Disassembly of a tadpole community by a multi-host fungal pathogen with limited evidence of recovery.

Emerging infectious diseases can cause host community disassembly, but the mechanisms driving the order of species declines and extirpations following a disease outbreak are unclear. We documented the community disassembly of a Neotropical tadpole community during a chytridiomycosis outbreak, triggered by the generalist fungal pathogen, Batrachochytrium dendrobatidis (Bd). Within the first 11 months of Bd arrival, tadpole density and occupancy rapidly declined. Species rarity, in terms of tadpole occupancy and adult relative abundance, did not predict the odds of tadpole occupancy declines. But species losses were taxonomically selective, with glassfrogs (Family: Centrolenidae) disappearing the fastest and tree frogs (Family: Hylidae) and dart-poison frogs (Family: Dendrobatidae) remaining the longest. We detected biotic homogenization of tadpole communities, with post-decline communities resembling one another more strongly than pre-decline communities. The entire tadpole community was extirpated within 22 months following Bd arrival, and we found limited signs of recovery within 10 years post-outbreak. Because of imperfect species detection inherent to sampling species-rich tropical communities and the difficulty of devising a single study design protocol to sample physically complex tropical habitats, we used simulations to provide recommendations for future surveys to adequately sample diverse Neotropical communities. Our unique data set on tadpole community composition before and after Bd arrival is a valuable baseline for assessing amphibian recovery. Our results are of direct relevance to conservation managers and community ecologists interested in understanding the timing, magnitude, and consequences of disease outbreaks as emerging infectious diseases spread globally.

Evidence for the persistence of food web structure after amphibian extirpation in a Neotropical stream.

Species losses are predicted to simplify food web structure, and disease-driven amphibian declines in Central America offer an opportunity to test this prediction. Assessment of insect community composition, combined with gut content analyses, was used to generate periphyton-insect food webs for a Panamanian stream, both pre- and post-amphibian decline. We then used network analysis to assess the effects of amphibian declines on food web structure. Although 48% of consumer taxa, including many insect taxa, were lost between pre- and post-amphibian decline sampling dates, connectance declined by less than 3%. We then quantified the resilience of food web structure by calculating the number of expected cascading extirpations from the loss of tadpoles. This analysis showed the expected effects of species loss on connectance and linkage density to be more than 60% and 40%, respectively, than were actually observed. Instead, new trophic linkages in the post-decline food web reorganized the food web topology, changing the identity of "hub" taxa, and consequently reducing the effects of amphibian declines on many food web attributes. Resilience of food web attributes was driven by a combination of changes in consumer diets, particularly those of insect predators, as well as the appearance of generalist insect consumers, suggesting that food web structure is maintained by factors independent of the original trophic linkages.

Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies.

A trophic niche shift can occur as an adaptive response to environmental change such as altered resource quality, abundance or composition. Alterations in digestive traits such as gut morphology and physiology may enable these niche shifts and affect the persistence of populations and species. Relatively few studies, however, have assessed how niche shifts influence suites of digestive traits through phenotypic plasticity and evolutionary mechanisms, and how these trait changes can subsequently alter the nutrition, fitness and life history of organisms. We investigated how population divergence and plasticity alter the gut physiology of wild Trinidadian guppies (Poecilia reticulata), assessing whether variation in digestive traits correspond with enhanced nutrient assimilation under a pronounced dietary shift. We examined gut enzyme activity, and gut size and mass of wild guppies from both high-predation (HP) and low-predation (LP) habitats when reared in the laboratory and fed on high- or low-quality diets designed to reflect their dietary differences previously found in nature. After 10 weeks on the experimental diets, HP guppies maintained shorter and lighter guts than LP guppies on either diet. Guppies also differed in their digestive enzymatic profiles, more often reflecting nutrient balancing so that increased enzyme expression tended to correspond with more deficient nutrients in the diet. LP guppies had increased somatic phosphorus at the end of the experiment, possibly related to the higher alkaline phosphatase activity in their guts. Our results suggest that differences in gut physiology exist among populations of Trinidadian guppies that may reflect local adaptation to their disparate environments.

Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis.

