Impact of natural enemies on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics in Chiapas, Mexico

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Biological Control 51 (2009) 51–60

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Impact of natural enemies on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics in Chiapas, Mexico J. Refugio Lomeli-Flores a,1, Juan F. Barrera b, Julio S. Bernal a,* a b

Department of Entomology, Biological Control Laboratory, Texas A&M University, MS 2475, College Station, TX 77843-2475, USA El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto, Km 2.5 Tapachula, Chiapas 30700, Mexico

a r t i c l e

i n f o

Article history: Received 11 September 2008 Accepted 25 March 2009 Available online 13 June 2009 Keywords: Biological control Life tables Formicidae Eulophidae Braconidae Predation Parasitism Coffea arabica

a b s t r a c t Coffee leafminer, Leucoptera coffeella, is a pest in many New World coffee growing areas. Previous studies suggested that its population dynamics were strongly affected by natural enemies, particularly of larvae, and physical environmental conditions. Our study documented through field surveys and life table analyses (i) the natural enemy complex associated with coffee leafminer and (ii) the impacts of natural enemies on the population dynamics of coffee leafminer, on coffee (Coffea arabica) at two elevations and two rainfall levels in the Soconusco region of Chiapas, Mexico. Twenty-two larval parasitoid species (including 14 morphospecies) were collected. Egg and pupal parasitoids were not recovered. Life table analyses showed that parasitism contributed 610% of real mortality, and parasitism rates were 8–10-fold higher at the low (950 m) elevation; parasitism rates were similar under low (400 mm) rainfall. Seventeen predator species (including five morphospecies) were collected, of which most were ants (Formicidae, 14 species) that contributed >58% of real mortality. Life table analyses showed that predation rates were higher at high versus low elevation and under high versus low rainfall. Independently of elevation and rainfall, egg predation (likely by ants) was the most important source of indispensable mortality (range = 0.13–0.30), except at low elevation and high rainfall where pupal predation (=0.14) was similarly important. Also, predation was the main source of coffee leafminer larval and pupal mortality during a 13-month period in a low elevation coffee farm and was highest during the rainy season (>400 mm rainfall/month), when coffee leafminer prevalence was highest. Overall, predation of eggs and pupae (the latter particularly at low elevation), mostly by ants, were the most important sources of coffee leafminer mortality. Because ants were the main source of coffee leafminer egg and pupal mortality, their importance and potential role in coffee pest management strategies were discussed. Ó 2009 Elsevier Inc. All rights reserved.

1. Introduction Coffee leafminer, Leucoptera coffeella (Guérin-Ménèville) (Lepidoptera: Lyonetiidae), is a nocturnal microlepidopteran whose larvae are known only from Coffea species (Mendoza, 1995; Ramiro et al., 2004). Previous studies addressing the effects of coffee plant characteristics on coffee leafminer distribution and abundance showed that coffee leafminer prevalence was positively correlated with leaf age (= position on a branch) and nitrogen content (Lomeli-Flores et al., unpubl. data), and oviposition with leaf caffeine concentrations (Magalha~es et al., 2008). In addition, laboratory studies showed that coffee leafminer larvae grew larger, developed faster, and survived better on leaves with moderate nitrogen levels compared to leaves with low or high nitrogen levels, and on tough * Corresponding author. Fax: +1 979 845 5926. E-mail addresses: [email protected], [email protected] (J.S. Bernal). 1 Permanent address: Instituto de Fitosanidad, Colegio de Postgraduados, Km 35.5 carretera México-Texcoco, Montecillo, Edo. de México 56230, Mexico. 1049-9644/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2009.03.021

versus soft leaves (Walker and Quintana, 1969; Nantes and Parra, 1977; Guerreiro-Filho, 2006; Lomeli-Flores et al., unpubl. data), though adult females did not generally select such leaves for oviposition in laboratory experiments (Lomeli-Flores et al., unpubl. data). Under field conditions, natural enemies and weather variables may have stronger influences than coffee plant characteristics on the distribution and abundance of coffee leafminer (Heisswolf et al., 2005). Indeed, prior studies assessing the impacts of different mortality factors suggested that coffee leafminer population dynamics were strongly affected both by natural enemies (Flórez and Hernández, 1981; Gravena, 1983; Campos et al., 1989; Paliz and Mendoza, 1993; Pereira et al., 2007; de la Mora et al., 2008), and environmental conditions prevalent at different elevations (e.g., Souza et al., 2003; Lomeli-Flores et al., unpubl. data). Previous studies of coffee leafminer documented a diverse suite of natural enemies, including at least 26 genera and 30 species of larval parasitoids, all Eulophidae or Braconidae (Hymenoptera), though no egg or pupal parasitoids were documented (Parra

