BIOLOGICAL CONTROLÐPARASITOIDS AND PREDATORS Predicting Caterpillar Parasitism in Banana Plantations 1 2, 3 2 LEE A. DYER, ROBERT B. MATLOCK, DARYA CHEHREZAD, AND RACHEL O’MALLEY Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118 Environ. Entomol. 34(2): 403Ð409 (2005) ABSTRACT This paper links ecological theory to the biological control of insect pests in banana plantations. Through an established predictive approach, ecological data on tritrophic interactions from natural systems were used to formulate simple recommendations for biological control in banana plantations. The speciÞc goals were (1) to determine the most effective parasitoid enemies for biological control of lepidopteran larvae in banana plantations and (2) to examine the impact of nematicides on enemy populations. To assess percent parasitism, we reared 1,121 lepidopteran larvae collected from six plantations managed under two nematicide regimens. Attack by parasitoids in the families Tachinidae (Diptera), Braconidae, Eulophidae, and Chalcididae (Hymenoptera) closely paralleled rates reported for species with similar characteristics in lowland wet forests, and statistical models predicted the relative importance of these parasitoids as sources of mortality. We found that tachinid ßies were the most important source of early instar larval parasitism in banana plantations, and their importance increased with more intensive nematicide applications. The statistical models that we derived from data on natural systems were useful in predicting which parasitoids would be important in banana and which larval characteristics they would preferentially attack. This approach could be used in other managed ecosystems where the identiÞcation of effective biological control agents is needed. KEY WORDS banana, parasitoids, caterpillar defense model, Tachinidae DESPITE DECADES OF RESEARCH on insect hostÐparasitoid to as the caterpillar defense model. This approach interactions (e.g., Nicholson 1933, Nicholson and relies on strong correlations between pest antiparasi- Bailey 1935, Salt 1934, 1935), ecological entomologists toid defenses and the rates of parasitism those pests have made little progress toward predicting the like- suffer from different parasitoid taxa. Although there lihood of biocontrol success for speciÞc pests. Predic- are many complex factors that affect the success of tion has languished, in part, because of a lack of di- biological control (Fig. 1), Dyer and Gentry (1999) agnostic pest and parasitoid parameters capable of focused on correlations between defenses, rates of forecasting when biological control will be successful parasitism, and success of all recorded programs for (Hawkins et al. 1993). Nevertheless, many authors biological control of lepidopteran pests, and showed have argued that pest characteristics, such as feeding that simple, easily scored information on defensive behavior, are good predictors of biological control traits explained over one-half of the variation in bio- success (Hall and Ehler 1979, Hall et al. 1980, Stiling logical control success. To test this model for banana 1990, Waage 1990, Gross 1991, Hawkins and Gross pests, we used previously published logit models 1992, Hawkins 1993, 1994, Hawkins et al. 1993, (Gentry and Dyer 2002) on natural hostÐparasitoid Hawkins and Cornell 1994, Dyer and Gentry 1999). systems in primary and secondary wet tropical forests Although quantitative predictions of biocontrol based at the La Selva Biological Station, Heredia Province, on models from natural systems are currently rare, Costa Rica (hereafter La Selva), to predict the most they have strong potential to guide biological control successful parasitoid taxa in nearby banana planta- in the future. tions. We also examined whether nematicides altered In this paper, we used data derived from natural the predicted levels of parasitism. We documented systems to construct predictive logit models of para- levels of parasitism in the three most common species sitism rates in banana plantations using methods out- of pest Lepidoptera encountered: Caligo memnon lined by Dyer and Gentry (1999), hereafter referred Felder, Opsiphanes tamarindi Felder (Nymphalidae), and Antichloris viridis Druce (Arctiidae). The work 1 Corresponding author: Ecology and Evolutionary Biology, 310 was conducted in six banana plantations under two Dinwiddie Hall, Tulane University, New Orleans, LA 70118 (e-mail: different pesticide regimens: (1) “conventional,” com- [email protected]). prised of treatments of fungicide-, nematicide-, her- 2 Department of Environmental Studies, San Jose State University, One Washington Square Hall 118, San Jose, CA 95192Ð0115. bicide-, and chlorypyrifos-treated fruit bags, and (2) 3 USDA-APHIS, 4700 River