Introduction
The Caribbean is the Colombian region with the largest and best-preserved fragments of Tropical Dry Forest (TDF) (Pizano & García, 2014), but it is also threatened by its increasing transformation (Freitas, et al., 2003; Orozco, et al., 2009; Montero, et al., 2009). The progressive loss of the forest enhances the importance of each fragment and its biodiversity and demands its conservation (Montero, et al., 2009). The tropical dry forest serves to the diagnosis and evaluation of conservation strategies (Vargas-Zapata, et al., 2011) and, therefore, its study is of great scientific interest.
Lepidoptera is the third most studied order of butterflies; the specimens are abundant and easy to collect and to identify (Llorente, et al., 1993; Montero, et al., 2009); they also play important roles in trophic chains and as plant pollinators (Constantino & Andrade-C., 2007). Many species have been used for environmental monitoring as indicators of habitat quality due to their rapid biological cycles, ecological specificity, and their easy evaluation at any time of year (Brown, 1991; Freitas, et al., 2003; Montero, et al., 2009).
The list of Colombian butterflies has undescribed areas of our country and the department of Bolívar is one such areas. The information on species is scarce and its Northern area is thought to house between one to 20 species (REF: Colombian Butterfly Database), whereas peripheral areas remain poorly explored (Andrade-C., 2002).
This study provides a species list of diurnal butterflies from El Carmen de Bolívar, in Montes de María sub-region including new findings for the Colombian Caribbean region. Our results offer basic scientific information for future studies, as the taxonomic listings are not only used for describing the biodiversity but also contribute to the conservation, monitoring, and improvement of the national biodiversity inventory and the elaboration of management plans for natural areas (Mielke, et al., 2008; Núñez, 2009).
Material and methods
Study area. Our study was conducted in Saltones de Mesa (9° 47' 34.23" N 75° 18' 5.58" W) and Camarón (9° 50' 32.32" N 75° 17' 36.53" W), in the jurisdiction of Santo Domingo de Mesa, El Carmen de Bolívar municipality (Figure 1), located in the Northeast of Montes de María, an undulating area with altitudes ranging from 50 to 989 m above sea level (Plataforma de Organizaciones de Desarrollo Europeas en Colombia - PODEC, 2011) and temperatures between 27 and 30 °C exhibiting both a semi-dry and slightly humid climate with a unimodal and bi-seasonal rainfall distribution regime (annual average: 174 mm) (Rangel-Ch. & Carvajal-Cogollo, 2012).
The vegetation in the studied areas consists in a mixture of fragments of semi-humid transitional dry forest (as classified by Etter, et al., 2008) in a good state of conservation, areas intervened by deforestation, shrub vegetation, small crops (such as corn, yucca, yam and avocado), and gardens of floral plants such as Asteraceae.
Fieldwork and laboratory. Specimens were collected using entomological nets between 8:00 and 16:00 hours from July 1 to 5, 2015, December 1 to 7, 2016, and May 21 to 27, 2017 with an effort of 152 hours-man in Santo Domingo de Mesa (Figure 1). The butterflies were sacrificed by digital pressure on the thorax and then stored in triangular paper envelopes; later, they were hydrated in a humid chamber and prepared for mounting. All these procedures were carried out according to the collection, preservation, and mounting protocol proposed by Andrade-C., et al. (2013). Specimens were identified using the keys provided by Le Crom, et al. (2004) and the illustrated list of American Butterflies by Warren, et al. (2017). The names of the species were updated and contrasted using the Neotropical Atlas of Lamas (2004). The identification of some species was confirmed with the Entomology Reference Collection of the Instituto de Ciencias Naturales of the National University of Colombia (ICN). The specimens were collected with permission granted through resolution 0751 of June 27, 2014, by the Corporación Autónoma Regional del Canal del Dique (CARDIQUE) and then stored in the research laboratories of the Biology program at Cartagena University (CUDC-INS).
