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Social rank and reproductive performance of pampas deer females (Ozotoceros bezoarticus, Linnaeus, 1758)
Behavioural Processes 105 (2014) 49–52
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Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Social rank and reproductive performance of pampas deer females (Ozotoceros bezoarticus, Linnaeus, 1758) a ˜ Jéssica Tatiana Morales-Pineyrúa , Gabriel Ciappesoni b , Rodolfo Ungerfeld a,∗ a b
Departamento de Fisiología, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay INIA-Las Brujas, Canelones, Uruguay
a r t i c l e
i n f o
Article history: Received 28 December 2013 Received in revised form 4 March 2014 Accepted 5 March 2014 Available online 13 March 2014 Keywords: Dominance Female competition Hierarchy, Social behavior Ruminant
a b s t r a c t Our objectives were to determine if success index of pampas deer females is related with females’ age and if social rank makes any influence on reproductive performance. Female social rank was determined in 18 groups of animals composed of 1 male: 5–9 females (total = 98 females). Date of parturition for each female and sex and birth weight of fawns were recorded for each birth. The females were categorized in three hierarchical ranks: low (<0.33) (group LR), medium (0.33–0.66) (group MR), and high (>0.66) (group HR). The success index increased with age in pampas deer females (P < 0.001). Social rank had no effect on calving success, relative calving dates, sex ratio or body weight at birth. In this study, the success index was related with females’ age, and the reproductive performance did not differ between females of different social ranks. © 2014 Published by Elsevier B.V.
1. Introduction Social deer species live in groups with hierarchical structures (red deer: Clutton-Brock et al., 1982; reindeer: Espmark, 1964; white-tailed deer: Verme, 1983), maintained by agonistic behaviors (Bebié and McElligott, 2006; Jackson, 1985; Thouless and Guinness, 1986). Females’ social rank has been positively related with age in several deer species (Espmark, 1964; Clutton-Brock et al., 1982, 1986; Thouless and Guinness, 1986; Holand et al., 2004). As a consequence of the hierarchical structures, individuals from different social ranks have unequal access to different resources (Clutton-Brock et al., 1982; Espmark, 1964; Verme, 1983), which may result in differences in their reproductive success (Cassinello, 1996). In this sense, in deer, social rank has been positively related to fecundity (Clutton-Brock et al., 1986), date of conception (Clutton-Brock et al., 1984), offspring reproductive success (Clutton-Brock et al., 1984), fawns’ birth weight (Clutton-Brock et al., 1984; Kojola, 1997), and fawns’ survival rate (Clutton-Brock et al., 1984, 1986). It has also been reported that high-ranked females calve a greater proportion of males than low-ranked females (Clutton-Brock et al., 1986). However, it should be considered that most of those data have been obtained in free living deer
∗ Corresponding author at: Departamento de Fisiología, Facultad de Veterinaria, Lasplaces 1550, Montevideo 11600, Uruguay. Tel.: +598 2628 6955; fax: +598 2628 0130. E-mail address: [email protected] (R. Ungerfeld). http://dx.doi.org/10.1016/j.beproc.2014.03.004 0376-6357/© 2014 Published by Elsevier B.V.
populations in which competition for resources may have greater influence on an individual animal’s reproductive biology than in captive populations. The pampas deer is a South American deer categorized as “near threatened” by IUCN (2013), and listed in Appendix I of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES, 2013). In Uruguay there are three populations, two living in wild conditions (González et al., 2002), and one maintained in semi-captive conditions since 1981, located at the Estación de Cría de Fauna Autóctona Cerro Pan de Azúcar (ECFA) (Ungerfeld et al., 2008a). Although the animals maintained at the ECFA have continuous access to sufficient food resources on a year around basis, pampas deer have a seasonal reproductive pattern (Ungerfeld et al., 2008a). The gestation length of the species has been estimated from the rut-birth period in wild populations as slightly more than 7 months (Jackson and Langguth, 1987; Redford and Eisenberg, 1992). Females give birth to a single fawn (Redford, 1987) of approximately 2 kg (Ungerfeld et al., 2008a). Pampas deer groups have hierarchical structures (Ungerfeld et al., 2008b), but no attempts have been made to relate social rank with females’ age and reproductive success. Therefore, the objective of this study was to determine if the success index of pampas deer females is affected by female age and if females’ social rank during the conception period influences calving success, calving date, fawns’ sex ratio and fawns’ birth weight. The study was performed with animals from the ECFA pampas deer population.
