Article

External fertilisation and paternal care in the paedomorphic salamander Siren intermedia Barnes, 1826 (Urodela: Sirenidae)

Authors:
If you want to read the PDF, try requesting it from the authors.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

Supplementary resources (3)

Data
November 2013
Sandy Reinhard · Sebastian Voitel · Alexander Kupfer
Data
November 2013
Sandy Reinhard · Sebastian Voitel · Alexander Kupfer
Data
November 2013
Sandy Reinhard · Sebastian Voitel · Alexander Kupfer
... These studies of fish parental care imply that preoviposition nest building and cleaning may also exist in fully aquatic salamanders with external fertilization. Among the 10 extant salamander families, the members of the three families, Cryptobranchidae, Hynobiidae and Sirenidae, perform external fertilization (Reinhard, Voitel & Kupfer, 2013). Two of these families, Cryptobranchidae and Sirenidae, consist of fully aquatic salamanders, and rare cases of parental care by male salamanders have recently been reported from these families (Reinhard et al., 2013;Okada, Fukuda & Takahashi, 2015;Takahashi, Okada & Fukuda, 2017). ...
... Among the 10 extant salamander families, the members of the three families, Cryptobranchidae, Hynobiidae and Sirenidae, perform external fertilization (Reinhard, Voitel & Kupfer, 2013). Two of these families, Cryptobranchidae and Sirenidae, consist of fully aquatic salamanders, and rare cases of parental care by male salamanders have recently been reported from these families (Reinhard et al., 2013;Okada, Fukuda & Takahashi, 2015;Takahashi, Okada & Fukuda, 2017). Among cryptobranchid salamanders, Okada et al. (2015) and Takahashi et al. (2017) revealed prolonged and complex care behaviours provided for both embryos and hatchlings by male Japanese giant salamanders (Andrias japonicus). ...
... Among cryptobranchid salamanders, Okada et al. (2015) and Takahashi et al. (2017) revealed prolonged and complex care behaviours provided for both embryos and hatchlings by male Japanese giant salamanders (Andrias japonicus). In contrast, paternal care in the family Sirenidae is relatively simple and short (Reinhard et al., 2013). Given the similar life history to the fish examples and the considerable amount of postoviposition parental investment provided by male A. japonicus, the fully aquatic giant salamanders, in particular A. japonicus, are good candidates for the exploration of preoviposition nest cleaning and building behaviours. ...
Article
Parental care in salamanders is thought to be simple and typically limited to female egg attendance. No elaborate preoviposition parental care had been described from salamanders. Recent studies revealed complex care behaviours by male Japanese giant salamanders (Andrias japonicus), a fully aquatic, secretive species with external fertilization. These studies emphasize behavioural convergence in paternal care between some of the fish species and the giant salamanders. The fish examples further imply the possibility that males of A. japonicus provide preoviposition parental care in the form of nest cleaning and building. We tested this possibility and also predicted that cleaning effort by a male salamander, if exists, would increase as it approaches the spawning event. Prior to the breeding season, large males (i.e. den masters) of A. japonicus occupy and guard suitable burrows well-hidden along the stream bank. In the falls of 2012, 2013 and 2015, we videotaped and examined a single den master's pre- and postoviposition behaviours at Asa Zoological Park in Hiroshima, Japan. The den master repeatedly exhibited vigorous movements of front and hind limbs in a paddling motion at the bottom of the nest every day for the three separate years. The cleaning effort by the den master lineally increased as the spawning event approached, after which the den master completely ceased cleaning. With the cleaning behaviour, the den master made the den filled with debris including leaves and twigs buried in the sand. The floating debris was subsequently removed by the water current flowing through the nest. Water mould infection is a major cause of offspring mortality of aquatic amphibians including A. japonicus. By reducing the amount of organic matter that provides food sources for water mould, the nest cleaning likely reduces the risk of water mould infection among the offspring, serving as an important preoviposition parental care.
... In contrast, parental care among salamanders is thought to be less complex and mostly limited to egg attendance by females of terrestrial salamanders that fertilize eggs internally (Nussbaum, 1985;Crump, 1996;Wells, 2010). A few recent studies, however, reported rare cases of male parental care from the family Sirenidae (Reinhard, Voitel & Kupfer, 2013) and Cryptobranchidae (Okada, Fukuda & Takahashi, 2015). These salamanders are fully aquatic and fertilize eggs externally. ...
... These salamanders are fully aquatic and fertilize eggs externally. Reinhard et al. (2013) used the data from captive breeding to confirm the presence of male parental care in lesser siren (Siren intermedia). Okada et al. (2015), on the other hand, conducted a field study of Japanese giant salamander (Andrias japonicus) and provided quantitative analyses of various care behaviours. ...
... As predicted, agitating behaviour continued as a form of 'checking' in the post-hatching care (Fig. 2). Agitating eggs, which is also described in maternal care of plethodontid salamanders (Nussbaum, 1985) as well as in paternal care of S. intermedia (Reinhard et al., 2013), is likely to be important in preventing yolk adhesions and developmental anomalies. Thus, both promoting healthy egg development and checking for predators and unhealthy or dead eggs are likely to be important during the pre-hatching period. ...
Article
Full-text available
Parental care is remarkably diverse in its modes both within and across taxa. Within amphibians, various pre- and post-hatching care behaviours have been described in frogs. In contrast, the current knowledge about salamander parental care is largely limited to pre-hatching attendance by females. In particular, post-hatching parental care by male salamanders have never been described and analysed in detail. A recent study revealed various modes of pre-hatching care provided by male Japanese giant salamanders (Andrias japonicus). Their hatched larvae are known to stay in the nest with the father (i.e. den master) for several months before dispersal, which led to the hypothesis that den masters continue providing care for hatchlings. To test this hypothesis, we videotaped and analysed post-hatching behaviours of two male A. japonicus that remained in the nests with hatchlings in situ. We also developed and tested several predictions regarding the post-hatching care behaviours in comparison to the pre-hatching behaviours. While one male abandoned the nest, the other male remained in the nest and provided care until the larvae dispersed in the following spring. The comparative analyses on three parental care behaviours (tail fanning, agitating/checking and hygienic filial cannibalism) between pre- and post-hatching care suggest their flexible and condition-dependent nature. Furthermore, the comparison in larval mortality and potential predators between the attended and abandoned nest revealed the crucial role of a den master in improving offspring survivorship. Our observations also disclosed the possibility of leech infection posing a serious threat to larval giant salamanders. The life-history traits associated with the evolution of such prolonged post-hatching paternal care in salamanders are fully aquatic life cycle, external fertilization and stream habitat. The rare combination of these traits is unique to the family Cryptobranchidae which consists of the three imperiled and secretive giant salamanders.
... Relative to the newts, only limited and anecdotal reports exist about another aquatic breeding urodele family, Sirenidae. Based on observations of two breeding pairs in captivity, Siren intermedia territorial males guard, move, and oxygenate (via fanning) their clutches, and aggressively defend developing and recently hatched larvae against intruders (Reinhard et al. 2013(Reinhard et al. , 2015)-a parental care mode first described by Hubbs (1962;U7). In contrast, parental behavior was not observed in Pseudobranchus striatus (Kowalski 2004). ...
... It is increasingly evident that amphibians are an excellent system to address timely and relevant questions about the evolution of reproductive strategies, including parental care (i.e., Kupfer et al. 2006;Brown et al. 2010;Poo and Bickford 2013;Reinhard et al. 2013;Stynoski et al. 2014b;Vargas-Salinas et al. 2014;Lehtinen et al. 2014;Rojas 2014;Bravo-Valencia and Delia 2016;Yoshioka et al. 2016;Delia et al. 2017;Ringler et al. 2017;Schulte and Mayer 2017;Stynoski et al. 2018). The advent of new technologies has broadened the range of questions that can be addressed concerning the molecular and physiological underpinnings of parental behaviors (Roland and O'Connell 2015;Fischer et al. 2019). ...
Article
Full-text available
Despite rising interest among scientists for over two centuries, parental care behavior has not been as thoroughly studied in amphibians as it has in other taxa. The first reports of amphibian parental care date from the early 18th century, when Maria Sibylla Merian went on a field expedition in Suriname and reported frog metamorphs emerging from their mother's dorsal skin. Reports of this and other parental behaviors in amphibians remained descriptive for decades, often as side notes during expeditions with another purpose. However, since the 1980s, experimental approaches have proliferated, providing detailed knowledge about the adaptive value of observed behaviors. Today, we recognize more than 30 types of parental care in amphibians, but most studies focus on just a few families and have favored anurans over urodeles and caecilians. Here, we provide a synthesis of the last three centuries of parental care research in the three orders comprising the amphibians. We draw attention to the progress from the very first descriptions to the most recent experimental studies, and highlight the importance of natural history observations as a source of new hypotheses and necessary context to interpret experimental findings. We encourage amphibian parental care researchers to diversify their study systems to allow for a more comprehensive perspective of the behaviors that amphibians exhibit. Finally, we uncover knowledge gaps and suggest new avenues of research using a variety of disciplines and approaches that will allow us to better understand the function and evolution of parental care behaviors in this diverse group of animals.
