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Caterpillars and host plant records for 59 species of Geometridae (Lepidoptera) from a montane rainforest in southern Ecuador

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Florian Bodner, Gunnar Brehm, Jürgen Homeier, Patrick Strutzenberger, Konrad Fiedler
DOI: http://dx.doi.org/10.1673/031.010.6701 First published online: 15 June 2010

Abstract

During four months of field surveys at the Reserva Biológica San Francisco in the south Ecuadorian Andes, caterpillars of 59 Geometridae species were collected in a montane rainforest between 1800 and 2800m altitude and reared to adults. The resulting data on host plant affiliations of these species was collated. The preimaginal stages of 58 and adult stages of all 59 species are depicted in colour plates. Observations on morphology and behaviour are briefly described. Five species, documented for the first time in the study area by means of larval collections, had not been previously collected by intensive light-trap surveys. Together with published literature records, life-history data covers 8.6% of the 1271 geometrid species observed so far in the study area. For 50 species these are the first records of their early stages, and for another 7 the data significantly extend known host plant ranges. Most larvae were collected on shrubs or trees, but more unusual host plant affiliations, such as ferns (6 geometrid species) and lichens (3 geometrid species), were also recorded. Thirty-four percent of the caterpillars were infested by wasp or tachinid parasitoids.

  • Andes
  • host plant affiliations
  • insect herbivores
  • larval morphology
  • pupal morphology
  • Neotropical
  • caterpillars

Introduction

Herbivorous insects are important primary consumers of plant biomass in terrestrial ecosystems. They also comprise a major fraction of animal biodiversity on earth (Meyhew 2001; Novotny et al. 2004). The diversity of tropical herbivorous arthropods has been at the centre of an ongoing debate about the magnitude of global animal species richness. While available estimates agree that true species richness is far higher than the number of species currently described, there is considerable controversy regarding the extent to which the various estimates diverge. Levels of host plant specificity in herbivorous insects play a critical role in all these estimates (Erwin 1982; Ødegaard 2000; Novotny et al. 2002). It is still debated whether host specificity is higher in tropical rather than temperate ecosystems (e.g. Fiedler 1998; Novotny and Basset 2005; Novotny et al. 2006; as opposed to: Dyer et al. 2007). However, what most authors tend to agree on is a severe lack of data, hindering a thorough investigation of this topic. Consequently the gathering of additional host plant data can be seen as the obvious step for improving our understanding of biodiversity, ecology and evolution of tropical herbivorous insects (Scriber 2002; Novotny and Basset 2005). This study aims to increase available host plant data for Neotropical representatives of the lepidopteran family Geometridae, at an Andean site where large-scale ecosystem studies are currently under way (Beck et al. 2008a).

Materials and Methods

Study organisms

Geometridae are one of the three largest families of Lepidoptera, with a global total of more than 21000 described species, 6450 of which occur in South America (Scoble 1999). Montane forests in the Ecuadorian Andes were recently identified as one of the global hotspots for geometrid species diversity (Brehm et al. 2005), with 1266 recorded species (and an estimated total of >1450 species) occurring in one relatively small nature reserve (Brehm et al. 2005, see below). Brehm (2002) collated host plant records for 48 geometrid species that occur in the study area, gathered mainly from his own caterpillar collections (Brehm 2003) and supplemented by web-based sources (Janzen and Hallwachs 2009, Robinson et al. 2009). Since then, host plant records for 11 more species occurring in the study area have been reported (Dyer and Gentry 2009; Dyer et al. 2009), increasing the data set to 59 species (=4.7% of the local species list).

Study area and field work

Data were collected in the Reserva Biológica San Francisco (RBSF), a privately owned nature reserve adjacent to Podocarpus National Park (since 2007 part of the UNESCO biosphere reserve “Podocarpus-El Condor“) in southern Ecuador (province Zamora-Chinchipe). The study area, located on the eastern slope of the Andes, has been the target of intensive ecological research since 1997 (Beck et al. 2008a). Caterpillar samples were taken at an elevation ranging from 1800–2800m above sea level. However, the majority of the data was collected at an elevation of 1800–2100m, in close proximity to the Estación Científica San Francisco (3°58’ S, 79°05’ W), during the period from February 1 to May 28, 2006.

RBSF is covered by nearly pristine montane rain forest (Beck et al. 2008b; Homeier et al. 2008). Its moth fauna has been studied intensively (1999–2006) by light-trapping, offering insight into patterns of moth diversity and community structure (e.g.: Brehm et al. 2003; Fiedler et. al. 2008; Hilt and Fiedler 2008).

