Cross-Kingdom Consumer Diversity Enhances Multifunctionality of a Coastal Ecosystem

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Cross-Kingdom Consumer Diversity Enhances Multifunctionality of a Coastal Ecosystem
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Hensel, Marc J
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Master's ( M.S.)
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Zoology, Biology
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Silliman, Brian
Committee Members:
Palmer, Todd
Osenberg, Craig Warren

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biodviersity -- foodweb -- functioning -- fungus -- marsh
Biology -- Dissertations, Academic -- UF
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Abstract:
The global biodiversity crisis impairs the valuable benefits ecosystems provide human society.  These nature-generated benefits (i.e. services) are defined by a multitude of different ecosystem functions that operate simultaneously. How species extinctions, either globally or locally, will affect simultaneous functioning (i.e. multifunctionality), remains unstudied in real-world food-web assemblages.  Here, we investigated experimentally the extinction impacts of dominant and phylogenetically diverse salt marsh consumers (i.e., Kingdom Animalia and Fungi) and reveal that a diverse consumer assemblage significantly enhances ecosystem multifunctionality.  High functional turnover among consumers was found to drive a positive diversity-function relationship, where each marsh consumer affected at least one different ecosystem function, but no individual function was affected by more than two consumers.  Although overlooked in past food web-diversity studies, microbes (i.e. fungi) were significant forces driving enhanced ecosystem functioning.  These results provide the first experimental evidence that maximizing ecosystem multifunctionality depends on maintaining high-levels of both functional and taxonomic consumer diversity. Moreover, it emphasizes the need to incorporate both micro- and macro-components of food webs to accurately predict biodiversity declines on integrated-ecosystem functioning.
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by Marc J Hensel.
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Thesis (M.S.)--University of Florida, 2013.
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Adviser: Silliman, Brian.
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1 CROSS KINGDOM CONSUMER DIVERSITY ENHANCES MULTIFUNCTIONALITY OF A COASTAL ECOSYSTEM By MARC JAMES SIMON HENSEL 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 2013

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2 2013 Marc James Simon Hensel

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3 To Don

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4 ACKNOWLEDGMENTS I thank Joan Simon and Dr. James Hensel for your continued support and encouragement on my path to becoming an ecologist. Your guided advice has helped me every step of the way. I thank Stephanie Buhler both for your pugnacious help in the field and for constantly challenging me to improve. I look forward to growing as eco logists and to our many future forays into the field together. I thank John Griffin and Christine Angelini for the countless hours of both field and writing help you have given me over the last three years. I thank James Nifong and Schuyler van Montfrans for being an enormous part of my academic and personal development as a graduate student I thank Danielle Abbey, Eric Monaco, and Alvin Beyerlein for their help in the field over the course of this project. The combination of hard work and great attitudes from each of you made long, hot Sapelo days much more enjoyable.

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5 TABLE OF CONTENTS page ACKNOWLEDGMENTS ................................ ................................ ................................ .. 4 LIST OF TABLES ................................ ................................ ................................ ............ 6 LIST OF FIGURES ................................ ................................ ................................ .......... 7 ABSTRACT ................................ ................................ ................................ ..................... 8 CHAPTER 1 INTRODUCTION ................................ ................................ ................................ .... 10 2 METHODS ................................ ................................ ................................ .............. 12 Study System ................................ ................................ ................................ .......... 12 Experiment ................................ ................................ ................................ .............. 12 Ecosystem Function 1: Net Primary Production (NPP) ................................ ........... 13 Ecosystem Function 2: Decomposition rate ................................ ............................ 14 Ecosystem Function 3: Infiltration rate measurement ................................ ............. 14 Assessing Multifunctionality ................................ ................................ .................... 15 Statistical Analysis ................................ ................................ ................................ .. 16 3 RESULTS ................................ ................................ ................................ ............... 17 4 DISCUSSION ................................ ................................ ................................ ......... 25 Consumer Diversity and Ecosystem Multifunctionality ................................ ............ 25 Consumer Regulation of Coastal Wetland Ecosystem Function ............................. 27 Incorporating Microbes into Consumer Diversity Ecosystem Function Studies ...... 28 LIST OF REFERENCES ................................ ................................ ............................... 30 BIOGRAPHICAL SKETCH ................................ ................................ ............................ 34