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et al., 1977; Souza, 1979; Villacorta, 1980; Aranda-Delgado, 1986; Gallardo, 1988; Flórez and Hernández, 1981; Mendoza, 1995; Lomeli-Flores et al., unpubl. data). A compilation of predator species from previous studies includes at least six genera and 11 species of Vespidae (Hymenoptera), one morphospecies (an unidentified species clearly distinguishable from others by its morphology) of Formicidae (Hymenoptera), and two of Chrysopidae (Neuroptera), all predatory on larvae; predators of pupae or eggs have not been reported (Enriquez et al., 1975; Parra et al., 1977; Tozatti and Gravena, 1988; Mendoza, 1995; Fragoso et al., 2002; Carvalho et al., 2002, 2005; Fernández and Bueno, 2002). However, most studies overtly ignored mortality of coffee leafminer eggs and pupae, focusing exclusively on larvae (e.g., Parra et al., 1977; Villacorta, 1980; Aranda-Delgado, 1986; Reis et al., 2000), though one study and observations preliminary to our study showed that eggs and pupae suffered high mortality rates due to predation (Pereira et al., 2007; Lomeli-Flores et al., unpubl. data). Coffee leafminer appears to be a secondary pest of coffee in Mexico because it is of concern only in occasional years or on specific farms, but few studies have assessed the impact of natural enemies on its population dynamics. Previously, it was noted in Brazil that the intensity and frequency of coffee leafminer outbreaks increased dramatically with the introduction of improved coffee varieties, which required greater agrochemical use and full-sun conditions (Fragoso et al., 2002), and that such outbreaks were due, in part, to faster coffee leafminer development and lower mortality due to natural enemies (Guharay et al., 2001). ArandaDelgado (1986) conducted the single known survey of coffee leafminer parasitoids in Mexico, but primarily focused on larval parasitoids, and largely in Veracruz state, which is located on the Gulf of Mexico coast. In prior studies in the Soconusco area of Chiapas state, located on Mexico’s Pacific coast, coffee leafminer occurred at higher densities in low (1000 m) elevation farms (Lomeli-Flores et al., unpubl. data), but it was unclear whether the difference was due to natural enemies or other environmental variables associated with elevation. Thus, for Mexico further research on the impacts of natural enemies on coffee leafminer population dynamics is needed, and targeting all leafminer developmental stages at different elevations and under varying weather conditions. Data derived from such research are necessary to improve evolving coffee IPM strategies (e.g., Barrera et al., 2000; Segura et al., 2004). Thus, our study sought to: (i) identify the parasitoid and predator complexes associated with coffee leafminer and assess their impacts on coffee leafminer population dynamics, and (ii) contrast the impacts of natural enemies on coffee leafminer population dynamics at two elevations and two rainfall levels, representing contrasting environmental conditions in the Soconusco region of Chiapas, Mexico.

2. Materials and methods 2.1. Study area Studies were conducted on three arabica-coffee (Coffea arabica L.) farms representing two elevations in the municipality of Cacahoatán, Chiapas, Mexico: El Encanto (14° 590 2100 N; 92° 090 5500 W; 480 m) and La Gloria (15° 000 0700 N; 92° 090 2400 W, 550 m), representing low elevation farms, and Alpujarras (15° 040 2400 N; 92° 100 1100 W, 960 m) representing high elevation farms. All three farms were traditionally managed. That is, the farms were planted with tall coffee varieties and a high density of shade trees (e.g., Inga spp.), had a minimal use of agrochemical inputs, and the fruits were hand-harvested as they matured. Shade cover was 38–87% in the low elevation farms and 45–91% in the high elevation farm. Rainfall amounts and patterns were similar at the

low and high elevation farms: yearly rainfall was >4000 mm, with a December–March dry season (rainfall < 100 mm/month), and an April–November rainy season (>200 mm/month) (Comisión Nacional del Agua, 2006). Yearly average temperature was 26.2 ± 0.2 °C at low elevation and 22.6 ± 0.3 °C at high elevation. The main coffee varieties on these farms were Borbon, Typica, and Catuai, but all studies involved Catuai plants. Insecticides were not used in any of the farms during the study period. All leaf samples to recover coffee leafminer or natural enemies were collected randomly (height, cardinal direction) from coffee plants. 2.2. Natural enemy complex associated with coffee leafminer Two hundred leaves with active coffee leafminer mines, and 100 coffee leafminer pupae were collected monthly at one low elevation (El Encanto) and the high elevation farm (Alpujarras) from June 2003 to July 2004 to document the parasitoid community associated with coffee leafminer. In addition, sporadic collections of leaves were made during the summers (May–July) of 2003– 2005 in these and other coffee farms in the Soconusco region to recover as many parasitoid species as possible. All leaves were taken to the laboratory and examined under a microscope at 25 magnification to confirm that mines were active or contained coffee leafminer pupae. All coffee leafminer eggs, larvae, and pupae recovered from leaves were incubated individually (on or within a portion of the corresponding leaf) in 5 cm diam petri dishes until adult parasitoids or adult leafminers emerged. Adult parasitoids were killed in 80% ethanol upon emergence and properly mounted for subsequent identification. Parasitoid specimens were identified to genus using the keys of Gibson et al. (1997), Burks (2003) and Wharton et al. (1997). Parasitoid species were identified using specific keys: Hansson (1987, 1997) for Chrysocharis; Hansson (1994) for Closterocerus; Hansson (1997) for Neochrysocharis; Yoshimoto (1983) for Pnigalio; Gordh (1978) for Zagrammosoma; and van Achterberg (1995) for Stiropius. A preliminary survey of potential predators of coffee leafminer was conducted in mid-July 2005. Thirty coffee plants were randomly selected in a low elevation farm (La Gloria), and all predators found on each plant during a 10-min per plant observation period were collected, including ants living inside coffee twigs or branches. Also, any arthropod observed preying on coffee leafminers during the parasitoid surveys described above was collected, though few collections were made in this manner due to a likely short interaction time between predators and coffee leafminer prey. Collected predators were killed in 80% ethanol and properly mounted for subsequent identification. The specimens thus collected, almost exclusively ants (see Section 3), were identified to genus using the keys of Mackay and Mackay (2004). Predators were collected also by exposing ‘‘sentinel” coffee leafminer eggs, larvae, and pupae on coffee plants to collect predators during the last week of July 2005 at a low elevation farm (La Gloria). Sentinel coffee leafminers were reared at El Colegio de la Frontera Sur (hereafter ECOSUR), Tapachula, Chiapas, Mexico, on detached coffee leaves, following Reis et al. (2000), with minor modifications. Sentinels were exposed on each of 10 coffee plants by stapling three coffee leaves with mature mines (mined area >4 cm2), three with coffee leafminer eggs (83% of the specimens recovered. Though 50% of the total number of specimens were collected at one of the low elevation farms (El Encanto), and 10% at the high elevation farm (Table 1), almost the same numbers of species/morphospecies were recovered at both elevations, 18 and 19, respectively; Allobracon sp. (45 specimens) was recovered only in the low elevation farm. All parasitoid specimens recovered from coffee leafminer were larval parasitoids, and most were recovered from mines (78%, 18 species or morphospecies), though some emerged from coffee leafminer larvae within cocoons (22%, four species or morphospecies). Primary parasitoids (18 species or morphospecies) represented 82% of the species recovered, secondary parasitoids were not recovered, and likely facultative secondary parasitoids (four species or morphospecies) were infrequent. Egg or pupal parasitoids were not recovered. 3.1.2. Predators Thirteen ant (Formicidae) species were recovered from the 30 coffee plants that were sampled (Fig. 1). The most frequent ant species were Pseudomyrmex simplex (Smith) (on 60% of the plants), Nesomyrmex echinatinodis (Forel) (37%), and Brachymyrmex sp.

