Article

Unique courtship and spawning behaviour in wrinkled frog, Nyctibatrachus humayuni

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Abstract

Frogs of the genus Nyctibatrachus (family Nyctibatrachidae) exhibit a unique reproductive behaviour. They may completely lack or have an abbreviated amplexus, deposit terrestrial eggs and even offer paternal care. We studied the courtship and spawning behaviour of Nyctibatrachus humayuni from Matheran located in the northern region of the Western Ghats of India. The breeding season of N. humayuni coincides with the onset of south-west monsoon. Adult males vocalise from their calling sites on wet rocks/dead logs that often harbour egg clutches and females approach the calling males, resulting in a loose cephalic amplexus that lasts up to 10 minutes. The male dismounts and sits aside; then the female deposits the eggs and moves away from the spawning site or into the water. The mean clutch size and the egg diameter are found to be 30.3 ± 1.89 and 2.44 ± 0.04 mm, respectively. Once the female moves away following spawning, the male slowly moves on to the eggs and fertilises them. The males of N. humayuni appear to be territorial and offer parental care by attending the eggs only during night. Paternal egg attendance most probably reduces the risk of predation by nocturnal predators.

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... Nyctibatrachidae), is one of the 35 species of night frogs described from India (Garg, Suyesh, Sukesan, & Biju, 2017). The frog is endemic to montane and submontane streams of the Western Ghats and exhibits unique courtship and breeding behaviour (Gramapurohit, Gosavi, & Phuge, 2011;Willaert et al., 2016). The species is sexually dimorphic with females being larger than males. ...
... Interestingly, males offer parental care by attending the eggs at night (Gramapurohit et al., 2011). Eggs deposited in the terrestrial environment hatch into the streams as tadpoles and complete their larval development in the aquatic ecosystem (Gramapurohit et al., 2011). ...
... Interestingly, males offer parental care by attending the eggs at night (Gramapurohit et al., 2011). Eggs deposited in the terrestrial environment hatch into the streams as tadpoles and complete their larval development in the aquatic ecosystem (Gramapurohit et al., 2011). Previously, we have shown that androgens are important for the expression of calling behaviour of N. humayuni as calling males have higher androgens than non-callers (Joshi et al., 2017). ...
Article
In anurans, vocalisation is used to communicate within and between the sexes during reproduction. Knowledge of vocal repertoire and its diversity is essential in understanding its significance in sexual selection. In this context, we studied the vocal behaviour of Nyctibatrachus humayuni and quantified the urinary metabolites of androgens and corticosterone to understand the associations among hormones, body condition index and vocalisation. Our results show that males of N. humayuni produce an amplitude‐modulated call consisting of a train of pulses. Interestingly, a high degree of inter‐individual variation was observed in the call parameters. The dominant frequency and pulse interval were negatively correlated with male body size, whereas pulse duration and pulse duty cycle were positively correlated with it. Dominant frequency was negatively correlated with androgens and corticosterone, whereas pulse interval was negatively correlated with corticosterone. Further, pulse duty cycle, pulse duration and pulses per call were positively associated with corticosterone. Surprisingly, none of the acoustic parameters was associated with male body temperature and body condition. A significant variation was evident in the vocal effort, dominant frequency and amplitude of advertisement calls produced under different social situations. Calls produced during territory establishment had lower dominant frequency but higher vocal effort, whereas those produced during courtship had higher amplitude and vocal effort than the calls produced in the absence of a competitor/female. Our results suggest that greater inter‐male variability in the advertisement call of N. humayuni could be important in female choice as it may help females to assess the quality of a male. Further, androgens and corticosterone could be important in modulating crucial parameters of the advertisement call.
... Furthermore, male advertisement calls have only been described in four species (Kuramoto & Joshy, 2001; Gururaja et al., 2014). Despite their poorly understood ecology, several studies suggest the presence of interesting forms of reproductive behaviour (Kunte, 2004; Biju et al., 2011; Gramapurohit, Gosavi & Phuge, 2011; Gururaja et al., 2014). In all Nyctibatrachus species, egg clutches are deposited on rocks or vegetation overhanging water, and tadpoles fall in the water after hatching, where they continue their development and metamorphosis (Biju et al., 2011; Gururaja et al., 2014). ...
... Afterwards, males of N. kumbara cover the deposited eggs with a layer of mud, a behaviour previously unknown for anurans. In N. aliciae Inger et al., 1984, N. humayuni Bhaduri & Kripalani, 1955, N. jog Biju et al., 2011 and N. minor Inger et al., 1984 a short, loose physical contact between the male and female takes place as the male sits on the dorsum of the female but does not clasp her as in a normal axillary amplexus (Biju et al., 2011; Gramapurohit, Gosavi & Phuge, 2011). In other species, such as N. petraeus Das & Kunte, 2005, amplexus behaviour may be completely absent, with the female depositing the eggs prior to the male fertilizing them (Kunte, 2004; Das & Kunte, 2005). ...
... Movies were analysed with iMovie 8.0.6 (Apple Inc.) to determine the duration of different steps of reproduction. In order to test the assumption that fertilization happens after the female has left the oviposition site (Gramapurohit, Gosavi & Phuge, 2011), Ziploc Ò bags were placed around egg clutches directly after deposition on five occasions to hinder male contact with the eggs. To determine the duration of embryo development, deposited and fertilised clutches were monitored every evening until hatching occurred. ...
