South American Journal of Herpetology, 2(2), 2007, 141-147 © 2007 Brazilian Society of Herpetology
SIGNS OF PARENTAL BEHAVIOR IN LIOLAEMUS ELONGATUS (SAURIA: LIOLAEMIDAE) OF NEUQUÉN, ARGENTINA MONIQUE HALLOY1,4, JORGELINA M. BORETTO2,3 AND NORA R. IBARGÜENGOYTÍA2,3 2
1 Instituto de Herpetología, Fundación Miguel Lillo, Miguel Lillo 251, 4000 San Miguel de Tucumán, Argentina. Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, U.P. Universidad del Comahue, San Carlos de Bariloche, 8400, Río Negro, Argentina,
[email protected],
[email protected] 3 Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina 4 Corresponding autor:
[email protected]
ABSTRACT: Parental care in reptiles has been correlated with cold climates and harsh environments. We investigated whether behavioral patterns indicating parental care occurred in the lizard, Liolaemus elongatus, a viviparous species found on rocky outcrops of the Argentinean Patagonia. Five pregnant females were captured during the austral summer and brought to the laboratory for observations. The females were filmed for short periods of time during six days after the birth of their young. During that time, the mothers and offspring were presented with three predatory stimuli, a Diplolaemus sexcinctus, a male Liolaemus elongatus, and a stuffed hawk, Elanus leucurus. Their responses were recorded as well as the distance between mothers and offspring during the experiments and when no stimuli were presented. Except for one female, mothers constructed burrows in which the neonates were born. Mothers and their offspring occupied the same shelter for the whole period of observation. When presented with predatory stimuli, females seemed to choose between remaining near or on top of the burrow with the young inside, or moving away from it. When the offspring were out of the burrow, a female occasionally covered a neonate, forming a bridge over it, particularly when threatened. Mothers showed individual variations in the way they responded to the different stimuli that were presented. KEYWORDS: lizards, Liolaemus elongatus, parental care, behavior.
INTRODUCTION Parental care in reptiles includes several behavioral patterns which are neither common (Somma, 2003) nor well understood, although their existence has been reported for more than 60 years (e.g., Rose, 1929; Fitzsimons, 1943). These may include the incubation of eggs and/or its defense (e.g., Greene et al., 2006), viviparity (Shine, 2004), or the care of recently hatched or live born neonates (Shine, 1988; Somma, 1985, 1990, 2003; Somma and Fawcett, 1989). In the latter case, it may take the form of assistance to the young at the time of hatching or birth, transportation, or defense against predators (Shine, 1988; Somma, 1990). In addition, the mother and her young may share the same area during long periods of time, including years (e.g., Halloy and Halloy, 1997; Lemos-Espinal et al., 1997; Bull and Baghurst, 1998; Mouton et al., 1999; Gardner et al., 2001; O’Connor and Shine, 2004). These various parental strategies should increase the parents’ reproductive success by favoring survival of their young (Gans, 1996; Greene, 2006). The study of parental care in reptiles may help understand the selective pressures involved. Present hypotheses point to environmental factors, especially low temperatures and scarce resources, as fundamental in the selection for parental behavior
(Shine, 1988). Since many lizard species of the genus Liolaemus are found at high latitudes or altitudes, in regions characterized by low temperatures, periods of reduced activities, paucity of resources, and possibly high predator pressure due to open habitats, there is a unique opportunity to investigate this behavior. In Liolaemidae, evidence of parental behavior has been reported in L. kingii, from Patagonia, Argentina (Ibargüengoytía et al., 2002), in L. huacahuasicus, from northwestern Argentina, 4000 m (Halloy and Halloy, 1997), in L. leopardinus, 75 km northeast of Santiago, Chile, 2900 m (Fox and Shipman, 2003), and in two species of Phymaturus, P. antofagastensis of Catamarca, 4000 m, and P. punae of San Juan, 3100-4200 m (Halloy et al., 2005). The purpose of this study was to investigate whether parental care occurs in Liolaemus elongatus, a species found in cold and semi-arid environments of the Argentinean Patagonia (Cei, 1986). In particular, we looked for: 1) an association between the mother and her young, considering the distance maintained between them through a certain period of time, including occupying the same refuge (e.g., Halloy and Halloy, 1997), and 2) protection of the young when confronted with a potential predator. Possible predators of this species are Diplolaemus lizards, raptors, foxes, some snakes, and even males of the same species. Infanticide has been reported in