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J.T. Morales-Pi˜ neyrúa et al. / Behavioural Processes 105 (2014) 49–52
2. Materials and methods
1.4
e
1.2
2.1. Animals and allocation
d
The study was conducted at the ECFA, Maldonado, Uruguay (34◦ 3 S, 55◦ 1 W; altitude: ∼200 m), where breeding and management of an Ozotoceros bezoarticus arerunguaensis (pampas deer) population started in 1981. Overall, the ECFA comprises 86 ha where only native fauna is bred. The pampas deer are kept in breeding groups composed by one stag and several hinds and their fawns, or single male groups. The offspring are weighed and the sex is recorded during the first 24 h after birth. Animals have the opportunity to graze native pastures and are fed a supplement of 600 g/d/deer of a commercial dairy cow ration that meets the requirements of these animals calculated from the NRC (2007) (∼3% of live weight; a total of 110 g of crude protein and 1.32 MCal of ME). The supplement was offered daily in the morning from Monday to Saturday. All animals were identified with numbered tags. Data were recorded during three consecutive years in six breeding groups housed in separated paddocks (total = 18 groups, 98 females). Each group was composed of one adult male, 5–9 adult females (3–10 years old), and young animals (1–2 years old). The age in years was obtained from the records kept by the ECFA manager. Size of each paddock ranged between 0.5 and 1 ha. All paddocks had abundant water, native pastures, trees and shrubs. 2.2. Determination of social rank On February each year (early breading season) all spontaneous agonistic behaviors between females were recorded as previously described by Freitas-de-Melo et al. (2013). Briefly, focal observations were performed in each group during two periods of 20–40 min, one in the morning (8:00–10:00 am) and one in the afternoon (4:00–6:00 pm), during ten consecutive days (total: 190 h). The observations were performed by two trained observers from a distance of 4 to 8 m (enough distance to avoid disturbing the normal behavior of animals). Inter-observer reliability was tested before the start of the study. Animals received ration at the beginning of the recording periods in three feeding stations in each paddock, separated approximately 2.5–3.0 m each from the other in a triangular arrangement. From these recordings, a success index (SI) for each female was calculated according to Clutton-Brock et al. (1979): SI =
number of individuals displaced number of individuals displaced + number of individuals that displace it
The animals were classified, as in Alvarez et al. (2003) and Barroso et al. (2000), in three categories according to their SI as low (LR; <0.33), medium (MR; 0.33–0.66), or high-ranked (HR; >0.66). Overall, 7251 behavioral agonistic events were recorded, which corresponded to 381.6 ± 43.7/group (mean ± SEM) (range: 93–717). During the recording period each animal interacted 153.4 ± 8.4 times (range: 6–505). Thirty-two females were categorized as HR, 30 as MR, and 35 as LR females. 2.3. Reproductive recordings From August to January of each year (peak of births; Ungerfeld et al., 2008a) all births were recorded, including the date, the fawns’ sex, and fawns’ birth weight. The fawns were weighed and sexed within 24 h of birth. 2.4. Statistical analysis To examine the effect of different factors on success index, a linear mixed model with repeated measures was performed with
Success index
1.0 0.8
cd
0.6
c
ab
0.4 0.2
c bc
a
0.0 2
3
4
5 6 Age (years)
7
8
9
Fig. 1. Plot of success index according to the females’ age in 98 pampas deer females (Ozotoceros bezoarticus) of the Estación de Cría de Fauna Autóctona Cerro Pan de Azúcar. Different letters between age indicate significant differences (P ≤ 0.05).
the procedure MIXED of SAS statistical package (Statistical Analysis System, Version 9.2, 2008). The effect of year (2010–2013), paddock (6 levels) and mother age (in years, 8 levels) were included as fixed effect, and the permanent effect of the female as random effect (49 levels). Generalized linear mixed model with binomial distribution (calving or not calving) and logit link function were used to test differences in calving success (probability of calving) between females of different rank, by the procedure GLIMMIX of SAS. Fixed effects included in the model were rank (HR, MR and LR), age of the hind (AH, in classes), and year (2010–2013). The effect of paddock (6 levels) was included in the model as random, because some paddocks have only successful cases. The age classes were defined as: (AH1) one to three years old, (AH2) from four to six years, and (AH3) from seven and more years old hinds. In addition, the permanent effect of the female was included as random effect (49 levels). A generalized lineal model with binomial distribution and logit link function was used to analyze sex ratio, modeling the probability of calving males. Rank, year, paddock and AH were included as fixed effects. The permanent effect of the female was not included because the model including the permanent effect of female demonstrated a worse fit statistic (higher AICC and BIC) and created convergence problems. The analysis was performed with the procedure GENMOD of SAS. To examine the effect of different factors on calving date and birth weight, a lineal mixed model with repeated measures was performed with the procedure MIXED of SAS. The trait analyzed for calving date was days in relation to the first January each year. Rank, year, paddock, AH and sex, were included as fixed effects. The permanent effect of the female was not included for the same reason as the precedent analysis. Results were considered significant at ˛ = 0.05. Data are expressed as mean ± SEM. 3. Results We recorded 59 calvings (HR = 23, MR = 16, LR = 20); the remaining 39 females did not calve or calved in other months of the year, those hinds were only included in the success index and calving success analysis. The success index was related to females’ age (P < 0.001): success index increased from two to three years, it was stable to seven and, then, increased again to nine years of age (Fig. 1). The nine years old level showed statistical differences with all levels (P < 0.05). The effects of the year and paddock were not statically significant (P > 0.05). The permanent effect of the hind corresponds to 51% of the total variance. The year and the social rank did not affect the calving success (HR = 92.6%, MR = 73.9%, LR = 75.9%), but females’ age was
J.T. Morales-Pi˜ neyrúa et al. / Behavioural Processes 105 (2014) 49–52 Table 1 Sex ratios of pampas deer were born in the Estación de Cría de Fauna Autóctona Cerro Pan de Azúcar in relation to their mothers’ success index.
