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Lanternfishes (Myctophiformes, ~260 species) are among the most abundant and species-rich groups of fishes endemic to the deep sea, and they play a major role in the oceanic ecosystem by transferring energy from shallower to deeper oceanic levels. Little is currently known regarding how lanternfishes have achieved such high species richness in the deep sea, and the majority of previous studies that have investigated diversification in this group have focused on bioluminescence. In this study, we investigate the variation in mouth size of lanternfishes in an effort to better understand potential mechanisms of speciation in this group, as previous studies have indicated that there is considerable variation in the size and biodiversity of prey items of lanternfishes. Geometric morphometrics were performed on 955 lanternfish specimens, and an ancestral character-state reconstruction was used to examine variation and evolution of mouth size in this group. We identify that mouth size in lanternfishes is highly variable, with general trends towards larger mouths in the subfamily Lampanyctinae (Myctophidae) and shorter mouths in the subfamily Myctophinae (Myctophidae). Within each subfamily there are discrete patterns of jaw-size differentiation among genera. Of particular note, the genus Diaphus, the most species-rich genus of lanternfishes (~30% of lanternfish diversity), was found to occupy a large range of morphospace, with broad plasticity in mouth size among the examined species. Ancestral character-state reconstructions indicate that a neoscopelid-like jaw was the likely ancestral state for Myctophiformes; whereas, a longer jaw, similar to that of the majority of species in the subfamily Lampanyctinae, was most likely the ancestral state for the family Myctophidae.
The conditions experienced during early development may have strong effects on the adult phenotype, and consequently on fitness. Diet quality is an important environmental variable, and, frequently, organisms with low protein diets should achieve higher fitness on high protein ones. As for many omnivores, tadpoles find a greater quantity of protein in animal materials, thus it is often assumed that tadpoles would increase fitness on carnivorous diets. Using an omnivorous tadpole, Rhacophorus arboreus, we tested the effects of animal diets (chironomid larvae and tubificid worm) and plant diets (high protein alga, spinach, and leaf litter) on post-metamorphic fitness-related traits: body size, locomotory performance, and gut length. All tadpoles metamorphosed at the same size except those on the leaf litter diet that exhibited the longest larval period, the smallest size at metamorphosis, and the lowest locomotory performance. The algal treatment induced faster growth in the tadpoles and produced juveniles with proportionally shorter guts than the smaller juveniles from the litter treatment. As suggested in recent studies, differential post-metamorphic gut length may influence food intake, assimilation efficiency, and growth in metamorphs, but such an assumption needs further clarification. The tadpoles on carnivorous diets metamorphosed into frogs with relatively shorter legs and poor locomotory performance. In contrast to expectations, carnivorous diets impaired post-metamorphic performance in an omnivorous tadpole. The causes of leg abnormalities remain unclear, but the tadpoles possibly suffered from nutritional imbalance on carnivorous diets.
The skin glands and cloacal morphology of the Korean crevice salamander, Karsenia koreana, were similar to those of other plethodontids. The skin contained mucous, granular, and modified granular glands in varying frequencies and sizes. Males had sexually dimorphic glands in the skin of the chin (mental glands) and the dorsal tail base (caudal courtship glands). On the ventral surface of the tail base, modified granular glands were sexually dimorphic in size, with male glands larger than those in females. The cloacal glands in males, as in other plethodontids, consisted of four eosinophilic gland clusters (dorsal pelvic glands, lateral pelvic glands, caudal pelvic glands, and vent glands) and three basophilic glands (anterior ventral glands, posterior ventral glands, and Kingsbury's glands). In females, the only cloacal gland was the spermatheca, which, as in other plethodontids, was a compound tubulo-alveolar gland in the roof of the cloaca.
Global amphibian declines have been attributed to a number of factors including disease, invasive species, habitat degradation, and climate change. Reintroduction is one management action that is commonly used with the goal of recovering imperiled species. The success of reintroductions varies widely, and evaluating their efficacy requires estimates of population viability metrics, such as underlying vital rates and trends in abundance. Although rarely quantified, assessing vital rates for recovering populations provides a more mechanistic understanding of population growth than numerical trends in population occupancy or abundance. We used three years of capture-mark-recapture data from three breeding ponds and a Cormack-Jolly-Seber model to estimate annual apparent survival for reintroduced populations of the federally threatened Chiricahua Leopard Frog (Lithobates chiricahuensis) at the Buenos Aires National Wildlife Refuge (BANWR), in the Altar Valley, Arizona, USA. To place our results in context, we also compiled published survival estimates for other ranids. Average apparent survival of Chiricahua Leopard Frogs at BANWR was 0.27 (95% CI [0.07, 0.74]) and average individual capture probability was 0.02 (95% CI [0, 0.05]). Our apparent survival estimate for Chiricahua Leopard Frogs is lower than for most other ranids and is not consistent with recent research that showed metapopulation viability in the Altar Valley is high. We suggest that low apparent survival may be indicative of high emigration rates. We recommend that future research should estimate emigration rates so that actual, rather than apparent, survival can be quantified to improve population viability assessments of threatened species following reintroduction efforts.
