ECOLOGY, BEHAVIOR AND BIONOMICS

Ithomiini Butterflies (Lepidoptera: Nymphalidae) of Antioquia,Colombia

CE GIRALDO1, KR WILLMOTT

2, R VILA3, SI URIBE1

1Grupo de Investigación en Sistemática Molecular, Univ Nacional de Colombia, Medellín, Colombia2McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, Univ of Florida, Gainesville, FL, USA3Institut de Biologia Evolutiva (CSIC-UPF), Barcelona, Spain

AbstractKeywords

Biodiversity, Danainae, neotropics,Papilionoidea

CorrespondenceCE Giraldo, Grupo de Investigación enSistemática Molecular, Univ Nacional deColombia, Calle 59A No 63 – 20 Bl 16-102,Medellín, Colombia; cegiral0@gmail.com

Edited by André VL Freitas – UNICAMP

Received 18 September 2012 and accepted2 December 2012

* Sociedade Entomológica do Brasil 2013

Colombia is one of the most biodiverse countries on the planet.However, economic and scientific investment in completing inven-tories of its biodiversity has been relatively poor in comparisonwith other Neotropical countries. Butterflies are the best studiedgroup of invertebrates, with the highest proportion of known toexpected species. More than 3,200 species of butterflies have beenrecorded in Colombia, although the study of the still many unex-plored areas will presumably increase this number. This work pro-vides a list of Ithomiini butterflies collected in the department ofAntioquia and estimates the total number of species present, basedon revision of entomological collections, records in the literatureand field work performed between 2003 and 2011. The list includes99 species and 32 genera, representing 27% of all Ithomiini species.We report 50 species of Ithomiini not formerly listed from Anti-oquia, and found the highest diversity of ithomiine species to be atmiddle elevations (900–1,800 m). The mean value of the Chao2estimator for number of species in Antioquia is 115 species, whichis close to a predicted total of 109 based on known distributions ofother Ithomiini not yet recorded from the department. Nine spe-cies are potentially of particular conservation importance becauseof their restricted distributions, and we present range maps foreach species. We also highlight areas in Antioquia with a lack ofbiodiversity knowledge to be targeted in future studies. This papercontributes to mapping the distribution of the Lepidoptera ofAntioquia department in particular and of Colombia in general.

Introduction

Latin America and the Caribbean possess 22% of theworld’s forested lands; however, 3 million of the 8.9 millionhectares lost per year (33%) throughout the world arefound in these regions. In Colombia, it is estimated thatthe deforestation rate is 120,000 ha per year, more than320 ha per day, a situation that severely threatens thebiodiversity and natural resources of the country (FAO2009). Colombia is one of the most biodiverse countries

in the world and contains two global biodiversity hotspots:the Tropical Andes region, the richest and most diverseregion on Earth, and the Tumbes-Chocó-Magdalena hot-spot, that includes the Chocó-Darién region (ConservationInternational Foundation 2007). According to this, there isan urgent need to conduct biodiversity inventories in manyregions, which have not been done because social conflictsmake it difficult to access some specific areas and also forsome of the called governmental obstacles to biodiversityresearch (Fernandez 2011).

Neotrop EntomolDOI 10.1007/s13744-012-0102-4

Butterflies contain more than 20,000 described species,making this group the largest invertebrate clade for whichdescription of species is nearing completion (Kristensen etal 2007). A total of 3,272 species have been listed forColombia (Constantino & Andrade 2007), and additionalspecies will probably be added to the list if unexploredareas are surveyed (Gonzalez & Andrade 2008).

The department of Antioquia covers an area of 62,776 km2,and it is divided into 125 municipalities grouped in nine ad-ministrative sub-regions. It is located in the central northwest-ern part of Colombia, between 05°25′–08°55′ North and 73°53′–77°07′ West, between the Atrato and Magdalena rivers,and ranges in elevation from sea level to 3,969 m (Galeano &Bernal 1987). It includes part of the Caribbean coast and of theinter-Andean valleys, Cauca and Magdalena, covering areas inthe foothills (Atrato, Urabá, Magdalena, Bajo Cauca), centraland western mountains of the Andes and the Canyon of theCauca River besides several areas of paramo (Arias 2011),resulting in a highly diverse mix of climates and biogeograph-ical regions. Also within its boundaries are found parts of theTumbes-Chocó-Magdalena and the Tropical Andes hotspots.

