foraging by mediterranean horseshoe bats - Oxford Academic [PDF]

Journal of Mammalogy, 89(2):493–502, 2008

FORAGING BY MEDITERRANEAN HORSESHOE BATS (RHINOLOPHUS EURYALE) IN RELATION TO PREY DISTRIBUTION AND EDGE HABITAT URTZI GOITI,* INAZIO GARIN, DAVID ALMENAR, EGOITZ SALSAMENDI,

AND JOXERRA

AIHARTZA

Department of Zoology and Animal Cell Biology, Faculty of Science and Technology, University of the Basque Country, 48080 Bilbao, P.O. Box 644, Basque Country (UG, IG, DA, ES, JA) Estacio´n Biologica de Don˜ana (CSIC), P.O. Box 1056, 41080 Seville, Spain (DA)

We studied the effect of habitat type and prey availability on the foraging decisions of the Mediterranean horseshoe bat (Rhinolophus euryale), a species specialized for cluttered environments. We modeled seasonal habitat selection using radiotelemetry in relation to prey availability in a heterogeneous landscape, determined seasonal diet and prey selection, and used geographic information system data to characterize the landscape surrounding 10 breeding colonies in order to assess the radiotracking results at the population level. Although R. euryale typically has been associated with woodland, our results suggest that the existence of edge habitat, created by semicluttered structures such as hedgerows and woodland edges, was a significant factor in the choice of foraging areas by these bats. Edge habitat was associated with meadows and pastures, creating a landscape highly suited to moths, the preferred prey of R. euryale. In the study area, however, moths were evenly distributed among habitat types; therefore, distribution of moths cannot explain the preference of these bats for semicluttered habitats. The results of our study are consistent with the presumed origin of R. euryale in an edgerich ecosystem (i.e., the savannahs of northern Africa) and establish a new paradigm for how this species uses habitat. This new paradigm, which might also apply to other members of the genus in Europe, should prompt reconsideration of the presumed habitat requirements for this species, and should be incorporated into the conservation policies for the Mediterranean horseshoe bat. Key words:

compositional analysis, diet, ecotone, prey distribution, Rhinolophus euryale

2004). However, horseshoe bats (family Rhinolophidae) may face different ecological pressures because they produce specialized echolocation calls that may affect their foraging decisions in a different manner. Indeed, their calls are characterized by high-frequency, long constant-frequency pulses, with a high duty cycle, and a Doppler-shift compensation mechanism. As a result, this echolocation system provides orientation, fine discrimination, and classification of fluttering insects in cluttered conditions (Emde and Menne 1989; Emde and Schnitzler 1990; Kober and Schnitzler 1990; Link et al. 1986; Schnitzler 1968; Schnitzler and Kalko 1998; Schuller 1986; Trappe and Schnitzler 1982). Furthermore, with their relatively broad wings and short wingspan, rhinolophids are morphologically adapted to perform the maneuverable and slow flight necessary for moving through vegetation (Norberg and Rayner 1987; but see Swartz et al. 2006). The Mediterranean horseshoe bat (Rhinolophus euryale) is found mainly in the Mediterranean ecoregion, which is characterized by low rainfall (which occurs mostly in winter) and hot, dry summers. The species also occurs in the continental humid and Atlantic subregions within the Euro-Siberian

Radiotelemetry studies on the foraging ecology of bats have traditionally focused on the habitat use of a single species, seldom assessing diet and even more rarely assessing prey availability and distribution (e.g., Arlettaz 1996, 1999; Duverge´ and Jones 1994). Consequently, most studies can only conjecture about the factors contributing to the foraging behaviors observed. Any study that addresses the relationship between habitat use and prey availability would add valuable information, especially for insectivorous microchiropterans, because both predator and prey are elusive, complicating the study and comprehension of their ecological scenario. In a study of vesper bats (family Vespertilionidae), for example, use of ultrasound detectors showed that foraging activity of bats was influenced by the abundance of insects and associated with habitats that offered an open canopy or still water (Kusch et al.

* Correspondent: [email protected]

