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Effects of group size on nest attendance in the communally breeding colonial tuco-tuco
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ORIGINAL INVESTIGATION
Effects of group size on nest attendance in the communally breeding colonial tuco-tuco Graciela Izquierdoa, Eileen A. Laceyb, a
Seccio´n Etologı´a, Instituto de Biologı´a, Facultad de Ciencias. Igua´ 4225, Montevideo 11400, Uruguay Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, CA 94720, USA
b
Received 30 May 2007; accepted 27 September 2007
Abstract Communal nesting is generally assumed to be adaptive, meaning that it confers a fitness advantage on the individuals that share a nest site. This advantage may accrue directly to adults, or it may affect adult fitness through gains in offspring survival. In particular, survival of juveniles reared in communal groups may be greater because adults are present in the nest more often to provide care to young. To test the hypothesis that communal nesting is associated with increased adult presence in the nest, we used radiotelemetry to examine patterns of adult nest attendance as a function of group size for free-living colonial tuco-tucos (Ctenomys sociabilis). Burrow systems of this social, subterranean rodent are inhabited by 1–6 adult females and, in some cases, a single adult male. Data obtained from residents of 26 burrow systems monitored during 1996–2000 indicated that the percentage of time that the nest was unattended (no adult present) did not vary predictably with date or time of day during the period between the birth and weaning of young. The percentage of time that the nest was unattended, however, decreased significantly as the number of adults per burrow system increased. This difference was most evident when the percentage of time that the nest was unattended was compared for lone females versus multi-adult groups. We suggest that increased nest attendance has important implications for the survival of juveniles reared in multi-adult burrow systems but that this effect may be confounded by the fitness consequences of other costs and benefits associated with communal nesting in this species. r 2007 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. Keywords: Ctenomys sociabilis; Communal nesting; Group size; Nest attendance; Tuco-tucos
Introduction Communal nesting is expected to occur when the fitness benefits of sharing a nest exceed those of living and rearing young alone (Gittleman 1985; Lewis and Pusey 1997; Hayes 2000). The selective factors favoring communal nesting may act directly upon the adults that share a nest (e.g., increased predator detection; Corresponding author.
E-mail address: [email protected] (E.A. Lacey).
Macdonald 1981; Pilastro 1992; Ebensperger and Wallen 2002) or they may act upon the young reared in communal nests (e.g., increased protection from infanticide; Brown and Burt 2004; Manning et al. 1995; Ebensperger 1998), thereby enhancing the fitness of parents that nest together. Because different selective factors may have distinct or even competing effects on the actions of individuals, it is important to understand how the various potential benefits of communal nesting interact to shape the behavior of animals that live and rear their young together.
1616-5047/$ - see front matter r 2007 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2007.09.007 Mamm. biol. 73 (2008) 438–443
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For juveniles, one potential benefit of communal nesting is the increased number of adults available to provide parental care. Among communally nesting mammals, parental care occurs in a variety of forms, including provisioning young with food (Gittleman 1985; Baker et al. 1998; Doolan and Macdonald 1999; Hayes and Solomon 2004), protecting young from predators (Pilastro 1992; Hoogland 1995), and helping young to thermoregulate (Trune and Slobodchikoff 1976; Bozinovic et al. 1988; Jacquot and Vessey 1994; Cutrera et al. 2003). For at least some forms of care, increasing the number of adults associated with a nest may increase the benefits accrued by young. For example, if the presence of an adult in the nest is critical to thermoregulation by neonates, then the presence of more adults or the presence of at least one adult for a greater total proportion of time may enhance the growth and survival of all young. Thus, patterns of nest attendance by adults may offer critical insights into fitness benefits to juveniles associated with communal nesting. Studies of the colonial tuco-tuco (Ctenomys sociabilis) provide an ideal opportunity to explore the adaptive consequences of communal nesting. Field research on these subterranean rodents has revealed that nearly 50% of burrow systems are occupied by multiple adults, including male–female pairs and multi-female groups that may or may not include an adult male (Lacey et al. 1997; Lacey and Wieczorek 2004). During the period when unweaned young are present, all animals in a burrow system share a single, communal nest site (Lacey et al. 1997). Although typically all females in single- and multi-female groups give birth to young, the per capita number of pups weaned each year is significantly less for group-living than for lone females (Lacey 2004), raising intriguing questions regarding the adaptive bases for communal nesting in this species. As a first step toward understanding how communal nesting influences juvenile survival and, hence, parental fitness, we explored the effects of group size on patterns of nest attendance by adults. To test the hypothesis that communal nesting is associated with increased nest attendance by adults, we quantified the percentage of time that nests were unattended (no adult present) as a function of the number of adults per burrow system. These data provide the first quantitative analyses of communal nest use by free-living C. sociabilis and yield critical insights into the potential benefits of sociality in this species.
