Reproductive ecology of the glass frog Espadarana prosoblepon (Anura: Centrolenidae) in an urban forest of the Central Andes of Colombia

Population and reproductive behaviour aspects of the glass frog Espadarana prosoblepon are well known for populations from Central America, but similar information is lacking for populations from South America. We recorded the reproductive ecology of a population of the glass frog E. prosoblepon in the city of Armenia, Central Andes of Colombia. With weekly surveys with mark-recapture between December 2013 and November 2015, we monitored activity patterns and evaluated if the probability of males mating is associated to their body size or to chorus tenure (i.e. the number of nights a same individual is calling for attracting a mate). In addition, upon observing an amplexus, we recorded the behaviour of the individuals until oviposition and noted characteristics of egg clutch. We recorded 47 males and 32 females, nine amplexus events, eight ovipositions, and 21 egg clutches (35.4 ± 4.79 eggs per clutch, N = 29). Activity of males and females and the number of egg clutches were positively correlated to rainfall. Mating success of males was not associated to their body size, but it was positively associated to longer chorus tenure; clutches from large females had a higher number of eggs than clutches from small females. Oviposition occurred on average 3.76 ± 1.74 hours after we first observed the amplexus, occurring 93.1% of the time in fronds of Selaginella geniculata at an average height of 1.58 ± 0.44 m. After the oviposition, the male left the site, while the female remained between 30 and 45 min, partially covering the eggs. The reproductive behaviour of E. prosoblepon did not vary widely between a population in Costa Rica and our population in time to oviposition, and mating success of males associated to chorus tenure; however, in our study population we recorded a larger clutch size and the preference for S. geniculata fronds as oviposition substrate.     

Reproductive behaviour of the glass frog Hyalinobatrachium cappellei (Anura: Centrolenidae) in the Southern Amazon

Frog species of the Centrolenidae family exhibit a high variation in reproductive behaviours. Herein we describe the reproductive, ecological, acoustic and behavioural features of Hyalinobatrachium cappellei in Southern Amazon. Two hypotheses were also evaluated: (1) are ecological characteristics of the reproductive site related to male size and quantity of eggs and clutches? And (2) do males with one or more existing clutches at reproductive sites accumulate more new clutches than those males initially without them? This study was conducted at two streams, with sampling at 1 km each in Southern Amazon. Species reproduction occurred during the wet season and was considered prolonged breeding. Although male vocalization occurred on both the upper and underside of leaves, clutches were most often deposited on the underside of leaves. Males emitted a courtship call upon female approach. The process of female approach until oviposition lasted approximately eight hours. After oviposition, females left the breeding site while males remained near the clutch, covering it with the belly in ventral brooding behaviour. Thus, egg attendance is reported for the first time for this species. No intraspecific or interspecific aggressive behaviour was recorded. There was no relationship between habitat characteristics of the reproductive sites and male size, number of eggs and clutches. However, after 10 days of monitoring, we found evidences that parental males had a higher number of clutches than those males initially without clutches. Similar to other glass frog species, the behavioural characteristics of H. cappellei make this species an excellent model to use in evaluating the cost-effectiveness of parental care and the importance of egg attendance for offspring survival. Therefore, these data contribute towards a better understanding of the complex phylogenetic and biogeographic relationships between centrolenid lineages.     

Reproductive site selection in the leaf-frog Phyllomedusa azurea Cope, 1862 (Anura: Hylidae) in altered areas of the Brazilian Cerrado

The selection of reproductive sites by anurans may be associated with each species’ behavioural restrictions, reproductive modes, morphology and physiology. We investigated the use of reproductive sites by Phyllomedusa azurea in an area of Cerrado, Central-Western Brazil, which has been modified by agricultural and cattle ranching. Reproductive activity was studied during the peak of the rainy season in two consecutive years. No correlation was found between male body size and position of the calling site, and calling sites did not vary among ponds. Conversely, the height and distance from the water margin where clutches were found varied among ponds. Phyllomedusa azurea used mainly Brachiaria sp. and Brachiaria humidicola grasses as calling sites and the grass Brachiaria sp. and the shrub Melochia villosa (Malvaceae) as oviposition sites. Calling males used the vegetation according to its availability; however, individuals seemed to exhibit significant preferences regarding the type of vegetation used for oviposition.     