Previous studies have shown that diet varies among seasons and age classes of lizard species inhabiting contrasting environments. The purpose of our study was to compare feeding habits between seasons (wet and dry), sexes (males and females), and age classes (juvenile and adult) of the arboreal lizard Anolis nebulosus from two different environments: a Pacific island (San Pancho Island) and the mainland Pacific Coast (Biological Field Station Chamela) of Mexico. Anolis nebulosus from island and mainland were generalist insectivores. During the dry season, the prey number consumed by lizards from island was lower than for lizards from mainland. With respect to numerical and volumetric data of prey items consumed by females and males for both age classes (adults and juveniles) in both populations (island and mainland), adult beetles, ants, orthopterans (grasshopper and crickets), and spiders were most frequently preyed upon. These results suggest that there are no ontogenetic changes in the diet of A. nebulosus and there is high dietary overlap of all groups (sexes and age classes) within both populations. Selection of this kind of prey by lizards from both age classes may be an overall trend in most species of Anolis, an opportunistic behavior toward the most abundant prey types that occur among seasons and years.
Luiz Flávio José dos Santos, Veronica Regina Lobato de Oliveira-Bahia, Laura Satiko Okada Nakaghi, Marta Verardino De Stefani, Adriano Marques Gonçalves, João Martins Pizauro Junior
The transition from aquatic to terrestrial phase in amphibians, called metamorphosis, is accompanied by ecological, morphological, physiological, and biochemical changes. These enable the digestive system of the animal to take up nutrients when the feeding habit changes from omnivorous/herbivorous in tadpoles to carnivorous in adults. To better understand this process, this study investigated the activity of four hydrolases in the digestive system of bullfrog (Lithobates catesbeianus) at all stages of larval development in which the animals feed from exogenous sources. Digestive enzyme activity increased from the beginning of the feeding phase until pre-metamorphosis, which is related to the maturation of the digestive system. The increase was more significant in the period of pro-metamorphosis, coinciding with the accumulation of energy reserves necessary for metamorphosis and the increased growth of the animal. During the climax of metamorphosis, the activities of digestive enzymes decreased, because the animal does not eat during this period. At the end of metamorphosis, in stage 45, the activity of proteolytic enzymes, acid proteases and trypsin, increased 35% and 400%, respectively, when compared to stage 44. Conversely, maltase activity remained constant whilst amylase activity decreased by 70%, which is consistent with the carnivorous feeding habit of the adult. These results enhance understanding of the development of digestive enzymes in the larval phase and in the change from omnivorous/herbivorous to carnivorous feeding habits. In addition, these findings provide insights for the formulation of appropriate diets for each developmental phase of tadpoles.
The perception that crocodilians exhibit indeterminate growth is common in the general reptilian literature. However, this assumption is frequently based on observations of immature and young adult animals and therefore lacks a complete understanding of adult growth patterns. Long-term mark-recapture studies appear to be the most certain method of determining growth patterns of adult crocodilians. From 1979–2015, we conducted a mark-recapture study of an American Alligator (Alligator mississippiensis) population on the Tom Yawkey Wildlife Center (YWC) in coastal South Carolina to examine long-term growth patterns and the influence of age on multiple reproductive parameters. We found no discernible linear growth in 19 of 31 adult female and 7 of 19 adult male alligators over periods of 5–33 years. The mean maximum reproductive lifespan for female alligators on the study site was 46 years, and females continued to reproduce for an extended period of time after reaching maximum size. The Schnute growth model predicted that male alligators grew at a faster rate and attained a greater estimated mean terminal snout–vent length (SVL) than females (males = 186.9, CI0.95 = 184.5, 189.3 cm; females = 135.9, CI0.95 = 134.1, 137.8 cm) at the hypothetical age 75. In addition, the model predicted that males exhibited a greater estimated mean size (SVL = 182.0, CI0.95 = 179.6, 184.4 cm) and age (43 years) at which growth essentially ceased when compared to females (SVL = 131.4, CI0.95 = 129.5, 133.2 cm; 31 years). However, actual growth records of individual alligators suggested that the growth model may have overestimated the age at which male alligator growth ceased. The estimated mean earliest age at sexual maturity was 11.6 years (CI0.95 = 10.5, 12.8) for males and 15.8 years (CI0.95 = 14.5, 17.1) for females. We also documented that alligators on the site commonly live to 50 and can possibly live to >70 years of age. This study provides evidence that both male and female American Alligators in a population in coastal South Carolina exhibit a pattern of determinate growth and adds to a growing list of studies suggesting crocodilians as a group exhibit this growth pattern rather than indeterminate growth. Our findings are important for modeling population growth and determining sustainable harvest rates, particularly for alligators living near their northern distributional limit where growing seasons may be shorter and onset of sexual maturity later than in more southern portions of their range.
