Hamish S. Greig

Warming shifts top-down and bottom-up control of pond food web structure and function

The effects of global and local environmental changes are transmitted through networks of interacting organisms to shape the structure of communities and the dynamics of ecosystems. We tested the impact of elevated temperature on the top-down and bottom-up forces structuring experimental freshwater pond food webs in western Canada over 16 months. Experimental warming was crossed with treatments manipulating the presence of planktivorous fish and eutrophication through enhanced nutrient supply. We found that higher temperatures produced top-heavy food webs with lower biomass of benthic and pelagic producers, equivalent biomass of zooplankton, zoobenthos and pelagic bacteria, and more pelagic viruses. Eutrophication increased the biomass of all organisms studied, while fish had cascading positive effects on periphyton, phytoplankton and bacteria, and reduced biomass of invertebrates. Surprisingly, virus biomass was reduced in the presence of fish, suggesting the possibility for complex mechanisms of top-down control of the lytic cycle. Warming reduced the effects of eutrophication on periphyton, and magnified the already strong effects of fish on phytoplankton and bacteria. Warming, fish and nutrients all increased whole-system rates of net production despite their distinct impacts on the distribution of biomass between producers and consumers, plankton and benthos, and microbes and macrobes. Our results indicate that warming exerts a host of indirect effects on aquatic food webs mediated through shifts in the magnitudes of top-down and bottom-up forcing.

Warming modifies trophic cascades and eutrophication in experimental freshwater communities

Climate warming is occurring in concert with other anthropogenic changes to ecosystems. However, it is unknown whether and how warming alters the importance of top-down vs. bottom-up control over community productivity and variability. We performed a 16-month factorial experimental manipulation of warming, nutrient enrichment, and predator presence in replicated freshwater pond mesocosms to test their independent and interactive impacts. Warming strengthened trophic cascades from fish to primary producers, and it decreased the impact of eutrophication on the mean and temporal variation of phytoplankton biomass. These impacts varied seasonally, with higher temperatures leading to stronger trophic cascades in winter and weaker algae blooms under eutrophication in summer. Our results suggest that higher temperatures may shift the control of primary production in freshwater ponds toward stronger top-down and weaker bottom-up effects. The dampened temporal variability of algal biomass under eutrophication at higher temperatures suggests that warming may stabilize some ecosystem processes.

A bioenergetic framework for the temperature dependence of trophic interactions

Changing temperature can substantially shift ecological communities by altering the strength and stability of trophic interactions. Because many ecological rates are constrained by temperature, new approaches are required to understand how simultaneous changes in multiple rates alter the relative performance of species and their trophic interactions. We develop an energetic approach to identify the relationship between biomass fluxes and standing biomass across trophic levels. Our approach links ecological rates and trophic dynamics to measure temperature-dependent changes to the strength of trophic interactions and determine how these changes alter food web stability. It accomplishes this by using biomass as a common energetic currency and isolating three temperature-dependent processes that are common to all consumer-resource interactions: biomass accumulation of the resource, resource consumption and consumer mortality. Using this framework, we clarify when and how temperature alters consumer to resource biomass ratios, equilibrium resilience, consumer variability, extinction risk and transient vs. equilibrium dynamics. Finally, we characterise key asymmetries in species responses to temperature that produce these distinct dynamic behaviours and identify when they are likely to emerge. Overall, our framework provides a mechanistic and more unified understanding of the temperature dependence of trophic dynamics in terms of ecological rates, biomass ratios and stability.

Absence of species replacements between permanent and temporary lentic communities in New Zealand

Abstract The species composition of lentic communities often shifts along hydroperiod gradients, in part because temporary-habitat specialists replace closely related permanent-habitat specialists. These replacements reflect tradeoffs between traits that facilitate coexistence with permanent-habitat predators and those that prevent desiccation. The evidence for species replacements and the underlying tradeoffs is considerable in North America, but few studies have explored this pattern in other regions. We compared benthic communities in permanent and temporary habitats on the South Island of New Zealand. Ordination across 58 sites showed that community composition was distinctly different between the 2 types of habitats. Assemblages in permanent habitats had >2× the number of species as those in temporary habitats. We found little evidence for temporary-habitat specialists; i.e., species in temporary communities were a nested subset of those in permanent communities. Quantitative sampling at 12 intensively studied sites revealed that chironomids, water bugs, beetles, and crustaceans accounted for 90% of the biomass in temporary, but only 14% of the biomass in permanent habitats, which were dominated by mollusks, annelids, caddisflies, and odonates. Damselflies, dragonflies, caddisflies, and several other large-bodied taxa common in permanent habitats were absent from most temporary habitats. We propose 2 explanations for the absence of species replacements in these groups in the New Zealand habitats that we studied. First, drying is unpredictable within and between years, perhaps precluding the evolution of temporary-habitat specialization. Second, fish predation on benthic invertebrates, a driver for phylogenetic diversification in North America, appears to be comparatively weak in New Zealand. Comparative studies across a range of climates and faunas will be needed to identify the ecological and phylogenetic contexts that favor evolution of generalists vs specialists along permanence gradients.

