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Endozoochory is a prominent form of seed dispersal in tropical dry forests. Most extant megafauna that perform such seed dispersal are ungulates, which can also be seed predators. White-tailed deer (Odocoileus virginianus) is one of the last extant megafauna of Neotropical dry forests, but whether it serves as a legitimate seed disperser is poorly understood. We studied seed dispersal patterns and germination after white-tailed deer gut passage in a tropical dry forest in southwest Ecuador. Over 23 mo, we recorded ca 2000 seeds of 11 species in 385 fecal samples. Most seeds belonged to four species of Fabaceae: Chloroleucon mangense, Senna mollissima, Piptadenia flava, and Caesalpinia glabrata. Seeds from eight of the 11 species dispersed by white-tailed deer germinated under controlled conditions. Ingestion did not affect germination of C. mangense and S. mollissima, whereas C. glabrata showed reduced germination. Nevertheless, the removal of fruit pulp resulting from ingestion by white-tailed deer could have a deinhibition effect on germination due to seed release. Thus, white-tailed deer play an important role as legitimate seed dispersers of woody species formerly considered autochorous. Our results suggest that more research is needed to fully understand the ecological and evolutionary effects of the remaining extant megafauna on plant regeneration dynamics in the dry Neotropics.
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White-tailed deer as the last megafauna dispersing seeds in Neotropical dry forests:
the role of fruit and seed traits
Andrea Jara-Guerrero
, Gema Escribano-Avila
, Carlos Iv
an Espinosa
, Marcelino De la Cruz
,and Marcos M
Departamento de Ciencias Biol
ogicas, Universidad T
ecnica Particular de Loja, CP.: 11-01-608 Loja, Ecuador
IMEDEA- Institut Mediterrani d’Estudis Avanc
ßats (CSIC-UIB), Esporles, Illes Balears, Spain
Departamento de Biolog
ıa y Geolog
ıa, F
ısica y Qu
ımica Inorg
Area de Biodiversidad y Conservaci
on, Universidad Rey Juan Carlos,
E-28933 Madrid, Spain
Endozoochory is a prominent form of seed dispersal in tropical dry forests. Most extant megafauna that perform such seed dispersal
are ungulates, which can also be seed predators. White-tailed deer (Odocoileus virginianus) is one of the last extant megafauna of Neotropi-
cal dry forests, but whether it serves as a legitimate seed disperser is poorly understood. We studied seed dispersal patterns and germi-
nation after white-tailed deer gut passage in a tropical dry forest in southwest Ecuador. Over 23 mo, we recorded ca 2000 seeds of 11
species in 385 fecal samples. Most seeds belonged to four species of Fabaceae: Chloroleucon mangense,Senna mollissima,Piptadenia ava, and
Caesalpinia glabrata. Seeds from eight of the 11 species dispersed by white-tailed deer germinated under controlled conditions. Ingestion
did not affect germination of C. mangense and S. mollissima, whereas C. glabrata showed reduced germination. Nevertheless, the removal
of fruit pulp resulting from ingestion by white-tailed deer could have a deinhibition effect on germination due to seed release. Thus,
white-tailed deer play an important role as legitimate seed dispersers of woody species formerly considered autochorous. Our results
suggest that more research is needed to fully understand the ecological and evolutionary effects of the remaining extant megafauna on
plant regeneration dynamics in the dry Neotropics.
Abstract in Spanish is available with online material.
Key words: anachronistic traits; deinhibition; dry brous pulp; germination; gut passage; herbivore; legume; megafauna fruits.
it promotes genetic connectivity and diversity of plant communi-
ties (Nathan & Muller-Landau 2000, Jordano et al. 2007), as well
as for the colonization of vacant habitats (Escribano-Avila et al.
2014). Zoochory (seed dispersal by animals) is a major dispersal
syndrome in tropical forests (Howe & Smallwood 1982, Jordano
2000), including dry tropical ecosystems, where fruit availability is
seasonally limited (Bullock 1995, Jordano 2000, Jara-Guerrero
et al. 2011). Not all dispersers are equally effective in tropical sys-
tems (Brodie et al. 2009, McConkey & Brockelmanm 2011).
Large-sized dispersers, like mammals, have no limitations of gape
width and present higher movement capacity and gut retention
time, thus generating more diverse, long-distance dispersal pat-
terns than smaller dispersers (Jordano et al. 2007, Nathan et al.
2008, O0Farrill et al. 2013). Therefore, large-sized mammals
(>35 kg) are especially important endozoochorous species,
because they are long-distance dispersers of many seeds of vari-
ous sizes (Escribano-
Avila et al. 2015).
The extinct Neotropical megafauna consisted mostly of wide
trophic-range herbivores (Corlett 2013). The role of herbivorous
megafauna as effective seed dispersers has been challenged due
to the low probability of seeds surviving passage through the gut
(Janzen 1981, Bodmer 1991, Picard et al. 2015). For instance,
tapirs (Tapirus terrestris), the largest members of the extant
Neotropical megafauna, have been identied as seed predators,
(Janzen 1981) or effective seed dispersers (O0Farrill et al. 2013),
depending on the plant species. One of the few tropical studies
comparing seed dispersal by different species of deer, peccaries,
and tapirs, showed that 0.41 cm seeds had better survival prob-
abilities than larger ones (Bodmer 1991). While deer and pecca-
ries acted mainly as seed predators, almost half of the seeds
dispersed by tapirs were still viable (Bodmer 1991). These nd-
ings highlight the species-specic seed-dispersal effects of large
herbivores, the effectiveness if which depends on not only their
own characteristics, but also seed traits (e.g., size and shape) (Jan-
zen 1982, O0Farrill et al. 2013, Albert et al. 2015). For example,
small round seeds seem more resistant to gut passage and suffer
less damage from chewing (Mouissie et al. 2005).
White-tailed deer are among the last extant and common
megafauna inhabiting Neotropical dry forests (NTDFs) (Ficcarelli
et al. 2003), probably the most endangered tropical biome due to
deforestation and climate change (Janzen 1988, Miles et al. 2006).
Given their body size and broad diet, white-tailed deer are likely
to disperse a wide spectrum of plant species (Myers et al. 2004,
Williams et al. 2008), which may include the so-called anachronis-
tic fruits(i.e., fruits dispersed by Pleistocene megafauna; Janzen
& Martin 1982, Guimar~aes et al. 2008). In addition, white-tailed
Received 27 February 2017; revision accepted 10 August 2017.
Corresponding author; e-mail:
ª2017 The Association for Tropical Biology and Conservation 1
BIOTROPICA 0(0): 1–9 2017 10.1111/btp.12507
deer are long-distance dispersers (Myers et al. 2004, Williams et al.
2008). Therefore, dispersal by white-tailed deer may promote
functional connectivity between fragmented patches (sensu Auffret
et al. 2017), as well as aid NTDF species to track new available
habitats resulting from climate change (Cain et al. 2000). Hence,
similar to their extinct counterparts or to tapirs in rainforests,
white-tailed deer may play a relevant ecosystem function. Unfor-
tunately, most studies about seed dispersal by white-tailed deer
have been conducted in temperate areas of North America and
mainly focused on invasive herbaceous species (Williams et al.
2008, Habeck & Schultz 2015). The scarce literature about dis-
persal of NTDF species by white-tailed deer reports anecdotic
dispersal events of a handful of species (Spondias mombin: Janzen
1985, Opuntia sp.: Gonzalez-Espinosa & Quintana-Ascencio
1986, Maximiliana maripa: Fragoso 1997, Spondias purpurea, Brosi-
mum alicastrum, Jacquinia pungens: Arceo et al. 2005) and fails to
provide crucial data on the capacity of seed germination of
NTDF woody species after white-tailed deer gut passage. Accord-
ingly, we do not know whether white-tailed deer are legitimate
seed dispersers or seed predators of NTDF species (Bodmer
1991). Ungulate species differ greatly in diet, suggesting that fruit
consumption is not random and therefore acts as an ecological
lter for species with particular traits (Albert et al. 2015). Thus,
we expect that traits of fruits and seeds will determine the role
of white-tailed deer as seed dispersers or seed predators.
In this study, we address the role of white-tailed deer as
legitimate seed dispersers in a well-preserved NTDF in Ecuador.
We asked several specic questions: (1) Which plant species are
more frequently dispersed by white-tailed deer? (2) Are white-
tailed deer consuming fruits and seeds with a particular subset of
traits? and (3) Do seeds of those species differentially survive
and germinate after white-tailed deer gut passage?
STUDY AREA.We conducted this study at the Arenillas Ecolog-
ical Reserve (REA), located in El Oro province, Southwest
Ecuador (03°34015.44S; 80°08046.15E, 30 m asl), (Fig-
ure S1). The REA has been protected for approximately 60 yr,
formally included in the National System of Protected Areas
of Ecuador since 2001 (BirdLife International 2014). Annual
mean precipitation is 667 mm, mainly concentrated between
January and May, with a strong dry season from June to
December. Mean maximum daily temperature is 25.2°C, with a
variation of 3.4°C between the coldest and warmest month
(Espinosa et al. 2015).
