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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)
Seed removal by the squirrel Notocitellus adocetus
(Rodentia: Sciuridae) in Western México
Daniel Flores-Alta1; https://orcid.org/0000-0002-1464-5868
Francisco Alberto Rivera-Ortiz2; https://orcid.org/0000-0002-5487-4817
Ana María Contreras González1*; https://orcid.org/0000-0003-4509-7865
1. Laboratorio de Ecología. Unidad de Biotecnología y Prototipos, Facultad de Estudios Superiores Iztacala. Avenida de
los Barrios 1, Los Reyes Iztacala, Tlalnepantla, Estado de México, México; danielfloresalta@gmail.com; *amcontre-
rasg@comunidad.unam.mx (*Correspondence).
2. Laboratorio de Ecología Molecular y Evolución. Unidad de Biotecnología y Prototipos, Facultad de Estudios
Superiores Iztacala. Avenida de los Barrios 1, Los Reyes Iztacala, Tlalnepantla, Estado de México, México; francisco.
rivera@iztacala.unam.mx
Received 18-VIII-2022. Corrected 13-XII-2022. Accepted 20-IV-2023.
ABSTRACT
Introduction: Seed dispersal and seed predation have important impacts on plant diversity and community
structure. Rodents participate in both of these types of interactions.
Objectives: To evaluate the removal of the seeds of Crescentia alata, Randia capitata, and Zea mays by the
squirrel Notocitellus adocetus to determine how it affects these plant species, by dispersing or preying on their
seeds.
Methods: We studied 14 individuals for C. alata, 24 for R. capitata, and for Z. mays 35 individuals. We observed
foraging and used camera traps to determine the part of the fruit (seed and/or pulp) consumed by the squirrels
and the amount of fruit or seed consumed. We also placed fine sand traps (FST) to measure the percentage of
seed removal. We quantified the fruits produced by the plant species studied and the percentage of damage
caused by N. adocetus throughout the plots.
Results: Notocitellus adocetus feeds on the seeds and pulp of C. alata and Z. mays. The species with the highest
removal rate and the highest percentage of damage was C. alata. Zea mays was the plant species that had the
highest percentage of removal from FST, the largest number of fruits, and the lowest percentage of damage. On
FST, R. capitata had the lowest seed remotion.
Conclusions: Notocitellus adocetus is considered a seed predator; however, due to its behavior and the charac-
teristics of the fruits of C. alata and R. capitata, this rodent could make the seeds available to secondary seed
dispersers.
Key words: tropical ground squirrel; Crescentia alata; Randia capitata; Zea mays; seed dispersal; seed preda-
tion; tropical deciduous forest.
RESUMEN
Remoción de semillas por la ardilla Notocitellus adocetus (Rodentia: Sciuridae) en el oeste de México.
Introducción: La dispersión y depredación de semillas tienen efectos importantes en la diversidad de plantas y
estructura de las comunidades. Los roedores participan en estos tipos de interacciones.
Objetivos: Evaluar la remoción de semillas de Crescentia alata, Randia capitata y Zea mays por la ardilla
Notocitellus adocetus, para determinar su efecto en estas especies de plantas, dispersando o depredando semillas.
https://doi.org/10.15517/rev.biol.trop..v71i1.51225
TERRESTRIAL ECOLOGY
2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)
INTRODUCTION
Ecological interactions can have positive,
negative, or neutral effects for the species
involved in them, and they play a crucial role
in the structure and organization of communi-
ties (Bertness & Callaway, 1994; Perea et al.,
2013). In the dispersal cycle of plants, there
are positive interactions with animals such as
seed dispersal, and negative interactions such
as seed predation (Howe, 1986; Howe & Small-
wood, 1982; Janzen, 1971b). These interactions
can affect the plant and animal populations
involved; on the one hand, they play a role in
maintaining the seed bank and, therefore, in
seed distribution in the environment, so that
the interactions have impact the recruitment of
plants and thus affect their fitness. While on the
other, animals depend on the resource provided
by plants for their survival (Howe & Small-
wood, 1982; Janzen, 1971b; Louda, 1989).
These interactions occur with very high fre-
quency, so their effects have consequences on
plant demography and genetic diversity and are
critical in the maintenance and plant diversity
(Calvino-Cancela, 2007; Howe & Smallwood,
1982; Janzen, 1971b; Jordano & Godoy, 2000;
Wang & Smith, 2002).
