Biology, Natural History and Temporal Fluctuation of the Geometrid Oospila Pallidaria Associated with Host Plant Phenology

Studies on Neotropical Fauna and Environment

ISSN: 0165-0521 (Print) 1744-5140 (Online) Journal homepage: http://www.tandfonline.com/loi/nnfe20

Biology, natural history and temporal fluctuation of the geometrid Oospila pallidaria associated with host plant phenology

Bruno de Sousa-Lopes, Alexandra Bächtold & Kleber Del-Claro

To cite this article: Bruno de Sousa-Lopes, Alexandra Bächtold & Kleber Del-Claro (2016): Biology, natural history and temporal fluctuation of the geometrid Oospila pallidaria associated with host plant phenology, Studies on Neotropical Fauna and Environment, DOI: 10.1080/01650521.2016.1199140

To link to this article: http://dx.doi.org/10.1080/01650521.2016.1199140

Published online: 17 Jul 2016.

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Download by: [Mr Kleber Del-Claro] Date: 18 July 2016, At: 05:20 STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT, 2016 http://dx.doi.org/10.1080/01650521.2016.1199140

ORIGINAL ARTICLE Biology, natural history and temporal fluctuation of the geometrid Oospila pallidaria associated with host plant phenology Bruno de Sousa-Lopesa, Alexandra Bächtoldb and Kleber Del-Claro b aPG Entomologia, Universidade de São Paulo, São Paulo, Brazil; bInstituto de Biologia, Universidade Federal de Uberlândia, Minas Gerais, Brazil

ABSTRACT ARTICLE HISTORY We investigated the temporal fluctuation of the geometrid moth Oospila pallidaria and related it Received 20 May 2015 to the leaf flush season of its host plant, Mimosa setosa, and to environmental factors. Aspects of accepted 6 June 2015 Mimosa setosa the natural history of adults are also described. produced leaves all year round, but KEYWORDS O. pallidaria abundance of larvae in the field was seasonal. The abundance of immatures showed Brazilian savanna; Fabaceae; a tendency to decrease with rainfall and temperature. Our study is pioneering in that it provides herbivory; Mimosa setosa; insights into factors related to the occurrence of O. pallidaria in natural areas. In addition, the swamp biology of immatures is provided.

Introduction delayed for some time following the leaf flush. Therefore, generalizations on the relationship between Among the range of folivorous insects, the lepidopterans tropical lepidopterans and the phenology of their host are the most diverse and abundant (Bernays & Chapman plants must be treated with caution, and more studies are 1994) and their intimate relationship with plants allows necessary to unravel the close interactions between but- the investigation of the main factors that influence the terflies and their host plants (Muniz et al. 2012). caterpillars’ abundance and distribution (Price 1992). Besides plant resources, environmental factors Food availability changes temporally and spatially and such as rainfall and temperature can also influence host plant phenology is an important temporal factor the occurrence and abundance of herbivores (Lawton influencing the occurrence of herbivores (Wolda 1988; 1983;Cornelissen2011; Del-Claro et al. 2013) van Asch & Visser 2007). In fact, the timing of plant because climate modifies the quality, abundance and phenophases indicates the availability of floral resources, geographical distribution of host plants (Schweiger young or mature leaves for herbivores and thus creates et al. 2008; Bauerfeind & Fischer 2013). Moreover, favorable conditions for local maintenance of insect not only climate, but the presence of natural enemies populations (Wolda 1988; Vilela et al. 2014). For cater- may represent a risk to the offspring of butterflies pillars with a specialized diet, host plant phenology is (Schmitz et al. 2004; Sendoya et al. 2009), thus Downloaded by [Mr Kleber Del-Claro] at 05:20 18 July 2016 considered to be crucial given that lepidopteran popula- restraining the occurrence of immatures to particular tions are synchronized with the phenological events (e.g. plant structures or even plants where the risk of flowering, leaf flush) of the host plant (Thompson & predation is lower (Sendoya et al. 2009). Ants, Gilbert 2014). This synchrony may be noticed even in wasps and birds are major threats to caterpillars polyphagous caterpillars like Operophtera brumata (Scoble 1995; Salazar & Whitman 2001), but many (Linnaeus, 1758), a geometrid species that showed syn- species have developed defense mechanisms to avoid chrony between the egg hatching and budburst of the contact with their predators (e.g. by building shelters host plant (Tikkanen et al. 2006). However, this close with leaves, by camouflage, body hairs), or escape relationship is far from being a pattern, especially for from attacks (by beat reflex display, regurgitation on lepidopteran herbivores. For instance, Bächtold et al. predators) (reviewed by Greeney et al. 2012). (2014) showed that the occurrence of larvae of the spe- Camouflaging on the plant is also an escape strategy cialist folivorous skipper Udranomia spitzi (Hayward to avoid visually guided predators like birds and some 1942) was not closely synchronized with the leafing of wasps (Stamp & Wilkens 1993), and this strategy is its hosts (species of Ouratea, Ochnaceae), but rather

