White-tailed deer as the last megafauna dispersing seeds in Neotropical dry forests: The role of fruit and seed traits

Abstract

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.

Full text

White-tailed deer as the last megafauna dispersing seeds in Neotropical dry forests:
the role of fruit and seed traits
Andrea Jara-Guerrero
1
, Gema Escribano-Avila
1,2,4
, Carlos Iv
an Espinosa
1
, Marcelino De la Cruz
3
,and Marcos M
endez
3
1
Departamento de Ciencias Biol
ogicas, Universidad T
ecnica Particular de Loja, CP.: 11-01-608 Loja, Ecuador
2
IMEDEA- Institut Mediterrani d’Estudis Avanc
ßats (CSIC-UIB), Esporles, Illes Balears, Spain
3
Departamento de Biolog
ıa y Geolog

ıa, F
ısica y Qu
ımica Inorg
anica,

Area de Biodiversidad y Conservaci
on, Universidad Rey Juan Carlos,
E-28933 Madrid, Spain
ABSTRACT
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 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.
Abstract in Spanish is available with online material.
Key words: anachronistic traits; deinhibition; dry fibrous pulp; germination; gut passage; herbivore; legume; megafauna fruits.
SEED DISPERSAL IS A KEY PROCESS IN THE LIFE OF A PLANT because
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 identified 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 0.4–1 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 find-
ings highlight the species-specific 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.
4
Corresponding author; e-mail: gema.escribano.avila@gmail.com
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.: Gonzalez-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
filter 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 specific 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?
METHODS
STUDY AREA.—We conducted this study at the Arenillas Ecolog-
ical Reserve (REA), located in El Oro province, Southwest
Ecuador (03°34015.44″S; 80°08046.15″E, 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 Pacific 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.
NATURAL HISTORY OF WHITE-TAILED DEER.—Odocoileus virginianus,
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 (50–120 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).
QUANTITATIVE DISPERSAL PATTERN:SEED DIVERSITY AND ABUNDANCE
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 identification of the dispersed seeds.
All seeds present in the feces were extracted by sample dis-
aggregation. We identified 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 flava 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 classified 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 & Perez-Ruız 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 filled 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 five 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 (N≥70, Table 1): Chloroleucon mangense,Caesalpinia glabrata,
and Senna mollissima. Our experiment assessed the scarification
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 Mann–Whitney 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 fisher.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 78–100 percent.
To evaluate the effect of scarification after gut passage on
seed germination, we fitted 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).
RESULTS
QUANTITATIVE DISPERSAL PATTERN:SEED DIVERSITY AND ABUNDANCE
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
five families (Table 1). We found up to five 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 flava (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. flava was most abundant.
CHARACTERISTICS OF THE FRUITS DISPERSED.—The most frequent
fruits dispersed by white-tailed deer were dehiscent legumes, 61–
250 mm in length and 13–20 mm in width with 8–15 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 flava 26 11/104
Senna mollissima 96 13/544
Vigna sp. 11 3/16
Cactaceae Unidentified 1 1/1
Convolvulaceae Unidentified 6 0/10
Primulaceae Bonellia sprucei 1 1/1
Rubiaceae Randia aurantiaca 2 0/7
Unidentified 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 Unidentified 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
3
, and in seed mass
from 0.016 to 0.176 g. Large-sized berries (length: 30–55 mm;
diameter: 17–40 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 confirmed
by the Fisher test, which indicated significant association between
fruit type and dispersal by white-tailed deer (Fig. 2). Mann–Whit-
ney tests showed significant 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.
GERMINATION AFTER WHITE-TAILED DEER GUT PASSAGE.—Eight out
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. flava, 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 unidentified Convolvulaceae species
did not germinate. We did not find any external damage on seeds
that failed to germinate.
No significant 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 significant reduction in germination capac-
ity (10% vs. 90%) for C. glabrata gut-passed seeds compared to
control seeds (Fig. 3; Table 2).
DISCUSSION
WHITE-TAILED DEER DISPERSAL PATTERNS IN NEOTROPICAL DRY
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 five 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 fibrous pulp but no apparent
adaptations for assisted dispersal and were previously considered
autochorous (Jara-Guerrero et al. 2011, Lopez-Martınez et al.
2013). Arceo et al. (2005) showed that species commonly dis-
persed by white-tailed deer fructified 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 &
Babinska-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 findings 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, Lopez-
Martınez 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 Benıtez-Malvido et al. 2003 and Hilje et al.
2015). Specialist frugivorous bats (Phyllostomidae) are rather
common in NTDF assemblages (4–10 species: Rıos-Blanco &
Perez-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 (fleshy 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
2012.
4 Jara-Guerrero et al.

and syconia, Ramos-Robles et al. 2016, Rıos-Blanco & Perez-
Torres 2015). In addition, the longer seed dispersal distances (up
to 3–5 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, Gonzalez-Varo et al. 2017, Jordano 2017), probably
make this species a relevant and complementary disperser of
NTDF plants.
INTERACTION BETWEEN WHITE-TAILED DEER AND FRUIT-SEED TRAITS:
THE IMPORTANCE OF THE DEINHIBITION EFFECT FOR INDEHISCENT
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 scarification, likely related
to seed size, and not to chewing. Herbivore body size and feed-
ing type (i.e., grazer or browser) greatly influence 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 scarifica-
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 first 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.
2005).
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 fleshy 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 beneficial deinhibiton effect resulting
from seed release of the dry, thick, fibrous pulp may offset the
excessive scarification, 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-
specific response, or a greater effect than scarification, 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.
AN UNGULATE DISPERSAL SYNDROME PREVIOUSLY OVERLOOKED IN
DRY ECOSYSTEMS.—Several studies report that woody species with
thick pods, dry fibrous 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
2
) 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). Significant 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 classified as
autochorous, show the expected spatial pattern (Jara-Guerrero
et al. 2015). Furthermore, white-tailed deer could move seeds and
facilitate gene flow, 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.
MEGAFAUNA DISPERSING MEGAFAUNA FRUITS.—Previous evidence
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 fibrous pulp, usually indehiscent and
contained in thick pods (Janzen 1984, Janzen & Martin 1982,
Gautier-Hion et al. 1985). The large, fleshy-fruited species occa-
sionally dispersed by white-tailed deer in this and previous studies
also match the megafauna fruits (Janzen 1985, Gonzalez-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 floor (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 findings 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).
LIMITATIONS AND FURTHER RESEARCH PRIORITIES.—Despite the
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.
CONCLUSIONS
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 fibrous pulp, which stay on the
floor 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 benefit
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.
ACKNOWLEDGMENTS
This work was partially supported by project PROY_CCNN_1054
financed by Universidad Tecnica Particular de Loja. The authors
thank Ministerio del Ambiente del Ecuador for facilities and opera-
tional support during field 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-Formacion program). We are grateful to two
anonymous reviewers and the subject matter editor T. Carlo for
their valuable suggestions and comments.
DATA AVAILABILITY
Data available from the Dryad Repository: https://doi.org/10.
5061/dryad.43d3g (Jara-Guerrero et al. 2017), and ambar: http://
ambar.utpl.edu.ec/dataset/deer-seed-dispersal.
SUPPORTING INFORMATION
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
with seeds.
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