The butterflies were photographed with a Nikon Coolpix compact camera and the pictures were edited with Adobe Photoshop® CS6 software.
Results
We found 67 species distributed in six families, 16 subfamilies, 31 tribes, and 57 genera (Table 1, figures 2-29). The richest family was Nymphalidae with 34 species followed by Pieridae with 12, whereas Lycaenidae was the least representative with three species, followed by Papilionidae and Riodinidae with four species. The most representative genera were Eurema and Phoebis with four and three species, respectively (Table 1).
TAXA | P/A | Distribution in the | Source | ||||
---|---|---|---|---|---|---|---|
Family | Subfamily | Tribe | Specie | Loc 1 | Loc 2 | Colombian Caribbean | |
*Battus polydamas (Linnaeus, 1758) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, Magdalena, Sucre, Bolívar | 1,3,4,8,9,11,12 | |||
Papilionidae | Papilioninae | Troidini | Parides iphidamas (Fabricius, 1793) | 1 | 1 | Atlántico, Cesar, Sucre | 3,7,11,14 |
Parides anchises serapis (Boisduval, 1836) | 0 | 1 | Atlántico, Córdoba, Cesar (including Serranía del Perijá), Sucre | 1,3,5,7,8,9,11,13 | |||
Papilionini | *Heraclides thoas nealces (Rothschild & Jordan, 1906) | 1 | 0 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, Magdalena | 3,4,5,6,8,9 | ||
*Anteos maerula (Fabricius, 1775) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, La Guajira | 1,5,7,8,9,10 | |||
Eurema agave (Cramer, 1775) | 1 | 1 | Cesar (including Serranía del Perijá), Córdoba | 5,8,9 | |||
Eurema albula (Cramer, 1775) | 1 | 0 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, Magdalena | 1,2,4,5,6,7,9 | |||
*Eurema daira (Godart, 1819) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, Sucre, San Andres | 1,2,3,5,6,9,11,13 | |||
Coliadinae | Phoebis agarithe (Boisduval, 1836) | 0 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba | 1,2,8,9 | ||
*Phoebis philea (Linnaeus, 1763) | 0 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba | 1,2,5,7,8,9 | |||
Pieridae | Phoebis sennae (Linnaeus, 1758) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, San Andrés and Providencia, La Guajira, Magdalena, Bolívar | 1,2,3,4,5,8,9,10,12,13 | ||
*Pyrisitia proterpia (Fabricius, 1775) | 1 | 1 | Atlántico, Cesar, Córdoba, Bolívar | 1,2,5,7,9,12 | |||
Pyrisitia venusta venusta (Boisduval, 1836) | 0 | 1 | Cesar (including Serranía del Perijá) | 7,9 | |||
Ascia monuste (Linnaeus, 1764) | 0 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, La Guajira, Magdalena, Sucre, Bolívar | 1,2,3,4,5,8,9,10,11,12 | |||
Pierinae | Pierini | *Itaballia demophile calydonia (Boisduval, 1836) | 0 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, Magdalena, Sucre | 1,2,3,4,7,8,9,11 | |
Glutophrissa drusilla (Cramer, 1777) | 0 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, Sucre | 1,5,8,9,11 | |||
Arawacus lincoides (Draudt, 1917) | 1 | 1 | Cesar | 7 | |||