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6 LIST OF TABLES Table page 3 1 Coefficient table from regression of consumer diversity and ecosystem functions. ................................ ................................ ................................ ............ 20

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7 LIST OF FIGURES Figure page 3 1 Ergosterol recovered. Mean ergosterol (ug/g) recovered from representative 5 cm Spartina leaves ................................ ................................ .......................... 2 0 3 2 Effect of each consumer removal ( ) and consumer presence (+) on a) decomposition rate b) net primary production c) infiltration, and d) average multifunctionality ................................ ................................ ................................ 21 3 3 Effect of species richness on single functions and multifunctionality. Increasing number of consumers (i.e. species richness) had variable effects on regressions of single ecosystem functions ................................ .................... 22 3 4 Multifunctionality threshold ................................ ................................ ................. 23 3 5 Probabil ity of maintaining multifunctionality thresholds ................................ ....... 24

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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 CROSS KINGDOM CONSUMER DIVER SI TY ENHANCES MULTIFUNCTIONALITY OF A COASTAL ECOSYSTEM By Marc James Simon Hensel August 2013 Chair: Brian Silliman Major: Zoology The global biodiversity crisis impairs the valuable benefits ecosystems provide human society. These nature generated benefits (i.e. services) are defined by a multitude of different ecosystem functions that operate simultaneously. How species extinction s, either globally or locally, will affect simultaneous functioning (i.e. multifunctionality), remains unstudied in real world food web assemblages. Here, we investigated experimentally the extinction impacts of dominant and phylogenetically diverse salt marsh consumers (i.e., Kingdom Animalia and Fungi) and reveal that a diverse consumer assemblage significantly enhances ecosystem multifunctionality. High functional turnover among consumers was found to drive a positive diversity function relationship, w here each marsh consumer affected at least one different ecosystem function, but no individual function was affected by more than two consumers. Although overlooked in past food web diversity studies, microbes (i.e. fungi) were significant forces driving enhanced ecosystem functioning. These results provide the first experimental evidence that maximizing ecosystem multifunctionality depends on maintaining high levels of both functional and taxonomic consumer

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9 diversity. Moreover, it emphasizes the need to incorporate both micro and macro components of food webs to accurately predict biodiversity declines on integrated ecosystem functioning.

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10 CHAPTER 1 INTRODUCTION Two decades of empirical studies reveal biodiversity loss can decrease the efficiency of ecosystem functions and reduce the magnitude and quality of services they provide ( 1 8 ) This body of work has demonstrated that, when measuring functions individually, maintaining high diversity can maximize certain functions ( 2 ) Because natural habitats are valued for performing more than one function at a time ( 9 ) we must now explore the link between biodiversity loss and the simultaneous performance of multiple ecosystem functions (i.e. multifunctionality). Only a few studies have explored this topic, and their findings suggest high species richness is required to maintain high levels of multifunctionality ( 5 10 14 ) These investigations, however, did not incorporate real world food web scenarios (i.e. studies were plant or microbe only in design) and thus the biodiversity multifunctionality hypothesis remains experimentally untested amongst the species most vulnerable to extinction [i.e. consumers ( 15 ) ]. Consumers, such as grazers and apex predators, play key roles in most natural communities (e.g., kelps, seagrasse s, coral reefs, tropical and temperate forests, grasslands, salt marshes, rocky shores, oyster reefs) regulating both key processes and habitat structure ( 16 20 ) From many studies, we know that decreases in consumer diversity can affect performance of single ecosystem functions, including primary and secondary production, decomposition and consumption rate across trophic levels ( 2 ) Although consumer diversity studies have taken important steps to better reflect real world scenarios ( 21 ) [e.g., studying species extinctions rather than additions ( 22 ) ], none have assessed effects of diver sity loss on an integrated measurement of ecosystem functioning and all have been limited in taxonomic scope, focusing on either macro or

