Biology and occurrence of Inga Busk species (Lepidoptera: Oecophoridae) on Cerrado host plants

Biologia e ocorrência de espécies de Inga Busk (Lepidoptera: Oecophoridae) em plantas hospedeiras de Cerrado

ECOLOGY, BEHAVIOR AND BIONOMICS

Biology and occurrence of Inga Busk species (Lepidoptera: Oecophoridae) on Cerrado host plants

Biologia e ocorrência de espécies de Inga Busk (Lepidoptera: Oecophoridae) em plantas hospedeiras de Cerrado

Ivone R. Diniz^I; Carolina Bernardes^II; Sheila Rodovalho^III; Helena C. Morais^IV

^IDepto. Zoologia, [e-mail]

^IIBacharelado em Ciências Biológicas

^IIIMestre em Ecologia. Instituto de Ciências Biológicas

^IVDepto. Ecologia, Instituto de Ciências Biológicas, [e-mail]

ABSTRACT

We sampled Inga Busk species caterpillars weekly in the cerrado on 15 plants of Diospyros burchellii Hern. (Ebenaceae) from January 2002 to December 2003, on 30 plants of Caryocar brasiliense (Caryocaraceae) from July 2003 to June 2004, and since 1991 on several other plant species. In total we found 15 species of Inga on cerrado host plants. Nine species were very rare, with only one to five adults reared. The other six species occurred throughout the year, with higher abundance during the dry season, from May to July, coinciding with overall peaks of caterpillar abundance in the cerrado. Caterpillars of the genus Inga build shelters by tying and lining two mature or old leaves with silk and frass, where they rest and develop (a common habit found in Oecophorinae). The final instar builds a special envelope inside the leaf shelter, where it will complete the larval stage and pupate. The species are very difficult to distinguish in the immature stages. External features were useful in identifying only four species: I. haemataula (Meyrick), I. phaecrossa (Meyrick), I. ancorata (Walsingham), and I. corystes (Meyrick). These four species are polyphagous and have wide geographical distributions. In this paper we provide information on the natural history and host plants of six Inga species common on cerrado host plants, for which there are no reports in the literature.

Key words:Caryocar, diet, Diospyros, leaf shelter, Oecophorinae

RESUMO

Dada a ausência de informações sobre a biologia de lagartas que ocorrem em plantas de cerrado, apresentamos aqui algumas informações sobre larvas do gênero Inga Busk. Lagartas foram coletadas, semanalmente, em 15 indivíduos de Diospyros burchelli Hern. (Ebenaceae), de janeiro de 2002 a dezembro de 2003, em 30 indivíduos de Caryocar brasiliense Camb. (Caryocaraceae), de julho de 2003 a junho de 2004 e, em várias outras espécies de plantas desde 1991. No total foram encontradas 15 espécies de Inga em plantas de cerrado, no DF. Nove espécies foram raras com até cinco adultos obtidos em criação no laboratório. As outras seis espécies ocorreram durante o ano sendo mais abundantes entre maio e julho (estação seca), o que coincide com a época de maior abundância de lagartas no cerrado. As lagartas do gênero Inga constroem abrigos, juntando duas folhas maduras ou velhas com fios de seda, onde se alimentam e desenvolvem (um hábito comum entre os Oecophorinae). Larvas de último instar constroem, dentro do abrigo, um tipo de envelope onde completam seu desenvolvimento e empupam. A separação das espécies das lagartas é muito difícil. Características externas permitem o reconhecimento de apenas quatro espécies de Inga: I. haemataula (Meyrick), I. phaecrossa (Meyrick), I. ancorata (Walsingham), and I. corystes (Meyrick). Essas quatro espécies têm ampla distribuição geográfica e são polífagas. Neste artigo, apresentamos informações não encontradas na literatura sobre a história natural de seis espécies de Inga comuns em plantas hospedeiras de cerrado.

