ISSN 2477-9458
BOLETÍN DEL
CENTRO DE
INVESTIGACIONES
BIOLÓGICAS
Sesonal damage by red squirrels (Notosciurus granatensis
Humboldt 1811) to cocoa (Theobroma cacao L.) pods in
Mérida, Venezuela.
Misael Molina Molina y Marina Mazón….………………………….
155
Paracymus de Venezuela (Coleoptera: Hidrophilidae: Lacobinii)
adición de seis nuevas especies: Parte VI.
Mauricio García y Erickxander Jiménez Ramos………………….....
167
Parasitofauna en murciélagos de los llanos orientales de
Venezuela.
Israel Cañizalez y Ricardo guerrero…………………......................
198
Florística y estructura de bosques ribereños en un sector de los
ríos Yudi y Erebato, cuenca alta del río Caura, estado
Bolívar.
Wilmer Díaz-Pérez, Williams Sarmiento y Lucy Perera-Romero…...
225
Composición de la comunidad de aves en la zona costera del
municipio Santa Rita, estado Zulia, Venezuela.
Luis Lárez y Jinel Mendoza……………..……………….……….…
249
Comunidades vegetales bajo el sombreado de Prosopis juliflora
(Sw) DC., Ciudad Universitaria “Antonio Borjas
Romero”, Universidad del Zulia, Maracaibo, Venezuela.
Antonio Vera………………….…………..…………………………
276
Estructura y dieta de macroinvertebrados acuáticos en parches
de hojarasca de corrientes andinas venezolanas: Rol de los
detritívoros fragmentadores.
Rincón-Ramírez José Elí y María Leal-Duarte…………………..…
291
Instrucciones a los autores……………….…..…………………………
317
Instructions for authors………………….……………………………
327
Vol. 56, N0 2, Pp. 155-342, Julio-Diciembre 2022
UNA REVISTA INTERNACIONAL DE BIOLOGÍA PUBLICADA POR
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UNIVERSIDAD DEL ZULIA, MARACAIBO, VENEZUELA
155
Seasonal damage by red squirrels (Notosciurus granatensis Humboldt
1811) to cocoa (Theobroma cacao L.) pods in Mérida, Venezuela.
Misael Molina Molina1,2* and Marina Mazón3
1Universidad Nacional Experimental Sur del Lago, Núcleo Universitario La Victoria.
Programa Ingeniería de la Producción Agropecuaria. Mérida, Venezuela.
2Programa de Doctorado en Ciencias Agrarias. Facultad de Agronomía, Universidad
del Zulia. Maracaibo, Venezuela. E-mail: molinam@unesur.edu.ve.
Orcid https://orcid.org/0000-0003-2495-7600
3Centro de Investigaciones Tropicales del Ambiente y Biodiversidad, Universidad de
Loja, Ecuador. E-mail: marina.mazon@unl.edu.ec.
Orcid https://orcid.org/0000-0002-5473-7660
*Corresponding author.
ABSTRACT
Throughout its distribution area, cocoa is damaged by fungi, insects, acari and
squirrels. In this study, we evaluated the climatic seasonality of damage by red
squirrels in ten farms of the Cordillera de Mérida, Venezuela. Although we did not
find statistically significant differences (p>0.05) between the dry and rainy seasons,
our results show a higher level of damage during the rainy season when the squirrels
reproduce, taking advantage of a greater food supply.
Key words: Andes, crop, weather, neotropics, losses, pests, rodents.
Boletín del Centro de Investigaciones Biológicas
Vol. 56. Nº 2, Julio- Diciembre 2022, Pp. 155- 166
DOI: https://doi.org/10.5281/zenodo.7469569
Seasonal damage of cocoa
pods by squirrel
156
Molina Molina and Mazón
Daño estacional por ardillas rojas (Notosciurus granatensis Humboldt
1811) a mazorcas de cacao (Theobroma cacao L.) en Mérida,
Venezuela.
RESUMEN
En toda su área de distribución el cacao es dañado por hongos, insectos, ácaros y
ardillas. En este estudio se evalúa la estacionalidad climática del daño por ardillas
rojas en diez unidades de producción de la Cordillera de Mérida, Venezuela. Aunque
no se encontraron diferencias estadísticamente significativas (p>0.05) entre las épocas
seca y lluviosa, los resultados muestran un mayor nivel de daño durante el periodo de
lluvias cuando las ardillas se reproducen aprovechando una mayor oferta de
alimentos.