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ecoregion (Aihartza 2001; Iba´n˜ez 1999; Uhrin et al. 1996), where it may experience climatic and habitat conditions (e.g., deciduous woodland) differing significantly from those typical of the Mediterranean. Those differences lead to differences in plant composition and structure, and different prey types. The most dramatic population declines of R. euryale have occurred in non-Mediterranean areas (Aihartza 2001; Brosset et al. 1988; Hora´cek 1983–1984). Previous radiotracking studies have demonstrated the importance of broad-leaved trees to R. euryale in the Mediterranean (Russo et al. 2002, 2005) and Euro-Siberian (Aihartza et al. 2003; Goiti et al. 2003) ecoregions. Although dense broadleaved woodland was preferred in the Mediterranean region, Goiti et al. (2003) reported that this species selected more open structures such as hedgerows in an Atlantic environment. Because each of these previous studies was limited to a single season, the researchers could only conjecture on habitat use in other seasons; moreover, none determined the food items consumed, or the effect of the distribution or abundance of potential prey. We hypothesized that decisions by R. euryale about where to forage would follow the distribution of the preferred prey items whenever they were found in cluttered conditions or habitats, and would be consistent across seasons. In this study, we applied 2 complementary approaches to investigate habitat choices of R. euryale in the northern Iberian Peninsula, located in the Atlantic subregion of the Euro-Siberian ecoregion. First, we determined the relationship between diet and the availability and distribution of prey in conjunction with a study of habitat selection based on radiotracking bats during 3 seasons: prebreeding, lactation, and postlactation. Because we studied a colony numbering up to 567 individuals (during the breeding season), we assumed that an environment sustaining such a relatively large colony (Iba´n˜ez 1999) reflected a favorable situation, and that the results would be representative of the species. Second, we studied the pattern of habitat use at the population level and attempted to depict a general preferred landscape for the species, following recommendations by Garshelis (2000) and Garton et al. (2001). To achieve this goal, we identified key habitats by relating breeding colony size to the availability of the habitats found around those sites. The breeding period is the most energetically demanding period (Kurta et al. 1990; Racey and Speakman 1987); therefore, only locations corresponding to breeding colonies were included in the analysis, because such sites are assumed to approximate a suitable condition for the species, and would provide the most relevant information for setting conservation goals.

MATERIALS AND METHODS Study area of the radiotelemetry study.— The study area was in the Karrantza Valley, Basque Country, northern Iberian Peninsula, southwestern Europe (438139N, 38229W). The area has an Atlantic climate and an annual rainfall of 1,400 mm that occurs throughout the year. The driest months are July and August, although drought conditions occur rarely. The landscape is rugged, with steep, rolling hills ranging between Downloaded from https://academic.oup.com/jmammal/article-abstract/89/2/493/938130 by guest on 23 January 2018

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200 and 900 m above sea level. Cattle- and sheep-rearing for dairy production was the main human activity in this area and there were no large arable fields, which resulted in a highly heterogeneous, seminatural landscape. Habitat categories.—We identified the following habitats: 1. Meadows and pastures were the most abundant (58% by area) and widespread habitats throughout the altitudinal profile. Land-management practices were highly variable and depended on the intensity, frequency, and season of grazing, mowing, or manuring, all carried out very similarly to the traditional manner. 2. Broad-leaved woodland was dominated by Quercus robur, along with Fraxinus excelsior, Castanea sativa, Acer campestre, Prunus avium, Corylus avellana, Salix atrocinerea, Crataegus monogyna, and others. In some places, the understory also may be covered by bramble (Rubus ulmifolius). This habitat was mainly restricted to steep areas and found in rather small woods. Riparian forest, dominated by Alnus glutinosa, covered a minor portion of the area and was included under this category. 3. Hedgerow included linear hedgerows of variable height and woodland copses 0.1 ha, which were composed of the same tree species that were found in deciduous woodlands and varied in structure and extent of connectivity. 4. Holm-oak woodland was found in karstic areas and was dominated by Quercus ilex, along with other scrubs such as Arbutus unedo, Prunus spinosa, Smilax aspera, C. avellana, and Rhamnus alaternus. In the recent past, this habitat was exploited for firewood or cleared to create pastures; consequently, it consisted mostly of young trees (,4–5 m tall), an extremely thick understory, and a high density of climbing and thorny species. 5. Coniferous plantations, most of which consist of Monterrey pine (Pinus radiata), have little economic importance in this area and were relatively scarce. Generally, they were not managed and, in some locations, had well-developed understories of invasive deciduous tree species and shrubs. 6. Eucalyptus (Eucalyptus globulus) plantations were relatively new in the area. They were densely planted and had 3 well-defined strata consisting of crown, bare trunk, and an understory that can be bare or dominated by bramble. These plantations were primarily used for paper production and are clear-cut every 10–15 years. 7. Isolated trees included trees that were at least 10 m apart (crown-to-crown); most were broad-leaved species. 8. Scrubland included upland heath-dominated areas and gorse- and fern-dominated areas created by the abandonment of pastures. 9. Other habitats included bare rock areas, urban habitat, and other human-created structures (e.g., quarry and reservoir). Bat capture, tagging, and fecal collection.—Bats were captured using a harp trap (Tuttle 1974) as they entered the roost. Some bats were placed individually in cloth bags and, to assure that enough droppings were expelled, held for up to 5 h. Fecal pellets were stored in vials. Other bats were fitted with radiotransmitters (PipII; Biotrack Ltd., Dorset, United Kingdom)