Palavras-chave: Abrigo de folhas, Caryocar, dieta, Diospyros, Oecophorinae

Except for species considered as pests in cultivated areas, very little is known of the immature stages of tropical Lepidoptera and their host plants in natural environments, especially for micromoths. Most knowledge is discontinuous and deals particularly with butterflies and macromoths (e. g. Brown & Freitas 1994, Furtado & Lemaire 1999, Morais & Diniz 2003).

The Oecophoridae are widely distributed in Australia where their caterpillars specialize in eating fallen Eucalyptus leaves (Gullan & Cranston 2005), and are common also throughout North America. Most Oecophoridae are of little or no economic importance; however, a few Oecophorinae can be serious pests throughout the world (Costa-Lima 1945, Stehr 1987). Despite the high species richness of Australian Oecophoridae the genus Inga Busk (Oecophorinae, Oecophorini) is predominantly Neotropical, with few species occurring in Neartic regions (Hodges 1972).

Heppner (1984) published a list of 98 Inga species, which, together with their synominies, comprised 110 names. Of these, 94 were first collected in South America, 28 at type localities in Brazil, especially in the Amazon Region (states of Amazonas and Pará) and in the states of São Paulo, Rio de Janeiro and Pernambuco. The only other information about the genus Inga in Brazil concerns the occurrence of I. crossota (Walsingham) (= Machimia crossota) whose caterpillar eats mango leaves (Ribeiro 1951).

Caterpillars of three large and diverse moth families, Oecophoridae, Gelechiidae and Cosmopterigidae, present very similar morphologies (Stehr 1987). These similarities are encountered amongst Inga caterpillars. It is very difficult to separate the species using characters of the caterpillars, and it is necessary in most cases to rear them to adults for identification. Additional studies that include caterpillar diagnosis are needed to provide more accuracy in species identification of immatures.

The present study provides data on biological and ecological aspects of Inga species on cerrado host plants in Brazil, especially on Diospyros burchelli Hern (Ebenaceae) and Caryocar brasiliense Camb. (Caryocaraceae). Our studies of these micro-moth caterpillars had three primary objectives: i) to describe morphological traits and behavior of the caterpillars of different species; ii) to determine their diet breadth on the cerrado vegetation; and iii) to compare the variation of this fauna on two taxonomically unrelated host plants.

Material and Methods

The data presented here were obtained from (a) previous surveys of Inga caterpillars on several cerrado host plant species, since 1991 (Diniz et al. 2001), and (b) specific surveys of Inga caterpillars carried out by us on D. burchelli from January 2002 to December 2003, and on C. brasiliense from July 2003 to June 2004.

D. burchelli is a deciduous plant, common in the cerrado vegetation, which looses and replaces leaves during the transition from dry to wet seasons (September-October), and is pubescence on both surfaces of new leaves. C. brasiliense is a tree, also very common in the cerrado, which reaches about 6 m in height, loosing and flushing its leaves at the end of the dry season (August-September), and producing pubescent new leaves.

The fieldwork was carried out in an area of cerrado sensu stricto (Oliveira-Filho & Ratter 2002), at the Fazenda Água Limpa (FAL), experimental farm of the Universidade de Brasilia (15° 56'S, 47° 54'W), near Brasilia in the Federal District, Brazil.

Fifteen plants of D. burchelli and 30 of C. brasiliense were examined weekly for caterpillars. All Inga caterpillars were collected, brought to the laboratory, and reared in plastic cages until adult emergence. To maintain the swelling turgidity of the leaves, the petioles were immersed in moist cotton, and fresh leaves were supplied to the caterpillars every two days. Behavioral and developmental aspects, such as the construction of shelters and the duration of the pupal stage, were observed in the field and under laboratory conditions. All data presented here were based on adult emergence in the laboratory.

Vitor O. Becker identified the moth species, and voucher specimens were deposited in the Entomological Collection of the Zoology Department of the University of Brasilia.