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some lizard species and involves males preying upon juveniles of their own species (e.g., in Leiocephalus schreibersi, Jenssen et al., 1989; in Liolaemus huacahuasicus, Halloy and Halloy, 1997; in Egernia saxatilis, O´Connor and Shine, 2004). Liolaemus elongatus is found from the San Guillermo Cordillera, in the North of San Juan province, to the San Bernardo Sierra close to the boundary between Chubut and Santa Cruz provinces, and from the mountain slopes, at more than 4000 m in San Juan province, towards the east, to the Añueque Sierra, in Río Negro province (Cei, 1986). It belongs to the elongatus group (Lobo, 2001; Avila et al., 2004), with new species being added to it periodically (e.g., Espinoza and Lobo, 2003; Avila et al., 2004). Typically lizards of this species occur on rocky outcrops scattered with low spiny bushes (Cei, 1986). It is a diurnal species, insectivorous and viviparous (Ibargüengoytía and Cussac, 1998). Although Liolaemus elongatus is considered a viviparous species (sensu Blackburn 1994), females lay eggs covered with a thin fibrous and translucent shell, that hatch between 15 minutes and 12 hours after being laid in burrows. While still in the eggs, the embryos move actively and break the shell membrane, possibly by using an egg tooth as well as their legs (Crocco et al., 2006). Once the neonates emerge from the burrow, they move about the terrarium, carrying along with them a small yolk sac, which is lost within a few hours to three days (Crocco, 2001). Eggs buried in appropriate microhabitats may facilitate the final stages of development of the embryos, their birth and their emergence from the burrows. MATERIALS AND METHODS Five pregnant females of Liolaemus elongatus were captured at the end of January, 2006, near the National Park Laguna Blanca, 40 km west of Za-
pala, Neuquén province, Argentina (39°4074’S and 70°22652’W, elevation 1300 m). This region is part of the Patagonian phytogeographic province, known for its barrenness, cold winters, and strong winds. Mean temperature in the region is 13.1°C, with absolute temperatures ranging between -10°C and 39°C, and an annual precipitation of 176 mm (Cabrera, 1976). The females were taken to the Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, San Carlos de Bariloche, Río Negro province. They were placed in individual terraria of 40 x 40 x 40 cm each, with a sandy substrate, water and food ad libitum (tenebrionid larvae, earwigs, wood lice, etc.). A Genius camera connected to a computer was placed above the terrarium of the female expected to give birth. Two females were filmed the day before giving birth (female L170, during 22.13 min, and female L173, during 56.22 min). Four females were filmed on the day the young were born and all were filmed on various occasions with and without external stimuli (see different treatments further) up to the sixth day (Table 1). Experiments were performed in which the mother and her young were presented with three types of stimuli that in natural conditions might indicate the presence of a potential predator. Each experiment was filmed and lasted an average of 13.5 ± 3.0 minutes with a minimum 10-minute rest period between experiments (Table 1). An experiment consisted in presenting to the female and young, in random order, a Diplolaemus sexcinctus, a male Liolaemus elongatus, and a stuffed hawk, Elanus leucurus. The first two stimuli were placed in an adjacent terrarium, allowing lizards to see each other but preventing physical contact. The raptor stimulus was passed over the terrarium, once every minute. To evaluate possible associations between a mother and her young, the distance between them was recorded each 15 seconds during the time filming lasted. A criterion was used defin-
TABLE 1: Filming times (in minutes) of five female Liolaemus elongatus and their offspring (age in days) in different conditions (see Methods for more details).
