Biodiversity and Conservation 5, 1221-1229 (1996)

Bat species diversity in a lake archipelago in central Sweden M A G N U S JOHANSSON and J O H N N Y D E JONG* Department of Wildlife Ecology, Swedish University of Agricultural Sciences, Box 7002, S-750 07 Uppsala, Sweden

Received 20 January 1995; revised and accepted 17 September 1995

The bat fauna of 35 islands in a large lake in central Sweden were examined using ultrasound detectors. We tested the hypothesis that there is no difference in species number between the mainland and the island fauna. Eight species were found. Species numbers were analysed against island area, area of some habitats (coniferous forest, deciduous forest, semi-open habitats and open habitats), degree of isolation (distance from mainland and from 'stepping stones') and time spent searching for bats. Species number increased with area of deciduous forest. Presence of houses tended to increase species number. There seems to be a negative relationship between species number and degree of isolation (nearly significant). The results suggest that at least three species, Myotis brandti (Eversmann, 1845), M. mystacinus (Kuhl, 1819) and Plecotus auritus (Linnaeus, 1758), are negatively affected by forest patchiness. These species occurred mainly on large islands. Thus, the results do not support the hypothesis. The reasons why some species avoid open habitats are discussed.

Keywords: bat; distribution; diversity; archipelago; Sweden.

Introduction

Living in a patchy landscape with small, isolated patches of suitable habitat often involves special problems for animals. The ability of a species to survive and reproduce there is determined by patch size, quality and isolation together with species-specific characteristics such as mobility, territory size, demography and habitat specialization (Wiens, 1985; As et al., 1992).

Are bats, despite their great mobility, affected by habitat patchiness? Few studies have dealt with this question. Baker and Genoways (1978) described distribution patterns in the Caribbean Islands and Ahl6n (1983) investigated islands in Scandinavia, both authors reporting some effects of isolation on species number and composition. These studies concerned islands on a large geographical scale. Recent work (Limpens and Kapteyn, 1991) has shown that certain small-sized bat species actually avoid open areas, which suggests that patchiness on a small geographic scale also may affect habitat use by bats.

Here we want to test the hypothesis that the number of bat species is unaffected by patchiness (an area with patches of forest surrounded by open habitats such as water, fields or clearcuttings). If this is the case we expect to find the same species on the islands as occur on the mainland. Species that are common on the mainland should also be common on the islands. However, if some species avoid open areas we will probably find another pattern.

*To whom correspondence should be addressed.

0960-3115 © 1996 Chapman & Hall

1222 Johansson and de Jong

During June and July the females form colonies and forage in the area nearby the roost (Nyholm, 1965; Racey and Swift, 1985; Rydell, 1989). If the species avoid open habitats we should not expect to find them on islands which are so small that the females frequently have to cross large open areas and commute to other islands. The critical size of such islands is likely to depend on their degree of isolation from other islands or from the mainland. It may also depen d on habitat composition which affects the insect abundance.

Many essential properties of fragmented landscapes are also found in archipelagoes of 'real' islands, and archipelagoes can thus provide considerable help in understanding and predicting the effects of habitat fragmentation (As et aL, 1992). Therefore, this study also introduces some suggestions of the vulnerability of certain bats to habitat fragmentation.

Materials and methods

The study took place on 35 islands situated in Lake M/~laren in the east-central part of Sweden (59°19'-59°35'N, 16°10'-17°46'E). Thirty-one islands had an area of between 1 and 92 ha, while the other four were considerably larger, between 412 and 2642 ha. Some islands were dominated by coniferous forest, but most were covered with deciduous forest. Arable fields occurred on the larger islands. Lake M~ilaren is Sweden's third largest lake, covering an area of 1140 km 2. However, numerous islands and peninsulas result in large unbroken water surfaces being rare. Few islands are situated more than 3 km from the mainland. Eleven bat species have been found in the region (Ahl6n and Gerell, 1989).

