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Posthatching Parental Care in Salamanders Revealed by Infrared Video Surveillance
Abstract
Posthatching parental care is known in amphibians for frogs and caecilians but, thus far, has never been reported for salamanders. Here, we describe the parental behavior of a female Northwest Italian Cave Salamander, Speleomantes strinatii, from egg deposition to nest site abandonment. The female was kept in seminatural conditions and filmed in complete darkness by an infrared video camera. In November 2007, the female laid nine eggs in a small depression of the terrarium floor, displaced the clutch with hind limbs, and showed antipredator behaviors toward a conspecific female and an intruding Roof Rat (Rattus rattus). During egg brooding, the female remained in contact with the clutch for about 98% of the time. In September 2008, two young hatched and shared the nesting site for six weeks with the female, which attended the nesting site for 87% of the time. Hatchlings repeatedly climbed over the female's body, lying on her for hours. The female walked out of the nesting site with a young on its back twice. These prolonged skin contacts between parent and offspring should be considered as the first certain case of young attendance in salamanders. This behavior may be related to increased survival of hatchlings during their first weeks of life, when young are particularly vulnerable to predation, skin infection, and dehydration.
... It can be either passive or active; for example, female rhacophorid frogs either passively shield their eggs with their body or actively attack egg predators (Poo et al. 2016). Similarly, European lungless salamanders actively bite cannibalistic conspecifics to defend their eggs and also passively coil around their eggs when predators approach, even much larger predators such as rats (Oneto et al. 2010). In poison frogs, eggs might even be cannibalized by male or female conspecifics if not attended by parents , Spring et al. 2019. ...
... In some leptodactylid frogs, females stay with their tadpoles after they hatch in shallow waters and actively defend them against predators (Rodrigues et al. 2011). Also, female European lungless salamanders remain with their hatchlings for several weeks at the nesting site (Oneto et al. 2010). ...
Parenting is considered a key evolutionary innovation that contributed to the diversification and expansion of vertebrates. However, we know little about how such diversity evolved. Amphibians are an ideal group in which to identify the ecological factors that have facilitated or constrained the evolution of different forms of parental care. Among, but also within, the three amphibian orders—Anura, Caudata, and Gymnophiona—there is a high level of variation in habitat use, fertilization mode, mating systems, and parental sex roles. Recent work using broad phylogenetic, experimental, and physiological approaches has helped to uncover the factors that have selected for the evolution of care and transitions between different forms of parenting. Here, we highlight the exceptional diversity of amphibian parental care, emphasize the unique opportunities this group offers for addressing key questions about the evolution of parenting, and give insights into promising novel directions of research.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 54 is November 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... Therefore, this species can be defined as a troglophile sensu Mammola (2019). Females lay clutches containing 8-13 eggs on the humid soil or in rock crevices and actively defend their clutches (e.g., Oneto et al. 2010). ...
Long-term effects of current climate on animal populations living in subterranean habitats are still poorly understood. In this study, we analyzed the variability of the demographic structure and abundance of a population of terrestrial plethodontid Strinati's Cave Salamanders (Speleomantes strinatii) (Aellen, 1958) living inside a northwestern Italian artificial cave over 27 yr from 1996 to 2022. The study site is situated in the Northern Apennines, where average air temperatures measured at two local weather stations were steadily increasing, whereas precipitation was relatively constant over the past 60 yr. Our objective was to evaluate whether the demographic traits of the population of Strinati's Cave Salamanders were showing detectable signs of directional shift during the 27 yr. Each year in July, the population abundance was estimated by a three-occasion removal experiment, salamanders' snout-vent length (SVL) was measured, and the population polymodal body-size distribution was decomposed into estimated age classes. The annual population abundance, adult sex ratio, recruitment, SVL, and growth increments of first-and second-year immature salamanders were analyzed. The Strinati's Cave Salamander time series was modeled by autoregressive moving average (ARMA) analysis, and demographic parameters were tested for temporal trends. There were no directional trends observed in any of the demographic parameters of the focal cave salamander population over the study period. The best autoregressive model describing the population variation was an ARMA (2,1). Results indicated that the salamander population had a complex fluctuating pattern in which the interaction of lagged density dependence and an external autocorrelated factor were influencing the population long-term dynamics. Our findings suggest that the population of this long-lived salamander species was probably buffered from external conditions by the thermal inertia of its subterranean habitat that is known to delay and reduce the amplitude of aboveground climatic signals.