Rd., Riverdale, MD 20737. “moderate-input,” consisting of pesticide treatments 0046-225X/05/0403Ð0409$04.00/0 ᭧ 2005 Entomological Society of America 404 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 2 Caterpillar “defenses” A F Levels of parasitism Other mortality E C B D Successful biological control H G Socioeconomic factors Random factors Fig. 1. Path diagram summarizing potential causal relationships between caterpillar defenses, parasitism rates, and successful biological control. Arrows depict hypothesized causal relationships between variables. Letters next to the arrows represent effect sizes, and those that are most relevant to this study (A, B, CÑalso with thicker arrows) were measured in previous studies. (A) Caterpillar defenses are correlated with parasitism rates; thus, some characters are reliable indicators of higher parasitism rates (e.g., Gentry and Dyer 2002). (B) Hawkins et al. (1993) showed that parasitism rates are highly correlated with successful biological control. (C) Dyer and Gentry (1999) showed that caterpillar defenses were effective predictors of successful biological control. There are many other relevant correlations that were not explored in this study (e.g., DÐH) that are also useful in predicting successful biological control. This study focused on predicting the association between caterpillar defenses and parasitism rates in banana pests. similar to conventional plantations, but reduced in- rupted biological control of the lepidopteran puts of nematicides (Table 1). defoliators by natural enemies, possibly parasitoids Banana (Musa acuminata Colla) is the most popular (see Table 2), causing secondary outbreaks. fruit consumed in the United States, exceeding sales of apples and oranges (USDA 2003), and is one of the Methods most important crops in Costa Rica. Beginning in 1954, extensive aerial applications of dieldrin were sprayed Sampling in Banana Plantations—Parasitism in over 12,000 ha of banana in the GolÞto region of Conventional Versus Moderate-Input Plantations. southwestern Costa Rica to combat the thrips Chaet- Three moderate-input plantations (those with re- anaphothrips orchidii Moulton. Thereafter, secondary duced applications of nematicides) and three conven- outbreaks by our focal caterpillar species and several tional plantations were surveyed. All plantations used other Lepidoptera were frequent until the aerial in- general application rates and dosages of active ingre- secticide treatments (Þrst dieldrin and later carbaryl) dient for fungicides, herbicides, and banana fruit bags were halted in 1973. These Lepidoptera have rarely recommended by Corbana, the Costa Rican govern- exceeded economic thresholds since that time (Ste- mental organization advising the banana industry in phens 1984). Thrupp (1990) suggests that the insec- Costa Rica (Table 3 in Matlock and de la Cruz 2002). ticides applied to banana during the 1950Ð1970s dis- For nematicides, the conventional plantations used at Table 1. Commercial banana plantations used for this study Plantation Region (Canto´n) Area (ha) Nematicide input Caterpillars collected Banaranja Pococõ´ 126 Moderate 489 Casa Pococõ´ 200 Conventional 479 Verde Guadalupe Pococõ´ 200 Conventional 421 Penjamo Sarapiquõ´ 148 Moderate 474 Rebusca Sarapiquõ´ 102 Conventional 424 Yuca Tica Pococõ´ 70 Moderate 511 Conventional plantations used at least Þve applications per year of 6Ð8 kg/ha Terbufos (a nematicide), and the moderate plantations used one application per year of 4Ð5 kg/ha Terbufos. The caterpillars encountered and collected at the plantations were not all successfully reared; thus, numbers collected are not equal to numbers reared. April 2005 DYER ET AL.: PARASITOIDS IN BANANA PLANTATIONS 405 Table 2. Parasitoids attacking focal caterpillar species in ba- underestimates parasitism, missing parasitoids that nana plantations and no. caterpillars parasitized by each emerge in early instars and some that attack later Caterpillars instars and pupae. Voucher specimens of reared adults Caterpillar Parasitoids parasitized were deposited at Tulane University. Model Predictions of Parasitism. Logit models C. memnon Meteorus laphygmae Pemberton 1 (Braconidae: Meteorinae) based on data from previous studies at La Selva (Gen- Brachymeria comitator Walker 1 try and Dyer 2002) were used to predict levels of (Chalcididae) parasitism on our focal caterpillar species by three Blepharipa sp. (Tachinidae) 3 Lespesia aletiae (Tachinidae) 12 broad parasitoid taxa: Tachinidae (Diptera), Bra- O. tamarindi M. laphygmae 1 conidae (Hymenoptera), and Eulophidae (Hymenop- Cotesia sp. (Braconidae: 4 tera) (Table 2). The data for these models were not Microgastrinae) L. aletiae 5 collected in the same year as the validation data. Dif- A.