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11 microbial consumers. Because of both the wide range of ecosystem functions that micro and macro consumers can regula te and that they commonly interact in nature (e.g. through facilitation, competition, parasitism), investigating the individual and interactive effects of taxonomically diverse consumers on multifunctionality is key to our understanding of realistic consum er biodiversity loss scenarios ( 23 24 ) In this study, we examine the relationship between consumer diversity and ecosystem multifunctionality in a Southeastern US salt marsh dominated by the cordgrass Spartina alterniflora (hereafter Spartina ). In an eight month field experiment, we manipulated the occurrences of the three most abundant salt marsh consumers: a snail Litoraria irrorata a crab Sesarma reticulatum and fungi [genus Phaesophaeria and Mycosphaerella ( 25 26 ) ], and measured effects on three separate ecosystem functions fundamental to the valuable services generated by coastal wetlands (i.e. rates of decomposition, net primary production, and infiltration). To assess the importance of marsh consumer diversity on multifunctionality, we quantified the average rate of the three functions ( 14 27 28 ) and how many of the functions exceeded a performance threshold ( 11 12 ) across different levels of diversity

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12 CHAPTER 2 METHODS Study System Field work was carried out in a salt marsh located within the Sapelo Island Spartina alterniflora dominates the plant communit y at this site, which is flooded twice daily by the tides. The field experiment was set up in the intermediate S. alterniflora zone (typically ~40 90 cm tall) where the invertebrate consumers, the purple marsh crab, Sesarma reticulatum and periwinkle snail Littoraria irrorata, are widely distributed and abundant (Soomdat et al. unpublished data ). Ascomycetes fungus (genera Phaesophaeria and Mycosphaerella ) has been shown in a prior study to be ubiquitous in this and other salt marshes on Sapelo Island (29) Experiment The experiment was run for 8 months from May December 2011. We manipulated the presence and absence of all three species in a factorial design that yielded 8 treatments and compromised 4 levels of diversity: three consumers (crabs+snails+fungus), two consumers (crabs+snails, crabs+fungus, snails+fungus), one consumer (crabs or snails or fungus), and no consumers. Sixty four plots were selected ( mean Spartina density: 120.8 6.2 stems/m 2 Treatments consisted of replicated (n=8) 1 m 2 roofless cages constructed out of 106cm tall aluminum flashing. To deter crab and snail movement in or out of cages, we sunk aluminum flashing, painted with anti fouling paint (Rust Oleum Boat Bottom Anti Fouling Paint, Rust Oleum, Vernon Hills, IL), 35 cm into the marsh. To reduce fungal biomass in fungal removal treatments, we sprayed Spartina stems with systemic fungicide (Daconil Ultrex

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13 Turf Care with Chloroth anla, Zeneca Company, Wilmington, DE) mixed with tap water every 5 days (29, 30) which has not been found to affect growth of Spartina plants in longer term experiments (29, 30) To control for possible positive effects of fungicide application, we sprayed an equivalent amount of tap water every 5 days in plots with ambient fungus levels. Negative effects of fungicide on the other microbes were like ly unimportant in overall functioning, as ascomycete fungi make up 95% of the microbial community by mass (<5% of the community is bacteria) ( 25 26 ) At the end of the experiment we used ergosterol proxy techniques to determine to determine the effect of fungicide on fungal biomass ( 26 ) and found fungicide application reduced fungal biomass by 60% ( P = 0.04, Fig. 3 1) Although Daconil can cause animal mortality, findings from this and other studies (29, 30) found no negative effect of fungicide on crabs or snails because fungicide was applied when marsh animals we re inactive (i.e. middle of the day, low tide). In each plot, the presence or absence of each consumer was manipulated and density was kept constant. We collected adult crabs (2.5 3.5cm carapace width) and adult snails (8 12 mm shell height) from nearby marshes and stocked cages with naturally high densities observed at our field site (10 crabs/m 2 500 snails/m 2 ) (Soomdat et al. unpublished data, (31) ). Densities were monitored once a week and crabs and snails were either added or removed as necessary to maintain treatment integrity. Ecosystem Function 1: Net Primary Production (NPP) To determine the effect of experimental consumer removals on net primary production, net Spartina production was estimated by measuring change in aboveground plant biomass from the beginning to end of the experiment. In May when the cages were dep loyed, we measured stem height and density in a representative

