Costs of inducible defence along a resource gradient

In addition to having constitutive defence traits, many organisms also respond to predation by phenotypic plasticity. In order for plasticity to be adaptive, induced defences should incur a benefit to the organism in, for example, decreased risk of predation. However, the production of defence traits may include costs in fitness components such as growth, time to reproduction, or fecundity. To test the hypothesis that the expression of phenotypic plasticity incurs costs, we performed a common garden experiment with a freshwater snail, Radix balthica, a species known to change morphology in the presence of molluscivorous fish. We measured a number of predator-induced morphological and behavioural defence traits in snails that we reared in the presence or absence of chemical cues from fish. Further, we quantified the costs of plasticity in fitness characters related to fecundity and growth. Since plastic responses may be inhibited under limited resource conditions, we reared snails in different densities and thereby levels of competition. Snails exposed to predator cues grew rounder and thicker shells, traits confirmed to be adaptive in environments with fish. Defence traits were consistently expressed independent of density, suggesting strong selection from predatory molluscivorous fish. However, the expression of defence traits resulted in reduced growth rate and fecundity, particularly with limited resources. Our results suggest full defence in predator related traits regardless of resource availability, and costs of defence consequently paid in traits related to fitness.     

Environmental calcium modifies induced defences in snails

Inducible defences are adaptive phenotypes that arise in response to predation threats. Such plasticity incurs costs to individuals, but there has been little interest in how such induced traits in animals may be constrained by environmental factors. Here, we demonstrate that calcium availability interacts with predation cues to modify snail shell growth and form. Small snails increased their growth and were heavier when exposed to fish chemical cues, but this response was calcium limited. There was also an interactive effect of fish cues and calcium on the shell growth of larger snails, but shell strength and aperture narrowness were affected by calcium alone. For small snails, behavioural avoidance was greatest for snails exhibiting least morphological plasticity, suggesting a trade-off. There was no trade-off of somatic growth with plasticity. We suggest that the expression of defensive traits in molluscs can be constrained by calcium availability, which has implications for molluscan ecology and evolution.     

Effects of behavioral and morphological plasticity on risk of predation in a Neotropical tadpole

Predator-induced phenotypic plasticity is widespread among aquatic animals, however the relative contributions of behavioral and morphological shifts to reducing risk of predation remain uncertain. We tested the phenotypic plasticity of a Neotropical tadpole (Rana palmipes) in response to chemical cues from predatory Belostoma water bugs, and how phenotype affects risk of predation. Behavior, morphology, and pigmentation all were plastic, resulting in a predator-induced phenotype with lower activity, deeper tail fin and muscle, and darker pigmentation. Tadpoles in the predator cue treatment also grew more rapidly, possibly as a result of the nutrient subsidy from feeding the caged predator. For comparison to phenotypes induced in the experiment, we quantified the phenotype of tadpoles from a natural pool. Wild-caught tadpoles did not match either experimentally induced phenotype; their morphology was more similar to that produced in the control treatment, but their low swimming activity was similar to that induced by predator cues. Exposure of tadpoles from both experimental treatments and the natural pool to a free-ranging predator confirmed that predator-induced phenotypic plasticity reduces risk of predation. Risk of predation was comparable among wild-caught and predator-induced tadpoles, indicating that behavioral shifts can substantially alleviate risk in tadpoles that lack the typical suite of predator-induced morphological traits. The morphology observed in wild-caught tadpoles is associated with rapid growth and high competition in other tadpole species, suggesting that tadpoles may profitably combine a morphology suited to competition for food with behaviors that minimize risk of predation.     

An inducible morphological defence is a passive by-product of behaviour in a marine snail

Many organisms have evolved inducible defences in response to spatial and temporal variability in predation risk. These defences are assumed to incur large costs to prey; however, few studies have investigated the mechanisms and costs underlying these adaptive responses. I examined the proximate cause of predator-induced shell thickening in a marine snail (Nucella lamellosa) and tested whether induced thickening leads to an increase in structural strength. Results indicate that although predators (crabs) induce thicker shells, the response is a passive by-product of reduced feeding and somatic growth rather than an active physiological response to predation risk. Physical tests indicate that although the shells of predator-induced snails are significantly stronger, the increase in performance is no different than that of snails with limited access to food. Increased shell strength is attributable to an increase in the energetically inexpensive microstructural layer rather than to material property changes in the shell. This mechanism suggests that predator-induced shell defences may be neither energetically nor developmentally costly. Positive correlations between antipredator behaviour and morphological defences may explain commonly observed associations between growth reduction and defence production in other systems and could have implications for the evolutionary potential of these plastic traits.     

