Journal of Science: Vol. 12 | Article 63 Morais et al.

Lepidopterans as potential agents for the biological control of the invasive plant, Miconia calvescens

Elisangela G.F. Morais1a*, Marcelo C. Picanço2b, Altair A. Semeão2c, Robert W. Barreto3d, Jander F. Rosado2e, and Julio C. Martins2f

1Embrapa Roraima - Brazilian Agricultural Research Corporation's, Boa Vista, Roraima, Brazil 2

Department of Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil Downloaded from 3Department of Fitopathology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil

Abstract This work investigated eight species of associated with Miconia calvescens DC. (Myrtales: Melastomataceae) in Brazil, including six defoliators, Salbia lotanalis Druce http://jinsectscience.oxfordjournals.org/ (Lepidoptera: Pyralidae), Druentia inscita Schaus (Mimallonidae), Antiblemma leucocyma Hampson (Noctuidae), three Limacodidae species, a fruit borer Carposina cardinata Meyrick (Carposinidae), and a damager of flowers Pleuroprucha rudimentaria Guenée (Geometridae). Based on host specificity and the damage caused to plants, S. lotanalis and D. inscita are the most promising species for biological control of M. calvescens. Furthermore, if C. cardinata and P. rudimentaria have host specificity in future tests, these caterpillars could also be considered as appropriate biocontrol agents. by guest on November 14, 2015

Keywords: caterpillar, host specificity, leaf roller, Salbia lotanalis, weed Correspondence: a [email protected], b [email protected], c [email protected], d [email protected], e [email protected], f [email protected], *Corresponding author Editor: J.P. Michaud was editor of this paper. Received: 14 June 2011, Accepted: 24 October 2011 Copyright : This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 12, Number 63 Cite this paper as: Morais EGF, Picanço MC, Semeão AA, Barreto RW, Rosado JF, Martins JC. 2012. Lepidopterans as potential agents for the biological control of the invasive plant, Miconia calvescens. Journal of Insect Science 12:63 available online: insectscience.org/12.63

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al.

Introduction damaging M. calvescens, including Salbia lotanalis Druce (Lepidoptera: Pyralidae) Exotic plant species can become great threats (mistakenly identified as Ategumia sp.), to the biodiversity of natural environments Druentia inscita Schaus (Mimallonidae) and and require expensive strategies for their Antiblemma leucocyma Hampson control. In most cas control with herbicides (Noctuidae). and removal is expensive and inefficient. In some cases, integration of biological control Several species of Lepidoptera have been and other strategies are also recommended. extensively used in the biological control of However, prior to the introduction, several invasive plants (Hight et al. 2002; Baars 2003; steps are required, such as a survey of Ostermeyer and Grace 2007; Boughton and feeding on the plant in its region of origin, and Pemberton 2009), and others have been an evaluation of damage and host specificity considered as potential agents (Dhileepan et Downloaded from of selected candidate agents (Morin et al. al. 2007). The major case of success was the 2009). introduction of Cactoblastis cactorum Miconia calvescens DC. (Myrtales: Bergroth (Lepidoptera: Pyralidae), a species Melastomataceae) is a severe weed found in native to Argentina that was introduced http://jinsectscience.oxfordjournals.org/ rainforest ecosystems on oceanic islands throughout the world for control of weedy (Medeiros et al. 1997), and is classified Opuntia spp. (Caryophyllales: Cactaceae) among the one hundred worst invasive species (Pettey 1948). Among the main around the world (Lowe et al. 2000; Murphy groups used in the biological control programs et al. 2008). Miconia calvescens is native to of weeds (Acarina, Coleoptera, Diptera, Central and South America and was Hemiptera, Hymenoptera, Lepidoptera, and introduced as an ornamental plant in French Thysanoptera), Lepidoptera were the fastest

Polynesia, Hawaii, New Caledonia, and dispersers (Paynter and Bellgard 2011). The by guest on November 14, 2015 Australia (Meyer 1996; Csurhes 1997; natural dispersal ability of a new agent is a Medeiros et al. 1997). On the Hawaiian and limiting factor for success of biological Tahitian Islands, the problems caused by the control of weeds. invasion of this weed are more serious, and many areas have become extensive In fact, establishment and spread are two monospecific stands of this plant (Meyer distinct issues in biological control programs 1996; Medeiros et al. 1997). In Australia, the of weeds. The population dynamics of an invasion of M. calvescens is more recent, but agent post–introduction can be influenced by it has been classified as a major threat to the factors such as climate (Dennill and Gordon native biodiversity in the country (Murphy et 1990; Zalucki and van Klinken 2006), natural al. 2008). enemies (Hill and Hulley 1995; Paynter et al. 2010), resource availability (quantity and To select agents for the biological control of quality of host plant) (Foxcroft et al. 2007), M. calvescens, surveys on the that and the appearance of more vigorous attack this weed in Brazil have been carried genotypes of weeds (Sheppard 1992; Nissen out since 2001 (Picanço et al. 2005; Morais et et al 1995). Crawley (1986) found that 44% of al. 2010a, 2010b). In these previous studies, the failures of weed control by biological some species of Lepidoptera were found agents are to due the non–adaptation of these