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14 0.5m 2 plot and converted these stem height and density values to an initial standing biomass using regressions based on plants sampled from just outside the plots. Inside each plot, we established a permanent 0.5 m 2 quadrat used to monitor live and dead Sparti na stem density every month. At the conclusion of the experiment, all Spartina remaining in a representative 0.5m 2 plot were harvested, rinsed in water, separated into live and dead stems, dried at 60C in an oven for 2 days, and weighed. Because initial conditions were nearly identical in all plots (mean Spartina biomass: 264.3 9.0 g/m 2 ) and because we used different methods at the start and end, net primary production was represented as total Spartina biomass remaining at the conclusion of the experim ent. Ecosystem Function 2: Decomposition rate We quantified the effect of consumer removals on marsh decomposition rate by deploying a plug consisting of 3 dead Spartina stems zip tied to a plastic flag post. In June 2011, stems were collected from a nearby marsh, rinsed, and dried for 24 hours at 60C before taking an initial mass. Each plug weighed 7.0 0.2g initially and was placed in the middle of each plot for 30 days. After 30 days the plug was retrieved from the plot, rinsed, and dried at 60 C for 24 hours. The dry stems were weighed and mass lost (g) was calculated. A new plug was placed in each plot and the procedure was repeated at the beginning of July and August. Mean percent biomass lost per month was calculated across three sampling periods (June, July, and August) Ecosystem Function 3: Infiltration rate measurement We quantified the effect of consumer removals on marsh infiltration at the conclusion of the experiment using a ring infiltrometer. Two hours after a high tide, we plac ed a 1.5L ring in a representative area of 4 plots per treatment and filled it with 1L of

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15 water from a nearby tidal creek and we measured the time required for the water to drain out of the ring (L/min). Assessing Multifunctionality To assess whether sn ail, crab and fungi consumers differed in their ability to perform all measured functions, we calculated an average multifunctionality index for each treatment. To do so, we defined the maximum from the three highest performing plots in the experiment. Fo r each plot, we then expressed its performance as the percentage of that maximum for decomposition, infiltration, and NPP, and averaged these percentages to obtain a multifunctionality index for each plot (see (13, 32, 33) for a simila r approach). To more directly assess the effect of diversity loss on simultaneous functioning, we also evaluated the ability for each treatment to achieve a multifunctionality threshold, which we defined as 50% of the maximum of the top three plots ( 11 12 32 ) As multifunctionality thresholds are a relatively new measure of functioning, there is no general criterion for maximum, average, or minimum functioning ( 12 ) On average, one species is needed to keep a given process at ~60% of its maximum rate ( 2 ) thus, using a 50% functioning threshold ensures that we can separate the effects of diversity loss functioning to be able to maintain multiple functions at this level (see ( 12 ) for similar approach). To ensure species richness effects on multifunctionality was not specific to the threshold chosen, we tested thresholds ranging from 30% to 80% functioning and f ound similar results (i.e. the ability for a community to maintain thresholds increases with diversity). For each level of diversity (zero, one, two, and three consumers), we calculated the mean number of functions that exceeded the 50% threshold.