Symbiotic bacteria often help their hosts acquire nutrients from their diet, showing trends of co-evolution and independent acquisition by hosts from the same trophic levels. While these trends hint at important roles for biotic factors, the effects of the abiotic environment on symbiotic community composition remain comparably understudied. In this investigation, we examined the influence of abiotic and biotic factors on the gut bacterial communities of fish from different taxa, trophic levels and habitats. Phylogenetic and statistical analyses of 25 16S rRNA libraries revealed that salinity, trophic level and possibly host phylogeny shape the composition of fish gut bacteria. When analysed alongside bacterial communities from other environments, fish gut communities typically clustered with gut communities from mammals and insects. Similar consideration of individual phylotypes (vs. communities) revealed evolutionary ties between fish gut microbes and symbionts of animals, as many of the bacteria from the guts of herbivorous fish were closely related to those from mammals. Our results indicate that fish harbour more specialized gut communities than previously recognized. They also highlight a trend of convergent acquisition of similar bacterial communities by fish and mammals, raising the possibility that fish were the first to evolve symbioses resembling those found among extant gut fermenting mammals.

Effect of nutrient availability on the uptake of PCB congener 2,2',6,6'-tetrachlorobiphenyl by a diatom (Stephanodiscus minutulus) and transfer to a zooplankton (Daphnia pulicaria).

The objective of this study was to examine the importance of nutrient status of a diatom (Stephanodiscus minutulus) to the uptake of PCB congener #54 (2,2',6,6'-tetrachlorobiphenyl) and the subsequent transfer of PCB to a pelagic grazing zooplankton (Daphnia pulicaria). The algae, which were grown under different nutrient treatments, were then fed to a zooplankton to examine the subsequent food chain transfer of PCB. Algal cultures were grown for at least 2 weeks in a steady state condition in (1) non-limiting, (2) low-Si, (3) low-N or (4) low-P media. Steady state algal cultures were dosed with 0.2 microg L(-1) PCB and were sampled for PCB uptake after 24h. D. pulicaria were allowed to graze on these same cultures for 48 h before being analyzed for PCB body burdens. Low-Si (68% or 0.135 microg L(-1) of PCB) and low-P cultures (62%) had significantly higher percentage uptake of total PCB than the non-limiting (55%) or low-N (52%) treatments. When these values were divided by biochemical or elemental parameters, PCB per lipids (microg microg(-1)) had one of the lowest coefficients of variation (CV) across the four treatments, indicating their importance in PCB uptake. When equal biovolumes of the four different treatment cultures were fed to zooplankton, both the low-N (13.9 ng PCB mg wet weight(-1)) and the low-P (9.6 ng PCB mg wet weight(-1)) grazing D. pulicaria had significantly higher PCB per wet weight than the low-Si (5.6 ng PCB mg wet weight(-1)) and non-limited (2.6 ng PCB mg wet weight(-1)) grazing D. pulicaria. There were no significant differences between algal nutrient treatments in PCB per wet weight of zooplankton grazing on clean algal food in PCB contaminated media. This study indicates that uptake of PCB by phytoplankton can be significantly altered by nutrient availability which subsequently affects transfer to zooplankton, potentially through such responses as grazing rate and lipid assimilation.

Population variation in the trophic niche of the Trinidadian guppy from different predation regimes.

Population variation in trophic niche is widespread among organisms and is of increasing interest given its role in both speciation and adaptation to changing environments. Trinidadian guppies (Poecilia reticulata) inhabiting stream reaches with different predation regimes have rapidly evolved divergent life history traits. Here, we investigated the effects of both predation and resource availability on guppy trophic niches by evaluating their gut contents, resource standing stocks, and δ15N and δ13C stable isotopes across five streams during the wet season. We found that guppies from low predation (LP) sites had a consistently higher trophic position and proportion of invertebrates in their guts and assimilate less epilithon than guppies from high predation (HP) sites. Higher trophic position was also associated with lower benthic invertebrate availability. Our results suggest that LP guppies could be more efficient invertebrate consumers, possibly as an evolutionary response to greater intraspecific competition for higher quality food. This may be intensified by seasonality, as wet season conditions can alter resource availability, feeding rates, and the intensity of intraspecific competition. Understanding how guppy diets vary among communities is critical to elucidating the role of niche shifts in mediating the link between environmental change and the evolution of life histories.

