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. Author manuscript; available in PMC: 2012 Feb 10.
Published in final edited form as: J Mammal. 2011;92(1):21–30. doi: 10.1644/09-MAMM-S-383.1

Burrow limitations and group living in the communally rearing rodent, Octodon degus

Luis A Ebensperger 1,*, Adrian S Chesh 1, Rodrigo A Castro 1, Liliana Ortiz Tolhuysen 1, Verónica Quirici 1, Joseph Robert Burger 1, Raúl Sobrero 1, Loren D Hayes 1
PMCID: PMC3277429  NIHMSID: NIHMS351260  PMID: 22328789

Abstract

Group living is thought to evolve whenever individuals attain a net fitness advantage due to reduced predation risk or enhanced foraging efficiency, but also when individuals are forced to remain in groups, which often occurs during high-density conditions due to limitations of critical resources for independent breeding. The influence of ecological limitations on sociality has been studied little in species in which reproduction is more evenly shared among group members. Previous studies in the caviomorph rodent Octodon degus (a New World hystricognath) revealed no evidence that group living confers an advantage and suggest that burrow limitations influence formation of social groups. Our objective was to examine the relevance of ecological limitations on sociality in these rodents. Our 4-year study revealed no association between degu density and use of burrow systems. The frequency with which burrow systems were used by degus was not related to the quality of these structures; only in 1 of the 4 years did the frequency of burrow use decrease with decreasing abundance of food. Neither the number of females per group nor total group size (related measures of degu sociality) changed with yearly density of degus. Although the number of males within social groups was lower in 2008, this variation was not related clearly to varying density. The percentage of females in social groups that bred was close to 99% and did not change across years of varying density. Our results suggest that sociality in degus is not the consequence of burrow limitations during breeding. Whether habitat limitations contribute to variation in vertebrate social systems is discussed.

Keywords: caviomorph rodents, density, ecological constraints, habitat, hystricognath, sociality

Animal sociality ranges from short-term associations and aggregations (e.g., foraging or roosting groups) to relatively long-term socially cohesive units (e.g., communal rearing groups—Krause and Ruxton 2002; Parrish et al. 1997). Social interactions that occur over long periods are thought to evolve because group-living individuals attain net fitness advantages in relation to solitary animals (Alexander 1974; Bertram 1978; Ebensperger 2001; Ebensperger and Blumstein 2006; Krebs and Davies 1993). Alternatively, sociality can be the result of limited availability of breeding sites due to high population density, a patchy distribution of critical resources, or a combination of these (Arnold and Owens 1998; Brown 1987; Emlen 1982; Johnson et al. 2002; Koenig et al. 1992; Waser 1988). Generally referred to as the ecological limitations (or constraint) hypothesis, this model states that limited availability of resources essential for independent breeding determines that the direct fitness cost of remaining philopatric (i.e., social) is small compared to the costs and risks of dispersal (i.e., leaving the group to live and reproduce independently—Emlen 1982 i.e., leaving the group to live and reproduce independently—Emlen 1995). Thus, the ecological limitations hypothesis predicts that sociality increases with increasing density of conspecifics and with decreasing availability of resources essential for breeding. From a proximate perspective the ecological limitations hypothesis states that changes in sociality (e.g., group size) are driven mainly by natal philopatry as opposed to other demographic processes such as immigration (Ebensperger and Hayes 2008; Emlen 1995). Establishing the relative importance of adaptation and constraints on the evolution of group living and subsequent variation in group size and composition is a major goal of sociality theory.

Most support for the ecological limitations hypothesis comes from studies of singularly breeding vertebrates (sensu Solomon and Getz 1997). In groups of singular breeders reproduction is dominated by a male–female pair, whereas offspring are reared communally. Thus, a variable number of nonbreeding adults, typically (but not always) previous offspring of the breeding pair (Ekman et al. 2004; Solomon and Getz 1997), contribute by giving care to the offspring of breeders. Observational studies on singularly breeding fishes and birds have reported links between habitat availability and philopatry or group size (Bergmüller et al. 2005; Buston 2003; Carrete et al. 2006; Moreira 2006; Russell 2001; Woolfenden and Fitzpatrick 1984). In addition, several studies on birds suggest that formation of social groups increases at high population densities but decreases when critical space needed for breeding (e.g., cavities) is enhanced experimentally (Komdeur et al. 1995; Pruett-Jones and Lewis 1990; Walters et al. 1992). Taken together, evidence from singularly breeding vertebrates indicates that ecological limitations to independent breeding can enforce sociality.

