Delbert L. Smee

The Sensory Ecology of Nonconsumptive Predator Effects

Nonconsumptive effects (NCEs) have been shown to occur in numerous systems and are regarded as important mechanisms by which predation structures natural communities. Sensory ecology—that is, the processes governing the production, propagation, and masking of cues by ambient noise—provides insights into the strength of NCEs as functions of the environment and modes of information transfer. We discuss how properties of predators are used by prey to encode threat, how the environment affects cue propagation, and the role of single sensory processes versus multimodal sensory processes. We discuss why the present body of literature documents the potential for strong NCEs but does not allow us to easily determine how this potential is expressed in nature or what factors or environments produce strong versus weak NCEs. Many of these difficulties stem from a body of literature in which certain sensory environments and modalities may be disproportionately represented and in which experimental methodologies are designed to show the existence of NCEs. We present a general framework for examining NCEs to identify the factors controlling the number of prey that respond to predator cues and discuss how the properties of predators, prey, and the environment may determine prey perceptive range and the duration and frequency of cue production. We suggest how understanding these relationships provides a schema for determining where, when, why, and how NCEs are important in producing direct and cascading effects in natural communities.

Alteration of sensory abilities regulates the spatial scale of nonlethal predator effects

Many studies have shown that nonlethal predator effects such as trait-mediated interactions (TMIs) can have significant impacts on the structure and function of communities, but the role that environmental conditions play in modulating the scale and magnitude of these effects has not been carefully investigated. TMIs occur when prey exhibit behavioral or physiological responses to predators and may be more prevalent when abiotic conditions increase prey reactions to consumers. The purpose of this study was to determine if turbulence would alter the distance over which prey in aquatic systems respond to chemical cues emitted by predators in nature, thus changing the scales over which nonlethal predator effects occur. Using hard clams and blue crabs as a model predator–prey system, we investigated the effects of turbulence on clam reactive distance to predatory blue crabs in the field. Results suggest that turbulence diminishes clam reactions to predators and that the environmental context must be considered when predicting the extent of indirect predator effects in natural systems.

Green crab (Carcinus maenas) foraging efficiency reduced by fast flows.

Predators can strongly influence prey populations and the structure and function of ecosystems, but these effects can be modified by environmental stress. For example, fluid velocity and turbulence can alter the impact of predators by limiting their environmental range and altering their foraging ability. We investigated how hydrodynamics affected the foraging behavior of the green crab (Carcinus maenas), which is invading marine habitats throughout the world. High flow velocities are known to reduce green crab predation rates and our study sought to identify the mechanisms by which flow affects green crabs. We performed a series of experiments with green crabs to determine: 1) if their ability to find prey was altered by flow in the field, 2) how flow velocity influenced their foraging efficiency, and 3) how flow velocity affected their handling time of prey. In a field study, we caught significantly fewer crabs in baited traps at sites with fast versus slow flows even though crabs were more abundant in high flow areas. This finding suggests that higher velocity flows impair the ability of green crabs to locate prey. In laboratory flume assays, green crabs foraged less efficiently when flow velocity was increased. Moreover, green crabs required significantly more time to consume prey in high velocity flows. Our data indicate that flow can impose significant chemosensory and physical constraints on green crabs. Hence, hydrodynamics may strongly influence the role that green crabs and other predators play in rocky intertidal communities.

Turbidity interferes with foraging success of visual but not chemosensory predators

Predation can significantly affect prey populations and communities, but predator effects can be attenuated when abiotic conditions interfere with foraging activities. In estuarine communities, turbidity can affect species richness and abundance and is changing in many areas because of coastal development. Many fish species are less efficient foragers in turbid waters, and previous research revealed that in elevated turbidity, fish are less abundant whereas crabs and shrimp are more abundant. We hypothesized that turbidity altered predatory interactions in estuaries by interfering with visually-foraging predators and prey but not with organisms relying on chemoreception. We measured the effects of turbidity on the predation rates of two model predators: a visual predator (pinfish, Lagodon rhomboides) and a chemosensory predator (blue crabs, Callinectes sapidus) in clear and turbid water (0 and ∼100 nephelometric turbidity units). Feeding assays were conducted with two prey items, mud crabs (Panopeus spp.) that rely heavily on chemoreception to detect predators, and brown shrimp (Farfantepenaus aztecus) that use both chemical and visual cues for predator detection. Because turbidity reduced pinfish foraging on both mud crabs and shrimp, the changes in predation rates are likely driven by turbidity attenuating fish foraging ability and not by affecting prey vulnerability to fish consumers. Blue crab foraging was unaffected by turbidity, and blue crabs were able to successfully consume nearly all mud crab and shrimp prey. Turbidity can influence predator–prey interactions by reducing the feeding efficiency of visual predators, providing a competitive advantage to chemosensory predators, and altering top-down control in food webs.

