Submitted to Oecologia, May 2005

Please treat confidential

Running head: Range use and dispersal distances in a fruit bat

Spatial use in the Neotropical short-tailed fruit bat, Carollia castanea (Phyllostomidae) and

its implications for seed dispersal

Wibke Thies1, Elisabeth K. V. Kalko2*,3 and Njikoha M. Ebigbo2

1
University of Tübingen, Animal Physiology, Auf der Morgenstelle 28, 72076 Tübingen,

Germany
2
University of Ulm, Experimental Ecology, Albert-Einstein Allee 11, 89069 Ulm, Germany
3
Smithsonian Tropical Research Institute, P. O. Box 2072, Balboa, Panama

* to whom correspondence and off-print requests should be sent

E-mail: Elisabeth.Kalko@biologie.uni-ulm.de

1
Abstract

Knowledge of foraging behaviour and movement patterns of frugivores is crucial to understand

recruitment and distribution patterns of zoochorous plants. We asked whether the foraging

behaviour of the chestnut-coloured fruit bat, Carollia castanea (Phyllostomidae) contributes to

seed dispersal limitation of pioneer plants, Piper sp. (Piperaceae), its main diet. For this, we

determined potential seed dispersal distances and assess the degree of seed dispersal contagion

by studying range size and range use of this bat in a neotropical lowland forest in Panama. Our

radio-tracking studies revealed small nightly foraging areas, mostly less than 10 ha, with core

areas of less than 2 ha. Individual C. castanea visited the same core areas consistently every

night. By combining movement data with gut retention time for Piper seeds we found that the

probability for seed deposition was highest 100 to 200 m away from the parent plant with a

maximum of 1.4 km for male C. castanea. Each bat used several (5-7) temporary night roosts per

night for processing food and resting. Individuals visited each temporary night roost on average

only twice per night and revisited only one or two of the night roosts in the following night.

Spatial point pattern analysis revealed a random distribution of night roosts in the foraging area.

Range use and distribution of night roosts are likely to lead to broad and scattered seed dispersal.

We conclude that C. castanea’s foraging behaviour does not limit dispersal of Piper on BCI but

increases chances for recruitment.

Key words: radio-tracking, seed dispersal, dispersal distances, range use, leaf-nosed bats, seed

shadow

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Introduction

Seed dispersal profoundly influences potential rates of recruitment and consequently spatial

distribution and genetic structure of plant populations (e.g., Howe and Smallwood 1982, Howe

and Miriti 2004, Hamrick and Loveless 1986, Hamrick et al 1993, Holbrook and Smith 2000,

Jordano and Godoy 2002, Matolweni et al 2000, Nathan and Muller-Landau 2000, Westcott and

Graham 2000, Godínez-Alvarez et al. 2002). Recent studies pay special attention to the question

whether and how recruitment limitation determines structure, diversity and dynamics of tropical

forests (Hurtt and Pacala 1995, Schupp & Fuentes 1995, Hubbell et al. 1999, Ehrlén & Eriksson

2000, Nathan & Muller-Landau 2000, Dalling et al. 2002). Recruitment limitation may arise due

to dissemination limitation (Schupp et al. 2002), i.e. the failure of seeds to arrive in potential

recruitment sites. This aspect is believed to be a major contributor to recruitment limitation but

has received little attention (Schupp et al. 2002) mainly due to our poor knowledge of the

foraging behaviour of the dispersers and their movement patterns that strongly influence the

spatial component of seed dispersal.

As about 90 % of the plant species in tropical forests are dispersed by animals (Howe and

Smallwood 1982, Gautier-Hion et al. 1985), particular emphasis needs to be placed on

understanding their foraging behaviour, the consequences it has on dispersal patterns and

whether this may lead to dissemination limitation (Nathan and Muller-Landau 2000, Schupp et

al. 2002). A thorough understanding of the contribution of frugivores to the spatial distribution of

their food plants and their overall effectiveness as dispersal agents as well as identifying which

plants may be recruitment limited is urgently needed as human-induced habitat degradation and

fragmentation continue to deeply affect maintenance and regeneration of tropical plant diversity

(Gorchov et al. 1993, Makana and Thomas 2004). Only this knowledge will allow the

3
development of meaningful conservation-oriented management plans to preserve biological

diversity and ecosystem functioning.