Putting prey back together again: integrating predator-induced behavior,morphology, and life history

The last decade has seen an explosion in the number of studies exploring predator-induced plasticity. Recently, there has been a call for more comprehensive approaches that can identify functional relationships between traits, constraints on phenotypic responses, and the cost and benefits of alternative phenotypes. In this study, we exposed Helisoma trivolvis, a freshwater snail, to a factorial combination of three resource levels and five predator environments (no predator, one or two water bugs, and one or two crayfish) and examined ten traits including behavior, morphology, and life history. Each predator induced a unique suite of behavioral and morphological responses. Snails increased near-surface habitat use with crayfish but not with water bugs. Further, crayfish induced narrow and high shells whereas water bugs induced wide shells and wide apertures. In terms of life history, both predators induced delayed reproduction and greater mass at reproduction. However, crayfish induced a greater delay in reproduction that resulted in reduced fecundity whereas water bugs did not induce differences in fecundity. Resource levels impacted the morphology of H. trivolvis; snails reared with greater resource levels produced higher shells, narrower shells, and wider apertures. Resource levels also impacted snail life history; lower resources caused longer times to reproduction and reduced fecundity. Based on an analysis of phenotypic correlations, the morphological responses to each predator most likely represent phenotypic trade-offs. Snails could either produce invasion-resistant shells for defense against water bugs or crush-resistant shells for defense against crayfish, but not both. Our use of a comprehensive approach to examine the responses of H. trivolvis has provided important information regarding the complexity of phenotypic responses to different environments, the patterns of phenotypic integration across environments, and the potential costs and benefits associated with plastic traits.     

Tuning in to multiple predators: conflicting demands for shell morphology in a freshwater snail

1. We examined the response to chemical cues from fish and crayfish, two predators with contrasting feeding modes, and their single and combined effect on shell morphology in the freshwater snail Radix balthica. 2. Snails were subjected to four treatments: tench (Tinca tinca), signal crayfish (Pacifastacus leniusculus), a combination of tench and signal crayfish and no predators (control). Shell shape, crushing resistance and shell thickness were quantified. We also analysed whether shape or shell thickness contributes most to crushing resistance. 3. Chemical cues from the fish induced a rounder shell shape in R. balthica, a thicker shell and a higher crushing resistance, whereas crayfish chemical cues had no effect on shell morphology, shell thickness or crushing resistance. Shell shape contributed more to crushing resistance than shell thickness. 4. The combined predator treatment showed an intermediate response between the fish and crayfish treatments. Shell roundness was reduced compared with the fish treatment, but the reduced crushing resistance that comes with a less rounded shell was compensated by an increased investment in extra shell material, exceeding that of the fish treatment. 5. Our study extends previous studies of multipredator effects on phenotypically plastic freshwater snails by showing that the snails are able to fine‐tune different elements of morphology to counter predator‐specific foraging modes.     

Crayfish induce a defensive shell shape in a freshwater snail

Abstract. This study was undertaken to determine whether intraspecific variation in shell morphology of the freshwater snail Elimia (= Goniobasis ) livescens is caused by predator-induced morphological changes. Juvenile snails from 3 populations were grown in the presence of effluent from predatory crayfish feeding on conspecific snails or in effluent from conspecific snails only. Snails from one population, Clear Creek, exhibited a predator-induced morphology; they grew a narrow body whorl when exposed to the effluent from crayfish. Experimental feeding trials with crayfish and snails from Clear Creek were conducted to determine whether a narrow body whorl reduced predation in the presence of the crayfish Orconectes propinquus . In the feeding trials, snails with a narrow body whorl were eaten less frequently than snails with wider shells. However, there was no difference in overall size (length) between snails that were eaten and those that were not. Thus, juvenile snails from Clear Creek exposed to the presence of crayfish were induced to develop relatively narrow shells, which reduce the risk of successful attack by these crayfish. Hence the induced shell morphology is probably a defense against predation by crayfish.     