There have been several papers published with lists ofbutterflies from Antioquia (Constantino 1997, Duque 2000,Henao 2006), but just one of them is focused on theNeotropical tribe Ithomiini (Muriel 2006). Ithomiini(Nymphalidae: Danainae) includes about 370 species ofbutterflies and over 1,500 geographical races occurringfrom sea level to 3,000 m, from Mexico to southernBrazil, Paraguay and across three Caribbean islands(Lamas 2004, Willmott & Freitas 2006). Ithomiini are ofspecial interest as entomological and ecological modelsbecause of their diversity, abundance, great variety ofoften precise mimicry patterns (Joron & Mallet 1998) andnarrow host plant relationships (Drummond & Brown1987), with host plant use apparently correlating in somecases with mimicry (Willmott & Mallet 2004). Most speciesinhabit shady places in the forest (García et al 2002),although several species can be found at the edges of theforest, disturbed areas and in urban or suburban systems(Brown & Freitas 2003). Ithomiines have been proposed asa biological indicator group at local, ecological scales(Brown 1991, Brown & Hutchings 1997, Fagua et al 1999,García et al 2002, Prado & Freitas 2009) and at broader,biogeographical scales (Beccaloni & Gaston 1995). Thistribe is defined by the presence in males of an elongatepatch of erectile, hair-like androconial scales at the anterioredge of the dorsal hindwing (Willmott & Freitas 2006), andis phylogenetically related to the Tellervini (containing thesingle Australasian genus Tellervo) and the largely OldWorld Danaini, together forming the subfamily Danainae(Wahlberg et al 2009).

This work extends the list of Ithomiini butterflies knownfrom the department of Antioquia, based on review of

entomological collections, literature and field work. Theinformation provided here highlights regions of Antioquiain most need of further research, in addition to increasingour knowledge of species distributions throughoutColombia.

Material and Methods

Data acquisition

Specimen locality data were obtained by examining majorpublic collections in Antioquia, through literature review,and by new field collections performed from 2003 to 2011.The entomological collections visited in Colombia were theMuseo Entomológico Francisco Luis Gallego (MEFLG-Medellín), Instituto de Ciencias Naturales–UniversidadNacional de Colombia (ICN-Bogotá), Colección Entomológicade la Universidad de Antioquia (Medellín) and ColecciónEntomológica Universidad Católica de Oriente (Rionegro). Inaddition, KRW also obtained data from a number of othercollections during taxonomic work on Ithomiini, including thefollowing: American Museum of Natural History, New York,USA; Collection André Victor Lucci Freitas, Campinas, Brazil;Booth Museum of Natural History, Brighton, UK; BMNH: TheNatural History Museum, London, UK; Carnegie Museum ofNatural History, Pittsburgh, USA; Florida Museum of NaturalHistory, Gainesville, USA; Fabio Vitale Collection, Lecce, Italy;Collection Gabriel Rodríguez, Medellín, Colombia; GSM:Grupo de Investigación en Sistemática Molecular,Universidad Nacional de Colombia sede Medellín, Colombia;Instituto de Investigación de Recursos Biológicos Alexandervon Humboldt, Claustro San Agustín, Villa de Leyva–Colombia; Collection Jean-François Le Crom Bogotá–Colombia; Museo de Historia Natural, Universidad NacionalMayor de San Marcos, Lima, Peru; Collection Sandra Muriel,Medellín–Colombia; Staatliches Museum für Naturkunde,Stuttgart, Germany; and Staatlische Museum für Tierkunde,Dresden, Germany.

Localities were georeferenced using municipality webpages and Google Earth®. Literature surveyed includedlocal publications such as thesis and conference abstracts,and published papers in indexed journals. Finally, informa-tion from recent collections and observations by theauthors in several localities of Antioquia since 2003 wasalso included.

Spatial analysis

For each locality, the political subdivision and the geomor-phological region were identified using the following sys-tem described by Arias (2011). Mid-Magdalena Valley: Eastpart of Antioquia department, characterized by alluvial

Giraldo et al

flood plains and terraces of the Magdalena river and itstributary system below 900 m; Cordillera Central: Eastern

slope of the central Colombian cordillera between 900 and3,200 m in the central area of Antioquia. This region is

Fig 1 Number of Ithomiini species by municipality in Antioquia, Colombia.

Ithomiini butterflies of Antioquia

characterized by the presence of three extensive highplateaus dissected into hills, separated by regional inclinedformations and producing a mountainous relief. The highplateaus and mountainous areas are broken up by somedeep lineal canyons (Medellín-Porce, Nus and Narecanyons).