The REA covers 13,170 ha of one of the last remnants of
NTDFs on the Ecuadorian Pacic Coast (Espinosa et al. 2015).
The most conspicuous tree species in the area are Tabebuia
chrysantha and T. billbergii (Bignoniaceae), along with Cynophalla
mollis (Capparaceae), Erythroxylum glaucum (Erythroxylaceae), Erio-
theca ruizii (Malvaceae), Leucaena trichodes, Chloroleucon mangense
(Fabaceae), and Cochlospermum vitifolium (Bixaceae). In the central
REA, one of the best- preserved areas, we established a 9-ha per-
manent plot consisting of transitional vegetation between tropical
dry forest and lowland dry scrubland (Figure S1). Since 2009, all
individual trees with a diameter at breast height 5 cm have been
inventoried within the plot (Jara-Guerrero et al. 2015), and we
inventoried shrubs and subshrubs in the central hectare of the
plot. A total of 49 woody species have been recorded. Fabaceae
is the predominant family, with 10 species (or 20 percent) of the
recorded individuals.
white-tailed deer, is the only deer species reported for the REA.
Although distribution of Mazama americana includes areas of
NTDF of southwestern Ecuador, there are no records for the
REA. Recently, camera trap sampling in the area did not detect
M. americana but pointed to O. virginianus as the mammal species
with the greatest number of records (0.13 individuals/day/trap;
Espinosa et al. 2016). This species is a large cervid (50120 kg),
usually solitary, but also forming small groups. Because of its
robust body and branched horns, it is more common in open
areas. Like other deer, it is a herbivorous ruminant (Eisenberg &
Redford 1999); as a browser, it feeds mainly on leaves, twigs, and
young shoots of trees and shrubs (Hoffman 1989), but also con-
sumes fruits during the dry season (Tirira 2007).
IN FECES.We established a 3.4 km transect in the central por-
tion (4.8 ha) of our 9-ha permanent plot, and surveyed this tran-
sect monthly for 23 mo, between October 2011 and September
2013. Each month, we collected all white-tailed deer feces
detected in a 2-m-wide band along the transect. We considered
each group of spatially aggregated pellets as an individual sample.
Each fecal sample was placed in a plastic bag and labeled, and
air-dried in the lab. In addition, we collected mature fruits from
plants within the study area to build a reference seed collection
for identication of the dispersed seeds.
All seeds present in the feces were extracted by sample dis-
aggregation. We identied each seed with the aid of the reference
seed collection and scored the number of seeds per plant species
for each fecal sample. We visually inspected seeds to assess viabil-
ity, i.e. identify possible damage during the ingestion, physical
damage signals or putrefaction.
For the most frequently dispersed seeds, we evaluated the
overlap between the period of fallen fruits and that of white-
tailed deer dispersal. The fall of fruits upon ripening (or even
before) has been considered a part of the megafauna dispersal
syndrome (Janzen & Martin 1982). A parallel study of seed rain
for trees and shrubs (Jara-Guerrero 2015) provided data used to
compare the phenology of seed-fruit fall with the presence of the
most frequently encountered seeds in our samples: Chloroleucon
mangense, Caesalpinia glabrata, Leucaena trichodes, and Senna mollissima.
The species Piptadenia ava was excluded as no seeds were
detected in the seed traps. Additionally, we explored the match
between seed abundance in the seed rain and presence in white-
tailed deer feces, by comparing the percentage of seeds in our
samples with the total availability of seeds in the seed rain, as an
indirect measure of availability.
2 Jara-Guerrero et al.
FRUIT AND SEED TRAITS.To analyze if white-tailed deer were
consuming fruits and seeds with a particular subset of traits, we
compiled information for six traits in the 49 species present in
the plot (Table S1). We classied fruit type in seven categories
following Jara-Guerrero et al. (2011), and measured fruit length
and width to the nearest mm in samples collected in the study
site. Number of seeds per fruit, seed mass, and volume were
measured in the same samples or taken from the literature
(Romero-Saritama & Perez-Ruız 2016). We used only the seed
volume to represent the seed size. Dispersal syndromes zoo-
chory, anemochory, or autochory were scored following Jara-
Guerrero et al. (2011).
GERMINATION PATTERNS.Seeds dispersed by white-tailed deer
were sown in plastic trays lled with moist peat and kept under
greenhouse conditions. To record the presence of unobserved
seeds, we sowed the remaining fecal material with the seeds. We
monitored germination for 90 d to determine the germination
percentage. We considered a seed germinated when the radicle
emerged from the seed coat. Seeds that failed to germinate were
visually inspected for possible damage after sowing.
To assess the effect of gut passage on seed germination, we
compared the germination capacity of white-tailed deer-dispersed
vs. control seeds. Control seeds were collected in June and July
2013 from at least ve trees per species. We randomly selected
100 control seeds and separated them into four trays of 25 seeds,
sown under the same conditions as dispersed seeds. We used
three species that were abundant enough in white-tailed deer
feces (N70, Table 1): Chloroleucon mangense,Caesalpinia glabrata,
and Senna mollissima. Our experiment assessed the scarication
effect resulting from white-tailed deer gut passage, given that pulp
from control seeds was removed by hand, but not the deinhibi-
tion effect resulting from pulp removal, as no intact fruits were
sown (Samuels & Levey 2005, Robertson et al. 2006).
DATA ANALYSIS.To assess if white-tailed deer were dispersing
fruits and seeds with a particular subset of traits, we performed
two kinds of tests. We used a MannWhitney test for each quan-
titative variable to test whether the distributions of fruit and seed
traits differ between dispersed and not dispersed. We used a
Fisher exact test to explore whether fruit type was associated
with dispersal or non-dispersal by white-tailed deer. We used the
functions wilcox.test and sher.test implemented in R. These tests
were performed only including the species for which trait values
were available (Table S1): fruit length, 40 species; fruit width, 43;
seed volume, 39; number of seeds per fruit, 35; and fruit type,
50. The percentage of species used in the analyses, with respect
to those present, varied between 78100 percent.
To evaluate the effect of scarication after gut passage on
seed germination, we tted Generalized Linear Models (GLM)
with germination occurrence as the response variable and origin
(white-tailed deer dispersal or control) as the independent vari-
able. We considered a binomial distribution of errors and a logit
link function. All data analyses were performed in the R environ-
ment (R Core Team 2016).
IN FECES.A total of 385 white-tailed deer fecal samples were
recorded, mainly detected between the end of the rainy season
(May) and the end of the dry season (January), with an abun-
dance ranging between 0 and 86 feces per month
(mean SE =19 4). 65.3 percent of fecal samples contained
seeds. The number of seeds ranged from one to 54
(mean SE =7.8 0.59 seeds per fecal sample, Table S2), giv-
ing a total of 1961 seeds belonging to 11 species from at least
ve families (Table 1). We found up to ve species in a fecal
sample, although 57 percent contained seeds of a single species.
All recorded seeds were intact with no apparent damage to the
seed coat. The most frequent and abundant species dispersed by
white-tailed deer was Chloroleucon mangense, followed by Senna mol-
lissima,Caesalpinia glabrata, and Piptadenia ava (Table 1). Although
the period of seed rain and white-tailed deer dispersal sampling
did not completely coincide, there was a trend that showed
white-tailed deer dispersal of these species several months after
peak fruit fall (Figure S2). Among the species dispersed by white-
tailed deer, the match between seed abundance in feces and seed
rain was variable (Fig. 1). From the ten species present in the
seed rain, C. mangense was abundant both in the seed rain and in
feces (Fig. 1), while C. glabrata showed a low abundance in both.
Conversely, R. aurantiaca, S. mollissima, L. trichodes, and Vigna sp.
were abundant in the seed rain but very scarce in our samples
(Fig. 1). Among the other four species recorded in the white-
tailed deer feces that were absent in the seed rain sampling,
P. ava was most abundant.
fruits dispersed by white-tailed deer were dehiscent legumes, 61
250 mm in length and 1320 mm in width with 815 seeds, and
TABLE 1. Seed frequency and abundance in white-tailed deer feces and germination.
Family Species FG/N
Fabaceae Chloroleucon mangense 206 136/1183
Caesalpinia glabrata 32 6/75
Leucaena trichodes 10 0/12
Piptadenia ava 26 11/104
Senna mollissima 96 13/544
Vigna sp. 11 3/16
Cactaceae Unidentied 1 1/1
Convolvulaceae Unidentied 6 0/10
Primulaceae Bonellia sprucei 1 1/1
Rubiaceae Randia aurantiaca 2 0/7
Unidentied 7 1/8
Seeds of plant species present in 385 white-tailed deer feces collected during
23 mo. F: Frequency, number of fecal samples containing at least one seed of
a given species. G/N: Number of germinated seeds (G) and total abundance
of dispersed seeds (N). Seeds coded as Unidentied showed similar characteris-
tics and were assumed to belong to the same species.