Disperser activity may influence three processes that in turn determine the degree of

dissemination limitation (Schupp et al. 2002): the number of seeds that are dispersed away from

the parent plant independent of seed production (quantitatively restricted seed dispersal), the

distance seeds are transported away from parent plants (distance-restricted seed dispersal) and the

degree of spatial clumping of seed deposition in the landscape (spatially contagious seed

dispersal).

To answer our question whether foraging behaviour of frugivores contributes to

dissemination limitation and thus potentially to the maintenance of species diversity of Piper we

studied the nightly movement and ranging patterns of the chestnut-coloured fruit-bat, Carollia

castanea (Phyllostomidae) and investigated two of the three processes proposed by Schupp et al.

(2002), distance-restricted seed dispersal and spatially contagious seed dispersal. Studies of

interactions between plants and bats are especially important not only because of the high

mobility of bats, but also because in the Neotropics, fruits of at least 180 plant genera with 500 to

600 species are eaten and potentially dispersed by bats of the species-rich, endemic family of

New World leaf-nosed bats (Phyllostomidae) (Dobat, pers. com.). Carollia castanea shows a

strong preference for fruits of the genus Piper (Piperaceae) (Thies and Kalko 2004). As pioneer

plants, Piper species are crucial for regeneration processes as they colonise forest gaps, forest

edges, and deforested areas. Typically, C. castanea picks a ripe Piper fruit stand in flight and

carries it to a night roost where the fruit pulp is eaten together with the tiny seeds. Carollia

castanea excretes the seeds intact with the faeces after about 30 minutes (Fleming 1988, pers.

4
obs.) either while still hanging in a night roost or in flight (Fleming 1981). During gut passage, C.

castanea frequently switches night roosts and thus transports the small seeds to other places.

The few existing observations on the foraging behaviour of New World frugivorous bats

suggest that seed dispersal by bats is rather patchy but may occur over quite long distances

(Janzen et al. 1976, Morrison 1978, Fleming 1988, Charles-Dominique 1991, Fleming and Sosa

1994, Gastal and Bizerril 1999, Lopez and Vaughan 2004). We established a standardized

recording and analysis protocol for radio-tracking and studied C. castanea for a period of over

three years in a semi-deciduous, tropical lowland forest in Panama. To account for possible

differences in foraging behaviour between male and female bats we tracked both, non-

reproductive males and females and analysed tracking results separately. We determined the

potential seed dispersal distances by combining radio-tracking results on home range use with

information on gut retention times of Piper seeds. We applied spatial point pattern analysis to

characterize the spatial distribution of night roosts within foraging areas of individual C.

castanea. By combining data on movement pattern as well as distribution and use of night roosts

we address the potential for C. castanea to contribute to spatially contagious or scattered seed

dispersal.

Methods

The study was conducted from May 1994 to August 1997 on Barro Colorado Island (BCI), a field

station of the Smithsonian Tropical Research Institute, Panama (9°09'N, 79°51'W). The 1,560 ha

island is covered with semi-deciduous, moist tropical lowland forest composed of young (80-100

years) to older (400-600 years) stands. Rainfall is seasonal with a dry season from mid December

to April and a wet season starting in May where most (90 %) of the annual rain (2630 mm) falls.

5
Annual temperature averages 27°C, with a diurnal variation of 9°C. For more details see Leigh

(1999).

Data collection

Bats were caught with mist nets set along trails within 200 m of the laboratory clearing. Age was

determined by closure of epiphysis, reproductive condition was assessed following Handley et al.