... Relative to the newts, only limited and anecdotal reports exist about another aquatic breeding urodele family, Sirenidae. Based on observations of two breeding pairs in captivity, Siren intermedia territorial males guard, move, and oxygenate (via fanning) their clutches, and aggressively defend developing and recently hatched larvae against intruders (Reinhard et al. 2013(Reinhard et al. , 2015)-a parental care mode first described by Hubbs (1962;U7). In contrast, parental behavior was not observed in Pseudobranchus striatus (Kowalski 2004). ...
... It is increasingly evident that amphibians are an excellent system to address timely and relevant questions about the evolution of reproductive strategies, including parental care (i.e., Kupfer et al. 2006;Brown et al. 2010;Poo and Bickford 2013;Reinhard et al. 2013;Stynoski et al. 2014b;Vargas-Salinas et al. 2014;Lehtinen et al. 2014;Rojas 2014;Bravo-Valencia and Delia 2016;Yoshioka et al. 2016;Delia et al. 2017;Ringler et al. 2017;Schulte and Mayer 2017;Stynoski et al. 2018). The advent of new technologies has broadened the range of questions that can be addressed concerning the molecular and physiological underpinnings of parental behaviors (Roland and O'Connell 2015;Fischer et al. 2019). ...
... Paquet and Smiseth (2016) summarize how maternal effects on offspring phenotypes (e.g., egg size, color, and hormones) might alter the cost and benefits of male care in ways that reduce conflict and influence male care on behavioral timescales. On evolutionary timescales, offspring phenotype might mediate the coevolution of parental investment more broadly and contribute to trait complexity in species with male-only care; which occurs in annelids, gastropods, and numerous groups of arthropods, fishes, and amphibians (Gross and Sargent 1985, Beck 1998, Tallamy 2001, Mank et al. 2005, Fletcher et al. 2009, Kamel and Grosberg 2012, Reinhard et al. 2013, Requena et al. 2014. The evolution of male care might enable females to reduce pre-zygotic forms of investment, which in turn could increase offspring dependency in ways that stabilize, refine, and even elaborate post-zygotic care. ...
... Given the functional interchangeability of female clutch contributions and prolonged male care in glassfrogs, the phylogenetic pattern we found suggests that clutch phenotype might provide a general mechanism for the coevolution of parental investment in species with uniparental care. Exclusive male care evolved repeatedly in many phyla, including annelids, molluscs, arthropods, and chordates (Gross and Sargent 1985, Beck 1998, Tallamy 2001, Mank et al. 2005, Fletcher et al. 2009, Kamel and Grosberg 2012, Reinhard et al. 2013, Requena et al. 2014. Comparative analyses in many of these groups indicate that male-only care most frequently evolved from no care (Beck 1998, Reynolds et al. 2002, Mank et al. 2005, Gilbert and Manica 2015. ...
Article
Full-text available
Many animals improve offspring survival through parental care. Research on coevolution between parents has provided key insight into the genesis and maintenance of biparental care. However, understanding family dynamics more broadly requires assessing potential male–female coevolutionary processes in the more widespread and common context of uniparental care. Here we explore how pre‐zygotic maternal contributions—jelly coats and oviposition sites—influence offspring dependency and change with the evolution of male‐only care in glassfrogs. Egg care appears ubiquitous among glassfrogs, with repeated evolutionary transitions from brief female‐only to extended male‐only care. Glassfrogs also exhibit a diversity of sex‐specific parental traits involving maternal egg‐jelly contributions, oviposition‐site choice, and egg‐attendance behaviors. We hypothesize these form functionally interchangeable suites of traits that mediate embryos’ susceptibility to environmental risk. First, using parent‐removal field experiments, egg‐hydration assays, and comparative analyses, we found no evidence that evolutionary transitions in caring sex or care duration alter the adaptive functions or overall benefits of care (across 8 species). Rather, the jelly‐contributions and oviposition‐site use associated with brief care influence embryo susceptibility to the same risks that are reduced by prolonged care. Next, we examined the diversity and evolutionary history of pre‐ and post‐zygotic parental traits, applying phylogenetic comparative methods to literature records and our field observations of 40 species (71 total, ~ 47 % of the family). Because pre‐zygotic maternal contributions determine embryo requirements, the evolution of male care might enable and/or compensate for reduced maternal contributions. Supporting this hypothesis, we found that the repeated evolution of complex male care is always associated with reductions in egg‐jelly and changes in oviposition sites. This phylogenetic pattern suggests that clutch phenotype might provide a general mechanism for the coevolution of parental investment in species with uniparental care. If different combinations of egg phenotypes and post‐zygotic care are ecologically equivalent, their interchangeability could allow parental traits to coevolve between the sexes without compromising offspring survival. Male‐only care is widespread in oviparous metazoans—from annelids and molluscs, to arthropods, fishes and amphibians. Investigations of egg and clutch phenotypes offer new prospects for broadening research on the coevolutionary dynamics of parental care.
... Although fairly common in fishes (Gross 2005), care of offspring by the male parent is relatively rare in tetrapods. Maternal care is common in salamanders, but paternal care has only been definitively observed in primitive aquatic species of the families Cryptobranchidae and Sirenidae (Nussbaum 2003;Reinhard et al. 2013). Detailed observations of parental care in natural habitats are rare due to the secretive nature of salamanders, with nests typically hidden under rocks, in mats of vegetation, in burrows, or under (or within) rotting logs (Petranka 1998). ...
... Over half of the fishes observed were centrarchids, which were frequently oriented toward the nest, indicating a higher level of interest in the nest than the other fish species. Some centrarchids are known to engage in nest-raiding behavior (Pflieger 1997), so their primary role may be as potential egg predators. Diet studies generally do not list centrarchids as prey (e.g., Nickerson and Mays 1973;Petranka 1998). ...
Article
Paternal care is relatively uncommon in tetrapods but appears to be the rule in the large aquatic salamanders of the primitive family Cryptobranchidae (North America: hellbenders, genus Cryptobranchus; Asia: giant salamanders, genus Andrias). For the Ozark hellbender, C. alleganiensis bishopi, a federally endangered subspecies, anecdotal observations of paternal care have been reported, but no quantitative assessments have been made. We quantified behavior of a guarding male hellbender from video footage collected over 6 weeks in 2008 from a naturally occurring nest. We quantified behavior of the guarding male to help develop hypotheses about costs and benefits of paternal care. Overall, there were high frequencies of tail fanning of the eggs and rocking behaviors (rhythmic, lateral back-and-forth movements of the body), which increase aeration of the nest. The male rarely left the nest unguarded and spent over half of the recorded time at the nest exposed at the nest entrance. Potential egg predators observed included centrarchid, cyprinid, ictalurid, and percid fishes, with centrarchids being the most common and exhibiting the most interest in the nest. The frequency of foraging by the male was low (n = 8 strikes at identifiable prey), with a 37% success rate. The male was observed to consume seven of his eggs. Our data represent the first systematic analysis of paternal care of Ozark hellbenders and elucidate some of the costs (low foraging success, potential energetic costs of tail fanning and rocking) and benefits (aeration of eggs, protection from egg predators) of paternal care. © 2018 Japan Ethological Society and Springer Japan KK, part of Springer Nature
... Controversy persists in the family-level phylogenetic relationships of salamanders because of the potential polyphyletic origin of paedomorphosis (Adler, 2003;Larson et al., 2003), internal fertilization (Frost et al., 2006), and sperm storage (Sever, 1994), as well as the difficulty of resolving conflicting morphological and molecular data (Duellman and Trueb, 1986;Larson and Dimmick, 1993;Wiens et al., 2005;Frost et al., 2006;Zhang and Wake, 2009). Also, the reproductive biology of Sirenidae has proven important to salamander phylogeny, as Sirenidae have unique morphological features (Duellman and Trueb, 1986), but also exhibit ancestral traits such as external fertilization (Kowalski, 2004;Reinhard et al., 2015) and no sperm storage structures (Sever et al., 1996). Most reproductive studies of Sirenidae have focused on females, but the male reproductive biology offers important insight into the phylogeny and ecology of this family. ...
Article
We examined the testicular histology of 32 adult male Pseudobranchus axanthus collected at Rainey Slough (Glades County), Florida, during 1974-76. The process of spermatogenesis was evident throughout all regions of the testes and appeared to occur year-round. The testes contain numerous, spherical-to-oblong testicular lobules that vary greatly in size. Unlike all other salamanders, which exhibit cystic spermatogenesis along with a caudo-cephalic wave of maturing cell types (leading to spatial and temporal segregation of germ cells), spermatogenesis in P. axanthus lacks testicular cysts. Instead, the testicular lobules possess an assortment of different spermatogenic cell stages, all arising from primary spermatogonia through mitotic and meiotic divisions, thus creating a germ cell/Sertoli cell syncytium along the lobular epithelium. Secondary spermatocytes then detach from the lobular epithelium and from their accompanying Sertoli cells and undergo spermiogenesis within the lumen. We propose naming this new type of germ cell development non-cystic lobular spermatogenesis. Upon maturation, sperm travel from the lobular lumen into a longitudinal testicular canal via an intratesticular duct. The testicular canal conveys sperm to about 15 vasa efferentia, which then connect to genital renal capsules. Sperm move through the renal tubules and eventually reach the Wollfian duct. This duct transports sperm to the cloaca. © 2017 by the American Society of Ichthyologists and Herpetologists.
