Blaine D. Griffen

Early warning signals of extinction in deteriorating environments

During the decline to extinction, animal populations may present dynamical phenomena not exhibited by robust populations. Some of these phenomena, such as the scaling of demographic variance, are related to small size whereas others result from density-dependent nonlinearities. Although understanding the causes of population extinction has been a central problem in theoretical biology for decades, the ability to anticipate extinction has remained elusive. Here we argue that the causes of a population’s decline are central to the predictability of its extinction. Specifically, environmental degradation may cause a tipping point in population dynamics, corresponding to a bifurcation in the underlying population growth equations, beyond which decline to extinction is almost certain. In such cases, imminent extinction will be signalled by critical slowing down (CSD). We conducted an experiment with replicate laboratory populations of Daphnia magna to test this hypothesis. We show that populations crossing a transcritical bifurcation, experimentally induced by the controlled decline in environmental conditions, show statistical signatures of CSD after the onset of environmental deterioration and before the critical transition. Populations in constant environments did not have these patterns. Four statistical indicators all showed evidence of the approaching bifurcation as early as 110 days (∼8 generations) before the transition occurred. Two composite indices improved predictability, and comparative analysis showed that early warning signals based solely on observations in deteriorating environments without reference populations for standardization were hampered by the presence of transient dynamics before the onset of deterioration, pointing to the importance of reliable baseline data before environmental deterioration begins. The universality of bifurcations in models of population dynamics suggests that this phenomenon should be general.

Detecting emergent effects of multiple predator species

When foraging together, multiple predator species that share a single prey often cause prey mortality that cannot be predicted based on knowledge of predation by each species separately. Modeling and managing the effects of multiple predator species depend on accurately assessing these combined effects. Two methods are currently used to experimentally examine combined predation by multiple predator species: the additive and substitutive experimental designs. I simultaneously employed both experimental designs to examine predation by two crab species on shared mussel prey. I show that the two methods yield results that disagree both quantitatively and qualitatively, leading to very different conclusions about the way that predator species combine to affect prey mortality. This discrepancy occurred because the two methods examine complimentary, but not interchangeable questions. I advocate using an experimental design that incorporates both additive and substitutive designs to achieve a more complete understanding of the combined effects of multiple predator species.

Partitioning mechanisms of Predator Interference in different Habitats

Prey are often consumed by multiple predator species. Predation rates on shared prey species measured in isolation often do not combine additively due to interference or facilitation among the predator species. Furthermore, the strength of predator interactions and resulting prey mortality may change with habitat type. We experimentally examined predation on amphipods in rock and algal habitats by two species of intertidal crabs, Hemigrapsus sanguineus (top predators) and Carcinus maenas (intermediate predators). Algae provided a safer habitat for amphipods when they were exposed to only a single predator species. When both predator species were present, mortality of amphipods was less than additive in both habitats. However, amphipod mortality was reduced more in rock than algal habitat because intermediate predators were less protected in rock habitat and were increasingly targeted by omnivorous top predators. We found that prey mortality in general was reduced by (1) altered foraging behavior of intermediate predators in the presence of top predators, (2) top predators switching to foraging on intermediate predators rather than shared prey, and (3) density reduction of intermediate predators. The relative importance of these three mechanisms was the same in both habitats; however, the magnitude of each was greater in rock habitat. Our study demonstrates that the strength of specific mechanisms of interference between top and intermediate predators can be quantified but cautions that these results may be habitat specific.

Inhibition between invasives: a newly introduced predator moderates the impacts of a previously established invasive predator

1. With continued globalization, species are being transported and introduced into novel habitats at an accelerating rate. Interactions between invasive species may provide important mechanisms that moderate their impacts on native species. 2. The European green crab Carcinus maenas is an aggressive predator that was introduced to the east coast of North America in the mid-1800 s and is capable of rapid consumption of bivalve prey. A newer invasive predator, the Asian shore crab Hemigrapsus sanguineus, was first discovered on the Atlantic coast in the 1980s, and now inhabits many of the same regions as C. maenas within the Gulf of Maine. Using a series of field and laboratory investigations, we examined the consequences of interactions between these predators. 3. Density patterns of these two species at different spatial scales are consistent with negative interactions. As a result of these interactions, C. maenas alters its diet to consume fewer mussels, its preferred prey, in the presence of H. sanguineus. Decreased mussel consumption in turn leads to lower growth rates for C. maenas, with potential detrimental effects on C. maenas populations. 4. Rather than an invasional meltdown, this study demonstrates that, within the Gulf of Maine, this new invasive predator can moderate the impacts of the older invasive predator.

Effects of habitat quality and size on extinction in experimental populations.

Stochastic population theory makes clear predictions about the effects of reproductive potential and carrying capacity on characteristic time-scales of extinction. At the same time, the effects of habitat size and quality on reproduction and regulation have been hotly debated. To trace the causal relationships among these factors, we looked at the effects of habitat size and quality on extinction time in experimental populations of Daphnia magna. Replicate model systems representative of a broad-spectrum consumer foraging on a continuously supplied resource were established under crossed treatments of habitat size (two levels) and habitat quality (three levels) and monitored until eventual extinction of all populations. Using statistically derived estimates of key parameters, we related experimental treatments to persistence time through their effect on carrying capacity and the population growth rate. We found that carrying capacity and the intrinsic rate of increase were each influenced similarly by habitat size and quality, and that carrying capacity and the intrinsic rate of increase were in turn both correlated with time to population extinction. We expected habitat quality to have a greater influence on extinction. However, owing to an unexpected effect of habitat size on reproductive potential, habitat size and quality were similarly important for population persistence. These results support the idea that improving the population growth rate or carrying capacity will reduce extinction risk and demonstrate that both are possible by improving habitat quality or increasing habitat size.