(1991). Except one late lactating female, only non-reproductive adults were tagged that weighed

12 g or more (12.6 ± 1.2 g; n = 17). We used two-stage radio-transmitters (BD-2A, Holohil

Systems, Ltd., Canada) and released the bats at the capture site. The transmitters (0.95-1.12 g)

were fixed on the bats' back with surgical glue (SkinbondTM). They corresponded to 6-8 % of the

bat's body mass, which is slightly above the 5 % suggested by Aldridge and Brigham (1988) and

below the 10 % reported by Fleming (1988) where transmitter weight is assumed not to influence

the bat’s behaviour. The bats carried the transmitters between 4 and 25 days (11.8 ± 5.1 days; n =

17 individuals) before they fell off or were scratched off. Most of the transmitters were equipped

with a mercury switch that changed pulse frequency from a slow pulse rate when a bat was

hanging to a faster rate when it was flying.

We used YAESU FT-290 R/II receivers (modified by Wagener Telemetrieanlagen,

Cologne, Germany), hand-held 5 element Yagi antennas (Wildlife Materials, Carbondale, USA)

with a custom-made amplifier (Wagener Telemetrieanlagen, Cologne, Germany) and Walkie-

talkies (YAESU FT-26) to triangulate the bats’ position every two to three minutes. We excluded

data from the first night since the bats may have been irritated from tagging. To avoid over-

representation of tracking points from resting bats, we triangulated those locations only once for

each resting phase. Since tagged bats returned to the same areas each night, we limited

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triangulation after an initial phase of all-night tracking (6 pm to 7 am) to the first half of the night

(6 pm to 00 am) when the bats were most active. One person continued to follow the tagged

individuals during the second half of night (00 am to 6 am) to document the bats’ activity pattern.

Range of transmitters in the forest was mostly limited to 200-300 m (max. 400 m) because

of high humidity, density of vegetation, and hilly topography. The triangulation error

encompassed 3° - 9° at distances of about 100 m. This corresponds to a precision of localization

of 5 to 15 m.

Data analysis

We used three categories, home range, foraging area, and core area to describe range size and

use. Following Hansteen et al. (1997), home range represents the area that is traversed by a bat

during the time it carries a functioning transmitter (4 to 21 days). Size of home range was

calculated with the non-parametric Minimum Convex Polygon method (MCP). Foraging area

represents the locality where a bat searches for and eats food. Within foraging areas, we

classified areas of concentrated use with most of our fixes as core areas sensu Harris et al. (1990).

Size of foraging area and core areas were determined with the probabilistic Kernel method

(Worton 1995, Seaman and Powell 1996). As the Kernel method requires temporally independent

observations (Swihart and Slade 1985), we only took those data points where the time interval

between bearings was long enough for a bat to potentially cross its range (Kenward 1987). This

procedure leads to time intervals of 4 to 6 minutes between fixes and estimated travelling

distances of 1440 to 2160 m.

We used a custom-made map (REV5, drafted 1997 by Stallard, Kinner, Clark, and Thies)

based on Universal Transverse Mercator (UTM) coordinates and analysed the tracking data with

7
the software program TRACKERTM (version 1.1, Camponotus, Sweden). For analyses, we

discarded all fixes with an arbitrarily chosen error ellipse of > 200 m in diameter. We created

isopleths enclosing 95 % of the fixes of a tracked bat (95 % isopleths) to identify location of

home range as well as foraging and core areas. We created successive kernel isopleths of 20 to

95% (Wray et al. 1992) to assess core areas within foraging areas. The percentage inclusion that

generated the isopleth with most cores was chosen for analyses. If no additional core area was

formed, we took the area that was enclosed by the 75 % isopleth (mean percentage inclusion).

