Ontogeny, phylogeny, and morphology in anuran larvae: morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae)

Comparative studies of chondrocranial morphology in larval anurans are typically qualitative in nature, focusing primarily on discrete variation or gross differences in the size or shape of individual structures. Detailed data on chondrocranial allometry are currently limited to only two species, Rana sylvatica and Bufo americanus. This study uses geometric morphometric and multivariate statistical analyses to examine interspecific variation in both larval chondrocranial shape and patterns of ontogenetic allometry among six species of Rana. Variation is interpreted within the context of hypothesized phylogenetic relationships among these species. Canonical variates analyses of geometric morphometric datasets indicate that species can be clearly discriminated based on chondrocranial shape, even when whole ontogenies are included in the analysis. Ordinations and cluster analyses based on chondrocranial shape data indicate the presence of three primary groupings (R. sylvatica; R. catesbeiana + R. clamitans; and R. palustris + R. pipiens + R. sphenocephala), and patterns of similarity closely reflect phylogenetic relationships. Analysis of chondrocranial allometry reveals that some patterns are conserved across all species (e.g., most measurements scale with negative allometry, those associated with the posterior palatoquadrate tend to scale with isometry or positive allometry). Ontogenetic scaling along similar allometric trajectories, lateral transpositions of individual trajectories, and variable allometric relationships all contribute to shape differences among species. Overall patterns of similarity among ontogenetic trajectories also strongly reflect phylogenetic relationships. Thus, this study demonstrates a tight link between ontogeny, phylogeny, and morphology, and highlights the importance of including both ontogenetic and phylogenetic data in studies of chondrocranial evolution in larval anurans.     

Broad-scale spatial patterns of canopy cover and pond morphology affect the structure of a Neotropical amphibian metacommunity

Spatial and environmental processes influence species composition at distinct scales. Previous studies suggested that the distribution of larval anurans at the landscape-scale is influenced by environmental gradients related to adult breeding site selection, such as pond canopy cover, but not by water chemistry. However, the combined effects of spatial, pond morphology, and water chemistry variables on metacommunity structure of larval anurans have not been analyzed yet. We used a partial redundancy analysis with variation partitioning to analyze the relative influence of pond morphology (e.g., depth, area, and aquatic vegetation), water chemistry, and spatial variables on a tadpole metacommunity from southeastern Brazil. We predict that pond morphology and canopy cover will influence the metacommunity at broad spatial scales, while water chemistry would play a larger role at finer scales. We found that broad-scale spatial patterns of pond canopy cover and pond morphology strongly influenced metacommunity structure, with water chemistry being not significant. Additionally, species composition was spatially autocorrelated at short distances. We suggest that the reproductive behavior of adult anurans is driving tadpole metacommunity dynamics, since pond morphology, but not water chemistry affects breeding site selection by adults. Our results contribute to the understanding of amphibian species diversity in tropical wetlands.     

Wingtip shape and flight performance in the European Starling Sturnus vulgaris

Although wingform is known to differ among individuals of the same species it is not known how intraspecific variation in wingtip shape is associated with flight performance. In this study, we have examined both among- and within-individual variation in wingtip shape in relation to changes in flight performance in the European Starling Sturnus vulgaris . We found that level flapping-flight speed and the ability to negotiate an aerial obstacle course were unrelated to wingtip shape. However, take-off parameters did vary with wingtip shape; birds with more rounded wingtips tended to take off from the ground at a steeper angle of ascent than those with relatively more pointed wingtips. The same relationships between wingtip morphology and flight were present in both the inter- and intra-individual experimental analyses. The evolutionary importance of this variation in take-off ability is discussed in terms of predator avoidance and enhancement of individual survival.     

