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Interaction of Bephratelloides cubensis (Hymenoptera: Eurytomidae)

with Annona macroprophyllata fruits in orchards of Chiapas, Mexico

José Norman González-Sánchez

, Alma Rosa González-Esquinca

Claudia Azucena Durán-Ruiz

, Iván De-la-Cruz-Chacón

& Marisol Castro-Moreno

1. Universidad de Ciencias y Artes de Chiapas, Laboratorio de Fisiología y Química Vegetal, Instituto de Ciencias

Biológicas, Tuxtla Gutiérrez, Chiapas, 29000, Mexico; norman.11@hotmail.es, aesquinca@unicach.mx,

claudia.duran.ex@unicach.mx, ivan.cruz@unicach.mx, marisol.castro@unicach.mx (*Correspondencia).

Received 11-IX-2020. Corrected 09-XII-2020. Accepted 17-XII-2020.

ABSTRACT. Introduction: Annona macroprophyllata Donn. Smith. (Annonaceae) (syn. Annona diversifolia

Saff.) is a valued fruit tree species known as papausa. In Mexico and Central America, this fruit has become an

important crop because of its tasty flavor and high pulp content. Its fruits are frequently damaged by the inci-

dence of wasps of the genus Bephratelloides Girault (Hymenoptera: Eurytomidae), which develop inside the

seeds. Objective: to report the interaction of Bephratelloides cubensis Ashmead during its life cycle in fruits

of A. macroprophyllata. Methods: We periodically collected fruits in different states of growth recording a)

oviposition, b) the moment of evident infection, c) the development of the wasps inside the seeds, and d) their

emergence as adults. We also determined the proportion of damaged fruits and seeds. Results: The data indi-

cate that wasps preferred to oviposit on fruits with a diameter of less than 8 cm, oviposition was more frequent

between 11:00 am and 03:00 pm., and there was 26 % infestation of fruits, and 9 % of seeds. Conclusion: It is

an obligatory interaction for the wasp, the highest proportion of attack on fruits was in the early stages of fruit

development and control actions should focus on the protection of these early stages.

Key words: larvae; pupae; adults; plant-insect interactions; pest of Annonaceae.

The family Annonaceae is made up of 128

genera and 2 400 recognized species (Chatrou et

al., 2012). The genus Annona stands out among

them with 166 species (Chatrou et al., 2012;

Rainer, 2006). There are around 60 species in

Mexico, some of them are important because of

their fruits, such as the soursop (Annona muri-

cata), the sugar-apple (A. squamosa), ilama or

papausa (A. macroprophyllata) and the cheri-

moya (A. cherimola) (De-la-Cruz-Chacón,

Castro-Moreno, Luna-Cázares, & González-

Esquinca, 2016). Annona macroprophyllata

(Annona diversifolia) is a Mexican and Central

America native fruit which has become an

important crop because of its tasty flavor, high

pulp content, nutritional value and antioxidant

properties (Julian-Loaeza, Sántos-Sánchez,

Valadez-Blanco, Sánchez-Guzmán, & Salas-

Coronado, 2011).

There are more than 296 species of arthro-

pods interacting with different Annonaceae,

but the knowledge of the biology and habits

of these species is scarce. Some groups of

insects that are reported as pests belong to

González-Sánchez, J.N., González-Esquinca, A.R., Durán-Ruiz, C.A., De-la-Cruz-

Chacón, I., & Castro-Moreno, M. (2021). Interaction of Bephratelloides cubensis

(Hymenoptera: Eurytomidae) with Annona macroprophyllata fruits in orchards of

Chiapas, Mexico. Revista de Biología Tropical, 69(1), 369-378. DOI 10.15517/rbt.

v69i1.43827

ISSN Printed: 0034-7744 ISSN digital: 2215-2075

DOI 10.15517/rbt.v69i1.43827

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the families Coccidae (Hemiptera), Noctui-

dae, Oecophoridae (Lepidoptera), Nitidulidae

(Coleoptera) and Eurytomidae (Hymenoptera)

(Peña & Bennett, 1995).

