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Author's personal copy
Basic and Applied Ecology 12 (2011) 505–515
Seed dispersal in red deer (Cervus elaphus L.) dung and its potential
importance for vegetation dynamics in subalpine grasslands
Majid Iravania,∗ , Martin Schützb , Peter J. Edwardsc , Anita C. Rischb , Christoph Scheideggerb ,
Helene H. Wagnerd
a
Department of Natural Resources, Isfahan University of Technology, 84156 Isfahan, Iran
Swiss Federal Institute for Forest, Snow and Landscape Research, Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland
c
Swiss Federal Institute of Technology ETH, Plant Ecology, Universitätsstrasse 16, CH-8092 Zürich, Switzerland
d
Department of Ecology and Evolutionary Biology, University of Toronto, 3359 Mississauga Road, Mississauga, ON, L5L 1C6 Canada
b
Received 13 June 2010; accepted 9 July 2011
Abstract
Free-ranging large herbivores can influence vegetation dynamics through seed dispersal within and among habitats. We
investigated the content of germinable seeds in the dung (endozoochory) of red deer (Cervus elaphus L.), the most ubiquitous
wild ungulate throughout the European Alps, and compared the results with the species composition of the vegetation type
in which the dung was dropped. The study was conducted in the subalpine zone of the Swiss National Park and included the
three most important vegetation types for red deer: (i) intensively grazed short-grass vegetation, (ii) less intensively grazed
tall-grass vegetation, and (iii) adjacent conifer forest understory vegetation. Seeds of 47 species, mostly from small-seeded
herbaceous species, were recorded in dung samples with three species accounting for 65% of germinated seeds. Our results
confirmed the hypotheses that (H1) small-seeded species were more likely to occur in red deer dung than larger-seeded species,
though seed size was unrelated to seed density, (H2) red deer dung contained mostly seeds from short-grass vegetation, with
seed species composition in dung collected from any vegetation type being most similar to species composition of relevés from
short-grass vegetation, and (H3) seeds were less likely to be dispersed between vegetation types than within vegetation types,
with dung dropped in short-grass vegetation having a different species composition and containing over twice as many seeds as
dung dropped in the other two vegetation types. These results collectively support the hypothesis that red deer endozoochory
contributes to maintaining short-grass vegetation, the favoured grazing sites of hinds in the Swiss National Park, by increasing
propagule pressure of seeds from herbaceous forage species adapted to endozoochory relative to other species and especially
those from later stages of secondary succession.
Zusammenfassung
Wilde Huftiere können die Vegetationsdynamik beeinflussen, indem sie Samen innerhalb und zwischen Habitaten verbreiten.
Wir untersuchten den Gehalt an keimfähigen Samen (Endozoochorie) im Kot von Rothirschen (Cervus elaphus L.), der in
den Europäischen Alpen am weitesten verbreiteten Huftierart und verglichen die Resultate mit der Artenzusammensetzung
des Vegetationstyps, in welcher der Kot gesammelt wurde. Die Studie wurde in der subalpinen Zone des Schweizerischen
Nationalparks durchgeführt und umfasste die drei für Rothirsche wichtigsten Vegetationstypen: (i) intensiv beweidete
∗ Corresponding author. Tel.: +98 311 391 35 82; fax: +98 311 391 28 40.
E-mail addresses: [email protected], [email protected] (M. Iravani).
1439-1791/$ – see front matter © 2011 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.
doi:10.1016/j.baae.2011.07.004
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M. Iravani et al. / Basic and Applied Ecology 12 (2011) 505–515
Kurzgrasrasen, (ii) weniger intensiv beweidete Langgrasrasen, und (iii) den Unterwuchs angrenzender Nadelwälder. In den
Kotproben wurden Samen von 47 Pflanzenarten gefunden, die meisten von kleinsamigen Krautarten, wobei 65% der gekeimten
Samen von nur drei Arten stammten. Die Resultate bestätigten die folgenden Hypothesen: (H1) Kleinsamige Arten kamen
mit grösserer Wahrscheinlichkeit in Kotproben vor, obschon die Samendichte im Kot nicht von der Samengrösse abhing. (H2)
Rothirschkot enthielt mehrheitlich Samen von Kurzgrasrasenarten, wobei die Artenzusammensetzung der Kotproben von allen
drei Vegetationstypen grösste Ähnlichkeit mit Vegetationsaufnahmen aus Kurzgrasrasen aufwies. (H3) Samen wurden häufiger
innerhalb desselben Vegetationstyps transportiert als zwischen verschiedenen Vegetationstypen, wobei Kot, der in Kurzgrasrasen gesammelt wurde, eine andere Artenzusammensetzung und eine mehr als doppelt so hohe Samendichte aufwies wie
Kot aus Langgrasrasen oder Nadelwäldern. Zusammengenommen unterstützen unsere Resultate die Hypothese, dass endozoochore Samenausbreitung durch den Rothirsch zum Erhalt von Kurzgrasrasen, dem bevorzugten Habitattyp der Hirschkühe im
Schweizerischen Nationalpark, beiträgt, indem die relative Häufigkeit keimfähiger Samen von bevorzugten und an Endozoochorie angepassten Pflanzenarten gegenüber anderen Arten, insbesondere Vertretern späterer Stadien der sekundären Sukzession,
erhöht wird.