The ability of the ecological limitations hypothesis to explain group living in mammals has been questioned. The available evidence for mammals is meager (Russell 2004), and life-history traits related to reproduction would make mammals less likely to be constrained than other vertebrates (Mumme 1997). Also, the applicability of this hypothesis appears to vary even within bird species or lineages (Doerr and Doerr 2006; Hatchwell and Komdeur 2000), implying that such variation might also apply to other vertebrates such as mammals. However, theoretical and empirical considerations suggest that ecological constraints can apply to social mammals. Mammals include species that use specialized burrows for living and rearing young (Hayes 2000). The relatively high energetic costs and risks of burrow construction and maintenance (Ebensperger and Bozinovic 2000) can constrain dispersal and force individuals to share these specialized structures (Jarvis et al. 1994; White and Cameron 2009). Correlative and experimental studies support a positive association between the formation of social groups and population density in at least 3 singularly breeding rodents (Cochran and Solomon 2000; Lucia et al. 2008; Powell and Fried 1992; Randall et al. 2005). For 2 of these species (Microtus pinetorum and Rhombomys opimus) underground burrows are essential for breeding, and the authors imply that abundance and quality of these structures can be a limiting resource (Powell and Fried 1992; Randall et al. 2005).

In contrast to singular breeding, in plurally breeding species groups multiple females breed and provide care to offspring communally (Hayes 2000; Lewis and Pusey 1997). The role of habitat limitations among social vertebrates known to breed plurally has been studied less than it has been in singularly breeding species. However, evidence supports an influence for habitat limitations in some species. Both group living and communal rearing of offspring increases with density conditions in at least 2 species of rodents (Peromyscus leucopus and P. maniculatus—Wolff 1994). The implication of these findings is that density can influence the formation of groups without compromising breeding activity of group members. More recently, it has been reported that availability of burrows does not influence communal nesting in warthogs (Phacochoerus africanus—White and Cameron 2009). Although intriguing, these findings imply that more attention to plurally breeding vertebrates (and mammals in particular) is needed to determine the extent to which limitations to independent breeding (if any) influence sociality and whether this factor imposes a fitness cost to group members. The objective of this study was to examine the role of ecological limitations in explaining group living in a burrowing, plurally breeding mammal. In particular, we examined whether burrow limitations due to high population density influence the tendency of semifossorial degus (Octodon degus) to form social groups.

Degus are New World hystricognaths, medium-sized rodents (about 180 g body mass) that feed mostly on grasses and forbs, breed once per year, and in which multiple lactating females share underground nests and rear their litters communally (Ebensperger et al. 2002, 2004, 2007). A recent study did not support roles for decreased predation risk or foraging benefits as benefits of group living in degus (Hayes et al. 2009). This study showed that group living does not enhance number of offspring produced per capita or survival of the young (Hayes et al. 2009). These direct-fitness patterns are more consistent with the ecological limitations hypothesis.

Some features of degus suggest that burrows could be a limiting factor. Members of social groups share a variable number of burrow systems, which include nest sites for rearing their offspring communally (Ebensperger et al. 2004; Soto-Gamboa 2004), and larger social groups use more burrows than do smaller groups (Hayes et al. 2009). Degus, which are diurnally active, use these underground burrows to hide from predators (Lagos et al. 2009). As in other semifossorial rodents (Taraborelli 2009), burrow systems of degus persist over a span of ≥5 years (L. A. Ebensperger, and L. D. Hayes, pers. obs.). Therefore there may be times, as during periods of high density, when the number of burrows is limited.

Other evidence, however, casts some doubts on the previous interpretation. Although degus live in year-round social groups, these groups are short-lived; only 31% of social groups persist from one year to the next (Ebensperger et al. 2009). Most critical, and contrary to predictions from the ecological limitations hypothesis, immigration seems to play an important role in determining the composition of social groups compared to adult fidelity and offspring philopatry (Ebensperger et al. 2009).

In summary, if burrows limit dispersal of young, enforce group living, and ultimately decrease independent breeding in degus, we expect use of individual burrows to increase with increasing degu density. Because burrow systems differ in quality and quantity (Komdeur et al. 1995; Stacey and Ligon 1991; White and Cameron 2009), high-quality burrows could be more important to degus than total number of burrows. Therefore, we also expect use of individual burrows to increase with increasing burrow quality. As a result, with increasing degu density we also expect size of social groups to increase and proportion of breeding females within social groups to decline.

