Acta Theriologica 51 (1): 000000, 2006.

PL ISSN 00017051

Population structure of Ctenomys minutus (Rodentia, Ctenomyidae) on the coastal plain of Rio Grande do Sul, Brazil
Jorge R. MARINHO and Thales R. O. de FREITAS

Marinho J. R. and de Freitas T. R. O. 2006. Population structure of Ctenomys minutus (Rodentia, Ctenomyidae) on the coastal plain of Rio Grande do Sul, Brazil. Acta Theriologica 51: 000000.

Ctenomys minutus Nehring, 1887 in hab its fields and pas tures of the coastal plains of Santa Catarina (SC) and Rio Grande do Sul (RS), southern Brazil. This species shows territoriality, low vagility, and sedentary behavior. The sex ratio is unbalanced; there are more females both in the general (1.3:1) and in the adult population (1.26:1). The population was sexually dimorphic, with males be ing sig nif i cantly larger than fe males in all mea sured individuals. Analysis indicated allometric form of variation in both sexes.
Graduate Program in Animal Biology, Federal University of Rio Grande do Sul, Porto Alegre, Brazil (JRM, TROF), Genetic Department, C.P. 15053, 91501-970 Porto Alegre, RS, Brazil; e-mail: thales.freitas@ufrgs.br (TROF)

Key words: Ctenomys minutus, Rodentia, Octodontidae, population structure, sex dimorphism

Introduction
Of 125 liv ing species of subterranean rodents, 56 belong to the genus Ctenomys and are endemic to southern South America (Reig et al. 1990). Ctenomys is strongly ter ri to rial, with a patchy dis tri bu tion due to its low vagility (Massarini et al. 1991, Freitas 1994), presenting high karyotypic di ver sity with chro mo some numbers ranging from 2n = 10 to 70 (Freitas 1997). In its morphology and ecology, Ctenomys is highly con ver gent with North Amer i can pocket gophers (Geomyidae), Middle Eastern and European mole rats (Spalacidae), and African mole-rats (Bathyergidae) (Nevo 1979). Although ctenomyids are abundant and spacious, their biology and ecology are poorly known. Few studies have provided data on spatial distribu[000]

tion, demography, burrow occupancy, sex ratio, reproductive success and population structure. Such information is lacking for most species. A study of an Argentinean population of C. talarum suggested that these animals are sedentary, and only juveniles showed some mobility (Pearson et al. 1968). The same behavioral patterns were subsequently reported in a population of C. torquatus from Estao Ecolgica do Taim, RS (Travi 1983). Higher adult mobility has, however, been suggested by reports of the disappearance of marked individuals of C. talarum from populations in Argentina (Bush et al. 1989); the reproductive parameters and population growth rates for this species were reported by Malizia and Bush (1991). In the Argentinean province of Rio Negro, Patagonian tuco-tucos (C. haigi) have been found as using solitary burrows (Lacey et

J. R. Marinho and T. R. O. de Freitas

al. 1998). A population of C. minutus Nehring, 1887 in the coastal plain of Rio Grande do Sul, southern Brazil, displayed a low male density distribution and a predominance of philopatric males (Gastal 1994). Further work on C. minutus (Freitas 1997, Marinho and Freitas 2000, Gava and Freitas 2002, 2003, Freygang et al. 2004) reported only genetic data although establishing more precisely the geographic distribution of C. minutus fields and pas tures through out the coastal plains of Rio Grande do Sul and Santa Catarina in southern of Brazil. This species presents high chromosomic variability (2n = 42, 46a, 46b, 47a, 47b, 48a, 48b, 49a, 49b, 50a and 50b) and hybrid forms (2n = 46a48a). Despite these results, ecological aspects in C. minutus are still an open question. Our study intends to fill this gap, providing new data on the pattern of spatial distribu tion and ar range ment, density, sex ratio, external morphology, sexual dimorphism and structure of a population of C. minutus inhabiting the coastal plains of Rio Grande do Sul.

monospecies dominance. Forest formations are normally present under the configuration of fragments, associated with deposits of sand or turfs or of gallery forests, which are related to fluvial and delta deposits (Waechter 1985). This study was performed in natural grasslands in the locality of Palmital (2950S, 5008W) in the coastal plain of Rio Grande do Sul.

