Scolytines (Coleoptera: Curculionidae: Scolytinae) Associated with Cacao Monoculture and Agroforestry Systems

Jessenia Castro-Olaya1, Dorys T. Chirinos1* and Takumasa Kondo2

1Facultad de Ingeniería Agronómica, Universidad Técnica de Manabí, Postal Code 130105, Portoviejo, Manabí Province, Ecuador; 2Corporación Colombiana de Investigación Agropecuaria- Agrosavia, Calle 23, Carrera 3, Palmira, Valle del Cauca, Palmira, Postal Code 763533, Colombia.

Received | May 25, 2024; Accepted | October 08, 2024; Published | October 30, 2024

*Correspondence | Dorys T. Chirinos, Facultad de Ingeniería Agronómica, Universidad Técnica de Manabí, Provincia de Manabí, Ecuador; Email: [email protected]

Citation | Castro-Olaya, J., Chirinos, D.T. and Kondo, T., 2024. Scolytines (Coleoptera: Curculionidae: Scolytinae) associated with cacao monoculture and agroforestry systems. Sarhad Journal of Agriculture, 39(Special issue 2): 93-102.

DOI | https://dx.doi.org/10.17582/journal.sja/2023/39/s2.93.102

Keywords | Ambrosia, Bark beetles, Diversity indices, Ecuador, Insect pests, Taxa

Copyright: 2024 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Cacao, Theobroma cacao L. (Malvaceae) is a crop of global importance because its beans are the basis for the production of chocolate and other products (Armengot et al., 2020). Its origin is found in the humid forests of South America and from there its cultivation expanded to Central America and later to other parts of the world, and now is grown pantropically (Tscharntke et al., 2023). Worldwide, 5,580,432 t of cacao beans are produced from 11,535,884 ha (FAO, 2024) of cacao planted areas. Ecuador contributes with 337,149 t of cacao beans harvested from 509,179 ha (MAG, 2024) of cacao planted areas, which represents 6% of world production.

Associated with cacao, there is a diverse entomofauna with different functional roles, i.e., natural enemies (predators and parasitoids), xylophages, xylomycetophages, and phytophages, including several species of scolytines (Coleoptera: Curculionidae: Scolytinae), among others (Mazón et al., 2018). Scolytines are commonly known as bark beetles, namely those that feed on phloem (phloeophagy) or sapwood and ambrosia beetles, namely those that burrow into sapwood and feed on ectosymbiotic fungi (xylomycetophagy) (Atkinson, 2017). However, other feeding habits can be found in species of scolytines such as xylophagy (wood feeders), myelophagy (pith feeders), spermophagy (seed feeders) and some feed on herbaceous plants (Gerómimo-Torres et al., 2015; Kirkendall et al., 2015).

Although scolytines play an important role in the biological decomposition and nutrient cycling of forests, some species cause significant economic damage to agroecosystems and forests around the world (Rodríguez et al., 2017; Nuriadi et al., 2023). Ambrosia beetles carry and introduce symbiotic fungi, which invade and grow on the wall of tunnels bored into the xylem of their host trees and serve as their sole food source (Kirkendall et al., 2015). Castrejón-Antonio et al. (2017) reported that the growth of fungi in the vascular system of living trees could hinder the flow of water and nutrients, which would cause the partial or total death of the plant. Some species are considered cacao pests in South America. For example, in Ecuador Xyleborus ferrugineus (Fabricius) is associated with the transmission of Ceratocystis cacaofunesta Engelbr. and T.C. Harr. (Microascales: Ceratocystidaceae) (Paladines-Rezabala et al., 2022) and Xylosandrus compactus (Eichhoff) has been reported causing damage to nursery plants in Peru (Delgado and Couturier, 2017).