Cauca Canyon

Formed by the western slope of the “Cordillera Central”and the eastern slope of the “Cordillera Occidental”, thisregion is a narrow and elongated basin (more than 350 kmlong) with inclined and very inclined slopes. The canyonbecomes deeper and narrower to the north.

Bajo Cauca

Frontal foothills of the “Cordillera Central” and “CordilleraOccidental” in the northern part of Antioquia, formed byhills of Tertiary sedimentary rocks, and containing alluvialfloodplains and terrace systems of the Cauca River.

Cordillera Occidental

Western slope of the “Cordillera Central” between 900 and3,969 m in the west-central part of Antioquia, and includ-ing three sections: high plateau next to the Cauca Canyonaround 2,000 m; the higher area on the “TriánguloMontañoso Tropical” including páramo areas with3,969 m as the highest altitude; and the Murrí-Mandécorridor around 1,800 m next to the Atrato valley.

Atrato–Uraba valley

Western and northwestern areas of Antioquia, bordered bythe Caribbean Sea to the north and the Antioquia Mid-Atrato area to the south. The region is characterized by

hills, alluvial flood plains and the terrace systems of theAtrato river and coast area.

Records were also categorized by elevation as tropical(0–900 m), subtropical (900–1,800 m), temperate (1,800–2,500), cold (2,500–3,400 m) and páramo (>3,400 m).Also, a finer division of the altitudinal gradient (500 m)was used to compare diversities among altitudinal rangesemploying the Jaccard similarity coefficient calculated inPast 2.17 (Hammer et al 2001).

Spatial analyses were performed to compare speciescomposition by municipality, sub-region, geomorphology,altitude and collection. Maps of species richness ofIthomiini in Antioquia were obtained using ArcGis® 10.1.All georeferenced records were plotted using a politicalbasemap divided into municipalities. We used a 0.2°×0.2°grid (25×25 km, 625 km2) to examine patterns of speciesrichness, with a single grid cell having approximately theaverage area of the municipalities of Antioquia. Grid cellswere also used as sampling units with presence–absencedata to estimate the Chao 2 richness value. The Chao 2estimator is a non-parametric method of incidence thatdoes not assume any distribution of data or model andjust requires absence/presence data (Moreno 2001). Chao2 estimator was calculated using Past 2.17 (Hammer et al2001)

Results

A total of 1,021 distribution records within Antioquia(Online Supplementary Material Appendix 1) were obtainedrepresenting all subtribes, 32 genera and 99 species(Online Supplementary Material Appendix 2), comprising27% of Ithomiini species. The mean value of Chao 2 esti-mator (95%), calculated for the grid cells sampled, was 115species. Data were obtained for 54.4% of the municipalitiesof Antioquia. The average was 11 species per municipality,

Fig 2 Number of Ithomiini species by subregion in Antioquia, Colombia.

Giraldo et al

but 44 of the 68 registered municipalities had less than 10species, and 17 municipalities had only a single species. Thehighest number of species was 48 for the municipality ofAmalfí (Fig 1). All of the sub-regions were represented, andthe average was 41 species per sub-region, but two of thenine sub-regions had less than ten species registered(Fig 2). The least diverse sub-region was Bajo Cauca with3 species, and the most diverse was Oriente with 66species. The analysis by geomorphology showed notablylow diversity for the lowland areas of the northern andwestern parts of Antioquia, Atrato-Urabá Valley and BajoCauca, with nine and three species, respectively (Fig 3). Incontrast, the richest area was Cordillera Central with 93species. The average number of species per geomorpho-logic area was 41 species. Classification of species by ele-vation showed the highest diversity for the subtropicalzone with 91 species recorded, and the lowest diversityfor the cold zone with just 4 species registered (Fig 4a).Also, the finer subdivision showed the highest diversity atelevation ranges of 1,000–1,499 and 1,500–1,999 m(Fig 4b). The Jaccard similarity coefficient showed the high-

est similarity between those altitudinal ranges too(Table 1).

The entomological collection with the highest number ofspecies from sites in Antioquia was the MEFLG with 68species, increasing to 72 species including the specimensunder cryopreservation at the associated GSM collection.In contrast, several otherwise important collections inColombia had just one record for Ithomiini butterflies col-lected in Antioquia, such as the ICN, the largestLepidoptera collection in Colombia (Fig 5). At the scale of25×25-km grid cells, the department was divided into 135cells of which 44 (33%) have at least one species registered(Fig 6).