Caterpillars were collected by visually scanning vegetation during the day and by searching with lights during the night, as well as by common plant-beating techniques (e.g. Schauff 1986; Leather 2005). Caterpillars were transferred to the laboratory and kept in plastic boxes. These were lined with damp paper towel to maintain high humidity. Caterpillars were fed with their appropriate host plant until pupation. Old food plant material was replaced every 2–3 days. Pupae were kept in similar plastic boxes until adult emergence.

One species, Pantherodes conglomerata, was reared from eggs obtained from a light-caught adult female. In this case, several plants were experimentally offered to find a suitable host plant.

Documentation

Larval stages were documented using digital photographs, taken from different aspects on a regular basis and whenever developmental changes were observed. For size measurements, scaled paper was used as background for caterpillar photographs. Host plants were also photographed. Pictures were taken with a Canon EOS 300D digital single lens reflex camera (3072 x 2048 pixel resolution), equipped with a Sigma 105mm F2.8 EX DG macro lens and a Sigma EM-140 DG macro flash.

Data processing and identification

Reared moths were identified to species when possible, or were sorted as morphospecies by comparison with previously identified specimens or with digital photographs of identified material. Caterpillars that failed to develop into adults were preserved in 70% ethanol, as were pupal exuviae and parasitoids that emerged in captivity. Nomenclature follows Pitkin (2002, 2005) for members of the subfamily Ennominae and Scoble (1999) for all remaining species. Morphospecies ID codes of Brehm et al. (2005) were used. New codes were assigned to five species previously unknown from the study area.

Hymenopteran parasitoids were identified to family level using the keys to the Hymenoptera of Costa Rica (Hanson and Gauld, 1995). One specimen was identified to family by Martin Schwarz (Biologiezentrum Linz-Dornach, Austria).

Host plants were identified from pictures taken in the field, in some cases with the help of the online data base Visual Plants (Homeier and Dalitz 2009). Plant family delimitations follow APG II (2003). Moth vouchers have been deposited in the research collection of G. Brehm at the Phyletisches Museum of the Zoological Institute, University of Jena, Germany.

Results and Discussion

During the field surveys 325 caterpillars of Geometridae were collected. Of these caterpillars, 105 individuals were successfully reared to adults. Four specimens of two Eois species (Larentiinae) that failed to develop were assigned to morphospecies, known from previous light trapping, by means of DNA barcoding. For barcoding we used a 676 bp fragment in the 5' part of the mitochondrial cytochrome oxidase subunit I (COI) gene (Valentini et al. 2008). Neighbour-joining clustering provided unambiguous assignments of the larval sequences to sequences from adult samples gathered by Strutzenberger (2010). Altogether, the surveys resulted in information on host plant associations and caterpillar morphology for 59 geometrid species (43 Ennominae, 2 Sterrhinae, and 15 Larentiinae). A search of the literature, as well as web-based databases, suggests that for 50 of these species, these are the first reports available.

Overview and rearing success

Two hundred and twenty caterpillars (68%) died in captivity: 54 (17%) due to the emergence of parasitoids, 166 (51%) from infections, moulting difficulties, handling mistakes, or food refusal. The overall rearing success (32%) was surprisingly close to the 33% success rate reported by Brehm (2003). Of the 220 caterpillars that failed to develop into adults, 81 (37%) could be reliably identified through caterpillar morphology, and four individuals representing 3 species were identified through DNA barcoding. The remaining 139 caterpillars represented approximately 40–50 additional morpho-species.

Parasitoids

Of the 325 caterpillars collected, 54 (17%) produced larvae or imagines of parasitoid wasps and flies. The parasitoids included 31 solitary hymenopterans (22 Braconidae, 8 Ichneumonidae, and 1 Chalcididae). One caterpillar produced three hymenopterans of the family Eulophidae. Seven hymenopteran individuals from five caterpillars failed to develop to adulthood and could not yet be assigned to family.

In addition, 11 representatives of the family Tachinidae successfully developed to the adult stage, one failed to develop. Another five solitary parasitoids, that did not develop successfully, could not be reliably assigned to either Hymenoptera or Diptera. No incidences of multiparasitism or superparasitism were observed (see Godfray 1994). If caterpillars that died from unknown reasons or by accident are excluded, the overall incidence of parasitism increased to 54 of 159 individuals (= 34%). However, due to the small sample size and the unstandardized sampling approach, these figures can only be viewed as a very crude gross estimate for parasitation rates of the whole family of Geometridae in this area.

Host plants

In general, all plants within the lower 2–3 m of vegetation were searched for caterpillars, but some plant taxa received particular attention. These included the genus Piper (Piperaceae) for investigation of the putative association between these plants and the geometrid genus Eois (see Dyer and Palmer 2004), the family Asteraceae, and the fern genus Pteridium (Dennstaedtiaceae). The latter are dominant plant taxa in disturbed habitats of the study area and are therefore of high ecological interest for understanding forest regeneration in the Andes of southern Ecuador (Beck et al. 2008c; Hartig and Beck 2003).