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Article
Anurans show the highest diversity in reproductive modes of all vertebrate taxa, with a variety of associated breeding behaviours. One striking feature of anuran reproduction is amplexus. During this process, in which the male clasps the female, both individuals’ cloacae are juxtaposed to ensure successful external fertilization. Several types of amplexus have evolved with the diversification of anurans, and secondary loss of amplexus has been reported in a few distantly related taxa. Within Nyctibatrachus, a genus endemic to the Western Ghats of India, normal axillary amplexus, a complete loss of amplexus, and intermediate forms of amplexus have all been suggested to occur, but many species remain unstudied. Here, we describe the reproductive behaviour of N. humayuni, including a new type of amplexus. The dorsal straddle, here defined as a loose form of contact in which the male sits on the dorsum of the female prior to oviposition but without clasping her, is previously unreported for anurans. When compared to known amplexus types, it most closely resembles the form of amplexus observed in Mantellinae. Furthermore, we prove that, opposed to the situation in most anurans, male semen release happens before egg deposition. We hypothesize that the male ejaculates on the female’s dorsum and that sperm subsequently runs from her back and hind legs before fertilizing the eggs. A second feature characterizing anuran breeding is the advertisement call, mostly produced solely by males. Despite recent descriptions of several new Nyctibatrachus species, few studies have explored their vocal repertoire. We describe both the male advertisement call and a female call for N. humayuni. The presence of a female call has not been reported within Nyctibatrachidae, and has been reported in less than 0.5% of anuran species. Altogether, our results highlight a striking diversity and several unique aspects of Nyctibatrachus breeding behaviour.
... Despite their poorly understood ecology, several studies suggest the presence of interesting forms of reproductive behaviour (Kunte, 2004;Biju et al., 2011;Gramapurohit, Gosavi & Phuge, 2011;Gururaja et al., 2014). In all Nyctibatrachus species, egg clutches are deposited on rocks or vegetation overhanging water, and tadpoles fall in the water after hatching, where they continue their development and metamorphosis (Biju et al., 2011;Gururaja et al., 2014). ...
... Afterwards, males of N. kumbara cover the deposited eggs with a layer of mud, a behaviour previously unknown for anurans. In N. aliciae Inger et al., 1984, N. humayuni Bhaduri & Kripalani, 1955, N. jog Biju et al., 2011and N. minor Inger et al., 1984 a short, loose physical contact between the male and female takes place as the male sits on the dorsum of the female but does not clasp her as in a normal axillary amplexus (Biju et al., 2011;Gramapurohit, Gosavi & Phuge, 2011). In other species, such as N. petraeus Das & Kunte, 2005, amplexus behaviour may be completely absent, with the female depositing the eggs prior to the male fertilizing them (Kunte, 2004;Das & Kunte, 2005). ...
... Movies were analysed with iMovie 8.0.6 (Apple Inc.) to determine the duration of different steps of reproduction. In order to test the assumption that fertilization happens after the female has left the oviposition site (Gramapurohit, Gosavi & Phuge, 2011), Ziploc Ò bags were placed around egg clutches directly after deposition on five occasions to hinder male contact with the eggs. To determine the duration of embryo development, deposited and fertilised clutches were monitored every evening until hatching occurred. ...
Full-text available
Article
Anurans show the highest diversity in reproductive modes of all vertebrate taxa, with a variety of associated breeding behaviours. One striking feature of anuran reproduction is amplexus. During this process, in which the male clasps the female, both individuals’ cloacae are juxtaposed to ensure successful external fertilization. Several types of amplexus have evolved with the diversification of anurans, and secondary loss of amplexus has been reported in a few distantly related taxa. Within Nyctibatrachus , a genus endemic to the Western Ghats of India, normal axillary amplexus, a complete loss of amplexus, and intermediate forms of amplexus have all been suggested to occur, but many species remain unstudied. Here, we describe the reproductive behaviour of N. humayuni , including a new type of amplexus. The dorsal straddle, here defined as a loose form of contact in which the male sits on the dorsum of the female prior to oviposition but without clasping her, is previously unreported for anurans. When compared to known amplexus types, it most closely resembles the form of amplexus observed in Mantellinae. Furthermore, we prove that, opposed to the situation in most anurans, male semen release happens before egg deposition. We hypothesize that the male ejaculates on the female’s dorsum and that sperm subsequently runs from her back and hind legs before fertilizing the eggs. A second feature characterizing anuran breeding is the advertisement call, mostly produced solely by males. Despite recent descriptions of several new Nyctibatrachus species, few studies have explored their vocal repertoire. We describe both the male advertisement call and a female call for N. humayuni . The presence of a female call has not been reported within Nyctibatrachidae, and has been reported in less than 0.5% of anuran species. Altogether, our results highlight a striking diversity and several unique aspects of Nyctibatrachus breeding behaviour.
... Despite their poorly understood ecology, several studies suggest the presence of interesting forms of reproductive behaviour (Kunte, 2004;Biju et al., 2011;Gramapurohit, Gosavi & Phuge, 2011;Gururaja et al., 2014). In all Nyctibatrachus species, egg clutches are deposited on rocks or vegetation overhanging water, and tadpoles fall in the water after hatching, where they continue their development and metamorphosis (Biju et al., 2011;Gururaja et al., 2014). ...
... Afterwards, males of N. kumbara cover the deposited eggs with a layer of mud, a behaviour previously unknown for anurans. In N. aliciae Inger et al., 1984, N. humayuni Bhaduri & Kripalani, 1955, N. jog Biju et al., 2011and N. minor Inger et al., 1984 a short, loose physical contact between the male and female takes place as the male sits on the dorsum of the female but does not clasp her as in a normal axillary amplexus (Biju et al., 2011;Gramapurohit, Gosavi & Phuge, 2011). In other species, such as N. petraeus Das & Kunte, 2005, amplexus behaviour may be completely absent, with the female depositing the eggs prior to the male fertilizing them (Kunte, 2004;Das & Kunte, 2005). ...
... Movies were analysed with iMovie 8.0.6 (Apple Inc.) to determine the duration of different steps of reproduction. In order to test the assumption that fertilization happens after the female has left the oviposition site (Gramapurohit, Gosavi & Phuge, 2011), Ziploc Ò bags were placed around egg clutches directly after deposition on five occasions to hinder male contact with the eggs. To determine the duration of embryo development, deposited and fertilised clutches were monitored every evening until hatching occurred. ...
... Frogs belonging to the genus Nyctibatrachus (family: Nyctibatrachidae) inhabit subtropical/tropical moist montane forests in the Western Ghats of peninsular India. All 35 species described so far from the genus are endemic to the Western Ghats (Biju et al., 2011;Gururaja et al., 2014;Garg et al., 2017) and exhibit unique courtship and spawning behaviors (Kunte, 2004;Das and Kunte, 2005;Gramapurohit et al., 2011;Willaert et al., 2016). For example, amplexus is completely absent in Nyctibatrachus petraeus in which males fertilize eggs after spawning (Kunte, 2004). ...