... The feeding behaviour of Siren intermedia nettingi had been studied for several months at the aquatic research animal facility at the FSU Jena. The animal husbandry of the FSU reproduced the natural habitat so well under laboratory conditions that the sirens were able to successfully reproduce in captivity (Reinhard et al. 2015(Reinhard et al. , 2013. The animals were offered potential foods from distinct categories (i.e., invertebrates, vertebrates, plants, and debris). ...
Article
Full-text available
Herbivory, and thus, the ability to acquire energy from consuming plant material, evolved numerous times independently within vertebrates. Several mechanical solutions for processing plant material have emerged along with the independent rise of herbivorous feeding strategies. Comparative studies of these mechanical solutions suggest that herbivory might generally relate to “improved” and hence comparatively effective food processing mechanisms, often involving the jaws. Such processing behaviours involving the jaws can be referred to as chewing sensu lato. While herbivory is relatively common among vertebrates, it is generally believed that salamanders exclusively feed on other animals (i.e., carnivory). Further, it had been hypothesized that salamander food processing is limited to “simple” and comparably ineffective puncture crushing movements (i.e., opening and closing movements of the jaws in combination with pointed teeth), which may not be efficient enough to break down plant material. However, sirenid salamanders (i.e., dwarf sirens and sirens, genera Pseudobranchus and Siren respectively) have long been reported to consume large amounts of plant material besides feeding on animal prey. Additionally, some sirenids have only recently been shown to apply complex three-dimensional chewing behaviours. These complex chewing behaviours could potentially enable the mechanical breakdown of plant material. Here we comparatively study sirens with particular regards to the form and function of their feeding apparatus and their feeding habits. We demonstrate that sirenids generally seem to apply complex chewing mechanisms and, in fact, consume both plant- and animal foods. Comparative gastrointestinal morphology, however, suggests that among sirenids, only sirens are apt to digest and extract energy from plant material, suggesting that dwarf sirens may not benefit from the energy of their “plant food”, while sirens appear to be facultative herbivorous - or better, omnivorous. Consequently, our results indicate that some salamanders can eat, process, and acquire energy from plant material, hence, contradicting the commonly accepted idea that salamanders are generally carnivorous.
... Both sites have also yielded isolated femora that show 1230 one potential synapomorphy with Hynobiidae (Skutschas, 2014(Skutschas, , 2015. Potentially, then, K. been presumed based on other considerations like the retention of external fertilization in sirenids 1256 (Reinhard et al., 2013). Likewise, Amphiumidae and Plethodontidae are consistently sister-groups in 1257 phylogenetic analyses of molecular data, rather than Amphiumidae being close to Proteidae or 1258 ...
Preprint
Full-text available
Identical to the full submission, including the updated figure, to the second round of peer review.
... This rarity of paternal care among salamanders is best explained by the association hypothesis, which predicts that the sex with closer association with embryos provides parental care (Williams 1975;Gross and Shine 1981). All salamander species, except those in three families, Cryptobranchidae, Hynobidae and Sirenidae, fertilize internally via spermatophores (Reinhard et al. 2013), in which females develop a closer association with the embryos and thus are the care providers when parental care exists. In Cryptobranchidae, fertilization occurs externally, and males defend courtship grounds (i.e., nests) in order to sequentially mate with multiple females, as the females leave the nests after depositing the eggs (Nussbaum 1985;Kawamichi and Ueda 1998). ...
Article
Full-text available
Parental care among salamanders is typically provided by females. A rare case of parental care by male salamanders appears to occur in Cryptobranchidae. Yet, paternal behaviors have rarely been reported from natural populations of any Cryptobranchid salamanders, and their adaptive significance is poorly understood. The present study aimed to examine paternal care behaviors in a fully aquatic Japanese giant salamander (Andrias japonicus) in situ. At the beginning of the summer breeding season, large males, called den-masters, occupy burrows along stream banks for breeding and nesting. We videotaped post-breeding behaviors of two den-masters that stayed with the eggs, one in a natural and the other in an artificial nest in natural streams. We identified three behaviors, tail fanning, agitating and egg eating, to be parental care. Tail fanning provides oxygenated water for the eggs. We found that the den-master in the artificial nest, where dissolved oxygen level was lower, displayed tail fanning more fre-quently. Agitating the eggs with its head and body likely prevents yolk adhesions. The den-masters selectively ate whiter eggs that appeared to be dead or infected with water mold. This behavior, which we termed hygienic filial cannibalism, likely prevents water mold from spreading over healthy eggs. Digital video images relating to this article are available at
... Most urodeles have internal fertilization, which is preceded by the use of spermatophores (Delsol, 1986;Duellman and Trueb, 1986). External fertilization occurs in the suborders Sirenoidea (Reinhard et al., 2013;Sever et al., 1996;Sever, 2013;Ultsch, 1973) and Cryptobranchoidea (Makino, 1934;Smith, 1907;Thorn, 1986). ...
Article
Full-text available
It is not well known how low temperatures, like a subarctic steppe–tundra climate, influence reproductive traits of ectothermic vertebrates. To begin answering this question, we studied male and female reproductive systems of Salamandrella keyserlingii inhabiting a Tomsk population (southeast of Western Siberia), Russia, in ecological and physiological terms. In males, before spermiation, the testicular size and weight in late April–early May were greatest of all. Spermiation occurred during breeding immigration in spring when mean air temperature was above 10°С, and at the same time rain fell. After spermiation, the testicular size and weight decreased sharply, and the diameter of the vasa deferentia increased. “Spawning” (i.e., simultaneous extrusion of sperm and oviposition) occurred from late April to late May, and this duration fluctuated in temperature and humidity. The testicular size and weight increased in summer. Sperm mass was detected in the testes by the smear method in April–September, except in June when single fragmented unrealized sperm was detected and in July when spermatids were detected. In females, ovarian weight was greatest in spring before ovulation. From late June, vitellogenesis began in ovarian follicles, in which mint green yolks accumulated. Melanin deposited in the surface of the ovary from July when oviducts were hypertrophying. In contrast, some large-sized females did not show any sexual maturity shortly before hibernation (although these females may be subadults). These results suggest that low temperatures in Siberia induce early timing of gamete maturation in females, but the females’ reproductive cycle might also be biennial. A reproductive cycle in males was annual with the completion of the gamete maturation process in August.
... Ihre Körperform ist langgestreckt, wobei die Hinterextremitäten sowie der gesamte Beckengürtel fehlen und die Arme nur sehr reduziert vorhanden sind. Anstelle von premaxillaren Zähnen besitzen die Sireniden verhornte Leisten, die einen kräftigen Biss und sogar ein Zerkleinern der Beute ermöglichen (Duellman & Trueb 1994, Petranka 1998, Wells 2007 ). Diese Merkmale führten dazu, dass die Sireniden zeitweise sogar in eine eigene Ordnung gestellt wurden (Trachystomata, siehe Cope 1889, Goin & Goin 1962, Cochran & Goin 1970, Duellman & Trueb 1994). ...
... There are many understudied families of amphibians, with growing evidence indicating that care patterns are more diverse than currently appreciated (e.g. Reinhard et al., 2013;Banerjee, 2014;Gururaja et al., 2014;Iskandar et al., 2014). Basic natural history is key to uncovering this diversity, as well as developing opportunities to test important hypotheses of parental care evolution. ...
Article
Many animals provide parental care to offspring. Parental sex-roles vary extensively across taxa, and such patterns are considered well documented. However, information on amphibians is lacking relative to other vertebrate groups. We combine natural history observations with functional and historical analyses to examine the evolution of egg care in glassfrogs (Centrolenidae). Parental care was considered rare and predominately provided by males. Our field observations of 40 species revealed that care occurs throughout the family, and the caregiving sex changes across lineages. We discovered that a brief period of maternal care is widespread and occurs in species previously thought to lack care. Using a combination of female-removal experiments, prey-choice tests with egg-eating katydids, and parental disturbance-tolerance assays, we confirm the adaptive benefits of short-term maternal care in wild Cochranella granulosa and Teratohyla pulverata. To examine historical transitions between caregiving sexes, we assembled a molecular phylogeny and estimated ancestral care states using our data and the literature. We assessed patterns indicative of sex-specific constraints by testing whether transitions between the sexes are associated with changes in care levels. Our analyses support that male-only care evolved 2-3 times from female-only care, and this change is associated with substantial increases in care levels-a pattern supporting the hypothesis that male-only care evolved via constraints on maternal expenditure. Many groups of amphibians remain poorly studied, with emerging evidence indicating that care patterns are more diverse than currently appreciated. Natural history remains fundamental to uncovering this diversity and generating testable hypotheses of sex-role evolution. This article is protected by copyright. All rights reserved.
Article
We analyzed growth in a population of Siren intermedia nettingi, Western Lesser Siren, from northwestern Louisiana using a markrecapture technique employing PIT tags from January 1992 through March 1998. Traps were monitored for eight consecutive trap nights for all four seasons from 1992 to 1996, January and December winter trapping sessions in 1997, and late February through early March in 1998. A total of 1,004 siren captures included 575 original captures and 429 recaptures. A total of 223 sirens were recaptured at least once for a recapture rate of 38.7%. Thirty-five of the original sirens captured were recaptured in the same season and year and were not used in the analyses. Therefore, we had a usable recapture rate of 32.7%. Based on captures, bites by conspecifics, and presence of juveniles in the study pond, we concluded that sirens in this population were most active in autumn and winter and presumably had a winter breeding season. Males grew faster and reached larger sizes than females due to the large energy investment of females that produced ova and the importance of male agonistic behavior toward other male and female conspecifics. The greatest growth occurred in the spring, despite increased activity in autumn and winter. Sirens were least active in the summer. Growth was inversely proportional to size and smaller sirens grew at a faster rate than larger ones.