© 2011 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.
Keywords: Endozoochory; European Alps; Free-ranging herbivores; Grazed ecosystems; Selective habitat use
Introduction
Large herbivores are generally recognized as one of the
main driving forces behind vegetation dynamics of grazed
ecosystems (e.g. Gill & Beardall 2001; Erschbamer, Virtanen
& Nagy 2003; Mouissie, Apol, van Diggelen & Heil 2008).
It has been suggested that the activities of free-ranging ungulates lead to maintaining the vegetation of their favoured
grazing sites (McNaughton 1984; Vera 2000). However,
empirical evidence for this hypothesis is largely lacking.
Comprehensive data on seed dispersal by wild ungulates
in unmanaged ecosystems may provide evidence for such
effects of large herbivores.
Wild ungulates are potentially important long-distance
dispersers of seeds (Janzen 1984). Seeds of many species
can be dispersed in dung (endozoochory), especially those
from herbaceous species with small, hard seeds (Yamashiro
& Yamashiro 2006; Rosas, Engle, Shaw & Palmer 2008;
Pakeman & Small 2009) that lack obvious morphological adaptation to a specific dispersal vector (Gill &
Beardall 2001; Eycott, Watkinson, Hemami & Dolman
2007). Endozoochory and epizoochory have been identified
as evolutionary adaptations that facilitate both the dispersal
of plant species and the reseeding of areas under intense herbivory (Howe & Smallwood 1982). Preferred forage species
often locate their reproductive organs and numerous seeds
among or above green leaves (Janzen 1984; Hülber, Ertl,
Gottfried, Reiter & Grabherr 2005), increasing the chance
of seeds being eaten inadvertently with other plant parts
(Shiponeni & Milton 2006), and their small seeds are more
likely to pass the herbivore’s digestive tract undamaged (Gill
& Beardall 2001; Pakeman & Small 2009; Kuiters & Huiskes
2010). Several studies have investigated seed dispersal in
wild ungulate dung (e.g. Welch 1985; Heinken, Hanspach,
Raudnitschka & Schaumann 2002; Myers, Vellend, Gardescu
& Marks 2004; Oheimb, Schmidt, Kriebitzsch & Ellenberg
2005; Brodie, Helmy, Brockelman & Maron 2009), but these
have rarely considered the spatial variation in the return of
seeds across a range of different vegetation types (but see
Malo, Jiménez & Suárez 2000; Yamashiro & Yamashiro
2006). Most wild ungulates range widely and move regularly
between different habitats for foraging (Georgii & Schröder
1983; Gill & Beardall 2001), and the seed content of dung
therefore reflects their foraging behaviour and the composition of the plant communities where they feed (Malo & Suarez
1995; Hülber et al. 2005). Since seeds normally remain in the
digestive tract for several hours (Oheimb et al. 2005; Bruun,
Lundgren & Philipp 2008), they may be dispersed among
other habitats within the animal’s range (Heinken et al. 2002;
Myers et al. 2004; Cosyns, Claerbout, Lamoot & Hoffmann
2005; Rosas et al. 2008).
Wild ungulates are selective in their use of habitat (Meyer
& Filli 2006; Mouissie et al. 2008), and in some sexually dimorphic ungulate species, patterns of habitat selection
also differ between the sexes (Clutton-Brock, Guinness &
Albon 1982; Georgii & Schröder 1983; Conradt, CluttonBrock & Thomson 1999). In red deer (Cervus elaphus L.),
the most ubiquitous wild ungulate throughout the European
Alps (Erschbamer et al. 2003), hinds prefer highly digestible,
nutrient-rich plant material because they have high energy
requirements for pregnancy and lactation (Clutton-Brock
et al. 1982; Conradt et al. 1999), whereas stags, with their
higher forage requirement due to larger body size, prefer
to graze vegetation with high forage biomass (Georgii &
Schröder 1983). The potential importance of habitat selection
for seed dispersal via wild ungulate dung (endozoochorous
seed dispersal) has rarely been considered (Malo et al. 2000;
Shiponeni & Milton 2006; Rosas et al. 2008). Red deer have
been shown to disperse seeds of several species in their
dung (e.g. Welch 1985; Malo & Suarez 1995; Malo et al.
2000; Oheimb et al. 2005; Eycott et al. 2007), potentially
affecting the dynamics and structure of the vegetation to
a considerable degree. For instance, red deer might maintain vegetation in their favoured grazing sites by promoting
some species, e.g. by dispersing their seeds to available germination sites, while constraining others, e.g. by destroying
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M. Iravani et al. / Basic and Applied Ecology 12 (2011) 505–515
their seeds through their digestive tracts (Janzen 1984; Welch
1985; Malo & Suarez 1995; Bakker & Olff 2003; Shiponeni
& Milton 2006; Pakeman & Small 2009; Kuiters & Huiskes
2010).