Palabras clave: Andes, cultivo, clima, neotrópico, pérdidas, plagas, roedores.
Recibido / Received: 15-07-2022 ~ Aceptado / Accepted: 21-09-2022
INTRODUCTION
Cocoa (Theobroma cacao L.) is affected by different diseases throughout its
distribution area. However, two pathologies cause the most significant losses: black
pod rot derived by various species of Phytophthora, and witches' broom caused by
Moniliophthora spp. (Marelli et al. 2019). Insects and mites also figure among the
pests that affect the crop. The most influential insects are the Coleoptera (Xyleborus
ferrugineus, Xilosandrus morigerus, Steirastoma depressum, S. breve, and
Brachyomus octotuberculatus), Thysanoptera (Selenothrips rubrocinctus),
Hymenoptera (Atta sp.), as well as some Hemiptera. The most relevant mites are
Floracarus theobromae and Eriophyes reyesi (ICCO 2022).
Boletín del Centro de Investigaciones Biológicas
Vol. 56. Nº 2, Julio- Diciembre 2022, Pp. 155-166 157
Cocoa is also damaged worldwide by squirrels (Lee 1982, Warren and Emamdie
1993, Chadee and Chadee 1994, Reyes and Capriles 2000, Abdul 2005, Monge and
Hilje 2006, Mollineau et al. 2008, Alvarado et al. 2014, López et al. 2014, Wood and
Singleton 2014, Sánchez-Mora et al. 2015). In the neotropical region, the red squirrel
(Notosciurus granatensis) causes significant damage to cocoa pods, and its
geographic distribution matches that of the crop (Warren and Emmandie 1993).
The squirrels gnaw the pods, extract the seeds and feed on the mucilage; when
they do not devour the pod entirely, the bacteria and fungi finally decompose the
exposed seeds (Parra and Camejo 2015). This damage reduces the crops' productivity
and the producers' income (Mollineau et al. 2008, López et al. 2014); consequently,
the producers loss millions of dollars annually throughout the region.
A management plan is required to reduce rodent damage effectively, and one of the
basic requirements to generate it is to know the damage seasonality and its
relationship with population dynamics (Lloyd and Baldwin 2021). That is because
rodents can adjust their activity patterns to optimize energy incomes and thus
guarantee their reproductive success and reduce the risk of predation throughout the
year (Guidobono 2013, Revollo-Cadima 2021, Wróbel and Bogdziewickz 2015).
In Venezuela, damage by red squirrels has only been studied by Molina and
Briceño (2018, 2021) with no published works related to the climate. This
contribution aims to evaluate the damage caused by red squirrels in cocoa plantations
in the Cordillera de Mérida, Venezuela, during the two climatic seasons: dry and
rainy.
Seasonal damage of cocoa
pods by squirrel
158
Molina Molina and Mazón
MATERIAL AND METHODS
The study area
The work was carried out in 10 farms distributed in the state of Mérida as indicated in
Table 1.
Table 1. Geographical location of the farms.
Code
Name
Coordinates
Parish
Municipality
F2
Santa Lucía
71°37'80''
Mesa Bolívar
Antonio Pinto
Salinas
F3
San Rafael
71°37'84''
Mesa Bolívar
Antonio Pinto
Salinas
F4
Mi Refugio
71°38'12''
Mesa Bolívar
Antonio Pinto
Salinas
F6
La Vega
071°38'74''
Mesa Bolívar
Antonio Pinto
Salinas
F7
La Escondida
71°38'76''
Mesa Bolívar
Antonio Pinto
Salinas
F9
Los Manzanos
71°38'75''
Mesa Bolívar
Antonio Pinto
Salinas
F32
La Esperanza
71°18'37''
Río Frío
Caracciolo Parra y
Olmedo
F33
El Rosal
71°18'35''
Río Frío
Caracciolo Parra y
Olmedo
F34
La Montaña
71°18'03''
Río Frío
Caracciolo Parra y
Olmedo
F35
Los Taguanes
8°56'07''
Río Frío
Caracciolo Parra y
Olmedo
Most crops have an area of 2 ha or fewer; criollo cocoas predominate, although it
is common to find hybrids and, less frequently, foreign cocoas. Plant spacing is 3 x 3
m. Weed control is mainly mechanical. There is a marked tendency towards scarcity
of shade vegetation, which, when present, is usually not very diverse, generally with
two tree strata: the upper one made up of native trees, mainly cedar (Cedrela odora-
Boletín del Centro de Investigaciones Biológicas
Vol. 56. Nº 2, Julio- Diciembre 2022, Pp. 155-166 159
ta), pardillo (Cordia alliodora), and bucare (Erythrina poeppigiana), nevertheless,
occasionally caraño (Protium sp.), jobo (Spondias mombin) and higuerón (Ficus spp.)