Number of males Number of females Males/total a b
HRa (n = 25)
LRb (n = 23)
16 9 0.64
10 13 0.43
High ranked. Low ranked.
significant (P < 0.05). Older females (AH3) showed greater probability of calving than females with age medium (AH2) (0.98 ± 0.02 vs. 0.78 ± 0.12, respectively; P = 0.01). Considering probability of calving, younger females (AH1) (0.87 ± 0.10) were not different than AH3 or AH2 (P > 0.05). The permanent effect of the hind explained 65% of the total variance. Whereas there was a numerically higher ratio of male calves by the HR hinds (Table 1), the difference are not statistically significant (P > 0.05). In addition, the sex ratio was not influenced by the effect of year, paddock and age of hind (P > 0.05). The calving date was not affected by year, age of hind and social rank (HR = 306.6 ± 8.2 days, MR = 313.6 ± 8.8, LR = 307.2 ± 7.8 days from January 1st each year, mean ± SEM). However, the calving date was affected by the fawns’ sex and paddock effect (P < 0.05). Mean birthdate of female fawns was 21 days earlier than male fawns (females = 286.6 ± 5.5 days, males = 308.3 ± 5.7 days; P < 0.05). The social rank did not affect (P > 0.05) the fawns’ birth weight (HR = 1873.9 ± 89.8 g, MR = 1876.7 ± 55.2 g, LR = 1805.3 ± 98.2 g). In addition, the birth weight was not influenced by the effect of year, paddock, age of hind and sex (P > 0.05). 4. Discussion In the conditions of this study, the results support the hypothesis of a relationship between success index pampas deer and females’ age. Our results were similar to results reported in previous studies in several ruminant species where social rank increased with females’ age bighorn sheep: Festa-Bianchet, 1991; gazelle: ibex nubian goat: Greenberg-Cohen et al., 1994). In red deer and reindeer, social rank was strongly related to age and did not decrease for the oldest females (Clutton-Brock et al., 1986; Thouless and Guinness, 1986; Holand et al., 2004). A possible explanation is that hinds improve fighting ability with age. However, Thouless and Guinness (1986) reported that fighting ability in red deer is not closely related to age. Their report indicates that when a younger, but mature, hind meets an older hind that she has not previously met, fighting is likely to occur, and the younger hind is more likely to win than would be expected by chance alone. Several authors (Rutberg, 1983; Thouless and Guinness, 1986; Festa-Bianchet, 1991) speculate that dyadic relationships are permanently established when the animals are young, by supposing that hinds adopt a rule of giving way to individuals that have beaten them in the past (who will generally be older than them), and only very rarely challenge the established ranks, therefore, older animals will remain dominant. In addition, age-related social rank is observed in linearity and stable hierarchy (Fournier and Festa-Bianchet, 1995). It is interesting to speculate that our results may be because the deer population is stable; therefore, it may lead to a stable hierarchy that favors this relationship. Our results do not support the hypothesis of a relationship between social rank of individual pampas deer females and calving date, sex ratio and fawns’ birth weight. Different to our results, in several small ruminant species (red deer: Clutton-Brock et al., 1984, 1986; caribou: Kojola, 1997; saharan arruí: Cassinello and Gomendio, 1996) there is a direct link between social position and the reproductive output: high-ranked females calve earlier, with a
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greater percentage of males, which were also heavier than those of low-ranked females. The lack of this relationship in our study may be explained by the differences in animal management and housing. Our work was performed with animals in semi-captive management, with enough food to minimize the effects of competition for access to food resources. In this sense, all females had similar nutritional status and body conditions (data not recorded), which may mask possible effects of social positions on reproduction (Goodwin et al., 1999) that may be observed in the wild. In this experiment there was no relation between social rank and calving date. Normally, such a relationship is due to females of high-rank ovulating earlier than females of low-rank (Alvarez et al., 2003), and/or having earlier access to the male (mate competition) (Bebié and McElligott, 2006; Bro-Jorgensen, 2002). The lack of this relationship in our experiment may also be explained by the homogeneous plane of nutrition of the females studied since nutritional effects on the ovarian cyclic activity may be similar between different individuals. A complementary explanation is the lack of female competition for mating that we have previously observed in this ˜ population during the rut (Morales-Pineyrúa and Ungerfeld, 2012). Calving success was significantly affected by females’ age. The fecundity (the probability of producing a calf) has been shown to be associated with females’ age in others cervids (Clutton-Brock et al., 1984; Langbein and Putman, 1992; Rönnegard et al., 2002); generally, the probability of calving increases to medium age (5–8 years), then it is kept constant, and finally decreases due to senescence (7–15 years depend of specie) (red deer: Guinness et al., 1978; Clutton-Brock et al., 1982; reindeer: Eloranta and Nieminen, 1986; Ropstad, 2000; Weladji et al., 2006). This relationship might be explained in terms of investment in reproduction; the reproductive effort in young animals is proportionally greater than in old animals because the former must allocate more energy toward growth while pregnant and lactating; therefore, the older females will have more energy to allocate toward reproduction (Skogland, 1983; Engen and Saether, 1994). The increase of the reproductive efficiency with age may be explained as old animals show better corporal condition and weight than young females (Kojola and Eloranta, 1989; Landete-Castillejos et al., 1998; Rönnegard et al., 2002). In our work we assumed that all females were in similar corporal condition: therefore, the relationship observed may be consequence of differential energy redistribution. Similar to our observation, in Cuvier’s gazelle (Alados and Escós, 1994) and bison (Green and Rothstein, 1993) there was no relationship between social rank and offspring sex ratio. The variation in the sex ratio may be consequence of differences in the cost of producing and rearing sons or daughters (Trivers and Willard, 1973; Williams, 1979). Indeed, Alados and Escós (1994) and Green and Rothstein (1993) suggested that their results were related to the lack of difference in the cost of producing one or the other gender. Similarly, in pampas deer maintained at the ECFA, the cost of rearing both genders probably did not differ. In this sense, we have not observed a difference on the time-length of suckling bouts of male or female fawns during the first three months of life (Villagrán et al., 2012). Overall, our result does not support the hypothesis of varied sex ratio as put forth by Trivers and Willard (1973). In conclusion, in our experimental conditions, the success index was related with females’ age, and reproductive performance (calving date, and fawns’ sex and birth weight) did not differ between females of different social ranks.