Sam pling
A capture-mark-release program was carried out in a 5.78 ha area to gather information about sex ratio, density, spatial distribution and population structure of C. minutus. Subterranean rodent traps (Oneida Victor n 0) covered with rubber to avoid injury to the animals. They were set in active burrow entrances that were identified by the presence of freshly excavated mounds of soil. The traps were set in all active mounds to ensure that closely spaced burrow systems were not missed. Animals were marked by tattooing the hind leg and released at the site of capture. The co-ordinates of the capture point of each animal were taken using a Global Positioning System (GPS). To minimize error in the GPS data, a reference point, taken from maps provided by the Brazilian Army, was used to calculate a correction factor (precision: 6 meters). This procedure adapted from Rempel and Rodgers (1997) was applied to each capture site, and reduced the error to less than one meter.

Morphometrics

Material and methods

Study site
The coastal plains of the State of Rio Grande do Sul has 2 35 000 km of lowlands and over 600 km of coastline. About half of this area is a complex lagoon system (Villwock 1984, Schwarzbold and Schaefer 1984) and the plant cover includes many communities distinguished both floristically and structurally (Klein 1967, Waechter 1985, Teixeira et al. 1986), including pastures and open field areas. The plant communities of this region present several distinctive characteristics when compared to those of other Brazilian states. These peculiarities are closely related to the relatively southern location of the state and, with the widening of the coastal plain and the lowering of the interior mountains to the south of 30 S latitude. The widening of the coastal plain, including the many deposit systems and the extensive lakes, defines an east-west gradient, where the plant communities vary from oceanic influences to relatively continental ones. The lowering of the interior high lands (Serra do Sudeste) and the presence of wide alluvial plains establish a differentiation on the landscape and on the vegetation which is less intense than on the more northern plains: such communities are limited by the Serra Geral and the Serra do Mar. Bush communities, fields and colonizer sites predominate on the coastal plain of Rio Grande do Sul. The bush communities usually constitute secondary successional stages, characterized by

For the morphological study of each individual the following data were recorded: body length, tail length, length of hind foot, length of hind foot with nail and weight. All linear measurements were log transformed, to minimize variance in the data (Ricklefs and Travis 1980).

Data anal y sis

All the comparisons were made using the two-sample t-test. Three ways of evaluating spatial arrangements by distance methods have been suggested (Peilou 1969): the Hopkins and Skellam method, the Clark and Evans method and the Peilou and Mountford method. In our study the Hopkins and Skellam method (Rabinovich 1978) was used. This method is based on the fact that only in random arrangements the dis tribution of distances from a random point to the nearest individual is the same as the distribution of distances from a random individual to its nearest neighbor. In the following equations, W1 is the sum of the squares of distances from random points to the nearest individuals, and W2, is the sum of the squares of the distances from random individuals to their nearest neighbors. Thus, calculating A = W1/W2, if A = 1 then the distribution is random, whereas for A < 1 it is a regular, and for A > l, it is grouped. The age classes of C. minutus were defined exclusively according to weight (modified from Wilks 1963): juveniles 105 g, female sub-adults from 105 to 170g, male sub-adults from 105 to 250g, and adults the limits found in sub-adults.

