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 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 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 in the families Tachinidae (Diptera), , Eulophidae, and Chalcididae () 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 encountered: Caligo memnon lined by Dyer and Gentry (1999), hereafter referred Felder, Opsiphanes tamarindi Felder (Nymphalidae), and 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 ( 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 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. viridis M. laphygmae 76 ferent predictions for each parasitoid taxon were Cotesia sp. 2 made based on caterpillar traits, using models in Gen- B. comitator 7 try and Dyer (2002). For model predictions and ba- Elachertus sp. (Eulophidae: 20 Eulophinae) nana plantation data, we scored the following cater- L. aletiae 129 pillar traits (for more detailed methods, see Gentry and Dyer 2002): (1) primary defensive behavior (gre- gariousness versus solitary feeding; exposed feeding least Þve applications per year of 6Ð8 kg/ha Terbufos versus shelter building), (2) secondary defensive be- (American Cynamid, Princeton Junction, New Jer- havior (no behavioral response versus thrashing, sey), and the moderate plantations used one applica- dropping, biting, regurgitating, or freezing in response tion per year of 4Ð5 kg/ha Terbufos. Actual dates of to a natural enemy), and (3) caterpillar morphology pesticide applications and exact dosage information (spines or hairs versus no morphological defense). All were not provided by managers of any of the planta- of these characteristics may act as defensive mecha- tions. The plantations were all of similar sizes (con- ϭ Ϯ ϭ Ϯ nisms, and combinations of these defenses are good ventional 167 33 ha, moderate 115 23 ha; predictors of parasitism by different taxa of enemies Table 1), sites were spatially interspersed in a broadly (reviewed by Edmunds 1974, DeVries 1987, Evans and fragmented landscape, sampling effort was identical Schmidt 1991, Godfray 1994, Dyer 1995, Gentry and among sites, and all plantations supported similar cat- Dyer 2002). Only caterpillar traits previously found to erpillar densities (conventional ϭ 441 Ϯ 19 individuals collected, moderate ϭ 491 Ϯ 11 individuals collected; successfully predict parasitism were used as explana- Table 1). Sampling was conducted 8 d/mo (by two tory variables in statistical analyses. people) during January to March 2002 and August to To generate model predictions, a dichotomous re- October 2002. Parasitism levels in forests and other sponse variable (parasitized versus not parasitized) banana plantations in the region are consistently high, was included in logit models with caterpillar traits as with little variation between years (Gentry and Dyer predictor variables. Each caterpillar record in the La 2002; L.A.D., unpublished data), thus we assumed that Selva database was treated as a random sample from a a single year of data for model validation would be population of individuals with a speciÞc combination sufÞcient. All caterpillars in third or later instars that of defensive characteristics (e.g., group feeding, hairy were encountered along haphazardly selected caterpillar that thrashes). Separate model predictions transects were collected and reared following the were generated for each of the three families of para- methods of Gentry and Dyer (2002). This method sitoids. Parasitoid families were ranked if the 95% CIs

Table 3. Predictions generated by logit models from Gentry and Dyer (2002) along with observed levels of parasitism in banana plantations

Predicted ranking of Observed parasitism in Logit modelsa Caterpillar species parasitoid controlb banana plantations ln͓PT͔ϭ1.2 ϩ 0.4G ϩ 0.2S ϩ 0.3GSM Caligo memnon (Nymphalidae) 1. Tachinidae TachinidaeÑ4% 2. Braconidae BraconidaeÑ1% 3. Eulphidae EulophidaeÑ0 ln͓PB͔ϭ1.9 ϩ 0.6B ϩ 0.6G Ϫ 0.2BM ϩ Opsiphanes tamarindi (Nymphalidae) 1. Tachinidae TachinidaeÑ9% 0.5BS ϩ 0.5SM Ϫ 0.7BG ϩ 0.3GMS 2. Braconidae BraconidaeÑ9% 3. Eulophidae EulophidaeÑ0 ln͓PE͔ϭ2.8 ϩ 1.1G ϩ 0.7BS Ϫ 1.2BG (Arctiidae) 1. Tachinidae TachinidaeÑ22% 2. Braconidae BraconidaeÑ15% 3. Eulophidae EulophidaeÑ4%