Without stimuli Mother’s identity L169 L170 L171 L172 L173
date of birth
# of neonates
days
22-Feb-06 3-Mar-06 28-Feb-06 6-Feb-06 3-Feb-06
3 2 2 4 3
0 to 2 0 to 6 0 to 2 0 to 1 3
time filmed 131.62 75.31 30.60 31.33 18.48
Conditions Diplolaemus male L. elongatus sexcinctus time time days days filmed filmed 2 11.40 2 10.47 5 11.30 5 12.12 2 10.42 2 18.53 0 18.23 0 13.68 3 17.83 3 15.77
stuffed hawk days 2 5 2 0 3
time filmed 10.58 11.22 11.37 15.35 14.83
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TABLE 2: Averages ± 1 standard deviation of the weights and the snout-vent lengths (SVL) of five female Liolaemus elongatus, before and after giving birth, and their neonates shortly after birth.
ing a distance of 5 cm around the mother (Halloy and Halloy, 1997), as an indicator of mother-young association. We hypothesized that the young and their mother would find themselves at least two-thirds of the time they were filmed within a 5 cm radius when presented with a “predatory” stimulus.
Females before birth Females after birth Neonates
Weight (gr) 13.20 ± 1.79 10.68 ± 2.36 1.23 ± 0.21
SVL (mm) 72.70 ± 1.47 Similar 34.06 ± 1.64
RESULTS The five females gave birth to two to four neonates between February 3 and March 3, 2006 (Table 1). Weight and snout-vent-length (SVL) averages of the mothers and their young are presented in Table 2. Four females were observed constructing an underground shelter, after which they remained inside, their head occasionally appearing at the entrance. Parturition could not be observed since the females gave birth (laid eggs, see Introduction) in the burrow. When they came out, their weight loss was noticeable. The
females were then observed to cover the refuge they had constructed, apparently with the eggs soon-to-behatched inside. Later the females were seen scratching the surface in areas where the young finally emerged and where an entrance became visible (Table 3). The scratching behavior was seen several times and could last for hours, alternated with short rest periods. After that, when a neonate entered the burrow, a female might again cover the entrance, settling down on top of it. This was observed mainly during the day that
TABLE 3: Behavioral activities observed in five female Liolaemus elongatus before and after the birth of their neonates, when no stimuli were presented. No observations were made on the fifth day after birth. Mother’s identity L169
day -1 -----
L170
Female in refuge or digging.
L171
-----
L172
-----
L173
Female going in and out of refuge or scratching nearby.
day 0
day 1
day 2
Neonates not visible. Female scratching near the refuge, covered entrance. One neonate comes out. Neonates coming out. Female on top of refuge, covered entrance with one neonate inside. Female and her offspring together in refuge. Female occasionally outside. Female did not construct a refuge. She covers one neonate. -----
One neonate out, the other two in refuge. Female digging.
Neonates ---outside refuge. Female digging near it.
----
----
----
----
----
Neonates going in and out of refuge. Female on top of it.
Neonates going in and out of refuge. Female on top of it.
Neonates in refuge. Female on top of it or scratching nearby.
One neonate in refuge, the other outside. Female at the entrance.
----
----
----
----
----
----
Female occasionally together with offspring in refuge.