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using surgical adhesive (Skinbond; Smith and Nephew, Largo, Florida). During the prebreeding period, the radiotransmitters used weighed 0.55 g; thereafter, 0.45-g and 0.35-g transmitters  ¼ 5.5% and 5% of body were used on adults and juveniles (X weight, respectively). Bats were captured in May 2001 (prebreeding period), July 2002 (an unusually cool summer), July 2003 (lactation period), and September 2003 (postlactation period). In the summer of 2002, the average temperature was 28C colder than normal (Basque Meteorology Service, www. euskalmet.net); on 2 July of that year, we trapped very few breeding female R. euryale, and most of the bats in the colony were nulliparous females and males. The weather did not appear to have a similar effect on Myotis emarginatus, and the majority of those captured were lactating females. In July 2003, when weather conditions were favorable, 86% of the adult R. euryale captured were lactating females (Goiti et al. 2006). All procedures were approved by the Regional Council of Biscay and meet guidelines recommended by the American Society of Mammalogists (Gannon et al. 2007). Fecal analysis.— Bat feces were soaked in 50% ethanol and fixed in glycerine before examination under a 40 magnifying lens. Arthropods were identified with the aid of Chinery (1977), Barrientos (1988), McAney et al. (1991), and a reference collection. We used the individual bat as the sampling unit (Whitaker et al. 1996). Prey consumption was measured using 2 methods. First, percentage volume was measured as the proportion (percentage) of the surface area of a grid covered by a given prey category from the total sample. In addition, to estimate the absolute volume of each prey type consumed per bat, we measured the volume of each fecal dropping. Second, percentage occurrence was measured as the number of bats from which the particular item was recovered divided by the total number of bats examined and multiplied by 100 (McAney et al. 1991; Whitaker 1988). To assess seasonal differences in prey categories consumed by the bats, we performed an analysis of variance (ANOVA) on arcsine-transformed volume percentages (Murray and Kurta 2002; Whitaker 2004). Availability of arthropods.— We assessed availability of arthropods each season by using ultraviolet light traps (G8010; Entomopraxis, Barcelona, Spain) to sample within the area delimited by all of the active radiotracking locations. Although the use of a single sampling method would give a biased result, it allows seasonal and between-habitat comparisons; in addition, light traps are a widely used method (Dunning and Kru¨ger 1996; Hickey et al. 1996; Jones 1990; Lacki et al. 1995; Sample and Whitmore 1993), permitting comparisons with other studies. We collected samples in the following woody habitats: broad-leaved woodland, hedgerow, coniferous plantations, Eucalyptus plantations, and holm-oak woodland. Each study season, we conducted 4–6 trapping sessions (nights), setting a light trap in each of those woody habitats from dusk to dawn for each session. Captured arthropods (for convenience hereafter referred to as insects) were preserved in alcohol and later identified with the same taxonomic accuracy as for fecal analysis, using Barrientos (1988) and Chinery (1977). Variation in abundance of insects between habitats and seasons was Downloaded from https://academic.oup.com/jmammal/article-abstract/89/2/493/938130 by guest on 23 January 2018

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compared on logarithmically transformed data using ANOVA and Tukey’s post hoc multiple comparison tests (P , 0.05). Radiotracking and habitat use.— Each study season, we radiotracked bats for a period of 3 weeks to assure interindividual comparability. Our 3 radiotracking units were equipped with receivers (1000-XRS; Wildlife Materials, Carbondale, Illinois, and FT-290RII; Andreas Wagener Telemetrieanlagen, Ko¨ln, Germany), handheld 3-element yagi antennas, and 2-way radios. Locations were recorded every 15 min during the prebreeding period and every 10 min during the lactation and postlactation periods. We recorded locations when bats were active and resting, but only active locations were used in analyses. In the field, locations were recorded on orthophotographs; locations were subsequently added to a geographic information system database (Arcview 3.2; ESRI, Redlands, California). Analyses of habitat and prey selection.— Habitat selection and prey selection were assessed by compositional analysis (Aebischer et al. 1993). The unit of statistical independence was the individual tracked bat. The significance of Wilk’s and t statistics were obtained using randomizations based on 1,000 iterations. Compositional analysis is sensitive to the number of categories used by the animals; therefore, only those categories (habitat or prey) used in a given season were considered ‘‘available’’ and included in the analyses (Aebischer et al. 1993). The data were analyzed as a single overall sample and by season. In the analyses at the level of the individual, unused but available categories were usually recorded as 0.1% (in 2 seasons by 0.01%), so the values were less than the lowest recorded nonzero percentage. The data were analyzed using Compos Analysis 5.1 (Smith Ecology Ltd., Abergavenny, United Kingdom). Habitat selection.—In each season, the study area was defined by the minimum convex polygon that encompassed all of the locations at which the bats were active (MCP%100). To quantify habitat type availability within the study area, we used land-use maps (Forest Inventory, Basque Government, Bilbao, Spain). Hedgerows and isolated trees were not included in the inventory; therefore, the abundance of those habitats was estimated using orthophotographs, in which we examined quadrats chosen at random from the meadows and pastures category and representing 10% of the total area. The analyses were performed using Arcview 3.2 geographic information system software (ESRI). Prey selection.— We considered absolute volumes of consumed prey categories as ‘‘used’’ values, and estimated available prey biomass using specific regression equations for each insect taxon (W ¼ aBLb, where W ¼ weight in milligrams, BL ¼ body length in millimeters, a ¼ intercept, and b ¼ slope [Ho´dar 1996]). To estimate the total biomass available, we applied the mean length of a given taxon in its specific equation, and multiplied the result by the number of specimens captured. Those equations are based on body length, which is an improvement over traditional estimates based on the means of allometric indices for 2 reasons: they include the individual weight variance within each taxon, and the predictive power of the equations is high (Ho´dar 1996).