Structure of a Ctenomys minutus population

Results
Our sample consisted of 62 specimens of C. minutus (35 females and 27 males with 6 recaptures), plotted on a spatial distribution map (Fig. 1) according to the coordinates of their collection points, showing age classes and sexes. The orig i nal and re cap ture po si tions of six marked individuals are also plotted. Considering the most extreme point of capture, the polygonal center area that covered 5.78 ha determined the study site. The relative density was 10.7 individuals per ha. Corrected GPS measurements showed that animals moved only short distances as indicated in Fig. 1, being these distances determined by recaptures of the same animal. A main population group also was detected considering a large number of adults and high density of individuals in this area. As

cal cu lated by the Hopkins and Skellams method, the distribution of C. minutus conforms to a grouped distribution (W1 = 780.18; W2 = 33.48, A = 23.3 > l; n = 20 random distances), which is known to be a consequence of physical events in the environment. Analyzing the population fluctuation of C. minutus over one year of captures showed a decrease in the total number of females, while the number of males remained stable. However, the absolute number of captures of females was greater than the number of males in summer, autumn and winter (Fig. 2). The spring season showed a different pattern of population structure: no adult females were recorded and juveniles were observed only in this season. The absolute number of individuals by sex, age class and season is presented in Table 1.

S A A S

A A S A A S S A

S A A
-v v-v-v-vv-v-vv-v-v -v-v v

A A

Sand fields Gallery forest

A S A J J S A S A A S S A A S A A S S J A A A A A A

A A A A A

A A A A S A A A A

A A A

A A S A

Pasture fields I 30 m I

Fig. 1. Distribution map of the population structure of C. minutus in the study area. J juvenile, S sub-adult and A adult. Males circled. Arrows indicate direction of movement from first to last capture.

J. R. Marinho and T. R. O. de Freitas

16 14

Males Females

Number of captures

12 10 8 6 4 2 0 Jan-Mar Apr-Jun Jul-Sep Oct-Dec

Months
Fig. 2. Number of male and female C. minutus captured by seasons.

The sex ratio was unbalanced, with females being more frequent than males: 1.3:1 (total) and 1.26:1 (adults). However, in spring, males predominanted, representing 63.6% of the total number of individuals, and 100% of the adults (Table 1). Sex ual di mor phism was ob served in C. minutus. The two-sample t-test indicated that the males were significantly larger than females in all mea sure ments (Ta ble 2). Pe riph eral groups in the population showed a burrow system with greater dis tance be tween burrows than that found in the main or central burrow system, as well as a small number of individuals; most were sub-adults, indicating recent dispersion and possible initiation of other structured or non-viable populations. All juvenile animals were still in the main population group, but they were distributed on the margins of the group. The complete absence of burrow sharing by adults in the population was also detected.

Table 1. Total number of individuals captured from January to December 1996 and sex ratio of the captured individuals of C. minutus near Palmital, RS, Brazil. M males, F females. Juvenile Months M JanuaryFebruaryMarch AprilMayJune JulyAugustSeptember OctoberNovemberDecember Total F M 4 2 1 2 1 F 4 2 1 2 M 3 5 6 5 F 6 12 6 Sub-adult Adult Total sample M (%) 41.18 33.33 46.15 63.63 43.55 Total adults M (%) 33.33 29.41 50 100 44.19

Sex ratio

Sex ratio

1/1.43 1/2 1/1.16 1.75/ 1 1/1.3

1/2 1/2.4 1/1 1/0 1/1.26

Table 2. Sex ratio of individuals of C. minutus captured at Palmital, RS, Brasil. Total sample Months Sex ratio JanuaryFebruaryMarch AprilMayJune JulyAugustSeptember OctoberNovemberDecember Total 1/1.43 1/2 1/1.16 1.75/1 1/1.3 Males (%) 41.18 33.33 46.15 63.63 43.55 Sex ratio 1/2 1/2.4 1/1 1/0 1/1.26 Males (%) 33.33 29.41 50 100 44.19 Adults

Structure of a Ctenomys minutus population

Table 3. Measurements of C. minutus captured at Palmital, RS, Brasil, between JanuaryDecember 1996. Males (n = 27) x SD 200.6 18.0 80.4 5.1 36.4 2.3 41.7 2.8 266.0 63.0 Females (n = 35) x SD 177.3 16.3 74.2 5.0 33.3 2.3 38.0 2.7 184.4 38.1

Measurement

t-values

Body length (mm) Tail length (mm) Hind foot (mm) Hind foot with nail (mm) Body weight (g)