... Further, males of N. kumbara offer parental care by covering the eggs with mud (Gururaja et al., 2014). In N. humayuni, a brief courtship between male and female results in an 'abbreviated amplexus' followed by spawning in the absence of amplexus, and males offer parental care by attending the eggs at night (Gramapurohit et al., 2011). Similarly, duration of hatching also varies among the species of Nyctibatrachus. ...
Article
Night frogs of the genus Nyctibatrachus are endemic to the Western Ghats of southern India, and these frogs exhibit unique courtship and spawning behavior. Herein, we studied the breeding biology of Nyctibatrachus humayuni and describe its tadpole. Our results show that N. humayuni is a terrestrial breeder that reproduces during the southwestern monsoon. Adults of N. humayuni are sexually dimorphic: females are larger, and males have femoral glands on the ventral surface of their thighs. The operational sex ratio is highly skewed in favor of males during the breeding season, while it is close to 1:1 during the rest of the year. Males choose suitable spawning sites, establish territories, and initiate calling, whereas females approach the vocalizing males and, following a brief courtship, deposit eggs at the sites chosen by males. Males produce amplitude-modulated advertisement calls consisting of single or multiple notes depending on the social situation. Unlike most frogs, females of N. humayuni do not spawn while in amplexus. Instead, spawning occurs after separation of the pair following a brief ‘abbreviated amplexus.’ Eggs are deposited on the moist rocks, boulders, and muddy surfaces in the middle and along the sides of montane streams. Clutch size is larger during the early breeding season, while it decreases with the season’s progression. Interestingly, egg size is comparable among the breeding season phases, suggesting the absence of a trade-off between egg size and clutch size. Tadpoles are moderately oval and dorsoventrally flattened with a blunt snout. The mouth is ventral; the oral disc consists of upper and lower labia and jaw sheaths. Teeth are completely absent; the jaw sheaths are keratinized and serrated. The upper and lower labia are surrounded by a single row of marginal papillae and 2–3 rows of sub-marginal papillae.
... The Bombay night frog, Nyctibatrachus humayuni (Family: Nyctibatrachidae) is endemic to montane and sub-montane streams of the Western Ghats of peninsular India, and exhibits unique courtship and breeding behaviour (Gramapurohit et al., 2011;Willaert et al., 2016). The species exhibits sexual size dimorphism with females being larger than males. ...
... Subsequently, males return to the spawning site and sit on the eggs (we believe fertilisation to occur at this moment). Interestingly, males offer parental care by attending the eggs at night (Gramapurohit et al., 2011). Information on breeding biology including the factors affecting their reproductive health is very scarce. ...
Article
Glucocorticoids (GCs) are primarily involved in mobilising energy reserves to various physiological processes including reproduction. During situations of stress, GCs also help in coping with stress by diverting energy away from processes such as growth and reproduction. Hence, studying annual and seasonal changes in GCs of wild populations can help in understanding their role in stress management and reproduction. The quantification of GCs in wild animals involves capturing, handling and restraining, which could be stressful. Moreover, different species may exhibit differential sensitivity to different stressors. Hence, determining species-specific sensitivities and responses to different stressors may help in developing effective conservation measures. In this context, we studied the annual and seasonal variations in corticosterone metabolites of the Bombay night frog, Nyctibatrachus humayuni. In addition, the effects of handling, marking and short-term captivity (24 h) on corticosterone metabolite levels of N. humayuni were determined. Our results show that urinary corticosterone metabolites (UCM) varied significantly annually and between the sexes; in males, the levels were highest during the breeding season, whilst in females, the levels were highest just before the breeding season. Interestingly, UCM levels of both the sexes were not affected by tagging with visual implant elastomer (VIE), and by short-term captivity, suggesting that these manipulations were not stressful in terms of corticosterone responses.
... The Bombay night frog, Nyctibatrachus humayuni is endemic to the Western Ghats of peninsular India and exhibits many unique features in its reproductive behaviour (Gramapurohit et al., 2011;Willaert et al., 2016). Males are non-chorusing but territorial and exhibit resource defense polygyny. ...
... Subsequently, females deposit eggs on the rocks and boulders situated in the middle and along the sides of streams. Surprisingly, spawning and fertilisation occur in the absence of physical contact between the sexes (Gramapurohit et al., 2011;Willaert et al., 2016). Further, males offer parental care by attending eggs until they hatch as tadpoles into the stream and complete their larval development in the aquatic ecosystem. ...
Article
Synergism between extrinsic and intrinsic factors is crucial for the seasonality of reproduction. Environmental factors such as photoperiod and temperature activate the hypothalamus-pituitary-gonadal axis leading to the secretion of steroid hormones that are crucial for reproduction. Sex steroids are not only essential for the maturation of gonads, but also for development of secondary sexual characters in males and reproductive behaviour of both the sexes. In the present study, we quantified the urinary testosterone (UTM) and corticosterone (UCM) metabolites in males and urinary estradiol metabolites (UEM) and UCM in females of Nyctibatrachus humayuni for two consecutive years to determine annual and seasonal variation in the levels of sex steroids, corticosterone and body condition index (BCI). The results show that sex steroids were highest during the breeding season and lowest during the non-breeding season in both the sexes. An increase in UTM and UEM was observed in males and females respectively during the breeding season. Testicular histology showed the presence of all stages of spermatogenesis throughout the year indicating that spermatogenesis is potentially continuous. Ovarian histology showed the presence of vitellogenic follicles only during the breeding season indicating that oogenesis is strictly seasonal. In males, UCM levels were highest during the breeding season, while in females their levels were highest just prior to the breeding season. In males, BCI was highest during the pre-breeding season, declined during the breeding season to increase again during the post-breeding season. In females, BCI was comparable throughout the year. In males, UTM levels were positively correlated with UCM levels but negatively correlated with BCI. Interestingly, UEM, UCM and BCI were not correlated in females. These results indicate that N. humayuni exhibits an associated pattern of reproduction. Quantification of urinary progesterone metabolites (UPM) during the breeding season showed UPM levels were higher in post-spawning females, suggesting the significance of progesterone in ovulation. Further, non-invasive enzyme immunoassay has been successfully standardized in N. humayuni for the quantification of urinary metabolites of steroid hormones.
