RESEARCH WORK

Arthropods associated to Jatropha curcas Linnaeus. Functions and strategy for their management

O. Alonso and J. C. Lezcano

Estación Experimental de Pastos y Forrajes Indio Hatuey, Universidad de Matanzas Camilo Cienfuegos, Ministerio de Educación Superior, Central España Republicana. CP 44280, Matanzas, Cuba
E-mail: osmel.alonso@ihatuey.cu

ABSTRACT

At present, Jatropha curcas Linnaeus constitutes one of the most studied plants worldwide due to its potential to produce oil, which can be transformed into biodiesel. However, there is not enough information yet about its ecological interactions with other plants and animals; for which the knowledge concerning the arthropods associated to J. curcas is an essential requisite for the adequate management of the crop. The objective of this paper is to present the results of a compilation made about these organisms (mainly insects, mites and spiders), to contribute to achieve a better exploitation of the plantations of this energy crop in Cuba. Within the group of plant-eaters, 151 insect species were found, among which two from order Hemiptera (Pachycoris klugii Burmeister (Scutelleridae) and Leptoglossus zonatus (Dallas)) stand out, in addition to four mite species. Among the beneficial ones, 90 insect, five mite and 13 predator spider species were found. Regarding pest management strategies, a higher emphasis is made on the chemical control measures and some cultural-type actions. Taking these antecedents into consideration, in Cuba it is essential to know the main organisms associated to this plant, in order to incorporate with higher accuracy the agroecological component in pest management, and thus contribute to the maintenance of the productive capacities of agroecosystems and their resilience.

Key words: plant-eaters, insects, pest.

Jatropha curcas Linnaeus (Euphorbiaceae), commonly known as piñón botija in Cuba (Roig, 1965), is native to Central America and northern South America. Nevertheless, since the 16^th century it was distributed in other tropical regions by European sailors and explorers; and it is disseminated in tropical areas throughout the world, including the Sub-Saharan countries of Africa, the Asian Southeast, India, among others (Van der Putten et al., 2010). In the last decades it has become a very popular plant due to its potentialities and multiple usages, specifically for the particularity of being an oil-producing crop, which can be transformed into biodiesel (Fairless, 2007).

In that sense, this oil easily extractable from its seeds (25-35 % of their content) is also used for energy production, lighting and food cooking. In addition, it is used in medicine, as biopesticide, and in soap elaboration. Besides, the seed press cake obtained as a byproduct of oil extraction can be used as organic fertilizer and for biogas production (Brittaine and Lutaladio, 2010).

According to Quiroga et al. (2010), J. curcas is considered a perennial forest tree, highly rustic, resistant to drought and provider of litter as a source of organic matter. In addition, it is efficient in carbon sequestration and water retention, and can be used in degraded soils and as living fence.

Due to the toxic and biopesticide characteristics of the plant, the pests that affect it do not seem to cause highly significant damage; however, a high incidence of such noxious agents is reported in monocrop plantations. Hence its sensitivity to plant-eaters can depend on the intensity of the actions carried out (Brittaine and Lutaladio, 2010), which should respond to an agroecological pest management (APM) within the agriculture that moves towards sustainable production, according to the criteria expressed by Vázquez and Álvarez (2011).

For such reason, the objective of this paper is to present the results of a compilation made about the main arthropods associated to J. curcas, as well as their functions and the possible strategies for their management, in order to project better the exploitation of plantations of this plant which recently began to be utilized as energy crop in Cuba

In spite of the popular belief that the toxic and insecticide properties of J. curcas are enough to prevent insects from causing economic damage to its plantations, there are several groups that overcome this barrier. These groups are mentioned in a global list of plant-eaters compiled in Australia (where J. curcas is considered an invasive plant), which was integrated by 60 species grouped in 21 families and four orders, according to the report by Shanker and Dhyani (2006), and whose number of plant-eating species was similar to the one found in Chiapas (Mexico) by Quiroga et al. (2010), although not all of them coincide. Yet, in this bibliographic compilation 151 species were found, which represent 131 genera and are grouped into 57 families; as well as eight orders, among which the following stand out: Hemiptera, Coleoptera, Lepidoptera and Orthoptera, with 66, 36, 17 and 13 species, respectively (table 1).

