Artículos

Butterflies diversity from a remnant of semiurban Caatinga, Septentrional Sertaneja Depression Ecoregion, Patos, Paraíba, Brazil (Lepidoptera: Papilionoidea)

Diversidad de mariposas de un remanente de Caatinga semiurbana, Ecorregión de la Depresión Sertaneja Septentrional, Patos, Paraíba, Brasil (Lepidoptera: Papilionoidea)

A. Ferreira-Júnior 1
Universidade Federal de Campina Grande, Brasil

Butterflies diversity from a remnant of semiurban Caatinga, Septentrional Sertaneja Depression Ecoregion, Patos, Paraíba, Brazil (Lepidoptera: Papilionoidea)

SHILAP Revista de lepidopterología, vol. 49, núm. 194, pp. 327-349, 2021

Sociedad Hispano-Luso-Americana de Lepidopterología

Received: 09 December 2019

Accepted: 08 October 2020

Published: 30 June 2021

Abstract: In order to perform a concise characterization and evaluation of the butterflies taxocenosis structure of the Rural Health and Technology Center (CSTR) of the Federal University of Campina Grande (UFCG), a semiurban area of the Caatinga biome, Semiarid region, in the Septentrional Sertaneja Depression Ecoregion, a species inventory with entomological net was conducted. There were recorded 81 species of butterflies, distributed in a general abundance of 2531 individuals; among them, 808 specimens were captured and collected, and none of the individuals marked with nontoxic pen and released were recaptured. The list of species was complemented by adding nine more butterflies species, mostly Hesperiidae, from collection before and after the sampling period, constituting a total of 90 species. Many of the butterflies species found in the CSTR are new records for Paraíba state and only four species are considered for the Northeast geographic region, based on other checklists for areas of Atlantic Forest, Caatinga, Cerrado and Amazon biomes in this region: Junonia genoveva infuscata Felder & Felder, 1867, Staphylus melangon epicaste Mabille, 1903, Clitosompa Evans, 1953 and Lerema ancillaris (Butler, 1877).

Keywords: Lepidoptera, Papilionoidea, species list, urban ecology, semiarid, seasonally dry tropical forest, Brazil.

Resumen: Para caracterizar y evaluar rápidamente la estructura de taxocenosis de mariposas del Centro de Salud y Tecnología Rural (CSTR) de la Universidad Federal de Campina Grande (UFCG), un área semiurbana del bioma Caatinga, región Semiárida, Ecorregión de Depresión Sertaneja Norteña, fue realizado un inventario de especies con red entomológica. Fueron registradas 81 especies de mariposas, distribuidas en una abundancia general de 2.531 individuos; de estos, 808 especímenes fueron capturados y colectados, ninguno de los individuos marcados con pluma no tóxica y liberados fueron recapturados. La lista de especies se complementó agregando nueve especies de mariposas más, principalmente Hesperiidae, de las recopilaciones antes y después del período de muestreo, lo que ha constituido un total de 90 especies. Muchas de las especies de mariposas encontradas en el CSTR son nuevos registros para el estado de Paraíba y solo cuatro especies se mencionan como nuevos registros para la región geográfica Noreste, basado en otros inventarios para las áreas de los biomas Bosque Atlántico, Caatinga, Cerrado y Amazonas de esta región: Junonia genoveva infuscata Felder & Felder, 1867, Staphylus melangon epicaste Mabille, 1903, Clito sompa Evans, 1953 y Lerema ancillaris (Butler, 1877).

Palabras clave: Lepidoptera, Papilionoidea, lista de especies, ecología urbana, semiárido, bosque tropical estacionalmente seco, Brasil.

