Recognising one’s enemies: a functional approach to risk assessment by prey

Little has been done to compare the relative importance of various mechanisms through which prey assess the potential risk from natural enemies. We used predator-naive spider mites (Tetranychus urticae, Tetranychidae) to (1) compare the responses of prey to chemical cues from enemy and non-enemy species and (2) investigate the source of these cues. In the laboratory, we observed the distribution of T. urticae in response to cues from nine mite species, including (1) predators of spider mites, (2) predators/parasites of other animals, and (3) fungivores/pollen-feeders. When given a choice over 24 h, spider mites foraged and oviposited in fewer numbers on leaf discs that were previously exposed to predatory or parasitic mites (including species incapable of attacking spider mites) than on clean leaf discs (unexposed to mites). Interestingly, previous exposure of leaf arenas to fungivores and pollen-feeders had no significant effect on spider mite distribution. We then observed the response of T. urticae to cues from two species of predator that had been reared on a diet of either spider mites or pollen. T. urticae showed stronger avoidance of leaf discs that were previously exposed to spider-mite-fed predators than of discs exposed to pollen-fed predators. Nevertheless, for one predator species (Amblyseius andersoni), T. urticae still preferred to forage and oviposit on clean (unexposed) discs than on discs exposed to pollen-fed predators. Protein-derived metabolic wastes of predatory or parasitic mites may provide a general cue about potential predation risk for T. urticae. However, T. urticae also avoided areas exposed to pollen-fed predators, suggesting there may be other sources of enemy recognition by the spider mites. We discuss the ecological and evolutionary mechanisms that may influence the scope of information through which animals assess predation risk. Received: 11 January 1999 / Received in revised form: 25 October 1999 / Accepted: 20 November 1999     

Increasing enemy biodiversity strengthens herbivore suppression on two plant species

Concern over biodiversity loss, especially at higher trophic levels, has led to a surge in studies investigating how changes in natural enemy diversity affect community and ecosystem functioning. These studies have found that increasing enemy diversity can strengthen, weaken, and not affect prey suppression, demonstrating that multi-enemy effects on prey are context-dependent. Here we ask how one factor, plant species identity, influences multi-enemy effects on prey. We focused on two plant species of agricultural importance, potato (Solanum tuberosum), and collards (Brassica oleracea L.). These species share a common herbivorous pest, the green peach aphid (Myzus persicae), but vary in structural and chemical traits that affect aphid reproductive rates and which may also influence inter-enemy interactions. In a large-scale field experiment, overall prey exploitation varied dramatically among the plant species, with enemies reducing aphid populations by approximately 94% on potatoes and approximately 62% on collards. Increasing enemy diversity similarly strengthened aphid suppression on both plants, however, and there was no evidence that plant species identity significantly altered the relationship between enemy diversity and prey suppression. Microcosm experiments suggested that, on both collards and potatoes, intraspecific competition among natural enemies exceeded interspecific competition. Enemy species showed consistent and significant differences in where they foraged on the plants, and enemies in the low-diversity treatment tended to spend less time foraging than enemies in the high-diversity treatment. These data suggest that increasing enemy diversity may strengthen aphid suppression because interspecific differences in where enemies forage on the plant allow for greater resource partitioning. Further, these functional benefits of diversity appear to be robust to changes in plant species identity.     

Cooperative web sharing against predators promotes group living in spider mites

I examined spider mite cooperative web sharing against predation as a factor promoting group living. Tetranychus urticae and Tetranychus kanzawai infest leaf surfaces under webs made of silk threads. Experimental observation of predation by the predatory mite Euseius sojaensis on spider mites of different group sizes revealed that fewer spider mites were preyed upon when the web-building period before the attack was prolonged, suggesting that established webs help protect spider mites. Moreover, per capita predation on spider mites was diluted in larger groups. This was not due to predator satiation but seemingly because webs had been completed while the initial prey was consumed. Spider mites lived more closely together in the presence of a predator, showing that the degree of group living is facultative. In the presence of a preceding spider mite with an established web, a newcomer spider mite gain protection by taking residence in the established webs; sharing the web was not disadvantageous for the preceding mite. The proportion of individuals preyed upon did not differ between preceding and newcomer mites, suggesting that there was no interference against the latter. These interactions were consistent between heterospecific spider mites. Because there was no detectable indirect interaction between mites sharing fresh webs, cooperative web sharing seemed to be a major force promoting group living in the spider mites. Moreover, the distances between spider mites did not differ between heterospecific and conspecific groups, demonstrating that mites living together do not distinguish between species; hence, heterospecific mites may cooperate and live together in the same manner as conspecifics.     