a Logit models are derived from data reported in Gentry and Dyer (2002). b Different ranking numbers indicate no overlap in 95% CIs of predictions. Although ranked predictions are the same for the three species, the rank orders are different for Lepidoptera with other characteristics. PT, tachinid parasitism; PB, braconid parasitism; PE, eulophid parasitism; G, group versus solitary feeding; S, shelter builder versus exophytic; M, smooth integument versus spiny or hairy; B, behavioral defenses versus no response to enemy contact. 406 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 2 of predictions did not overlap. The relevant equations lected in another study conducted in the same plan- for generating predictions are presented in Table 3. tations for C. memnon (30 Ϯ 15 in the Þeld), but higher Model Validation. Logit model predictions for par- for O. tamarindi (5 Ϯ 4 in the Þeld) (Stireman et al. asitism in the three focal species of Lepidoptera were 2004). Predation on these two species measured from compared with data for caterpillars collected in ba- the same life history experiment was higher than par- nana plantations. Data were analyzed using linear re- asitism, but other sources of mortality were inconse- gression, with predicted percent parasitism as a con- quential. Antichloris viridis was the only species par- tinuous independent variable and actual levels of asitized at levels (34%; Hawkins and Cornell 1994, parasitism as the response variable. A set of traits Dyer and Gentry 1999) considered high enough to be unique to each caterpillar species was used as a pre- correlated with effective biological control (Table 3). dictor variable in the previously published logit mod- The caterpillar defense logit models from studies in els (see equations in Table 3) to predict parasitism for the forest at La Selva predicted that tachinids would the three most abundant parasitoid families in banana rank Þrst and that braconids and eulophids would separately. This approach yielded nine predictions usually rank second and third in parasitism for each of and observations (three parasitism levels ϫ three cat- the three species of banana Lepidoptera studied (Ta- erpillar species). ble 3). Observed levels of parasitism for caterpillars The caterpillar defense model predicts parasitism collected from banana plantations were consistent from pest defensive characteristics rather than from with these predictions. The regression uncovered a empirical measurements of parasitism levels for a pest signiÞcant relationship between predicted and ob- ϭ ϭ 2 ϭ species in its natural range (as recommended by served parasitism (F1,8 16.5, P 0.005, R 0.70, Hawkins et al. 1993), because such measurements are slope ϭ 1.2; Fig. 2). Levels of parasitism in the forest unavailable for most pests. However, because data on for three species of Lepidoptera that occurred both in parasitism levels from La Selva were available for sev- plantations and at La Selva successfully predicted par- eral banana pest species, we also used levels of forest asitism on each pest by tachinids, braconids, and eu- parasitism to predict parasitism in plantations for those lophids and by all parasitoids combined, this regres- species, as a standard of comparison for our validation sion explaining less of the variance in parasitism than ϭ ϭ of the Dyer-Gentry model. Simple least-squares re- the caterpillar defense model (F1,11 15.0, P 0.003, gression was used for this analysis, with percent par- R2 ϭ 0.60, slope ϭ 0.93). asitism in the forest serving as the independent vari- The total proportion of parasitism by parasitic Hy- able and observed parasitism in the banana plantations menoptera was lower in conventional (32%) versus as the response variable. moderate-input (68%) plantations, whereas the op- Parasitism–Nematicide Associations. Matlock and posite was found for dipteran parasitoids: 74% of de la Cruz (2002) found greater abundance and di- dipteran parasitism occurred in conventional and 26% versity of hymenopteran parasitoids in plantations in moderate-input farms. This three-way interaction with reduced inputs of pesticides versus conventional (parasitism by parasitoid order by nematicide) was plantations. To test the hypothesis that nematicides signiÞcant (␹2 ϭ 42.3, df ϭ 1, P Ͻ 0.0001) in the modify the community of natural enemies attacking parsimonious loglinear model that statistically Þt the lepidopteran larvae in