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! ! ! ! ! ! ! ! BIOTIC INTERACTIONS ALTER TOP-DOWN PRESSURE ON A LEAF-SHREDDING CADDISFLY, PHYLLOICUS HANSONI (TRICHOPTERA: CALAMOCERATIDAE), IN TRINIDADIAN STREAMS by KELLY MACKENZIE MURRAY A Thesis Submitted to the Honors Program of the University of Georgia in Fulfillment of the Requirements for ENTO 4990H ©2014 Kelly Murray All Rights Reserved ! ! KELLY MACKENZIE MURRAY Biotic interactions alter top-down pressure on a leaf-shredding caddisfly, Phylloicus hansoni (Trichoptera: Calamoceratidae), in Trinidadian streams (Under the direction of CATHERINE PRINGLE, Thesis Director, and TROY SIMON, Thesis Reader) ABSTRACT The influence of predators can play a prominent role in shaping characteristics of prey populations, but it is also important to study species interactions within the context of an ecological community. Headwater streams in Trinidad’s Northern Range Mountains are often characterized by high densities of killifish (Anablepsoides hartii) upstream of barrier waterfalls, with downstream reaches containing killifish at lower densities as well as guppies (Poecilia reticulata); when sympatric, intraguild predation between these two species results in changes in killifish populations and life history. Killifish are predators of the leaf-shredding caddisfly Phylloicus hansoni (Trichoptera: Calamoceratidae), and previous research has suggested that there is increased predation pressure where guppies are absent. Larval P. hansoni play a key role in controlling rates of leaf decomposition in Trinidadian streams; therefore, predator-mediated effects on this tropical caddisfly are important to understand. In this study, we examined the effects of fish assemblage on the size structure of larval P. hansoni populations in streams (n=5) with distinct killifish-only (KO) and killifish-guppy (KG) reaches. Analysis of size distributions of P. hansoni from KO and KG reaches confirmed our prediction that killifish alter the size structure of larvae differently depending on the presence or absence of guppies: larvae from KO reaches exhibited a size frequency peak at a smaller size than in KG reaches. These results indicate that the influence of a predatory fish on an important macroinvertebrate species differs at small spatial scales with changes in the community assemblage. 2 ! ! INTRODUCTION Predators can affect prey populations in many different ways beyond exerting topdown control of the numerical abundance (Peckarsky et al. 2008). Predators can induce population cycling in prey species (Krebs et al. 2001) and subsequent adaptation (Abrams and Matsuda 1997, Yoshida et al. 2003) in prey species, influence trophic cascades (Carpenter and Kitchell 1988), and alter the size structure of prey populations (Brooks and Dodson 1965). Theory predicts that populations of organisms experiencing predation pressure will be driven to reproduce at an earlier age and reduced size (Abrams and Rowe 1996), and empirical studies have shown that predators can prompt a reduction in size at emergence of aquatic insect prey (Peckarsky et al. 2001) as well as reductions in fecundity in both aquatic (Greig and McIntosh 2008) and terrestrial systems (Dixon and Agarwala 1999). Often, to elucidate the specifics of such impacts on prey populations, studies must focus comparing prey populations with the presence or absence of a predator, but other biotic interactions occurring within the community are important to consider; intraguild predation, for example, is one source of complexity (Davenport and Chalcraft 2012, Anderson and Semlitsch 2014). Here we examine how the effects of a predator can shift in the context of an ecological community by evaluating how the topdown pressure of a predatory fish on a functionally important leaf-shredding caddisfly is mediated by differences in the total stream fish assemblage. Our research focuses on larval populations of the caddisfly Phylloicus hansoni (Trichoptera: Calamoceratidae) in Trinidadian headwater streams. P. hansoni (syn. P. angustior) is native to the island of Trinidad, as well as Venezuela, and the genus is found throughout Central and South America (Flint 1996, Prather 2003). The aquatic 3 ! ! larvae are leaf-shredders, which is a role often essential to the distribution of fine particulate organic matter resources to filter-feeding invertebrates (Cummins et al. 1989, Wallace and Webster 1996), which can control secondary production throughout the stream community (Wallace et al. 1997). Using allochthonous leaf inputs for both feeding purposes and the construction of protective cases, Phylloicus spp. break down leaves containing a broad range of nutrient, polyphenol, and lignin contents (Rincón and Martínez 2006). Phylloicus spp. are consistently reported as key decomposers of organic matter in tropical headwater streams when present (Table 1), making this genus a notable exception to the general scarcity of insect shredders in the tropics compared to temperate zones (Wantzen and Wagner 2006, Boyero et al. 2011); P. hansoni is thought to be the only macroinvertebrate shredder on the island of Trinidad (Botosaneanu and Sakal 1992). Its important role in the facilitation of leaf breakdown motivated the study of larval P. hansoni populations experiencing varying levels of predation from the killifish Anablepsoides hartii (syn. Rivulus hartii) in Trinidadian streams. Headwater streams located in Trinidad’s Northern Range Mountains provide an ideal system for studying the interaction of both ecological and evolutionary processes (Reznick and Endler 1982, Palkovacs et al. 2009, Bassar et al. 2010). Large barrier waterfalls segregate fish communities between stream reaches by preventing certain species from migrating upstream. As elevation increases, there are fewer fish species present (Gilliam et al. 1993). Often, the killifish A. hartii is the only fish present in the highest-elevation stream reaches (killifish-only, or “KO” reaches). Immediately downstream from these KO reaches, guppies (Poecilia reticulata) and killifish are sympatric (in killifish-guppy, or “KG” reaches) – see Figure 1. In the KG reaches of our 4 ! ! focal streams, guppies are thought to primarily consume algae, detritus, and small invertebrates (Zandonà