The disruption of an ant-aphid mutualism increases the effects of birds on pine herbivores

Predators affect herbivores directly and indirectly, by consumptive and nonconsumptive effects, and the combined influence of multiple predators is shaped by interactions among predators. I documented the individual and combined effects of birds (chickadees, nuthatches, warblers) and ants (Formica podzolica) on arthropods residing in pine (Pinus ponderosa) canopies in a factorial field experiment. Birds and ants removed herbivores but simultaneously benefited them by removing predatory arthropods. Birds and ants had net negative and positive effects, respectively, on the abundance of herbivore prey, supporting the notion that vertebrate predators have stronger negative effects on herbivores than do arthropod predators. Aphids (ant-tended and untended species) constituted three-quarters of herbivore biomass. The effect of birds on ant-tended aphids was twice that on untended aphid species or tended aphid species without ants. This was not due to there being more ant-tended aphids for birds to prey on; tended and untended aphid species were in similar abundances in the absence of birds. Instead, the effects of birds were strengthened by attributes of the mutualism that rendered tended aphids susceptible to predation. These dynamics led to nonadditive effects of birds and ants: birds only reduced tended aphid species and total herbivore abundances on trees with ants, while ants only increased tended aphid species and total herbivore abundances in the absence of birds. Consequently, top predators in this system only influenced total herbivore abundance when they disrupted an ant-aphid mutualism.     

Multiple plant exploiters on a shared host: testing for nonadditive effects on plant performance.

The combined impact of multiple plant parasites on plant performance can either be additive (the total damage equals the sum of the individual effects) or nonadditive (synergistic or antagonistic damage). Two statistical models are available for testing the independent (=additive) effects of two factors. Here we suggest that the natural history of the plant-parasite system should motivate the choice of a statistical model to test for additivity. Using in-field, manipulative experiments, we examined the interactions between the herbivorous mite Calacarus flagelliseta Fletchmann, De Moraes and Barbosa (Acari: Eriophyidae), the fungal pathogen Oidium caricae F. Noack (a powdery mildew), and their host plant Carica papaya L. in Hawaii. First, we found that herbivorous mites had a moderate negative effect on powdery mildew: when mites were absent, powdery mildew colonies were larger and more numerous. Second, we showed that each plant parasite, when evaluated alone, significantly reduced several measures of plant performance. Third, we found that the combined impact of mites and mildew on plant performance is mostly additive and, for a few variables, less than additive. Finally, we explored compensatory responses and found no evidence for nonlinearities in the relationship between plant performance and cumulative parasite impact. Plants are almost universally subject to attack by multiple herbivores and pathogens; thus a deeper understanding of how multiple plant parasites shape each other's population dynamics and plant performance is essential to understanding plant-parasite interactions.     

An overlooked side effect of nest-scattering behavior to decrease predation risk (Acari: Tetranychidae,Stigmaeidae)

The number of nests containing egg masses a female makes over her lifetime and the pattern of scattering nests vary among species in a genus of nest-weaving spider mites (Stigmaeopsis). We hypothesized that the scattered nests of small nest builders have a previously overlooked indirect effect in that the void nests created after predation take on a new role as hindering devices that effectively decrease predator searching efficiency. First, we demonstrated that the experimental design used in this study is a good reflection of the nest distribution pattern of Stigmaeopsis takahashii (an intermediate-sized nest builder) in the field. Using this species as a model, we tested how different nest-scattering patterns affect the predator to examine how scattering may indirectly provide an anti-predation strategy by increasing a predators searching time. Next, we observed how artificially arranged void nests disturb predatory behavior in both starved and fully fed predator females and showed that void nests have a strong hindering effect on predators. Thus, we concluded that the nesting behavior of this mite species not only has anti-predator effects but must also have a stabilizing effect on predator–prey interaction systems at the population level.     