‘On the rocks’: reproductive biology of the endemic toad Xanthophryne (Anura: Bufonidae) from the Western Ghats,India

Xanthophryne is a toad genus endemic to the northern Western Ghats of India, with two extant sister species – Xanthophryne koynayensis and Xanthophryne tigerina. Both species are local endemics and endangered. We studied reproductive biology of these toads and found that they are specialized to the lateritic rocky outcrops at mid-elevations in high rainfall areas. Xanthophryne toads have sporadic, multiple spawning bouts lasting 2–4 days during early monsoon. In this explosive breeding behaviour, we observed male toads to engage in ‘pelvic thrusts’, a unique and novel behaviour among anurans. Females oviposit in shallow pools in depressions of lateritic boulders where their tadpoles metamorphose. These ephemeral rocky pools have limited resources and they desiccate rapidly with a break in the rains. To mitigate the stochastic risk of desiccation and subsequent large-scale egg/tadpole mortality, females may disperse their reproductive investment spatially and temporally in multiple clutches, and tadpoles metamorphose rapidly. Here, we describe the amplexus, spawning and male advertisement call, and provide a comparative account of the life history traits of the two Xanthophryne species. These toads face numerous threats and are in need of urgent conservation action. These toads, seemingly well adapted to the isolated rocky outcrops, offer an excellent opportunity to understand endemism, mating systems, anuran ecology and behaviour.     

On the natural history of the South American pepper frog,Leptodactylus labyrinthicus (Spix, 1824) (Anura: Leptodactylidae)

Some species of Leptodactylus of the L. pentadactylus group lay their eggs outside water but the tadpoles need to reach water to complete the larval phase; other species complete development in terrestrial nests. Here we present details of the reproduction of L. labyrinthicus in south‐eastern Brazil. The proportion of tadpoles and trophic eggs in aged egg clutches was determined, as well as the growth of the tadpoles while in the nest. The gut contents of tadpoles that were in egg clutches of frogs were analysed. Adult males did not differ from females in size and had hypertrophied forearms and an enlarged spine on the thumb. Reproduction was initiated with the first rains of August/September and extended to mid‐January. Calling and spawning occurred at permanent or temporary water bodies. The foam nests were built in excavated basins outside of, but close to the water. The male determined the place of the basin construction; after amplexus, the female completed the excavation. The amplexus was axillary. One female spent the day after spawning in the foam. The eggs were pale grey, the yolk averaging 2.3?mm in diameter. The mean number of eggs was 2101 per egg clutch. The number of tadpoles in individual nests varied between 0.05% and 11.40% in relation to the total laid eggs. The tadpoles entered water when rains flooded the basin. The tadpoles grew to 12 times the weight of an individual egg while in the nest; no nesting tadpole was beyond stage 25. The longest time we followed tadpoles in a nest was 25 days. Tadpoles were found preying upon eggs of three other frog species and upon conspecific eggs. Males fought by grasping each other in a belly‐to‐belly position; the powerful arms and the thumb spines represent weapons. Even though males can reach maturity in the season following birth, small size would prevent them from establishing their own territory. All the species of the L. pentadactylus group may build their foam nests within excavated basins. The basins may protect the eggs and embryos from cannibalistic tadpoles and may have an anti‐desiccation effect. In order to produce trophic eggs, the female may delay laying additional unfertilized eggs until after the male has abandoned the foam nest. Anuran eggs represent an important food item for tadpoles after they leave the nest.     