et al. 2011). Guppy prey can also include killifish juveniles, and killifish growth rates are altered when coexisting with guppies (Walsh et al. 2011, Fraser and Lamphere 2013). Killifish are primarily insectivorous (Gilliam et al. 1993, Fraser et al. 1993), and are more abundant in streams where they are the sole fish species (Gilliam et al. 1993, Walsh and Reznick 2008, 2009, 2010, 2011). Killifish also occasionally consume guppies in KG reaches (K. Murray, personal observation from gut content analysis). Here, we investigate how intraguild predation between of these two fish species can influence the effects of killifish on populations of P. hansoni, which occur in both reaches of these streams. Previous experiments examined how the presence of guppies alters trophic cascades within this system (Binderup 2011) using exclusion experiments (as in Pringle and Blake 1994) to isolate the effects of macroconsumers on leaf decomposition. Binderup (2011) reported that the presence of guppies released P. hansoni larvae from the top-down control of killifish, which indirectly altered leaf decomposition: within a KO reach, killifish predation reduces P. hansoni abundance to a greater degree, thereby reducing leaf decay rates. Alternatively, within a KG reach, killifish did not reduce P. hansoni abundance and leaf decay rates were not affected by top consumers. This strongly suggests that leaf-shredding P. hansoni larvae experience reduced predation pressure in the presence of guppies, and this decoupling of a trophic cascade could change resource dynamics within the stream ecosystem (Binderup 2011). Our study investigates whether the presence of guppies produces a consistent influence on killifish’s effects on P. hansoni populations by using multiple streams with similarly partitioned 5 ! ! fish communities. We also focus on characteristics of killifish impacts in the context of guppy presence beyond reductions in abundance of P. hansoni larvae by evaluating differences in larval size structure. Growth of aquatic macroinvertebrates is an important process to understand within the framework of a stream ecosystem. Holometabolous aquatic insects, such as caddisflies, undergo complex life cycles and must achieve a balance between growth and predator avoidance under time constraints (Rowe and Ludwig 1991). Once adult insects emerge from their aquatic environment, they can become important subsidies of prey and nutrients to terrestrial ecosystems (Nakano and Murakami 2001, Hoekman et al. 2012). Secondary production of aquatic macroinvertebrates is tied to growth rates and other life history characteristics (Huryn and Wallace 2000), but predators can mediate these values (Huryn 1998). Studying the size structures of P. hansoni experiencing the effects of different fish assemblages may provide insight into how the biomass of aquatic insect populations can be mediated by other biotic interactions within the community. We used the unique microgeographic variation found in stream systems of Trinidad’s Northern Range Mountains as a natural “experiment” to investigate whether the ecological context (in this case, the presence or absence of guppies) in which a predator is found can alter characteristics of its prey population across small spatial scales (above and below waterfalls). We examined whether larval populations of P. hansoni exhibit different size structures between areas where killifish and its intraguild predator, guppies, are sympatric (reduced predation pressure on larvae) and where killifish are found alone above barrier waterfalls (higher predation pressure on larvae). We predicted that there would be a greater proportion of large individuals where P. hansoni individuals 6 ! ! coexist with killifish and guppies, compared to the frequency of large individuals in killifish-only reaches. We also investigated a potential mechanism for any such change, size-selective predation by killifish on P. hansoni larvae, by performing a gut content analysis of killifish. We predicted that killifish would selectively consume the largest P. hansoni individuals. DESCRIPTION OF STUDY SITES This study was conducted in streams on the southern slope of Trinidad’s Northern Range Mountains, within the Caroni drainage. The Caroni drainage is located on the northwestern side of the island and encompasses a total of ≈ 60,000ha. We conducted our sampling efforts in mid-May 2013, a time corresponding to the end of the dry season in Trinidad. The montane, spring-fed streams we studied (n=5: El Cedro “CED,” Endler “END,” Guard Dog Creek “GDC,” Ramdeen “RDN,” and Trip Trace “TRT”) were composed of reaches with distinct fish assemblages due to the presence of large barrier waterfalls, which prevent guppies, but not killifish, from migrating upstream. We sampled streams above waterfalls where killifish were found alone (“KO” reaches), and directly below waterfalls, where killifish and guppies were sympatric (“KG” reaches). METHODS In order to better understand the consequences of killifish predation on P. hansoni population dynamics, we evaluated the size structure of larval populations in relation to fish assemblage by using five streams with distinct paired KO and KG reaches. To determine whether physical and environmental differences between these upstream and downstream areas could also influence P. hansoni habitats, we compared the stream 7 ! ! morphology and habitat quality between paired reaches. Stream Characteristics We measured four types of environmental characteristics along transects in each reach: wetted width (cm), depth (cm), canopy cover (%), and leaf standing stocks (coarse benthic organic matter, or CBOM, g cm-2). Three transects perpendicular to the stream were chosen at random points along each 100m reach where sampling was conducted. Average depth along transects was calculated from five readings at uniform distance along the wetted width of the stream. We used a spherical densiometer to estimate percent canopy cover over the stream by taking measurements at each edge and in the middle of the stream. We collected leaf standing stocks from the stream benthos within 28cm of each transect line between the wetted width, then washed, dried for 36 hours, and weighed the leaves. We estimated killifish abundance in the study reaches to ensure that our streams were consistent with previous findings that killifish are generally more abundant in reaches where they are the only fish species present (Gilliam et al. 1993, Walsh and Reznick 2008, 2009, 2010, 2011, Fraser and Lamphere 2013), thus potentially exerting greater predation pressure on P. hansoni. We used baited minnow traps and measured the catch per unit effort (CPUE). Three traps were placed in deep pools evenly spaced across our 100m sampling reach. All killifish captured within 10 minutes of placing the trap were counted and released. Each killifish was measured and categorized into one of the following size classes based on body length: Juvenile (<15mm), Small (15-30mm), Medium (30-45mm), Large (45-60mm), and Extra Large (>60mm). 