... Therefore, this species can be defined as a troglophile sensu Mammola (2019). Females lay clutches containing 8-13 eggs on the humid soil or in rock crevices and actively defend their clutches (e.g., Oneto et al. 2010). ...
... Using a facility provided by a semi-natural laboratory, some researchers were able to study female parental care in S. strinatii. Researchers observed an active protection of the mothers of both their eggs and newborns [51]. Future studies aiming to deepen research on this topic should include more species and (hopefully) include wild observations, as individuals may change their behavior when translocated into different environments [52]. ...
Simple Summary
Recently, the study of amphibian behavioral ecology has received increased interest from ethologists and evolutionary biologists. In fact, plethodontid salamanders (family Plethodontidae) are often used as model organisms to better understand different aspects of behavioral adaptation. We reviewed the recent scientific literature published on the behavioral ecology of European cave salamanders belonging to the genus Speleomantes, to highlight recent advancements and possible future directions for successful research. We found that, in recent years, several aspects of Speleomantes behavior were investigated, such as trophic strategies and parental care, while others were neglected, in particular, chemical communication at the intraspecfic level. Finally, we propose European cave salamanders as useful models to understand the gradual adaptation of behaviors that facilitate the permanent colonization of subterranean habitats.
Abstract
There is a recent growing interest in the study of evolutionary and behavioral ecology of amphibians. Among salamanders, Plethodontidae is the most speciose family, with more than 500 species, while in Europe, there are only 8 species, all belonging to the genus Speleomantes. European plethodontids recently received increasing attention with regard to the study of their natural history, ecology and behavior; however, the lack of standardized data, especially for the latter, hampers comparative analysis with the species from the New World. We here synthetized the recent advances in Speleomantes behavioral ecology, considering as a starting point the comprehensive monography of Lanza and colleagues published in 2006. We identified the behavioral categories that were investigated the most, but we also highlighted knowledge gaps and provided directions for future studies. By reviewing the scientific literature published within the period 2006–2022, we observed a significant increase in the number of published articles on Speleomantes behavior, overall obtaining 36 articles. Behavioral studies on Speleomantes focused mainly on trophic behavior (42%), and on intraspecific behavior (33%), while studies on pheromonal communication and interspecific behavioral interactions were lacking. In addition, most of the studies were observational (83%), while the experimental method was rarely used. After providing a synthesis of the current knowledge, we suggest some relevant topics that need to be considered in future research on the behavioral ecology of European plethodontids, highlighting the importance of a more integrative approach in which both field observations and planned experiments are used.
... Juvenile attendance may occur in extremely rare cases 33 , however, as it is only a short extension of egg attendance, we did not denote it as a separate type of care. We considered attendance as absent where this is explicitly stated in the sources or when it is not referred to in otherwise detailed descriptions of the reproductive behaviour that included observations on courtship and data on clutch size and egg-laying substrate. ...
Complex parenting has been proposed to contribute to the evolutionary success of vertebrates. However, the evolutionary routes to complex parenting and the role of parenting in vertebrate diversity are still contentious. Although basal vertebrates provide clues to complex reproduction, these are often understudied. Using 181 species that represent all major lineages of an early vertebrate group, the salamanders and newts (Caudata, salamanders henceforth) here we show that fertilisation mode is tied to parental care: male-only care occurs in external fertilisers, whereas female-only care exclusively occurs in internal fertilisers. Importantly, internal fertilisation opens the way to terrestrial reproduction, because fertilised females are able to deposit their eggs on land, and with maternal care provision, the eggs could potentially develop outside the aquatic environment. Taken together, our results of a semi-aquatic early vertebrate group propose that the diversity and follow-up radiation of terrestrial vertebrates are inherently associated with a complex social behaviour, parenting.