----
----
Female staying ---some time near 2 neonates but away from the other two. -------
day 3
day 4
day 6
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the young were born. At night, the mother and her young occupied the same refuge. During the days following birth, the mother spent a large amount of time resting on top of the refuge or close to its entrance, observing neonates coming in and out of it. Observations made during the presentation of a predator stimulus (Diplolaemus sexcinctus, male L. elongatus, and stuffed hawk) indicate a change in the mothers’ behaviors with respect to their young (Table 4). Three strategies were observed. One consisted in the mother settling over the refuge with the neonates inside, remaining there as long as the stimulus lasted. In the other, the mother walked away from the refuge as if she wanted to distract the attention of the potential predator. At other times, when a neonate was not in the burrow, the mother was observed to cover it with her body, forming a bridge over it, or the neonate looked for a refuge under her (Fig. 1, Table 4). Although this behavior was also observed when no stimuli were presented (L172 covered one neonate during 31.3 minutes of filming, this female being the only one who had not constructed a refuge, Tables 1 and 3), it was observed with greater frequency during the experimental treatments. On these occasions, six neonates were covered by their mothers in 43.3 minutes of filming, or one neonate being covered on average every 7.2 minutes. This is 4.3 times more frequent than when no stimuli were presented (Tables 1 and 4). Both the Diplolaemus sexcinctus lizard, and the male L. elongatus that were used in the experiments, placed themselves in front of the terrarium where the female and young could be seen. The first lizard was much more active than the latter, attempting to pass to the female’s terrarium, standing on the glass and scratching vigorously. Only one female was found more than two-thirds of the time she was filmed within 5 cm of her off-
spring, when no stimuli were presented (L 170, 95.2%, Fig. 2). This also occurred in the “Diplolaemus” condition for another female (L169, 90.7%, Fig. 2). This changed in the other conditions. Four females were found more than two-thirds of the time they were filmed, at less than 5 cm of their young, in the “male L. elongatus” condition (L169 and L171 close to two thirds of the time, and L170 and L173 over two-thirds, average 75.4%, Fig. 2), and three females in the “stuffed hawk” condition (L170, L171, and L173, average 80.0%, Fig. 2). The behavior exhibited by individual females were the following. Female L169, although apart from her young (> 5 cm) when no stimuli were presented and in the “stuffed hawk” condition, approached the offspring in the “Diplolaemus” and the “male L. elongatus” conditions (Fig. 2, Tables 3 and 4). Female L170 was found near her young in all conditions except in the “Diplolaemus” condition. In this case, the female was first away from the refuge in which the neonates were, after which she approached and remained in front of the entrance. Female L171 was seen more time away from her young than near them when no stimuli were presented and she remained apart from the entrance to the refuge where the neonates were when the Diplolaemus was presented. As for the other two conditions, this female remained more time near her young than away from them. Finally, female L173 showed similar responses as female L171. Female L172 remained away from her young most of the time during all treatments. This female was the only one that had not constructed a refuge. She also was the only female that had 4 neonates, sometimes finding her away from two of the young but near the other two who used her as a refuge (Fig. 1, Tables 3 and 4).
TABLE 4: Behavior of five female Liolaemus elongatus when presented with different predation stimuli. Female L172 and her young did not have access to a shelter as the other females. Mother’s identity L169 L170 L171 L172
L173
Diplolaemus sexcinctus One neonate in refuge. Female near entrance covering two neonates. Neonates in refuge. Female away from it, later approaching it. Neonates in refuge. Female away from entrance. One neonate finds cover under female for 1 min, then another neonate. Other two neonates away. Female and one neonate in refuge. The other two away from them.
male L. elongatus Neonates in refuge. Female near entrance. Neonates in refuge. Female near entrance. Neonates in refuge. Female remains most of the time near entrance. At one point, two neonates under female. The other two neonates away from them Female and neonates in refuge all the time.
stuffed hawk Neonates in refuge. Female first near refuge, later away from it. Neonates in refuge. Female near entrance. Female and one neonate in refuge, followed by second neonate. All running around or “freezing”.
Female and two neonates in refuge. The third neonate remained outside.
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FIGURE 1: Drawing based on video images of a mother Liolaemus elongatus covering a neonate.
FIGURE 2: Percent of time five female Liolaemus elongatus and their young were within a 5 cm radius when no stimuli were presented (white bars) and in three experimental conditions (light gray bars: “Diplolaemus sexcinctus” condition; grey bars: “male Liolaemus elongatus” condition; and black bars: “stuffed hawk” condition).