... They also display some sort of parental care; in many species it is obligatory 3,16 . Parents often care for the eggs by avoiding desiccation or protect them from predators by attending to them 3,17 . Indirana sp. ...
... Inguinal amplexus in Indirana validates that this was the predominant means of reproduction in ancient frogs. It is believed that this type of amplexus would be inefficient in fertilization 3 , this was corroborated in this species as only 87% of the eggs were successfully fertilized, whereas like most anurans, even members of the genus Nyctibatrachus such as N. humayuni and N. petraeus that have a pseudo amplexus achieved 100% fertilization 15,17 . ...
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The Western Ghats biodiversity hotspot is rich in her- petofauna and harbours numerous endemic species. Unfortunately, many of these understudied species are threatened due to habitat loss, pollution, infectious diseases and climate change. Indirana (family Ranix- alidae) is an ancient frog genus, endemic to the West- ern Ghats of India. Unlike most amphibians, it lays terrestrial eggs and has semi-terrestrial tadpoles. We barely have any knowledge about their development, life history, mating systems and reproductive ecology. Such information is crucial to design and implement successful conservation programmes. Hence, we studied the courtship, spawning behaviour and reproduc- tive mode of an Indirana sp. from Amboli Reserve Forest located in the northern Western Ghats, Maha- rashtra, India. This species showcases a primitive type of inguinal amplexus and exhibits pronounced sexual size dimorphism, where females are significantly lar- ger than the males. Average clutch size was 226  41.5 eggs, with an egg diameter of 3.25  0.32 mm. Fertili- zation rate was 87% with 100% hatching success. Ad- ditionally, this frog has evolved terrestrial eggs without the dependent traits like parental care and large egg size/small clutch size witnessed in other ter- restrially egg-laying anurans (frogs and toads). This frog has reproductive mode 19, with its characteristic semi-terrestrial tadpoles. This genus represents the ex- treme of the trend (from obligatory aquatic to com- pletely terrestrial) that amphibians show towards terrestriality.
... The genera Nyctibatrachus and Pseudophilautus have both evolved in the Western GhatseSri Lanka biodiversity hotspot (Meegaskumbura et al., 2019;Torsekar, 2019;Van Bocxlaer et al., 2012;Vijayakumar et al., 2016), and are distantly related, having diverged about 63.8e94.7 million years ago (Van Bocxlaer et al., 2006). Members of both lineages use vocalizations to communicate and are prolonged, territorial breeders Gramapurohit et al., 2011). They are thus likely to communicate both with potential mates and with territorial rivals. ...
Article
Acoustic signals in animals serve to convey context-dependent information to receivers. Birds and mammals combine diverse sounds into complex sequences to communicate, but the role of temporal sequencing of signals remains understudied in other taxa. Anuran vocalizations are a prominent feature of their life history, and function in defence of territories and to attract mates. However, there are few data on whether anurans pattern their calls into sequences, and whether temporal sequences convey information about context. Here, we investigated the context-dependent vocal repertoire and the use of vocal sequences by two anuran species belonging to different lineages, comparing frogs vocalizing alone and in the presence of a territorial rival. Using a robust analytical framework, we present evidence that both species modify their vocal sequence structure according to context. Specifically, one species (with a smaller repertoire, from a more basal lineage) appends notes to generate more complex sequences, whereas the other (more recently diverged and with a larger repertoire) shifts to different note types, resulting in different sequences for different contexts. Thus, despite differences in repertoire size, both frog species are capable of adjusting the temporal sequence of vocalizations to communicate in different contexts. Vocal sequences and context-dependent ‘syntax’ may be more common in anurans than previously thought, and our methodology presents a paradigm to study the evolution and function of these complex vocal patterns.
... The males would then transport the females to those sites. Male selection of oviposition sites has arisen in phylogenetically and geographically distant taxa including in Bombay night frogs (Nyctibatrachidae: Nyctibatrachus humayuni) from India (Gramapurohit et al. 2011), fuscous foam frogs (Leptodactylidae, Leptodactylus fuscus; Wells 2007), Boraceia tree toads (Hylodidae, Hylodes phyllodes; Haddad and Sawaya 2000), and some poison dart frogs (Dendrobatidae; Crump 1972, Wells 2007 from Central and South America. The ability of a male to find and defend a suitable oviposition site and then attract a female to that site will be favored by sexual selection. ...
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Abstract Amphibians exhibit diverse reproductive behaviors, including nine documented types of amplexus, the behavior in which male and female frogs position themselves for courtship, oviposition, and fertilization. All known forms of amplexus involve the male on top of or in line horizontally (cloacal apposition) with the female. Here, we report a novel form of amplexus observed in Lau’s leaf litter toad (Leptobrachella laui; Megophryidae) in Hong Kong, China. Termed “sex‐reversed inguinal amplexus,” the female climbs on top of a male and the male transports the female to a concealed breeding site. We were unable to determine whether this was the amplectant position in which frogs engaged during oviposition or solely during courtship and prior to oviposition, but there are a number of possible evolutionary drivers that may have given rise to this behavior, including limiting suitable oviposition sites or strong competition for males among females. Further research will be necessary to understand the evolutionary origins of this novel reproductive behavior.
... In contrast, a study on leafhoppers (Aphrodes makarovi) suggested that a female responded equally to advertisement calls emitted by both winners and losers, and mated with the first male that located her, regardless of his investment in calling (Kuhelj et al., 2017). Usually, a female frog initiates courtship by approaching a calling male, and the male initiates amplexus by climbing on the back of the female (Gramapurohit et al., 2011;Montanarin et al., 2011;Ovaska and Rand, 2001). Therefore, once a female is nearby, it is possible that locating the female is more productive than continued calling. ...