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. organisms to climate conditions in the country company (CAF Santa Bárbara Ltea.). The of introduction. Surveys of abundance of locality was at 344 m altitude and was located possible biocontrol agent can be used to at 19º 50' 34" S, 42º 46' 36" W. During the improve understanding of the climate effects experimental period, the average temperature on the agent and of its establishment in new was 23.2 ºC, and rainfall reached 1003 mm/yr. areas (Zalucki and van Klinken 2006). According to Paynter and Bellgard (2011), the knowledge about parameters of a biocontrol The experimental area in Guaraciaba was agent, prior to its introduction (agent located in an abandoned pasture, under an voltinism, parasitoid diversity in the native initial natural recovery process, and was 1 km range, habitat, fecundity, taxon and life–style away from the Rio Piranga. This area was 580 category) could be used to predict if it will m in altitude and located at 20º 34' 36" S, 43º establish and disperse in a new environment. 02' 26" W. During the evaluation period, the average temperature was 19.6 ºC, and rainfall Downloaded from This work presents the damage, host reached 988.5 mm/yr. Miconia calvescens specificity, population dynamics, and the field plants in this area were discovered at the occurrence of natural enemies of Lepidoptera beginning of 2005; therefore, evaluations at species associated with M. calvescens in this site started only in that year. http://jinsectscience.oxfordjournals.org/ Brazil; the defoliators S. lotanalis, D. inscita, and A. leucocyma, three Limacodidae species, the fruit borer Carposina cardinata Meyrick Evaluations were performed during three (Carposinidae) and the flower damaging different periods: the first period spanned June Pleuroprucha rudimentaria Guenée 2001 to June 2002; the second period was (Geometridae). The mass–rearing techniques from February 2004 to February 2005; and the of these species are also described. third period was from March 2005 to February 2006. During the first period, the plants were

by guest on November 14, 2015 assessed every three weeks in Viçosa and Materials and Methods Dionísio. During the second period, Population dynamics evaluations were carried out at 10-day The population density of Lepidoptera intervals in Viçosa and monthly in Dionísio. associated with M. calvescens was evaluated In the third period, evaluations were made in the municipalities of Viçosa, Dionísio, and every two weeks in Viçosa and Guaraciaba. Guaraciaba in Minas Gerais, Brazil. The experimental area in Viçosa was located in a Each evaluation involved the randomised secondary forest fragment under an advanced sampling of ten M. calvescens plants, each stage of natural recovery. The area was one with a height of 1-7 m and a basal trunk located at an altitude of 700 m (20º 46' 37" S, diameter of 6-15 mm. For each plant, the 42º 50' 36" W). During the experimental number of Lepidoptera was counted in the period, the average temperature was 19.4 ºC, main stem, six secondary branches, six and rainfall reached 1221 mm/yr. inflorescences, and six infructescences. Leaves and buds from the secondary branches were examined. Six infrutescences were also In Dionísio, the experimental area was located brought to the laboratory to determinate in a riparian forest at the margins of the Rio whether Lepidoptera larvae were present Doce in an area belonging to a private inside the fruits. During the evaluations, the

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. organ that each Lepidoptera attacked and the were made until February 2006 because after type and level of the damage caused by each this time, the seedlings did not establish in the species were recorded. field due to defoliation by ants (Atta spp.).

Representative samples of these species were Effect of climatic parameters on caterpillar deposited in the Museu Regional de population dynamics Entomologia of the Universidade Federal de Canonical correlations and Pearson Viçosa. correlations were carried out to determinate Climate data from Viçosa were obtained from the relationship between the population the climate station belonging to the density of Lepidoptera and the climatic Universidade Federal de Voçoa; data for parameters (average, maximum, and Guaraciaba were obtained from the climate minimum air temperature, relative humidity,

station at Ponte Nova (also belonging to the rainfall, photoperiod, and wind speed). Downloaded from Universidade Federal de Viçosa); and data for Statistical analyses were performed using the Dionísio came from the Ponte Alta Climate SAS procedures PROC CANCOR and PROC Station (belonging to the private company COR. In these analyses, the related to

