Naturally occurring variation in tadpole morphology and performance linked to predator regime

Divergent natural selection drives a considerable amount of the phenotypic and genetic variation observed in natural populations. For example, variation in the predator community can generate conflicting selection on behavioral, life‐history, morphological, and performance traits. Differences in predator regime can subsequently increase phenotypic and genetic variations in the population and result in the evolution of reproductive barriers (ecological speciation) or phenotypic plasticity. We evaluated morphology and swimming performance in field collected Bronze Frog larvae (Lithobates clamitans) in ponds dominated by predatory fish and those dominated by invertebrate predators. Based on previous experimental findings, we hypothesized that tadpoles from fish‐dominated ponds would have small bodies, long tails, and large tail muscles and that these features would facilitate fast‐start speed. We also expected to see increased tail fin depth (i.e., the tail‐lure morphology) in tadpoles from invertebrate‐dominated ponds. Our results support our expectations with respect to morphology in affecting swimming performance of tadpoles in fish‐dominated ponds. Furthermore, it is likely that divergent natural selection is playing a role in the diversification on morphology and locomotor performance in this system.     

不同程度的尾损伤对镇海林蛙(Rana zhenhaiensis)蝌蚪游泳速度的影响

无尾两栖类蝌蚪的尾巴通过产生强大的游泳速度在反捕食中起到了重要的作用。以镇海林蛙(Rana zhenhaiensis)蝌蚪为实验动物来评估断尾的运动代价。以74尾具有完整尾蝌蚪作为实验组,通过截去不同尾长片段,人为分成轻微尾损伤组(30%)和严重尾损伤组(30%)并测定两组蝌蚪在断尾前后的游泳速度。以16尾完整尾蝌蚪作为对照组在实验组断尾前后同时进行游泳速度的测定。实验结果显示断尾影响蝌蚪的游泳速度,但仅在尾损伤程度达到尾长的30%以上时才产生不利的影响。这表明轻微尾损伤并不对镇海林蛙蝌蚪的游泳速度产生严重影响。在断尾前后实验组蝌蚪的游泳速度均与尾长呈正相关。在相同尾长状态下,尾损伤蝌蚪的相对游泳速度明显快于完整尾蝌蚪。因此,尾损伤的镇海林蛙蝌蚪有可能通过改变尾和身体的摆动频次等方式在断尾后对游泳速度进行了一定的补偿。尾损伤在野外频繁发生于蝌蚪的尾远端,据此推测镇海林蛙蝌蚪在自然条件下的尾损伤并不会产生严重运动代价。     

Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation

In many amphibian larvae a suite of morphological and behavioural characters varies together in an induced defence against predators, but it remains unclear which features are functionally related to defence. We independently manipulated behaviour and morphology in tadpoles of Hyla versicolor and assessed their consequences for swimming performance and predator escape. Data on burst swimming showed that tadpoles which accelerated rapidly were elongate, with shallow bodies and tails. Predator escape was measured by exposing tadpoles to predators (larval Anax dragonflies or larval Ambystoma salamanders) and recording time until death. Tadpoles were first reared for 30 days in ponds containing either caged Anax or no predators; individuals responded to predators by developing large brightly coloured tails and short bodies. We placed tadpoles of both morphological phenotypes into plastic tubs, and manipulated their behaviour using food and chemical cues from predators. Mortality risk experienced by the predator‐induced phenotype was about half that of the no‐predator phenotype, and risk increased with time spent swimming. An interaction between morphology and behaviour arose because increasing activity caused higher risk for tadpoles with deep tail fins but not shallow tail fins.     

Fish and dragonfly nymph predators induce opposite shifts in color and morphology of tadpoles

Many prey species, including amphibian larvae, can adaptively alter coloration and morphology to become more or less conspicuous to predators. Despite abundant research on predator-induced plasticity in tadpoles, the combination of color and morphological responses to predators remains largely unexplored. We measured predator-induced morphological and color plasticity in tadpoles. We reared tadpoles of the neotropical treefrog Dendropsophus ebraccatus with dragonfly nymph or fish predators, or in a predator-free control. After 10 days, we digitally photographed tadpoles and measured eight morphometric variables and five tail color variables. Tadpoles reared with nymphs developed the largest and reddest tails, but incurred a developmental cost, being the smallest overall. Cues from fish induced an opposite tail phenotype in tadpoles, causing shallow achromatic tails. Control tadpoles developed intermediate tail phenotypes. This provides the first experimental evidence that tadpoles can shift both color and morphology in opposite, predator-specific directions in response to a fish and an odonate predator. Despite mean differences, however, there was substantial variation in the degree of phenotype induction across treatments. Tail redness was correlated with tail spot size, but not perfectly, indicating that color and morphology may be partially decoupled in D. ebraccatus . Balancing selection from multiple conflicting predators may result in genetic variation for developmental plasticity.     