Materials and Methods

Study site

The study was conducted between 2005 and 2008, in months when females are gravid and lactating (June–October), on a natural population of degus at the Estación Experimental Rinconada de Maipú, a field station of Universidad de Chile. This study area is characterized by a Mediterranean climate with cold, wet winters and warm, dry summers. Data from the Pudahuel weather station (Dirección Meteorológica de Chile, Santiago, Chile), 15 km from the Rinconada field station, indicate that mean annual rainfall was 239 mm during 2005–2008, most of which (73% on average) was during the austral winter, from June to August. Mean monthly temperature (8.9°C) is relatively low from June to August and highest from December to March (19.6°C).

We designated as our study site a 4- to 5-ha area in a locality known as Pajaritos (33°23′S, 70°31′W, altitude 495 m) and in which degus were sighted frequently. We established 2 grids approximately 150 m apart. The grids were characterized by a similar distribution of grasses, forbs, and shrubs and covered 0.18 ha (30 × 60 m; grid 1) and 0.25 ha (50 × 50 m; grid 2), respectively.

Our study involved 2 stages. First we conducted grid trapping to determine density of the population in June, and then in August–October we determined social group composition using telemetry to locate degus at night and trapping at burrow entrances in the morning. No trapping relevant to this study was conducted in July. Grid trapping was restricted to the 2 grids, but night telemetry and morning burrow trapping were extended to a larger area because of the natural movement of social groups (Burger et al. 2009; see below).

Grid trapping and radiocollaring

We conducted grid trapping to estimate density on the 2 study grids during mid-June (late austral fall). Degus were captured using locally produced metal live traps (9.5 × 10 × 30 cm, similar to Sherman live traps [H. B. Sherman Traps, Inc., Tallahassee, Florida] in design) baited with rolled oats. Traps were set at fixed stations at 5-m intervals, resulting in 91 traps (7 × 13 array) on grid 1 and 121 traps (11 × 11 array) on grid 2. Traps were opened for 5 days during the morning (0800 h) prior to emergence of degus from burrows and closed after 3 h. We determined sex, body mass (to 0.1 g), and reproductive condition of females (whether they had perforate vaginas—an indicator of sexual receptivity, were gravid, or were lactating) for each degu. Gravid females typically had enlarged abdomens, and fetuses could be detected easily by gentle palpation. Lactation was recorded if a female exhibited milk after we gently squeezed 2 randomly selected nipples. We estimated degu density on each grid by dividing the total number of individual degus caught through the 5 days of trapping by the area covered by the grid (grid 1 = 0.18 ha; grid 2 = 0.25 ha). Density estimates for the 2 grids were averaged for each year.

Adults weighing >170 g were fitted with 8-g radiocollars (BR radiocollars; AVM Instrument Co., Colfax, California) or 7- to 9-g radiotransmitters (RI-2D; Holohil Systems Limited, Carp, Ontario, Canada, and SOM-2190A; Wildlife Materials Incorporated, Murphysboro, Illinois) with unique pulse frequencies. Later, as additional degus were trapped during burrow trapping, they also were given radiocollars. All radiocollars were removed from radiocollared degus during late October.

We assigned each adult degu a unique identification number and marked it at 1st capture by removing the 1st or 2nd phalanges of 1–4 toes, no more than 1 toe per foot (Hayes et al. 2009; Quirici et al. 2010). We used toe clipping because of the need to permanently mark a large number of individuals required to quantify spatial patterns (Ebensperger et al. 2009; Hayes et al. 2007) and reproduction (Hayes et al. 2009; Quan et al. 2009). We minimized pain by making rapid cuts with sharp sterilized clippers. In the event that an individual was bleeding (estimated <20%), we applied light pressure to stop bleeding before an individual was released. We applied a topical antibiotic to reduce the risk of subsequent infections. Infections were extremely rare (1 infection for every 100 degus clipped). Tissue samples (toe clippings) were kept for genetic analyses (Quan et al. 2009). This study followed the guidelines of the American Society of Mammalogists (Gannon et al. 2007) and was approved by the Institutional Animal Care and Use Committee of University of Louisiana at Monroe and adhered to laws of the United States and Chile (permit 1–58.2005 [2711] by the Servicio Agrícola y Ganadero).