CAF Santa Bárbara Ltda). Lepidoptera density of each evaluation and http://jinsectscience.oxfordjournals.org/ the averages of climatic parameters 15 days Population dynamics: Hawaiian biotype preceding the evaluations were applied, except for rainfall, for which the total rain in In September 2005, 10 M. calvescens the 15 days before the evaluations was seedlings of Hawaiian biotype were applied. transplanted into the ground at the experimental area in Guaraciaba. These Parasitism seedlings were used because plants from During the population peaks of Lepidoptera, Hawaii have a distinct appearance, with leaves 10 caterpillars of each species were collected by guest on November 14, 2015 slightly softer and different in color (purple in in the field and brought to the laboratory to abbatial face; in Brazilian plants this part is verify the emergence of parasitoids. These green). Therefore, the objective of this study caterpillars were maintained in a rearing room was observed whether the seedlings of with a light regime of 12:12 L:D, 26 ± 2 ºC air Hawaiian biotype were naturally attacked by temperature, and 70 ± 10% relative humidity. caterpillars. The defoliator caterpillars were placed in plastic bags (40 × 50 cm) with leaves of M. Seeds were collected in Hawaii and calvescens. Fruit borer caterpillars were germinated in a box with sand. When the placed into transparent 2 L plastic pots (14 cm seedlings were at a height of 30-40 cm, they diameter, 14 cm height) with fruits inside. were transplanted into the ground at Flower feeding caterpillars were put inside Guaraciaba the experimental area next to M. wooden cage (0.5 × 1.0 × 1.2 m), enclosed in calvescens plants that grew naturally. organza containing inflorescences of M. Seedlings were arranged in a row with 2 m calvescens. The bags, pots, and cages that spacing between the plants. From September contained the caterpillars were maintained in a 2005 to February 2006, the natural attacks on rearing room until the caterpillars pupated. these seedlings by caterpillars were also The number of parasitized caterpillars and the assessed during the site visits. Evaluations number of emerged adult parasitoids of each

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. caterpillar were counted every day. The adult transplanted to 5 L pots with soil. When the parasitoids were collected and forwarded to seedlings were 70-100 cm tall, four seedlings Dr. Maria Angélica Penteado-Dias for species of each Melastomataceae species were put in a identification. wooden cage (0.5 × 1.0 × 1.2 m), enclosed in organza and infested with five S. lotanalis Host specificity: field conditions caterpillars of the third instar. The caterpillars During the evaluations, all vegetation in the 2 were reared in rooms similar to that described m radius of M. calvescens sampled during the above. The instar of the caterpillars, their population dynamics experiment was also survival and the damage they caused to the observed to check whether the Lepidoptera seedlings were recorded daily. species had attacked other plant species. Among the species found close to M. Mass–rearing calvescens, other Melastomataceae were Salbia lotanalis, D. inscita, A. leucocyma, C. found. The most common were as follows: cardinata, and P. rudimentaria were reared in Downloaded from Clidemia capitellata (Bonpl.) D. Don., rearing rooms similar to the room described Clidemia hirta (L.) Don, Leandra lacunosa above. Caterpillars of S. lotanalis, D. inscita, Cogn, Miconia albicans (Sw.) Triana, M. and A. leucocyma were collected and placed mendoncaei Cogn., Miconia ibaguensis into transparent plastic bags (40 × 50 cm) with http://jinsectscience.oxfordjournals.org/ (Bonpl.), and Ossala confertiflora (DC.). leaves of M. calvescens. Five M. calvescens Organs of these species were carried to the leaves were placed in each bag along with five laboratory to determinate whether Lepidoptera caterpillars of similar size. These bags were larvae were present inside. maintained in a rearing room until the caterpillars pupated. The pupae were separated by sex according to characters Host specificity tests: Salbia lotanalis described by Butt and Cantu (1962) and Host specificity tests of S. lotanalis were placed into plastic pots with wet vermiculite by guest on November 14, 2015 carried out in glasshouses. These tests were to avoid desiccation. conducted with the following Emerged adults were transferred to a wooden Melastomataceae species: C. capitellata, C. cage (0.5 × 1.0 × 1.2 m) and enclosed in hirta, M. mendoncaei, M. albicans, M. organza with a young M. calvescens plant ibaguensis, L. lacunosa, O. confertiflora, (0.8-1.0 m high). 10 pairs were placed inside Tibouchina granulosa (Desr.) Cogn., and T. each cage and fed with a 10% honey solution. moricandiana (DC.) Baill. The Hawaiian After the eggs hatched, the caterpillars were biotype of M. calvescens was also included in transferred with a fine brush to leaves of M. the tests. calvescens, which were put inside plastic bags (40 × 50 cm) and maintained in a rearing The seeds of the Melastomataceae species room, following the same procedures were extracted from fresh fruits of trees mentioned above. located in the field where the evaluations were performed. The seeds of the Hawaiian biotype Miconia calvescens fruits attacked by C. of M. calvescens were collected in Hawaii. cardinata were collected in the field and put The seeds were germinated in a box with in into transparent 2 L plastic pots (14 cm sand. After about three months, when diameter, 14 cm height). Each pot received seedlings were 10-20 cm tall, they were about 80 g of fruit. The pots were capped with

