Reproductive ecology and behaviour of a species of Adenomera (Anura,Leptodactylinae) with endotrophic tadpoles: Systematic implications

The species of the Leptodactylus fuscus group and those of the genus Adenomera lay their eggs in underground chambers. According to current systematic arrangement of these genera, this behaviour is convergent. Here we describe reproduction, courtship, tadpole morphology, calls, chamber structure, and populational phenology of an Adenomera species, and compare some of these features with those of other species of the genus and with species of Leptodactylus of the fuscus and pentadactylus groups. We tested the tadpoles of the Adenomera sp. and those of Leptodactylus labyrinthicus (pentadactylus group) for their foam‐making abilities. There was sexual dimorphism in size; males averaged 22.0?mm and females 24.3?mm in snout–vent length. Males called from late September to late February; calling often began about 2–3?h before sunset. Males called exclusively in open (non‐forest) areas. Egg clutches were found around male calling sites. Males excavated spherical chambers which had a direct entrance. During mating, the male led the female towards a previously excavated chamber. Territorial interactions (aggressive calls and fights) occurred when an intruder male approached a calling male. Late‐stage tadpoles and newly metamorphosed juveniles were found within underground chambers. Clutch size averaged 10.6; eggs averaged 3.7?mm in diameter and were cream coloured. Tadpoles had horny beaks, but no labial tooth; spiracle was present. All tested groups of tadpoles generated foam within 10?h. As we report for Adenomera sp., the males of Leptodactylus species of the fuscus group lead the female to a previously excavated chamber. Tadpole foam‐making behaviour was reported in Leptodactylus of the fuscus group and was previously unknown for any species of Adenomera or for Leptodactylus of the pentadactylus group. The way in which the tadpoles of Adenomera sp., Leptodactylus spp. (of the fuscus group) and L. labyrinthicus made foam was quite similar. The foam‐making behaviour of the studied tadpoles may act to avoid compaction of the tadpoles at the bottom of the basin or underground chamber, avoiding overcrowding and increasing respiratory and excretory efficiency. As presently recognized, the phylogenetic position of Adenomera suggests that reproductive major behavioural features are convergent with some Leptodactylus species. Alternatively, our data point to close phylogenetic relationships between Adenomera and Leptodactylus of the fuscus and pentadactylus groups, reinforcing the paraphyletic nature of the genus Leptodactylus.     

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.     

Reproductive features of three maternal-caring species of Leptodactylus (Anura: Leptodactylidae) with a report on alloparental care in frogs

We describe aspects of the reproduction of three shoaling/maternal-caring Leptodactylus species (Leptodactylus aff. latrans, Leptodactylus podicipinus and Leptodactylus aff. leptodactyloides), pointing to the relevance of the female to tadpoles and describe a case of alloparental care in frogs. Females of the three species connected water bodies by digging channels to their tadpoles. Leptodactylus aff. latrans females often expelled predatory snakes and conspecific males that approached shoals to prey upon tadpoles. In water bodies containing predatory teleosts, tadpoles of L. aff. latrans only reached metamorphosis in the presence of guardian females. Channel digging can provide tadpoles with access to new feeding grounds and prevent predation and desiccation. We found brood mixing and alloparental care between L. aff. latrans and L. podicipinus which, as in some Teleostei, may be regarded as the result of identification mistakes.     

Vocalization and territorial behaviour of Phyllomedusa nordestina Caramaschi, 2006 (Anura: Hylidae) from southern Bahia,Brazil

Territoriality is common among amphibians with a prolonged breeding season and can be expressed through the defence of territories with vocalizations and aggressive interactions. The present study aims to describe the territorial behaviour of male Phyllomedusa nordestina, test whether the physical characteristics of males influence the results of disputes, and describe the vocalizations of the species. The study was conducted at temporary and permanent ponds located in the Ecological Reserve Michelin, Igrapiúna, Bahia, Brazil. Male P. nordestina defended territories and showed aggressive behaviour, consisting of vocal disputes, chasing and physical fighting. Winners were not bigger, heavier, or in better condition than the losers. The victory may be associated with the vocalization activity. Three types of vocalizations were recorded: the advertisement call, composed of one or two multipulsed notes, and two types of territorial calls. We also report on male patrolling behaviour and habitat use.     