Discussion

We report here 50 species that were not previously listedfor the tribe from Antioquia (Henao 2006). The number ofspecies recorded is notable because it doubles that hither-to reported and represents 27% of all Ithomiini species in

Fig 3 Number of Ithomiini species by geomorphological area in Antioquia, Colombia.

Fig 4 Number of Ithomiini species by altitude in Antioquia, Colombia. a Broader altitudinal classification; b Finer altitudinal classification.

Ithomiini butterflies of Antioquia

approximately 0.4% of its distribution area (approximately16,601,693 km2). Although 54% of Antioquia municipalitieshave been “sampled”, 25% of municipalities have just onespecies reported. Even with one half of the municipalitiessampled, the analysis by sub-region shows that there areseveral zones that are significantly deficient in distributiondata, such as Bajo Cauca and Urabá, which represent 30%of Antioquia. Valle de Aburra is the only sub-region thathas records in all of its municipalities. This region contains53 recorded species despite being the smallest sub-region,representing just 2.4% of the departmental area. The highlevels of collection activity here are due to the area’sproximity to Medellín, but even here collections have beenlargely opportunistic rather than systematic. Expandingcollection efforts in other areas will likely result in highertotals; for example, the inventory study at Porce II (Amalfi–Gomez Plata municipalities), mainly made by Duque(2000), lists 51 species. This number is more than a halfof the current list for the department, and these specieswere collected in a very small area (10 km2). This localitycompares in diversity with the Napo region of easternEcuador, one of the most diverse regions of the world,where 58 Ithomiini species were recorded in approximately

21 km2 (Elias et al 2007). Thus, additional species areexpected to be reported in Antioquia if similar studies arecarried out in other areas such as Urabá and Bajo Cauca.

The geomorphological areas analysis showed a similarpattern of uneven sampling. The Cordillera Central showedthe highest diversity, perhaps explained by the influence offaunas from the Magdalena valley, the Cauca canyon andBajo Cauca foothills, although it must be noted that in thisarea are located the municipalities where major collectingefforts have been made. The lowlands associated withfoothills and valleys appeared less diverse except forMagdalena, but this pattern once again could be relatedto the lack of sampling in these areas, as in Bajo Caucawhere just one locality in the municipality of Caucasia hasbeen sampled. The Cordillera Occidental might beexpected to have as many species as the CordilleraCentral, in part because of the influence of the Chocóbiogeographic region.

The altitudinal distribution patterns are in accordancewith those from studies of ithomiines in other regions, withthe highest diversity at the mid-elevation, probably relatedto overlaps of upper montane and lowland faunas at theseelevations (Elias et al 2009, Lisa de-Silva et al 2011). Mid-

Table 1 Comparison of altitudi-nal diversity of Ithomiini inAntioquia, using the Jaccardsimilarity coefficient calculatedamong altitudinal range of500 m.

Range Jaccard similarity coefficient

0–499 500–999 1,000–1,499 1,500–1,999 2,000–2,499 2,500–3,000

0–499 1 0.267606 0.314607 0.329545 0.238806 0.0454545

500–999 – 1 0.597561 0.541176 0.276316 0.0344828

1000–1499 – – 1 0.698925 0.458824 0.0740741

1500–1999 – – – 1 0.493976 0.0740741

2000–2499 – – – – 1 0.152174

2500–3000 – – – – – 1

Fig 5 Number of Ithomiini species with Antioquia records by collection or publication.

Giraldo et al

elevations (subtropical-temperate climate) in Antioquiarepresent just 25% of its surface, but they contain 97% ofthe species here listed. Museum collections are undoubt-edly the main source of information about Ithomiini distri-bution. The local collection MEFLG includes the highestnumber of species from Antioquia in any collection.Created in 1937, this is one of the younger museums

studied here, but it nevertheless contains more than1,300 specimens of ithomiines collected in Antioquia.However, there are 12 species that are known from thedepartment only from specimens deposited in collectionsoutside of Colombia. Collections in other countries arelocated principally in Europe, such as the BMNH inLondon, which contains 54 species for Antioquia, and they

Fig 6 Species richness of Ithomiini in Antioquia, Colombia. Grid cells are 0.2°×0.2° (2× 25 km, 625 km2).