8 ! ! To test whether the environmental parameters were consistently different between KO and KG reaches, we calculated the mean and standard error of depth, wetted width, percent canopy cover, and leaf standing stocks of the three transects per reach, and the number of killifish caught per trap. We compared these measurements between KO and KG reaches across all five streams with a paired t-test. For this and all other analyses, significance was determined at p≤0.05. Phylloicus hansoni Size Structure For our evaluation of differences in larval size structures between the two different types of fish community, we collected P. hansoni larvae in the KO and KG reaches of the five focal streams. In each stream reach, we collected P. hansoni larvae in pools with ample leaf litter availability with a standardized sampling effort: searching ~7 minutes per pool, or until at least 50 individuals were found. P. hansoni individuals were preserved in 5% formalin, and larval measurements were taken under a dissecting microscope to the nearest 0.1mm in the laboratory. Insect measurements included body length, head capsule width, and leaf case length and width at three points evenly spaced along the length of the case. Body length was measured from the top of the head capsule to the caudal end. The average of the three case width measurements and case length were multiplied to estimate leaf case surface area (mm2), to be compared with larva size. We measured the case surface area so as to compare whether P. hansoni build larger leaf cases when under greater predation threat. The distributions of larval body size violated the assumptions of parametric 9 ! ! statistical tests, even when standard data transformations were used. Therefore, we used non-parametric statistics for hypothesis testing. We used a two-sample KolmogorovSmirnov (K-S) test to evaluate differences in the distribution of P. hansoni larvae body length between KO and KG reaches. We also used the Wilcox rank sum test to compare the mean body length and head capsule width of larvae from KO and KG reaches. Killifish Gut Content Analysis To determine whether killifish preferentially consume larvae of a specific size class, and whether this differs between killifish from different stream reaches, we analyzed the size of P. hansoni found in killifish gut contents. Killifish used for gut content analysis were collected from KO and KG reaches of 4 streams (3 of which were used in the larval size structure collections: Endler, Guard Dog Creek, and El Cedro) in late April 2011, as part of a separate study. All killifish used in this study were female. Fish were dissected and the digestive tract was preserved in 10% formalin. Gut contents were then extracted from the stomach and searched to identify P. hansoni larvae. Typically only the head capsule remained intact, so this was measured to compare the average size of larvae consumed. We also calculated the percentage of killifish with P. hansoni larvae in their guts from both reaches, an “occurrence method,” as described by Hyslop (1980). RESULTS Environmental variables evaluated by our stream transects did not show any marked differences between upstream KO reaches and downstream KG reaches. Mean values of wetted width, depth, percent canopy cover, and leaf standing stocks did not 10 ! ! significantly differ between KO and KG reaches overall (p = 0.2, 0.4, 0.5, and 0.2 respectively, Table 2). However, in accordance with our predictions, killifish CPUE was higher in KO reaches than KG reaches (p=0.014, Table 2). Our estimates of killifish body length showed that size distributions are similar, though KO reaches had greater proportions of the largest (>60mm) individuals (Figure 2). KO and KG reaches exhibited different patterns in the size of P. hansoni larvae. Plots of head capsule size and body length for larvae (Figure 3) enabled us to classify a range of body sizes into classes roughly corresponding to instar. Generally, the largest size classes were most abundant in the KG samples, except in the case of GDC larvae, which showed a size frequency peak shifted towards a smaller size (Figure 4). The mean body size of all larvae was higher in KG reaches (7.8 ± 0.13mm [mean ± SE]) than in KO reaches (6.81 ± 0.19mm), p=0.032, and the mean head capsule width of KG larvae (0.78 ± 0.015mm) was also higher than KO larvae (0.69 ± 0.088mm), p=0.003 (Figure 5). Comparing reaches within individual streams with our Wilcox rank sum tests, TRT, RDN, CED had significantly higher larval body lengths (p=0.036, <0.001, 0.008 respectively) and head capsule widths (p=0.02, <0.001, 0.01 respectively) in KG reaches. END KO and KG body lengths (p=0.93) and head capsule widths (p=0.69) were not significantly different. In GDC, KO larvae had larger body lengths (p<0.001) and head capsule widths (p=0.002). The length and surface area of the leaf case increased with increasing larva size, and there were no differences in these relationships between KO and KG reaches (Table 3). With the two-sample K-S test of larval body length, we concluded that the overall KO and KG size distributions are different (p=0.046). The majority of KO larvae body 11 ! ! sizes are localized around a smaller size, ~4-6mm, while KG larvae exhibit a peak near 8mm (Figure 6). Because this analysis did not control for the larvae’s stream of origin, we conducted a two-sample K-S test for each of the four streams separately. The KO and KG larval size distributions of