Mating behaviour,territoriality and natural history notes of Phyllomedusa ayeaye Lutz, 1966 (Hylidae: Phyllomedusinae) in south-eastern Brazil

The mating (male courtship, amplexus and oviposition) and male territorial behaviours of Phyllomedusa ayeaye are described from a high-altitude site in the state of Minas Gerais, south-eastern Brazil. Information related to male breeding success and territoriality, as well as egg clutch parameters, is provided, together with qualitative information regarding tadpole phenology and juvenile recruitment. In addition, estimations of sexual dimorphism and numbers of marked individuals are available through capture-mark-recapture sampling. Females bred with males within spatially clustered oviposition sites (broadleaf plants). In some cases, the amplectant couple actively searched for the oviposition site. Males defended territories from other males, employing both acoustic and physical interactions. Some males successfully maintained their calling sites over successive nights, and others seemed to switch among nearby sites during successive nights and tried to disrupt ongoing ovipositions. No significant relationship was found between physical attributes (snout vent length or body mass) of males with breeding success. Also, no influence of the number of nights a male was active in chorus and its breeding success was detected. Therefore, it is proposed that the mating system in P. ayeaye may be opportunistic. Additional information related to reproduction (egg clutch parameters and breeding behaviours) is also discussed for other species of the Phyllomedusa hypochondrialis group and compared with the results of the present study.     

Reproductive ecology of a Tibetan frog Nanorana parkeri (Anura: Ranidae)

Endemic to the Tibetan Plateau, Nanorana parkeri figures among the highest altitude amphibians in the world. The present work, which was conducted in an alpine marsh at 4300 m altitude, is the first report of the species’ reproductive ecology. The breeding season, as indicated by the presence of amplectant pairs and fresh eggs in ponds, lasted from early Mary to early July. The ratios of adult male to female were 1.3 in hibernation ponds and 2.3 in spawning ones. Males were smaller than females. Amplexus was typically axillary (81.7%), with a few exceptional amplexus in which a male clasped another male or object rather than gravid females. Scramble competition occurred in 6.8% of the normal amplexus located. The body sizes of amplexed couples correlated positively. Deposited eggs were attached to submerged plants solitarily (60.5%) or in small clusters (39.5%), and the scattered arrangement of individual eggs could be a strategy to ensure embryonic development in oxygen-poor environments. Clutch size averaged 189 [standard deviation (SD) = 64], and correlated positively with female body size; egg size averaged 2.18 mm (SD = 0.10), independent of female body size; both traits within a clutch were negatively related with each other even controlling for female body size. Relatively few and large eggs laid by the Tibetan frogs, compared with those by lowland aquatic-spawning anuran species, should be adaptive to the harsh high-altitude conditions. Larvae hatched from eggs after 16.4 days on average (SD = 5.8). Froglets emerged between late July and early August, but some tadpoles were present in winter. These findings may help to understand the evolution of amphibians in extreme environments and to protect these remote species.     

Activity and reproductive patterns of lizards in the Chaco of Argentina

We studied the activity and breeding pattern of dominant lizard species in the Arid Chaco, the southernmost subregion of the Chaco ecoregion (Chancaní Reserve, Córdoba province, Argentina). Lizards were captured with pitfall traps over a 4-year period. In total, 1449 individuals belonging to 11 of the 12 lizard species recorded in the area were trapped. Of these, we selected six species for a detailed analysis: Teius teyou and Stenocercus doellojuradoi accounted for 63% of the captures, Tropidurus etheridgei, Liolaemus chacoensis and Homonota fasciata accounted for 32%, and 5% comprised Leiosaurus paronae and the remaining five species. All the studied species were active during the warm–rainy season (September to March). Monthly lizard captures were highly correlated with monthly mean temperature and rainfall. No captures occurred during the remaining months of the year. All reproductive tactics known for the Chaco lizards were observed in Chancaní, including single clutch in a short breeding season in summer or autumn, as well as an extended breeding season with multiple clutches. Stenocercus doellojuradoi and L. paronae showed a singular reproductive timing, suggesting the occurrence of egg retention. Compared with sub-tropical Chaco sites, the Arid Chaco only differs in the lack of winter activity, resulting from the lower temperature and rainfall regime of our study site.     

