Radiation of the polymorphic Little Devil poison frog (Oophaga sylvatica) in Ecuador

Some South American poison frogs (Dendrobatidae) are chemically defended and use bright aposematic colors to warn potential predators of their unpalatability. Aposematic signals are often frequency‐dependent where individuals deviating from a local model are at a higher risk of predation. However, extreme diversity in the aposematic signal has been documented in poison frogs, especially in Oophaga. Here, we explore the phylogeographic pattern among color‐divergent populations of the Little Devil poison frog Oophaga sylvatica by analyzing population structure and genetic differentiation to evaluate which processes could account for color diversity within and among populations. With a combination of PCR amplicons (three mitochondrial and three nuclear markers) and genome‐wide markers from a double‐digested RAD (ddRAD) approach, we characterized the phylogenetic and genetic structure of 199 individuals from 13 populations (12 monomorphic and 1 polymorphic) across the O. sylvatica distribution. Individuals segregated into two main lineages by their northern or southern latitudinal distribution. A high level of genetic and phenotypic polymorphism within the northern lineage suggests ongoing gene flow. In contrast, low levels of genetic differentiation were detected among the southern lineage populations and support recent range expansions from populations in the northern lineage. We propose that a combination of climatic gradients and structured landscapes might be promoting gene flow and phylogenetic diversification. Alternatively, we cannot rule out that the observed phenotypic and genomic variations are the result of genetic drift on near or neutral alleles in a small number of genes.     

Non-gradual variation in colour morphs of the strawberry poison frog Dendrobates pumilio: genetic and geographical isolation suggest a role for selection in maintaining polymorphism

The relative roles that geographical isolation and selection play in driving population divergence remain one of the central questions in evolutionary biology. We approached this question by investigating genetic and morphological variation among populations of the strawberry poison frog, Dendrobates pumilio, in the Bocas del Toro archipelago, Panama. We found significant population genetic structure and isolation by distance based on amplified fragment length polymorphism markers. Snout vent length (SVL), coloration and the extent and size of dorsal black spots showed large variation among the studied populations. Differences in SVL correlated with genetic distance, whereas black spot patterns and other coloration parameters did not. Indeed, the latter characters were observed to be dramatically different between contiguous populations located on the same island. These results imply that neutral divergence among populations may account for the genetic patterns based on amplified fragment length polymorphism markers and SVL. However, selective pressures need to be invoked in order to explain the extraordinary variation in spot size and coverage, and coloration. We discuss the possibility that the observed variation in colour morphs is a consequence of a combination of local variation in both natural selection on an aposematic signal towards visual predators and sexual selection generated by colour morph-specific mate preferences.     

Maternally derived chemical defences are an effective deterrent against some predators of poison frog tadpoles (Oophaga pumilio)

Parents defend their young in many ways, including provisioning chemical defences. Recent work in a poison frog system offers the first example of an animal that provisions its young with alkaloids after hatching or birth rather than before. But it is not yet known whether maternally derived alkaloids are an effective defence against offspring predators. We identified the predators of Oophaga pumilio tadpoles and conducted laboratory and field choice tests to determine whether predators are deterred by alkaloids in tadpoles. We found that snakes, spiders and beetle larvae are common predators of O. pumilio tadpoles. Snakes were not deterred by alkaloids in tadpoles. However, spiders were less likely to consume mother-fed O. pumilio tadpoles than either alkaloid-free tadpoles of the red-eyed treefrog, Agalychniscallidryas, or alkaloid-free O. pumilio tadpoles that had been hand-fed with A. callidryas eggs. Thus, maternally derived alkaloids reduce the risk of predation for tadpoles, but only against some predators.     

Natural selection and the distribution of shell colour morphs in three species of Littoraria (Gastropoda: Littorinidae) in Moreton Bay, Queensland

The distribution of yellow, brown and red morphs of sympatric species of Littoraria were recorded on mangrove trees of the genus Avicennia within Moreton Bay, Queensland. The roles of background mimicry (leaf vs. bark, dark vs. light), niche selection and thermal tolerance (sunny vs. shaded positions and height above ground) were examined. The yellow advantage found previously in the area was tested. Total yellow morph frequency adjusted to a reduction in leaf background on pruned trees. Morph frequencies in Littoraria species reflect differences in habitat use. L. filosa (high yellow frequency) was more frequently found on leaves at the highest tree levels, while L. luteola (high brown frequency) was more frequently found on branches at lower levels. It is therefore argued that morphs mimic background elements. Previously reported niche selection by yellow and brown morphs of leaf and bark backgrounds is shown to be a result of the distribution of L. luteola on branches and L. filosa on leaves. At warmer times of the year, yellow L. filosa were more common in sunny positions; this is thought to be a result of thermal tolerance. There appears to be some advantage to particular morphs on particular tree types, but this relationship needs to be examined further. Mangrove-dwelling Littoraria are a promising model to investigate molluscan polymorphism. In the past, erroneous identification of sympatric species may have influenced the accuracy of reported patterns. We used allozyme electrophoretic markers as a precise identification technique. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 75 , 219–232.     