We measured linear distances between day roost and furthest point of a bat's home range,

between day roost and centre of first foraging area each night, and between centres of foraging

and core areas when more than one was used during tracking. To assess the distance of potential

seed dispersal by C. castanea, we calculated first the distance between the location where the bat

potentially picked up a fruit and the subsequently visited night-roost. Based on the time it takes

C. castanea to search for and approach a ripe fruit within a feeding patch (Thies et al. 1998), we

assumed that the bearing taken one to two minutes after a bat had left its night-roost corresponds

to the location of a fruit bearing plant. We then estimated the probability of seed dispersal

distances from the movement patterns of C. castanea and the gut passage time of swallowed

seeds to generate a seed-dispersal distance frequency distribution. Considering that seeds are

excreted after an average time of 30 min (Fleming 1988), the probability that seeds were

deposited at a certain distance away from the original locality where the fruit was picked up can

be derived from the distances moved by C. castanea within 30 min. When the bats stayed more

than 30 min within a core area, we considered the radius of the respective core area as the

potential range of seed dispersal. When the bats left the core area within 30 min, we measured the

distance between the last bearing taken within the core area and the first bearing taken outside the

8
core area. We did not include distances when a bat travelled between a core area and the day-

roost since seeds dropped in the day-roost (mostly overhanging banks and tree cavities) most

probably cannot germinate.

To assess spatial patterns of potential seed dispersal by C. castanea we determined the

distribution of night roosts within the foraging area and the frequency bats visited each night

roost in subsequent nights. The locations of the night roosts were organised as a list of

coordinates based on a 1m2 grid and loaded as a shape file within a rectangular area into the

spatial point pattern analysis software Programita © (Wiegand and Moloney 2004). We applied

the L-function, a transformation of Ripley’s K function (Ripley 1981), to assess clumping or

evenness in the distribution of the night roosts as recommended in Wiegand and Moloney (2004).

Statistical significance was resolved by n=99 simulations of the null model to generate 99%

confidence envelopes. We tested the pattern of night roosts according to a null hypothesis of

complete spatial randomness, which was modified to account for first order heterogeneity of the

point patterns according to a heterogeneous Poisson null model (see Wiegand and Moloney

(2004) for details). We used the pattern of night roosts itself as basis for estimating the non-

constant first-order intensity using a circular moving window estimator (Wiegand and Moloney

2004) with a bandwidth of R=15 m. Our choice of bandwidth was based on the estimated

resolution of the tracking data which was around 15 m. This way, we excluded the effects of

“virtual aggregation or repulsion”, which has been shown to lead to erroneous interpretation of

the L-function (Wiegand and Moloney 2004).

Data base

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We tagged 13 individuals between May 1994 and August 1997. Seven animals (five females, two

males) were tracked during rainy season and six bats (one female, five males) during dry season

(one female and five males). Our data include 111 nights with 735.5 hours of tracking and 656.6

hours of contact (89.4 %). We took a total of 1,847 bearings and omitted 18 % because of large

error ellipses. Calculation of area asymptotes of home ranges (area size against number of fixes)

verified that enough tracking points had been sampled except for one male that we excluded from

analysis of nightly range use. Size of home range did not increase after about half of the fixes

which corresponded to about four successive tracking nights. All statistical tests were performed

using SYSTAT with p < 0.05 as level of significance.

Results

Potential patterns of seed dispersal in space

In order to achieve a better understanding of seed dispersal patterns in space, we first studied the

size and use of home ranges. We then documented number and visitation rates of night roosts of

individual C. castanea and determined the spatial pattern of night-roost distribution within

foraging areas.

Home range size of C. castanea varied widely and ranged between 5.5 ha to almost 100

ha (Tab. 1). Home ranges of males were significantly larger than those of females (Mann-

Whitney U test; U = 4.0000, p = 0.0446). Excluding the distance to the roost, this trend was even

more pronounced (Mann-Whitney U test; U = 5.0000, p = 0.0374). Foraging areas of female and

male C. castanea were located in areas with streams, often with steep banks where Piper plants

occurred in large numbers. We found distinct gender-specific differences in the number of

foraging areas. Female C. castanea mostly used only one foraging area of 2 to 8 ha (Fig. 1a, Tab.

10
1). In contrast, most male C. castanea had more than one foraging area (Fig. 1b) that covered 8 to

43 ha (Tab. 1) with a trend towards larger-sized foraging areas than in females.