Acknowledgements Authors acknowledge Aline Freitas-de-Melo, Claudia Ambrosi, Flávia Franchini and Josefina Roberts for help with data collection, and to Dr. Milan Shipka (Fairbanks University, USA) and Pamela
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Ungerfeld for their help with language revision. Financial support was provided by CSIC (Universidad de la República, Uruguay) and Intendencia Departamental de Maldonado (Uruguay). References Alados, C.L., Escós, J.M., 1994. Variation in the sex ratio of a low dimorphic polygynous species with high levels of maternal reproductive effort: Cuvier’s gazelle. Ethol. Ecol. Evol. 6, 301–311. Alvarez, L., Martin, G.B., Galindo, F., Zarco, L.A., 2003. Social dominance of female goats affects their response to the male effect. Appl. Anim. Behav. Sci. 8, 119–126. Barroso, F.G., Alados, C.L., Boza, J., 2000. Social hierarchy in the domestic goat: effect on food habits and production. Appl. Anim. Behav. Sci. 69, 35–53. Bebié, N., McElligott, A.G., 2006. Female aggression in red deer: does it indicate competition for mates? Mammal. Biol. 71, 347–355. Bro-Jorgensen, J., 2002. Overt female mate competition and preference for central males in a lekking antelope. PNAS 99, 9290–9293. Cassinello, J., 1996. High-ranking females bias their investment in favour of male calves in captive Ammotragus lervia. Behav. Ecol. Sociobiol. 38, 417–424. Cassinello, J., Gomendio, M., 1996. Adaptive variation in litter size and sex ratio at birth in a sexually dimorphic ungulate. Proc. R. Soc. Lond. B: Biol. Sci. 263, 1461–1466. CITES, 2013. Convention of International Trade in Endangered Species of Wild Fauna and Flora, Appendix I, II and III. http://www.cites.org/eng/app/appendices.php (accessed 26.08.13). Clutton-Brock, T.H., Albon, S.D., Gibson, R.M., Guinness, F.E., 1979. The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus). Anim. Behav. 27, 211–225. Clutton-Brock, T.H., Guiness, F.E., Albon, S.D., 1982. Red Deer: Behavior and Ecology of Two Sexes. University of Chicago Press, Chicago. Clutton-Brock, T.H., Albon, S.D., Guinness, F.E., 1984. Maternal dominance, breeding success and birth sex ratios in red deer. Nature 308, 358–360. Clutton-Brock, T.H., Albon, S.D., Guiness, F.E., 1986. Great expectations: dominance, breeding success and offspring sex ratios in red deer. Anim. Behav. 34, 460–471. Eloranta, E., Nieminen, M., 1986. Calving of the experimental reindeer herd in Kaanianen during 1970–85. Rangifer 1, 115–121 (special issue). Engen, S., Saether, B.E., 1994. Optimal allocation of resources to growth and reproduction. Theor. Popul. Biol. 46, 232–248. Espmark, Y., 1964. Studies in dominance-subordination relationship in a group of semi-domestic reindeer (Rangifer tarandus). Anim. Behav. 12, 420–426. Festa-Bianchet, M., 1991. The social system of bighorn sheep: grouping patterns, kinship and female dominance rank. Anim. Behav. 42, 71–82. Fournier, F., Festa-Bianchet, M., 1995. Social dominance in adult female mountain goats. Anim. Behav. 49, 1449–1459. ˜ Freitas-de-Melo, A., Morales-Pineyrúa, J.T., Ungerfeld, R., 2013. Agonistic malefemale and female-female behaviour in pampas deer (Ozotoceros bezoarticus). North-West. J. Zool. 9, 127–130. González, S., Álvarez-Valin, F., Maldonado, J., 2002. Morphometric differentiation of endangered pampas deer (Ozotoceros bezoarticus), with description of new subspecies from Uruguay. J. Mammal. 83, 1127–1140. Goodwin, N., Hayssen, V., Deakin, D.W., Flint, A.P.F., 1999. Influence of social status on ovarian function in farmed red deer (Cervus elaphus). Physiol. Behav. 65, 691–696. Green, W.C.H., Rothstein, A., 1993. Persistent influences of birth date on dominance, growth and reproductive success in bison. J. Zool. 230, 177–186. Greenberg-Cohen, D., Alkon, P.U., Yom-Tov, Y., 1994. A linear dominance hierarchy in female Nubian ibex. Ethology 98, 210–220. Guinness, F.E., Albon, S.D., Clutton-Brock, T.H., 1978. Factors affecting reproduction in red deer (Cervus elaphus) hinds on Rhum. J. Reprod. Fertil. 54, 325–334.