(30%). The remaining 10 ant species were present on 0.9 larvae/leaf during most (June–October) of the 2003 rainy season, and was highest in June–July of the 2004

Table 1 Parasitoid species and numbers of specimens per species recovered from coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) from coffee farms in the Soconusco region of Chiapas, Mexico, June, 2003–July 2005. Genus/species

Habitb

No. of specimens (%) by locality

Total

Alpujarras N 15° 040 2400 W 92° 100 1100 960 m

El Encanto N 14° 590 2100 W 92° 090 5500 480 m

Othera

Eulophidae Cirrospilus spp.c Closterocerus spp.c C. cinctipennis Ashmead Elachertus spp.c Horismenus spp.c Miotropis sp. Neochrysocharis spp.c N. arvensis Gram. N. chalybea Hansson N. formosa (Westwood) Pnigalio spp.c P. sarasolai De Santis Zagrammosoma lineaticeps (Girault) Z. multilineatum (Ashmead)

L, L, L, L, L, L, L, L, L, L, L, L, L, L,

FS, Ec PP, En FS, En PP, Ec PP, Ec PP, Ec PP, En PP, En PP, En FS, En PP, Ec PP, Ec PP, Ec PP, Ec

2 (2.5) 26 (32.9) 1 (1.3) 2 (2.5) 3 (3.8) 3 (3.8) 10 (12.7) 1 (1.3) 3 (3.8) 1 (1.3) 6 (7.6) 3 (3.8) 0 (0) 1 (1.3)

4 (1.0) 11 (2.8) 35 (8.9) 16 (4.1) 8 (2.0) 3 (0.8) 98 (24.9) 13 (3.3) 7 (1.8) 27 (6.9) 28 (7.1) 17 (4.3) 0 (0) 30 (7.6)

15 (4.7) 20 (6.3) 7 (2.2) 29 (9.1) 2 (0.6) 0 (0) 87 (27.3) 14 (4.4) 13 (4.1) 10 (3.1) 39 (12.2) 5 (1.6) 1 (0.3) 32 (10.0)

21 (2.7) 57 (7.2) 43 (5.4) 47 (5.9) 13 (1.6) 6 (0.8) 195 (24.7) 28 (3.5) 23 (2.9) 38 (4.8) 73 (9.2) 25 (3.2) 1 (0.1) 63 (8.0)

Braconidae Allobracon sp. Stiropius letifer (Mann)

L, PP, En L, PP, En

0 (0) 17 (21.5)

45 (11.5) 51 (13.0)

0 (0) 45 (14.1)

45 (5.7) 113 (14.3)

79 (10)

393 (49.7)

319 (40.3)

791

Total (% specimens) a b c

Localities where collections were unsystematic. L, larval parasitoid; PP, primary parasitoid; FS, facultative secondary parasitoid; Ec, ectoparasitoid; En, endoparasitoid. Includes at least two morphospecies.

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30

(a) Eggs

0.6

Proportion (+ SE)

25 20 0.4

15 10

0.2

5 0.0 P. sim Br N. pl ac ec ex hy hi m na yr . m S. ex pi A cea C . ve . a lo bs x C C . s cisu re tr s m ia at tu o C ga s . p st l e C ana r ep tu P. ha s el lot o n es P. gat u S. gra s ge cili M min s .f a lo ta r Bl icol at a Sa tar lti ia ci da e

0

Fig. 1. Predatory species collected in a 10 min period per each of 30 coffee plants in a low elevation farm (La Gloria, 550 m), Cacahoatán, Chiapas, Mexico, July, 2005. Bars show the proportion of coffee plants on which each species was collected. N. echina. = N. echinatinodis; see Table 2 for complete names of species.