Animals, as small invertebrates to large
mammals, are agents involved in seed removal
(Howe & Smallwood, 1982;. Janzen, 1971b;
Martínez-Orea et al., 2009). Rodents are con-
sidered seed dispersers (Acevedo-Quintero &
Zamora-Abrego, 2016; Ouden et al., 2005;
Sunyer et al., 2013; Xiao et al., 2006), and seed
predators (DeMattia et al., 2006; Galetti et al.,
2015a; Ibáñez & Soriano, 2005; Janzen, 1971b;
Traveset et al., 2009). Rodents are important
in communities; by excavating and building
their burrows, they provide benefits to eco-
systems, such as water infiltration, improved
soil texture, and changing the level of available
nutrients, making soils more heterogeneous
(Ewacha et al., 2016; Reichman & Seabloom,
2002; Zhang et al., 2003), increasing landscape
variability, and maintenance of species rich-
ness in changing environments (Brown et al.,
2001; Davidson & Lightfoot, 2008; Reichman
& Seabloom, 2002; Valkó et al., 2021; Zhang
et al., 2003).
However, the environment has a problem
around the world, which is the high social
importance (Blackie et al., 2014), as a land-use
change that caused habitat fragmentation and
altered the original vegetation structure (Emer
et al., 2018; Haddad et al., 2015). Approxi-
mately 90 % of the tropical deciduous for-
est (TDF) in the world has been altered by
agriculture or ranching (Banda et al., 2016),
which increase rodent densities, since these
organisms obtain their food more efficiently
in farmlands (Castillo-Castillo & González-
Romero, 2010; Galetti et al., 2015a), where
they can be considered pests (Elias & Valencia,
1984; Villar-González, 2000). In México, for
example, crops including corn, sorghum, rice,
Métodos: Estudiamos 14 individuos de C. alata, 24 para R. capitata y 35 individuos para Z. mays. Observamos
el forrajeo y usamos cámaras trampas para determinar la parte del fruto (semilla y/o pulpa) consumida y la inten-
sidad de consumo por las ardillas. También colocamos trampas de arena fina (FST) para medir el porcentaje de
remoción de semillas. Cuantificamos los frutos producidos por las especies estudiadas y el porcentaje de daño
ocasionado por N. adocetus, mediante parcelas.
Resultados: Notocitellus adocetus se alimenta de las semillas y pulpa de C. alata y Z. mays. La especie que tuvo
mayor tasa de remoción y mayor porcentaje de daño fue C. alata. La especie con mayor porcentaje de remoción,
mayor número de frutos y menor daño en las FST fue Z. mays. En las trampas de arena fina, R. capitata tuvo la
menor remoción de semillas.
Conclusiones: Notocitellus adocetus es considerada depredadora de semillas, no obstante, por su comportamien-
to y las características de los frutos de C. alata y R. capitata, este roedor podría dejar disponibles las semillas a
dispersores secundarios de semillas.
Palabras clave: ardilla tropical del suelo; Crescentia alata; Randia capitata; Zea mays; dispersión de semillas;
depredación de semillas; bosque tropical caducifolio.
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beans, sugarcane, coconut, and squash are
affected by rodents (Bello & Hidalgo, 2009;
Brooks & Fiedler, 2001; Panti-May et al., 2017;
Villar-González, 2000). The land-use change
causes species loss due to migrations to vegeta-
tion patches or agricultural areas and even the
local extinction of native species. In addition,
this species loss induces a decrease in ecologi-
cal functions, including interactions between
plants and animals (Bolger et al. , 1997; Galetti
et al., 2015b; Marjakangas et al., 2020).
In Western México, Notocitellus adocetus
is a terrestrial squirrel, an endemic rodent spe-
cies (Flores-Alta et al., 2019; Valdés & Cebal-
los, 2014), considered a pest by people who
refer that squirrels cause damage to their crops;
for this reason, they kill individuals of this spe-
cies. This human activity can change commu-
nity structure and ecological functions derived
from land-use change; therefore, it is essential
to know the role of the N. adocetus in the envi-
ronment to determine conservation strategies
for this species. So, the question for this work
was, what role does N. adocetus play in seed
removal on three plant species? Then the aim
of the present study was to evaluate the removal
by N. adocetus of C. alata, R. capitata, and Z.
mays seeds to determine whether this squir-
rel species participates in seed dispersal and/
or seed predation. Also, evaluate the rodents
impact on these plant species to know the
importance of this species on the environment.
