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.     

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.     

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.     

Breeding biology of the Pale-bellied Tyrant-manakin Neopelma pallescens (Aves: Pipridae) in south-eastern Brazil

The Pale-bellied Tyrant-manakin (Neopelma pallescens) inhabits semi-deciduous and riparian forests in central-north South America. Contrary to most manakins, there is no evident sexual dichromatism in the species and little is known about its breeding biology. We studied the breeding biology of a colour-banded population of the species from August to December 2016 and from August to October 2017 in the Campus Florestal of the Universidade Federal de Viçosa, south-eastern Brazil. The breeding season extended from early September to late November. The species is promiscuous, with males exhibiting simple courtship displays (exploded leks) in individual arenas. The nest (n = 13) is a cup attached by its top lip between forked branches and is very simple, with a structural layer made with dry grass stems and heads, attached to the branch with spider silk. The outer and lining layers are absent. The mean clutch size was 1.8 eggs (n = 11), which are oval and pale coloured, covered with spots of different shades of brown, often concentrated in the larger pole. Mean egg length and width (± SD) were 21.0 ± 0.9 × 15.8 ± 0.7 mm (n = 14) and the mean weight was 2.8 ± 0.4 g (n = 10). The incubation period could not be estimated, but the nestling period was 15 days (n = 2). The simple percentage of successful nests was 15.4%, with 76.9% of the nests depredated and 7.7% abandoned. This is the first detailed study about the breeding biology of any Neopelma species, providing relevant data for the study of the evolution of life history strategies not only for the genus, but for the whole family Pipridae.     

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.     

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.     

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.     

Home ranges and aspects of the natural history of the Black-masked Finch Coryphaspiza melanotis (Gray, 1840) (Aves,Thraupidae) in central Cerrado,Brazil

ABSTRACT

In the Cerrado, native grasslands have been dramatically lost, leading to an alarming decline in populations of bird species that require these vegetation physiognomies. Species such as the Black-masked Finch Coryphaspiza melanotis (Gray, 1840) are vulnerable to extinction and remain poorly studied. The objective of this study was to examine home ranges of the Black-masked Finch at the Parque Nacional da Chapada dos Veadeiros, central Brazil. Ten males were studied in a patch of shrubby grassland (campo sujo) between February and December 2008. The mean sizes of home ranges were 4.47 ± 1.49 ha (Minimum Convex Polygon) and 3.48 ± 1.44 ha (Kernel 95%), and this varied significantly between seasons. Home ranges were significantly larger in the non-breeding dry season than during other periods, and significantly smaller in the breeding season than during other periods. Core areas (Kernel 50%) had a mean of 0.46 ± 0.26 ha. A large overlap of home ranges was observed. The home ranges of all banded males overlapped those of at least three co-specifics, and most had an area overlap of more than 50%. A nest containing an egg and a nestling was found in November. Small and largely overlapped home ranges can be considered as positive for the conservation of the Black-masked Finch. This is because both small grassland fragments and conservation units can substantially contribute to the conservation of its populations through the Cerrado extension.     

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 the Sayaca Tanager (Thraupis sayaca) in southeast Brazil

ABSTRACT

Thraupis is a genus of the American endemic Thraupidae (subfamily Thraupinae), comprising seven species that inhabit tropical forests to urban centres. The Sayaca Tanager (Thraupis sayaca) is a disturbance-tolerant species of high representativeness in plant-frugivore networks, but information on its breeding biology is scarce and often restricted to non-systematic surveys. We studied the breeding biology of the T. sayaca, following 39 active nests in a periurban area of southeast Brazil during two breeding seasons (2017/2018, 2018/2019). The breeding season ranged from early September to middle December, and the nests were placed in native and exotic plants and human buildings (nest height above ground: 3.35 ± 1.73 m, mean ± SD). Only females incubated and brooded, but both adults built the nests, fed the nestlings, and removed their faecal sacs. Clutch size was 2.86 ± 0.38 eggs and nest attentiveness was 71.2%. The incubation and nestling periods were, respectively, 13.4 and 17.4 days. Males and females did not differ on nestling provisioning and nest sanitation rates. Nestling provisioning (13.35 ± 6.25 trips/hour) increased with nestling age, while mean brooding time was 37.2% and decreased with nestling age. Apparent nest success was 38.7%, and nest survival according to the Mayfield method was 27.2%. Five nests (20.8%) were parasitised by the Shiny cowbird (Molothrus bonariensis), and we recorded five events of nest-site reuse. We concluded that the most remarkable breeding traits of T. sayaca in comparison with close-related tanagers are the use of anthropogenic nest sites, the higher clutch size and number of feeding trips, and the longer nestling period.     