CONTACT Kleber Del-Claro [email protected] Universidade Federal de Uberlândia, Rua Ceará, s/n. Bloco 2D-Campus Umuarama, CEP 38400902 Uberlândia, Minas Gerais, Brazil © 2016 Informa UK Limited, trading as Taylor & Francis Group 2 B. DE SOUSA-LOPES ET AL.

widespread and well developed in geometrid caterpil- at risk the persistence of specialist herbivores (Araújo lars (McFarland 1988). et al. 2015). Geometrid moths (c.21,250 species worldwide) are The aim of our study was to describe the biology of very diverse in the Neotropics (Heppner 1991), but immature stages of the Neotropical specialist geometrid information about the immature stages, host plants moth Oospila pallidaria (Schaus 1897) (Figure 1(a,b)). and distribution is still emerging (Passoa 1983; Vargas This moth was recorded from Argentina, Bolivia, 2007, 2014; Marconato et al. 2008; Bodner et al. 2010; Paraguay and Brazil but records of host plants are Robinson et al. 2015). Such knowledge, especially on lacking (Cook & Scoble 1995). In current surveys in the natural history, is the first step in investigating the Brazilian savanna, we observed larvae of O. palli- and understanding multitrophic interactions in the daria feeding on leaves of Mimosa setosa var. paludosa field (Bächtold et al. 2012) and gives support to further (Benth.) Barneby (Fabaceae, Mimosoideae). To inves- ecological studies (Del-Claro et al. 2013). Furthermore, tigate this insect–plant association we conducted obser- for insects with a specialized diet, knowledge of their vations of this moth species both in the field and in the relationships with the host plant is paramount as laboratory to describe its host plant use, natural history changes, both natural and anthropic, in the habitat and behavior, as well as its interactions with natural such as fire, fragmentation and deforestation may put enemies. We also analyzed the annual fluctuation of Downloaded by [Mr Kleber Del-Claro] at 05:20 18 July 2016

Figure 1. Adults of Oospila pallidaria. (a) Male; (b) female (left: dorsal view; right: ventral view). STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 3