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There is increasing evidence that many anurans use multimodal cues to detect, discriminate and/or locate conspecifics and thus modify their behaviors. To date, however, most studies have focused on the roles of multimodal cues in female choice or male-male interactions. In the present study, we conducted an experiment to investigate whether male serrate-legged small treefrogs (Kurixalus odontotarsus) used visual or chemical cues to detect females and thus altered their competition strategies in different calling contexts. Three acoustic stimuli (advertisement calls, aggressive calls and compound calls) were broadcast in a randomized order after a spontaneous period to focal males in one of four treatment groups: combined visual and chemical cues of a female, only chemical cues, only visual cues and a control (with no females). We recorded the vocal responses of the focal males during each 3-min period. Our results demonstrate that males reduce total number of calls in response to the presence of females, regardless of how they perceived the females. In response to advertisement calls and compound calls, males that perceived females through chemical cues produced relatively fewer advertisement calls but more aggressive calls. In addition, they produced relatively more aggressive calls during the playback of aggressive calls. Taken together, our study suggests that male Kodontotarsus adjust their competition strategies according to the visual or chemical cues of potential mates and highlights the important role of multisensory cues in male frogs' perception of females.
... A comprehensive systematic revision by Biju et al. (2011) provided taxonomic stability for various previously available names in this genus. The latest studies on Nyctibatrachus frogs have particularly drawn attention towards their natural history, including reproductive behaviour and ecology (e.g., Kunte, 2004;Biju et al., 2011;Gramapurohit, Gosavi & Phuge, 2011;Gururaja et al., 2014;Willaert et al., 2016) and tadpole development (Annandale, 1918;Annandale, 1919;Rao, 1923;Bhaduri & Kripalani, 1955;Pillai, 1978;Priti, Gururaja & Ravikanth, 2015), as well as patterns of distribution and endemism in the Western Ghats (Van Bocxlaer et al., 2012). Male advertisement calls have so far been described for N. major (Kuramoto & Joshy, 2001), N. jog, N. kempholeyensis, N. kumbara (Gururaja et al., 2014) and N. humayuni (Willaert et al., 2016). ...
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The Night Frog genus Nyctibatrachus (Family Nyctibatrachidae) represents an endemic anuran lineage of the Western Ghats Biodiversity Hotspot, India. Until now, it included 28 recognised species, of which more than half were described recently over the last five years. Our amphibian explorations have further revealed the presence of undescribed species of Nights Frogs in the southern Western Ghats. Based on integrated molecular, morphological and bioacoustic evidence, seven new species are formally described here as Nyctibatrachus athirappillyensis sp. nov., Nyctibatrachus manalari sp. nov., Nyctibatrachus pulivijayani sp. nov., Nyctibatrachus radcliffei sp. nov., Nyctibatrachus robinmoorei sp. nov., Nyctibatrachus sabarimalai sp. nov. and Nyctibatrachus webilla sp. nov., thereby bringing the total number of valid Nyctibatrachus species to 35 and increasing the former diversity estimates by a quarter. Detailed morphological descriptions, comparisons with other members of the genus, natural history notes, and genetic relationships inferred from phylogenetic analyses of a mitochondrial dataset are presented for all the new species. Additionally, characteristics of male advertisement calls are described for four new and three previously known species. Among the new species, six are currently known to be geographically restricted to low and mid elevation regions south of Palghat gap in the states of Kerala and Tamil Nadu, and one is probably endemic to high-elevation mountain streams slightly northward of the gap in Tamil Nadu. Interestingly, four new species are also among the smallest known Indian frogs. Hence, our discovery of several new species, particularly of easily overlooked miniaturized forms, reiterates that the known amphibian diversity of the Western Ghats of India still remains underestimated.
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In vertebrates, the increase in plasma androgens and corticosteroids is essential for the expression of reproductive behaviour. In male anurans, the interaction between hypothalamus-pituitary-gonadal and hypothalamus-pituitary-interrenal axes plays a pivotal role in calling behaviour and energy mobilisation through the secretion of testosterone and corticosterone respectively. To explain the association among body condition, testosterone, corticosterone and calling behaviour the energetic-hormone-vocalisation (EHV) model has been proposed. The model predicts that with continued participation in chorus activity within and across nights, levels of circulating androgens, corticosterone and vocal effort tend to increase and should be positively correlated in calling males. Consequently, decreasing energy reserves should be inversely correlated with corticosterone level in calling males. Depleted energy reserves lead to the peaking of circulating corticosterone, which suppresses androgen production and calling behaviour. In the present study, we used Nyctibatrachus humayuni with unique reproductive behaviour to test the model by quantifying calling behaviour and urinary metabolites of testosterone and corticosterone. We also computed the body condition index to assess the association among energetics, levels of testosterone, corticosterone and calling behaviour. The results show that calling males had higher levels of urinary testosterone metabolites (UTM) than non-calling males indicating the importance of testosterone in controlling the calling behaviour. Surprisingly, urinary corticosterone metabolite (UCM) levels were comparable between calling and non-calling males. Further, calling males had higher body condition estimates than non-calling males. The vocal effort was not associated with UTM, UCM or body condition index (BCI). However, a positive association was observed between UTM and UCM levels in calling males indicating the requirement of higher energy for advertisement. Analysis of UTM and UCM levels throughout the breeding season revealed that breeding basal of UTM was significantly higher than that of UCM. Interestingly, UCM levels were maintained at a lower threshold during the breeding season. These observations are in line with some of the predictions of EHV model.
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Reproductive modes are diverse and unique in anurans. Selective pressures of evolution, ecology and environment are attributed to such diverse reproductive modes. Globally forty different reproductive modes in anurans have been described to date. The genus Nyctibatrachus has been recently revised and belongs to an ancient lineage of frog families in the Western Ghats of India. Species of this genus are known to exhibit mountain associated clade endemism and novel breeding behaviours. The purpose of this study is to present unique reproductive behaviour, oviposition and parental care in a new species Nyctibatrachus kumbara sp. nov. which is described in the paper. Nyctibatrachus kumbara sp. nov. is a medium sized stream dwelling frog. It is distinct from the congeners based on a suite of morphological characters and substantially divergent in DNA sequences of the mitochondrial 16S rRNA gene. Males exhibit parental care by mud packing the egg clutch. Such parental care has so far not been described from any other frog species worldwide. Besides this, we emphasize that three co-occurring congeneric species of Nyctibatrachus, namely N. jog, N. kempholeyensis and Nyctibatrachus kumbara sp. nov. from the study site differ in breeding behaviour, which could represent a case of reproductive character displacement. These three species are distinct in their size, call pattern, reproductive behaviour, maximum number of eggs in a clutch, oviposition and parental care, which was evident from the statistical analysis. The study throws light on the reproductive behaviour of Nyctibatrachus kumbara sp. nov. and associated species to understand the evolution and adaptation of reproductive modes of anurans in general, and Nyctibatrachus in particular from the Western Ghats.
