Metapopulation in bats of Southern Brazil

The purpose was to show that displacements, promoters of genetic diversity in metapopulations, increase the probability of survival of bat species adapted to medium and long-distance flights. Samples were taken in four forest fragments, distributed in three municipalities in northern Paraná, and the maximum distance between the studied areas is 20 km. A monthly sampling was performed for each fragment, for the period of July 2008 to June 2009. We used eight nets for collection which remained open during the first four hours of the night, totalling 192 hours during a year of study. The marking occurred from October 2008 to March 2009 and was accomplished through the use of anodised metal rings of four different colours. One hundred and fifty individuals were banded and since the first capture, four displacements were recorded. After five months of collecting and marking, one Carollia perspicillata was found three km away. Two Artibeus lituratus were recorded about 20 km from the marking place: the first one after 22 months and the second one after 24 months. Additionally, one Platyrrhinus lineatus was captured at about 20 km, after 26 months. As they moved around over considerable distances and are not monogamous, they mate with females of other fragments, exchanging genes and reducing or even avoiding inbreeding. Thus, populations of bats have the ability to increase genetic diversity in metapopulations, provided by displacements between the forest fragments. Species that behave like this are not vulnerable to isolation.


Introduction
A set of populations connected by individuals who move between them constitute a metapopulation (Ricklefs, 1993;Paglia et al., 2006), as well as a population of populations. Initially, the metapopulation theory was proposed by North American ecologist Levins (1970), shortly after the release of the theory of island biogeography (MacArthur and Wilson, 1967). Historically, one was already aware of long migratory shifts of species common in Brazil, as Tadarida brasiliensis (I. Geoffroy, 1824), flying over 1,000 km, from the United States to Mexico, south or northbound, depending on climatic variables (temperature) and also the genus Myotis, which move more than 300 km, between Alabama and Tennessee, south of North America (Fleming and Eby, 2003). It is known that in southeastern and southern Brazil, the fragmented landscape is surrounded by modified environments that may or may not be unfavourable for bat species. The matrix surrounding forest fragments may be used and re-populated by species with some adaptive potential and extinguish those "estenobiontes" (Primack, 1993), so the degree of utilization of areas between the fragments ranges widely, causing changes in the population dynamics of species.
The size of the populations that relate to each other and form metapopulations depends on the number of individuals, migration and power of colonisation of each species. The exchange of genes between bats that seek, colonise and forage large areas is a decisive factor for the maintenance of gene flow, which is necessary to prevent a greater incidence of deleterious alleles within populations, which protect the survival of species (Pires et al., 2003).
What is the main advantage in bats exchanging genes with other populations, through displacement, forming metapopulations? To avoid the loss of evolutionary flexibility that occurs due to reduced genetic variability, which induces the population to not respond positively to environmental variances, a fundamental process for evolutional adaption in environments that suffer disturbances (Stockwell et al., 2003;Begon et al., 2007).
It is important to emphasize that "k" strategists like bats, which have a long life and generate very few offspring, need mechanisms to protect their population and continue the survival of the species (Odum and Barrett, 2007).
The objective here is to show that displacements, promoters of genetic diversity in metapopulations, increase the probability of survival of bat species adapted to medium and long-distance flights.
The maximum distance between the studied areas is of 20 km and the minimum is 4.1 km. Since the sites are close, they have similar characteristics in relation to climate and vegetation. According to Köppen's classification, the climate is humid subtropical and all fragments are remnants of semideciduous forest, which has highly diversified tree flora, compared to other forest types (Gusson, 2007).

Methodology
A monthly sampling was performed for each fragment, for the period of July 2008 to June 2009. We used eight nets for collection, which remained open during the first four hours of the night, totalling 192 hours over a year of study. The nets were set on trails and examined at intervals of 15 minutes (Reis, 1984), to avoid the stress of captive animals and prevent damage to the nets, caused by them.
The captured animals were marked and identified in the field with the aid of keys produced by Vizotto and Taddei (1973), Reis et al. (1993). The marking occurred from October 2008 to March 2009 and was accomplished through the use of anodised metal rings of four different colours, each colour corresponding to a fragment, to monitor possible displacements. Three sizes were used (2.5 mm, 4 mm and 6 mm in diameter) to cover bats considered small, medium and large.

