Jonathan H. Grabowski

REVISITING THE CLASSICS: CONSIDERING NONCONSUMPTIVE EFFECTS IN TEXTBOOK EXAMPLES OF PREDATOR-PREY INTERACTIONS

Predator effects on prey dynamics are conventionally studied by measuring changes in prey abundance attributed to consumption by predators. We revisit four classic examples of predator-prey systems often cited in textbooks and incorporate subsequent studies of nonconsumptive effects of predators (NCE), defined as changes in prey traits (e.g., behavior, growth, development) measured on an ecological time scale. Our review revealed that NCE were integral to explaining lynx-hare population dynamics in boreal forests, cascading effects of top predators in Wisconsin lakes, and cascading effects of killer whales and sea otters on kelp forests in nearshore marine habitats. The relative roles of consumption and NCE of wolves on moose and consequent indirect effects on plant communities of Isle Royale depended on climate oscillations. Nonconsumptive effects have not been explicitly tested to explain the link between planktonic alewives and the size structure of the zooplankton, nor have they been invoked to attribute keystone predator status in intertidal communities or elsewhere. We argue that both consumption and intimidation contribute to the total effects of keystone predators, and that characteristics of keystone consumers may differ from those of predators having predominantly NCE. Nonconsumptive effects are often considered as an afterthought to explain observations inconsistent with consumption-based theory. Consequently, NCE with the same sign as consumptive effects may be overlooked, even though they can affect the magnitude, rate, or scale of a prey response to predation and can have important management or conservation implications. Nonconsumptive effects may underlie other classic paradigms in ecology, such as delayed density dependence and predator-mediated prey coexistence. Revisiting classic studies enriches our understanding of predator-prey dynamics and provides compelling rationale for ramping up efforts to consider how NCE affect traditional predator-prey models based on consumption, and to compare the relative magnitude of consumptive and NCE of predators.

HABITAT COMPLEXITY DISRUPTS PREDATOR–PREY INTERACTIONS BUT NOT THE TROPHIC CASCADE ON OYSTER REEFS

Despite recognition of the significance of both food web interactions and habitat complexity in community dynamics, current ecological theory rarely couples these two processes. Experimental manipulations of the abundance of the two predators in an oyster-reef trophic cascade, and the structural complexity provided by reefs of living oysters, demonstrated that enhanced habitat complexity weakened the strengths of trophic interactions. The system of tri-trophic interactions included oyster toadfish (Opsanus tau) as the top predator that consumed the mud crab (Panopeus herbstii), which preys upon juvenile oysters (Crassostrea virginica). On reefs of low complexity, toadfish controlled mud crab abundances and indirectly determined the level of mortality of juvenile oysters. The indirect effects of toadfish on oysters emerged through their influence on how intensely mud crabs preyed on oysters. Augmentation of habitat complexity by substituting vertically oriented, living oysters for the flat shells of dead o...

Cascading of habitat degradation: Oyster reefs invaded by refugee fishes escaping stress

Mobile consumers have potential to cause a cascading of habitat degradation beyond the region that is directly stressed, by concentrating in refuges where they intensify biological interactions and can deplete prey resources. We tested this hypothesis on structurally complex, species-rich biogenic reefs created by the eastern oyster, Crassostrea virginica, in the Neuse River estuary, North Carolina, USA. We (1) sampled fishes and invertebrates on natural and restored reefs and on sand bottom to compare fish utilization of these different habitats and to characterize the trophic relations among large reef-associated fishes and benthic invertebrates, and (2) tested whether bottom-water hypoxia and fishery-caused degradation of reef habitat combine to induce mass emigration of fish that then modify community composition in refuges across an estuarine seascape. Experimentally restored oyster reefs of two heights (1 m tall “degraded” or 2 m tall “natural” reefs) were constructed at 3 and 6 m depths. We sampled...

Restoring oyster reefs to recover ecosystem services

This chapter discusses how to quantify the economic value of each of the ecosystem services provided by oyster reefs. The chapter also provides quantitative estimates of the value of some specific functions (i.e., oyster harvests, water quality improvements, and recreational and commercial fishery benefits) where data are available to compare the value of harvesting oysters in a traditional fishery to the monetary value of providing other oyster reef services. Placing oyster reefs in the greater context of the estuary requires landscape-scale data with simultaneous evaluation of each habitat across multiple trophic levels, which is difficult to obtain. However, larger-scale restoration efforts to assess the recovery of ecosystem services are currently being conducted in the Gulf of Mexico and in several estuaries along the East Coast of the United States. These studies will greatly enhance ones ability to develop more holistic economic models that account for spatial variability in the provision of ecosystem goods and services by oyster reefs.

