Morphological and life‐history responses of anurans to predation by an invasive crayfish: an integrative approach

Predator‐induced phenotypic plasticity has been widely documented in response to native predators, but studies examining the extent to which prey can respond to exotic invasive predators are scarce. As native prey often do not share a long evolutionary history with invasive predators, they may lack defenses against them. This can lead to population declines and even extinctions, making exotic predators a serious threat to biodiversity. Here, in a community‐wide study, we examined the morphological and life‐history responses of anuran larvae reared with the invasive red swamp crayfish, Procambarus clarkii, feeding on conspecific tadpoles. We reared tadpoles of nine species until metamorphosis and examined responses in terms of larval morphology, growth, and development, as well as their degree of phenotypic integration. These responses were compared with the ones developed in the presence of a native predator, the larval dragonfly Aeshna sp., also feeding on tadpoles. Eight of the nine species altered their morphology or life history when reared with the fed dragonfly, but only four when reared with the fed crayfish, suggesting among‐species variation in the ability to respond to a novel predator. While morphological defenses were generally similar across species (deeper tails) and almost exclusively elicited in the presence of the fed dragonfly, life‐history responses were very variable and commonly elicited in the presence of the invasive crayfish. Phenotypes induced in the presence of dragonfly were more integrated than in crayfish presence. The lack of response to the presence of the fed crayfish in five of the study species suggests higher risk of local extinction and ultimately reduced diversity of the invaded amphibian communities. Understanding how native prey species vary in their responses to invasive predators is important in predicting the impacts caused by newly established predator–prey interactions following biological invasions.     

Post-metamorphic change in activity metabolism of anurans in relation to life history

Summary Newly-metamorphosed individuals of some species of frogs and toads differ from adults in behavior, ecology, and physiology. These differences may be related to broader patterns of the life histories of different species of frogs. In particular, the length of larval life and the size of a frog at metamorphosis appear to be significant factors in post-metamorphic ontogenetic change. These changes in performance are associated with rapid post-metamorphic increases in oxygen transport capacity. Bufo americanus (American toads) and Rana sylvatica (wood frogs) spend only 2–3 months as tadpoles and metamorphose at body masses of 0.25 g or less. Individuals of these species improve endurance and aerobic capacity rapidly during the predispersal period immediately following metamorphosis. Increases in hematocrit, hemoglobin concentration, and heart mass relative to body mass are associated with this improvement in organismal performance. Rana clamitans (green frogs) spend from 3 to 10 months as larvae and weigh 3 g at metamorphosis. Green frogs did not show immediate post-metamorphic increases in performance. Rana palustris (pickerel frogs) are intermediate to wood frogs and green frogs in length of larval life and in size at metamorphosis, and they are intermediate also in their post-metamorphic physiological changes.American toads and wood frogs appear to delay dispersal from their natal ponds while they undergo rapid post-metamorphic growth and development, whereas green frogs disperse as soon as they leave the water, even before they have fully absorbed their tails. The very small body sizes of newly metamorphosed toads and wood frogs appear to limit the scope of their behaviors. The brief larval periods of these species permit them to exploit transient aquatic habitats, but impose costs in the form of a period of post-metamorphic life in which their activities are restricted in time and space compared to those of adults.     

Behavioural and life history responses to predation risk by common frog tadpoles exposed to two predators during ontogeny

The presence of predators can induce changes in both the morphology and behaviour of Anuran larvae, affecting both their size and developmental stage at metamorphosis and, consequently, the fitness of adult individuals. Tadpoles have been shown to be capable of finely tuning their defensive responses according to the actual risk perceived, which is expected to vary according to the prey-to-predator size ratio. In this study, we exposed common frog (Rana temporaria) tadpoles (Gosner stages 28–30), for a period of 2 weeks, to the non-lethal presence of dragonfly larvae (Anax imperator) and backswimmers (Notonecta glauca). In such a narrow window of time, we expected behavioural responses to be similar for both predators and exposure to predation risk to have negligible effects on tadpole development and weight. Overall, tadpoles increased hiding behaviour and were less active when predators were present in the experimental mesocosms, but behavioural responses were constrained to the early phase of the ontogeny and were no longer used when tadpoles reached a threshold size. Developmental rate slightly slowed down for predator treatments in comparison to controls, possibly as a consequence of energetic investment in unrecorded morphological defences. Although variation in laboratory conditions and protocols makes it hard to compare the results of different experiments, our results contribute to verify the consistency of behavioural responses in Anuran larvae.     