All tracked bats used the same foraging areas night after night with little variations in this

behaviour in two males. One male explored a different area than its regular foraging area in one

night, the other gradually switched from one foraging area to another during the tracking session.

Within foraging areas, most of the bats had several core areas. All of them were located

along creeks where Piper plants occurred in high abundance. Although core areas included only

about 25 % of the total size of foraging areas (Tab. 1), they encompassed 70 to 90 % of all fixes.

While females had only one to two core areas covering between 0.5 and 2.6 ha males visited

between one and four core areas ranging from 1.6 to 12 ha (Tab. 1).

Both female and male C. castanea used several night roosts each night. Because bats

spent most of the time in the core areas, night roosts were mainly located in core areas. Females

visited about 5, males about 7 night roosts in the first half of the night (Tab. 1). There was no

significant difference in the mean number of night roosts between females and males (Mann-

Whitney U test: U = 14.5, p = 0.5745). Each night roost was visited roughly twice during a given

night (Tab. 1), with no significant difference in the mean nightly visitation rate between females

and males (Mann-Whitney U test: U =19.5, p = 0.8095). Only about one to two of the night

roosts used in one night were revisited during the following night (Tab. 1). During the entire

tracking period, females and males visited about two thirds of their night roosts only once (Tab.

1).

Spatial point pattern analysis revealed that distribution of the individual bats’ night roosts

was consistently random over all scales . No specific distances between points showed any

11
particular deviation from the null model (Fig. 2). This was consistent for both male and female

individuals despite differences in range size and use.

Potential distances of seed dispersal

The probability of seed dispersal by female C. castanea was highest (over 90 %) within a range

of 100 and 200 m from the original food source, with a mean of 106 ± 26 m (n = 6 individuals)

(Fig. 3). Fruits were initially carried 60.5 ± 39.7 m away from the fruiting plant (n = 85, range 15

to 186 m). The probability of seed deposition beyond 250 m was very low (about 3 %) (Fig. 3).

In males, fruits were initially carried 67.8 ± 58.8 m away from the fruiting plant (n = 103, range

15 to 374 m). The frequency distribution of potential dispersal distances in males was slightly

skewed with a mean dispersal distance of 280 ± 165 m (n = 6 individuals). The median, however,

was at 207 m. As in females, the probability of seed deposition in males was also highest (about

50 %) within a range of 100 to 200 m (Fig. 3). However, about 20 % of the seeds were

potentially transported further than 350 m, up to a maximum of 1400 m (Fig. 3). Overall, male C.

castanea may disperse seeds over longer distances than females because they visited more than

one foraging area per night. In females, the probability of long-range dispersal was much lower

because females used only one foraging area per night.

Discussion

Recent studies on seedling recruitment have shown, that limitations to recruiting new individuals

can increase species richness in tropical forest communities (e.g. Dalling et al. 2002, Hurtt and

Pacala 1995, Nathan and Muller-Landau 2000, Schupp et al. 2002). Of the three mechanisms that

influence recruitment limitation, dissemination limitation, the failure to disperse seeds to

12
potential recruitment sites, is especially relevant to animal-dispersed plants, because the foraging

behaviour of dispersers determines the degree of dissemination limitation and thus the future of a

species within a forest community. In several pioneer plant species whose fruits are dispersed by

birds, primates, rodents or wind, strong limitations to seed dispersal were found, which in turn

influence seedling distribution patterns and species diversity (Dalling et. al 2002). Our results on

the foraging behaviour of C. castanea indicate that this bat contributes only little to

dissemination limitation of Piper species on BCI in Panama: (i) long distance seed dispersal of

several hundred meters is not a rare event, therefore seed dispersal is unlikely to be distance-

restricted; (ii) the use of night roosts where seed deposition is most likely to occur is random,

thus reducing the degree of spatial contagion of seed fall. We conclude that the foraging

behaviour of C. castanea increases the chance of Piper seeds reaching suitable recruitment sites

and thus may not contribute to maintenance of high species diversity of Piper through the

mechanism of dissemination limitation.