Introduction

Brazil is cited as one of the main megadiverse countries, housing a significant number of terrestrial invertebrates (LEWINSOHN & PRADO, 2005). However, knowledge of the diversity of this group, especially butterflies, is still incipient and unequally distributed among the political (geoeconomic) and biogeographic divisions, with evident negligence for the Northeastern Semiarid region (LEWINSOHN et al., 2005; CARNEIRO et al., 2008; FREITAS & MARINI-FILHO, 2011; SANTOS et al., 2011). Thus, it is required to acquire knowledge of biodiversity for its contribution and development of multiple conservation approaches, mitigation strategies and compensation of the various environmental impacts, given the growing pace of imbalance of natural ecosystems, habitat loss, extinction of species and the devastating effects of the global warming (WILSON, 1997; CHAPIN et al., 2000; BONEBRAKE et al., 2010; WARREN et al., 2013; GARCÍAROBLEDO et al., 2016; MELLO etal., 2016).

The term diversity, commonly used in works focusing on Community Ecology and Conservation Biology, represents the variety of living beings and may include information on richness and equitativity, this last expressing the relative importance of each species through abundance in sampling (MELO, 2008). Information about the diversity of butterflies in a given habitat, even those considered urban or with varied anthropogenic disturbance, can contribute to their conservation and understanding landscape connectivity, quali-quantitative monitoring and as a starting point for detecting spatial or temporal environmental changes, in addition to supporting biogeographic studies and specific patterns (HARDING et al., 1995; BROWN-JUNIOR & FREITAS, 1999; SOGA & KOIKE, 2012).

Specifically, the species richness (A, B, C, D, E or 1, 2, 3, 4, 5) does not express the number of individuals, a function of the abundance (A, A, A, A, A or 1, 1, 1, 1, 1, or yet A1, A2, A3, A4, A5, ... AN, or eventually for the composition A1, B1, B2, B3, B4, C1, C2, C3, D1, D2, E1, structure of distinct qualities with equal or different quantities of individuals), and consist of key metrics in the various fields of research in Ecology that generally underestimate the counts in samples of different characteristics (homogeneous and heterogeneous), with two large structural groups of statistical tests, parametric and non-parametric models, and two approaches to infer species richness based on data measures (computational simulations), incidence (absence 0 or ≥ 1 presence), numbers of uniques (1 sample) and duplicates (2 samples), and abundance (0 or ≥ 1), numbers of singletons (1 individual) and doubletons (2 individuals), - as expressed by KHALIGHIFAR et al. (2020), with more details, depending of the disposition and conformation, the data of binary incidence, 0 or 1, cannot be permuted into abundance finite data, however, the contrary transformation is possible - asymptotic and non-asymptotic approaches, that can be compared to the multiple assemblies (convergents/divergents, similars/dissimilars) and arrive at a theoretical (speculative) and experimental relationship of the appropriate real number of the richness (statistical approximation theory) in certain environments with possible undetected species, hypotheses that can be proven indispensably through the standardized application of collection protocols (sample integrity) and the sampling effort, once again highlighting the support to the understanding of the arbitrators to the causes of biodiversity phenomena and the consequences of unsustainable human exploration for making decisions based on a well-founded environmental policy (CHAO & CHIU, 2016a; 2016b; CHAO & COLWELL, 2017).