MATERIALS AND METHODS
Species: Notocitellus adocetus belongs
to the Sciuridae family, has terrestrial habits
and is known locally as the “cuinique”, it is
commonly referred to as the tropical ground
squirrel and is endemic to Western México
(Flores-Alta et al., 2019; Valdez, 2003).
The three plant species studied were cho-
sen because they are the most consumed by
N. adocetus in the locality of Cuambio, Guer-
rero (Flores-Alta et al., 2019). Also, in TDF
only these species had fruit during the study.
The seed of Z. mays is an important seed con-
sumed by humans, to which N. adocetus causes
economic losses, for this reason the people
kill them.
Crescentia alata and R. capitata are wild
TDF species, whose fruit production occurs
during the dry season. Zea mays is the most
cultivated species in the region (Duque, 2016
personal communication) and produce fruit at
the end of the rainy season.
Crescentia alata (Bignoniaceae) (Cirián/
Mexican Calabash) is a tree from 6.96 ± 0.92
height (Table 1), has an indehiscent fleshy fruit
measuring 7 to 15 cm diameter, with a hard
shell, has seeds from 0.6 to 1 cm long (Briones-
Salas et al., 2006; CONABIO, 2020; Flores-
Alta, 2018; Janzen & Martin, 1982). The fruits
of this species are consumed by rodents (Lio-
mys salvi) in Costa Rica (Janzen, 1982). Rand-
ia capitata (Rubiaceae) (Tecuche or Cruceta) is
a tree from 3.67 ± 0.15 m height (Table 1), has
indehiscent globose berry fruits measuring 5
cm in diameter, with a hard shell (Felger et al.,
2012; Flores-Alta, 2018), has seeds from 0.79
± 0.03 cm long and 0.63 ± 0.2 cm wide (Obs.
pers.). Zea mays (Poaceae) (corn) is an herb
with caryopsis-type fruits that together form
an ear; the seed size measure 0.55 to 0.95 cm
long and 0.3 to 0.7 cm wide (Espinosa-García
& Sarukhán, 1997; Quiroz, 2019).
Study area: The study site
is in the Northwest of the state of
TABLE 1
Number and size of individuals of C. alata and R. capitata in tropical dry forest plots.
Species Number of
individuals Height (m) DBH (cm) Coverage
individual (m2)Coverage (m2)Coverage (%)
C. alata 0.33 ± 0.16 6.96 ± 0.92 51.82 ± 92.61 49.75 ± 27.01 83.13 ± 22.93 2.77
R. capitata 11.66 ± 2.56 3.67 ± 0.15 5.39 ± 0.52 4.84 ± 0.89 262.16 ± 0.62 8.73
DBH = Diameter at breast height.
4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)
Guerrero, in the municipality of Zirándaro
de Los Chávez in the locality of Cuambio,
at coordinates (18°26’28.54”-18º26’06.63” N
& 101°01’21.68”-100º59’39.56” W), between
209 and 324 m.a.s.l. (Flores-Alta et al., 2019).
The mean annual temperature is 28.4 °C, and
the mean annual rainfall is 977.2 mm, with a
dry season lasting eight months (CONAGUA,
2020). The vegetation type is TDF, with areas
that have suffered land-use change on the
alluvial terraces. Some sites are used to farm
seasonal and irrigation-based crops including
corn, sorghum, sesame, and to a lesser extent,
mango, watermelon, plum, pumpkin, cucum-
ber, tomato, chili, hibiscus, and beans. In the
same way, there are areas dedicated to cattle
grazing (Mendoza, in prep.). The extension of
the study area in the TDF was 6.45 ha, while
in the corn crops was 7.45 ha, and the distance
between the two areas was 1.9 km.
