Key words

Costa Rica, disturbance, montane cloud forest, rodents.
 

Terrestrial rodents are known to be important seed dispersers and predators in tropical forest ecosystems (e.g. Adler 1995). Often they form the staple food of many avian and mammal predators and therefore play a prominent role in maintaining the structure and composition of species-rich tropical habitats.

However, little is known about their response to changes in the environment and particularly to disturbance by man (Adler 1994). Indeed, it has been recorded that some rodent species populations may flourish due to human activities in natural and seminatural ecosystems (Johnson & Vaughan 1993). Untill now, knowledge on the effects of deforestation and habitat fragmentation on the presence and abundance of small terrestrial rodents in tropical forests is still limited. This is particularly the case in tropical upland regions where we count with just a few studies (Lanzewizki 1991, Johnson & Vaughan 1993). Even less is known on the role terrestrial Rodentia play in forest succession, canopy closure and biodiversity recovery following clearing and burning.

In order to gain insight in the intrinsic recovery capacity of the biodiversity inhabiting a shredded Costa Rican montane cloud forest area and to provide knowledge needed for the conservation and sustainable use of this threatened ecosystem, we studied the diversity and distribution of small terrestrial rodent species along a disturbance gradient, ranging from undisturbed mature primary oak forest to graminoid dominated pastureland suffering from intensive cattle grazing. The principal aim of the present study is to identify key indicator rodent species characteristic for certain levels of disturbance and recovery.
  ]]> Materials and Methods

This study was conducted in the Los Santos Forest Reserve near San Gerardo de Dota in the NW part of the Costa Rican Cordillera de Talamanca (9° 35'40'' N; 83° 44'30''). Originally, the watershed area (2000-3200 m altitude) was completely covered with mature, primary Quercus dominated montane cloud forest, but since the 1950s forest conversion for agricultural purposes has led to a landscape mosaic with vegetation patches of different size, structure, composition, level of disturbance and successional age (Kappelle & Juárez 1995, Kappelle et al. 1995). In Villa Mills, at a distance of 10 km E of the selected forest plot, the average annual temperature is 10.9°C and the average annual rainfall is 2812 mm. A detailed description of the study area's physical setting and botanical aspects can be found in Kappelle (1993, 1996).

At the end of the dry season (March-April 1996), using B&W aerial photographs (1992, scale 1: 15,000) five different habitats were selected along a man induced disturbance gradient in the upper montane forest belt (2200-2800 m a.s.l.). These habitats are, from low to high levels of disturbance: (i) 30 to 40 m tall, dense oak dominated 'Closed Mature Forest' (CMF); (ii) oak dominated 'Open Mature Forest' with a relatively open, 30 to 35 m high canopy (OMF); (iii) 3 to 7 m high secondary 'Successional Shrubland' (SSL); (iv) 0.5 to 2 m tall secondary 'Abandoned Pastureland' (APL); and (v) less than 0.5 m high 'Grazed Pastureland' (GPL); see Table 1. At each habitat site a 0.25 ha plot (50 x 50 m) was established, with exception of APL where a 0.28 ha plot (37.5 x 75 m) was laid out, since the site's patch dimensions required so.

In all but APL a total of 25 Sherman traps (trap size: 23 x 9 x 8 cm) were placed in a 5 x 5 grid with a 12.5 m distance between two neighbouring traps. Similarly, in APL 28 traps were located in a 4 x 7 grid. A standardized capture-recapture method was used to estimate species diversity, distribution and abundance in each habitat type (Leslie et al. 1952). Plots were studied from April to June 1996, covering the transition from the dry to the wet season. Sherman traps were checked ten consecutive days before noon. Only in OMF traps were checked nine days. Bait consisted of a mixture of rolled oats and peanut butter with a touch of vanilla flavour. In the afternoon traps were checked for diurnal catches and bait was renewed for the next trap-night. Traps were covered with litter and/or leaves for camouflage and insulation.

Data on the presence, sex, weight and length of trapped individuals were recorded. Weight was measured using a Pesola pocket scale (max. weight 300 g). Length measurements included the head-body length measured from the tip of the nose to the inflection point of the tail, and the tail length measured from the inflection point with the body to the fleshy tip of the tail. In situ species identification was done with the aid of Emmon & Feer's (1990) field guide, after studying rodent specimens in Costa Rica's national collections. Control specimens were collected and and stored at the Museo Nacional. Specimens were identified with help of B. Rodríguez (pers. com.) and on basis of field guides (Mora & Moreira 1984, Emmons & Feer 1990). Trapped individuals were marked upon first capture with acrylic paint before being released. Additionally, terrestrial vascular plant inventories were undertaken in each habitat and collected plant specimens stored and identified at the Museo Nacional. Species data were grouped and analysed for habitat sites along the disturbance gradient. Richness, abundance, density and capture frequency were assessed and preliminar conclusions drawn.