Phenotypic plasticity in oysters (Crassostrea virginica) mediated by chemical signals from predators and injured prey

Prey organisms reduce predation risk by altering their behavior, morphology, or life history. Avoiding or deterring predators often incurs costs, such as reductions in growth or fecundity. Prey minimize costs by limiting predator avoidance or deterrence to situations that pose significant risk of injury or death, requiring them to gather information regarding the relative threat potential predators pose. Chemical cues are often used for risk evaluation, and we investigated morphological responses of oysters (Crassostrea virginica) to chemical cues from injured conspecifics, from heterospecifics, and from predatory blue crabs (Callinectes sapidus) reared on different diets. Previous studies found newly settled oysters reacted to crab predators by growing heavier, stronger shells, but that adult oysters did not. We exposed oysters at two size classes (newly settled oyster spat and juveniles ~2.0 cm) to predation risk cue treatments including predator or injured prey exudates and to seawater controls. Since both of the size classes tested can be eaten by blue crabs, we hypothesized that both would react to crab exudates by producing heavier, stronger shells. Oyster spat grew heavier shells that required significantly more force to break, an effective measure against predatory crabs, when exposed to chemical exudates from blue crabs as compared to controls. When exposed to chemical cues from injured conspecifics or from injured clams (Mercenaria mercenaria), a sympatric bivalve, shell mass and force were intermediate between predator treatments and controls, indicating that oysters react to injured prey cues but not as strongly as to cues released by predators. Juvenile oysters of ~ 2.0 cm did not significantly alter their shell morphology in any of the treatments. Thus, newly settled oysters can differentiate between predatory threats and adjust their responses accordingly, with the strongest responses being to exudates released by predators, but oysters of 2.0 cm and larger do not react morphologically to predatory threats.     

Predator-induced morphological plasticity across local populations of a freshwater snail

The expression of anti-predator adaptations may vary on a spatial scale, favouring traits that are advantageous in a given predation regime. Besides, evolution of different developmental strategies depends to a large extent on the grain of the environment and may result in locally canalized adaptations or, alternatively, the evolution of phenotypic plasticity as different predation regimes may vary across habitats. We investigated the potential for predator-driven variability in shell morphology in a freshwater snail, Radix balthica, and whether found differences were a specialized ecotype adaptation or a result of phenotypic plasticity. Shell shape was quantified in snails from geographically separated pond populations with and without molluscivorous fish. Subsequently, in a common garden experiment we investigated reaction norms of snails from populations' with/without fish when exposed to chemical cues from tench (Tinca tinca), a molluscivorous fish. We found that snails from fish-free ponds had a narrow shell with a well developed spire, whereas snails that coexisted with fish had more rotund shells with a low spire, a shell morphology known to increase survival rate from shell-crushing predators. The common garden experiment mirrored the results from the field survey and showed that snails had similar reaction norms in response to chemical predator cues, i.e. the expression of shell shape was independent of population origin. Finally, we found significant differences for the trait means among populations, within each pond category (fish/fish free), suggesting a genetic component in the determination of shell morphology that has evolved independently across ponds.     

Cue reliability, risk sensitivity and inducible morphological defense in a marine snail