Seed dispersal distances

Many seeds are dispersed only short distances with highest seed concentrations under the parent

plant (Janzen 1970, Pratt and Stiles 1983, Thomas 1988, Wheelwright 1991, Green 1993, Laman

1996, Wenny 2000, Westcott and Graham 2000). Short dispersal distances not only reduce the

chance of reaching suitable sites for seedling establishment distant from the parent plant (Schupp

et al. 2002) but also reduce the chance of seeds escaping detrimental effects of pathogens,

herbivores and conspecifics near the parent plant (Janzen 1970).

Determining seed dispersal distances in bats is challenging because movement of these

nocturnal animals is difficult to observe. Most observations on flight distances of phyllostomid

13
bats are anecdotal implicating that seed dispersal might occur over quite long distances (Heithaus

and Fleming 1978, Morrison 1978, Morrison 1980). Higgins et al. (2003) recently suggested a

mechanistic model to assess potential dispersal distances by combining data of animal movement

patterns with seed retention times and predicted exceptionally large dispersal distances for a

number of animals. This is supported by several studies on birds and monkeys that also combined

movement with retention data to estimate dispersal distances and found that the estimated

distances were larger than those found by searching for marked seeds or by small-scale

observations of animal movements in the vicinity of a fruiting tree (Sun et al. 1997, Yumoto et al.

1999, Holbrook and Smith 2000, Murray 1988, Westcott and Graham 2000). Several years

earlier, Fleming (1988) had used a similar approach including radio-tracking data to estimate

potential seed dispersal distances for a close relative of C. castanea, the short-tailed fruit bat

Carollia perspicillata. He calculated average dispersal distances of about 100 m with less than 10

% of the seeds transported more than 1 km. In our study, we combined results on home range use

of C. castanea with information on Piper seed retention times to generate a seed-dispersal

distance frequency distribution. We found that the probability for seed transportation by C.

castanea was highest within a range of 100 and 200 m from the food source. These results

support Fleming’s findings and indicate that long distance seed dispersal of several hundred

meters by C. castanea is not a rare event. From this finding we conclude that seed dispersal by C.

castanea is not distance restricted. Thus, by dispersing seeds far from parent plants, C. castanea

probably increases the number of potential colonisation sites.

We found clear differences in the potential seed dispersal distances between the two

genders of C. castanea, with larger distances in males than in females. Moreover, we found that

only males had the probability of very long-distance dispersal up to 1.4 km. This discrepancy was

14
mainly the result of differential range use in males and females. The home range, and therefore

also the nightly area used by females, was smaller than that used by males. Within their home

ranges, females visited fewer foraging areas and core areas than males. The findings are

independent of reproductive status of the tracked individuals because only non-reproductive

males and females were studied. We conclude, although seed dispersal by C. castanea occurs

over long distances, the contribution of males and females to seed dispersal and thus their

influence on recruitment may differ.

Spatial pattern of seed dispersal

If animals deposit seeds patchily in the landscape some sites receive seeds, others do not, thus

reducing the plants’ chance for recruitment by further reducing the number of potential

germination sites independent of distance from the parent plant. This spatially contagious seed

dispersal is largely driven by animal behaviour (Schupp et al. 2002). Spatially contagious seed

dispersal can occur at small scales, when clumps of seeds are deposited in sites preferred by

dispersers, e.g. beneath perches, night roosts, or along travel routes, etc. (e.g. Loiselle 1990,

Laman 1996, Voysey et al. 1999, Jordano and Godoy 2002), up to large scales when non-random

foraging and uneven use of home range lead to uneven distribution of dispersed seeds (Thomas

1988, Thomas 1991).