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.     

Where to Live? How Morphology and Evolutionary History Predict Microhabitat Choice by Tropical Tadpoles

Tadpoles have diverse morphologies and occupy diverse habitats. The morphological differences between tadpoles can be represented by linear and geometric measurements and used to explain the organization of tadpole assemblages. However, the effects of evolutionary history must be isolated from the morphological differences before we can determine which patterns result from the use and sharing of common ecological resources. Here, we aimed to determine how morphological similarities and phylogenetic distances affect microhabitat choice by tadpoles. We analyzed the tadpoles of 101 anuran species and classified them according to ecomorphological guild, habitat use, position in the water column, and floor substrate. We used geometric and traditional morphometric approaches to describe the morphological variation among tadpoles and calculated the patristic distance for each species. Afterwards, we used morphometric and phylogenetic matrices as predictors of the variance in the ecological matrix, using a partial redundancy analysis. When we used traditional morphometric data, phylogeny explained a large amount of the ecological variation. By contrast, when we used geometric morphometric data, morphology and phylogeny explained similar amounts of the ecological variation, showing that the technique used to extract morphological variation affects the results. We provide evidence that both morphology, as a surrogate for contemporary factors, and evolutionary inertia are important in determining the behavior of tadpoles. Thus, niche conservatism can be important in modeling the behavior of tadpoles, but does not explain all the preferences of tadpoles.     

用功能生态学方法揭示峨眉髭蟾蝌蚪和棘腹蛙蟾蝌蚪共存的原因

采用功能生态学的研究方法,选取了3个指标(功能丰富度、功能定位和功能生态位的重叠程度)对峨眉山清音阁黑龙江中峨眉髭蟾蝌蚪和棘腹蛙蝌蚪共存的原因进行了解析。结果表明,峨眉髭蟾蝌蚪功能丰富度的实测值远远小于棘腹蛙蝌蚪。采用自助法随机抽样15和51个个体时,峨眉髭蟾蝌蚪的功能丰富度值显著小于棘腹蛙蝌蚪。同时,非参数多元方差分析的结果显示二者的功能定位存在显著差异。此外,二者功能生态位重叠程度的实测值与采用自助法计算所得值均极低。以上结果表明二者的功能生态位存在明显分化,表现为峨眉髭蟾蝌蚪个体较大,开口较小,眼间距较大,尾部发达且多采用背腹弯曲的游泳模式;而棘腹蛙蝌蚪开口较大,眼睛间距较小,尾部较为短小且多采用脊椎弯曲的游泳模式。鉴于功能性状可以反映生物体对生长环境的响应,推测两种蝌蚪主要栖息地的微生境也存在分化。     

Bat Species Comparisons Based on External Morphology: A Test of Traditional versus Geometric Morphometric Approaches

External morphology is commonly used to identify bats as well as to investigate flight and foraging behavior, typically relying on simple length and area measures or ratios. However, geometric morphometrics is increasingly used in the biological sciences to analyse variation in shape and discriminate among species and populations. Here we compare the ability of traditional versus geometric morphometric methods in discriminating between closely related bat species – in this case European horseshoe bats (Rhinolophidae, Chiroptera) – based on morphology of the wing, body and tail. In addition to comparing morphometric methods, we used geometric morphometrics to detect interspecies differences as shape changes. Geometric morphometrics yielded improved species discrimination relative to traditional methods. The predicted shape for the variation along the between group principal components revealed that the largest differences between species lay in the extent to which the wing reaches in the direction of the head. This strong trend in interspecific shape variation is associated with size, which we interpret as an evolutionary allometry pattern.     

Morphological convergence of shell shape in distantly related scallop species (Mollusca: Pectinidae)

Morphological convergence is a central concept in evolutionary biology, but convergent patterns remain under‐studied in nonvertebrate organisms. Some scallop species exhibit long‐distance swimming, a behaviour whose biomechanical requirements probably generate similar selective regimes. We tested the hypothesis that shell shape similarity in long‐distance swimming species is a result of convergent evolution. Using landmark‐based geometric morphometrics, we quantified shell shape in seven species representing major behavioural habits. All species displayed distinct shell shapes, with the exception of the two long‐distance swimmers, whose shells were indistinguishable. These species also displayed reduced morphological variance relative to other taxa. Finally, a phylogenetic simulation revealed that these species were more similar in their shell shape than was expected under Brownian motion, the model of character evolution that best described changes in shell shape. Together, these findings reveal that convergent evolution of shell shape occurs in scallops, and suggest that selection for shell shape and behaviour may be important in the diversification of the group. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163 , 571–584.     