Density dependence in the terrestrial life history stage of two anurans

Populations of species with complex life cycles have the potential to be regulated at multiple life history stages. However, research tends to focus on single stage density-dependence, which can lead to inaccurate conclusions about population regulation and subsequently hinder conservation efforts. In amphibians, many studies have demonstrated strong effects of larval density and have often assumed that populations are regulated at this life history stage. However, studies examining density regulation in the terrestrial stages are rare, and the functional relationships between terrestrial density and vital rates in amphibians are unknown. We determined the effects of population density on survival, growth and reproductive development in the terrestrial stage of two amphibians by raising juvenile wood frogs (Rana sylvatica) and American toads (Bufo americanus) at six densities in terrestrial enclosures. Density had strong negative effects on survival, growth and reproductive development in both species. We fitted a priori recruitment functions to describe the relationship between initial density and the density of survivors after one year, and determined the functional relationship between initial density and mass after one year. Animals raised at the lowest densities experienced growth and survival rates that were over twice as great as those raised at the highest density. All female wood frogs in the lowest density treatment showed signs of reproductive development, compared to only 6% in the highest density treatment. Female American toads reached minimum reproductive size only at low densities, and male wood frogs and American toads reached maturity only in the three lowest density treatments. Our results demonstrate that in the complex life cycle of amphibians, density in the terrestrial stage can reduce growth, survival and reproductive development and may play an important role in amphibian population regulation. We discuss the implications of these results for population regulation in complex life cycles and for amphibian conservation.     

Host life history responses to parasitism

Parasites and their infections can adversely effect a host's growth, reproduction and survival. These effects are often not immediate, but increase with time since infection. A general prediction from evolutionary biology is that hosts suffering from this type of infection should preferentially allocate resources towards reproduction, even if this is at the expense of their growth and survival. This review illustrates this argument with several empirical studies showing hosts behaving in this manner. These studies indicate that one way for hosts to reduce the costs of parasitism is by altering their life history traits to bring forward their schedule of reproduction.     

Warming erodes individual-level variability in life history responses to predation risk in larvae of the mayfly Cloeon dipterum

1. Warming and predation risk are ubiquitous environmental factors that can modify life histories and population dynamics of aquatic ectotherms. While separate responses to each of these factors are well understood, their joint effects on individual life histories and population dynamics remain largely unexplored. Current theory predicts that the magnitude of prey behavioural, physiological, and life history responses to predation risk should diminish with warming due to the reduced metabolic scope. However, empirical support for this prediction remains equivocal, and experiments covering a substantial proportion of individual prey ontogeny until maturation are lacking.
2. To fill these gaps, we ran a laboratory experiment to investigate how warming and non-consumptive predation risk influence life history responses in the larvae of the mayfly Cloeon dipterum, an aquatic insect with highly plastic development. We reared larvae of varying initial sizes at three temperatures (21, 24, and 27°C) in a risk-free environment and under predation risk signalled by chemical cues from dragonfly larvae (Aeshna cyanea), and followed their individual survival, growth, and development until emergence.
3. Some C. dipterum larvae substantially prolonged their development and the proportion of these slow individuals declined rapidly with temperature and increased with predation risk. We attribute this response to cohort splitting, a common life history strategy of aquatic insects and other taxa in unpredictable environment.
4. Growth, development, and maturation varied predictably with temperature in the fast larvae that did not prolong their development. They grew and developed faster but matured at smaller sizes with increasing temperature. Predation risk tended to slow down individual growth and development in line with the reduced metabolic scope hypothesis, but the differences were relatively minor and observable only at 21°C.
5. Survival to subimago increased with predation risk, possibly due to indirect effects mediated by dissolved micronutrients, but did not vary significantly with temperature. Survival also tended to be higher in the slow individuals. This partly compensated for a smaller final size relative to the fast individuals and made both strategies comparable in overall fitness.
6. Our results show that warming may erode individual-level variability in life history responses to predation risk. This implies that warming can synchronise population dynamics and consequently make such populations more vulnerable to unpredictable disturbances.