abundance of O. pallidaria larvae with regard to the in vivo with a Nikon Coolpix L810 digital camera. The host plant phenology and climate conditions. terminology used in the descriptions is in accordance with Peterson (1962), McGuffin (1963), Salkeld (1983) and Stehr (1987). Larval behavior was recorded for all Material and methods instars by observations ad libitum (sensu Altmann Study area 1974) on plants along the trail at the study area. Two pairs of adults, which were reared from the immatures Fieldwork was conducted from May 2013 to April 2014 in the laboratory, were observed during mating. in a Brazilian savanna area (cerrado biome) in Uberlândia city, southeastern Brazil (18°59ʹS, 48° 17ʹW). Local vegetation is dominated by herbaceous Assessing the phenology of Mimosa setosa plants with some trees ranging between 2 and 4 m in Phenological observations were carried out fortnightly height. We used a preexistent trail to locate plants of from May 2013 to April 2014 on 40 tagged individuals Mimosa setosa. The climate in the region is markedly of M. setosa. The intensity (%) of the presence of seasonal, characterized by a rainy summer (October to mature leaves was recorded for each plant. The method April) which may account for up to 75% of the annual used to evaluate these phenophases was the Fournier’s rainfall, and a dry winter (May to September) per cent index of intensity adapted by Ribeiro and (Laboratory of Climatology, Federal University of Castro (1986), which ranges from zero to four, where Uberlandia). 0 = absence of a given phenophase, and 1, 2, 3 and 4 indicate that a given phenophase was recorded in – – – – Host plant 1 25%, 26 50%, 51 75% and 76 100% of plants, respectively (adapted from Morellato et al. 2000). Mimosa setosa is a swampy-shrub species (Simon et al. 2011; Dutra & Garcia 2014) which rarely exceeds 2.0 m in height. Leaves are pinnately compound with a Annual variation of Oospila pallidaria abundance rachis; aculeate and glandular trichomes occur all In order to assess whether the temporal variation of the over the rachis, the stems and inflorescences; leaves larval population of O. pallidaria was influenced by have trichomes only on the abaxial side (Barneby abiotic factors, we evaluated the occurrence of larvae 1991). All M. setosa used in this study (n = 40) were fortnightly from May 2013 to April 2014 on the same located on a trail inside the cerrado reserve, near a 40 M. setosa individuals used for the phenological natural pond (18°58ʹ59ʺ S, 48°17ʹ44ʺ W) at the end of investigation. Leaves, flower buds and flowers were a vereda, a swampy area located in the headwater of a carefully examined. As soon as an immature of O. stream. The trail is 3 m wide and c.1.5 km long (for pallidaria was found, it was collected with a fine more details on the area see Guillermo-Ferreira & Del- brush and placed individually in a transparent plastic Claro 2011). pot, which was then labeled. Immatures were taken to the laboratory and reared until the adult stage (follow- Downloaded by [Mr Kleber Del-Claro] at 05:20 18 July 2016 ing Bächtold et al. 2012). In order to contribute to the Assessing the biology of Oospila pallidaria database of lepidopterans and their host plants, other Description of the immature stages of O. pallidaria was caterpillar species found on M. setosa were also col- based on 17 eggs collected from M. setosa leaves and lected and reared in the laboratory. Climate data, such inflorescences from May to November 2014. These as temperature (monthly means) and rainfall (monthly eggs were taken to the laboratory where they were values), were provided by the Laboratory of reared until the adult stage. Larvae were kept individu- Climatology (Federal University of Uberlandia), and ally in transparent plastic pots (500 ml) which were used as possible factors influencing O. pallidaria cleaned daily, and food (leaves) was offered ad libitum. occurrence. During the egg stage, measures of length, width and thickness were taken (according to Salkeld 1983). Head Statistical analysis capsule width was recorded for each instar. All these measurements were made with a stereomicroscope Quantitative data are displayed as mean ± standard equipped with a micrometric scale (µm). deviation. In order to examine whether the occur- The duration of each instar and of pupal develop- rence of O. pallidaria larvae was related to leaf flush, ment were recorded in days. General aspects of imma- we first examined the seasonality of larvae abun- ture morphology, including coloration, were recorded dance and leaves, as it might indicate possible 4 B. DE SOUSA-LOPES ET AL.