The main species of phytophagous insects considered as pests vary according to the geographical region (Nielsen, 2010). In Africa, specifically in Mozambique, Aphthona dilutipes Jacoby (Coleoptera: Chrysomelidae) prevails; the adults of this species defoliate the crop and its larvae feed on the roots (Gagnaux, 2009). In India (Asia) Scutellera nobilis Fabricius (Hemiptera: Scutelleridae) stands out, causing the fall of the flowers that form the inflorescence, as well as the abortion of fruits and the malformation of the seeds, according to Shanker and Dhyani (2006). In Oceania (Australia), these last authors cite other species of the same family, Agonosoma trilineatum (Fabricius), which causes severe damage to the seed. Also, in the Asian and African continents, the cited authors make emphasis on the presence of Stomphastis (=Acrocercops) thraustica (Meyrick) (Lepidoptera: Gracillariidae), that feeds on the inflorescences.

On the other hand, in Central and South America (particularly in Nicaragua and Honduras) the existence of the hemipterans Pachycoris klugii Burmeister (Scutelleridae) and Leptoglossus zonatus (Dallas) (Coreidae), which remarkably damage developing fruits, is reported (Alfonso, 2008; Grimm and Maes, 2008). Besides, in Brazil, Saturnino et al. (2005) report the presence of the hemipterans Empoasca spp. (Cicadellidae) (from which some species are vectors or virus-transmitters), that affect considerably the leaves, and Pachycoris torridus (Scopoli) (Scutelleridae), that damages fruits.

Regarding phytophagous mites, four species that belong to the order Trombidiformes, suborder Prostigmata were related: 1) Polyphagotarsonemus latus (Baks) (Tarsonemidae), 2) Tetranychus sp., 3) Tetranychus bastosi Tuttle, Baker & Sales, and 4) Panonychus citri McGregor, which are found in Australia, Brazil, United States, Republic of Cape Verde and Italy, and affect the leaf shoots and flower buds. The last three ones (from the family Tetranychidae) damage the leaves, mainly on the underside, in Brazil (Grimm and Maes, 1997; De Arruda et al., 2005; Vedana, 2006; Dos Santos et al., 2007; Carels, 2009; Sarmento et al., 2011; Erazo (s.f.) and Contran et al., 2013); and it should be emphasized that P. latus causes remarkable economic loses in that country (Saturnino et al., 2005).

With regards to beneficial arthropods, they were grouped into 103 species: 90 of insects separated into 37 predators, 21 parasitoids and 32 pollinators, taking into consideration that the predator Polistes sp. (Hymenoptera: Vespide) is also a pollinator (table 2) and 13 of spiders (predators), number that exceeds the 65 species -40 of insectivores and spiders, and 25 pollinators found in Chiapas (Mexico) by Quiroga et al. (2010).

On the other hand, as another result of this compilation (table 2) it could be observed that there is a prevalence of insect species belonging to the orders Hymenoptera (18 parasitoids, 11 predators and four pollinators), Coleoptera (11 pollinators and 5 predators), Lepidoptera (represented by 16 pollinators) and Hemiptera (including 13 predators). Within that group of insects, according to the criteria expressed by Grimm and Maes (1997), Gagnaux (2009), Quiroga et al. (2010) and Contran et al. (2013), a remarkable group of insectivores to which reference is made below, stands out.