For each plant species, we carried out one
sampling period during each sampling month,
which were selected based on when fruits are
produced. For Z. mays, this was in September
and October 2016, for C. alata in January,
March, and May 2017, and in January and
March 2017 for R. capitata. Each sampling
lasted three days at two sites. For each of the
plant species, we made direct observations
at fixed points daily (Altmann, 1974) dur-
ing the peak activity periods of N. adocetus
(9:00-14:00 h) (Flores-Alta et al., 2019). Three
observers remained still at different points at a
distance of ten to 15 m from the focal plants
so as not to disturb the activity of the squirrels
and observed their behavior using 10X42 bin-
oculars (Bushnell and Alpen). Each observer
attended from one to three focal individuals
of C. alata (1.32 ± 0.09 individuals), with 14
individuals observed in total, for R. capitata we
observed five to nine individuals (6 ± 1.77 indi-
viduals), with 24 individuals observed in total,
and for Z. mays for each observer was attended
from seven to ten individuals with 35 individu-
als observed in total (8.3 ± 0.88 individuals).
The total observation time for each spe-
cies was 32.25 h for C. alata, 50.06 h for R.
capitata, and 49.66 h for Z. mays. The lower
total observation time of C. alata is due to the
lower number of individuals (Table 1) in the
study area.
To complement the foraging observations,
we placed three digital camera traps (Bushnell
Trophy cam HD, Essential E2) near three focal
individuals of each of the plant species for
three consecutive days (Trolliet et al., 2014).
The cameras were focused on open fruits
located on the ground in the case of C. alata
and R. capitata, while in the case of Z. mays,
we placed fruits on the ground. The cameras
were programmed to film 60 s videos, which
were reviewed in the laboratory. During the
foraging observations and videos, we noted the
part of the fruit consumed (pulp and/or seeds),
stage of development (ripe or immature), num-
ber of feeding observations recorded, number
of seeds consumed, number of individuals of
N. adocetus feeding per event, time foraging
(Contreras-González & Arizmendi, 2014), for-
aging behavior (consumption of seeds in situ
or storage in cheek pouches), as well as their
behavior and movements after feeding (e.g. to
their burrows or places with better visibility,
such as rocks).
To quantify the number of seeds that N.
adocetus removes and determine its impact on
the three plant species studied, we quantified
the percentage of seed removal. For this, we
placed six fine sand traps (FST) per species
per sample close to the parent plant (1.5 m dis-
tance), with a minimum of 15 m between traps.
We set the traps before the squirrel’s activity
period in the morning, and we checked them
at the end of this activity for two consecutive
days. The trapping method consisted of clear-
ing a 1m2 area of litter and vegetation for each
trap and placing a layer of fine sand so that
the squirrels would leave tracks in the sand
when removing the seeds (Giraldo & Moreno,
2011). We put 40 seeds previously obtained
from mature fruits at the center of each FST.
For FST containing N. adocetus tracks, we
quantified the number of seeds removed for
each plant species and expressed these data as a
percentage. We identified N. adocetus tracks by
comparing tracks left in the FST to the tracks
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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)
of Mexican Ground Squirrel (Spermophilus
mexicanus) and Rock Squirrel (S. variegatus)
in the Mexican wild mammal tracking guide
(Aranda, 2012; N. adocetus are not described in
the guide). There is little chance of misidentify-
ing tracks as belonging to N. adocetus, since no
similar squirrels are distributed in the area.
Fruit abundance and damage: Because
the abundance of resources available in the
environment influences seed removal (Izha-
ki, 2002; Ortiz-Pulido et al., 2007; Wästljun,
1989), we quantified the resources available for
N. adocetus. During each sampling in the TDF,
we randomly placed three 50 x 20 m plots in
which we quantified the number of individuals
and the number of fruits per individual of each
of the two plant study species. When fruits
were too numerous to efficiently count directly,
we estimated the number of fruits by multiply-
ing the average fruit count from three branches
by the total number of branches per individual
(Chapman et al., 1992; Contreras-González
et al., 2009). In addition, to know the height,
coverage, and space occupied by the individu-
als of C. alata and R. capitata, we measured
the diameter at breast height (DBH), the height
of the individuals, and the coverage for each
individual using the ellipse formula to estimate
the percentage that each species occupies in the
sampled space, since these variables influence
fruit production (Chapman et al., 1992). In the
case of Z. mays, we reduced the plot size to
5 x 5 m due to the high density of plants. We
quantified the total number of individuals and
the number of fruits per individual.
We also quantified the number of fruits
with damage caused by N. adocetus (bites,
partially opened fruits, or partially consumed
fruits; Fig. 1), identifying the source of damage
with the help of a person from the Cuambio
locality who has observed squirrel activity for
many years. We estimate the percentage of
damage by dividing the number of damaged
fruits by the total fruits in the plot.