... Speleomantes are fully terrestrial amphibians that live and reproduce exclusively in subaerial environments [15]. Courtship can occur all year round, while gravid females lay their eggs twice per year (beginning of spring or autumn) in hidden places where they provide prolonged parental care (≥4 months) until the hatchlings are ready to leave the nest [19][20][21][22]. The narrow microhabitat requirements and the k-selected reproductive strategy of these species make them deserving of special protection [18,23,24]. ...
Simple Summary
Studies on species’ trophic niches are essential to understand the characteristics of species’ ecology and life traits, as well as to improve conservation strategies. In the absence of competitors, species realize their trophic niche including in their diet the most profitable food resources. In the presence of competitors, species modify their preferences to reduce competition and maintain the highest benefits at the same time. In this study, we assessed the trophic niche of two species of salamanders coexisting in a forested area of Italy and evaluated which might be the mechanisms that these two species adopted to reduce competition. We found that the Italian cave salamander (Speleomantes italicus) mostly consumed flying prey with a hard cuticle, while the fire salamander (Salamandra salamandra) preferred worm-like and soft-bodied prey. In conclusion, we hypothesize that in our case, the two species of salamanders did not have to change their prey preference in order to avoid competition, but divergences in metabolism and behavioral traits likely worked as natural deterrent.
Abstract
The trophic niche of a species is one of the fundamental traits of species biology. The ideal trophic niche of a species is realized in the absence of interspecific competition, targeting the most profitable and easy-to-handle food resources. However, when a competitor is present, species adopt different strategies to reduce competition and promote coexistence. In this study, we assessed the potential mechanisms that allow the coexistence of two generalist salamanders: the Italian cave salamander (Speleomantes italicus) and the fire salamander (Salamandra salamandra). We surveyed, in April 2021, a forested area of Emilia-Romagna (Italy) during rainy nights. Analyzing the stomach contents of the captured individuals, we obtained information on the trophic niche of these two sympatric populations. Comparing our results with those of previous studies, we found that the two species did not modify their trophic niche, but that alternative mechanisms allowed their coexistence. Specifically, different prey preferences and predator metabolisms were likely the major factors allowing reduced competition between these two generalist predators.
... Furthermore, although observations in the wild are highly desirable for providing accurate quantitative estimates of natural history traits, they can be challenged by sample size limitations, especially in secretive species. Thus, observations in enclosures subject to natural environmental conditions may also prove useful, especially for recording large numbers of detailed observations in a controlled environment and allow-to some extent-researchers to control for confounding factors (Weygoldt, 1980;Gibson & Buley, 2004;Warkentin, Buckley & Metcalf, 2006a;Warkentin, Caldwell & McDaniel, 2006b;Oneto et al., 2010;Poo & Bickford, 2014;Salica, Vonesh & Warkentin, 2017;Spring et al., 2019). ...
