Consequences of climate-induced range expansions on multiple ecosystem functions.

Climate-driven species range shifts and expansions are changing community composition, yet the functional consequences in natural systems are mostly unknown. By combining a 30-year survey of subalpine pond larval caddisfly assemblages with species-specific functional traits (nitrogen and phosphorus excretion, and detritus processing rates), we tested how three upslope range expansions affected species' relative contributions to caddisfly-driven nutrient supply and detritus processing. A subdominant resident species (Ag. deflata) consistently made large relative contributions to caddisfly-driven nitrogen supply throughout all range expansions, thus "regulating" the caddisfly-driven nitrogen supply. Whereas, phosphorus supply and detritus processing were regulated by the dominant resident species (L. externus) until the third range expansion (by N. hostilis). Since the third range expansion, N. hostilis's relative contribution to caddisfly-driven phosphorus supply increased, displacing L. externus's role in regulating caddisfly-driven phosphorus supply. Meanwhile, detritus processing contributions became similar among the dominant resident, subdominant residents, and range expanding species. Total ecosystem process rates did not change throughout any of the range expansions. Thus, shifts in species' relative functional roles may occur before shifts in total ecosystem process rates, and changes in species' functional roles may stabilize processes in ecosystems undergoing change.

Species-specific traits predict whole-assemblage detritus processing by pond invertebrates.

Functional trait diversity determines if ecosystem processes are sensitive to shifts in species abundances or composition. For example, trait variation suggests detritivores process detritus at different rates and make different contributions to whole-assemblage processing, which could be sensitive to compositional shifts. Here, we used a series of microcosm experiments to quantify species-specific coarse and fine particulate organic matter (CPOM and FPOM) processing for ten larval caddisfly species and three non-caddisfly species in high-elevation wetlands. We then compared trait-based models including life history, dietary, and extrinsic traits to determine which traits explained interspecific variation in detritus processing. Finally, we compared processing by mixed caddisfly assemblages in microcosms and natural ponds to additive predictions based on species-specific processing to determine if single-species effects are additive in multi-species assemblages. We found considerable interspecific variation in biomass-specific CPOM (13-fold differences) and FPOM (8-fold differences) processing. Furthermore, on a mass-specific basis, amphipods, chironomids, and caddisflies processed similar amounts of detritus, suggesting non-shredder taxa could process more than previously recognized. Trait models including dietary percent detritus, development rate, body size, and wetland hydroperiod explained 81 and 57% of interspecific variation in CPOM and FPOM processing, respectively. Finally, species-specific additive predictions were strikingly similar to mixed-assemblage processing in microcosms and natural ponds, with the largest difference being a 15% overestimate. Thus, additivity of species-specific processing suggests single-species rates may be useful for understanding functional consequences of shifting assemblages, and a trait-based approach to predicting species-specific processing could support generating additive predictions of whole-assemblage processing.

Perils of life on the edge: Climatic threats to global diversity patterns of wetland macroinvertebrates.

Climate change is rapidly driving global biodiversity declines. How wetland macroinvertebrate assemblages are responding is unclear, a concern given their vital function in these ecosystems. Using a data set from 769 minimally impacted depressional wetlands across the globe (467 temporary and 302 permanent), we evaluated how temperature and precipitation (average, range, variability) affects the richness and beta diversity of 144 macroinvertebrate families. To test the effects of climatic predictors on macroinvertebrate diversity, we fitted generalized additive mixed-effects models (GAMM) for family richness and generalized dissimilarity models (GDMs) for total beta diversity. We found non-linear relationships between family richness, beta diversity, and climate. Maximum temperature was the main climatic driver of wetland macroinvertebrate richness and beta diversity, but precipitation seasonality was also important. Assemblage responses to climatic variables also depended on wetland water permanency. Permanent wetlands from warmer regions had higher family richness than temporary wetlands. Interestingly, wetlands in cooler and dry-warm regions had the lowest taxonomic richness, but both kinds of wetlands supported unique assemblages. Our study suggests that climate change will have multiple effects on wetlands and their macroinvertebrate diversity, mostly via increases in maximum temperature, but also through changes in patterns of precipitation. The most vulnerable wetlands to climate change are likely those located in warm-dry regions, where entire macroinvertebrate assemblages would be extirpated. Montane and high-latitude wetlands (i.e., cooler regions) are also vulnerable to climate change, but we do not expect entire extirpations at the family level.

Predators balance consequences of climate-change-induced habitat shifts for range-shifting and resident species.