We applied Shapiro-Wilk normality tests
to all the data obtained to determine whether
the data conformed to parametric assumptions
(Zuur et al., 2009). Because we did not observe
N. adocetus feeding on R. capitata in direct
observations or camera trap videos, analyses of
some data included only C. alata and Z. mays.
We applied a Wilcoxon test to determine
whether the number of squirrels feeding on
the fruits differed between C. alata and Z.
mays. We calculated the rate of seed removal
to evaluate the intensity with which a squirrel
consumes the seeds from C. alata and Z. mays
by dividing the number of seeds consumed by
the time that squirrels spent foraging. We used
a generalized linear model (GLM) test with a
Poisson error distribution to determine whether
the rate of seed removal of N. adocetus differed
between these species (Zuur et al., 2009).
Fig. 1. Fruits of C. alata A. and B. R. capitata, C. and D.
and Z. mays, E. damaged by N. adocetus.
6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)
To evaluate the differences in the percent-
age of seeds removed in the FST among the
three species studied in the different months
sampled, we used a generalized linear mixed
model (GLMM) with a Poisson distribution
(Zuur et al., 2009), with percentage of seed
removed as the dependent variable, and time
and species as independent variables. We ana-
lyzed the wild TDF species separately from the
corn crops because human management influ-
ences fruit production in corn crops (Nadal,
1999). For this analysis, we used a linear mixed
model (LMM) for the TDF species, with fruit
abundance as the dependent variable, and time
and species as independent variables and a
GLM with a Poisson distribution for the corn
crops (Zuur et al., 2009), with crop size as
dependent variable, and time as independent
variable. In addition, due to pseudoreplication,
we applied a GLMM analysis with a Poisson
distribution to examine differences in the per-
centage of damaged fruits between the studied
species (Zuur et al., 2009).
RESULTS
We found that N. adocetus feeds on the
pulp and seeds of ripe and immature fruits of C.
alata and Z. mays (Table 2). We did not record
squirrels feeding on R. capitata, though we did
observe fruits of R. capitata and C. alata with
marks from N. adocetus (Fig 1A, Fig. 1B, Fig.
1C, Fig. 1D). Also, we observed individuals
of N. adocetus opening fruits of C. alata by
making a hole in the hard shell, from which
they extracted pulp and seeds. Squirrels fed on
seeds of C. alata and Z. mays in situ, taking
seeds with their hands, opening them with their
teeth and consuming the embryo, leaving only
the seed coat. Some seeds were carried in the
cheek pouches to their burrows or to later feed
in areas with greater visibility (e.g., on rocks,
protruding roots, or dry logs). We observed
1.14 (± 0.06) individuals feeding on 6.47 (±
1.15) seeds of C. alata per visit, while for Z.
mays we observed 1.02 (± 0.02) individuals
feeding (Wilcoxon = 381, P > 0.05). Squirrels
removed more C. alata (removal rate) (13.60 ±
0.24 seeds / minute) seeds per minute than Z.
mays seeds (10.42 ± 0.84 seeds / minute) (X2 =
2.55, d.f. = 22, P < 0.05; Table 2).
In the FST, N. adocetus removed seeds
from all three study species. The highest seed
removal was from Z. mays (43.43 ± 4.88 %;
X2= 14.89, d.f. = 122, P < 0.05), followed by C.
alata (29.5 ± 6.15 %), and finally R. capitata
(23.17 ± 8.41 %) (Table 2).
In terms of resource abundance, in the TDF
plots C. alata had higher height and DBH and
more coverage than R. capitata (Table 2). How-
ever, in the sampled area, C. alata occupied a
lower percentage of the area than R. capitata
(2.77 % and 8.73 %, respectively) and there
were fewer individuals of C. alata than R. capi-
tata (0.33 ± 0.16 and 11.66 ± 2.56 individuals
respectively (Table 2). For C. alata, we found a
larger number of fruits per hectare than for R.
capitata. C. alata had higher fruit abundance
in March than in January and May, while R.
capitata had similar fruit abundance between
January and March, and we did not record
fruits in May (Fig. 2A, LMM = 11.68, d.f. = 74,
TABLE 2
Species eaten by N. adocetus in TDF and corn crops.