Results

The caterpillars of 15 species of Inga were reared to adults (n = 388) (Fig. 1). These species were found and reared on 36 host species representing 21 plant families. However, only six species were identified to species level. These species showed wide geographical distribution based on each type localities: I. ancorata (Walsingham) from Costa Rica, I. corystes (Meyrick) from Guyana, I. encamina (Meyrick) from Venezuela, I. erythema (Walsingham) from Guatemala, I. haemataula (Meyrick,) from São Paulo, Brazil, and, I. phaeocrossa (Meyrick) from Rio de Janeiro, Brazil (Heppner 1984) (Table 1).

Inga phaeocrossa and I. haemataula were the most abundant species on the majority of plant species surveyed, and the type localities of both species are Brazil (Heppner 1984). Nine species were very rare, with only one to five adults reared (Table 1). Of the six species with more than 10 adults reared, five were polyphagous, and the other (sp. # 14) had been found, up to now, only on Davilla elliptica St.Hil. (Dilleniaceae). Though I. ancorata was found on three host plants, it showed a strong preference for C. brasiliense as evidenced by the fact that only three individuals out of 69 were encountered on other plants. Two plant species D. burchellii and Qualea parviflora Mart. (Vochysiaceae) supported the highest richness of Inga species (seven species).

We surveyed 1,464 plants of D. burchellii and found 419 caterpillars, 83 of which belonged to the genus Inga. We reared 56 caterpillars to adults representing seven species of Inga, of which I. haemataula was the most abundant, accounting for 75% of all Inga fauna of D. burchellii (Table 1). The caterpillars of Inga on D. burchellii were present from January to August, being most frequent from May to July, which coincides with the first half of the dry season in the cerrado (Fig. 2). None of the Inga caterpillars on D. burchellii (n = 83) suffered from parasitoid attacks.

We surveyed 1,250 plants of C. brasiliense and found 570 caterpillars of which 88 belonged to Inga species. Four species of Inga were represented, of which I. ancorata was the most abundant, accounting for 75% of the Inga fauna on C. brasiliense (Table 1). Inga caterpillars on C. brasiliense were present all year, except in September and October, and were most frequent from May to July, which is the first half of the dry season in the cerrado (Fig.2). Five (9%) caterpillars of I. ancorata were parasitized by Hymenoptera.

The early-instars of all species build their shelters, opened at the extremities, by binding two mature or senescent leaves together with silk, and lining them with a layer of frass interwined with silk threads, where, they feed and use it as a resting place. As the larvae mature they begin to forage outside the leaf shelter. Caterpillars reacted to any disturbance outside the shelter by wiggling off the leaf and suspending themselves by silken threads. Later instars cut spheres of about 3 cm in diameter and build an envelope-like structure big enough to fit inside the leaf shelter. All Inga species pupated inside the envelopes on the same host plant where they lived and fed as caterpillars.

In the laboratory, the pupal duration of I. haemataula was an average of 27.7 days ± 5.4 (n = 10), noticeably longer than that of I. ancorata (18.3 days ± 8.3, n = 66), I. phaeocrossa (20 days ± 2.3, n = 7), or I. encamina (15 days ± 2.9, n = 11), and pupal duration varied enormously within each species, even when reared on the same host plant. In I. ancorata, for example, the minimum duration was seven days and the maximum was 74 days (n = 66).

The immature stages of some Inga species are extremely difficult to distinguish using morphological features. Two species, I. ancorata (Fig. 3a) and I. corystes, have pale green tegument but can be distinguished by the color of the head, which is pale green in the former and shiny black in the latter. Inga sp. 5 and Inga sp. 15 are similar to I. corystes, and no particular feature was found to distinguish among these three species.