Holand, O., Weladji, R.B., Gjøstein, H., Kumpula, J.M., Smith, M.E., Nieminen, M., Røed, K., 2004. Reproductive effort in relation to maternal social rank in reindeer (Rangifer tarandus). Behav. Ecol. Sociobiol. 57, 69–76. IUCN, International Union for Conservation of Nature and Natural Resources, 2013. Red List of Threatened Species. Ozotoceros bezoarticus uruguayensis, http://www.iucnredlist.org (accessed 26.08.13). Jackson, J., 1985. Behavioural observations on the Argentinean pampas deer (Ozotoceros bezoarticus celer Cabrera, 1943). Z. Säugetierkd. 50, 107–116. Jackson, J.E., Langguth, A., 1987. Ecology and status of pampas deer (Ozotoceros bezoarticus) in the Argentinean pampas and Uruguay. In: Wemmer, C. (Ed.), Biology and Management of the Cervidae. Smithsonian Institution Press, Virginia, pp. 402–409. Kojola, I., 1997. Social status and physical condition of mother and sex ratio offspring in cervids. Appl. Anim. Behav. Sci. 51, 267–274. Kojola, I., Eloranta, E., 1989. Influences of maternal body weight, age, and parity on sex ratio in semidomesticated reindeer (Rangifer t. tarandus). Evolution 43, 1331–1336. Landete-Castillejos, T., Garde, J., Gracía, A., Gallego, L., 1998. Selección de sexo en múflon en función de la edad y peso de la madre. Prod. Ov. Capr. 23, 583–586. Langbein, J., Putman, R., 1992. Reproductive success of female Fallow Deer in relation to age and condition. In: Brown, R.D. (Ed.), The Biology of Deer. Springer Press, New York, pp. 293–299. ˜ Morales-Pineyrúa, J.T., Ungerfeld, R., 2012. Pampas deer (Ozotoceros bezoarticus) courtship and mating behavior. Acta Vet. Scand. 54, 60. National Research Council (NRC), 2007. Nutrient Requirements of Small Ruminants: Sheep, Goats, Cervids, and New World Camelids. National Academies Press, Washington. Redford, K.H., 1987. The pampas deer (Ozotoceros bezoarticus) in central Brazil. In: Wemmer, C. (Ed.), Biology and Management of the Cervidae. Smithsonian Institution Press, Virginia, pp. 410–414. Redford, K.H., Eisenberg, J.F., 1992. Mammals of the Neotropics: Southern Cone, vol. 2. University Chicago Press, Chicago. Rönnegard, L., Forslund, P., Danell, Ö., 2002. Lifetime patterns in adult female mass, reproduction, and offspring mass in semidomestic reindeer (Rangifer tarandus tarandus). Can. J. Zool. 80, 2047–2055. Ropstad, E., 2000. Reproduction in female reindeer. Anim. Reprod. Sci. 61 (60), 561–570. Rutberg, A.T., 1983. Factors influencing dominance status in American bison cows (Bison bison). Z. Tierpsychol. 63, 206–212. Skogland, T., 1983. The effects of density dependent resource limitation on size of wild reindeer. Oecologia 60, 156–168. Thouless, C.R., Guinness, F.E., 1986. Conflict between red deer hinds: the winner always wins. Anim. Behav. 34, 1166–1171. Trivers, R.L., Willard, D.E., 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 90–92. Ungerfeld, R., González-Sierra, U.T., Piaggio, J., 2008a. Reproduction in a semi-captive herd of pampas deer, Ozotoceros bezoarticus. Wildlife Biol. 14, 350–357. Ungerfeld, R., González-Pensado, S., Bielli, A., Villagrán, M., Olazábal, D., Pérez, W., 2008b. Reproductive biology of the pampas deer (Ozotoceros bezoarticus): a review. Acta Vet. Scand. 50, 16. Verme, L.J., 1983. Sex ratio variation in Odocoileus: a review. J. Wildlife Manage. 47, 573–582. Villagrán, M., De-la-Fuente, L., Ungerfeld, R., 2012. Pampas deer fawns (Ozotoceros bezoarticus Linnaeus, 1758) feeding time budget during the first twelve weeks of life. North-West. J. Zool. 8, 85–91. Weladji, R.B., Gaillard, J.M., Yoccoz, N.G., Holand, O., Mysterud, A., Loison, A., Nieminen, M., Stenseth, N.C., 2006. Good reindeer mothers live longer and become better in raising offspring. Proc. R. Soc. B 273, 1239–1244. Williams, G.C., 1979. The question of adaptive sex ratio in outcrossed vertebrates. Proc. R. Soc. Lond. B Biol. Sci. 205, 567–580.
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Social rank and reproductive performance of pampas deer females (Ozotoceros bezoarticus, Linnaeus, 1758) a ˜ Jéssica Tatiana Morales-Pineyrúa , Gabriel Ciappesoni b , Rodolfo Ungerfeld a,∗ a b
Departamento de Fisiología, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay INIA-Las Brujas, Canelones, Uruguay
a r t i c l e
i n f o
Article history: Received 28 December 2013 Received in revised form 4 March 2014 Accepted 5 March 2014 Available online 13 March 2014 Keywords: Dominance Female competition Hierarchy, Social behavior Ruminant
a b s t r a c t Our objectives were to determine if success index of pampas deer females is related with females’ age and if social rank makes any influence on reproductive performance. Female social rank was determined in 18 groups of animals composed of 1 male: 5–9 females (total = 98 females). Date of parturition for each female and sex and birth weight of fawns were recorded for each birth. The females were categorized in three hierarchical ranks: low (<0.33) (group LR), medium (0.33–0.66) (group MR), and high (>0.66) (group HR). The success index increased with age in pampas deer females (P < 0.001). Social rank had no effect on calving success, relative calving dates, sex ratio or body weight at birth. In this study, the success index was related with females’ age, and the reproductive performance did not differ between females of different social ranks. © 2014 Published by Elsevier B.V.