Following the foundation of the Swiss National Park
(SNP) in 1914, the population of red deer increased rapidly
to nearly 2000 (Haller 2002). This has resulted in a relatively high grazing pressure by red deer on the grassland
ecosystems in the Park (Schütz, Risch, Leuzinger, Krüsi, &
Achermann 2003). The main vegetation types in the SNP are
forests (29%, mainly pine forests) and alpine and subalpine
grasslands 21%, the remaining 50% are un-vegetated. The
subalpine grasslands, which occupy only 3 km2 or less than
2% of the Park’s area, were created by clear-cutting of forest stands for agricultural use in the Middle Ages and were
used as cattle and sheep pastures as well as for hay production for approximately 500 years until livestock grazing was
banned in 1914. Today, two main vegetation types can be
distinguished on these former pastures: short-grass vegetation dominated by Festuca rubra L. is intensively grazed by
red deer. Seed production is high (2300 seeds/m−2 ; Iravani
2009) and most of the foliage and reproductive structures of
plants are packed into a small volume near the soil surface
(Thiel-Egenter et al. 2007). Tall-grass vegetation is dominated by tussocks of Carex sempervirens Vill, and Nardus
stricta L., is little grazed and has low seed production (1350
seeds/m−2 ; Iravani 2009). Within these grasslands, there
exist remnant patches of nutrient-rich agricultural communities, the predominant plant communities of cattle resting
areas before Park foundation (Wildi & Schütz 2000). The
subalpine grasslands are surrounded by conifer forests dominated by mountain pine (Pinus montana Miller), with an
understory vegetation characterised by ericaceous dwarf
shrubs (Schütz, Wildi, Achermann, Krüsi, & Nievergelt
2000).
In the SNP, hinds selectively graze on the nutrient-rich
short-grass vegetation (Schütz et al. 2003; Meyer & Filli
2006; Schütz et al. 2006). However, likely due to daytime
disturbance by visitors, hinds rest and ruminate in forest
habitats close to their favoured grazing sites (Schütte-Krug
& Filli 2006). Meyer and Filli (2006) estimated the size of
red deer hinds’ summer home ranges in the SNP to vary
between 344 and 494 ha (based on kernel analysis of tracking records from 21 radio-collared individuals). Stags, on
the other hand, range more widely and mostly prefer to
graze in tall-grass (forest edge) and forest understory vegetation (Haller 2002; Meyer & Filli 2006), where food is
more abundant but of lower quality (Schütz et al. 2003;
Schütz et al. 2006; Thiel-Egenter et al. 2007), though stags
also visit the short-grass vegetation occasionally during the
grazing season (Haller 2002; Schütte-Krug & Filli 2006).
Based on the sexual differences in red deer summer habitat
selection in the SNP and differences in forage seed density
between vegetation types, we would thus expect that hinds
disperse many seeds from short-grass vegetation, returning
most of these seeds to short grass vegetation and dispersing
507
some to other types of vegetation, whereas stags disperse
fewer seeds from tall-grass and forest understory vegetation, returning them mostly within these vegetation types.
Such behaviour could contribute to maintaining short-grass
vegetation by affecting the propagule pool in grassland communities and thus slowing down or preventing secondary
succession.
This study aimed at testing whether red deer endozoochory contributes to maintaining short-grass vegetation, the
favoured grazing sites of hinds in the SNP. In a greenhouse
germination experiment, we investigated the germinable
seed content of dung samples collected from short grass,
tall grass and forest understory vegetation in the Park. In
addition, we conducted vegetation relevés to compare the
species composition of red deer dung and of the vegetation
type in which the dung had been dropped. We hypothesized that (H1) species with small seeds potentially adapted
to endozoochory are more likely to occur in red deer
dung and occur in higher seed densities than larger-seeded
species, (H2) red deer dung contains mostly seeds from
short-grass vegetation, and (H3) seeds are less likely to be
dispersed between vegetation types than within vegetation
types, as expected if habitat selection differs between the
sexes.
Methods
Study area
The study was carried out in grassland and forest
sites of the Swiss National Park (SNP). The Park is
located in the southeastern part of Switzerland and covers an area of 172 km2 ranging from 1400 to 3170 m
above sea level (a.s.l.). The mean annual temperature
in the Park is 0.2 ◦ C ± 0.76 (mean ± SD) and the mean
annual precipitation 925 mm ± 162 (recorded at the Park’s
weather station: Buffalora 1977 m a.s.l.). The growing season extends from early June to the end of September,
the seed production season from mid July to late August,
respectively.
Based upon the known distribution of red deer (Meyer &
Filli 2006; Schütte-Krug & Filli 2006) and the major vegetation types in the SNP, we chose three areas for this study:
Alp Stabelchod (1950 a.s.l.), Alp La Schera (2090 m), and
Val Minger (2168 m). In each area, one site from each of
the three main vegetation types in the Park (short- and tallgrass vegetation, conifer forests) was selected, resulting in
three replicate sites per vegetation type and nine sites in
total.