Materials and methods The population of C. sociabilis studied was located on Estancia Rincon Grande, Provincia Neuque´n, Argentina (401560 S, 711030 W). The study site, which is described in detail
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by Lacey and Wieczorek (2003), consisted of a ca. 10-ha area of open meadow characterized by seasonal grasses, sedges, and several species of woody shrubs. Each year, the site contained 13–25 burrow systems occupied by C. sociabilis. Typically, about half of these burrow systems contained a single adult female, with the remaining burrow systems occupied by a mean (71 SD) of 3.0 (71.2) females (range ¼ 2–6; Lacey and Wieczorek 2004). Approximately 44% of burrow systems also contained an adult male (Lacey and Wieczorek 2004), yielding a mean (71 SD) population density of 4.0 (72.7) adults per hectare. C. sociabilis is almost exclusively subterranean. Individuals typically emerge only briefly from their burrows to crop surface-growing vegetation and, while at the surface, the animals rarely emerge more than half a body length from their burrows. Members of the study population were captured as they emerged to forage using hand-held nooses (Lacey et al. 1997). Capture localities were recorded to the nearest meter using a geo-referenced grid (4 m 4 m cell size) established on the study site in 1996. The criteria used to determine when all animals resident in a burrow system had been captured are described in Lacey et al. (1997). In brief, by placing a small twig across each entrance to a burrow system, we were able to determine whether uncaptured animals remained in that system; if no twigs were displaced during two consecutive foraging periods (morning and evening), we considered all animals in that system to have been captured. Upon first capture, members of the study population were individually marked by injecting a magnetically coded bead (IMI-1000 Implantable Transponders, BioMedic Data Systems, Seaford, DE) beneath the skin at the nape of the neck. Implanted beads were read using a hand-held scanner (DAS 4004 Pocket Scanner, BioMedic Data Systems). Typically, adults in the study population were captured during early to mid-October, which corresponds to the period when females are giving birth to their single litter of young per year. Adults were recaptured and juveniles were captured for the first time between mid-November and mid-December, as soon as young of the year began foraging for themselves on surface-growing vegetation (age: ca. 4–5 weeks). Used in conjunction with radiotelemetry (see below), this protocol allowed us to determine the number and identities of adults resident in almost all burrow systems occupied during 1996–2000. Because the extent of a burrow system cannot be accurately assessed from surface evidence of activity (e.g., freshly excavated dirt, active burrow entrances), capture localities alone do not provide a reliable means of determining which adults share a burrow system. Consequently, we used radiotelemetry to confirm that animals captured in close proximity to one another occupied the same burrow system. Adults captured in October were fitted with small (o7 g) radiocollars consisting of an acrylic-encased transmitter (SM1-Mouse transmitters, AVM Instruments, Inc., Colfax, CA) attached to a plastic cable tie. Following their release, the locations of radiocollared animals were determined several times per day using hand-held antennas and receivers (Yagi antennas, CE-12 receivers, AVM Instruments, Inc.). Previous research has revealed that localities recorded using this procedure are accurate to within 0.5 m (Lacey et al. 1997). Individuals that exhibited extensive (466%) spatial overlap and that shared the same nest site were considered resident in the same burrow
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system (Lacey et al. 1997). Radiocollars were removed when adults were recaptured during November and December. Radiotelemetry was also used to document patterns of nest attendance by adult C. sociabilis during the period between the birth and weaning of young. Previous field studies (Lacey et al. 1997) have revealed that during this portion of the reproductive cycle, all residents of a burrow system share a single, communal nest. For each burrow system monitored during this study, the location of the nest was identified by determining the location at which all radiocollared adults spent the majority of their time (Lacey et al. 1997). This was done by recording the locations of all radiocollared animals X6 times per day (minimum of 1 h between successive data points) for a period of 3–4 days. In addition, the locations of radiocollared animals were determined after sunset. C. sociabilis is strictly diurnal and adults only rarely leave the nest during non-daylight hours (Lacey et al. 1997). As a result, telemetry data obtained at night provided a convenient means of determining nest locations. Once the nest site for a burrow system had been determined, the presence of adults in the nest was monitored by placing a Yagi antenna directly over the nest site, with the long axis of the antennae held perpendicular to the soil surface. The identities of all adults present in the nest were determined by quickly scanning through the radiotransmitter frequencies for adults resident in that burrow system and noting the intensity of associated radio signals. Intensity was assessed both aurally and by noting the amplitude of the signal as indicated on the radio receiver. This procedure provided an unambiguous means of determining whether an individual was present in the nest and produced no detectable effects on adult behavior. Scans of adult presence were repeated at 5-min intervals for a total of 30 min. Typically, up to three 30-min scan sessions were completed daily between 0800 and 2100 h, with a minimum of 2 h allowed between scan sessions for the same burrow system. The times at which scans were completed for a given burrow system varied so that all portions of the day were represented in the data collected from each system. Because the number of adults per burrow system varied (Lacey et al. 1997; Lacey and Wieczorek 2004), we use the term ‘‘social unit’’ to describe the set of animals – adults and juveniles – that were resident in a single burrow system during a given field season. In terms of benefits to juveniles of communal nesting, the variable that seemed most likely to influence offspring growth and survival was the percentage of time that the nest was unattended (no adults in the nest) during each 30-min scan session. Although tuco-tucos produce relatively precocial young (Lacey and Ebensperger 2007), studies of captive animals indicate that juvenile C. sociabilis remain closely associated with the nest for the first few weeks following birth (M. Soares pers. comm.). As a result, the percentage of time that the nest is unattended may reflect periods during which parental care is not available to young. Although each social unit represented an independent data set, data collected from the same social unit during different 30-min scan sessions were not independent and thus time series analyses were used to assess whether nest attendance was influenced by the date or the time of day when scans were conducted. For each social unit, the percentage of time that the nest was unattended was calculated per scan session and per day by dividing the number of scans during which no adults
were in the nest by the associated total number of scans. Time series analyses were then run using date and time of day as the independent variables. t-tests were used to compare correlation coefficients from all social units against the null hypothesis of no consistent relationship (mean r ¼ 0) between nest attendance and date or hour of data collection (Zar 1999). The effects of social unit size on nest attendance were examined using ANOVAs and linear regressions. For all other analyses, parametric statistical tests were used whenever the associated assumptions of normality and homogeneity of variances were met. All statistical analyses were completed using Statistica 6.0 (Statsoft, Inc., 2002). Throughout the text, means are reported 71 SD.
Results Nest attendance by adult C. sociabilis was monitored for 61 individuals in 26 social units resident on the study site during 1996–2000. All adults in 24 (92.3%) of these social units were monitored via radiotelemetry. Although one adult in each of the remaining social units was not captured until after telemetry data had been collected, visual inspection of the data obtained from these groups revealed no apparent differences in nest attendance between these social units and same-sized groups in which all adults were monitored. As a result, analyses of nest attendance for the two incomplete social units were based on the total number of adults resident in each burrow system. Twelve of the social units monitored contained a single adult female; the remaining social units each contained multiple adult females (mean ¼ 2.071.1 females per social unit, range ¼ 2–4; Table 1). Ten (38.5%) social units contained an adult male; the distribution of males between burrow systems occupied by one versus multiple adult females was not significantly different from that expected if males are equally represented in both types of social units (w21 ¼ 1:38, P40.05). For each social unit, a minimum of 10 30-min nest attendance scans (mean ¼ 24.7710.8 scans per social unit; range ¼ 10–48) was completed over at least 5 different days (mean ¼ 23.6710.5 days per social unit, range ¼ 5–40) between the birth and weaning of pups reared by that social unit. As expected, within each multi-adult social unit, all adults shared a common nest site; in no case did the nest Table 1. Composition of the social units monitored during this study Number of adult females
Male present No male present Total
Total
1
2
3
4
3 9
3 1
2 5
2 1
10 16
12
4
7
3
26
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sites identified for individuals differ among members of the same social unit. The percentage of time that the nest was left unattended (no adults present) did not vary predictably with the date of data collection (mean r ¼ 0.02470.352, N ¼ 26; t-test: t23 ¼ 0.35, twotailed P40.05), providing no evidence that patterns of adult activity changed predictably as a function of juvenile age. Although the percentage of time that the nest was unattended appeared to increase over the course of a day (mean r ¼ 0.19370.222, N ¼ 26; t-test: t23 ¼ 4.43, two-tailed Po0.01), a strict interpretation of this result indicates only that there was a consistently non-zero relationship between time of day and nest attendance among the social units monitored. Closer inspection of these data revealed that, across social units, both positive and negative relationships occurred between these variables. Further, significant correlations between time of day and percentage of time that the nest was unattended were detected for only 2 (7.7%) of the 26 social units monitored, indicating that, within social units, nest use by adults was not strongly temporally patterned. Given these findings, we did not partition the data according to date or time of day at which scans were completed. Instead, for each social unit, all scans were pooled for the following analyses of nest attendance by adults. Because not all social units in our sample contained an adult male (Table 1), we examined the effects of the presence of a male on patterns of nest attendance by females. A two-way analysis of variance revealed no significant effect of a male on the percentage of time that the nest was unattended (ANOVA: F1,18 ¼ 1.23, P ¼ 0.283). Consequently, we did not distinguish between the sexes but instead used the total number of adults resident in a burrow system for subsequent analyses of the effects of group size on nest attendance. When the total number adults per burrow system was considered, there was a significant effect of social unit size on the percentage of time that no adults were present in the nest (one-way ANOVA: F4,21 ¼ 12.57, Po0.001). Visual inspection of the data suggested that the percentage of time that the nests of lone females were unattended was considerably greater than that for social units containing multiple adults (Fig. 1); post hoc comparisons revealed significant contrasts between data from lone females and those from all other sizes of social unit (Tukey’s HSD tests, all Po0.01), suggesting that the primary determinant of the percentage of time that a nest is left unattended is the presence of one versus multiple adults in a burrow system. Accordingly, although the percentage of time that the nest was unattended declined significantly as a function of the number of adults in a burrow system when all social units were considered (R2 ¼ 0.533, N ¼ 26, F1,25 ¼ 27.35, Po0.001; Fig. 1), no significant relationship between number of adults and percentage of time the
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Fig. 1. Percentage of time that nests of C. sociabilis were unattended (no adult present) as a function of the total number of adults resident in a burrow system. Data are from 26 social units monitored during 1996–2000. Burrow systems containing an adult male are indicated. The regression line indicates a significant (Po0.001) negative relationship between number of adults and percentage of time the nest was unattended.
