Long term survey of the butterfly fauna of Curitiba, Paraná, Brazil: How does a scientific collection gather local biodiversity information? (Lepidoptera: Papilionoidea)
Muestreo general, a largo plazo, de la fauna de mariposas de Curitiba, Paraná, Brasil: ¿Cómo se recoge la información de biodiversidad de una colección científica local? (Lepidoptera: Papilionoidea)
Long term survey of the butterfly fauna of Curitiba, Paraná, Brazil: How does a scientific collection gather local biodiversity information? (Lepidoptera: Papilionoidea)
SHILAP Revista de lepidopterología, vol. 45, no. 179, pp. 433-446, 2017
Sociedad Hispano-Luso-Americana de Lepidopterología
This work is licensed under Creative Commons Attribution 4.0 International.
Received: 23/09/2016
Accepted: 05/02/2017
Published: 30/09/2017
Funding
Funding source: CNP
Award recipient: Long term survey of the butterfly fauna of Curitiba, Paraná, Brazil: How does a scientific collection gather local biodiversity information? (Lepidoptera: Papilionoidea)
Abstract: Butterfly species lists are commonly published aiming to describe local or regional diversity, thus being primordial tools for subsiding nature preservation and management. However, tropical lands usually lack this kind of information. Inventories of megadiverse organisms, such as butterflies, usually require long term studies to detect a substantial fraction of species present in certain location. Through biological collections in scientific institutions it is possible to preserve a considerate amount of biodiversity information, which is not available in the literature, but can promote studies over time. Aiming at supplementing the knowledge on butterfly diversity in Curitiba, Paraná, Brazil, and to demonstrate how a scientific collection accumulates such information from the nearby surroundings, this study lists all species of butterflies recorded in the city since 1938. Since then, 554 species were recorded. Although there have been large sampling efforts since the 60s, 45 species were only recorded in the last decade. Species lists published in 1938, 1995, 2011 and 2015 contributed to a considerable fraction of species records and monitoring, but species richness observed in each study is usually low (less than 1/3 of all historical records). Therefore, the long term deposition of specimens gathered in a single collection evidences that Curitiba harbors a distinct higher number of species, though new records are still frequent. Taking into account that long term surveys of megadiverse insects offer a more complete analysis of their biological diversity, studies measuring diversity impacts, such as urban sprawl, must include historical data whenever available.
Keywords: Lepidoptera, Papilionoidea, conservation, species richness, urban ecosystems, Atlantic Forest, Brazil.
Resumen: Los listados de mariposas se publican normalmente aspirando a describir la diversidad local o regional, siendo, por tanto, herramientas primordiales para subvencionar la conservación y su gestión. Los inventarios de organismos mega o superdiversos, como las mariposas, requieren habitualmente estudios a largo plazo para detectar una fracción significativa de las especies presentes en una localidad. Sin embargo, las regiones tropicales carecen, generalmente, de esta clase de información. A través de colecciones biológicas en las instituciones científicas es posible mantener una considerable información de biodiversidad, que no se dispone en la literatura, pero puede promover estudios con el tiempo. Teniendo como objetivo complementar los conocimientos sobre la diversidad de mariposa en Curitiba, Paraná, Brasil y demostrar cómo una colección científica acumula tal información de los entornos cercanos desde entonces, este estudio recoge una lista, todas las especies de mariposas registradas en la ciudad desde 1938, desde entonces, se han registrado 554. Aunque ha habido grandes esfuerzos de muestreos desde el los 60, 45 especies sólo fueron registradas en la última década. Las listas de especies se publicadas en 1938, 1995, 2011 y 2015 han aportando los registros de una fracción considerable de especies, pero la riqueza de especies observadas en cada estudio resulta usualmente baja (menos de 1/3 de todos los archivos históricos). Por lo tanto, el depósito a largo plazo de los especímenes en una sola colección, muestra claramente que Curitiba da refugio a un mayor número de especies, donde los nuevos registros todavía son frecuentes. Teniendo en cuenta que los muestreos a largo plazo de insectos megadiversos ofrecen un análisis más completo de su diversidad biológica, aquellos estudios que midan los impactos sobre la diversidad, como por ejemplo la aglomeración urbana, deben incluir los datos históricos disponibles.
Palabras clave: Lepidoptera, Papilionoidea, conservación, riqueza de especies, ecosistema urbano, Bosque Atlántico, Brasil.
Introduction
Butterflies are recognized as the most common invertebrates used as bioindicators, given their sensitive to landscape changes from different types of anthropic disturbances (WOOD & GILLMAN, 1998; KITCHING et al., 2000; BROWN & FREITAS, 2000; SUMMERVILLE & CRIST, 2001; UEHARA-PRADO& RIBEIRO, 2012), besides being easy to sample and to identify (DEVRIES et al., 1997; KITCHING et al., 2000). Therefore, there are several studies listing butterfly species aiming to quantify local or regional diversity (BROWN, 1991; KREMEN et al., 1993; KREMEN, 1994). On the other hand, basic information of butterfly diversity, distribution, and population dynamics are still scarce in tropical region (BROWN & FREITAS, 1999; UEHARA-PRADO et al., 2004; SANTOS et al., 2008).