Reproductive behaviour and development dynamics of Odontophrynus cordobae (Anura,Cycloramphidae)

We provide detailed information on breeding sites, release call, satellite behaviour, courtship, and embryonic and larval development of Odontophrynus cordobae. Field observations were carried out during two breeding seasons (2004–2005 and 2008–2009). Clutches were raised in captivity (artificial ponds) to analyse the development of embryos and tadpoles. Breeding sites were represented by streams and their backwaters, as well as temporary and permanent ponds of varying sizes. Operational sex ratio was male-biased varying between 0.154 and 0.25. Acoustic activity started about 8–10 pm and ended between 2 and 4 am the next day. Distance among calling males was approximately three metres. Male satellite behaviour was observed. Amplexus attempts among males were common. Release calls were structurally similar although shorter than advertisement calls. Courtship and formation of amplexus were documented.     

Orchid bees (Apidae: Euglossini) in Cerrado remnants in northeast Brazil

There is a general lack of information concerning the diversity of bees belonging to the Euglossini tribe in Cerrado areas closest to the Brazilian Amazon. The state of Maranhão is situated in the northeast Brazilian Cerrado and has become the agricultural frontier of the country due to the advancement of monoculture and cattle farming. These activities have suppressed animal and plant populations in large areas of the Cerrado remnants, for which we have not yet obtained adequate scientific knowledge of local species. The objective of this study was to conduct a survey of Euglossini fauna in the northeast Cerrado. We evaluated the variation in species richness, composition and abundance between two distinct vegetation types: Cerrado sensu stricto (s.s.) and gallery forest. Male bees were captured from 7:00 a.m. to 5:00 p.m. over two consecutive days. Captures were carried out once per month from July 2012 to December 2013, using a combination of passive and active collection techniques, including baited traps, as well as a collector with an entomological net to collect bees near traps. We collected a total of 766 Euglossini males belonging to 24 species and five genera. The most abundant species were Eulaema bombiformis, Eulaema nigrita and Eulaema cingulata for the gallery forest site, whereas Eulaema nigrita, Euglossa melanotricha and Euglossa cordata were more abundant in the Cerrado s.s. The gallery forest yielded a higher number of male Euglossini (n = 503, 21 species) compared with the Cerrado s.s. (n = 263, 16 species). The presence of seven exclusive species in the gallery forest and three in the Cerrado s.s. indicated that both environments are important for the maintenance of Euglossini species in this region and highlight the increasing need for conservation programmes for the protection of Cerrado environments.     

Reproduction,phenology and mortality sources of a species of Physalaemus (Anura: Leptodactylidae)

Physalaemus cf. fuscomaculatus is a foam-nesting frog of seasonally dry environments of south-eastern Brazil. We report on the reproduction and other natural history features of this species. Population parameters were based on trapped specimens. The advertisement call is described. The calling and spawning season is coincident with the rainy period. Calling and spawning were performed in ponds. Most of the adults were trapped in October and the juveniles during wetter months and the beginning of the dry season. At the end of the reproductive season, the median size of adults lowered. Egg clutches averaged 2350 eggs, each egg being about 1.4?mm in diameter. Males were more abundant than females in traps. Communal foam nests were frequent, involving up to 40 individual nests. Tadpoles entered the water within about 40?h. Maggots (Diptera) infested egg clutches; water bugs and mammals preyed upon adults. In this region, the dry/cold season may be so difficult for survival that early maturation at small size would be advantageous. The male-biased sample may be related to the greater motility of males. The rapid abandonment of the foam by the tadpoles and communal nesting may help to reduce predation by maggots. Skin toxins were not effective in deterring predation upon adults. The call of P. cf. fuscomaculatus differs from that of other species in the biligonigerus group and can help to define the specific status of the studied population.     