Article
Full-text available
We review the phylogeny, sperm competition, morphology, physiology, and fertilization environments, of the sperm of externally fertilizing fish and amphibians. Increased sperm competition in both fish and anurans generally increases sperm numbers, sperm length and their energy reserves. The difference between the internal osmolarity and iconicity of sperm cells and those of the aquatic medium control the activation, longevity, and velocity of sperm motility. Hypo-osmolarity of the aquatic medium activates the motility of freshwater fish and amphibian sperm and hyper-osmolarity activates the motility of marine fish sperm. The average longevity of the motility of marine fish sperm (∼550 sec) was significantly (P<0.05) greater than that of freshwater fish sperm (∼150 sec), with the longevities of both marine and freshwater fish being significantly (P<0.05) lower than that of anuran sperm (∼4100 sec). The velocity of anuran sperm (25 μm/sec) was significantly (P<0.05) lower than the velocity of marine fish (140 μm/sec) or freshwater fish (135 μm/sec) sperm. The longevity of the sperm of giant salamanders (Cryptobranchoidea) of ∼600 sec. was greater than that of freshwater fish sperm but much lower than anuran sperm. Our experiments and the literature showed that higher osmolarities promote greater longevity in anuran sperm, and some freshwater fish sperm, and that anuran and cryptobranchid sperm maintained membrane integrity long after the cessation of motility, demonstrating a sharing of energy reserves between motility and the maintenance of membrane integrity. The maintenance of the membrane integrity of anuran sperm in fresh water for up to 6 hrs showed an extremely high osmotic tolerance relative to fish sperm. The very high longevity and osmotic tolerance of anuran sperm and high longevity of cryptobranchid sperm, relative to those of freshwater fish, may reflect the complex fertilization history of amphibian sperm in general and anurans recent reversion from internal to external fertilization. Our findings provide a greater understanding of the reproductive biology of externally fertilizing fish and amphibians, and a biological foundation for the further development of reproduction technologies for their sustainable management.
Article
Social animals with a monophasic life cycle exhibit a more complex social system for reproduction than that of other social animals in which the life cycle is biphasic. The family Hynobiidae (Amphibia: Caudata) is phylogenetically basal to most other salamander families, practices external fertilization, and has a biphasic life cycle alternating between aquatic breeding and terrestrial nonbreeding phases. There are many controversial and specific social interactions during the aquatic breeding phase in several of the inspected species of this family when comparing their sexual or social behaviors with those of other animal species. Some papers describing these social interactions have misled us by erroneously referring to phenomena of territoriality, chase, amplexus/midwifing, mating ball formation, scramble competition, and parental care. Especially, I am skeptical of the male’s premating displays (e.g., chase, clasp, snout contact, chin rubbing, tail undulation, smelling, digging) regarded as “courtship” in some papers, except for Ranodon sibiricus that may produce a single large spermatophore, because most of these displays result in the female’s escape from the male. Also, I am skeptical of the behavior of a male, staying near deposited egg sacs, regarded as “parental care” because such a male can be predicted to change easily with other males and not to guard eggs or embryos against predators. Thus, I provide a focal review and correct observations on hynobiid sexual and social behavior by incorporating some unignorable descriptions that do not fit with previous descriptions on aquatic social interactions of this family.
Preprint
Full-text available
Molecular divergence dating has the potential to overcome the incompleteness of the fossil record in inferring when cladogenetic events (splits, divergences) happened, but needs to be calibrated by the fossil record. Ideally but unrealistically, this would require practitioners to be specialists in molecular evolution, in the phylogeny and the fossil record of all sampled taxa, and in the chronostratigraphy of the sites the fossils were found in. Paleontologists have therefore tried to help by publishing compendia of recommended calibrations, and molecular biologists unfamiliar with the fossil record have made heavy use of such works. Using a recent example of a large timetree inferred from molecular data, I demonstrate that calibration dates cannot be taken from published compendia without risking strong distortions to the results, because compendia become outdated faster than they are published. The present work cannot serve as such a compendium either; in the slightly longer term, it can only highlight known and overlooked problems. Future authors will need to solve each of these problems anew through a thorough search of the primary paleobiological and chronostratigraphic literature on each calibration date every time they infer a new timetree; over 40% of the sources I cite were published after mid-2016. Treating all calibrations as soft bounds results in younger nodes than treating all calibrations as hard bounds. The unexpected exception are nodes calibrated with both minimum and maximum ages, further demonstrating the widely underestimated importance of maximum ages in divergence dating.
Article
Physiological condition linked to reproduction-related morphological traits (e.g., body mass, head width, tail height) is a key determinant of ecotypes related to fitness in ecological selection. In migratory salamanders such as the families Ambystomatidae (internal fertilization), Salamandridae (internal), and Hynobiidae (external), such morphological traits change at the transition between terrestrial and aquatic habitats. Unlike many other migratory salamanders, Hynobius kimurae (Hynobiidae) immigrates from land to water for aquatic hibernation during fall, and the immigration is not related to fall breeding. In this context, does fall immigration to water for winter dormancy induce changes in reproduction-related morphological traits? We analyzed changes in body shape and mass concurrent with physiological condition of 244 males and 131 females of H. kimurae with only data on first capture during fall and spring from 1996 to 2016. Although reproduction-related morphological traits in other migratory salamanders change simultaneously when they enter the water and subsequently initiate breeding during either season of fall–spring, such changes occurred both in male and female H. kimurae firstly during fall (shortly after entering the water) and secondly during spring (shortly after awaking from hibernation), except for head width being static throughout seasons. The differences suggest that these two-step changes during a prolonged period from fall to spring would be concentrated in a short period of breeding activity during either season of fall–spring in other migratory salamanders without hibernating in the water. As sexually selected, sexual dimorphism was detected in size and shape, especially shape of the tail, both height and length of which were greater in males than in females regardless of the sexes being terrestrial or aquatic. The male’s larger tail during the terrestrial phase may be a stock for a more developed tailfin (amount of reproductive output) in the aquatic-phase male potentially related to fitness.
Article
Full-text available
Salamanders are an important group of living amphibians and model organisms for understanding locomotion, development, regeneration, feeding, and toxicity in tetrapods. However, their origin and early radiation remain poorly understood, with early fossil stem-salamanders so far represented by larval or incompletely known taxa. This poor record also limits understanding of the origin of Lissamphibia (i.e., frogs, salamanders, and caecilians). We report fossils from the Middle Jurassic of Scotland representing almost the entire skeleton of the enigmatic stem-salamander Marmorerpeton . We use computed tomography to visualize high-resolution three-dimensional anatomy, describing morphologies that were poorly characterized in early salamanders, including the braincase, scapulocoracoid, and lower jaw. We use these data in the context of a phylogenetic analysis intended to resolve the relationships of early and stem-salamanders, including representation of important outgroups alongside data from high-resolution imaging of extant species. Marmorerpeton is united with Karaurus , Kokartus , and others from the Middle Jurassic–Lower Cretaceous of Asia, providing evidence for an early radiation of robustly built neotenous stem-salamanders. These taxa display morphological specializations similar to the extant cryptobranchid “giant” salamanders. Our analysis also demonstrates stem-group affinities for a larger sample of Jurassic species than previously recognized, highlighting an unappreciated diversity of stem-salamanders and cautioning against the use of single species (e.g., Karaurus) as exemplars for stem-salamander anatomy. These phylogenetic findings, combined with knowledge of the near-complete skeletal anatomy of Mamorerpeton, advance our understanding of evolutionary changes on the salamander stem-lineage and provide important data on early salamanders and the origins of Batrachia and Lissamphibia.
Preprint
Full-text available
Molecular divergence dating has the potential to overcome the incompleteness of the fossil record in inferring when cladogenetic events (splits, divergences) happened, but needs to be calibrated by the fossil record. Ideally but unrealistically, this would require practitioners to be specialists in molecular evolution, in the phylogeny and the fossil record of all sampled taxa, and in the chronostratigraphy of the sites the fossils were found in. Paleontologists have therefore tried to help by publishing compendia of recommended calibrations, and molecular biologists unfamiliar with the fossil record have made heavy use of such works. Using a recent example of a large timetree inferred from molecular data, I demonstrate that calibration dates cannot be taken from published compendia without risking strong distortions to the results, because compendia become outdated faster than they are published. The present work cannot serve as such a compendium either; in the slightly longer term, it can only highlight known and overlooked problems. Future authors will need to solve each of these problems anew through a thorough search of the primary paleobiological and chronostratigraphic literature on each calibration date every time they infer a new timetree; over 40% of the sources I cite were published after mid-2016. Treating all calibrations as soft bounds results in younger nodes than treating all calibrations as hard bounds. The unexpected exception are nodes calibrated with both minimum and maximum ages, further demonstrating the widely underestimated importance of maximum ages in divergence dating.