Table 1 presents the resulting data on host plant affiliation, together with information on the approximate body length of the last instar caterpillars and references to additional records on the preimaginal stages of each species (if available).

View this table:
Table 1

Reared Geometridae species, sorted by subfamily, tribe and genus. For every species the number of emerged adults and the number of assigned dead caterpillars (in brackets) are shown. Also information on host plants and approximate body length in mm (L) of the last instar larvae before entering the prepupal phase is listed. ID numbers follow BREHM et al. (2005, electronic supplement). In five cases, new IDs were assigned to species not previously recorded in the study area; all five species are so far identified at generic level. References to available literature on the caterpillars or host plant affiliations are coded: GB: BREHM (2003), JH: JANZEN & HALLWACHS (2008), D: DYER et al. (2008) and R: ROBINSON et al. (2008). Species that could not yet be formally identified and therefore could not be compared with literature are marked with *. Geometrid taxonomy follows Pitkin (2002, 2005) for the subfamily Ennominae and Scoble (1999) for all remaining subfamilies.

Fam. / Subfam. / Genus/ SpeciesHost plant familyHost plant speciesLNIDLit.
Ennominae
Azelinini
Pero maculicosta Warren, 1897MyricaceaeMyrica pubescens451251
Boarmiini
Bryoptera sp. 21 66LamiaceaeHyptis sp.5512166(n)*
Glena sp. nr. juga Rindge, 1967TiliaceaeHeliocarpus americanus401265*
Glena sp. 21 67BegoniaceaeBegonia parviflora4012167(n)*
Iridopsis scolancala Prout, 1932AsteraceaeAgeratina dendroides351259
Iridopsis sp. nr. subnigrata Warren, 1905ViburnaceaeViburnum stipitatum401256*
EricaceaeCavendishia sp.1
Melanolophia atigrada Dognin, 1893MyricaceaeMyrica pubescens401199
Melanolophia corza Dognin, 1895AsteraceaeBaccharis latifolia4012103
TiliaceaeHeliocarpus americanus1
Melanolophia reducta meridiana Rindge, 1964AsteraceaeBaccharis latifolia401269D,GB
Caberini-Baptini
Oenoptila sp. nr. nigriceps Warren, 1907Lichensp. Indet.251 (2)1002*
Physocleora curvifera Dognin, 1906Solanaceaeprob. Solanum sp.301905
Melastomataceaesp. indet.1
Cratoptera-Group
Apiciopsis sp. 21 68SolanaceaeSolanum nutans3512168*
Callipseustes sp. 2169UrticaceaeBoehmeria sp.2022169*
Mychonia corticinaria Herrich-Schäffer, 1855AsteraceaeMunnozia hastifolia251166
Mychonia violacea Warren, 1907MelastomataceaeMonochaetum lineatum251921
Nacophorini
Cargolia arana Dognin, 1895MelastomataceaeTibouchina lepidota25175R
Ischnopteris brehmi Pitkin, 2005MelastomataceaeTibouchina laxa451308GB 7
ClethraceaeClethra revoluta2
Rucana bisecta Dognin, 1914ViburnaceaeViburnum stipitatum351660
Nephodiini
Bonatea duciata Maassen, 1890Ericaceaesp. indet.60180(JH8)
Bonatea viridilinea Warren, 1904AsteraceaeErato polymnioides60276D,GB
MalvaceaeSida rhombifolia1
MelastomataceaeMonochaetum lineatum1
MyricaceaeMyrica pubescens(1)
Nephodia admirationis Prout, 1911AnacardiaceaeTapirira guianensis4011092
Nephodia sp. nr. astyochiodes Warren, | 904 5Ericaceae 1sp. indet. 1351299*