Data collection
Dung samples were collected in late July and late August
2006, within the main period of seed set of the plant species
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M. Iravani et al. / Basic and Applied Ecology 12 (2011) 505–515
in the alpine and subalpine vegetation (Körner 2003). At each
collecting period, ten red deer fecal pellet groups (each corresponding to a complete deer defecation) were collected
randomly within a 20 m × 20 m area with homogeneous vegetation in each site. Only fresh (completely wet and intact),
pellet groups were collected to avoid seed contamination
from the soil and by seed rain. To make the species composition of red deer dung and of the vegetation type in which
the dung had been dropped comparable, the collected fecal
pellet groups were pooled, resulting in a pooled dung sample
for each site. In total, 18 pooled dung samples (180 pellet
groups) were collected over the two collecting periods in the
nine sites under study. The pooled dung samples, hereafter
referred to as dung samples, were air-dried at room temperature. We then took two dung subsamples with a dry mass of
100 g from each sample. To promote germination, one subsample was exposed to frost by storing it in a paper bag in a
dark and dry place in the study area during the winter period
(i.e. cold stratification).
The germinable seed content of the dung subsamples (with
and without cold stratification, 36 samples in total) was
determined in a greenhouse germination experiment over
a period of nine months. Before the experiment, we carefully crushed the pellets to ensure that all seeds received
enough light to germinate within a short time period. The
crushed dung was mixed with approximately the same volume of sterilized tree bark compost and spread out in a
thin layer (<0.5 cm) on trays filled with sterilized tree bark
compost covered with cotton fleece. The trays were placed
randomly on shelves in a greenhouse at the Swiss Federal
Institute for Forest, Snow and Landscape Research and were
rearranged every two weeks to prevent local micro-climatic
effects. Trays were illuminated with natural light, shaded
from bright sunlight and regularly watered with tap water.
The air temperature ranged between 30 ◦ C during the day
and 15 ◦ C during the night. We used an additional five trays
containing sterilized compost but no fecal material to test for
seed contamination of the substrate; no seedlings germinated
in these trays. As soon as possible after germination, we identified, counted and removed the seedlings. If a seedling could
not be identified immediately, it was transplanted to a pot to
allow further growth until identification was possible. A final
count was carried out after six months. We then remixed the
samples and returned them into the trays. The experiment
was continued for another three months, but few additional
seedlings emerged during this period. We did not attempt
to assess how many dormant seeds remained in the dung
samples.
All sites were part of recent field studies on forest and
grassland succession as well as ecosystem productivity. The
species composition of the vascular vegetation recorded
for a 10 m × 10 m plot in the centre of each selected area
(20 m × 20 m) was already known from these studies (Schütz
et al. 2006; Thiel-Egenter et al. 2007; Risch, Jurgensen,
Page-Dumroese, Wildi & Schütz, et al. 2008). Species cover
was estimated as the percentage of surface area covered
by each plant species (with a maximum of 100% total
cover). Only understory vegetation was studied in forest
sites. Species nomenclature follows Hess, Landolt, and Hirzel
(1984).
Data analysis
Germination from the two subsamples of each dung sample
(with vs. without cold stratification) was highly correlated
(Pearson’s correlation tests; n = 18, seedling density: r = 0.85,
P < 0.001, number of plant species: r = 0.90, P < 0.001). We
therefore pooled the data from the two associated subsamples
to obtain a single value: we then combined the data from the
two temporal samples (late July and late August) collected
at each site to obtain the germinable seed content of red deer
dung for the entire growing season. For further statistical
analyses, the number of seeds was calculated per 100 g dung
dry mass for each site.
We categorized the species that germinated from dung
samples according to growth form, seed length, and habitat preference (Table 1). Seed length data were obtained from
Müller-Schneider (1986) where possible or alternatively from
the LEDA trait base (Kleyer et al. 2008). Information about
habitat preference was obtained from Schütz et al. (2000). It
is not feasible to further classify grassland species into shortgrass and tall-grass species as many occur in both vegetation
types, though with different abundances (see Appendix A).
We tested the hypothesis that species with small seeds are
more likely to occur in red deer dung and occur in higher
seed densities than larger-seeded species in two steps. First,
we used a permutation test to test whether the proportion
of small seeded species among the species that germinated
from the dung samples was higher than expected from the
proportion of small seeded species present in the vegetation, or from the percent cover of small-seeded species,
based on the pooled vegetation relevés from all nine sites.
A permutation test was necessary to account for percent
cover. For each of 999 permutations, we randomly selected
42 species from all species listed in Appendix A without
replacement, either with equal probability or with probability proportional to percent cover, and calculated the number
of small-seeded species among those randomly selected to
derive the sampling distribution for the observed number
of small-seeded species among the 42 species that germinated from the dung samples (Table 1) and were observed
in the vegetation relevés (see Appendix A). Five species
that germinated from dung samples but did not occur in
the vegetation relevés were excluded from this test. For
species with <0.1% cover, we substituted cover = 0.05%.