Natural history of Phyllomedusa megacephala (Miranda-Ribeiro, 1926) (Anura: Hylidae) in southeastern Brazil,with descriptions of its breeding biology and male territorial behaviour

The breeding biology and male territorial behaviour of the large-headed leaf-frog (Phyllomedusa megacephala) were studied in three temporary altitudinal streams located in the Cerrado biome of southeastern Brazil, during three consecutive years (2007–2009). Phyllomedusa megacephala showed significant sexual dimorphism, with females being bigger and heavier than males. Acoustic and physical interactions between males defending or not defending territories including amplectant and non-amplectant males, patrolling behaviour by males without established territories, and triple amplexus were observed. Neither males nor females were observed using visual cues when searching for mates. We found that males that were present at breeding sites in previous years bred more successfully and maintained territory better.     

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.     

Helminth biodiversity of Costa Rican Anurans (Amphibia: Anura)

One hundred and sixty-three frogs representing 21 species collected in Costa Rica were examined for helminths. Those found were: one species of Digenea (Mesocoelium monas), one species of Cestoda (Cylindrotaenia americana), 15 species of Nematoda, 11 species represented by gravid individuals (Aplectana hylambatis, Aplectana incerta, Aplectana itzocanensis, Capillaria recondita, Cosmocerca parva, Cosmocerca podicipinus, Falcaustra costaricae, Hedruris heyeri, Oswaldocruzia costaricensis, Oswaldocruzia nicaraguensis, Rhabdias savagei) and four species represented by larvae (Physaloptera sp., Porrocaecum sp., Spirocamallanus sp., Ascarididae gen. sp.) and three species of Acanthocephala, one species represented by gravid individuals (Anuracanthorhynchus lutzi) and two species by cystacanths (Centrorhynchidae gen. sp. and Oligacanthorhynchidae gen. sp.). Mean helminth diversity (number of helminth species) per frog species was 2.4 ± 0.3 SE, range: 1–6. Forty-nine new host records are reported. Costa Rican frogs are infected by generalist helminths, which infect other species of frogs from Central and South America.     

Development and demography of Phasmahyla jandaia (Bokermann and Sazima, 1978) (Anura,Hylidae) tadpoles in an Atlantic Forest site,southeastern Brazil

Mortality rates are often high during the anuran tadpole stage, making demographic parameters in this phase of their life cycle important to the understanding of population demography. Nevertheless, information on mortality rates or population size is lacking for most Brazilian anurans. Herein we report on the demographic parameters of Phasmahyla jandaia (Hylidae) during the larval stage, including number of individuals through time, mortality rates and time of recruitment. Tadpole recruitment occurred year‐round, although froglet recruitment to the terrestrial habitat was restricted to the warm, rainy season. This trend seems to result in high plasticity of the tadpole developmental period. Mortality rates decreased with advancing tadpole stage, totalling 77% during the whole aquatic phase. Survivorship can be regarded as intermediate compared with other anurans for which data are available, and is in accordance with a high investment in egg size and the low number of eggs laid by P. jandaia.     

Reproductive aspects of Leptodactytus hylaedactylus (Anura: Leptodactylidae), a member of the Leptodactylus marmoratus species group,with a description of tadpoles and calls

In this paper we describe some aspects of the reproductive biology of Leptodactylus hylaedactylus from open areas of Central Amazonia, Brazil. We describe the calling site, reproductive season, daily pattern of calling activity, chamber structure, vocalizations and tadpole morphology. Males of Leptodactylus hylaedactylus called amidst grasses and bushes in open and urban areas, throughout the year, and a greater number of males were heard in the period from 16:00 to 20:00 h. The eggs are deposited in underground chambers, which are spherical or elliptical. Larval development occurs inside the chambers. Two types of vocalizations were detected, the advertisement and the territorial call. The advertisement call of the species studied herein differs from other calls described for L. hylaedactylus from other localities of Brazil, but is very similar to that described from Peru. Tadpole morphology is similar to that described from individuals in French Guiana.     