Results ]]> A total of 389 captures corresponded to 185 individuals distributed over 7 species in 2 families. The captured species were: (i) Muridae (Cricetidae): Peromyscus mexicanus (Mexican Deer Mouse, ratón pata blanca, closely related to P. nudipes, the Naked-footed Deer Mouse), Scotinomys xerampelinus (Singing Mouse, ratón cantante), Oryzomys albigularis (White-throated Rice Rat, ratón arrocero), Reithrodontomys creper (Chiriquí Harvest Mouse, ratón de las cosechas), and R. cf. sumichrasti (Sumichrasti's Harvest Mouse, ratón de las cosechas); and, (ii) Heteromyidae: Heteromys oresterus and H. cf. desmarestianus, being Spiny Pocket Mice (ratas de campo).

Table 1 presents some general data on the terrestrial rodent population in the five habitats. Richness was very similar for all habitat sites, with 4 to 5 species per habitat regardless its position along the disturbance axis. Population density and capture frequency (absolute and per area values), however, were particularly higher in habitats with intermediate levels of disturbance, being twice as high in OMF, SSL and APL when compared to both undisturbed CMF and intensively-used GPL. Abundance values differed strongly among species (Table 2).
 

Discussion

The vaired abundance values were concordant with classical rank-abundance Figs. (Magurran 1988). High abundances (60 - 75 individuals) were recorded for P. mexicanus and S. xerampelinus, whereas the other three Muridae, O. albigularis, R. creper and R. cf. sumichrasti, appeared to be four to five times less common. Together, P. mexicanus and S. xerampelinus represented 79.4 % of all captures (including recaptured individuals) and 73.5 % of all captured individuals. Both Heteromyidae species, in their turn, seemed to be rather rare in the area (-< 6 indiv.) and appeared to avoid both abandoned and grazed pasturelands (Table 2). P. mexicanus and S. xerampelinus occured at all five sites, although they differed in habitat preference with P. mexicanus appearing with higher numbers in CMF and OMF, and S. xerampelinus showing a higher abundance in SSL and APL. This difference is explained by the fact that the latter, more insectivorous species requires a rather dense vegetation cover at ground level, as its peak in activity is during morning hours (Hooper 1972). The species O. albigularis preferred OMF as well as the edge of GPL bordering mature forest. This observation concides with data earlier presented by Timm et al. (1989) for the Braulio Carrillo Park. R. creper and R. cf. sumichrasti were most abundant in APL (Table 2). These observations are concordant with data on habitat preferences of Nicaraguan Reithrodontomys species (Jones & Genoways 1970). R. creper was also trapped in OMF, but in lower numbers. Similarly, two individuals of R. cf. sumicharsti occured in GPL. Low capture results of H. oresterus and H. cf. desmarestianus suggest these species' rarity in the area. While H. oresterus preferred mature forest habitats, H. cf. desmarestianus was only recorded in SSL. H. oresterus may be qualified as an indicator species referring to low levels of disturbance. ]]>  
 

 
In general, male individuals were more often trapped in CMF and OMF as well as APL, while males and females appeared equally in SSL and GPL (Table 2). Whether these capture differences between sexes is due to behaviour or population make up remains unknown. O. albigularis was the largest terrestrial rodent species captured, being over six times as heavy and twice as long as R. cf. sumichrasti (Table 3). Data on weight and head-body and tail length of captured individuals were in accordance with data in Emmons & Feer (1990), with exception of values recorded for H. cf. desmarestianus. Individuals of the latter appeared to be much smaller in this study (mean weight 24.0 g; mean head-body length 8.8 cm) than the data range given by these authors would suggest (49-103 g; 10.8-14.8 cm). This outcome stresses the difficulties that occurred in the preliminary species identification. The weight distribution for male and female individuals of the most abundant species, P. mexicanus, clearly illustrates within-species weight differences found between sexes in rodents (Fig. 1). Whereas the weight distribution (expressed in 3 g weight classes) for males depicts a normal bell curve, the weight distribution for female individuals is asymmetrical, with an abrupt change at the 53 g weight level. This striking discrepancy may be explained by the presence of a number of pregnant adults in the 50-53 g weight class. If non-pregnant, these individuals would have been recorded in lower weight classes such as the 44-47 and 47-50 g classes. Indeed, four heavy adults (13 %) out of a total of 32 females were in a certain stage of pregnancy.
 
