Egg attendance imposes costs on parents, including decreased food intake and increased mortality risks. By concentrating parental activities when egg prédation is greater and abiotic conditions are ...less stressful, parents may decrease these costs. Here, we quantify the costs and benefits of temporary egg desertion in the frog Thoropa taophora, whose males care for eggs on rocky shores. We tested hypotheses on the effect of the period of the day (day vs. night) and breeding site (exposed vs. protected from sunlight) on the frequency of temporary desertion, water loss, and egg prédation. Using naturalistic observations, we show that parental males deserted their clutches more often during daytime and in exposed sites. Using a field experiment with agar models simulating adult males, we show that water loss was greater during daytime and in exposed sites. Finally, using field observations and a male removal experiment, we show that male presence improves egg survival and that egg predation was higher during the night, with no effect of breeding site. Because the main egg predators are conspecifics, which are mostly inactive when parental males are not attending their clutches, the costs of temporary desertion in terms of egg loss are relatively low when compared with the benefits related to decreased exposure of parental males to stressful abiotic conditions. In conclusion, we predict that temporary offspring desertion should be found especially among ectotherms, when periods of harsher environmental abiotic conditions for the parents are coincident with periods of low offspring demand for protection against predators.
Abstract
Semiterrestrial tadpoles live on wet rock surfaces and have evolved independently in at least seven anuran families. They have a flat venter, laterally compressed keratinized jaws and ...elongated, largely finless tails. When threatened, they can jump. Here, we describe the kinematics of locomotion for semiterrestrial tadpoles of the genera Cycloramphus and Thoropa (Cycloramphidae). Forward locomotion can be accomplished solely by the upper jaw cyclically engaging and disengaging from the substrate. Undulating tail movements, in contrast, cause the tadpoles to move laterally, like sidewinding snakes, rather than forwards. Jumping is an explosive escape behaviour with an unpredictable trajectory. Jumping requires rapid elevation of the head and extension of the torso and tail. This is made possible by epaxial musculature that extends onto the cranium and movement of the tail in the sagittal plane. Tadpoles near metamorphosis extend their hindlimbs symmetrically when jumping, even when the limbs are too small to provide thrust. The rapid rostral elevation of the snout, extension of the trunk and symmetrical extension of the hindlimbs is a kinematic pattern shared with post-metamorphic frogs when they jump. This suggests that semiterrestrial tadpoles use essentially the same neural programme as that used by frogs to jump.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, UILJ, UKNU, UL, UM, UPUK
Climatic oscillations throughout the Pleistocene combined with geological and topographic complexity resulted in extreme habitat heterogeneity along the Atlantic coast of Brazil. Inferring how these ...historic landscape patterns have structured the current diversity of the region's biota is important both for our understanding of the factors promoting diversification, as well as the conservation of this biodiversity hotspot. Here we evaluate potential historical scenarios of diversification in the Atlantic Coastal Forest of Brazil by investigating the population genetic structure of a frog endemic to the region. Using mitochondrial and nuclear sequences, we generated a Bayesian population-level phylogeny of the Thoropa miliaris species complex. We found deep genetic divergences among five geographically distinct clades. Southern clades were monophyletic and nested within paraphyletic northern clades. Analyses of historical demographic patterns suggest an overall north to south population expansion, likely associated with regional differences in habitat stability during the Pliocene and early Pleistocene. However, genetic structure among southern populations is less pronounced and likely represents more recent vicariant events resulting from Holocenic sea-level oscillations. Our analyses corroborate that the Atlantic Coastal Forest has been a biogeographically dynamic landscape and suggest that the high diversity of its fauna and flora resulted from a combination of climatic and geologic events from the Pliocene to the present.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
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•A new molecular phylogeny for species in the genus Thoropa is presented.•Thoropa species show deep divergences, beginning in the Oligocene and continuing until the Pleistocene.•The ...phylogeny for this genus shows 12 deeply divergent lineages across the four species analyzed.•The species Thoropa miliaris was paraphyletic with respect to Thoropa taophora.•A single sample of Thoropa lutzi included in the study calls into question the monophyly of the genus Thoropa.
The Brazilian Atlantic coastal forest is one of the most heterogeneous morphoclimatic domains on earth and is thus an excellent region in which to examine the role that habitat heterogeneity plays in shaping diversification of lineages and species. Here we present a molecular phylogeny of the rock frogs of the genus Thoropa Cope, 1865, native to the Atlantic forest and extending to adjacent campo rupestre of Brazil. The goal of this study is to reconstruct the evolutionary history of the genus using multilocus molecular phylogenetic analyses. Our topology reveals 12 highly supported lineages among the four nominal species included in the study. Species T. saxatilis and T. megatympanum are monophyletic. Thoropa taophora is also monophyletic, but nested within T. miliaris. Populations of T. miliaris cluster in five geographically distinct lineages, with low support for relationships among them. Although all 12 lineages are geographically structured, some T. miliaris lineages have syntopic distributions with others, likely reflecting a secondary contact zone between divergent lineages. We discuss a biogeographic scenario that best explains the order of divergence and the distribution of species in Atlantic forest and adjacent areas, and outline the implications of our findings for the taxonomy of Thoropa.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK, ZRSKP
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•Thoropa miliaris is monophyletic and the sister taxon to T. taophora.•Thoropa miliaris harbors at least seven evolutionarily independent lineages.•Four of the seven lineages of ...Thoropa miliaris show some genetic admixture.•The eight lineages of Thoropa miliaris + T. taophora complex have little ongoing gene flow in sympatry.•Divergences occurred mostly in Pliocene-Pleistocene.