Burrow trapping, night telemetry, and determination of social groups

Degus are diurnally active and remain in underground burrows during the night (Ebensperger et al. 2004). Thus, the main criterion used to assign degus to social groups was the sharing of burrow systems during the night (Ebensperger et al. 2004; Hayes et al. 2009). To determine which degus shared burrows we used night telemetry (to identify which degus were in the burrow) and morning trapping, both conducted in August–October (to identify degus as they emerged from burrows).

During night telemetry radiocollared adults were located from above the ground as they rested in burrows at night. Telemetry was conducted once per night and began approximately 1 h after sunset. We used an LA 12-Q receiver (for radiocollars tuned to 150,000–151,999 MHz frequency; AVM Instrument Co.) and a handheld, 3-element yagi antenna (AVM Instrument Co.).

For burrow trapping we defined a burrow system as a group of burrow openings around a central location, with the systems having a diameter of 1–3 m (Fulk 1976; Hayes et al. 2007). Because of the natural distribution and movement of the degus during the study, burrow systems were trapped over an area that varied in size from year to year and included the 2 density grids and area around each of them. The total area sampled ranged from 0.61 to 2.16 ha across years of study.

In burrow trapping live traps (model 201 Tomahawk; Tomahawk Live Trap Company, Tomahawk, Wisconsin) were set near burrow entrances before adults emerged from burrows in the morning (0600 h). After 1.5 h the identity and location of all captured degus were determined, and traps were closed until the next early morning trapping. As for grid trapping, we determined sex, body mass (to 0.1 g), reproductive condition of females (perforate, gravid, or lactating), and individual identification of degus.

To determine group composition we compiled a symmetrical similarity matrix of pairwise association of burrow locations for all adult degus detected by burrow trapping and night telemetry (Whitehead 2008). We determined the association (overlap) between every pair of individuals by dividing the number of times that the 2 degus were captured at or tracked with telemetry to the same burrow system by the total number of times that both individuals were detected by trapping or telemetry in the same trapping day or telemetry night (Ebensperger et al. 2004). Adult degus were considered to associate with a given social group if they overlapped in ≥10% of the same trapping or telemetry sessions with other individuals in the group (Hayes et al. 2009). Animals with <10% overlap were not considered part of the same group; typically, degus overlap 50% or more with other group members (Ebensperger et al. 2004; Hayes et al. 2009).

Burrow quantity

We considered 2 complementary measures of the extent to which burrows were used (i.e., limited, or not available to other individuals) in terms of quantity. We monitored burrow systems that were used repeatedly by individuals radiocollared during density trapping. To this sample we added a variable number of randomly selected burrow systems that exhibited fresh droppings at their burrow entrances and where animals were seen active nearby. Upon determining social groups, we categorized burrow systems as in use or vacant. Burrow systems considered to be in use were those in which group members were repeatedly trapped and located during night telemetry; those considered to be vacant were those with no records of captures and those in which a minority of group members were trapped infrequently or found only occasionally during night telemetry. Burrow systems were categorized as in use (i.e., occupied) or vacant for each year of the study. This population-level, quantitative measure of burrow system availability provided only 4 temporal replicates (1 per year).

Because a variable number of degu captures were recorded in both used and vacant burrow systems, we complemented this population-level approach with another that examined use of individual burrows. In particular, we used yearly data from burrow trapping to quantify use of burrows as the total number of captures per burrow system, standardized by the number of traps used and days of trapping at each burrow. Thus, this burrow-level measure included the total number of burrow systems sampled (used and vacant). The total number of burrow systems examined in our population every year (Table 1) represented a compromise between the natural movement of animals and our logistic ability to monitor a relatively large number of burrow systems.

Table 1.

Trapping and radiocollaring effort of degus (Octodon degus) in central Chile for each year of the study.