Other species such us I. phaeocrossa, I. haemataula, and I. encamina are much more difficult to distinguish without careful observation of their features under high magnification. Inga haemataula has the head and prothothoracic shield reddish chestnut color, body paler than head and prothothoracic shield, with longitudinal pale brownish stripes with spots of the same color between them; mesothoracic segment with two black pinacula surrounded by a pale yellow circle; metathoracic segment pale yellow with chestnut-color stripes; prolegs each with a bright orange spot (Fig. 3b). I. encamina is similar to I. haemataula except that the head is reddish brown and lacks the two black pinacula. Inga sp.3 is similar to I. haemataula, and no particular feature was found to distinguish the caterpillars of these two species. Inga phaeocrossa (Fig.3c) colored and patterned as I. haemataula, but with pale brownish head and tegument, and the body with brownish stripes paler and less well defined than those of I. haemataula, and the prolegs lacking the orange spots.

Discussion

Inga abundance increases sharply from April to July (the peak) during the first half of the dry season, matching the general peak of caterpillar abundance in the cerrado (Morais et al. 1999). Larvae of all species of Inga were found mainly on mature leaves that were reaching senescence or even dry. That wasn't surprising because most members of the Oecophorinae eat dead plant material, and rarely eat live plants (Hodges 1972, Gullan & Cranston 2005).

Young leaves of D. burchellii have high concentrations of trichomes on both surfaces. Caterpillar preference for mature or senescent leaves could be due to the low density of trichomes found on mature leaves of this plant, or perhaps reflects lower concentrations of protective chemicals. D. burchellii leaves mature from March to August, coinciding with the highest abundance of Inga species on them. The total absence of any species of Inga from September to December corresponds to the falling of leaves or the recent flushes on this host plant.

Apart from I. phaeocrossa, I. haemataula, I. corystes and I. encamina, the immature stages of other species could not be identified precisely using external features. I. haemataula and I. phaeocrossa were the most abundant species, making it easier to find external features that would distinguish them from the others. Other species must be found in large enough numbers to permit specific identifying features of each species to be found. According to Vitor Becker (pers. com.), even the adults of many species belonging to this genus are unnamed and more studies are needed for their identification.

Leaf shelters are known to protect caterpillars from predators (Damman 1987, Ruehlmann et al. 1988, Loeffler 1996), to create favorable microclimates (Henson 1958, Larsson et al. 1997), and to increase the quality of the leaves on which they feed. (Sagers 1992, Costa & Varanda 2002). Inga shelters in the Brazilian cerrado are found during the driest season, and perhaps help caterpillars to avoid desiccation by creating a more humid microclimate. The shelters may help as well to avoid parasitoids, given that very few larvae were parasitized. Another explanation for the low proportion of parasitized larvae might be that dry season is the period of lowest parasitoid abundance in the cerrado, providing enemy free space (Morais et al. 1999).

Whereas pupation duration and shelter building of some species of Inga could be well observed under laboratory conditions, and the larvae of a few could be identified easily, experiments involving complete life cycles still need to be carried out to increase our understanding on biological aspects of all species of Inga. Also, very little information is available about the biology of the adults. Further studies are needed to determine whether individuals of polyphagous species lay their eggs on the same plant species that they developed on. This work provides the first set of ecological and biological information for the moth genus Inga. Although it is well recognized that most phytophagous insects tend to feed on more or less closely related host plants rather than on a random selection of plants from a local flora (Strong et al. 1984, Novotny et al. 2002), we have shown that in the cerrado Inga caterpillars feed on a wide variety of non-related host plant families including some isolated ones, such as Caryocaraceae and Proteaceae both of which are monotypic in this region. Our results are based on an extensive data set that showed a strong preference by I. ancorata for C. brasiliense, suggesting a change of host plant utilization by this species during its life cycle.

Acknowledgments

We thank M. Haridassan and two anonymous reviewers for their useful suggestions, several students at the University of Brasília with data collection, and valuable information, B. Baker-Méio for copies of articles, Fausto Silva for the photographs and, V. O. Becker for identification of Inga species. This research was supported by CNPq and FAPDF.

Received 28/III/06. Accepted 18/IX/06.

