Conference PaperPDF Available

Nuovi dati sul comportamento di cura parentale nei Caudati: Hydromantes (Speleomantes) strinatii (Amphibia, Plethodontidae)

Authors:
  • CESBIN Srl
  • Agenzia Regionale per la Protezione dell'Ambiente Ligure
  • Gruppo Speleologico Ligure "Arturo Issel" -Busalla

Abstract and Figures

New data about parental care behaviour in Caudata: Hydromantes (Speleomantes) strinatii (Amphibia, Plethodontidae). In Hydromantes (Speleomantes) strinatii the egg guarding female shows a complex array of parental behaviours such as clutch displacement and active defence. Moreover, recent observations demonstrated that the female also displays post-hatching parental cares consisting in prolonged skin contacts with newborns, that last about 40 days. In 2011, an experiment was performed to test the existence of other types of post-hatching parental behaviours of the female towards its young. These experiments were performed inside the Biospeleological Station of Besolagno (GE), in complete darkness, and were recorded by means of an infrared video camera. Two adults male cave salamanders were introduced inside a terrarium in which two females were guarding a group of eight and nine hatchlings, respectively. In all cases, the approaching male elicited an aggressive behaviour of the female that intercepted and repelled the intruder by physical contacts, head pushes and bites. After these aggressive bouts, both females always re-established skin contacts with their young. These are the first experimental observations in salamanders of an active anti predatory behaviour of the female parent to protect hatchlings. Nei Caudati le cure parentali prima della schiusa sono ben documentate e comprendono vari tipi di sorveglianza (Forester, 1984; Austin, 2000) e di difesa delle uova contro eventuali predatori (Nussbaum, 2003; Wells, 2007). Per quanto riguarda il comportamento parentale dopo la schiusa, i dati sono invece piuttosto scarsi e a volte aneddotici. Ad esempio, nel genere americano Desmognathus è noto che la femmina staziona in vicinanza dei neonati appena schiusi per circa quattro settimane, ma non si conoscono le relazioni che essa stabilisce coi neonati (Mathis et al., 1995). Nel geotritone di Strinati Hydromantes (Speleomantes) strinatii le cure parentali della femmina dopo la deposizione delle uova sono complesse e sono state descritte per la prima volta da Durand
Content may be subject to copyright.
Scillitani G., Liuzzi C., Lorusso L., Mastropasqua F., Ventrella P. (curatori), 2013.
Atti IX Congresso Nazionale della Societas Herpetologica Italica
(Bari - Conversano, 26-30 settembre 2012). Pineta, Conversano (BA).
ISBN 9 78-88-908-7160-3
Nuovi dati sul comportamento di cura parentale nei Caudati:
Hydromantes (Speleomantes) strinatii (Amphibia,
Plethodontidae)
FABRIZIO ONETO1,2, DARIO OTTONELLO2,3, MAURO V. PASTORINO1, SEBASTIANO
SALVIDIO1,2
1 Gruppo Speleologico Ligure “A. Issel”, Villa Comunale ex Borsino, 16012 Busalla (GE).
2 DISTAV, Università degli Studi di Genova, corso Europa 26, 16132 Genova.
3 Autore per la corrispondenza: E-mail: dario.ottonello@studionatura.net
Abstract. New data about parental care behaviour in Caudata: Hydromantes
(Speleomantes) strinatii (Amphibia, Plethodontidae). In Hydromantes (Speleomantes)
strinatii the egg guarding female shows a complex array of parental behaviours such as
clutch displacement and active defence. Moreover, recent observations demonstrated
that the female also displays post-hatching parental cares consisting in prolonged skin
contacts with newborns, that last about 40 days. In 2011, an experiment was performed
to test the existence of other types of post-hatching parental behaviours of the female
towards its young. These experiments were performed inside the Biospeleological
Station of Besolagno (GE), in complete darkness, and were recorded by means of an
infrared video camera. Two adults male cave salamanders were introduced inside a
terrarium in which two females were guarding a group of eight and nine hatchlings,
respectively. In all cases, the approaching male elicited an aggressive behaviour of the
female that intercepted and repelled the intruder by physical contacts, head pushes and
bites. After these aggressive bouts, both females always re-established skin contacts
with their young. These are the first experimental observations in salamanders of an
active anti predatory behaviour of the female parent to protect hatchlings.