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16 Statist ical Analysis Data were analyzed with JMP 9.0 (SAS Institute 2010). Differences in NPP, decomposition rate, and percolation rates were assessed with three way (crab x snail x hoc analysis. To separate the effe cts of diversity loss on ecosystem functioning we constructed one way ANOVAs using number of consumers as a predictor and functions as responses.

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17 CHAPTER 3 RESULTS Each consumer primarily affected one of the ecosystem functions (Fig. 3 2). Because we found no statistical interactions between consumers, we assessed the effect of each consumer on ecosystem functioning by quantifying the main effect of each consumer (crab, snail, fungi). Decomposition rate, measured in grams of dead Sparti na removed per month, was affected by removal of snails and fungicide application (Fig. 3 1a ). Decomposition rate was 1.6 slower when snails were removed ( P < 0.0001) and 1.2 slower when fungicide was added ( P < 0.0001). Net primary production (NPP) was most affected by crabs and fungicide (Fig. 3 2b); crab removal increased total biomass by 62% ( P < 0.0001) and fungicide application decreased total biomass by 33% ( P = 0.0005). Crab removal reduced infiltration rate by 83% (Fig. 3 2c, P < 0.0001), a findi ng that has negative effects on overall marsh biogeochemistry and slows nutrient transfer (34) Averaged across the three functions, multifunctionality was affected by both snails and fungus (Fig. 3 2d). Snail removal decreased multifunctionality by 16% ( P = 0.0017) and fungicide application decreased multifunctionality by 19% ( P < 0.0001), revealing that both macro and micro consumers played important roles in enhancing ecosystem multifunctionality. Crab removal, reduced multifunctionality by only 1% and this reduction was not statistically significant ( P = 0.95) To determine ho w species richness affected ecosystem functioning, irrespective of the identity of species included in treatments of a given richness level, we grouped treatments into levels of diversity (i.e. zero, one, two, or three consumers) and performed regressions with each single function and average multifunctionality.

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18 Additionally, to conservatively estimate the effects of diversity on each function, we calculated D max an overyielding criterion and measure of transgressive overyielding (Table 1) (35) Dec omposition rate (Fig. 3 3a) exhibited increased functioning with increasing diversity. Decomposition was the only ecosystem function significantly affected by diversity (P < 0.0001) where each increasing level of diversity resulted in a 14% rise in decompo sition rate. Decomposition was strongly influenced by overyielding (Table 1), most likely because two consumers (i.e. fungi, snails) significantly increased decomposition rate (Fig. 3 2a). Net primary production was not significantly affected by diversity (P = 0.2344, Fig. 3 3b), most likely because the negative effect of fungicide application was cancelled out by the positive effect of crab removal (see Fig. 3 2a) and because the best performing single species treatments outperformed diversity treatments ( D max = 0.04, Table 1). Infiltration was also not affected by diversity ( P = 0.0604, Fig. 3 3c) because this function was only increased by the crab ( Fig 3 2c). Despite variable effects on single functions, diversity strongly enhanced average salt marsh multifunctionality, increasing multifunctionality by 8.3% for every consumer added (Fig. 3 3d, Table 3 1, P = 0.0011). Multifunctionality measurements also exhibit ed the smallest amount of variance amongst all measures of ecosystem function (R 2 = 0.520). Post response variables, was significantly higher in intact communities (3 consumers) than in all other treatments (0, 1, or 2 consumers) (P = 0.001). We also assessed the ability for treatments to achieve a multifunctionality threshold which we defined as a value that is (36) Consumer diversity had a significant, positive effect on the number of functions maintained above the

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19 multifunctionality threshold ( P < 0.0001, R 2 = 0.2370, Fig. 3 4). An increase in one consumer yielded, on average, an increase in 0.4 0.09 functions maintained over the 50% threshold (t = 4 .39, P < 0.0001). In fact, only intact treatments were able to maintain all functions over the threshold and the probability of a given plot maintaining the threshold decreased as species loss and number of functions considered increased (Fig. 3 5, P < 0. 0001).