Results
Of the four hundred and ninety-five individuals captured, one hundred and fifty were banded and since the first capture, four displacements were recorded (Table 1). After five months of collecting and marking, one Carollia perspicillata (Linnaeus, 1758) was found 3 km from the fragment where the marking occurred (Sítio Santana), being near the other remaining forest area (Parque Municipal) inserted in the studied area. The second displacement was recorded after one year and 10 months and one Artibeus lituratus (Olfers, 1818) was found at about 20 km (at the State University of Londrina) from the marking site (Sitio Cazado). The third displacement happened two years after the first collection, where another A. lituratus was located at about 20 km (also at the State University of Londrina) from the marking site (Sitio Cazado). And finally, a fourth movement was recorded after two years and two months, and one Platyrrhinus lineatus (E. Geoffroy, 1810) was captured at about 20 km (State University of Londrina) from the marking fragment (Sítio Cazado) (see Figure 2). For the time between marking and recapture, Gardner et al. (1991) estimated the life time of Artibeus fimbriatus Gray, 1838 in 4.5 years and Wilson and Tyson (1970) obtained an average of 7 years. Corroborating with these studies, we note here that the species mentioned have great potential for survival, which provides a better use of the landscape.

Discussion
If individuals of a population move between patches of certain habitats, establishing a connection, there is the formation of a metapopulation. Bats, like mammals, are evolutionarily superior when compared to other taxons. So they have three basic activities: feeding, reproduction and protection (Branco and Rocha, 1980). As they move around over large distances, and as they are not monogamous, they are obviously induced by hormones to mate with females of other distant fragments. Therefore, populations of bats have the ability to increase genetic diversity in metapopulation, provided by the displacements between the forest fragments. Species that behave like this are not as vulnerable to disappearance, as those with little displacement. That is, this is simply the practice of their second strongest instinct after feeding, i.e. reproduction, through crosses between individuals from different populations. Still, in relation to mating behaviour, polygamy is seen as a potentially important factor for the effective size of a population and gene flow (Salgueiro, 2007). Costa et al. (2006) reported the displacement of a male Artibeus fimbriatus in the state of Rio de Janeiro, which was recaptured 20 days after the first capture, at a distance of 21.7 km, with descent testicles, which indicates the maintenance of gene flow between mainland and islands in the southern state. This fact clearly suggests the establishment of a metapopulation. Bianconi et al. (2006) recaptured, after banded 653 bats of seven species, 54 individuals of six species in three different forest fragments in southern Brazil, and C. perspicillata and A. lituratus were recaptured more frequently, suggesting high mobility, showing, as the authors say, that the species are spatially arranged to use the landscape as a whole.
Esberárd (pers. obs.) cited a displacement of 71 km of an individual of the species A. lituratus and even small movements of C. perspicillata, Glossophaga soricina (Pallas, 1766), Anoura caudifer (E. Geoffroy, 1818), A. fimbriatus, Artibeus obscurus Schinz, 1821 and P. lineatus. When the bats move, they promote an increase in reproductive success, which could be in decline by the reduction of their populations generated by fragmentation of habitats. Consequently the variability increases within populations that are interrelated and it is known that genetic variability is vital for the maintenance of populations (Frankham et al., 2002).
Large displacements of Molossidae have always been clear (Altringham, 1996), forming large colonies, where sometimes millions of individuals live, which surely exchange genes. This knowledge is also essential for future studies with phylostomidae families and probably other families that are in the south and the rest of Brazil. That is, you need to know that these individuals can exchange genes between populations, living as metapopulations and trying to survive, despite the resistance imposed by the destruction and loss of habitat, since many regions show mosaics only (Begon et al., 2007). Some areas have small populations or are inhabited because individuals fail to disperse to reach them (Andrewartha and Birch, 1954). However the bats fly and several species of bats, especially of the genera Artibeus, Uroderma, Carollia and Phyllostomus probably treat the modified habitats as homogeneous compared to frequent records of their environmental plasticity (Fenton et al., 1992;Medellin et al., 2000;Sazima et al., 1994;Zortéa and Chiarello, 1994;Pedro et al., 1995;Reis and Muller, 1995;Reis et al., 2003). It is obvious, therefore, the fact that the bats were inserted within the context of metapopulation. For migratoty vespertilionids and Molossidae, insertion is more evident, since they have narrow and elongated wings, which provide long flights. Now phyllostomids must also be addressed, cited in the course of the text, which exploit large areas and different fragments in a landscape with patches of vegetation.