Table 2 Predator species observed preying on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) eggs, larvae, or pupae in the Soconusco region of Chiapas, Mexico, including 16 h each of diurnal and nocturnal observation in a low elevation coffee farm (La Gloria, 550 m), Cacahoatán, July, 2005.

20 15 10 5

Larva

Pupa

30

X X X

0

(c) Pupae X X

X X X X

25 20

X X X

X X X X X X X X X

Includes two morphospecies.

rainy season (1.2 larvae/leaf). The lowest coffee leafminer density, 0.1, occurred during the dry season (December 2003–February 2004) (Fig. 3a). Total larval mortality was highest during the rainy season and declined during the dry season (Fig. 3b). Predation was the mortality factor that most influenced the dynamics of total larval mortality, followed by parasitism and FOPP (Table 3). Total pupal mortality, which was not measured during most of the dry season, was highest during rainy-season months (>0.45, except July 2004), and lowest during a dry-season month, March 2004 (Fig. 3c). Predation was the factor that most influenced the dynamics of total pupal mortality, followed by FOPP, and parasitism (Table 3). 3.3. Contribution of natural enemies to coffee leafminer mortality at two elevations and rainfall levels Coffee leafminer total real mortality was lowest at low elevation under low rainfall (Table 4a), followed by low elevation under high

15 10 5 0 .a b P. scis gr us P. ac sim ilis p P. A. lex el ve on lo N gat x .e u ch s Bl ina at . Sa tar lt ia C Cep icid re h ae Br ma alo ac tog tes hy as m t C yr er .p m l e C ana x . s tu M tria s . f tu lo s ri c S. S. ola ge pic m ea in at a

a

25

Coffee leafminer stage used as prey Egg

Vespidae unidentified Formicidae Azteca velox Forel Camponotus abscisus Roger Camponotus planatus (Roger) Camponotus striatus Smith Cephalotes sp. Crematogaster spp.a Nesomyrmex echinatinodis (Forel) Monomorium floricola (Jerdon) Pseudomyrmex simplex (Smith) Pseudomyrmex elongatus (Mayr) Pseudomyrmex gracilis (F.) Solenopsis picea (Emery) Solenopsis geminata (F.) Blattaria unidentified Salticidae (Arachnida) unidentified

(b) Larvae

C

Genus/species

Predation events (frequency)

Predator species

30

Predator species Fig. 2. Predation events by individual predator species on sentinel coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) eggs (a), larvae (b), and pupae (c). Predation frequencies are from 384 point (5 s) observations during 16 h of diurnal and 16 h of nocturnal observations (July, 2005) in a low elevation coffee farm (La Gloria, 550 m), Cacahoatán, Chiapas, Mexico. Predator species with nil frequencies are species known to occur in coffee farms in the study area (see Table 2), though they were not observed during the 32 h of observation. All but two events (Blattaria, one Cephalotes) were recorded during daytime. N. echina. = N. echinatinodis; see Table 2 for complete names of species.

rainfall (Table 4b), and highest at high elevation independently of rainfall level (Table 5a and b) (G = 137.25, df = 3, P  0.001). Egg predation contributed the most to total mortality rates independently of elevation and rainfall levels (Fig. 4); independently of rainfall level, egg predation contributed >90% of total mortality at

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Coffee leafminers per leaf

1.4

(a)

1.2 1.0 0.8

Dry season Coffee leafminer density Total mortality Predation Parasitism FOPP

0.6 0.4 0.2 0.0

Larval mortality (Proportion + SE)

1.0

(b)

0.8

0.6

0.4

0.2

0.0

Pupal mortality (Proportion + SE)

1.0

(c) Col 21 Plot 2 Zero Month vs LaParasitized Month vs LaPredated Month vs LaOther Month vs LaMort

0.8

0.6

0.4

0.2

03 Au g0 3 Se p0 3 O ct 03 N ov 03 D ec 03 Ja n0 4 Fe b0 4 M ar 04 Ap r0 4 M ay 04 Ju n0 4 Ju l0 4

Ju l

Ju n

03

0.0

Month Fig. 3. Coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics (larvae/leaf) (a), and dynamics of larval (b) and pupal (c) within-stage total mortality, and mortality due to predation, parasitism, or factors other than predation or parasitism (FOPP) (all mortality shown as within-stage proportion ± SE) at a low elevation farm (El Encanto, 480 m), Cacahoatán, Chiapas, Mexico. The dry season (85% of arthropod biomass in forest canopies (Davidson et al., 2003), and may be the most important source of insect mortality in tropical rainforests (Way and Khoo, 1992; Floren et al., 2002; Armbrecht and Perfecto, 2003). Correspondingly, ants are one of the most abundant groups of arthropods in traditionally managed coffee farms (Ramos-Suarez et al., 2002; Armbrecht and Perfecto, 2003; Philpott and Foster, 2005), where they likely are important sources of herbivore mortality (Lachaud et al., 1995; Bustillo et al., 2002). Previous studies in Chiapas coffee farms uncovered at least 26 ant species associated with coffee plants, most of them with predatory habits (Armbrecht and Perfecto, 2003; Philpott and Foster, 2005). While those studies did not investigate the impacts of ants on populations of coffee pests, our study documented 14 ant species predating coffee leafminer, and four addi-