Keywords. Plethodontid salamanders, post-hatching parental cares, IR video
recording
Nei Caudati le cure parentali prima della schiusa sono ben documentate e
comprendono vari tipi di sorveglianza (Forester, 1984; Austin, 2000) e di difesa delle uova
contro eventuali predatori (Nussbaum, 2003; Wells, 2007). Per quanto riguarda il
comportamento parentale dopo la schiusa, i dati sono invece piuttosto scarsi e a volte
aneddotici. Ad esempio, nel genere americano Desmognathus è noto che la femmina
staziona in vicinanza dei neonati appena schiusi per circa quattro settimane, ma non si
conoscono le relazioni che essa stabilisce coi neonati (Mathis et al., 1995). Nel geotritone di
Strinati Hydromantes (Speleomantes) strinatii le cure parentali della femmina dopo la
deposizione delle uova sono complesse e sono state descritte per la prima volta da Durand
Nuovi dati sul comportamento di cura parentale di Hydromantes (Speleomantes) strinatii
205
(1967, 1970). Recentemente l’uso di una videocamera a raggi infrarossi (IR) ha permesso di
descrivere e analizzare in dettaglio anche il comportamento di una femmina verso i suoi
due neonati dopo la schiusa (Oneto et al., 2010). In questo caso, femmina e neonati hanno
stabilito e mantenuto ripetuti contatti fisici fino all’abbandono del sito da parte dei piccoli,
40 giorni dopo la nascita. In questo studio sono stati registrati i comportamenti parentali di
altre due femmine di H. strinatii, con lo scopo di confermare le precedenti osservazioni di
Oneto et al. (2010) e di ottenere ulteriori dati sull’etologia della specie. In particolare sono
stati condotti esperimenti al fine di testare la presenza di un comportamento protettivo delle
femmine contro eventuali predatori dei neonati.
Le registrazioni sono state effettuate nella Stazione Biospeleologica di Besolagno
(Savignone, Genova), allestita dal Gruppo Speleologico Ligure “A. Issel” per studiare
l’etologia e l’ecologia dei geotritoni in condizioni semi-naturali (Salvidio et al., 1994). La
strumentazione consisteva in un sistema di videosorveglianza equipaggiata con sensore
ottico e illuminatore a led infrarossi in grado di registrare, in condizioni di totale assenza di
disturbo luminoso e in continuo, il comportamento dei geotritoni. Due femmine (A e B)
apparentemente gravide sono state immesse e stabulate in un ampio terrario aperto
(dimensioni: 70 x 50 x 30 cm) nel mese di novembre 2010. I bordi superiori del terrario
sono ripiegati a U al fine di ridurre la possibilità di fuga degli animali. La registrazione
delle immagini ha avuto inizio con la schiusa delle uova dopo circa 11 mesi di sviluppo,
nella prima metà di ottobre 2011, ed è proseguita fino alla dispersione dei nuclei familiari
avvenuta dopo circa 40 giorni. In totale sono state effettuate 840 ore di registrazione che
hanno permesso di ricostruire le relazioni e i comportamenti che si stabiliscono tra madre e
neonati.
In questo caso, tutte le uova deposte sono giunte alla schiusa, per un totale di otto
neonati per la femmina A e nove per la femmina B. L’analisi delle immagini registrate ha
permesso di confermare innanzitutto le precedenti osservazioni che erano state condotte
però su una sola femmina (Oneto et al., 2010):
1. i neonati e la madre mantengono contatti fisici che durano alcune ore per circa 35
giorni dopo la schiusa (Figura 1);
2. i neonati dopo pochi giorni dalla schiusa aumentano gradualmente la propria
mobilità e si allontanano dalla madre, facendo tuttavia sempre ritorno in
prossimità del sito di schiusa dove staziona la madre;
3. i neonati salgono spesso e permangono a lungo sul dorso della madre e, a volte
vengono trasportati passivamente per brevi tratti;
4. la madre lascia periodicamente e per un tempo variabile il sito di schiusa ma vi fa
sempre ritorno ristabilendo ogni volta il contatto fisico con i neonati.