Predator-driven phenotypic diversification in Gambusia affinis

Predation is heterogeneously distributed across space and time, and is presumed to represent a major source of evolutionary diversification. In fishes, fast-starts--sudden, high-energy swimming bursts--are often important in avoiding capture during a predator strike. Thus, in the presence of predators, we might expect evolution of morphological features that facilitate increased fast-start speed. We tested this hypothesis using populations of western mosquitofish (Gambusia affinis) that differed in level of predation by piscivorous fish. Body morphology of G. affinis males, females, and juveniles diverged in a consistent manner between predatory environments. Fish collected from predator populations exhibited a larger caudal region, smaller head, more elongate body, and a posterior, ventral position of the eye relative to fish from predator-free populations. Divergence in body shape largely matched a priori predictions based on biomechanical principles, and was evident across space (multiple populations) and time (multiple years). We measured maximum burst-swimming speed for male mosquitofish and found that individuals from predator populations produced faster bursts than fish from predator-free populations (about 20% faster). Biomechanical models of fish swimming and intrapopulation morphology-speed correlations suggested that body shape differences were largely responsible for enhanced locomotor performance in fish from predator populations. Morphological differences also persisted in offspring raised in a common laboratory environment, suggesting a heritable component to the observed morphological divergence. Taken together, these results strongly support the hypothesis that divergent selection between predator regimes has produced the observed phenotypic differences among populations of G. affinis. Based on biomechanical principles and recent findings in other species, it appears that the general ecomorphological model described in this paper will apply for many aquatic taxa, and provide insight into the role of predators in shaping the body form of prey organisms.     

Thermal acclimation of interactions: differential responses to temperature change alter predator-prey relationship

Different species respond differently to environmental change so that species interactions cannot be predicted from single-species performance curves. We tested the hypothesis that interspecific difference in the capacity for thermal acclimation modulates predator-prey interactions. Acclimation of locomotor performance in a predator (Australian bass, Macquaria novemaculeata) was qualitatively different to that of its prey (eastern mosquitofish, Gambusia holbrooki). Warm (25°C) acclimated bass made more attacks than cold (15°C) acclimated fish regardless of acute test temperatures (10-30°C), and greater frequency of attacks was associated with increased prey capture success. However, the number of attacks declined at the highest test temperature (30°C). Interestingly, escape speeds of mosquitofish during predation trials were greater than burst speeds measured in a swimming arena, whereas attack speeds of bass were lower than burst speeds. As a result, escape speeds of mosquitofish were greater at warm temperatures (25°C and 30°C) than attack speeds of bass. The decline in the number of attacks and the increase in escape speed of prey means that predation pressure decreases at high temperatures. We show that differential thermal responses affect species interactions even at temperatures that are within thermal tolerance ranges. This thermal sensitivity of predator-prey interactions can be a mechanism by which global warming affects ecological communities.     

Thermal plasticity of diving behavior, aquatic respiration, and locomotor performance in the Mary River turtle Elusor macrurus

Locomotion is a common measure of performance used in studies of thermal acclimation because of its correlation with predator escape and prey capture. However, for sedentary animals such as freshwater turtles, we propose that diving behavior may be a more ecologically relevant measure of performance. Increasing dive duration in hatchling turtles reduces predator exposure and therefore functions as an ecological benefit. Diving behavior is thermally dependent, and in some species of freshwater turtles, it is also reliant on aquatic respiration. This study examined the influence of thermal acclimation on diving behavior, aquatic respiration, and locomotor performance in the endangered, bimodally respiring Mary River turtle Elusor macrurus. Diving behavior was found to partially acclimate at 17 degrees C, with turtles acclimated to a cold temperature (17 degrees C) having a significantly longer dive duration than hatchlings acclimated to a warm temperature (28 degrees C). This increase in dive duration at 17 degrees C was not a result of physiological alterations in metabolic rate but was due instead to an increase in aquatic oxygen consumption. Increasing aquatic oxygen consumption permitted cold-acclimated hatchlings to remain submerged for significantly longer periods, with one turtle undertaking a dive of over 2.5 d. When burst-swimming speed was used as the measure of performance, thermal acclimation was not detected. Overall, E. macrurus demonstrated a partial ability to acclimate to changes in environmental temperature.     

Predator–prey interactions in anurans of the tropical dry forests of the Colombian Caribbean: A functional approach

Anuran–prey selection might be mediated by traits, either by mismatches in predator and prey traits (preventing interactions) or by predator selection of prey traits (encouraging interactions). These effect traits could be summarized in two contrasting foraging strategies: “active” and “sit-and-wait” foragers. We evaluated whether anurans could be classified into groups of species sharing traits associated with their diet, and what is the relation between particular effect traits of anurans and their prey. We collected anurans and identified their stomach contents once during dry, minor, and major rain seasons in six dry forest sites in the Colombian Caribbean. For each of the 19 anuran species and 436 prey items, we registered six effect traits. We applied RLQ and fourth-corner methodologies to relate predator and prey traits through their interaction matrix. Predators were assigned to five groups according to their differences in locomotion, body shape, proportion of the jaw width, mode of tongue protrusion, and strata preferred. Regarding preys, species were assigned to four groups according to their gregariousness, body shape and hardness, defensive traits, and mobility. Body size of both, predators and prey, had a minor contribution in the group assignment. We found that predators using active search target low-mobility preys, whereas species using sit-and-wait strategy target highly nutritive prey that are difficult to manipulate. By linking amphibian diet with foraging strategies, we hope to contribute to the understanding of mechanisms behind anuran–prey food web patterns and to build more realistic models of functional response to changing environments.     