DISCUSSION Liolaemus elongatus mothers were observed to scratch the surface of the substrate before and after the birth of their offspring. We suggest that this behavior may help stimulate the hatching of the young, and later their emergence from the covered burrow. Both mothers and their offspring occupied the same refuge for several days (observations were discontinued after the sixth day). This may help the neonates to thermo and hydroregulate (e.g., Somma, 2003; Greene et al., 2006) during the cold, dry nights of
Patagonia, in addition to the protection mothers may be providing. Observed parental behaviors included a mother covering a neonate (Fig. 1, Tables 3 and 4, also reported in the anguid Barisia imbricata, Greene et al., 2006), and females deciding on one or another strategy when presented with predatory stimuli. A mother either remained near or on top of the burrow where her offspring were or she moved away from it. We suggest that the latter behavior, moving away from the entrance to the shelter, may serve the purpose of distracting the potential predator, as has been reported in some birds, such as the South American lapwing, Vanellus chilensis, or Wilson´s plovers, Charadrius wilsonia, which simulate brooding away from their nest, “mock-brooding”, among other distracting displays (Canevari et al., 1991; Bergstrom, 1988, respectively). Instead of finding a general pattern of response among the females to predatory stimuli, i.e. remaining more than two-thirds of the time close to the offspring, females changed strategies possibly depending on their individual perceptions of the immediate threat (Fig. 2, Tables 3 and 4). Somma (1987) observed individual variations in the maternal behavior of Eumeces septentrionalis (for other examples in lizards, see Fox et al., 2003). The formation of family groups and possible defense or protection of the young has been reported in various groups of lizards. For example, in Scincidae and Gekkonidae (Somma, 1990), in Anguidae (Greene et al., 2006), in various species of Egernia (Chapple, 2003; O’Connor and Shine, 2004), in Xenosaurus
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newmanorum (Lemos-Espinal et al., 1997), in Cordylus cataphractus (Mouton et al., 1999), in two species of agamids (Panov and Zykova, 1993; Zykova and Panov, 1993), and in Leiocephalus schreibersi (Jenssen et al., 1989). In Liolaemidae, it has been reported in Liolaemus leopardinus (Fox and Shipman, 2003), in L. huacahuasicus (Halloy and Halloy, 1997), and in Phymaturus punae and P. antofagastensis (Halloy et al., 2005). To this list, we may now add Liolaemus elongatus, although field studies are needed to confirm the observations presented here. RESUMEN El cuidado parental en reptiles ha sido asociado con climas fríos y ambientes rigurosos. El objetivo de este trabajo fue estudiar la presencia de patrones de comportamiento relacionados con el cuidado parental en el lagarto Liolaemus elongatus, especie vivípara que habita zonas de roquedales de la Patagonia Argentina. Cinco hembras grávidas fueron capturadas durante el verano austral y trasladadas al laboratorio para su estudio. Las hembras fueron filmadas por cortos períodos de tiempo durante seis días luego del nacimiento de las crías. Durante ese tiempo, se les presentó a las madres y sus crías tres estímulos de predación, un Diplolaemus sexcinctus, un macho Liolaemus elongatus, y un aguilucho embalsamado, Elanus leucurus. Sus respuestas fueron registradas así como también la distancia a la que las madres y las crías se mantenían durante los experimentos y cuando no se presentaba ningún estímulo. Todas las hembras, excepto una, construyeron refugios donde nacieron los neonatos. Madres y crías ocuparon el mismo refugio durante todo el período de observación. Durante los experimentos de predación, las hembras parecían elegir entre mantenerse cerca o encima del refugio donde se encontraban las crías, o se alejaban del mismo. Cuando las crías estaban afuera del refugio, una hembra ocasionalmente cubría un neonato, formando un puente sobre él, particularmente cuando estaba amenazada. Se observaron variaciones individuales en las respuestas de las madres a los distintos estímulos presentados. ACKNOWLEDGMENTS We thank Joel Gutierrez and Manuela Martinez for their help in the field. The study was funded by CONICET-PIP 02668 (Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires) and CIUNT G218 and G315 (Universidad Nacional de Tucumán, Argentina) to MH and CONICET-PIP 5625 to NI.
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