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. organza and their bottoms were covered with where they feed and eventually pupate. One paper for absorbing the dampness of the fruits. caterpillar is able to destroy an entire leaf, When the fruits began to rot, the caterpillars causing its abscission. Adults are small brown were removed and transferred to pots with yellowish patterns on the wings containing fresh fruits. As caterpillars attained and caterpillars are green with black patterns the pupa stage outside the fruits, the pupae on the body (Figure 1A-C). could be seen and removed from the pots. The pupae were separated by sex according to The density of S. lotanalis was higher in characters described by Butt and Cantu (1962) Dionísio and Guaraciaba than Viçosa. In and placed into plastic pots with wet Dionísio, population peaks occurred from vermiculite. The emerged adults were January to April 2002 and from May to transferred to pots containing mature fruits of October 2004. In Guaraciaba, S. lotanalis M. calvescens. 10 pairs of C. cardinata were caterpillars were found throughout the whole put in each pot, and they were fed with a 10% evaluation period, with population peaks from Downloaded from honey solution. Emerged caterpillars from June to September 2005. In Viçosa, S. these pots were reared as mentioned above. lotanalis caterpillars were found occasionally and at a low density (Figure 2A). During Caterpillars of P. rudimentaria were reared in population peaks, the damage caused by these http://jinsectscience.oxfordjournals.org/ wooden cages (0.5 × 0.5 × 0.5 m) and caterpillars to M. calvescens plants was high, enclosed in organza with M. calvescens amounting to 50% defoliation. In these inflorescences. The inflorescences were periods, some M. calvescens seedlings collected in the field and maintained with their (Brazilian biotype) died due the high levels of peduncle immersed in glass bottles containing defoliation by this leaf roller. 100 mL of water. 20 caterpillars of the same instar and four inflorescences were put in each Salbia lotanalis and one species of

cage. The inflorescences were changed every Limacodidae were observed attacking sentinel by guest on November 14, 2015 five days. Pupae were separated by sex plants (Hawaiian biotype) at Guaraciaba according to characters described by Butt and (Table 1). Two weeks after the sentinel plants Cantu (1962) and placed into plastic pots with were taken to the field S. lotanalis caterpillars wet vermiculite. The emerged adults were were already found on these plants. The transferred to wooden cages (same characters highest intensity of attack occurred from described above) with four M. calvescens September to December 2006 (Figure 2A). In inflorescences. 10 pairs of P. rudimentaria this period, all seedlings were attacked by at were placed in each cage, and they were fed least one caterpillar. Furthermore, in with a 10% honey solution. After the eggs Table 1. Host range of Salbia lotanalis as revealed by attack (+) hatched, caterpillars were transferred to new or non–attack (−) on Melastomataceae species in field M. calvescens inflorescences and reared as evaluations and in host specificity tests.

mentioned above.

Results

Salbia lotanalis Salbia lotanalis is a leaf roller. Its caterpillars

roll leaves longitudinally, forming tubes

n.e. = not evaluated

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. December, one seedling died due to the lotanalis, D. inscita caterpillars are found damage caused by this caterpillar species. singly inside the leaf tubes. This species was Only four Limacodidae caterpillars were also more abundant in Dionísio, with found defoliating the seedlings in October. population peaks from May to June 2002 and from February to June 2004. In Viçosa, this Nearly 10% of S. lotanalis caterpillars brought caterpillar species was found occasionally and from the field were parasitized. Three at low density. In Guaraciaba, it was found parasitoid species were found: two only in March 2005 (Figure 2B). Hymenoptera [Apanteles sp. (Braconidae) and Pediobius sp. (Eulophidae)] and a Diptera No parasitism was verified in D. inscita. No (Tachinidae). Apanteles sp. larvae emerged caterpillars of this lepidopteran were found in from the last instar of S. lotanalis and pupated other plant species during the field outside the caterpillars. The pupae of this evaluations, including the other braconid are white, and about 20-30 larvae Melastomataceae that were assessed (Table Downloaded from emerged from each caterpillar. Pupae of 1). Tachinidae were also found in the last instar of S. lotanalis. The pupae of this Diptera are Antiblemma leucocyma brown, and about 6-10 pupae emerged in each Antiblemma leucocyma caterpillars are http://jinsectscience.oxfordjournals.org/ caterpillar. Three S. lotanalis pupae were also defoliators that make irregular holes in leaves. parasitized by Conura sp. (Hymenoptera: They are green and have a distinctive looping Chalcididae) in October 2004. walk (Figure 1E-F), and were found in all three places (Figure 2C). Caterpillars of this In the field, S. lotanalis caterpillars were not species were found during the evaluation found on other plants species, including the period in Dionísio. In Viçosa, their population other Melastomataceae assessed (Table 1). peaks occurred from April 2005 to February

However, a similar species, Ategumia 2006, while in Guaraciaba, they occurred only by guest on November 14, 2015 matutinalis Guenée, was observed attacking from May to July 2005 (Figure 2C). C. hirta. Ategumia matutinalis caterpillars are very similar to S. lotanalis, with similar wing About 30% of the A. leucocyma caterpillars color patterns as adults (Figure 1D). In host brought from the field were parasitized by specificity tests, S. lotanalis caterpillars were Hymenoptera (Apanteles sp. (Braconidae)). able to develop through to pupation on both C. Many A. leucocyma caterpillars found in the hirta and the Hawaiian biotype of M. field had dark coloration, indicating that they calvescens. In other Melastomataceae, no were parasitized. Caterpillars of this damage by caterpillars was verified, and they Lepidoptera were not found in the other plant died of starvation (Table 1). species assessed (Table 1).