Comparative morphology of pond,stream and phytotelm‐dwelling tadpoles of the South American Redbelly Toads (Anura: Bufonidae: Melanophryniscus)

We present a comprehensive review of larval morphology in the Neotropical toad genus Melanophryniscus. The taxa studied included 23 species with representatives of recognized phenetic groups and different larval ecomorphological guilds: pond, stream, and phytotelm‐dwelling tadpoles. Their external morphology variation is congruent with current phenetic arrangement based on adult features, but also reflects the habitat where larvae develop. Lotic tadpoles (i.e. M. tumifrons group and M. krauczuki) in general exhibit a more depressed body, a longer tail with lower fins, and larger oral discs than lentic forms (i.e. M. stelzneri group, M. moreirae, M. sanmartini, and M. langonei). Despite their peculiar, confined microhabitat, phytotelm larvae do not diverge markedly from non‐arboreal species. The distinctive features of all species are the presence of a pineal end organ and the placement of the intestinal reversal point at the left of the abdomen in typical larval stages. The buccal cavity and musculoskeletal anatomy are quite conserved between species, yet some characteristics differ from those of other bufonids. The presence of one pair of subhyoid muscles is apparently an exclusive trait of Melanophryniscus among Bufonidae. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 417–441.     

The evolution of sexually dimorphic tail feathers is not associated with tail skeleton dimorphism

Sexual selection can influence the evolution of sexually dimorphic exaggerated display structures. Herein, we explore whether such costly ornamental integumentary structures evolve independently or if they are correlated with phenotypic change in the associated skeletal system. In birds, elongate tail feathers have frequently evolved in males and are beneficial as intraspecific display structures but impart a locomotor/energetic cost. Using the sexually dimorphic tail feathers of several passeriform species as a model system, we test the hypothesis that taxa with sexually dimorphic tail feathers also exhibit sexual dimorphism in the caudal skeleton that supports the muscles and integument of the tail apparatus. Caudal skeletal morphology is quantified using both geometric morphometrics and linear morphometrics across four sexually dimorphic passeriform species and four closely related monomorphic species. Sexual dimorphism is assessed using permutational MANOVA. Sexual dimorphism in caudal skeletal morphology is found only in those taxa that exhibit active functional differences in tail use between males and females. Thus, dimorphism in tail feather length is not necessarily correlated with the evolution of caudal skeletal dimorphism. Sexual selection is sufficient to generate phenotypic divergence in integumentary display structures between the sexes, but these change are not reflected in the underlying caudal skeleton. This suggests that caudal feathers and bones evolve semi‐independently from one another and evolve at different rates in response to different types of selective pressures.     

Locomotion in Amphibian Larvae (or "Why Aren't Tadpoles Built Like Fishes?")

SYNOPSIS. A variety of morphological features that affect locomotiondistinguish larvae of the three living amphibian orders fromfishes and their larvae. The oddest amphibian larvae are anurantadpoles. With their globose bodies, concealed forelimbs, abruptlycompressed and terminally tapered tails, tadpoles not only differradically from fishes but they—unlike caecilians or salamanders—alsodiffer radically from their adults. Tadpoles typically haveless axial musculature and much simpler myotomes than fishes.Surprisingly, in terms of mechanical (propeller) efficiencyand maximum sprint speeds, tadpoles still perform as well asmany teleosts of comparable sizes. From a consideration of hydromechanics,no amphibian larvae appear to be designed for sustained swimmingat high speeds. High maneuverability, rather than sustainablespeed, are important for amphibian larval survival.Two key featuresof tadpoles are the absence of caudal vertebrae and unexposedpectoral appendages. With only a notochord to serve as a skeleton,the tadpole tail is extremely flexible. Because of this exceptionalflexibility, tadpoles can fold their tails up against the bodyand turn rapidly with virtually no displacement of their centerof mass. Caudal flexibility can be regulated by muscle activityin the tadpole to effect turning. Lateral appendages are notneeded for this movement and are free to develop directly intotheir adult morphology; the anterior ones develop under coverof an opercular fold where they do not contribute to drag. Acase is presented, based on the ecology of metamorphosis, thatanuran transformation should be as brief as possible. With nobone to resorb, metamorphosis of the anuran caudal appendagecan, indeed, be very rapid.The basic kinematics of constantvelocity straightforward swimming for tadpoles and salamanderlarvae is reviewed, as well as the kinematics and electromyographyof starting, stopping, and turning in tadpoles. An attempt ismade to relate swimming kinematics to the characteristic morphologiesof amphibian larvae. Swimming speed in Rana, Bufo and Aynbystomalarvae, which swim only intermittently, is modulated by changingtail beat frequency. However, Xenopus, which swims constantlyby sculling with its tail, regulates swimming speed (at lowto intermediate velocities) by varying the length of the propulsivewave in its tail. Xenopus and Rana differ in the morphologyof their notochord, spinal cord, spinal nerves, and spinal motorpool distribution within the spinal cord. These differencesmay underlie the different way these larvae regulate swimming.They may also reflect their phylogenetic history.     

Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color

Predator-induced defenses are well studied in plants and invertebrate animals, but have only recently been recognized in vertebrates. Gray treefrog (Hylachrysoscelis) tadpoles reared with predatory dragonfly (Aeshnaumbrosa) larvae differ in shape and color from tadpoles reared in the absence of dragonflies. By exposing tadpoles to tail damage and the non-lethal presence of starved and fed dragonflies, we determined that these phenotypic differences are induced by non-contact cues present when dragonflies prey on Hyla. The induced changes in shape are in the direction that tends to increase swimming speed; thus, the induced morphology may help tadpoles evade predators. Altering morphology in response to predators is likely to influence interactions with other species in the community as well. Received: 17 April 1996 / Accepted: 18 September 1996     

Divergent responses of exposed and naive Pacific tree frog tadpoles to invasive predatory crayfish

Invasive predators can devastate native species and ecosystems. However, native species may be able to coexist with invasive predators through a variety of mechanisms, such as changes in morphology or behavior due to a plastic response or selection on fixed anti-predator traits. We examined whether exposed and naive populations of Pacific tree frog tadpoles (Pseudacris regilla) display divergent morphological and behavioral traits in response to the invasive predatory red swamp crayfish (Procambarus clarkii). Tadpoles were collected from three study streams with and three without crayfish, in the Santa Monica Mountains of Southern California. We analyzed tadpole morphology and tested anti-predator behavior and survival in the laboratory. Tadpoles from streams with crayfish had shallower, narrower tails than tadpoles from streams without crayfish. Tadpoles from streams with and without crayfish were less active after exposure to crayfish chemical cues. The divergent morphology of naive and exposed tadpoles is consistent with tadpoles exhibiting a plastic response to crayfish or undergoing selection from crayfish predation. In laboratory predation experiments, we found no difference in survival between tadpoles from streams with and without crayfish but tadpoles that survived predation had deeper tail muscles than those that were killed or injured. Our results suggest that deeper tails are advantageous in the presence of crayfish, yet tadpoles from crayfish streams had shallower tails than those from crayfish-free streams. Shallower tails may have an alternative unmeasured advantage or there may be a physiological constraint to developing deeper tails in the wild. These results highlight the ability of a native frog to respond to an invasive predatory crayfish, potentially allowing for coexistence.     

Can members of the south‐western Gila robusta species complex be distinguished by morphological features?

The goal for this project was to re‐examine key morphological characters hypothesized to differentiate Gila intermedia, Gila robusta and Gila nigra and outline methods better suited for making species designations based on morphology. Using a combination of meristic counts, morphological measurements and geometric morphometrics, morphological dissimilarities were quantified among these three putative species. Traditional meristic counts and morphological measurements (i.e. distances between landmarks) were not useful for species identification. Geometric morphometrics, however, identified differences among species, while also suggesting an effect of geographic location on morphological variation. Using canonical variate analysis for the 441 fish sampled in this study, geometric morphometrics accurately predicted true group membership 100% of the time for G. nigra, 97% of the time for G. intermedia and 91% of the time for G. robusta. These results suggest that geometric morphometric analysis is necessary to identify morphological differences among the three species. Geometric morphometric analysis used in this study can be adopted by management officials as a tool to classify unidentified individuals.     