In species with parental care behaviors, parents may adjust the intensity and duration of their care if fluctuation in factors such as environmental variables or body condition affects offspring survival. In the face of environmental changes, many egg-laying species remain with their clutch for extended periods if this behavioral adjustment provides tangible benefits to the offspring. However, the length of time parents stay with the offspring may also differ depending on the individual's body condition. In the glass frog family (Centrolenidae), several species exhibit long-term egg attendance in which they remain with their clutch for several days after oviposition takes place. For some of them, changes in environmental variables lead to increased parental care efforts. For the species in which parents remain with their offspring for a short period (less than 24 hours), it is less clear if this constitutes parenting behavior, and whether parents adjust their efforts as a function of environmental change or the parent's body condition remains unexplored. We studied a population of the Emerald Glass Frog, Espadarana prosoblepon, a species that exhibits a short period of quiescence after oviposition (less than three hours). Our study aimed to determine whether females alter the length of their post-oviposition quiescence period in response to changes in environmental variables (i.e., temperature, humidity, rainfall, and mean wind speed) or female body condition. Pairs in amplexus were captured in the field and transported to semi-natural enclosures to record the duration of post-oviposition quiescence using infrared cameras. Females' post-oviposition quiescence lasted an average of 67.4 ± 26.6 min (range = 22.7-158.3 min). We did not find a significant relationship between the duration of the post-oviposition quiescence and any of the environmental variables tested. Similarly, post-oviposition quiescence duration was not influenced by female body condition. Because the variation observed in the duration of post-oviposition quiescence was not related to changes in extrinsic (environmental) or intrinsic (body condition) factors, we found no evidence that females of E. prosoblepon modify their post-oviposition behavior in response to any of the variables examined in this study. Future research investigating the adaptive significance of the post-oviposition quiescence observed in this species is needed to understand how this behavior is related to parental care efforts.
... In frogs, egg attendance can last until tadpole emergence or even until the froglet stage (Oneto et al., 2010). A range of parental strategies are now well documented, with eggs and larvae guarded either exclusively by males (Noronha and Rodrigues, 2018;Garavito-David et al., 2020), by females (Sorokin and Steigerwald, 2018;Cassiano-Lima et al., 2020), or by both sexes (Brown et al., 2010). ...
... This is why observations obtained from studies in the laboratory must be carefully interpreted and preferably confirmed by in situ approaches(Blin et al., 2020). For example, by surveying seminatural replicas of the sheltered reproductive sites of Hydromantes salamanders (Amphibia: Plethodontidae) with infrared cameras,Oneto et al. (2010) were able to provide some of the first observational data on their complex reproductive behavior and parental care. Subsequent observations performed under natural conditions ...
• Caves and other subterranean habitats fulfill the requirements of experimental model systems to address general questions in ecology and evolution. Yet, the harsh working conditions of these environments and the uniqueness of the subterranean organisms have challenged most attempts to pursuit standardized research.
• Two main obstacles have synergistically hampered previous attempts. First, there is a habitat impediment related to the objective difficulties of exploring subterranean habitats and our inability to access the network of fissures that represents the elective habitat for the so-called “cave species.” Second, there is a biological impediment illustrated by the rarity of most subterranean species and their low physiological tolerance, often limiting sample size and complicating laboratory experiments.
• We explore the advantages and disadvantages of four general experimental setups (in situ, quasi in situ, ex situ, and in silico) in the light of habitat and biological impediments. We also discuss the potential of indirect approaches to research. Furthermore, using bibliometric data, we provide a quantitative overview of the model organisms that scientists have exploited in the study of subterranean life.
• Our over-arching goal is to promote caves as model systems where one can perform standardized scientific research. This is important not only to achieve an in-depth understanding of the functioning of subterranean ecosystems but also to fully exploit their long-discussed potential in addressing general scientific questions with implications beyond the boundaries of this discipline.
(1) Caves and other subterranean habitats fulfill the requirements of experimental model systems to address general questions in ecology and evolution. Yet, the harsh working conditions of these environments and the uniqueness of the subterranean organisms have challenged most attempts to pursuit standardized research
(2) Two main obstacles have synergistically hampered previous attempts. First, there is a habitat impediment related to the objective difficulties of exploring subterranean habitats and our inability to access the network of fissures that represent the elective habitat for the so-called “cave species.” Second, there is a biological impediment illustrated by the rarity of most subterranean species and their low physiological tolerance, often limiting sample size and complicating lab experiments.
(3) We explore the advantages and disadvantages of four general experimental setups (in-situ, quasi in-situ, ex-situ, and in-silico) in the light of habitat and biological impediments. We also discuss the potential of indirect approaches to research. Furthermore, using bibliometric data, we provide a quantitative overview of the model organisms that scientists have exploited in the study of subterranean life.