nest was unattended was detected among social units containing X2 adults (R2 ¼ 0.114, N ¼ 17, F1,15 ¼ 1.94, P40.100).
Discussion Our data indicate that nest attendance by free-living C. sociabilis was influenced by the number of adults that shared a burrow system. When all social units were considered, the percentage of time that the communal nest was unattended (no adults present) decreased significantly as the number of adults per burrow system increased. The presence of an adult male appeared to have no effect on the percentage of time that the nest was unattended. When the number of adults per social unit was considered regardless of sex, the only significant contrasts detected were between lone females and social units containing multiple adults. Thus, the greatest effect of communal nesting on nest attendance occurred with the addition of a second adult to social units containing only a single female. Reducing the time that the nest is unattended may be beneficial to juveniles in several ways. In general, because the presence of an adult is essential to many forms of parental care, increasing the percentage of time during which at least one adult is present in the nest may increase the overall availability of such care, potentially leading to enhanced juvenile growth and survival (Hayes and Solomon 2006). More specifically, the presence of one or more adults may have thermoregulatory benefits for young; juvenile ctenomyids do not thermoregulate effectively until they are more than 15 days old (Cutrera
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et al. 2003; Zenuto et al. 2002) and, hence, regular nest attendance may reduce the chances of hypothermia of young. At the same time, the presence of an adult may increase the tendency for pups to remain inside the nest (M. Soares, pers. comm.), thereby decreasing the risk of predation as well as hypothermia. If, as these arguments suggest, the regular presence in the nest of X1 adult increases juvenile survival, then decreasing the time that the nest is unattended may be an adaptive consequence of group living in C. sociabilis. If increased nest attendance is an adaptive benefit of group living, why do individuals in multi-female social units rear fewer young to weaning than lone females? On an annual basis, the per capita direct fitness of female C. sociabilis declines significantly as a function of group size (Lacey 2004), indicating that social units in which nest attendance by adults is greater produce fewer surviving pups per female. Communal nesting is a complex social phenomenon that likely reflects the combined effects of multiple selective factors that confer both benefits and costs on animals that live and rear their young together (Alexander 1974; Hayes 2000). As a result, while increasing nest attendance may improve juvenile survival, other aspects of communal nesting (e.g., reproductive skew, infanticide, and other manifestations of increased competition among burrow-mates: Alexander 1974; Clutton-Brock 1998; Ebensperger 1998; Woodroffe and Macdonald 2000) may counter this potential fitness gain. Hence, to understand the net fitness consequences of communal nesting, it is necessary to consider the full range of selective pressures leading to this behavior. Future studies of communal nesting in C. sociabilis will address this issue by exploring other mechanisms (e.g., communal nursing) by which young may benefit from increased parental presence, as well as by exploring the fitness consequences to adults of sharing a nest with conspecifics.
Acknowledgements For permission to work on Estancia Rincon Grande, we thank Alain Thouyaret and the Delegacio´n Tecnica de Parques Nacionales Argentinas, in particular Claudio Chehebar and Eduardo Ramilo. For logistic assistance, we thank Miguel Christie, Gustavo Iglesias, and the members of the Sociedad Naturalista Andino Patagonica in Bariloche, Argentina. Field assistance was provided by A. Chiesa, I. Tomasco, and, in particular, M. Soares and J. Wieczorek. Previous versions of this manuscript benefited from comments by G. Francescoli, M. Hauber, M. Soares, and J. Wieczorek. Melitta Meneghel kindly translated the abstract to German. Financial support was provided by the Comision Sectorial de Investigacion Cientifica and Programa de Desarrollo de las Ciencias Ba´sicas (Uruguay), and the
Museum of Vertebrate Zoology and Department of Integrative Biology at the University of California, Berkeley. This work was conducted in compliance with all relevant institutional, national, and international regulations.
