Population consequences of a predator-induced habitat shift by trout in whole-lake experiments

In a replicated whole-lake experiment, we (a) tested for the existence of a flexible habitat shift in response to predator presence in age-0 rainbow trout (Oncorhynchus mykiss) at risk of cannibalism and (b) evaluated the population-level consequences of habitat shifts in terms of growth and survival over their first growing season. Daphnid food and adult trout predators were substantially more abundant in pelagic than in littoral habitats. Age-0 trout used all habitats in populations without adult trout predators, whereas age-0 trout were observed only in the less profitable littoral habitat in populations with adult trout. Consequently, mean fall mass of age-0 trout in the presence of predators was almost half that observed in populations without adult trout. Despite the shift in habitat use, age-0 trout experienced 90% mortality when adult trout predators were present, in comparison to only 36% mortality when absent. We conclude that the commonly observed habitat shifts by fish at risk of predation, observed at smaller scales, do in fact occur at the whole-system scale over long time intervals. These results suggest that fish are able to perceive risk at large spatial scales and thus take advantage of profitable (but normally risky) habitats when predators are absent, or move to less profitable refuge habitats when predators are present.

Parasite- and predator-induced maternal effects in the great tit (Parus major)

Both predators and parasites can elicit behavioral and physiological responses in prey and hosts, respectively. These responses may involve the reallocation of resources and may thus limit each other. We investigated the effects of concurrent pre-laying exposure of great tit females (Parus major) to both a simulated predation risk and a nest-based ectoparasite, the hen flea (Ceratophyllus gallinae), on nestling growth and development. We manipulated perceived predation risk using models and vocalizations of sparrowhawks (Accipiter nisus). At the start of incubation, we swapped whole clutches between treated and untreated nests to separate pre-laying maternal effects from posthatching effects. Since costs and benefits of maternal responses to parasites need to be assessed under parasite pressure, we infested half of the rearing nests with hen fleas. Parasites had negative effects on mass gain and wing growth, both via maternal effects and via direct exposure of nestlings, whereas maternal predation risk had no significant effect. The interaction between predator and parasite treatments was not significant and, thus, suggests the absence of a trade-off between the 2 stressors operating at the level of maternal effects. Alternatively, the complexity of the design, despite a relatively large sample size, may have limited the power for detection of this expected trade-off.

Predator-Induced Plasticity in Spotted Salamanders (Ambystoma maculatum)

The ability to respond plastically to the environment has allowed amphibians to evolve adaptive responses to spatial and temporal variation in predation threat. However, animals exposed to predators may also show costs of plasticity or tradeoffs. This study examines predator-induced plasticity in larval development, behavior, and metamorphosis in the spotted salamander, Ambystoma maculatum. Salamanders were raised in two treatments: with predator cues (a fish predator, genus Lepomis, on the other side of a divided tank), or without predator cues. During the larval stage the predator treatment group experienced higher mortality rates than the no-predator treatment group. Behavioral trials revealed that predator treatment animals ate less than those not exposed, and that this feeding response was immediately inducible and had lasting effects. Animals in the predator treatment group had smaller tail areas during the mid-larval period. Feeding and body size effects may have contributed to increased mortality in the predator-treatment animals. The timing of metamorphic onset was not affected by the presence of predators, but predator-treatment salamanders had shorter snout/vent lengths at metamorphosis. The duration of metamorphosis showed a potentially adaptive plastic response to the presence of predator cues: metamorphosis was longest in the no-predator treatment group, reduced in the predator treatment group, and even further reduced for animals exposed to predator cues only during metamorphosis. Overall, we found a mix of potentially adaptive and costly plastic responses in spotted salamanders.

Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor)

Global declines in amphibians likely have multiple causes, including widespread pesticide use. Our knowledge of pesticide effects on amphibians is largely limited to short-term (4-d) toxicity tests conducted under highly artificial conditions to determine lethal concentrations (LC50). We found that if we used slightly longer exposure times (10–16 d), low concentrations of the pesticide carbaryl (3–4% of LC504-d) killed 10–60% of gray treefrog (Hyla versicolor) tadpoles. If predatory cues also were present, the pesticide became 2–4 times more lethal, killing 60–98% of tadpoles. Thus, under more realistic conditions of increased exposure times and predatory stress, current application rates for carbaryl can potentially devastate gray treefrog populations. Further, because predator-induced stress is ubiquitous in animals and carbaryl's mode of action is common to many pesticides, these negative impacts may be widespread in nature.