Approximately 6,000 species included in 247 genera of scolytines have been reported in the world, of which 40% are estimated to exist in the Neotropics and 25% in South America (Martínez et al., 2019). Scolytine species have been detected in Ecuador in natural, secondary forests and in balsa plantations of Ochroma pyramidale (Cav. ex Lam.) Urb. (Malvaceae) (Martinez et al., 2019; Dole et al., 2021). Smith and Cognato (2021) reported that the neotropical diversity of scolytines is largely undescribed and suggested that the diversity of Ecuadorian scolytines must be three to four times higher than currently known.

Cacao has traditionally been produced as an agroforestry system associated with other crops and timber species (Tscharntke et al., 2023). However, in recent years, cacao planting in a monoculture system has increased dramatically in order to increase productivity (Lagneaux et al., 2021). This simplification in modern intensive systems have led to the loss of biodiversity in cacao agroecosystems (Lagneaux et al., 2021; Tscharntke et al., 2023). In Ecuador, Xyleborus ferrugineus (Fabricius) is the only species of scolytine that has been reported associated with cacao (Paladines-Rezabala et al., 2022). Since Ecuador is part of the center of origin of cacao, it is expected that there should be a greater number of scolytine taxa associated with this crop, which should also be greater in diverse agroecosystems.

Manabí province is the main cacao-producing region in the country, where cacao is planted in both agroforestry and monoculture. However, little is known about the scolytine taxa in agroforestry and monoculture systems in this province and in the country. Thus, the main objective of this work was to identify the scolytine taxa (genus or species) associated with cacao monoculture and agroforestry systems in Manabí province, Ecuador.

Materials and Methods

Location and timing of sampling

During March-August 2021, this research was carried out on farms in the areas of Lodana, Pachinche and Santa Ana de Vuelta Larga (Figure 1), which are towns located in Manabí province, Ecuador.

The study sites are characterized as agricultural systems, with cacao, corn, coffee, banana and rice crops grown at small and medium scales, with traditional production systems, and the crops are shared by a diversity of fruit species (MAGAP, 2012). According to the life zones system, this region is classified as a tropical dry forest (Holdridge, 1967). This area is characterized by having two well-defined climatic seasons, a rainy season from December to May and another dry season from June to November (Rivadeneira et al., 2020). In each area, two farms were selected, one in a cacao monoculture system and the other in a cacao agroforestry system. The selection requirements were an area of one to three hectares in which cacao had been cultivated for four years. Precipitation data were obtained for each area from the meteorological station of the National Institute of Meteorology and Hydrology (INAMHI), located in La Teodomira (code M1208).

 

In Lodana, cacao agroforestry is associated with a native tree known as guaba, Inga edulis Mart. (Fabaceae), as shade. In Pachinche, the cacao agroforestry system is intercropped with soursop, Annona muricata L. (Annonaceae), key lime, Citrus aurantiifolia Swingle, mandarin orange, Citrus reticulata Blanco, orange, Citrus sinensis Osbeck (Rutaceae), coconut, Cocos nucifera L. (Arecaceae), mango, Mangifera indica L. (Anacardiaceae), banana, Musa paradisiaca L. (Musaceae), and avocado, Persea americana Miller (Lauraceae). In Santa Ana, cacao was planted with A. muricata, C. aurantiifolia, C. sinensis, araza, Eugenia stipitata McVaugh (Myrtaceae), M. paradisiaca, P. americana and guava, Psidium guajava L. (Myrtaceae).

Sampling, counting and identification

In each cacao plantation, seven traps baited with ethanol were placed on cacao plants 1.3 m above the ground. The traps were placed in the center of each plantation to avoid edge effects with an approximate separation of 22 m between traps, covering a 160 m transect. The trap was developed following the model proposed by Steininger et al. (2015), which consisted of a two-liter plastic bottle with its lid maintained closed, with two openings (25 cm2) near the base to allow the entrance of the attracted scolytines. A puncture hole was made at the base of the bottle and with the help of a rope, which was attached to a branch of the tree at a height of one meter, leaving the bottle with its mouth downwards. A plastic bag containing 96% ethyl alcohol was hung inside the trap. A small perforation was made in the bag so that the alcohol was released slowly to attract the insects. Gel alcohol was placed in the mouth of the bottle to trap the insects. The specimens were collected every fortnight, for which the trap lid was removed, and the individuals were placed in a 100 mL plastic bottle containing ethyl alcohol (70%). A total of 504 samples were taken during the study, obtained from seven traps in 12 samplings (biweekly) in the six agroecosystems.