The effects of disturbance, including prescribed fire, vary among species and their ability to adjust to the altered environment. Our objective was to link fire-caused habitat changes with shifts in habitat use and behavioral changes in the Southern Black Racer (Coluber constrictor priapus). We compared habitat availability between burned (experimental) and unburned (control) plots and used radio telemetry to evaluate snake behavior and habitat use. The numerical abundance of C. constrictor in burned habitat was nearly twice that in the control. In both treatments, C. constrictor was associated with areas that were more open, had less canopy cover, more new vegetative growth, and less, shallower leaf litter. However, the availability of these habitats was greater in the burn treatment. Snakes were more surface active in the burn treatment and tended to be more arboreal in the control treatment. Differences in available habitat may have caused an increase in surface activity in the burn treatment, which could have biased detection rates and created higher apparent abundance in the burned treatment. Females moved more often in the control treatment, which may be due to a lack of preferred thermal habitat and reproductive thermoregulatory demands. Ultimately, fire changed habitat availability and altered the movement rates and behavior of C. constrictor causing ecological effects that may not be detected when researchers only compare abundance.
Information on population genetic structure and connectivity among populations is essential for the implementation of effective conservation and management strategies for threatened species. The giant Arapaima is one of the most heavily exploited and threatened freshwater fishes in Guyana. Using nuclear microsatellite markers and mitochondrial (mtDNA) sequences (partial 16S rRNA gene, tRNA-Leu gene, and ND1 gene), we evaluated the genetic structure of Arapaima from the Essequibo and Branco (i.e., Amazon) river basins in Guyana. Both markers showed low genetic diversity compared to previously reported studies of Arapaima from the Amazon. Only two mtDNA haplotypes were recovered in Guyana that differed in a single nucleotide position. One was novel and restricted to the Branco basin; the other had previously been reported from the Amazon but, in this study, was restricted to the Essequibo basin. Surprisingly, STRUCTURE analysis of microsatellite markers grouped Arapaima from Guyana into three distinct clusters; one was again restricted to the Branco basin, while the other two were sympatric at multiple sites in the Essequibo basin. This is the first time genetically distinct groups of Arapaima have been found in sympatry at multiple sites. Results have important implications for management of Arapaima and conservation of their genetic diversity.
A local hybrid swarm between Etheostoma radiosum and Etheostoma spectabile, found in June 1985 in a short reach of Little Glasses Creek, southern Oklahoma, consisted by eye of 35% phenotypic E. radiosum, 18% phenotypic E. spectabile, and 47% hybrids. In July 1985, investigation of an additional longer reach downstream of the initial discovery site showed that hybrids also were present there, although fewer. Thus, in 1985 both parental species, and substantial numbers of hybrids, were present in approximately a 300 m reach of the stream. No further collections were made until 2003, when sampling in the former hybrid reach and substantially further downstream showed E. radiosum to be the only species of Etheostoma present, and neither E. spectabile nor hybrids (by eye) were detected. From 2003 to 2013 the reach was surveyed 11 times, with a total of 363 darters identified phenotypically as E. radiosum, and none as E. spectabile or hybrids. Of 20 individuals sampled in December 2011 for molecular analyses, 19 had E. radiosum mitochondrial DNA, but one individual that had been identified phenotypically as E. radiosum exhibited a mtDNA control region sequence that was 97% similar to E. spectabile. These molecular findings are consistent with at least some genetic admixture and retention of maternal genes of E. spectabile in this now morphologically uniform population of E. radiosum. We suggest two hypotheses for the breakdown of the hybrid swarm, and the prevalence of E. radiosum over E. spectabile, including asymmetric introgressive backcrossing to largely eliminate E. spectabile, and environmental sorting by droughts or other stressors that favored E. radiosum.