Predator-induced phenotypic plasticity in tadpoles: extension or innovation?

Phenotypic plasticity, the ability of a trait to change as a function of the environment, is central to many ideas in evolutionary biology. A special case of phenotypic plasticity observed in many organisms is mediated by their natural predators. Here, we used a predator-prey system of dragonfly larvae and tadpoles to determine if predator-mediated phenotypic plasticity provides a novel way of surviving in the presence of predators (an innovation) or if it represents a simple extension of the way noninduced tadpoles survive predation. Tadpoles of Limnodynastes peronii were raised in the presence and absence of predation, which then entered a survival experiment. Induced morphological traits, primarily tail height and tail muscle height, were found to be under selection, indicating that predator-mediated phenotypic plasticity may be adaptive. Although predator-induced animals survived better, the multivariate linear selection gradients were similar between the two tadpole groups, suggesting that predator-mediated phenotypic plasticity is an extension of existing survival strategies. In addition, nonlinear selection gradients indicated a cost of predator-induced plasticity that may limit the ability of phenotypic plasticity to enhance survival in the presence of predators.

Predator-mediated phenotypic plasticity in tadpoles of the striped marsh frog, Limnodynastes peronii

We tested the phenotypic responses of larval striped marsh frogs (Limnodynastes peronii) to the odonate nymph predator, Aeshna brevistyla. When reared in the presence of dragonfly nymphs feeding upon conspecifics of L. peronii larvae the tadpoles showed a strong change in morphology. Morphological changes included an increase in total tail height, but also an unexpected marked change in head-body shape. In addition, we examined how tadpole development, as well as mass and length at metamorphosis, was affected by exposure to dragonfly nymphs. Larval development of L. peronii was strongly influenced by exposure to the predatory behaviour of dragonfly nymphs. Predator-induced tadpoles had significantly slower developmental rates than control larvae. Although metamorphs of non-exposed L. peronii were approximately 33% lighter than predator-exposed metamorphs and possessed lower jump distances, after adjusting for mass there was no difference in jump distance. The newly described morphological response may assist in more accurately relating morphological plasticity to fitness.

Predator-specific changes in the morphology and swimming performance of larval Rana lessonae

1. We investigated the morphological responses of larval Rana lessonae to the presence of two predators with substantially different prey-detection and capture techniques; larval dragonflies (Aeshna cyanea) and the Pumpkinseed Sunfish (Lepomis gibossus). 2. We also examined the functional implications of any predator-induced morphological variation on their swimming ability by assessing performance during the initial stages of a startle response. 3. We found the morphological responses of larval R. lessonae were dependent on the specific predator present. Tadpoles raised in the presence of dragonfly larvae preying upon conspecific tadpoles developed total tail heights 5.4% deeper and tail muscles 4.7% shallower than tadpoles raised in a non-predator environment, while tadpoles raised with sunfish possessed tails 2% shallower and tail muscles 2.5% higher than non-predator-exposed tadpoles. 4. Predator-induced morphological variation also significantly influenced swimming performance. Tadpoles raised with sunfish possessed swimming speeds 9.5 and 14.6% higher than non- and dragonfly predator groups, respectively. 5. Thus, the expression of these alternative predator-morphs leads to a functional trade-off in performance between the different environments.