Seed Dispersal by White-Tailed Deer 3
varying in seed volume from 12 to 323 mm
, and in seed mass
from 0.016 to 0.176 g. Large-sized berries (length: 3055 mm;
diameter: 1740 mm) and dehiscent capsules were the other fruit
types dispersed by white-tailed deer, though in much lower
amounts than dry pods (Table S1). This pattern was conrmed
by the Fisher test, which indicated signicant association between
fruit type and dispersal by white-tailed deer (Fig. 2). MannWhit-
ney tests showed signicant differences between species dispersed
and not dispersed by white-tailed deer in relation to fruit length,
fruit width, and number of seeds, but not seed volume (Fig. 2).
Compared to the average available fruit, white-tailed deer
consumed fruits that were longer, wider, and had more seeds.
The fruit types dispersed by white-tailed deer were primarily
legumes, although berries were found in a low frequency; drupes
and achenes were never recorded in our samples.
of the eleven plant species dispersed by white-tailed deer germi-
nated (Table 1). From the four most frequent and abundant spe-
cies, three (C. mangense,P. ava, and C. glabrata) presented a
germination percentage around 10 percent, while only 2 percent
of S. mollissima seeds germinated. A very small sample size was
available for the remaining species (Table 1). From B. sprucei and
the Cactaceae species, only one seed each was present in the
feces and both species germinated, while seeds of Randia auranti-
aca, Leucaena trichodes, and the unidentied Convolvulaceae species
did not germinate. We did not nd any external damage on seeds
that failed to germinate.
No signicant differences in germination percentage were
found for C. mangense and S. mollissima seeds after white-tailed
deer gut passage, compared to controls (Fig. 3 and Table 2).
However, we found a signicant reduction in germination capac-
ity (10% vs. 90%) for C. glabrata gut-passed seeds compared to
control seeds (Fig. 3; Table 2).
FOREST.White-tailed deer was a frequent seed disperser in the
NTDF of southwestern Ecuador. First, white-tailed deer con-
sumed, and therefore potentially dispersed by via endozoochory,
20 percent (10 out of 49) of all woody species in the study area,
and 35 percent (10 out of 28 species) of those species that can be
dispersed by animals (Table S1). In addition, one climber species,
not sampled in the seed rain experiment, was found in the fecal
samples. Although only a few species were dispersed in large
numbers, these are among the most frequent and abundant spe-
cies in the study area (Fabaceae species). Second, 65 percent of
white-tailed deer feces contained seeds, indicating that dry fruits
are a regular component of its diet. Thus, white-tailed deer moved
seeds of 11 species belonging to ve families. Third, plant species
dispersed by deer shared particular fruit traits, such as large size
and many seeds. The most frequently dispersed fruits were dry
pods from legumes, which had brous pulp but no apparent
adaptations for assisted dispersal and were previously considered
autochorous (Jara-Guerrero et al. 2011, Lopez-Martınez et al.
2013). Arceo et al. (2005) showed that species commonly dis-
persed by white-tailed deer fructied during the dry months,
which was also the case in this study. During the dry months, the
proportion of feces with seeds was higher than in the rainy sea-
son. However, this pattern must be taken with caution due to the
low quantity of feces recorded during the rainy months, which
could be related to a lower detectability rate (Wiles 1980, Aulak &
Babinska-Werka 1990). Fourth, contrary to our expectations,
white-tailed deer dispersal did not adversely affect seed survival or
germination of the three species evaluated; the majority were able
to germinate to some extent. Together, these ndings point to
white-tailed deer a pivotal seed-dispersal species, maintaining
regeneration dynamics and colonization capacity.
Anemochory and zoochory are considered the most relevant
dispersal modes in NTDFs (Jara-Guerrero et al. 2011, Lopez-
Martınez et al. 2013, Hilje et al. 2015). Among zoochorous spe-
cies, birds and bats seem the most relevant dispersers (Nassar
et al. 2013), with a minor role recognized for reptiles and terres-
trial mammals (but see Benıtez-Malvido et al. 2003 and Hilje et al.
2015). Specialist frugivorous bats (Phyllostomidae) are rather
common in NTDF assemblages (410 species: Rıos-Blanco &
Perez-Torres 2015) in contrast to specialist frugivorous birds (1
3 plant species: Ramos-Robles et al. 2016), which are usually
absent (Nassar et al. 2013). According to our study, white-tailed
deer disperse a similar number of species as other NTDF special-
ized frugivores, although this comparison is made from different
study areas and therefore should be taken with caution. However,
it seems clear that the species and fruit type dispersed by white-
tailed deer (mainly dry legumes) are distinctive and complemen-
tary to those dispersed by other frugivores (eshy drupes, berries,
FIGURE 1. Percentage of seeds per species in white-tailed deer feces and in
the seed traps, with respect to the total number of seeds in white-tailed deer
feces (N=824) and in seed traps (N=287) from October 2011 to July
4 Jara-Guerrero et al.
and syconia, Ramos-Robles et al. 2016, Rıos-Blanco & Perez-
Torres 2015). In addition, the longer seed dispersal distances (up
to 35 km) performed by white-tailed deer (Myers et al. 2004,
Williams et al. 2008), compared to smaller-bodied frugivores, such
as birds and bats (up to 1 km, Carlo et al. 2013, Abedi-Lartey
et al. 2016, Gonzalez-Varo et al. 2017, Jordano 2017), probably
make this species a relevant and complementary disperser of
NTDF plants.
SPECIES.Seed survival after ingestion by ungulates depends
mainly seed treatment, such as chewing, swallowing, or spiting
(Gardener et al. 1993, Myers et al. 2004, Mouissie et al. 2005).
According to our results, white-tailed deer defecated undamaged
seeds. Thus, the negative effects found on germination for
C. glabrata seem to be due to excessive scarication, likely related
to seed size, and not to chewing. Herbivore body size and feed-
ing type (i.e., grazer or browser) greatly inuence seed retention
time, which in some cases has been negatively related to seed sur-
vival probability (Janzen 1982, Bodmer 1991, Picard et al. 2015).
White-tailed deer, as browsers, consume plant materials that
require a rumination process. This may lead to a strong scarica-
tion of seeds that, together with high acid secretion in white-
FIGURE 2. (A) Frequency of fruit types dispersed (black bars) and not dispersed (gray bars) by white-tailed deer. Box plots for (B) fruit length, (C) fruit width
(D), seed volume, and (E) seed number of fruits dispersed and not dispersed by white-tailed deer. Segments in box plots indicate minimum and maximum values,
the box denotes rst and third quartile. Bolded line denotes the median value.
Seed Dispersal by White-Tailed Deer 5
tailed deer gut (Clauss et al. 2008), may produce internal damage
to seed embryos. Caesalpinia glabrata seeds are twice the size of all
other studied species that were not negatively affected by gut pas-
sage. A larger seed size implies greater surface contact and expo-
sure to digestive effects, which may explain the costs of
herbivore gut passage on seed germination, as previously seen in
other large-seeded species (Pakeman et al. 2002, Mouissie et al.
A seldom recognized advantage of endozoochory is the
release of seeds from the pulp (Miller 1995, Samuels & Levey
2005). This depulping can entail a positive effect on seed germi-
nation (i.e., deinhibition effect), by removing inhibitory substances
present in the pulp, (Traveset et al. 2007) and removing patho-
gens and attractants to seed predators (Fricke et al. 2013). For
the dehiscent species studied, whose seeds are spontaneously
released, the deinhibition effect may be irrelevant, but it may be
important for the eshy or indehiscent legumes species dispersed
by white-tailed deer, such as C. glabrata. Legumes are known to
suffer high rates of pre-dispersal loss owing to bruchiids and
other beetles. In addition, ongoing research (GEA, unpubl. data)
suggests that several species dispersed by white-tailed deer show
very low rates of germination when kept in the fruits. Notably,
<1 percent of C. glabrata seeds inside pods germinated, while
released seeds germinated up to 80 percent (GEA, unpubl.
results). For C. glabrata, the benecial deinhibiton effect resulting
from seed release of the dry, thick, brous pulp may offset the
excessive scarication, yielding an overall positive effect of white-
tailed deer dispersal.
The few experiments on gut passage that have utilized intact
fruits as controls, found that deinhibition had either a species-
specic response, or a greater effect than scarication, on germi-
nation success (Robertson et al. 2006, Traveset et al. 2007).
Therefore, the release of seeds from indehiscent pods may be an
underestimated service performed by white-tailed deer with a net
effect on plant regeneration. The dependence of plant regenera-
tion on the release of seeds from inhibition is poorly understood
and deserves further attention, especially in highly defaunated
ecosystems in which plants may be deprived of their dispersers.
