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PREDATION ON INVASIVE LIONFISH VARIES WITH THEIR SIZE, AMONG HABITATS, AND WITH CONDITIONING OF NATIVE PREDATORS By JESSICA L DILLER A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2014
2014 Jessica L Diller
To my dad, who inspired my love of the ocean and science
4 ACKNOWLEDGMENTS I thank the MANY volunteers who helped with fish collections on this project, especially G reg Locher Nick McIntosh, and the divemasters at Southern Cross Club, Little Cayman Beach Resort, and Pirates Point Resort. I thank the CCMI girls for their willingness to be my dive buddies and always giving moral support, especially Heather Murray, Katie Lohr, Emma Camp Becks Green, and Savanna Ba rry Additionally, I appreciate the logistical support from the Little Cayman Research Centre and its staff Lowell Forbes and Rob Hedges I also thank my funding sources: National Science Foundation Graduate Research Fellowship under Grant No. DGE 1315138 the University of Florida Tropical Conservation and Development Field Research Grant, the University of Florida Office of Research, and the Central Caribbean Marine Institute. I also thank Dr. Chuck Jacoby for his patience in helping guide me through ana lysis and interpreting results. Lastly, I thank Dr. Tom Frazer for allowing me the freedom and time to develop this project and explore my interdisciplinary interests throughout my masters program.
5 TABLE OF CONTENTS page ACKNOWLEDGMENTS ................................ ................................ ................................ .. 4 LIST OF TABLES ................................ ................................ ................................ ............ 6 LIST OF FIGURES ................................ ................................ ................................ .......... 7 ABSTRACT ................................ ................................ ................................ ..................... 8 CHAPTER 1 I NTRODUCTION ................................ ................................ ................................ ........ 10 2 METHODS ................................ ................................ ................................ ................. 13 3 RESULTS ................................ ................................ ................................ ................... 14 4 DISCUSSION ................................ ................................ ................................ ............. 17 LIST OF REFERENCES ................................ ................................ ............................... 21 BIOGRAPHIC AL SKETCH ................................ ................................ ............................ 26
6 LIST OF TABLES Table page 3 1. L ogistic regressions pr edicting potential for predation ................................ ........... 15
7 LIST OF FIGURES Figure page 3 1. Potential for predation versus total length by A) time and B) habitat ..................... 16
8 Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science PREDATION ON INVASIVE LIONFISH VARIES WITH THEIR SIZE, AMONG HABITATS, AND WITH CONDITIONING OF NATIVE PREDATORS By Jessica L Diller May 2014 Chair: Thomas Frazer Major: Interdisciplinary Ecology Invasive species often exacerbate global and local stresses on ecosystems, with invaders commonly experiencing a release from enemies, including diseases and predators. Release from predation helps explain the lionfish ( Pterois volitans / miles ) invasion of the western Atlantic, Caribbean and Gulf of Mexico However the extent of biological control exerted by native predators is a topic of debate centered on interpretation of spatial distributions of lionfish and predators In many places, control of lionfish relies on people acting as predators via culls. In some cases the resulting dead or injured lionfish are eaten by sharks and groupers, which may condition these nave, native pre dators. T his study complements existing field surveys by assess ing the potential for predation on invasive lionfish at Little Cayman Island, BWI with tethering experiments We tethered 132 live lionfish (52 220 mm total length) in three different habitats: seagrass beds, rarely culled reefs, and intensely culled reefs. Binary logistic regression indicated that the potential for predation increased slightly (1.02 ) but significantly with 1 mm increases in total length. In addition, lionfish tethered on intensely culled reefs were 30 and 14 more likely to be taken by piscivores than fish
9 tethered in seagrass or on rarely culled reefs. Overall, results suggested that native predators were capable of consuming healthy, tethered lionfish off Little Cayman Island and the navet of native predators was overcome by conditioning. Of course, conditioning designed to increase predation on lionfish, augment culling and help control the invasion must be implemented without endangering people.