Changes in seagrass species composition in northwestern Gulf of Mexico estuaries: effects on associated seagrass fauna.

The objective of this study was to measure the communities associated with different seagrass species to predict how shifts in seagrass species composition may affect associated fauna. In the northwestern Gulf of Mexico, coverage of the historically dominant shoal grass (Halodule wrightii) is decreasing, while coverage of manatee grass (Syringodium filiforme) and turtle grass (Thalassia testudinum) is increasing. We conducted a survey of fishes, crabs, and shrimp in monospecific beds of shoal, manatee, and turtle grass habitats of South Texas, USA to assess how changes in sea grass species composition would affect associated fauna. We measured seagrass parameters including shoot density, above ground biomass, epiphyte type, and epiphyte abundance to investigate relationships between faunal abundance and these seagrass parameters. We observed significant differences in communities among three seagrass species, even though these organisms are highly motile and could easily travel among the different seagrasses. Results showed species specific relationships among several different characteristics of the seagrass community and individual species abundance. More work is needed to discern the drivers of the complex relationships between individual seagrass species and their associated fauna.

Eastern Oysters Crassostrea virginica Produce Plastic Morphological Defenses in Response to Crab Predators Despite Resource Limitation

Many prey react to predation risk by altering their phenotype to reduce their chances of being consumed but incur reductions in growth and fecundity when reacting to predators. To determine when to produce defenses, prey collect information and evaluate the costs and benefits of defense induction. Resource availability can affect prey ability and willingness to incur defense costs. When resources are scarce, defenses may suffer disproportionate decreases in energy allocation if defenses would further reduce prey access to resources or if resources are needed to maintain metabolic functions. We tested the effects of predation risk and resource availability on plastic defenses in eastern oysters Crassostrea virginica and present novel findings that oysters continued to produce defended shells in response to predators when resources were limited, even though they grew smaller, lighter shells when deprived of food in control conditions. Predation risk affected all three tested shell metrics (area, weight, and strength), but food availability did not. Although low food levels often limit expression of predator defenses, predator cues caused oysters to build shells that were larger and heavier, with a similar trend for shell strength, in treatments with both low and high food levels, suggesting that predation is an important pressure in this system. The differences between predator and control treatments were greater under conditions of low food availability, and thus, resource availability may influence interpretations of plastic responses to predators.

Predatory blue crabs induce stronger nonconsumptive effects in eastern oysters Crassostrea virginica than scavenging blue crabs

By influencing critical prey traits such as foraging or habitat selection, predators can affect entire ecosystems, but the nature of cues that trigger prey reactions to predators are not well understood. Predators may scavenge to supplement their energetic needs and scavenging frequency may vary among individuals within a species due to preferences and prey availability. Yet prey reactions to consumers that are primarily scavengers versus those that are active foragers have not been investigated, even though variation in prey reactions to scavengers or predators might influence cascading nonconsumptive effects in food webs. Oysters Crassostrea virginica react to crab predators by growing stronger shells. We exposed oysters to exudates from crabs fed live oysters or fed aged oyster tissue to simulate scavenging, and to controls without crab cues. Oysters grew stronger shells when exposed to either crab exudate, but their shells were significantly stronger when crabs were fed live oysters. The stronger response to predators than scavengers could be due to inherent differences in diet cues representative of reduced risk in the presence of scavengers or to degradation of conspecific alarm cues in aged treatments, which may mask risk from potential predators subsisting by scavenging.

Investigating oyster shell thickness and strength using three imaging modalities: hyperspectral imaging, thermal imaging and digital photography

A comparative study of three imaging technologies has been conducted to nondestructively assess the thickness and strength of oyster shells grown in various environmental conditions. Oyster shell thickness and strength are expected to be dependent on the harshness of the oysters environment as well as other factors. Oysters have been grown in environments with and without predators, and within and out of tidal zones. Hyperspectral imaging has been used to detect possible differences in hyperspectral properties among oyster shells from each of the four environments. Thermal Imaging has been utilized to identify hot spots in the shells based on the principles of heat capacitance, indicating density or thickness of the shells. Finally, a visible-range digital photographic camera has been used to obtain digital images. The three technologies are compared to evaluate the effectiveness of each technology in identifying oyster shell thickness and strength. Although oyster shell thickness and strength are related, they may not be exactly correlated. The local thickness of the oyster shells have been measured with a micro caliper, and shells broken with a crush tester to establish a baseline and ground truth for average shell thickness and shell strength, respectively. The preliminary results from the three methods demonstrate that thermal imaging correlates the best with the invasive strength test results and weight measurements. Using hyperspectral data and principal component analysis, classification of the four oyster shell groups were achieved. Visible-range images mainly provided size, shape, color and texture information.