• Brown, K.S. & A.V.L. Freitas. 1994. Juvenile stages of Ithomiinae: An overview and systematics (Lepidoptera: Nymphalidae). Trop. Lepid. 5: 9-20.
• Costa, A.A. & E.M. Varanda. 2002. Building of leaf shelters by Stenoma scitiorella Walker (Lepidoptera: Elachistidae): Manipulation of host plant quality? Neotrop. Entomol. 31: 537-540.
• Costa-Lima, A. 1945. Insetos do Brasil. 5ş tomo, Lepidópteros 1Ş parte. Rio de Janeiro, Escola Nacional de Agronomia, 379p.
• Damman, H. 1987. Leaf quality and enemy avoidance by the larvae of a Pyralid moth. Ecology 68: 88-97.
• Diniz, I.R., H.C. Morais & A.J.A. Camargo. 2001. Host plants of Lepidopteran caterpillars in the cerrado of the Distrito Federal, Brazil. Rev. Bras. Entomol. 45: 107-122.
• Furtado, E. & C. Lemaire. 1999. The biology and immature stages of Automeris granulosa (Lepidoptera: Saturniidae: Hemileucinae). Trop. Lepid. 10: 27-29.
• Gullan, P.J. & P.S. Cranston. 2005. The insects: An outline of entomology. New York, Blackwell, 505p.
• Henson, W.R. 1958. Some ecological implications of the leaf rolling habits in Compsolechia niveopulvella Can. J. Zool. 36: 809-818.
• Heppner, J.B. (ed.). 1984. Atlas of Neotropical Lepidoptera. Checklist: Microterigoidea-Immoidea. Gainesville, Junk Publishers, 112p.
• Hodges, R.W. 1972. Taxonomic notes on the Gelechioidea Part 1: The genus Inga Proc. Entomol. Soc. Wash. 74: 371-374.
• Larsson, S., H.E. Häggström & R.F. Denno. 1997. Preference for protected feeding sites by larvae of the willow-feeding leaf beetle Galerucella lineola Ecol. Entomol. 22: 445-452.
• Loeffler, C.C. 1996. Caterpillar leaf folding as a defense against predation and dislodgement: Staged encounters using Dichomeris (Gelechiidae) larvae on goldenrods. J. Lepidopterists' Soc. 50: 245-260.
• Morais, H.C. & I.R. Diniz. 2003. Larva and host plant of the Brazilian cerrado moth Aucula munroei (Lepidoptera: Noctuidae). Trop. Lepid. 11: 49-50.
• Morais, H.C., I.R. Diniz & D.M.S. Silva. 1999. Caterpillar seasonality in a central Brazilian cerrado. Rev. Biol. Trop. 47: 1025-1033.
• Novotny, V., Y. Basset, S.E. Miller, G.D. Weiblen, B. Bremer, L. Cizek & P. Drozd. 2002. Low host specificity of herbivorous insects in a tropical forest. Nature 416: 841-844.
• Oliveira Filho, A.T. & J.A. Ratter. 2002. Vegetation physiognomies and woody flora of the Cerrado Biome, p.91-120. In P.S. Oliveira & R.J. Marquis (eds.), The cerrados of Brazil. New York, Columbia University Press, 398p.
• Ribeiro, J.H.C. 1951. Um ecoforídeo em folhas de mangueira (Lepidoptera, Tineoidea). Agronomia 10: 105-108.
• Ruehlmann, T.E., R.W. Matthews & J.R. Matthews. 1988. Roles for structural and temporal shelter changing by fern-feeding lepidopteran larvae. Oecologia 75: 228-232.
• Sagers, C.L. 1992. Manipulation of host plant quality: Herbivores keep leaves in the dark. Funct. Ecol. 6: 741-743.
• Stehr, F.W. (ed.) 1987. Immature insects. Duduque, Kendall/Hunt Publ., 478p.
• Strong, D.R., J.H. Lawton & S.R. Southwood. 1984. Insects on plants. Cambridge, Harvard University Press, 347p.

Publication Dates

• Publication in this collection
  02 Oct 2007
• Date of issue
  Aug 2007

History

• Received
  28 Mar 2006
• Accepted
  18 Sept 2006