10 CHAPTER 1 INTRODUCTION Invasive species often exacerbate problems caused by climate change, nutrient pollution, overfishing and other global and local anthropo genic stresses, with many negative outcomes impinging heavily on threatened and endangered species (Vitousek et al. 1997a; Mack et al. 2000). Each year, invasive species ultimately generate hundreds of billions of dollars in global environmental and econom ic costs (Pimental et al. 2001). Once established, invasive species create direct, detrimental impacts via predation and competition for resources; indirect impacts by altering habitats and interactions among species; and disruptions of ecosystem structure and function by decreasing or homogenizing biodiversity (Vitousek et al. 1997b; Mack et al. 2000; Pimental et al. 2001). All of these concerns apply to invasive, predatory, Indo Pacific lionfish ( Pterois volitans and P. miles or Pterois spp .). Since 1985, lionfish have spread up the Atlantic seaboard from Dania Beach, Florida, expanded throughout the Caribbean, colonized the northern Gulf of Mexico, and reached densities of 400 650 fish ha 1 in multiple locations (Morris and Whitfield 2009; Schofield 2010; Green and Ct 2009; Frazer et al. 2012). As voracious predators that consume up to 4% of their body weight per day in fish and invertebrates, lionfish potentially reduce numbers of native species and increase competition for food (Albins and Hixon 2008; Morris and Akins 2009; Morris and Hixon 2013; Ct et al. 2013). For example, lionfish on experimental patch reefs in the Bahamas reduced recruitment of native, reef fishes that serve as prey for important fishery species by ~80% (Albins and Hixon 2008). Furthermore, lionfish occupy and
11 feed in mangroves (Barbour et al. 2010) and seagrass beds (Claydon et al. 2012), which serve as important nurseries for juvenile reef fish ( Nagelkerken et al. 2002). Through predation and competition, lionfish can reduce recruitment of species that support fisheries and further lower yields that are predicted to decrease 30 45% by 2015 due to degradation of Caribbean reefs (Burke and Maidens 2 004). In addition, predation on parrotfishes, surgeonfishes and damselfishes reduces grazing on algae that can overgrow corals (Lesser and Slattery 2011). In combination, reduced biodiversity, increased overgrowth of corals by algae, and the possibility of envenomation from lionfish spines can compromise the attractiveness of popular dive destinations, which presently generate US$2.1 billion per year (Burke and Maidens 2004 ; Morris and Whitfield 2009 ). In many places, these deleterious effects will exacerba te detrimental changes from other stressors, including anthropogenic nutrient loads, overfishing, pollution, coral bleaching and disease, and climate change (Frazer et al. 2012; Albins and Hixon 2013; Ct et al. 2013). Lionfish possess a suite of characte ristics that promote a successful invasion. They grow quickly; mature early; potentially reproduce often; release their eggs in a protective, gelatinous mass that may enhance fertilization and provide protection; feed voraciously on diverse prey using nove l techniques that include blowing jets of water; and appear to have been released from mortality caused by disease, parasites or predators (Morris and Whitfield 2009; Albins and Lyons 2012; Albins and Hixon 2013; Ct et al. 2013). The potential release fr om predation comprises the focus of this work. Reduced predation would explain why lionfish are substantially more abundant in the invaded range (Darling et al. 2011; Cure et al. 2012; Kulbicki et al. 2012). For
12 example, nave predators approaching lionfis h likely are deterred when their potential prey do not flee but rather display their dorsal and pectoral fins equipped with venomous spines (Morris and Whitfield 2009; Ct et al. 2013). In fact, there have been no reported observations of predation on uni njured lionfish in either their native or invaded ranges, with such events being inferred from the presence of lionfish in the Two peer reviewed manuscripts (Jud et al. 201 1; Pimiento et al. 2013) and numerous anecdotal reports indicated that predators consumed dead or injured lionfish from organized culls, including culls conducted off Little Cayman Island (Frazer et al. 2012). The dearth of direct observations has not dete rred scientists from inferring either the presence or absence of significant predation based on spatial patterns in abundance or biomass documented during field surveys comprising mensurative experiments (Mumby et al. 2011; Hackerott et al. 2013; Mumby et al. 2013; Bruno 2013; Bruno et al. 2013). In combination, the absence of direct observations of predation on uninjured lionfish, the debate surrounding interpretation of field surveys, records of native predators eating dead or injured lionfish generated d uring culls, and evidence that fish learn to feed on novel prey (Warburton 2003) led us to design and implement a manipulative, tethering experiment at Little Cayman Island. This experiment tested the hypotheses that i) native predators will consume health y, tethered lionfish and ii) experience with consuming dead or injured lionfish will enhance the likelihood of predation, i.e., nave predators will learn to feed on lionfish.