overlapping between them. Circular statistical analy- by the arrow in Figure 2(c)) which are present to the fifth sis of directional data was performed by using the (last) instar. Approximate duration: 4–5days(n =11). monthly abundance of moths as well as the percen- tage of plants with mature and young leaves (follow- Third instar ing Bächtold et al. 2014). Months were converted Maximum body length 10 mm. Head capsule width into angles (30° intervals) and were combined with 0.44–0.49 mm (n = 6). Similar to the second instar the respective value of plant phenology and moth except for body size and for more elongated projections abundance. Circular statistics provide (i) the mean in head and prothorax. Duration: 5–6 days (n = 11). angle µ, which is the period when a given variable (e.g. leaves, moths) occurred most often; (ii) the Fourth instar vector r, which is a direct measure of seasonality Maximum body length 16 mm. Head capsule width (the closer to “1” the more seasonal); and (iii) the 0.67–0.70 mm (n = 7). Light green head, green body Rayleigh test (z), which indicates whether seasonality with smooth cuticle, yellow ventral median line (thin- is significant. The interaction of both season (dry ner than in third instar) and brown dorsal median line and wet) and mature leaf phenology in the occur- maintained to the last instar (Figure 2(d)). Duration: rence of O. pallidaria was analyzed with a two-way 6–7 days (n = 11). Anova test. The influence of the abiotic factors (temperature and rainfall) on the temporal variation of Fifth (last) instar the O. pallidaria was analyzed with Pearson correla- Maximum body length 28 mm. Head capsule width tion tests. 0.92–1.04 mm (n = 7). Similar to the fourth instar, except for size and brown-colored anal plate (Figure 2 (e)). The dorsal median line becomes thinner in the Results prepupa. Duration: 8–9 days (n = 11).

Description of immature stages of Oospila Pupa pallidaria Maximum body length 10 mm. Mostly green with dark Egg red dorsal side (Figure 2(f)). Dorsal median line is a Average length 0.69 mm (SD ± 0.07; n = 6), average narrow dotted line. After five days the pupa becomes width 0.35 mm (SD ± 0.07; n = 6) and average thick- beige and near to hatching, wing shape and venation ness 0.21 mm (SD ± 0.03; n = 6). Greenish in the become visible (Figure 2(g)). Duration 8–9days(n =10). beginning of the development and yellow near hatching (Figure 2(a)). Oval shape in top view, compressed Natural history of Oospila pallidaria laterally with narrow sides and flattened perpendicular to the longitudinal axis. Smooth with rounded edges Oospila pallidaria eggs were found singly on different and anterior pole slightly deeper than posterior. parts of M. setosa, such as the abaxial surface of leaves, Duration: 6–7 days (n = 17). flower buds and trichomes. All eggs were attached Downloaded by [Mr Kleber Del-Claro] at 05:20 18 July 2016 horizontally by the widest side. Larvae fed mainly on mature leaves, flower buds and rarely on young devel- First instar oping fruits. Adults (Figure 2(h)) were not found in the Maximum body length 4.5 mm. Head capsule width field. Mature larvae (fourth and fifth instars) resemble 0.20–0.24 mm (n = 7). Orange head and light yellow compound leaves (when folded) by their similar colora- body to the second day of development (Figure 2(b)). tion (Figure 2(i)). We observed the ability for self- Thereafter there is a brown dorsal median line on the cleaning in O. pallidaria caterpillars. After expelling body. Both legs and anal plate are light yellow. Prolegs the frass pellets, the larva bent the body backwards bearing eight crochets arranged in a meso-series. and grabbed each pellet with the thoracic legs, and Duration: 5–6 days (n = 11). tossed it from the plant. Six (4%) O. pallidaria larvae were parasitized Second instar by the microhymenopteran Cotesia sp. (Braconidae, Maximum body length 6.5 mm. Head capsule width Microgastrinae) in January 2014. Parasitized caterpil- 0.30–0.34 mm (n = 7). Orange head, light yellow body lars had swollen bodies in the posterior half (Figure 2 with smooth cuticle (Figure 2(c)). Presence of brown (j)). The solitary parasitoid larvae left the caterpillars dorsal median line and orange ventral median line. near the fifth abdominal segment, wove a yellowish Head and prothorax with a pair of projections (indicated cocoon and adults hatched five days later (Figure 2(k)). STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 5 Downloaded by [Mr Kleber Del-Claro] at 05:20 18 July 2016 Figure 2. Immatures and adult of Oospila pallidaria: (a) lateral view of egg; (b) first instar; (c) second instar with projections on the head and prothorax (arrow); (d) fourth instar; (e) fifth (last) instar; (f) early pupa; (g) mature pupa; (h) adult; (i) fifth instar larva in mimetic posture (arrow); (j) parasitized fourth instar larva with swollen posterior half of body (arrow); (k) and its respective parasitoid Cotesia sp.