The cyprinid genus Lobocheilos in mainland Southeast Asia has a complex taxonomic history, with 12 nominal species described in the early- to mid-20th Century from Thailand, Laos, and Vietnam by several authors based primarily on lateral melanin pigmentation and morphometric data. More recent works tentatively recognize anywhere from two to six valid species in the region. The goal of this study was to examine morphological variation between these putative species to determine if they represent distinct species. Examinations of 445 specimens, including all available type material, from throughout the region failed to define morphologically distinct groups or any differences between allopatric populations in the major zoogeographic regions in the area. Furthermore, an ontogenetic pattern of lateral melanin pigmentation was identified that has likely contributed to taxonomic confusion. One species is recognized from this region, with the oldest available name being L. rhabdoura (Fowler, 1934). Lobocheilos rhabdoura is herein redescribed, and phylogenetic relationships of populations throughout the region are reconstructed.
Two new species of snailfishes are described from the central Aleutian Islands: Careproctus staufferi and Careproctus nelsoni. The new species have trilobed teeth, moderately large pelvic discs approximately 33–49% head length, a cephalic pore pattern of 2-6-7-2, and low counts of median fins and vertebrae, including dorsal-fin rays 39–42, anal-fin rays 33–37, and total vertebrae 44–46, which distinguish them from all other congeners. Most similar to one another, they may be readily distinguished by the configuration of the chin pores, which are paired in a single pit in C. staufferi and in separate pits in C. nelsoni. Although both are overall red and pale in coloration, C. staufferi has a lateral yellow slash across the dorsal part of the abdomen and posterior, while C. nelsoni has a broad, pale, unpigmented area across the anterior part of the dorsal fin extending and broadening ventrally to a bright white abdomen. Careproctus staufferi was collected at depths of 205–366 m; C. nelsoni, at 220–329 m.
The Nurseryfish, Kurtus gulliveri, is known for “forehead brooding” parental care behavior in which the adult male carries the egg mass on a hook that overhangs the “forehead” region. This hook is derived from the supraoccipital bone, and it has been suggested to be formed through absorption rather than growth of the supraoccipital crest (SOC). Here we employed X-ray microtomography to investigate the neurocranium with focus on occurrence of the supraoccipital hook in a series of specimens from postflexion larva to adult male and female (10–200 mm SL). A slit-like cavity filled with soft tissue but not spongy bony tissue was revealed in the SOC in all examined specimens except the two smallest larvae (<15 mm SL), thus the cavity appears in the late postflexion-stage. The SOC can be divided into three parts from anterior to posterior in juveniles and adult females by reference to the cavity. 1. The crest rostrum is the most anterior end of the supraoccipital, and it increases in height with a sloped dorsal edge at about a 30° angle. 2. The intermediate segment in the middle of the crest contains a slit-like cavity filled with soft tissue, and its dorsal edge is horizontal and serrated. 3. The posterior process occupies the entire rear portion and is vertically expanded with two transverse ridges. The supraoccipital hook in adult males is derived from this basic configuration by the modifications: the crest rostrum is resorbed ontogenetically, and the dorsal anterior part of the intermediate segment protrudes forward to form the hook; the cavity within the intermediate segment extends into the hook termination. The function of cavity is not yet known; however, our results combined with the previous histological study imply that it may accommodate vessels nourishing the SOC in K. gulliveri. Apogonid fishes, putative relatives of the family Kurtidae, were included in this study for comparison. The SOC is a simple laminar structure without any cavity in Jaydia lineata and J. truncata. Based on the above findings, we suggest that: 1. the supraoccipital hook in adult males is formed by resorption of the crest rostrum combined with growth of the anterodorsal part of the intermediate segment of the SOC; 2. the SOC with a cavity is a unique osteological feature and may represent an anatomical pre-adaption allowing the development of the supraoccipital hook which made possible the evolution of the unique method of paternal forehead brooding in K. gulliveri.
The genus Notoliparis (family Liparidae) includes five species (one provisionally included) of the deepest known living fishes, distributed in four Southern Hemisphere trenches at depths from 5400 to 7554 m. A key to the species is included herein. The Kermadec Trench north of New Zealand has the deepest known species, N. kermadecensis. In 2011, seven specimens were collected in traps by the R/V Kaharoa at depths from 7000 to 7261 m. Another 41 Notoliparis were collected in 2014 at depths down to 7554 m. Examination of these individuals showed that seven represent a new species, and the others are N. kermadecensis, originally described in 1964 from five specimens taken by HMDS Galathea in 1952. At that time, the types were in such poor condition that the original description was of necessity incomplete; a redescription is included here. Examination of the new specimens showed that N. kermadecensis has several undescribed characters, including one that is apparently unique in the family.