Thus, considering that butterfly diversity surveys can support several aspects of conservation manegement (BROWN & FREITAS, 1999; DOLIBAINA et al., 2011), two main sources are of particular interes: published inventories, and biological collections. In this context, biological collections stands out because data can be used to evaluate space and time changes (FATTORINI, 2013), besides holding voucher material as demanded by the scientific method. Brazilian entomological collections are among the most significant from South America, in terms of Neotropical representatives, with a wide number of collections all over the country, products of different projects and expeditions done during several decades. In terms of Lepidoptera, the Museu Nacional and Instituto Oswaldo Cruz (Rio de Janeiro), Museu de Zoologia de São Paulo (São Paulo) and the Departamento de Zoologia, Universidade Federal do Paraná (Paraná), hold the largest collections from the Neotropical fauna (MARINONI, 2010).
The orgin of specimens deposited in these collections is of course biased by locations within the Brazilian territory and by sites easily accessible to collectors (MARINONI, 2010). Butterfly species lists in Brazil, for example, are more common closer to the biggest metropoles and research centers (SANTOS et al., 2008). These sites may regard most records from butterfly diversity in Brazil, but still historical studies on how this information accumulates trough time are scarce. Curitiba is an example of a city where some butterfly species lists were produced (BIEZANKO, 1938; MIELKE, 1995; BONFANTTI, et al., 2011; PEREIRA et al., 2015), most of them depositing vouchers in a single collection located in the city. However, no study has investigated and compared historical variations in butterfly records gathered in species lists and random collects. This study’s main objective was to rank butterfly species, based on records from Brazilian biological collections, and demonstrate, through this study model, how scientific collections accumulate and preserve biodiversity knowledge, especially on the megadiverse groups.
Material and Methods
STUDY AREA
Curitiba (25º 25’ 40”S, 49º 16’ 23”W), Paraná, Brazil, has 432.7 km2 and is at approximately 930 m of altitude. The city is located in a Cfb type region, with a humid mesothermal climate, without a dry season, with cool summers, and winters with frequent frost and occasional snowfall (IPPUC, 2012). Average annual temperature is of 16.4 C and rainfall of 1600 mm/year. Nowaday, the landscape of Curitiba is predominatly urbanized, but the original vegetation was characterized by fragments of mixed ombrophilous forest, isolated by a matrix of grassland. Currently, the city still presents some green areas (HILDEBRAND, 2001), but the matrix is urbanized. Its current vegetation cover is estimated in 129945000 m2 (around 5% of its territory), composed of 22 parks, 454 public squares, 55 lakes, and four private reserves (VIEIRA & BIONDI, 2008; IPPUC, 2012; GRISE et al., 2016).
DATA COLLECTION
A data matrix was built from the specimens deposited in the Coleção Entomológica Padre Jesus Santiago Moure, Departamento de Zoologia (DZUP), Universidade Federal do Paraná (UFPR), the private collection of Olaf H. H. Mielke, Curitiba, Paraná, compared to the names listed in previous survey data (BIEZANKO, 1938; MIELKE, 1995; BONFANTTI et al., 2011; PEREIRA et al., 2015). The specimens were identified through comparisons with specimens previously identified in the DZUP collection, through the use of specialized literature, or were identified / confirmed by specialists. Taxonomical nomenclature for Papilionoidea follows LAMAS (2004) and for Hesperioiidea follows O. MIELKE (2005). Records of all surveyed species are deposited in the DZUP.
Results and discussion
According to data obtained from surveys done in Curitiba and in the DZUP, there are 554 species recorded in the city, belonging to six families, 25 subfamilies, and 320 genera (Table I). The family with highest species richness was Hesperiidae 237 ssp. (42.8%), followed by Nymphalidae 161 ssp. (29%), Lycaenidae 68 ssp. (12.27%), Riodinidae 44 ssp. (7.94%), Pieridae 32 ssp. (5.78%) and Papilionidae 12 spp. (2.17%) (Figure 1).
Figure 1
Number of species records per decade during 50 sampling years in Curitiba, Paraná, Brazil.
BIEZANKO (1938) presented the first list with 24 species of butterflies and, after approximately five decades without updates, MIELKE (1995) published a new list with 498 species, using the same collection to gather butterfly records, but adding additional municipalities on Curitiba surroundings. From those, 446 species were confirmed to occur within Curitiba limits. Since than, recent studies on different urban parks of Curitiba, from 2010 and onward (BONFANTTI et al., 2011; PEREIRA et al., 2015), ocassionally added more records (Figure 2).
Figure 2
Historical records of Lepidoptera species based on the entomological collection (DZUP) and species lists from Curitiba, Paraná, Brazil.