Second, we tested whether small-seeded species germinated
in higher densities from dung samples than larger-seeded
species with a t-test with log-transformed number of
seeds.
Testing of the second hypothesis that red deer dung contains mostly seeds from short-grass vegetation was based
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M. Iravani et al. / Basic and Applied Ecology 12 (2011) 505–515
509
Table 1. Species germinated from red deer dung with their plant families, habitat preferences (G: grassland; F: forest; T: transition between
grassland and forest; after Schütz et al. 2000), growth forms (F: forb; G: graminoid; S: shrub and dwarf shrub), seed lengths (S: small or
less than 2 mm; M: medium or between 2 and 4 mm; L: large, or greater than 4 mm; after Müller-Schneider 1986; Kleyer et al. 2008), and
their number of occurrences (max. = 9), and total number of seeds from unfrosted and frosted dung samples. Species are sorted by the mean
number of seeds germinated from dung samples.
Species
Habitat
Growth form
Seed length
Nr. of occurrence
Total number of seeds
Unfrosted samples
Minuartia vernab
Cerastium caespitosumb
Veronica serpyllifoliab
Festuca rubrab
Stellaria nemoruma,b
Arabis corymbiflorab
Plantago majorb
Veronica chamaedrysb
Urtica dioicaa,b
Trifolium repensb
Luzula campestrisb
Poa alpinab
Agrostis alpinab
Galium pusillumb
Ranunculus montanusb
Trifolium pratenseb
Dactylis glomeratab
Ajuga pyramidalis
Thymus serpyllumb
Helianthemum alpestre
Plantago montanaa,b
Festuca ovinab
Poa annuab
Ranunculus repens
Crepis aurea
Sesleria caeruleab
Antennaria dioica
Arenaria ciliataa
Lotus corniculatusb
Polygala alpestris
Aconitum compactumb
Helianthemum nummularium
Cerastium arvenseb
Carex sempervirensb
Crepis alpestrisb
Plantago alpinaa
Gentiana campestris
Plantago mediab
Achillea millefolium
Campanula scheuchzeri
Erigeron alpinus
Hieracium pilosella
Phyteuma orbiculareb
Koeleria pyramidata
Polygonum viviparumb
Viola rupestrisb
Erica carnea
a Species
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
T
G
G
G
G
G
G
T
G
G
T
G
G
S
G
G
T
G
G
G
G
G
G
G
G
G
G
G
F
F
F
F
G
F
F
F
F
F
F
G
G
G
F
F
F
G
F
F
S
F
G
G
F
F
G
F
F
F
F
F
S
F
G
F
F
F
F
F
F
F
F
F
G
F
F
S
S
S
S
M
S
S
S
S
S
S
S
S
S
S
M
S
M
M
S
S
M
M
S
M
L
M
S
S
S
S
M
4
S
M
L
S
S
S
S
S
S
S
S
M
M
S
S
9
9
9
9
7
7
5
9
9
9
9
9
9
9
9
9
9
8
7
8
8
7
8
6
6
7
2
1
6
5
5
6
3
4
5
3
3
2
2
2
1
1
2
1
1
1
1
recorded only in dung samples and not in the vegetation relevés of the nine sites.
species germinated from dung deposited in conifer forests.
b Grassland
368
222
288
12
37
23
30
18
37
19
5
9
4
11
7
12
5
4
6
13
5
7
2
3
8
3
7
9
3
3
7
2
5
4
1
2
3
2
1
3
3
3
2
0
1
0
0
Frosted samples
332
362
34
60
33
41
24
26
7
23
33
27
30
23
21
14
17
16
14
5
13
9
10
9
4
7
3
1
5
5
1
4
3
2
3
2
1
2
3
1
1
1
0
1
0
2
1
Mean
350
292
161
36
35
32
27
22
22
21
19
18
17
17
14
13
11
10
10
9
9
8
6
6
6
5
5
5
4
4
4
4
3
2
2
2
2
2
2
2
2
1
1
1
1
1
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M. Iravani et al. / Basic and Applied Ecology 12 (2011) 505–515
on detrended correspondence analysis (DCA; Legendre &
Legendre 1998). The DCA analysis was performed with the
‘vegan’ package (Oksanen et al. 2010) in R (R Development
Core Team 2010) using the relative abundance of species
recorded in both dung samples and vegetation relevés. The
effect of the fixed factor vegetation type on the DCA scores
of the dung samples and of the vegetation relevés was tested
using two-way ANOVA. If the effect was significant, a
Tukey’s multiple comparison test (family-wise significance
level of α = 0.05) was performed.
To test the third hypothesis that seeds are less likely to be
dispersed between vegetation types than within vegetation
types, we tested for a difference in the number of species and
in the number of seeds germinated from dung samples among
vegetation types using ANOVA followed by Tukey’s multiple
comparison test (family-wise significance level of α = 0.05).