Bephratelloides Girault (Hymenoptera:

Eurytomidae) is a genus composed of seven

species of stingless wasps that are associated

with Annonaceae because five of those species

complete part of their life cycle inside the seeds

of these plants (Grissell & Foster, 1996; Noyes,

2019). In particular, Bephratelloides pomorum

Fabricius and B. cubensis Ashmead are among

the most important pests of the commercial

species of Annona because of the damage they

cause to the fruits (Grissell & Schauff, 1990;

Peña & Bennett, 1995; Castañeda-Vildózola,

Nava-Díaz, Franco-Mora, Lomeli-Flores, &

Peña, 2011; Silva, Broglio, Lemos, Salvador,

& Neves, 2014). There are also reports of their

presence in other genera of the Annonaceae

like Cymbopetalum (Grissell & Foster, 1996).

Bephratelloides cubensis begins its life

cycle when the females oviposit inside the

seeds of fruits in early phenological stages

(Nadel & Peña, 1991). Females lay one egg per

seed and these require approximately two or

three weeks to hatch (Brunner & Acuña, 1967;

Castañeda-Vildózola et al., 2010; Hernández-

Fuentes, Urias-López, & Bautista-Martínez,

2010). The larvae that hatch feed on the endo-

sperm, and after three to six weeks these larvae

transform into pupae and later the adult wasps

exit from holes, they chew through the seed

and fruit, to finally mate and begin a new cycle

(Castañeda-Vildózola et al., 2010; Hernández-

Fuentes et al., 2010; Durán-Ruiz et al., 2019;

Nadel & Peña, 1991).

The Annona macroprophyllata market is

still local; however, it´s delicious flavor and

biotechnological use give it potentially wider

market. That means that A. macroprophyllata

is a potential fruit crop, important because it

is a source of possible bioactive compounds

(González-Esquinca, De-la-Cruz-Chacón, Cas-

tro-Moreno, Orozco-Castillo, & Riley-Saldaña,

2014). In Chiapas A. macroprophyllata is a

tree of incipient cultivation, increasingly rare

in the wild, it is cultivated in backyards and as

living fences, or it inhabit areas of Deciduous

and Semideciduous Dry Forests (González-

Esquinca, De-la-Cruz-Chacón, Castro-Moreno,

& Riley-Saldaña, 2016). Studies like those of

Castañeda-Vildózola et al. (2010) and Durán-

Ruiz et al. (2019) allow for the detection of

B. cubensis parasitizing A. macroprophyllata.

Studies indicate that the main damages to A.

macroprophyllata crops are the exit holes from

the seed which allow the development of fungi

such as Colletotrichum sp. provoking anthrac-

nose disease and therefore a loss in harvest

(Nadel & Peña, 1991; Peña & Bennett, 1995;

Cruz & Deras, 2000; Castañeda-Vildózola et

al., 2010; Hernández-Fuentes et al., 2010).

This study characterizes the attack process

of Bephratelloides cubensis and its life cycle

during the fructification of A. macroprophyl-

lata in backyard crops. Our hypothesis is that

wasps damage a low proportion (less than 50

%) of the fruits when trees are cultivated in

backyards, where their density is lower than in

places of intensive commercial cultivation. In

order to test this hypothesis, we collected fruits,

made observations throughout the season of

fruit development, and related that information

to the development of the wasps.

MATERIALS AND METHODS

Study site: We conducted the fieldwork in

the community of Nuevo Carmen Tonapac, in

the municipality of Chiapa de Corzo, Chiapas,

Mexico, which is located in the Central Depres-

sion of Chiapas (16°41’48’’ W & 92°57’20’’

N). The original vegetation in this place cor-

responds to Deciduous Dry Forest, with eco-

tone of Semideciduous Medium Dry Forest.

The fieldwork was carried out from July to

August 2014.

