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Recent discussion in the life-history literature has examined “adaptive maternal effects,” defined as maternal effects that benefit offspring, and concluded that this definition is too narrow, because maternal effects may not always benefit current offspring fitness, but can still be adaptive to female lifetime reproductive success. The “maternal manipulation hypothesis” suggests that females modify their physiology and behavior when gravid to increase offspring fitness, an example of adaptive maternal effects in the narrow sense. The maternal manipulation hypothesis has been tested almost exclusively using studies of reptiles, especially viviparous species. We argue that interpretations of modifications of female reptile behavior and physiology while gravid are hampered by the maternal manipulation hypothesis' exclusive focus on offspring fitness. We suggest broadening the approach of such studies to attempt to determine whether behaviors benefit fitness of the current batch of offspring, or benefit female lifetime reproductive success, or both. Using this approach, researchers acknowledge that females may modify physiology and behavior when gravid to benefit their own lifetime reproductive success, which may, or may not, also enhance fitness of the current batch of offspring. We recommend tests of benefits in reptiles to include the idea that females may increase their lifetime reproductive success by engaging in specific behaviors while gravid, independent of (or in addition to) benefits to offspring. We conclude that a broader view of maternal effects, less focused on offspring fitness and including both mothers and offspring, is the way forward for understanding maternal effects.
Catherine M. Bodinof, Jeffrey T. Briggler, Randall E. Junge, Jeff Beringer, Mark D. Wanner, Chawna D. Schuette, Jeff Ettling, Robert A. Gitzen, Joshua J. Millspaugh
Postrelease movements can determine the success of wildlife translocations. We monitored movements of 36 captive-reared Ozark Hellbenders (Cryptobranchus alleganiensis bishopi) released to augment wild populations at two sites on the North Fork of the White River (Missouri, USA). We used radiotelemetry to collect 3610 Hellbender locations from May 2008 to August 2009. We quantified movements at multiple spatio-temporal scales and made comparisons between two seasons of monitoring (1 = release–December 2008; 2 = January 2009–August 2009). At the finest (daily) scale, most Hellbenders (90%–94% per season) were highly sedentary (≥50% of observations indicated no movement). Typical distances between daily locations when Hellbenders moved were <5 m in Season 1 (median = 3.08 m, n = 331; range = 0.19–903.00) and <2 m in Season 2 (median = 1.80 m; n = 161; range = 0.21–34.00). During the study Hellbenders rarely (35 of 492 movements) travelled >20 m between daily locations, and virtually all (34 of 35) such movements occurred in Season 1. At a broader scale, home ranges of Hellbenders varied widely in Season 1 (range = 0.66–986.92 m2, n = 26), but in Season 2 averaged only 31.33 m2 (± 11.81 SE, n = 8) and 11.08 m2 (± 3.25 SE, n = 7) at respective sites. Among Hellbenders monitored long enough to exhibit settlement (estimation of a home range) 69% (18 of 26) dispersed ≤50 m from the point of release. We only noted mortality associated with dispersals >50 m at one site, when it coincided with abandonment of core habitat that was one-third as large as at the other site. At the broadest scale, 68% and 86% of Hellbenders settled in core habitat of respective release sites, and most had settled within 21 d postrelease (range = 0–49 d). Collectively, Hellbender movements indicated a short period of exploration followed by more permanent settlement and high site fidelity typical of wild conspecifics. Captive-reared juvenile Hellbenders may be well suited for translocation; however, the quality of habitat at fine scale (10–30 m2) and the extent of suitable habitat within release sites are important considerations.
Anthropogenic stressors, such as contaminants or pollutants, can change the outcome of competition in a variety of communities. We examined potential competitive interactions between American Toad (Anaxyrus americanus) and Gray Treefrog (Hyla versicolor) tadpoles by manipulating the presence and absence of each species and overall tadpole density and how they may be affected by anthropogenic nutrient enrichment by manipulating the presence and absence of nitrate and phosphate. Interactions with Gray Treefrogs did not affect American Toad survivorship, mass at metamorphosis, or time to metamorphosis. Nutrient enrichment reversed the relative effects of interspecific and intraspecific conditions on Gray Treefrog survivorship. Namely, in enriched mesocosms Gray Treefrog tadpoles living with American Toad tadpoles had higher survivorship than those in Gray Treefrog–only communities, whereas the opposite was true in no-enrichment mesocosms. Nutrient enrichment accelerated metamorphosis in American Toads but did not affect Gray Treefrogs. Overall tadpole density had no effect on Gray Treefrogs, but American Toads metamorphosed earlier and at a larger size at high tadpole densities. Our results provide further confirmation that the alteration of the environment by humans can have a variety of effects, both directly through their effects on each species and indirectly by altering the interactions among species.