Year
2005 2006 2007 2008
Total no. adults trapped and assigned to a social group 82 65 60 44
No. radiocollared individuals 30 16 34 21
Locations per radiocollared individual (± SE) 24.8 ± 1.8 34.0 ± 3.2 18.3 ± 4.2 16.0 ± 0.9
No. burrow systems trapped 32 58 32 43
No. trapping days per burrow system (± SE) 16.8 ± 0.5 17.3 ± 0.5 31.4 ± 1.2 45.3 ± 1.6
No. traps used per burrow system (± SE) 11.9 ± 0.2 11.9 ± 0.2 9.7 ± 0.2 8.0 ± 0.1
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Burrow quality

To examine whether quality of burrows influences use by degus, we recorded 3 ecological attributes of burrows that we thought reflected their quality: abundance of preferred food, hardness of soil, and density of openings at each burrow system. We considered burrow quality to increase with increasing abundance (biomass) of preferred food—grasses and forbs (Meserve et al. 1983). We considered harder soils to be of lower quality, because burrowing costs for degus increase with hardness of soil (Ebensperger and Bozinovic 2000). Predation risk for degus increases with distance to the nearest burrow entrance (i.e., safe havens—Lagos et al. 2009), so we considered burrow systems with more openings per unit area to be safer and of higher quality. We did not find any other species that potentially could affect the quality of burrows to be permanent residents of burrows.

Ecological sampling was conducted during early spring (September and October) when most offspring began to emerge from burrows to forage aboveground. To track changes in the abundance of primary food (Meserve et al. 1983) we collected samples of green forbs and grasses at 3 and 9 m from the center (a point located centrally between entrances) of each burrow system in the north, east, south, or west directions. We placed a 250 × 250-mm quadrat at each sampling point and removed the aboveground parts of all green forbs and grasses within the quadrat. Samples were stored immediately inside 2-kg-capacity paper bags. In the laboratory we oven-dried each plant sample at 60°C for 72 h to determine its dry mass (biomass in g—Ebensperger and Hurtado 2005). We used the same sampling pattern to record soil penetrability as an index of soil hardness (Lacey and Wieczorek 2003). Soil penetrability was recorded with the use of a handheld soil compaction meter (Lang Penetrometer Inc., Gulf Shores, Alabama). The penetrometer expressed pressure in units of pounds (of force) per square inch (psi), which we converted to SI pressure units, kPa. We 1st used the equivalence of 1 psi = 87.55 × spring elongation reading (inches), obtained from load and elongation data (available at http://www.langanalytical.com/). Then, we converted psi units into kPa with the equivalence of 1 psi = 6.894 kPa (Pennycuick 1988). Density of burrow openings (number/m2) at each burrow system was determined by quantifying the number of burrow openings in a circular area with a radius of 9 m from the center of burrow systems.

Reproductive status of females

Females were categorized as reproductive (gravid or lactating) or nonreproductive. We categorized as gravid those females with an increase in body mass of about 50–100 g between August and September. The transition from pregnancy to lactation was detected easily, as females lost body mass between consecutive captures and milk was present in the nipples. The total number of adult females in this analysis was 53, 43, 45, and 38 in 2005, 2006, 2007, and 2008, respectively.

Statistical analysis

Before we analyzed data we ranked yearly estimates of degu population density from 1 to 4, with 1 the lowest density and 4 the highest. We then conducted nonparmetric correlation analysis (Spearman rank correlation, rs) between ranks of increasing degu density and percentage of burrows systems that were vacant, that is, our population-level estimate of available burrows. Given the overall low sample size involved (1 data point per year of study), we treated this analysis as qualitative. Assumptions of normality and homoscedasticity, assessed with the use of Kolmogorov–Smirnov tests and Cochran Q-tests, respectively, were not met for data on burrow use, so we used Kruskal–Wallis analysis of variance (H), followed by nonparametric multiple comparison tests (Siegel and Castellan 1988) to examine whether burrow use changed across an increasing rank of yearly density. We then used a nonparametric Spearman rank correlation test to verify whether burrow use was influenced by ecological attributes of burrow quality: food abundance, soil hardness, and density of burrow openings.

We used 1-way parametric analyses of variance to examine variation in total group size and number of females per social group across yearly density conditions. Variation in the number of males per social group was examined using the Kruskal-Wallis test, followed by nonparametric multiple comparisons tests. The Kruskal–Wallis test also was used to verify whether the proportion of females that bred within their social groups changed across years. All data are reported as means ± SE. Analyses were conducted using Statistica 9.0 (StatSoft Inc., Tulsa, Oklahoma).