Zusammenfassung Einfluss der Gruppengro¨ße auf die Nestanwesenheit kolonialer Tucotucos (Ctenomys sociabilis) Gemeinschaftliche Jungenaufzucht wird als adaptiv angenommen, wenn es den Individuen, die dasselbe Nest benutzen, einen Fitnessvorteil verleiht. Dieser Vorteil kann direkt fu¨r die adulten Tiere nu¨tzlich sein oder deren Fitness durch la¨ngere U¨berlebensrate ihrer Nachkommen beeinflussen. Insbesondere Jungtiere, die in gemeinschaftlichen Gruppen aufgezogen wurden, du¨rften eine la¨ngere U¨berlebensrate durch die ha¨ufigere Anwesenheit mehrerer pflegeversorgenden Adulten haben. Es wurden radiotelemetrische Analysen durchgefu¨hrt, um zu pru¨fen, wie gemeinschaftliche Vermehrung mit erho¨hter Anwesenheit adulter Tiere in Verbindung steht, um damit die Hypothese zu testen, dass das Anwesenheitsmuster adulter Tiere im Nest abha¨ngig von der Gruppengro¨ße freilebender kolonialer Tucotucos (Ctenomys sociabilis) ist. Die Bausysteme dieses sozialen, unterirdischen Nagetieres werden von 1–6 adulten Weibchen und in einigen Fa¨llen von einem einzigen adulten Ma¨nnchen bewohnt. Die Daten, die wir von 1996 bis 2000 von 26 u¨berwachten Bausystemen erhielten, deuteten an, dass die Zeit, in der das Nest ohne adulte Tiere zwischen Geburt und Absetzen war, nicht von Datum oder Tageszeit abhing. Die Zeit, in der das Nest unbeaufsichtigt war, verminderte sich mit der Zunahme an erwachsenen Tieren fu¨r jedes Bausystem erheblich. Als die Zeit, in der das Nest unbegleitet war, fu¨r solita¨re Weibchen mit der von Gruppen mehrerer Weibchen verglichen wurde, war der Unterschied offensichtlich. Es wird vorgeschlagen, dass zunehmende Nestanwesenheit eine wichtige Rolle fu¨r das U¨berleben von Jungtieren, die in ‘‘Multi-Erwachsenen’’-Bausystemen aufgezogen werden, spielt. Dieses ko¨nnte jedoch mit den Fitnessfolgen anderer Kosten und Vorteile, die mit der gemeinsamen Jungenaufzucht in dieser Art verbunden sind, verwechselt werden.
References Alexander, R.D., 1974. The evolution of social behavior. Ann. Rev. Ecol. Syst. 5, 325–388. Baker, P.J., Robertson, C.P.J., Funk, S.M., Harris, S., 1998. Potential fitness benefits of group living in the red fox, Vulpes vulpes. Anim. Behav. 56, 1411–1424.
ARTICLE IN PRESS G. Izquierdo, E.A. Lacey / Mamm. biol. 73 (2008) 438–443
Bozinovic, F.M., Rosenmann, M., Veloso, C., 1988. Termorregulacio´n conductual en Phillotis darwini (Rodentia: Cricetidae): efecto de la temperatura ambiente, uso de nidos y agrupamiento social sobre el gasto de energı´ a. Rev. Chil. Hist. Nat. 61, 81–86. Brown, J.S., Burt, P., 2004. Hazardous duty pay and the foraging cost of predation. Ecol. Lett. 7, 999–1014. Clutton-Brock, T.H., 1998. Reproductive skew, concessions, and limited control. Trends Ecol. Evol. 13, 288–292. Cutrera, A.P., Antinuchi, C.D., Busch, C., 2003. Thermoregulatory development in pups of the subterranean rodent Ctenomys talarum. Physiol. Behav. 79, 321–330. Doolan, S.P., Macdonald, D.W., 1999. Cooperative rearing by slender tailed meerkats (Suricata suricatta) in the southern Kalahari. Ethology 105, 851–866. Ebensperger, L.A., 1998. Strategies and counterstrategies to infanticide in mammals. Biol. Rev. Cambridge Philos. Soc. 73, 321–346. Ebensperger, L.A., Wallen, P.K., 2002. Grouping increases the ability of the social rodent, Octodon degus, to detect predators when using exposed microhabitats. Oikos 98, 491–497. Gittleman, J.L., 1985. Functions of communal care in mammals. In: Greenwood, P.J., Harvey, P.H., Slatkin, M. (Eds.), Evolution: Essays in Honour of John Maynard Smith. Cambridge University Press, Cambridge, pp. 187–205. Hayes, L.D., 2000. To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Anim. Behav. 59, 677–688. Hayes, L.D., Solomon, N.G., 2004. Costs and benefits of communal rearing to female prairie voles (Microtus ochrogaster). Behav. Ecol. Sociobiol. 56, 585–593. Hayes, L.D., Solomon, N.G., 2006. Mechanisms of maternal investment by communal prairie voles, Microtus ochrogaster. Anim. Behav. 72, 1069–1080. Hoogland, J.L., 1995. The Black-Tailed Prairie Dog: The Social Life of a Burrowing Mammal. University of Chicago Press, Chicago. Jacquot, J.J., Vessey, S.H., 1994. Non-offspring nursing in the white-footed mouse, Peromyscus leucopus. Anim. Behav. 48, 1238–1240.
443
Lacey, E.A., 2004. Sociality reduces individual direct fitness in a communally breeding rodent, the colonial tuco-tuco (Ctenomys sociabilis). Behav. Ecol. Sociobiol. 56, 449–457. Lacey, E.A., Ebensperger, L.A., 2007. Social structure in octodontid and ctenomyid rodents. In: Wolff, J.O., Sherman, P.W. (Eds.), Rodent Societies: An Ecological and Evolutionary Perspective. University of Chicago Press, Chicago, IL, USA, pp. 403–415. Lacey, E.A., Wieczorek, J.R., 2003. The ecology of sociality in rodents: a ctenomyid perspective. J. Mammal. 84, 1198–1211. Lacey, E.A., Wieczorek, J.R., 2004. Kinship in colonial tucotucos: evidence from group composition and population structure. Behav. Ecol. 15, 988–996. Lacey, E.A., Braude, S.H., Wieczorek, J.R., 1997. Burrow sharing by colonial tuco-tucos (Ctenomys sociabilis). J. Mammal. 78, 556–562. Lewis, S.E., Pusey, A.E., 1997. Factors influencing the occurrence of communal care in plural breeding mammals. In: Solomon, N.G., French, J.A. (Eds.), Cooperative Breeding in Mammals. Cambridge University Press, Cambridge, pp. 335–363. Macdonald, D.W., 1981. Dwindling resources and the social behaviour of capybaras (Hydrochoerus hydrochaeris) (Mammalia). J. Zool. (London) 194, 371–391. Manning, C.J., Dewsbury, D.A., Wakeland, E.K., Potts, W.K., 1995. Communal nesting and nursing in house mice, Mus musculus domesticus. Anim. Behav. 50, 741–751. Pilastro, A., 1992. Communal nesting between breeding females in a free-living population of fat dormouse (Glis glis L). Boll. Zool. 59, 63–68. Trune, D.R., Slobodchikoff, C.N., 1976. Social effects of roosting on the metabolism of the pallid bat (Antrozous pallidus). J. Mammal. 57, 656–663. Woodroffe, R., Macdonald, D.W., 2000. Helpers provide no detectable benefits in the European badger (Meles meles). J. Zool. (London) 250, 113–119. Zar, J.H., 1999. Biostatistical Analysis. Prentice-Hall, New Jersey. Zenuto, R.R., Antinuchi, C.D., Busch, C., 2002. Bioenergetics of reproduction and pup development in a subterranean rodent (Ctenomys talarum). Physiol. Biochem. Zool. 75, 469–478.