Lycaenidae | Theclinae | Eumaeini | Pseudolycaena marsyas (Linnaeus, 1758) | 1 | 0 | Atlántico, Cesar, Córdoba | 1,5,7,9 |
Polyonmatinae | Hemiargus hanno (Stoll, 1790) | 0 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba | 1,5,7,8,9 | ||
Eurybiini | Eurybia lycisca Westwood, 1851 | 1 | 0 | Bolívar | 15 | ||
Riodinidae | Riodininae | Helicopini | *Emesis fatimella (Westwood, 1851) | 0 | 1 | Bolívar | 15 |
Nymphidiini | Aricoris erostratus (Westwood, 1851) | 0 | 1 | Atlántico, Cesar | 1,9 | ||
Nymphidium onaeum Hewitson, 1869 | 0 | 1 | Serranía del Perijá, Córdoba | 1,9 | |||
Danaini | Danaus plexippus (Linnaeus, 1758) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, San Andrés and Providencia | 1,5,8,9,13 | ||
Danainae | Danaus gilippus (Cramer, 1775) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, La Guajira, Magdalena | 1,4,5,7,8,9,10 | ||
Ithomiini | *Mechanitis polymnia Linnaeus, 1758 | 1 | 1 | Córdoba, Serranía del Perijá | 5,8,14 | ||
Pteronymia aletta (Hewitson, [1855]) | 0 | 1 | 13 | ||||
Agraulis vanillae vanillae (Linnaeus, 1758) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, San Andrés, La Guajira | 1,5,7,8,9,10,13 | |||
Nymphalidae | Heliconiini | *Dryas iulia (Fabricius, 1775) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, San Andrés and Providencia, Magdalena, Sucre | 1,2,5,7,8,9,11,13 | |
Heliconiinae | Eueides isabella (Stoll, 1781) | 1 | 1 | Cesar (including Serranía del Perijá) | 7,8 | ||
*Heliconius erato hydara (Hewitson, 1867) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, La Guajira, Sucre | 1,2,5,3,6,7,8,9,10,11 | |||
Argynnini | *Euptoieta hegesia (Cramer, 1779) | 1 | 1 | Atlántico, Cesar (including Serranía del Perijá), Córdoba, La Guajira, Magdalena | 1,4,5,7,8,9,10 | ||
Limenitidinae | Limenitidini | *Adelpha cytherea daguana (Fruhstorfer, 1913) | 1 | 0 | Serranía del Perijá | 9 | |
*Biblis hyperia (Cramer, 1779) | Atlántico, Cesar (including | ||||||
Biblidini | 0 | 1 | Serranía del Perijá), Córdoba | 1,5,6,7,8,9 | |||
Ectima thecla | 0 | 1 | Serranía del Perijá | 8 | |||
(Fabricius, 1796) | |||||||
*Hamadryas | Atlántico, Cesar (including Serranía del Perijá) | ||||||
Ageroniini | amphinome | 1 | 0 | 1,2,7,8,9 | |||
(Linnaeus, 1767) | |||||||
Hamadryas feronia (Linnaeus, 1758) | Cesar (including Serranía | ||||||
Biblidinae | 1 | 0 | del Perijá), Córdoba, La | 5,8,9,10,11,14 | |||
Guajira, Sucre | |||||||
Epiphelini | *Nicaflavilla | 1 | 1 | Atlántico, Cesar, Córdoba, | 1,2,3,5,7,11 | ||
(Godart, [1824]) | Sucre | ||||||
*Haematera pyrame | 1 | 0 | Atlántico | 1 | |||
(Hübner, [1819]) | |||||||
Callicorini | Atlántico, Cesar (including | ||||||
*Callicore pitheas | 1 | 0 | Serranía del Perijá), | 1,2,4,5,6,7,8,9,11 | |||
(Latreille, [1813]) | Magdalena, Córdoba, Sucre | ||||||
Atlántico, Cesar (including | |||||||
Coeini | Historis odius dious | 1 | 0 | Serranía del Perijá), | 2,3,4,5,7,8,9,13 | ||
Lamas, 1995 | Córdoba, San Andrés and Providencia, Magdalena | ||||||