Results

Burrow quantity and quality

Population density varied from 63 to 215 individuals and was unrelated to quantity or quality of burrows that were in use. At a population level the proportion of burrows used was highest in 2007 at 88% and lowest in 2006 at 40% (Table 2). However, no association was found between the proportion of burrows used each year and degu density (rs = 0.40, n = 4, P = 0.60). Additionally, no trend was apparent from scanning of data. Similarly, at a level of individual burrows we found no overall association between yearly population density and burrow use. Although burrow use in 2008, the year with the lowest degu density, was significantly lower than burrow use in 2005 and 2007, it was similar to burrow use in 2006, the year with the 2nd highest population density (H3,167 = 17.87, P < 0.001, and nonparametric multiple comparison tests, P < 0.05; Table 2).

Table 2.

Population density and quantity and quality of burrows for a population of degus (Octodon degus) in central Chile. Burrow quantity was measured by percentage of available burrows used and by number of degus using each burrow. Burrow quality was measured by abundance of food (grasses and forbs) and by soil hardness—each at 3 m and 9 m from center of main burrow system—and by density of openings into burrow system. Sample sizes are given in Table 1.

Year
2005 2006 2007 2008
Population density (degus/ha) 133 199 215 63
Burrow quantity
 Percentage of burrow systems used 84 40 88 65
 Burrow use (captures per trap-day; ± SE) 0.16 ± 0.02 0.16 ± 0.02 0.17 ± 0.03 0.11 ± 0.03
Burrow quality
 Abundance of food at 3 m from main burrow system (g/m2; ± SE) 128.4 ± 10.9 91.8 ± 8.4 107.2 ± 10.8 119.2 ± 10.0
 Abundance of food at 9 m from main burrow system (g/m2; ± SE) 154.4 ± 11.1 85.0 ± 8.6 106.3 ± 10.9 114.9 ± 10.2
 Soil hardness at 3 m from main burrow system (kPa; ± SE) 10,474 ± 93 11,102 ± 72 11,068 ± 92 11,440 ± 85
 Soil hardness at 9 m from main burrow system (kPa; ± SE) 10,403 ± 96 11,149 ± 74 11,132 ± 95 11,386 ± 88
 Density of burrow openings (no./m2; ± SE) 0.13 ± 0.01 0.13 ± 0.01 0.14 ± 0.01 0.11 ± 0.01
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The number of entrances to burrow systems for all years combined ranged from 6 to 71 per burrow system. Density of burrow openings had a range of 0.024–0.283 openings/m2 and did not differ significantly with year of study (H3,157 = 6.37, P = 0.095). Food abundance at 3 m from individual burrow systems was variable, ranging from 0 to 347 g/m2. The mean value in 2006 was significantly lower than in 2005 but similar to means for 2007 and 2008 (H3,157 = 9.87, P = 0.0197; and for all nonparametric multiple comparison tests, P < 0.02; Table 2). At 9 m from main burrow systems food abundance ranged from 0 to 355 g/m2. Mean value for food at 9 m was higher in 2005 than in 2006 and 2007 but similar to mean for food in 2008 (H3,157 = 21.20, P = 0.0001, and for all nonparametric multiple comparison tests, P < 0.04; Table 2). Hardness of soil at 3 m from main burrow systems ranged from 502,287 to 695,130 kg/m2. This measure was significantly lower in 2005, higher in 2008, and intermediate in 2006 and 2007 (H3,157 = 43.40, P < 0.0001, and for all nonparametric multiple comparison tests, P < 0.02; Table 2). Hardness of soil at 9 m from main burrow systems ranged from 511,557 to 690,645 kg/m2. This measure was significantly lower in 2005 than in 2006, 2007, and 2008 (H3,157 = 43.01, P < 0.0001, and nonparametric multiple comparison tests, P < 0.001; Table 2).

We found no statistically significant associations between burrow use and food (at 3 or 9 m), soil hardness (at 3 or 9 m), or density of burrow openings in 2006, 2007, and 2008 (P > 0.06 for all correlations). In 2005 burrow use decreased with increasing abundance of green herbs at 3 m from main burrows (rs = −0.39, n = 32, P = 0.028). No other associations examined in 2005 were statistically significant (P > 0.15 for all correlations).

Size of social groups and female breeding

Population density did not predict size of social groups nor number of breeding females per social groups. Size of social groups (including females and males) ranged from 2 to 12 adults throughout the study. Groups contained 1–8 females and 0–5 males. Neither number of females (F3,39 = 0.77, P = 0.518) nor total group size (F3,39 = 1.50, P = 0.230) changed across yearly estimates of degu density (Fig. 1). In contrast, number of males per social group was significantly lower in 2008, the year with the lowest degu density, than in 2005, the year with the 3rd highest degu density recorded, but similar to males in 2006 and 2007 (H3,43 = 9.49, P = 0.024, and nonparametric multiple comparison tests, P < 0.05; Fig. 1).