Species Part eaten and stage
of ripenessaFOR SF FT (min) CR (seed/min) RFST % Month
C. alata rp, pl, se 103 1.14 ± 0.06 6.47 ± 1.15 13.06 ± 0.24 29.5 ± 6.15 Jan, Mar, May 2017
R. capitata rp, pl, se 0 0 UN UN 23.17 ± 8.41 Jan, Mar 2017
Z. mays rp, unrp, dr, pl, se 61.02 ± 0.02 UN 10.42 ± 0.84 43.43 ± 4.88 Sep, Oct 2016
In part eaten and stage of ripeness: rp = ripe, unrp = unripe, dr = dry, pl = pulp, se = seed; FOR = number of feeding
observations records; SF = number of squirrels feeding per event; FT = time foraging per event observed; CR= consumption
rate; RFST = percentage seed removal in fine sand traps; UN = unidentified).
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P < 0.05). In the corn crops we recorded more
fruits in September than in October (Fig. 2B,
X2 = 6.07, d.f. = 14, P < 0.05).
Based on the number of available fruits of
the studied plant species, we found that the per-
centage of fruits damaged by N. adocetus was
highest for C. alata (38.74 ± 11.92 %), while
for R. capitata it was 10.34 % (± 5.75) and for
Z. mays was 5.16 % (± 2.55; GLMM= 1.82, d.f.
= 74, P > 0.05).
DISCUSSION
Notocitellus adocetus feeds on the pulp
and embryo of the seeds of C. alata and Z.
mays, which indicating that this rodent is a seed
predator (Janzen, 1971b), as is the case of the
other squirrels in tropical forests (Notosciurus
granatensis, Sciurus variegatoides, S. colli-
aei y S. ingrami) (Acevedo-Quintero et al.,
2018; Henn, et al. 2014; Herrerías-Diego et
al., 2008; Janzen, 1971a). In addition, when
N. adocetus fed on C. alata, it scared away
reptiles and birds, and some members of these
groups are considered seed dispersers (Howe
& Smallwood, 1982; Valido & Olesen, 2007).
However, when squirrels feed on C. alata, the
iguana Ctenosaura pectinata scares them away.
Members of the Iguanidae family have been
described as seed dispersers, increasing the
reproductive success of some plants (Traveset,
1990; Vásquez-Contreras & Ariano-Sánchez,
2016), which can influence the seed dispersal
from C. alata.
One of the feeding behaviors we observed
was that N. adocetus made a hole in the tough
outer shell of C. alata through which it extract-
ed the pulp and seeds. This behavior has also
been described in the squirrel S. variegatorides
in Costa Rica, which can spend up to 15 min
making the hole in the fruit, then extracts the
pulp in pieces and feeds on the seeds (Janzen,
1982). The characteristics of C. alata and R.
capitata fruits, such as a thick, hard covering,
make it difficult for other organisms to access
the seeds. In addition, when the fruits of C.
alata fall to the ground and mature, the seeds
can die due to desiccation when not opened
(Janzen, 1982). Therefore, N. adocetus, by
breaking the fruits of C. alata and R. capi-
tata, plays an important role since it makes the
seeds available to seed dispersers, as occurs for
the plant species Heteroflorum sclerocarpum
(Urrea-Galeano & Andresen, 2018). Similar
dynamics have been described for the squirrels
S. granatensis, Microsciurus mimulus, and the
rat, Proechymys sp., which make the seeds of
Oenocarpus bataua available to seed dispersers
(Rojas-Robles et al., 2012).
Notocitellus adocetus removed a higher
percentage of C. alata seeds in the FST, influ-
encing negatively on this plant species (Vander-
Wall et al., 2005). However, this rate of removal
is lower than chipmunks Tamias amoenu, which
can consume a seed per second (Vander-Wall,
1994). Seed removal by N. adocetus in the TDF
Fig. 2. Abundance of fruits per hectare in study plots in C.
alata and R. capitata in tropical dry forest plots A. and in
B. Z. mays in plots in corn fields.
8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)
and the corn crops is lower compared to other
rodent species, since has been described seed
removal by rodents for the forest 96 % of seed
removal, and in agroforestry systems 76 %
(Escobar et al., 2020; Li & Zhang, 2007). This
indicates that the effects of N. adocetus on the
plant species consumed are likely less severe
than other rodent species, which can be useful
for conservation programs for this species.