While many species distributions are shifting poleward or up in elevation in response to a changing climate, others are shifting their habitats along localized gradients in environmental conditions as abiotic conditions become more stressful. Whether species are moving across regional or local environmental gradients in response to climate change, range-shifting species become embedded in established communities of competitors and predators. The consequences of these shifts for both resident and shifting species are often unknown, as it can be difficult to isolate the effects of multiple species interactions. Using a model system of insects in high-elevation ponds in the Rocky Mountains of Colorado, we sought to disentangle the effects of predation and intraguild interactions on the survival and development of a semi-permanent pond resident caddisfly Limnephilus externus and the habitat-shifting caddis Asynarchus nigriculus that is being forced into semi-permanent ponds as temporary ponds dry too quickly to complete development. We conducted a manipulative in-situ pond cage experiment in which L. externus and A. nigriculus caddisfly larvae in single-species treatments and together were exposed to the presence/absence of predatory Dytiscus diving beetle larvae. This approach allowed us to isolate the effects of intraguild interactions and predation on the survival and development of both the resident and habitat-shifting species. We found that intraguild interactions had strong negative effects on the resident and habitat-shifting species. Intraguild interactions reduced the survival of the resident L. externus and increased the variation in survival of the shifting A. nigriculus. However, Dytiscus predators reduced these negative effects, stabilizing the community by increasing L. externus survival and reducing variation in A. nigriculus survival. We also found that intraguild interactions reduced L. externus biomass but resulted in increased A. nigriculus development. A. nigriculus development was also increased by predation. Our results show that strong intraguild interactions between resident and shifting species are likely to have negative consequences for both species. However, the presence of predators reduces these negative consequences of the habitat shift on both the resident and the shifting.

Elevation alters outcome of competition between resident and range-shifting species.

Species' geographic range shifts toward higher latitudes and elevations are among the most frequently reported consequences of climate change. However, the role of species interactions in setting range margins remains poorly understood. We used cage experiments in ponds to test competing hypotheses about the role of abiotic and biotic mechanisms for structuring range boundaries of an upslope range-shifting caddisfly Limnephilus picturatus. We found that competition with a ubiquitous species Limnephilus externus significantly decreased L. picturatus survival and emergence at subalpine elevations supporting the notion that species interactions play a critical role in determining upslope range limits. However, without competitors, L. picturatus survival was greater at high-elevation than low-elevation sites. This was contrary to decreases in body mass (a proxy for fecundity) with elevation regardless of the presence of competitors. We ultimately show that species interactions can be important for setting upslope range margins. Yet, our results also highlight the complications in defining what may be abiotically stressful for this species and the importance of considering multiple demographic variables. Understanding how species ranges will respond in a changing climate will require quantifying species interactions and how they are influenced by the abiotic context in which they play out.

Assessment of Long-Term Trends in Fish Distributions at Multiple Scales Decreases Uncertainty Associated with Historical Datasets.

Monitoring long-term changes in aquatic biodiversity requires the effective use of historical data that were collected with different methods and varying levels of effort. Aggregating data into different spatial scales can control for such differences and provide a robust framework for monitoring distribution trends. We used a quantitative, multi-scale assessment to evaluate the potential drivers of distribution change for 60 fish species at three spatial scales, using 503 unique sampling events conducted between 1931 and 2019 in a stream biodiversity hotspot (French Creek, Pennsylvania, U.S.A). Trends delineated at multiple scales demonstrated that only one cyprinid species consistently declined through time. In contrast, several species, particularly centrarchids (bass and sunfish), appeared to increase with time. However, evidence for species' increases varied among the different spatial scales, and our observations suggest that differences in effort and detection across time periods may contribute to patterns of species increases. There was agreement among scales that agricultural land use, non-native brown trout (Salmo trutta), and anthropogenic barriers did not explain patterns in biodiversity change from the distribution trends in this study. The lack of species declines is likely due to the limited levels of historical impacts in the watershed compared with other locations in the region that experienced more acute pollution bottlenecks. Species increases were most prevalent for sportfish and baitfish species, suggesting that distribution increases were human mediated. Similar multi-scale assessments should provide more robust insight into patterns of biodiversity loss and distribution changes by maximizing the use of historical data.

Seasonal differences in climate change explain a lack of multi-decadal shifts in population characteristics of a pond breeding salamander.