The data on the number of species and seeds dispersed were
subjected to log transformation to meet the criteria of normality and homogeneity. All analyses were performed in
R (R Development Core Team 2010). Untransformed data
are presented in the figures. We repeated the analysis without those species that germinated >100 times from the dung
samples to check for a potential masking effect of frequent
species. However, similar patterns were observed. Hence,
we discuss the results obtained by taking into account all
species.
Results
Germinable seed content of red deer dung
Overall, a total of 1230 seedlings (henceforth germinable
seeds) from 47 species germinated from the dung samples
(Table 1). Thirty of these species were recorded in five or
more of the nine dung samples. The vast majority of seeds
came from three species, Minuartia verna (L.) Hiern (28.5%
of seeds), Cerastium caespitosum L. (23.8%), and Veronica
serpyllifolia L. (13.1%), while 28 species were represented
by fewer than 10 seeds (Table 1).
The majority of species recorded in dung were plants of
grassland habitats (89.4%), and most were forbs (72.3%;
Table 2). A similar pattern was observed for the density of
seeds, where the seed species composition in red deer dung
was dominated by grassland species (98.2% of seeds) and
forbs (88.9%; Table 2). Only seeds of three woody plant
species (Erica carnea L., Helianthemum alpestre (Jacq.) DC.,
and Helianthemum nummularium (L.) Miller) germinated
from dung samples (1.1% of all seeds). The only species from
forest understory vegetation was E. carnea, and this species
only germinated from dung samples deposited in conifer forest. Moreover, seeds of five herbaceous grassland species
(Arenaria ciliata L., Plantago alpina L., Plantago montana
Lam., Stellaria nemorum L., Urtica dioica L.) that were not
recorded in any of the relevés germinated from dung samples (6% of all seeds). The majority of seeds germinated
Table 2. Characteristics of the seeds germinated from dung samples
with the number of species (S), the percentage of the total species
(%Stot , with Stot = 47), and the proportion of total germinable seeds
dispersed in each category (%Seeds).
Growth form
Forb
Graminoid
Dwarf shrub
Habitat
Grassland
Transition
Forest
Seed length
Small (<2 mm)
Medium (2–4 mm)
Large (>4 mm)
S
%Stot
%Seeds
34
10
3
72.3
21.3
6.4
88.9
10.0
1.1
42
4
1
89.4
8.5
2.1
98.2
1.7
0.1
33
12
2
70.2
25.5
4.3
90.8
8.6
0.6
from dung samples were small (<2 mm, 33 species, 90.8%;
Table 2). Crepis alpestris (Jacq.) Tausch. and Crepis aurea
(L.) Cass. were the only species with large seeds (>4 mm;
Table 1). Permutation tests showed that among the 104
species recorded in the vegetation relevés, more small-seeded
species germinated from the dung samples than expected by
chance, both without (P < 0.001, 999 permutations) and with
accounting for species cover (P < 0.001, 999 permutations).
An average of 34 seedlings were recorded for the smallseeded plant species that germinated from the dung samples,
which was not significantly different from the 8 seedlings that
were recorded on average from larger-seeded plant species
(independent samples I-test of log-transformed abundances,
df = 37.25, t = −1.166, P = 0.251).
Patterns of seed ingestion by red deer
Overall, the species composition of the dung samples and
of the vegetation type in which they had been dropped differed significantly (F1,12 = 1139.2, P < 0.001; Figs. 1 and 2).
The species located at the negative side of DCA axis 1 (61.5%
of inertia) corresponded closely to those species dispersed via
red deer dung (Fig. 1 and Table 1), whereas those detected at
the positive side of axis 1 represented the vegetation of the
receiving plant communities (Fig. 1 and Appendix A). Overall, the seed species composition of the dung dropped in any
vegetation type was most similar with the plant species composition of the short-grass communities (Fig. 2). For example,
a total of 40 of the 47 species recorded in the red deer dung
were present in the vegetation relevés of the short-grass vegetation, while only 25 species were in the tall-grass vegetation
and 13 in the conifer forest. Moreover, the species with 5 or
more seeds in red deer dung (28 species; Table 1) composed
42% of vegetation cover in short-grass vegetation but only
14% in tall-grass vegetation and 6% in conifer forest (see
Appendix A).
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M. Iravani et al. / Basic and Applied Ecology 12 (2011) 505–515
511
Fig. 1. Detrended correspondence analysis (DCA) of dung samples (empty symbols) and of vegetation relevés (filled symbols). DCA axis
1 (DCA1) and axis 2 (DCA2) explained 61.5% and 24.5% of inertia, respectively. Triangles denote short-grass vegetation, circles denote
tall-grass vegetation, and squares denote conifer forest understory vegetation. Only abundant plant species are shown in the DCA plot. Species
abbreviations include the first three letters of the genus name and of the species name (see Table 1 and Appendix A for full species names).