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tional species present on coffee plants. One recent investigation conducted in a Soconusco region coffee farm showed a significantly negative relationship between abundance of arboreal, twig-nesting ants and coffee leafminer prevalence on coffee plants (de la Mora et al., 2008). The results of that investigation coincide with our results in that twig-nesting ants, in the genera Pseudomyrmex, Nesomyrmex, Camponotus, and Azteca, were the most frequently observed on coffee plants (Fig. 1), and most frequently seen preying on coffee leafminer (Fig. 2). Overall, the results of our study support prior suggestions (e.g., Perfecto and Snelling, 1995; Philpott and Foster, 2005; de la Mora et al., 2008) that ants are important predators of coffee pests, including coffee leafminer. While several studies suggested that parasitism was the main mortality factor determining coffee leafminer distribution and abundance (e.g., Flórez and Hernández, 1981; Gravena, 1983; Aranda-Delgado, 1986; Campos et al., 1989; Paliz and Mendoza, 1993), the results of our study suggested that in the Soconusco region, predation is more important than parasitism. However, though the results of our study showed that total mortality due to parasitism represented 1/4 of that due to predation, it is likely that we did not fully quantify the impact of the parasitoids. Under field conditions, predation of previously parasitized coffee leafminer (e.g., Reis et al., 2000) and destructive parasitoid host feeding (Urbaneja et al., 2001) are difficult to quantify, though they likely affected the parasitoid contribution to total coffee leafminer mortality, as measured in our study. Previous studies showed that weather conditions influenced coffee leafminer distribution and abundance, and those of its natural enemies (Reis et al., 1976; Villacorta, 1980; Nestel et al., 1994; Pereira et al., 2007). The life table analyses of our study showed that total mortality rates were higher in the high versus the low elevation farm, and that mortality rates at high elevation were not affected by rainfall levels, whereas mortality rates at low elevation were higher under high versus low rainfall. Moreover, reproductive rates per generation (R0), calculated from the life table results (Tables 4 and 5) and a lifetime fecundity value of 41.9 eggs/female (at constant 25 °C in the laboratory, LomeliFlores et al., unpubl. data), are near replacement values in the high elevation farm (R0 = 0.7 under low rainfall, and R0 = 0.9 under high rainfall), whereas they are doubling to quadrupling values in the low elevation farm (R0 = 2.3 under low rainfall, and R0 = 4.5 under high rainfall). In addition, prior studies showed that coffee leafminer fecundity was near nil at 20 °C but increased with temperatures >20 °C (Parra et al., 1995; Lomeli-Flores et al., unpubl. data), and that while rainfall levels and patterns were similar in high and low elevation Chiapas farms, average temperatures were consistently higher (by 4 °C) in low elevation farms (Lomeli-Flores et al., unpubl. data). Together, these results suggested that lower average temperatures may partially account for the lower coffee leafminer densities in the high elevation farm: Lower temperatures in the high elevation farm likely decreased coffee leafminer fecundity and lengthened its developmental time, thus reducing its reproductive rate and prolonging its exposure to natural enemies and other mortality factors. Overall, the results of our study showed that predation of eggs and pupae were the main sources of coffee leafminer mortality in the Soconusco region of Chiapas, Mexico, and suggested that ants were the main source of coffee leafminer egg and pupal mortality. In high elevation coffee farms, it is likely that high levels of indispensable egg mortality by predators coupled with cool temperatures lead to lower reproductive rates per coffee leafminer generation in comparison with low elevation farms. The results of our study are in line with hypotheses pointing to ants as the most important mortality factor affecting herbivore populations in tropical systems (e.g., Way and Khoo, 1992). Moreover, some authors recommended augmenting ant populations to increase

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predation rates and reduce pest population densities in coffee farms (Philpott and Foster, 2005). At the same time, other authors showed that ants interfered with the actions of other natural enemies and were associated with higher pest populations suggesting that biological control of coffee pests could be enhanced by reducing ant densities (Reimer et al., 1993; Infante et al., 2003). The results of our study point to the importance of ants for biological control of coffee leafminer, and to the potential of managing ant populations for enhancing biological control in low elevation farms. However, because our study was limited in scope (e.g., 13month population dynamics, three farms), more work is needed to ascertain the net impact of ants on pests, and herbivores generally, including coffee leafminer, in Chiapas coffee farms before advocating their manipulation within the framework of evolving IPM programs for coffee. Acknowledgments We thank Messrs. Joel Herrera M., Enrique López P. Román Montes, Guillermo López G., and Heber García (all at ECOSUR) for their help with the work conducted in Chiapas, Mexico, and Federico Ochoa (Finca Alpujarras), Alejandro Álvarez (Finca La Gloria), Humberto Prada (Finca El Encanto), and Joaquín Erhlich (Finca Lindavista) for permission to work on their farms. We also thank Eduardo Aránda Delgado (Terranova Lombricultores, Xalápa, Mexico) for lending his collection of coffee leafminer parasitoids, Drs. James Woolley and Robert Wharton (both at TAMU) for their help in identifying coffee leafminer parasitoids, and Dr. Jorge Valenzuela and Mr. Luis Quiroz Robledo (both at Instituto de Ecología, Xalapa, Mexico) for their help in identifying ants. Also, the critical reviews of the manuscript by Drs. Carlos Bográn, Roel López, R. Wharton, J. Woolley (all at TAMU), Les Ehler (University of California, Davis), and two anonymous reviewers helped us produce an improved final version. We greatly appreciate the timely assistance of Editor Dr. Harry Kaya who expedited the manuscript’s handling after significant early delays, for which he was not responsible. This work was supported in part by CONACyT (Mexico) (Doctoral Fellowship to JRLF, #91539), El Colegio de la Frontera Sur (Fundación Produce-Chiapas project Bioecología y manejo de plagas del café en el Soconusco y Sierra de Chiapas), Texas Agri-Life Research (Hatch Project H-8707), Texas A&M University-CONACyT Collaborative Research Grants Program, and Colegio de Postgraduados.