banana plantations, we used a data (␹2 ϭ 0.3, df ϭ 1, P ϭ 0.9). Because tachinids were nonhierarchical log-linear model that included ob- the most important source of parasitoid mortality, served parasitism, parasitoid order, and nematicide overall parasitism was signiÞcantly higher in conven- use as potentially associated variables. The speciÞc tional (29%) versus moderate-input plantations (20%; hypothesis tested by this model was that nematicides ␹2 ϭ 9.8, df ϭ 1, P ϭ 0.002). Despite these differences, alter parasitism by parasitic Hymenoptera more than parasitism rankings (Table 3) were not different in by Diptera (Tachinidae). Each datum in the model conventional versus moderate-input plantations. was a single reared caterpillar. Discussion Results It is clear that recognizing the similarities between We reared 680 A. viridis, 319 C. memnon, and 62 O. natural and managed systems will facilitate improved tamarinidi larvae, 260 of which were parasitized. Al- management of both (Kareiva 1996, Murdoch and though these were the most common lepidopterans Briggs 1996, Waage 1990). Our study in banana shows encountered in the plantations, 60 individuals from that the caterpillar defense model, derived from hostÐ three other species were also reared. Parasitoids at- parasitoid data for primary and secondary lowland wet tacking the three focal banana pests included tachinid tropical forests, is predictive for pests in banana plan- ßies and braconid, eulophid, and chalcidid wasps (Ta- tations. Any attempts to manage for continued sup- ble 2). Tachinids were the most important source of pression of Lepidoptera outbreaks in Costa Rican ba- parasitism (N ϭ 149) at all plantations, followed by nana should take the natural associations between braconids (84), eulophids (20), and chalcidids (8), a caterpillar defenses and levels of parasitism by differ- parasitism proÞle similar to that found in lowland wet ent insect taxa into account. The approach outlined forest at La Selva (Gentry and Dyer 2002; L.A.D., here can also be expanded to predict levels of preda- unpublished data). Percent parasitism was similar to tion (Dyer 1997, Dyer and Gentry 1999), which is also that obtained in experimental life history data col- potentially an important component of biological con- April 2005 DYER ET AL.: PARASITOIDS IN BANANA PLANTATIONS 407

Fig. 2. Regression of actual parasitism values (proportion of hosts parasitized) by tachinids, braconids, and eulophids against levels of parasitism predicted from models. Predictions were derived by applying logit models to data from natural ecosystems, using characteristics unique to each of three focal caterpillar species as predictor variables. For each caterpillar species, levels of parasitism were predicted for each of the three parasitoid families detected in plantations, yielding N ϭ 9 comparisons. For label legends: 1 ϭ C. memnon,2ϭ O. tamarindi,3ϭ A. viridis;aϭ Tachinidae, b ϭ Braconidae, c ϭ Eulophidae. trol in Costa Rican banana plantations (Stireman et al. Dognin (Limacodidae), and parasitism by braconids 2004). and tachinids should be equal in importance for Our results are fairly limited, considering the high Talides sinois Hu¨ bner (Hesperiidae) (Table 4). It is diversity of Lepidoptera and natural enemies found in also possible that some lepidopteran herbivores in banana plantations and in surrounding natural sys- banana plantations suffer more predation than para- tems. An expanded test of the caterpillar defense sitism, although this is not the case for C. memnon model would allow for extensive predictions of para- (Stireman et al. 2004). sitism and predation by a diverse guild of predators In our study, tachinids seem to be important sources and parasitoids on at least 20 species of pest Lepidop- of mortality for Costa Rican banana pests, but based on tera that occur in Costa Rican banana plantations previous predictive models (Hawkins et al. 1993, Dyer (Lara 1964, 1965, 1966, 1970, Ostmark, 1974, Stephens and Gentry 1999), are only potentially controlling A. 1984, H. Garcia, D.C., and L.A.D., unpublished data). viridis. This correlation between parasitism and suc- While we predicted that tachinids would be the most cessful control is not perfect, and our measures of important source of parasitoid mortality for all three parasitism are not