CED, TRT, GDC, and RDN were different (p=0.008, 0.036, <0.001, <0.001 respectively), yet those of END were not (p=0.93). From the gut content analysis of killifish collected in 2011, the means of head capsule widths of larvae consumed by killifish in both KO (0.095 ± 0.0109mm) and KG (0.144 ± 0.0235mm) reaches were smaller than 0.2mm (Table 4). Killifish from KG reaches had a higher percentage of P. hansoni head capsules in their guts than killifish from KO reaches, and in KO reaches, the killifish with P. hansoni in their gut had a mean body length (42.57 ± 3.29mm) smaller than the mean size of all KO killifish (47.83 ± 1.48mm) analyzed (Table 4). DISCUSSION Our results show that size distributions of P. hansoni larvae in killifish-only reaches are different than in killifish-guppy reaches within the same stream, with a shift toward larger individuals in the KG reach compared to the KO. Based on a reduction in both the mean body size and head capsule width in KO larvae, and because head capsule width is an indicator of age, we can infer that the individuals in KO reaches are, on average, smaller and younger than their KG counterparts. This supports our prediction that large individuals would be more frequent in reaches where killifish and guppies coexist, and less frequent where killifish are the only fish species present. These data provide only a snapshot of P. hansoni populations, but differences are consistent in three out of five streams surveyed. 12 ! ! The disparity in top-down pressure exerted by killifish on P. hansoni between KO and KG reaches, evidenced by the differences in larval size structures, are likely the result of several factors stemming from guppy-killifish interactions in KG reaches. Previous studies of these stream systems (Walsh and Reznick 2008, 2009, 2010, 2011, Walsh et al. 2011), in addition to our CPUE abundance estimates, suggest that killifish densities are lower in reaches where they coexist with guppies. Rates of killifish growth increase in the presence of guppies, likely as a response to guppy predation on killifish juveniles (Walsh et al. 2011, Fraser and Lamphere 2013). In accordance with these findings, our surveys found greater incidences of the largest (>60mm) killifish in KO reaches (Figure 2). Additionally, there may be differences in the foraging behavior of killifish when coexisting with guppies; it has been shown in other systems that habitat partitioning within the fish community can result from interference competition between two species (Nakano and Furukawa-Tanaka 1994, Katano and Aonuma 2001). We have shown using multiple streams that these shifts in killifish population dynamics due to the presence of guppies provide enough change to influence the shape of the size structure of P. hansoni larvae. The reduced frequency of larger individuals of P. hansoni in KO reaches is ecologically significant in the context of the life cycle of this tropical caddisfly, providing evidence of increased predation pressure altering development. The exact characteristics of the P. hansoni life cycles in Trinidad have not been documented, but we can make predictions based on those of other organisms. Studies of larval development of Trichopterans in Costa Rica that included three Phylloicus species (P. elegans, P. ornatus, and P. undescribed sp. nr. ornatus) provided evidence for multivoltinism 13 ! ! (having multiple generations within one year) in this group (Jackson and Sweeney 1995). While emergence of P. hansoni adults may occur throughout the year, it may exhibit a peak in a particular season; this would be similar to patterns demonstrated by studies of adult caddisfly abundance in Panama (McElravy et al. 1982), which included sampling of Phylloicus spp. adults, and surveys of another leaf-shredding Calamoceratid, Anisocentropus kirramus, in tropical Australia (Nolen and Pearson 1992). Both studies found increases in the number of adults in the summer rainy season. Additionally, a survey of Phylloicus sp. larvae in Brazilian streams documented an increase in the largest individuals in the spring, and predicted that adult emergence would most likely start after the beginning of the wet season (Huamantinco and Nessimian 2000). If populations of P. hansoni in Trinidad also follow this seasonal pattern, we would expect that our samples taken in May (corresponding to the end of the dry season in Trinidad) would contain the largest larvae in greatest proportions; however, this is only the case with samples from KG sections of streams, not in the KO reaches. The differential effects of killifish predation in KO and KG reaches as given by our size structure data may be influencing the timing of emergence, the size of adults, or both. Life histories of stream insects are marked by trade-offs. Caddisflies such as P. hansoni typically possess an ephemeral adult stage, so it is beneficial for these organisms to synchronize emergence with an environmental cue, like increasing discharge (which may explain the pattern of increased adult emergence in rainy seasons). It is also advantageous for larvae to achieve a maximum size before emerging, because adult size after metamorphosis is governed by larval growth, and is directly correlated to fecundity and reproduction; however, the threat of predation may drive caddisflies to escape the 14 ! ! stream earlier than is ideal (Rowe and Ludwig 1991). More research is necessary to how the effects of predation on the P. hansoni life cycle are potentially manifested, but we have shown that another organism in the fish community can mediate these influences of a predator. Even though emergence may be more common in one season, growth and development of aquatic larvae can be controlled by a variety of physical factors (Sweeney 1984). We found no consistent differences in the physical habitat between upstream and downstream reaches based on the environmental features measured, which included an estimation of food and habitat resources for P. hansoni larvae by leaf standing stock mass. Temperature is an important element controlling rates of larval insect development (Sweeney 1984), but differences are likely minimal over the small spatial scale separating KO and KG reaches of these spring-fed headwater streams with similar canopy