HOW HABITAT SETTING INFLUENCES RESTORED OYSTER REEF COMMUNITIES

Integrating how habitat heterogeneity influences food web dynamics is critical to enhance our understanding of community structure. This study quantified resident (invertebrates) and transient (juvenile and piscivorous fish) fauna within restored intertidal oyster reefs and analogous control sites without reef habitat in each of three habitats (on the edge of salt marsh away from seagrass, on mudflats isolated from vegetated structures, and in between seagrass and salt marsh habitat). Reefs enhanced the abundance of resident invertebrates (e.g., polychaetes, nemerteans, epibenthic anemones, bivalves, and resident decapods) that comprise >90% of juvenile fish prey biomass. However, the increase in food availability due to reef presence did not affect abundance of juvenile fish in either of the vegetated habitats, suggesting that resources may not limit juvenile fish when restored in these habitats. Only mudflat reefs augmented juvenile fish abundances, most likely due to a combination of greater resource availability and relative isolation from functionally equivalent habitats. In addition, lower abundances of piscivorous fish in mudflat reefs relative to control areas likely contributed to this pattern. Thus, community structure and important ecosystem functions such as secondary production depend on the spatial configuration of surrounding habitats, in much the same way that species interactions can depend on their biotic and abiotic context.

Economic Valuation of Ecosystem Services Provided by Oyster Reefs

Valuation of ecosystem services can provide evidence of the importance of sustaining and enhancing those resources and the ecosystems that provide them. Long appreciated only as a commercial source of oysters, oyster reefs are now acknowledged for the other services they provide, such as enhancing water quality and stabilizing shorelines. We develop a framework to assess the value of these services. We conservatively estimate that the economic value of oyster reef services, excluding oyster harvesting, is between

FROM INDIVIDUALS TO ECOSYSTEM FUNCTION: TOWARD AN INTEGRATION OF EVOLUTIONARY AND ECOSYSTEM ECOLOGY

5500 and

Historical ecology with real numbers: past and present extent and biomass of an imperilled estuarine habitat

99,000 per hectare per year and that reefs recover their median restoration costs in 2–14 years. In contrast, when oyster reefs are subjected to destructive oyster harvesting, they do not recover the costs of restoration. Shoreline stabilization is the most valuable potential service, although this value varies greatly by reef location. Quantifying the economic values of ecosystem services provides guidance about when oyster reef restoration is a good use of funds.

HABITAT COMPLEXITY INFLUENCES CASCADING EFFECTS OF MULTIPLE PREDATORS

An important goal in ecology is developing general theory on how the species composition of ecosystems is related to ecosystem properties and functions. Progress on this front is limited partly because of the need to identify mechanisms controlling functions that are common to a wide range of ecosystem types. We propose that one general mechanism, rooted in the evolutionary ecology of all species, is adaptive foraging behavior in response to predation risk. To support our claim, we present two kinds of empirical evidence from plant-based and detritus-based food chains of terrestrial and aquatic ecosystems. The first kind comes from experiments that explicitly trace how adaptive foraging influences ecosystem properties and functions. The second kind comes from a synthesis of studies that individually examine complementary components of particular ecosystems that together provide an integrated perspective on the link between adaptive foraging and ecosystem function. We show that the indirect effects of predators on plant diversity, plant productivity, nutrient cycling, trophic transfer efficiencies, and energy flux caused by consumer foraging shifts in response to risk are qualitatively different from effects caused by reductions in prey density due to direct predation. We argue that a perspective of ecosystem function that considers effects of consumer behavior in response to predation risk will broaden our capacity to explain the range of outcomes and contingencies in trophic control of ecosystems. This perspective also provides an operational way to integrate evolutionary and ecosystem ecology, which is an important challenge in ecology.

PREDATOR‐AVOIDANCE BEHAVIOR EXTENDS TROPHIC CASCADES TO REFUGE HABITATS

Historic baselines are important in developing our understanding of ecosystems in the face of rapid global change. While a number of studies have sought to determine changes in extent of exploited habitats over historic timescales, few have quantified such changes prior to late twentieth century baselines. Here, we present, to our knowledge, the first ever large-scale quantitative assessment of the extent and biomass of marine habitat-forming species over a 100-year time frame. We examined records of wild native oyster abundance in the United States from a historic, yet already exploited, baseline between 1878 and 1935 (predominantly 1885–1915), and a current baseline between 1968 and 2010 (predominantly 2000–2010). We quantified the extent of oyster grounds in 39 estuaries historically and 51 estuaries from recent times. Data from 24 estuaries allowed comparison of historic to present extent and biomass. We found evidence for a 64 per cent decline in the spatial extent of oyster habitat and an 88 per cent decline in oyster biomass over time. The difference between these two numbers illustrates that current areal extent measures may be masking significant loss of habitat through degradation.