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We conducted a field study in Mar.-June 2007 to evaluate the importance of egg attendance by male Kurixalus eiffingeri to egg survivorship. We found 38 egg clutches and visited them on a fixed scheme by checking all nests at night for 6 d, yielding 1368 visits of 10 min each. Egg attendance frequency was highly uneven among nests and was positively correlated with clutch size. On average, 6.8% ± 4.4% of eggs in an egg clutch died each day. Daily egg mortality was inversely correlated with the attendance frequency, suggesting that paternal care is important to egg survival even though this is a low nest-attendance species. Variances of egg mortality were low when paternal care effort was high, but opposite results were found when paternal care effort was low, suggesting the fate of eggs can also be affected by factors other than paternal care, such as stump conditions. Our results suggest that parental care effort varies via a cost-benefit relationship of investment in the present offspring vs. future reproductive chances. Male frogs spent more time attending eggs when the clutch sizes were large but sought additional mating opportunities if the egg clutches were small, which resulted in large variations in egg mortality among clutches.
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The reproductive biology of Eleutherodactylus cooki was studied in a cave system in San Lorenzo, Puerto Rico. I investigated frequency of multiple clutches in nests, clutch size, nest site locations, reproductive timing, embryonic development, and hatching success for 16 months from September 1995 to December 1996. Males guarded multiple clutches of eggs from up to four different females at a time. The mean clutch size was 17.35 eggs per clutch, and the difference in developmental timing among multiple clutches was between 4-14 days. Triple and quadruple clutches were less frequent than single and double clutches, and were associated with nest location. I examined experimentally the fitness benefit of parental care in the field. Compared to control clutches (males not removed), experimental clutches had significantly lower hatching success. Paternal care offers a significant fitness value through increased hatching success at virtually no cost to males in terms of energy expenditure or missed opportunities to mate. An evaluation of the differential reproductive effort, parental investment, and potential reproductive rate between sexes, considering the operational sex ratio, suggests that sexual selection acts on males in this species. I suggest that the mechanisms of sexual selection are female choice and intrasexual exploitative competition. Males with the greatest reproductive success had more yellow coloration than average in the ventral region and guarded at least one clutch of eggs in recessed surfaces of rock, thereby suggesting that visual cues are important in mate choice. Females were scarce and had higher parental investment, and a lower potential reproductive rate than males. Hence, they represent a resource for which males compete.
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The terrestrial eggs of the coqui of Puerto Rico are brooded almost continuously by the male parent from the time of oviposition until the fully metamorphosed hatchlings emerge from the eggs 15-20 d later. The gelatinous layer surrounding each egg offers no resistance to the exchange of water by the egg, and rates of exchange are determined by microclimatic conditions, structural characteristics of the nest, and the behaviour of the male frog. During development in natural nests, the eggs experience a 3- to 4-fold increase in mass, the result of transfer of liquid water from the incubating male to his eggs. A water uptake that doubles the initial mass of the egg is necessary to produce a full-size hatchling with normal tissue water content.-from Authors
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Parental care in Elmtherodactytus johwtonsi, a terrestrially breeding frog, was uniparentaL but care was provided by either sex. I tested Maynard Smith's evohitionarily stable strategy, continuous breeding model HI, by ^ramining social and ecological conditions under which die sexes provided parental care in Georgetown, Guyana, South America. During the long wet season most males chosen by females as mates provided parental care. No males that acquired females through satellite behavior and displacement competition provided care. Females provided parental care in most cases when males failed to do so, and some returned to nests for 72 h, even after being repeatedly driven away by attending males. Females initiated maternal care up to 72 h after ovipoarion following temporary removal of males. Male-biased operational sex ratios were signtfirandy different for wet and dry months, and no females provided care when monthly rainfall was
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A new species of ranid frog of the genus Nyctibatrachus is described from Castle Rock, Karnataka State, Southwest India. The new species is compared with all known congeners and is diagnosed by the following combination of characters: head wider than long; snout projecting beyond mouth; supratympanic fold poorly defined; webbing on toes reaching base of disks except on Toe IV, where it reaches distal subarticular tubercle; tips of digits on fingers and toes flattened to form disks with distinct grooves separating dorsum of disks from venter; and femoral gland present. The largest specimen in the type series has a snout-vent length of 43.2 mm. Nyctibatrachus hussaini Krishnamurthy, Reddy and Gururaja, 2001, is shown to be an invalid nomen, for lack of typification.
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Males of the glass frog Hyalinobatrachium valerioi engage in diurnal and nocturnal attendance of egg clutches. To study the effect of parental care on embryonic survivorship, we conducted a male removal experiment and measured embryonic survival rates on day 4, 8, and 12 after oviposition in attended and unattended clutches. Embryonic survivorship was significantly higher in the control group than in the male removal group but decreased with time in both groups. Arthropod predation accounted for most of the mortality in both groups. Desiccation of clutches only occurred in unattended clutches. We hypothesize that egg attendance in H. valerioi increases embryonic survivorship by deterring egg predators and preventing desiccation.