Reliable cues that communicate current or future environmental conditions are a requirement for the evolution of adaptive phenotypic plasticity, yet we often do not know which cues are responsible for the induction of particular plastic phenotypes. I examined the single and combined effects of cues from damaged prey and predator cues on the induction of plastic shell defenses and somatic growth in the marine snail Nucella lamellosa. Snails were exposed to chemical risk cues from a factorial combination of damaged prey presented in isolation or consumed by predatory crabs (Cancer productus). Water-borne cues from damaged conspecific and heterospecific snails did not affect plastic shell defenses (shell mass, shell thickness and apertural teeth) or somatic growth in N. lamellosa. Cues released by feeding crabs, independent of prey cue, had significant effects on shell mass and somatic growth, but only crabs consuming conspecific snails induced the full suite of plastic shell defenses in N. lamellosa and induced the greatest response in all shell traits and somatic growth. Thus the relationship between risk cue and inducible morphological defense is dependent on which cues and which morphological traits are examined. Results indicate that cues from damaged conspecifics alone do not trigger a response, but, in combination with predator cues, act to signal predation risk and trigger inducible defenses in this species. This ability to “label” predators as dangerous may decrease predator avoidance costs and highlights the importance of the feeding habits of predators on the expression of inducible defenses.     

Adaptive plasticity in predator-induced defenses in a common freshwater snail: altered selection and mode of predation due to prey phenotype

Studies of putatively adaptive plasticity, such as inducible defenses, frequently explore the fitness consequences of expressing alternative phenotypes in alternative environments, but few studies examine how and why the pattern of selection changes in relation to trait induction. We induced snails in the presence/absence of nonlethal predatory crayfish, exposed both phenotypes (alone and combined) to selection by lethal crayfish, and quantified linear and nonlinear selection differentials. Crayfish induced an increase in mass, shell thickness, and absolute (but not relative) shell dimensions. Crayfish predation on uninduced snails was rapid, accomplished via shell-crushing and revealed strong selection for increased size (i.e., mass and shell dimensions). Conversely, crayfish predation on predator-induced snails was slower, often accomplished using an alternative mode of predation (shell-crushing 70% of the time, but shell-extraction 30% of the time), and revealed selection for wide apertures and thick shells. Crayfish selection on uninduced snails in the presence of predator-induced snails was stronger than predation on uninduced snails alone demonstrating that selection can be frequency dependent. Therefore, predator-induced changes in size and shell thickness appear to be adaptive and, along with reciprocal adjustments in the mode of predation, result in altered patterns of selection.     

Transgenerational plasticity of inducible defences: Combined effects of grand‐parental,parental and current environments

Phenotypic plasticity can occur across generations (transgenerational plasticity) when environments experienced by the previous generations influenced offspring phenotype. The evolutionary importance of transgenerational plasticity, especially regarding within‐generational plasticity, is a currently hot topic in the plasticity framework. How long an environmental effect can persist across generations and whether multigenerational effects are cumulative are primordial—for the evolutionary significance of transgenerational plasticity—but still unresolved questions. In this study, we investigated how the grand‐parental, parental and offspring exposures to predation cues shape the predator‐induced defences of offspring in the Physa acuta snail. We expected that the offspring phenotypes result from a three‐way interaction among grand‐parental, parental and offspring environments. We exposed three generations of snails without and with predator cues according to a full factorial design and measured offspring inducible defences. We found that both grand‐parental and parental exposures to predator cues impacted offspring antipredator defences, but their effects were not cumulative and depended on the defences considered. We also highlighted that the grand‐parental environment did alter reaction norms of offspring shell thickness, demonstrating an interaction between the grand‐parental transgenerational plasticity and the within‐generational plasticity. We concluded that the effects of multigenerational exposure to predator cues resulted on complex offspring phenotypic patterns which are difficult to relate to adaptive antipredator advantages.     

SHELL STRENGTH OF COLOUR MORPHS OF THE MANGROVE SNAIL LITTORARIA PALLESCENS

The load required to break shells of the snail Littor-aria pallescens(Philippi) (Gastropoda: Littorinidae) has been established.Mass increases more than proportionally with size. Size forsize, relatively heavy shells are thicker than relatively lightones, and the thicker shells are stronger. Three samples fromdifferent localities differ significantly in strength. Littorariapallescens is polymorphic for shell colour. It is shown thatin two of the three samples, both from Papua New Guinea, individualsof the dark morph are significantly heavier and stronger thanthose of the yellow morph, while there is no difference betweenmorphs in the third sample, from Thailand. In the sample withthe most robust shells the dark individuals are stronger, massfor mass, than yellows. Thus, colour morph is sometimes, butnot always, associated with differences in shell characteristicswhich are likely to affect fitness. Where there is a difference,the dark morph is estimated to be on average about 22% strongerthan the yellow morph. The difference between morphs is smallcompared with the large variation in shell characters associatedwith size. (Received 20 May 1992; accepted 22 June 1992)     