The collected insects were taken to the Entomology Laboratory of the Faculty of Agricultural Engineering, Technical University of Manabí (TUM), where scolytines were observed under a Motic® SMZ 165 stereoscope (magnification: 10 to 75X). The scolytine specimens were first sorted out according to their morphological characteristics and later they were identified using the taxonomic keys of Wood (2007) and through comparisons with photographs in the Atkinson (2023) catalogs. Specimens of identified scolytines are stored in the Entomology Laboratory of the TUM.

Data analysis

Diversity indices, Shannon Index, Margalef Index, Dominance D Index and Chao 1 Index as well as the number of taxa and abundance were estimated to the six cacao agroecosystems. A non-parametric multivariate permutational analysis (PERMANOVA) was performed to compare agroecosystems using Bray-Curtis distances (P<0.05). An analysis was carried out to associate the abundance of the different taxa of scolytines in the studied agroecosystems using the value of IndVal (%), in order to determine the indicator taxa of the agroecosystems (P<0.05). A Spearmanʼs correlation analysis (P<0.05) was performed between the number of scolytines versus rainfall, temperature and relative humidity for each agroecosystem. The fluctuation of the number of total individuals per agroecosystem was plotted together with precipitation data. These analyses were performed using the program PAST software version 4.04 (Hammer et al., 2001).

Results and Discussion

General abundance and diversity of scolytines in cacao

A total of 8,372 individuals separated into 14 taxa within nine genera in four tribes were observed associated with the six cacao agroecosystems (Table 1). The tribe Trypophloeini to which Hypothenemus belongs to was the most abundant with 87.91% of the total number of captured individuals. Corthylus sp. 1 and Premnobius cavipennis Eichhoff were the next most abundant taxa with 3.93 and 3.12% of the total number of individuals, respectively. Xyleborus affinis Eichhoff and Xyleborus spinulosus Blandford showed an abundance of approximately 1% while for the rest of the taxa, the abundance ranged from 0.01 to 0.97%. In the tribes Corthylini and Xyleborini, six taxa were detected in each one, which represents the largest number of taxa compared to the other two tribes. All taxa found in this study had been previously reported for Ecuador, associated with natural forests and balsa plantations (Martinez et al., 2019).

Diversity indices by agroecosystem

The Shannon index (range: 0.391–0.715) and the Margalef index (range: 1.147–1.600) indicate a low diversity of scolytine taxa associated with a high abundance of Hypothenemus sp. in the six agroecosystems studied (range: 374–2849 individuals) (Table 1). In fact, the Dominance D Index determined values close to one (range: 0.710 to 0.861) which corroborates the dominance of Hypothemus sp. over the rest of the taxa (Table 1). We estimate that our sampling efforts of the scolytine taxa were appropriate. According to Chao 1 Index, the observed taxa (Sobs) were 100% of those expected in Pachinche monoculture farm (PMF), Pachinche agroforestry farm (PAF) and Lodana agroforestry farm (LAF) while it constituted at least 88% of the species in both systems, agroforestry (SAAF) and monoculture farm (SAMF) in Santa Ana and 81% in Lodana monoculture farm (LMF) (Table 1).

 

Table 1: Abundance of taxa by tribes detected in the six cacao agroecosystems.