cover. Therefore, it is more likely that overall differences observed between KO and KG P. hansoni populations are primarily driven by the differences in fish community. However, patterns were not consistent or significant throughout every stream we surveyed. The shape of the larval size distributions from both the KO and KG reaches of Guard Dog Creek (GDC) were shifted towards smaller sizes (Figure 4) and had smaller mean larval body length and head capsule widths (Table 3) compared to other streams, and differences between reaches in Endler (END) were not significant. Certain environmental and geomorphological factors could influence whether a particular stream reach is suitable for larvae growth and survivorship. Studies of mayfly oviposition and recruitment have found that the availability of suitable rock substrate corresponds to 15 ! ! female ovipoisition (Encalada and Peckarsky 2006), and these streams providing ideal hydrogeomorphic habitats host greater egg densities even though they also have trout predators (Encalada and Peckarsky 2011). One factor such as this that may have influenced our results is the stream depth. The KO and KG reaches in GDC were on average ~1.8x deeper than the means for both reaches from all five streams (Table 2), which indicates that the quality of physical habitat for P. hansoni larvae may not be as suitable in the sampled portions of this particular stream; Phylloicus spp. larvae are usually found in pools along the stream margin (Wantzen and Wagner 2006, Turner et al. 2008). So certain abiotic characteristics may overwhelm the effects of fish community, but with consistent differences in the size structure P. hansoni larval populations between KO and KG reaches in three streams, the influence of fish assemblage is nevertheless an important factor. There could be several explanations for a reduced prey size due to increased predation pressure, as found in the KO reaches. Our gut content analysis showed that the prevalence of smaller P. hansoni larvae in such reaches is probably not solely due to positive size-selection from killifish, contrary to our prediction. Killifish are not expected to be gape-limited (Binderup 2011), and large, late-instar P. hansoni individuals were witnessed inside killifish guts (K. Murray, personal observation), but killifish may avoid larger instars due to their unpalatable leaf case, which increases with body size. However, the difference of two years in the gut content sampling (2011) and the P. hansoni collections (2013), even in similar seasons, might not reflect an alignment in the availability of large larvae as prey in these streams. Other factors to consider include the potential suppression of prey activity levels 16 ! ! in order to avoid predators, or “adaptive foraging behavior,” a common occurrence (Schmitz et al. 2008) that prompts a trade-off with growth (Werner and Anholt 1993). Reductions in prey activity as a response to predator presence have been observed in other aquatic, detrital-based systems (Boyero et al. 2008), but this is not always the case (Greig and McIntosh 2006). Even when foraging is unchanged, prey populations may exhibit altered growth due to reductions in nutrient assimilation when under the stress of predation threat (Stoks et al. 2005). Predators can also impose selection on prey life history evolution (Rowe and Ludwig 1991) or phenotypically plastic responses, which may include emergence at smaller sizes (Peckarsky et al. 2001) and reductions in fecundity (Greig and McIntosh 2008) in the case of aquatic insects. We do not know the extent of genetic mixing between P. hansoni from KO and KG reaches due to dispersal in the winged adult stage, and source-sink dynamics within the metacommunity are important to consider (Leibold et al. 2004). The presence of predators has been shown to elicit plastic responses in a variety of aquatic systems where prey experience variable predation pressure (Van Buskirk and Schmidt 2000, Peckarsky et al 2002, Torres-Dowdall et al. 2012), and the differential predation pressure on P. hansoni larvae between nearby KO and KG reaches may provide selection for such plasticity. Further investigations are needed to provide insight into the mechanisms driving the altered size structures of P. hansoni populations observed in our study between KO and KG reaches. Recently, there has been emphasis on the need to evaluate differences in ecological communities that may be causing adaptation at the “microgeographic” scale (Richardson et al. 2014). Our study suggests that a shift in biotic interactions occurring 17 ! ! along a small spatial scale (within-stream distance <500m) can have consequences throughout the community, in this case affecting a functionally important macroinvertebrate species. Closer examinations of community-level differences within an ecosystem may elucidate more complexity in ecological and evolutionary interactions than previously estimated. 18 ! ! ACKNOWLEDGEMENTS This project received support from the following programs at the University of Georgia: the 2013 Honors International Scholars Program, the Center for Undergraduate Research Opportunities 2013 Summer Fellowship, and the College of Agricultural and Environmental Sciences 2013 Undergraduate Research Initiative. I would not have been able to conduct this research or complete this thesis without the continuous support, guidance, and dedication of Troy Simon, PhD Candidate in the Odum School of Ecology, and Dr. Catherine Pringle, Distinguished Research Professor in the Odum School of Ecology. I am also very grateful to Dr. Marianne Shockley of the UGA Department of Entomology for her support in applying for the CAES Undergraduate Research Initiative grant and in the application of this thesis to fulfill the requirements of ENTO 4990H. Thank you to David Stoker and John Kronenberger for their assistance with 2013 data collection in Trinidad, as well as Travis McDevitt-Galles, William Roberts, Michael Rautenberg, Anika Bratt, Tierney Schipper, Emily Nash, and Joshua Soden for the 2011 collections and initial processing of the killifish used in this study. Thank you to the graduate students in the Pringle lab group for their advice and helpful comments on this manuscript: Tom Barnum, Jessica Chappell, Maura Dudley, Carissa Ganong, Jeremy Sullivan, and Pedro Torres. And thank you to Dr. Darold Batzer, UGA Department of Entomology, for advice on appropriate methodologies prior my trip to Trinidad. Finally, thank you to my friends and family, who all provided invaluable support throughout my undergraduate research career. 