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Population characteristics of Dromiciops gliroides (Philippi, 1893), an endemic marsupial of the temperate forest of Patagonia Mariano A. Rodrı´ guez-Cabala,, Guillermo C. Amicoa, Andre´s J. Novarob, Marcelo A. Aizena a

Laboratorio Ecotono-CRUB, Universidad Nacional del Comahue, Quintral 1250, San Carlos de Bariloche, (8400) Rı´o Negro, Argentina b CONICET-Wildlife Conservation Society, Centro de Ecologı´a Aplicada del Neuque´n, C.C. 7 Junı´n de los Andes, (8371) Neuque´n, Argentina Received 30 August 2006; accepted 15 June 2007

Keywords: Abundance, Dromiciops gliroides, marsupials, population characteristics, Patagonia

The only living representative of Microbiotheriidae, one of the oldest lineages of marsupials (Marshall 1978), is Dromiciops gliroides (Philippi, 1893, monito del monte). This marsupial is endemic to the northern portion of the temperate forest of Patagonia, between 361 and 431 South in Chile and Argentina, where it dwells mainly in old-growth Nothofagus forest (Hershkovitz 1999; Saavedra and Simonetti 2001; Lobos et al. 2005). Morphological, chromosomal and molecular studies suggest that this marsupial shares more phylogenetic affinity with the Australian marsupials (Diprotodontia) than with other South American marsupials (Didelphidae) (Kirsch et al. 1997; Nilsson et al. 2004). Recent research suggests that the monito del monte may disperse seeds of 80% of the flora with fleshy fruits, in addition to its role as the sole disperser of the keystone mistletoe Tristerix corymbosus (Amico and Aizen 2000; Amico et al. unpubl.). This role makes this marsupial essential for preservation of biodiversity of the temperate forest of Patagonia. In spite of the potential key role of monito del monte in the temperate forest of Patagonia, little is known about its population Corresponding author. Department of Wildlife Ecology and Conservation, University of Florida. 110 Newins-Ziegler Hall, P.O. Box 110430, Gainesville, FL 32611-0430, USA. E-mail address: rcabal@ufl.edu (M.A. Rodrı´ guez-Cabal).

structure and abundance. Few individuals have been captured in previous studies (Mann 1955; Meserve et al. 1999), leading to the conclusion that this marsupials are rare in terms of abundance (Redford and Eisenberg 1992; Murua 1996). The objectives of this study were (1) to estimate population abundance, and (2) to describe the population structure of monitos del monte in an old-growth Nothofagus forest in the temperate forest of Patagonia. This study constitutes the first detailed ecological research focused on the identification of the population characteristics of the monito del monte. We conducted the study during two summer seasons (2000–2001) in a 2-ha plot in the Llao-Llao Municipal Reserve (41180 S, 711190 W, 770 m), 25 km West of San Carlos de Bariloche, Argentina. Dominant trees are evergreen southern-beech, Nothofagus dombeyi, and a conifer, Austrocedrus chilensis. The understory is dominated by the shrubs Aristotelia chilensis and Azara microphylla and the bamboo Chusquea culeou. We estimated abundance of monitos del monte using a capture-mark-recapture method (Nichols and Dickman 1996). We sampled each year with 20 wire live-traps placed about 5-m apart along a 100-m transect. Traps were run over 4 consecutive days each month from December to March. Traps were checked daily and all trapped marsupials were marked and released in the

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.2007.06.002 Mamm. biol. 73 (2008) 74–76

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1.0

25

0.8

20

0.6

15

0.4

10

0.2

5

No of captures

Relative frequency of individuals

same place where captured. For each animal captured, we recorded the weight, total length (from nose to tip of the tail), total length of the tail (from the 1st tail vertebra to the tip of the tail), basal perimeter of the tail, sex and age (juvenile or adult) based on presence and size of reproductive organs (scrotum or marsupium). In addition, we monitored arboreal mammals with automatic cameras (CamTrakker Wildlife Pro Cameras). Cameras were mounted on wooden poles about 3 m above the ground for 90 days from January to March 2000. In the summer of 2000, we live-trapped a total of 21 different individuals of monitos del monte, and in the summer 2001, we captured 29 individuals. In the two summer seasons, the monito del monte was the most abundant species in the understory stratum (80% of small mammals captured in 2000 and 83% in 2001). The estimated population size of monitos del monte in the study area for the summer 2001 (using the Jackknife population estimator with the program CAPTURE) was 54 individuals SE ¼ 8.6 (confidence interval 95% ¼ 42–77 individuals, estimated capture probability on every trapping occasion ¼ 0.190). Photographs taken with automatic cameras in summer 2000 recorded 101

0

0.0 Jan

Feb

Mar

Jan

2000 Juvenile

Feb

Mar

2001 Male

Female

Fig. 1. Number of captures (captures and recaptures; lines) and relative frequency of capture during the summers of 2000 and 2001 (bars). The number of captures included the recaptured individuals.