*Colobura dirce | Atlántico, Cesar (including | ||||||
Nymphalini | dirce (Linnaeus, | 1 | 1 | Serranía del Perijá), | 2,5,7,8,9,11 | ||
Nymphalidae | 1758) | Córdoba, Sucre | |||||
*Anartia amathea (Linnaeus, 1758) | Atlántico, Cesar (including | ||||||
1 | 1 | Serranía del Perijá), | 3,4,5,8,9 | ||||
Córdoba, Magdalena | |||||||
Atlántico, Cesar (including | |||||||
Anartia jatrophae (Linnaeus, 1763) | Serranía del Perijá), | ||||||
Victorinini | 0 | 1 | Córdoba, San Andrés and | 1,3,5,8,9,10,12,13 | |||
Providencia, La Guajira, Bolívar | |||||||
Nymphalinae | Atlántico, Cesar (including | ||||||
*Siproeta stelenes | 1 | 0 | Serranía del Perijá), | 1,3,5,7,8,9, 11,13 | |||
(Linnaeus, 1758) | Córdoba, Sucre, San Andrés | ||||||
Atlántico, Cesar (including | |||||||
Junoniini | Junonia evarete (Cramer, 1979) | 1 | 1 | Serranía del Perijá), Córdoba, La Guajira, Magdalena, Bolívar | 1,3,4,5,7,8,9,10,12 | ||
Anthanassa drusilla | Cesar (including Serranía | ||||||
(C. Felder y R. | 1 | 1 | del Perijá), Córdoba, | 4,5,7,8,9 | |||
Felder, 1861) | Magdalena | ||||||
Melitaeini | Atlántico, Cesar (including | ||||||
Chlosyne lacinia | 1 | 0 | Serranía del Perijá), | 1,3,4,5,7,8,9,11 | |||
(Geyer, 1837) | Córdoba, Magdalena, Sucre | ||||||
*Fountainea ryphea | |||||||
Charaxinae | Anaeini | ryphea (Cramer, 1775) | 0 | 1 | Serranía del Perijá | 8,13 | |
*Morpho helenor peleides Kollar, 1850 | Cesar (including Serranía | ||||||
Morphini | 0 | 1 | del Perijá), Córdoba, | 4,5,7,8,9,14 | |||
Magdalena | |||||||
Brassolini | Caligo brasiliensis | 1 | 1 | Sucre | 11,14 | ||
(von Felder,1862) | |||||||
Haeterini | *Pierella luna luna | 1 | 0 | Cesar (including Serranía | 5,8,9,14 | ||
(Fabricius 1793) | del Perijá), Córdoba | ||||||
Cissiapompilia (C. | Cesar (including Serranía del Perijá), Córdoba | ||||||
Felder & R. Felder, | 1 | 1 | 5,7,8,9 | ||||
1867) | |||||||
Nymphalidae | Satyrinae | *Hermeuptychia hermes (Fabricius, | 0 | 1 | Cesar (including Serranía del Perijá), Córdoba, Sucre | 5,7,8,9,11,14 | |
1775) | |||||||
Magneuptychia | Cesar (including Serranía del Perijá), Córdoba | ||||||
Satyrini | libye (Linnaeus, | 5,7,8,9 | |||||
1767) | |||||||
Pareuptychia ocirrhoe (Fabricius, 1776) | 1 | 1 | Cesar (including Serranía | 5,8,9 | |||
del Perijá), Córdoba | |||||||
*Taygetis laches | Atlántico, Cesar (including | ||||||
laches (Fabricius, | 1 | 0 | Serranía del Perijá), | 1,5,7,8,9,10,11,14 | |||
1793) | Córdoba, La Guajira, Sucre | ||||||
Typhedanus | Atlántico, Córdoba, Cesar | ||||||
undulatus (Hewitson, | 0 | 1 | (including Serranía del | 1,5,8,9 | |||
1867) | Perijá) | ||||||
Eudamminae | Eudamini | *Urbanus simplicius | 1 | Cesar (including Serranía | 5,8,9,14 | ||
(Stoll, 1790) | del Perijá), Córdoba | ||||||
Urbanus teleus | 1 | 15 | |||||
(Hübner, 1821) | |||||||
Carcharodini | *Nisoniades sp. | 0 | |||||
Hesperiinae | Hesperiini | *Hylephila phyleus | 1 | Atlántico, Cesar, | 1,7,13,14 | ||
(Drury, 1773) | Providencia | ||||||