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ORIGINAL INVESTIGATION
Effects of group size on nest attendance in the communally breeding colonial tuco-tuco Graciela Izquierdoa, Eileen A. Laceyb, a
Seccio´n Etologı´a, Instituto de Biologı´a, Facultad de Ciencias. Igua´ 4225, Montevideo 11400, Uruguay Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, CA 94720, USA
b
Received 30 May 2007; accepted 27 September 2007
Abstract Communal nesting is generally assumed to be adaptive, meaning that it confers a fitness advantage on the individuals that share a nest site. This advantage may accrue directly to adults, or it may affect adult fitness through gains in offspring survival. In particular, survival of juveniles reared in communal groups may be greater because adults are present in the nest more often to provide care to young. To test the hypothesis that communal nesting is associated with increased adult presence in the nest, we used radiotelemetry to examine patterns of adult nest attendance as a function of group size for free-living colonial tuco-tucos (Ctenomys sociabilis). Burrow systems of this social, subterranean rodent are inhabited by 1–6 adult females and, in some cases, a single adult male. Data obtained from residents of 26 burrow systems monitored during 1996–2000 indicated that the percentage of time that the nest was unattended (no adult present) did not vary predictably with date or time of day during the period between the birth and weaning of young. The percentage of time that the nest was unattended, however, decreased significantly as the number of adults per burrow system increased. This difference was most evident when the percentage of time that the nest was unattended was compared for lone females versus multi-adult groups. We suggest that increased nest attendance has important implications for the survival of juveniles reared in multi-adult burrow systems but that this effect may be confounded by the fitness consequences of other costs and benefits associated with communal nesting in this species. r 2007 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. Keywords: Ctenomys sociabilis; Communal nesting; Group size; Nest attendance; Tuco-tucos
Introduction Communal nesting is expected to occur when the fitness benefits of sharing a nest exceed those of living and rearing young alone (Gittleman 1985; Lewis and Pusey 1997; Hayes 2000). The selective factors favoring communal nesting may act directly upon the adults that share a nest (e.g., increased predator detection; Corresponding author.
E-mail address: [email protected] (E.A. Lacey).
Macdonald 1981; Pilastro 1992; Ebensperger and Wallen 2002) or they may act upon the young reared in communal nests (e.g., increased protection from infanticide; Brown and Burt 2004; Manning et al. 1995; Ebensperger 1998), thereby enhancing the fitness of parents that nest together. Because different selective factors may have distinct or even competing effects on the actions of individuals, it is important to understand how the various potential benefits of communal nesting interact to shape the behavior of animals that live and rear their young together.
1616-5047/$ - see front matter r 2007 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2007.09.007 Mamm. biol. 73 (2008) 438–443
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For juveniles, one potential benefit of communal nesting is the increased number of adults available to provide parental care. Among communally nesting mammals, parental care occurs in a variety of forms, including provisioning young with food (Gittleman 1985; Baker et al. 1998; Doolan and Macdonald 1999; Hayes and Solomon 2004), protecting young from predators (Pilastro 1992; Hoogland 1995), and helping young to thermoregulate (Trune and Slobodchikoff 1976; Bozinovic et al. 1988; Jacquot and Vessey 1994; Cutrera et al. 2003). For at least some forms of care, increasing the number of adults associated with a nest may increase the benefits accrued by young. For example, if the presence of an adult in the nest is critical to thermoregulation by neonates, then the presence of more adults or the presence of at least one adult for a greater total proportion of time may enhance the growth and survival of all young. Thus, patterns of nest attendance by adults may offer critical insights into fitness benefits to juveniles associated with communal nesting. Studies of the colonial tuco-tuco (Ctenomys sociabilis) provide an ideal opportunity to explore the adaptive consequences of communal nesting. Field research on these subterranean rodents has revealed that nearly 50% of burrow systems are occupied by multiple adults, including male–female pairs and multi-female groups that may or may not include an adult male (Lacey et al. 1997; Lacey and Wieczorek 2004). During the period when unweaned young are present, all animals in a burrow system share a single, communal nest site (Lacey et al. 1997). Although typically all females in single- and multi-female groups give birth to young, the per capita number of pups weaned each year is significantly less for group-living than for lone females (Lacey 2004), raising intriguing questions regarding the adaptive bases for communal nesting in this species. As a first step toward understanding how communal nesting influences juvenile survival and, hence, parental fitness, we explored the effects of group size on patterns of nest attendance by adults. To test the hypothesis that communal nesting is associated with increased nest attendance by adults, we quantified the percentage of time that nests were unattended (no adult present) as a function of the number of adults per burrow system. These data provide the first quantitative analyses of communal nest use by free-living C. sociabilis and yield critical insights into the potential benefits of sociality in this species.
