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Costa, A.; Lunghi, E.; Rosa, G.; Salvidio, S. Behavioral Ecology of European Plethodontid Salamanders. Encyclopedia. Available online: https://encyclopedia.pub/entry/52334 (accessed on 21 December 2024).
Costa A, Lunghi E, Rosa G, Salvidio S. Behavioral Ecology of European Plethodontid Salamanders. Encyclopedia. Available at: https://encyclopedia.pub/entry/52334. Accessed December 21, 2024.
Costa, Andrea, Enrico Lunghi, Giacomo Rosa, Sebastiano Salvidio. "Behavioral Ecology of European Plethodontid Salamanders" Encyclopedia, https://encyclopedia.pub/entry/52334 (accessed December 21, 2024).
Costa, A., Lunghi, E., Rosa, G., & Salvidio, S. (2023, December 04). Behavioral Ecology of European Plethodontid Salamanders. In Encyclopedia. https://encyclopedia.pub/entry/52334
Costa, Andrea, et al. "Behavioral Ecology of European Plethodontid Salamanders." Encyclopedia. Web. 04 December, 2023.
Behavioral Ecology of European Plethodontid Salamanders
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This entry is adapted from the peer-reviewed paper 10.3390/ani13233667

Plethodontid salamanders (family Plethodontidae) are often used as model organisms to better understand different aspects of behavioral adaptation. This contributed to increase the interest from ethologists and evolutionary biologists regarding amphibian behavioral ecology. The recent advancements on the behavioral ecology of European cave salamanders belonging to the genus Speleomantes are presented herein. 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. Possible future directions for successful research should integrate field observations and planned experiments to understand those topics still uninvestigated (e.g., chemical communication and behavioral adaptation that facilitate the permanent colonization of subterranean habitats).

behavior comparative ethology experiments Plethodontidae salamanders Hydromantes Speleomantes