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This paper reports a new reproductive mode in anurans, observed for the green treefrog, Hyla leucopygia, a species from the Atlantic Forest of Brazil and a member of the H. albosignata group. The reproductive mode of H. leucopygia is defined as follows: aquatic eggs and embryos in subterranean constructed nests; subsequent to flooding, feeding tadpoles in ponds or streams. We suggest that the new reproductive mode is widespread among the species in the H. albosignata group. The specialized courtship behaviors of H. leucopygia, characterized by vocalizations and a stereotyped sequence of mutual touches between male and female, are described. A review of the reproductive modes of hylid frogs is provided, with 11 modes recognized for the Atlantic Forest hylids and 12 modes for hylids around the world.RESUMONo presente trabalho descrevemos um novo modo reprodutivo em anuros, observado em Hyla leucopygia, espécie de Mata Atlântica, pertencente ao grupo de H. albosignata. O modo reprodutivo de H. leucopygiaé definido como: ovos e embriões aquãticos em ninhos subterrãneos construídos; após a inunda¸ão, girinos que se alimentam são observados em riachos e po¸as. Sugerimos que o novo modo reprodutivo ocorre entre as espécies do grupo de H. albosignata.Descrevemos o comportamento de corce especializado, observado para H. leucopygia, caraccerizado por vocaliza¸õcs c uma sequencia estereotipada de toques mútuos entre macho e fêmea. é apresentada uma revisbo sobre os modos reprodutivos da família Hylidae, sendo reconhecidos 11 modos para 0s Hylidae da Maca Atlãntica e 12 modos para os Hylidae do mundo.
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In the Puerto Rican frog Eleutherodactylus coqui, parental care is performed exclusively by males, and consists of attending the eggs and hatchlings at a terrestrial oviposition site. The two major behavioural components of parental care are egg brooding and nest defence against conspecific egg cannibals. Defence behaviour includes aggressive calling, biting, sustained biting, wrestling, and blocking directed against nest intruders. Parental care lasts from oviposition to hatching (17–26 days) and often for several days after hatching. During pre-hatching development, males are present in their nests 97.4% of the time during the day and 75.8% of the time at night. A large portion of this time is spent brooding eggs. In a field experiment, males were removed from their nests and the fate of clutches was monitored. Compared to control clutches (males not removed), experimental clutches had significantly lower hatching success and suffered significantly greater mortality from desiccation and cannibalism. Hence, parental care yields significant benefits to male fitness via increased offspring survival.
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Female multiple mating and alternative mating systems can decrease the opportunity for sexual selection. Sperm competition is often the outcome of females mating with multiple males and has been observed in many animals, and alternative reproductive systems are widespread among species with external fertilization and parental care. Multiple paternity without associated complex behaviour related to mating or parental care is also seen in simultaneously spawning amphibians and fishes that release gametes into water. Here we report 'clutch piracy' in a montane population of the common frog Rana temporaria, a reproductive behaviour previously unknown in vertebrates with external fertilization. Males of this species clasp the females and the pair deposits one spherical clutch of eggs. No parental care is provided. 'Pirate' males search for freshly laid clutches, clasp them as they would do a female and fertilize the eggs that were left unfertilized by the 'parental' male. This behaviour does not seem to be size-dependent, and some males mate with a female and perform clutch piracy in the same season. Piracy affected 84% of the clutches and in some cases increased the proportion of eggs fertilized, providing direct fitness benefits both for the pirate males and the females. Sexual selection--probably caused by a strong male-biased sex ratio--occurs in this population, as indicated by size-assortative mating; however, clutch piracy may reduce its impact. This provides a good model to explore how alternative mating strategies can affect the intensity of sexual selection.
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Field observations were conducted on egg attendance in Chirixalus eiffingeri from April to August 2003. Parental attendance during embryonic development was performed exclusively by males. The frequency of egg attendance was low (27%), but it had a distinct diel pattern in which males were observed to attend eggs more frequently at night than during the day. Attendance frequency significantly decreased with increasing developmental stage of the embryos, but it was not statistically significantly related to clutch size. Field observations confirmed that male frogs actively moisten egg clutches using their ventral surfaces, presumably to prevent desiccation of egg clutches. The non-significant relationship between hatching success and frequency of egg attendance suggests that embryonic survival of C. eiffingeri is more than a function of egg attendance, and ecological and environmental factors, such as climate and characteristics of microhabitats, may also influence the survivorship of the embryos.
Article
Begins with a description and summary of the phylogenetic distribution of parental care. Next, the five major modes of parental care (egg attendance, egg transport, tadpole attendance, tadpole transport, and tadpole feeding) and their presumed functions are discussed. Three correlates of parental care in amphibians are then reviewed: large egg size, small clutch size, and terrestrial modes of reproduction. Fourth, various aspects of the evolution of parental care in amphibians are addressed. What factors influence the existence and type of parental care? What empirical data are available on the benefits and costs of parental care? Why do some species have parental care whereas others do not? Why do only females provide care in some species, only males in others? Why is biparental care so rare in amphibians? Lastly, evidence for flexibility in parental behaviours is reviewed and the extent to which parental care is adjusted to variation in the benefits to offspring and costs to parents is examined. -from Author
Article
A new species of ranid frog of the genus Nyctibatrachus is described from Castle Rock, Karnataka State, Southwest India. The new species is compared with all known congeners and is diagnosed by the following combination of characters: head wider than long; snout projecting beyond mouth; supratympanic fold poorly defined; webbing on toes reaching base of disks except on Toe IV, where it reaches distal subarticular tubercle; tips of digits on fingers and toes flattened to form disks with distinct grooves separating dorsum of disks from venter; and femoral gland present. The largest specimen in the type series has a snout-vent length of 43.2 mm. Nyctibatrachus hussaini Krishnamurthy, Reddy and Gururaja, 2001, is shown to be an invalid nomen, for lack of typification.
Article
The Western Ghats of India are very rich in amphibian species with 117 species of frogs, toads and caecilians. Eighty-nine species are endemic to this biogeographical region. Analysis of ranges and patterns of geographical distribution of amphibians on the Western Ghats suggest that the southern half of the Western Ghats and the low-medium elevation hills are more diverse in species than the northern half and higher hills. This is attributed to the more widespread rainfall and the less variable climatic conditions in the south. About half the species are apparently localized. Of those species with wider ranges, a majority show patchy distribution. Species preferring the moist evergreen forests as habitats tend to have patchy distributions. This appears to be a result of habitat destruction and fragmentation. The overall patterns of species richness and local endemism are rather different from those of the angiosperms and birds. In birds and angiosperms, a significant proportion of endemics are found on the higher hills. On the contrary, endemic amphibian species are found in the lower altitudinal range of 0-1000 m, with a majority between 800 and 1000 m.