Hesperiidae | Timochares | ||||||
Erynnini | trifasciata (Hewitson, 1868) | 0 | Atlántico, Cesar | 1,7,9 | |||
Heliopetes arsalte | 1 | Cesar (including Serranía | 5,7,8 | ||||
del Perijá), Córdoba | |||||||
Pyrginae | Polyctor sp. | 1 | |||||
Pyrgus orcus (Stoll, | 1 | Cesar (including Serranía | 5,7,8,9 | ||||
1780) | del Perijá), Córdoba | ||||||
Timochreon satyrus | Cesar (including Serranía del Perijá), Córdoba | ||||||
(C. Felder & R. | 0 | 1 | 5,6,7,8 | ||||
Felder, 1867) |
P/A: Presence/Absence, Loc 1: Saltones de Mesa, Loc 2: Camarón. The column "Source" lists the publications made in the Colombian Caribbean recording the presence of species of diurnal butterflies in the departments of Atlántico: 1 = Montero, et al. (2009), 2 = Boom-Urueta, et al. (2013), 3 = Prince-Chacón, et al. (2011); Magdalena: 4 = Vargas-Zapata, et al. (2011); Córdoba: 5 = Campos-Salazar, et al. (2011); Cesar: 6 = Pulido-B. & Andrade-C. (2007), 7 = Erazo & González-Montaña (2008), 8 = Pulido-B. & Andrade-C. (2009), 9 = Campos-Salazar & Andrade-C. (2009); La Guajira: 10 = Moreno-M. & Acuña-Vargas (2015); Sucre: 11= Mercado-Gómez, et al. (2018); Bolivar: 12= Ahumada-C. (2017); San Andrés and Providencia Islands: 13 = Emmel (1975); and records for the Caribbian region without specific location: 14 = Andrade-C. (2002). Additionally, number fifteen (15) was used to indicate the new records for the Colombian Caribbean. The asterisk (*) refers to the species shown in figures 2-29.
The following are the geographical distributions of the species registered for the first time in the Colombian Caribbean:
Family Riodinidae
Eurybia lycisca Westwood, 1851
Examined material (Annexed, https://www.raccefyn.co/index.php/raccefyn/article/view/808/2551): 1c?. COLOMBIA, Bolivar, El Carmen de Bolivar, Santo Domingo de Mesa, Saltones de Mesa, 9° 47' 34.23" N 75° 18' 5.58" W, 110 m, entomological net, 1-7 xii. 2016, H. Vides Leg. CUDC-INS-654.
Distribution: From the southeast of México to Ecuador (Warren, et al., 2017). In Colombia, this species has been recorded in the Andean regions of Quindío and Antioquia departments (Orozco, et al., 2009, Marín-Gómez, et al., 2011) and in the Pacific region of Nariño and Chocó departments (Palacios & Constantino, 2006, Vargas-Ch. & Salazar, 2014).
Emesis fatimella (Westwood, 1851)
Examined material (Annexed, https://www.raccefyn.co/index.php/raccefyn/article/view/808/2551): 1cC. COLOMBIA, Bolivar, El Carmen de Bolivar, Santo Domingo de Mesa, Camarón, 9°50'32.32"N 75°17'36.53"W, 91 m, entomological net, 1-5. vii. 2015, A. Sandoval, A. Segovia-Paccini, G. Ríos, D. Ahumada-C. and D. Rodríguez Leg.CUDC-INS 772 (Figure 8).
Distribution: From México to Colombia, Guianas and Trinidad (Warren, et al., 2017). In Colombia, this species has been recorded in the Pacific region of Chocó department (Vargas-Ch. & Salazar, 2014) and in the Amazon region (Andrade-C., et al., 2015) in Vaupés Department (Rodríguez & Miller, 2013).