DRY ECOSYSTEMS.Several studies report that woody species with
thick pods, dry brous pulp, and no apparent adaptations for ani-
mal dispersal, are frequently consumed by large herbivores (Gar-
dener et al. 1993, Granados et al. 2014). Similar results were
found in this study, suggesting a herbivore dispersal syndrome. Con-
trary to Janzen (1984), this may not be related to the foliage but
to diaspore characteristics (i.e., pods), mainly of Fabaceae species.
Apart from African savannas, where the relationship between Aca-
cia species and large African herbivores has been documented
(Tybirk 1997), a herbivore dispersal syndrome has rarely been consid-
ered for seed dispersal in NTDFs or other dry ecosystems. Yet, in
a recent review of seed dispersal and frugivory by large herbivores
in Asia, pods were a common fruit type among those consumed
by several herbivore families, especially elephants, bovids, and
large cervids (Sridhara et al. 2016). Thus, the herbivore dispersal
TABLE 2. Effect of white-tailed deer dispersal on germination.
Deviance table Parameters estimates
Model Residual df Deviance Pr(>X
) Fixed Factor Estimate SE z-Value P(>|z|)
Caesalpinia glabrata
NULL 174 Intercept 2.197 0.333 6.592 <0.001
Treatment 173 134.12 <0.001 Dispersed 4.64 0.54 8.58 <0.001
Chloroleucon mangense
NULL 1282 Intercept 1.82 0.29 6.30 <0.001
Treatment 1281 0.53 0.47 Dispersed 0.23 0.30 0.75 0.46
Senna mollissima
NULL 643 Intercept 2.94 0.46 6.42 <0.001
Treatment 642 2.15 0.14 Dispersed 0.85 0.54 1.56 0.12
Deviance table (left) of the GLMs performed. Treatment is a factor with two levels: Dispersed, seeds recovered from deer feces; and Control, seeds collected
from the trees. Note that degrees of freedom (df) differ among species according to the number of seeds used for testing the effects of deer dispersal. Parameter
estimates, standard errors (SE), and P-values are shown (right). Signicant effects are shown in bold.
FIGURE 3. Germination probability (mean SD) resulting from seeds dis-
persed and not dispersed by white-tailed deer.
6 Jara-Guerrero et al.
syndrome warrants further research; it may provide new insights
about why species previously considered as autochorous have been
surprisingly successful colonizers (Pakeman 2001, Jara-Guerrero
et al. 2015). Therefore, in our study area, white-tailed deer dispersal
might explain the random spatial distribution of Senna mollissima
(Jara-Guerrero et al. 2015), instead of the aggregated distribution
pattern expected for autochorous species. On the contrary, the
other species dispersed by white-tailed deer, previously classied as
autochorous, show the expected spatial pattern (Jara-Guerrero
et al. 2015). Furthermore, white-tailed deer could move seeds and
facilitate gene ow, but without modifying the aggregate distribu-
tion pattern. Other factors, such as differences in seed germination
and survival, might be related to these differences in the white-
tailed deer dispersal effects among species.
showed that white-tailed deer may disperse seeds matching the
description of megafauna fruits, those with traits that extinct mega-
fauna species would have consumed (Janzen & Martin 1982,
Guimar~aes et al. 2008). This is also supported by our results,
since species regularly dispersed by white-tailed deer were large,
brownish fruits, with dry brous pulp, usually indehiscent and
contained in thick pods (Janzen 1984, Janzen & Martin 1982,
Gautier-Hion et al. 1985). The large, eshy-fruited species occa-
sionally dispersed by white-tailed deer in this and previous studies
also match the megafauna fruits (Janzen 1985, Gonzalez-Espi-
nosa & Quintana-Ascencio 1986, Fragoso 1997, Arceo et al.
2005). Another trait related to the megafauna dispersal syndrome
is high availability of fruits on the forest oor (Janzen & Martin
1982). In this study, white-tailed deer dispersed seeds after peak
fruit fall, indicating those fruits were available on the ground.
White-tailed deer, together with tapirs, peccaries, and a handful
of other cervids, are the only extant Pleistocene megafauna in the
NTDF that may function as seed dispersers. These species pre-
sent unique evolutionary and morphological characteristics that
make them relevant and likely non-replaceable, from an ecological
functioning perspective (Malhi et al. 2016). Our ndings provide
further support to such a relevant and unique ecological role:
plants with larger diaspores are not adapted to other ways of dis-
persal, making white-tailed deer a conservation priority (Pires
et al. 2014). It has recently been suggested that medium to large
cervids may replace the ecological functions played by larger
megaherbivores, such as tapirs and elephants, at higher risk of
extinction and already gone in many ecosystems. This highlights
the conservation value of common and extant megafauna, such
as medium to large deer (Sridhara et al. 2016).
robustness of our data and the clear importance of white-tailed deer
as seed dispersers, we acknowledge that this study included only one
forest community. Accordingly, further research along the Neotrop-
ics should be performed to establish the generality of white-tailed
deer as an important seed disperser. This can also be extended to
other ecosystems in which megaherbivores are still present, as there
is a serious empirical gap in this respect. Clearly, further efforts
should try to unveil the dispersal networks established between
megaherbivores and fruiting plants, their functional traits, and the
ecological and evolutionary consequences of such interaction.
White-tailed deer effectively dispersed at least 11 native woody spe-
cies typical of NTDFs, about half of them were considered auto-
chorous. Species dispersed by white-tailed deer had fruit traits
matching the megafauna fruits, with large size and numerous seeds;
most of these were dry pods with brous pulp, which stay on the
oor for many months. This dispersal service is especially relevant
considering these fruits could not be dispersed by other means in
the study area. Even the plant species that suffered a decrease in
germination due to white-tailed deer gut passage seems to benet
from other dispersal services such as pod-release. Therefore, white-
tailed deer played a relevant ecological role in NTDFs by dispersing
viable seeds of a wide array of species, contributing to local recruit-
ment and long-distance dispersal. This is particularly important in
NTDFs, given their high levels of fragmentation and the possibility
of recovery in newly available niches resulting from climate change
(Cain et al. 2000, Miles et al. 2006). White-tailed deer are among the
few extant megafauna functioning as seed dispersers in the NTDF.
Consequently, white-tailed deer dispersal services and associated
ecological functions are likely unique.
This work was partially supported by project PROY_CCNN_1054
nanced by Universidad Tecnica Particular de Loja. The authors
thank Ministerio del Ambiente del Ecuador for facilities and opera-
tional support during eld work. GEA is grateful to the Prometeo
Program of the Ecuadorian National Secretariat for Education,
Science and Technology for the funding provided for her post-doc-
toral stay in Loja, Ecuador and further support during the period
of manuscript writing was provided by Spanish ministry for Science
(Juan de la Cierva-Formacion program). We are grateful to two
anonymous reviewers and the subject matter editor T. Carlo for
their valuable suggestions and comments.
Data available from the Dryad Repository:
5061/dryad.43d3g (Jara-Guerrero et al. 2017), and ambar: http://
Additional Supporting Information may be found online in the
supporting information tab for this article:
FIGURE S1. Map and location of the study area.
FIGURE S2. Monthly proportion of seed density in seed rain
and white-tailed deer feces for the four most abundant species in
white-tailed deer feces.
Seed Dispersal by White-Tailed Deer 7
TABLE S1. Fruit and seed traits of woody species in the 9 ha plot of
Arenillas Ecological Reserve.
TABLE S2. Number of feces collected each month and number of feces
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Seed Dispersal by White-Tailed Deer 9
... Large mammals, collectively, represent highly effective seed dispersers, due to their ability to disperse large seeds and high abundances of seeds (Tiffney and Mazer 1995;Escribano-Avila et al. 2014;Jara-Guerrero et al. 2018). Seed dispersal mutualism usually relies on guilds of animals, what Tiffney (2004) refers to as diffuse coevolution (Janzen and Martin 1982;Wenny 2001). ...
... Other studies have demonstrated that the loss of megafaunal dispersers results in a loss of seed dispersal and subsequently extinction or fragmentation of large-fruiting plant populations (Galetti et al. 2006Eriksson 2008;Malhi et al. 2016;Pires et al. 2018). Seed-dispersal studies consistently illustrate that perissodactyla (including rhinoceroses and tapirs) are far more likely to disperse large seeds and consume sugary fruits than true ruminants, notably artiodactyla (including cattle, deer, and their relatives), and are more readily featured in zoochory studies (Nathan et al. 2008;O'Farrill et al. 2013;Jara-Guerrero et al. 2018). Extensive research has also gone into the study of proboscidean seed dispersal rates (Kitamura et al. 2007;Campos-Arceiz et al. 2008;Harich et al. 2016;McConkey et al. 2018). ...