Dopo circa dieci giorni dalla nascita è stata predisposta la seconda fase della
sperimentazione. Due esemplari maschi di geotritone di Strinati sono stati immessi nel
terrario al fine di registrare le loro eventuali interazioni con le femmine ed i neonati.
I geotritoni maschi hanno individuato in poco tempo le femmine, e più volte si sono
avvicinati ai gruppi familiari causando questi comportamenti in entrambe le femmine:
1. ciascuna femmina ha reagito solo alla presenza del maschio che giungeva in
prossimità dei propri neonati;
2. l’avvicinamento dell’intruso provocava in tutti i casi l’aumento della reattività
delle femmine che intercettavano e invitavano l’intruso ad allontanarsi, tramite
contatti e spinte della testa e anche morsi. Queste interazioni, in alcuni casi hanno
206
F. Oneto, D. Ottonello, M.V. Pastorino e S. Salvidio
Fig. 1. Interazione della femmina di Hydromantes (Speleomantes) strinatii coi neonati dopo la schiusa
(foto Renato Cottalasso).
portato a vere e proprie lotte che sono sempre terminate con l’allontanamento del
maschio/intruso;
3. dopo ogni atto aggressivo verso l’intruso, le femmine tornavano sempre verso i
propri neonati ristabilendo nuovamente il contatto fisico.
Queste osservazioni dimostrano l’utilità dell’uso di videocamere a IR, che non
disturbano gli animali, per la registrazione di comportamenti che si svolgono in ambienti
totalmente primi di luce. Inoltre, sono la prima testimonianza diretta di un comportamento
di difesa attiva dei neonati da parte delle femmine dei Plethodontidae e aprono interessanti
prospettive sullo studio e l’analisi dell’evoluzione del comportamento parentale dopo la
schiusa delle uova nei Caudati.
Le autorizzazioni alla cattura temporanea dei geotritoni sono stati rilasciati dal
Ministero dell’Ambiente e della Tutela del Territorio e del Mare (permesso DPN-2010-
0010807 valido per gli anni 2010-2012).
BIBLIOGRAFIA
Austin, R.M. jr. (2000): Cutaneous microbial flora and antibiosis in Plethodon ventralis.
Interferences for parental care in the Plethodontidae. In: The biology of plethodontid
salamanders, p. 127-136. Bruce, R.C., Jaeger, R.G., Houck L.D., Eds. Kluwer
Academic/Plenum Publishers, New York.
Durand, J.-P. (1967): Sur l’ontogenèse d’Hydromantes italicus strinatii Aellen (Urodèle,
Plethodontidae). C. R. Acad. Sci., Paris 265: 1533-1535.
Nuovi dati sul comportamento di cura parentale di Hydromantes (Speleomantes) strinatii
207
Durand, J.-P. (1970): Fortplanzung und Entwicklung von Hydromantes, dem Höhlenmolch.
Aqua Terra 7: 42-48.
Forester, D.C. (1984): Brooding behaviour by the mountain dusky salamander: can the
female’s presences reduce clutch dessication? Herpetologica 40: 105-109.
Mathis, A., Jaeger, R.G., Keen, W.H., Ducey P.K., Walls, S., Buchanan, B.W. (1995):
Aggression and territoriality by salamanders and a comparison with the territorial
behaviour of frogs. In: Amphibian Biology, 2, Social Behaviour., p. 633-676.
Heatwole, H., Sullivan, B.K., Eds., Surrey Beatty and Sons, Chipping Norton, NSW,
Australia.
Nussbaum, R.A. (2003): Parental care. In: Reproductive Biology and Phylogeny of
Urodela, p. 527-612. Sever, D.M., Ed., Science Publishers Inc., Enfield, New
Hampshire.
Oneto, F., Ottonello, D., Pastorino, M.V., Salvidio, S. (2008): Dati preliminari sul
comportamento di Speleomantes strinatii (Aellen, 1958) ottenuti con un sistema di
videocontrollo a raggi infrarossi. In: Biospeleologia dell’Appennino, studi e ricerche
su Anfibi e Invertebrati con particolare riferimento all’Appennino Umbro-
Marchigiano, pp 50-53. Fiacchini, D., Carotti, G, Fusco, G., Eds., Ostra Vetere
(AN).