Larvae reared in the lab built shelters with silk-tied October to February, when up to 75% of M. setosa leaves just before pupation. However, this behavior was individuals were recorded with new leaves. In compar- not observed in the field. Mating behavior was per- ison, roughly 25% of individuals produced new leaves formed in end-to-end position and lasted about two in the other months. Mature leaves had two peaks of hours. Subsequently (10–15 min later) the two females occurrence, from March to April and from August to laid 70 and 60 eggs, respectively. September (Figure 3). In the other periods, individuals still had mature leaves, as M. setosa does not shed all leaves. Because of the presence of both young and Phenology of Mimosa setosa mature leaves all year round, the seasonal differences Mimosa setosa produced young leaves all year round, in M. setosa phenology were not statistically significant but leafing was concentrated in the wet season, from (Table 1). 6 B. DE SOUSA-LOPES ET AL.

Figure 3. Annual variation of abundance of Oospila pallidaria larvae (gray area) and mature leaves (arrows, %) in Mimosa setosa. Note a delay between the peak of mature leaves between March and April and the peak occurrence of moths in June. Numbers within the circle indicate the abundance of larvae. Moreover, the mean angle (dashed arrow) of both larvae and mature leaves overlaps between May and June.

Annual variation of abundance of Oospila study period, June was the driest month and December pallidaria had the greatest amount of rainfall (Figure 4(b)). The abundance of larvae was negatively related to tempera- The record of O. pallidaria larvae, on the other hand, ture and rainfall, but the test was significant only in the was seasonal (Table 1) and the mean angle µ coincided former case (r = −0.5889, p < 0.05 and r = −0.4252, with the mean angle of mature leaves (Table 1, p > 0.05). Figure 3). We found 149 larvae throughout the year Besides O. pallidaria, caterpillars of Erebidae and predominantly in the dry season, which occurs (Hypercompe sp.; n = 1), Lycaenidae (Hemiargus from May to September (56.4%, n = 84 immatures); hanno (Stoll 1790); n = 12), Pieridae (Pyrisitia sp.;

Downloaded by [Mr Kleber Del-Claro] at 05:20 18 July 2016 their abundance peaked in June (21%, n = 31 imma- n = 2) and another geometrid (Macaria sp.; n =18 tures) and was minimal in October (1.3%, n = 2 imma- individuals) were also found on M. setosa. tures) (Figure 4(a)). The interaction effect of both seasons (dry and wet) and mature leaf phenology were not significantly related to the occurrence of O. Discussion pallidaria larvae (F = 3.0856, p = 0.0922). During the In general, the morphology of the immature stages of O. pallidaria is very similar to that of other geometrids. Eggs are flattened and pillbox-shaped, as found in Table 1. Circular statistical analyses of the seasonality of Oospila pallidaria abundance together with young and mature other species of the Geometrinae (Salkeld 1983) and leaves of its host plant, Mimosa setosa. The mean angle of caterpillars present the well-developed prothorax with larvae and mature leaves is very similar, indicating that abun- one pair of protuberant projections. This trait is also dance of larvae is correlated to mature leaves. reported in other geometrid species, e.g. Nemoria glau- Plant phenology – circular statistics comarginaria (Porter 1986) and Iridopsis parrai Mean angle µ Mean month Vector r Rayleigh Z test (Vargas & Parra 2013). The presence of dorsal projec- Larvae 144.35º May 0.322 15.455*** Mature leaves 142.91º May 0.147 0.54 ns tions on the head in Oospila species seems to be com- Young leaves 330.0º November 0.331 2.417 ns mon (see Janzen & Hallwachs 2009). Oospila pallidaria ***p < 0.0001; ns = not significant (p > 0.05). have such small dorsal projections on the head, like O. STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 7

