Environmental variables drive spatial patterns of trophic diversity in mammals.

Understanding environmental drivers of species diversity has become increasingly important under climate change. Different trophic groups (predators, omnivores and herbivores) interact with their environments in fundamentally different ways and may therefore be influenced by different environmental drivers. Using random forest models, we identified drivers of terrestrial mammals' total and proportional species richness within trophic groups at a global scale. Precipitation seasonality was the most important predictor of richness for all trophic groups. Richness peaked at intermediate precipitation seasonality, indicating that moderate levels of environmental heterogeneity promote mammal richness. Gross primary production (GPP) was the most important correlate of the relative contribution of each trophic group to total species richness. The strong relationship with GPP demonstrates that basal-level resource availability influences how diversity is structured among trophic groups. Our findings suggest that environmental characteristics that influence resource temporal variability and abundance are important predictors of terrestrial mammal richness at a global scale.

Landscape configuration affects probability of apex predator presence and community structure in experimental metacommunities.

Biodiversity is declining at an unprecedented rate, highlighting the urgent requirement for well-designed protected areas. Design tactics previously proposed to promote biodiversity include enhancing the number, connectivity, and heterogeneity of reserve patches. However, how the importance of these features changes depending on what the conservation objective is remains poorly understood. Here we use experimental landscapes containing ciliate protozoa to investigate how the number and heterogeneity in size of habitat patches, rates of dispersal between neighbouring patches, and mortality risk of dispersal across the non-habitat 'matrix' interact to affect a number of diversity measures. We show that increasing the number of patches significantly increases γ diversity and reduces the overall number of extinctions, whilst landscapes with heterogeneous patch sizes have significantly higher γ diversity than those with homogeneous patch sizes. Furthermore, the responses of predators depended on their feeding specialism, with generalist predator presence being highest in a single large patch, whilst specialist predator presence was highest in several-small patches with matrix dispersal. Our evidence emphasises the importance of considering multiple diversity measures to disentangle community responses to patch configuration.

Metal concentrations in wetland plant tissues influences transfer to terrestrial food webs.

Wetland plants tolerate potentially hazardous metals through a variety of strategies, including exclusion or accumulation. Whether plants sequester metals and where they store them in their tissues is important for understanding the potential role of plants as remediators or vectors of metals to terrestrial food webs. Here we evaluate metal sequestration in Great Salt Lake wetlands for one invasive (Phragmites australis; phragmites) and three native plant species, i.e. threesquare bulrush (Schoenoplectus americanus), hardstem bulrush (Schoenoplectus acutus), alkali bulrush (Bolboschoenus maritimus), and their terrestrial invertebrates. We observed higher concentrations of arsenic and copper than other metals in plant tissues, although high lead concentrations were observed in phragmites. All plants acted as excluders of arsenic and selenium, retaining the bulk of the metal mass in belowground tissues. In contrast, lead, copper, and cadmium were transferred to above ground tissues of hardstem bulrush and phragmites. The aboveground translocation facilitated the movement of these metals into invertebrates, with the highest concentrations in most cases found in predators. Though our results highlight the potential for metal remediation via wetland plant growth and removal, care should be taken to ensure that remediation efforts do not lead to bioaccumulation.

Imperfect detection alters the outcome of management strategies for protected areas.

Designing protected area configurations to maximise biodiversity is a critical conservation goal. The configuration of protected areas can significantly impact the richness and identity of the species found there; one large patch supports larger populations but can facilitate competitive exclusion. Conversely, many small habitats spreads risk but may exclude predators that typically require large home ranges. Identifying how best to design protected areas is further complicated by monitoring programs failing to detect species. Here we test the consequences of different protected area configurations using multi-trophic level experimental microcosms. We demonstrate that for a given total size, many small patches generate higher species richness, are more likely to contain predators, and have fewer extinctions compared to single large patches. However, the relationship between the size, number of patches, and species richness was greatly affected by insufficient monitoring, and could lead to incorrect conservation decisions, especially for higher trophic levels.

Bromeliads affect the interactions and composition of invertebrates on their support tree.