Considering the ontological and ontogenetic mutability of the linguistic sign “species”, this word can express multiplicity of significant (among the various idioms and languages of the human species) and significances (concept) according to the dialectical contextual insertion in the systems (analogy, minor valence relationship, and homology, major valence relationship, of Aristotelian origin applied over time), introduced and felt between enunciator (emitter) and enunciatory (receptor) through of the channels of enunciation of the enunciated (D’SAUSSURE, 2012). Species can be defined in the stricto sensu as a biological taxonomic category that includes its taxa by the unified concept of species, - genophenotypic (intrinsically) and/or phenogenotypic (extrinsically) living beings/organisms - segments of metapopulational lineages evolving separately, possible common denominator, through secondary and primary contingent properties used as operational criteria of the point of cut and circumscription of the lines of speciative evidence, with the metamorphosis occurring at the level of anagenesis and the speciation in the dimension of cladogenesis, analyzed by the robustness of integrated methods (emphasize for the phylogenetic-cladistic with your inferences) by genetic scrutineers (coalescence theory), phylogeographic, morphological, physiological and behavioral, among other aspects of the evolutionary biological taxonomic systematic (organization of knowledge), conducted and legislated by associations and commissions with yours consolidated international nomenclature codes, botanical (IAPT, 1950; TURLAND et al., 2018) and zoological (ICZN, 1895; ICZN, 1999), in addition to international committees and codes for the nomination of prokaryotes (ICSP, 2020; PARKER et al., 2019) and viruses (ICTV, 2018; ICTV, 2019); aditional groups with their supra and infracategorical epithets, inter and intraspecific interactions, evolutionarily involved throughout natural history through the various types of speciation with potential gene introgressions, parallel speciation and hybridizations in the flow of genetic pools (e.g., ecotypes zones with semipermeable reproductive barriers and occurrence of at least two sympatric subspecies of the same species of butterfly that do not evolve completely apart), followed by heuristic, syntactic-semantic, nomenclatural-terminological conflicts (controversies), subject to the reviews and adequations submitted to the scientific community consensus or dissent (see MAYDEN, 1997; D’QUEIROZ, 2007; ALEIXO, 2007; HAUSDORF, 2011; NAOMI, 2011; BRABY et al., 2012 for more details of the heated debate about delimitation and conceptualization parameters of species and subspecies).

While the identity of the “species” can be applied to objects and subjects, living and nonliving beings, memes, money banknotes, agents, patients, epidemiological cases (medical science), bugs in software programs (computer science and information technologies), characters that make up the atomicity of numbers and letters in different languages in the websites, books and physicaldigital-virtual articles (Literature), genes or alleles of the genetic code and other discrete, elementary and substantial entities, contents within of categorical continents of the monistic hierarchical organization, not only of biological sciences, trans-interdisciplinary topics in the spectrum of conceptual applications and discussions of information theory (CHAO & CHIU, 2016a; 2016b); including not only the pertinent contemporary philosophical-anthropologicalsociological reflections (considering other perspectives, see DANOWSKI & D’CASTRO, 2014), that together with Biology representatives (Zoology, Ecology, etc.) try to restructure and balance the coexistence of desires among beings for a more reasonable, tolerable, peaceful and just world during the probable most prominent viral pandemic of the 21st century, probably caused by the random events, misfortunes of the consequence by the human hyper-impaction on wild biodiversity, through the unpredictable strains of high mutagenic power transversely the species of the new coronavirus (SIDDELL et al., 2020) of Chiroptera origin (ZHOU et al., 2020), etiological agent Sars-Cov-2 (CSG/ICTV, 2020) that infects millions of individuals of the human species expressing ample deadly power pathogenic by the Covid-19 disease (ICTV, 2019).

Various environmental factors, biotic and abiotic, can influence relatively on the distribution and structure of neotropical butterfly communities, such as different latitude and altitude gradients, topographic, floristic and microhabitat heterogeneity, seasonality, microclimatic conditions and varying degrees of fragmentation and vegetative disturbance, thus the assemblies may have different composition, richness and abundance (BROWN-JUNIOR, 1991; BROWN-JUNIOR & FREITAS, 2000a, b; BROWN-JUNIOR & FREITAS, 2002).

Specifically, the effects of urbanization gradient and other anthropogenic disturbances in natural ecosystems, associated on butterfly assemblages, can lead to forest fragmentation, modification of habitats and species composition, through the emergence of exotic or cultivated species and the loss of native species, with consequent decrease in diversity (BROWN, 1989; RUSZCZYK & SILVA, 1997; HARDY & DENNIS, 1999; NEW & SANDS, 2002; FAHRIG, 2003; MCKINNEY, 2008). So, the presence or absence and population density of a particular species may serve as bioindicators of the conservation level and quality of the environmental landscapes, as they are insects characteristic of this assessment and susceptible to such impacts (FREITAS et al., 2003; FREITAS et al., 2006; OLIVEIRA et al., 2018).