Studies on fruit-eating bats suggest spatially contagious seed shadows because they are

often observed to excrete seeds in clumps under night roosts that, in addition, are frequently re-

visited during the night (Janzen et al. 1976, Morrison 1978, Fleming 1981, Fleming 1988,

Charles-Dominique 1991, Fleming and Sosa 1994, Gastal and Bizerril 1999, Lopez and Vaughan

2004). However, these results were based on observations of only few night roosts in the whole

15
foraging area of a bat. Radio-tracking allowed us to take into account the entire foraging area of

C. castanea and thus estimate the use of all potential night roosts. C. castanea visited on average

5 to 7 night roosts in the first half of the night. The distance between a fruiting plant and the night

roost a ripe fruit was initially carried to, was about 60 to 70 m. Each night roost was visited only

about twice per night. Although C. castanea used the same foraging areas throughout the

tracking period, each individual bat visited different night roosts in consecutive nights. Overall,

when comparing the whole tracking period, almost two thirds of all night roosts were visited only

once during the entire time. These results, that already suggest a rather homogenous seed rain

with almost no opportunities for clumped seed dispersal except within the splash of faeces, are

supported by our data on spatial point pattern analysis: night roosts of both males and females are

scattered randomly over foraging areas and are likely to lead to a scattered and predominantly

random seed shadow. Our results therefore contradict former studies on night roost use by bats

but concur with recent studies on flying foxes using also spatial point pattern analysis (Ebigbo et

al., submitted). Here, the authors found that shuttle-foraging behaviour of flying foxes on large

Cola cordifolia seeds (Sterculiaceae) do not give rise to spatially contagious seed dispersal

within forest islands.

An important point when dealing with spatial patterns concerns the scale at which

biological phenomena occur. Our inferences and conclusions on the spatial arrangement of night

roosts are relevant within foraging areas over which bats disperse seeds. Further steps will need

to tease apart processes and relevant spatial scales. Information on how and at what scales Piper

plants are spatially structured as well as factors that determine such spatial structures (e.g. soil,

microclimate, seed dispersal), are important factors to consider when analysing and interpreting

spatial data. Such information will further underline the relevance of C. castanea’s foraging

16
behaviour for Piper populations. Our approach is an important albeit first step in understanding

the implications of bats’ high mobility on plant populations that allows us, given the available

information on foraging behaviour and foraging area, to consider spatially contagious seed

dispersal as highly unlikely. We conclude that the high turn-over rate in the use of night roosts as

well as the random distribution of night roosts within foraging areas of C. castanea do not favour

spatially contagious dispersal of Piper seeds. In summary, foraging behaviour of C. castanea

does not contribute to dissemination limitation sensu Schupp et al. (2002) but probably increases

the chances of Piper seeds to reach suitable sites for recruitment.

Implications of seed dispersal on the genetic structure of Piper plant populations

Seed dispersal is the only process that ensures the transfer of maternal genes between individuals

and /or populations (Hamilton 1999) and thus influences genetic structure within and among

populations. In a model on the genetic structure within populations of animal-dispersed plants,

Hamrick and Loveless (1986) suggested that Piper should be highly genetically structured within

populations (i.e. forming subpopulations). They assumed that bats transport fruits to a night roost

close to a fruiting plant and deposit clumps of seeds under this night roost. Consequently,

because the seeds originate mainly from the fruiting plant closest to the night-roost the seedlings

should be genetically related to each other and the Piper plants nearby. This model implies low

seed movement and low gene diversity within populations as well as high genetic differentiation

among populations.

Whereas studies on the allozyme variation in three species of Piper in Costa Rica

(Heywood and Fleming 1986) in fact showed very low genetic diversity within species, they

revealed also low genetic differentiation among populations of a species. While the very low

17
genetic diversity of Piper species can be caused by a variety of factors other than low seed

movement, such as bottleneck, founder effects (Heywood and Fleming 1986) or vegetative

propagation, low genetic differentiation among populations of a species can only be explained by

long-distance dispersal and a relatively homogenous deposition of seeds (Hamrick and Loveless

1986). Considering our results on the rather wide and scattered seed shadows created by C.

castanea we would expect higher gene flow among the primarily bat-dispersed Piper plant

populations on BCI than predicted by the model of Hamrick and Loveless (1986).