The Body Size Dependence of Trophic Cascades

Trophic cascades are indirect positive effects of predators on resources via control of intermediate consumers. Larger-bodied predators appear to induce stronger trophic cascades (a greater rebound of resource density toward carrying capacity), but how this happens is unknown because we lack a clear depiction of how the strength of trophic cascades is determined. Using consumer resource models, we first show that the strength of a trophic cascade has an upper limit set by the interaction strength between the basal trophic group and its consumer and that this limit is approached as the interaction strength between the consumer and its predator increases. We then express the strength of a trophic cascade explicitly in terms of predator body size and use two independent parameter sets to calculate how the strength of a trophic cascade depends on predator size. Both parameter sets predict a positive effect of predator size on the strength of a trophic cascade, driven mostly by the body size dependence of the interaction strength between the first two trophic levels. Our results support previous empirical findings and suggest that the loss of larger predators will have greater consequences on trophic control and biomass structure in food webs than the loss of smaller predators.

Heavy metals: confounding factors in the response of New Zealand freshwater fish assemblages to natural and anthropogenic acidity

Acidification of freshwaters is a global phenomenon, occurring both through natural leaching of organic acids and through human activities from industrial emissions and mining. The West Coast of the South Island, New Zealand, has both naturally acidic and acid mine drainage (AMD) streams enabling us to investigate the response of fish communities to a gradient of acidity in the presence and absence of additional stressors such as elevated concentrations of heavy metals. We surveyed a total of 42 streams ranging from highly acidic (pH 3.1) and high in heavy metals (10 mg L(-)(1) Fe; 38 mg L(-)(1) Al) to circum-neutral (pH 8.1) and low in metals (0.02 mg L(-)(1) Fe; 0.05 mg L(-)(1) Al). Marked differences in pH and metal tolerances were observed among the 15 species that we recorded. Five Galaxias species, Anguilla dieffenbachii and Anguillaaustralis were found in more acidic waters (pH<5), while bluegill bullies (Gobiomorphus hubbsi) and torrentfish (Cheimarrichthys fosteri) were least tolerant of low pH (minimum pH 6.2 and 5.5, respectively). Surprisingly, the strongest physicochemical predictor of fish diversity, density and biomass was dissolved metal concentrations (Fe, Al, Zn, Mn and Ni) rather than pH. No fish were detected in streams with dissolved metal concentrations >2.7 mg L(-)(1) and nine taxa were only found in streams with metal concentrations <1 mg L(-)(1). The importance of heavy metals as critical drivers of fish communities has not been previously reported in New Zealand, although the mechanism of the metal effects warrants further study. Our findings indicate that any remediation of AMD streams which seeks to enable fish recolonisation should aim to improve water quality by raising pH above approximately 4.5 and reducing concentrations of dissolved Al and Fe to <1.0 mg L(-)(1).

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.

Vertical stratification in the spatial distribution of the beech scale insect (Ultracoelostoma assimile) in Nothofagus tree canopies in New Zealand

Abstract.  1. The degree of infestation by New Zealand sooty beech scale insects (Ultracoelostoma assimile, Homoptera: Margarodidae) varies dramatically among adjacent southern beech trees (Nothofagus spp., Fagaceae), but has previously been assumed to be uniformly or randomly distributed within individual host trees. In this study, a full‐census survey was conducted from ground level to canopy level on 14 naturally occurring, canopy‐dominant red beech (Nothofagus fusca) trees (size range 38.7–107.6 cm diameter at breast height) to determine the degree of within‐tree heterogeneity in herbivore density.

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.