The field work was carried out between 9 June and 9 August 1992 (i.e. during the period of bat pregnancy and lactation) and was performed by listening for bats using ultrasound detectors (Pettersson D-940 and D-980) during the 4 to 5 darkest hours of the night. Head lamps were used for better ability to spot bats by sight. The islands were visited at least twice but in most cases three times (mean time for islands < 100 ha = 197 min, SE = 19 rain, islands > 100 ha = 652 min, SE = 74m in). The search covered a variety of habitats, but mainly concentrated on areas considered as most rewarding (e.g. forests, forest edges and glades, and gardens). The time spent searching for bats was noted for each island.

Species and number of individuals were noted at each bat observation. In cases where species identification was difficult in the field (e.g. some species of Myotis), sound recordings were made and analysed in the laboratory (Ahldn, 1990). Since it was difficult to distinguish between the sounds of Myotis mystacinus and M. brandti, such observations were noted as M. mystacinus/brandti. Another problem was Plecotus auritus which often uses weak sounds. However, the flight behaviour of this species is very typical and during most of the field period it was easy to see the bats (except during the last week in July and in August).

Buildings were searched for bats during the periods at dusk and dawn when bats leave and return to their roosts, respectively. On larger islands, where there were too many buildings to be checked properly, the effort was concentrated on key buildings like churches, barns and houses where villagers had observed bats. The fieldwork was performed on rain-free nights, since bats are known to avoid heavy rain (Nyholm, 1965; Fenton, 1970; Kunz, 1974) and may reduce their activity even at moderate rain intensities.

Habitat mapping was carried out by analysing IR colour pictures in stereo. When measuring habitat area, a PC using the polygon method of area estimation was utilized. The habitats were classified as follows:

(1) coniferous forest,

Bat diversity in a lake archipelago 1223

(2) deciduous forest, defined as forest with at least 30% deciduous trees, (3) rock with a few trees, (4) garden, (5) pasture with a few trees, (6) grassland, (7) field, (8) reed, (9) clearcutting.

Habitats 3-9 were not present on all islands. To include these in the analysis, they were pooled by vegetation structure into two new habitat categories: (10) Semi-open (10=3+4+5) and (11) open (11 = 6 + 7 + 8 + 9 ) .

Two isolation concepts were used: isolation 1 = distance to mainland, and isolation 2 = distance to nearest potential 'stepping stone', defined as a forested island > 1ha strategically situated along a reasonable invasion route between a larger island and the mainland (Fig. 1).

The influences on species number of isolation 1 (ISO1), isolation 2 (ISO2), searching time (TIME), log area of coniferous forest (LOG 1), log area of deciduous forest (LOG2), log area of semi-open habitats (LOG 10) and log area of open habitats (LOG 11) were then analysed in a stepwise multiple regression (SAS/SYST): species number = LOG(l) LOG(2) LOG(10) LOG( l l ) ISO(1) ISO(2) TIME.

Results

Eight bat 'species' were observed: Myotis daubentoni (Kuhl, 1819), M. mystacinus/brandti (Kuhl, 1819)/(Eversmann, 1845), Eptesicus nilssoni (Keyserling and Blasius, 1839), Pipistrellus pipistrellus (Schreber, 1774), P. nathusii (Keyserling and Blasius, 1839), Nyctalus noctula (Schreber, 1774), Vespertilio murinus (Linnaeus, 1758) and Plecotus auritus. Two rare species, Myotis nattereri (Kuhl, 1818) and M. dasycneme (Boie, 1825), which have been reported from the surrounding mainland (Ahldn, personal communication) were not observed on the islands. The most common species were M. daubentoni, which occurred at 97% of the islands, followed by E. nilssoni (89%), P. pipistrellus (77%), N. noctula (43%), V. murinus (34%), M. mystacinus/brandti (26%), P. nathusii and P. auritus (6%).