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.     

Hotspot of Adult Cuban Treefrog and Cane Toad Multi-organ Abnormality in Suburban South-west Florida

This study represents a continuation of the Florida hotspot of tadpole abnormality found in the Southwest Florida suburban roadside drainage ditches in 2012 to determine if the adult frogs and toads frequenting the study sites were anatomically abnormal. The gross examination of all organs included 397 adult anurans and 40 metamorphs representing five anuran species:Osteopilus septentrionalis(N=364), Rhinella marina(N=60), Lithobates sphenocephala(N=7), Anaxyrus terrestris(N=5) and Anaxyrus americanus(N=1). The gonads, liver, kidney and intestines were abnormal at a frequency of 87.4%. The few normal anurans(12.6%) were females and young male adults. We found a significant difference in organ abnormality type and f requency between sexes. Almost all f rog and toad males had testicular abnormality(92%) with only 6% with normal testes, whereas the female gonad abnormality was lower,at 41.6%. Hermaphroditism was found in both sexes at a frequency of 26.2%. The toads had a significantly higher frequency of hermaphroditism than the frogs. The toad hermaphroditism frequency was found to be 40%,whereas the frog hermaphroditism 23.3%. A hermaphrodite Cane toad male with a female phenotype coexisted with the normal male phenotype hermaphrodite. The fertility of 27 in situ pairs was assessed. The fertile testicular abnormal male and hermaphrodite pairs produced offspring with abnormal larval morphology. This information adds new evidence of the effect of chemicals on wild populations and the effect on non-target species which has always been underestimated.     

Relaxed predation results in reduced phenotypic integration in a suite of dragonflies

Although changes in magnitude of single traits responding to selective agents have been studied intensively, little is known about selection shaping networks of traits and their patterns of covariation. However, this is central for our understanding of phenotypic evolution as traits are embedded in a multivariate environment with selection affecting a multitude of traits simultaneously rather than individually. Here, we investigate inter‐ and intraspecific patterns of trait integration (trait correlations) in the larval abdomen of dragonflies as a response to a change in predator selection. Species of the dragonfly genus Leucorrhinia underwent a larval habitat shift from predatory fish to predatory dragonfly‐dominated lakes with an associated relaxation in selection pressure from fish predation. Our results indicate that the habitat‐shift‐induced relaxed selection pressure caused phenotypic integration of abdominal traits to be reduced. Intraspecific findings matched patterns comparing species from both habitats with higher abdominal integration in response to predatory fish. This higher integration is probably a result of faster burst swimming speed. The abdomen holds the necessary morphological machinery to successfully evade predatory fish via burst swimming. Hence, abdominal traits have to function in a tight coordinated manner, as maladaptive variation and consequently nonoptimal burst swimming would cause increased mortality. In predatory dragonfly‐dominated lakes, no such strong link between burst swimming and mortality is present. Our findings highlight the importance of studying multivariate trait relationships as a response to selection for understanding patterns of phenotypic diversification.     

Morphology and escape performance of tiger salamander larvae (Ambystoma tigrinum mavortium)

The ability of an individual to escape predators is an important component of fitness. Several adaptive explanations of body shape variation in amphibians hypothesize relationships between swimming performance and morphology, but these ideas have rarely been tested. Here we investigate bivariate and multivariate relationships between natural variation in morphology and performance. We used high-speed video to examine fast-starts associated with escape responses in small tiger salamander larvae (Ambystoma tigrinum). Our results indicate that performance is influenced by interactions among aspects of morphology, physiology, and behavior. Relationships between morphometric variables and velocity could be detected with multivariate, but not bivariate statistical analyses. In particular, relationships between morphology and velocity depend on tail beat frequency (potentially a measure of effort or vigor). Relationships between morphology and acceleration were detected with bivariate analyses, but multivariate analysis suggests that acceleration performance, too, depends on interactions between morphology and tail beat frequency. We found a positive relationship between tail area and propulsive performance, which supports adaptive interpretations of variation in larval tail shape within and between amphibian species.     