Nucella lapillus: imposex transcriptome analysis and phenotypic plasticity

O conhecimento de mecanismos de genómica funcional tem sido maioritariamente adquirido pela utilização de organismos modelo que são mantidos em condições laboratoriais. Contudo, estes organismos não reflectem as respostas a alterações ambientais. Por outro lado, várias espécies, ecologicamente bem estudadas, reflectem bem as interacções entre genes e ambiente mas que, das quais não existem recursos genéticos disponíveis. O imposex, caracterizado pela superimposição de caracteres sexuais masculinos em fêmeas, é induzido pelo tributilestanho (TBT) e trifenilestanho (TPT) e representa um dos melhores exemplos de disrupção endócrina com causas antropogénicas no ambiente aquático. Com o intuito de elucidar as bases moleculares deste fenómeno, procedeu-se à combinação das metodologias de pirosequenciação (sequenciação 454 da Roche) e microarrays (Agilent 4*180K) de forma a contribuir para um melhor conhecimento desta interacção gene-ambiente no gastrópode Nucella lapillus, uma espécie sentinela para imposex. O trancriptoma de N. lapillus foi sequenciado, reconstruído e anotado e posteriormente utilizado para a produção de um “array” de nucleótidos. Este array foi então utilizado para explorar níveis de expressão génica em resposta à contaminação por TBT. Os resultados obtidos confirmaram as hipóteses anteriormente propostas (esteróidica, neuroendócrina, retinóica) e adicionalmente revelou a existência de potenciais novos mecanismos envolvidos no fenómeno imposex. Evidência para alvos moleculares de disrupção endócrina não relacionados com funções reprodutoras, tais como, sistema imunitário, apoptose e supressores de tumores, foram identificados. Apesar disso, tendo em conta a forte componente reprodutiva do imposex, esta componente funcional foi a mais explorada. Assim, factores de transcrição e receptores nucleares lipofílicos, funções mitocondriais e actividade de transporte celular envolvidos na diferenciação de géneros estão na base de potenciais novos mecanismos associados ao imposex em N. lapillus. Em particular, foi identificado como estando sobre-expresso, um possível homólogo do receptor nuclear “peroxisome proliferator-activated receptor gamma” (PPARγ), cuja função na indução de imposex foi confirmada experimentalmente in vivo após injecção dos animais com Rosiglitazone, um conhecido ligando de PPARγ em vertebrados. De uma forma geral, os resultados obtidos mostram que o fenómeno imposex é um mecanismo complexo, que possivelmente envolve a cascata de sinalização envolvendo o receptor retinoid X (RXR):PPARγ “heterodimer” que, até à data não foi descrito em invertebrados. Adicionalmente, os resultados obtidos apontam para alguma conservação de mecanismos de acção envolvidos na disrupção endócrina em invertebrados e vertebrados. Finalmente, a informação molecular produzida e as ferramentas moleculares desenvolvidas contribuem de forma significativa para um melhor conhecimento do fenómeno imposex e constituem importantes recursos para a continuação da investigação deste fenómeno e, adicionalmente, poderão vir a ser aplicadas no estudo de outras respostas a alterações ambientais usando N. lapillus como organismo modelo. Neste sentido, N. lapillus foi também utilizada para explorar a adaptação na morfologia da concha em resposta a alterações naturais induzidas por acção das ondas e pelo risco de predação por caranguejos. O contributo da componente genética, plástica e da sua interacção para a expressão fenotípica é crucial para compreender a evolução de caracteres adaptativos a ambientes heterogéneos. A contribuição destes factores na morfologia da concha de N. lapillus foi explorada recorrendo a transplantes recíprocos e experiências laboratoriais em ambiente comum (com e sem influência de predação) e complementada com análises genéticas, utilizando juvenis provenientes de locais representativos de costas expostas e abrigadas da acção das ondas. As populações estudadas são diferentes geneticamente mas possuem o mesmo cariótipo. Adicionalmente, análises morfométricas revelaram plasticidade da morfologia da concha em ambas as direcções dos transplantes recíprocos e também a retenção parcial, em ambiente comum, da forma da concha nos indivíduos da F2, indicando uma correlação positiva (co-gradiente) entre heritabilidade e plasticidade. A presença de estímulos de predação por caranguejos estimulou a produção de conchas com labros mais grossos, de forma mais evidente em animais recolhidos de costas expostas e também provocou alterações na forma da concha em animais desta proveniência. Estes dados sugerem contra-gradiente em alterações provocadas por predação na morfologia da concha, na produção de labros mais grossos e em níveis de crescimento. O estudo das interacções gene-ambiente descritas acima demonstram a actual possibilidade de produzir recursos e conhecimento genómico numa espécie bem caracterizada ecologicamente mas com limitada informação genómica. Estes recursos permitem um maior conhecimento biológico desta espécie e abrirão novas oportunidades de investigação, que até aqui seriam impossíveis de abordar.