Two 'species' which are common on the mainland (Ahl6n and Gerell, 1989), P. auritus

SQ

M

NOT STEPPING STONE STEPPING STONE

IC)

S o

a b c

Figure 1. Definition of 'stepping stone'. S = Stepping stone, I = studied island, M = mainland. (a) The small island (S) was strategically located along a reasonable invasion route and therefore regarded as a stepping stone. (b) The potential stepping stone is not situated along a reasonable invasion route. (c) and (d) The potential stepping stone is not strategically situated.

1224 Johansson and de Jong

and M. mystacinus/brandti, mainly occurred on the larger islands: Only two out of 27 islands smaller than 50 ha were used by M. rnystacinus/brandti, while five out of eight islands > 50 ha were used. P. auritus were found only on two of the largest islands.

In a stepwise multiple regression analysis bat species number was positively related to the area of deciduous forest (n = 35, p > 0.001, Fig. 2), and tended to be significantly influenced by the distance to mainland (n = 35, p -- 0.0569, Fig. 3). No other variables met the 0.15 significance level for entry into the model. Several of the variables were correlated to each other (Table 1).

The islands were divided into three size classes and the mean number of bat species in each class was calculated: < 20 ha; 3.2 species, 20-100 ha: 4.2 species, > 100 ha: 5.8 species (n -- 21, 10 and 4, respectively). Islands > 100 ha had significantly more species than islands < 2 0 h a (ANOVA/Tukey multiple range test, p <0.0]) . Other differences were not significant. Presence of houses tended to increase the number of species among islands < 100 ha in size (Mann-Whitney unpaired test; n = 31, two-tailed p --0.07).

8 -

0

O .

0

E

Z 3 -

l i •

• i •

.

° I ' I I '

0 10 100

Log[deciduous area]

Figure 2. The number of species was positively related to Log area (ha) of deciduous forest (stepwise multiple regression analysis, n = 35, r z = 0.55, F = 19.68, DF = 2, 32, Parameter estimate -- 2.54, p = 0.0001).

Bat diversity in a lake archipelago

8 -

1225

g 0

E

Z

• • • mmmm

' I

0 1000

' I ' I ' I

2000 3000 4000

Distance to mainland (m)

Figure 3. The number of species tended to be negatively related to distance to mainland (stepwise multiple regression, n=35, r2=0.55, F=19.68, DF=2, 32, Parameter estimate = -4.38"10 4, p = 0.0569).

Discussion

Some bat species avoid open areas (Limpens and Kapteyn, 1991). What are the reasons for this, and is this fact enough to explain their absence from islands in Lake M~ilaren? This investigation clearly suggests that at least two such 'species' are disfavoured by habitat patchiness: P. auritus and M. mystacinus/brandti, which generally were confined to the larger islands. The species-area relationship in Lake M~ilaren (Fig. 2) is a consequence of their preference for large islands. These species, which are common on the mainland, may be sensitive to habitat fragmentation.

Why do some bat species avoid open areas?

There are several hypotheses that could explain why certain bat species avoid open areas (Limpens and Kapteyn, 1991). One of them suggests that it reflects insect abundance, which is assumed to be lower in open habitats than in forests and forest edges. Open habitats would then be relatively unprofitable to hunting bats. The distribution of bats has indeed been shown to be affected by insect abundance (de Jong and Ahl6n, 1991). However, several bat species usually hunt in open spaces (Barclay, 1985; Rydell, 1986;

1226 Johansson and de Jong

Table 1. Correlation matrix for all variables. The matrix shows the correlation coefficient (r~) and the significance value (p). SPEC = number of species, ISO1 = distance to mainland, ISO2 = distance to stepping stone, TIME = survey time at each island, LOG1 = log area of coniferous forest, LOG2 -- log area of deciduous forest, LOG10 = log area of semi-open habitats, L O G l l = log area of open habitats, LOGTOT = log total island area, LOG1 + 2 = log area of forest.