Tree selection: We randomly selected

50 of the 70 adult trees counted in the com-

munity. On each tree, we marked 5 fruits of

4-5 cm diameter. We visited the trees every 15

days during two consecutive months (which is

the mean duration of the development of the

fruits) and collected one of the five fruits from

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each tree (50 fruits each time). The fruits were

placed in a portable cooler and transferred to

the Laboratorio de Fisiología y Química Veg-

etal of UNICACH. The fruits were collected

in five stages of development: a) initial harvest

or first stage of development (day 0), second

harvest or stage (day 15), third harvest or stage

(day 30), fourth harvest or stage (day 45), and

fifth harvest or stage (day 60).

Measurement of fruits and seeds and

monitoring of larvae, pupae and adults: At

the moment of collecting fruits, we measured

their length and width with a measuring tape.

We also measured the seeds with a caliper. We

opened the seeds longitudinally. The larvae,

pupae and adults of B. cubensis were preserved

in a 70 % alcohol solution. In all the five stage

of fruit development, we quantified the dam-

aged fruits and the infested seeds.

The identification was carried out in the

Colección Nacional de Insectos of the Insti-

tuto de Biología of the Universidad Nacio-

nal Autónoma de México (IB-UNAM),

following the taxonomic keys of Grissell &

Schauff (1990) and Grissell & Foster (1996).

Observations were made on a Carl Zeiss ste-

reoscope microscope.

Larval instar determination: Mandibles

were isolated from the soft body with a 10 %

potassium hydroxide solution for 24 hours and

preserved in glycerin for microscopic observa-

tion, mandibles were observed on a ZEISS®

Primo Star optic microscope. We determined

the larval instars comparing the progressive

development of the mandibles, considering the

development of the teeth, condyle and tip. This

method was modified from Hernández-Fuentes

et al. (2010) and used in Durán-Ruiz et al.

(2019) avoiding the use of the mandible size

due to its heterogeneity.

Statistical analysis: We tested the dif-

ferences in the morphometry of seeds and

fruits with a one-way analysis of variance

and a post-hoc least significant difference test

(LSD). To characterize the fruit morphometric

measurements, their apparent damage and the

ratio of females to males, we performed a non-

parametric analysis Kruskal-Wallis (KW) and

the post-hoc Dwas-Steel-Crichtlow-Fligner

(DSCF) tests. To compare the final sizes of

the seeds with and without damage caused by

the insect, we carried out a student t-test. To

determine the relationships between fruit and

insect development we carried out polynomial

regressions. In all cases, we used the statistical

program PAST3.26 (Hammer, Harper, & Ryan,

2001) and the free version of the program

Jamovi to perform the KW and the DSCF tests.

RESULTS

Development of fruits and seeds: Fruits

had an ovoid shape, and a thick, coriaceous and

green exocarp (Fig. 1A, Fig. 1B, Fig. 2A). The

fruits reached their final size after 45 days and

ripen after approximately 60 days (F = 2041,

P = 0.0001). The seeds of the unripe fruits of

the first stage, were small, white translucent

(Fig. 2C), with an oily (to the touch), white

endosperm and a soft seed coat. Seeds grew

constantly until 30 to 45 days, and then they

acquired their final characteristics: Dark brown

seed coat (dark brown 3/3 in the scale of the

Munsell colors chart 2009), with a crustaceous

texture and with a size four times larger than

the initial stage (F = 8.4, P = 0.0001) (Fig. 1G,

Fig. 2B). All the infected and healthy seeds had

on average, the same characteristics of size and

color (F = 6.7, P = 0.7).