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TABLE 1.—Mean seasonal light-trap captures of moths per night in 5 arboreal habitats in the Atlantic region of the Basque Country, northern Iberian Peninsula, 2001–2003, and the results of the analysis of variance for each period (P , 0.05). Pooled Habitat

 X

HED BW HOW CON EUC ANOVA

199 306 180 202 242

a

a

SD

Prebreeding  X

n

138.7 20 251.7 20 146.9 19 116.1 19 186.2 20 F ¼ 1.61, d.f. ¼ 4, 93, P ¼ 0.18

79 133 88 106 97

SD

Lactation n

38.7 5 94.3 5 36.0 4 85.2 4 44.7 5 F ¼ 0.50, d.f. ¼ 4, 18, P ¼ 0.74

 X 335 548 294 285 428

SD

Cool summer n

125.1 6 319.6 6 173.2 6 118.4 6 232.7 6 F ¼ 1.70, d.f. ¼ 4, 25, P ¼ 0.18

 X

SD

Postlactation n

195 202 160 232 199

123.2 4 44.4 4 183.4 4 109.2 4 108.9 4 F ¼ 0.18, d.f. ¼ 4, 15, P ¼ 0.95

 X

SD

n

158 271 133 154 198

104.8 5 157.9 5 49.7 5 73.2 5 59.1 5 F ¼ 1.57, d.f. ¼ 4, 20, P ¼ 0.22

HED ¼ hedgerow; BW ¼ broad-leaved woodland; HOW ¼ holm-oak woodland; CON ¼ coniferous plantation; EUC ¼ Eucalyptus plantation.

Habitat composition around maternity colonies using geographic information systems.— We determined the habitat composition around colonies where breeding was confirmed. As previously noted, the time during which offspring are reared, particularly lactation, is the most energy-demanding period in the life cycle of bats (Racey and Speakman 1987); therefore, we assumed that the larger the breeding colony was, the closer it was to an optimal condition. Therefore, we looked for relations between colony size and any of the habitats surrounding the colonies. For comparability, all of the known breeding colonies within 10,000 km2 of the Atlantic climatic subregion were included in the analysis. To estimate the area covered by each habitat, geographic information system data were used to overlay roost locations on forestry inventory layers (Forestry Inventory, Basque Government and Land Use Inventory of Navarre, Pamplona, Basque Country, and Inventaire Forestier National du France, Paris, France). Because hedgerows and isolated trees were not included in any of the forest inventories, their abundance was calculated as described above. In accordance with data from previous radiotelemetry studies (Aihartza et al. 2003; Goiti et al. 2003, 2006; Russo et al. 2002), we delimited 2 areas of analysis with a 5- and 10-km radius around the main roost of each colony. Additionally, we determined the ‘‘length of ecotone index,’’ which is the interface between any broad-leaved woodland, hedgerow, or isolated tree and a pasture or meadow. The ecotone index was estimated using orthophotographs of the areas of analysis that covered a total area of 800 ha (8 quadrats of 100 ha each, chosen at random) within a 5-km radius around each maternity colony. Significance of the correlations between the proportion of each habitat category, the ecotone index, and the colony size were determined using Spearman’s rank correlation coefficient.

RESULTS Availability of arthropods.— In 20 trapping nights using 98 light trap sets, we captured a total of 46,086 flying or airborne insects, corresponding to 14 orders. The most abundant taxa were moths (Lepidoptera), representing 49% of the insects trapped. Flies (Diptera) were the 2nd most numerous group (42%), followed by beetles (Coleoptera; 2.9%), wasps (Hymenoptera; 2.2%), and Homoptera (2.2%). Other taxa were collected in trace quantities. In almost all periods, moths were the Downloaded from https://academic.oup.com/jmammal/article-abstract/89/2/493/938130 by guest on 23 January 2018

most abundant insects (55–66%), except during the prebreeding period (only 18%), when flies dominated the samples (76%). Because of the importance of moths in the diet (see next section) and the low availability for other prey categories, further analyses were performed only with moths. The abundance of moths varied significantly among seasons, regardless of habitat (ANOVA: F ¼ 18.02, d.f. ¼ 3, 94, P , 0.0001), and was significantly higher in July 2003 (Tukey’s test, P , 0.001 for all combinations). The abundance of moths did not differ between May 2002, July 2002, and September 2003 (pairwise Tukey’s tests, all P . 0.05). Abundance of moths also did not differ among habitats when the data were pooled across seasons or analyzed by season (Table 1). Although high within-habitat variation precluded detection of statistical significance, broad-leaved woodlands had the highest abundance of moths in all seasons, except for the cool summer of 2002 (Table 1). Hedgerows always had a medium-to-low abundance of moths and frequently had fewer moths than did Eucalyptus and coniferous plantations (Table 1). Seasonal diet and prey selection.— Bats were assigned to 1 of 8 classes based on season, sex, reproductive status, and age (Table 2). Within each class, bats corresponded to 2 capture sessions that occurred within a 1-week interval. Fecal analysis  ¼ 4.8 droppings/ included 810 feces from 168 individuals (X bat). Overall, the diet of R. euryale included 10 prey categories (Table 2), but moths were by far the most abundant (by volume, seasonal values ranged between 68% and 99% of the diet). Furthermore, by volume, moths represented at least 90% of the diet in 5 of the 8 classes of bats. Moths were found in the fecal droppings of 96% of individual bats and, among sampling periods, that value varied between 85% and 100%. Moths appeared to be the most important prey during the lactation and postlactation periods of female and male adults, and for the juveniles as well. The proportion of moths in the diet differed significantly (ANOVA: F ¼ 9.74, d.f. ¼ 7, 160, P , 0.0001) among the 8 classes of bats. The diets of males and females in May were similar, but both were significantly different from all of the other classes, except for the diet of females in the cool July 2002. The diet of these latter females only differed significantly from that of juveniles and adults in September 2002. No other difference between classes was detected (Tukey’s test, P , 0.05 for all of the pairwise comparisons).