References Aranda-Delgado, E., 1986. Control Natural del Minador de la Hoja del Cafeto en México, Leucoptera coffeella (Guer-Men 1842) (Lep-Lyonetiidae). Bachelor’s thesis Universidad Veracruzana, Xalapa, Veracruz, Mexico. Armbrecht, I., Perfecto, I., 2003. Litter-twig dwelling ant species richness and predation potential within a forest fragment and neighboring coffee plantations of contrasting habitat quality in Mexico. Agriculture, Ecosystems and Environment 97, 107–115. Barrera, J.F., Infante, F., de la Rosa, W., Castillo, A., Gómez, J., 2000. Control biológico de broca del café. In: Badii, M.H., Flores, A.E.L.J., Galan, W. (Eds.), Fundamentos y perspectivas de control biológico. Universidad Autónoma de Nuevo León, Mexico, pp. 211–229. Bellows, T.S., van Driesche, R.G., 1999. Life table construction and analysis for evaluating biological control agents. In: Bellows, T.S., Fisher, T.W. (Eds.), Handbook of Biological Control: Principles and Applications of Biological Control. Academic Press, San Diego, CA, pp. 199–223. Burks, R.A., 2003. Key to the Nearctic genera of Eulophidae, subfamilies Entedoninae, Euderinae, and Eulophinae (Hymenoptera Chalcidoidea). University of California, Riverside, CA, 92521; USA. Available from: (accessed December 2005). Bustillo, A.E., Cardenas, R., Posada, F.J., 2002. Natural enemies and competitors of Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae) in Colombia. Neotropical Entomology 31, 635–639. Campos, O.G., Decazy, B., Carrillo, E., 1989. Dinámica poblacional del minador de la hoja del cafeto Leucoptera coffeella y sus enemigos naturales en la zona de Nuevo San Carlos, Retalhuleu, Guatemala. Turrialba 3, 393–399.