5.2632 4.8464 5.2615 5.2450 6.3061

< 0.05 < 0.05 < 0.05 < 0.05 < 0.05

Discussion
The ecology, geographic distribution and systematic relationships of Ctenomys populations have been reported since the work on ecology of this genus by Pearson et al. (1968), Travi (1983), Contreras and Scolaro (1986), Reig et al. (1990), Cook et al. (1990), Malizia and Bush (1991), Malizia et al. (1991), Gastal (1994), Cook and Yates (1994) and Freitas (1995). The present report supports a previous study on C. minutus (Gastal 1994) that found the distribution of this species showed the same pattern as that observed for C. talarum (Pearson et al. 1968) and C. torquatus (Travi 1983), which suggests territoriality and sedentary behavior as adult characteristics. Following these studies it was observed that juveniles disperse a few months after birth to occupy new territories, and are exposed to predation (remnants of a skull and coat of a juvenile were found in the study area), while the adults remain in the same place. The large number of adults recorded could be related to the predation suffered by juvenile forms when there is dispersion (Hansen 1962, Pearson et al. 1968). The main population group could be a center of dispersion that provides for the emergence of peripheral groups through the displacement of juvenile animals. The grouped distribution of C. minutus can be explained by the presence of areas with a higher density of individuals. This distribution is a direct consequence of environmental physical factors where groups are formed without social character and could be a mechanism for controlling ecological density as well as for pop-

ulation regulation (Rabinovich 1978, Ricklefs 1991). Due to sedentary behavior and fossorial habitat, populations of C. minutus inhabit open field areas. These areas are void of risk of flooding and the conditions are favorable to sustaining a pop ula tion that permits crossbreeding without the need for wide dispersion which reduces the risk of predation. Contiguous distributions in mammals are found when only short-distance movements occur or environmental factors change irregularly. Discontinuous changes in the environment may produce zones with environmental characteristics close to the optimum, and thus support a high density of individuals. Zones with intermediate conditions present an intermediate number of individuals, and zones with minimum survival conditions present very small (or zero) number of individuals (Rabinovich 1978). The low number of recaptured individuals may have resulted because traps were not reset in the same burrow systems. Individual animals tended to stay in the same burrow as indicated by the movement of sand in the mounds covering the burrows. This observation indicated that trapping did not cause damage to individual animals. The short distances moved by individuals confirm the sedentary population structure of C. minutus. These observations, together with the solitary habit of C. minutus, show the importance of spatial distribution in the reproductive process of this species. Since burrow occupancy is unitary (Lacey et al. 1998), a burrow distribution is needed in which distance between burrows is short enough to allow crossbreeding. As indicated in figure 1 C. minutus individuals do not move far from their burrows.

J. R. Marinho and T. R. O. de Freitas

The sex ratio of C. minutus was skewed towards females, probably due to the possibility of higher mortality and greater mobility of males. Similar sex ratios were previously found in C. minutus (Gastal 1994) and in C. talarum (Malizia et al. 1991). A sex ratio of 1:2 was found in field populations of C. torquatus while laboratory populations showed sex ratios of 1:1 (Talice et al. 1973). Spring was the only season where the number of males captured was greater than females. This was probably due to the reproductive status of females, which were occupied with caring for their young. The sexual dimorphism of C. minutus recorded in this study has been observed in this species (Gastal 1994) as well as in C. opimus (Pearson 1959, Cook 1990), C. talarum (Pearson et al. 1968), C. torquatus (Travi 1983) and C. flamarioni (Bretschneider 1987). In all cases males were larger than females. The coastal plain environment inhabited by C. minutus suffers from constant modifications because of urbanization, cattle-raising and agricultural land use, and drainage procedures associ ated with rice-paddy cul ti va tion (Freitas 1995). After our study ended, the study area was completely modified by soil preparation for agriculture, which strongly influenced the habitat of C. minutus. The growth in the size and number of farms is adversely affecting the environment of C. minutus, the distribution of this species being restricted by farming activities. The knowledge of the population biology of C. minutus will help to understand and solve conservation problems and as sist in the determination of re-location patterns for populations at risk.
Ac knowl edge ments: CNPq, FAPERGS and FINEP supported this work.