Fig. 1.

Fig. 1

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Size of social groups in years of different population density in a natural population of Octodon degus in central Chile. Bars indicate number of adult members (total, females, and males) of social groups, arranged by rank of increasing population density. Yearly estimates of degu density were obtained from 2 trapping grids and were 133, 199, 215, and 63 degus/ha in 2005, 2006, 2007, and 2008, respectively. A total of 13, 11, 9, and 10 social groups were identified and examined in 2005, 2006, 2007, and 2008, respectively. Bars with the same lowercase letters indicate no statistically significant difference in group size within totals, females, or males. Data are means ± SE.

All female members of social groups bred in 2007 and 2008. The proportion of females that bred within their social groups reached 0.981 ± 0.015 in 2005 and 0.977 ± 0.016 in 2006. Statistically, proportions across years were not different (H3,43 = 1.65, P = 0.649).

Discussion

Contrary to our predictions, our population measure of available burrows did not vary with degu density. Burrow use did not clearly increase or decrease with density; burrow use was similarly high in 2005 and 2007, yet density conditions differed by 38% during these years. In contrast, burrow use was similar in 2006 and 2008, yet density differed by 68%. Second, we found little evidence that variation in the quality of burrows affected their use by degus. Only in 1 year (2005) did burrow use decrease with increasing abundance of food (as measured 3 m from main burrow systems), a pattern that contradicted the predicted influence of food abundance on burrow use. Although we cannot eliminate the possibility that relatively high burrow use depleted food at formerly food-abundant main burrows, this trend was noted only in 2005, and for no other measure of burrow quality examined. Moreover, these findings paralleled the observation that abundance of food at burrows used is a poor predictor of group size in degus (Hayes et al. 2009). Third, neither total group size nor number of females per social group (2 related proxies of degu sociality) varied predictably with annual changes in density. Males were less numerous in 2008 (i.e., the year with the lowest density) than in other years, whereas number of females did not differ among years. Fourth, the fraction of females within social groups that bred was close to 100% irrespective of variation in social group size or population density. Pending additional long-term data, these results suggest that limitations in availability of breeding sites do not influence group living in our study population. Based on Mitchell and Dill (2005), we suggest that future studies examine other potentially relevant indicators of quality of breeding habitat in degus, specifically the inner space of underground burrows and its associated physical conditions (e.g., ambient temperature, humidity, and oxygen concentration of air).

From a proximate perspective the seemingly low importance of ecological limitations on burrow availability is consistent with previous findings in degus. Theory predicts that when population density is high and burrows are limited, offspring delay dispersal and remain philopatric at natal sites, resulting in the formation of kin groups (Emlen 1995). Although natal philopatry occurs in degus, immigration of adult males and females also plays a major role in group formation and maintenance (Ebensperger et al. 2009), possibly explaining why social groups consist of both kin and nonkin (Ebensperger et al. 2004). Greater kinship among group members would be expected if offspring followed the expected pattern of delayed dispersal and natal philopatry at high density (Emlen 1995). In this context, observed variation in number of males in social groups remained puzzling. In 2008, the year with the lowest degu density, number of males per group was lower than in years with higher population density (2005–2007). This finding is consistent with males being less constrained in 2008 to remain in social groups. However, juvenile and adult males are known to disperse and emigrate from their natal social groups (Ebensperger et al. 2009), implying that males generally are not forced to remain in their groups of origin. The absence of a relationship between dispersal and density also has been reported in other rodents (Maher 2006).

A potential alternative to the ecological limitations hypothesis is that social groups occur in species with predictable life-history variation. In particular, species characterized by relatively low annual mortality could reach high densities and then saturate the breeding habitat (Arnold and Owens 1998; Hatchwell and Komdeur 2000). Under these conditions low turnover of social groups, and consequently natal philopatry of most offspring, is expected. In contrast to this prediction offspring mortality in degus (based on disappearance) is extremely high (Ebensperger et al. 2009; Le Boulengé and Fuentes 1978), and typically, 80–90% of adults die after 1 breeding season (Meserve et al. 1993). Consequently, social groups are short-lived and characterized by an extensive turnover of members across years (Ebensperger et al. 2009). Second, dispersal and immigration both play important roles in group dynamics compared to adult fidelity and offspring philopatry (Ebensperger et al. 2009). Thus, life-history traits such as annual mortality and density do not hold much explanatory power for social group formation in degus.

