Non-consumptive predator effects in a pelagic community

Food webs are traditionally studied in terms of trophic relationships, but species interactions are much more complex than 'what eats what?'. For example,

predators may induce changes in prey behavior, which can affect the interaction strength of the reacting prey species with other species in the food web. Such interaction modifications are called 'non-consumptive effects' because they occur without consumption of the prey species. In Lake Michigan, the invasive predatory cladoceran Bythotrephes has been credited with the loss and reduction of multiple zooplankton species. This loss of zooplankton has led to concerns about the indirect effects of Bythotrephes on fish, which at early life-history stages rely on zooplankton as a food resource. Bythotrephes is known to be a voracious planktivore and so may have potentially strong consumptive effects on zooplankton; but it also induces strong changes in zooplankton behavior opening up the possibility of strong non-consumptive effects on zooplankton and the species they interact with. For my post-doctoral research with Scott Peacor at Michigan State University I am combining laboratory studies, field monitoring and modeling to answer the question 'Are non-consumptive effects by Bythotrephes on zooplankton important in Lake Michigan?'  Our goal is to provide information we can use to help explain the effect of Bythotrephes on the Lake Michigan food web, alert ecologists to the potential importance of non-consumptive effects in pelagic ecosystems, and develop methods to incorporate NCEs into food web models.


The role of behavior in the expression of predator-induced morphological defenses

Predator-induced morphological defenses (PIMDs) are used as text-book examples of adaptive phenotypic plasticity. It is commonly assumed that PIMDs are an active physiological response to cues from predators, but recent studies of two classical examples of inducible defenses have shown that these defenses are instead by-products of prey behavioral responses to predators. The frequently observed association between predator-induced activity reduction and morphological defense production in prey, suggests that this phenomenon may be common. Frank Johansson (Umea University) and I have reviewed published studies of PMIDs with the goal of determining where this mechanism is likely to be operating. Based on experimental studies of fish and snails and our review of the literature we have developed two alternative mechanistic models for behaviorally-mediated morphological defenses; the growth limitation model (based on studies of amphibians and snails) and the energy-saving model (based on studies of fish). The models differ in their pathways but predict the same outcome: predators induce a reduction in prey activity, which subsequently affects prey growth and morphological defense production.

Predator-induced behavioral and morphological plasticity in carnivorous intertidal gastropods, Nucella spp.

Predator-induced changes in the defensive traits of prey organisms are widespread
 in nature and have important ecological consequences. Much of ourunderstanding of inducible defense comes from studies focused on single trait responses to single predators. Consequently, we have little understanding of how prey express multivariate phenotypes in the presence of multiple predators. My dissertation explored the ecology and evolution of inducible defenses, using marine snails in the genus Nucella as a model system. Specifically I investigated predator-induced behavior and morphology in three sympatric intertidal snails, (Nucella spp.) in response to the presence of two predators with different attack modes (crab and seastar). My objectives were to determine: 1) whether snails exhibit adaptive responses to different types of predation risk, 2) how prey respond to combined predators, 3) what mechanisms underlie inducible morphological defenses, and 4) whether snails in the genus Nucella exhibit species- and population-specific responses to predators. I found that inducible responses to a given predator were dependent on the predator’s diet and prey prioritized their response to the most dangerous predator when exposed to multiple predators simultaneously. I also found that consideration of single traits alone can lead to erroneous interpretations about how prey respond to combined predators. Growth rates were slowed in the presence of predators, indicating that snails are paying a cost for defending themselves. However, reduced feeding activity rather than an active physiological response appears to be the mechanism underlying predator-induced shell thickening, suggesting that the cost is associated with lost feeding opportunity rather than the production of structural defenses.  Finally, all species and populations tested altered their feeding behavior and shell morphology in the presence of predators, but exhibited species- and population-specific differences that can be linked to their distribution across a predation gradient.

Biological invasion of marine reserves by aquatic nuisance species.

The non-native oyster  Crassostrea gigas has invaded marine reserves in the San Juan Islands, potentially undermining the utility of these sites as

conservation tools. To better understand the source of these invasions I, in collaboration with my dissertation advisor, Dianna Padilla and Terrie Klinger of the University of Washington conducted population monitoring and genetic analysis to determine genetic similarity and differences between invasive and farmed populations of C. gigas. Microsatellite DNA markers revealed genetic differentiation between invasive and farmed populations, suggesting that the invading oysters are not escapees from local farming operations. Additional genetic analyses will determine whether the sources of invasion are remote farming operations or whether other factors such as genetic drift, natural selection or hybridization have influenced the genetic makeup of invasive populations.

Phenotypic plasticity in feeding structures, food preferences and dispersal behavior.

In addressing how organisms respond to environmental cues with plastic traits, the primary focus has been on predator-induced defenses. Less attention has been paid to inducible offenses; traits that increase the feeding abilities of an individual. In collaboration with my dissertation advisor Dianna Padilla, I examined how snails in the genus Lacuna alter feeding structures and dispersal to determine the functional relationships between plastic morphological and behavioral offenses. We found that differences in inducible offensive morphology (i.e., feeding structures) and experience (i.e. recent feeding history) affect a snails behavioral (i.e. dispersal) decisions. Snails can stay in a habitat, keeping their feeding structures matched to the food environment, or they can disperse from environment-phenotype mismatches, presumably to find a better match elsewhere. Thus the decision to disperse depends the match between the snails' phenotype and environment. Using dispersal to better match a morphological phenotype to the environment suggests that flexible behavior can enhance the adaptive value of inducible offensive morphology.                                                                                   

Effects of the Asian shore crab,  Hemigrapsus sanguineus in southern New England and Long Island Sound.

My master's thesis examined the feeding preferences of the invasive shore crab  Hemigrapsus sanguineus in southeastern New England. Thought to be

primarily herbivorous, these crabs feed voraciously on mussels on rocky shores. Recently H. sanguineus has invaded salt marshes in Long Island Sound. In collaboration with Bengt Allen at Cal State Long Beach, J. Matthew Hoch at Florida International and Sarah Gray at Stony Brook University, I examined the effects of this crab, and the European green crab, Carcinus maenas, on the growth, survival and inducible shell-thickening of the ribbed mussel  Guekensia demissa, an important foundation species in mid-Atlantic marshes. Both crabs readily consume small mussels, but only green crabs induce shell thickening in Guekensia. This is likely due to differences in the invasion histories of the two crabs - green crabs have been in the region for over 100 years, while Hemigrapsus has only invaded the marsh within the last decade. The mussel's failure to respond to waterborne cues from Hemigrapsus may lead to increased predation risk from this relatively new invader.