The hemipterans of the family Reduviidae Apiomerus pictipes Herrich-Schaeffer and Rocconota sp., as well as the stink bug Euthyrhynchus floridanus (Linnaeus), constitute predators of nymphs and adults of the shield-backed bug P. klugii. In addition, Procheiloneurus sp. (Encyrtidae) and Telenomus (=Pseudotelenomus) pachycoris (Costa-Lima) (Scelionidae) are hymenopterans which parasite the eggs of such pest, and the latter is also a pest of P. torridus.

Likewise, an unidentified dipteran species hymenopteran Brancon hebetor Say (Braconidae) and undetermined species from the family Tachinidae are cited, as parasitoids of the snout moth P. morosalis. In addition, reference is made to: the parasitoid of eggs from the leaf-footed bug L. zonatus, the hymenopteran Gryon sp. (Scelionidae); the parasitoid of different thrip species, Megaphragma sp. (Hymenoptera: Trichogrammatidae); and the aphid predator, the coleopteran Hippodamia sp.

Other examples are the predator Oplomus pulcher (Dallas) (Hemiptera: Pentatomidae) and the parasitoid Brachymeria sp. (Hymenoptera: Chalcididae), which control the populations of A. monuste; although this last insectivore also feeds on the owlet moths Remigia latipes Gueneé and Spodoptera frugiperda (Smith). On the other hand and undetermined species is cited (Hymenoptera: Scelionidae) which, in addition to being a parasitoid of S. frugiperda, equally controls the hemipteran N. viridula and the acridic orthopterans.

Meanwhile, five species of the family Phytoseiidae, present in Brazil, were compiled as predator mites: Amblyseis herbicolus (Chant), Euseius concordis Chant, Iphiseiodes zuluagai Denmark & Muma, Neoseiulus californicus (McGregor) and N. idaeus Denmark & Muma. They are predators of the thread-footed mite P. latus, but the second and third species are also predators of the spider mite T. bastosi (Dos Santos et al., 2007; Sarmento et al., 2011).

Likewise, the 13 species of predator spiders found are included in seven families: Araneidae (Gasteracantha cancriformis (L.) and Micrathena sp.); Eresidae (Stegodyphus sp., predator of the jewel bug S. nobilis); Oxyopidae (Peucetia viridans (Hentz), predator of the stink bug N. viridula; P. longipalpis F. O. P.-Cambridge and Hamataliwa flebilis F. O. P.-Cambridge); Philodromidae (Apollophanes sp.); Salticidae (unidentified species, predator of nymphs of the shield-backed bug P. klugii; Lyssomanes diversus Galinao and Thiodina sp.); Tetragnathidae (Leucage sp., predator of the jewel bug C. variabilis) and Thomisidae (unidentified species, predator of nymphs of the leaf-footed bug L. zonatus; and Misumenoides sp.). The third species is distributed in India; while the first, second, fourth, eighth, eleventh and twelfth are found in Nicaragua; and the others in Mexico (Grimm and Maes, 1997; Shanker and Dhyani, 2006; Quiroga et al., 2010).

The main strategy for the phytosanitary pest management in J. curcas is integrated pest management IPM (Gagnaux, 2009). Several examples are shown below.

In the case of the leaf beetle A. dilutipes, the first element that should be taken into consideration is the management of the planting date (in order to evade the initial emergence of adults); then, the performance of deep plowing, taking into consideration the dormancy of the larval state at remarkable depths in the soil, to expose larvae to predators, sun rays and the physical damage with agricultural tools. On the other hand, the use of biopesticides of botanical origin, available in the different localities, is possible, specifically those obtained from plants of the family Meliaceae which are very effective for the control of chewing insects such as lepidopterans and coleopterans; as well as those of microbial origin based on Beauveria bassiana (Bals.-Criv.) Vuill. Finally, the use of synthetic (conventional) pesticides is recommended: Carbaryl pH 80 % (at 2 g/l^-1 or 0,7 kg ha^-1), Cymbush CE 25 % (at 0,5 mL L^-1 or 0,2 L ha^-1), Basudine CE 60 % (at 2 mL L^-1 or 0,7 L ha^-1), among others.