19 ! ! REFERENCES Abrams, P.A. and H. Matsuda. 1997. “Prey adaptation as a cause of predator-prey cycles.” Evolution 51(6): 1742-1750. Abrams, P.A. and L. Rowe. 1996. “The effects of predation on the age and size of maturity of prey.” Evolution 50(3): 1052-1061. Anderson, T.L. and R.D. Semlitsch. 2014. “High intraguild predator density induces thinning effects on and increases temporal overlap within prey populations.” Population Ecology 56: 265-273. Bassar, R.D., M.C. Marshall, A. López-Sepulcre, E. Zandonà, et al. 2010. “Local adaptation in Trinidadian guppies alters ecosystem processes.” Proceedings of the National Academy of Sciences 107(8): 3616-3621. Benstead, J.P. 1996. “Macroinvertebrates and the processing of leaf litter in a tropical stream.” Biotropica 28(3): 367-375. Binderup, A.J. 2011. “Isolating top-down effects of aquatic macroconsumers on benthic structure and function in a Neotropical stream.” Masters Thesis, University of Georgia. Botosaneanu, L. and D. Sakal. 1992. “Ecological observations on the caddisflies (Insecta: Trichoptera) from Trinidad and Tobago (W. Indies).” Revue d’hydrobiologie tropicale 25(3): 197-207. Boyero, L., P.A. Rincon, and R.G. Pearson. 2008. “Effects of predatory fish on a tropical detritus-based food web.” Ecological Research 23: 649-655. Boyero, L., R.G. Pearson, D. Dudgeon, M.A.S. Graça, et al. 2011. “Global distribution of a key trophic guild contrasts with common latitudinal diversity patterns.” Ecology 20 ! ! 92(9): 1839-1848. Brooks, J.L. and S.I. Dodson. 1965. “Predation, body size, and composition of plankton.” Science 150: 28-35. Carpenter, S.R. and J.F. Kitchell. 1988. “Consumer control of lake productivity.” BioScience 38: 794-769. de Carvalho, E.M. and V.S. Uieda. 2009. “Diet of invertebrates sampled in leaf-bags in a tropical headwater stream.” Zoologia 26(4): 694-704. Cummins, K.W., M. A. Wilzbach, D.M. Gates, J.B. Perry, and W.B. Taliaferro. 1989. “Shredders and riparian vegetation.” BioScience 39(1): 24-30. Davenport, J.M. and D.R. Chalcraft. 2012. “Evaluating the effects of trophic complexity on a keystone predator by disassembling a partial intraguild predation food web.” Journal of Animal Ecology 81: 242-250. Dixon, A.F.G. and B.K. Agarwala. 1999. “Ladybird-induced life-history changes in aphids.” Proceedings of the Royal Society B-Biological Sciences 266(1428): 1549-1553. Encalada, A.C., J. Calles, V. Ferreira, C. Canhoto, and M.A.S. Graça. 2010. “Riparian land use and the relationship between benthos and litter decomposition in tropical montane streams.” Freshwater Biology 55: 1719-1733. Encalada, A.C., and B.L. Peckarsky. 2006. “Selective oviposition of the mayfly Baetis bicaudatus.” Oecologia 148(3): 526-537. Encalada, A.C., and B.L. Peckarsky. 2011. “The influence of recruitment on withingeneration population dynamics of a mayfly.” Ecosphere 2(10): 107. Flint, O.S. Jr. 1996. “Studies of Neotropical caddisflies LV: Trichoptera of Trinidad and 21 ! ! Tobago.” Transactions of the American Entomological Society (1890-) 122(2/3): 67-113. Fraser, D.F. and B.A. Lamphere. 2013. “Experimental evaluation of predation as a facilitator of invasion success in a stream fish.” Ecology 94(3): 640-649. Greig, H.S. and A.R. McIntosh. 2006. “Indirect effects of predatory trout on organic matter processing in detritus-based stream food webs.” Oikos 112: 31-40. Greig, H.S. and A.R. McIntosh. 2008. “Density reductions by predatory trout increase adult size and fecundity of surviving caddisfly larvae in a detritus-based stream food web.” Freshwater Biology 53(8): 1579-1591. Gilliam, J.F., D.F. Fraser, and M. Alkins-Koo. 1993. “Structure of a tropical stream fish community: a role for biotic interactions.” Ecology 74(6): 1856-1870. Hoekman, D., M. Bartrons, and C. Gratton. 2012. “Ecosystem linkages revealed by experimental lake-derived isotope signal in heathland food webs.” Oecologia 170: 735-743. Huamantinco, A.A. and J.L. Nessimian. 2000. “Variation and life strategies of the Trichoptera (Insecta) larvae community in a first order tributary of the Paquequer River, Southeastern Brazil.” Rev. Brasil. Biol. 60(1): 73-82. Huryn, A.D. 1998. “Ecosystem-level evidence for top-down and bottom-up control of production in a grassland stream system.” Oecologia 115: 173-183. Huryn, A.D. and J.B. Wallace. 2000. “Life history and production of stream insects.” Annual Review of Entomology 45: 83-110. Hyslop, E.J. 1980. “Stomach contents analysis—a review of methods and their application.” Journal of Fish Biology 17: 411-429. 22 ! ! Jackson, J.K. and B.W. Sweeney. 1995. “Egg and larval development times for 35 species of tropical stream insects in Costa Rica.” Journal of the North American Benthological Society 14(1): 115-130. Katano, O. and Y. Aonuma. 2001. “Negative effect of ayu on the growth of omnivorous pale chub in experimental pools.” Journal of Fish Biology 58(5): 1371-1382. Krebs, C., S. Boutin, R.Boonstra, and A. Sinclair. 2001. “What drives the 10-year cycle of snowshoe hares?” BioScience 51: 25-35. Landeiro, V.L., N. Hamada, B.S. Godoy, and A.S. Melo. 2010. “Effects of litter patch area on macroinvertebrate assemblage structure and leaf breakdown in Central Amazonian streams.” Hydrobiologia 649: 355-363. Nakano, S. and T. Furukawa-Tanka. 1994. “Intra- and interspecific dominance hierarchies and variation in foraging tactics of two species of stream-dwelling chars.” Ecological Research 9(1): 9-20. Nakano, S. and M. Murakami. 2001. “Reciprocal subsides: Dynamic interdependence between terrestrial and aquatic food webs.” Proceedings of the National Academy of Sciences of the United States of America 98(1): 166-170. Nolen, J.A. and R.G. Pearson. 1992. “Life history studies of Anisocentropus kirramus Neboiss (Trichoptera: Calamoceratidae) in a tropical Australian rainforest stream.” Aquatic Insects 14(4): 213-221. Palkovacs, E.P., M.C. Marshall, B.A. Lamphere, B.R. Lynch, D.J. Weese, D.F. Fraser, D.N. Reznick, C.M. Pringle, and M.T. Kinnison. 