Effects of perceived predation risk and social environment on the development of three‐spined stickleback (Gasterosteus aculeatus) morphology

Phenotypically plastic changes in response to variation in perceived predation risk are widespread, but little is known about if and how social environment modulates induced responses to predation risk. We investigated the influence of perceived predation risk (i.e. chemical cues from a predator) and social environment (i.e. one, two or 20 individuals reared together) on three‐spined stickleback (Gasterosteus aculeatus) morphology in a factorial common garden experiment. We found that exposure to chemical cues from potential predators did not influence growth or body condition or induce more robust morphological defences (i.e. lateral plate numbers and dorsal spine lengths). However, sticklebacks exposed to predator cues developed longer caudal peduncles and larger eyes as compared with fish from the control treatment. As these responses may improve sticklebacks’ ability to avoid piscine predation, they might be adaptive. Social environment/density also influenced expression of some traits, but these effects were independent of predation‐risk treatment effects. In general, these results suggest that apart from the classic morphological defence structures, which appear mostly constitutive, three‐spined sticklebacks are capable of expressing potentially adaptive morphological responses to chemical cues from potential predators.     

Endocrine regulation of predator-induced phenotypic plasticity

Elucidating the developmental and genetic control of phenotypic plasticity remains a central agenda in evolutionary ecology. Here, we investigate the physiological regulation of phenotypic plasticity induced by another organism, specifically predator-induced phenotypic plasticity in the model ecological and evolutionary organism Daphnia pulex. Our research centres on using molecular tools to test among alternative mechanisms of developmental control tied to hormone titres, receptors and their timing in the life cycle. First, we synthesize detail about predator-induced defenses and the physiological regulation of arthropod somatic growth and morphology, leading to a clear prediction that morphological defences are regulated by juvenile hormone and life-history plasticity by ecdysone and juvenile hormone. We then show how a small network of genes can differentiate phenotype expression between the two primary developmental control pathways in arthropods: juvenoid and ecdysteroid hormone signalling. Then, by applying an experimental gradient of predation risk, we show dose-dependent gene expression linking predator-induced plasticity to the juvenoid hormone pathway. Our data support three conclusions: (1) the juvenoid signalling pathway regulates predator-induced phenotypic plasticity; (2) the hormone titre (ligand), rather than receptor, regulates predator-induced developmental plasticity; (3) evolution has favoured the harnessing of a major, highly conserved endocrine pathway in arthropod development to regulate the response to cues about changing environments (risk) from another organism (predator).     

Phenotypic plasticity and predator effects on morphology and physiology of crucian carp in nature and in the laboratory

Crucian carp Carassius carassius show great phenotypic plasticity in individual morphology and physiology, and strong variation in population density in different fish communities. Small fish with shallow bodies and large heads are typical in overcrowded monospecific fish communities in small ponds, whereas deep-bodied, large fish are found in larger, multispecies lakes. Crucian carp are especially vulnerable to predation by piscivorous fish and their greater relative body depth in multispecies fish communities has been proposed to be an induced defence against size-limited predation, and hence to be an adaptive feature. Data are presented here on the two divergent body forms in field populations in eastern Finland, together with results of laboratory experiments on predator effects on morphology and physiology (growth, respiration, heart rate). The deep body can be achieved in a few months by introducing a low population density of shallow-bodied fish into a food-rich environment with no piscivores. In the laboratory, both the presence of piscivores (chemical cues) and enhanced food availability increased the relative depth of crucian carp, but only to a modest extent when compared to natural variation. It is concluded that the deep-body form of crucian carp in the low density populations of multispecies fish communities is the normal condition. Reproduction in monospecific ponds results in high intraspecific competition, low growth rate and a stunted morphology. According to pilot tests, the mechanism behind the predator effect in the laboratory might be a behavioural reaction to chemical cues (alarm substances/predator odour) causing changes in energy allocation: predator-exposed crucian carp adopt a 'hiding' mode with decreased activity (less swimming, lower respiration and heart rate) and with higher overall growth. Whether, and to what extent, this predator-induced mechanism works in nature is unclear.     