Druentia inscita Limacodidae Druentia inscita caterpillars are also leaf Three species of Limacodidae caterpillars rollers. They feed mostly on apical foliage, were found occasionally in Viçosa, Dionísio, which they can completely destroy. The and Guaraciaba, causing defoliation of M. caterpillars are yellow with brown stripes and calvescens plants. These caterpillars were also the adults are brown with two darker stripes found on the other sampled plant species on the wings (Figure 1E-F). Similarly to S.

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. neighboring M. calvescens, including plants they were present from May to September belonging to the Melastomataceae family. 2005 (Figure 3B). During these population peaks, about 40% of inflorescences were Carposina cardinata completely stripped by this caterpillar species, Carposina cardinata is a fruit borer of M. and the fruit production of the M. calvescens calvescens and is found only in Guaraciaba. plants was extremely low. No P. rudimentaria Its caterpillars are beige and in the last instar caterpillars brought to the laboratory were they measure about 3 mm long. Adults are parasitized. This caterpillar was not found in micro moths, bright gray, and measure about 5 other plant species, including the other mm (Figure 1H-I). They live inside fruits and Melastomataceae assessed (Table 1). feed on the flesh and seeds, causing severe damage. One to five caterpillars were found in Effect of climatic parameters on caterpillar each M. calvescens fruit. Carposina cardinata population dynamics caterpillars were found in Guaraciaba in 2005, There was a significant canonical correlation Downloaded from from March to September, which between the density of each Lepidopteran corresponded to the period of M. calvescens associated with M. calvescens and climatic fruit production (Figure 3A). No parasitized parameters (Wilks’ Lambda = 0.35, F = 2.72, http://jinsectscience.oxfordjournals.org/ caterpillars were found. During this period, df num/den= 35/335, p < 0.01). Five canonical the following Melastomataceae were also in axes were generated, out of which only the their fruiting periods: C. capitellata, C. hirta, first two were significant at 5% probability L. lacunosa, M. albicans, M. mendoncaie, M. and explained 86% of the correlation. ibaguenscens, and O. confertiflora. However, According to the first canonical axis, among no C. cardinata was found in the fruits of any the Lepidoptera, S. lotanalis was the most of these species (Table 1). influenced by the climatic parameters (r = −0.89), and according to the second axis, D.

Pleuroprucha rudimentaria inscita (r = 0.86) was the most influenced by by guest on November 14, 2015 Pleuroprucha rudimentaria caterpillars feed the climatic parameters. The climatic on flowers. These caterpillars are brown, with parameters that most affected the Lepidoptera white stripes and a distinctive looping walk density were the maximum (r = 0.75) and (Figure 1J-L). This species was found only in average (r = 0.79) air temperature according Viçosa and Guaraciaba. In Viçosa, caterpillars to the first axis, and the minimum air attacked M. calvescens from April to June temperature (0.57) according to the second 2005 and in December 2005. In Guaraciaba, axis (Table 2). Table 2. Canonical correlations and canonical pairs between the abundance of Lepidoptera associated with Miconia calvescens and climatic parameters in Viçosa, Dionísio and Guaraciaba, Minas Gerais, Brazil.

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There was a positive Pearson correlation Carposina cardinata and P. rudimentaria can among the minimum, maximum, and average be reared in the laboratory only during the air temperatures and the population density of flowering and fruiting periods of M. D. inscita (r = 0.34, p < 0.01, r = 0.25, p < 0.01 calvescens. Only two generations of these and r = 0.28, p < 0.01, respectively). In fact, Lepidoptera were reared in the laboratory highest densities of D. inscita were observed because afterwards there were no fruits or Dionísio, where air temperatures were higher flowers in the field for feeding the caterpillars (28.6, 19.6, 23.2 ºC maximum, average, and or for egg–laying by the adults. Carposina minimum air temperatures, respectively) than cardinata caterpillars survived and fed on Viçosa (27.2, 15.1, 20.1 ºC maximum, average, fruits maintained in plastic pots. Their adults and minimum air temperatures, respectively) also laid eggs in M. calvescens fruits inside and Guaraciaba (22.9, 16.3, 16.3 ºC maximum, the pots. Pleuroprucha rudimentaria average, and minimum air temperatures, caterpillars fed on the inflorescences brought Downloaded from respectively) (Figure 4). There was a negative from the field, and adults laid their eggs in Pearson correlation among the maximum and these inflorescences. average air temperatures and the population density of S. lotanalis (r = −0.38, p < 0.01 and Discussion http://jinsectscience.oxfordjournals.org/ r = −0.39, p < 0. 01, respectively). On the other hand, S. lotanalis was more frequent in Salbia lotanalis has already been recognized Guaraciaba, where the temperatures were as a potential biological control agent due its lowest. In addition the population peaks of high reproductive capacity and impact on this caterpillar occurred in colder months young plants (Morais et al. 2010b). The (Figure 4). constant presence of S. lotanalis in the field under a range of climatic conditions indicates

