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.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)

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

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).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51225, enero-diciembre 2023 (Publicado May. 04, 2023)

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.

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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