Species delimitation can be challenging and affected by subjectivity. Sibling lineages that occur in sympatry constitute good candidates for species delimitation regardless of the adopted species concept. The Thoropa miliaris + T. taophora species complex exhibits high genetic diversity distributed in several lineages that occur sympatrically in the southeastern Atlantic Forest of Brazil. We used 414 loci obtained by anchored hybrid enrichment to characterize genetic variation in the Thoropa miliaris species group (T. saxatilis, T megatympanum, T. miliaris, and T. taophora), combining assignment analyses with traditional and coalescent phylogeny reconstruction. We also investigated evolutionary independence in co-occurring lineages by estimating gene flow, and validated lineages under the multispecies coalescent. We recovered most previously described lineages as unique populations in assignment analyses; exceptions include two lineages within T. miliaris that are further substructured, and the merging of all T. taophora lineages. We found very low probabilities of gene flow between sympatric lineages, suggesting independent evolution. Species tree inferences and species delimitation yielded resolved relationships and indicate that all lineages constitute putative species that diverged during the Pliocene and Pleistocene, later than previously estimated.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK, ZRSKP
Two of the most fundamental questions in tadpole biology, also applicable to most small, under‐studied organisms are: (1) ‘Why are they built the way they are?’ and (2) ‘Why do they live where they ...do?’ Regrettably, despite significant progress in most aspects of tadpole biology, the answers to these questions are not much better now than they were in the last century. We propose that an autecological approach, that is the careful observation of individuals and how they interact with the environment, is a potential path towards a fuller understanding of tadpole ecomorphology and evolution. We also discuss why more attention should be given to studying atypical tadpoles from atypical environments, such as torrential streams, water‐filled cavities of terrestrial plants and wet rock surfaces neighbouring streams. Granted, tadpoles are rare in these settings, but in those unusual habitats the physical environments can be well described and characterized. In contrast, the more common ponds where tadpoles are found are typically too structurally complex to be easily delineated. This makes it difficult to know exactly what individual tadpoles are doing and what environmental parameters they are responding to. Our overall thesis is that to understand tadpoles we must see exactly what they are doing, where they are doing it, and how they are doing it. This takes work, but we suggest it is feasible and could greatly advance our understanding of how anuran larvae have evolved. The same strategies for studying tadpoles that we encourage here can be applied to the study of many other small and fast‐moving animals.
中文摘要
为什么蝌蚪拥有自己独特的形态以及它们怎样适应不同的生境，是蝌蚪生物学的两个基本问题。尽管我们对蝌蚪的研究在过去几十年中获得了长足进步，但对这些问题仍需更加深入的理解。在此文中，我们建议基于个体生态学，对蝌蚪个体以及它们与环境的相互关系进行仔细观察和记录，从而全面地理解蝌蚪中不同生态型的演化。我们特别讨论了适应于非典型生境(例如，湍急的溪流、陆生植物的积水和溪流附近的潮湿表面)的蝌蚪，以及研究它们形态及功能特化的重要意义。基于对自然状态下的蝌蚪的观察和研究，可以有效推进我们对无尾类幼体多样性及演化的理解；类似策略也适用于对其他小型动物的研究。
Resumen
Dos de las preguntas más fundamentales en biología de renacuajos, también aplicables a la mayoría de los organismos pequeños y poco estudiados son: (1) ‘¿Por qué son construidos cómo son?’ y (2) ‘¿Por qué viven dónde viven?’ Lamentablemente, pese al significativo progreso en la mayoría de los aspectos de la biología de los renacuajos, las respuestas a esas preguntas no son mucho mejores ahora que en el siglo passado. Nosotros proponemos que un enfoque autoecológico, que es la observación cuidadosa de individuos y cómo ellos interactuam con el ambiente, es um camino potencial en la dirección de un entendimiento más completo de la ecomorfología y la evolución de los renacuajos. También discutimos por qué se debe prestar más atención al estudio de los renacuajos atípicos de ambientes atípicos, como los arroyos torrenciales, las cavidades de plantas terrestres llenas de água y las superficies rocosas húmedas cercanas a arroyos.Es cierto, renacuajos son raros en estas conformaciones, pero en esos hábitats inusuales el ambiente físico puede ser bien descrito y caracterizado. Al contrario, los estanques más comunes de encontrar renacuajos son tipicamente muy complejos estructuralmente para seren facilmente delineados. Eso dificulta saber exactamente qué los renacuajos individuales están haciendo y qué parâmetros ambientales ellos están respondiendo. Nuestra tesis general es que para comprender los renacuajos necesitamos ver exactamente lo que ellos están haciendo, dónde lo están haciendo, y cómo lo están haciendo. Eso requiere trabajo, pero sugerimos que es factible y puede mejorar nuestro entendimiento de cómo las larvas de anuros evolucionaron. Las mismas estratégias para estudiar renacuajos que estamos alentando aquí pueden ser aplicadas al estudio de muchos otros animales pequeños y rápidos.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