Individual species can have profound effects on ecological communities, but, in hyperdiverse systems, it can be challenging to determine the underlying ecological mechanisms. Simplifying species' responses by trophic level or functional group may be useful, but characterizing the trait structure of communities may be better related to niche processes. A largely overlooked trait in such community-level analyses is behaviour. In the Neotropics, epiphytic tank bromeliads (Bromeliaceae) harbour a distinct fauna of terrestrial invertebrates that is mainly composed of predators, such as ants and spiders. As these bromeliad-associated predators tend to forage on the bromeliads' support tree, they may influence the arboreal invertebrate fauna. We examined how, by increasing associated predator habitat, bromeliads may affect arboreal invertebrates. Specifically, we observed the trophic and functional group composition, and the behaviour and interspecific interactions of arboreal invertebrates in trees with and without bromeliads. Bromeliads modified the functional composition of arboreal invertebrates, but not the overall abundance of predators and herbivores. Bromeliads did not alter the overall behavioural profile of arboreal invertebrates, but did lead to more positive interactions in the day than at night, with a reverse pattern on trees without bromeliads. In particular, tending behaviours were influenced by bromeliad-associated predators. These results indicate that detailed examination of the functional affiliations and behaviour of organisms can reveal complex effects of habitat-forming species like bromeliads, even when total densities of trophic groups are insensitive.

Adaptation to agricultural pesticides may allow mosquitoes to avoid predators and colonize novel ecosystems.

Human activities such as the application of agrochemicals may detrimentally disturb natural ecosystems, generating novel selection pressures. Here we examine how pesticides may influence community composition using the aquatic communities within bromeliad phytotelmata, and how adaptive responses to pesticides may influence community-level patterns. We first quantified the composition of macroinvertebrate communities from pesticide-free and pesticide-exposed locations. Complementary manipulative experiments where bromeliads were transplanted between pesticide-free and pesticide-exposed sites were then performed. Finally, pesticide bioassays on the most common predators (Mecistogaster modesta damselflies) and prey (Wyeomyia abebela mosquitoes) assessed a potential evolutionary mechanism that may influence community compositional differences. Our field survey revealed differences in W. abebela and M. modesta abundances between pesticide-free and pesticide-exposed areas. Our transplant experiment suggested compositional differences were not due to physical differences between bromeliads from different locations. Pesticide bioassays revealed that M. modesta from pesticide-free locations had higher innate pesticide tolerances than W. abebela from pesticide-free areas, but M. modesta larvae showed no evidence of adapted resistance as none were found where pesticides were used. Conversely, W. abebela larvae from pesticide-exposed locations had higher pesticide tolerances than individuals from pesticide-free sites, suggesting an adaptive response. This evolved resistance to pesticides may, therefore, allow W. abebela to colonize habitats free of the dominant predator in the system, explaining the higher W. abebela abundances in pesticide-exposed areas than in pesticide-free locations. We suggest that the total effect of novel stressors is driven by interactions between ecological and evolutionary processes.

Landscape heterogeneity strengthens the relationship between ß-diversity and ecosystem function.

Consensus has emerged in the literature that increased biodiversity enhances the capacity of ecosystems to perform multiple functions. However, most biodiversity/ecosystem function studies focus on a single ecosystem, or on landscapes of homogenous ecosystems. Here, we investigate how increased landscape-level environmental dissimilarity may affect the relationship between different metrics of diversity (α, ß, or γ) and ecosystem function. We produced a suite of simulated landscapes, each of which contained four experimental outdoor aquatic mesocosms. Differences in temperature and nutrient conditions of the mesocosms allowed us to simulate landscapes containing a range of within-landscape environmental heterogeneities. We found that the variation in ecosystem functions was primarily controlled by environmental conditions, with diversity metrics accounting for a smaller (but significant) amount of variation in function. When landscapes were more homogeneous, α, ß, and γ diversity was not associated with differences in primary production, and only γ was associated with changes in decomposition. In these homogeneous landscapes, differences in these two ecosystem functions were most strongly related to nutrient and temperature conditions in the ecosystems. However, as landscape-level environmental dissimilarity increased, the relationship between α, ß, or γ and ecosystem functions strengthened, with ß being a greater predictor of variation in decomposition at the highest levels of environmental dissimilarity than α or γ. We propose that when all ecosystems in a landscape have similar environmental conditions, species sorting is likely to generate a single community composition that is well suited to those environmental conditions, ß is low, and the efficiency of diversity-ecosystem function couplings is similar across communities. Under this low ß, the effect of abiotic conditions on ecosystem function will be most apparent. However, when environmental conditions vary among ecosystems, species sorting pressures are different among ecosystems, producing different communities among locations in a landscape. These conditions lead to stronger relationships between ß and the magnitude of ecosystem functions. Our results illustrate that abiotic conditions and the homogeneity of communities influence ecosystem function expressed at the landscape scale.