Ithomiini butterflies of Antioquia

constitute a very important source of information becausethey preserve many specimens collected before the in-crease in deforestation in Antioquia that started with theColombian Industrial Revolution. Species that are repre-sented only by historical material are perhaps of particularconservation interest because of their apparent rarity inrecent years, and could be the subject of future studies inlocal population dynamics, regional distribution and con-servation priorities. These species include Callithomia lenea

(Cramer), Episcada hymenaea (Prittwitz), Greta ochretis(Haensch), Greta esula (Hewitson), Hyalenna sulmona(Hewitson), Hyalyris exelsa (Felder & Felder), Hyposcadaschausi (Fox), Ithomia jucunda (Godman & Salvin), Oleriacyrene (Latreille), Ollantaya olerioides (d'Almeida), Oleriaquadrata (Haensch), Tithorea pacifica (Willmott & Lamas)and Velamysta phengites (Fox). However, species that areuncommon in Antioquia are not necessarily endemic to thedepartment or to Colombia. Of far greater significance for

Fig 7 Distribution maps of priority Ithomiini species for study in and around Antioquia.

Giraldo et al

conservation efforts in Antioquia are those species that areendemic, or almost endemic, to Colombia that also occur inAntioquia: Ceratinia iolaia (Hewitson), Godyris nepos(Weymer), Greta n. sp., Ithomia hymettia (Staudinger),Ithomia lagusa (Hewitson), Napeogenes benigna(Weymer), Pteronymia medellina (Haensch), Pteronymialaura (Staudinger) and Oleria thiemei (Oberthür). Becauseof their high endemism and low frequency in collections,these species should be priorities for research into theirdistribution, biology and local population dynamics, and weprovide distribution maps in Fig 7.

In contrast, there are several species that may be con-sidered common because they have been collected in morethan 25% of the municipalities with specimen records.However, species records by municipality provide a rela-tively unreliable measure of distribution because munici-palities differ in area. Using an equal-area analysis (25×25 km grid) (Fig 6), we identified several “common” speciesincluding: Athesis clearista (Doubleday), Ceratinia tutia(Hewitson), Dircenna dero (Hübner), Dircenna olyras(Felder & Felder), Elzunia humboldt (Latreille), Episcadapolita (Weymer), Greta andromica (Hewitson), Ithomiaiphianassa (Doubleday), Mechanitis polymnia (Linnaeus),Mechanitis menapis (Hewitson), Mechanitis lysimnia(Fabricius), Napeogenes stella (Hewitson), Oleria fumata(Haensch), Oleria amalda (Hewitson), Pseudoscada timna(Hewitson), Pteronymia aletta (Hewitson), Pteronymia lat-illa (Hewitson), Hypoleria lavinia (Hewitson), Hypoleria oca-lea (Doubleday), Hypothyris euclea (Godart) and Hypothyrislycaste (Fabricius) (Fig 8). The grid cell analysis showedonce more the undersampling in much of Antioquia, with67% of grid cells without records. Grid cells were also usedas sampled units of presence/absence data to estimaterichness. The lower value of Chao 2 estimator (95%) sug-gests a maximum of 104 species for the cells sampled(Fig 9). Even though the number of species here registered

is 99, an additional 10 species are expected to occur inAntioquia based on their known distributions in Colombia,including: Callithomia hydra (Felder & Felder; known fromPanama to Venezuela, but not yet recorded in Colombia),Episcada sylpha (Haensch; known from Magdalena andCésar departments), Methona confusa (Butler) (knownfrom Panama, Nariño department and Amazon region),Napeogenes cranto (Felder & Felder; known from Nariño,Boyacá, Cundinamarca, Magdalena, Tolima and Valle delCauca departments), Oleria n. sp. (known from Nariño andValle del Cauca departments), Pteronymia alissa(Hewitson; known from Cundinamarca and Nariño depart-ments), Pteronymia alida (Hewitson; known from Valle delCauca and probably the Cordillera Oriental), Pteronymiafumida (Schaus; known from Valle del Cauca andRisaralda departments), Pteronymia obscuratus (Fabricius;known from Magdalena department) and Velamystapupilla (Hewitson; known from Quindío department).