  ]]>  

This study's results are in general consistent with those from two previous studies conducted in the same region (Lanzewizki 1991; Johnson & Vaughan 1993). Johnson & Vaughan (1993) recorded five Myomorph species of which P. mexicanus (P. nudipes, in their study) and S. xerampelinus were the most common. This study revealed seven species of terrestrial Myomorph rodents, including O. albigularis and H. oresterus as new local records. Both our data and those collected by Johnson & Vaughan (1993) indicate the importance of within-habitat microenvironmental heterogeneity for rodent populations in tropical montane cloud forests.
 

Acknowledgements

We are much indebted to F. Bouman and A.M. Cleef for providing scientific support. M.B.v.d.B. was supported by grants of the Hugo de Vries and Van Tienhoven Foundations, the European Science Foundation and Bever Outdoor Sports. M.K. was supported by NWO grant 895.100.003. The VZZ Association provided Sherman traps. A. Velázquez (UNAM, Mexico) gave helpful advise and practical support. B. Rodríguez (UCR, Costa Rica) identified rodents. The Monge and Chacón families kindly offered field facilities.
 

Resumen ]]> Se estudió la distribución y diversidad de roedores terrestres en cinco hábitats perturbados en un área de bosque montano nuboso en Costa Rica. Un total de 389 capturas correspondió a 185 individuos (siete especies en 2 familias). La riqueza de especies resultó muy similar para todos los hábitats, con 4-5 especies/hábitat. La densidad de población y la frecuencia de captura fueron más altas en hábitats con niveles intermedios de perturbación; Peromyscus mexicanus y Scotinomys xerampelinus fueron cuatro a cinco veces más comunes que otras especies de Muridae. Estas representaron el 79.4 % de todas las capturas y el 73.5 % de todos los individuos. Se capturo pocos Heteromyidae.
 

References

Adler, G.H. 1994. Tropical forest fragmentation and isolation promote asynchrony among populations of a frugivorous rodent. J. Anim. Ecol. 63: 903-911.         [ Links ]

Adler, G.H. 1995. Fruit and seed exploitation by Central American spiny rats, Proechimys semispinosus. Stud. Neotrop. Fauna & Environ. 30: 237-244.         [ Links ]

Emmons, L.H. & F. Feer. 1990. Neotropical rainforest mammals, a field guide. The University of Chicago, Chicago.         [ Links ]

Hooper, E.T. 1972. A synopsis of the rodent genus Scotinomys. Museum of Zoology, University of Michigan. Occas. paper 665: 1-32         [ Links ]

Johnson, W.E. & C. Vaughan. 1993. Habitat use of small terrestrial rodents in the Costa Rican highlands. Rev. Biol. Trop. 41: 185-191.         [ Links ]

Jones, J.K., Jr. & H.H. Genoways. 1970. Harvest mice (Genus Reithrodontomys) of Nigaragua. W. Found. Vert. Zool. Occas. paper 2.         [ Links ]

Kappelle, M. 1993. Recovery following clearing of an upper montane Quercus forest in Costa Rica. Rev. Biol. Trop. 41: 47-56.         [ Links ]

Kappelle, M. 1996. Los bosques de roble (Quercus) de la Cordillera de Talamanca, Costa Rica: Biodiversidad, ecología, conservación y desarrollo. Universidad de Amsterdam & Instituto Nacional de Biodiversidad (INBio). Amsterdam - Santo Domingo de Heredia, Costa Rica.         [ Links ]

Kappelle, M. & M.E. Juárez. 1995. Agroecological zonation along an altitudinal gradient in the montane belt of the Los Santos Forest Reserve in Costa Rica. Mount. Res. & Devel. 15: 19-37.         [ Links ]

Kappelle, M., P.A.F. Kennis & R.A.J. de Vries. 1995. Changes in diversity along a successional gradient in a Costa Rican upper montane Quercus forest. Biodiv. Cons. 4: 10-34.         [ Links ]