Ocean acidification alters zooplankton communities and increases top-down pressure of a cubozoan predator.

The composition of local ecological communities is determined by the members of the regional community that are able to survive the abiotic and biotic conditions of a local ecosystem. Anthropogenic activities since the industrial revolution have increased atmospheric CO2 concentrations, which have in turn decreased ocean pH and altered carbonate ion concentrations: so called ocean acidification (OA). Single-species experiments have shown how OA can dramatically affect zooplankton development, physiology and skeletal mineralization status, potentially reducing their defensive function and altering their predatory and antipredatory behaviors. This means that increased OA may indirectly alter the biotic conditions by modifying trophic interactions. We investigated how OA affects the impact of a cubozoan predator on their zooplankton prey, predominantly Copepoda, Pleocyemata, Dendrobranchiata, and Amphipoda. Experimental conditions were set at either current (pCO2 370 µatm) or end-of-the-century OA (pCO2 1,100 µatm) scenarios, crossed in an orthogonal experimental design with the presence/absence of the cubozoan predator Carybdea rastoni. The combined effects of exposure to OA and predation by C. rastoni caused greater shifts in community structure, and greater reductions in the abundance of key taxa than would be predicted from combining the effect of each stressor in isolation. Specifically, we show that in the combined presence of OA and a cubozoan predator, populations of the most abundant member of the zooplankton community (calanoid copepods) were reduced 27% more than it would be predicted based on the effects of these stressors in isolation, suggesting that OA increases the susceptibility of plankton to predation. Our results indicate that the ecological consequences of OA may be greater than predicted from single-species experiments, and highlight the need to understand future marine global change from a community perspective.

Geographic range size and extinction risk assessment in nomadic species.

Geographic range size is often conceptualized as a fixed attribute of a species and treated as such for the purposes of quantification of extinction risk; species occupying smaller geographic ranges are assumed to have a higher risk of extinction, all else being equal. However many species are mobile, and their movements range from relatively predictable to-and-fro migrations to complex irregular movements shown by nomadic species. These movements can lead to substantial temporary expansion and contraction of geographic ranges, potentially to levels which may pose an extinction risk. By linking occurrence data with environmental conditions at the time of observations of nomadic species, we modeled the dynamic distributions of 43 arid-zone nomadic bird species across the Australian continent for each month over 11 years and calculated minimum range size and extent of fluctuation in geographic range size from these models. There was enormous variability in predicted spatial distribution over time; 10 species varied in estimated geographic range size by more than an order of magnitude, and 2 species varied by >2 orders of magnitude. During times of poor environmental conditions, several species not currently classified as globally threatened contracted their ranges to very small areas, despite their normally large geographic range size. This finding raises questions about the adequacy of conventional assessments of extinction risk based on static geographic range size (e.g., IUCN Red Listing). Climate change is predicted to affect the pattern of resource fluctuations across much of the southern hemisphere, where nomadism is the dominant form of animal movement, so it is critical we begin to understand the consequences of this for accurate threat assessment of nomadic species. Our approach provides a tool for discovering spatial dynamics in highly mobile species and can be used to unlock valuable information for improved extinction risk assessment and conservation planning.

Conspecific density modulates the effect of predation on dispersal rates.