With these additional species, the estimated number ofithomiine species for Antioquia department reaches 109,close to the mean value of Chao 2 estimator (115 species;see Fig 9). Spatial patterns of species richness in Ithomiiniin Antioquia show a similar pattern to those found for thevascular plants in this department, where collection effortsare highly correlated with proximity to the capital city(Medellín) (Idarraga & Callejas 2001). Since areas near tothe capital are among the most deforested in Antioquia,areas of the department with the best preserved forestareas, likely to have the most intact ithomiine faunas(Brown 1991, Beccaloni & Gaston 1995, García et al 2002;Brown & Freitas 2003), have yet to be intensively sampled(Fig 10). In addition, these little-studied areas are located inthe Tumbes-Chocó-Magdalena hotspot, particularly in thewestern (next to the Atrato river and Urabá region) andnortheastern regions (Bajo Cauca region). Most of the spe-cies listed here appear to have been collected in forest relicts

Fig 8 Proportion of all grid cells occupied by common species of Ithomiini in Antioquia, Colombia.

Ithomiini butterflies of Antioquia

within the most deforested region of Antioquia, highlightingthe importance of these relict forests for biodiversity conser-vation and demonstrating that protection and managementmeasures directed to these regions are worthwhile. In addi-tion, it is likely that surveys of unexplored well-preservedforested areas will also result in new discoveries.

Finally, several priority areas for future research on but-terfly biodiversity in Antioquia department are suggested.

Firstly, areas to the north and northeast, including munici-palities of the Bajo Cauca and Nordeste sub-regions, espe-cially municipalities with well-preserved forest such as Anorí,El Bagre, Nechí, Tarazá, Zaragoza and Zegovia, included in theTumbes-Chocó-Magdalena hotspot and currently a targetarea for mining. Secondly, unstudied areas next to theAtrato river in the municipalities of Vigía del Fuerte andMurindó, also part of the Tumbes-Chocó-Magdalena

Fig 10 Comparison of patterns of a Ithomiini richness and b extent of forested areas in 2006 in Antioquia (Modified of Instituto GeográficoAgustín Codazi 2007a, b).

Fig 9 Species accumulation curve and Chao 2 estimator of Ithomiini richness, using grid cells as units of analysis with specimen record presence/absence data.

Giraldo et al

hotspot. Unfortunately, these areas mentioned above havereduced accessibility because of social conflict, and biodiver-sity studies in such regions are not easily accomplished.

It is clear that a considerable amount of sampling is stillneeded to obtain a reliable inventory of Ithomiini speciesfor Antioquia and, eventually, for Colombia. The majorissues preventing an increase in our knowledge ofColombian biodiversity are not the lack of training or moti-vated researchers, but the social conflict in many areas thatlimits accessibility, the lack of financial support and therecent numerous governmental barriers to studying biodi-versity in Colombia. Antioquia is one of the best studieddepartments for insect diversity in Colombia, together withCundinamarca and Valle del Cauca departments, so an evenworse panorama is expected for the rest of the country. It isbecoming clear that much of the biodiversity of the countryis still unknown while deforestation and mining exploitationcontinue and habitats are reduced and fragmented. It is thusurgent to increase efforts to document and protect biodiver-sity in Colombia and, to this end, government strategiesshould be directed to support scientific investigation.

Acknowledgments We thank Efraín Henao, Gonzalo Andrade, JeanFrancois LeCrom, Marta Wolff, Oscar Ortega and John Quiroz for lettingus review local collection. We also thank Luis Alberto Arias for hissupport in the geomorphological description of Antioquia and Alba LucíaMarín for her help in maps design. Support for this research wasprovided by the Sciences School of the Universidad Nacional de Colom-bia sede Medellín and the Fundación BBVA (MARIPOSA Proyect: BIO-CON08_021). KRW acknowledges support from the Leverhulme Trust,and thanks to the many museum curators and individuals who facilitat-ed access and research in ithomiine collections. Gerardo Lamas, JimMallet and Fraser Simpson provided particularly important data andsupport for databasing efforts at the BMNH.

Electronic supplementary material The online version of this article(doi:10.1007/s13744-012-0102-4) contains supplementary material,which is available to authorized users.