Pupal warning color development in above-ground pupating species but cryptic color in ground-surface pupating species of the nine-spotted diurnal moths (Erebidae: Arctiinae: Syntomini)

Insects usually have cryptic colors to avoid detection by visually hunting predators. However, if the insects acquire toxic or repellent substances against predators, some of them develop conspicuous coloration to exhibit their unpalatability. Such warning colors allow insects to survive. In the nine-spotted diurnal moths (Erebidae: Arctiinae: Syntomini), we found the above-ground pupating species to have conspicuous colored pupae, but the ground-surface pupating species to have cryptic colored pupae. In this study, the relationships between unpalatability and coloration of these pupae are examined among three species of Amata and one species of Syntomoides. Pupae of the two species (A. germana and A. flava) are conspicuous in their color pattern with seven black dotted lines longitudinally on their pale-yellow bodies. These pupae are exposed to the aerial predators in a coarse silk mesh hanging from leaves and/or branches. The other two species (A. fortunei and S. imaon) pupate in spaces under stones, fallen twigs and leaves on the ground surface, and the pupae in a coarse silk cocoon is cryptic dark brown. Their pupation site selections are reproduced in the rearing glass vessels. Palatability assessment using lizards as a potential predator suggests that pupae of A. germana, A. flava and A. fortunei are unpalatable and the lizard's feeding response decreases with experience. However, pupae of S. imaon are all eaten (palatable). Finally, the possible evolutionary scenario of pupal colors of these four species is discussed in relation to pupation site selection and palatability.     

Geographic variation in the colour/ pattern polymorphism of British Philaenus spumarius (L) (Homoptera: Aphrophoridae) populations *

Geographic variation in the frequency of colour/pattern morphs of Philaenus spumarius is described at 48 localities in England and Wales. The sites have been divided into four broad environmental categories, two urban and two rural. There is a distinction between the urban and rural groupings in the relative proportions of the colour morphs; in urban localities there is a higher combined frequency of the eight ‘melanic’ morphs. Differences also exist between locality groupings, and between the sexes, in the relative frequencies of the eight morphs within the ‘melanic’ phenotypic category. Morphs limited to the female sex in some other parts of the species range occur among males in British populations. It is suggested that the different dominance hierarchy between the sexes which exists in Fennoscandian populations may not be characteristic of British populations.     

Morphological divergence of North‐European nine‐spined sticklebacks (Pungitius pungitius): signatures of parallel evolution

Parallel evolution is characterised by repeated, independent occurrences of similar phenotypes in a given habitat type, in different parts of the species distribution area. We studied body shape and body armour divergence between five marine, four lake, and ten pond populations of nine‐spined sticklebacks [Pungitius pungitius (Linnaeus, 1758)] in Fennoscandia. We hypothesized that marine and lake populations (large water bodies, diverse fish fauna) would be similar, whereas sticklebacks in isolated ponds (small water bodies, simple fish fauna) would be divergent. We found that pond fish had deeper bodies, shorter caudal peduncles, and less body armour (viz. shorter/absent pelvic spines, reduced/absent pelvic girdle, and reduced number of lateral plates) than marine fish. Lake fish were intermediate, but more similar to marine than to pond fish. Results of our common garden experiment concurred with these patterns, suggesting a genetic basis for the observed divergence. We also found large variation among populations within habitat types, indicating that environmental variables other than those related to gross habitat characteristics might also influence nine‐spined stickleback morphology. Apart from suggesting parallel evolution of morphological characteristics of nine‐spined sticklebacks in different habitats, the results also show a number of similarities to the evolution of three‐spined stickleback (Gasterosteus aculeatus Linnaeus, 1758) morphology. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 403–416.     