Preference for feeding at habitat edges declines among juvenile blue crabs as oyster reef patchiness increases and predation risk grows

Both habitat patchiness and behaviorally-mediated indirect effects (BMIEs; predator- induced changes in prey behavior that affect the prey's resources) are important in many food webs, but the relationships between these 2 factors have yet to be investigated. To explore effects of habitat patchiness and variation in perceived risk of predation on food-web dynamics, we conducted a factorial experiment in a model aquatic food chain of predator-prey-resource using 2 contrasting predators (adult blue crab Callinectes sapidus and toad fish Opsanus tau), juvenile blue crab as prey, and mussel Geukensia demissa as resource. Both predator presence and habitat patchiness influenced the prey's preference for consuming resources at patch edges instead of interiors. The preference of prey for consuming resources at habitat edges was 4 times stronger in continuous oyster reef habitat than in smaller habitat patches. This suggests that interior resources in continuous habitat experience a refuge from consumption, but this refuge is largely lost in patchy habitat. The mere presence of predators reduced the prey's preference for consuming resources at habitat edges. This BMIE was significant for the ambush predator (toadfish) and the treatment containing both predators, but not for the actively hunting predator (adult blue crab). We conclude that habitat patchiness and predator presence can jointly affect resource distribution by inducing shifts in prey foraging behavior, revealing a need to incorporate BMIEs into habitat fragmentation studies. This conclusion has broad and growing relevance as anthropogenic factors increasingly modify predator abundances and fragment coastal habitats. © Inter-Research 2012.

Modelo de avaliação de risco : São o crescimento e a estequiometria dos girinos afetados pelo efeito interativo entre a presença do predador e da densidade de coespecíficos?

Many prey organisms change their phenotype to reduce the predation risk. However, such changes are associated with trade-offs, and can have negative effects on prey growth or reproduction. Understand how preys assess the predation risk is essential to evaluate the adaptive value of predator-induced phenotypic and its ecological consequences. In this study, we performed a mesocosm experiment to test: i) if growth and stoichiometry of Lithobates catesbeianus tadpoles is altered in response to giant water bug presence (Belostoma spp.); ii) if these responses depend on tadpoles density in environment. Here, we show that tadpoles growth and stoichiometry are not changed by predator presence, neither in low nor in high densities. Our results suggest that tadpoles exposed to predation risk regulate their physiology to preserve the elemental stoichiometric homeostase of their body and excretion. Further, point out to need for future studies that elucidate under what conditions growth and stoichiometry are changed in response to predation risk

Finite Element Modeling of Shell Shape in the Freshwater Turtle Pseudemys concinna Reveals a Trade-Off between Mechanical Strength and Hydrodynamic Efficiency

Aquatic species can experience different selective pressures on morphology in different flow regimes. Species inhabiting lotic regimes often adapt to these conditions by evolving low-drag (i.e., streamlined) morphologies that reduce the likelihood of dislodgment or displacement. However, hydrodynamic factors are not the only selective pressures influencing organismal morphology and shapes well suited to flow conditions may compromise performance in other roles. We investigated the possibility of morphological trade-offs in the turtle Pseudemys concinna. Individuals living in lotic environments have flatter, more streamlined shells than those living in lentic environments; however, this flatter shape may also make the shells less capable of resisting predator-induced loads. We tested the idea that ‘‘lotic’’ shell shapes are weaker than ‘‘lentic’’ shell shapes, concomitantly examining effects of sex. Geometric morphometric data were used to transform an existing finite element shell model into a series of models corresponding to the shapes of individual turtles. Models were assigned identical material properties and loaded under identical conditions, and the stresses produced by a series of eight loads were extracted to describe the strength of the shells. ‘‘Lotic’’ shell shapes produced significantly higher stresses than ‘‘lentic’’ shell shapes, indicating that the former is weaker than the latter. Females had significantly stronger shell shapes than males, although these differences were less consistent than differences between flow regimes. We conclude that, despite the potential for many-to-one mapping of shell shape onto strength, P. concinna experiences a trade-off in shell shape between hydrodynamic and mechanical performance. This trade-off may be evident in many other turtle species or any other aquatic species that also depend on a shell for defense. However, evolution of body size may provide an avenue of escape from this trade-off in some cases, as changes in size can drastically affect mechanical performance while having little effect on hydrodynamic performance.