References

Arias LA (2011) Estructura y clasificación del relieve en el departa-mento de Antioquia. In Callejas R, Idarraga A (eds). Flora deAntioquia: Catálogo de las plantas vasculares, vol. I, Introducción.Programa Expedición Antioquia −2103. Series Biodiversidad yRecursos Naturales–Universidad de Antioquia, Missouri BotanicalGarden y Oficina de Planeación departamental de la gobernaciónde Antioquia. Bogotá, D’Vinni, p. 326

Beccaloni GW, Gaston KJ (1995) Predicting the species richness ofNeotropical forest butterfl ies: Ithomiinae (Lepidoptera:Nymphalidae) as indicators. Biol Conserv 71(1):77–86

Brown KS JR (1991) Conservation of neotropical environments insectsas indicators. The conservation of insects and their habitats, 349–404. In: Symposium XV Royal Entomology Society. Academic Press,London, p 450

Brown KSJR, Freitas AVL (2003) Butterfly communities of urban forestfragments in Campinas, São Paulo, Brazil: structure, instability,

environmental correlates and conservation. J Insect Conserv6:217–231

Brown KS JR, Hutchings RW (1997) Disturbance, fragmentation andthe dynamics of diversity in Amazonian forest butterflies. In:Laurance WF, Bierregaard RO Jr (eds) Tropical forest remnants.Ecology, management, and conservation of fragmented communi-ties. The University of Chicago Press, Chicago, pp 91–110, 632

Conservation International Foundation (2007) Biodiversity Hotspots.Web site: http://www.biodiversityhotspots.org/xp/hotspots/Pages/default.aspx. Accessed 23 Jan 2012

Constantino LM (1997) Conocimiento de los ciclos de vida y plantashospederas de lepidópteros diurnos de Colombia como estrategiapara el manejo, uso y conservación de poblaciones silvestres, pp.259–278. In: Seminario Aconteceres Entomológicos, para compren-der los insectos: estudiarlos. Universidad Nacional de Colombia,Medellín, p 282

Constantino LM, Andrade G (2007) Mariposas diurnas y nocturnas,p.107-143. In Amat G, Andrade G, Amat E (eds) Libro Rojo de losInvertebrados Terrestres de Colombia. Bogotá, Instituto de CienciasNaturales – Universidad Nacional de Colombia, ConservaciónInternacional Colombia, Instituto Alexander von Humbolt, Ministeriode Ambiente, Vivienda y Desarrollo Territorial.Colombia, 216p

Drummond BA III Jr, Brown KS (1987) Ithomiinae (Lepid.:Nymphalidae): summary of know larval foodplants. Ann Mo BotGard 74:341–358

Duque P (2000) Diversidad de Mariposas diurnas en diferentes frag-mentos de bosque en la zona de influencia del proyectohidroeléctrico Porce II. Tesis de Maestría Universidad Nacional deColombia sede Medellín

Elias M, Hill RI, Willmott KR, Dasmahapatra KK, Brower AVZ, Mallet J,Jiggins CD (2007) Limited performance of DNA barcoding in adiverse community of tropical butterflies. Proc R Soc London SerB 274:2881–2889

Elias M, Joron M, Willmott KR, Silva-Brandão KL, Kaiser V, Arias CF,Gomez LM, Uribe S, Brower AV, Jiggins CD (2009) Out of theAndes: patterns of diversification in clearwing butterflies. MolEcol 18:1716–1729

Fagua G, Aarillo AR, Andrade MG (1999) Las mariposas (LEPIDOPTERA:RHOPALOCERA) como indicadores del grado de intervención en lacuenca del Río Pato (Caquetá, Colombia), p. 285–315, In Amat G,Andrade-C G, Fernandez F (eds) "Insectos de Colombia. Vol. 2".Bogotá, Academia Colombiana de Ciencias Exactas, Físicas yNaturales. Instituto de Ciencias Naturales, Universidad Nacionalde Colombia, 433p

FAO (Organización de las Naciones Unidas para la Agricultura y laAlimentación) (2009) Situación de los bosques del mundo.Subdivisión de Políticas y Apoyo en Materia de PublicaciónElectrónica División de Comunicación. FAO, Rome, p 158

Fernandez F (2011) The greatest impediment to the study of biodiver-sity in Colombia. Caldasia 33(2):1–5

Galeano G, Bernal R (1987) Palmas del Departamento de Antioquia.Región Occidental. 1ra. Edición. Universidad Nacional de Colombia,Bogotá, p 221

García CA, Constantino LM, Heredia MD, Katan G (2002) Mariposascommunes de la cordillera central de Colombia, Guía de campo.Editorial Feriva, Cali, p 130

Gonzalez LA, Andrade G (2008) Diversidad y biogeografía preliminarde las mariposas saltarinas (Lepidoptera: Hesperiidae) de Colombia.Rev Acad Colomb Cienc 32(124):421–433

Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statisticssoftware package for education and data analysis. PalaeontologiaElectronica 4(1): 9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm. Accessed 30 Nov 2012