     

Morphological plasticity in the tropical sponge Anthosigmella varians: responses to predators and wave energy

The goal of the research presented here was to examine phenotypic plasticity exhibited by three morphotypes of the common Caribbean sponge Anthosigmella varians (Duchassaing & Michelotti). We were interested in examining the biotic (and, to a lesser extent, abiotic) factors responsible for branch production in this species. We also tested the hypothesis that the skeleton may serve an antipredator function in this sponge, focusing on vertebrate fish predators (i.e., angelfish) in this work. In transplant and caging experiments, unprotected forma varians replicates were immediately consumed by angelfish, while caged replicates persisted on the reef for several months. These findings support the hypothesis that predators (and not wave energy) restrict forma varians to lagoonal habitats. Branch production was not observed in A. varians forma incrustans when sponges were protected from predators or placed in predator-free, low-wave-energy environments. It is not clear from our work whether forma incrustans is capable of producing branches (i.e., whether branch production is a plastic trait in this morph). Additional field experiments demonstrated that A. varians forma varians increased spicule concentrations, compared to uninjured sponges, in response to artificial predation events, and A. varians forma rigida reduced spicule concentrations, compared to uncaged controls, when protected from predators. These findings indicate that spicule concentration is a plastic morphological trait that can be induced by damage, and that A. varians may be able to reduce spicule concentrations when environmental conditions change (e.g., in the absence of predators). The potential significance of inducible defenses and structural anti-predator defenses in sponges is discussed in relation to recent work on sponge chemical defenses.     

Morphological abnormalities in anurans from southern Brazil

In recent years, the progressive decline in populations of anuran amphibians has left many species increasingly vulnerable to extinction. The potential role of morphological abnormalities as a mechanism of this decline has attracted attention in many recent studies. We investigated the occurrence and frequency of morphological abnormalities in anurans from northern of the state of Rio Grande do Sul, Brazil. We sampled 1674 individuals from three different environments – forest, farmland and peri‐urban areas – between 2001 and 2017. We recorded 89 individuals with morphological abnormalities, with 12 different types of abnormality in 19 anuran species. We recorded nine types of abnormality in forest and seven in the farmland, with brachydactyly being the most common abnormality in both areas. Only three abnormalities were recorded in the peri‐urban area, and all three were equally frequent. Studies of morphological alterations provide important insights into the potential effects of environmental impacts on anuran populations and may be essential for the planning of effective conservation strategies.     

Fungal plant endosymbionts alter life history and reproductive success of aphid predators

Endosymbionts occur in most plant species and may affect interactions among herbivores and their predators through the production of toxic alkaloids. Here, we ask whether effects of mycotoxins produced by the symbiosis of the fungal endophyte Neotyphodium lolii and the grass Lolium perenne are transmitted to the aphidophagous ladybird Coccinella septempunctata when feeding on cereal aphids Rhopalosiphum padi on infected plants. The larval development of coccinellids was extended, while their survival was reduced when feeding exclusively on aphids from infected plants. Ladybirds developing on aphids from infected plants showed reduced fecundity and impaired reproductive performance. Body size and symmetries of ladybird adults were not affected by the endophytes. Consistently strong, negative effects of endophytes on the lifetime performance of ladybirds indicates that mycotoxins are transmitted along food chains, causing significant damage for top predators. Such cascading effects will influence the population dynamics of aphid predators in the long term and could feedback to the primary plant producers.     

The dynamics of predation risk assessment: responses of anuran larvae to chemical cues of predators

1. While the antipredator behaviour of prey has been well studied, little is known about the rules governing the predation risk assessment of prey. In this study, I measured the activity levels of predator-naive green frog (Rana clamitans) tadpoles during and after exposures to the chemical cue of predatory larval dragonflies (Anax spp.). I then used the lengths of the time lags from the end of the cue exposures until the tadpoles returned to a control level of activity as an index of the perceived risk of the tadpoles. 2. While tadpoles always responded upon exposure to the Anax chemical cue by strongly reducing their activity level, their perceived risk increased asymptotically over time during the initial period of the cue exposure. Tadpoles of all size classes perceived increasing risk in proportion to chemical cue concentration, but the length of time that tadpoles responded during cue exposure and the length of their post-exposure time lags decreased with increasing body mass. 3. The results suggest that the perceived risk of green frog tadpoles varies over time and does not correspond directly to their behavioural response (i.e. activity level). However, their perceived risk does appear to vary in accordance with the predation risk associated with the Anax chemical cue and the reliability of the information from the cue, and therefore may be predictable.     