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 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.     

A comparative study of the mating call of Pelophylax ridibundus and Pelophylax kurtmuelleri (Anura: Ranidae) from syntopic and allotopic populations

The mating call of Pelophylax ridibundus and Pelophylax kurtmuelleri from three syntopic and five allotopic populations was studied. All recordings were made during the mating season. We tested the hypothesis that the call of P. ridibundus from allotopic populations would differ from that in syntopic populations with P. kurtmuelleri. For the comparative analysis we used univariate and multivariate statistical methods and the following characteristics: call duration, pulse group duration, pulse group interval, pulse group period, pulse group number, minimum, maximum, fundamental and dominant frequencies and pulse energy. Analyses reveal a trait divergence in most of the studied characteristics of the signals, with stronger differentiation between P. kurtmuelleri and P. ridibundus in syntopic populations than between the two species in allotopic ones. The possible evolutionary implications of this divergence are discussed.     

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.     

Age,body size and growth pattern of Argenteohyla siemersi pederseni (Anura: Hylidae) in northeastern Argentina

In this study we analysed the body size, age structure, age at maturity, longevity and growth pattern of Argenteohyla siemersi pederseni in north-eastern Argentina using skeletochronological methods. Body size was sexually dimorphic; females were significantly larger and heavier than males, regardless of age. As A. s. pederseni is an explosive breeder with only one reproductive episode per year, we assumed that each Line of Arrested Growth (LAG) observed was equivalent to one period of decreasing growth, LAGs reflecting a direct estimation of individual age. The minimum number of LAGs counted was two for males and three for females, but there was no sexual difference in longevity. The von Bertalanffy's growth coefficients (K) were higher in males than in females for both size and body mass. Females had a lower growth rate than males, took longer to reach the minimum maturation size, and were older and larger at reproduction.     

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.     

Oviposition site preference and reproductive ecology of Teratohyla midas (Anura: Centrolenidae) in the Colombian Amazon

ABSTRACT

The family Centrolenidae (Glass frogs) includes 157 species of anurans with a Neotropical distribution. Although glass frogs have been the subject of several studies encompassing various aspects of their biology, natural history data on their reproductive ecology is still scarce. One of the important aspects of reproductive ecology is the oviposition site since it can impact the reproductive success of a species. Herein, we provide detailed information on the reproductive ecology of a population of Teratohyla midas from the Colombian Amazon foothills and test whether this species shows a preference on substrate and height of oviposition site. We monitored a population using capture-mark-recapture of individuals identified by a photograph of their unique pattern of dorsal yellow spots. Wild-ID Software was used to corroborate if the dorsal pattern was different between individuals. Additionally, we monitored the presence of egg clutches, amplexus and oviposition behaviour. We observed 110 males and 5 females of T. midas, seen at an average height of 3.1 m ± 2.9 (0–17.8 m) from the ground. Likewise, we recorded the amplexus behaviour of two pairs for approximately 150 min. Once the oviposition happened, the male retreated, and the female covered the egg clutches for approximately 60 min. We observed 25 egg clutches with 60% being deposited in leaves of Selaginella sp and found at an average height of 2.9 ± 1.7 m (1.1–7.0 m). Thus, the selection of oviposition site was not random but mostly specific to one type of substrate. Furthermore, there was an overlap of the re-sampled median height distributions of active individuals and clutches, which suggests that oviposition does not occur at a preferred height within the vertical distribution of individuals. The information presented here is the first detailed record of reproductive ecology for this species and we hope to provide a basis to improve our knowledge on the biology of this species and other glass frogs.