Dispersal decisions underlie the spatial dynamics of metacommunities. Prey individuals may disperse to reduce the risk of either predation or starvation, and both of these risks may depend on conspecific density. Surprisingly, there is little theory examining how dispersal rates should change in response to the combined effects of predation and changes in conspecific density. We develop such a model and show that, under certain conditions, predators may induce dispersal at low prey densities but not high prey densities. We then experimentally manipulate the density of the ciliate Paramecium aurelia and the perceived presence of its predator, the flatworm Stenostomum virginiamum, in a two-patch metacommunity to parameterise the model. Paramecium dispersed in response to Stenostomum at low densities, but they reduced their dispersal in response to predation risk at high predator densities. By applying our model to the empirical data, we show that this switch in dispersal strategy, linked to increases in prey density, occurred because predators increased the difficulty or risk of dispersal. Together, the model and experiment reveal that the effects of predators on dispersal are contingent on prey density. Previous studies have sometimes reported an increase in dispersal rate when predation risk is elevated, and other times a decrease in dispersal rate. Our demonstration of a switch point, with predation risk increasing dispersal at low prey densities but reducing dispersal above a threshold of prey density, may reconcile the diversity of prey dispersal behaviours reported in these previous investigations and observed in nature.

Food web persistence is enhanced by non-trophic interactions.

The strength of interspecific interactions is often proposed to affect food web stability, with weaker interactions increasing the persistence of species, and food webs as a whole. However, the mechanisms that modify interaction strengths, and their effects on food web persistence are not fully understood. Using food webs containing different combinations of predator, prey, and nonprey species, we investigated how predation risk of susceptible prey is affected by the presence of species not directly trophically linked to either predators or prey. We predicted that indirect alterations to the strength of trophic interactions translate to changes in persistence time of extinction-prone species. We assembled interaction webs of protist consumers and turbellarian predators with eight different combinations of prey, predators and nonprey species, and recorded abundances for over 130 prey generations. Persistence of predation-susceptible species was increased by the presence of nonprey. Furthermore, multiple nonprey species acted synergistically to increase prey persistence, such that persistence was greater than would be predicted from the dynamics of simpler food webs. We also found evidence suggesting increased food web complexity may weaken interspecific competition, increasing persistence of poorer competitors. Our results demonstrate that persistence times in complex food webs cannot be predicted from the dynamics of simplified systems, and that species not directly involved in consumptive interactions likely play key roles in maintaining persistence. Global species diversity is currently declining at an unprecedented rate and our findings reveal that concurrent loss of species that modify trophic interactions may have unpredictable consequences for food web stability.

Trophic-level dependent effects on CO2 emissions from experimental stream ecosystems.

Concern over accelerating rates of species invasions and losses have initiated investigations into how local and global changes to predator abundance mediate trophic cascades that influence CO2 fluxes of aquatic ecosystems. However, to date, no studies have investigated how species additions or losses at other consumer trophic levels influence the CO2 flux of aquatic ecosystems. In this study, we added a large predatory stonefly, detritivorous stonefly, or grazer tadpole to experimental stream food webs and over a 70-day period quantified their effects on community composition, leaf litter decomposition, chlorophyll-a concentrations, and stream CO2 emissions. In general, streams where the large grazer or large detritivore were added showed no change in total invertebrate biomass, leaf litter loss, chlorophyll-a concentrations, or stream CO2 emissions compared with controls; although we did observe a spike in CO2 emissions in the large grazer treatment following a substantial reduction in chlorophyll-a concentrations on day 28. However, the large grazer and large detritivore altered the community composition of streams by reducing the densities of other grazer and detritivore taxa, respectively, compared with controls. Conversely, the addition of the large predator created trophic cascades that reduced total invertebrate biomass and increased primary producer biomass. The cascading effects of the predator additions on the food web ultimately led to decreased CO2 emissions from stream channels by up to 95%. Our results suggest that stream ecosystem processes were more influenced by changes in large predator abundance than large grazer or detritivore abundance, because of a lack of functionally similar large predators. Our study demonstrates that the presence/absence of species with unique functional roles may have consequences for the exchange of CO2 between the ecosystem and the atmosphere.

Competitive displacement alters top-down effects on carbon dioxide concentrations in a freshwater ecosystem.