Ourapterygini
Isochromodes brumosa Dognin, 1896GleicheniaceaeSticherus sp.401828D
MelastomataceaeAxinaea sp. JH263 11
DennstaedtiaceaePteridium arachnoideum1
Isochromodes duplicata Warren, 1904Urticaceaesp. indet.451842
Isochromodes fraterna Warren, 1904ActinidiaceaeSaurauia sp.401109GB
PiperaceaePiper sp. "Type III"1
OnagraceaeFuchsia lehmannii1
Isochromodes polvoreata Dognin, 1893BegoniaceaeBegonia parviflora45198D
BignoniaceaeTabebuia chrysantha401106*
ClethraceaeClethra revoluta1
Isochromodes sp. 106MelastomataceaeTibouchina lepidota1
Miconia sp.1
DennstaedtiaceaePteridium arachnoideum1
Mesedra sp. nr. confinis Warren, 1904MelastomataceaeTibouchina laxa301178*
Mesedra sp. 180DennstaedtiaceaePteridium401180*
Perusia praecisaria Herrich-Schäffer, 1855ScrophulariaceaeStemodia suffruticosa201812
Unplaced genera
Certima sp. 97AsteraceaeMunnozia hastifolia40197*
Eustenophasma fuscata Warren, 1907UrticaceaeBoehmeria sp.--12075
Microxydia colorata Warren, 1904 4RubiaceaeFaramea cf. uniflora151159
Microxydia sp. nr. ruficomma Prout, 1910AsteraceaeBaccharis latifolia154 (2)695GB
Baccharis sp.1
Nematocampa sp. nr. falsa Warren,Lichensp. indet.151130*
Pantherodes conglomerata Warren, 1894UrticaceaeBoehmeria sp. 230--298
Phyllodonta flabellaria Thierry-Mieg, 1894MyricaceaeMyrica pubescens40145
Phyllodonta semicava Warren, 1904MelastomataceaeAxinaea sp. JH263 140147
Prochoerodes pilosa Warren, 1897Ericaceae 1sp. indet. 150189JH 6
Sabulodes bolivaria Oberthür, 1911BignoniaceaeTabebuia chrysantha40192D
SapindaceaePaullinia grandifolia1
Sabulodes thermidora Thierry-Mieg, 1894AsteraceaeBaccharis genistelloides351 (1)125GB
Sabulodes sp. nr. carbina Druce, 1892Lichensp. indet.251 (1)122*
Sterrhinae
Cosymbiini
Cyclophora costinotata Warren, 1900SiparunaceaeSiparuna aspera2011D
Cyclophora viator Prout, 1920MyricaceaeMyrica pubescens251845
Larentiinae
Erateinini
Erateina radiaria Herrich-Schäffer, 1853MelastomataceaeMonochaetum206 (8)1057(D 8)
Erateina siliquata Guenée, 1858MelastomataceaeTibouchina laxa2021055
Euphyiini
Perizoma emmelesiata Snellen, 1874MelastomataceaeTibouchina laxa301 (1)486
Eupitheciini
Eois encina Dognin, 1899PiperaceaePiper sp. "Type III"204 (3)378
Eois muscosa Dognin, 1910 3PiperaceaePiper sp. "Type VIII"--3803
Eois olivacea Felder & Rogenhofer, 1875PiperaceaePiper perareolatum151416D
Eois tegularia Guenée, 1858 3PiperaceaePiper sp. "Type I"---1836(D 8)
Eois sp. nr. encina Dognin, 1899PiperaceaePiper carpunya208 (6)412*
Eois sp. nr. odatis Druce, 1892PiperaceaePiper sp. "Type I"152 (7)419*
Eupithecia lachaumei Herbulot, 1987DennstaedtiaceaePteridium203(1 5)563
Eupithecia sobria Prout, 1910EricaceaeGaultheria erecta154 (2)674
Eupithecia yangana Dognin, 1899MyricaceaeMyrica pubescens201 (3)667GB
Eupithecia sp. 2170DennstaedtiaceaePteridium arachnoideum1512170 (n)*
Hydriomenini
Psaliodes inundulata Guenée, 1858DennstaedtiaceaePteridium104(28)488
Larentiini
Spargania narangilla Dognin, 1893ActinidiaceaeSaurauia sp. JH1 604252451
  • 1 Original host plant unknown, since specimen was not found on a plant, but later accepted alternative food