Infected fruits by sample collection:

Most of the damaged fruits were detected in

the last three stages (~50 %) while damage was

significantly less in the first two (H´ = 3.9, P =

0.001) (Fig. 2D). Of the 250 collected fruits,

86 were damaged by B. cubensis (26 %) and

of the 3011 seeds, 9 % were infected (4 % with

some larval instar, 4 % with pupae, and 1 %

with adults). The developmental stage of the

fruits was associated with the developmental

phase of the insects (r = 0.97 Legth, 0.87 p,

0.68 Width, P = 0.001) (Fig. 2C).

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The external appearance of the unripe

seeds infected with larvae in the first instar was

similar to the healthy seeds. Both infected and

healthy seeds had the same color (dark brown

3/3 according to the Munsell color scale 2009)

and did not show visible perforations in the

seed coat. However, when dissected, active

larvae were found, and the endosperm was

partially destroyed by feeding activity (Fig.

3B, Fig. 3C).

The most developed seeds with larvae

or pupae inside showed subtle signs of the

presence of insects, such as changes in the color

of the seed coat (from dark to light brown) and

low resistance to compression. Seeds with

adult wasps ready to leave and seeds where the

wasps already left had an exit pit parallel and

opposite to the micropyle (Fig. 3K).

Inside the seeds, we observed the initial

and late phases of the larvae, pupae and adults.

Still, the frequency of each collection varied.

For instance, in the first stage, when fruits

were 4.8 ± 0.5 cm diameter, we did not find

any eggs or larvae (Fig. 3A); in the second

Fig. 1. Fruits in development. A. all stages of development, B-C. First stage (initial harvest, day 0), D. Second stage of

development (day 15), E. Third stage (day 30), F. Fourth stage (day 45), G. Fifth stage (day 60).

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stage, we found fewer larvae and pupae than

in the third and fourth collections, but as the

size of the fruits increased both, larvae and

pupae increased in number. We observed the

firsts adults in the third stage (H = 31.75657.6,

P = 0.001) (Fig. 3B). When the fruits reached

their final stage of development (fifth stage) the

number of larvae decreased significantly, while

the number of pupae remained stable and the

number of adults increased (H = 32.443, P =

0.001). It is interesting to note that in the three

stages there were more females than males (H

= 43.72, P = 0.001).

DISCUSSION

Bephratelloides cubensis has been report-

ed as a frequent parasite in Annona muricata,

A. reticulata, A. squamosa, A. reticulata, A.

cherimola, A. glabra, A. montana and A. bul-

lata. This wasp completes almost its entire life

cycle inside the seeds and is free-living only

Fig. 2. Fruit and seed growth and development of the life cycle of Bephratelloides cubensis in Annona macroprophyllata

seeds during the fruiting season. A. Fruit growth, B. Seed growth, C. Number of pupae and adult larvae during fruiting, D.

Fruits damaged or with insects inside the seeds, E. Incidence of sexes of the adult stage. The different letters on the bars

in A., B., D. and E. indicate significant differences p = 0.001, in c) the frequency of larvae, pupae and adults (r = 0.97, P =

0.001), pupae (r = 0.87, P = 0.001) and adults (r = 0.68, P = 0.0001).

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as adults (Grissell & Schauf, 1990; Castañeda-

Vildózola et al., 2010; Hernández-Fuentes et

al., 2010; Cham et al., 2019). The presence of

B. cubensis in A. macroprophyllata has been

reported in some areas of Guerrero and More-

los (Castañeda-Vildózola et al., 2010), but in

Chiapas there is only one formal report (Durán-

Ruiz et al., 2019).

The development of B. cubensis was

simultaneous with that of fruits and seeds of

A. macroprophyllata. Similar to Durán-Ruiz

et al. (2019), the growth and accumulation of

Fig. 3. Development of B. cubensis in the seeds of A. macroprophyllata. A. Seed arrangement in the fruit, B. early larva,

C. developed larva, D-H. jaws of the larvae of the five instar, I. early pupa, J. late pupa, K. exit hole of the seeds, L. adult

inside the seed, M. adult female, N. adult male.