Variation in life history responses of Daphnia to toxic Microcystis aeruginosa

Three clones of Daphnia pulex and two clones of Daphnia longispinawere exposed to toxic Microcystis aeruginosa for 21 days ina lifetable experiment. The growth and reproduction of individualdaphnids were followed daily to study the long-term effectsof toxic Microcystis. Exposure to Microcystis increased mortality,decreased growth, delayed maturation and decreased offspringproduction, indicating nutritional deficiency and toxic effects.We found variation in life history responses between speciesand among clones. Our results suggest that toxic cyanobacteriamay act as a modifying agent in zooplankton communities at boththe species and clonal level.     

Colonization dynamics and life history traits of seven Daphnia pulex genotypes

Summary A series of experiments revealed significant differences in the potential ability of seven Daphnia pulex genotypes to colonize two lakes in which this species does not naturally reside. Life table experiments, in which individuals from each genotype were raised separately on water and natural phytoplankton from the two lakes, revealed several significant differences among genotypes in life history traits, including age and size at first reproduction, clutch size and offspring body size. Significant differences among genotypes were also found in mean genotype fitness and rate of population increase, although all genotypes were able to increase in absolute numbers. Significant genotypexlake interaction was found for several life history traits and mean fitness, indicating that the relative success of invading genotypes may depend on habitat characteristics. Enclosure experiments, in which all seven genotypes were introduced together into enclosures in both lakes, revealed that some genotypes increased greatly while others declined in relative abundance, and that the most successful genotypes differed between lakes. In addition, the most successful genotypes in the enclosures were not necessarily the genotypes that displayed the highest fitness in the life table experiments, possibly because individuals in the enclosures competed for food resources, leading to exclusion of certain genotypes.     

Understanding chilling responses in Arabidopsis seeds and their contribution to life history

Winter chilling is of central importance in the phenology of temperate annual and perennial plants. Chilling accelerates flowering through the process of vernalization and breaks both bud and seed dormancy, permitting the onset of growth in the spring. The quantitative effects of chilling in floral promotion in winter annual Arabidopsis accessions are well-documented, but very little is known about the basic physiology underlying summer annual responses to winter chilling, which acts on seeds within the soil seed bank. Here, we analyse the response of wild accessions to extended chilling in seeds, and explore the interaction between seed-maturation temperature and chilling responses. We show that two weeks of chilling induces secondary dormancy, and that this time period is not dependent on seed-maturation temperature. In addition, we found that seeds for most accessions set under simulated summer conditions in the laboratory are unable to overwinter in the soil seed bank, as they germinate without light during extended chilling treatments. This shows that these seeds are committed to re-establishment in the same growing season. Understanding how winter chilling affects the timing of Arabidopsis phenology will enable us to explore the genetics behind adaptation to changing climates, and inform rational approaches to breeding crops with improved performance under new climate scenarios and develop a systems ecology of Arabidopsis.     

Dispersal strategies in sponge larvae: integrating the life history of larvae and the hydrologic component

While known to be uniformly non-feeding, short-lived, and potentially short dispersing, sponge larvae display different behaviours (swimming ability and taxis). Our aim was to show whether sponge larvae with different behaviours exhibit different dispersal strategies under variable intensity of water movements. We first assessed the distribution of larvae of six taxa: Dictyoceratida spp., Dysidea avara, Crambe crambe, Phorbas tenacior, Scopalina lophyropoda, and Cliona viridis, collected through plankton sampling, and the abundance of the corresponding adult sponges across three hard bottom communities and a sandy bottom from a north-west Mediterranean rocky shore. We then tested adult–larvae couplings (abundance of larvae vs abundance of adults) under increasing levels of water movements (surge) to assess the importance of this environmental factor in driving differences in dispersal strategies. Adults of Dictyoceratida spp., D. avara, and P. tenacior were most abundant in semi-dark caves (SDC), C. crambe and C. viridis in communities of sciaphilic algae (SA), whereas the distribution of S. lophyropoda was extremely patchy, being present almost only in the SA community of one of the five stations studied. Larvae of Dictyoceratida spp. and P. tenacior were more abundant in the SDC, whereas D. avara and C. crambe were homogeneously distributed across the communities. The larvae of C. viridis were more abundant in the SA communities and the S. lophyropoda larvae were mostly present in one station and one community (SA). Increased water movement did not modify the adult–larvae coupling for Dictyoceratida spp., D. avara, and C. crambe, whereas it broke up the positive association for P. tenacior and to some extent S. lophyropoda. For C. viridis, possible variability in adult–larvae coupling was not tested because the larvae were collected on only one day under calm sea conditions. We confirm that efficient-swimming larvae with some cue response can actively counteract hydrodynamic forces and highlight the importance of both larval behaviour and environmental conditions in determining small-scale patterns of dispersal.     