Patterns of seed deposition by red deer
4.5
3.5
Vegetation relevés
e
Dung samples
DCA1 scores
2.5
d
1.5
0.5
c
-0.5
-1.5
-2.5
a
Short-grass
b
Tall-grass
b
Conifer forest
Vegetation types
Fig. 2. Comparison of the DCA axis 1 (DCA1) scores of the dung
samples and of the vegetation relevés of the plant communities in
which they had been dropped (Tukey’s multiple comparison test).
Bars indicate mean ± SE. Different letters indicate significant differences (family-wise significance level of α = 0.05).
In terms of species composition, the first DCA axis significantly separated the seeds in dung samples from short-grass
vegetation and from those of the other two vegetation types
(F2,12 = 31.9, P < 0.001; Fig. 2). The species composition of
seeds in the dung collected from short-grass vegetation was
significantly different from that collected in tall-grass vegetation (P = 0.01) and conifer forest (P = 0.007; Fig. 2), whereas
there was no significant difference between the species composition in the dung collected from tall-grass vegetation and
conifer forest (P = 0.80; Fig. 2).
Overall, species richness and seed density of dung collected in different vegetation types ranged from 24 to 36
species, and from 54 to 286 seeds per 100 g dung dry mass,
respectively. The number of dispersed species did not vary
among vegetation types (F2,6 = 0.09, P = 0.92; Fig. 3A), but
there was significant variation in the mean number of seeds
dispersed (F2,6 = 12.6, P = 0.007; Fig. 3B). The seed density
in dung collected in short-grass vegetation was higher (in
fact, over twice as high) than that obtained from tall-grass
vegetation (P = 0.01) and conifer forest (P = 0.007), whereas
there was no significant difference between the seed density in
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M. Iravani et al. / Basic and Applied Ecology 12 (2011) 505–515
A
40
Number of species dispersed
35
30
a
a
a
25
20
15
10
5
0
Short-grass
Tall-grass
Conifer forest
Vegetation types
Number of seeds dispersed (Nr./ 100g)
300
a
250
200
150
b
b
100
50
0
Short-grass
Tall-grass
Conifer forest
Vegetation types
Fig. 3. Comparison of species richness (A) and seed density (B)
of the dung dropped in different vegetation types (Tukey’s multiple
comparison test). Bars indicate mean ± SE. Different letters indicate
significant differences (family-wise significance level of α = 0.05).
dung from tall-grass vegetation and conifer forest (P = 0.80;
Fig. 3B).
Discussion
Germinable seed content of red deer dung
This study showed that many plant species were dispersed
by red deer (47 species), with 40% of the species recorded in
the vegetation relevés being also found as seeds in the dung
samples (see Appendix A). Note that these results assess
potential endozoochory, based on greenhouse germination,
whereas rates of establishment in the field are likely considerably lower (Pakeman & Small 2009).
Our results confirmed the hypothesis (H1) that smallseeded species were more likely to occur in red deer dung
than larger-seeded species. However, the second part of the
hypothesis, stating that small-seeded species occur in higher
densities than larger-seeded species, was not supported by our
data. Seed dispersal in red deer dung mostly included herbaceous species of grassland habitats with no specific dispersal
adaptations except the small size of their seeds. The bias
towards small-seeded species is consistent with the expectation that small seeds are more likely to pass the herbivore’s
digestive tract undamaged (Gill & Beardall 2001; Pakeman
& Small 2009; Kuiters & Huiskes 2010). High seed density, however was not related to seed size. The three species
that dominated seed content of red deer dung, accounting for
65% of germinable seeds, showed typical growth forms of
preferred forage species by concentrating their reproductive
organs and numerous seeds above (M. verna, C. caespitosum)
or among green leaves (V. serpyllifolia). Based on the present
data, it is not possible to fully disentangle the effects of seed
availability, feeding selection, or differences in the viability of seeds in the gut, and further research will be needed to
ascertain whether these species have additional adaptations to
endozoochory that affect either the number of seeds ingested
or their germinability after passing the digestive tract.
Seeds of species from the conifer forest understory were
almost absent from dung. This was rather surprising as it is
known that red deer in the SNP often browse forest understory
species such as E. carnea (Suter, Suter, Krüsi & Schütz 2004).
One explanation could be that the relatively larger seeds of
these late-successional species (Gill & Beardall 2001; Eycott
et al. 2007) are no longer viable after passing the digestive tract of red deer (Welch 1985; Bruun et al. 2008). It
is also possible that relatively few seeds are ingested, despite
large amounts of plant material being consumed, due to the
generally low seed production of forest understory plants
(Heinken et al. 2002; Eycott et al. 2007; Iravani 2009) and
also the position of seeds and reproductive organs compared
to the foliage part of these plants (Thiel-Egenter et al. 2007).
The five plant species that germinated from dung samples
but were not recorded in the vegetation relevés were smallseeded herbaceous species characteristic of remnant patches
of nutrient-rich agricultural communities (Wildi & Schütz
2000; Iravani 2009).