Oneto, F., Ottonello, D., Pastorino, M.V., Salvidio, S. (2010): Post-hatching parental care
in salamanders revealed by infrared video surveillance. J. Herpetol. 44: 649-653.
Salvidio, S., Lattes, A., Tavano, M., Melodia, F., Pastorino, M.V. (1994): Ecology of a
Speleomantes ambrosii population inhabiting an artificial tunnel. Amph.- Rept. 15:
35-45
Wells, K. D. (2007): The Ecology and Behavior of Amphibians. University of Chicago
Press, Chicago.
... More recently, Papinuto (2005) observed one female H. genei with eggs in a shot hole of an abandoned mine and followed the egg development until hatching. For the other species, information on reproduction and subsequent parental care essentially refers to individuals maintained in terraria or under semi-natural conditions (reviewed in Lanza et al. 2006; see also Oneto et al. 2010Oneto et al. , 2013. ...
... A small hole may also increase the female's chances of successfully protecting her eggs (e.g., against predators, cannibalism, or through skin secretions that might protect eggs from fungi or bacteria; see Lanza et al. 2006, Oneto et al. 2010. A small crevice may allow mothers to keep their offspring safe during the first days after hatching, protecting them against predators like the orb-weaver spider Meta menardi, or from intraspecific aggression (Lanza et al. 2006, Oneto et al. 2013. While finding Hydromantes individuals in suitable caves is rather easy, nesting sites have been discovered only a few times, probably because of their specific geomorphological features that make detection extremely difficult. ...
... In H. flavus, during the first observation after hatching, several hatchlings were perched on the body of the female, without contact to the substrate (Fig. 2a). These behavioural expressions are in agreement with the published observations on H. strinatii (Oneto et al. 2010(Oneto et al. , 2013. In summary, our observations in wild conditions suggest similar nesting behaviours among Hydromantes species for multiple parameters, including the selection of nesting sites, hatching period, and the presence of parental care after hatching. ...
Article
Full-text available
The reproductive biology of European salamanders of the genus Hydromantes (subgenus Speleomantes) is poorly known. The lack of information is related to their cryptic behaviour and habitat, which make detection extremely difficult, especially during breeding-related activities. Most of the information on Hydromantes reproduction refers to observations in captivity and in semi-natural conditions, while observations in the wild are extremely limited. We report on the first observations of brooding and maternal care in Hydromantes italicus and H. flavus in natural environments. In both species, brooding females and eggs were found in small fissures within the aphotic zone of caves where microclimates are stable. After hatching, the females of both species attended continuously to their newborns. Available information on breeding biology suggests high similarity amongst species, but more studies, under both natural and controlled conditions, are required to better understand the complex breeding behaviour of Hydromantes salamanders and evaluate interspecific variation. © 2014 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany.
Article
Full-text available
During the dry season, the European Plethodontid salamanders (genus Hydromantes) usually occupy underground environments (i.e. caves), where they can find cold temperatures and high moisture. Hydromantes breed in hypogean environments, where they usually lay eggs in hidden shelters. Mothers perform a long-lasting parental care of the eggs, which also continues after hatching. Due to the cryptic habitat and behaviour, their breeding biology is poorly known. Most of the available data refer to observations in captivity, while data from wild populations are scarce and deal with the findings of single nests. Here we report the first study on the Imperial cave salamander H. imperialis nesting ecology and behaviour, by performing quantitative observations on multiple nests. We found four nests in a cave located in Central Sardinia. We monitored them through five months, recording environmental features. Nests were associated with cold, humid and dark sectors of the cave, but sectors with nests did not show greater climatic stability than the superficial ones. Nests were continuously attended by females; temporary desertion became more frequent when temperatures were high and it was later in the season. Newborns were attended by their mothers for up to 52 days after hatching. The comparison of breeding biology across multiple Hydromantes species suggests earlier hatch in population/species living in warmer areas, with similar post-hatch brood attendance among species.
Article
Full-text available
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
Article
Full-text available
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.
