernandez-Duque E. Getting through the winter: dry season resources and their inuence on owl monkey ( Aotus azarai ) reproduction. Vick LG. Developmental exibility in immature spider monkeys ( Ateles georoyi ). Vidal-Garcia F, Serio-Silva JC. Verication of predicted distribution of howler monkeys ( Alouatta pigra and Al ouatta palliata ) in Tabasco, Mexico. Watsa M. A revision of eld methods for capturing and marking free-ranging saddleback tamarins ( Saguinus fusi colis ) and emperor tamarins ( Saguinus imperator ). Williams LE, Brady AG, Abee CR. e owl monkey breed ing and research resource: a national resource in the USA. Winandy MM, Verderane MP, Ferreira GR, Izar P. Eects of demography on the social structure of tufted capuchin monkeys ( Sapajus sp.) Wolovich CK, Perea-Rodriguez, Evans S. Behavioral re sponses to chemical signals in the nocturnal owl monkey ( Aotus nancymaae ). Zarate DA, Santos-Heredia C, Andresen E, Stevenson PR. Shaded cocoa plantations provide habitat and food re sources to howler monkeys ( Alouatta pigra ) and woolly monkey ( Lagothrix lagotricha) in Mexico and Colombia.
68 Mnb PRIMER CONGRESO ARGENTINO DE BIOLOGIA DEL COMPORTAMIENTO El primer congreso Argentino de Biologa del Comporta miento se llevar a cabo del 15-17 de abril, 2013, en Mar del Plata, Argentina. Este ser un espacio para la presenta cin, discusin y sntesis del conocimiento cientco sobre biologa y ecologa del comportamiento. Se promover la comparacin de resultados obtenidos a travs de distintos sistemas de estudio y en relacin al conocimiento generado en otros lugares del mundo. Fecha lmite para envo de re smenes: 10 de diciembre de 2012. Para mayores informes visitar: www.grieta.org.ar/comporta/index.htm 36TH MEETING OF THE AMERICAN SOCIETY OF PRIMATOLOGISTS e 36th meeting of the American Society of Primatolo gists will be held in San Juan, Puerto Rico, with tentative dates of June 18-22, 2013, in conjunction with the Ca ribbean Primate Research Centers 75th anniversary. Our annual meetings allow primatologists worldwide to meet and discuss their latest research. Each meeting includes a mix of invited addresses by eminent primatologists, themed symposia, and the presentation of contributed papers. For more information go to www.asp.org/meetings/ II CONGRESSO LATINOAMERICANO DE PRIMATOLOGIA E XV CONGRES SO BRASILEIRO DE PRIMATOLOGIA Agosto 4, 2013 Agosto 9, 2013, Recife, Pernambuco, Brasil. Organizado pela Sociedade Brasileira de Primatologia. Para mais informaes visite o seguinte link: http://www. cbprimatologia.com.br/ 5TH CONGRESS OF THE EUROPEAN FEDERA TION FOR PRIMATOLOGY We are pleased to invite you to the 5th Congress of the Eu ropean Federation for Primatology, which will take place in Antwerp, Belgium from 10 th 13 th September 2013. e general theme of the conference Primates in our hands refers to fact that, to date, survival of many primate species lies in the hands of mankind. erefore, sharing and ex changing scientic knowledge on all aspects of primate bi ology is our duty. A broad range of topics will be addressed ranging from conservation biology, behaviour and cogni tion, physiology, ecology to functional morphology. More details will be posted on the website www.efp2013.org
Scope e journal/newsletter aims to provide a basis for conservation information relating to the primates of the Neotropics. We welcome texts on any aspect of primate conservation, including articles, thesis abstracts, news items, recent events, recent publications, primatological society information and suchlike. Submissions Please send all English and Spanish contributions to: Erwin Palacios, Conservacin Internacional Colombia, Carrera 13 # 71-41 Bogot D.C., Colombia, Tel: (571) 345-2852/54, Fax: (571) 3452852/54, e-mail:
Neotropical Primates A Journal and Newsletter of the IUCN/SSC Primate Specialist Group Vol. 19(1), December 2012ContentsArticlese Ecology of Trunk-to-Trunk Leaping in Saguinus fuscicollis: Implications for Understanding Locomotor Diversity in Callitrichines . ...................................................................................................................... 1P. A. Garber, A. C. McKenney and E. K. MallottDistribution, Habitat and Status of the White-Coated Titi Monkey (Callicebus pallescens) in the Chaco Chiquitano Forests of Santa Cruz, Bolivia . ................................................................................................................ 8Damin I. RumizPrimates of the Lower Urubamba Region, Peru, with Comments on Other Mammals . ........................................... 16Tremaine Gregory, Farah Carrasco Rueda, Jessica L. Deichmann, Joseph Kolowski and Alfonso AlonsoShort ArticlesI ndcios de P redao de O vos de C aiman c rocodilus (J acar T inga) por S aimiri sp. (M acaco d e C heiro) ................................................ 24 Rafael S Leito Barboza, Jos Francisco Reis da Costa, Alfredo Fonseca Andrade, Juarez Carlos de Brito Pezzuti George Henrique Reblo Identifying and Prioritizing Forest Patches Key for the Survival of the Golden-Headed Lion Tamarin (Leontopithecus chrysomelas) . .... 28 Sara L. Zeigler Correo da Distribuio Geogrca do Parauacu-Cinza (Pithecia irrorata Gray 1842) no Limite Sudoeste da Amaznia Brasileira . ... 34 Ricardo Sampaio Robson Odeli Espndola Hack, Kurazo Mateus Okada Aguiar Adriana Akemi Kuniy e Jos de Sousa e Silva Jr Predation Attempt on a Road-Killed Brown-Eared Woolly Opossum ( C aluromys lanatus) by a Black-Horned Capuchin (Sapajus nigritus) . ........................................................................................................................................................................ 36 Francesca Belem Lopes Palmeira and Camila Camara Pianca Parasitos Gastrointestinales en el Mono Choro Cola Amarilla (Oreonax avicauda) y el Mono Nocturno Andino (Aotus miconax) en Amazonas, Peru . ........................................................................................................................................... 38 Jssica Snchez Larraaga y Sam Shanee Twins and Infanticide in Red Howler Monkeys Inhabiting a Fragment in Western Orinoquia . .................................................. 41 Marta L. Beltrn and Pablo R. Stevenson Morphometric data from a wild female titi monkey, Callicebus cupreus . ...................................................................................... 42 Eckhard W. Heymann, Jenni G. Prez Yamacita and Britta Mller Alouatta caraya: Nuevo Sitio de Estudio en Argentina . ................................................................................................................ 44 Gabriela Bruno Carola Milozzi y Marta D. Mudry A Record of the Variegated Spider Monkey (Ateles hybridus brunneus) in Selva de Florencia National Park, Colombia . .............. 46 Nstor Roncancio Duque Registros de Juvenis Perdidos de Alouatta fusca (Georoy Saint-Hilaire, 1812) (Primates; Atelidae) no Parque Nacional da Serra dos rgos . .................................................................................................................................................................... 47 Bruna Maia e Pedro Henrique dos Santos DiasObituary . ................................................................................................................................................................ 49 News . ...................................................................................................................................................................... 57 Recent Publications . ................................................................................................................................................ 58 Meetings . ................................................................................................................................................................ 68