Lanzewizki, T. 1991. Populationsökologische Untersuchungen an Kleinsäugern in einem Eichen-Wolkenwald (Quercus spp.) der Montanstufe Costa Ricas. Thesis. Philipps-Universität, Marburg.         [ Links ]

Leslie, P.H. 1952. The estimation of population parameters from data obtained by means of the capture-recapture method. II. The estimation of total numbers. Biometrika 39: 363-88.         [ Links ]

Magurran, A.E. 1988. Ecological diversity and its measurement. Croom Helm, London.         [ Links ]

Mora, J.M. & I. Moreira. 1984. Mamíferos de Costa Rica. Universidad Estatal a Distancia, San José, Costa Rica.         [ Links ]

Timm, R.M., D.E. Wilson, B.L. Clauson, R.K. Laval & C.S. Vaughan. 1989. Mammals of the La Selva - Braulio Carrillo Complex, Costa Rica. United States Department of the Interior Fish and Wildlife Service. North American Fauna 75.         [ Links ]

  
¹University of Amsterdam, Hugo de Vries Laboratory, Kruislaan 318, 1098 SM Amsterdam, The Netherlands ]]> ² Present address: INBio, apartado postal 22-3100, Santo Domingo, Heredia, Costa Rica.
 
Fig. Caption
 

Fig. 1. Weight distribution for male and female individuals of Peromyscus mexicanus in the montane cloud forest zone of the upper Río Savegre watershed area, Cordillera de Talamanca, Costa Rica.
 

TABLE 1

General data on physiographic aspects, vegetation layering and terrestrial rodent populations of five different habitat sites in the montane cloud forest zone of the upper Río Savegre watershed area, Cordillera de Talamanca, Costa Rica.
 

Habitat site Closed Open Successional Abandoned Grazed all Mature Mature Shrubland Pastureland Pastureland habitat Forest Forest sites ]]> Plot size (ha) 0.25 0.25 0.25 0.28 0.25 1.28

Altitude (m a.s.l.) 2750 2330 2360 2780 2260 -

Exposition E SW W N W -

Slope angle 10 o 33 o 35 o 15 o 5 o -

Vegetation layering 1: Canopy layer - height (m) 40 35 - - - - - cover (%) 90 80 - - - - Subcanopy layer - height (m) 18 18 7 - - - - cover (%) 70 65 10 - - - Shrub layer - height (m) 3 3 3 2 - - - cover (%) 50 35 90 20 - - Herb layer - height (m) 0.5 0.5 0.5 0.5 0.4 - - cover (%) 20 10 30 90 98 -

Nr. of trap nights 10 9 10 10 10 49

Species richness (nr. spp. per plot) 4 5 4 4 4 7

Density (nr. indiv. per ha) 92 180 160 196 80 142 *

Capture frequency 2 3.2 10.7 11.6 8.0 5.8 7.9 *

Capture frequency per ha 12.8 42.8 46.4 28.6 23.2 30.8 * ]]>  

* Mean values with n = 5 habitat sites.

1 Vegetation layering is expressed in maximum height and relative aerial crown cover of each stratum.

2 Capture frequency = mean number of captures per trap night.
 

TABLE 2

Abundance data of seven terrestrial rodent species found in five different habitat sites in the montane cloud forest zone of the upper Río Savegre watershed area, Cordillera de Talamanca, Costa Rica. Abundance data are subdivided per sex.
 

Habitat site Closed Open Successional Abandoned Grazed all Mature Mature Shrubland Pastureland Pastureland habitat Forest Forest sites
  ]]> Abundance 1 Sex ab. capt. ab. capt. ab. capt. ab. capt. ab. capt. ab. capt.
 

Peromyscus mexicanus both 19 26 21 67 17 58 13 26 5 30 75 207 male 14 19 11 33 9 28 8 13 1 9 43 102 female 5 7 10 34 8 30 5 13 4 21 32 105

Scotinomys xerampelinus both 3 3 7 12 20 44 24 29 7 14 61 102 male 2 2 4 8 8 13 17 22 5 10 36 55 female 1 1 3 4 12 31 7 7 2 4 25 47

Oryzomys albigularis both 1 1 7 12 1 1 - - 6 9 15 23 male - - 4 8 1 1 - - 3 3 8 12 female 1 1 3 4 - - - - 3 6 7 11

Reithrodontomys creper both - - 6 9 - - 9 15 - - 15 24 male - - 6 9 - - 7 12 - - 13 21 female - - - - - - 2 3 - - 2 3