Mass–rearing that this lepidopteran may establish well in by guest on November 14, 2015 Salbia lotanalis, D. inscita, and A. leucocyma new areas if introduced as a classical can be reared throughout the year under biocontrol agent against M. calvescens, since laboratory conditions. As M. calvescens trees natural enemies that are frequent in the native maintain a large number of leaves throughout range are likely to become frequent in the the year, the caterpillars of these species have introduced environment (Sheppard 2002). The plenty of food throughout the year. host specificity study demonstrated that S. Furthermore, M. calvescens leaves stayed in lotanalis could feed on the leaves of M. good condition for a week when they were calvescens and C. hirta. Additionally, its kept in the plastic bags. Salbia lotanalis was caterpillars were not found in other species in the easiest to rear in the laboratory because of the field. Although this species may attack C. its shorter life cycle (about 70-100 days), high hirta in the new range, this does not hinder its reproductive rate (~90 eggs/female), and low introduction as a biocontrol agent for M. mortality rate (more than 70% of individuals calvescens, because C. hirta is also a major reached the adult stage). The life cycles of D. invasive outside the neotropics (Wester and inscita and of A. leucocyma are longer, lasting Wood 1977; Medeiros et al. 1997). In case S. 150-200 and 100-120 days, respectively. The lotanalis attacks C. hirta in the Pacific islands reproductive rate of both these species is this would be regarded as highly beneficial. smaller (about 30 eggs/female).

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. A closely related leaf roller, Salbia only in Oahu (Culliney and Nagamine 2000; haemorrhoidalis was used in successful Conant 2002). programs for the biological control of Lantana camara in South Africa. This species showed Carposina cardinata is an important fruit good establishment and distribution in this borer of M. calvescens. Attacks of this country, as well as high population densities lepidopteran can reduce seed fruit production. (Baars 2003). Another great advantage of Studies have verified that herbivores of employing S. lotanalis as a biocontrol agent is reproductive structures can be very effective that it can be easily reared under laboratory weed biocontrol agents because they can conditions, with high population growth rates reduce recruitment to the seedling stage of the (Morais et al. 2010). populations (Bellows and Headrick 1999). A similar Carposina, C. bullata Meyrick, was Druentia inscita also causes severe damage to M. used as a biocontrol agent of C. hirta in calvescens plants in the field. During the Hawaii, where it established and became very Downloaded from evaluations, dead branches were observed due effective. This species feeds internally in the to the attack of this caterpillar on terminal flower buds and is specific to the Miconia and buds. Nakahara et al. (1992) verified that D. Clidemia and the damage to the flowers of C. inscita is restricted to 13 species of hirta prevents seed production (Nakahara et http://jinsectscience.oxfordjournals.org/ Melastomataceae out of the 39 species surveyed, al. 1992). The major difficulty in the and no larval feeding damage was observed on introduction of C. bullata was obtaining non–Melastomataceae from the 15 families tested. sufficient numbers of individuals to be Druentia inscita was introduced in Hawaii for the released because no mass–rearing method was control of C. hirta, occupying upper–elevation developed (Culliney and Nagamine 2000). sites and shaded environments (Nakahara et al. Here, we verified that C. cardinata could be 1992). However, its establishment was not very reared in the laboratory during the fruiting

successful probably because few individuals were period of M. calvescens and a great number of by guest on November 14, 2015 introduced (Culliney and Nagamine 2000). No adults could be obtained. Another example of records of it attacking M. calvescens were Carposina used in control of weed is the recorded after its introduction in Hawaii. seed–, C. autologa introduced in South Africa to control a serious invasive plant Compared with S. lotanalis and D. inscita, A. Hakea sericea, a small tree Australian origin leucocyma caused less damage to M. (Gordon and Fourie 2011). calvescens, and there were long periods where this species was not found in the field. The Pleuroprucha rudimentaria is also a potential low density of A. leucocyma may be due to biocontrol agent for M. calvescens. Fruit the high parasitism rates by Apanteles sp. production decreased about 40% in the However, the indications of a high host flowering period of 2005 in Viçosa and specificity of this Lepidoptera is of relevance Dionísio possibly owing to this insect's attack. for its use as a biological control agent to be Furthermore, an ad hoc observation of a used against M. calvescens (Badenes-Perez severe attack was observed in Viçosa in 2006 and Johnson 2008). A similar caterpillar, (Morais, personal observations). Antiblemma acclinalis Hübner, from Trinidad Pleuroprucha rudimentaria is reported to was introduced into Hawaii for the control of occur in Costa Rica, Peru, Jamaica, and C. hirta and had a confirmed establishment Venezuela, but there is no information about