comprehensive (egg parasitoids and species studied here, this is not the case for all Lep- those attacking later stages are ignored with this meth- idoptera in banana (Table 4). For example, parasitism od); thus, it is possible that tachinids control all three should be greatest by braconids for Acharia hyperoche pests. To fully examine control of these herbivores, the roles of all parasitoid taxa, predators, pathogens, and Table 4. Percent parasitism predictions (with SE in parenthe- other sources of mortality must be examined. With the ses) for common species of Lepidoptera found in Costa Rican data at hand, it is impossible to conclude whether banana plantations based on the logit models presented in Table 3 banana pest Lepidoptera are controlled by natural Caterpillar Predicted parasitisma enemies (Thrupp 1990), but when our results are combined with life tables that rank parasitism as the Acharia hyperoche (Limacodidae) BraconidaeÑ70.0 (7.3) EulophidaeÑ53.3 (4.9) most important source of mortality (Stireman et al. TachinidaeÑ19.7 (1.9) 2004), it seems as if tachinids play a central role in the Hypercompe laeta Walker (Arctiidae) TachinidaeÑ19.7 (1.9) control of A. viridis. According to model predictions, BraconidaeÑ4.8 (1.2) EulophidaeÑ2.6 (0.7) pests with the same traits as A. viridis should also Talides sinois (Hesperiidae) TachinidaeÑ25.7 (2.2) experience high tachinid parasitism and may be suc- BraconidaeÑ24.4 (2.4) cessfully controlled. Other pests in banana, however, EulophidaeÑ12.2 (1.8) are equally or more likely to be controlled by other enemies (Table 4). a One individual host can support multiple parasitioid taxa (Gentry and Dyer 2002); thus, overall parasitism is not the sum of parasitism There are many factors that could lessen the effec- by families. tiveness of this simple predictive approach. For ex- 408 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 2 ample, many complex aspects of parasitoid biology are Evans, D. L., and J. O. Schmidt. 1991. Insect defenses: adap- not accounted for in this model, such as the broad host tive mechanisms and strategies of prey and predators. range of Lespesia aletiae Riley and the effects of al- University of New York Press, Albany, NY. ternative hosts on parasitoid population dynamics; Gentry, G., and L. A. Dyer. 2002. On the conditional nature these aspects could alter parasitoid rankings. Nemati- of neotropical caterpillar defenses against their natural cide use did not alter observed parasitoid rankings, but enemies. Ecology. 83: 3108Ð3119. the different effects on Hymenoptera versus Diptera Godfray, H.C.J. 1994. Parasitoids: behavioral and evolution- ary ecology. Princeton University Press, Princeton, NJ. suggest that success of our approach could be very Gross, P. 1991. Inßuence of target pest feeding niche on sensitive to variation in management strategies. Mat- success rates in classical biological control. Environ. En- lock and de la Cruz (2002) found negative effects of tomol. 20: 1217Ð1227. chlorpyrifos and organophosphate and carbamate ne- Hall, R. W., and L. E. Ehler. 1979. Rate of establishment of maticides on hymenopteran parasitoid diversity in ba- natural enemies in classical biological control. Bull. En- nana plantations. In this study, we also found a neg- tomol. Soc. Am. 25: 280Ð282. ative association between high nematicide use and Hall, R. W., L. E. Ehler, and B. Bisabri-Ershadi. 1980. Rates hymenopteran parasitism rates of banana caterpillars. of success in classical biological control of . It is possible that parasitic Hymenoptera are more Bull. Entomol. Soc. Am. 26: 111Ð114. sensitive to nematicides than tachinids, but the posi- Hawkins, B. A. 1993. Parasitoid species richness, host mor- tive association between tachinid parasitism and pes- tality, and biological control. Am. Nat. 141: 634Ð641. ticide use would require further study. Hawkins, B. A. 1994. Pattern and process in host-parasitoid interactions. Cambridge University Press, Cambridge, In conclusion, tachinid ßies are important sources of UK. mortality for lepidopteran pests in banana plantations, Hawkins, B. A., and H. V. Cornell. 1994. Maximum parasit- and this importance increases with more intensive ism rates and successful biological control. Science. 266: applications of nematicides. 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