We studied growth, development, and metamorphic traits of Polypedates braueri tadpoles in Taiwan to elucidate the cause of tadpole overwintering in man-made water containers in lowland orchards on the Bagua Terrace. Polypedates braueri bred from March to August, but tadpoles were present year round. Laboratory experiments demonstrated that tadpole overwintering was facultative; low temperatures and limited food retarded both growth and development, resulting in overwintering in the tadpole stage. Tadpoles at the lowest experimental temperature (15°C) never reached metamorphosis. A field experiment demonstrated that 78, 28, and 4% of tadpoles raised in high, medium, and low food regimes, respectively, metamorphosed before the onset of winter. Tadpoles that did not metamorphose by fall continued to grow slowly and either metamorphosed during the winter or the following spring. These findings indicate that food availability plays a key role in inducing overwintering in tadpoles. Jumping performance of metamorphs was positively correlated with food regimes, but body lipid content was significantly higher in metamorphs raised with either low or high food regimes than in those with medium levels of food. Overwintering by P. braueri tadpoles has not been previously reported; however, agricultural activities have created new breeding habitats (i.e., man-made bodies of water), some of which are sufficiently food-limited that tadpoles overwinter to complete development and metamorphosis. An understanding of the survivorship, life history traits, and physiology of these frogs is needed to shed light on how man-made breeding sites affect the population dynamics of native frog populations.
Although estimates of survival and population density are available for several snake populations, most of these are for populations in northern temperate environments. Here we present the results of a 3-yr mark–recapture study for an African species, the Namaqua Dwarf Adder (Bitis schneideri). We estimated survival, recapture probability, and population density by marking 279 adders (121 males, 108 females, 50 juveniles) on two study sites along the Namaqualand coast of South Africa. We recaptured 54 individuals (27 males, 23 females, 4 juveniles), yielding absolute recapture rates of 20.4% and 17.9% at each site respectively. The adult sex ratio of our sample did not differ significantly from equality. We fitted eight models that included both individual-dependent and time-dependent covariates to our recapture data, and compared models using Akaike information criterion corrected for small samples. The best models included snout–vent length and search effort covariates. Mean (±SD) estimated monthly apparent survival was low (0.86 ± 0.11 and 0.86 ± 0.12), as were mean recapture likelihoods (0.06 ± 0.04 and 0.06 ± 0.01). Population density estimates were similar for the two sites (7.52 ± 3.62 ha−1 and 8.31 ± 7.38 ha−1). Juvenile snakes exhibited higher survival than adult females, which, in turn, had higher survival than adult males. Juveniles had a lower recapture probability than adult males or females. The likelihood of an individual leaving the study area was 6.8% and 9.4% per month for the larger and smaller sites, respectively. On the basis of our measures of apparent survival and emigration, we estimate annual survival rates of 39% and 56% for the two sites respectively. Population characteristics of B. schneideri differ substantially from those of other viperids, highlighting the need for additional population studies of African snakes.
Studies of diet are central to our understanding of organismal biology. We describe the diet of the Red Diamond Rattlesnake (Crotalus ruber) using data collected from museum specimens, live specimens from a field study, road kills, opportunistic behavioral observations, and existing literature. Dietary samples were collected from across the species' range, including Southern California (USA) and Baja Norte and Baja Sur (Mexico). Examination of 272 individuals resulted in 227 prey items recorded from 219 snakes. The diet of C. ruber consisted largely of mammals (91.6%), but also included lizards (7.5%) and birds (0.9%). No ontogenetic shift in prey type was evident, with mammals consumed by all snake size classes. However, adults fed on larger prey than juveniles. Sexual dimorphism existed in snake length, with adult males averaging longer than adult females. Juvenile males consumed larger prey than females, but no sexual differences in prey mass existed for adults when controlling for snake body length. Snakes from coastal populations averaged longer in body length than snakes from desert populations. Coastal snakes consumed a higher proportion of rodents, and prey of larger body mass when controlling for snake length, than snakes from desert populations. The presence of prey was independent of snake collection month, suggesting year-round feeding, as supported by observations of occasional winter feeding by snakes in California. Although C. ruber may scavenge food opportunistically, behavioral observations suggest that it relies heavily on ambushing mammal prey.