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Carvalho, C.E., Silva, R.A., Louzada, J.N.C., Morales, J.C., Barbosa, L.R., Ambrogi, B.G., 2002. Predation of eggs, and larvae, and pupae of coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) by Chrysoperla externa (Hagen, 1861) (Neuroptera: Chrysopidae). Ciencia Agrotecnologica. Lavras 26, 318–324. Carvalho, G.A., Miranda, J.C., Moura, A.P., Rocha, L.C.D., Reis, P.R., Vilela, F.Z., 2005. Controle de Leucoptera coffeella (Guérin-Ménèville and Perrottet, 1842) (Lepidoptera: Lyonetiidae) com insecticides granulados e sus efeitos sobre vespas predadoras e parasitoids. Arquivos do Instituto do Biologia Sao Paulo 72, 63–72. Comisión Nacional del Agua, 2006. Normales climatológicas estándar y provisionales 1961–1990. Comisión Nacional del Agua, Subdirección General Técnica, Unidad del Servicio Meteorológico Nacional, Mexico. Available from: (accessed 20.11.06). Davidson, D.W., Cook, S.C., Snelling, R.R., Chua, T.H., 2003. Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300, 969–972. de la Mora, A., Livingston, G., Philpott, S.M., 2008. Arboreal ant abundance and leaf miner damage in coffee agroecosystems in Mexico. Biotropica 40, 742– 746. Enriquez, E., Bejarano, S., Vila, V., 1975. Morfología, ciclo de vida y comportamiento de Leucoptera coffeella Gue.-Men. Revista Peruana de Entomología 18, 79–81. Fernández, O.A., Bueno, A.F., 2002. MIP-Café. Available from: . (accessed 20.01.05). Floren, A., Biun, A., Linsenmair, K.E., 2002. Arboreal ants as key predators in tropical lowland rainforest trees. Oecologia 131, 137–144. Flórez, E., Hernández, M.R., 1981. Fluctuación de la población del minador de las hojas del cafeto, Leucoptera coffeella y de sus enemigos naturales en el Valle del Cauca. Revista de la Sociedad Colombiana de Entomología 7, 29–38. Fragoso, D.B., Jusselino-Filho, P., Guedes, R.N.C., Porque, R., 2001. Seletividade de inseticidas a vespas predadoras de Leucoptera coffeella (Guer-Menev.) (Lepidoptera: Lyonetiidae). Neotropical Entomology 30, 139–144. Fragoso, D.B., Guedes, R.N.C., Picanco, M.C., Zambolim, L., 2002. Insecticide use and organophosphate resistance in the coffee leaf miner Leucoptera coffeella (Lepidoptera: Lyonetiidae). Bulletin of Entomological Research 92, 203–212. Gallardo, C.F., 1988. Faunal survey of the coffee leafminer, Leucoptera coffeella, parasitoids in Puerto Rico. Journal of Agriculture of the University of Puerto Rico 72, 255–263. Gibson, G.A.P., Huber, J.T., Woolley, J.B., 1997. Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). NRC Research Press, Ottawa, Ontario, Canada. Gordh, G., 1978. Taxonomic notes on Zagrammosoma, a key to the Nearctic species and descriptions of new species from California (Hymenoptera: Eulophidae). Proceedings of the Entomological Society of Washington 80, 344–359. Gravena, S., 1983. Tácticas de manejo integrado do bicho mineiro do cafeeiro Perileucoptera coffeella (Guerin-Meneville, 1842): I. Dinamica populacional e inimigos naturals. Anais da Sociedade Entomologica do Brasil 12, 61–71. Guerreiro-Filho, O., 2006. Coffee leaf miner resistance. Brazilian Journal of Plant Physiology 18, 109–117. Guharay, F., Monterroso, D., Staver, C., 2001. El diseño y manejo de la sombra para la supresión de plagas en cafetales de América Central. Agroforesteria en las Américas 8, 22–29. Hansson, C., 1987. Revision of the New World species of Chrysocharis Förster (Hymenoptera: Eulophidae). Entomologica Scandinavica Supplement 31, 1–87. Hansson, C., 1994. Re-evaluation of the genus Closterocerus Westwood (Hymenoptera: Eulophidae), with a revision of the Nearctic species. Entomologica Scandinavica 25, 1–25. Hansson, C., 1997. Survey of Chrysocharis Förster and Neochrysocharis Kurdjumov (Hymenoptera, Eulophidae) from Mexico, including eight new species. Miscellania Zoologica (Barcelona) 20, 81–95. Heisswolf, A., Obermaied, E., Poethke, H.J., 2005. Selection of large host plants for oviposition by a monophagous leaf beetle: nutritional quality or enemy-free space. Ecological Entomology 30, 299–306. Infante, F., Mumford, J., García-Ballinas, A., 2003. Predation by native arthropods on the African parasitoid Prorops nasuta (Hymenoptera: Bethylidae) in coffee plantations of Mexico. Florida Entomologist 86, 86–88. Lachaud, J.P., Ibarra, G., García, J.A., López, J.A., Moreno, M., 1995. Impacto de depredación de dos hormigas ponerinas y de algunas arañas tejedoras en los agroecosistemas de café en el Soconusco, Chiapas, México. Memoria del XVIII Congreso Nacional de Control Biológico, Tapachula, Chiapas, México. pp. 105– 106. Mackay, W.P., Mackay, E.E., 2004. Clave de los géneros de de hormigas en México (Hymenoptera: Formicidae). Available from: (accessed 10.07.04). Magalha~es, S.T.V., Guedes, R.N.C., Demuner, A.J., Lima, E.R., 2008. Effect of coffee alkaloids and phenolics on egg-laying by the coffee leaf miner Leucoptera coffeella. Bulletin of Entomological Research 98, 483–489. Mendoza, M.J., 1995. El Minador de la Hoja del Café Perileucoptera cofeella y su Control. Instituto Nacional Autónomo de Investigaciones Agropecuarias, Boletín divulgativo No. 247. Estación Experimental Tropical Pichilingue, Ecuador. Monterrey, J., Suarez, D., Gonzalez, M., 2001. Comportamiento de insectos en sistemas agroforestales con café en el Pacífico sur de Nicaragua. Agroforesteria en las Americas 8, 15–21. Nantes, J.F.D., Parra, J.R.P., 1977. Queda de folhas em mudas de tres variedades de café, provocadas por Perileucoptera coffeella (Guérin-Ménèville) [Lepidoptera: Lyonetiidae]. Agros 12, 55–58.