... Gnathic morphology suggests that many fossil apes in Europe were frugivorous, and few non-rosaceous fruiting trees would have been present on the landscape Dentil carries and use wear on fossil primate teeth from Eurasia suggest a high fruit-based diet, specifically of high-sugar fruits Other extinct mega-primates, such as Gigantopithecus and giant subfossil lemurs, appear to have been seed dispersers While there were other frugivores or opportunistic browsers on the late Miocene landscape, a significant portion of the herbivores were grazers Malus spp. maintain smaller seeds, possibly suggesting a disperser that had a restrictive digestive system Hominids of the Pleistocene onward maintained a close mutualistic relationship with large-fruiting Rosaceae, and it is likely that this trend stretches back in time is important in maintaining diversity and genetic connectivity within and across populations (Nathan and Muller-Landau 2000;Jara-Guerrero et al. 2018). Seed dispersal is also essential for colonization, especially in arboreal species (Escribano-Avila et al. 2014). ...
Full-text available
Extinct megafaunal mammals in the Americas are often linked to seed-dispersal mutualisms with large-fruiting tree species, but large-fruiting species in Europe and Asia have received far less attention. Several species of arboreal Maloideae (apples and pears) and Prunoideae (plums and peaches) evolved large fruits starting around nine million years ago, primarily in Eurasia. As evolutionary adaptations for seed dispersal by animals, the size, high sugar content, and bright colorful visual displays of ripeness suggest that mutualism with megafaunal mammals facilitated the evolutionary change. There has been little discussion as to which animals were likely candidate(s) on the late Miocene landscape of Eurasia. We argue that several possible dispersers could have consumed the large fruits, with endozoochoric dispersal usually relying on guilds of species. During the Pleistocene and Holocene, the dispersal guild likely included ursids, equids, and elephantids. During the late Miocene, large primates were likely also among the members of this guild, and the potential of a long-held mutualism between the ape and apple clades merits further discussion. If primates were a driving factor in the evolution of this large-fruit seed-dispersal system, it would represent an example of seed-dispersal-based mutualism with hominids millions of years prior to crop domestication or the development of cultural practices, such as farming.
... La evidencia señala que los frutos anacrónicos de los bosques tropicales estacionalmente secos (BTES), estuvieron potencialmente dispersados durante el Pleistoceno por megafauna extinta que incluye especies de las familias Gomphotheriidae, Equidae, Tayassuidae y Cervidae (Janzen & Martin, 1982;Lindsey & Lopez, 2015). Actualmente, algunos de estos frutos están siendo dispersados por el venado de cola blanca, Odocoileus virginianus Trouessart (Jara-Guerrero, Escribano-Avila, Espinosa, De la Cruz, & Méndez, 2018), los cuales se caracterizan por ser de tamaño grande, colores opacos, pulpa seca y fibrosa y, en muchos casos, sin adaptaciones obvias para la dispersión por animales (Janzen & Martin, 1982;Jara-Guerrero et al., 2018). Varias de estas características hacen que únicamente animales de gran tamaño puedan ofrecer los servicios de dispersión. ...
... La evidencia señala que los frutos anacrónicos de los bosques tropicales estacionalmente secos (BTES), estuvieron potencialmente dispersados durante el Pleistoceno por megafauna extinta que incluye especies de las familias Gomphotheriidae, Equidae, Tayassuidae y Cervidae (Janzen & Martin, 1982;Lindsey & Lopez, 2015). Actualmente, algunos de estos frutos están siendo dispersados por el venado de cola blanca, Odocoileus virginianus Trouessart (Jara-Guerrero, Escribano-Avila, Espinosa, De la Cruz, & Méndez, 2018), los cuales se caracterizan por ser de tamaño grande, colores opacos, pulpa seca y fibrosa y, en muchos casos, sin adaptaciones obvias para la dispersión por animales (Janzen & Martin, 1982;Jara-Guerrero et al., 2018). Varias de estas características hacen que únicamente animales de gran tamaño puedan ofrecer los servicios de dispersión. ...
... Las especies encontradas en las fecas fueron en su mayoría especies que tienen semillas con una testa dura y que pueden resistir el paso por el tracto digestivo (Jara-Guerrero et al., 2018). Al menos un 50 % de esas especies son leguminosas, todas con vainas indehiscentes, pero, además registramos la presencia de semillas de C. iguanaea y Z. thyrsiflora, ambas con frutos tipo drupa. ...
Full-text available
Introducción: Los bosques tropicales estacionalmente secos están sujetos a procesos de degradación crónica que ponen en riesgo su diversidad. La ganadería intensiva dentro de los remanentes de bosque se plantea como una de las principales causas de estos procesos de degradación. Sin embargo, el ganado también podría estar cumpliendo el rol de dispersor de semillas para algunas especies. Objetivo: Evaluar el rol de las cabras en la dispersión de semillas de especies leñosas y las posibles consecuencias de su comportamiento alimenticio sobre la estructura de la vegetación. Métodos: Entre diciembre 2016 y junio 2017 se recolectaron fecas de corrales (N = 38) y parcelas de vegetación (N = 42) de tres localidades de bosque seco en el Suroccidente de Ecuador. Todas las semillas encontradas en las fecas (N = 13 326) se registraron e identificaron taxonómicamente. Para evaluar el efecto de la ingestión de semillas sobre la germinación, se estableció un experimento de siembra de semillas extraídas de fecas procedentes de corrales y semillas recolectadas directamente de la planta. Resultados: Las cabras dispersaron 10 especies leñosas, de las cuales al menos el 50 % son leguminosas. Las semillas de Acacia macracantha representaron más del 70 % de semillas presentes en fecas de cabra. El paso de semillas por el tracto digestivo de las cabras mejoró significativamente el porcentaje y velocidad de germinación en Albizia multiflora, Piscidia carthagenensis y Ziziphus thyrsiflora, mientras que en Choroleucon mangense y Prosopis juliflora no se obtuvo germinación. No encontramos una correlación entre la riqueza de árboles establecidos y el número de especies encontradas en las fecas (χ² = -0.23, P = 0.53). La composición de especies de semillas dispersadas en las fecas no mostró una dependencia de la localidad, a pesar de que la composición de la vegetación establecida cambia entre localidades. La abundancia de semillas en las fecas no mostró relación con la abundancia de árboles en la vegetación establecida. Conclusiones: Las cabras pueden suplir en cierta medida el rol de otros ungulados localmente extintos, mejorando la germinación de especies de leguminosas con testa dura. Sin embargo, su comportamiento alimenticio y la alta dominancia en la dispersión de ciertas especies puede tener importantes efectos en la estructura de la comunidad.
... Evolutionary studies illustrate that mutualism often evolves from a predatory relationship [11,12]. In some cases, plants evolved sugar-rich fruits in order to recruit dispersers, and in other cases, dispersers were enticed by the green foliage that surrounded small, dry-fruited seeds. ...
... In plants, both intra-and interspecies gene flow push evolution forward [18,19]. As part of the gene flow system, seed dispersal allows plants to (i) avoid kin (sibling and parent) competition [20][21][22], (ii) avoid interspecific competition, (iii) reduce inbreeding [11,12], and (iv) colonize new areas [23][24][25]. Biotic dispersal can also lead to directed dispersal, targeting prime colonization areas and allowing greater offspring success rates than if dispersal were random [26]. ...
... Often these dense, clonally reproducing wild stands continue to produce extensive generations with energetically costly fruits, which then decompose under the trees, leading to density-dependent seed death through fungal attack, fermentation, seed predation from small animals, or parent/sibling competition. Large fruits coevolved with megafaunal mammals around the world [12,25], and humans are the most ubiquitous megafaunal mammal to survive the Pleistocene/Holocene boundary. The evolution of even larger fruits and larger seeds under human dispersal is substantially no different from the evolution of large fruits in response to proboscideans (notably gomphotheres), Xenarthra (e.g., Glyptodon spp., megalonychids, megatheriids), Perissodactyl (e.g., rhinoceroses, equids), or earlier large primates. ...
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It is well documented that ancient sickle harvesting led to tough rachises, but the other seed dispersal properties in crop progenitors are rarely discussed. The first steps toward domestication are evolutionary responses for the recruitment of humans as dispersers. Seed dispersal–based mutualism evolved from heavy human herbivory or seed predation. Plants that evolved traits to support human-mediated seed dispersal express greater fitness in increasingly anthropogenic ecosystems. The loss of dormancy, reduction in seed coat thickness, increased seed size, pericarp density, and sugar concentration all led to more-focused seed dispersal through seed saving and sowing. Some of the earliest plants to evolve domestication traits had weak seed dispersal processes in the wild, often due to the extinction of animal dispersers or short-distance mechanical dispersal.
... A O menor percentual médio de germinação obtido por sementes coletadas nas fezes dos caprinos, isto é, que completaram todo o trajeto pelo trato digestivo dos animais, em relação às sementes que foram regurgitadas, pode ser indicativo de uma maior exposição aos ácidos gástricos, que estariam danificando seus embriões (Mancilla, Fernández & Martín, 2012;Jara-Guerrero et al., 2018). Para as sementes regurgitadas, que chegam a atingir apenas o retículo dos ruminantes e retornam a boca, a exposição observada é inferior (Bell, 1958). ...