Differential visual predation on morphs of Timema cristinae (Phasmatodeae:Timemidae) and its consequences for host range

Timema cristinae is a herbivorous insect that exhibits polymorphism for body coloration (green, red and grey morphs) and for pattern (striped, expressed only in the green morph, and unstriped). The striped green morph is associated with ceanothus ( Ceanothus spinosus ) and the unstriped green morph is associated with chamise ( Adenostoma fasciculatum ). This study examines the relative vulnerabilities to predation of the different pattern and colour morphs on their natural backgrounds. The vulnerabilities of the striped and unstriped morphs on their two food plants were tested using uncaged wild birds (Scrub Jays) and captive western fence lizards. Strong differential predation was observed suggesting that each morph is most cryptic on the food plant on which it is most common. Furthermore, in a mark-recapture experiment in a patch of ceanothus the unstriped and red morphs were recaptured in higher proportion than the other morphs. The vulnerabilities of the grey and green morphs on the ground and foliage were tested using lizards. The grey morph was more vulnerable on the plants than the green morph, but the inverse was observed on the ground (where they drop after a disturbance). This may be why the grey morph is not associated with specific food plants. The striped and colour polymorphisms in T. cristinae appear to be an evolutionary consequence of differential predation on different backgrounds. The implications of differential predation to food-plant utilization are discussed.     

Sperm ultrastructure of the Brazilian Amazon poison frogs Epipedobates trivittatus and Epipedobates hahneli (Anura, Dendrobatidae)

The sperm ultrastructure of Epipedobates trivittatus and E. hahneli is described. The spermatological characteristics are identical in both species, except for the extension of the acrosomal vesicle. The structure of the acrosomal complex is shared with species of the Bufonoidea neobatrachian lineage, which differs from the condition observed in species included in the ranoid lineage. The phylogenetic significance of the mitochondrial collar, also seen in Eubufonoidea groups, is still unclear. Also the significance of the alternative mitochondrial arrangement seen here is unclear. The perpendicular arrangement of the centrioles is also shared with the Bufonoidea and is considered a synapomorphic condition. An expanded undulating membrane and the absence of a juxtaxonemal fibre appear to be apomorphic characteristics of dendrobatid species, as also observed (homoplastically) for species of Litoria and Cyclorana. However, the notable expansion of the undulating membrane appears to be an autapomorphy of Dendrobatidae frogs. The ultrastructural data presented here do not support the proposed placement of E. trivittatus in a separate genus.     

Prey resources are equally important as climatic conditions for predicting the distribution of a broad-ranged apex predator

Aim

A current biogeographic paradigm states that climate regulates species distributions at continental scales and that biotic interactions are undetectable at coarse-grain extents. However, advances in spatial modelling show that incorporating food resource distributions are important for improving model predictions at large distribution scales. This is particularly relevant to understand the factors limiting the distribution of widespread apex predators whose diets are likely to vary across their range.

Location

Neotropical Central and South America.

Methods

The harpy eagle (Harpia harpyja) is a large raptor, whose diet is largely comprised of arboreal mammals, all with broad distributions across Neotropical lowland forest. Here, we used a hierarchical modelling approach to determine the relative importance of abiotic factors and prey resource distribution on harpy eagle range limits. Our hierarchical approach consisted of the following modelling sequence of explanatory variables: (a) abiotic covariates, (b) prey resource distributions predicted by an equivalent modelling for each prey, (c) the combination of (a) and (b), and (d) as in (c) but with prey resources considered as a single prediction equivalent to prey species richness.

Results

Incorporating prey distributions improved model predictions but using solely biotic covariates still resulted in a high-performing model. In the Abiotic model, Climatic Moisture Index (CMI) was the most important predictor, contributing 76% to model prediction. Three-toed sloth (Bradypus spp.) was the most important prey resource, contributing 64% in a combined Abiotic-Biotic model, followed by CMI contributing 30%. Harpy eagle distribution had high environmental overlap across all individual prey distributions, with highest coincidence through Central America, eastern Colombia, and across the Guiana Shield into northern Amazonia.

Main Conclusions

With strong reliance on prey distributions across its range, harpy eagle conservation programmes must therefore consider its most important food resources as a key element in the protection of this threatened raptor.     

Female‐limited colour polymorphism in the crab spider Synema globosum (Araneae: Thomisidae)

Conspicuous colour variation, caused by the influence of the environment on phenotype or by genetic differences among individuals, is frequently observed in nature. If genetic in origin, colour variation can facilitate the study of mechanisms that contribute to the maintenance of true polymorphisms. Here we describe, for the first time, the female‐limited colour polymorphism in the crab spider, Synema globosum. We looked for associations between life‐history traits and female colour morph, and identified potential agents of selection that could influence the maintenance of the polymorphism. Our results showed that the polymorphism is discrete and heritable, and that differences in colour among morphs are likely to be detectable by honeybees, birds, and conspecifics. We found limited evidence of differences among morphs in morphology and ecology, and found no differences in components of reproduction. Based on the lines of evidence obtained in this study, we suggest that selection exerted by prey, predators, and/or mates is likely to influence the maintenance of the polymorphism observed in S. globosum. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 368–383.     