1. Introduction Social deer species live in groups with hierarchical structures (red deer: Clutton-Brock et al., 1982; reindeer: Espmark, 1964; white-tailed deer: Verme, 1983), maintained by agonistic behaviors (Bebié and McElligott, 2006; Jackson, 1985; Thouless and Guinness, 1986). Females’ social rank has been positively related with age in several deer species (Espmark, 1964; Clutton-Brock et al., 1982, 1986; Thouless and Guinness, 1986; Holand et al., 2004). As a consequence of the hierarchical structures, individuals from different social ranks have unequal access to different resources (Clutton-Brock et al., 1982; Espmark, 1964; Verme, 1983), which may result in differences in their reproductive success (Cassinello, 1996). In this sense, in deer, social rank has been positively related to fecundity (Clutton-Brock et al., 1986), date of conception (Clutton-Brock et al., 1984), offspring reproductive success (Clutton-Brock et al., 1984), fawns’ birth weight (Clutton-Brock et al., 1984; Kojola, 1997), and fawns’ survival rate (Clutton-Brock et al., 1984, 1986). It has also been reported that high-ranked females calve a greater proportion of males than low-ranked females (Clutton-Brock et al., 1986). However, it should be considered that most of those data have been obtained in free living deer
∗ Corresponding author at: Departamento de Fisiología, Facultad de Veterinaria, Lasplaces 1550, Montevideo 11600, Uruguay. Tel.: +598 2628 6955; fax: +598 2628 0130. E-mail address: [email protected] (R. Ungerfeld). http://dx.doi.org/10.1016/j.beproc.2014.03.004 0376-6357/© 2014 Published by Elsevier B.V.
populations in which competition for resources may have greater influence on an individual animal’s reproductive biology than in captive populations. The pampas deer is a South American deer categorized as “near threatened” by IUCN (2013), and listed in Appendix I of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES, 2013). In Uruguay there are three populations, two living in wild conditions (González et al., 2002), and one maintained in semi-captive conditions since 1981, located at the Estación de Cría de Fauna Autóctona Cerro Pan de Azúcar (ECFA) (Ungerfeld et al., 2008a). Although the animals maintained at the ECFA have continuous access to sufficient food resources on a year around basis, pampas deer have a seasonal reproductive pattern (Ungerfeld et al., 2008a). The gestation length of the species has been estimated from the rut-birth period in wild populations as slightly more than 7 months (Jackson and Langguth, 1987; Redford and Eisenberg, 1992). Females give birth to a single fawn (Redford, 1987) of approximately 2 kg (Ungerfeld et al., 2008a). Pampas deer groups have hierarchical structures (Ungerfeld et al., 2008b), but no attempts have been made to relate social rank with females’ age and reproductive success. Therefore, the objective of this study was to determine if the success index of pampas deer females is affected by female age and if females’ social rank during the conception period influences calving success, calving date, fawns’ sex ratio and fawns’ birth weight. The study was performed with animals from the ECFA pampas deer population.
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2. Materials and methods
1.4
e
1.2
2.1. Animals and allocation
d
The study was conducted at the ECFA, Maldonado, Uruguay (34◦ 3 S, 55◦ 1 W; altitude: ∼200 m), where breeding and management of an Ozotoceros bezoarticus arerunguaensis (pampas deer) population started in 1981. Overall, the ECFA comprises 86 ha where only native fauna is bred. The pampas deer are kept in breeding groups composed by one stag and several hinds and their fawns, or single male groups. The offspring are weighed and the sex is recorded during the first 24 h after birth. Animals have the opportunity to graze native pastures and are fed a supplement of 600 g/d/deer of a commercial dairy cow ration that meets the requirements of these animals calculated from the NRC (2007) (∼3% of live weight; a total of 110 g of crude protein and 1.32 MCal of ME). The supplement was offered daily in the morning from Monday to Saturday. All animals were identified with numbered tags. Data were recorded during three consecutive years in six breeding groups housed in separated paddocks (total = 18 groups, 98 females). Each group was composed of one adult male, 5–9 adult females (3–10 years old), and young animals (1–2 years old). The age in years was obtained from the records kept by the ECFA manager. Size of each paddock ranged between 0.5 and 1 ha. All paddocks had abundant water, native pastures, trees and shrubs. 2.2. Determination of social rank On February each year (early breading season) all spontaneous agonistic behaviors between females were recorded as previously described by Freitas-de-Melo et al. (2013). Briefly, focal observations were performed in each group during two periods of 20–40 min, one in the morning (8:00–10:00 am) and one in the afternoon (4:00–6:00 pm), during ten consecutive days (total: 190 h). The observations were performed by two trained observers from a distance of 4 to 8 m (enough distance to avoid disturbing the normal behavior of animals). Inter-observer reliability was tested before the start of the study. Animals received ration at the beginning of the recording periods in three feeding stations in each paddock, separated approximately 2.5–3.0 m each from the other in a triangular arrangement. From these recordings, a success index (SI) for each female was calculated according to Clutton-Brock et al. (1979): SI =