... As taxas de germinação das sementes, após passagem pelo trato gastrointestinal, seja completa ou não, são bastante variadas, resultado das características morfofisiológicas das próprias sementes, como a dureza do tegumento, tamanho e o tipo de dormência, quando presente (Fedriani & Delibes, 2009;Jara-Guerrero et al., 2018). Ademais, existe também o papel do animal dispersor, que pode apresentar distintas estratégias de consumo dos frutos e sementes (Fenner, 1985). ...
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Elevadas densidades de caprinos em florestas tropicais secas têm causado sérios problemas em relação ao recrutamento, crescimento, distribuição e capacidade regenerativa de plantas, especialmente para espécies endêmicas. Plântulas de Spondias tuberosa Arr. (umbu), uma frutífera endêmica da Caatinga e de grande importância sociocultural, estão escassas em virtude da alimentação destes animais. Apesar dessa problemática, uma eventual tarefa desses animais como dispersores de sementes em regiões mais defaunadas é desprezada. Diante disso, o objetivo do estudo foi avaliar o poder germinativo de sementes de umbuzeiro após passagem pelo trato gastrointestinal de caprinos. Sementes foram oferecidas a 13 caprinos, alojados em um pequeno cercado. Todas as sementes regurgitadas e as dispostas nas fezes foram coletadas. Sementes com escarificação física e controle também foram testadas. A taxa de recuperação de sementes foi de 69%. O percentual médio de germinação apresentou índices maiores para o tratamento das sementes regurgitadas quando comparado aos demais. O tempo médio de germinação, o índice de velocidade de emergência e a sincronia foram estatisticamente diferentes nas sementes escarificadas mecanicamente. As sementes de umbu consumidas por caprinos obtiveram um percentual de recuperação elevado especialmente pelo processo de regurgitação das mesmas, sendo responsável também pelo incremento porcentagem média de germinação da espécie. Apesar destes pontos, é necessário considerar o modo como as sementes são depositadas, que neste caso, é normalmente agregado, diminuindo as chances de estabelecimento da espécie em ambientes naturais, não podendo, portanto, considerá-lo como dispersor legítimo.
... In fact, seed dispersal by deer is hypothesized to have promoted the rapid migration north of forest forbs at the end of the last ice age, as well as their rapid recolonization of forests once cleared for agriculture in the 19th century (Vellend et al., 2003). Fruits dispersed by deer matched those of megafauna-dispersed fruits, with large size and numerous seeds; dry pods with fibrous pulp may remain available on the forest floor for long intervals (Jara-Guerrero et al., 2018). Seed dispersal by deer is likely a non-replaceable service, considering deer are the last wide-ranging animal capable of providing local recruitment and long-distance (5 km) dispersal (Jara-Guerrero et al., 2018). ...
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Natural disturbances are critical ecosystem processes, with both ecological and socioeconomic benefits and disadvantages. Large herbivores are natural disturbances that have removed plant biomass for millions of years, although herbivore influence likely has declined during the past thousands of years corresponding with extinctions and declines in distributions and abundances of most animal species. Nonetheless, the conventional view, particularly in eastern North America, is that herbivory by large wild herbivores is at unprecedented levels, resulting in unnatural damage to forests. Here, we propose consideration of large herbivores as a natural disturbance that also imparts many crucial ecological advantages, using white-tailed deer (Odocoileus virginianus), the only wild large herbivore remaining throughout the eastern U.S., as our focal species. We examined evidence of detrimental effects of browsing on trees and forbs. We then considered that deer contribute to both fuel reduction and ecological restoration of herbaceous plants and historical open forests of savannas and woodlands by controlling tree and shrub densities, mimicking the consumer role of fire. Similarly to other disturbances, deer disturbance 'regimes' are uneven in severity across different ecosystems and landscapes, resulting in heterogeneity and diversity. In addition to biodiversity support and fuel reduction, socioeconomic benefits include >$20 billion dollars per year by 10 million hunters that support jobs and wildlife agencies, non-consumptive enjoyment of nature by 80 million people, cultural importance, and deer as ecological ambassadors, whereas costs include about $5 billion and up to 450 human deaths per year for motor vehicle accidents, along with crop damage and disease transmission. From a perspective of historical ecology rather than current baselines, deer impart a fundamental disturbance process with many ecological benefits and a range of socioeconomic effects.
... The white-tailed deer (Odocoileus virginianus), a medium-size ungulate distributed from Canada to Bolivia (Gallina and Lopez-Arevalo 2016;Gallina et al. 2019), is an herbivorous ruminant browser, feeding mostly on leaves, twigs, sprouts, shrubs, and fruits (Gallina et al. 2010;Jara-Guerrero et al. 2018). In the tropics, this deer species is considered an opportunistic concentrate feeder (Gallina et al. 2010) that selects forest patches or areas with abundant and high-quality vegetation (López-Pérez et al. 2012), but whose diet and habitat selections change with seasons. ...
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Herbivores obtain nutrients mostly from the vegetation they consume, but may obtain additional minerals during periods of nutritional stress by consuming bones (osteophagia), a behavioral strategy that has been reported for many wild ungulate species, including the white-tailed deer (Odocoileus virginianus). Here we document multiple records (n = 183 camera-trap records) of osteophagia by white-tailed deer chewing sea turtle remains (resulting from jaguar [Panthera onca] predation) near a nesting beach in Santa Rosa National Park, Costa Rica during January-September 2017. Females with fawns, males with hard and velvet-covered antlers, and non-spotted fawns reached a peak of sea turtle bone consumption during June to August. We hypothesize that seasonality, sex, age, and individual growth stage influence the frequency of osteophagy as a strategy to cope with environmental changes and food resource scarcity. Finally, these observations highlight the role of an apex predator as indirectly influencing rare but important ecological processes.
... This suggests that the implementation of a system of rotation of fenced areas with periods of 8-15 years could lead to the installation and growth of new recruits with enough size to avoid being grazed and to guarantee local persistence, sustainability and conservation of this valuable forest species. Finally, it is important to note that while fencing promotes the regeneration of Bursera graveolens, it may hinder the regeneration of other important species such as Chloroleucon mangense, Senna mollissima, Piptadenia flava, and Caesalpinia glabrata, dispersed by ungulates (Jara- Guerrero et al. 2018), which are also favored by livestock grazing. In forests were these species coexist with Bursera graveolens, it could be necessary to implement alternative management measures. ...
Global change pressures are jeopardizing the functioning and structure of most tropical forests and clouding the future for their biodiversity and provided services. Although the impact of direct destruction through deforestation and fragmentation is currently in the research portfolio, overgrazing, which is more diffuse and generalized but chronic, especially in the seasonal dry forests, has been by far less addressed. Overgrazing can lead to a dramatic change in natural regeneration, often triggering the collapse of dominant species. The almost monospecific dry forests of Bursera graveolens, one of the most representative forest of the Tumbesian region, are on the verge of extinction due to both direct destruction and chronic overgrazing and regeneration collapse in forest remnants. Here, we evaluated the impact of a very simple measure, the installation of fences, on the regeneration of ecological processes affecting the dominant species. We mapped and measured all Bursera individuals with a height greater than or equal to 30 cm in six 1-ha plots, 3 within and 3 outside fenced areas. Using spatial point pattern analysis, we inferred the importance of demographic and ecological processes affecting adults and juveniles in fenced and unfenced areas. The spatial structure of adults was similar in fenced and unfenced areas, varying from random to aggregated patterns, showing that fences did not interfere with ecological processes affecting adult trees. On the contrary, we found 2765 juveniles in the three fenced plots but none in free ranging areas. Juveniles showed heterogeneous clustered patterns, and their distribution and growth were negatively influenced both by the presence and the height of adult trees. On average, there was an exclusion zone of 10 m around adult trees were recruitment of juveniles was limited. Competition among juveniles appeared to be negligible. All in all, these results suggest that, in addition to recruitment, two of the main mechanisms that rule tree population dynamics in tropical forests, i.e., dispersal limitation and a Janzen-Connell-like mechanism favoring recruiting far from adult trees have been immediately restored in the fenced area. This shows that fencing is a viable tool for a fast regeneration and conservation of Bursera forests.
... Mutualistic relationships for seed dispersal select for traits that allow seeds to move their offspring away from the parent plant, reducing parent-offspring and sibling-sibling competition (Howe and Miriti, 2000;Wang and Smith, 2002;Schupp et al., 2010;Tarszisz et al., 2018). Seed dispersal also reduces densitydependent mortality, a process linked to the Janzen-Connell Hypothesis (Nathan and Muller-Landau, 2000;Wang and Smith, 2002;Santamaría et al., 2007), interspecific competition (Garant et al., 2007), inbreeding depression (Nathan and Muller-Landau, 2000;Jara-Guerrero et al., 2018), and it promotes gene flow, diversification, adaptive evolution, and overall fitness (Eriksson, 2008). Seed dispersal allows for the colonization of new areas (Escribano-Avila et al., 2014), and dispersal by animals can increase the chance of seed deposition at ecologically favorable sites, what ecologists call directed dispersal (Eriksson, 2008). ...