Article
Females of some Asian salamanders of the genus Hynobius deposit in streams their eggs embedded in a translucent envelope called an ‘egg sac’. The edges of the envelope exhibit a spectacular blue-to-yellow iridescent glow, which instantaneously disappears when the sac is removed from water. First, our scanning electron microscopy analyses reveal that the inner surface of the 100 μm-thick envelope displays striations (length scale of about 3 μm), which are themselves covered by much smaller (190 ± 30 nm) and quasi-periodic corrugations. The latter could constitute a surface diffraction grating generating iridescence by light interference. Second, our transmission electron microscopy and focused-ion-beam scanning electron microscopy analyses show that the bulk of the egg sac wall is composed of meandering fibres with a quasi-periodic modulation of 190 ± 60 nm along the thickness of the envelope, generating a photonic crystal. Third, Fourier power analyses of 450 electron microscopy images with varying incident angles indicate that changing the surrounding medium from water to air shifts most of the backscattered power spectrum to the ultraviolet range, hence, explaining that the egg sac loses visible iridescence when removed out of the water. Fourth, the results of our photography and optical spectroscopy experiments of submerged and emerged egg sacs rule out the possibility that the iridescence is due to a thin film or a multilayer, whereas the observed non-specular response is compatible with the backscattering expected from surface diffraction gratings and volumetric photonic crystals with spatial 1D modulation. Finally, although we mention several potential biological functions of the egg sac structural colours and iridescence, we emphasise that these optical properties might be the by-products of the envelope material internal structure selected during evolution for its mechanical properties.
Article
Synopsis Teeth are critical to the functional ecology of vertebrate trophic abilities, but are also used for a diversity of other non-trophic tasks. Teeth can play a substantial role in how animals move, manipulate their environment, positively interact with conspecifics, antagonistically interact with other organisms, and sense the environment. We review these non-trophic functions in an attempt to place the utility of human and all other vertebrate dentitions in a more diverse framework that emphasizes an expanded view of the functional importance and ecological diversity of teeth. In light of the extensive understanding of the developmental genetics, trophic functions, and evolutionary history of teeth, comparative studies of vertebrate dentitions will continue to provide unique insights into multi-functionality, many-to-one mapping, and the evolution of novel abilities.
Preprint
Full-text available
This version is identical to the first revision being peer-reviewed at Frontiers in Genetics. Because a few calibration dates have changed, the analysis has to be repeated; this is ongoing and will change the parts of the text highlighted in yellow (and the figure, which is not included in this version), but most likely not by much.
Article
A taxon, traditionally referred to the rank order, encompassing all recent taxa of salamanders and their close fossil relatives, is highly supported as holophyletic in all recent phylogenetic analyses of amphibians. Under the Duplostensional Nomenclatural System, among about thirty nomina available for this taxon in the literature, two only qualify as sozodiaphonyms: Urodela Duméril, 1805 and Caudata Duméril, 1805. The conflict for validity between these two nomina is solved by the Principle of Airesy (first reviser). The valid nomen for this taxon is therefore Urodela Duméril, 1805, which corresponds to the majority of uses in the literature since their creation, and which should replace all other nomina, authorships and dates sometimes credited to this taxon in publications, catalogues and databases.
Article
Full-text available
Molecular divergence dating has the potential to overcome the incompleteness of the fossil record in inferring when cladogenetic events (splits, divergences) happened, but needs to be calibrated by the fossil record. Ideally but unrealistically, this would require practitioners to be specialists in molecular evolution, in the phylogeny and the fossil record of all sampled taxa, and in the chronostratigraphy of the sites the fossils were found in. Paleontologists have therefore tried to help by publishing compendia of recommended calibrations, and molecular biologists unfamiliar with the fossil record have made heavy use of such works (in addition to using scattered primary sources and copying from each other). Using a recent example of a large node-dated timetree inferred from molecular data, I reevaluate all 30 calibrations in detail, present the current state of knowledge on them with its various uncertainties, rerun the dating analysis, and conclude that calibration dates cannot be taken from published compendia or other secondary or tertiary sources without risking strong distortions to the results, because all such sources become outdated faster than they are published: 50 of the (primary) sources I cite to constrain calibrations were published in 2019, half of the total of 280 after mid-2016, and 90% after mid-2005. It follows that the present work cannot serve as such a compendium either; in the slightly longer term, it can only highlight known and overlooked problems. Future authors will need to solve each of these problems anew through a thorough search of the primary paleobiological and chronostratigraphic literature on each calibration date every time they infer a new timetree, and that literature is not optimized for that task, but largely has other objectives.
Article
Full-text available
Summary The order Caudata includes about 660 species and displays a variety of important developmental traits such as cleavage pattern and egg size. However, the cleavage process of tailed amphibians has never been analyzed within a phylogenetic framework. We use published data on the embryos of 36 species concerning the character of the third cleavage furrow (latitudinal, longitudinal or variable) and the magnitude of synchronous cleavage period (up to 3-4 synchronous cell divisions in the animal hemisphere or a considerably longer series of synchronous divisions followed by midblastula transition). Several species from basal caudate families Cryptobranchidae (Andrias davidianus and Cryptobranchus alleganiensis) and Hynobiidae (Onychodactylus japonicus) as well as several representatives from derived families Plethodontidae (Desmognathus fuscus and Ensatina eschscholtzii) and Proteidae (Necturus maculosus) are characterized by longitudinal furrows of the third cleavage and the loss of synchrony as early as the 8-cell stage. By contrast, many representatives of derived families Ambystomatidae and Salamandridae have latitudinal furrows of the third cleavage and extensive period of synchronous divisions. Our analysis of these ontogenetic characters mapped onto a phylogenetic tree shows that the cleavage pattern of large, yolky eggs with short series of synchronous divisions is an ancestral trait for the tailed amphibians, while the data on the orientation of third cleavage furrows seem to be ambiguous with respect to phylogeny. Nevertheless, the midblastula transition, which is characteristic of the model species Ambystoma mexicanum (Caudata) and Xenopus laevis (Anura), might have evolved convergently in these two amphibian orders.
Chapter
Full-text available
Chapter
Full-text available
A comprehensive review of courtship behavior in salamanders was last presented by Salthe (1967). Many new behavioral observations have been made in the ensuing 35 years. Below, we summarize trends in courtship behavior within and among salamander families. We also consider the nature of major transitions in courtship behavior.
Article
Full-text available
Conducimos un estudio de marcarecaptura de Siren intermedia en un humedal del sureste de Missouri que es manejado intensamente para aves acuáticas. Durante un período de 9 meses, examinamos características de la población, tasas de crecimiento y actividad espacial. Estimaciones de densidad y biomasa fueron de 1.35 a 2.17 animales/m2 y de 44.9 a 72.2 g/m2. Los juveniles formaron el 39% de la población. Machos adultos fueron significativamente más grandes tanto en longitud total como en masa comparados con hembras adultas. Las sirenas de nuestra población tuvieron relativamente bajas tasas de crecimiento comparadas con algunas poblaciones en otras áreas. Individuos pequeños solieron crecer más rápido que los más grandes. La distancia máxima entre capturas no difirió significativamente entre los juveniles y los machos y hembras adultos. Los rangos de hogar de adultos se sobrepusieron bastante y variaron mucho en tamaño, desde 1 a 232 m2. Las sirenas pueden ser el vertebrado dominante en muchas comunidades de humedales, y su historia natural y ecología espacial deben ser consideradas en decisiones del manejo.
Article
Full-text available
Posthatching parental care is known in amphibians for frogs and caecilians but, thus far, has never been reported for salamanders. Here, we describe the parental behavior of a female Northwest Italian Cave Salamander, Speleomantes strinatii, from egg deposition to nest site abandonment. The female was kept in seminatural conditions and filmed in complete darkness by an infrared video camera. In November 2007, the female laid nine eggs in a small depression of the terrarium floor, displaced the clutch with hind limbs, and showed antipredator behaviors toward a conspecific female and an intruding Roof Rat (Rattus rattus). During egg brooding, the female remained in contact with the clutch for about 98% of the time. In September 2008, two young hatched and shared the nesting site for six weeks with the female, which attended the nesting site for 87% of the time. Hatchlings repeatedly climbed over the female's body, lying on her for hours. The female walked out of the nesting site with a young on its back twice. These prolonged skin contacts between parent and offspring should be considered as the first certain case of young attendance in salamanders. This behavior may be related to increased survival of hatchlings during their first weeks of life, when young are particularly vulnerable to predation, skin infection, and dehydration.
Chapter
Full-text available
Parental care is common throughout the animal kingdom and among caring species there is a bewildering variation in how parents care for offspring, as well as in the amount of resources parents invest in care. For instance, there is considerable variation in the relative parental investment by the sexes – in some species females invest more, in others males invest more, and in some investment is more or less equally shared. Different hypotheses have been proposed to explain patterns of parental investment between the sexes, as well as among species, and work is still ongoing to develop an overarching hypothesis that can explain the various patterns observed.