trees are found; and an intermediate stratum made up mainly of E. poeppigiana, and
guamo (Inga spp.), sporadically finding surure (Myrcia fallax) and yagrumo
(Cecropia spp.) plants, and even exotic species such as bamboo (Bambusa vulgaris).
In some cases, we found more than two vertical layers in the shade vegetation.
The plants that make up the lower stratum were fruit trees: avocado (Persea
americana), soursop (Annona muricata), orange (Citrus cinensis), mandarin (Citrus
reticulata), lemon (Citrus auratiifolia), banana (Musa AAA) and plantain banana
(Musa AAB).
The study area has three sub-landscapes: hills, cones, and valleys. The hills
modeled by Quaternary erosion in Tertiary and Lower Pleistocene are small, with
slopes between 10° and 30°; the cones are alluvial plains with slopes between 3 and
8°; and the valleys are the product of the river cuts through the cones or hills and have
slopes that vary between 3 and 5° (Vivas 1992).
The relief and altitude are the principal determinants of climate due to its
mountainous condition; these parameters regulate the temperature and rainfall. As a
rule, altitude causes a decrease in temperature between 0.60 to 0.65oC for every 100
m of elevation. The hottest months are May-June. There is a bimodal pattern typical
of the Lake Maracaibo depression with two precipitation maxima: the first between
April and May and the second between June and August, and two minima: one
between January or February and the other in March, July, August, or September
(Vivas 1992).
Identification of the biological agent causing the damage
Woodpeckers principally the red-crowned woodpecker Melanerpes rubricapillus,
Seasonal damage of cocoa
pods by squirrel
160
Molina Molina and Mazón
and red squirrels damage the cocoa pods in the study area. Although rats and
monkeys can also attack these fruits worldwide, we did not find evidence of bites by
smaller rodents in this work; likewise, we did not detect the attack by primates, whose
presence hardly goes unnoticed because they are very conspicuous and noisy.
Damage by red squirrels begins when they break the pod to feed on the mucilage
that covers the seeds (Fig. 1A). The damage is easily distinguished from that caused
by woodpeckers because these birds pierce the pods, leaving circular holes whose
diameter is usually not more than 2 cm (Fig. 1D), while red squirrels leave much
bigger and irregularly shaped holes (Fig. 1C) that can cover almost the entire fruit
(Fig. 1B); in addition, in the pods bitten by squirrels, the grooves left by the incisor
teeth can be easily seen.
Damage assessment
We randomly selected 12 plants in each farm and counted twice, during the rainy
season of 2018 and the dry season of 2021, the number of pods bitten by the squirrels
and the total number of pods occurring in the plant to calculate the percentage of
damage. We consider each farm as a replica.
Data analysis
We defined the two groups of data corresponding to the climatic periods
following the criteria of López et al. (2010). We used the Wilcoxon signed-rank test
(Siegel and Castellan 2007) to check the existence of statistically significant
differences in the level of damage between the dry season (November- March) and
the rainy season (May- September). We processed data using the SPSS20 (IBM
2011).
Boletín del Centro de Investigaciones Biológicas
Vol. 56. Nº 2, Julio- Diciembre 2022, Pp. 155-166 161
Figure 1. Cocoa pods without damage (A, note the mucilage
that coats the seeds), squirrel-damaged (B and C), and
woodpecker-damaged (D, note hole size and shape). Source:
M. Molina.
RESULTS AND DISCUSSION
The average damage level was 3.6% for the dry season and 8.8% for the rainy
period. Nevertheless, the differences between the two seasons were not statistically
significant (p>0.05).