Climate change and invasive species have the potential to alter species diversity, creating novel species interactions. Interspecific competition and facilitation between predators may either enhance or dampen trophic cascades, ultimately influencing total predator effects on communities and biogeochemical cycling of ecosystems. However, previous studies have only investigated the effects of a single predator species on CO2 flux of aquatic ecosystems. In this study, we measured and compared the individual and joint effects of predatory damselfly larvae and diving beetles on total prey biomass, leaf litter processing, and dissolved CO2 concentrations of experimental bromeliad ecosystems. Damselfly larvae created strong trophic cascades that reduced CO2 concentrations by ~46% relative to no-predator treatments. Conversely, the effects of diving beetles on prey biomass, leaf litter processing, and dissolved CO2 were not statistically different to no-predator treatments. Relative to multiplicative null models, the presence of damselfly larvae and diving beetles together resulted in antagonistic relations that eliminated trophic cascades and top-down influences on CO2 concentrations. Furthermore, we showed that the antagonistic interactions between predators occurred due to a tactile response that culminated in competitive displacement of damselfly larvae. Our results demonstrate that predator identity and predator-predator interactions can influence CO2 concentrations of an aquatic ecosystem. We suggest that predator effects on CO2 fluxes may depend on the particular predator species removed or added to the ecosystem and their interactions with other predators.

Contributions of mean temperature and temperature variation to population stability and community diversity.

Future climate changes are predicted to not only increase global temperatures but also alter temporal variation in temperature. As thermal tolerances form an important component of a species' niche, changes to the temperature regime have the capacity to negatively impact species, and therefore, the diversity of the communities they inhabit. In this study, we used protist microcosms to assess how mean temperature, as well as temporal variation in temperature, affected diversity. Communities consisted of seven species in a multitrophic food web. Each ecosystem was inoculated with the same abundances of each species at the start of the experiment, and species densities, Hill's numbers (based on Shannon diversity), the number of extinctions, and the probability the microcosm contained predators were all calculated at the end of the experiment. To assess how mean temperature and temperature fluctuations affect stability, we also measured population densities through time. We found that increased temporal variation in temperature increased final densities, increased Hill's numbers (at low mean temperatures), decreased rates of extinctions, and increased the probability that predators survived till the end of the experiment. Mean temperatures did not significantly affect either the number of extinctions or the probability of predators, but did reduce the positive effect of increased temporal variation in temperature on overall diversity. Our results indicate that climatic changes have the potential to impact the composition of ecological communities by altering multiple components of temperature regimes. However, given that some climate forecasts are predicting increased mean temperatures and reduced variability, our finding that increased mean temperature and reduced temporal variation are both generally associated with negative consequences is somewhat concerning.

Transcriptomics of environmental acclimatization and survival in wild adult Pacific sockeye salmon (Oncorhynchus nerka) during spawning migration.

Environmental shifts accompanying salmon spawning migrations from ocean feeding grounds to natal freshwater streams can be severe, with the underlying stress often cited as a cause of increased mortality. Here, a salmonid microarray was used to characterize changes in gene expression occurring between ocean and river habitats in gill and liver tissues of wild migrating sockeye salmon (Oncorhynchus nerka Walbaum) returning to spawn in the Fraser River, British Columbia, Canada. Expression profiles indicate that the transcriptome of migrating salmon is strongly affected by shifting abiotic and biotic conditions encountered along migration routes. Conspicuous shifts in gene expression associated with changing salinity, temperature, pathogen exposure and dissolved oxygen indicate that these environmental variables most strongly impact physiology during spawning migrations. Notably, transcriptional changes related to osmoregulation were largely preparatory and occurred well before salmon encountered freshwater. In the river environment, differential expression of genes linked with elevated temperatures indicated that thermal regimes within the Fraser River are approaching tolerance limits for adult salmon. To empirically correlate gene expression with survival, biopsy sampling of gill tissue and transcriptomic profiling were combined with telemetry. Many genes correlated with environmental variables were differentially expressed between premature mortalities and successful migrants. Parametric survival analyses demonstrated a broad-scale transcriptional regulator, cofactor required for Sp1 transcriptional activation (CRSP), to be significantly predictive of survival. As the environmental characteristics of salmon habitats continue to change, establishing how current environmental conditions influence salmon physiology under natural conditions is critical to conserving this ecologically and economically important fish species.

Predator functional response changed by induced defenses in prey.