Contrasting Population and Diet Influences on Gut Length of an Omnivorous Tropical Fish, the Trinidadian Guppy (Poecilia reticulata).

Phenotypic plasticity is advantageous for organisms that live in variable environments. The digestive system is particularly plastic, responding to changes in diet. Gut length is the result of a trade-off between maximum nutrient absorption and minimum cost for its maintenance and it can be influenced by diet and by evolutionary history. We assessed variation in gut length of Trinidadian guppies (Poecilia reticulata) as a function of diet, season, ontogeny, and local adaptation. Populations of guppies adapted to different predation levels have evolved different life history traits and have different diets. We sampled guppies from sites with low (LP) and high predation (HP) pressure in the Aripo and Guanapo Rivers in Trinidad. We collected fish during both the dry and wet season and assessed their diet and gut length. During the dry season, guppies from HP sites fed mostly on invertebrates, while guppies in the LP sites fed mainly on detritus. During the wet season, the diet of LP and HP populations became very similar. We did not find strong evidence of an ontogenetic diet shift. Gut length was negatively correlated with the proportion of invertebrates in diet across fish from all sites, supporting the hypothesis that guppy digestive systems adapt in length to changes in diet. Population of origin also had an effect on gut length, as HP and LP fish maintained different gut lengths even in the wet season, when their diets were very similar and individuals in both types of populations fed mostly on detritus. Thus, both environment and population of origin influenced guppies gut length, but population of origin seemed to have a stronger effect. Our study also showed that, even in omnivorous fish, gut length adapted to different diets, being more evident when the magnitude of difference between animal and plant material in the diet was very large.

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies.

Diverse microbial consortia profoundly influence animal biology, necessitating an understanding of microbiome variation in studies of animal adaptation. Yet, little is known about such variability among fish, in spite of their importance in aquatic ecosystems. The Trinidadian guppy, Poecilia reticulata, is an intriguing candidate to test microbiome-related hypotheses on the drivers and consequences of animal adaptation, given the recent parallel origins of a similar ecotype across streams. To assess the relationships between the microbiome and host adaptation, we used 16S rRNA amplicon sequencing to characterize gut bacteria of two guppy ecotypes with known divergence in diet, life history, physiology and morphology collected from low-predation (LP) and high-predation (HP) habitats in four Trinidadian streams. Guts were populated by several recurring, core bacteria that are related to other fish associates and rarely detected in the environment. Although gut communities of lab-reared guppies differed from those in the wild, microbiome divergence between ecotypes from the same stream was evident under identical rearing conditions, suggesting host genetic divergence can affect associations with gut bacteria. In the field, gut communities varied over time, across streams and between ecotypes in a stream-specific manner. This latter finding, along with PICRUSt predictions of metagenome function, argues against strong parallelism of the gut microbiome in association with LP ecotype evolution. Thus, bacteria cannot be invoked in facilitating the heightened reliance of LP guppies on lower-quality diets. We argue that the macroevolutionary microbiome convergence seen across animals with similar diets may be a signature of secondary microbial shifts arising some time after host-driven adaptation.

EFFECT OF NUTRIENT AVAILABILITY ON THE BIOCHEMICAL AND ELEMENTAL STOICHIOMETRY IN THE FRESHWATER DIATOM STEPHANODISCUS MINUTULUS (BACILLARIOPHYCEAE).