  • 2Species was not reared from collected caterpillars, but from eggs obtained from caught female

  • 3Caterpillars failed to develop and were later identified through DNA barcodes

  • 4Leg. Friedrich Angermüller & Alexander Hähnel

  • 5Leg. Jutta Kapfer

  • 6Probably not conspecific with specimen from present study (conflicting preliminary identifications)

  • 7Unnamed at date of publication of BREHM (2003), hence there reported as 'Ischnopteris sp. nr. chryses'

  • 8Not conspecific with specimen from present study (conflicting preliminary identifications)

Our observations increase the number of Geometridae species from the Reserva Biológica San Francisco, for which life-history information is available, from 59 to 109. This amounts to 8.6% of the 1271 species recorded so far in the general study area, and to 10.2% (100 species) if the fauna is restricted to the 977 species so far recorded at the elevation covered by this research.

Remarks on host plant affiliations

Two thirds of the moth species covered in this study were encountered only once, therefore those host plant affiliations must be interpreted with care. It may sometimes occur that a species is found and successfully reared on a plant, which is not part of its natural host plant range. On the other hand, even single records may provide important insight into patterns of host use if they can be placed in a comparative context.

In our study, a high number of species use host plants or food sources that are considered unusual for Geometridae (and for macromoths in general), such as ferns (e.g. Hendrix 1980; Lawton 1982; Weintraub et al. 1995) and lichens (e.g. Lawrey 1987; Hesbacher et al.1995). Of the 59 species treated in this study, six (10%) were recorded from bracken fern (Mesedra sp. [180, see Table 1], Eupithecia lachaumei, Eupithecia sp. [2170], Psaliodes inundulata,Isochromodes brumosa, Isochromodes sp. [106]). Isochromodes brumosa feeds on umbrella fern (genus Sticherus, Gleicheniaceae) in addition to bracken fern.

Fern feeding in the Geometridae is confined to a few isolated specialists or to small sub-clades (e.g. Ennominae-Lithinini: Holloway 1987; Weintraub et al. 1995), although polyphagous feeders of spermatophytes occasionally accept ferns as minor hosts (Hendrix 1980; Robinson et al. 2009). While Hendrix (1980) described ferns as generally underutilized, Lawton (1982) pointed out that bracken fern does support a sizable fauna of herbivores, at least in parts of its distribution. Three geometrid species (5%) were recorded on lichens (Sabulodes sp. nr. carbina, Perusia sp. nr. nigriceps, Nematocampa sp. nr. falsa).

The species-rich genus Eois (Geometridae: Larentiinae) is of particular interest for questions regarding host plant specialization. Eois species are hypothesized to specialize on Piper (Piperacee) throughout the Neotropics (e.g. Dyer and Palmer 2004). In our study, caterpillars of four Eois species were reared to adults and caterpillars of two more were identified by DNA barcodes. All were found exclusively on Piper. Each Eois was encountered only on a single species of Piper, and only E. sp. nr. odatis and E. tegularia shared the same host plant.

Eois olivacea feeds on two different hostplants in northeastern Ecuador (Dyer et al. 2009): Piper baezanum, which appears very similar to the host plant recorded in our study and Piper longifolium. However, different caterpillar color morphs are consistent in feeding each Piper, suggesting that ‘Eois olivacea’ might comprise more than one species (G. Rodríguez and L. Dyer, personal communication). This is supported by DNA barcoding results and phylogenetic analysis using a combination of nuclear and mitochondrial genes (Strutzenberger 2010) as well as by caterpillar records from our study site (F. Bodner, unpublished data).

Observations on morphology and behaviour

In general, geometrid caterpillars are cryptic in appearance, with brown, green and grey tones predominating. Some resemble twigs (e.g.: Pero maculicosta, Figure 1), lichens (e.g.: Oenoptila sp. cf. nigriceps, Figure 11; Nematocampa sp. nr. falsa, Figure 39), or mossy bark (e.g. Phyllodonta semicava, Figure 42; Cargolia arana,Figure 17), while others seem to be inconspicuously coloured to the human eye. Whether their crypsis pertains to particular predators, such as visually hunting birds, requires further assessment (Church et al. 1998). An account of notable observations on certain species is given below.

Figure 1

Pero maculicosta Warren, 1897.

Figure 2. Bryoptera sp. [2166].

Figure 3. Glena sp. nr. juga Rindge, 1967.

Figure 4. Glena sp. [2167].

Figure 5. Iridopsis scolancala Prout, 1932

Figure 6-7. Iridopsis sp. nr. subnigrata Warren, 1905.

Figure 8. Melanolophia atigrada Dognin, 1893.

Figure 9. Melanolophia corza Dognin, 1895.

Figure 10. Melanolophia reducta meridianaRindge, 1964.

Figure 11. Oenoptila sp. nr. nigriceps Warren, 1907.

Figure 12. Physocleora curvifera Dognin, 1906.

Figure 13. Apiciopsis sp. [2168]; probably L4 (top) and L5 (bottom).

Figure 14. Callipseustes sp. [2169]; probably L5.

Figure 15. Mychoniacorticinaria Herrich-Schäffer, 1855; probably L4 (left) and L5 (right).

Figure 16. Mychonia violacea Warren, 1907; probably L4(left) and L5 (right).

Figure 17. Cargolia arana Dognin, 1895. Caterpillars are last instars except where indicated differently. The scale bars are 1 cm in length, except where indicated as “1/2”. High quality figures are available online.

The two specimens of Iridopsis sp. nr. subnigrata differ strongly in colouration (Figure 6–7) remarkably matching that of their respective host plants. Callipseustes sp. [2169] (Figure 14) shows bright red colouration making it conspicuous against the green leaves of its host plant (Boehmeria species, family Urticaceae), but matching the red twigs.

The caterpillars of Mychonia violacea (Figure 16) and Mychonia corticinaria (Figure 15) show similar colouration, but differ in the number and shape of their dorsal protuberances. However, adult wing pattern and colouration in both specimens (Figure 87 and Figure 88) is similar. Further morphological studies are required in this species complex.