Morphological correlates of burst speed and field movement patterns: the behavioural adjustment of locomotion in wall lizards (Podarcis muralis)

Locomotion of lizards has clear morphological determinants and is important for developing activities such as feeding, social interaction and predator avoidance. Thus, morphological variation is believed to have fitness consequences through affecting locomotor performance. This paper firstly evaluates the dependence of burst speed on morphology, and secondly examines the movement patterns of free-ranging undisturbed wall lizards ( Podarcis muralis ) engaged in several kinds of activity. Body size was the most important correlate of burst speed as performed at the optimal temperature for running in the laboratory. After removing size effects from performance and morphological traits, the length of some particular limb segments had positive influence on burst speed, but these effects were weak, each trait explaining less than 16% of variance in burst speed. Free-ranging P. muralis exhibited intermittent locomotion, with movement sequences interrupted by frequent short pauses. Field movement patterns greatly differed depending upon the kind of activity and were in most aspects independent of the size and sex of the animal. P. muralis involved in thermoregulation performed short and low-speed displacements; exploratory activities were characterized by frequent, slow and short movements. On the contrary, lizards involved in intraspecific pursuits and predator escape developed comparatively high speeds, although only exceptionally did they attain the size-specific burst speed predicted from the laboratory trials. Speed of escape increased with distance to the refuge and the animals are able to assess predation risks to modulate approach distance, speed and pauses, so maximum exertion is seldom required. The evolution of locomotor capacities exceeding routine needs is discussed in the context of the principle of 'excessive construction'.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 135–146.     

A Large-Scale Pattern of Ontogenetic Shape Change in Ray-Finned Fishes

Fishes exhibit a remarkable diversity of body shape as adults; however, it is unknown whether this diversity is reflected in larval stage morphology. Here we investigate the relationship between larval and adult body shape as expressed by body elongation. We surveyed a broad range of ray-finned fish species and compared body shape at larval and adult stages. Analysis shows that the vast majority of fish are more elongate at the larval stage than at the adult stage, and that adults display greater interspecies variation than larvae. We found that the superorder Elompomorpha is unique because many species within the group do not follow the observed elongation trends. These results indicate that much of the diversity observed in adults is achieved in post-larval stages. We suggest that larval morphology is subject to common constraints across the phylogeny.     

Morphological convergence during pregnancy among predator and nonpredator populations of the livebearing fish Brachyrhaphis rhabdophora (Teleostei: Poeciliidae)

Predation can drive morphological divergence in prey populations, although examples of divergent selection are typically limited to nonreproductive individuals. In livebearing females, shape often changes drastically during pregnancy, reducing speed and mobility and enhancing susceptibility to predation. In the present study, we document morphological divergence among populations of nonreproductive female livebearing fish (Brachyrhaphis rhabdophora) in predator and nonpredator environments. We then test the hypothesis that shape differences among nonreproductive females are maintained among reproductive females between predator and nonpredator environments. Nonreproductive females in predator environments had larger caudal regions and more fusiform bodies than females in nonpredator environments; traits that are associated with burst speed in fish. Shape differences were maintained in reproductive females, although the magnitude of this difference declined relative to nonreproductive females, suggesting morphological convergence during pregnancy. Phenotypic change vector analysis revealed that females in predator environments became more similar to females in nonpredator environments in the transition from nonreproductive to reproductive. Furthermore, the level of reproductive allocation affected shape similarly between predator environments. These results suggest a life‐history constraint on morphology, in which predator‐driven morphological divergence among nonreproductive B. rhabdophora is not maintained at the same level during pregnancy. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 386–392.     

Ontogeny of the Thyroid Glands During Larval Development of South American Horned Frogs (Anura,Ceratophryidae)