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TABLE 2.—Seasonal diet of Rhinolophus euryale in the Atlantic region of the Basque Country, northern Iberian Peninsula, 2001–2003, expressed as percentage volume and percentage occurrence. nb ¼ number of bats; nf ¼ number of feces. May

July 2003

July 2002 (cool)

September

Females (nb ¼ 21; nf ¼ 70)

Males (nb ¼ 22; nf ¼ 70)

Lactating females (nb ¼ 37; nf ¼ 207)

Males (nb ¼ 6; nf ¼ 30)

Females (nb ¼ 14; nf ¼ 79)

Males (nb ¼ 14; nf ¼ 84)

Adults (nb ¼ 29; nf ¼ 145)

Juveniles (nb ¼ 25; nf ¼ 125)

Lepidoptera Neuroptera

68.5

70.3

94.2

91.3

82.6

94.7

99.4

97.3

Chrysopidae Hemerobiidae

0.0 0.1

0.0 0.3

2.6 1.0

2.5 3.7

3.6 2.2

1.7 0.0

0.3 0.0

1.7 0.0

7.4 0.2

4.5 2.5

0.8 1.3

0.2 0.1

9.5 1.4

1.4 0.5

0.0 0.3

0.1 1.0

20.7

22.3

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.1

0.0

0.4

0.2

0.0

0.0

0.0 3.0 0.1

0.0 0.0 0.1

0.0 0.0 0.1

2.2 0.0 0.0

0.3 0.0 0.0

1.1 0.0 0.3

0.0 0.0 0.0

0.0 0.0 0.0

90

86

100

100

92

100

100

100

0 1

0 3

21 4

13 10

92 14

57 0

4 0

10 0

24 3

23 14

5 6

3 7

43 14

14 14

0 2

1 3

24

24

0

0

0

0

0

0

0

0

1

0

7

7

0

0

0 7 1

0 0 3

0 0 1

10 0 0

7 0 0

21 0 7

0 0 0

0 0 0

Taxon Percentage volume

Diptera Tipulidae Brachycera Coleoptera Rhizotrogus Unidentified Psocoptera Hymenoptera Unidentified Percentage occurrence Lepidoptera Neuroptera Chrysopidae Hemerobiidae Diptera Tipulidae Brachycera Coleoptera Rhizotrogus Unidentified Psocoptera Hymenoptera Unidentified

The scarabaeid beetle Rhizotrogus was another important prey taxon, although its consumption was highly seasonal and restricted to the prebreeding period. Percentage occurrence illustrated the importance of moths as well but also emphasized consumption of other taxa such as green (Chrysopidae) and brown (Hemerobiidae) lacewings (Neuroptera) and craneflies (Diptera, Tipulidae). Lacewings were consumed in both summers studied, but were particularly common in the cool

July 2002, when they appeared in the diet of 92% of the females and 57% of the males. Craneflies were most frequent in the diet in spring and in the cool July 2002. Other items (brachyceran flies, Psocoptera, and Hymenoptera) appeared less frequently or in smaller amounts. The prey selection index was highly significant in the pooled data and in the seasonal compositional analyses (Wilk’s k ¼ 0.029–0.099, P ¼ 0.001 for all cases; Table 3). In the pooled

TABLE 3.—Compositional preference order for seasonal and pooled prey selection of Rhinolophus euryale. Habitats were ranked from the most preferred to the least preferred. A significant preference between 2 prey categories was indicated by ‘‘...,’’ whereas a nonsignificant difference was indicated by ‘‘..’’ Analysis

n

Wilk’s k

P

Prey preference rankinga

Pooled Prebreeding Lactation Postlactation Juveniles Cool summer

168 43 43 29 25 28

0.029 0.088 0.029 0.047 0.042 0.099

0.001 0.001 0.001 0.001 0.001 0.001

LEP ... CHR ... HEM ... PSO . RHI . TIP ... BRA ... HYM ... COL LEP . RHI . HEM ... TIP ... BRA . HYM LEP . CHR ... HEM ... TIP ... BRA . COL LEP ... CHR ... BRA LEP . CHR ... TIP ... BRA CHR ... LEP . HEM . PSO ... TIP ... BRA . COL

a LEP ¼ Lepidoptera; CHR ¼ Chrysopidae; HEM ¼ Hemerobiidae; PSO ¼ Psocoptera; RHI ¼ Rhizotrogus; TIP ¼ Tipulidae; BRA ¼ Brachycera; HYM ¼ Hymenoptera; COL ¼ Coleoptera except Rhizotrogus.