13 C HAPTER 2 M ETHODS Lionfish were hand collected off Little Cayman Island in January August 2013. On the day of deployment, each fish was anesthetized, measured (mm total length; TL), and fitted with 20 cm of monofilament line secured to its lower jaw. Fish were held for 2 h to ensure tethers were secure, transported to field sites, and attache d to lead weights (13:00 15:00 h). The following morning (07:30 09:00 h), missing fish and cleanly broken tethers were recorded as predation events and the remaining lionfish were euthanized. Controls for tethering effects comprised three fish tethered in tanks for 24 h and video surveillance of fish in the field. From 9 to 15 lionfish were tethered at intensely culled fore reef sites where spearfishers had removed lionfish approximately monthly for 3 years (Frazer et al. 2012; n = 3), rarely culled fore re ef sites (n = 3), and back reef seagrass sites with no record of culling (n = 4). At sites with Thalassia testudinum lionfish were tethered at 3 m intervals along transects at ~1 m depth. At reef sites, lionfish were tethered 3 5 m apart on sand or hard b ottom at depths of 4.5 9.0 m. Tethered fish could not access a refuge, and fish were not deployed when large piscivores were visible. Data were analyzed with a one way analysis of variance and three binary logistic regressions. The analysis of variance ass essed differences in fish size among habitats. An initial binary logistic regression assessed total length as a covariate and temporal differences in potential for predation between independent trials at rarely culled reefs. Additional regressions tested f or differences with total lengths and among habitats using deviance and Hosmer Lemeshow tests assessed goodness of fit for these regressions.
14 CHAPTER 3 R ESULTS In total, 132 lionfish we re tethered to lead weights in the three habitats, and these fish were similar in size (F 2,129 = 0.80, p = 0.451), with mean TLs standard deviations (SD) of 115.3 34.9 mm in seagrass, 119.7 34.8 mm on rarely culled reefs, and 126.6 44.1 mm on intensely culled reefs. Tethering was not considered a potential cause of mortality because tethere d lionfish survived for 24 h after being attached to weights in a controlled laboratory environment In addition, a total of 21 videos showed that lionfish in the field did not exhibit signs of stress, with fish resting just above the substrate or swimming slowly within 5 min of being deployed. Videos also revealed that tethered lionfish assumed a typical head down, fins spread position (Ct et al. 2013) as their initial response to Nassau grouper ( Epinephelus striatus ) and nurse sharks ( Ginglymostoma cirr atum ), with multiple encounters culminating in predation. Logistics associated with capturing live specimens meant that trials were conducted in January, March, May, July and August 2013. An initial binary logistic regression indicated that the potential f or predation varied significantly with the TL of lionfish (range = 52 220 mm), but the potential for predation was not significantly different between the two, temporally independent trials at the rarely culled reefs (January May and July August 2013, Tabl e 3 1, Fig ure 3 1A). As the TLs of lionfish increased by 1 mm, they became 1.02 more likely to be consumed. The lack of a significant difference between the two trials at the rarely culled reefs led us to pool all data to examine variation in predation among th e three habitats. The remaining logistic regressions indicated significant variation with TLs and between the intensely culled reefs and the other two habitats (Table 3 1; Fig ure 3 1B).