Acknowledgements

We thank the Smithsonian Tropical Research Institute (STRI, Panama) for excellent logistic

support and good working conditions and the many people who helped to accomplish this work:

Bob Stallard and Charles Handley for patient reading and corrections on the manuscript, Egbert

Leigh for valuable discussions, Peter Pilz for statistical advice, Maria-Elena Cedeño, Marina

Ballardo, Melva Olmos, José-Luis Justavino, and Sonia Tejada (Panama) for their untiring help

in radio-tracking, Thorsten Wiegand for providing the statistical software programm Programita

© and Ingrid Kaipf for help with the drawings. This study was supported by a PhD stipend of the

Deutscher Akademischer Austauschdienst (DAAD) to Thies and by grants of the Deutsche

Forschungsgemeinschaft (DFG), Schwerpunktprogramm „Mechanismen der Aufrechterhaltung

tropischer Diversität“, to Schnitzler and Kalko.

18
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Tables

Tab. 1

Home range use of 6 female and 6 male C. castanea on Barro Colorado Island, Panama. Values

are given as means (± 1 standard deviation), minimum and maximum. Numbers in parenthesis

indicate number of nights (minimum distances / night) and number of night-roosts analysed

(night-roosts). Abbreviations: MCP = Minimum Convex Polygon; FA = foraging area; CA = core

area; # = number, ha = hectare, m = meters.

Females Males
mean min max mean min max

Home range
Home range (MCP; roost 13.8 ± 12.1 5.5 34.9 41.3 ± 33.0 6.8 99.1
included) [ha]

Home range (MCP; roost not 9.5 ± 9.6 2.4 28.5 35.9 ± 29.2 6.8 84.3
included) [ha]

FA (95% Kernel) [ha] 6.9 ± 2.3 2.3 8.6 22.9 ± 16.3 8.1 43.3

FAs [#] 1.0 1 1 1.8 1 3

Total CA [ha] 1.5 ± 0.9 0.5 2.6 6.3 ± 5.0 1.1 12.0

Area included by CA [%] 24.8 ± 15.8 8.2 48.4 22.5 ± 8.8 10.8 34.9

CAs [#] 1.3 1 2 2.3 1 4

Night-roosts (06 pm to 00 am)

Night-roosts / night [#] 5.4 ± 2.4 (201) 1 10 6.9 ± 3.1 (185) 2 13

Visitation frequency / night roost 1.5 ± 0.6 1 3.7 1.5 ± 0.4 1 2.2

Night-roosts revisited in 1.4 ± 0.9 (26) 0 3 1.7 ± 1.1 (15) 0 3

subsequent night [#]

Night-roosts visited once during 74.1 ± 6.9 60.9 80.0 77.6 ± 10.9 60.9 93.8
tracking period [%] (106) (105)

26
Figures

Fig. 1

Foraging areas of female (a) and male (b) C. castanea on BCI. Individuals are indicated with

different line patterns.

Fig. 2

Results of spatial point pattern analysis (Ripley’s K statistic) for distribution patterns of night

roosts of a male Carollia castanea (#4). Significant spatial aggregation or spatial evenness at

each spatial scale is revealed when test statistic results (open circles) are above or below 99%

confidence limits (continuous lines without circles), which bounds the null model implying a

random distribution pattern.

Fig. 3

Potential dispersal distances of female and male C. castanea given as the probability (% of all

distances calculated) that seeds are deposited away from the site where a fruit was originally

picked up.

27
 a)

0 500m

b)

0 500 m

Figure 1a, b
Thies, Kalko, Ebigbo

28
 85 clumping
75 randomness
65
55
L (r)

45
35
25
15
5 evenness
-5
0
20
40
60
80
100
120
140
160
180
200
220
scale r [m]

Figure 2

Thies, Kalko, Ebigbo

29
 0.50

0.45

0.40
probability of deposition

0.35 females
males
0.30

0.25

0.20

0.15

0.10

0.05

0.00
100 200 300 400 500 600 700 800 900 1000 > 1400

distance from origin [m]

Figure 3
Thies, Kalko, Ebigbo

30