References
Bretschneider D. S. 1987. [Alguns aspectos da biologia e e c o l o gi a d e C t e n o m y s f l a m a r i o n i T r a v i , 1 9 8 1 (Rodentia-Ctenomyidae)]. Federal Uni versity of Rio Grande do Sul, Brasil: 198 [In Portuguese] Busch C., Malizia A. I., Scaglia O. A. and Reig O. A. 1989. Spa tial dis tri bu tion of a pop u la tion of Ctenomys t a l a r u m ( R o de n t i a, O ct o d o nt i d ae ) . J o u r n a l o f Mammalogy 70: 204208.

Contreras L. C. and Escolaro J. A. 1986. Distribucion y relaciones taxonomicas en tre los cuatro nucleos geograficos disyiuntos de Ctenomys dorbignyi en la Provincia de Corrientes, Argentina (Rodentia: Ctenomyidae). Historia Naural 6: 2130. Cook J. A., Anderson S. and Yates A. 1990. Notes on Bolivian mam mals 6. The ge nus Ctenomys (Rodentia, Ctenomyidae) in the high lands. Amer i can Mu seum Novitates 2980: 127. Cook J. A. and Yates A. 1994. Systematic relationship of the Bo liv ian tuco-tucos. Ge nus Ctenomys (Rodentia, Ctenomyidae). Journal of Mammalogy 75: 583599. Freitas T. R. O. 1994. Geographical variation of heterochromatin in Ctenomys flamarioni (RodentiaOctodontidae) and its cytogenetic relationship with other species of the genus. Cytogenetics and Cell Genetics 67: 193198. Freitas T. R. O. 1995. Geographic distribution and conservation of four species of the genus Ctenomys in Southe r n Br a z il ( R o d e n ti a Oc t o d o nt i d ae ) . S t u d i e s Neotropical Fauna and Environmental 30: 5359. Freitas T. R. O. 1997. Chro mo some poly mor phism in Ctenomys minutus (RodentiaOctodontidae). Revista Brasileira de Gentica 20: 17. Freygang C. C., Marinho J. R. and Freitas T. R. O. 2004. New karyo types and some considerations about the chro mo somal di ver si fi ca tion of Ctenomys minutus (Rodentia: Ctenomyidae) on the coastal plain of the Brazil ian state of Rio Grande do Sul. Genetica 121: 125132. Gastal M. L. A. 1994. Densidade, razo sexual e dados biomtricos de uma populao de C. minutus Nehring, 1887 (Rodentia, Caviomorpha, Ctenomyidae). Iheringia 77: 2534. Gava A. and Freitas T. R. O. 2002. Characterization of a hybrid zone between chromosomally divergent populations of Ctenomys minutus (Rodentia Ctenomyidae). Journal of Mammalogy 83: 843851. Gava A. and Freitas T. R. O. 2003. Inter and intra-specific hybridization in tuco-tucos (Ctenomys) from Brazilian coastal plains (Rodentia: Ctenomyidae). Genetica, 119, 1117. Hansen R. M. 1962. Movements and survival of Thomomys talpoides in a mima-mound habitat. Ecology 43:151154. Hopkins B. and Skellam J. G. 1954. A new method for deermining the type of distribution of plant individuals. Annals of Botany 18:213227 Klein R. M. 1967. Aspectos predominantes da vegetao sul-brasileira. [In: Congresso da Sociedade Botnica do Brasil]. Porto Alegre: 25576. Lacey E. A., Braude S. H. and Wieczorek J. R. 1998. Solitary bur row use by adult patagonian tuco-tucos (Ctenomys haigi). Journal of Mammalogy 79: 986991. Malizia A. I. and Busch C. 1991. Reproductive parameters and growth in the fossorial rodent Ctenomys talarum (Rodentia: Octodontidae). Mammalia 55: 293305. Malizia A. I., Vassallo A. I. and Busch C. 1991. Population and habitat characteristics of two sympatric species of