Do top-down or bottom-up forces determine Stephanitis pyrioides abundance in urban landscapes?

This study examined the influence of habitat structural complexity on the collective effects of top-down and bottom-up forces on herbivore abundance in urban landscapes. The persistence and varying complexity of urban landscapes set them apart from ephemeral agroecosystems and natural habitats where the majority of studies have been conducted. Using surveys and manipulative experiments. We explicitly tested the effect of natural enemies (enemies hypothesis), host plant quality, and herbivore movement on the abundance of the specialist insect herbivore, Stephanitis pyrioides, in landscapes of varying structural complexity. This herbivore was extremely abundant in simple landscapes and rare in complex ones. Natural enemies were the major force influencing abundance of S. pyrioides across habitat types. Generalist predators, particularly the spider Anyphaena celer, were more abundant in complex landscapes. Predator abundance was related to greater abundance of alternative prey in those landscapes. Stephanitis pyrioides survival was lower in complex habitats when exposed to endemic natural enemy populations. Laboratory feeding trials confirmed the more abundant predators consumed S. pyrioides. Host plant quality was not a strong force influencing patterns of S. pyrioides abundance. When predators were excluded, adult S. pyrioides survival was greater on azaleas grown in complex habitats, in opposition to the observed pattern of abundance. Similarly, complexity did not affect S. pyrioides immigration and emigration rates. The complexity of urban landscapes affects the strength of top-down forces on herbivorous insect populations by influencing alternative prey and generalist predator abundance. It is possible that habitats can be manipulated to promote the suppressive effects of generalist predators.     

Loss of mating opportunities influences refuge use in the Iberian rock lizard,<Emphasis Type="Italic"> Lacerta monticola</Emphasis>

Because time spent in refuge may be costly if prey lose opportunities to forage, fight, or mate, prey allow predators to approach closer before beginning to flee when opportunity costs are high. Because the same opportunity costs may apply to refuge use as to escape, prey should make similar trade-offs between risk of emerging and cost of remaining in refuge. In the Iberian rock lizard, Lacerta monticola, we studied the effects of sex, reproductive season, speed of predator approach, and potential loss of mating opportunities on time spent in refuge following simulated predatory attacks. Lizards of both sexes adjusted refuge use to the level of risk by spending more time in refuge when approached rapidly than slowly. Females remained in refuge for equal times in the mating and postreproductive seasons, but males emerged sooner during the mating season, suggesting adjustment to a cost of lost opportunity to search for mates during the mating season. When a tethered female was nearby, males emerged from refuge earlier than if no female was present, indicating a trade-off between risk and mating opportunity. Approach speed affected emergence time when females were absent, but not when a female was present. Approach speed did not affect the probability that, after emerging, a male would return to court the female. For males that courted females intensely (bit them) before entering refuge, approach speed did not affect latency to emerge, but males that courted less intensely emerged sooner if approached slowly than rapidly. These findings show that males adjust the length of time spent in refuge to both risk of predation and reproductive cost of refuge use.Communicated by A. Mathis     

Taste-rejection by predators and the evolution of unpalatability in prey

Aposematic species advertise their unpalatability to potential predators using conspicuous warning colouration. The initial evolution of aposematism is thought to occur by warningly coloured mutants emerging in an already unpalatable cryptic species. However, possessing defence chemicals is often costly, and it is difficult to understand what the selective benefits might be for a mutation causing its bearer to be defended in a population of otherwise palatable cryptic prey. One solution to this problem is that chemically defended individuals are tasted and rejected by predators, and are, therefore, more likely to survive predatory attacks than undefended individuals. Using naïve domestic chicks Gallus gallus domesticus as predators and cryptic green chick crumbs as prey, we asked whether the accuracy with which birds discriminated between palatable and unpalatable prey was affected by the palatability of the unpalatable prey (moderately or highly defended), or their frequency in the population (10 or 25%). Birds could discriminate between green prey on the basis of their defences, and showed better discrimination between palatable and unpalatable prey when defended crumbs were highly unpalatable, compared to when they were moderately unpalatable. Although there was no detectable effect of the frequency of unpalatable prey in the population on predator taste-rejection behaviour in our main analysis, frequency did appear to affect the strategies that birds used in their foraging decisions when prey were only moderately unpalatable. How birds used taste to reject prey also suggests that birds may be able to monitor and regulate their chemical intake according to the frequency and defence levels of the unpalatable prey. Taken together, these results show that avian predators can generate selection for unpalatability in cryptic prey by sampling and taste-rejecting prey, but that a relatively large chemical difference between palatable and unpalatable prey may be necessary before unpalatable prey can enjoy a selective advantage. The exact nature of this evolutionary dynamic will depend on other environmental factors, such as defence costs and prey availability, but it provides a mechanism by which defences can evolve in a cryptic population.     