(4) Our over-arching goal is to promote caves as model systems where one can perform standardised scientific research. This is important not only to achieve an in-depth understanding of the functioning of subterranean ecosystems but also to fully exploit their long-discussed potential in addressing general scientific questions with implications beyond the boundaries of this discipline.
A review of systematics, taxonomy, genetics, biogeography and natural history of the genus Speleomantes Dubois, 1984 (Amphibia Caudata Plethodontidae).
Outside the American continent the family Plethodontidae includes only the south Korean Karsenia koreana Min,Yang, Bonett, Vieltes, Brandon et Wake, 2005, and the European genus Speleomantes Dubois, 1984, whose systematics and taxonomy have rather recently been object of a morphologic and genetic review, which allowed to recognize 3 continental species [S. strinatii (Aellen, 1958); S. ambrosii ambrosii (Lanza, 1955) and S. ambrosii bianchii Lanza, Cimmaruta, Forti, Bullini et Nascetti, 2005; S. italicus (Dunn, 1923)] and 4 Sardinian ones [ S. flavus (Stefani, 1969); S. supramontis (Lanza, Nascetti et Bullini, 1986); S. imperialis imperialis (Stefani, 1969) and S. imperialissarrabusensis Lanza, Leo, Forti, Cimmaruta, Caputo et Nascetti, 2001); S. genei (Temminck et Schlegel, 1838) with subsp A and subsp. B]. Until recently the knowledge of Speleomantes’ ecoethology has been widely lacunose and specific research on this topic started only in the nineties. The present paper summarizes the current knowledge onthe European plethodontid salamanders, genus Speleomantes. The authors deal with systematics, taxonomy, geographical and altitudinal distribution, genetics (two keys to species and subspecies are given: one based on morphology and geographical distribution, the other based on genetic characters), biogeography, ecology (habitats, herpetocoenosis, predators, parasites, food), ethology (feeding behaviour, activity, habitat use, displacement, antipredator adaptations, communication), reproduction (sexual dimorphism, gametogenesis, mating behaviour, oviparity, ovovi-viparity, parental cares), development, population dynamics, conservation (abundance, threats, conservation guidelines), as well as with research prospects. The quoted bibliography includes 565 titles. Key words: Amphibia, Plethodontidae, Speleomantes, systematics, taxonomy, keys, genetics, biogeography, biology,conservation, France, Italy.
Revisione della sistematica, tassonomia, genetica, biogeografia e storia naturale del genere Speleomantes Dubois, 1984 (Amphibia Caudata Plethodontidae). Al di fuori del continente americano la famiglia Plethodontidae conta solo la specie sud coreana Karsenia koreana Min, Yang, Bonett, Vieltes, Brandon et Wake, 2005, e il genere europeo Speleomantes Dubois, 1984, la cui sistematica e tassonomia, oggetto di una relativamente recente revisione su basi genetiche e morfologiche, ha portato a riconoscere 3 specie continentali [S. strinatii (Aellen, 1958); S. ambrosii ambrosii (Lanza, 1955) e S. ambrosii bianchii Lanza, Cimmaruta, Forti, Bullini et Nascetti, 2005; S. italicus (Dunn, 1923)] e 4 sarde [S. flavus (Stefani, 1969); S. supramontis (Lanza, Nascetti et Bullini, 1986); S. imperialis imperialis (Stefani, 1969) e S. imperialis sarrabusensis Lanza, Leo, Forti, Cimmaruta, Caputo et Nascetti, 2001); S. genei (Temminck et Schlegel, 1838) con le sottospecie A e B]. Sino a poco tempo fa le conoscenze sull’ecoetologia dello Speleomantes sono rimaste ampiamente lacunose e ricerche approfondite in proposito sono state avviate solo a partire dagli anni ‘90. Il presente contributo riassume le attuali conoscenze sui Pletodontidi europei del genere Speleomantes. Gli autori trattano sistematica, tassonomia, distribuzione geografica ed altitudinale, genetica (vengono fornite due chiavi per l’identificazione delle specie e sottospecie: una basata sulla morfologia e la distribuzione geografica, l’altra basata sulle caratteristiche genetiche), biogeografia, ecologia (habitat, erpetocenosi, predatori, parassiti, dieta), etologia (comportamento predatorio, attività, uso dell’habitat, spostamenti, adattamenti antipredatori, comunicazione), riproduzione (dimorfismo sessuale, gametogenesi, corteggiamento, oviparità, ovoviviparità e cure parentali), sviluppo, dinamica di popolazione, conservazione (abbondanza, minacce, linee guida per la conservazione) e prospettive di ricerca. La bibliografia citata comprende 565 titoli. Parole chiave: Amphibia, Plethodontidae, Speleomantes, sistematica, tassonomia, chiavi, genetica, biogeografia, biologia, conservazione, Francia, Italia.