Seasonal damage of cocoa
pods by squirrel
162
Molina Molina and Mazón
Figure 2 reveals more damage to most of crops during the rainy season; however,
the statistical analysis did not reflect significant differences. Except for farms 3 and
33, the damage was higher in the rainy season.
Our results contrast with those of López et al. (2014), who found losses between
26 and 34% for Nicaragua, and those of Mollineau et al. (2008), who reported losses
above 30% for Trinidad and Tobago. Although the average level of damage found is
lower than those reported by these authors, it is very important for Mérida producers
since they face a crisis that is reflected mainly through scarcity and high costs of
agro-inputs at the field level.
Figure 2. Relationship between the magnitude of damage and the climatic
seasonality. F: farm.
Boletín del Centro de Investigaciones Biológicas
Vol. 56. Nº 2, Julio- Diciembre 2022, Pp. 155-166 163
However, the losses caused by red squirrels are related to those generated by
fungi which in some neotropical regions is approximately 40% (Correa et al. 2014).
In fact, after red squirrels attack the cocoa pods, fungi and bacteria enter,
deteriorating them completely (Molina and Briceño 2018).
In Venezuela, red squirrels reproduce at the end of the rainy season (Linares
1998); thus, it is reasonable to expect more significant damage at that time since the
energy expenditure for lactation and rearing, generally, is higher. Rodents can adjust
their daily and seasonal activity patterns to optimize energy gains and reduce
predation risk according to climate variations (Wróbel and Bogdziewickz 2015).
The squirrels are likely taking advantage of the greater availability of cocoa fruits
during the rainy season (Wilcoxon Signed Ranks Test, p<0.05) and a higher supply of
complementary foods (Molina, M., unpublished data). According to Witmer and
Proulx (2010), when rodents have access to food in high quantity or quality, the
percentage of the population in reproductive condition can increase, adult animals can
mate earlier than usual, the proportion of females giving birth can grow, even the size
of the litter can be increased, which would consequently generate an increment in the
level of damage.
Producers can use the present results to enhance their knowledge of the cocoa
plantation and to take better decisions regarding the pest management. Therefore,
they would control the damage and reduce losses.
ACKNOWLEDGMENTS
We acknowledge to the producers of the Antonio Pinto Salinas and Caracciolo
Parra and Olmedo municipalities of the Mérida state, especially Juvenal Dávila,
Carmelo contr Contreras, and Ramón Araujo, for their passion for cocoa and for the
collaboration provided during the field work.
Seasonal damage of cocoa
pods by squirrel
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Molina Molina and Mazón
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ENEZUELA
Vol. 56, No 2, Pp. 155-342, Julio-Diciembre 2022
CONTENTS
Daño estacional por ardillas rojas (Notosciurus granatensis)
Humboldt 1811) a mazorcas de cacao (Theobroma cacao
L.) en Mérida, Venezuela.
Misael Molina Molina y Marina Mazón.…......................................
155
Paracymus of Venezuela (Coleoptera: Hydrophilidae: Laccobiini),
adición de seis nuevas especies: Parte VI.
Mauricio García and Erickxander Jiménez-Ramos..….………….....
167
Parasite fauna in bats of the Eastern plains of Venezuela.
Israel Cañizales and Ricardo Guerrero...............................................
198
Floristic and structure of riparian forest in a sector of the Yudi
and Erebato river, Caura river higher river basin, Bolívar
state, Venezuela.
Wilmer Díaz-Pérez and Raúl Rivero...………...................................
225
Composition of the community in the coastal zone of Santa Rita
municipality, Zulia state, Venezuela.
Luis Lárez and Jinel Mendoza…..………………………….….……
249
Plant communities under the shade Prosopis juliflora (Sw.) DC.,
“Antonio Borjas Romero” University city, University of
Zulia, Maracaibo, Venezuela.
Antonio Vera………………………………….……………………..
276
Structure and diet of aquatic macroinvertebrates in leaf litter
patches of venezuelan Andean streams: Role of shredders.
José Elí Rincón-Ramírez y María Leal-Duarte …..………………….
291
INSTRUCTIONS FOR AUTHORS…………………………………...
327