Article
Cophixalus parkeri is a terrestrial breeding microhylid frog from the montane moss forests of northeastern New Guinea. The pattern of parental care in this species and its adaptive significance was studied in the field and in the laboratory. Egg brooding, is performed by the male in most cases, and much less frequently by the female. The parent remains with the clutch throughout the 85–100 day prehatching period. Egg removal experiments demonstrated that survivorship of embryos significantly decreased in the absence of the attending parent. Mortality of unattended embryos may be caused by a variety of factors, including fungal infection, egg cannibalism, predation by arthropods, and abnormal development.Brooding adults can provide protection to their developing offspring via several possible mechanisms eg. aggressive defense of territories on which eggs are deposited, ingestion of potential arthropod predators, and egg turning (Fig. 2).Several differences were found in the quality and quantity of food ingested by brooding versus non-brooding adults collected in the same locality during the same period. On average, brooding adults consumed less food and of lower quality than non-brooding adults (Table 1). These differences in diet were correlated with length of time parents had attended their eggs before they were examined (Fig. 3). The reduced food intake during egg brooding is reflected by significantly smaller fat bodies and less carcass fat in egg brooders relative to nonbrooding adults (Table 1). These results are discussed in terms of relative costs and benefits of parental care in this species.
Article
I studied the ecology of parental care behaviors displayed by two closely related sympatric species of microhylid frogs in Papua New Guinea that occupy different microhabitats. Adult removal experiments on the terrestrial frog Hylophorbus rufescens and the undescribed arboreal frog Oreophryne sp. A demonstrate a significant positive effect of parental attendance on offspring survivorship and differential causes of egg mortality between microhabitats. Desiccation was the primary cause of egg mortality for the arboreal frog, whereas predation was the main source of mortality for the terrestrial frog. These selection pressures (desiccation and predation) are comparable to two of Wilsons prime movers of the evolution of parental care (harsh environment and predation) and may have driven and/or are maintaining the evolution of parental care behaviors in these Papuan microhylid frogs. These results highlight microhabitat-specific selection pressures in the evolution and maintenance of parental care behaviors.
Article
I present the first behavioural study of natural populations of a Madagascan poison frog. Focal watches of marked individuals were conducted for 925 h, in five populations, across two seasons. Like the New World dendrobatids, these diurnal anurans eat ants and are aposematically coloured. Data are presented that provide additional instances of convergence with the dendrobatids, including (1) extended male–male fights over defended resources necessary for reproductive success of both sexes, (2) stereotyped, highly tactile courtships in which the female may reject initial oviposition sites and (3) complex maternal care. Females return to water-filled phytotelmata, or wells, and lay trophic eggs for their tadpoles. Mantella laevigata has the minimum possible clutch size in anurans (usually one) suggesting a high degree of parental investment. Males defend wells, which attract females that oviposit in the wells. Fertilized eggs may hatch and metamorphose, or may be eaten by a tadpole already in that well, of which the territorial male is probably the father. Unfertilized eggs serve as food for tadpoles. Oviposition-site scouting behaviour of both sexes, and the dependency of tadpole presence on the position of eggs laid, provide evidence of context-dependent, and assessment, behaviour. Females leave courtships most often only after visiting potential oviposition sites, while males usually leave to engage other males in aggression, suggesting that territory maintenance may be the most important component of male reproductive success. Two other species of frogs often prevent M. laevigata from using defended oviposition sites, and larval crane flies predate the eggs of all frog species using water-filled wells.
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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.
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SPEC. COLL. HAS ARCHIVAL COPY; ZOOLOGY HAS CIRCULATING COPY; MICRO. ROOM HAS CIRCULATING MICROFICHE COPY (2 SHEETS). Thesis (Ph.D.)--U. of Calif., Davis. Typescript. Degree granted in Zoology.
Article
Conservationists are far from able to assist all species under threat, if only for lack of funding. This places a premium on priorities: how can we support the most species at the least cost? One way is to identify 'biodiversity hotspots' where exceptional concentrations of endemic species are undergoing exceptional loss of habitat. As many as 44% of all species of vascular plants and 35% of all species in four vertebrate groups are confined to 25 hotspots comprising only 1.4% of the land surface of the Earth. This opens the way for a 'silver bullet' strategy on the part of conservation planners, focusing on these hotspots in proportion to their share of the world's species at risk.
Écologie et développement de Mantella aurantiaca Mocquard 1900
  • J Arnoult
Arnoult, J. (1966): Écologie et développement de Mantella aurantiaca Mocquard 1900. Bull. Mus. Natl. Hist. Nat. Paris 37: 931-940.
Contribution a l'étude des batraciens de Madagascar
  • J Arnoult
  • M Razarihelisoa
Arnoult, J., Razarihelisoa, M. (1967): Contribution a l'étude des batraciens de Madagascar. Le genre Mantidactylus.
A study of clutch attendance in the Neotropical frog Centrolenella fleischmanni
  • M P Hayes
Hayes, M.P. (1991): A study of clutch attendance in the Neotropical frog Centrolenella fleischmanni. Ph.D. Dissertation, Univ. of Miami, Coral Gables, FL, 239 pp.
A check list of amphibia of India
  • K P Dinesh
  • C Radhakrishnan
  • K V Gururaja
  • K Deuti
  • G Bhatt
Dinesh, K.P., Radhakrishnan, C., Gururaja, K.V., Deuti, K., Bhatt, G. (2010): A check list of amphibia of India. Zool. Sur. India. Online database. 1-11.
M. curtus (Blgr.) et M. alutus (Peracca)
  • M Adultes Et Formes Larvaires De
  • Betsileanus
Adultes et formes larvaires de M. betsileanus (Blgr.), M. curtus (Blgr.) et M. alutus (Peracca). Bull. Mus. Natl. Hist. Nat. 39: 471-487.
  • J Arnoult
  • M Razarihelisoa
Arnoult, J., Razarihelisoa, M. (1967): Contribution a l'étude des batraciens de Madagascar. Le genre Mantidactylus. Adultes et formes larvaires de M. betsileanus (Blgr.), M. curtus (Blgr.) et M. alutus (Peracca). Bull. Mus. Natl. Hist. Nat. 39: 471-487.