Figure 73. Pero maculicosta Warren, 1897. Figure 74. Bryoptera sp. [2166]. Figure 75. Glena sp. nr. juga Rindge, 1967. Figure 76. Glena sp. [2167]. Figure 77. Iridopsis scolancala Prout, 1932. Figure 78. Iridopsis sp. nr. subnigrata Warren, 1905. Figure 79. Melanolophia atigrada Dognin, 1893. Figure 80. Melanolophia corza Dognin, 1895. Figure 81. Melanolophia reducta meridiana Rindge, 1964. Figure 82. Oenoptila sp. nr. nigriceps Warren, 1907. Figure 83. Physocleora curvifera Dognin, 1906. Figure 84. Apiciopsis sp. [2168]. Figure 85-86. Callipseustes sp. [2169]. Figure 87. Mychonia corticinaria Herrich-Schäffer, 1855. Figure 88. Mychonia violacea Warren, 1907. Pictures show both dorsal (left half) and ventral (right half) side of same individual. High quality figures are available online.

Figure 89. Cargolia arana Dognin, 1895. Figure 90-91. Ischnopteris brehmi Pitkin, 2005. Figure 92. Rucana bisecta Dognin, 1914. Figure 93. Bonatea duciata Maassen, 1890. Figure 94. Bonatea viridilinea Warren, 1904. Figure 95. Nephodia admirationis Prout, 1911. Figure 96. Nephodia sp. nr. astyochiodes Warren, 1904. Figure 97. Isochromodes brumosa Dognin, 1896. Figure 98. Isochromodes duplicata Warren, 1904. Figure 99. Isochromodes fraterna Warren, 1904. High quality figures are available online.

Figure 100. Isochromodes polvoreata Dognin, 1893. Figure 101. Isochromodes sp. [106]. Figure 102. Mesedra sp. nr. confinis Warren, 1904.Figure 103. Mesedra sp. [180]. Figure 104. Perusia praecisaria Herrich-Schäffer,1855. Figure 105. Certima sp. [97]. Figure 106. Eustenophasma fuscata Warren, 1907. Figure 107. Microxydia colorata Warren, 1904. Figure 108-109. Microxydia sp. nr. ruficomma Prout, 1910. Figure 110. Nematocampa sp. nr. falsa Warren, 1906. Figure 111. Pantherodes conglomerata Warren, 1894. High quality figures are available online.

Figure 112. Phyllodonta flabellaria Thierry-Mieg, 1894. Figure 113. Phyllodonta semicava Warren, 1904. Figure 114. Prochoerodes pilosa Warren, 1897. Figure 115. Sabulodes bolivaria Oberthür, 1911. Figure 116. Sabulodes thermidora Thierry-Mieg, 1894. Figure 117. Sabulodes sp. nr. carbina Druce, 1892. Figure 118. Cyclophora costinotata Warren, 1900. Figure 119. Cyclophora viator Prout, 1920. Figure 120. Erateina radiaria Herrich-Schäffer, 1853. Figure 121. Erateina siliquata Guenée, 1858. High quality figures are available online.

Caterpillars of Ischnopteris brehmi (Figure 19) have lateral bulges at at the 2nd abdominal segment. Pupae of I. brehmi (pupae not shown) and Rucana bisecta (Figure 21) have the antenna and trunk sheaths extended to a spike that reaches down to about half of the free moving portion of the abdomen. In the third reared Nacophorini, Cargolia arana (Figure 18), the antenna and trunk sheaths extended only beyond the wing sheaths. This feature was not mentioned by Rindge (1983) in his revision of the Nacophorini or by Pitkin (2002, 2005), but may be a synapomorphy for the tribe. On the other hand, Parra and Henriquez-Rodriguez (1993) showed the pupae of two Nacophorini (Mallomus falcatus and M. tumidus) that lacked this feature, possibly suggesting that this character state is restricted to a smaller clade within the Nacophorini.

Figure 18. Cargolia arana Dognin, 1895; pupa. Figure 19. Ischnopteris brehmi Pitkin, 2005; probably L4 (top) and L5 (bottom).

Figure 20-21. Rucana bisecta Dognin, 1914; L5 (Figure 20) and pupa (Figure 21).

Figure 22. Bonatea duciata Maassen, 1890.

Figure 23-24. Bonatea viridilinea Warren, 1904; L5 (Figure 23 and 24 bottom); L3 or L4 (Figure 24 top).

Fig ure 25-2 6. Nephodia admirationis Prout, 1911; L5 (Figure 25) and pupa (Figure 26). Figure 27. Nephodia sp. nr. astyochiodes Warren, 1904.

Figure 28. Isochromodes brumosa Dognin, 1896. Figure 29. Isochromodes duplicata Warren, 1904. High quality figures are available online.