defense behavior against visually guided predators like birds and wasps (see also Castellanos 2010). Larvae of O. pallidaria occurred all year round on M. setosa, especially during the months of the dry season. This result is in accordance with the pattern of occurrence of caterpillars in seasonal environments like the Brazilian savanna (Morais et al. 1999; Scherrer et al. 2010; Diniz et al. 2012). According to Morais et al. (1999) the dry season is a period with a relatively low number of predators and parasitoids, and therefore a high abundance of caterpillars can be expected in this “enemy-free” period of the year (Diniz et al. 2012). In our study, all parasitism events occurred in January (wet season) corroborating the pattern described in the aforementioned studies. The abundance of O. pallidaria larvae was seasonal and correlated to the availability of M. setosa with mature leaves, as the mean angle of both larvae and mature leaves overlapped. This result is opposed to the pattern reported by Morais et al. (1995, 1999) who found that caterpillar abundance in the cerrado was not correlated with host plant phenology. Nonetheless, these authors did not dis- criminate between specialist and generalist caterpillars. Interestingly, Pessoa-Queiroz et al. (2008) showed that Figure 4. Seasonal pattern of (a) occurrence (mean ± SD) of the abundance of caterpillars of Gonioterma exquisita Oospila pallidaria larvae and (b) of temperature and rainfall Duckworth, 1964, a specialist species from the cerrado, is during the study period. The gray area represents the dry associated to leaf phenology. Therefore, the knowledge of season. diet breadth, particularly for specialists like O. pallidaria, permits the understanding of how the host plant’sphenol- venezuelata, while other species present well pro- ogy may be responsible for the occurrence of herbivores nounced dorsal projections (e.g. O. dicraspeda and O. (Bernays & Chapman 1994; Thompson & Gilbert 2014). permagna; see Janzen & Hallwachs 2009). In our study, there seemed to be a delayed Geometrid caterpillars are known for the absence of response in the maximum abundance of O. pallidaria three pairs of prolegs, which is why their locomotion is larvae (June) following the maximum availability of characterized by a looping process (Wagner 2005). It is mature leaves (March to April). This can be likely that this movement type reduces the surface area explained by the time lapse from egg to adult, Downloaded by [Mr Kleber Del-Claro] at 05:20 18 July 2016 of the caterpillar’s body that comes in contact with the which lasts about 49 days. Larvae from eggs laid in substrate. For O. pallidaria, looping locomotion per- March and April turned into adults which mated and mits the larvae to move easily among branches covered laid eggs in June, in accordance with the observed with glandular trichomes, which are common in M. data. Bächtold et al. (2014) also noted a delayed setosa. The presence of trichomes may also deter other responseintheoccurrenceofskippercaterpillars potential herbivores, predators and competitors of O. and the availability of new leaves on their host pallidaria on M. setosa. In fact, only a few other insects plants. Surprisingly, the other peak of mature leaves were found on this plant, the most abundant being in M. setosa (August to September) was not related another geometrid moth (Macaria sp.). to subsequent O. pallidaria occurrence. Presumably, Morphological and behavioral aspects of mature the coming of the rainy season negatively influenced larvae of O. pallidaria revealed the ability to camou- the oviposition patterns or even deterred the mating flage on their host plant. These larvae bear a coloration behavior of adults, thus reflecting the low abundance that is similar to the green leaves and their mimetic of geometrids in the following months. posture resembles a folded leaf. This is the strategy of For herbivores with restricted diets, like O. palli- cryptic coloration, a common trait in several geome- daria, the availability of their host plants is the most trids (Montgomery 1983; Janzen 1988; Pitkin et al. important factor accounting for their occurrence in 2007; Canfield et al. 2008), and represents an important natural areas. Hence, changes in tropical habitats 8 B. DE SOUSA-LOPES ET AL.