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habitat locations (MCP%100 ¼ 1,333 ha). In July 2002, we tracked 6 bats and obtained 81 habitat locations (MCP%100 ¼ 2,910 ha), whereas in July 2003, 15 bats were studied and we obtained 373 habitat locations (MCP%100 ¼ 10,707 ha). Finally, in September 2003, 9 juveniles (311 habitat locations and MCP%100 ¼ 3,494 ha) and 7 adults (175 habitat locations and MCP%100 ¼ 7,152 ha) were radiotracked. Bats always foraged in areas where there were trees, and never foraged over open meadows, pastures, heath, gorse- or fern-covered areas, or any other open habitats. Foraging habitats were diverse in terms of tree density and structure, and ranged from isolated trees to closed woodland. Hedgerows were used by 96% of all tagged bats, with use of hedgerows (expressed as the mean of individual means) ranging seasonally  ¼ 53%; Fig. 1). The next between 45% and 66% (seasonal X most used habitat was broad-leaved woodland, used by 90% of all the bats, with its use ranging seasonally between 27% and  ¼ 33%). Isolated trees comprised 1–12% of 45% (seasonal X  ¼ 9%), and 52% of all the bats foraging locations (seasonal X used this habitat type in any season. Neither holm-oak woodland nor coniferous plantation reached 4% of locations either in a given season or across seasonal average, and each was used by only 14% of the bats. Eucalyptus plantations were used only in September 2003, by both adults (5%) and juveniles (3%), and overall this habitat was used by a mere 4% of the bats studied. Across all individuals studied, compositional analysis identified hedgerow as the most preferred habitat, regardless of season, and this was used significantly more than broadleaved woodland (Table 4). Seasonally, although hedgerow was also ranked 1st during all time periods except postlactation, differences were not significant compared with broad-leaved woodland and isolated trees (Table 4). Coniferous plantation was the least preferred of all the habitats both in the pooled analyses and in all seasonal analyses except during prebreeding (Table 4). Interestingly, of the locations assigned to any wood type, we determined that at least 33% corresponded to bats foraging along edge habitat; therefore, semicluttered habitats (i.e., hedgerow, isolated trees, and woodland edge) represented at least 73% of all of the habitat-use locations. Habitat composition around maternity colonies and its relation to colony size.— Only 10 roosts fulfilled our requirements for further analysis, likely a consequence of both the highly clumped breeding period distribution and ongoing

FIG. 1.—Mean (%) habitat use by Rhinolophus euryale during the prebreeding, lactation, and postlactation periods revealed by radiotracking in an Atlantic seminatural landscape in the Basque Country, northern Iberian Peninsula, 2001–2003. HED ¼ hedgerow; BW ¼ broad-leaved woodland; IST ¼ isolated tree; EUC ¼ Eucalyptus plantation; CON ¼ coniferous plantation; HOW ¼ holm-oak woodland.

data set, moths were the preferred prey (Table 3). Green and brown lacewings were 2nd and 3rd, respectively, in preference. Less preferred were, in decreasing order, brachyceran flies, wasps, and beetles other than Rhizotrogus, which was midranked. For the seasonal compositional analyses, sexes were combined within seasons because of the lack of differences observed in moth consumption. Seasonally, moths were the most preferred item, along with other prey such as Rhizotrogus and brown lacewings during the prebreeding period, and green lacewings during the lactation period. During the cooler summer of 2002, however, green lacewings were preferred to moths (Table 3). Seasonal habitat use and selection.— Overall, we radiotracked 50 bats, for which 1,144 habitat locations were recorded while bats were active, averaging 23 locations/bat (SD ¼ 11.7 locations/bat), and 4 tracking days/bat (SD ¼ 1.7 tracking days/bat). We favored the homing-in method, and generally discarded locations obtained by triangulation unless we were very confident about the correct assignment to a habitat. During prebreeding, we tracked 13 bats and obtained 204

TABLE 4.—Results of compositional analysis on seasonal habitat selection in Rhinolophus euryale in the Atlantic region of the Basque Country, northern Iberian Peninsula, 2001–2003. Habitats were ranked from the most preferred to the least preferred. A significant preference between 2 habitats was indicated by ‘‘...,’’ whereas a nonsignificant difference was indicated by ‘‘..’’ Analysis

n

Wilk’s k

P

Habitat rankinga

Pooled Prebreeding Lactation Postlactation Juveniles Cool summer

50 13 15 7 9 6

0.087 0.020 0.125 0.000 0.014 0.046

0.001 0.001 0.005 0.013 0.013 0.098

HED ... BW ... IST ... HOW . EUC . CON HED . BW . IST ... CON . HOW HED . BW . IST ... HOW . CON BW . HED . HOW . IST ... EUC ... CON HED . IST . BW ... HOW . EUC . CON HED ... BW . IST . HOW . CON

a

HED ¼ hedgerow; BW ¼ broad-leaved woodland; IST ¼ isolated tree; HOW ¼ holm-oak woodland; EUC ¼ Eucalyptus plantation; CON ¼ coniferous plantation.