In contrast, urban environments, with green areas that maintain considerable vegetation and favorable weather conditions, even provide shelter and resources for the establishment and survival of adults and butterfly larvae, also becoming refuge for birds, reptiles and other insects, highlighting the importance of these remnants for the study and conservation of the biodiversity (RUSZCZYK, 1986a, 1986b, 1986c, 1986d; MURPHY, 1997; BROWN-JUNIOR & FREITAS, 2002; KOH & SODHI, 2004; COLLIER et al., 2006; CLARK et al., 2007). From this perspective, there is a tendency in the reduction of butterfly dispersion and diversity in relation to the increased degree of urbanization and alteration, where less impacted semiurban and peripheral areas present greater richness compared to more altered central urban green areas, with few exceptions (RUSZCZYK & ARAÚJO, 1992; FORTUNATO & RUSZCZYK, 1997; RUSZCZYK, 1998; HARDY & DENNIS, 1999; NEW & SANDS, 2002; HOGSDEN & HUTCHINSON, 2004; OLIVEIRA et al., 2018; TZORTZAKAKIA et al., 2019).

Most of the Brazilian works developed with butterflies in fragments of urban and semiurban vegetation are described for areas of plazas, cemeteries, university campuses, municipal parks and other conservation units for the Atlantic Forest (sensu lato), involving the listing of species through active and/or passive collection, and various ecological analysis, with greater representativeness for the Southern (RUSZCZYK, 1986a, b, c, d, e; RUSZCZYK, 1987; RUSZCZYK & ARAUJO, 1992; LEMES et al., 2008; SACKIS & MORAIS, 2008; BONFANTTI et al., 2009; BONFANTTI et al., 2011; LEMES et al., 2015; FAVRETTO et al., 2015; PEREIRA et al., 2015) and Southeast regions (RODRIGUES et al., 1993; FORTUNATO & RUSZCZYK, 1997; RUSZCZYK & SILVA, 1997; VANINI et al., 1999; BROWN-JUNIOR & FREITAS, 2002; SILVA et al., 2007; PEREIRA et al., 2011; SILVA et al., 2012; SOARES et al., 2012). Few inventories can be cited for Midwest region (PINHEIRO et al., 2008; BOGIANI et al., 2012), Northern region (GARCIA et al., 1990; GARCIA & BERGMANN, 1994) and Northeast region, described for Cerrado and Amazon (MARTINS et al., 2017; PEREIRA et al., 2018), Atlantic Forest (KESSELRING & EBERT, 1982; VASCONCELOS et al., 2009; OLIVEIRA et al., 2018; MELO et al., 2019) and Caatinga urban areas (COSTA et al., 2013; ROQUE et al., 2014), where very few butterfly studies are known for the urban locations of the Semiarid region, demonstrating the importance of this survey work.

The present study was developed to contribute to the knowledge and conservation of the butterflies fauna of the Semiarid region of Northeastern Brazil through the elaboration of a species list and characterization of alpha diversity in an area of semiurban xerophytic caatinga located in the town of Patos, state of Paraíba. It is noteworthy that the area covered by the municipality is considered of extreme biological importance for the invertebrate group and priority for knowledge and conservation of the Caatinga biome biodiversity (MMA/SBF, 2002; SILVA et al., 2003).

Material and methods

Study area

The Health and Rural Technology Center (CSTR) of the Federal University of Campina Grande (UFCG) is located on the outskirts of the urban area of Patos town, Paraíba state (07º03’32” S e 37º16’29” W), it has an average altitude of 250 meters, rocky outcrops and an approximate area of 220 m2 , inserted in the Caatinga biome, Semiarid region, Septentrional Sertaneja Depression Ecoregion (VELLOSO et al., 2002). The regional climate is semiarid, BSh, according to the classification of Köppen, marked by a dry and a rainy season (ÁLVARES et al., 2014). The annual average temperature is around 25ºC, while the relative humidity 65,9% and the rainfall has an annual average of inferior 1000 mm (SOUSA et al., 2019), being irregularly distributed between the months of the year. It is in a high degree of anthropization, with much of the total area occupied by constructions. However, it has an area that concentrates a relatively considerable vegetation, where is inserted a forest vivarium with seedlings, next to one of the largest and oldest water reservoir of the municipality, Jatobá weir; besides extensions with ruderal vegetation spots, especially during the rainy season, and shrub-tree caatinga, which undergo periodic weeding and pruning. Both places provide food and oviposition substrates to butterflies, where native angiosperm species of different habits are present, mostly represented by families Fabaceae, Anacardiaceae, Bignoniaceae, Euphorbiaceae and Myrtaceae (SOUSA et al., 2019), Convolvulaceae, Malvaceae, Rubiaceae, Apocynaceae, Asteraceae, in addition to exotic and native ornamental species of others families located in regularly irrigated flower beds.