caused mainly by fragmentation and deforestation may Arnold AE, Asquith NM. 2002. Herbivory in a fragmented directly affect herbivore populations, especially lepi- tropical forest: patterns from islands at Lago Gatún, – dopteran larvae (Arnold & Asquith 2002). The same Panama. Biodivers Conserv. 11(9):1663 1680. Bächtold A, Del-Claro K, Kaminski LA, Freitas AVL, may be true for O. pallidaria, whose population Oliveira PS. 2012. Natural history of an ant–plant–butter- depends exclusively on M. setosa. Despite the diversity fly interaction in a Neotropical savanna. J Nat Hist. of Oospila, which is a Neotropical genus with 74 spe- 46:943–954. cies (Cook & Scoble 1995), host plant information is Bächtold A, Lange D, Del-Claro K. 2014. Influence, or the provided for only nine species (Janzen & Hallwachs lack thereof, of host phenology, architecture and climate 2009), three of which feed on Fabaceae, like O. palli- on the occurrence of Udranomia spitzi (Hesperiidae: Lepidoptera). Entomol Sci. 17:66–74. daria. Ecological information on geometrids remains Barneby CR, Censitae S. 1991. Sensitivae Censitae. A descrip- insufficiently known, but the evidence so far indicates tion of the genus Mimosa L. (Mimosaceae) in the New that Fabaceae are important hosts for these caterpillars. World. N Y Bot Garden. 65:1–835. The present study provides insights into the natural Bauerfeind SS, Fischer K. 2013. Testing the plant stress history of O. pallidaria and provides the first record hypothesis: stressed plants offer better food to an insect herbivore. Entomol Exp Appl. 149:148–158. of a host plant for this geometrid species. Further Bernays EA, Chapman RF. 1994. Host-plant selection by investigations of the behavior and multitrophic inter- phytophagous insects. New York (NY): Chapman & Hall actions of this moth with the host plant and natural Press. enemies shall be the focus of future studies. Bodner F, Brehm G, Homeier J, Strutzenberger P, Fiedler K. 2010. Caterpillars and host plant records for 59 species of Geometridae (Lepidoptera) from a montane rainforest in – Acknowledgments southern Ecuador. J Insect Sci. 10(67):1 22. Canfield MR, Greene E, Moreaus CS, Chen N, Pierce NE. The authors would like to thank the staff of Clube de Caça e 2008. Exploring phenotypic plasticity and biogeography in Pesca Itororó de Uberlândia where the study was carried out, emerald moths: a phylogeny of the genus Nemoria Nayane Alves and Melissa Lopes for help in rearing larvae, (Lepidoptera: Geometridae). Mol Phylogenet Evol. – Manoel Martins Dias Filho, Eduardo Proença Barbosa and 49:477 487. Lucas Augusto Kaminski for identification of the lepidopter- Castellanos I. 2010. Does the mimetic posture of Macaria ans, Geraldo Salgado Neto for identification of the parasi- aemulataria (Walker) (Geometridae): larvae enhance sur- – toids, Rubens Queiroz for identification of plants and vival against bird predation? J Lepid Soc. 64(2):113 115. Estevão Alves da Silva for important comments and data Cook MA, Scoble MJ. 1995. Revision of the Neotropical analyses. genus Oospila Warren (Lepidoptera: Geometridae). Bull Nat Hist Mus Entomol. 64(1):1–115. Cornelissen T. 2011. Climate change and its effects on ter- restrial insects and herbivory patterns. Neotrop Entomol. Disclosure statement 40:155–163. No potential conflict of interest was reported by the authors. Del-Claro K, Lange D, Nahas L, Velasque M, Torezan- Silingardi HM. 2013. The importance of natural history studies for a better comprehension of animal-plant interactions networks. Biosc J. 29:439–448.

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