Tribes/ Taxa	LAF	LMF	PAF	PMF	SAAF	SAMF	Total	%
Corthylini
Corthylus sp. 1	152	59	33	46	15	24	329	3.93
Corthylus sp. 2	2	6	2	43	14	14	81	0.97
Corthylus sp. 3	9	5	8	0	0	1	23	0.27
Corthylus sp. 4	4	4	4	3	0	1	16	0.19
Cryptocarenus sp.	3	0	3	0	0	0	6	0.07
Monarthrum sp.	0	1	0	0	0	0	1	0.01
Ipini
Premnobius cavipennis	108	20	29	40	30	34	261	3.12
Trypophloeini
Hypothenemus sp.	2849	1683	831	918	374	705	7360	87.91
Xyleborini
Coptoborus ochromactonus	5	1	5	0	0	1	12	0.14
Sampsonius sp.	3	1	0	1	0	0	5	0.06
Xyleborus affinis	32	18	16	7	8	27	108	1.29
Xyleborus ferrugineus	25	4	5	7	1	2	44	0.53
Xyleborus spinulosus	36	3	24	17	1	11	92	1.10
Xylosandrus sp.	3	10	6	8	3	4	34	0.41
Total abundance	3,231	1,815	966	1,090	446	824	8,372	100
Taxa (Sobs)	13	13	12	10	8	11	14
Shannon index	0.560	0.391	0.689	0.715	0.685	0.672	0.598
Margalef index	1.485	1.599	1.600	1.287	1.147	1.489	1.439
Dominance_D index	0.781	0.861	0.743	0.714	0.710	0.736	0.775
Chao 1 index	13	16	12	10	9	12.5	14

LAF: Lodana Agroforestry Farm, LMF: Lodana Monoculture Farm, PAF: Pachinche Agroforestry Farm, PMF: Pachinche Monoculture Farm, SAAF: Santa Ana Agroforestry Farm, SAMF: Santa Ana Monoculture Farm.

 

The low diversity observed in agroforestry systems differs from that found by Perez-De la Cruz et al. (2009) who in cacao associated with different fruit and forest trees found values for the Shannon Index that ranged from 2.29 to 2.45, which is higher than that detected in this study. However, these values are similar to those found by Mazón et al. (2013) who estimated values of 0.89 to 1.29 for the Shannon Index in cacao associated with I. edulis as shade tree.

Scolytine communities in the agroecosystems

Although the Shannon and Margalef Index values indicated low diversity, PERMANOVA detected differences among the scolytine communities in the evaluated agroecosystems (Table 2). LAF differed from the rest of the agroecosystems with the highest abundance of scolytines (3,231 individuals) and 13 taxa in total. On the other hand, SAAF exhibited the lowest numbers of scolytines (446 individuals) and taxa (9 taxa). Additionally, the species indicator (IndVal %) (Figure 2) estimated showed that LAF is the agroecosystem that presented the highest number of indicator taxa (six in total) with values ranging from 25.4 to 48.7%, suggesting the preference of these taxa for this agroecosystem.

 

Regarding the abundance of Hypothenemus sp. found in LAF, these results are similar to those reported in other studies, which point out the higher abundance of this genus in a cacao plantation associated with I. edulis trees as shade (Mazón et al., 2013) and in cacao agroecosystems associated with fruit trees and agroforestry (Perez-De la Cruz et al., 2009). However, it contrasts with the findings of Cajaiba et al. (2018) who did not observe individuals of the genus Hypothenemus, while that Xyleborus species were abundant in a cacao monoculture.

The importance of the taxa found in this research is emphasized. Ramos and Montilla (2018) reported Hypothenemus sp. as a pest of cacao beans. Hernandez et al. (2015) reported the species Hypothenemus birmanus (Eichhoff) and Hypothenemus interstitialis (Hopkins) as cacao stem and branch borers. In the tribe Corthylini, four Corthylus species (5.36%), one Cryptocarenus species and one Monarthrum species were observed (Table 1). The genera Corthylus and Monarthrum are classified as ambrosia beetles, while myelophagy is attributed to the genus Cryptocarenus (Kirkendall et al., 2015). Premnobius cavipennis was the only scolytine species detected from the tribe Ipini, accounting for 3.12% of the total species. The genera and species of the tribes Corthylini and Ipini found in the present study had been found in cacao crops in Mexico and Venezuela (Pérez-De La Cruz et al., 2009; Mazón et al., 2013). In Ecuador, P. cavipennis has been reported in both balsa plantations, O. pyramidale (Averos et al., 2021) and in natural forests (Martinez et al., 2019).