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20 Table 3 1 Coefficient table from regression of consumer diversity and ecosystem functions. m SE t p R 2 D max Decomposition (g/mth) 0.87 0.19 4.67 <0.0001 0.260 0.292 NPP (g/m 2 ) 23.96 19.95 1.20 0.2344 0.023 0.402 Infiltration (L/hr) 1.15 0.59 1.95 0.0604 0.113 0.008 Multifunctionality (%) 0.08 0.02 4.11 0.0003 0.520 0.464 Significant p and R 2 values (at an alpha level of 0.05) are bolded. D max > 0 indicates that overyielding contributes to the effect of diversity on functioning. Figure 3 1. Ergosterol recovered. Mean ergosterol (ug/g) recovered from representative 5 cm Spartina leaves in plots that were sprayed with fungicide and plots that were sprayed with water every 5 days (n = 12). Confi dence intervals represent s.e.m.

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21 Figure 3 2 Effect of each consumer removal ( ) and consumer presence (+) on a ) decomposition rate b ) net primary production c ) infiltration, and d ) average multifunctionality. Means and s.e.m. confidence interva ls are from pair wise comparison of main effects of consumer removals from 3 way ANOVAs (crab x snail x fungicide) and represents significant ( P < 0.0001) differences from post hoc Tukey tests between removal ( ) and present (+) for each consumer. a b c d

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22 Figure 3 3. Effect of species richness on single functions and multifunctionality. Increasing number of consumers (i.e. species richness) had variable effects on regressions of single ecosystem functions a ) decompositi on, b ) net primary production, and c ) infiltration, and had a positive effect on average multifunctionality d ) Fits of regression models only shown where significant ( P a b c d R 2 = 0.2 60 R 2 = 0.0 23

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23 Figure 3 4 Multifunctionality threshold. The number of functions maintained over 50% threshold increases as consumer diversity increases. Values and s.e.m. confidence intervals are the mean number of functions maintained over 50% threshold per level of diversity. 0 1 2 3 0 1 2 3 Functions maintained over 50% threshold number of consumers

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24 Figure 3 5 Probability of maintaining multifunctionality thresholds. Probability of maintaining a 50% threshold for a given plot decreases within each level of diversity. The number of functions (f) maintained at the 50% threshold is the mean of all possible combinations for e ach level of functioning (f = 1, f = 2, or f = 3). Only intact communities (0 consumers removed) were able to maintain 3 functions at 50% of the maximum functioning. Note change in x axis values to represent consumer removal method.

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25 CHAPTER 4 DISCUSSION Consumer Diversity and Ecosystem Multifunctionality This is the first experimental study to directly assess consumer diversity effects on multifunctionality and its results validate qualitative analyses suggesting that maximizing consumer divers ity will increase overall ecosystem functioning ( 17 ) Specifically, average multifunctionality increased as consumer richness increased (Fig. 3 3d), and con sumer diversity had a strong, positive effect on the number of functions maintained above multifunctionality thresholds (Fig. 3 4). Within this salt marsh consumer assemblage our results revealed that functional diversity is high (i.e. each consumer increa ses a different ecosystem function) while functional redundancy is low (i.e. each function is controlled by no more than two consumers) (Fig. 3 2 a c), a finding sensu ( 10 ) underlies the observed strong effect of species richness on multifunctionality despite weak effects of richness on single functions. Thus, as suggested from other studies ( 10 12 ) more species are needed to enhance multifunctionality because different species affect different functions and, in salt marshes, the high functional turnover (i.e. complementarity) of consumers likely compensated for the relatively low species div ersity present in this system. In contrast to previous plant multifunctionality studies ( 10 12 ) the diversity in our study was considerably lower (3 species vs. at least 6 species) but represented the en tire suite of dominant marine consumers in this natural system. Despite this relatively low diversity, we found that a few, abundant species can maintain high levels ecosystem multifunctionality and the loss of a small number of species has large, negative effects on functioning (Fig. 3 5), a result which is consistent with