Functional responses play a central role in the nature and stability of predator-prey population dynamics. Here we investigate how induced defenses affect predator functional responses. In experimental communities, prey (Paramecium) expressed two previously undocumented inducible defenses--a speed reduction and a width increase--in response to nonlethal exposure to predatory Stenostomum. Nonlethal exposure also changed the shape of the predator's functional response from Type II to Type III, consistent with changes in the density dependence of attack rates. Handling times were also affected by prey defenses, increasing at least sixfold. These changes show that induced changes in prey have a real defensive function. At low prey densities, induction led to lower attack success; at high prey densities, attack rates were actually higher for induced prey. However, induction increased handling times sufficiently that consumption rates of defended prey were lower than those of undefended prey. Modification of attack rate and handling time has important potential consequences for population dynamics; Type III functional responses can increase the stability of population dynamics and persistence because predation on small populations is low, allowing a relict population to survive. Simulations of a predator-prey population dynamic model revealed the stabilizing potential of the Type III response.

Stronger inducible defences enhance persistence of intraguild prey.

1. Intraguild predation is widespread in nature despite its potentially destabilizing effect on food web dynamics. 2. Anti-predator inducible defences affect both birth and death rates of populations and have the potential to substantially modify food web dynamics and possibly increase persistence of intraguild prey. 3. In a chemostat experiment, we investigated the long-term effects of inducible defences on the dynamics of aquatic microbial food webs consisting of an intraguild predator, intraguild prey, and a basal resource. We controlled environmental conditions and selected strains of intraguild prey that varied in the strength of expressed inducible defences. 4. We found that intraguild prey with a stronger tendency to induce an anti-predator morphology persist for significantly longer periods of time. In addition, model selection analysis implied that flexibility in defensive phenotype (inducibility itself) is most likely the factor responsible for the enhanced persistence. 5. As patterns at the community level often emerge as a result of the life-history traits of individuals, we propose that inducible defences increase the persistence of populations and may contribute to the widespread occurrence of theoretically unstable intraguild predation systems in nature.

Reciprocity in predator-prey interactions: exposure to defended prey and predation risk affects intermediate predator life history and morphology.

A vast body of literature exists documenting the morphological, behavioural and life history changes that predators induce in prey. However, little attention has been paid to how these induced changes feed back and affect the predators' life history and morphology. Larvae of the phantom midge Chaoborus flavicans are intermediate predators in a food web with Daphnia pulex as the basal resource and planktivorous fish as the top predator. C. flavicans prey on D. pulex and are themselves prey for fish; as D. pulex induce morphological defences in the presence of C. flavicans this is an ideal system in which to evaluate the effects of defended prey and top predators on an intermediate consumer. We assessed the impact on C. flavicans life history and morphology of foraging on defended prey while also being exposed to the non-lethal presence of a top fish predator. We tested the basic hypothesis that the effects of defended prey will depend on the presence or absence of top predator predation risk. Feeding rate was significantly reduced and time to pupation was significantly increased by defended morph prey. Gut size, development time, fecundity, egg size and reproductive effort respond to fish chemical cues directly or significantly alter the relationship between a trait and body size. We found no significant interactions between prey morph and the non-lethal presence of a top predator, suggesting that the effects of these two biological factors were additive or singularly independent. Overall it appears that C. flavicans is able to substantially modify several aspects of its biology, and while some changes appear mere consequences of resource limitation others appear facultative in nature.

Herbivores at the highest risk of extinction among mammals, birds, and reptiles.

As a result of their extensive home ranges and slow population growth rates, predators have often been perceived to suffer higher risks of extinction than other trophic groups. Our study challenges this extinction-risk paradigm by quantitatively comparing patterns of extinction risk across different trophic groups of mammals, birds, and reptiles. We found that trophic level and body size were significant factors that influenced extinction risk in all taxa. At multiple spatial and temporal scales, herbivores, especially herbivorous reptiles and large-bodied herbivores, consistently have the highest proportions of threatened species. This observed elevated extinction risk for herbivores is ecologically consequential, given the important roles that herbivores are known to play in controlling ecosystem function.

Protecting endangered species in the USA requires both public and private land conservation.

Crucial to the successful conservation of endangered species is the overlap of their ranges with protected areas. We analyzed protected areas in the continental USA to assess the extent to which they covered the ranges of endangered tetrapods. We show that in 80% of ecoregions, protected areas offer equal (25%) or worse (55%) protection for species than if their locations were chosen at random. Additionally, we demonstrate that it is possible to achieve sufficient protection for 100% of the USA's endangered tetrapods through targeted protection of undeveloped public and private lands. Our results highlight that the USA is likely to fall short of its commitments to halting biodiversity loss unless more considerable investments in both public and private land conservation are made.