Toward a predictive theory of risk effects: hypotheses for prey attributes and compensatory mortality

Risk effects, or the costs of antipredator behavior, can comprise a large proportion of the total effect of predators on their prey. While empirical studies are accumulating to demonstrate the importance of risk effects, there is no general theory that predicts the relative importance of risk effects and direct predation. Working toward this general theory, it has been shown that functional traits of predators (e.g., hunting modes) help to predict the importance of risk effects for ecosystem function. Here, I note that attributes of the predator, the prey, and the environment are all important in determining the strength of antipredator responses, and I develop hypotheses for the ways that prey functional traits might influence the magnitude of risk effects. In particular, I consider the following attributes of prey: group size and dilution of direct predation risk, the degree of foraging specialization, body mass, and the degree to which direct predation is additive vs. compensatory. Strong tests of these hypotheses will require continued development of methods to identify and quantify the fitness costs of antipredator responses in wild populations.     

Predation, habitat complexity, and variation in density-dependent mortality of temperate reef fishes

Density dependence in demographic rates can strongly affect the dynamics of populations. However, the mechanisms generating density dependence (e.g., predation) are also dynamic processes and may be influenced by local conditions. Understanding the manner in which local habitat features affect the occurrence and/or strength of density dependence will increase our understanding of population dynamics in heterogeneous environments. In this study I conducted two separate field experiments to investigate how local predator density and habitat complexity affect the occurrence and form of density-dependent mortality of juvenile rockfishes (Sebastes spp.). I also used yearly censuses of rockfish populations on nearshore reefs throughout central California to evaluate mortality of juvenile rockfish at large spatial scales. Manipulations of predators (juvenile bocaccio, S. paucispinus) and prey (kelp, gopher, and black-and-yellow [KGB] rockfish, Sebastes spp.) demonstrated that increasing the density of predators altered their functional response and thus altered patterns of density dependence in mortality of their prey. At low densities of predators, the number of prey consumed per predator was a decelerating function, and mortality of prey was inversely density dependent. However, at high densities of predators, the number of prey killed per predator became an accelerating response, and prey mortality was directly density dependent. Results of field experiments and large-scale surveys both indicated that the strength of density-dependent mortality may also be affected by the structural complexity of the habitat. In small-scale field experiments, increased habitat complexity increased the strength of density-dependent mortality. However, at large scales, increasing complexity resulted in a decrease in the strength of density dependence. I suggest that these differences resulted from scale-dependent changes in the predatory response that generated mortality. Whether increased habitat complexity leads to an increase or a decrease in the strength of density-dependent mortality may depend on how specific predatory responses (e.g., functional or aggregative) are altered by habitat complexity. Overall, the findings of this study suggest that rates of demographic density dependence and the resulting dynamics of local populations may largely depend upon attributes of the local habitat.     

Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree

The net benefits of mutualism depend directly on the costs and effectiveness of mutualistic services and indirectly on the interactions that affect those services. We examined interactions among Cordia alliodora myrmecophytic trees, their symbiotic ants Azteca pittieri, coccoid hemipterans, and foliar herbivores in two Neotropical dry forests. The tree makes two investments in symbiotic ants: it supplies nesting space, as domatia, and it provides phloem to coccoids, which then produce honeydew that is consumed by ants. Although higher densities of coccoids should have higher direct costs for trees, we asked whether higher densities of coccoids can also have higher indirect benefits for trees by increasing the effectiveness of ant defense against foliar herbivores. We found that trees benefited from ant defense against herbivores. Ants defended trees effectively only when colonies reached high densities within trees, and ant and coccoid densities within trees were strongly positively correlated. The benefits of reduced foliar herbivory by larger ant colonies were therefore indirectly controlled by the number of coccoids. Coccoid honeydew supply also affected per capita ant aggression against tree herbivores. Ants experimentally fed a carbohydrate-rich diet, analogous to sugar obtained from coccoids, were more aggressive against caterpillars per capita than ants fed a carbohydrate-poor diet. Ant defense was more effective on more valuable and vulnerable young leaves than on older leaves. Young domatia, associated with young leaves, contained higher coccoid densities than older domatia, which suggests that coccoids may also drive spatially favorable ant defense of the tree. If higher investments by one mutualistic partner are tied to higher benefits received from the other, there may be positive feedback between partners that will stabilize the mutualism. These results suggest that higher investment by trees in coccoids leads to more effective defense by ants against the tree's foliar herbivores.     

Indirect effects of prey swamping: differential seed predation during a bamboo masting event

Resource pulses often involve extraordinary increases in prey availability that "swamp" consumers and reverberate through indirect interactions affecting other community members. We developed a model that predicts predator-mediated indirect effects induced by an epidemic prey on co-occurring prey types differing in relative profitability/preference and validated our model by examining current-season and delayed effects of a bamboo mass seeding event on seed survival of canopy tree species in mixed Patagonian forests. The model shows that predator foraging behavior, prey profitability, and the scale of prey swamping influence the character and strength of short-term indirect effects on various alternative prey. When in large prey-swamped patches, nonselective predators decrease predation on all prey types. Selective predators, instead, only benefit prey of similar quality to the swamping species, while very low or high preference prey remain unaffected. Negative indirect effects (apparent competition) may override such positive effects (apparent mutualism), especially for highly preferred prey, when prey-swamped patches are small enough to allow predator aggregation and/or predators show a reproductive numerical response to elevated food supply. Seed predation patterns during bamboo (Chusquea culeou) masting were consistent with predicted short-term indirect effects mediated by a selective predator foraging in large prey-swamped patches. Bamboo seeds and similarly-sized Austrocedrus chilensis (ciprés) and Nothofagus obliqua (roble) seeds suffered lower predation in bamboo flowered than nonflowered patches. Predation rates on the small-seeded Nothofagus dombeyi (coihue) and the large-seeded Nothofagus alpina (rauli) were independent of bamboo flowering. Indirect positive effects were transient; three months after bamboo seeding, granivores preyed heavily upon all seed types, irrespective of patch flowering condition. Moreover, one year after bamboo seeding, predation rates on the most preferred seed (rauli) was higher in flowered than in nonflowered patches. Despite rapid predator numerical responses, short-term positive effects can still influence community recruitment dynamics because surviving seeds may find refuge beneath the litter produced by bamboo dieback. Together, our theoretical analysis and experiments indicate that indirect effects experienced by alternative prey during and after prey-swamping episodes need not be universal but can change across a prey quality spectrum, and they critically depend on predator-foraging rules and the spatial scale of swamping.     

Consequences of patch reef spacing for density-dependent mortality of coral-reef fishes