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TABLE 5.—Habitat composition (mean % and SD) within 5- and 10-km radius of 10 maternity colonies of Rhinolophus euryale, Spearman correlation coefficient for each category relative to colony size, and Mann–Whitney test to compare composition around both radii. NS ¼ not significant. Radius 5 km Habitat

a

MEAD/PAST SCR HOW CON BW EUC OTH LECOT (m)

 X

SD

30 25 2 16 24 2 1 60

15.0 18.3 2.9 21.4 11.8 2.9 1.3 18.2

Radius 10 km R 0.47, 0.10, 0.25, 0.45, 0.22, 0.44, 0.14, 0.63,

2

NS NS NS NS NS NS NS P , 0.05

 X

SD

R2

31 25 2 15 23 2 2 —

10.9 16.0 1.8 20.6 12.4 3.2 3.8 —

0.44, 0.18, 0.10, 0.35, 0.13, 0.43, 0.12, —

NS NS NS NS NS NS NS

U

P

44.5 47.5 47.0 48.0 49.0 48.0 — —

0.677 0.850 0.797 0.879 0.939 0.864 — —

a MEAD/PAST ¼ meadows and pastures; SCR ¼ scrubland; HOW ¼ holm-oak woodland; CON ¼ coniferous plantation; BW ¼ broad-leaved woodland; EUC ¼ Eucalyptus plantation; OTH ¼ other habitat; LECOT ¼ length of ecotone index (in meters) in a sample of 800 ha (see text for details).

declines in population size during the last decades. These roosts  ¼ 260, SD ¼ ranged in size from 85 to 567 individuals (X 203.9); 6 were located in caves, 3 in buildings, and 1 in an underground canal. No significant differences were found for the percentage habitat composition between the areas delimited by a radius of 5 km and that of 10 km around the study colonies (Table 5). The most abundant habitats around the colonies were meadows and pastures, accounting on average for 30% of the area, followed by scrubland (25%) and broad-leaved woodland (24%). Correlation coefficients between colony size and percentage area of a given category did not reach significance in any habitat type except for the ecotone index (Table 5).

DISCUSSION Diet and prey selection.—In this study in the northern Iberian Peninsula, moths were the staple diet of R. euryale. Other studies have documented moths as important prey for this species, but they also indicated a much broader spectrum of prey (Grabovac et al. 1999; Koselj 2002; Koselj and Krystufek 1999). In all of those studies, however, diet was estimated using bat droppings found beneath roosting colonies, which might have been contaminated by the droppings of other species, given the propensity of R. euryale to form multispecies colonies (e.g., Aihartza 2001; Brosset and Caube´re 1959; Paz 1985; Russo et al. 2002). Thus, our study provides the most comprehensive and reliable assessment of the diet of R. euryale to date. The compositional analyses demonstrated that moths generally were the most preferred prey, although other prey species contributed seasonally to the diet. In the northern Iberian Peninsula and likely elsewhere, R. euryale is a moth specialist. Adults and juveniles had a similar diet, unlike findings in studies of other microchiropteran species (Adams 1997; Hamilton and Barclay 1998; Ransome 1996; Rolseth et al. 1994). All those studies concluded that the age-related differences in diet were a product of the novelty of echolocation and flight among juveniles, or were due to an active effort by adults to avoid competition with juveniles. The rather restricted diet of juvenile R. euryale, which consisted almost exclusively of moths, reinforces the view that Mediterranean horseshoe bats are moth specialists. In addition, in the cooler summer of 2002, Downloaded from https://academic.oup.com/jmammal/article-abstract/89/2/493/938130 by guest on 23 January 2018

when abundance of moths was significantly lower than in normal summers, the number of lactating females was dramatically lower. Arlettaz et al. (2001) demonstrated that the availability of key prey species directly influences the timing of parturition in Myotis myotis. Such a moth-specialized diet is consistent with the diets of the closely related Rhinolophus mehelyi (Sharifi and Hemmati 2001) and R. blasii (Findley and Black 1983; Whitaker and Black 1976), and also is consistent with the allotonic frequency hypothesis (Jones 1992; Jones and Waters 2000; Rydell et al. 1995). The dietary importance of lacewings, which also possess a specialized auditory system to avoid bats (Miller and Olesen 1979; Miller and Surlykke 2001), was previously documented by Koselj (2002) and corroborated by our findings. Habitat selection in relation to the distribution and abundance of moths.— Most foraging by Mediterranean horseshoe bats occurred in edge habitats, predominantly hedgerows but also woodland edge and isolated trees, whereas exotic tree plantations were the least preferred habitat. Interestingly, we found no differences in abundance of moths across habitats. Usher and Keiller (1998) found that distances , 2.5 km did not prevent moths from travelling between farm woodlands scattered in arable land, which is consistent with the characteristics of our study area: highly heterogeneous, small patch size of woodland and plantations, and having an important hedgerow network interspersed with meadows and pastures of varied composition and size, shaping a diverse and favorable landscape for Lepidoptera (Dover and Sparks 2000; Kitahara 2004; Kitazawa and Ohsawa 2002; Po¨yry et al. 2004, 2005; Pywell et al. 2004; Saarinen and Jantunen 2005). At the demographic level, the availability of edge habitats around breeding sites was the only variable correlated with colony size; the amount of broad-leaved woodland yielded no significant correlation. Indeed, meadows and pastures covered large areas around all of the breeding colonies analyzed. Despite the similarity in availability of moths across all habitat categories, exotic tree plantations were the least preferred habitats. Typically, plantations lack simultaneous successional stages and form a single compact crown, thereby offering an edge area per crown volume lower than that of any natural woodland. In a Mediterranean patchy landscape in southern Italy, R. euryale preferentially used broad-leaved woodland and olive