R. cf. sumichrasti both - - - - - - 9 10 2 5 11 15 male - - - - - - 3 4 1 1 4 5 female - - - - - - 6 6 1 4 7 10

Heteromys oresterus both 2 2 4 4 - - - - - - 6 6 male 1 1 1 1 - - - - - - 2 2 female 1 1 3 3 - - - - - - 4 4

H. cf. desmarestianus both - - - - 2 12 - - - - 2 12 male - - - - 1 6 - - - - 1 6 female - - - - 1 6 - - - - 1 6

all species both 25 32 45 104 40 115 55 80 20 58 185 389 male 17 22 26 59 19 48 35 51 10 23 107 203 female 8 10 19 45 21 67 20 29 10 35 78 186 ]]>  

1 ab. = abundance measured as the total number of individuals captured; capt. = total number of captures including recaptures.
 

TABLE 3

Weight and length data of captured individuals belonging to seven terrestrial rodent species. Data are subdivided per sex and based on all five habitat sites in the montane cloud forest zone of the upper Río Savegre watershed area, Cordillera de Talamanca, Costa Rica.
 

Species Sex Weight 2 (g) Head-body length 2,3 (cm) Tail length 2,4(cm) mean + s.d. (n) mean + s.d. (n) mean + s.d. (n)
 

P. mexicanus both 51.6 + 4.6 (56) 11.9 + 0.7 (74) 12.3 + 0.6 (74) male 54.8 + 3.4 (26) 12.1 + 0.7 (42) 12.3 + 0.6 (42) female 48.8 + 4.4 (30) 11.6 + 0.7 (32) 12.3 + 0.6 (32)

S. xerampelinus both 14.0 + 2.2 (48) 6.9 + 0.4 (57) 5.9 + 0.8 (58) male 13.2 + 1.8 (24) 6.9 + 0.4 (35) 5.9 + 0.8 (35) female 14.8 + 2.2 (24) 6.8 + 0.5 (22) 5.8 + 0.8 (23) ]]> O. albigularis both 93.4 + 14.2 (11) 14.8 + 0.9 (12) 17.1 + 2.8 (14) male 93.4 + 13.1 (07) 14.2 + 1.3 (07) 17.3 + 3.4 (08) female 88.0 + 17.1 (04) 15.0 + 0.6 (05) 16.8 + 1.1 (06)

R. creper both 22.8 + 2.9 (14) 8.7 + 0.8 (14) 13.0 + 1.0 (14) male 22.7 + 3.0 (12) 8.6 + 0.7 (12) 13.0 + 0.9 (12) female 23.0 + 0.0 (01) 9.0 + 1.0 (02) 13.0 + 1.0 (02)

R. cf. sumichrasti both 14.9 + 2.5 (08) 7.4 + 0.5 (12) 8.7 + 0.8 (12) male 13.5 + 1.7 (04) 7.1 + 0.4 (05) 8.7 + 0.9 (05) female 16.3 + 2.5 (04) 7.6 + 0.4 (07) 8.7 + 0.8 (07)

H. oresterus both 74.8 + 3.8 (03) 12.7 + 0.8 (03) 17.0 + 0.7 (03) male 71.0 + 0.0 (01) 13.0 + 0.0 (01) 16.0 + 0.0 (01) female 76.0 + 3.6 (02) 12.6 + 0.8 (02) 17.3 + 0.3 (02)

H. cf. desmarestianus both 24.0 + 5.0 (02) 8.8 + 0.3 (02) 9.8 + 1.3 (02) male 29.0 + 0.0 (01) 9.0 + 0.0 (01) 11.0 + 0.0 (01) female 19.0 + 0.0 (01) 8.5 + 0.0 (01) 8.5 + 0.0 (01)
 

1 ab. = abundance measured as the total number of individuals captured;

capt. = total number of captures including recaptures.

2 Weight and length values are based on measurements taken at each individual's first catch.

3 Head-body length is measured as the length from the tip of the nose to the inflection point of the tail. ]]> 4 Tail length is measured as the length from the inflection point with the body to the fleshy tip of the tail. ]]> 1994 63 903-911 1995 30 237-244 1990 1972 665 1-32 1993 41 185-191 1970 2 1993 41 47-56 1996 1995 15 19-37 1995 4 10-34 1991 1952 39 363-88 1988 1984 1989