number of individuals displaced number of individuals displaced + number of individuals that displace it
The animals were classified, as in Alvarez et al. (2003) and Barroso et al. (2000), in three categories according to their SI as low (LR; <0.33), medium (MR; 0.33–0.66), or high-ranked (HR; >0.66). Overall, 7251 behavioral agonistic events were recorded, which corresponded to 381.6 ± 43.7/group (mean ± SEM) (range: 93–717). During the recording period each animal interacted 153.4 ± 8.4 times (range: 6–505). Thirty-two females were categorized as HR, 30 as MR, and 35 as LR females. 2.3. Reproductive recordings From August to January of each year (peak of births; Ungerfeld et al., 2008a) all births were recorded, including the date, the fawns’ sex, and fawns’ birth weight. The fawns were weighed and sexed within 24 h of birth. 2.4. Statistical analysis To examine the effect of different factors on success index, a linear mixed model with repeated measures was performed with
Success index
1.0 0.8
cd
0.6
c
ab
0.4 0.2
c bc
a
0.0 2
3
4
5 6 Age (years)
7
8
9
Fig. 1. Plot of success index according to the females’ age in 98 pampas deer females (Ozotoceros bezoarticus) of the Estación de Cría de Fauna Autóctona Cerro Pan de Azúcar. Different letters between age indicate significant differences (P ≤ 0.05).
the procedure MIXED of SAS statistical package (Statistical Analysis System, Version 9.2, 2008). The effect of year (2010–2013), paddock (6 levels) and mother age (in years, 8 levels) were included as fixed effect, and the permanent effect of the female as random effect (49 levels). Generalized linear mixed model with binomial distribution (calving or not calving) and logit link function were used to test differences in calving success (probability of calving) between females of different rank, by the procedure GLIMMIX of SAS. Fixed effects included in the model were rank (HR, MR and LR), age of the hind (AH, in classes), and year (2010–2013). The effect of paddock (6 levels) was included in the model as random, because some paddocks have only successful cases. The age classes were defined as: (AH1) one to three years old, (AH2) from four to six years, and (AH3) from seven and more years old hinds. In addition, the permanent effect of the female was included as random effect (49 levels). A generalized lineal model with binomial distribution and logit link function was used to analyze sex ratio, modeling the probability of calving males. Rank, year, paddock and AH were included as fixed effects. The permanent effect of the female was not included because the model including the permanent effect of female demonstrated a worse fit statistic (higher AICC and BIC) and created convergence problems. The analysis was performed with the procedure GENMOD of SAS. To examine the effect of different factors on calving date and birth weight, a lineal mixed model with repeated measures was performed with the procedure MIXED of SAS. The trait analyzed for calving date was days in relation to the first January each year. Rank, year, paddock, AH and sex, were included as fixed effects. The permanent effect of the female was not included for the same reason as the precedent analysis. Results were considered significant at ˛ = 0.05. Data are expressed as mean ± SEM. 3. Results We recorded 59 calvings (HR = 23, MR = 16, LR = 20); the remaining 39 females did not calve or calved in other months of the year, those hinds were only included in the success index and calving success analysis. The success index was related to females’ age (P < 0.001): success index increased from two to three years, it was stable to seven and, then, increased again to nine years of age (Fig. 1). The nine years old level showed statistical differences with all levels (P < 0.05). The effects of the year and paddock were not statically significant (P > 0.05). The permanent effect of the hind corresponds to 51% of the total variance. The year and the social rank did not affect the calving success (HR = 92.6%, MR = 73.9%, LR = 75.9%), but females’ age was
J.T. Morales-Pi˜ neyrúa et al. / Behavioural Processes 105 (2014) 49–52 Table 1 Sex ratios of pampas deer were born in the Estación de Cría de Fauna Autóctona Cerro Pan de Azúcar in relation to their mothers’ success index.
Number of males Number of females Males/total a b
HRa (n = 25)
LRb (n = 23)
16 9 0.64
10 13 0.43
High ranked. Low ranked.