Yellow-lipped Sea Kraits (Laticauda colubrina) are tropical amphibious snakes that divide their time between land and sea. When moving between habitats, the kraits experience rapid and sometimes extreme shifts in body temperature that can have profound metabolic effects. We quantified cutaneous and pulmonary oxygen uptake in sea kraits from Hoga Island, southeast Sulawesi, Indonesia, at temperatures commonly encountered in aquatic (27.6°C) and aerial (35.2°C) habitats. Total oxygen uptake rate was 49.14 mL Kg−1 h−1 at 27.6°C and 115.27 mL Kg−1 h−1 at 35.2°C. Pulmonary and cutaneous uptake rates were 44.58 and 104.70, and 4.56 and 10.57 mL Kg−1 h−1, at 27.6 and 35.2°C, respectively. Sea kraits had a temperature coefficient (Q10) of approximately 3, suggesting that metabolic rates triple with every 10°C temperature increase. High Q10 values may minimize time on land by increasing digestion and nutrient absorption rates as well as promoting faster healing and injury recovery times. Cooler reef temperatures would decrease metabolic demand, thus increasing submergence and foraging times.
The Trans-Mexican Volcanic Belt and surrounding areas contain substantial biological diversity. The mountains that make up the Trans-Mexican Volcanic Belt are a hypothesized biogeographic barrier for the terrestrial fauna found in the region. Several phylogeographic studies have provided genetic evidence in support of this historical narrative; however, the species examined represent a small percentage of the diversity found in this part of Mexico. Thus, additional studies are needed to identify concordant phylogeographic patterns and infer the historic species composition of particular ecoregions. In this study we investigated genetic variation in the Lowland Burrowing Treefrog, Smilisca fodiens, a species that occurs on both sides of the Trans-Mexican Volcanic Belt. We used mitochondrial (12S and 16S ribosomal subunits; 1039 base pairs [bp]) and nuclear (tyrosinase precursor; 513 bp) DNA to perform phylogenetic analyses on frogs from several localities in Mexico. Mitochondrial DNA supported two well-defined clades that correspond to populations found north and south of the Trans-Mexican Volcanic Belt, respectively. These analyses of matrilineal lineages also found higher levels of genetic diversity south of the Trans-Mexican Volcanic Belt. Although our nuclear DNA analysis did not reveal a phylogeographic split at the Trans-Mexican Volcanic Belt, we observed higher genetic variation among our southern samples, similar to the mitochondrial analyses. Our results are consistent with studies in other sympatric taxa that propose the Trans-Mexican Volcanic Belt as a biogeographic barrier. Additionally, our results suggest recent northern range expansion of S. fodiens. We suggest retaining S. fodiens as a single species until future work can clarify the amount and direction of gene flow between the mitochondrial clades.
Fossil anuran remains from an outcropping of Oligocene sediments in central Patagonia have been attributed to the extant genus Eupsophus based on their putative similarity to the skeleton of living members of this genus. These remains would represent the only and oldest evidence of the existence not only of Eupsophus, but also of any cycloramphid anuran in Patagonia during the past. Given the scarcity of the anuran fossil record, these fossils have been long considered as significant evidence in the discussion of the evolutionary history of the South American batrachofauna. However, re-examination of these specimens reveals that some skeletal structures were misinterpreted and that these anurans clearly differ from living Eupsophus. Although osteological synapomorphies of this genus are still unknown, there is no evidence to link these fossil remains with the presence of Eupsophus in the Oligocene batrachofauna of Patagonia.
We describe a new species of Pristimantis from evergreen lowland forest in the Amazon Basin of Ecuador. We observed all specimens to be active at night, located over leaves of shrubs in both primary forest and in the edge of forest clearings. The new species is tentatively assigned to Pristimantis (Pristimantis) frater group based on its small size (17.0–22.1 mm in snout–vent length of four males and 24.1 mm in a single female), relatively narrow head, short and subacuminate snout, lack of canthal stripes and labial bars, moderately long limbs, Finger I shorter than Finger II, and Toe V longer than Toe III. The new species differs from other congeneric species in Amazonia by possessing dense black reticulations on upper and lower borders of the iris, a dorsum that is orange or dark reddish brown without distinct pattern in life, a tympanic membrane not differentiated but ventral part of the tympanic annulus visible, and a small tubercle on each heel and eyelid.