Henao E (2005) Los Papilionidae del Museo Entomológico “FranciscoLuis Gallego” (Lepidoptera: Papilionoidea). Bol Cient Mus Hist NatUniv Caldas 9:154–163

Ithomiini butterflies of Antioquia

Henao E (2006) Aproximación a la distribución de mariposas delDepartamento de antioquia (papilionidae, Pieridae y Nymphalidae:Lepidoptera) con base en Zonas de vida. Bol Cient Mus Hist Nat UnivCaldas 10:279–312

Idarraga A, Callejas R (2001) Análisis florístico de la vegetación delDepartamento de Antioquia. In: Idarraga A, Ortiz R del C,Callejas R, Merello M (eds) Flora de Antioquia: Catálogo de lasplantas vasculares. Vol II. Programa Expedición Antioquia −2103.Series Biodiversidad y Recursos Naturales - Universidad deAntioquia, Missouri Botanical Garden y Oficina de Planeacióndepartamental de la gobernación de Antioquia. Bogotá,D’Vinni, 939p

IGAC (Instituto Geográfico Agustín Codazi) (2007a) Estudio semi-detallado de las coberturas terrestres, Departamento deAntioquia 2007. Instituto Geográfico Agustín Codazzi,Subdirección de Agrología –Gobernación de Antioquia, Medellín,p 260

IGAC (Instituto Geográfico Agustín Codazi) (2007b) Leyenda de cober-turas terrestres, según metodología CORINE Land Cover,Departamento de Antioquia, escala 1:25000. Instituto GeográficoAgustín Codazzi, Subdirección de Agrología–Gobernación deAntioquia, Medellín, p 260

Joron M, Mallet J (1998) Diversity in mimicry: paradox or paradigm?Trends in Ecology and Evolution 13:461–466

Kristensen NP, Scoble MJ, Karsholt O (2007) Lepidoptera phylogenyand systematics: the state of inventorying moth and butterflydiversity. Zootaxa 1668:699–747

Lisa De Silva D, Day J, Elias M, Willmott K, Whinnett A, Mallet J (2011)Molecular phylogenetics of the neotropical butterfly subtribeOleriina (Nymphalidae: Danainae: Ithomiini). Mol Phylogenet Evol55:1032–1041

Lamas G, ed. (2004) Ithomiinae, pp.172–191. In Atlas of neotropicalbutterflies. Checklist: 4A. Hesperioidea–Papilionoidea. Scientific,Gainesville, p. 439

Moreno CE (2001) Métodos para medir la biodiversidad. Zaragoza,M&T–Manuales y Tesis SEA, vol.1, 84p

Muriel S (2006) Mariposas Ithomiinae (Fam: Nymphalidae) deparches de vegetación natural del suroccidente Antioqueño(Colombia). Bol Mus Entomol Univ Valle 7(2):1–8

Orozco JM (2006) Mariposas: guía de campo. Universidad Católica deOriente, Cornare, CIFFA, Rionegro, p 88

Orozco S, Muriel S, Palacio J (2009) Diversidad de lepidópterosdiurnos en un área de bosque seco tropical del Occidenteantioqueño. Actualid Biol Medellin 31(90):31–41

Prado MU, Freitas AVL (2009) The effect of rainforest fragmentationon species diversity and mimicry ring composition of ithomiinebutterflies. Insect Conserv Divers 2:23–28. doi:10.1111/j.1752-4598.2008.00025.x

Velez A, Duque P, Wolff M (2009) Mariposas del Parque ecológicoPiedras Blancas: Guía de Campo. Fondo editorial ComfenalcoAntioquia, Medellín, p 201

Wahlberg N, Leneveu J, Kodandaramaiah U, Peña C, Nylin S, FreitasAVL, Brower A (2009) Nymphalid butterflies diversify followingnear demise at the Cretaceous/Tertiary boundary. Proc R SocLond B Biol Sci. doi:10.1098/rspb.2009.1303

Willmott KR, Freitas AV (2006) Higher-level phylogeny of theIthomiinae (Lepidoptera: Nymphalidae): classification, patterns oflarval hostplant colonization and diversification. Cladistics 22(4):297–368

Willmott KR, Mallet J (2004) Correlations between adult mimicry andlarval hostplants in ithomiine butterflies. Proc R Soc London Ser B271 (Biology Letters S5): S266–S269

Giraldo et al