Not every drought is bad: quantifying reproductive effort in the harlequin frog Atelopus laetissimus (Anura: Bufonidae)

Atelopus laetissimus is an endemic and threatened harlequin frog from the high mountain forests of Sierra Nevada de Santa Marta, Colombia. Knowledge of its reproductive biology is essential for understanding the intraspecific interactions that can help the conservation of Atelopus species. We quantified the energy, measured in body weight, invested by males and females of A. laetissimus for reproduction, and how this energetic investment is related to the survival of individuals and rainfall conditions in habitats during two years (2014 and 2015). Our results show plasticity in terms of reproductive phenology linked to rainfall with short- and long-duration breeding strategies. The first year of this study, 2014, had a precipitation level in accordance with the annual averages at the area. During this time frogs exhibit a short breeding period. Contrary to 2014, 2015 was a year with little precipitation, below the annual averages, which probably facilitated the females’ quick spawning in the creeks and a consequent reduction in the duration of amplexus and low breeding efforts by males. This, in turn, was related to a long breeding period that favors the survival and reproduction of males during the entire year. In 2014 we found a decrease of 25% to 30% body weight of potentially reproductive males, which may be attributed to a prolonged duration of amplectant events.     

Breeding behaviour of Bokermannohyla nanuzae (Anura: Hylidae) at an Atlantic Forest site in southeastern Brazil

We studied the breeding activities of Bokermannohyla nanuzae at an Atlantic Forest site in southeastern Brazil from August 2010 to April 2012. We described courtship behaviour, acoustic parameters of calls, egg clutch features and the egg-laying site, and characterized the reproductive mode. We recorded calling males and gravid females almost year-round, except for a few months in the dry season. We observed the interaction of five male–female pairs that exhibited stereotyped behavioural sequences including visual and tactile signals. We identified three different types of calls that we considered as the advertisement call and two types of courtship calls. Egg clutches were placed in rocky crevices with water or in streamside puddles, among rocks, that would be likely to be flooded as stream water level raises, which characterizes a reproductive mode different from the one previously recognized for this species. The breeding biology of B. nanuzae is complex, with elaborate courtship behaviour and signalling.     

Aspects of the natural history of Leptodactylus knudseni Heyer, 1972 (Anura: Leptodactylidae) in a pristine forest in Central Amazonia,Brazil, with comments on ontogenetic variation of its tadpoles

The Leptodactylus pentadactylus species group is comprised of medium to large species of Neotropical frogs. Leptodactylus knudseni, a member of this species group, has a wide distribution throughout the Amazon Basin. Herein we describe aspects of the reproductive biology of L. knudseni and provide notes about the ontogenetic variation of its tadpoles based on a population in a non-flooded forest near Manaus, Amazonian Brazil. Amplectant pairs of L. knudseni lay foam nests in excavated basins on the edge of temporary ponds located on clay soil and at least 50 m from a stream. The tadpole development happens initially in the foam nests with access to the pond after the rain flooding the basins. Studied clutches lacked trophic eggs and tadpoles did not produce foam. Ontogenetic variations in L. knudseni tadpoles are related to size, teeth formulae and body colour. The use of excavated basins for the deposition of foam nests has been reported in several species of the L. pentadactylus group. The absence of trophic eggs and production of foam by the tadpoles differ from other species of the L. pentadactylus group. The tadpole morphology is similar to that described for other species of the group.     

Goliath frogs build nests for spawning – the reason for their gigantism?