Reproduction,planula development,and substratum selection in three species of Stylactaria (Cnidaria: Hydrozoa) from Hokkaido,Japan

Modes of reproduction, morphology and behaviour of planulae, and substratum specificity were studied and compared in three species of the hydrozoan genus Stylactaria from Hokkaido, S. conchicola, S. uchidai, and S. multigranosi. Observed differences in these attributes provide additional characters for discrimination of the three species. Stylactaria conchicola is oviparous, its planulae are sedentary, and its hydroid is substratum specific (living only on shells of the gastropod Homalopoma amussitatum). Stylactaria uchidai differs in being ovoviviparous, in having crawling planulae, and in being a substratum generalist. Stylactaria multigranosi is parthenogenetic, its planulae are sedentary, and it is substratum specific (occurring exclusively on the gastropod Nassarius multigranosus). Only female colonies of S. multigranosi are known, and gonophores of this species differ from those of S. conchicola and S. uchidai in being eumedusoid rather than styloid. Correlations were noted between attributes of the planula larva and substratum specificity in the three species. The cnidome differences between the species suggest that penetrant nematocysts are particularly important for sedentary planulae colonizing moving substrata. These characters are also considered useful in the taxonomy of species of Stylactaria. The phylogenetic significance of different gonophore types in the genus is considered.     

Tadpole deposition behaviour in male stream frogs Mannophryne trinitatis (Anura: Dendrobatidae)

Male Mannophryne trinitatis transport their larvae on their backs to predator‐free pools and deposit them there. The experiments reported here investigated M. trinitatis male deposition behaviour in containers placed near a heavily fish‐populated stream at Mount Saint Benedict, northern Trinidad. Choice of deposition site was not related to height above or distance from the stream. The low mean number of tadpoles deposited in each container in the field and in a laboratory experiment indicated that most males tended not to deposit complete clutches in single pools. Deposition experiments in the laboratory with a choice of different‐sized containers showed that deposition was pool size dependent, with more tadpoles deposited in larger containers. Deposition behaviour when given a choice of containers with leaf litter (a source of food and shelter) and with no leaf litter showed no significant preference. Tadpoles grown in different water volumes with different food sources revealed that tadpole growth was best in larger water volumes containing leaf litter. Regular tadpole inspections at a pool in the field established that most tadpoles present were the result of downstream movement.     

Breeding biology of Ameerega braccata (Steindachner, 1864) (Anura: Dendrobatidae) in the Cerrado of Brazil

Reproductive aspects of Ameerega braccata, a Cerrado endemic species of Dendrobatidae, were studied in the surroundings of the type locality of the species, Chapada dos Guimarães, mid-southern Mato Grosso State, Brazil. We found that males call mainly early in the morning and in the late afternoon. During courtship, the female approaches a calling male and tactile and visual communication occurs. Males call continuously while guiding females to the oviposition site, which may be situated as far as 24 m (in a straight line) from the initial encounter site. Spawn are deposited over fallen leaves on the soil surface or in burrows. Female snout–vent length and body mass did not explain the variation in ovary mass, or the variation in the number and size of post-vitellogenic oocytes. The results reported here for A. braccata might help to understand trends in the evolution of dendrobatids in open Cerrado environments.     

Breeding biology of Phyllomedusa azurea Cope, 1862 and P. sauvagii Boulenger, 1882 (Anura) from the Cerrado,Central Brazil

Phyllomedusa azurea and P. sauvagii are treefrogs from seasonal dry environments of Central Brazil. We report on reproductive and other natural history features of these species. The study was carried out in Serra da Bodoquena, Mato Grosso do Sul, Brazil. The reproductive period was determined by the presence of vocalizing males, amplectant pair or presence of tadpoles. The reproductive effort was measured as the ratio of gonad mass in relation to body mass (BM). The reproduction of both species was correlated with the rainy season. Female P. sauvagii produced more eggs and their eggs were larger than those of P. azurea. Both species showed sexual dimorphism in relation to the snout–vent length (SVL) and BM. The mating behaviour of both species was similar. Males in both species showed similar reproductive efforts, but females of P. azurea invested more in gonads compared to the males of P. sauvagii. Phyllomedusa azurea showed a significant relation between SVL versus number of the mature eggs (NME), and P. sauvagii between SVL versus NME and BM versus ovarian mass.     