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reserve material in the endosperm did not stop

even if the larvae fed on the endosperm. The

morphometry, and the external appearance of

the infested and the healthy seeds were statisti-

cally similar during the immature stages of the

insect (larvae and pupae). But, the biomass of

the damaged seeds decreased by up to 50 %

due to the active feeding of the larvae. With

the emergence of the adult wasps, the seed

coat also presented an exit hole, which dif-

ferentiated the infested from the healthy seeds.

Therefore, this hole is associated with the dam-

age perceived on the surface of the fruit. The

fruits attacked by B. cubensis differed from the

healthy fruits only when the exit holes from the

seed to the exocarp were observed. Thus, the

number of holes in the fruit is a physiologic and

agronomic indication of the degree of infesta-

tion and/or damage caused.

The lack of apparent damage in the early

stages of development suggests that wasps ovi-

posit directly inside the immature seeds when

the seed coat is still soft and not directly in the

pulp, as described by Evangelista, Llanos, &

Valdés (1999). We detected larvae in second

stage fruits, and their number increased in

the third stage, the highest incidence was in

the fourth stage fruits, with and an important

decrease in the final stage. In A. muricata,

Hernández-Fuentes et al. (2010), reported that

females oviposit in fruits with a minimal diam-

eter of 3.1 cm, and a maximum of 7.6 cm. Peña,

Glenn, & Baranowski (1984) mention that the

lack of fruit availability forces females of B.

cubensis to oviposit in fruits of any size even

when preferring seeds in development.

We did not observe eggs in any seeds,

perhaps due to their resemblance to the semi-

nal endosperm and their small size (0.1 mm

diameter) (Hernández-Fuentes et al., 2010).

In the first fruiting stage (4 cm diameter), we

did not detect nor larvae any pupae, probably

because only eggs were present which can have

an incubation period of up to 24 days according

to Hernández-Fuentes et al. (2010). We began

to find larvae and pupae of B. cubensis in the

seeds in the second stage and they increased

significantly in the following stage, in all cases

there was only one individual per seed.

The larvae in 2nd, 3rd and 4th stage fruits,

belonged to all the larval instars, while in the

fifth stage, we only found the two last instars,

indicating they were ready to pupate. The

simultaneous presence of larvae at different

instars, even in the same fruit, can be attributed

to the quality and the quantity of food inside

the seeds and to the oviposition time (Hernán-

dez-Fuentes et al., 2010). Barbosa, dos Anjos,

& Picanço (1997) also suggested that the over-

lapping instars in the same fruit is attributed to

the different nutritional potential of each seed.

Pupae were found from the third stage

onward, which indicates that larvae require

more than 15 days to pupate, this time corre-

sponds to the estimated by Hernández-Fuentes

et al, (2010). In that development stage (3th),

we found translucent white pupae (less mature)

and brown pupae (before entering the adult

stage). In the three last stages, we found adult

wasps, but when fruits achieved their final size

we found adults, larvae and pupae, the latter

being in the highest proportion. These data

indicate that there is partial synchrony between

the phenological stages of fruits, seeds, and

wasps. It is noteworthy that the exit hole was

presented in all cases in the opposite position

to the micropyle, which could indicate that the

embryo of the seed could be intact due to its

small size (1 mm).

This plant-animal interaction is coordi-

nated phenologically and is an obligatory rela-

tionship for the wasp since most of its life cycle

(egg through pupae) occurs inside the seed, and

only the adult stage in wasps occurs in free-life

(Hernández-Fuentes et al., 2010; Durán-Ruiz et

al., 2019). Durán-Ruiz et al. (2019), observed a

high synchronization between the life cycle of

the insect and the stages of fruit development.

Other studies have found a high dependence

of the genus Bephratelloides on the species of

Annonaceae, which could indicate a possible

coevolutionary process. This interaction has

been widely described in cultivated Annona-

ceae and less frequently in wild Annonaceae.

Some of the attacked species in Annonaceae

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are A. muricata, A. reticulata, A. squamosa

(Castañeda-Vildózola et al., 2010), and Cym-

bopetalum mayanum (Grissel & Foster, 1996).