Article
Full-text available
Cloacae were examined from salamanders representing the three families in which fertilization of eggs is known or inferred to occur externally. The cloacae of male and female sirenids are aglandular and lack cilia. Sexual dimorphism in sirenid cloacae occurs only in the extent of epithelial stratification in the cloacal chamber in females (entire chamber) versus males (posterior angle of the vent). Both male and female Cryptobranchus alleganiensis possess ventral glands that secrete an acid mucopolysaccharide and have ciliated cloacal linings. The ventral glands are more numerous and hypertrophied in breeding male than female C. alleganiensis, but in males, ventral glands secrete only onto the surface of the cloacal lips along the anterior three-fifths of the cloacal orifice, whereas in females, the glands secrete onto the border of the entire cloacal orifice. Except for male Onychodactylus japonicus, male and female hynobiids also possess only ventral glands and have ciliated cloacal linings. Hynobiid ventral glands secrete a glycoprotein. Much variation occurs, however, among these hynobiids in cloacal conformation, extent of epidermis into the cloaca, and anatomy of the ventral gland. Male O. japonicus possess an unciliated cloaca in which three types of cloacal glands occur, each giving unique reactions to tests for carbohydrates and proteins. The glands in male O. japonicus do not seem to be homologous to those found in spermatophore producing salamanders in the Salamandroidea, but this does not negate the possibility that O. japonicus makes spermatophores. Examination of cloacal characters in additional species of hynobiids may be useful in resolving intrafamilial phylogenetic relationships.
Article
Full-text available
The safe harbor hypothesis includes the suggestion that parental care causes the embryonic stage to be the safest harbor, and, therefore, egg size will increase in populations with parental care to decrease the duration of subsequent, higher risk stages. Neither the safe habor hypothesis nor r and K theory seem adequate to explain the correlation between egg size and the presence/absence of parental care among salamanders, a group in which there is a further correlation between the larval (hatchling) habitat and egg size/parental care. Pond-breeding salamanders generally have small eggs and lack parental care, and stream-breeding salamanders generally have large eggs and parental care. I argue that the fundamental difference in the food available to hatchling salamanders between lentic (plankton-rich) and lotic (plankton-poor) environments selects for relatively lower parental investment in the lentic environment. From the standpoint of parental fitness, small (more numerous) hatchlings have a greater payoff where the available food is mall and dense (zooplankton in lentic environments), and large hatchlings are selectively advantageous where the food is of large size and less dense (benthic invertebrates in lotic environments). Selection for larger hatchlings in lotic environments results in longer embryonic periods and,ceteris paribus, greater total embryonic mortality. Embryo hiding and guarding have evolved among lotic-breeding salamanders as compensatory mechanisms to reduce the rate of embryonic mortality. In this view, parental care is a consequence of selection for larger egg size and not an umbrella that allows egg size to increase, contrary to the safe harbor hypothesis. The relationship between variance in parental investment and food available to offspring, developed here for salamanders, may be of general significance. YosiakiItô, a critic of r and K theory, independently arrived at a similar conclusion from a broader data base.
Article
Full-text available
Linking specific ecological factors to the evolution of parental care pattern and mating system is a difficult task of key importance. We provide evidence from comparative analyses that an ecological factor (breeding pool size) is associated with the evolution of parental care across all frogs. We further show that the most intensive form of parental care (trophic egg feeding) evolved in concert with the use of small pools for tadpole deposition and that egg feeding was associated with the evolution of biparental care. Previous research on two Peruvian poison frogs (Ranitomeya imitator and Ranitomeya variabilis) revealed similar life histories, with the exception of breeding pool size. This key ecological difference led to divergence in parental care patterns and mating systems. We present ecological field experiments that demonstrate that biparental care is essential to tadpole survival in small (but not large) pools. Field observations demonstrate social monogamy in R. imitator, the species that uses small pools. Molecular analyses demonstrate genetic monogamy in R. imitator, the first example of genetic monogamy in an amphibian. In total, this evidence constitutes the most complete documentation to date that a single ecological factor drove the evolution of biparental care and genetic and social monogamy in an animal.
Article
Full-text available
Although the initial growth and development of most multicellular animals depends on the provision of yolk, there are many varied contrivances by which animals provide additional or alternative investment in their offspring. Providing offspring with additional nutrition should be favoured by natural selection when the consequent increased fitness of the young offsets any corresponding reduction in fecundity. Alternative forms of nutrition may allow parents to delay and potentially redirect their investment. Here we report a remarkable form of parental care and mechanism of parent-offspring nutrient transfer in a caecilian amphibian. Boulengerula taitanus is a direct-developing, oviparous caecilian, the skin of which is transformed in brooding females to provide a rich supply of nutrients for the developing offspring. Young animals are equipped with a specialized dentition, which they use to peel and eat the outer layer of their mother's modified skin. This new form of parental care provides a plausible intermediate stage in the evolution of viviparity in caecilians. At independence, offspring of viviparous and of oviparous dermatotrophic caecilians are relatively large despite being provided with relatively little yolk. The specialized dentition of skin-feeding (dermatophagous) caecilians may constitute a preadaptation to the fetal feeding on the oviduct lining of viviparous caecilians.
Article
Full-text available
We sequenced 15 complete mitochondrial genomes and performed comprehensive molecular phylogenetic analyses to study the origin and phylogeny of the Hynobiidae, an ancient lineage of living salamanders. Our phylogenetic analyses show that the Hynobiidae is a clade with well resolved relationships, and our results contrast with a morphology-based phylogenetic hypothesis. These salamanders have low vagility and are limited in their distribution primarily by deserts, mountains, and oceans. Our analysis suggests that the relationships among living hynobiids have been shaped primarily by geography. We show that four-toed species assigned to Batrachuperus do not form a monophyletic group, and those that occur in Afghanistan and Iran are transferred to the resurrected Paradactylodon. Convergent morphological characters in different hynobiid lineages are likely produced by similar environmental selective pressures. Clock-independent molecular dating suggests that hynobiids originated in the Middle Cretaceous [≈110 million years ago (Mya)]. We propose an “out of North China” hypothesis for hynobiid origins and hypothesize an ancestral stream-adapted form. Given the particular distributional patterns and our molecular dating estimates, we hypothesize that: (i) the interior desertification from Mongolia to Western Asia began ≈50 Mya; (ii) the Tibetan plateau (at least on the eastern fringe) experienced rapid uplift ≈40 Mya and reached an altitude of at least 2,500 m; and (iii) the Ailao–Red River shear zone underwent the most intense orogenic movement ≈24 Mya. • mitochondrial DNA • phylogenetics • homoplasy • Tibetan Plateau
Article
Full-text available
Biologists and other scientists routinely need to know times of divergence between species and to construct phylogenies calibrated to time (timetrees). Published studies reporting time estimates from molecular data have been increasing rapidly, but the data have been largely inaccessible to the greater community of scientists because of their complexity. TimeTree brings these data together in a consistent format and uses a hierarchical structure, corresponding to the tree of life, to maximize their utility. Results are presented and summarized, allowing users to quickly determine the range and robustness of time estimates and the degree of consensus from the published literature. Availability: TimeTree is available at http://www.timetree.net Contact:sbh1{at}psu.edu
Article
Full-text available
The fossil record of modern amphibians (frogs, salamanders, and caecilians) provides no evidence for major extinction or radiation episodes throughout most of the Mesozoic and early Tertiary. However, long-term gradual diversification is difficult to reconcile with the sensitivity of present-day amphibian faunas to rapid ecological changes and the incidence of similar environmental perturbations in the past that have been associated with high turnover rates in other land vertebrates. To provide a comprehensive overview of the history of amphibian diversification, we constructed a phylogenetic timetree based on a multigene data set of 3.75 kb for 171 species. Our analyses reveal several episodes of accelerated amphibian diversification, which do not fit models of gradual lineage accumulation. Global turning points in the phylogenetic and ecological diversification occurred after the end-Permian mass extinction and in the late Cretaceous. Fluctuations in amphibian diversification show strong temporal correlation with turnover rates in amniotes and the rise of angiosperm-dominated forests. Approximately 86% of modern frog species and >81% of salamander species descended from only five ancestral lineages that produced major radiations in the late Cretaceous and early Tertiary. This proportionally late accumulation of extant lineage diversity contrasts with the long evolutionary history of amphibians but is in line with the Tertiary increase in fossil abundance toward the present.
Article
Full-text available
Maternal dermatophagy, the eating of maternal skin by offspring, is an unusual form of parental investment involving co-evolved specializations of both maternal skin and offspring dentition, which has been recently discovered in an African caecilian amphibian. Here we report the discovery of this form of parental care in a second, distantly related Neotropical species Siphonops annulatus, where it is characterized by the same syndrome of maternal and offspring specializations. The detailed similarities of skin feeding in different caecilian species provide strong evidence of its homology, implying its presence in the last common ancestor of these species. Biogeographic considerations, the separation of Africa and South American land masses and inferred timescales of amphibian diversification all suggest that skin feeding is an ancient form of parental care in caecilians, which has probably persisted in multiple lineages for more than 100 Myr. These inferences support the hypotheses that (i) maternal dermatophagy is widespread in oviparous direct-developing caecilians, and (ii) that viviparous caecilians that feed on the hypertrophied maternal oviduct evolved from skin-feeding ancestors. In addition to skin-feeding, young S. annulatus were observed to congregate around, and imbibe liquid exuded from, the maternal cloacal opening.