2009. “Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams.” Philosophical Transactions of the Royal Society B-Biological Sciences 23 ! ! 364: 1617-1628. Peckarsky, B.L., P.A. Abrams, D.I. Bolnick, L.M. Dill, J.H. Grabowski, B. Luttbeg, J.L. Orrock, S.D. Peacor, E.L. Preisser, O.J. Schmitz, and G.C. Trussell. 2008. “Revisiting the classics: Considering nonconsumptive effects in textbook examples of predator-prey interactions.” Ecology 89(9): 2416-2425. Peckarsky, B.L., A.R. McIntosh, B.W. Taylor, and J. Dahl. 2002. “Predator chemicals induce changes in mayfly life history traits: A whole-stream manipulation.” Ecology 83(3): 612-618. Peckarsky, B.L., B.W. Taylor, A.R. McIntosh, M.A. McPeek, D.A. Lytle. 2001. “Variation in mayfly size at metamorphosis as a developmental response to risk of predation.” Ecology 82(3): 740-757. Prather, A.L. 2003. “Revision of the Neotropical caddisfly genus Phylloicus (Trichoptera: Calamoceratidae).” Zootaxa 275: 1-214. Pringle, C.M. and G.A. Blake. 1994. “Quantitative effects of atyid shrimp (Decapoda: Atyidae) on the depositional environment in a tropical stream: Use of electricity for experimental exclusion.” Canadian Journal of Fisheries and Aquatic Sciences 51: 1443-1450. Reznick, D. and J.A. Endler. 1982. “The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata).” Evolution 36(1): 160-177. Richardson, J.L., M.C. Urban, D.I. Bolnick, and D.K. Skelly. 2014. “Microgeographic adaptation and the spatial scale of evolution.” Trends in Ecology and Evolution 29(3): 165-176. Rincón, J. and I. Martínez. 2006. “Food quality and feeding preferences of Phylloicus sp. 24 ! ! (Trichoptera: Calamoceratidae).” Journal of the North American Benthological Society 25(1): 209-215 Rowe, L. and D. Ludwig. 1991. “Size and timing of metamorphosis in complex life cycles: Time constraints and variation.” Ecology 72(2): 413-427. Schmitz, O.J., J.H. Grabowski, B.L. Peckarsky, E.L. Preisser, G.C. Trussell, and J.R. Vonesh. 2008. “From individuals to ecosystem function: Toward an integration of evolutionary and ecosystem ecology.” Ecology 89(9): 2436-2445. Stoks, R., M. De Block, M.A. McPeek. 2005. “Alternative growth and energy storage responses to mortality threats in damselflies.” Ecology Letters 8: 1307-1316. Sweeney, B.W. 1984. “Factors influencing life-history patterns of aquatic insects.” In V.H. Resh and D.M. Rosenberg (Eds.), The Ecology of Aquatic Insects 56-100. New York: Praeger. Torres-Dowdall, J., C.A. Handelsman, E.W. Ruell, S.K. Auer, D.N. Reznick, and C.K. Ghalambor. 2012. “Fine-scale local adaptation in life histories along a continuous environmental gradient.” Functional Ecology 26(3): 616-627. Turner, D., D.D. Williams, and M. Alkins-Koo. 2008. “Longitudinal changes in benthic community composition in four neotropical streams.” Caribbean Journal of Science 44(3): 380-394. Van Buskirk, J. and B.R. Schmidt. 2000. “Predator-induced phenotypic plasticity in larval newts: Trade-offs, selection and variation.” Ecology 81(11): 3009-3028. Wallace, J.B., S.L. Eggert, J.L. Meyer, and J.R. Webster. 1997. “Multiple trophic levels of a forest stream linked to terrestrial litter inputs.” Science 277: 102-104. Wallace, J.B. and J.R. Webster. 1996. “The role of macroinvertebrates in stream 25 ! ! ecosystem function.” Annual Review of Entomology 41: 115-139. Walsh, M.R., D.F. Fraser, R.D. Bassar, and D.N. Reznick. 2011. “The direct and indirect effect of guppies: implications for life-history evolution in Rivulus hartii.” Functional Ecology 25(1): 227-237. Walsh, M.R. and D.N. Reznick. 2008. “Interactions between the direct and indirect effects of predators determine life history evolution in a killifish.” Proceedings of the National Academy of Sciences of the United States of America 105(2): 594595. Walsh, M.R. and D.N. Reznick. 2009. “Phenotypic diversification across an environmental gradient: A role for predators and resource availability on the evolution of life histories.” Evolution 63(12): 3201-3213. Walsh, M.R. and D.N. Reznick. 2010. “Influence of the indirect effects of guppies on life-history evolution in Rivulus hartii.” Evolution 64(6): 1583-1593. Walsh, M.R. and D.N. Reznick. 2011. “Experimentally induced life-history evolution in a killifish in response to the introduction of guppies.” Evolution 65(4): 1021-1036. Wantzen, K.M. and R.Wagner. 2006. “Detritus processing by invertebrate shredders: a Neotropical-temperate comparison.” Journal of the North American Benthological Society 25(1): 216-232. Werner, E.E and B.R. Anholt. 1993. “Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity.” The American Naturalist 142(2): 242-272. Yoshida, T., L.E. Jones, S.P. Ellner, G.F. Fussmann, and N.G. Hairston Jr. 2003. “Rapid evolution drives ecological dynamics in a predator-prey system.” Nature 424: 26 ! ! 303-306. Zandonà, E., S.K. Auer, S.S. Kilham, J.L. Howard et al. 2011. “Diet quality and prey selectivity correlate with life histories and predation regime in Trinidadian guppies.” Functional Ecology 25: 964-973. ! 27 ! ! Table 1. Studies discussing the presence of Phylloicus spp. in Central and South America and their role as shredders in the stream community. Location Species Ecuador 00°06’N, 78°39’W Phylloicus sp. Information Phylloicus abundance is a major driver of litter breakdown in tropical montane streams, having a “disproportionate impact” Brazil 02°25’S, 59°43’W Phylloicus sp. Suggests that leaf breakdown in headwater streams is controlled by shredder abundance: Phylloicus and Triplectides caddisflies São Paulo State, Brazil Ribeirão da Quinta stream 23°06’47”S, 48°29’46”W Phylloicus sp. Brazil 15°54’S, 55°10’W Phylloicus sp. Guanapo watershed, Northern Range, Trinidad P. angustior Ulmer 1905 (as syn. P. hansoni Denning 1983) Heredia Province, Costa Rica 10°17’N; 84°02’W NW Venezuela 10°42’-11°08N, 72°42’72°22’W Calamoceratidae sp. Phylloicus sp. Phylloicus was the only true shredder species found in leaf-pack samples; abundance may be negatively impacted by riparian deforestation Phylloicus is one of the few leaf-feeders in a Neotropical system; inhabiting “slowly flowing zones near the stream bank, especially in flood pools” – “localized specialists,” possibly in response to the effects of current on surface area of leaf case Phylloicus is one of the largest caddisfly species and are possibly the only true shredders, but “relatively important;” inhabits 2nd, 3rd and 4th order streams. Leaf decomposition study: case-building by Calamoceratid larvae “responsible for marked losses in leaf area” and made up 15.7% of community in litter bags. One of two insect species found to be classified as a shredder. Laboratory feeding trials of different leaves – larvae preferred to feed on leaves with high N and P content and low content of polyphenols and lignin, though used leaves with high polyphenol and lignin content for case construction. 