Coptoborus ochromactonus Smith and Cognato, Sampsonius sp., three species of Xyleborus and Xylosandrus sp. were the taxa found in the tribe Xyleborini with low percentages of abundance (3.5%). All of these ambrosia beetle species can occasionally kill healthy trees (Kirkendall et al., 2015).

 

Table 2: P-values obtained from Permanova analysis comparing the six agroecosystems.

	Lodana agroforestry farm	Lodana monoculture farm	Pachinche agroforestry farm	Pachinche monoculture farm	Santa ana agroforestry farm
Lodana agroforestry farm
Lodana monoculture farm	0.04695*
Pachinche agroforestry farm	0.000999*	0.1558
Pachinche monoculture farm	0.001998*	0.1888	0.6194
Santa ana agroforestry farm	0.001998*	0.000999*	0.01099*	0.01099*
Santa ana monoculture farm	0.002997*	0.03996*	0.5275	0.5974	0.01998*

* Asterisk when significant (p < 0.05).

 

Coptoborus ochromactonus has been found in Ecuador building galleries in young plants of O. pyramidale with an incidence of 50% and causing 15% tree mortality (Castro et al., 2017). The genus Sampsonius was observed for the first time in Ecuador in 2008 in samples taken from the Amazonian forests (Petrov and Flechtmann, 2013). On agroforestry cacao plantations, Sampsonius sp. has been detected with low percentages of abundance in Mexico (Pérez-De La Cruz et al., 2009) and Venezuela (Mazón et al., 2013).

Xyleborus affinis is an ambrosia beetle that stains the wood when building galleries in timber trees; however, the damage of this insect is restricted to sporadic records and its impact has not been evaluated (Rangel et al., 2012). Xyleborus spinulosus has a range of hosts circumscribed to the Americas (Castrejón-Antonio et al., 2017) and its presence in agroforestry cacao has been reported in Mexico (Pérez-De La Cruz et al., 2009) and Venezuela (Mazón et al., 2013; Navarro and Liendo, 2010). Although X. ferrugineus is the species reported in Ecuador associated with cacao (Paladines-Rezabala et al., 2022), in this study, it reached 0.53% abundance (Table 1). Species of Xylosandrus are reported attacking different organs of the cacao plant (Asman et al., 2021; Delgado and Couturier, 2017; Thube et al., 2022). Xylosandrus compactus was detected building galleries in stems and branches of nursery plants in Peru (Delgado and Couturier, 2017). Xylosandrus crassiusculus (Motschulsky) has been observed causing perforations in cacao pods affected by Helopeltis theivora Waterhouse (Hemiptera: Miridae) in India (Thube et al., 2022). In Indonesia, X. compactus is reported as a major pest in cacao plantations, associated with phytopathogenic fungi (Asman et al., 2021).

Climate variables and abundance of scolytines by agroecosystem

Abundance of scolytines showed a negative correlation with rainfall and temperature, being highly significant in LAF, LMF, SAAF and SAMF (Figure 3). It is important to note that, in the study areas, temperatures are high in the rainy season, which decrease in the dry season (Rivadeneira et al., 2020). With variations in the number of scolytines according to the locality and system, the highest flight activity was observed during the dry season compared to the rainy season (Figure 4). Regarding the fluctuation of the scolytines in dry and rainy seasons, the present results indicate that adults exhibit a greater flight activity in the dry season compared to the rainy season.

 

 

Previous studies have shown that some species of scolytines show greater flight activity in times of low rainfall. Navarro and Liendo (2010) collected samples in cacao farms in marine valleys of the coastal mountain range, Venezuela, which life zone is a tropical dry forest; and found a negative and significant association of populations of X. spinulosus, Hypothenemus erectus LeConte, and Hypothenemus opacus Latreille with precipitation. The scolytine taxa present in a plantation of O. pyramidale in Ecuador showed a high negative correlation with precipitation (Martínez et al., 2019). However, other studies have obtained contrasting results with those detected in this study. Sittichaya et al. (2012) in a study carried out in fruit orchards on the eastern coast of southern Thailand found greater flight activity of xyleborines in the rainy season.