(10) (PDF) A review of systematics, taxonomy, genetics, biogeography and natural history of the genus Speleomantes Dubois, 1984 (Amphibia Caudata Plethodontidae). Available from: https://www.researchgate.net/publication/292730134_A_review_of_systematics_taxonomy_genetics_biogeography_and_natural_history_of_the_genus_Speleomantes_Dubois_1984_Amphibia_Caudata_Plethodontidae [accessed Mar 09 2023].
Reviews the territorial behaviour of salamanders, with sections based on fundamental life history strategies: completely terrestrial; species that are terrestrial as adults but have complex life cycles (ie aquatic larvae); species with complex life cycles and predominantly semi-aquatic adults; and predominantly or completely aquatic species. After a brief discussion on salamander territoriality including sections on definitions and resource-area competition, frog territorality is covered, by way of comparison. -S.R.Harris
A Speleomantes ambrosii population living in an artificial tunnel in NW Italy was studied for two consecutive years. Activity on the walls varied cyclically in relation to seasonal temperatures and food abundance. The main food item was the trogloxenic dipteran Limonia nubeculosa, which accounted for more than 80% of the total ingested prey by volume. Juvenile cave salamanders had a broader trophic nich than adults. Oviposition and juvenile recruitment appeared to be seasonal. The spatial distribution inside the tunnel was related to microhabitat heterogeneity and particularly to the distance from the entrance. Juveniles were observed outside or close to the entrance more often than adults. Movement of adult salamanders were generally low and averaged 7 cm/day; some repeatedly recaptured individuals had a mean home range of 6 m2.
Gravid females frequently become associated with a potential nesting site well in advance of oviposition. During the reproductive season, females reduce their foraging and become generally less active. Nutritional intake is greatly reduced and results in a significant decrease in dry body weight as compared to male controls.
We conducted a comparative investigation of nest relocation and egg recognition by four species of streamside salamanders indigenous to eastern North America: Seepage Salamander (Desmognathus aeneus), Santeetlah Salamander (Desmognathus santeetlah), Ocoee Salamander (Desmognathus ocoee), and Northern Dusky Salamander (Desmognathus fuscus). Females of all four species were able to relocate their nest sites following displacement of 1 m. Upon return to a nest site following natural displacement, females must be able to recognize their eggs and, in some instances, choose between their own clutch and the unattended clutch of a conspecific. In two-choice behavioral tests, female salamanders of all four species moved randomly within the test chamber in the absence of eggs, but preferred their own eggs to a filter paper blank. One species, D. fuscus, exhibited a similar attraction to conspecific eggs suggesting that the presence of eggs, regardless of their origin, may stimulate maternal care in physiologically primed females. We found that egg discrimination is not as infallible as previously reported. All four species spent more time with their own eggs than they did with the eggs of a conspecific female; however, this trend was significant for D. ocoee only. Interspecific variation in egg discrimination is attributed to differential selection associated with the life history of individual species.