There have been very few studies of seed dispersal by
wild ungulates in the European Alps, but the predominance of small-seeded herbaceous plants of open habitats
has been reported for red deer dung samples collected from
other subalpine grasslands (Müller-Schneider 1948), heather
moorlands (Welch 1985), Mediterranean dehesa (Malo &
Suarez 1995; Malo et al. 2000), and forests (Heinken et al.
2002; Oheimb et al. 2005; Eycott et al. 2007).
Patterns of seed ingestion and deposition by red
deer
If red deer grazed all species and vegetation types equally
and deposited their dung randomly, their activities would
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M. Iravani et al. / Basic and Applied Ecology 12 (2011) 505–515
lead to a homogenization of the propagule pool among vegetation types (assuming that all species were equally able
to germinate after endozoochorous dispersal). However, our
second hypothesis that red deer dung contains mostly seeds
from short-grass vegetation was supported by the results. We
found that the species composition of seeds in dung was most
similar to that of short-grass communities, suggesting a net
transfer of seeds from short-grass communities to the other
communities.
Our third hypothesis that seeds are less likely to be dispersed between vegetation types than within vegetation types
was also supported by the results. We found significant differences in mean seed density and seed species composition
between dung deposited in short-grass communities and dung
deposited in the other two vegetation types, suggesting nonrandom deposition related to patterns of habitat use. These
results are consistent with the expectation that hinds primarily
forage on short-grass vegetation, whereas stags preferentially
forage in tall-grass and forest understory vegetation.
We are unaware of any previous study that investigated
sexual differences in endozoochory by large herbivores.
However, in a study of seed dispersal in the hair of bison (epizoochory), Rosas et al. (2008) found differences in species
composition between bulls and cows, possibly due to differing use of habitats. While the present study suggests a
possible sexual difference in the pattern of endozoochorous
seed dispersal by red deer, further research including sex
determination of fecal pellet groups with molecular genetic
markers is needed to gain further insights into seed dispersal
patterns resulting from sex-specific habitat use.
Importance for grassland dynamics
Our results suggest that red deer hinds disperse seeds
of several herbaceous species typical of short-grass communities primarily within intensively grazed short-grass
vegetation. This seed dispersal behaviour may considerably
influence the dynamics and structure of their preferred vegetation type (Janzen 1984; Malo & Suarez 1995; Gill &
Beardall 2001; Shiponeni & Milton 2006; Pakeman & Small
2009). In the SNP, Schütz et al. (2003) found that the proportion of such preferred forage species increased where red deer
hinds were grazing at high density since the foundation of
the Park. Up to 70% of the soil seed bank of such intensively
grazed grassland areas consisted of species found in red deer
dung on these sites, many of these species were not present
in the local vegetation, and seed bank composition differed
considerably between grazed areas and exclosures (Iravani
2009). The abundance of certain species in both the dung
and the grassland soils increases their capacity to occupy any
gaps created by disturbances such as grazing (Malo & Suarez
1995; Bakker & Olff 2003; Kuiters & Huiskes 2010). Red
deer behaviour may thus contribute to maintaining the vegetation of their favoured grazing sites by increasing propagule
pressure of seeds from preferred forage species adapted to
513
endozoochory relative to other species and especially those
from later stages of secondary succession.
Taken together, our results support the hypothesis that red
deer endozoochory contributes to maintaining short-grass
vegetation, the favoured grazing sites of hinds in the SNP.
Vera (2000) proposed that large herbivores are important in
maintaining an open landscape, but the empirical evidence
for this hypothesis has been lacking. Foraging behaviour and
patterns of habitat use by red deer in the SNP are largely
unaffected by human interference (Meyer & Filli 2006;
Schütte-Krug & Filli 2006), so that the observed seed dispersal behaviour of hinds may be taken as indirect evidence
in support of Vera’s hypothesis. This is further supported
by the surprisingly slow rate of secondary succession after
abandonment as evidenced by permanent plot data recorded
since 1917 (Schütz et al. 2000; Wildi & Schütz 2000; Iravani
2009). If gap creation is largely due to deer grazing, then
regeneration niches will become available mostly in the intensively grazed areas that also receive the highest input of seeds
through red deer dung. In ungrazed areas (e.g. within permanent exclosures), secondary succession may thus be halted
by gap limitation, whereas the dominance of seeds of earlysuccessional herbaceous species adapted to endozoochory
may prevent the establishment of species characteristic of
later successional stages in grazed areas.
Acknowledgments
We would like to thank Josef Senn for his valuable comments on earlier drafts of the manuscript and translation of
the abstract into German, and three anonymous reviewers for
helpful comments on an earlier version of the manuscript.
The authors are especially grateful to Dieter Trummer and
Liven Dekonink for their collaboration in the field and to
Werner Läuchli for his assistance in the greenhouse. We also
appreciate the support by the Swiss National Park administration.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the online version, at
doi:10.1016/j.baae.2011.07.004.
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