15 Again, as the TLs of lionfish increased by 1 mm, they were 1.02 more likely to be consumed. The potential for predation was significantly higher on intensely culled reefs, with lionfish tethered at these reefs being 13.56 more likely to be consumed than fish tethered on a rarely culled reef and 29.88 more likely to be consumed than fish tethered in seagrass. The potential for predation differed less between rarely culled reefs and seagrass (p = 0.089, Table 3 1), but lionfish tethered on rarely culled reefs were 2.20 more likely to be taken. In combination, the relati onships with lionfish size when tethered o n intensely cu lled reefs (Figure 3 1 ). Note: Pred = predictor; Coef = coefficient; SE = standard error for coefficient; OR = odds ratio; 95% CL = 95% confidence limits for coefficient; L = lower confidence limit; U = upper confidence limit; G o F = goodness of fit tests; Con = constant; TL = total length (mm); T1 = Januar y May 2013; T2 = July August 2013; In = intensely culled; Sg = L Hosmer Lemeshow test. Table 3 1. Results of logistic regressions predicting potential for predation on Pterois spp. Pred Coef SE Z p OR 95% CL G o F 2 df p L U Con 2.605 1.064 2.45 0.014 P 56.00 54 0.400 TL 0.020 0.009 2.27 0.023 1.02 1.00 1.04 D 70.17 54 0.069 T1 v T2 0.198 0.557 0.36 0.722 0.82 0.28 2.44 H L 9.97 8 0.267 Con 3.350 0.864 3.87 < 0.001 P 117.49 114 0.392 TL 0.018 0.006 2.96 0.003 1.02 1.01 1.03 D 125.58 114 0.216 In v Sg 3.397 0.740 4.59 < 0.001 29.88 7.01 127.32 H L 4.88 8 0.770 Ra v Sg 0.790 0.465 1.70 0.089 2.20 0.89 5.48 Con 2.560 0.809 3.16 0.002 P 117.49 114 0.392 TL 0.018 0.006 2.96 0.003 1.02 1.01 1.03 D 125.58 114 0.216 In v Ra 2.607 0.687 3.79 < 0.001 13.56 3.52 52.17 H L 4.88 8 0.770 Sg v Ra 0.790 0.465 1.70 0.089 0.45 0.18 1.13
16 Figure 3 1. Potential for predation versus total length for Pterois spp. tethered A) on rarely culled reefs at two different times and B) on intensely culled reefs, on rarely culled reefs and in seagrass.
17 CHAPTER 4 D ISCUSSION Successful invasions by medium sized predators, such as lionfish, are facilitated by nave prey (prey navet), nave top predators (enemy release hypothesis), and diversion of time and energy from avoiding predators into feeding and reproducing (evolution of increased competitive ability; Sih et al. 2010). In fact, lionfish appear to be successful competitors in their invaded range because their feeding and antipredator behaviors are unlike those of similar predators in the Caribbean (Albins and Lyons 2012 ; Green et al. 2012; Albins 2013; Albins and Hixon 2013; Ct et al. 2013). With respect to the enemy release hypothesis, estimates of potential for predation in the three habitats suggested that predation on lionfish by native piscivores can be increased by taking advantage of the behavioral plasticity displayed by native predators (Carlsson et al. 2009). The potential for predation documented at the intensely culled reefs indicated that native predators conditioned to eat lionfish killed or injured during culls learned to hunt, capture and consume this novel prey without human intervention. Similar learning has been observed in other predator prey systems, including laboratory training of small spotted catsharks ( Scyliorhinus canicula ) that was retained wi thout reinforcement for up to 3 weeks (Warburton 2003; Carlsson et al. 2009; Santos et al. 2009; Kimber et al. 2014). Thus, results indicated that biological control exerted by native predators could augment culling as a tool to manage the lionfish invasio n. The observed increase in potential for predation with lionfish body size could be explained in part by lionfish crypticity. Juvenile lionfish are light colored and the smallest individuals are nearly transparent They become darker and more conspicuo us
18 as they age and grow (Allen and Eschmeyer 1973). If juvenile lionfish are indeed more cryptic, prey would be an important management intervention because culling tends to target larger lionfish (Frazer et al. 2012) and models have identified removal of juvenile lionfish as a way to increase the efficacy of this management technique (Barbour et al. 2011 ; Morris et al. 2011 ). Previous studies have shown that repeated exposure to novel prey items i ncreases predator recognition efficiency (Ware, 1972; Colgan et al. 1986); t herefore, conditioning native predators with juvenile lionfish could be a crucial addition to control ling lionfish populations. Furthermore, a tethering experiment targeting larger lionfish may identify a size refuge from native predators. In this study, nurse sharks ( G. cirratum ) and Nassau grouper ( E. striatus ) definitely consumed healthy, tethered lionfish. Data on the abundance and distribution of these predators from Little Cay man Island provided explanations for increases in potential for predation from seagrass to rarely culled reefs to intensely culled reefs. The abundance and diversity of sharks in the waters surrounding the Cayman Islands were equal to or greater than recor ds for other locations in the Caribbean region according to a recent study of sharks and cetaceans (Department of Environment Cayman Islands 2012). Nurse sharks were common, and they were observed, tracked and caught in multiple habitats, including seagras s and reefs. Nurse sharks tended to spend less time in shallow seagrass than in deeper habitats, with similar results al. 2005), the Florida Keys (Heithaus et al. 2007) and the United States Virgin Islands