SPEC ISO1 ISO2 TIME LOG1 LOG2 LOG10 LOG11 LOGTOT LOG1+2

SPEC 1.000 -0.183 -0.146 0.543 0.576 0.705 0.466 0.539 0.648 0.699 0.0 0.292 0.403 0.001 0.000 0.000 0 .005 0 . 0 0 1 0.000 0.000

ISO1 -0.183 1.000 0.465 0.088 -0.031 0.071 0.019 -0.149 0.061 0.068 0.292 0.0 0 .005 0.614 0.859 0.684 0.914 0.393 0.728 0.699

ISO2 -0.146 0.465 1.000 -0.010 -0.122 -0.099 -0.036 -0.227 -0.085 -0.091 0.403 0.005 0.0 0.956 0.485 0.572 0.838 0.190 0.630 0.603

TIME 0.543 0.088 -0.010 1.000 0.602 0.827 0.599 0.708 0.819 0.815 0.001 0.614 0.956 0.0 0.000 0.000 0.000 0.000 0.000 0.000

LOG1 0.576 -0.031 -0.122 0.602 1.000 0.798 0.850 0 . 8 5 1 0.877 0.858 0.000 0.859 0.485 0.000 0.0 0.000 0.000 0.000 0.000 0.000

LOG2 0.705 0.071 -0.099 0.827 0.798 1.000 0.734 0.804 0.966 0.989 0.000 0.684 0.572 0.000 0.000 0.0 0.000 0.000 0.000 0.000

LOG10 0.466 0.019 -0.036 0.599 0.850 0.734 1 .000 0 . 8 2 3 0.822 0.760 0.005 0.914 0.838 0.000 0.000 0.000 0.0 0.000 0.000 0.000

LOG11 0.539 -0.149 -0.227 0.708 0.851 0.804 0 .823 1 . 0 0 0 0.889 0.807 0.001 0.393 0.190 0.000 0.000 0.000 0.000 0.0 0.000 0.000

LOGTOT 0.648 0.061-0.085 0.819 0.877 0.966 0.822 0.889 1.000 0.975 0.000 0.728 0.630 0.000 0.000 0.000 0.000 0.000 0.0 0.000

LOG1 + 2 0.699 0.068 -0.091 0.815 0.858 0.989 0.760 0.807 0.975 1.000 0.000 0.699 0.603 0.000 0.000 0.000 0.000 0.000 0.000 0.0

Rachwald, 1992) - so other factors than insect abundance may also be important for the choice of hunting habitat.

The behaviour may be bet ter explained by the foraging strategy of these species than by absolute prey abundance. Bats choose foraging sites with respect to manoeuvrabil i ty and ability to localize prey (Aldridge, 1985), which may differ greatly between habitats and bat species (Habersetzer et aL, 1984; BaagCe, 1987; Norberg, 1987). Some species, e.g. P. auritus and M. nattereri, are adapted to foraging close to the vegetation. They readily hunt between branches in the canopy and the former species is even capable of picking insects f rom leaves. Norberg and Rayner (1987) classify this type of foraging behaviour as 'gleaning' or 'slow-hawking'. They could also be classified as ' forest bats ' because they forage near or within the forest. The high energy requirements of foraging bats makes the choice of high-quality hunting habitats especially important to this group of animals (Kalko and Braun, 1991) and many species hunt mainly within specific habitats (Ahlrn, 1990). Forest bats therefore should be expected to minimize the time spent foraging outside the forest.

Can forest bats live in a patchy landscape?