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. its host specificity (BLDS 2010). During the inscita are defoliators, S. lotanalis feed on field evaluations, no caterpillars of P. mature leaves, and D. inscita feed on young rudimentaria and C. cardinata were found leaves in terminal buds, which prevents attacking others plant species. Therefore, it competition between them. Furthermore, S. would be worth conducting additional host– lotanalis and D. inscita showed differences in specificity tests for these species. their temporal distribution; S. lotanalis occurs in cooler periods, and D. inscita occurs in warmer Parasitism may be a limiting factor for periods. The same pattern was observed for C. establishment of lepidopteran species in new cardinata and P. rudimentaria, the first areas. Native parasitoids have reduced the species feeds on fruits and the second feeds on efficacy of some biocontrol agents, such as flowers. An effective result in the control of Neogalea sunia and S. haemorrhoidalis in the Sesbania punicea was obtained with the control of Lantana camara (Hill and Hulley combined action of a seed–feeder 1995; Baars and Neser 1999). Nevertheless, Rhyssomatus marginatus, two defoliators Downloaded from although S. lotanalis has been parasitized by Tyria jacobaeae, and a flea beetle Longitarsus several species, this caterpillar maintains its jacobaeae (McEvoy et al. 1990; Hoffmann high density in the field, causing severe and Moran 1992). damage to M. calvescens. Moreover, no http://jinsectscience.oxfordjournals.org/ parasitism was verified in D. inscita, C. Considering the difficulty and high cost of M. cardinata, or P. rudimentaria. calvescens control by chemical or mechanical removal (Burnett et al. 2007; Hester et al. Climate is also an important factor for the 2010), the introduction of effective biocontrol establishment of any biocontrol agent. agents is regarded as necessary to reduce the Climatic factors can limit the dispersal of population density of M. calvescens in Tahiti biological agents to new areas within the and Hawaii. Therefore, the traits of S.

geographic range of the weeds (Baars 2003). lotanalis and D. inscita, such as host by guest on November 14, 2015 Air temperature is one of the most important specificity, high population growth rate, high factors interfering with the establishment, rate of damage to the plants, relatively easy dispersal, and impact of organisms in new mass–rearing under laboratory conditions, and areas of distribution (Baker 2002). Salbia occurrence in the field throughout the year lotanalis seems to develop better in periods of indicate that these lepidopterans can become cooler air temperatures and D. inscita in hotter good classical biocontrol agents against M. seasons (Figures 2A and 4). calvescens. Furthermore, if C. cardinata and P. rudimentaria have a sufficient degree of The introduction of multiple herbivores as host specificity demonstrated in future tests, biocontrol agents against a single weed these caterpillars could also be considered for species may be advantageous, particularly use as biocontrol agents. where they attack different plant parts and suppress plant growth and reproduction. In Acknowledgements this case, the introduction of S. lotanalis and D. inscita (defoliators) and C. cardinata and P. This study was supported by the USGS BRD rudimentaria (attacking reproductive organs) Pacific Island Ecosystem Research Centre, the might be a good strategy for the control of M. National Park Service, the Research calvescens. Although S. lotanalis and D. Corporation of Hawaii, and the Conselho

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. Nacional do Desenvolvimento Científico e Tecnológico (CNPq) – Brazil. We thank the Barcode of Life Data Systems. 2010. company CAF Santa Bárbara Ltda for Lepidoptera Barcode of Life: Geometridae. allowing access to one experimental area (at Biodiversity Institute of Ontaro. Available Dionísio) and providing the climatic data from online, their climate station. We also thank Dr. Vitor http://www.lepbarcoding.org/geometridae/spe Becker (Universidade Federal de Brasília, cies.php?region=1&id=40667 Brazil) for identifying of the species of Lepidoptera and Dr.Maria Angélica Penteado- Boughton AJ, Pemberton RW. 2009. Dias (l Universidade Federal de São Carlos, Establishment of an imported natural enemy, Brazil) for identifying the species of Neomusotima conspurcatalis (Lepidoptera: parasitoids. ) against an invasive weed, Old World climbing fern, Lygodium References microphyllum, in Florida. Biocontrol Science Downloaded from and Technology 19(7): 769-772. Baars JR. 2003. Geographic range, impact, and parasitism of lepidopteran species Burnett K, Kaiser B, Roumasset J. 2007. associated with the invasive weed Lantana Economic lessons from control efforts for an http://jinsectscience.oxfordjournals.org/ camara in South Africa. Biological Control invasive species: Miconia calvescens in 28(3): 293-301. Hawaii. Journal of Forest Economics 13(2-3): 151-167. Baars JR, Neser S. 1999. Past and present initiatives on the biological control of Lantana Butt BA, Cantu E. 1962. Sex Determination of camara (Verbenaceae) in South Africa. Lepidopterous Pupae. pp. 33-75. USDA. African Entomology Memoir 1: 21-34.