Among social mammals, species generally can be categorized as facultative or obligate social breeders depending on their tendency to form groups. For example, facultatively social species of Peromyscus are solitary at low to moderate densities but delay dispersal and form social groups at high density (Wolff 1994). Other taxa such as some canids and other carnivores are obligate social breeders, forming groups regardless of ecological variation (Moehlman 1979). Our results, in combination with previous observations at our study site (Ebensperger et al. 2004, 2007; Hayes et al. 2009), suggest that most female degus live in social groups regardless of ecological variation. Variation in the size and composition of degu social groups is still evident. Our current long-term study is aimed at testing some alternative explanation to this variation, namely that fitness consequences to females are not the same within groups (e.g., breeding success is skewed), or that other ecological factors (such as parasitism) play roles.

Regarding ultimate causation, evidence is accumulating to suggest that fitness consequences of group living vary both within (Brown and Brown 1996; Harrington et al. 1983) and among (Cant 2000; Hoogland 1995; Randall et al. 2005) social species. In particular, negative or neutral fitness consequences are expected in social groups that form due to habitat or other limitations. A density-dependent formation of social groups coupled to neutral fitness consequences of group size supports a role for habitat limitations in some rodents (Randall et al. 2005; Travis et al. 1995; Wolff 1994). Studies on degus have provided little support for this expectation. Although negative and neutral fitness consequences characterize degu social groups (Hayes et al. 2009), the size of these groups does not appear to be influenced by density-driven burrow limitations. However, our estimates of fitness are based on a per capita number of offspring per female. Under habitat limitations direct reproduction might not be shared equally among all group members, a hypothesis that we are currently evaluating with microsatellite tools (Quan et al. 2009). Although >95% of adult females captured appeared to breed during all years of this study, preliminary molecular evidence from 10 social groups observed in 2005 suggests that reproductive success is highly skewed (L. D. Hayes, pers. obs.; P. Quan, pers. comm.). Understanding the relationship between ecological variation, group size, and direct fitness (based on molecular tools) could be the key to understanding degu sociality.

Aside from ecologically based explanations, sociality in degus could represent a case of phylogenetic inertia. Group living seems common within Octodontidae, particularly in the most derived forms, which include degus (Ebensperger et al. 2008). Given that group living is also common within other hystricognath families basal to Octodontidae (Ebensperger and Blumstein 2006; Opazo et al. 2005), comparative studies are needed to determine whether sociality in degus evolved independently or represents an ancestral trait that arose in a context different from that faced by current degu populations.

Overall, the role of ecological limitations as a cause of vertebrate sociality remains largely unresolved. Although correlative and experimental evidence support an effect of ecological limitations in some cooperatively breeding birds, fishes, and mammals (Bergmüller et al. 2005; Carrete et al. 2006; Lucia et al. 2008; Moreira 2006; Woolfenden and Fitzpatrick 1984), controversy persists (Doerr and Doerr 2006; Hatchwell and Komdeur 2000). Existing evidence about the role of habitat limitations among less-studied communal (or plural) breeders also is not consistent (Lucia et al. 2008; White and Cameron 2009).

Acknowledgments

We are indebted to the Universidad de Chile, and particularly to former and current Field Station Administrators J. D. García and M. Orellana Reyes, for providing facilities during fieldwork. We thank M. J. Hurtado, C. León, D. Lahr, J. Childers, and M. Pardue for their assistance. G. Adler, 3 anonymous reviewers, and the special feature editor kindly provided constructive suggestions that improved an earlier version of this article. Funding was provided by the Chilean Fondo Nacional de Desarrollo Científico y Tecnológico grants 1020861, 1060499, and 1090302 to LAE, and by National Science Foundation EPSCoR grant 0553910, Louisiana Board of Regents Research and Development grant LEQSF 2007-09-RD-A-39, and a Percy Sladen Memorial grant to LDH. Other funding sources were the Program 1 of Centro de Estudios Avanzados en Ecología and Biodiversidad (FONDAP 1501-001), the University of Louisiana at Monroe Howard Hughes Medical Institute Program, the Office of Academic Affairs at the University of Louisiana at Monroe, the American Society of Mammalogists, and Sigma Xi, The Scientific Research Society.

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