The objective of this study was to examine the differences in the biochemical and elemental stoichiometry of a freshwater centric diatom, Stephanodiscus minutulus (Grun.), under various nutrient regimes. Stephanodiscus minutulus was grown at µmax or 22% of µmax under limitation by silicon, nitrogen, or phosphorus. Cell sizes for nutrient-limited cultures were significantly smaller than the non-limited cell sizes, with N-limited cells being significantly smaller than all other treatments. Compared with the nutrient-replete treatment, both carbohydrates and lipids increased in Si- and P-limited cells, whereas carbohydrates increased but proteins decreased in N-limited cells. All of the growth-limited cells showed an increase of carbohydrate and triglyceride, and a decrease of cell size and polar lipids as a percentage of total lipids. The non-limited cells also had a significantly higher chl a concentration and galactolipids as a percentage of total lipids than any of the limited treatments, and the low-Si and low-P cells had significantly higher values than the low-N cells. The particulate C concentrations showed significant differences between treatments, with the Si- and P-limited treatments being significantly higher than the N- and non-limited treatments. Particulate Si did not show a strong relationship with any of the parameters measured, and it was the only parameter with no differences between treatments. The low-Si cells had a significantly higher P content (about two times more) than any other treatment, presumably owing to the luxury consumption of P, and a correspondingly high phospholipid concentration. The elemental data showed that S. minutulus had a high P demand with low optimum N:P (4) and Si:P (10) ratios and a C:N:P ratio of 109:16:2.3. The particulate C showed a positive relationship with POM (r = 0.93), dry weight (r = 0.88), lipid (r = 0.87) and protein (r = 0.84, all P < 0.0001). Particulate N showed a positive relationship with galactolipids (r = 0.95), protein (r = 0.90), dry weight (r = 0.78), lipid (r = 0.75), and cell volume (r = 0.64, all P < 0.0001). It is evident that nutrient limitation in the freshwater diatom S. minutulus has pronounced effects on its biochemical and elemental stoichiometry.

Stable isotopes of C and N reveal habitat dependent dietary overlap between native and introduced turtles Pseudemys rubriventris and Trachemys scripta.

Habitat degradation and species introductions are two of the leading causes of species declines on a global scale. Invasive species negatively impact native species through predation and competition for limited resources. The impacts of invasive species may be increased in habitats where habitat degradation is higher due to reductions of prey abundance and distribution. Using stable isotope analyses and extensive measurements of resource availability we determined how resource availability impacts the long term carbon and nitrogen assimilation of the invasive red-eared slider turtle (Trachemys scripta elegans) and a native, threatened species, the red-bellied turtle (Pseudemys rubriventris) at two different freshwater wetland complexes in Pennsylvania, USA. At a larger wetland complex with greater vegetative species richness and diversity, our stable isotope analyses showed dietary niche partitioning between species, whereas analyses from a smaller wetland complex with lower vegetative species richness and diversity showed significant dietary niche overlap. Determining the potential for competition between these two turtle species is important to understanding the ecological impacts of red-eared slider turtles in wetland habitats. In smaller wetlands with increased potential for competition between native turtles and invasive red-eared slider turtles we expect that when shared resources become limited, red-eared slider turtles will negatively impact native turtle species leading to long term population declines. Protection of intact wetland complexes and the reduction of introduced species populations are paramount to preserving populations of native species.

Effects of consumer interactions on benthic resources and ecosystem processes in a neotropical stream.

The effect of consumers on their resources has been demonstrated in many systems but is often confounded by trophic interactions with other consumers. Consumers may also have behavioral and life history adaptations to each other and to co-occurring predators that may additionally modulate their particular roles in ecosystems. We experimentally excluded large consumers from tile periphyton, leaves and natural benthic substrata using submerged electrified frames in three stream reaches with overlapping consumer assemblages in Trinidad, West Indies. Concurrently, we assessed visits to (non-electrified) control frames by the three most common large consumers-primarily insectivorous killifish (Rivulus hartii), omnivorous guppies (Poecilia reticulata) and omnivorous crabs (Eudaniela garmani). Consumers caused the greatest decrease in final chlorophyll a biomass and accrual rates the most in the downstream reach containing all three focal consumers in the presence of fish predators. Consumers also caused the greatest increase in leaf decay rates in the upstream reach containing only killifish and crabs. In the downstream reach where guppies co-occur with predators, we found significantly lower benthic invertebrate biomass in control relative to exclosure treatments than the midstream reach where guppies occur in the absence of predators. These data suggest that differences in guppy foraging, potentially driven by differences in their life history phenotype, may affect ecosystem structure and processes as much as their presence or absence and that interactions among consumers may further mediate their effects in these stream ecosystems.