Terrestrial predator alarm vocalizations are a valid monitor of stress in captive brown capuchins (Cebus apella)

The vocal behavior of captive animals is increasingly exploited as an index of well‐being. Here we show that the terrestrial predator alarm (TPA) vocalization, a robust and acoustically distinctive anti‐predation vocal response present in many mammal and bird species, offers useful information on the relative well‐being and stress levels of captive animals. In a 16‐week experiment evaluating the effects of varying levels of physical environmental enrichment (control < toys < foraging box < foraging box and toys) in the cages of eight singly housed adult male brown capuchins, we quantified the 1) emission rate of TPAs, 2) proportions of normal and abnormal behavior sample intervals, and 3) fecal and plasma cortisol levels. Variation in TPA emission across the experimental conditions was significant. We found significant reductions in the mean TPA production rate by the group in the enriched (toys, foraging box, and foraging box and toys) compared to the control condition; pre‐ and post‐experimental conditions, however, did not differ from the control condition. Mean TPA production by the group was also significantly positively correlated to mean group levels of fecal cortisol and proportion of abnormal behavior sample intervals, and significantly negatively correlated to the average proportion of normal behavior sample intervals in the group. Based on group means, plasma cortisol levels were positively, but not significantly, related to increasing TPA rate. At the level of the responses of an individual subject, however, the covariation between the vocal and non‐vocal behavioral measures and the cortisol assays seldom attained significance. Nevertheless, the direction of the relationships among these parameters within individual subjects typically mirrored those correlations based on group means. At both the group mean and individual levels, our results are consistent with the interpretation that in conditions of low environmental enrichment the study subjects were more stressed, and therefore more reactive to the presence of a threatening terrestrial stimulus (human observer), than when in more enriched conditions. We suggest that protocols to evaluate the effectiveness of enrichment for captive species other than brown capuchins could also profitably exploit TPAs as a first‐line monitor or as corroboratory evidence of current well‐being. Zoo Biol 18:295–312, 1999. © 1999 Wiley‐Liss, Inc.     

Why are fruit traits of Cistus ladanifer (Cistaceae) so variable: A multi-level study across the western Mediterranean region

Variation is the raw material for evolution. Differences among populations in the expression of traits related to plant fitness may result from natural selection, phenotypic plasticity (in response to local conditions), and developmental instability (manifested as high intra-individual variation in repeated patterns or characters). Cistus ladanifer is a highly polymorphic plant distributed in the Mediterranean and the only species in the family (Cistaceae, 180 species) with a variable number of valves per fruit. We herein analysed the variation in the number of valves (5–12) and seeds (318–1185) per fruit in 36 populations (607 individuals, 1821 fruits) at different levels: temporal, geographical, ecogeographical, taxonomic, and phylogeographical. In addition, we tested whether an increased number of fruit valves influences pre-dispersal seed predation. Large variation in the number of valves and seeds per fruit among populations, individuals, and years was reported. The number of ovules and seeds per valve increased with a higher number of fruit valves. Geographical and taxonomic variables did not significantly explained this fruit variation. On the contrary, we found a negative relationship between the number of fruit valves and altitude and a positive relationship with precipitation. We argue that ecogeographical factors, in addition to some phylogeographical and phylogenetic signals, are involved in the multiplication of carpels during the development of the ovary wall. This, coupled with the results of the evolutionary history of Cistus in previous studies, indicates active evolutionary processes in C. ladanifer populations.     

Experimental test of the ecosystem impacts of the keystone predator Triops cancriformis (Branchiopoda: Notostraca) in temporary ponds

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Comparison of the wing polyphenic response of pea aphids (Acyrthosiphon pisum) to crowding and predator cues

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Predation of frog eggs by the water strider Gerris latiabdominis Miyamoto (Hemiptera: Gerridae)

Water striders (Hemiptera: Gerridae) are predators found on the water surface that prey mainly on arthropods. The feeding on other organisms (dead vertebrates, fishes and tadpoles) is a rare event. To our knowledge, predation of frog eggs by water striders has not yet been reported. We observed that adult water striders, Gerris latiabdominis Miyamoto, 1958 (Hemiptera: Gerridae), preyed on the eggs of three frog species, Pelophylax nigromaculata Hallowell, 1861 (Anura: Ranidae), Rana japonica Boulenger, 1879 (Anura: Ranidae), and Rhacophorus schlegelii Günther, 1858 (Anura: Rhacophoridae). We found predation by the water striders affects the survival rate of frog eggs floating on the water surface. We suggest that this hunting event would occur in water bodies in which water striders and frogs coexist, especially the region where their phenology overlaps.