The flight activity of P. cavipennis in plantations of O. pyramidale located in the provinces of Guayas (tropical dry forest), and Los Ríos (tropical humid forest), Ecuador, did not show a significant association with precipitation (Averos et al., 2021). Nevertheless, a positive and highly significant correlation of scolytines with precipitation was detected in the plantation located in Cotopaxi (premontane very humid forest) (Averos et al., 2021).

A study conducted by De Abreu et al. (2012) in a primary forest of the Amazon, Brazil, found no correlation between the abundance of scolytines and precipitation. These researchers indicated that, although previous studies indicate that high rainfall affects the abundance of these insects, there are conflicting results about the effect of rainfall. Hulcr et al. (2008) based on research conducted in two primary forests in northern Thailand reported that species with a circumtropical distribution, such as X. affinis, Xyleborinus andrewesi (Blandford), Xyleborus perforans (Wollaston) and Hypothenemus spp. are not affected by seasonality.

Given that all agroecosystems are located in the same life zone, the differences detected in the scolytine community of the agroecosystems (agroforestry or monoculture) are likely related to the specific characteristics of each site, such as the type of surrounding vegetation, diversification, agronomic management practices, among others. Rodriguez et al. (2017) pointed out that associating native trees in agroforestry systems can favor the survival of scolytines because older and larger trees limit the amount of solar radiation, generating adequate microclimates for the development of these beetles. Hence, the greater abundance of scolytine communities in LAF would be related to the association of cacao with I. edulis, a native tree from South America, unlike other cacao agroforestry systems that are associated with fruit trees.

This study represents a scientific contribution to the diversity and abundance of scolytines found in cacao agroecosystems in Ecuador, where until now only the presence of X. ferrugineus had been reported. It was not unexpected that in a country that is the center of origin of cacao, at least 14 taxa were found associated with this Neotropical plant under anthropic management. Scolytines play important roles in decomposition, nutrient cycling, and ecosystem dynamics. These insects are considered secondary pests because most species feed on dying plants or under conditions of nutritional stress, however, several species can attack healthy trees or play an important role in the transmission of phytopathogenic fungi. Fortunately, in Ecuador, little damage caused by this group of beetles have been reported on cacao so far. It is worth noting that the bioecological characteristics of insect pests, including scolytines, would be influenced by agronomic management practices and climate change, which poses important challenges in cacao agroecosystems.

Conclusions and Recommendations

In this study, the diversity of scolytine taxa was low in both agroforestry and monoculture systems and Hypothenemus sp. was superior to the other species. In spite of this, we found a higher community of scolytines in LAF and a lower one in SAAF. Another important finding was the detection of at least 14 taxa of scolytines associated with cacao agroecosystems, which until now was limited to X. ferrugineus. This represents an important contribution to the knowledge of the diversity of scolytines in Ecuador.

Acknowledgements

Many thanks to Dr. Penny J. Gullan (Australian National University, Canberra, Australia) for kindly reviewing the manuscript. This research was partially funded by a research project No. PYTAUTO3607-2020-FIAG0023 of the Universidad Técnica de Manabí, Ecuador.

Novelty Statement

This article represents an important contribution to the knowledge of the diversity of scolytines in Ecuador. In this study, 14 taxa were observed associated with cacao agroecosystems, a country that is considered the center of origin of the crop and where only a single species had been reported.

Author’s Contribution

Jessenia Castro-Olaya: Conceptualization, data curation, funding acquisition, investigation, methodology, project administration, writing-original draft.

Dorys T. Chirinos: Data curation, investigation, formal analysis, methodology, validation, writing-review and editing.

Takumasa Kondo: Methodology, supervision, validation, visualization, writing-review and editing.

All co-authors reviewed the final version and approved the manuscript before submission.

Conflict of interest

The authors have declared no conflict of interest.

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