19 (DeAngelis et al. 2008). Thus, the distribution of nurse sharks helped explain a higher potential for predation at reef sites. Similarly, Nassau grouper occupied both seagrass and reef habitats off Little Cayman Islan d (Camp et al. 2013). Small Nassau grouper (mean TL SD = 184 34 mm) predominately occupied seagrass habitats (Camp et al. 2013), and data collected during Atlantic and Gulf Rapid Reef Assessments in 1999, 2006, 2007 and 2009 indicated that larger group er (110 mm to > 400 mm TL) were evenly distributed on reefs around the island (F 1,279 = 0.61 p =0.437 ; mean density standard error for leeward and windward reefs = 6.1 2.1 grouper ha 1 and 6.4 2.2 grouper ha 1 respectively). Given the tendency for Nassau grouper to eat prey that average 15% of their body size (Sadovy and Eklund 1999), grouper in seagrass habitats would have been limited to preying on the smallest lionfish, which also helped explain a lower potential for preda tion in this habitat. The relatively consistent spatial distribution of larger grouper across all reefs suggested that variation in numbers of this predator did not cause a difference in potential for predation between intensely and rarely culled reefs. Ov erall, available information suggested that the potential for predation should be greater on reefs than in seagrass, which it was. In addition, the abundances of nurse sharks and Nassau grouper on all reefs at Little Cayman Island pointed to conditioning a s the cause of variation in potential for predation between intensely and rarely culled reefs. There are caveats associated with tethering experiments (Peterson and Black 1994; Aronson and Heck 1995; Aronson et al. 2001), but several lines of evidence sugg est the results reported here yield value. Tethering generated minimal injury and
20 did not release body fluids that would attract predators. As reported elsewhere (Aronson and Heck 1995), the fact that fewer tethered lionfish were consumed at seagrass sites where vertical structure was denser, indicated that entanglement was not a substantial bias. Videos showed that tethered fish behaved similarly to untethered lionfish by hovering near the substrate within minutes of deployment and employing a typical res ponse to predators (Ct et al. 2013). Despite this latter behavior, videos documented predation by two different piscivores, nurse sharks and Nassau grouper, with neither predator deterred by contact with the venomous spines. In addition, independent tria ls at rarely culled reefs yielded consistent and statistically equivalent results, which suggest the potential for predation was stable through time. The results of tethering experiments indicated that conditioning of native piscivores will augment spatial ly restricted culling and potentially overcome the resilience to culling predicted for lionfish (Barbour et al. 2011 ; Morris et al. 2011 ) Even if the current geographic range and rapid population growth of lionfish make complete eradication untenable inc reased predation would extend the effects of culling in space and through time, which would alleviate predation pressure on species that are vulnerable to extinction or critical to the health of coral reefs (Frazer et al. 2012; Albins and Hixon 2013; Ct et al. 2013 ; de Leon et al. 2013 ) Any attempt to condition native piscivores must be done in a way that minimizes threats to humans who share the environment with the predators being trained and invasive lionfish.
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26 BIOGRAPHICAL SKETCH Jessica received a Bachelor of Science in Biology from the University of Texas in 2008. She became interested in integrating human dimensions into natural sciences while working on the Deepwater Horizon Oil Spill in 2010, and was accepted into the Universi 2011. While taking diverse coursework focusing on marine ecology, tropical conservation and development, communication skills, environmental education, and science education, sh e earned a graduate certificate in Environmental Education and Communication. In May of 2014 she received her Master of Science degree in Interdisciplinary Ecology.