ABSTRACT

In contrast to its popularity, astonishingly few facts have become known about the biology of the Goliath Frog, Conraua goliath. We herein report the so far unknown construction of nests as spawning sites by this species. On the Mpoula River, Littoral District, West Cameroon we identified 19 nests along a 400 m section. Nests could be classified into three types. Type 1 constitutes rock pools that were cleared by the frogs from detritus and leaf-litter; type 2 constitutes existing washouts at the riverbanks that were cleared from leaf-litter and/or expanded, and type 3 were depressions dug by the frogs into gravel riverbanks. The cleaning and digging activities of the frogs included removal of small to larger items, ranging from sand and leaves to larger stones. In all nest types eggs and tadpoles of C. goliath were detected. All nest types were used for egg deposition several times, and could comprise up to three distinct cohorts of tadpoles. Nests seemed to be clustered. Camera trapping revealed that nests are guarded by adult frogs at night. The breeding nests may allow the frogs to deposit their eggs away from the torrent rivers, and potential egg and tadpole predators. As nest construction, at least in some cases, requires the removal of large and heavy items, we hypothesize that this can only be achieved by decent sized frogs, possibly explaining the unique size of the species.     

Reproductive biology and strategies of nine meloid beetles from Central Europe (Coleoptera: Meloidae)

The reproductive biology of meloid species from Central Europe is investigated by means of laboratory breeding experiments. They show that the total reproductive potential of meloids, with up to 40,000 eggs, largely exceeds prior data. Furthermore, the number of laid eggs strongly relates to the way by which the triungulins find their host. Clutch size correlates significantly with the size of the beetle, while egg size is independent of this. Both clutch size and egg size decrease with each oviposition. For some species, reproductive data are used to demonstrate how they have adapted to their habitat and to point out existing trade‐offs. Based on the obtained results and on an evaluation of the relevant literature, three types of reproductive strategy can be distinguished within the meloids: (1) very high reproductive rates of open field species with phoretic larvae; (2) average reproductive rates of forest populations of species with phoretic larvae and of species the larvae of which search the nests of their hosts actively; and (3) small to average reproductive rates of those species depositing their clutches in the immediate proximity of their hosts' nests.     

Activity and reproduction in Megalobulimus paranaguensis (Gastropoda,Eupulmonata): implications for conservation in captivity for a South American land snail

ABSTRACT

In South America, Megalobulimus includes a number of threatened species, as well the largest land snails on the continent. The activity patterns and reproductive aspects of this group have not been documented. This work describes the daily and seasonal activity patterns and reproduction of M. paranaguensis. We maintained specimens in the laboratory for one year, and we quantified their behaviour for one hour at four different times of the day (0 h, 6 h, 12 h and 18 h) during three days in four months (August, September, April and May). The number of postures, hatching rate, time of hatching since oviposition and mortality rate among juveniles for each month were also quantified. Megalobulimus paranaguensis was more active in August, and had a egg laying peak one month after. Fifty-one eggs were laid by 12 captive individuals throughout the year, with a mean value of 4.25 eggs per individual. The hatching rate was 80.39%, and the time of hatching since oviposition was 56.7 ± 4.3 days. In two eggs, we observed the presence of twins. The mortality rate among juveniles was low (9.30%) indicating that rearing land snails in captivity has the potential to be an important and viable tool for the management and conservation of these organisms.     

Field and laboratory observations on reproductive aspects of Pseudopaludicola ameghini (Cope, 1887) (Leptodactylidae: Leiuperinae)

ABSTRACT

The genus Pseudopaludicola includes small-sized anurans, widely distributed throughout South America. Twenty-three out of the 25 species occur in Brazil. Although described more than a century ago, from mid-southern Mato Grosso state, central Brazil, Pseudopaludicola ameghini is poorly known. Here we describe the characteristics of reproductive site, amplexus, egg-laying behaviour, eggs and tadpoles of P. ameghini based on specimens and observations performed in the vicinities of the type locality. Pairs of P. ameghini reproduce in shallow and slow groundwater established on hydromorphic terrains, in open environments amidst the Brazilian Cerrado savanna. Reproductive activity occurred between 17:00 and 21:00 h at two sites studied from December 2013 to April 2014. Amplexus is axillary. Eggs are spherical, with a mean diameter of 5.1 mm (yolk plus jelly envelope). Oviposition occurs in shallow sites at a depth of nearly 2.0 cm. Females deposit their eggs one at a time, directly onto sediment at the bottom of waterbodies or attached to submerged vegetation. The tadpole body is oval in dorsal view and globular/depressed in lateral view; eyes are large and dorsally positioned. Nares are large, round, with a small apophysis on marginal rim, dorsally positioned, near the eyes. The spiracle is short, with posterodorsal opening. The oral disc is anteroventral, emarginated laterally, with one dorsal and two ventral gaps; the tooth row formula is 2(2)/2(1), and the upper jaw sheath is ‘arc’ shaped. Pseudopaludicola ameghini has a unique behaviour of oviposition among members of the genus. The differences in reproductive pattern and larval characteristics of P. mystacalis and P. ameghini reinforce the taxonomic validity of the latter, questioned until recently.     