Nestel, D., Dickschen, F., Altieri, M.A., 1994. Seasonal and spatial population loads of a tropical insect: the case of the coffee leaf-miner in Mexico. Ecological Entomology 19, 159–167. Noyes, J.S., 2003. Universal Chalcidoidea Database. Available from: (accessed 20.01.07). Paliz, V., Mendoza, J., 1993. Plagas del cafeto. In: Sotomayor, H.I. (Ed.), Manual del Cultivo del Café. Estación Experimental Pichilingue, Quevedo, Ecuador, pp. 144– 166. Parra, J.R.P., Gonçalves, W., Gravena, S., Marconato, A.R., 1977. Parasites e predadores do bicho-mineiro do cafeeiro, Perileucoptera coffeella (GuérinMénèville, 1842). Anais da Sociedade Entomologica do Brasil 6, 138–143. Parra, J.R.P., Haddad, M.L., Silveira Neto, S., 1995. Tabela de vida de fertilidade de Perileucoptera coffeella (Guérin-Ménèville, 1842) (Lepidoptera: Lyonetiidae) em tre s temperaturas. Revista Brasileira de Entomologia 39, 125–129. Pereira, E.J.G., Picanco, M.C., Bacci, L., Crespo, A.L.B., Guedes, R.N.C., 2007. Seasonal mortality factors of the coffee leafminer, Leucoptera coffeella. Bulletin of Entomological Research 97, 421–432. Perfecto, I., Snelling, R., 1995. Biodiversity and the transformation of a tropical agroecosystem: ants in coffee plantations. Ecological Applications 5, 1084– 1097. Philpott, S.M., 2005. Changes in arboreal ant populations following pruning of coffee shade-trees in Chiapas, Mexico. Agroforestry Systems 64, 219–224. Philpott, S.M., Foster, P., 2005. Nest-site limitation in coffee agroecosystems: artificial nest maintain diversity of arboreal ants. Ecological Applications 15, 1478–1485. Ramiro, D.A., Guerreiro-Filho, O., Queiroz-Volta, R.B., Matthiesen, S.C., 2004. Caracterizacao anatomica de folhas de caffeiros resistentes e suscetiveis ao bicho-mineiro. Bragantia 63, 363–372. Ramos-Suarez, M.P., Morales, H., Ruiz-Montoya, L., Soto-Pinto, L., Rojas-Fernandez, P., 2002. Se mantiene la diversidad de hormigas con el cambio de bosque mesófilo a cafetales? Revista Protección Vegetal, Actas del Simposio Café y Biodiversidad 12, 17–30. Reimer, N.J., Cope, M.L., Yasuda, G., 1993. Interference of Pheidole megacephala (Hymenoptera: Formicidae) with biological control of Coccus viridis (Homoptera: Coccidae) in coffee. Environmental Entomology 22, 483–488. Reis, R.P., Gomez, L.J., Souza, L.J., 1976. Fluctuacao populacional do ‘‘bicho mineiro” das folhas do cafeeiro, Perileucoptera coffeella (Lep: Lyonetiidae), nas regioes caffeiras do Estado de Minas Gerais e identificacao de inimigos naturais. Congreso Brasileiro de Pesquisas Cafeeiras, vol. 4. Resumenes, Caxambú, Brasil. pp. 105–106. Reis Jr., R., Lima, E.R., Vilela, E.F., Barros, R.S., 2000. Method for maintenance of coffee leaves in vitro for mass rearing of Leucoptera coffeellum (GuérinMénèville) (Lepidoptera: Lyonetiidae). Anais da Sociedade Entomologica do Brasil 29, 849–854. Segura, H.R., Barrera, J.F., Nazar, A., Morales, H., 2004. Farmers’ perceptions, knowledge and management of the coffee pests and diseases and their natural enemies in Chiapas, Mexico. Journal of Economic Entomology 97, 1491–1499. Southwood, T.R.E., 1978. Ecological Methods, with Particular Reference to the Study of Insect Populations. Chapman & Hall, London. Souza, J.C., 1979. Levantamento, identificacao e eficencia dos parasitoi do ‘‘bichomineiro” das folhas do cafeeiro, Perileucoptera coffeella (Guérin- Ménèville, 1842) no Estado de Minas Gerais. p. 91. Thesis M.S. Piracicaba, Escuela Superior de Agricultura Luíz de Queiroz, Brasil. Souza, T., de Oliveira, R.N., Carvalho, G., Magalhaes, L.C., 2003. Ocorrencia de bichomineiro do cafeeiro (Leucoptera coffeella) influenciada pelo periodo estacional e pela altitude. Acta Scientiarum: Agronomy 25, 119–124. Tozatti, G., Gravena, S., 1988. Natural mortality factors of Perileucoptera coffeella Guérin-Ménèville (Lepidoptera, Lyonetiidae) on coffee in Jaboticabal State of Sao Paulo, Brazil. Científica 16, 179–187. Urbaneja, A., Llácer, E., Garrido, A., Jacas, J., 2001. Effect of variable photoperiod on development and survival of Cirrospilus sp. nr. lyncus (Hymenoptera: Eulophidae), an ectoparasitoid of Phyllocnistis citrella (Lepidoptera: Gracillariidae). Florida Entomologist 84, 305–307. Van Achterberg, C., 1995. Generic revision of the subfamily Betylobraconinae (Hymenoptera: Braconidae) and other groups with modified fore tarsus. Zoologische Verhandelingen 298, 1–242. Villacorta, A., 1980. Alguns factores que afetam a populacao estacional de Perileucoptera coffeella Guerin-Meneville, Norte do Parana, Londrina Pr. Anais do Sociedad Entomologica do Brasil 9, 23–32. Walker, D.W., Quintana, V., 1969. Mating and oviposition behavior of the coffee leaf miner, Leucoptera coffeella (Lepidoptera: Lyonetiidae). Proceedings of the Entomological Society of Washington 71, 88–90. Way, M.J., Khoo, K.C., 1992. Role of ants in pest management. Annual Review of Entomology 37, 479–503. Wharton, R.A., Marsh, P.M., Sharkey, M.J., 1997. Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special Publications of the International Society of Hymenopterists 1, London, United Kingdom. Whitfield, J.B., 1988. Revision of the Nearctic species of the genus Stiropius Cameron (=Bucculatriplex Auct.) with the description of a new related genus (Hymenoptera: Braconidae). Systematic Entomology 13, 373– 385. Yoshimoto, C.M., 1983. Review of North American Pnigalio Schrank (Hymenoptera: Eulophidae). Canadian Entomologist 115, 971–1000. Zar, J.H., 1996. Biostatistical Analysis, vol. 622. Upper Saddle River, Prentice Hall, London, UK.