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26 multifunctionality experiments conducted in high plant diversity systems. Specifically, this consumer diversity study and previous plant multifunctionality studies ( 11 12 ) indicate that losing about a third of species resu lts in ~20% loss in ecosystem multifunctionality (Fig. 3 3d). Incorporating multiple, instead of only single function impact assessments into ecosystem processes. Specifical ly our findings highlight that if multifunctionality responses are not measured in biodiversity and ecosystem function (BEF) studies, the effect of diversity on ecosystem function can be underestimated or missed entirely. When measuring effects on single e cosystem functions, we found that salt marsh consumer diversity significantly enhanced only one of the measured functions (i.e. decomposition, Table 3 1, Fig. 3 3 a c). Interpreting these single function responses alone, as is the norm for past studies, wo uld have led us to the conclusion that diversity, in general, was not important in overall marsh functioning. However, when we assessed ecosystem function through integrated measurement of simultaneously occurring functions, we found that the ability for a consumer assemblage to maintain multifunctionality was positively correlated with species diversity (Fig. 3 3d, Fig. 3 4). Additionally, only fully intact consumer assemblages consistently maintained all functions above the threshold (Fig. 3 5). Thus, by assessing effects on integrated measurements of processing, we were able to accurately detect and predict the overall effect of species extinctions on ecosystem functioning. Human society places value on a great number of services (e.g. fisheries prod uction, runoff filtration, coastal protection) generated by ecosystems ( 9 ) Our results

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27 highlight that using both multiple and diverse assessments of ecosystem functionality will likely generate a more accurate p rediction of how biodiversity losses will impact provisioning of these services. For example, in contrast to previous multifunctionality studies which measured numerous but highly related ecosystem functions ( 10 13 32 ) [e.g. Maestre et al ( 13 ) considered 14 functions contributing to nutrient cycling in terrestrial dryland plants], we used a broader test of ecosystem multifunctionality in our study by measuring functions that are linked to contrasting ecosystem services such as marsh hydrology and storm protection (37 ) biogeochemistry and nutrient cycling (34) and carbon sequestration (37) Because each function measured was linked to a different ecosystem service instead of all functions being linked to just one, our use of multifunctionality likely provided a more robust test of diversity effects on service provisioning at the whole ecosy stem scale. That is, if we had measured 3 functions all related to primary production (e.g. plant biomass accumulation, plant carbon content, and photosynthesis rates) we would not have detected a diversity loss either single or multifunctionality. We the refore not only concur with recent studies ( 10 13 ) calling for future BEF studies to incorporate multifunctionality as a response variable, but also suggest that those measured functions be div erse and linked to as many different services as possible. Consumer Regulation of Coastal Wetland Ecosystem Function Our results have important implications for understanding process regulation and structure in economically important coastal wetlands. In salt marshes, the link between consumers and ecosystem functioning has been well established through an emphasis on grazer control of marsh plant production (16, 30, 38 40) By incorporating other important marsh functions (i.e. decomposition, infiltration) and multifunctionality, this

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28 study greatly expands on our understanding of the role played by marsh consumers in controlling other key processes. Here, we find that not o nly do individual consumers drive single marsh functions that are diverse (from hydrology to decomposition), but that their combined presence results in maximized rates of marsh multifunctionality. Because predators exert strong control on potent marsh her bivores through trophic cascades ( 16 ) and predator diversity has been shown to be key in regulating marsh grazer impacts (41 ) we predict that diversity across all trophic levels is essential in maintaining salt marsh multifunctionality. More generally, these results call for a greatly expanded line of research in coastal wetland ecology, long dominated by a bottom control only perspective on community and ecosystem processes (42) that investigates linkages between community structure (e.g. biodiversity at all trophic levels) and ecosystem level processes (e.g. shoreline stabilization carbon sequestration, infiltration, nutrient cycling, and nursery production) that go beyond marsh primary production alone. Incorporating Microbes into Consumer Diversity Ecosystem Function Studies Our work also reveals that incorporating microbes into consumer diversity studies is key to further understanding the mechanistic relationship between biodiversity and ecosystem multifunctionality. In this study, microbial consumers contributed to the positive relationship between multifunctionality and consu mer diversity and, without their inclusion, the impact of diversity would be underestimated, as fungal removal affected two ecosystem functions and multifunctionality (Fig. 3 2 a,b, and d). The positive effect of fungi on marsh net primary production, as o pposed to a negative effect seen in other studies (30) likely came about for two reasons: fungi reduced dead plants and leaf litter in experimental plots which can shade marsh plants and suppress their growth (43) and