Conant P. 2002. Classical biological control by guest on November 14, 2015 Badenes-Perez FR, Johnson MT. 2008. of Clidemia hirta (Melastomataceae) in Biology, herbivory, and host specificity of Hawaii using multiple strategies. In: Smith Antiblemma leucocyma (Lepidoptera: CW, Denslow JS, Hight S, Editors. Workshop Noctuidae) on Miconia calvescens DC. on Biological Control of Invasive Plants in (Melastomataceae) in Brazil. Biocontrol Native Hawaiian Ecosystems. pp. 13-20. Science and Technology 18(2): 183-192. Pacific Cooperative Studies Unit, University of Hawaii at Manoa. Baker RHA. 2002. Predicting the limits to the potential distribution of alien crop pests. In: Crawley MJ. 1986. The population biology of Hallman GJ, Schwalbe CP, Editors. Invasive invaders. Philosophical Transactions of the Arthropods in Agriculture Problems and Royal Society of London B: Biological Solutions. pp. 207-241. Science Publishers. Sciences 314(1167): 711-731.

Bellows TS, Headrick DH. 1999. Arthropods Csurhes SM. 1997. Miconia calvescens, a and vertebrates in biological control of plants. potentially invasive plant in Australia’s In: Bellows TS, Fischer TW, Editors. tropical and sub–tropical rainforests. First Handbook of Biological Control. pp. 505-516. Regional Conference on Miconia Control, pp. Academic Press. 72-77.

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Journal of Insect Science: Vol. 12 | Article 63 Morais et al. geographical range of Cactoblastis cactorum Culliney TW, Nagamine WT. 2000. (Lepidoptera: Pyralidae) in North America. Introductions for Biological Control in The Florida Entomologist 85(5): 527-529. Hawaii, 1987-1996. Proceedings of the Hawaiian Entomological Society 34(1): 101- Hill MP, Hulley PE. 1995. Host–range 113. extension by native parasitoids to weed biocontrol agents introduced to South Africa. Dennill GB, Gordon AJ. 1990. Climate– Biological Control 5(2): 297-302. related differences in the efficacy of the Australian gall wasp (Hymenoptera: Hoffmann JH, Moran VC. 1992. Oviposition Pteromalidae) released for control of Acacia patterns and the supplementary role of a seed– longifolia in South Africa. Environmental feeding weevil, Rhyssomatus marginatus Entomology 19(1): 130-136. (Coleoptera: Curculionidae), in the biological control of a perennial leguminous weed, Downloaded from Dhileepan K, Snow EL, Rafter MA, Trevino Sesbania punicea. Bulletin of Entomological M, McCarthy J, Senaratne K. 2007. The leaf– Research 82(3): 343-347. tying moth Hypocosmia pyrochroma (Lep., Pyralidae), a host–specific biological control Lowe S, Browne M, Boudjelas S, De Poorter http://jinsectscience.oxfordjournals.org/ agent for cat's claw creeper Macfadyena M. 2000. 100 of the World’s Worst Invasive unguis-cati (Bignoniaceae) in Australia. Alien Species: A Selection from the Global Journal of Applied Entomology 131(8): 564- Invasive Species Database. The Invasive 568. Species Specialist Group (ISSG) a specialist group of the Species Survival Commission Foxcroft LC, Hoffmann JH, Viljoen JJ, Kotze (SSC) of the World Conservation Union JJ. 2007. Factors influencing the distribution (IUCN). Available online,

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Hight SD, Carpenter JE, Bloem KA, Bloem S, Meyer JY. 1996. Status of Miconia calvescens Pemberton RW, Stiling P. 2002. Expanding (Melastomataceae), a dominant invasive tree

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Figure 1. (A)Adult, (B) caterpillar, and (C) damage caused by Salbia lotanalis to Miconia calvescens seedlings (Hawaiian biotype); (D) adult of Ategumia matutinalis; (E) adult and (F) caterpillar of Druentia inscita; (G) caterpillar of Antiblemma leucocyma; (H) caterpillar and (I) adult of Carposina cardinata; (J) caterpillar and (K-L) damage caused by Pleuroprucha rudimentaria to inflorescences of Miconia calvescens. High quality figures are available online.

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Figure 2. Population dynamics of leaf feeders: (A) Salbia lotanalis in plants of Brazilian and Hawaiian biotypes, (B) Druentia inscita and (C) Antiblemma leucocyma in Viçosa, Dionísio and Guaraciaba, Minas Gerais, Brazil,

between 2001-2006. Vertical bars = standard error. High quality figures are available online. by guest on November 14, 2015

Figure 3. Population dynamics of reproductive organ feeders: (A) Carposina cardinata and and (B) Pleuroprucha rudimentaria in Viçosa, Dionísio and Guaraciaba, Minas Gerais, Brazil, between 2001-2006. Vertical bars = standard error. High quality figures are available online.

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Figure 4. Average air temperature (ºC), photoperiod (hours), wind speed (m/s), relative humidity (%), and total rainfall (mm) in Viçosa, Dionísio and Guaraciaba, Minas Gerais, Brazil, between 2001-2006. High quality figures are available online. by guest on November 14, 2015

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