The reproductive strategies of clausiliid land snails from Northern Vietnam (Gastropoda: Stylommatophora)

Under laboratory conditions we scrutinized the reproduction and development of two clausiliid land snail species from northern Vietnam: Phaedusa paviei (Morlet, 1892) and Oospira vanbuensis (Bavay and Dautzenberg, 1899). These species, very similar in shell size and shape, feature different reproductive modes. The former is viviparous, giving birth to one or two neonates on a single occasion, with the number of developing embryos retained in the reproductive tract ranging from 1 to 11. The embryonic shells are 1.8–4.7 mm in height. The latter species is oviparous and produces eggs in clutches (four to six per clutch). Hatching occurs 18–21 days after egg-laying. Both species exhibit a similar growth pattern: the ultimate shell size is attained after 6.5–8.5 months and reproduction starts 5–7 months later. The distribution of viviparous reproduction among the Phaedusinae and its taxonomic importance are discussed.     

The reproductive ecology of Leptodactylus fuscus (Anura,Leptodactylidae): new data from natural temporary ponds in the Brazilian Cerrado and a review throughout its distribution

Recent studies indicate that populations historically called Leptodactylus fuscus (Schneider, 1799) comprise at least three well‐differentiated lineages. Herein, we describe the reproductive ecology of a southeastern clade population of L. fuscus, and review the characters of the reproductive ecology for several populations of the northern and southeastern clades. Most reproductive activity occurred in December and January, which coincided with the highest rainfall period. Males had an aggregated spatial distribution in the central area of the ponds. Three courtship interactions were observed. A female was observed closing the entrance to a burrow with moist sand after oviposition. This behaviour is described for the first time in L. fuscus. The review of the reproductive biology of the northern and southeastern clades indicates a relatively high plasticity in L. fuscus. Furthermore, the results corroborate the suggestion, based on molecular data, that the northern and southeastern clades of L. fuscus represent distinct evolutionary units.     

Reproductive strategies used by moorhens (Gallinula chloropus) colonizing an artificial wetland habitat in south Wales

Over the last ten years, a high-density breeding population (c.180 individuals) of moorhens Gallinula chloropus (Linnaeus) has become established in an artificially created wetland habitat at the Wildfowl and Wetlands Trust (WWT) centre in Llanelli. The reproductive behaviour and success of this population was the subject of an intensive study between 1997–1999. Whilst monogamy was the dominant breeding system used at the site, some individuals bred annually in communal and co-operative groups. The majority of individuals within communal and co-operative groups in 1998 and 1999 were first order relatives. The number of communal groups recorded progressively declined whereas the number of co-operative groups increased over the period of study. Territory size of breeding groups was unrelated to either breeder type or group number. Most nests were constructed in Juncus although many birds also nested in trees and nest boxes intended for captive bred wildfowl. Vegetation height above nests strongly influenced breeding success, and nest site choice at the site was partially determined by vegetation management practices. Such practices may have been responsible for decreased nesting success in specific areas. Rats were the principal egg predators on site accounting for approximately 80% of eggs predated. The study reveals how the reproductive dynamics of this opportunistic bird influences its successful colonization of a new habitat.