Materials and methods The population of C. sociabilis studied was located on Estancia Rincon Grande, Provincia Neuque´n, Argentina (401560 S, 711030 W). The study site, which is described in detail
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by Lacey and Wieczorek (2003), consisted of a ca. 10-ha area of open meadow characterized by seasonal grasses, sedges, and several species of woody shrubs. Each year, the site contained 13–25 burrow systems occupied by C. sociabilis. Typically, about half of these burrow systems contained a single adult female, with the remaining burrow systems occupied by a mean (71 SD) of 3.0 (71.2) females (range ¼ 2–6; Lacey and Wieczorek 2004). Approximately 44% of burrow systems also contained an adult male (Lacey and Wieczorek 2004), yielding a mean (71 SD) population density of 4.0 (72.7) adults per hectare. C. sociabilis is almost exclusively subterranean. Individuals typically emerge only briefly from their burrows to crop surface-growing vegetation and, while at the surface, the animals rarely emerge more than half a body length from their burrows. Members of the study population were captured as they emerged to forage using hand-held nooses (Lacey et al. 1997). Capture localities were recorded to the nearest meter using a geo-referenced grid (4 m 4 m cell size) established on the study site in 1996. The criteria used to determine when all animals resident in a burrow system had been captured are described in Lacey et al. (1997). In brief, by placing a small twig across each entrance to a burrow system, we were able to determine whether uncaptured animals remained in that system; if no twigs were displaced during two consecutive foraging periods (morning and evening), we considered all animals in that system to have been captured. Upon first capture, members of the study population were individually marked by injecting a magnetically coded bead (IMI-1000 Implantable Transponders, BioMedic Data Systems, Seaford, DE) beneath the skin at the nape of the neck. Implanted beads were read using a hand-held scanner (DAS 4004 Pocket Scanner, BioMedic Data Systems). Typically, adults in the study population were captured during early to mid-October, which corresponds to the period when females are giving birth to their single litter of young per year. Adults were recaptured and juveniles were captured for the first time between mid-November and mid-December, as soon as young of the year began foraging for themselves on surface-growing vegetation (age: ca. 4–5 weeks). Used in conjunction with radiotelemetry (see below), this protocol allowed us to determine the number and identities of adults resident in almost all burrow systems occupied during 1996–2000. Because the extent of a burrow system cannot be accurately assessed from surface evidence of activity (e.g., freshly excavated dirt, active burrow entrances), capture localities alone do not provide a reliable means of determining which adults share a burrow system. Consequently, we used radiotelemetry to confirm that animals captured in close proximity to one another occupied the same burrow system. Adults captured in October were fitted with small (o7 g) radiocollars consisting of an acrylic-encased transmitter (SM1-Mouse transmitters, AVM Instruments, Inc., Colfax, CA) attached to a plastic cable tie. Following their release, the locations of radiocollared animals were determined several times per day using hand-held antennas and receivers (Yagi antennas, CE-12 receivers, AVM Instruments, Inc.). Previous research has revealed that localities recorded using this procedure are accurate to within 0.5 m (Lacey et al. 1997). Individuals that exhibited extensive (466%) spatial overlap and that shared the same nest site were considered resident in the same burrow
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system (Lacey et al. 1997). Radiocollars were removed when adults were recaptured during November and December. Radiotelemetry was also used to document patterns of nest attendance by adult C. sociabilis during the period between the birth and weaning of young. Previous field studies (Lacey et al. 1997) have revealed that during this portion of the reproductive cycle, all residents of a burrow system share a single, communal nest. For each burrow system monitored during this study, the location of the nest was identified by determining the location at which all radiocollared adults spent the majority of their time (Lacey et al. 1997). This was done by recording the locations of all radiocollared animals X6 times per day (minimum of 1 h between successive data points) for a period of 3–4 days. In addition, the locations of radiocollared animals were determined after sunset. C. sociabilis is strictly diurnal and adults only rarely leave the nest during non-daylight hours (Lacey et al. 1997). As a result, telemetry data obtained at night provided a convenient means of determining nest locations. Once the nest site for a burrow system had been determined, the presence of adults in the nest was monitored by placing a Yagi antenna directly over the nest site, with the long axis of the antennae held perpendicular to the soil surface. The identities of all adults present in the nest were determined by quickly scanning through the radiotransmitter frequencies for adults resident in that burrow system and noting the intensity of associated radio signals. Intensity was assessed both aurally and by noting the amplitude of the signal as indicated on the radio receiver. This procedure provided an unambiguous means of determining whether an individual was present in the nest and produced no detectable effects on adult behavior. Scans of adult presence were repeated at 5-min intervals for a total of 30 min. Typically, up to three 30-min scan sessions were completed daily between 0800 and 2100 h, with a minimum of 2 h allowed between scan sessions for the same burrow system. The times at which scans were completed for a given burrow system varied so that all portions of the day were represented in the data collected from each system. Because the number of adults per burrow system varied (Lacey et al. 1997; Lacey and Wieczorek 2004), we use the term ‘‘social unit’’ to describe the set of animals – adults and juveniles – that were resident in a single burrow system during a given field season. In terms of benefits to juveniles of communal nesting, the variable that seemed most likely to influence offspring growth and survival was the percentage of time that the nest was unattended (no adults in the nest) during each 30-min scan session. Although tuco-tucos produce relatively precocial young (Lacey and Ebensperger 2007), studies of captive animals indicate that juvenile C. sociabilis remain closely associated with the nest for the first few weeks following birth (M. Soares pers. comm.). As a result, the percentage of time that the nest is unattended may reflect periods during which parental care is not available to young. Although each social unit represented an independent data set, data collected from the same social unit during different 30-min scan sessions were not independent and thus time series analyses were used to assess whether nest attendance was influenced by the date or the time of day when scans were conducted. For each social unit, the percentage of time that the nest was unattended was calculated per scan session and per day by dividing the number of scans during which no adults
were in the nest by the associated total number of scans. Time series analyses were then run using date and time of day as the independent variables. t-tests were used to compare correlation coefficients from all social units against the null hypothesis of no consistent relationship (mean r ¼ 0) between nest attendance and date or hour of data collection (Zar 1999). The effects of social unit size on nest attendance were examined using ANOVAs and linear regressions. For all other analyses, parametric statistical tests were used whenever the associated assumptions of normality and homogeneity of variances were met. All statistical analyses were completed using Statistica 6.0 (Statsoft, Inc., 2002). Throughout the text, means are reported 71 SD.
Results Nest attendance by adult C. sociabilis was monitored for 61 individuals in 26 social units resident on the study site during 1996–2000. All adults in 24 (92.3%) of these social units were monitored via radiotelemetry. Although one adult in each of the remaining social units was not captured until after telemetry data had been collected, visual inspection of the data obtained from these groups revealed no apparent differences in nest attendance between these social units and same-sized groups in which all adults were monitored. As a result, analyses of nest attendance for the two incomplete social units were based on the total number of adults resident in each burrow system. Twelve of the social units monitored contained a single adult female; the remaining social units each contained multiple adult females (mean ¼ 2.071.1 females per social unit, range ¼ 2–4; Table 1). Ten (38.5%) social units contained an adult male; the distribution of males between burrow systems occupied by one versus multiple adult females was not significantly different from that expected if males are equally represented in both types of social units (w21 ¼ 1:38, P40.05). For each social unit, a minimum of 10 30-min nest attendance scans (mean ¼ 24.7710.8 scans per social unit; range ¼ 10–48) was completed over at least 5 different days (mean ¼ 23.6710.5 days per social unit, range ¼ 5–40) between the birth and weaning of pups reared by that social unit. As expected, within each multi-adult social unit, all adults shared a common nest site; in no case did the nest Table 1. Composition of the social units monitored during this study Number of adult females
Male present No male present Total
Total
1
2
3
4
3 9
3 1
2 5
2 1
10 16
12
4
7
3
26
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sites identified for individuals differ among members of the same social unit. The percentage of time that the nest was left unattended (no adults present) did not vary predictably with the date of data collection (mean r ¼ 0.02470.352, N ¼ 26; t-test: t23 ¼ 0.35, twotailed P40.05), providing no evidence that patterns of adult activity changed predictably as a function of juvenile age. Although the percentage of time that the nest was unattended appeared to increase over the course of a day (mean r ¼ 0.19370.222, N ¼ 26; t-test: t23 ¼ 4.43, two-tailed Po0.01), a strict interpretation of this result indicates only that there was a consistently non-zero relationship between time of day and nest attendance among the social units monitored. Closer inspection of these data revealed that, across social units, both positive and negative relationships occurred between these variables. Further, significant correlations between time of day and percentage of time that the nest was unattended were detected for only 2 (7.7%) of the 26 social units monitored, indicating that, within social units, nest use by adults was not strongly temporally patterned. Given these findings, we did not partition the data according to date or time of day at which scans were completed. Instead, for each social unit, all scans were pooled for the following analyses of nest attendance by adults. Because not all social units in our sample contained an adult male (Table 1), we examined the effects of the presence of a male on patterns of nest attendance by females. A two-way analysis of variance revealed no significant effect of a male on the percentage of time that the nest was unattended (ANOVA: F1,18 ¼ 1.23, P ¼ 0.283). Consequently, we did not distinguish between the sexes but instead used the total number of adults resident in a burrow system for subsequent analyses of the effects of group size on nest attendance. When the total number adults per burrow system was considered, there was a significant effect of social unit size on the percentage of time that no adults were present in the nest (one-way ANOVA: F4,21 ¼ 12.57, Po0.001). Visual inspection of the data suggested that the percentage of time that the nests of lone females were unattended was considerably greater than that for social units containing multiple adults (Fig. 1); post hoc comparisons revealed significant contrasts between data from lone females and those from all other sizes of social unit (Tukey’s HSD tests, all Po0.01), suggesting that the primary determinant of the percentage of time that a nest is left unattended is the presence of one versus multiple adults in a burrow system. Accordingly, although the percentage of time that the nest was unattended declined significantly as a function of the number of adults in a burrow system when all social units were considered (R2 ¼ 0.533, N ¼ 26, F1,25 ¼ 27.35, Po0.001; Fig. 1), no significant relationship between number of adults and percentage of time the
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Fig. 1. Percentage of time that nests of C. sociabilis were unattended (no adult present) as a function of the total number of adults resident in a burrow system. Data are from 26 social units monitored during 1996–2000. Burrow systems containing an adult male are indicated. The regression line indicates a significant (Po0.001) negative relationship between number of adults and percentage of time the nest was unattended.