The role of thyroid hormone (TH) in anuran metamorphosis has been documented from a variety of approaches, but the sequence of morpho-histological development of the thyroid glands that produce the secretion of the hormone was assumed invariant from studies of relatively few species even when the effects of environmental influences on larval development and metamorphosis have been largely documented. There are anurans in which developmental and growth rates diverge, and the resulting heterochrony in growth and development produces giant/miniature tadpoles, and or rapid/delayed metamorphosis suggesting changes of the activity of the thyroid glands during larval development. Herein, we analyze the morpho-histological variation of the thyroid glands in larval series of Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis and L. llanensis that share breeding sites along semiarid environments of the Chaco in South America, belong to a monophyletic lineage, and present accelerated patterns in growth and development in order to have a morphological evidence about a possible shift of TH physiology. We describe gross morphology and histology of the thyroid glands and find features shared by all studied species such as the presence of supernumerary heterotopic follicles; changes in the volume and number of follicles towards the metamorphic climax, and cuboidal epithelia with occasional intra-cellular vacuoles as signs of low glandular activity without a manifest peak at the climax as it was assumed for anurans. We discuss different lines of evidence to interpret sources of extra supplement of TH to support the rapid metamorphosis. These interpretations highlight the necessity to design a research program to investigate the endocrine variation during development of ceratophryids taking in account their morphology, physiology and ecology in order to learn more about the effects of environmental and developmental interactions involved in the anuran evolution.     

Head shape variation in cerambycid saproxylic beetles as a function of host plant selection

Saproxylic insects depend on deadwood for larval development, and a certain degree of specialization may be involved in their choice of host plants and/or wood in a particular stage of degradation. The plant species chosen for oviposition in turn act as an environmental pressure on the head morphology of larvae and it is expected that head shape plasticity varies directly with the number of woody plant species used for larval development in each insect species. We analyzed head shape variation in saproxylic beetles with respect to host plant species, maximum time of larval emergence and season of the year when insects colonized branches. Generalist species in the use of host plants showed significant variation in head shape and size. Time of emergence and season did not appear to affect head shape, although season was a determinant factor of abundance and possibly head size variation.     

The advantage of no defense: predation enhances cohort survival in a desert amphibian

The impacts that predators have on prey behavior, growth, survival, and ultimately the composition of many ecological communities are mediated by prey defenses and the susceptibility of prey to predators. We hypothesized that prey populations inhabiting short-lived, species-poor, aquatic environments should lack significant morphological, developmental, and behavioral responses to predators and are therefore highly susceptible to predation. Furthermore, we predicted that the resultant decrease in prey density and increase in per capita resources due to high susceptibility to predators should enhance overall cohort survival because of enhanced growth of surviving prey. To test these ideas, we performed laboratory and outdoor mesocosm experiments to disentangle multiple effects of predators on an anuran (Scaphiopus couchii); a species highly adapted to breeding in ephemeral habitats and that has one of the shortest larval periods of all anurans. Chemical (presence of predator) and lethal predator cues (predator plus consumed conspecific) elicited no response in behavior, development, or morphology, indicating a lack of defensive mechanisms. Survivorship was significantly reduced in treatments where tadpoles were exposed to predators. However, this reduction in prey density led to accelerated time to metamorphosis, conferring an advantage to survivors who must metamorphose before ephemeral ponds dry. Our experiments demonstrated that in short-lived environments, prey may exhibit little or no response to the presence of predators presumably because selection for anti-predator defenses is countered by selection for rapid metamorphosis. However, predation actually resulted in an increase in overall cohort survival. Although predators are relatively rare in highly ephemeral aquatic environments, they may play an important role in facilitating the long-term persistence of their prey by reducing prey density.     

Interacting effects of predation risk and resource level on escape speed of amphibian larvae along a latitudinal gradient

Fast‐growing genotypes living in time‐constrained environments are often more prone to predation, suggesting that growth‐predation risk trade‐offs are important factors maintaining variation in growth along climatic gradients. However, the mechanisms underlying how fast growth increases predation‐mediated mortality are not well understood. Here, we investigated if slow‐growing, low‐latitude individuals have faster escape swimming speed than fast‐growing high‐latitude individuals using common frog (Rana temporaria) tadpoles from eight populations collected along a 1500 km latitudinal gradient. We measured escape speed in terms of burst and endurance speeds in tadpoles raised in the laboratory at two food levels and in the presence and absence of a predator (Aeshna dragonfly larvae). We did not find any latitudinal trend in escape speed performance. In low food treatments, burst speed was higher in tadpoles reared with predators but did not differ between high‐food treatments. Endurance speed, on the contrary, was lower in high‐food tadpoles reared with predators and did not differ between treatments at low food levels. Tadpoles reared with predators showed inducible morphology (increased relative body size and tail depth), which had positive effects on speed endurance at low but not at high food levels. Burst speed was positively affected by tail length and tail muscle size in the absence of predators. Our results suggest that escape speed does not trade‐off with fast growth along the latitudinal gradient in R. temporaria tadpoles. Instead, escape speed is a plastic trait and strongly influenced by the interaction between resource level and predation risk.