1. Introduction

The behavioral ecology of amphibians remains largely understudied [1][2], although there is growing interest in the study of ecological processes and adaptive behaviors that shape the evolutionary dynamics of amphibian species and populations [3]. Amphibians represent a highly diverse group that include species with different habitus (from fossorial to exclusively aquatic), different reproductive strategies (oviparous and ovoviviparous) and even individuals that revolutionize their shape through life (larva vs. adult form). According to the intrinsic features of the species, but also to the local environmental conditions, the behavior of amphibians may change dramatically. For examples, in species adopting an r reproductive strategy, eggs are produced and laid by females in mass, which are often externally fertilized. On the other hand, in K-selected species, parents may spend substantial time taking care of their eggs and newborns, actively fighting against potential predators, driving them to a safer environment, or even feeding their brood [4]. The evolution of parental care in amphibians indeed seems to have played an important role for their colonization of different habitats. Looking at bi-phasic species, the behaviors of aquatic larvae can be completely different from those adopted by terrestrial adults. It is, therefore, quite complicated to standardize and compare amphibians’ behavior, unless specific groups with a similar ecology and life traits are considered.
Among Urodela, the family Plethodontidae (Gray, 1850) is the most speciose [4]. This family comprises more than 500 species out of 800 worldwide salamander and newt species, of which the overwhelming majority is found in Northern, Central and Southern America, while there are just 8 species in Europe and only 1 in Asia [4][5][6]. Plethodontids are characterized by the absence of lungs at the adult stage, and by the presence of naso-labial grooves that connect the upper lip to the external naris [4]. The main function of these peculiar structures is to canalize chemicals towards the olfactory structures [7][8].The wide diversity and the high local abundances that New World Plethodontids can reach make them relevant nodes within local ecological webs, where functional guilds are composed of many different interacting species [9][10][11][12]. Indeed, epigean plethodontids are predators which often occupy an intermediate position in the local food web, meaning that they hold the critical role of being prey and predators at the same time. Many species of New World plethodontids occur sympatrically, a condition that allowed several studies on species habitat selection and competition to be performed. Plethodontid salamanders have been even used as proxy for biodiversity assessments and monitoring in North American forests, cases that further highlight the importance of this group of amphibians and the need to deepen our knowledge on their biology and life traits [3].
On the other hand, the discovery of the Old World plethodontid species is relatively recent, and studies on their ecology and behavior lagged behind compared to their American relatives. Some not exclusive causes may contribute to this knowledge gap. Asian and European plethodontid species usually do not occur in sympatry, preventing the completion of studies on competitive behaviors of species living sympatrically. To this purpose, syntopy between two European plethodontid species has been artificially created, but such unnatural conditions do not provide any substantial information for advancing our knowledge on their behavior. Furthermore, although eight species of European plethodontids are currently known, they have been historically considered equivalent in their biology and ecology, meaning that single-species studies were often translated to the whole genus (see [13] and references therein). Indeed, only recently has more emphasis been given on evaluating interspecific (or even intraspecific) divergences among European plethodontid species, emphasis that strongly contributed in raising the number of studies performed. Furthermore, European plethodontids usually occur in subterranean environments, habitats where prolonged studies and monitoring activities are more challenging compared to surface ones.
American plethodontids became one of the main amphibian model systems used to better understand ecological questions in amphibians such as interspecific competition, predation and hybridization. Starting from field observations, classical ecological manipulative experiments were carried out, initially in natural woodland habitats [14][15][16]. However, in natural settings, there are many external uncontrollable factors that may influence the observed outcomes. For these reasons, plethodontids are often tested in laboratories to facilitate the avoidance of external confounding factors, while simultaneously controlling biological variables such as age, sex or reproductive status [17][18][19].
In this context, the current understanding of the behavioral ecology of European plethodontids, known as European cave salamanders, remains poorly developed in comparison to American plethodontids. The eight European species belong to the genus Speleomantes Dubois, 1984, although they are sometimes referred to as Hydromantes [5][20][21]. However, the use of Speleomantes better highlights the phylogenetic independence of European plethodontids, which form a well-defined monophyletic group with a large genetic distance from the five Californian species of Hydromantes [22][23][24]. All European cave salamanders are fully terrestrial and usually inhabit habitats where specific microclimatic conditions (e.g., high humidity and relatively low temperature variations) occur, such as humid crevices, forest floor environments and natural or artificial subterranean habitats [13][25][26]. Historically, behavioral studies on European plethodontids were sporadic because zoologists were focusing mainly on species description at the morphological and genetical level [25][27].
The monography dedicated to the taxonomy, biogeography and ecology of European cave salamanders written by Lanza et al. [13] constitutes the main reference concerning the natural history, ecology and behavior of the genus Speleomantes. This monograph lists under the chapter “Ethology” four sub-sections: “Feeding behaviour”, “Activity, habitat use and displacement”, “Antipredatory adaptations” and “Communication”. Concerning “Feeding behaviour”, most of the studies dealt with the anatomical structure of the eye [28] and of the tongue [29][30]. This sub-section summarizes the extraordinary tongue protrusion capability of Speleomantes and the ability to capture static prey in complete darkness [31][32]. Finally, the trophic strategy of Speleomantes is described as an “ambush strategy”, although this assertion seems based more on sporadic observations than on robust evidence [13]. The second sub-section, “Activity, habitat use and displacement”, relates exclusively to the species’ auto-ecological requirements, such as habitat features and seasonal activity, with little connection to behavior ecology sensu [3]. The third sub-section, “Antipredatory adaptations”, describes the presence of yellow-reddish or ochre dorsal colorations and the production of toxic skin secretion observed in many Speleomantes individuals and populations [13]. Finally, in the fourth sub-section, “Communication”, the presence of chemical intraspecific interactions was inferred from anatomical and histological studies on mating glands, but without providing any experimental evidence of their use during courtship and mating. In any case, the typical “nose tapping” behavior of plethodontids was reported in S. strinatii, suggesting that this specific behavior related to chemical communication is present [33]. Consequently, the relative paucity of the literature on European cave salamanders’ behavior does not allow robust comparative studies with American plethodontids [3][34][35].