If open water surfaces are considered as being hostile to forest bats, how would this affect their ability to live in an archipelago such as Lake M~ilaren? There should be no problem for animals as mobile as bats to reach islands located 1-5 km from the mainland. The

Bat diversity in a lake archipelago 1227

slowest species in Sweden, P. auritus, needs about 20 min to fly 5 km (flight speed 4.1 ms-l; BaagCe, 1987). However, commuting between patches may be costly for species roosting on small patches in a patchy landscape, if the foraging success in the matrix habitat is low. The food resource may be too small on small islands, at least temporarily, which means that the bats have to visit other islands with higher insect abundance. This may be a problem especially for lactating females, that have very high energy requirements and need to visit the nursery several times during the night (Barclay, 1989). Thus, female bats should use only islands that are big enough to support a nursery. In this study it was evident that area of deciduous forest and probably also degree of isolation were two important variables which determine whether the island is suitable for bat colonies.

Males and non-reproductive females, on the other hand, have lower energy demands and do not have to return to the same island every night. Such individuals may be expected to visit even small islands. Barclay (1991) has also shown that males and females of the same species can have different distributions due to their energy requirements. Forest bats can, thus, survive in a patchy landscape but only reproduce on patches that are big enough to sustain the energetic demands of reproduction.

Distribution patterns in Lake Miilaren

Large continuous hunting grounds seem to be important to P. auritus and M. mystacinus/ brandti. Searching time was not related to the recorded species number when area was held constant. This means that positive sampling phenomena are probably unimportant here, which makes a true relationship with area realistic. ,~s et aL (1992) discuss this subject in greater detail. By definition, habitat fragmentation reduces patch sizes, and may be expected to affect the bat fauna negatively.

Some forest species preferred large islands during the reproductive season. However, some non-forest (aerial-hawking) species (e.g. the high-hunting N. noctula and E. nilssoni) paid much less attention to island area and isolation. They occurred on islands of all sizes, suggesting large hunting areas and a great deal of travelling during the night. N. noctula also often hunts at high altitude above lakes and borders between forests and cultivated land (Kronwitter, 1988), thereby taking advantage of matrix habitats. Lord and Norton (1989) predicted that only very mobile species would be able to use entire coarse- fragmented landscapes for foraging. N. noctula and E. nilssoni may well belong to this group of species.

The importance of specific habitats to bat species diversity

Bat species diversity increased with the amount of deciduous forest but was not affected by any other habitat parameter (Table 1). This is also what de Jong (1995) found in a study concerning bat species richness on woodland patches in cultivated fields. This result is not easily interpreted. For example, coniferous forest might well be expected to play an important role to bats - forest species, e.g.M, brandti, M. nattereri and P. auritus, often hunt in coniferous forest. However, deciduous forest is an important early season habitat for bats (de Jong and Ahl6n, 1991) and a greater insect abundance in deciduous forest (which has not been proven) could provide a large part of the explanation. Deciduous trees are also richer in cavities which could serve as bat roosts. In a recent study by Sandstrtim (1992), deciduous trees contained 80% of all cavities in natural forests. Furthermore, on the studied islands, coniferous forest was more intensely managed than deciduous forest, which also could make it less attractive to bats. However, on many islands there are houses,

1228 Johansson and de Jong

which may reduce the importance of natural cavities as bat roosts. There was actually a tendency (not significant) for the presence of houses to increase species number among islands < 100 ha. This suggests that access to roosts may be an important feature for certain species.

Conclusion

This study of bat species distributions on islands in a lake did not support the hypothesis that the number of bat species is unaffected by patchiness. The species were not randomly distributed, as expected from a simple sampling hypothesis. Two 'species' - P. auritus and M. mystacinus/brandti - were absent from small islands. Species number was significantly affected by area of deciduous forest, but unaffected by other habitat variables. Both degree of isolation and presence of houses tended to affect species number.

Acknowledgements

This study was part of a project on bat ecology supported by the Swedish Council for Forestry and Agricultural Research. The fieldwork was performed with the skilled assistance of M. Ekman and J. Gertz, while T. P~rt and H. Jernelid provided technical support for the data analyses. S. Ulfstrand and I. Ahl6n reviewed the manuscript.

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