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29 snails that facilitate their negative effect on plants did not themselves have a significant effect on marsh plant growth (Fig. 3 2b), likely because their negative impacts primarily emerge under intense drought stress or increased densities during predator release ( 16 ) In addition to positively affecting plant growth, fungi also enhanced decomposition (Fig. 3 2a) and multifunctionality (Fig. 3 2d). Although microbes are known to impact key ecosystem processes (44 46) and the probability of sustaining multiple ecosystem functions has been shown to increase with microbial species richness ( 32 ) this is the first experimental inclusion of microbial consumers with animal consumers into a BEF study. In this study, the microbial consumer had a positive effect on ecosystem functioning, but the inclusion of other types of microbes in other systems such as pathogens or parasites could also influence multifunctionality in different ways. Because they control diverse and multiple functions microbial consumers must be included within the greater, ma cro consumer assemblage to gain an accurate understanding of BEF relationship and impacts of trophic feedbacks on multifunctionality.

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30 LIST OF REFER E NECES 1. Balvanera P et al. (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 9:1146 56. 2. Cardinale BJ et al. (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989 92. 3. Cardinale BJ et al. (2012) Biodiversity loss and its impact on humanity. Nature 486:59 67. 4. Hooper D, Iii FC, Ewel J (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol ogical Monographs 75:3 35. 5. Isbell F et al. (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199 202. 6. Stachowicz JJ, Bruno JF, Duffy JE (2007) Understanding the Effects of Marine Biodiversity on Communities and Ecosystems. Annual Review of Ecology, Evolution, and Systematics 38:739 766. 7. Tilman D, Reich P, Isbell F (2012) Biodiversity impacts ecosystem productivity as much as resources, disturbance, or herbivory. Proceeding s of the National Academy of Sciences 109:10394 10397. 8. Loreau M et al. (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Sci ence 294:804 808. 9. MEA [Millennium Ecosystem Assessment] (2005) Ecosystems and human well being: current state and trends. Coastal systems (Island Press, Was hington, DC, USA) 10. Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188 90. 11. Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD (2010) Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Proceedings of the National Academy of Sciences of the U nited States of America 107:1443 6. 12. Gamfeldt L, Hillebrand H, Jonsson P (2008) Multiple functions increase t he importance of biodiversity for overall ecosystem functioning. Ecology 89:1223 1231. 13. Maestre FT et al. (2012) Plant species richness and ecosystem multif unctionality in global drylands. Science 335:214 8.

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34 BIOGRAPHICAL SKETCH Marc Hensel was born and raised in Temple Terrace, Florida where he attended King High School International Baccalaureate Program. Here, through the direction of biology teacher Mr. William Ward, he became interested in the biological sciences. He earned a 3.89 GPA in high school and decided to attend the Univeristy of Florida in 2006. He gradua ted cum laude with my Bachelor of Science in z oology from the University of Florida in 2010. For my senio r thesis he conducted a field experiment funded through the University Scholars Program investigating the role of consumers on salt marsh productivity. This research sparked his interest in marine ecolo gy and was the catalyst for his m UF. Marc will be attending the University of Massachusetts Boston to earn his doctorate.