The spatial configuration of habitat patches can profoundly affect a number of ecological interactions, including those between predators and prey. I examined the effects of reef spacing on predator-prey interactions within coral-reef fish assemblages in the Bahamas. Using manipulative field experiments, I determined that reef spacing influences whether and how density-dependent predation occurs. Mortality rates of juveniles of two ecologically dissimilar species (beaugregory damselfish and yellowhead wrasse) were similarly affected by reef spacing; for both species, mortality was density dependent on reef patches that were spatially isolated (separated by 50 m), and density independent on reef patches that were aggregated (separated by 5 m). A subsequent experiment with the damselfish demonstrated that a common resident predator (coney) caused a substantial proportion of the observed mortality, independent of reef spacing. Compared to isolated reefs, aggregated reefs were much more likely to be visited by transient predators (mostly yellowtail snappers), regardless of prey density, and on these reefs, mortality rates approached 100% for both prey species. Transient predators exhibited neither an aggregative response nor a type 3 functional response, and consequently were not the source of density dependence observed on the isolated reefs. These patterns suggest that resident predators caused density-dependent mortality in their prey through type 3 functional responses on all reefs, but on aggregated reefs, this density dependence was overwhelmed by high, density-independent mortality caused by transient predators. Thus, the spatial configuration of reef habitat affected both the magnitude of total predation and the existence of density-dependent mortality. The combined effects of the increasing fragmentation of coral reef habitats at numerous scales and global declines in predatory fish may have important consequences for the regulation of resident fish populations.     

Three-dimensional barricading of a predatory trap reduces predation and enhances prey capture

Animal structures come at material, energetic, time, and expression costs. Some orb-web spiders add three-dimensional barrier structures to their webs, but many do not. Predator protection is considered to be the principal benefit of adding these structures. Accordingly, it remains paradoxical why some orb-web spiders might construct the barriers while others do not. Here, we experimentally determined whether the barrier structure added to the horizontal orb web of the spider Cyrtophora moluccensis deters predators at the cost of reducing the amount of prey captured in the field. We conducted experiments by day and night to assess whether the effects vary with the time of day. We found that the three-dimensional barriers not only offered protection from predatory wasps by day but also enhanced the amount of prey captured by day and night. Moreover, the barrier structure appears particularly useful at catching moths, the largest and most energetically profitable prey that it encounters. We, therefore, concluded that reducing the energetic and time costs associated with producing and depositing extra silk threads is the principal reason why barrier structures are used intermittently among orb-web spiders.     

Are soil mite assemblages structured by the identity of native and invasive alien grasses?

Associations between plants and animals in aboveground communities are often predictable and specific. This has been exploited for the purposes of estimating the diversity of animal species based on the diversity of plant species. The introduction of invasive alien plants into an ecosystem can result in dramatic changes in both the native plant and animal assemblages. Few data exist at the species level to determine whether belowground animal assemblages share the same degree of association to plants. The hypotheses that soil mites (Acari) form assemblages specifically associated with different native grass species in an unmanipulated natural ecosystem and that invasive alien grasses will impact soil mite assemblage composition in this setting were tested. Soil mites sampled beneath five native and two invasive alien species of grasses at the Konza Prairie Biological Station, Kansas, USA, were similarly abundant, species rich, diverse, and taxonomically distinct. No mite species had affinities for a specific grass species. There was no evidence from analysis of similarity, canonical correspondence analysis, or a nonparametric assemblage analysis that the assemblage composition of soil mites was specific to grass species. Results suggest that soil mite assemblages were more related to characteristics of the plant assemblage as a whole or prevailing soil conditions. The most recent invasive alien grass did not support a successionally younger mite fauna, based on the ratio of mesostigmatid to oribatid mites, and neither of the two invasive grasses influenced mite assemblage structure, possibly because they had not yet substantially altered the soil environment. Our results suggest that extrapolations of soil mite diversity based on assumptions of plant specificity would be invalid.     

Tritrophic effects of birds and ants on a canopy food web, tree growth, and phytochemistry

Insectivorous birds and ants co-occur in most terrestrial communities, and theory predicts that emergent properties (i.e., nonadditive effects) can determine their combined influence on arthropods and plants. In a three-year factorial experiment, I investigated whether the effects of birds on pine and its arthropods differed based on the presence of ants that were predators of most arthropods, but mutualists with tended aphid species. Birds and ants reduced the abundance of most herbivorous and carnivorous arthropods in an additive fashion, with the effects of ants being stronger than those of birds. In sharp contrast, the opposing influences of birds and ants on tended aphid species interacted strongly; ants only increased tended aphid abundance in the absence of birds, while birds only reduced their abundance in the presence of ants. This interaction was mirrored in total herbivore abundance because tended aphids dominated the herbivore community. I develop a novel lexicon to discuss the emergent properties from these effects of opposing sign (predation, mutualism). Despite having emergent effects on herbivores, birds indirectly increased pine wood and foliage growth to a similar extent whether or not ants were present, while ants had no detectable effects. Birds also indirectly increased the abundance of some pine phloem monoterpenes, but these effects differed based on the presence or absence of ants. Thus, I report on a novel yet possibly widespread indirect interaction between intraguild predators, herbivore mutualists, and plant traits (growth, secondary chemistry) mediated through a species-rich community of arthropods.     