There is considerable variation among studies that evaluate how amphibian populations respond to global climate change. We used 23 years of annual survey data to test whether changes in climate have caused predictable shifts in the phenology and population characteristics of adult spotted salamanders (Ambystoma maculatum) during spring breeding migrations. Although we observed year-to-year correlation between seasonal climate variables and salamander population characteristics, there have not been long-term, directional shifts in phenological or population characteristics. Warm winters consistently resulted in early migration dates, but across the 23-year study, there was no overall shift towards warmer winters and thus no advanced migration timing. Warm summers and low variability in summer temperatures were correlated with large salamander body sizes, yet an overall shift towards increasing body sizes was not observed despite rising summer temperatures during the study. This was likely due to the absence of long-term changes of within-year variation in summer temperatures, which was a stronger determinant of body size than summer temperature alone. Climate-induced shifts in population characteristics were thus not observed for this species as long-term changes in important seasonal climate variables were not observed during the 23-years of the study. Different amphibian populations will likely be more resilient to climate change impacts than others, and the probability of amphibians exhibiting long-term population changes will depend on how seasonal climate change interacts with a species' life history, phenology, and geographic location. Linking a wide range of seasonal climatic conditions to species or population characteristics should thus improve our ability for explaining idiosyncratic responses of species to climate change.

Top-down control of prey increases with drying disturbance in ponds: a consequence of non-consumptive interactions?

1. Biotic interactions are often expected to decrease in intensity as abiotic conditions become more stressful to organisms. However, in many cases, food-web and habitat complexity also change with abiotic stress or disturbance, potentially altering patterns of species interactions across environmental gradients. 2. We used a combination of field assays and mesocosm experiments to investigate how disturbance from desiccation moderates top-down control of prey by predators across a gradient of pond duration in New Zealand. 3. Field manipulations of predator abundance in ponds led to an unexpected decrease in the top-down control of prey biomass by predatory invertebrates as pond duration increased (decreasing abiotic stress). Predatory fish, which are restricted to permanent ponds, had negligible effects on prey biomass. Mesocosm experiments further indicated the consumptive effects of fish are weak; a result that cannot be explained by an increase in physical habitat refugia in relatively more permanent ponds. 4. Manipulations of invertebrate predator diversity in mesocosms (both substitutive and additive treatments), and the addition of olfactory fish cues, revealed that strong non-consumptive effects of fish reduced predation by predatory invertebrates, and these effects overwhelmed the positive influence of invertebrate predator diversity on prey consumption. 5. These results suggest that decreases in top-down control with increasing pond permanence are likely a result of non-consumptive effects of fish weakening predation by invertebrate predators in the more complex food webs of permanent ponds. Therefore, considering non-consumptive effects of predators in complex food webs will likely improve the understanding of biotic interactions across environmental gradients.

Nonlinear effects of consumer density on multiple ecosystem processes.

1. In the face of human-induced declines in the abundance of common species, ecologists have become interested in quantifying how changes in density affect rates of biophysical processes, hence ecosystem function. We manipulated the density of a dominant detritivore (the cased caddisfly, Limnephilus externus) in subalpine ponds to measure effects on the release of detritus-bound nutrients and energy. 2. Detritus decay rates (k, mass loss) increased threefold, and the loss of nitrogen (N) and phosphorus (P) from detrital substrates doubled across a range of historically observed caddisfly densities. Ammonium and total soluble phosphorus concentrations in the water column also increased with caddisfly density on some dates. Decay rates, nutrient release and the change in total detritivore biomass all exhibited threshold or declining responses at the highest densities. 3. We attributed these threshold responses in biophysical processes to intraspecific competition for limiting resources manifested at the population level, as density-dependent per-capita consumption, growth, development and case : body size in caddisflies was observed. Moreover, caddisflies increasingly grazed on algae at high densities, presumably in response to limiting detrital resources. 4. These results provide evidence that changes in population size of a common species will have nonlinear, threshold effects on the rates of biophysical processes at the ecosystem level. Given the ubiquity of negative density dependence in nature, nonlinear consumer density-ecosystem function relationships should be common across species and ecosystems.

Consumptive and nonconsumptive effects of cannibalism in fluctuating age-structured populations.

Theory and empirical studies suggest that cannibalism in age-structured populations can regulate recruitment depending on the intensity of intraspecific competition between cannibals and victims and the nature of the cannibalism window, i.e., which size classes interact as cannibals and victims. Here we report on a series of experiments that quantify that window for age-structured populations of salamander larvae and paedomorphic adults. We determined body size limits on cannibalism in microcosms and then the consumptive and nonconsumptive (injuries, foraging and activity, diet, growth) effects on victims in mesocosms with seminatural levels of habitat complexity and alternative prey. We found that cannibalism by the largest size classes (paedomorphs and > or = age 3+ yr larvae) occurs mainly on young-of-the-year (YOY) victims. Surviving YOY and other small larvae had increased injuries, reduced activity levels, and reduced growth rates in the presence of cannibals. Data on YOY survival in an experiment in which we manipulated the density of paedomorphs combined with historical data on the number of cannibals in natural populations indicate that dominant cohorts of paedomorphs can cause observed recruitment failures. Dietary data indicate that ontogenetic shifts in diet should preclude strong intraspecific competition between YOY and cannibals in this species. Thus our results are consistent with previous empirical and theoretical work that suggests that recruitment regulation by cannibalism is most likely when YOY are vulnerable to cannibalism but have low dietary overlap with cannibals. Understanding the role of cannibalism in regulating recruitment in salamander populations is timely, given the widespread occurrences of amphibian decline. Previous studies have focused on extrinsic (including anthropogenic) factors that affect amphibian population dynamics, whereas the data presented here combined with long-term field observations suggest the potential for intrinsically driven population cycles.