2. Advances in the Behavioral Ecology of European Plethodontid Salamanders

Despite the increasing number of peer-reviewed papers published since the review of Lanza et al. [13], the behavioral ecology of European plethodontids belonging to the genus Speleomantes remains poorly known.
Recent research interests were focusing on three main topics in particular, related to foraging tactics, intraspecific social behavior (but the majority of papers were dealing with clutch guarding and parental care rather than on interactions among free-living conspecifics) and with predators or parasites. Foraging ecology is very relevant when assessing the role of salamanders as top predators on invertebrate communities that inhabit the superficial soil stratum [3]. Therefore, the dietary habits and feeding behavior of all eight species of Speleomantes were investigated at least once. Researchers mostly explored the trophic spectrum of Speleomantes with the analysis of stomach contents, identifying diet composition in multiple conspecific populations and assessing how seasonality contributes to defining the type and amount of consumed prey [36][37]. In some instances, assessments of individuals’ food specialization were also performed [19][38]. On the other hand, many other aspects of Speleomantes foraging behavior are still unexplored or just hypothesized [39]. For example, we still do not know which foraging strategies these species adopt, or where they forage the most. Furthermore, do Speleomantes show prey preferences? Studies of gut contents were usually not supported by analyses aiming to quantify the local trophic supply, but see [40][41], making research topics related to individuals’ prey preferences virtually unexplored in many species. To date, all trophic ecology studies were performed using a stomach flushing technique on live individuals, a relatively simple technique that has been often performed in the field on different species of salamanders [40], while stable isotopes or DNA barcoding are rarely used [42].
Most of the studies regarding predation and parasitism on Speleomantes deal with the observations of these events in both epigean and ipogean environments. Consequently, the knowledge regarding this topic is still lacking (e.g., potential predators and predation avoidance) and more experimental studies should be carried out to explore the subject.
The second most explored research topic was related to reproductive behavior and parental care. Considering the cryptic behavior of Speleomantes, especially when they reproduce, the discovery of some nests in the wild is of high importance to comprehend their reproductive behavior, although it is limited to some species and mostly concentrated in the spring–summer period [43][44]. Indeed, most of the available information identifies the beginning of spring as the time in which females usually lay eggs, which are then protected until they hatch at the end of summer [45]. Different is the case of parental care. 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 [46]. 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 [47].
The lack of interspecific behavioral studies may be due to the allopatric distribution characterizing the genus Speleomantes. This condition does not occur in only two narrow contact zones of mainland Italy, where, inter alia, hybridization between species is present [48][49]. In the past, a couple of experiments involving the creation of artificial sympatry of two mainland Speleomantes species were performed; their aim was to study their habitat selection and competition [50]. However, data from such unnatural conditions are not considered useful herein. In addition, only two other terrestrial salamanders are found in sympatry with one Speleomantes species at a time, i.e., the fire salamander Salamandra salamandra and the Northern spectacled salamander Salamandrina perspicillata [13]. Such co-occurrence is mostly realized in epigean environments (e.g., in forested areas), although both species can occasionally exploit subterranean environments [51][52]. A few studies performed on this system provided the first information related to the potential mechanisms (e.g., temporal and trophic niche partitioning) that these species adopt to avoid competition [53][54]. However, more natural observations and experimental tests are needed to shed light on this topic.
The behavioral trait for which our knowledge is the poorest is Speleomantes communication and social interactions at an intraspecific level. We still have uncertainty on the nature of intraspecific interactions between individuals. Some authors highlighted the potential occurrence of agonistic interactions between age classes [55] within subterranean environments, while some others found no evidence of such behavior [56]. The single study performed on surface population does not report any evidence of agonistic interactions [57].
New World plethodontids are currently used as laboratory models for experimental studies on comparative and adaptive behavior [3]. Characteristics promoting the use of plethodontids as model species are their easy maintenance, survival and breeding in animal research facilities [3]. In controlled environments, selected individuals can be exposed to experimental conditions to test for multiple hypotheses. In fact, the experimental hypothesis-testing approach seems very informative in the study of behavioral ecology, since it allows researchers to infer causality [3][17][18]. Although, caveats should be always considered when extrapolating results observed in simplified, and possibly stressing, settings compared to natural habitats [19]. This type of approach was performed mostly on the continental species S. strinatii, with only one exception concerning S. italicus. However, similarly to many New World plethodontids, Speleomantes are medium-sized terrestrial salamanders that can be easily hosted in the laboratory within terraria or small containers for relatively long periods of time. However, reproducing a suitable microhabitat for these species may be not trivial. In fact, due to their strictly cutaneous respiration, European plethodontids are highly dependent on microclimatic conditions, which should be characterized by high air relative humidity, and air temperatures usually lower than 18 °C [26]. Therefore, maintaining these environmental features within such ranges would assure animal welfare. These environmental conditions can be reproduced only in laboratory cold rooms or in natural or artificial subterranean habitats, thus limiting the experimental approach, as we, in fact, observed. Based on the analysis of the recent published research on European cave salamanders, researchers propose a preliminary list of possible topics for future research (Table 1).
Table 1. Suggested topics for future research on European cave salamanders species.
Behavioral Category Behavioral Ecology Question Suggested Focal Species Suggested Experimental
Approach
Intraspecific social
behavior, courtship,
mating and parental care;
Pheromonal glands and pheromonal
communication		 Do individuals communicate through tactile, visual or chemical signals? All species Experiments/observations in controlled conditions
Intraspecific social behavior, courtship, mating, and parental care;
Pheromonal glands and pheromonal communication		 How is mate selection made? All species Experiments/observations in controlled conditions
Intraspecific social behavior, courtship, mating, and parental care How different species/populations adjust their behavior depending on habitat features? All species Experiments/observations in controlled conditions or in the wild
Intraspecific social behavior, courtship, mating, and parental care Is the behavior of hybrid individuals related to that of a parent? S. ambrosii,
S. italicus, S. strinatii and their hybrids		 Experiments in controlled conditions of genetically identified individuals
Cognitive ecology and personality Are space use, displacement patterns and overall fitness linked to individual behavioral traits? All species Capture-mark-recapture study in the wild
Cognitive ecology and personality How individuals modify their behavior after environmental or social experiences? All species Controlled conditions in outdoor mesocosms
Interspecific territoriality How interspecific coexistence shapes resource use or activity patterns? S. ambrosii;
S. italicus;
S. strinatii		 Controlled conditions as laboratory settings or outdoor mesocosms

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Enrico Lunghi
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Sebastiano Salvidio
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