A comparative study of activity levels in larval anurans and response to the presence of different predators

Activity level is a key behavioral trait in many animals whichmediates a trade-off between finding food and avoiding predation.Optimal activity level will therefore depend on environment,and plasticity in response may increase fitness (if an organismencounters multiple environments in a lifetime). One groupin which activity level, and its relationship to foraging andpredation risk, has been well studied is larval anurans. Anuransinhabit a range of distinct freshwater aquatic community typesthat are created by differences in pond permanency and toppredator. Species segregate across these pond types and thereforetadpoles from different species encounter different selection regimes. I hypothesized that species from different pond typeswould therefore differ in activity behavior, and in plasticityof this behavior. I tested this in a phylogenetic frameworkto consider the evolution of plasticity in anurans diversifyinginto different pond types. Time spent active was quantifiedfor larvae of each of 13 anuran species (from three taxonomicfamilies) in four conditions: when no predator was present,and in the non-lethal presence of a dragonfly, newt, or fishpredator. Species nested within pond type by taxonomic familydiffered significantly in time spent active. A significant interaction between predator treatment and taxonomic familywas also observed. A phylogenetic analysis of change in behaviorrevealed strong positive correlations in evolution of thesebehaviors and suggests constraints on the ability of larvalanurans to independently modify activity levels in the presenceversus absence of predators.     

Evolutionary responses of Drosophila melanogaster life history to differences in larval density

The study examined the effects of evolution at two different larval densities on pre-adult and adult fitness traits. Five replicate selection lines each were cultured at either 50 or 150 larvae per vial, avoiding selection on development time, age at breeding or for adaptation to adult density, one or more of which factors has been a confounding variable in previous studies. Low density selection lines evolved extended development times at both growth densities. The extended development times were associated with greater adult body size at the lower growth density only, and particularly in females. The lines did not differ significantly in larval competitive ability at either growth density. At neither growth density did the early adult fertility of females or the lifespan of either sex differ between the lines from the two selection regimes, but at the lower growth density the late fertility of low density line females was significantly enhanced. The results suggest that larval density does have important effects on the expression and resolution of life history trade-offs in Drosophila melanogaster, but that these may be somewhat different from those reported in previous studies.     

Facilitation of fisheries by natural predators depends on life history of shared prey

Predators commonly share prey with human exploiters, intuitively suggesting that there is an inherent human–predator conflict through competition for prey. Here we studied the effects of fishing and predation mortality on biomass distributions and yields of shared prey using a size‐structured model of competing populations, describing the life histories of Baltic Sea sprat and herring. Whereas both species responded in a similar fashion to increased fishing mortality, with decreasing juvenile and adult biomasses, we found that responses to predation mortality differed between species. Sprat only display weak compensatory responses with increasing predation mortality, while over a substantial range of mortalities there was a strong increase in adult (and total) herring biomass, i.e. overcompensation. The observed biomass overcompensation results from relaxed intraspecific competition as predation mortality increased, allowing for faster individual growth rates that in turn lead to a change in population composition (juvenile:adult biomass ratio). Our results suggest that the potential for biomass overcompensation is higher for species exhibiting substantial growth after maturation. Differences in size‐selectivity of predators and fishing mortality resulted in a positive effect of predation mortality on fisheries yields, which can be explained by an overcompensatory response in adult herring biomass. Thus, somewhat counter intuitive, our results suggest that fishermen, depending on prey life history, may actually benefit from allowing for a higher abundance of predators, despite competing for shared prey.     

Divergent phenotypic responses to predators and cyanobacteria in Daphnia lumholtzi

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