A review of extinction in experimental populations

1. Population extinction is a fundamental ecological process. Recent experimental work has begun to test the large body of theory that predicts how demographic, genetic and environmental factors influence extinction risk. We review empirical studies of extinction conducted under controlled laboratory conditions. Our synthesis highlights four findings. First, extinction theory largely considers individual, isolated populations. However, species interactions frequently altered or even reversed the influence of environmental factors on population extinction as compared to single-species conditions, highlighting the need to integrate community ecology into population theory. 2. While most single-species studies qualitatively agree with theoretical predictions, studies are needed that quantitatively compare observed and predicted extinction rates. A quantitative understanding of extinction processes is needed to further advance theory and to predict population extinction resulting from human activities. 3. Many stresses leading to population extinction can be assuaged by migration between subpopulations. However, too much migration increases synchrony between subpopulations and thus increases extinction risk. Research is needed to determine how to strike a balance that maximizes the benefit of migration. 4. Results from laboratory experiments often conflict with field studies. Understanding these inconsistencies is crucial for extending extinction theory to natural populations.

Community impacts of two invasive crabs: the interactive roles of density, prey recruitment, and indirect effects

Assessing the implications of species invasion for native communities requires determining whether effects of invaders are novel, or are redundant with effects of species that are already present. Using a pair of field experiments conducted over two successive years, we examined factors that influence community impacts of a recent predatory crab invader (Hemigrapsus sanguineus) and a previously established invasive crab (Carcinus maenas) on New England coasts. We demonstrate that effects of these species differ temporally with changes in the ambient prey community, and are influenced by density differences between the two species and by different strengths and types of indirect effects that each elicits. Our study highlights the importance of including bottom-up processes (i.e., prey recruitment) when examining the redundancy of consumers.

Trait‐mediated functional responses: predator behavioural type mediates prey consumption

The predator functional response (i.e. per capita consumption rate as a function of prey density) is central to our understanding of predator-prey population dynamics. This response is behavioural, depending on the rate of attack and time it takes to handle prey. Consistent behavioural differences among conspecific individuals, termed behavioural types, are a widespread feature of predator and prey populations but the effects of behavioural types on the functional response remain unexplored. We tested the effects of crab (Panopeus herbstii) behavioural type, specifically individual activity level, on the crab functional response to mussel (Brachidontes exustus) prey. We further tested whether the effects of activity level on the response are mediated by the presence of toadfish (Opsanus tau) predation threat in the form of waterborne chemical cues known to reduce crab activity level. The effects of crab activity level on the functional response were dependent on crab body size. Individual activity level increased the magnitude (i.e. slope and asymptote) of the type II functional response of small crabs, potentially through an increase in time spent foraging, but had no effect on the functional response of large crabs. Predation threat did not interact with activity level to influence mussel consumption, but independently reduced the slope of the type II functional response. Overall, this study demonstrates size-specific effects of a behavioural type on a predator-prey interaction, as well as a general pathway (modification of the functional response) by which the effects of individual behavioural types can scale up to influence predator-prey population dynamics.

Predicting diet and consumption rate differences between and within species using gut ecomorphology

1. Rapid environmental changes and pressing human needs to forecast the consequences of environmental change are increasingly driving ecology to become a predictive science. The need for effective prediction requires both the development of new tools and the refocusing of existing tools that may have previously been used primarily for purposes other than prediction. One such tool that historically has been more descriptive in nature is ecomorphology (the study of relationships between ecological roles and morphological adaptations of species and individuals). 2. Here, we examine relationships between diet and gut morphology for 15 species of brachyuran crabs, a group of pervasive and highly successful consumers for which trophic predictions would be highly valuable. 3. We show that patterns in crab stomach volume closely match some predictions of metabolic theory and demonstrate that individual diet differences and associated morphological variation reflect, at least in some instances, individual choice or diet specialization. 4. We then present examples of how stomach volume can be used to predict both the per cent herbivory of brachyuran crabs and the relative consumption rates of individual crabs.

Influence of predator density on nonindependent effects of multiple predator species

Interactions between multiple predator species are frequent in natural communities and can have important implications for shared prey survival. Predator density may be an important component of these interactions between predator species, as the frequency of interactions between species is largely determined by species density. Here we experimentally examine the importance of predator density for interactions between predator species and subsequent impacts on prey. We show that aggressive interactions between the predatory shore crabs Carcinus maenas and Hemigrapsus sanguineus increased with predator density, yet did not increase as fast as negative interactions between conspecifics. At low density, interactions between conspecific and heterospecific predators had similar inhibitory impacts on predator function, whereas conspecific interference was greater than interference from heterospecifics at high predator density. Thus the impact of conspecific interference at high predator density was sufficient in itself that interactions with a second predator species had no additional impact on per capita predation. Spatial and temporal variability in predator density is a ubiquitous characteristic of natural systems that should be considered in studies of multiple predator species.