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groves, although the latter habitat was frequently surrounded by broad-leaved woodland and therefore by its edge (Russo et al. 2002). In southern Spain, half of the foraging time of radiotagged R. euryale was recorded in riparian woodland, even though this habitat covered just 0.9% of that study area (Russo et al. 2005). In fact, the linear structure of riparian woodland more closely resembles hedgerow than woodland as regards its proportion of edge habitat. Aihartza et al. (2003) reported that R. euryale in an Atlantic landscape also shows a different pattern of habitat use, although that observation was likely related to local altered habitat conditions and is considered not to be representative of the species (Goiti et al. 2003). The only radiotelemetry study published for R. mehelyi reported that this species preferred a habitat with a high proportion of edge habitat, the dehesa (Russo et al. 2005). The largest member of the genus in Europe, R. ferrumequinum, was found to forage extensively in edge habitats (Billington 2000, 2002, 2003a, 2003b, 2004; Bontadina et al. 1997; Jones and Morton 1992) and even over open spaces such as meadows and pastures (Duverge´ and Jones 1994; Robinson et al. 2000). The only exception to this pattern seems to be R. hipposideros (Bontadina et al. 2002; Schofield et al. 2002), for which woodland was found to be the main foraging habitat. However, these studies of foraging by R. hipposideros located bats mainly via triangulation, which would have prevented distinguishing between foraging within woodlands and in clearings or on the edge. Moreover, grazed pastures interspersed with woodland predominated in both study areas, with a high degree of interface between those habitats. Indeed, it was argued that the population decrease of R. hipposideros occurred in a period in which broad-leaved woodland increased all over Europe (Bontadina et al. 2002). To our knowledge, all publications describing the surroundings of any European colony of horseshoe bats report the existence of open habitats (meadows, pastures, or scrubland) interspersed with woodland (copses or larger stands) creating a heterogeneous landscape. Further, no colonies are reported to be in a completely forested area (see also Brosset et al. 1988; McAney and Fairley 1988; Motte and Libois 2002; Ohlendorf 1997). Accordingly, the origins of the Mediterranean horseshoe bat, and also those of R. mehelyi, R. blasii, and R. ferrumequinum, are surmised to be in Africa, and specifically in a semiarid environment (Guille´n et al. 2003) such as a savannah landscape. This African origin would have allowed a 1st intrusion of R. euryale into the not-so-different Mediterranean region (Guille´n et al. 2003). Subsequently, as human activity promoted clearance of woodlands, open habitats such as meadows and pastures became extended creating a savannahlike landscape that presumably aided in the expansion of R. euryale to more northern temperate zones and the colonization by the species of a new bioclimatic region. Implications for conservation and management.— To date, conservation of the Mediterranean horseshoe bat has focused on the preservation of broad-leaved woodlands (Aihartza et al. 2003; Russo et al. 2002, 2005). Based on our results, increased attention should be paid to the structure of habitats and thus to the preservation and enhancement of edge habitats, preferably Downloaded from https://academic.oup.com/jmammal/article-abstract/89/2/493/938130 by guest on 23 January 2018

formed by broad-leaved trees, meadows, and pastures, at least in the Euro-Siberian bioclimatic region. Although edge habitat has appeared to be important for R. euryale, broad-leaved woodland is also seasonally important for the species, especially in late summer. Further research also is required to identify any key species of moth that are prey for this bat. A recently developed method based on the analysis of fecal DNA (McCracken et al. 2005), has proven to be a useful tool to achieve this goal.

ACKNOWLEDGMENTS This research was funded by IKT S.A. and the University of the Basque Country (projects 1/UPV 0076.310-E-13994/2001, 1/UPV 00076.310-E-15341/2003, and 9/UPV 00076.310-15849/2004). UG was supported by a grant from the Programa de Formacion de Investigadores of the Department of Education, University and Research of the Basque Government and also by a contract with the University of the Basque Country. We thank J. T. Alcalde, J. P. Urcun, P. Arlot, and the Group Chiropte`res Aquitaine, who kindly provided information on the location and size of several breeding colonies. Thanks to B. MacWhirter for his help improving the English. For assistance in the field we thank I. Blanco, A. Casis, Z. Fernandez, A. Herrero, L. Latierro, and J. Sanchez.

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Submitted 15 February 2007. Accepted 21 September 2007. Associate Editor was Douglas A. Kelt.