Preparing Offspring for a Dangerous World: Potential Costs of Being Wrong

Adaptive maternal responses to stressful environments before young are born can follow two non-exclusive pathways: either the mother reduces current investment in favor of future investment, or influences offspring growth and development in order to fit offspring phenotype to the stressful environment. Inducing such developmental cues, however, may be risky if the environment changes meanwhile, resulting in maladapted offspring. Here we test the effects of a predator-induced maternal effect in a predator-free postnatal environment. We manipulated perceived predation-risk for breeding female great tits by exposing them to stuffed models of either a predatory bird or a non-predatory control. Offspring were raised either in an environment matching the maternal one by exchanging whole broods within a maternal treatment group, or in a mismatching environment by exchanging broods among the maternal treatments. Offspring growth depended on the matching of the two environments. While for offspring originating from control treated mothers environmental mismatch did not significantly change growth, offspring of mothers under increased perceived predation risk grew faster and larger in matching conditions. Offspring of predator treated mothers fledged about one day later when growing under mismatching conditions. This suggests costs paid by the offspring if mothers predict environmental conditions wrongly.

Ontogenetic Effects of Hatching Plasticity in the Spotted Salamander (Ambystoma maculatum) due to Egg and Larval Predators

The ability to respond plastically to the environment has allowed amphibians to evolve a response to spatial and temporal variation in predation threat (Benard 2004). Embroys exposed to egg predation are expected to hatch out earlier than their conspecifics. Larval predation can induce a suite of phenotypic changes including growing a larger tail area. When presented with cues from both egg and larval predators, embryos are expected to respond to the egg predator by hatching out earlier because the egg predator presents an immediate threat. However, hatching early may be costly in the larval environment in terms of development, morphology, and/or behavior. We created a laboratory experiment in which we exposed clutches of spotted salamander (Ambystoma maculatum) eggs to both egg (caddisfly larvae) and larval (A. opacum) predators to test this hypothesis. We recorded hatching time and stage and took developmental and morphological data of the animals a week after hatching. Larvae were entered into lethal predation trials with a larval predatory sunfish (Lepomis sp.) in order to study behavior. We found that animals exposed to the egg predator cues hatched out earlier and at earlier developmental stages than conspecifics regardless of whether there was a larval predator present. Animals exposed to larval predator cues grew relatively larger tails and survived longer in the lethal predation trials. However the group exposed to both predators showed a cost of early hatching in terms of lower tail area and shorter survival time in predation trials. The morphological and developmental effects measured of hatching plasticity were transient as there were no developmental or morphological differences between the treatment groups at metamorphosis. Hatching plasticity may be transient but it is important to the development and survival of many amphibians.

Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain

Predators of herbivorous animals can affect plant populations by altering herbivore density, behavior, or both. To test whether the indirect effect of predators on plants arises from density or behavioral responses in a herbivore population, we experimentally examined the dynamics of terrestrial food chains comprised of old field plants, leaf-chewing grasshoppers, and spider predators in Northeast Connecticut. To separate the effects of predators on herbivore density from the effects on herbivore behavior, we created two classes of spiders: (i) risk spiders that had their feeding mouth parts glued to render them incapable of killing prey and (ii) predator spiders that remained unmanipulated. We found that the effect of predators on plants resulted from predator-induced changes in herbivore behavior (shifts in activity time and diet selection) rather than from predator-induced changes in grasshopper density. Neither predator nor risk spiders had a significant effect on grasshopper density relative to a control. This demonstrates that the behavioral response of prey to predators can have a strong impact on the dynamics of terrestrial food chains. The results make a compelling case to examine behavioral as well as density effects in theoretical and empirical research on food chain dynamics.

Substantial changes in the genetic basis of tadpole morphology of Rana lessonae in the presence of predators

Predator-induced morphological plasticity is a model system for investigating phenotypic plasticity in an ecological context. We investigated the genetic basis of the predator-induced plasticity in Rana lessonae by determining the pattern of genetic covariation of three morphological traits that were found to be induced in a predatory environment. Body size decreased and tail dimensions increased when reared in the presence of preying dragonfly larvae. Genetic variance in body size increased by almost an order of magnitude in the predator environment, and the first genetic principal component was found to be highly significantly different between the two environments. The across environment genetic correlation for body size was significantly below 1 indicating that different genes contributed to this trait in the two environments. Body size may therefore be able to respond to selection independently in the two environments to some extent.