Una nueva especie de Pristimantis es descrita de los bosques siempreverde de tierras bajas de las Cuenca Amazónica de Ecuador. Todos los especímenes fueron observados durante la noche localizados sobre hojas de arbustos, tanto en áreas de bosque primario y en los bordes con áreas abiertas. La nueva especie es tentativamente asignada al grupo Pristimantis (Pristimantis) frater, por su tamaño pequeño (17.0–22.1 mm en la longitud hocico-cloaca de cuatro machos; 24.1 mm en una hembra), con la cabeza relativamente angosta, rostro corto subacuminado, carece de líneas cantales o barras en los labios y extremidades moderadamente largas; con el dedo I más corto que el dedo II en las manos, y el dedo V más largo que el dedo III en el pie. La nueva especie difiere de otras especies congenéricas de la Amazonía por poseer densas reticulaciones negras en el borde superior e inferior del iris, exhibir el dorso anaranjado o café rojizo uniforme en vida, con la membrana timpánica no diferenciada pero la parte ventral del anillo timpánico visible, y por presentar un pequeño tubérculo en los párpados y talones.
I rediagnose the microhylid frog Callulops robustus (Boulenger) based on examination of the type series and recently collected topotypic material. The species is distinguished by its large size, narrowly expanded finger and toe discs lacking or with poorly developed circum-marginal grooves, pustulose dorsal skin, long snout, unpatterned orange-brown or reddish-brown dorsal coloration, and uniformly brown ventral coloration. The species is almost certainly restricted to the type locality, Misima Island, at the easternmost extremity of the geographic range of Callulops. Based on examination of the holotype and recently collected material from the general area of the type locality, I then rediagnose Mantophryne microtis Werner and remove it from synonymy with C. robustus. It is readily distinguished from the latter species by its somewhat smaller body size, well-developed circum-marginal grooves on at least some of the fingers and toes, short snout, and color pattern of tiny white flecks on a dark gray or black ground color. This species is currently known from mountain ranges on the northeastern coast of New Guinea, but it may prove to occur in similar North Coast ranges farther to the west. I also discuss the taxonomic status of Pomatops valvifera Barbour and Liophryne kampeni Boulenger, currently placed in synonymy with C. robustus. Both species are clearly not referable to C. robustus, but each is known only from single, faded specimens, and compelling rediagnosis of each awaits collection of fresh topotypic material.
We describe a new species of brachycephalid frog from Atlantic forest of Serra do Morato, Municipality of Guaraqueçaba, state of Paraná, Brazil. Brachycephalus tridactylus sp. nov. is characterized by the absence of external trace of finger IV, orange color in life, dorsolateral and ventrolateral regions with regular small olive-gray spots, and ventral region and thighs orange with olive-grayish irregular coalescent spots and small dots; skin on the dorsum of head and central body dorsum smooth with no dermal co-ossification. The advertisement call of the new species has a single short note that decreases in dominant frequency from beginning to end.
In spite of Amazonia's large biodiversity, we still understand relatively little about how it evolved. Phylogeographic studies help us to understand the spatial and temporal context in the diversification of organisms, but only a few such studies have been done in Amazonia, where regional and local variation exists that may have been influenced by different events or similar events at different times. Here we test whether, and to what degree, the phylogeographic structure of faunal elements reflects a recently proposed geological scenario for the establishment of the lower Amazon–Tocantins basins in eastern Amazonia. We test an area cladogram that assumes that the Amazon River represents the first potential barrier (≥3.6 million years ago [mya]), followed by an east–west separation south of the Amazon caused by the paleo-Tocantins River (∼2.5 mya), and most recently by the shift of the lower Tocantins eastward to its present course (∼6000–8000 yr ago). We examined mtDNA (∼520 base-pairs [bp] of 16S, 815 bp of cytochrome b) of two widely distributed and distantly related lizard species, Gonatodes humeralis (Sphaerodactylidae) and Kentropyx calcarata (Teiidae). The phylogeographic structure of G. humeralis indicates that the species is characterized by deep splits between localities, preventing us from recovering well-supported relationships between populations. Kentropyx calcarata haplotype networks and our Bayesian mtDNA tree identify a number of clades that we compare through an AMOVA. The overall phylogeny of K. calcarata was partially congruent with the geological scenario, but some unforeseen relationships were also recovered. Our results reinforce the potential of phylogeographic studies to help understand the recent evolution of Amazonia, and at the same time point to the necessity of refined sampling and the use of multiple molecular markers in such studies.
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