Reinforcing abiotic and biotic time constraints facilitate the broad distribution of a generalist with fixed traits.

Many species are habitat specialists along environmental gradients as a result of contrasting selection pressures, but others maintain broad distributions along such gradients. Phenotypic plasticity explains the persistence of some generalists, but not the broad distributions of species with fixed traits. We combined comparative and experimental data to investigate the role of multiple selection pressures on the distribution of a cased caddisfly (Asynarchus nigriculus) across a pond permanence gradient in the Mexican Cut Nature Preserve, Elk Mountains, Colorado, USA. Rapid development in this species facilitates the exploitation of short-duration vernal pools. Comparative data document that slowly growing individuals die from desiccation, suggesting an ongoing selection for rapid development. Surprisingly, development is as fast or faster in long-duration, autumnal ponds where emergence occurs long before drying, and overlaps with the appearance of beetle (Dytiscus) predators. In field experiments we found that the last two instars of beetle larvae pose a significant mortality threat to Asynarchus, but that threat declines after caddisfly pupation. In natural populations, the caddisflies pupate and emerge just as large beetle instars appear in the ponds. Experimental manipulation of caddisfly size suggests that rapid development in autumnal ponds will both facilitate intraguild predation on other caddisflies and reduce Asynarchus cannibalism. Both types of caddisfly interactions should have a positive feedback effect on rapid development via a protein supplement to their detrital diet. All of these biotic time constraints should select for rapid Asynarchus development in autumnal habitats, despite relaxed drying time constraints. Asynarchus did not display flexible antipredator responses to beetles (no changes in activity rates, morphology, or development), suggesting that the traits that lead to rapid development are fixed, regardless of habitat type and presence of predators. We propose that different, but convergent, selection pressures across different habitat types have led to fixed specialized traits that enable a broad distribution along this environmental gradient. These selection pressures are dependent on the relative phenologies of interacting species and appear to trump the trade-offs between other types of physical and biotic constraints across habitats.

Predator defense along a permanence gradient: roles of case structure, behavior, and developmental phenology in caddisflies.

Species replacements along freshwater permanence gradients are well documented, but underlying mechanisms are poorly understood for most taxa. In subalpine wetlands in Colorado, the relative abundance of caddisfly larvae shifts from temporary to permanent basins. Predators on caddisflies also shift along this gradient; salamanders (Ambystoma tigrinum nebulosum) in permanent ponds are replaced by predaceous diving beetles (Dytiscus dauricus) in temporary habitats. We conducted laboratory and field experiments to determine the effectiveness of caddisfly cases in reducing vulnerability to these predators. We found that larvae of a temporary-habitat caddisfly (Asynarchus nigriculus) were the most vulnerable to salamanders. Two relatively invulnerable species (Limnephilus externus, L. picturatus) exhibited behaviors that reduced the likelihood of detection and attack, whereas the least vulnerable species (Agrypnia deflata) was frequently detected and attacked, but rarely captured because cases provided an effective refuge. Vulnerability to beetle predation was also affected by cases. The stout cases of L. externus larvae frequently deterred beetle larvae, whereas the tubular cases of the other species were relatively ineffective. Two of these vulnerable species (A. nigriculus and L. picturatus) often co-occur with beetles; thus, case construction alone is insufficient to explain patterns of caddisfly coexistence along the permanence gradient. One explanation for the coexistence of these two species with beetles is that they develop rapidly during early summer and pupate before beetle larvae become abundant. One species (L. picturatus) pupates by burying into soft substrates that serve as a refuge. The other (A. nigriculus) builds stone pupal cases, which in field experiments, more than doubles survival compared to organic pupal cases. The combined results of these experiments suggest that caddisfly distributions along permanence gradients depend on a suite of primary and secondary predator defenses that include larval and pupal case structure, predator-specific escape behaviors, and the phenology of larval development.