Individuals from N. adocetus feed on fruits
and seeds of C. alata and Z. mays in situ.
However, some seeds are carried in their cheek
pouches to their burrows or to places with bet-
ter visibility to continue feeding. This behavior
could lead to some seeds being dispersed when
they are dropped during transport or feeding
(Gottfried, 1987). Moreover, outside burrows
of N. adocetus, we found empty fruits of R.
capitata with holes (Fig. 1D); the same feed-
ing behavior has been reported for this squir-
rel species when it feeds on H. sclerocarpum
(Urrea-Galeano & Andresen, 2018). Squirrels
can store seeds temporarily in their burrows,
which can even germinate when squirrels fail
to find and eat all of the seeds they have
cached (Steele et al., 2015; Vander-Wall, 1994;
Vander-Wall, 2003; Zong et al., 2010). How-
ever, the absence of large seed dispersers due
to fragmentation has led to a loss of ecological
interactions and an increase in rodent popula-
tions, such that seeds are deposited mainly in
an aggregate manner (Marjakangas et al., 2020;
Rojas-Robles et al., 2012), which may affect
plant populations (Hulme, 1998; Hulme, 2002).
We found that Z. mays had the highest
abundance of fruits of the three species stud-
ied, which influences that more seeds of this
species are removed (Elmouttie, 2009; Kelrick
et al., 1986). There is a higher density of squir-
rels in the corn crops (Flores-Alta et al., 2019),
which increases the intensity of seed predation
(Gharnit et al., 2020; Minor & Koprowski,
2015). This is similar to what occurs with the
mouse Peromyscus leucopus, in which seed
predation increases with increasing population
density (Ostfeld et al., 1997). In addition, when
resource abundance is high in a small area,
rodents do not have to move long distances to
acquire resources, so they are less exposed to
predators (Hannon et al., 2006).
Although total seed removal was higher
in corn crops than in the forest species, the
percent damage in plots of Z. mays was low.
Conversely, C. alata had higher percent dam-
age, although the density of squirrels is lower
(Flores-Alta et al., 2019). Nevertheless, in
sub-deciduous forests, the intensity of seed
predation by rodents is less intense than in frag-
mented sites (Fleury & Galetti, 2006), since
fragmented areas do not present the appropriate
conditions for the rodents’ predators. In addi-
tion, squirrels have better visibility to detect
predators when they feed in fragmented areas
than in forests (Fleury & Galetti, 2006; Hannon
et al., 2006; Herrerías-Diego et al., 2008).
Due to the interactions present in the
environment, it is necessary to observe the
ecological and evolutionary history of the plant
species. Unfortunately, there is no information
for R. capitata. However, C. alata has been
described as having a rare adaptation to survive
and avoid seed predation which makes the fruit
inaccessible to most animals. Members of the
now extinct proboscidean family Gomphotheri-
idae were proposed as their previous dispersers
(Janzen & Martin, 1982). Once the members
of this family became extinct, other organisms,
such as horses, dispersed the seeds (Janzen,
1982). However, these organisms could not be
considered seed dispersers in the study area in
the TDF since their distribution is restricted
to farmlands and grazing lands and is hardly
found in the TDF. So that is necessary to carry
out studies from seed dispersal for both species.
We conclude that N. adocetus is a seed
predator of the three species studied, which can
decrease or regulate the populations of these
plant species; however, the intensity of seed
predation is not a result of the number of fruits.
Nevertheless, the characteristics of sites in
TDF, such as the proximity to areas dedicated
to farmland and grazing land can influence seed
predation, so it would be essential to carry out
a study that quantifies the predation of seeds in
conserved areas far from disturbed areas.
9
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)
Ethical statement: the authors declare
that they all agree with this publication and
made significant contributions; that there is
no conflict of interest of any kind; and that we
followed all pertinent ethical and legal proce-
dures and requirements. All financial sources
are fully and clearly stated in the acknowled-
gements section. A signed document has been
filed in the journal archives.
ACKNOWLEDGMENTS
We thank Irais Duque Díaz, Marleth S.
Mendoza Orozco, Edgar Yafhed Martínez,
Osman Rogelio Díaz González and David
Adolfo Mota Aldrete and Hernández for help
doing field work. We also thank Sergio Díaz
Infante Maldonado and María Felix Ramos-
Ordoñez for lending digital cameras traps.
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