nest was unattended was detected among social units containing X2 adults (R2 ¼ 0.114, N ¼ 17, F1,15 ¼ 1.94, P40.100).
Discussion Our data indicate that nest attendance by free-living C. sociabilis was influenced by the number of adults that shared a burrow system. When all social units were considered, the percentage of time that the communal nest was unattended (no adults present) decreased significantly as the number of adults per burrow system increased. The presence of an adult male appeared to have no effect on the percentage of time that the nest was unattended. When the number of adults per social unit was considered regardless of sex, the only significant contrasts detected were between lone females and social units containing multiple adults. Thus, the greatest effect of communal nesting on nest attendance occurred with the addition of a second adult to social units containing only a single female. Reducing the time that the nest is unattended may be beneficial to juveniles in several ways. In general, because the presence of an adult is essential to many forms of parental care, increasing the percentage of time during which at least one adult is present in the nest may increase the overall availability of such care, potentially leading to enhanced juvenile growth and survival (Hayes and Solomon 2006). More specifically, the presence of one or more adults may have thermoregulatory benefits for young; juvenile ctenomyids do not thermoregulate effectively until they are more than 15 days old (Cutrera
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et al. 2003; Zenuto et al. 2002) and, hence, regular nest attendance may reduce the chances of hypothermia of young. At the same time, the presence of an adult may increase the tendency for pups to remain inside the nest (M. Soares, pers. comm.), thereby decreasing the risk of predation as well as hypothermia. If, as these arguments suggest, the regular presence in the nest of X1 adult increases juvenile survival, then decreasing the time that the nest is unattended may be an adaptive consequence of group living in C. sociabilis. If increased nest attendance is an adaptive benefit of group living, why do individuals in multi-female social units rear fewer young to weaning than lone females? On an annual basis, the per capita direct fitness of female C. sociabilis declines significantly as a function of group size (Lacey 2004), indicating that social units in which nest attendance by adults is greater produce fewer surviving pups per female. Communal nesting is a complex social phenomenon that likely reflects the combined effects of multiple selective factors that confer both benefits and costs on animals that live and rear their young together (Alexander 1974; Hayes 2000). As a result, while increasing nest attendance may improve juvenile survival, other aspects of communal nesting (e.g., reproductive skew, infanticide, and other manifestations of increased competition among burrow-mates: Alexander 1974; Clutton-Brock 1998; Ebensperger 1998; Woodroffe and Macdonald 2000) may counter this potential fitness gain. Hence, to understand the net fitness consequences of communal nesting, it is necessary to consider the full range of selective pressures leading to this behavior. Future studies of communal nesting in C. sociabilis will address this issue by exploring other mechanisms (e.g., communal nursing) by which young may benefit from increased parental presence, as well as by exploring the fitness consequences to adults of sharing a nest with conspecifics.
Acknowledgements For permission to work on Estancia Rincon Grande, we thank Alain Thouyaret and the Delegacio´n Tecnica de Parques Nacionales Argentinas, in particular Claudio Chehebar and Eduardo Ramilo. For logistic assistance, we thank Miguel Christie, Gustavo Iglesias, and the members of the Sociedad Naturalista Andino Patagonica in Bariloche, Argentina. Field assistance was provided by A. Chiesa, I. Tomasco, and, in particular, M. Soares and J. Wieczorek. Previous versions of this manuscript benefited from comments by G. Francescoli, M. Hauber, M. Soares, and J. Wieczorek. Melitta Meneghel kindly translated the abstract to German. Financial support was provided by the Comision Sectorial de Investigacion Cientifica and Programa de Desarrollo de las Ciencias Ba´sicas (Uruguay), and the
Museum of Vertebrate Zoology and Department of Integrative Biology at the University of California, Berkeley. This work was conducted in compliance with all relevant institutional, national, and international regulations.