Article
Sexual dimorphism is common in vertebrates that exhibit male-male combat. The Eastern Hellbender, Cryptobranchus a alleganiensis, exhibits such combat and sexual dimorphism has been reported. The most easily discernable dimorphic character, swelling around the cloaca in males, is detectable only during and around the autumn breeding season. We used univariate and multivariate analyses to determine if other morphological characters could be used to determine the sex of adult hellbenders outside the breeding season. We analyzed six morphological features of 105 preserved specimens and found that males differed significantly from females in snout-vent length, thoracic girth, and mass. However, the differences detected were not sufficient to allow positive determination of sex of an individual. Although hellbenders exhibit sexual dimorphism in several morphological characters, the only reliable external morphological character is the presence of swelling around the cloaca of males during the autumn breeding season.
Article
This paper reviews published literature on amphibians to examine predicted correlations between male combat and sexual dimorphism. Females grow larger than males in most species (61% of urodeles, 90% of anurans), but males are often larger than females in species in which males engage in physical combat with each other. Although amphibian male combat has been reported only rarely (in 19% of urodeles and 5% of anurans), the association between male combat and male body size equal to or larger than female body size is highly significant within the urodele suborders Salamandroidea (n = 25 spp.) and Ambystomatoidea (n = 46), in the urodeles as a whole (n = 79), in the anuran Dendrobatidae (n = 34) and Ranidae (n = 149), and in the anurans as a whole (n = 589). Similarly, large male size and the occurrence of male combat are highly correlated in a comparison between several anuran families. Spines and tusks of male anurans appear to be adaptations to male combat. Combat, large male size and sexually dimorphic weapons appear to be most common in species that are relatively invulnerable to predation while fighting, by virtue of large body size or toxic skin secretions.
Article
Male and female Hynobius nigrescens show pronounced changes in body shape associated with aquatic reproduction. Soon after entering the breeding pond there is a large increase in body mass, head width, and tail height in males, caused by changes in connective tissue under the skin and by storage of seminal fluid in the vasa deferentia. These features decline gradually in postbreeding males prior to leaving the pond. Females show little seasonal variation in head width or tail height, but exhibit a large increase in body mass after ovulation. This is the result of absorption of water during the formation of egg sacs.
Article
Male giant bullfrogs Pyxicephalus adspersus exhibit paternal care through construction of channels that guide tadpoles to larger bodies of water. We found the following. These channels (which may exceed 15 m in length) make available cooler water to broods in the rapidly drying breeding puddles that frequently reach critically high temperatures. Eggs of P. adspersus exposed to temperatures above 38°C died, a temperature reached in a third of the puddles measured. In contrast, tadpoles readily survived temperatures above 38°C, and experiments showed that tadpoles can survive the highest temperatures recorded at the puddles. Males actively defended their offspring against predators and were sometimes killed while performing this behavior. Survival of eggs and larvae in territorial broods was roughly twice that of broods in nonterritorial breeding arenas. The large cost of paternal care in the giant bullfrog is therefore offset by strong fitness gains. We suggest that channel construction and predator defence, crucial for tadpole survival, can be performed most efficiently by large-bodied parents, explaining why males (not the smaller females) perform parental care.
Article
There are three different basic courtship patterns found in the Salamandridae. In Euproctus the male captures the female with his tail and the spermatophores are deposited on her body, near or in the cloacal lips. In the salamandrines, and also in Pleurodeles and Tylototriton, courtship is based on capturing the female from below. The spermatophore is deposited while still gripping the female, and she is maneuvered to it by the male. In the other newts courtship is based on capturing the female from above, and the sexes must disengage for spermatophore deposition. This pattern involves the induction of quiescent or "obedient" states in the females, and they must be induced to pass over the spermatophore. A courtship pattern essentially like the latter is found also in Ambystoma and in the plethodontoids. Courtship behavior in these groups probably evolved in parallel. The courtships of Euproctus and the salamandrids that capture the female from below are probably related to mating in running water, and on this basis it is hypothesized that they have had a montane history. The pattern where the male captures the female from above is certainly related to mating in still waters, and it is visualized that salamanders possessing this type of capture spread into the waters of lowland regions. Plethodontoid courtship shows modification probably relating to mating on land, and it is hypothesized that these animals represent a reinvasion of upland regions. The spermatophore may originally have been an adaptation to mating in running water, and on this basis the ancestral salamanders are visualized as having lived in montane regions. It is suggested that courtship behavior should be used in salamander systematics, and on this basis, taxonomic problems are raised concerning the Salamandridae and also the genus Ambystoma.
Article
In both fishes and amphibians, paternal care correlates with external fertilization and maternal care with internal fertilization. Three different hypotheses have been proposed to explain these relationships: (1) "gamete-order" (Dawkins and Carlisle, 1976; Ridley, 1978); (2) "reliability of paternity" (Trivers, 1972; Ridley, 1978); and (3) "parent-offspring association" (Williams, 1975). We have attempted to test these hypotheses by drawing specific predictions and using detailed data on teleost and amphibian parental care. We reject the gamete-order hypothesis because male care remains correlated with external fertilization independent of the physical ability of females and males to first desert the zygotes. Although the reliability of paternity hypothesis predicts the correlation between male care and external fertilization, the hypothesis is not supported by the distribution of female care. Two further objections are that the assumption of differences in paternity reliability with mode of fertilization is questionable, and that theoretical models cast doubt on the generality of the basic hypothesis (Maynard Smith, 1978; Werren et al., 1980). Overall, the association hypothesis is most consistent with the available data. This hypothesis successfully predicts patterns of both male and female parental care, and offers possible explanations for differences in the incidence of male versus female parental care in different vertebrate groups. We interpret the prevalence of male parental care with external fertilization as resulting from male territoriality, which in turn results from female discrimination of oviposition sites. Internal fertilization preadapts females to selection for embryo retention, leading to live-bearing.
Article
Two spent female Siren intermedia were found attending eggs in early February in a S Florida water hyacinth community. Embryos from both nests tended to hatch synchronously, averaged 11.5 mm in total length and showed more advanced development than those reported from Arkansas. The two attendant females had several distinct epidermal marks, which closely matched the cornified beaks and vomerine teeth of conspecifics, and possibly were made by courting males. Examinations of 487 additional S. intermedia collected from this site indicated that bite-marks were restricted to breeding females. The larger body size and enlarged masseter muscles of male S. intermedia probably are related to social interaction and sexual activity.
Article
While recently studying the development of Siren with material received from Florida and Arkansas we have found that there are two forms confused under the name Siren lacertina Linn& These forms differ from one another in the size of the egg-capsules, the coloration of the young, the size at sexual maturity, and the average number of costal grooves. Since the two species occur together throughout most of their ranges we consider that they represent distinct species and not races. The case is comparable to that exhibited by certain southern species of Desmognathus, but differs in that the adults of the small species are much more difficult to distinguish from the immatures of the large one. The evidence for the validity of the small species will, therefore, be consid-ered in detail. First the question arises as to what name to apply to the small species. In 1826 LeConte described Siren intermedia, distinguishing it from S. lacertina only by its smaller size and reduced gills. It is now known that the latter character is of no value, since S. lacertina immersed in irritating fluids undergoes the same regression of the gills (Noble, 1924). LeConte made use of none of the diagnostic characters of our small species in defining S. intermedia. He did state that the greatest length of his species was twelve inches but added that he had not seen an "oviferous femnale." Since LeConte did not designate a type speci-men, it is impossible to determine whether he was describing the adults of the small species of Siren which we are defining or whether his descrip-tion was based solely on the young of the large species. Linnaeus appar-ently gave the name lacertina to the large species, for in an early descrip-tion (1767) he states that the species measures a foot and a half in length. Moreover, Ellis (1766), who supplied Linnaeus with his specimens, has figured a Siren that agrees with the large species in size. We have not been able to locate any of the material that LeConte had before him when he drew up his description of intermedia. Even if a specimen should be found and its specific status determined, this will not exclude the possibility that LeConte had other material at hand, possibly the AMERICAN MUSEUM NOVITATES , .." other species as well, when the description was written. Under these circumstances it seems most advisable for us to define the two species of Siren and to restrict LeConte's name intermedia -to our small species.
Article
The Lesser Siren (Siren intermedia) is a fully aquatic salamander with functionally limited overland dispersal. Details of the ecology of this species throughout its geographic range and diversity of habitats are limited. In this study, I investigated the ecology of a presumably isolated population of S. intermedia in eastern Texas. The conservative estimated population density was 0.33 sirens/m2 with a standing crop biomass of 9.66 g/m2. Growth rates averaged 0.022 mm/day in total length, slightly slower than other populations. Growth rate was not significantly different between males and females, nor was it correlated with size. The diet of the study population included at least 10 different taxa, of which tadpoles and snails (Order Basommatophora) were the most important prey. Like other populations, activity was highest during late winter and early spring, which coincides with the breeding season. The abundance of siren captures was weakly influenced by water temperature but not correlated with precipitation. Bite marks are hypothesized to be a result of siren courtship behavior. The abundance of males and females captured with fresh bite marks was significantly correlated with the number of gravid females. Because sirens are predatory generalists and represent a significant proportion of biomass in many aquatic environments, it is important to understand siren ecology throughout its geographic range and broad use of habitat types.