Reproduction and morphology of Polydorella (Polychaeta: Spionidae), including the description of a new species from the Philippines

A new spionid polychaete, Polydorella kamakamai, associated with sponges is described from the Philippines. Polydorella kamakamai is characterized by acicular neurosetae in segments 2–7, a fifth segment containing a ventral row of spines with digitiform bosses, and lack of branchiae. As in all members of the genus, P. kamakamai undergoes asexual reproduction via paratomy; the process of paratomy is examined through scanning electron and light microscopy. This species exhibits a growth zone following segment 10, leading to the production of stolon individuals budding from the stock individual; five or more individuals can thus be formed in a single chain. Paratomic division typically occurs in chains containing four to five individuals and as a result colonies are dominated by chains of two individuals. Sexual reproduction is documented for only the second time in the genus; P. kamakamai produces eggs in segments 13–15. Asexual reproduction and fine morphological structure of the ventral spines of the fifth segment are examined by SEM in P. dawydoffi and P. stolonifera. Polydorella dawydoffi is recorded for the first time from the Philippines and the Red Sea and these are compared to type specimens from Vietnam. The ventral spines of P. dawydoffi contain eight or nine rounded or pointed teeth along the apical end and a capillary extension not previously observed with light microscopy. Notes on feeding biology, parasitism by copepods, and a discussion of the evolutionary relationships of Polydorella and other polydorids are provided.     

Vocalizations of the Brazilian torrent frog Hylodes heyeri (Anura: Hylodidae): Repertoire and influence of air temperature on advertisement call variation

In this study we analysed the acoustic activity of Hylodes heyeri in areas of Atlantic Forest, in southern Brazil. Observations were made in November 2001 and from January to April 2002, at Estação II Instituto Agronômico do Paraná, municipality of Morretes, State of Paraná. Males displayed three different vocalizations: advertisement calls, territorial calls, and courtship calls. Temporal and spectral parameters of advertisement and territorial calls were analysed, along with call intensity. The duration of the advertisement call showed a negative correlation with air temperature, with males decreasing the duration of advertisement calls at higher temperatures. Male body size was not correlated with any of the acoustic parameters. Details on habitat use, distances to nearest vocalizing neighbour, and daily calling activity are also included.     

On the natural history of Leptodactylus syphax with comments on the evolution of reproductive features in the L. pentadactylus species group (Anura,Leptodactylidae)

We describe the reproduction of Leptodactylus syphax from Brazil and attempt to trace the evolution of reproductive traits within the L. pentadactylus species group. We quantified the proportion of eggs/embryos from fresh nests. We test whether L. labyrinthicus and L. syphax tadpoles can prey on eggs from heterospecific foam nests. Egg clutches were found outside the water at the edges of rocky/seasonal streams, usually within excavated basins. Males beat the foam with their legs moving from side to side. Clutches do not have trophic eggs, since most of their eggs develop into tadpoles. Tadpoles cling on rocks in current/shallow waters. Only L. labyrinthicus tadpoles could prey on eggs from heterospecific foam nests. If the L. pentadactylus group is monophyletic, excavated basins and foam‐beating in lateral motions may be possible synapomorphies of this group. However, large adults, carnivorous tadpoles and trophic eggs appear to be associated synapomorphies of a less inclusive group.     

Breeding biology of the rapids frog Limnomedusa macroglossa (Anura: Cycloramphidae) in southern Brazil

Limnomedusa is a monotypic genus that occurs in association with rocky outcrops and stream beds. Based on observational and mark–recapture fieldwork from 2005 to 2008, we report the breeding biology of Limnomedusa macroglossa in southern Brazil. The reproductive season lasted from late August to early February. Tadpoles were recorded from early September to late February. A clear pattern of emergence/recruitment was observed in juveniles. The occurrence of reproductive activities was clearly related to the longest photoperiods, when the highest temperatures occur. Males called from rocky or concrete substrates, mostly under rocks. Amplexus was axillary and the operational sex ratio was nearly even. Spawn occurred in lentic water bodies but tadpoles also completed their development in slow‐flowing water. Although using similar habitats for reproduction, L. macroglossa reached lower levels of specialization toward terrestriality than did the cycloramphids Cycloramphus and Thoropa. We classify L. macroglossa as a breeding habitat specialist that would be threatened by river damming.