For the control of the leaf miner of J. curcas the lepidopteran S. thraustica, as main measure, and the chemical pesticides Mospilan PS 20 % (at 40 g 100 L of water^-1), Disyston GR 5 % (at 30 g 100 L of water^-1 m^-1 of the tree height), are recommended, among others. Nevertheless, Quiroga et al. (2010) report that there are diverse natural enemies of this pest that can regulate its populations, for example: seven-spotted ladybug (Coccinelidae), green lacewings (Chrysopidae), assassin bugs (Reduviidae), tiny wasps (Encyrtidae), spiders and predator ants.

Likewise, for the hemipterans P. klugii and L. zonatus the use of chemicals is suggested as main control measure, among them: the insecticides Monarca SE 11,25 % and Karate CE 2,5 % in doses of 360-500 mL ha^-1 (Alfonso, 2008). However, it is possible to use insectivores as an effective biological measure, as it was mentioned above when the beneficial insects (predators and parasitoids) and the predator spiders found in this compilation were addressed.

Nevertheless, it is evident that taking phytosanitary measures in a preventive way, such as the ones proposed by Nielsen (2010), would be an important contribution for the management of J. curcas plantations; among these measures are:

The use of resistant varieties or, at least, the utilization of plants as "mother plants" for seed and cutting production.

J. curcas should not be planted when the pest incidence is intense, especially at the end of the rainy season, when the temperature and relative humidity are high; because the infestation rates can be higher years after the plant has been sown.

To avoid dense J. curcas plantations and massive pest outbreaks it is necessary to widen the planting frame; to cultivate in small fields separated and isolated from each other in the landscape; to sow on the edges, instead of in the plots; and to cultivate J. curcas associated to other species.

To use the biopesticides obtained from J. curcas to be applied to young plants, because it is then that they have a lower toxin concentration.

In addition, it is necessary to take into consideration that in the sites of J. curcas plantations, the most important element is the agroecological management of the farm, because it means to act on the causes for which organisms that are noxious for plants become pests and affect the crops present in it, every time they are sown. Hence it is necessary to understand that the farm must be managed as a system, precisely to reduce the causes of pest appearance. This is basic and constitutes an important part of the success in pest suppression, which, regrettably, is not considered in intensive production systems and much less in monocrops (Vázquez, 2011).

According to the compiled information to elaborate this review, it can be concluded that there is a large number of arthropods associated to the J. curcas crop. Among the plant-eating organisms considered as potential pests, the insects of the order Hemiptera and four mite species stand out. Among the beneficial ones (mainly predators, parasitoids and pollinators), the insects of the order Hymenoptera stand out, in addition to five species of predator mites and the predators spiders of the families Oxyopidae and Salticidae with three species each.

Regarding the pest management strategies, higher emphasis is made on the chemical control measures and some cultural-type actions, which indicates the importance of establishing programs of selection of local lines (accessions) and breeding, in accordance with their performance and adaptation in the regions that produce J. curcas; the use of certified seeds; the timely determination of the economic threshold level; as well as the agroecological management of the farm: from the organic and innocuous nutrition (through compost, organic manures, and others of this kind) to the phytosanitary protection based on biological products; the physical, mechanical, cultural control and with the minimum use of conventional chemicals, for example, using herbicides only at the beginning of the establishment of the plantation, if it is necessary.

For such reasons, and taking into consideration these antecedents, in Cuba it is essential to know the main organisms associated to this recently-introduced plant for the production of oil and its conversion into biodiesel; and, based on these experiences, to incorporate more accurately the agroecological component in pest management, and thus achieve sustainable land management, related to the socioeconomic development of the country, with the maintenance of the productive capacities of agroecosystems and their resilience.

The authors thank the contribution made by the Doctors of Science Jesús Suárez Hernández and Rey L. Machado Castro, regarding the bibliographic information provided.