Castañeda-Vildózola et al. (2011) present the

only report of a species of Bephratelloides

developing in another plant family B. ablusus

in Diospyros digyna (Ebenaceae) seeds.

Several studies have reported 60 to 100 %

of fruits attacked in intensive and semi-inten-

sive tree crops of A. muricata, with harvest

losses of 25 to 70 % (Castañeda-Vildózola et

al., 2010; Hernández-Fuentes et al., 2010). In

Nuevo Carmen Tonapac, Chiapas, A. macro-

prophyllata is cultivated in backyards, so it is

not considered an intensive crop. In this study,

we report damages of 26 % in the sampled

fruits and 9 % in seeds.

The serious problems caused by B. cuben-

sis in soursops and its low incidence in A.

macroprophyllata can have multiple explana-

tions, perhaps the most important being habitat

management in the intensive crops where the

species diversity that could control the pest has

decreased significantly (Schowalter, 1986). A.

muricata is a plant from the Antilles that has

been domesticated to ameliorate the organo-

leptic quality of the fruit but at the expense of

other attributes (including phytochemicals) that

lead to low genetic variation which is reflected

in lower resistance to pests (Shelef, Weisberg,

& Provenza, 2017). In contrast, according to

Provenza, Meuret, & Gregorini (2015) native

crops, such as A. macroprophyllata (which is

native to Chiapas) have higher genetic diversity

compared with A. muricata, which gives them

more possibilities of adaptation to pests.

In the study site, there are no extensive

crops of A. macroprophyllata, and even when

the incidence of B. cubensis is low (26 %), the

quality of the fruits is affected when the wasps

emerge from the exit holes in the seeds. The

attack of the insect occurs in a higher propor-

tion of fruits at their early stages, demonstrat-

ing that actions to control populations of B.

cubensis should focus on the early stages of

fruit development when proposing crops of

Annonaceae in the area.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We are indebted to the inhabitants of

Nuevo Carmen Tonapac, Chiapas, who allowed

the early samples collection of fruits for this

study. We thank Dr. Alejandro Zaldivar Riv-

erón from the Colección Nacional de Insectos

IB-UNAM, for his help with the identification

of the organisms.

RESUMEN

Interacción de Bephratelloides cubensis (Hyme-

noptera: Eurytomidae) con frutos de Annona macropro-

phyllata en huertos de Chiapas, México. Introducción:

Annona macroprophyllata Donn. Smith. (Annonaceae) es

una especie de árbol frutal, conocida como papausa. En

México y América Central, esta fruta se ha convertido en

un cultivo importante y valorado debido a su delicioso

sabor y la cremosa textura de su pulpa. Sus frutos son fre-

cuentemente dañados por la incidencia de avispas del géne-

ro Bephratelloides Girault (Hymenoptera: Eurytomidae),

que se desarrollan dentro de las semillas. Objetivo: des-

cribir la interacción de Bephratelloides cubensis Ashmead

durante su ciclo de vida en frutos de A. macroprophyllata.

Método: Recolectamos frutos en diferentes estados de

crecimiento registrando a) la ovoposición, b) el momento

de la infección evidente, c) el desarrollo de las avispas

dentro de las semillas, y d) su emergencia como adultos.

También determinamos la proporción de frutas y semillas

dañadas. Resultados: Los datos indican que las avispas

preferían ovipositar en frutas con un diámetro de menos de

8 cm, la oviposición era más frecuente entre las 11:00 a.m.

y las 3:00 p.m., y que había un 26 % de la infestación en

las frutas y un 9 % en semillas. Conclusión: Es una inte-

racción obligada para la avispa y la mayor proporción de

ataque a los frutos fue en las etapas tempranas de desarrollo

de frutos y las acciones de control se deberían enfocar a la

protección de estas etapas.

Palabras clave: larvas; pupas, avispas adultas; interaccio-

nes planta-insecto; plaga de Annonaceae.

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