Zusammenfassung Einfluss der Gruppengro¨ße auf die Nestanwesenheit kolonialer Tucotucos (Ctenomys sociabilis) Gemeinschaftliche Jungenaufzucht wird als adaptiv angenommen, wenn es den Individuen, die dasselbe Nest benutzen, einen Fitnessvorteil verleiht. Dieser Vorteil kann direkt fu¨r die adulten Tiere nu¨tzlich sein oder deren Fitness durch la¨ngere U¨berlebensrate ihrer Nachkommen beeinflussen. Insbesondere Jungtiere, die in gemeinschaftlichen Gruppen aufgezogen wurden, du¨rften eine la¨ngere U¨berlebensrate durch die ha¨ufigere Anwesenheit mehrerer pflegeversorgenden Adulten haben. Es wurden radiotelemetrische Analysen durchgefu¨hrt, um zu pru¨fen, wie gemeinschaftliche Vermehrung mit erho¨hter Anwesenheit adulter Tiere in Verbindung steht, um damit die Hypothese zu testen, dass das Anwesenheitsmuster adulter Tiere im Nest abha¨ngig von der Gruppengro¨ße freilebender kolonialer Tucotucos (Ctenomys sociabilis) ist. Die Bausysteme dieses sozialen, unterirdischen Nagetieres werden von 1–6 adulten Weibchen und in einigen Fa¨llen von einem einzigen adulten Ma¨nnchen bewohnt. Die Daten, die wir von 1996 bis 2000 von 26 u¨berwachten Bausystemen erhielten, deuteten an, dass die Zeit, in der das Nest ohne adulte Tiere zwischen Geburt und Absetzen war, nicht von Datum oder Tageszeit abhing. Die Zeit, in der das Nest unbeaufsichtigt war, verminderte sich mit der Zunahme an erwachsenen Tieren fu¨r jedes Bausystem erheblich. Als die Zeit, in der das Nest unbegleitet war, fu¨r solita¨re Weibchen mit der von Gruppen mehrerer Weibchen verglichen wurde, war der Unterschied offensichtlich. Es wird vorgeschlagen, dass zunehmende Nestanwesenheit eine wichtige Rolle fu¨r das U¨berleben von Jungtieren, die in ‘‘Multi-Erwachsenen’’-Bausystemen aufgezogen werden, spielt. Dieses ko¨nnte jedoch mit den Fitnessfolgen anderer Kosten und Vorteile, die mit der gemeinsamen Jungenaufzucht in dieser Art verbunden sind, verwechselt werden.
References Alexander, R.D., 1974. The evolution of social behavior. Ann. Rev. Ecol. Syst. 5, 325–388. Baker, P.J., Robertson, C.P.J., Funk, S.M., Harris, S., 1998. Potential fitness benefits of group living in the red fox, Vulpes vulpes. Anim. Behav. 56, 1411–1424.
ARTICLE IN PRESS G. Izquierdo, E.A. Lacey / Mamm. biol. 73 (2008) 438–443
Bozinovic, F.M., Rosenmann, M., Veloso, C., 1988. Termorregulacio´n conductual en Phillotis darwini (Rodentia: Cricetidae): efecto de la temperatura ambiente, uso de nidos y agrupamiento social sobre el gasto de energı´ a. Rev. Chil. Hist. Nat. 61, 81–86. Brown, J.S., Burt, P., 2004. Hazardous duty pay and the foraging cost of predation. Ecol. Lett. 7, 999–1014. Clutton-Brock, T.H., 1998. Reproductive skew, concessions, and limited control. Trends Ecol. Evol. 13, 288–292. Cutrera, A.P., Antinuchi, C.D., Busch, C., 2003. Thermoregulatory development in pups of the subterranean rodent Ctenomys talarum. Physiol. Behav. 79, 321–330. Doolan, S.P., Macdonald, D.W., 1999. Cooperative rearing by slender tailed meerkats (Suricata suricatta) in the southern Kalahari. Ethology 105, 851–866. Ebensperger, L.A., 1998. Strategies and counterstrategies to infanticide in mammals. Biol. Rev. Cambridge Philos. Soc. 73, 321–346. Ebensperger, L.A., Wallen, P.K., 2002. Grouping increases the ability of the social rodent, Octodon degus, to detect predators when using exposed microhabitats. Oikos 98, 491–497. Gittleman, J.L., 1985. Functions of communal care in mammals. In: Greenwood, P.J., Harvey, P.H., Slatkin, M. (Eds.), Evolution: Essays in Honour of John Maynard Smith. Cambridge University Press, Cambridge, pp. 187–205. Hayes, L.D., 2000. To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Anim. Behav. 59, 677–688. Hayes, L.D., Solomon, N.G., 2004. Costs and benefits of communal rearing to female prairie voles (Microtus ochrogaster). Behav. Ecol. Sociobiol. 56, 585–593. Hayes, L.D., Solomon, N.G., 2006. Mechanisms of maternal investment by communal prairie voles, Microtus ochrogaster. Anim. Behav. 72, 1069–1080. Hoogland, J.L., 1995. The Black-Tailed Prairie Dog: The Social Life of a Burrowing Mammal. University of Chicago Press, Chicago. Jacquot, J.J., Vessey, S.H., 1994. Non-offspring nursing in the white-footed mouse, Peromyscus leucopus. Anim. Behav. 48, 1238–1240.
443
Lacey, E.A., 2004. Sociality reduces individual direct fitness in a communally breeding rodent, the colonial tuco-tuco (Ctenomys sociabilis). Behav. Ecol. Sociobiol. 56, 449–457. Lacey, E.A., Ebensperger, L.A., 2007. Social structure in octodontid and ctenomyid rodents. In: Wolff, J.O., Sherman, P.W. (Eds.), Rodent Societies: An Ecological and Evolutionary Perspective. University of Chicago Press, Chicago, IL, USA, pp. 403–415. Lacey, E.A., Wieczorek, J.R., 2003. The ecology of sociality in rodents: a ctenomyid perspective. J. Mammal. 84, 1198–1211. Lacey, E.A., Wieczorek, J.R., 2004. Kinship in colonial tucotucos: evidence from group composition and population structure. Behav. Ecol. 15, 988–996. Lacey, E.A., Braude, S.H., Wieczorek, J.R., 1997. Burrow sharing by colonial tuco-tucos (Ctenomys sociabilis). J. Mammal. 78, 556–562. Lewis, S.E., Pusey, A.E., 1997. Factors influencing the occurrence of communal care in plural breeding mammals. In: Solomon, N.G., French, J.A. (Eds.), Cooperative Breeding in Mammals. Cambridge University Press, Cambridge, pp. 335–363. Macdonald, D.W., 1981. Dwindling resources and the social behaviour of capybaras (Hydrochoerus hydrochaeris) (Mammalia). J. Zool. (London) 194, 371–391. Manning, C.J., Dewsbury, D.A., Wakeland, E.K., Potts, W.K., 1995. Communal nesting and nursing in house mice, Mus musculus domesticus. Anim. Behav. 50, 741–751. Pilastro, A., 1992. Communal nesting between breeding females in a free-living population of fat dormouse (Glis glis L). Boll. Zool. 59, 63–68. Trune, D.R., Slobodchikoff, C.N., 1976. Social effects of roosting on the metabolism of the pallid bat (Antrozous pallidus). J. Mammal. 57, 656–663. Woodroffe, R., Macdonald, D.W., 2000. Helpers provide no detectable benefits in the European badger (Meles meles). J. Zool. (London) 250, 113–119. Zar, J.H., 1999. Biostatistical Analysis. Prentice-Hall, New Jersey. Zenuto, R.R., Antinuchi, C.D., Busch, C., 2002. Bioenergetics of reproduction and pup development in a subterranean rodent (Ctenomys talarum). Physiol. Biochem. Zool. 75, 469–478.