The benefit of obligate versus facultative strategies in a shrimp–goby mutualism

Obligate mutualists are predicted to benefit more from mutualism than facultative mutualists and harbor traits that help derive this extra benefit. I tested these predictions with a shrimp–goby mutualism. Individual shrimp (Alpheus floridanus) construct burrows that are shared with individual gobiid fishes that warn shrimp when emergence from burrows is unsafe. The benefit to gobies is refuge from predation. I compared predator avoidance performance of obligate (Nes longus) and facultative (Ctenogobius saepepallens) shrimp-associated gobies with access to a shell, a shrimp burrow, or no shelter. The two gobies performed similarly with shells and no shelter, but N. longus outperformed C. saepepallens with shrimp burrows. Thus, N. longus benefits more from mutualism than C. saepepallens. Also, N. longus has four behavioral traits that likely allow it to benefit from mutualism more than does C. saepepallens: (1) diving into the nearest shrimp burrow when confronted with predators, (2) long flight initiation distance, (3) long time-until-re-emergence after taking refuge, and (4) remaining close to shelter. The latter three likely come with a cost to foraging or mate acquisition as they limit searching range outside the burrow and detract from time spent outside burrows. Thus, N. longus likely harbors traits that allow it to deal with these costs. I discuss a framework for determining whether traits crucial to obligate association with shrimp (both for reaping benefits and dealing with costs) are pre-adaptations or are created through coevolution with shrimp.     

The effects of size-dependent predation risk on the interaction between behavioral and life history traits in a stream-dwelling isopod

In field surveys, laboratory observations and field-based assays of behavior, I examined the effects of size-dependent predation risk on the interaction between size at reproductive maturity and maternal care behavior in the stream-dwelling isopod, Lirceus fontinalis. L. fontinalis exhibit population-specific sizes at reproductive maturity which result in population differences in predation risk during the adult phase. Females from streams containing salamander larvae (that prefer small prey) mature at large sizes and then become relatively safe from predation. Females from streams containing fish (that consume all size classes of prey equally) mature at small sizes and remain at risk. I tested whether these differences in expected survival were reflected in the behavior of females during the maternal phase (i.e., the period during which females exhibit maternal care). Female L. fontinalis carry developing juveniles inside a brood pouch. I simulated predatory attacks on gravid female L. fontinalis from the different population types and found that female behavior correlated with population differences in risk. When “attacked”, females from streams with predatory fish (that experience high risk to adult females) released juveniles from the brood pouch, whereas females from populations with predatory salamander larvae (that pose relatively little risk to adult females) did not release juveniles. I discuss the results with reference to the joint evolution of behavioral and life history traits. Received: 6 March 1996 /Accepted after revision: 12 August 1996     

Species invasion shifts the importance of predator dependence

The strength of interference between foraging individuals can influence per capita consumption rates, with important consequences for predator and prey populations and system stability. Here we demonstrate how the replacement of a previously established invader, the predatory crab Carcinus maenas, by the recently invading predatory crab Hemigrapsus sanguineus shifts predation from a species that experiences strong predator interference (strong predator dependence) to one that experiences weak predator interference (weak predator dependence). We demonstrate using field experiments that differences in the strength of predator dependence persist for these species both when they forage on a single focal prey species only (the mussel Mytilus edulis) and when they forage more broadly across the entire prey community. This shift in predator dependence with species replacement may be altering the biomass across trophic levels, consistent with theoretical predictions, as we show that H. sanguineus populations are much larger than C. maenas populations throughout their invaded ranges. Our study highlights that predator dependence may differ among predator species and demonstrates that different predatory impacts of two conspicuous invasive predators may be explained at least in part by different strengths of predator dependence.