significant (P < 0.05). Older females (AH3) showed greater probability of calving than females with age medium (AH2) (0.98 ± 0.02 vs. 0.78 ± 0.12, respectively; P = 0.01). Considering probability of calving, younger females (AH1) (0.87 ± 0.10) were not different than AH3 or AH2 (P > 0.05). The permanent effect of the hind explained 65% of the total variance. Whereas there was a numerically higher ratio of male calves by the HR hinds (Table 1), the difference are not statistically significant (P > 0.05). In addition, the sex ratio was not influenced by the effect of year, paddock and age of hind (P > 0.05). The calving date was not affected by year, age of hind and social rank (HR = 306.6 ± 8.2 days, MR = 313.6 ± 8.8, LR = 307.2 ± 7.8 days from January 1st each year, mean ± SEM). However, the calving date was affected by the fawns’ sex and paddock effect (P < 0.05). Mean birthdate of female fawns was 21 days earlier than male fawns (females = 286.6 ± 5.5 days, males = 308.3 ± 5.7 days; P < 0.05). The social rank did not affect (P > 0.05) the fawns’ birth weight (HR = 1873.9 ± 89.8 g, MR = 1876.7 ± 55.2 g, LR = 1805.3 ± 98.2 g). In addition, the birth weight was not influenced by the effect of year, paddock, age of hind and sex (P > 0.05). 4. Discussion In the conditions of this study, the results support the hypothesis of a relationship between success index pampas deer and females’ age. Our results were similar to results reported in previous studies in several ruminant species where social rank increased with females’ age bighorn sheep: Festa-Bianchet, 1991; gazelle: ibex nubian goat: Greenberg-Cohen et al., 1994). In red deer and reindeer, social rank was strongly related to age and did not decrease for the oldest females (Clutton-Brock et al., 1986; Thouless and Guinness, 1986; Holand et al., 2004). A possible explanation is that hinds improve fighting ability with age. However, Thouless and Guinness (1986) reported that fighting ability in red deer is not closely related to age. Their report indicates that when a younger, but mature, hind meets an older hind that she has not previously met, fighting is likely to occur, and the younger hind is more likely to win than would be expected by chance alone. Several authors (Rutberg, 1983; Thouless and Guinness, 1986; Festa-Bianchet, 1991) speculate that dyadic relationships are permanently established when the animals are young, by supposing that hinds adopt a rule of giving way to individuals that have beaten them in the past (who will generally be older than them), and only very rarely challenge the established ranks, therefore, older animals will remain dominant. In addition, age-related social rank is observed in linearity and stable hierarchy (Fournier and Festa-Bianchet, 1995). It is interesting to speculate that our results may be because the deer population is stable; therefore, it may lead to a stable hierarchy that favors this relationship. Our results do not support the hypothesis of a relationship between social rank of individual pampas deer females and calving date, sex ratio and fawns’ birth weight. Different to our results, in several small ruminant species (red deer: Clutton-Brock et al., 1984, 1986; caribou: Kojola, 1997; saharan arruí: Cassinello and Gomendio, 1996) there is a direct link between social position and the reproductive output: high-ranked females calve earlier, with a
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greater percentage of males, which were also heavier than those of low-ranked females. The lack of this relationship in our study may be explained by the differences in animal management and housing. Our work was performed with animals in semi-captive management, with enough food to minimize the effects of competition for access to food resources. In this sense, all females had similar nutritional status and body conditions (data not recorded), which may mask possible effects of social positions on reproduction (Goodwin et al., 1999) that may be observed in the wild. In this experiment there was no relation between social rank and calving date. Normally, such a relationship is due to females of high-rank ovulating earlier than females of low-rank (Alvarez et al., 2003), and/or having earlier access to the male (mate competition) (Bebié and McElligott, 2006; Bro-Jorgensen, 2002). The lack of this relationship in our experiment may also be explained by the homogeneous plane of nutrition of the females studied since nutritional effects on the ovarian cyclic activity may be similar between different individuals. A complementary explanation is the lack of female competition for mating that we have previously observed in this ˜ population during the rut (Morales-Pineyrúa and Ungerfeld, 2012). Calving success was significantly affected by females’ age. The fecundity (the probability of producing a calf) has been shown to be associated with females’ age in others cervids (Clutton-Brock et al., 1984; Langbein and Putman, 1992; Rönnegard et al., 2002); generally, the probability of calving increases to medium age (5–8 years), then it is kept constant, and finally decreases due to senescence (7–15 years depend of specie) (red deer: Guinness et al., 1978; Clutton-Brock et al., 1982; reindeer: Eloranta and Nieminen, 1986; Ropstad, 2000; Weladji et al., 2006). This relationship might be explained in terms of investment in reproduction; the reproductive effort in young animals is proportionally greater than in old animals because the former must allocate more energy toward growth while pregnant and lactating; therefore, the older females will have more energy to allocate toward reproduction (Skogland, 1983; Engen and Saether, 1994). The increase of the reproductive efficiency with age may be explained as old animals show better corporal condition and weight than young females (Kojola and Eloranta, 1989; Landete-Castillejos et al., 1998; Rönnegard et al., 2002). In our work we assumed that all females were in similar corporal condition: therefore, the relationship observed may be consequence of differential energy redistribution. Similar to our observation, in Cuvier’s gazelle (Alados and Escós, 1994) and bison (Green and Rothstein, 1993) there was no relationship between social rank and offspring sex ratio. The variation in the sex ratio may be consequence of differences in the cost of producing and rearing sons or daughters (Trivers and Willard, 1973; Williams, 1979). Indeed, Alados and Escós (1994) and Green and Rothstein (1993) suggested that their results were related to the lack of difference in the cost of producing one or the other gender. Similarly, in pampas deer maintained at the ECFA, the cost of rearing both genders probably did not differ. In this sense, we have not observed a difference on the time-length of suckling bouts of male or female fawns during the first three months of life (Villagrán et al., 2012). Overall, our result does not support the hypothesis of varied sex ratio as put forth by Trivers and Willard (1973). In conclusion, in our experimental conditions, the success index was related with females’ age, and reproductive performance (calving date, and fawns’ sex and birth weight) did not differ between females of different social ranks.
Acknowledgements Authors acknowledge Aline Freitas-de-Melo, Claudia Ambrosi, Flávia Franchini and Josefina Roberts for help with data collection, and to Dr. Milan Shipka (Fairbanks University, USA) and Pamela
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