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Megafaunal extinctions are recurring events that cause evolutionary ripples, as cascades of secondary extinctions and shifting selective pressures reshape ecosystems. Megafaunal browsers and grazers are major ecosystem engineers, they: keep woody vegetation suppressed; are nitrogen cyclers; and serve as seed dispersers. Most angiosperms possess sets of physiological traits that allow for the fixation of mutualisms with megafauna; some of these traits appear to serve as exaptation (preadaptation) features for farming. As an easily recognized example, fleshy fruits are, an exaptation to agriculture, as they evolved to recruit a non-human disperser. We hypothesize that the traits of rapid annual growth, self-compatibility, heavy investment in reproduction, high plasticity (wide reaction norms), and rapid evolvability were part of an adaptive syndrome for megafaunal seed dispersal. We review the evolutionary importance that megafauna had for crop and weed progenitors and discuss possible ramifications of their extinction on: (1) seed dispersal; (2) population dynamics; and (3) habitat loss. Humans replaced some of the ecological services that had been lost as a result of late Quaternary extinctions and drove rapid evolutionary change resulting in domestication.
... seed dispersal (Corlett, 2017;Jara-Guerrero, Escribano-Avila, Espinosa, De la Cruz, & Méndez, 2018;Paolucci et al., 2019), soil disturbance (Keuroghlian & Eaton, 2009;Pastor et al., 1998), nutrient deposition (Berzaghi et al., 2018), and seed and seedling predation (Bodmer, 2001;Keuroghlian & Eaton, 2008). In addition, forest ungulates act as long-distance links of forest processes such that their disappearance can have irreversible, negative effects on forest regeneration (Beck, Maurício, Duarta, & Reyna-Hurtado, 2016;Galetti, Bovendorp, & Guevara, 2015;Sobral et al., 2017;Villar et al., 2020). ...
en Much of what remains of the Earth's tropical forests is embedded within agricultural landscapes, where forest is reduced and fragmented. As native forest ungulates are critical to maintaining forest function, it is imperative to understand how this functional group responds to declines in forest cover and connectivity resulting from agricultural expansion. We addressed this issue by evaluating selection of forest cover and forest connectivity by a key native ungulate of Neotropical forests, the white‐lipped peccary (Tayassu pecari Link 1795, Tayassuidae, Cetartiodactyla), in agricultural landscapes of Brazil. We evaluated selection using compositional analysis at two hierarchical levels, landscape, and home range. From 2013 to 2019, we GPS‐tracked eight white‐lipped peccary herds in Southwest Brazil, resulting in a total of 14,460 GPS locations. We found that herds can live in landscapes with a wide range of forest cover (35%–81% of home ranges covered by native forest), with significant, but not strong, selection at the landscape level (p = .045). Nevertheless, herds strongly select for forest cover within their home ranges (81%–97% of locations within native forest; highly significant selection at the home‐range level: p = .008). As for connectivity, herds significantly select the largest, most connected forest fragments at the landscape level (p = .04), but not at the home‐range level (p = .07). Our results support that Neotropical forests within agricultural landscapes need to be well connected in order to preserve this key native ungulate and maintain long‐term forest function. Abstract in Portuguese is available with online material. RESUMO fr Grande parte das florestas tropicais da Terra ocorre em paisagens rurais. Ungulados são fundamentais na manutenção das funções das florestas tropicais, sendo essencial compreendermos melhor como este grupo de animais responde ao declínio e fragmentação destas florestas em paisagens rurais. Neste contexto, avaliamos a ocorrência e seleção por remanescentes florestais de uma espécie‐chave de ungulado nativo da região neotropical, a queixada (Tayassu pecari Link 1795, Tayassuidae, Cetartiodactyla), em paisagens rurais brasileiras. Avaliamos seleção através de Análise Composicional, em dois níveis espaciais, paisagem e área de vida. Entre 2013 e 2019, monitoramos oito bandos de queixadas por meio de telemetria de GPS, no sudoeste do Brasil, totalizando 14.460 localizações. Nossos resultados mostram que as áreas de vida variam bastante em proporção de cobertura florestal nativa (35%–81%), mas que ainda assim, ocorre seleção significativa por cobertura florestal nativa em nível da paisagem (p = .045) e ainda mais significativa dentro das áreas de vida (p = .008), com 81%–97% das localizações ocorrendo em floresta nativa. Não só os bandos selecionam cobertura florestal nativa como também selecionam matas mais conectadas, com seleção significativa em nível de paisagem (p=0.04), mas não dentro das áreas de vida (p = .07). Nossos resultados sugerem que a presença e conectividade das matas nativas é fundamental para manter esse ungulado chave em paisagens rurais neotropicais, bem como para garantir que as matas continuem saudáveis e sustentáveis em longo prazo.
... The increase in European rowan density in size class A could be caused by the improvement of seed dispersion and the germination processes facilitated by wild ungulates. Indeed, they are known to act as seed dispersal agents by eating fruits, which pass through their guts, and are released on the ground elsewhere (endozoochory) [47]. This dispersal mechanism is operational, particularly in autumn, when many species, such as European rowan, are fruiting. ...
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Forest ecosystems are threatened by different natural disturbances. Among them, the irruption of large herbivores represents one of the most alarming issues. Several local-scale studies have been carried out to clarify the mechanisms governing ungulate–forest interactions, to understand the effect of wild ungulates overabundance, and to apply conservation plans. However, information at large scales, over long periods of observation and from unmanipulated conditions is still scarce. This study aims to improve our knowledge in this field by using repeated inventories to investigate: the types of damage produced by ungulate populations on young trees, the drivers that stimulate browsing activity and its consequences on the specific composition of seedlings and saplings. To reach these goals, we used data collected during a twenty-year monitoring program (1994–2014) in the forests of Paneveggio-Pale di San Martino Nature Park (Italy). We applied descriptive statistics to summarize the data, GLMs to identify the drivers of browsing activity and Non-Metric Multidimensional Scaling (nMDS) ordinations to investigate the changes in specific composition of young trees across 20 years. We detected increasing browsing activity from 1994 to 2008 and a decline in 2014. Ungulates browsed preferentially in mature stands, and fed mostly on seedlings and saplings under 150 cm of height. The analysis of the environmental drivers of browsing pressure on the smallest size classes of plants suggests that foraging behavior is influenced by snowpack conditions, ungulate density and seasonality. Moreover, results underline the fact that ungulates feed mostly on palatable species, especially European rowan, but can also use unpalatable plants as emergency food under high competition levels. nMDS results suggest that rowan seed dispersion might be promoted by deer movements, however, saplings of this species were not able to exceed 30 cm of height because of heavy browsing. This bottleneck effect led to the dominance of unpalatable species, mostly Norway spruce, reducing diversity during forest regeneration. If prolonged, this effect could lead to a reduction of tree species richness, with cascading effects on many parts of the ecosystem, and threatening the resilience of the forest to future disturbances.
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Seed dispersal constitutes a pivotal process in an increasingly fragmented world, promoting population connectivity, colonization and range shifts in plants. Unveiling how multiple frugivore species disperse seeds through fragmented landscapes, operating as mobile links, has remained elusive owing to methodological constraints for monitoring seed dispersal events. We combine for the first time DNA barcoding and DNA microsatellites to identify, respectively, the frugivore species and the source trees of animal-dispersed seeds in forest and matrix of a fragmented landscape. We found a high functional complementarity among frugivores in terms of seed deposition at different habitats (forest vs. matrix), perches (isolated trees vs. electricity pylons) and matrix sectors (close vs. far from the forest edge), cross-habitat seed fluxes, dispersal distances and canopy-cover dependency. Seed rain at the landscape-scale, from forest to distant matrix sectors, was characterized by turnovers in the contribution of frugivores and source-tree habitats: open-habitat frugivores replaced forest-dependent frugivores, whereas matrix trees replaced forest trees. As a result of such turnovers, the magnitude of seed rain was evenly distributed between habitats and landscape sectors. We thus uncover key mechanisms behind "biodiversity-ecosystem function" relationships, in this case, the relationship between frugivore diversity and landscape-scale seed dispersal. Our results reveal the importance of open-habitat frugivores, isolated fruiting trees and anthropogenic perching sites (infrastructures) in generating seed dispersal events far from the remnant forest, highlighting their potential to drive regeneration dynamics through the matrix. This study helps to broaden the "mobile-link" concept in seed dispersal studies by providing a comprehensive and integrative view of the way in which multiple frugivore species disseminate seeds through real-world landscapes.