In Squamate reptiles, vitellogenesis in females is marked by an increase in the number and size of follicles, leading to an increase in aerobic metabolism to support the rising energy demand during ...reproductive activity. Male gametes are smaller than female gametes, and spermiogenesis requires less energy than vitellogenesis. This investigation compares the relationship between aerobic metabolism and reproductive effort in male and female viviparous Tomodon dorsatus snakes. We evaluated the influence of the males' and females' reproductive stages, along with the masses of follicles and testicles, on their aerobic metabolic rate. Our findings show that females have higher maintenance cost of pregnancy than metabolic costs of vitellogenesis. In males, we found no evidence of the reproductive effort influencing aerobic metabolic rates. In T. dorsatus, females have a long period of development and high fecundity. Therefore, the metabolic costs of vitellogenesis represent a critical component in the reproductive effort. On the other hand, males of T. dorsatus maintain a similar mass of gonads throughout the year with constant energy demand. These results reflect the difference in reproductive efforts between females and males of T. dorsatus.
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DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, SIK, UILJ, UKNU, UL, UM, UPUK
It is well known that environmental temperature influences several biological functions of ectotherms, notably in amphibians. The high permeability of anuran skin, associated with the effect of ...elevated environmental temperature, potentiates the dehydration process and this combination may restrict locomotor performance. Thoropa taophora is an endemic species from the Atlantic Rainforest whose tadpoles are semiterrestrial and predominantly diurnal, and are found in rocky seashores where they are exposed to sea spray and high temperatures. In this study we investigated how temperature and salinity conditions affect the locomotor performance in Thoropa taophora tadpoles. We also assessed how different osmotic concentrations affect the activity of the metabolic pathways that support muscle function. We measured the sprint speed of tadpoles of various sizes at different temperatures and salinities in the field. We also measured the activity of the enzymes pyruvate kinase (PK), lactate dehydrogenase (LDH) and citrate synthase (CS) in different temperatures and osmotic concentrations, and calculated the thermal sensitivity and the activity constants for each osmolality. Our results showed that, in general, sprint speed decreased with increasing temperature and salinity. However, whereas the effect of increased salinity was similar in smaller and larger tadpoles, increased temperature had a higher negative impact on sprint speed of larger tadpoles, thus indicating low thermal sensitivity of small tadpoles. PK and LDH thermal sensitivities and LDH constant of activity decreased as the osmolality increased. In conclusion, the locomotor capacity of tadpoles was decreased by temperature and salinity, which may be related to a decrease in anaerobic metabolism both in terms of sensitivity and total energy turnover through enzymatic activity. We discuss the ecological consequences, including the potential impacts on predator escape behavior promoted by changes in metabolism and locomotor performance in an early stage of development of this species.
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FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
We describe a new species of Physalaemus from central Brazil. It is characterized by the following combination of traits: medium-sized; snout subelliptical in dorsal view, varying between rounded and ...protruding in lateral view; head longer than wide; snout long; dorsolateral fold present; small inguinal gland associated with dark ocellus present; tarsal tubercle present; poorly developed tarsal fold present and supernumerary tubercles on feet absent. The advertisement call is a single note with eight harmonics lasting 0.7–1.0 s in duration and emitted at intervals of 0.6–5.8 s. The dominant frequency varies from 1.9 to 3.1 kHz. The occurrence of the new species is in open habitats (disturbed or preserved) in central Brazil.
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BFBNIB, IZUM, KILJ, NMLJ, NUK, PILJ, PNG, SAZU, UL, UM, UPUK
Polygynous mating systems with group fidelity are a common animal organization, typically consisting of multiple females in a mated group with a single male for an extended period (sometimes referred ...to as harem polygyny). Single-male polygyny with reproductive fidelity occurs in invertebrates, bony fishes, and some tetrapods, such as lizards, mammals, and birds. In amphibians, reproductive fidelity in polygynous groups is not fully demonstrated. Combining data on larval development, molecular paternity assignment, and in situ behavioral observations, we reveal high fidelity during a prolonged breeding season in a Neotropical polygynous frog. Males dominate scarce breeding sites, guarding offspring, and mating exclusively with multiple females that exhibit dominance rank. This system likely evolved in response to intense competition for breeding sites and intrasexual competition for mates.
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