The number of species represents 17.1 % of the butterfly richness that is estimated to occur in Brazil. It is more than what was recorded in other city surveys in Paraná (e.g. Jaguariaíva, 226 spp., Diamante do Norte, 379 spp., Foz do Iguaçú, 106 spp. (Hesperiidae), Maringá, 106 spp., Balsa Nova, 432 spp and Palmito-Paranagua, 200 spp. (MIELKE, 1968; ALMEIDA et al., 1986; CASAGRANDE et al., 2012; BELTRAMI et al., 2014; GARCIA-SALIK et al., 2014; LEVISKI et al., 2016). However, studies with similar sampling efforts, and additional data from collections, presented species number closer or superior to the ones recorded for Curitiba (DOLIBAINA et al., 2011; MIELKE et al., 2012). These differences in the number of species are obviouly related to sampling effort and number of localities sampled in these municipalities (DOLIBAINA et al., 2011; RITTER et al., 2011; BOGIANI et al., 2012; BELLAVER et al., 2012). Furthermore, we should emphizize that such differences might also be influenced by the presence of a nearby scientific collection. Besides the use of specimens deposited in local collections, the surveys available for Curitiba, Guarapuava and Ponta Grossa count with the active participation of collectors such as Hipólito Schneider and Felipe Justus, who founded the first Lepidoptera collections of the state (DOLIBAINA et al., 2011; MIELKE et al., 2012). As demonstrated by FATTORINI (2013), the sampling effort of amateurs often surpasses those of scientists in biological collections of renowned historical importance, contributing as an important legacy to local collections, biodiversity and science awareness.
The lepidopterofauna of Curitiba was sampled with different efforts since 1938, as expected for any museum data. There are several factors that contribute to maximize or minimize specimen deposition during certain periods. The 90s, as an example, was especially important for the publication of species lists for Curitiba and neighbouring cities (MIELKE, 1995), as mentioned before. Until then, there was only BIEZANKO (1938) list (24 spp.) as a published reference. Besides the available information from a long historical period, new records are constantly deposited, reflecting the complexity of sampling high diverse groups, such as butterflies.
From September / 2015 until March / 2016, 45 new records for Curitiba were added: Hesperiidae (17), Lycaenidae (13), Nymphalidae (11) and Riodinidae (4) (Table I). Families such as Hesperiidae and Nymphalidae are commonly reported as the most representative in Neotropical surveys (BROWN & FREITAS, 2000; SANTOS et al., 2008), although the percentual number of species for each family depends on the sampling effort employed (ISERHARD et al., 2013). In short surveys, with low sampling effort or systematic collectings, Nymphalidae usually exhibits the highest number of recorded species (MARCHIORI & ROMANOWSKI, 2006; DESSUY & MORAIS, 2007; LEMES et al., 2008; PAZ et al., 2008; PEREIRA et al., 2015). Nevertheless, long term record additions are expected to show a disproportional increase in the number of species of Hesperiidae (FRANCINI et al., 2011; ISERHARD et al., 2013; THIELE et al., 2014), which is currently corroborated by the high number of recent records for the family, even after four decades of sampling efforts. Thus, the high number of Hesperiidae species recorded in a survey can be considered a good indicator of the total butterfly species richness in a region (MIELKE et al., 2008). Similarly, Riodinidae and Lycaenidae species numbers also tend to increase disproportionally to Nymphalidae although their richness is expected to be lower in temperate regions (BROWN & FREITAS, 2000; UEHARA-PRADO et al., 2007; SANTOS et al., 2008; SIEWERT et al., 2014).
One of the great advantages of exploring historical data is the possibility of monitoring the presence/absence of species over time. Some of these species are particularly important to conservation strategies, such as the endangered and endemic Pampasatyrus glaucope (C. Felder & R. Felder, 1867). This species has disappeared from the Curitiba records after 47 years (DZ 24.474, DZUP), even though it was relatively common in grassland habitats within the city (pers. obs.). Currently, the urban matrix replaced all grasslands habitats previously present in Curitiba. Additionaly, Cyanophrys bertha (Jones, 1912) and Symmachia arion (C. Felder & R. Felder, 1865) were also included in red lists of threatened fauna but, for different reasons. These species are represented only by sparse records in the national scientific collections. Thus, their disappearance from the collection records might be an artefact of the difficulty of detecting them in nature.
Therefore, the continuous development of butterfly species lists is of extreme relevance to planning conservation strategies in diferente kind of habitats. In highly degraded areas, such as urbans places, the addition of historical records permits current species distribution to be more precicely determined as a fator of antropogenic disturbance. Thus, conservation practices could also be applied based on local assemblage trends and its habitats preferences (BROWN & FREITAS, 1999, 2000; SUMMERVILLE & CRIST, 2001). We expect that the presente species list to influence future ecological and conservation studies in Curitiba, besides contributing to circusncribing the original distribution of the Neotropical Lepidoptera.
Acknowledgments
To colleagues Msc. Thamara Zacca (Satyrinae), Msc. Gabriela Leviski (Pieridae), Dr. Fernando Dias (Charaxinae and Limenitidinae), Dr. Diego Rodrigo Dolibaina (Lycaenidae and Riodinidae) for the critical review and aid metrial sampling and identification. To the funding agency CNP for the study / research scholarships.
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Apéndice
Author notes