Maternal control of calcium concentration in the larval nursery of the bromeliad crab,Metopaulias depressus (Grapsidae)

It has been proposed that parental care in invertebrates controls for physicochemical conditions. This suggests that the parent detects deviations from optimal conditions and responds by correcting the deviation for the benefit of the offspring. In the bromeliad crab, Metopaulias depressus, mothers accumulate snail shells (CaCO₃) in the leaf axil containing the larvae, which results in an increase in Ca²⁺ and pH, both beneficial to the young. I tested the hypotheses that mothers: (i) control for calcium levels and only collect shells when calcium is too low; (ii) always collect shells, independent of the calcium content of the nursery; (iii) collect shells if encountered, but increase their activity if the calcium content becomes critical. In a field experiment, I reduced the initial calcium concentration in the nurseries of one group and increased it in another group. In both groups mothers collected shells. However, they collected significantly more shell mass per day in the group with reduced levels than in the group with high levels. The results support hypothesis (iii) and unequivocally demonstrate maternal control of physicochemical conditions in the nursery. This is the first proof that crustacean mothers actively regulate abiotic conditions for their offspring.     

Predator discrimination in the hermit crab Calcinus californiensis: tight for shell breakers,loose for shell peelers

Prey exposed to predators with different hunting and feeding modes are under different selective pressures, therefore it is expected that they should exhibit plastic and adaptive antipredator responses according to current risks. The hermit crab Calcinus californiensis faces two contrasting predators, the shell peeler Arenaeus mexicanus that hunts by active searching and the shell breaker Eriphia squamata that hunts by ambush. In order to discover whether C. californiensis displays plastic responses depending on the type of predatory challenge, we examined the shell size preference, the hiding time, and the escape velocity of hermit crabs in the presence of chemical cues from a shell peeler, a shell breaker, and a control. We also examined the role of shell fit on the escape velocity of the hermit crabs in natural tidal pools. Crabs chose shells with a loose fit (relatively large shells) in the presence of chemical cues from the shell peeler Arenaeus and shells with a tight fit when exposed to cues from the shell breaker Eriphia. The hermit crabs hid for shorter times and moved away faster from Eriphia than from Arenaeus stimulus. The use of a tight shell favours faster movement away from the shell breaker (pre‐capture strategy), but prevents the crab retracting deeper inside the shell, increasing the risk of be eaten by the shell peeler once captured. Hence, the use of loose shells that protect the crab from the shell peeler hinders fast escape. This study shows specific and plastic antipredatory responses to contrasting predators, each bringing adaptive benefits at different levels of the predator sequence.     

QUANTITATIVE GENETICS OF SHELL FORM OF AN INTERTIDAL SNAIL: CONSTRAINTS ON SHORT-TERM RESPONSE TO SELECTION

We investigated the genetic and environmental determinants of shell form in an intertidal snail (Prosobranchia: Littorina sp.) to identify constraints on the short-term response to selection. Our quantitative genetic parameters were estimated from a half-sib experimental design using 288 broods of snails. Each brood was divided into two treatments differing in snail population density, and therefore in grazing area per snail. Differences in population density induced marked differences in shell form. Snails in the low density treatment grew faster and had lighter shells with narrower whorls and narrower apertures than their siblings at high density. Despite this environmental plasticity in shell shape we found significant additive genetic variance for components of shell shape. We discuss two mechanisms that may maintain additive genetic variance for shell shape in intertidal snail populations: migration between environments with different selective pressures and migration between environments with different mean growth rates. We also estimated a genetic variance-covariance matrix for shell form traits and used the matrix to identify constraints on the short-term response to selection. We predict the rate of response to selection for predator-resistant morphology such as would occur upon invasion of predatory crabs. The large negative genetic correlation between relative spire height and shell weight would facilitate simultaneous selection for a lower spire and a heavier shell, both of which would increase resistance to predatory crabs.