Article
Reproduction was studied in a South Carolina population of the paedomorphic salamander Siren intermedia with emphasis on anatomy of the female oviduct. The oviduct forms 67–79% of the snout-vent length in this elongate species and can be divided into three portions. The atrium, 7–13% of oviducal length, is the narrow anteriormost portion, with the ostial opening immediately caudad of the transverse septum. The ampulla, 63–75% of oviducal length, is the highly convoluted, middle portion in which gelatinous coverings are added to the eggs during their passage. Hypertrophy of the oviducal glands in the ampulla causes the ampulla to increase in diameter during the ovipository season. The secretion of the eosinophilic oviducal glands is intensely positive following staining with the periodic acid-Schiff procedure and does not react with alcian blue at pH 2.5. This staining reaction, coupled with the presence of abundant rough endoplasmic reticulum and Golgi complexes, indicates that the secretion contains a glycoprotein. The ovisac, 16–25% of oviducal length, is the most posterior portion of the oviduct and holds up to 10–11 eggs prior to oviposition. Oviducal glands similar to those in the ampulla are absent in the ovisac. Oviposition in female sirens occurs during February-April in this population, and male spermiation is concurrent. Entire oviducts were sectioned from three females collected during the ovipository season and from two collected prior to the breeding season, and sperm were not found in the oviducts of these specimens. Thus no evidence was found for internal fertilization or sperm storage in the oviducts of sirens. © 1996 Wiley-Liss, Inc.
Article
This review presents a systematic compilation of species in which only the male cares for the offspring. Such species occur rarely in the polychaetes, Hemiptera, Amphibia and birds and more often in the pycnogonids and fish. The facts are interpreted in the light of sexual selection theories. Care by only the male is more likely to occur if fertilization is external and might often be selected for as a consequence of site-attached behaviour by males. An explanation is suggested for the evolution of total role-reversal: it might result from the breakdown of a state of secondary equality of parental investment by the two sexes.
Article
The extant amphibians are one of the most diverse radiations of terrestrial vertebrates (>6800 species). Despite much recent focus on their conservation, diversification, and systematics, no previous phylogeny for the group has contained more than 522 species. However, numerous studies with limited taxon sampling have generated large amounts of partially overlapping sequence data for many species. Here, we combine these data and produce a novel estimate of extant amphibian phylogeny, containing 2871 species (∼40% of the known extant species) from 432 genera (∼85% of the ∼500 currently recognized extant genera). Each sampled species contains up to 12,712 bp from 12 genes (three mitochondrial, nine nuclear), with an average of 2563 bp per species. This data set provides strong support for many groups recognized in previous studies, but it also suggests non-monophyly for several currently recognized families, particularly in hyloid frogs (e.g., Ceratophryidae, Cycloramphidae, Leptodactylidae, Strabomantidae). To correct these and other problems, we provide a revised classification of extant amphibians for taxa traditionally delimited at the family and subfamily levels. This new taxonomy includes several families not recognized in current classifications (e.g., Alsodidae, Batrachylidae, Rhinodermatidae, Odontophrynidae, Telmatobiidae), but which are strongly supported and important for avoiding non-monophyly of current families. Finally, this study provides further evidence that the supermatrix approach provides an effective strategy for inferring large-scale phylogenies using the combined results of previous studies, despite many taxa having extensive missing data.
Article
Consisting of more than six thousand species, amphibians are more diverse than mammals and are found on every continent save Antarctica. Despite the abundance and diversity of these animals, many aspects of the biology of amphibians remain unstudied or misunderstood. The Ecology and Behavior of Amphibians aims to fill this gap in the literature on this remarkable taxon. It is a celebration of the diversity of amphibian life and the ecological and behavioral adaptations that have made it a successful component of terrestrial and aquatic ecosystems. Synthesizing seventy years of research on amphibian biology, Kentwood D. Wells addresses all major areas of inquiry, including phylogeny, classification, and morphology; aspects of physiological ecology such as water and temperature relations, respiration, metabolism, and energetics; movements and orientation; communication and social behavior; reproduction and parental care; ecology and behavior of amphibian larvae and ecological aspects of metamorphosis; ecological impact of predation on amphibian populations and antipredator defenses; and aspects of amphibian community ecology. With an eye towards modern concerns, The Ecology and Behavior of Amphibians concludes with a chapter devoted to amphibian conservation. An unprecedented scholarly contribution to amphibian biology, this book is eagerly anticipated among specialists.
Article
In this paper we propose an explanation for (a) the predominance of male care in fishes, and (b) the phylogenies and transitions that occur among care states. We also provide a general evolutionary model for studying the conditions under which parental care evolves. Our conclusions are as follows: (i) Parental care has only one benefit, the increased survivorship of young. It may, however, have three costs: a “mating cost,” an “adult survivorship cost,” and a “future fertility cost.” (ii) On average, males and females will derive the same benefit from care. They probably also pay the same adult survivorship cost. However, their mating cost and future fertility costs may differ, (iii) A mating cost usually applies only to males. However, this cost may be reduced by male territoriality and, in some situations, be entirely removed. Under this condition, natural selection on present reproductive success is equivalent for males and females, (iv) When fecundity accelerates with body size in females, while male mating success follows a linear relationship with body size, future fertility costs of parental care are greater for females than males. Although further tests are needed, a preliminary analysis suggests this often may be the case in fishes. Thus, the predominance of male parental care in fishes is not explained by males deriving greater benefits from care, but by males paying smaller future costs. Males thus accrue a greater net fitness advantage from parental care (see expressions [6] and [12]). (v) The evolution of biparental care from uniparental male care may occur because male care selects for larger egg sizes and increased embryo investment by females. This increases the benefit to the female of parental care, (vi) By contrast, uniparental female care may originate from biparental care when males are selected to desert. This occurs when female care creates a mating cost to males. In some cases male desertion may “lock” females into uniparental care. However, in many other cases females may be selected to desert, giving rise to “no care.” (vii) The origin of uniparental female care from no care is rare in externally fertilizing fishes. This is because the benefits of care rarely outweigh a female's future fertility costs (expression [9]). For internally fertilizing species, however, the benefit of care is high whereas the cost is probably low. Most of these species have evolved embryo retention, (viii) When parental care begins with male care and moves to biparental care, our analysis suggests that care evolution will include cyclical dynamics. Parental care in some fishes may thus be seen as transitional and changing through evolutionary time rather than as an evolutionarily stable state. In theory, “no care” may be a phylogenetically advanced state.
Nests and eggs of the pacific giant salamander, Dicamptodon ensatus (Eschscholtz)
  • R A Nussbaum
Nussbaum, R.A., 1969. Nests and eggs of the pacific giant salamander, Dicamptodon ensatus (Eschscholtz). Herpetologica 25, 257–262.
Effects of a hurricane on the fish fauna of a coastal pool and drainage ditch
  • C Hubbs
Hubbs, C., 1962. Effects of a hurricane on the fish fauna of a coastal pool and drainage ditch. The Texas Journal of Science 14, 289–296.
The salamander Siren intermedia intermedia LeConte in North Carolina
  • B B Collette
  • F R Gehlbach
Collette, B.B., Gehlbach, F.R., 1961. The salamander Siren intermedia intermedia LeConte in North Carolina. Herpetologica 17, 203–204.
Salamanders of the Old World: An Online Catalogue Accessible at http://science.naturalis.nl/salamanders A Natural History of Amphibians
  • M Sparreboom
Sparreboom, M., 2012. Salamanders of the Old World: An Online Catalogue, Accessible at http://science.naturalis.nl/salamanders Stebbins, R.C., Cohen, N.W., 1997. A Natural History of Amphibians. Princeton University Press, Princeton, NJ.
An arrangement of the genera of batracian animals, with a description of the more remarkable species; including a monograph of the doubtful reptiles
  • D H Barnes
Barnes, D.H., 1826. An arrangement of the genera of batracian animals, with a description of the more remarkable species; including a monograph of the doubtful reptiles. American Journal of Science and Arts 11, 268–297.
Observations on the life history of Siren lacertina
  • G R Ultsch
Ultsch, G.R., 1973. Observations on the life history of Siren lacertina. Herpetologica 29, 304–305.
Food habits of the Texas dwarf siren
  • J B Scroggins
  • W B Davis
Scroggins, J.B., Davis, W.B., 1956. Food habits of the Texas dwarf siren. Herpetologica 12, 231–237.
Husbandry and breeding of the narrow-striped dwarf siren (Pseudobranchus axanthus)
  • E Kowalski
Kowalski, E., 2004. Husbandry and breeding of the narrow-striped dwarf siren (Pseudobranchus axanthus). Caudata.org Magazine 1, 40–43.
Newts and Salamanders. Everything about selection, care, nutrition, diseases, breeding, and behavior. In: Barron's Educational Series
  • F Indiviglio
Indiviglio, F., 2010. Newts and Salamanders. Everything about selection, care, nutrition, diseases, breeding, and behavior. In: Barron's Educational Series. Hauppauge, NY.
Description of a new species of Siren, with some observations on animals of a similar nature
  • J E Leconte
LeConte, J.E., 1824. Description of a new species of Siren, with some observations on animals of a similar nature. Annals of the Lyceum of Natural History of New-York 1, 52–58.
  • C J Goin
  • O B Goin
Goin, C.J., Goin, O.B., 1962. Introduction to Herpetology. W.H. Freeman, San Francisco.
  • W E Duellman
  • L Trueb
Duellman, W.E., Trueb, L., 1994. Biology of Amphibians. Johns Hopkins University Press, Baltimore.