Figure 30. Isochromodes fraterna Warren, 1904. Figure 31. Isochromodes polvoreata Dognin, 1893. Figure 32. Isochromodes sp. [106]. Figure 33. Mesedra sp. nr. confinis Warren, 1904.Figure 34. Mesedra sp. [180]. Figure 35. Perusia praecisaria Herrich-Schäffer,1855. Figure 36. Certima sp. [97]. Figure 37. Microxydia colorata Warren, 1904. Figure 38. Microxydia sp. nr. ruficomma Prout, 1910. Figure 39. Nematocampa sp. nr. falsa Warren, 1906. Figure 40. Pantherodes conglomerata Warren, 1894; probably L4 (top) and L5 (bottom). Figure 41. Phyllodonta flabellaria Thierry-Mieg, 1894. Figure 42. Phyllodonta semicava Warren, 1904. Figure 43. Prochoerodes pilosa Warren, 1897. Figure 44-46. Sabulodes bolivaria Oberthür, 1911; L5 (Figure 44-45) and pupa (Figure 46). High quality figures are available online.

Five species that, according to their adult morphology, belong in the genus Isochromodes, showed divergent caterpillar morphology. Caterpillars of I. duplicata (Figure 29) have two black bulges on the 5th abdominal segment that were present in all instars. The caterpillar of I. polvoreata (Figure 31) has the third thoracic leg elevated on an enlarged basis and a dorsal and lateral protuberance on the 3rd abdominal segment. Together these made the caterpillar resemble a dead twig with two leaf scars. Caterpillars of Isochromodes sp. [106] (Figure 32) and I. fraterna (Figure 30) varied in a similar range of green and brown colours with or without white and brown dorsal markings. No clear diagnostic characters could be identified.

The caterpillar of Perusia praecisaria (Figure 35) shows two thin elongated dorsal protuberances: a long one forking into two points, and a shorter one on the 2nd and 3rd abdominal segments, respectively. The caterpillar is similar to that of Melinodes subapicata (see Brehm 2003). Perusia and Melinodes are currently placed in different tribes (Ourapterygini and Cratoptera-group, respectively, Pitkin 2002). The striking similarity between Perusia praecisaria and Melinodes subapicata caterpillars instead suggests a close relationship between these species. Further studies in both genera as well as in related taxa are required to resolve the relationships between the Ourapterygini and the Cratoptera-group.

The Microxydia colorata caterpillar was of pronouncedly different appearance than those of Microxydia sp. nr. Ruficomma. On adult morphology, Pitkin (2002) stated that “M. colorata has a more complex wing pattern unlike that of other Microxydia species.” Taken the differences of adult and larval morphology into accout, we suggest that M. colorata is misplaced within this genus. Further morphological studies are required.

The caterpillar of Prochoerodes pilosa (Figure 43) displayed a behaviour of pulling the first three segments together to form a uniform knob with the head and thoracic legs (Figure 43 top). The caterpillar thus mimicked a dead twig or leaf stalk. Sabulodes bolivaria (Figure 44–46) was found in two individuals. One (Figure 44), found as an early instar, developed a rather intensive, dark colouration. The other caterpillar (Figure 45), found in its last instar, had a pale colouration with some parts of the pattern completely missing. Both caterpillars preferred to hide within a leaf-tent, as mentioned by Brehm (2003) for this genus.

Two Cyclophora species (C. costinotata, Figure 4950 and C. viator, Figure 5152) were reared. In both, the anteriorly truncated pupae bear a silk girdle around the 3rd abdominal segment (Figure 50 and52). This trait is supposedly apomorphic for the genus Cyclophora and some, possibly all, other genera in the tribe Cosymbiini (Holloway 1997; Sihvonen and Kaila 2004).

Figure 47. Sabulodes thermidora Thierry-Mieg, 1894. Figure 48. Sabulodes sp. nr. carbina Druce, 1892; probably F5. Figure 49-50. Cyclophora costinotata Warren, 1900; L5 (Figure 49) and pupa (Figure 50). Figure 51-52. Cyclophora viator Prout, 1920; L5 (Figure 51) and pupa (Figure 52). Figure 53-54. Erateina radiaria Herrich-Schäffer, 1853. Figure 55. Erateina siliquata Guenée, 1858. Figure 56. Perizoma emmelesiata Snellen, 1874. Figure 57. Eois encina Dognin, 1899. Figure 58. Eois muscosa Dognin, 1910; probably L4 or L5. Figure 59. Eois olivacea Felder and Rogenhofer, 1875. Figure 60 & 63. Eois tegularia Guenée, 1858; probably L4 or L5. Figure 61-62. Eois sp. nr. encina Dognin, 1899. Figure 64. Eois sp. nr. odatis Druce, 1892. Figure 65-66. Eupithecia lachaumei Herbulot, 1987; probably L5 (Figure 65) and L4 or L5 (Figure 66). Figure 67. Eupithecia sobria Prout, 1910; L2 or L3 (left) and L5 (right). Figure 68. Eupithecia yangana Dognin, 1899; L3 or L4 (top) and L4 or L5 (bottom). Figure 69. Eupithecia sp. [2170]; probably L4. Figure 70-71. Psaliodes inundulata Guenée, 1858. Figure 72. Spargania narangilla Dognin, 1893. High quality figures are available online.