Dealing with allometry in linear and geometric morphometrics: a taxonomic case study in the Leporinus cylindriformis group (Characiformes: Anostomidae) with description of a new species from Suriname

To achieve maximum efficacy, taxonomic studies that seek to distinguish amongst species must first account for allometric shape variation within species. Two recently developed software packages (SMATR and MorphoJ) offer regression‐based allometric approaches that are notable for their statistical power and ease of use and that may prove highly useful to taxonomists working with linear or geometric morphometric data. We investigate species delimitation of the slender‐bodied fishes in the Leporinus cylindriformis group using these programs and demonstrate the utility of the allometric corrections that they provide. Without allometric correction, many pairs of species are difficult to distinguish on the basis of morphometrics, but once regressions are used to account for marked allometric variation within species, most of the recognized species in this group can be readily distinguished with linear or geometric morphometrics, particularly using variation in the depth of the body. Both approaches returned congruent patterns of separation amongst putative species, but the geometric approach in MorphoJ distinguished amongst four more pairs of species than did the linear approach in SMATR and appears to provide slightly more statistical power. Based on distinctive morphometrics, meristics, and coloration, a highly elongate species of Leporinus from the Suriname, Corantijn, and Coppename rivers of Suriname is described herein as a new species, Leporinus apollo sp. nov. The unique L. cylindriformis holotype from Porto de Moz, Brazil differs in morphology, meristics, and pigmentation from specimens commonly referred to that species from the main basin of the Amazon; the latter specimens may represent an additional undescribed species. The L. cylindriformis holotype itself may represent a rare species or a specimen collected at the edge of its native range. Measurements of the holotype and paratype of Leporinus niceforoi, which were collected in the Amazonian slope of Colombia, differ substantially from similarly pigmented and putatively conspecific specimens from Amazonian portions of Ecuador and Peru. Recently collected specimens from Colombia are needed to determine whether the observed morphometric variation encompassed by the current concept of L. niceforoi indicates a morphocline within a single species, suggests the presence of multiple cryptic species, or results from shrinkage of the types. In all these cases, linear or geometric morphometric data can reliably differentiate amongst species, but only after one accounts for allometric shape variation. The new SMATR and MorphoJ software packages both offer easy and effective approaches to such allometrically informed taxonomy, and may prove useful to any systematist working on taxa that change shape as they grow. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 103–130.     

The effects of acute and developmental temperature on burst swimming speed and myofibrillar ATPase activity in tadpoles of the Pacific tree frog, Hyla regilla

The effects of acute and developmental temperature on maximum burst swimming speed, body size, and myofibrillar ATPase activity were assessed in tadpoles of the Pacific tree frog, Hyla regilla. Tadpoles from field-collected egg masses were reared in the laboratory at 15 degrees (cool) and 25 degrees C (warm). Body size, maximum burst swimming speed from 5 degrees to 35 degrees C, and tail myofibrillar ATPase activity at 15 degrees and 25 degrees C were measured at a single developmental stage. Burst speed of both groups of tadpoles was strongly affected by test temperature (P<0. 001). Performance maxima spanned test temperatures of 15 degrees -25 degrees C for the cool group and 15 degrees -30 degrees C for the warm group. Burst speed also depended on developmental temperature (P<0.001), even after accounting for variation in body size. At most test temperatures, the cool-reared tadpoles swam faster than the warm-reared tadpoles. Myofibrillar ATPase activity was affected by test temperature (P<0.001). Like swimming speed, enzyme activity was greater in the cool-reared tadpoles than in the warm-reared tadpoles, a difference that was significant when assayed at 15 degrees C (P<0. 01). These results suggest a mechanism for developmental temperature effects on locomotor performance observed in other taxa.     

Correlated evolution of body and fin morphology in the cichlid fishes

Body and fin shapes are chief determinants of swimming performance in fishes. Different configurations of body and fin shapes can suit different locomotor specializations. The success of any configuration is dependent upon the hydrodynamic interactions between body and fins. Despite the importance of body–fin interactions for swimming, there are few data indicating whether body and fin configurations evolve in concert, or whether these structures vary independently. The cichlid fishes are a diverse family whose well‐studied phylogenetic relationships make them ideal for the study of macroevolution of ecomorphology. This study measured body, and caudal and median fin morphology from radiographs of 131 cichlid genera, using morphometrics and phylogenetic comparative methods to determine whether these traits exhibit correlated evolution. Partial least squares canonical analysis revealed that body, caudal fin, dorsal fin, and anal fin shapes all exhibited strong correlated evolution consistent with locomotor ecomorphology. Major patterns included the evolution of deep body profiles with long fins, suggestive of maneuvering specialization; and the evolution of narrow, elongate caudal peduncles with concave tails, a combination that characterizes economical cruisers. These results demonstrate that body shape evolution does not occur independently of other traits, but among a suite of other morphological changes that augment locomotor specialization.