Structure of a Ctenomys minutus population

Ctenomys (Rodentia-Octodontidae). Acta Theriologica 36: 8794. Marinho J. R. and Freitas T. R. O. 2000. Intraspecific craniometric variation in chromosomal hybrid zone of Ctenomys minutus (Rodentia, Hystricognathi). Z. Saugetierkunde 65:226231. Massarini A. I., Barros M. A., Ortells M. O. and Reig O. A. 1991. Evolutionary biology of fossorial Ctenomyne rodents (Caviomorph: Octodontidae). I. Chro mo somal polymorphism and small karyotypic differentiation in Central Argentinian populations of tuco-tucos. Genetica 83: 131144. Nevo E. 1979. Adaptive convergence and divergence of subterranean mammals. Annual Review of Ecology and Systematics 10: 269308. Pearson O. P. 1959. Biology of the subterranean rodents, Ctenomys, in Peru. Memorias del Museu de Historia Naural Javier Prado 9: 156. Pearson O. P., Binsztein N., Boiry l., Busch C., Dipace M., Gallopin G., Penchaszadeh P. and Piantanida M., 1968. Estructura social, distribucion espacial e composicion por edades de una poblacion de tuco-tucos (Ctenomys talarum). Investigaciones Zoologicas Chilenas 13: 4780. Peilou E. C. 1969. An introduction to mathematical ecology. Tohn Wiley, New York: 1286. Rabinovich J. E. 1978. Ecologia de Poblaciones Animales. Secretaria General de la Organizacin de los Estados Americanos. Washington, DC :1114. Reig O. A., Bush C., Ortells M. O. and Contreras J. R. 1990. An overview of evolution, systematic, population biology, cytogenetics, molecular biology and speciation in Ctenomys. [In: Evolution of subterranean mammals at the organismal and molecular level. E. Nevo and O. A. Reig, eds]. Alan R. Liss, New York: 1422.

Rempel R. S. and Rodgers A. R. 1997. Effects of differential correction on accuracy of a GPS animal location system. The Journal of Wildlife Management 61: 525530. Ricklefs R. and Travis J. 1980. A morphology approach to the study of avian community organization. Auk 97: 321338. Ricklefs R. 1991. Ecology. Freeman, San Francisco: 1896. Schwarzbold A. and Schafer A. 1984. GLnese e morfologia das lagoas costeiras do Rio Grande do Sul Brasil. Amazoniana Kiel 9: 87104. Talice R. V., Mosera S. L. and Sprechmann A. M. S. 1973. Problemas de captura y sobrevivencia en cautividad en Ctenomys torquatus. Revista de Biologia del Uruguay 1: 121128. Teixeira A. B. 1986. Vegetao. In: Levantamento de recursos naturais. Rio de Janeiro: IBGE. 33: 541632. Travi V.H. 1983. [Etologia de Ctenomys to rquatus Lichtenstein, 1830 Rodentia-Ctenomyidae) na estao ecolgica do Taim, Rio Grande do Sul, Brasil]. Federal University of Rio Grande do Sul, Brasil: 1101. [In Portuguese] Villwock J. A. 1984. Geology of the coastal province of Rio Grande do Sul, Southern Brazil. A synthesis. Pesquisas 16: 549. Waechter J. L. 1985. Aspectos ecolgicos da vegetao de Restinga no Rio Grande do Sul, Brasil. Comunicaes do Museu de CiLncias da PUCRS 33: 4968. Wilks B. J. 1963. Some aspects of ecology and population dynamics of the pocket gopher (Geomys bursarius) in southern Texas. Texas Journal of Sciences 15:241283. Received 15 September 2003, accepted 25 May 2005. Associate Editor was Joseph F. Merrit.

Please translate all Portuguese titles into English and put them in square brackets