Article
Full-text available
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.
Article
The Desmognathus ochrophaeus female decreases clutch desiccation by reducing the exposed surface of her egg mass. -from Author
Chapter
Salamanders of the family Plethodontidae exhibit extreme diversity in the expression of many life history characteristics (e.g., Tilley and Bernardo, 1993;Wake and Marks, 1993). The conservatism in their reproductive biology, however, particularly the near universality of parental care in the form of egg attendance (e.g., Salthe and Mecham, 1974), is well documented (Forester, 1978, e.g., Forester, 1978,Forester, 1979; Highton and Savage,1961; Piersol,1909; Ritter,1903; Tilley,1972). While exceptions occur in the expression of parental care in plethodontids, such as Hemidactylium (Forester, 1978) and Batrachoseps (Jockusch and Mahoney,1997), these have been interpreted as examples of a derived state (Bruce,1998).
Article
Consisting of more than six thousand species, amphibians are more diverse than mammals and are found on every continent save Antarctica. Despite the abundance and diversity of these animals, many aspects of the biology of amphibians remain unstudied or misunderstood. The Ecology and Behavior of Amphibians aims to fill this gap in the literature on this remarkable taxon. It is a celebration of the diversity of amphibian life and the ecological and behavioral adaptations that have made it a successful component of terrestrial and aquatic ecosystems. Synthesizing seventy years of research on amphibian biology, Kentwood D. Wells addresses all major areas of inquiry, including phylogeny, classification, and morphology; aspects of physiological ecology such as water and temperature relations, respiration, metabolism, and energetics; movements and orientation; communication and social behavior; reproduction and parental care; ecology and behavior of amphibian larvae and ecological aspects of metamorphosis; ecological impact of predation on amphibian populations and antipredator defenses; and aspects of amphibian community ecology. With an eye towards modern concerns, The Ecology and Behavior of Amphibians concludes with a chapter devoted to amphibian conservation. An unprecedented scholarly contribution to amphibian biology, this book is eagerly anticipated among specialists.
Brooding behaviour by the mountain dusky salamander: can the female’s presences reduce clutch dessication? Aggression and territoriality by salamanders and a comparison with the territorial behaviour of frogs
  • D C Forester
  • A Mathis
  • R G Jaeger
  • W H Keen
  • P K Ducey
  • S Walls
  • B W Buchanan
Forester, D.C. (1984): Brooding behaviour by the mountain dusky salamander: can the female’s presences reduce clutch dessication? Herpetologica 40: 105-109. Mathis, A., Jaeger, R.G., Keen, W.H., Ducey P.K., Walls, S., Buchanan, B.W. (1995): Aggression and territoriality by salamanders and a comparison with the territorial behaviour of frogs. In: Amphibian Biology, 2, Social Behaviour., p. 633-676
Parental care In: Reproductive Biology and Phylogeny of Urodela
  • R A Nussbaum
Nussbaum, R.A. (2003): Parental care. In: Reproductive Biology and Phylogeny of Urodela, p. 527-612. Sever, D.M., Ed., Science Publishers Inc., Enfield, New Hampshire
  • J.-P Durand
Durand, J.-P. (1967): Sur l'ontogenèse d'Hydromantes italicus strinatii Aellen (Urodèle, Plethodontidae). C. R. Acad. Sci., Paris 265: 1533-1535.
Dati preliminari sul comportamento di Speleomantes strinatii (Aellen, 1958) ottenuti con un sistema di videocontrollo a raggi infrarossi
  • F Oneto
  • D Ottonello
  • M V Pastorino
  • S Salvidio
  • D Fiacchini
  • G Carotti
  • G Fusco
Oneto, F., Ottonello, D., Pastorino, M.V., Salvidio, S. (2008): Dati preliminari sul comportamento di Speleomantes strinatii (Aellen, 1958) ottenuti con un sistema di videocontrollo a raggi infrarossi. In: Biospeleologia dell'Appennino, studi e ricerche su Anfibi e Invertebrati con particolare riferimento all'Appennino UmbroMarchigiano, pp 50-53. Fiacchini, D., Carotti, G, Fusco, G., Eds., Ostra Vetere (AN).