Vitellogenin (VTG) is an egg yolk-precursor protein that serves as a nutrient source for developing embryos in oviparous vertebrates. The hormonal control of this protein has been studied in a variety of taxa, but details about the dynamics of this protein remain to be elucidated in sea turtle species. To investigate the dynamics of VTG in a multi-clutch species under natural conditions, 38 adult Loggerhead females entrained in the Florida Power and Light St. Lucie Nuclear Plant intake canal in Hutchinson Island, Florida were sampled from May–August of 2014. Blood samples were drawn to measure testosterone, estradiol 17β, and vitellogenin (T, E2, and VTG, respectively) using enzyme-linked immunosorbent assays. Ultrasound imaging of the gonads was used to determine ovarian status and to measure ovarian follicle and oviductal egg size. Results showed that VTG concentration increased from May (8.27 mg mL−1) to June (15.37 mg mL−1) and declined into July and August (9.44 mg mL−1); this decline corresponded with the end of the nesting season. E2 declined from 718.02 pg mL−1 in May to 95.89 pg mL−1 in July–August, and T declined from 2,008.35 pg mL−1 in May to 1,221.24 pg mL−1 in July–August. Mean concentration for both gonadal steroids was significantly higher in reproductively active females than means of reproductively inactive females, though overlapping concentrations of the steroids occurred between active and inactive animals. However, VTG concentration was high in reproductively active turtles and undetectable in gonadally quiescent turtles. We concluded that the addition of VTG measurement in conjunction with the gonadal steroids provides a more accurate and easily interpretable way to predict reproductive status of adult Loggerhead females. Finally, gonadal steroid and VTG concentration in our study corresponded only with late nesting animals, indicating that early season females do not become entrained in the intake canal of the power plant.
Squamate reptiles have highly developed chemosensory systems used to detect both predators and prey. Although the general ability of squamates to assess predation risk using chemical cues is well known, the detail to which squamates can make discriminations concerning risk is largely unexamined. Granite Night Lizards (Xantusia henshawi) are habitat specialists that live in exfoliations of granite boulders in dense populations. We measured the responses of Granite Night Lizards to the scent of a sympatric predator, the Lyre Snake (Trimorphodon lyrophanes), maintained on two different diets (lizard-fed and mouse-fed), as well as a non-predatory snake (the Shovelnose Snake, Chionactis occipitalis) and a blank control. We also evaluated the potential use of conspecific chemical cues to assess predation risk by quantifying the response of lizards to the scent of both calm and stressed conspecifics. We collected scents for both experiments on paper pads, which we then placed at the entrance of a shelter within a testing arena containing a focal lizard. We then used video cameras to record the behavior of focal lizards over a 60-minute period. We found that, compared to the blank control, Night Lizards in the presence of chemical cues from snakes took longer to enter the shelter, spent longer investigating chemical cues, and traveled further before entering the shelter. Lizards also spent longer investigating chemical cues from Lyre Snakes than Shovelnose Snakes. However, there were no significant differences between responses to lizard-fed and mouse-fed Lyre Snake chemical cues. We also found no evidence that lizards use conspecific chemical cues to evaluate predation risk. This study demonstrates that Granite Night Lizards can use chemical cues from their predators to assess predation risk, but further research is needed to assess whether these responses differ based on the diet of the predator.
Density-dependent growth has ordinarily been studied in aquatic ecosystems by varying the abundance of animals in mesocosms of equal volume. Aside from the unequal sample sizes involved with using this abundance-limited method, confounding factors potentially associated with levels of social interactions may also be introduced. The alternative, volume-limited method, i.e., varying the volume while maintaining equal numbers of animals, can provide a test for the presence of potentially confounding factors. Using tadpoles of Fowler's Toad, Anaxyrus fowleri, we examined the effect of density on growth rate, timing of metamorphosis, and size at metamorphosis in both abundance-limited and volume-limited experiments. We found no difference in tadpole growth rate or timing of metamorphosis between these two methods, but the metamorphs emerging from abundance-limited low density treatments were significantly smaller when compared to those in volume-limited low density treatments. Because toad tadpoles may naturally form social aggregations and schools, this suggests that the actual number of animals present may be important for normal social behavior and optimizing feeding rate. If volume-limited and abundance-limited methods of manipulating density are not equivalent, treatment method may itself be a factor that can differentially affect growth variables.
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