28 ! Source Encalada et al. 2010 Landeiro et al. 2010 de Carvalho & Uieda 2009 Wantzen & Wagner 2006 Botosaneanu & Sakal 1992 Benstead 1996 Rincón & Martínez 2006 ! Table 2. Five streams were used to collect Phylloicus hansoni larvae for size frequency analysis, each with a downstream KillifishGuppy, or KG, reach and an upstream Killifish-Only, or KO, reach. Values for each stream reach reflect means obtained for wetted width, depth, percent area of canopy cover, and leaf standing stocks (or, coarse benthic organic matter, “CBOM” mass) along three transects. Killifish Catch Per Unit Effort (CPUE) is the average of individuals caught from three baited minnow traps within each reach. Numbers in parentheses represent standard error. Stream Reach RDN KG Mean Depth (cm) % Canopy Cover 100.3 (26.08) 4.0 (1.38) 95.7 (1.80) 0.149 (0.115) 3.0 (3.0) (7.02) 5.5 (1.85) 94.6 (0.35) 0.413 (0.141) 13.7 (2.0) KG 244.3 (52.30) 12.1 (3.85) 94.9 (0.46) 0.199 (0.152) 8.3 (1.2) KO 244.3 (34.70) 12.4 (1.45) 89.7 (2.50) 0.065 (0.003) 10.7 (1.2) KG 357.0 (44.19) 3.5 (0.05) 84.2 (3.06) 0.176 (0.022) 7.0 (2.0) KO 195.0 (21.13) 7.8 (2.81) 90.1 (1.82) 0.138 (0.066) 13.7 (5.0) KG 378.7 (66.80) 8.5 (0.80) 93.3 (0.61) 0.180 (0.037) 13.0 (1.5) KO 221.0 (62.17) 6.2 (1.69) 94.2 (2.28) 0.245 (0.080) 19.7 (0.7) KG 141.3 (12.87) 5.7 (2.03) 92.4 (1.50) 1.103 (0.840) 12.0 (5.0) KO 149.0 3.4 (0.63) 92.4 (1.25) 0.133 (0.068) 19.0 (8.0) KO GDC CED END TRT 86.0 (9.29) 29 ! CBOM (g m-2) Wetted Width (cm) Killifish CPUE ! Table 3. Average size measurements of P. hansoni larvae and their leaf cases from each stream (± standard deviation) and mean of KO and KG reaches (with standard error). Larvae and cases were measured on a dissecting microscope to the nearest tenth of a millimeter. Case surface area was measured by multiplying the length by the average of three width measurements. Total number of larvae sampled: KO = 337, KG = 730. Stream Reach Body Length (mm) Head Capsule Width (mm) Case Length (mm) Case Area (mm2) RDN KG 8.7 (3.06) 0.85 (0.23) 15.7 (6.94) 123.1 (108.56) KO 7.0 (2.96) 0.69 (0.24) 13.0 (6.11) 81.6 (68.70) KG 3.9 (2.30) 0.49 (0.21) 8.0 (4.53) 35.2 (43.54) KO 5.4 (1.83) 0.57 (0.19) 9.9 (2.86) 47.3 (25.44) KG 9.0 (2.79) 0.84 (0.21) 18.4 (7.33) 188.1!(156.97)! KO 7.7 (2.94) 0.74!(0.27)! 14.0 (5.87) 103.6 (94.16) KG 7.3 (2.86) 0.78!(0.23)! 15.9 (6.97) 130.0 (107.90)! KO 7.5 (3.30) 0.77!(0.26)! 16.9 (8.69) 172.0 (183.14) KG 6.3 (3.21) 0.66 (0.29) 12.6 (6.80) 87.9!!(94.52)! KO 5.4 (2.97) 0.57 (0.25) 10.8 (6.50) 68.9 (95.17) KG 7.1 (0.92) 0.72 (0.07) 14.1 (1.78) 112.9 (25.20) KO 6.6 (0.50) 0.67 (0.04) 12.9 (1.24) 94.7 (21.37) GDC CED END TRT Mean 30 ! ! Table 4. Measurements of killifish gut contents from the 2011 site survey, from 4 streams: KG (n=40), and KO (n=52) killifish. Killifish length and P. hansoni head capsule width are of KG and KO samples; numbers in parentheses represent standard error.! Stream Reach % Killifish with P. hansoni in gut [with P. hansoni] Killifish length (mm) [Total] Killifish length (mm) P. hansoni head capsule width (mm) KG 30.0% 39.80 (3.38) 41.82 (3.29) 0.144 (0.0235) KO 9.6% 42.57 (3.29) 47.83 (1.48) 0.095 (0.0109) 31 ! ! KO reach KG reach Figure 1. Representation of fish assemblage of the streams we studied in Trinidad’s Northern Range: Upstream from barrier waterfalls are reaches with killifish as the only fish species (Killifish-Only or “KO” reaches), and downstream are reaches with both killifish (at lower densities) and guppies (Killifish-Guppy or “KG” reaches). Symbols courtesy of the Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/symbols/). 32 ! ! 60 % sampled 50 40 30 KG KO 20 10 0 J S M L XL A. hartii size class Figure 2. Average percent size class composition of killifish caught in minnow traps in KG and KO reaches of the streams (n=5) sampled. The size classes, measuring body length are: J – Juvenile: < 15mm, S – Small: 15-30mm, M – Medium: 30-45mm, L – Large: 45-60mm, and XL – Extra Large: >60mm. Error bars represent standard error. 33 ! ! 16 Body length (mm) 14 y = 10.757x - 0.5961 R² = 0.81518 KO 12 10 8 6 4 2 0 0.2 0.4 0.6 0.8 1 1.2 Head capsule width (mm) 16 Body length (mm) 14 KG y = 11.188x - 0.8914 R² = 0.81104 12 10 8 6 4 2 0 0.2 0.4 0.6 0.8 1 1.2 Head capsule width (mm) Figure 3. Scatter plot, showing measurements of body length and head capsule width (mm) of P. hansoni larvae for KO and KG larvae (KO, n = 281; KG, n = 598). 34 ! ! 60 60 50 KO 40 KG 30 20 Frequency Frequency 50 40 30 20 10 10 0 0 2 4 6 8 2 10 12 14 16 RDN - Body length (mm) 50 30 40 25 Frequency Frequency 4 6 8 10 12 14 GDC - Body length (mm) 30 20 10 20 15 10 5 0 0 2 4 6 8 10 12 14 2 CED - Body length (mm) 4 6 8 10 12 14 END - Body length (mm) 70 Frequency 60 50 40 30 20 10 0 2 4 6 8 10 12 14 TRT - Body length (mm) Figure 4. Size frequency distributions of larvae from KO and KG reaches of five streams individually. A two-sample K-S test was used to determine the difference between distributions of RDN, CED, END, and TRT: p=0.0002, 0.008, 0.93, and 0.036 respectively. 35 ! ! 0.85 A KO KG 8 7.5 7 6.5 6 Head capsule width (mm) Body length (mm) 8.5 5.5 KO B KG 0.8 0.75 0.7 0.65 0.6 Figure 5. Mean body length (A) and head capsule width (B) of total P. hansoni larvae collected in KO and KG reaches of four streams (END, RDN, TRT, CED). Error bars represent standard error. 140 KO 120 KG Frequency 100 80 60 40 20 0 2 4 6 8 10 12 14 16 P. hansoni body length (mm) Figure 6. Size frequency distribution of the body length of P. hansoni larvae collected in KO and KG reaches of four streams (END, RDN, TRT, CED). Individual body length was measured to the nearest 0.1mm. Total KO = 281, total KG = 598. 36 !