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Seed dispersal constitutes a pivotal process in an increasingly fragmented world, promoting population connectivity, colonization and range shifts in plants. Unveiling how multiple frugivore species disperse seeds through fragmented landscapes, operating as mobile links, has remained elusive owing to methodological constraints for monitoring seed dispersal events. We combine for the first time DNA barcoding and DNA microsatellites to identify, respectively, the frugivore species and the source trees of animal-dispersed seeds in forest and matrix of a fragmented landscape. We found a high functional complementarity among frugivores in terms of seed deposition at different habitats (forest vs. matrix), perches (isolated trees vs. electricity pylons) and matrix sectors (close vs. far from the forest edge), cross-habitat seed fluxes, dispersal distances, and canopy-cover dependency. Seed rain at the landscape-scale, from forest to distant matrix sectors, was characterized by turnovers in the contribution of frugivores and source-tree habitats: open-habitat frugivores replaced forest-dependent frugivores, whereas matrix trees replaced forest trees. As a result of such turnovers, the magnitude of seed rain was evenly distributed between habitats and landscape sectors. We thus uncover key mechanisms behind ‘biodiversity–ecosystem function’ relationships, in this case, the relationship between frugivore diversity and landscape-scale seed dispersal. Our results reveal the importance of open-habitat frugivores, isolated fruiting trees, and anthropogenic perching sites (infrastructures) in generating seed dispersal events far from the remnant forest, highlighting their potential to drive regeneration dynamics through the matrix. This study helps to broaden the ‘mobile link’ concept in seed dispersal studies by providing a comprehensive and integrative view of the way in which multiple frugivore species disseminate seeds through real-world landscapes.
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Dispersal is a key individual-based process influencing many life-history attributes and scaling up to population-level properties (e.g. metapopulation connectivity). A persistent challenge in dispersal ecology has been the robust characterization of dispersal functions (kernels), a fundamental tool to predict how dispersal processes respond under global change scenarios. Particularly, the rightmost tail of these functions, that is the long-distance dispersal (LDD) events, are difficult to characterize empirically and to model in realistic ways. But, when is it a LDD event? In the specific case of plants, dispersal has three basic components: (i) a distinct (sessile) source, the maternal plant producing the fruits or the paternal tree acting as a source of pollen; (ii) a distance component between source and target locations; and (iii) a vector actually performing the movement entailing the dispersal event. Here, I discuss operative definitions of LDD based on their intrinsic properties: (i) events crossing geographic boundaries among stands; and (ii) events contributing to effective gene flow and propagule migration. Strict-sense long-distance dispersal involves movement both outside the stand geographic limits and outside the genetic neighbourhood area of individuals. Combinations of propagule movements within/outside these two spatial reference frames result in four distinct modes of LDD. Synthesis. I expect truncation of seed dispersal kernels to have multiple consequences on demography and genetics, following to the loss of key dispersal services in natural populations. Irrespective of neighbourhood sizes, loss of LDD events may result in more structured and less cohesive genetic pools, with increased isolation by distance extending over broader areas. Proper characterization of the LDD events helps to assess, for example, how the ongoing defaunation of large-bodied frugivores pervasively entails the loss of crucial LDD functions.
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Habitat loss and subsequent fragmentation of natural habitats caused by anthropogenic activities constitute a major threat to biodiversity. A conservation strategy for habitat remnants is the creation of protected areas, although the size and connectivity of reserves may restrict the viability of populations. In this context, protected areas generate a "refuge effect", with an accumulation of species. However, long-term processes of species loss can be also triggered, generating widespread defaunation ("extinction islands"). In this paper we discuss the role of Arenillas Ecological Reserve (REA) in wildlife conservation of the Tumbesian dry forest. Specifically, we are interested in understanding the role of the reserve in the maintenance of mastofauna. For this purpose, we used 14 camera traps that were installed between August 2015 and February 2016. A total of 762 records of medium and large mammals of 12 species were recorded. Species richness was consistent with respect to the reserve size. We found no association between the occurrence of species and body size of species in the REA, yet other reserves of Ecuador do show this association. The difference in probability of presence of megafauna between reserves allows us to understand the processes that might be happening and how they affect the richness and composition of the mastofauna. Initially, although the REA is isolated from other Ecuador reserves, there are connections with northern Peru, allowing the maintenance of species that would have otherwise disappeared.
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Ecological communities are dynamic collections whose composition and structure change over time, making up complex interspecific interaction networks. Mutualistic plant–animal networks can be approached through complex network analysis; these networks are characterized by a nested structure consisting of a core of generalist species, which endows the network with stability and robustness against disturbance. Those mutualistic network structures can vary as a consequence of seasonal fluctuations and food availability, as well as the arrival of new species into the system that might disorder the mutualistic network structure (e.g., a decrease in nested pattern). However, there is no assessment on how the arrival of migratory species into seasonal tropical systems can modify such patterns. Emergent and fine structural temporal patterns are adressed here for the first time for plant-frugivorous bird networks in a highly seasonal tropical environment. Methods. In a plant-frugivorous bird community, we analyzed the temporal turnover of bird species comprising the network core and periphery of ten temporal interaction networks resulting from different bird migration periods. Additionally, we evaluated how fruit abundance and richness, as well as the arrival of migratory birds into the system, explained the temporal changes in network parameters such as network size, connectance, nestedness, specialization, interaction strength asymmetry and niche overlap. The analysis included data from 10 quantitative plant-frugivorous bird networks registered from November 2013 to November 2014. Results. We registered a total of 319 interactions between 42 plant species and 44 frugivorous bird species; only ten bird species were part of the network core. We witnessed a noteworthy turnover of the species comprising the network periphery during migration periods, as opposed to the network core, which did not show significant temporal changes in species composition. Our results revealed that migration and fruit richness explain the temporal variations in network size, connectance, nestedness and interaction strength asymmetry. On the other hand, fruit abundance only explained connectance and nestedness. Discussion. By means of a fine-resolution temporal analysis, we evidenced for the first time how temporal changes in the interaction network structure respond to the arrival of migratory species into the system and to fruit availability. Additionally, few migratory bird species are important links for structuring networks, while most of them were peripheral species. We showed the relevance of studying bird–plant interactions at fine temporal scales, considering changing scenarios of species composition with a quantitative network approach.
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The study of functional morphological traits enables us to know fundamental aspects of the dynamics of plant communities in local and global habitats. Regenerative morphological traits play an important role in defining plant history and ecological behavior. Seed and fruit characteristics determine to a large extent the patterns for dispersal, germination, establishment and seedling recruitment a given species exhibits on its natural habitat. Despite their prominent role, seed and fruit traits have been poorly studied at the community level of woody plant species in neo-tropical dry forests. In the present study we aimed at i) evaluate the functional role of morphological traits of seeds, fruits and embryo in woody plant species; ii) determine which are the morphological patterns present in seeds collected from the community of woody species that occur in neo-tropical dry forests; and iii) compare woody plant species seed mass values comparatively between neo-tropical dry and tropical forests. To do so, mature seeds were collected from 79 plant species that occur in the Tumbesian forest of Southwest Ecuador. The studied species included the 42 and 37 most representative tree and shrubbery species of the Tumbesian forest respectively. A total of 18 morphological traits (seven quantitative and 11 qualitative) were measured and evaluated in the seeds, fruits and embryos of the selected species, and we compared the seeds mass with other forest types. Our results showed a huge heterogeneity among traits values in the studied species. Seed mass, volume and number were the traits that vary the most at the community level, i.e. seed length ranged from 1.3 to 39 mm, and seed width from 0.6 to 25 mm. Only six embryo types were found among the 79 plant species. In 40 % of the cases, fully developed inverted embryos with large and thick cotyledons to store considerable amount of nutrients were recorded. We concluded that highly variable and functionally complementary morphological traits occur among the studied woody plants of the Tumbesian dry forest. The latter favors a plethora of behavioral mechanisms to coexist among woody species of the dry forest in response to the environmental stress that is typical of arid areas. Rev. Biol. Trop. 64 (2): 859-873. Epub 2016 June 01.
1.Dispersal is essential for species to survive the threats of habitat destruction and climate change. Combining descriptions of dispersal ability with those of landscape structure, the concept of functional connectivity has been popular for understanding and predicting species’ spatial responses to environmental change. 2.Following recent advances, the functional connectivity concept is now able to move beyond landscape structure to consider more explicitly how other external factors such as climate and resources affect species movement. We argue that these factors, in addition to a consideration of the complete dispersal process, are critical for an accurate understanding of functional connectivity for plant species in response to environmental change. 3.We use recent advances in dispersal, landscape and molecular ecology to describe how a range of external factors can influence effective dispersal in plant species, and how the resulting functional connectivity can be assessed. 4.Synthesis. We define plant functional connectivity as the effective dispersal of propagules or pollen among habitat patches in a landscape. Plant functional connectivity is determined by a combination of landscape structure, interactions between plant, environment and dispersal vectors, and the successful establishment of individuals. We hope that this consolidation of recent research will help focus future connectivity research and conservation.