Table 1.

photographs of monito del monte and 23 photographs of small rodents (Irenomys tarsalis or Oryzomis longicaudatus) corroborating that the monito del monte is the most common small mammal in the arboreal stratum, and that the results obtained with captures are not a product of the trap’s baits. The relative number of females, males and juveniles captured was similar between these 2 years (w2 ¼ 9.2, d.f. ¼ 1, P ¼ 0.63), and for each month (January, February and March) between these summers (all P40.05 for all Contrasts). In both years, we captured fewer individuals in January than in February and March. We observed a relative increase in the number of juvenile individuals in the last 2 months. The proportion of males was larger in January. However, in March the relative number of females was larger than males (Fig. 1). There were no significant differences in morphometry between 2000 and 2001 within sexes and age classes (P40.05 in all comparisons). However, weight, total length, tail length and tail perimeter differed significantly between females and males. Females were, on average, significantly longer and heavier than males (Table 1). Weight of females and males was similar in January, but not during other months. Tail perimeter was only significantly different between females and males in March. An increase in weight was observed towards the end of the summer for females. Although we did not obtain estimates of absolute densities, the abundances observed in this study indicate that monitos del monte may have much higher densities than previous studies estimated of one individual/2 ha (see Redford and Eisenberg 1992; Murua 1996). Monito del monte in the 2 years of fieldwork was the most abundant small mammal in the understory stratum. The high abundance of this austral marsupial could be related to a high availability of T. corymbosus fruits in the study area, its main food resource during the summer months in the study area (personal observation). The monito del monte is the only marsupial in South America that hibernates when temperatures fall in winter (from April to August; Geiser 1994). Weight gain as a means of surviving unfavorable times has been observed for several species of Didelphidae

Weight and size of females, males and juveniles of D. gliroides ðX¯  SEÞ P-values correspond to Kruskal-Wallis test.

Number of individuals Weight (g) Total length (cm) Tail length (cm) Perimeter tail (mm) a

75

Female

Male

Juvenile

Female vs. male

15 33.2+1.9 21.5+0.3 11.4+0.5 15.1+2.0

23 28.9+1.4 20.6+0.3 10.6+0.9 12. 2+1.5

12 22.8+2.6 19.0+0.2 10.15+0.1 10.9+3.1

5.44 4.93 6.73 1.25

Adult is the average of the totals females and males. We exclude recapture data.

P ¼ 0.019 P ¼ 0.026 P ¼ 0.009 P ¼ 0.042

Adulta vs. Juvenile 7.89 10.53 6.85 4.10

P ¼ 0.005 P ¼ 0.002 P ¼ 0.008 P ¼ 0.040

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M.A. Rodrı´ guez-Cabal et al. / Mamm. biol. 73 (2008) 74–76

(Charles-Dominique et al. 1981; Caceres and MonteiroFilho 1999; Silva-Duran and Bozinovic 1999). The tail in this species of marsupial is known to be a storage organ (Kelt and Martinez 1989). The females are larger than the males by the end of summer, contrasting with most mammals (Andersson 1994; Fairbairn 1997; Caceres and Monteiro-Filho 1998). In particular, the females’ tails in our study were thicker than those of the males, indicating that females need more energy during hibernation. We did not find females with juveniles during the summer fieldwork. This result suggests that reproduction in this species occurs in spring (September– December) or before the beginning of in hibernation. We hypothesize that the females need to have resources for gestation before or during hibernation and that is why they show thicker tails and more overall weight by the end of summer.

Acknowledgements We thank Parque Municipal Llao Llao and A. Chavez for assistance; we also thank N. Barrios Garcia, L. Simpson and N. Tercero-Bucardo who provided logistical support and field assistance. Special thanks to L. Branch, R. Vidal-Russell and K. Watrous for comments and suggestions to improve this manuscript. Fieldwork was supported by National Geographic Society (Grant 6192-98), Fundacio´n Antorchas (Proyecto A-13740/1-14) and Wildlife Conservation Society.

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