Family Hesperiidae
Urbanus teleus (Hübner, 1821)
Examined material (Annexed, https://www.raccef.yn.co/index.php/raccefyn/article/view/808/2551): 1cC, 1?. COLOMBIA, Bolivar, El Carmen de Bolivar, Santo Domingo de Mesa, Camarón, 9°50'32.32"N 75°17'36.53"W, 91 m, entomological net, 1-5. vii. 2015, A. Sandoval, A. Segovia-Paccini, G. Ríos, D. Ahumada-C. and D. Rodríguez Leg. CUDC-INS 1038, 1039.
Distribution: from Texas in the USA to Argentina (Valencia, et al., 2005, Warren, et al., 2017). In Colombia, it has been registered for the Andean region (González & Andrade-C., 2008) in the departments of Tolima (Camero, et al., 2007), Cundinamarca (Suárez, 2014), Antioquia (Orozco, et al., 2009), Caldas (Ríos-Málaver, 2007) and Santander (Quintero, et al., 2014). In the Pacific region, it has been registered for Valle del Cauca department (Zambrano-González & Ortiz-Ordóñez, 2009, Ascuntar-Osnas, et al., 2010, Gaviria-Ortiz & Henao-Bañol, 2011), and in the Orinoquia region, in the Casanare department (Urbano, et al., 2014).
Discussion
Six families of Neotropical butterflies were found in Santo Domingo de Mesa coinciding with observations by Emmel (1975), Pulido-B. & Andrade-C. (2007, 2009), Campos & Andrade-C. (2009), Montero, et al. (2009), Campos-Salazar, et al. (2011), Prince-Chacón, et al. (2011), Vargas-Zapata, et al. (2011), Boom-Uruetea, et al. (2013), and Moreno-M. & Acuña-Vargas (2015) in tropical dry forest fragments in the Caribbean region.
In this study, we registered 67 species, 12 more than those recorded by Mercado-Gómez, et al. (2018) for the Serranía de la Coraza, Montes de María, Sucre. As expected in the Neotropics (Brown, 1996, Marín-Gómez, et al., 2011), the Nymphalidae was the family with the most subfamilies and species. Nymphalidae has been found to be associated with the dry forests of Montes de María, in Sucre department (Mercado-Gómez, et al., 2018), and in all the Caribbean plain (Campos-Salazar & Andrade-C., 2009; Campos-Salazar, et al., 2011, Montero, et al., 2009, Prince-Chacón, et al., 2011 Moreno-M. & Acuña-Vargas, 2015) including the Sierra Nevada of Santa Marta (Vargas-Zapata, et al., 2011). The Pieridae family was the second family with the highest number of species coinciding with the study by Campos-Salazar, et al. (2011) in Córdoba department and Vargas-Zapata, et al. (2011) in Magdalena department.
Papilionidae had a low richness, which coincides with the findings by Montero, et al. (2009) and Prince-Chacón, et al. (2011) for Atlántico department, and so did Riodinidae, which coincided with the results obtained for the departments of Sucre (Montes de María) by Mercado-Gómez, et al. (2018), Córdoba by Campos-Salazar, et al. (2011), Atlántico by Boom-Urueta, et al. (2013), and Magdalena by Vargas-Zapata, et al. (2011). The Lycaenidae family also registered a low richness, which differs from studies conducted in the Neotropics where it is considered one of the most diverse families (Brown, 1996, Marín-Gómez, et al., 2011).
Conclusions and recommendations
This is the first study on diurnal butterflies in Montes de María, Bolívar. We provide a preliminary list of species confirming the presence of three species for the Colombian Caribbean. Throughout history, the Montes de María subregion has been characterized by its difficult access but this has improved greatly since the post-conflict, thus opening the possibility of giving the first steps to investigate the insects in the area and highlighting the need of greater scientific explorations to establish the richness of this region, one of the most biodiverse areas of the Colombian Caribbean, which has been subjected to processes of agricultural and livestock transformation.