Most Eois caterpillars show some shade of green and have black, sometimes also white markings (Figure 57–64). The amount of these markings generally increased with development, but was also variable between individuals within the species Eois encina (Figure 57) and Eois sp. nr. encina (Figure 61-62). Images of several Eois species shown by Dyer and Gentry (2009), Dyer at al. (2009) and Janzen and Hallwachs (2009) provide further examples of pronounced intraspecific variation.

The status of Eupithecia lachaumei is uncertain, where pronounced variation in caterpillar coloration (Figure 65-66) is paralleled by subtle differences in wing pattern (Figure 130-131), possibly pointing to the existence of a species complex.

Figure 122. Perizoma emmelesiata Snellen, 1874. Figure 123. Eois encina Dognin, 1899. Figure 124. Eois muscosa Dognin, 1910. Figure 125. Eois olivacea Felder and Rogenhofer, 1875. Figure 126 & 128. Eois tegularia Guenée, 1858. Figure 127. Eois sp. nr. encina Dognin, 1899. Figure 129. Eois sp. nr. odatis Druce, 1892. Figure 130-131. Eupithecia lachaumei Herbulot, 1987. Figure 132. Eupithecia sobria Prout, 1910. Figure 133. Eupithecia yangana Dognin, 1899. Figure 134. Eupithecia sp. [2170]. Figure 135. Psaliodes inundulata Guenée, 1858. Figure 136. Spargania narangilla Dognin, 1893. High quality figures are available online.

Most caterpillars of Psaliodes inundulata are green (Figure 70), but a few showed diffuse dark patterns making them almost black (Figure 71).

Spargania narangilla (Figure 72) displayed interesting pupation behaviour; caterpillars build their cocoon in a hole in the leaf and covered it with chewed bits of leaf (data not shown). This gave the impression of a dead leaf area, rather than a cocoon.

In general, the geometrid larvae we studied are ectophagous, except that caterpillars of Eupithecia sobria feed inside the flowers of their host plant in the early stages (Figure 67 left). Later instars (Figure 67 right) feed partially exposed on the flowers and fruits.

Conclusions

With these results, the number of Geometridae species from the Reserva Biológica San Francisco, for which life-history information is now available, nearly doubled. The simple sampling methods used in this study have the potential to unravel many novel facets of the interactions between herbivorous insects and their host plants in Andean rain forests. These forests suffer heavily from ongoing deforestation (Beck et al. 2008a; Mosandl et al. 2008). Therefore, the Andean fauna deserves more intense research so that, as additional information is gathered, this will allow for more in-depth comparisons with ongoing studies at the well established focal sites in tropical lowland forests (e.g., Janzen and Hallwachs 2009; Novotny et al. 2009).

Acknowledgments

Cordial thanks go to Manuela Zimmermann for most friendly collaboration in the field and for kindly taking care of some pupae and caterpillars. We also thank Dr. Sabine Fischer for her kind assistance in field and laboratory work. Dr. Linda Pitkin (formerly at the Natural History Museum London, UK) helped with the identification of Ischnopteris species and provided helpful information on these. Dr. Genoveva Rodríguez and Dr. Lee Dyer (both Tulane University, New Orleans, USA) shared information on Eois olivacea and its host plants. Dr. Martin Schwarz (Biologiezentrum Linz-Dornach, Austria) helped with the identification of a hymenopteran parasitoid. Benjamin Hell (University of Oldenburg, Germany) provided help in Piper identifications. Further thanks go to several collaborators of the German Research Group in Ecuador for providing caterpillars they found during forest trips and also to all the remaining staff and inhabitants of the Estación Científica San Francisco. Alexandra Zach (University of Göttingen, Germany) kindly undertook a large part of the sample transport to Europe. Dr. Christian Schulze, Dr. Martin Wiemers and two anonymous reviewers gave valuable comments and helped to improve the manuscript. Additional thanks go to Dr. James Miller who much improved the style of the manuscript. The Deutsche Forschungs-gemeinschaft financed this project within the framework of the research groups FOR 402 (Fi 547/6-3) and FOR 816 (Fi 547/10-1). The Ministerio del Medio Ambiente del Ecuador issued research permits, and the foundation Nature and Culture International (Loja, Ecuador) as well as the Universidad Técnica Particular de Loja gave logistic support and allowed access to the study area and their facilities.

Footnotes

  • Associate Editor: James Miller was editor of this paper

  • Received October 10, 2008.
  • Accepted June 17, 2009.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, providedthe original work is properly cited.

References

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