Sampling

The butterflies were captured with the aid of an entomological net, identified in the field when possible, marked with a nontoxic pen and released or collected. Visual counts were also performed of individuals of species with population explosions, once per transect and without net capture, mostly some species of Pieridae and Nymphalidae. At the time of the catch the transect was recorded. Registries were made in ruderal open areas, shrub and tree vegetation spots, within three transects proportional to the campus length and explored from February 2011 to December 2011 (10 months), except October, one day per month, from 08 am to 04 pm, alternately, 2:40 hours per transect, totaling a sampling effort of 80 hours/net/collector with one more auxiliary for spreadsheet annotations and marking of the entomological envelopes. Also, butterfly species that were not captured during the sampling period, but they have records for the study area, were added to complement the richness of the CSTR.

Specimens (vouchers) were deposited in the butterfly Collection of the Caatinga Insect Ecology and Interactions Laboratory (CLEIIC) of the Federal University of Campina Grande (UFCG), Patos, Paraíba, Brazil.

The systematic follows the one proposed by LAMAS (2004, 2008) and ESPELAND (2018). For the suprageneric categories of Nymphalidae, WAHLBERG et al. (2009), Riodinidae, SERAPHIM et al. (2018) and Hesperiidae, WARREN et al. and LI et al. (2019). Many identifications were obtained through physical (BROWN-JUNIOR, 1992; CANALS, 2003) and digital guides (WARREN et al., 2013), consulting specialists when needed.

Data analysis

Are described richness data, absolute and relative frequencies by abundance of species, subfamilies and families, as well as the presence and absence of species in the rainy and dry seasons of the year. In sequence, to evaluate the collection effort, richness extrapolations (previsions) were performed through the nonparametric estimators that quantify rarities, Bootstrap, Jackknife 1, 2 and Chao 1, 2 (DIAS, 2004), using the software PAST 3.24 (HAMMER et al., 2019), comprising only the information for the 10 months of sampling.

The constancy of the butterfly species was obtained through the relation between the proportion of the samples in which a given species was registered and the total number of samples, through the formula C = p.100/N, being p the number of sampling occasions recorded for each species and N the total of sampling occasions, categorizing the species as constant, present in more than 50% of the collections (6-10 months), accessory, between 25 and 50% (3-5 months), and accidental, in less than 25% of the collections (1-2 months) (BODENHEIMER, 1955; SILVEIRA-NETO et al., 1976); while the dominance was calculated from the relative abundance of each species using the formula D = (i/t).100, being i the total of individuals of a species and t the total of sampled individuals, characterized as eudominant > 10%, dominant > 5-10%, subdominant > 2-5%, recessive = 1-2% and rare < 1% (FRIEBE, 1983).

Simple comparisons of richness and composition were also made with the intention to achieve some similarity with other available inventories for urban green areas in the Pampa, Cerrado and Atlantic Forest biomes (SILVA et al., 2007; SACKIS & MORAIS, 2008; PINHEIRO et al., 2008; BONFANTTI et al., 2009; VASCONCELOS et al., 2009; BONFANTTI et al., 2011; SOARES et al., 2012; BOGIANI et al., 2012; PEREIRA et al., 2015; LEMES et al., 2015; MELO et al., 2019), and with the other inventories developed in the northeastern Semiarid region (NOBRE et al., 2008; PALUCH et al., 2011; ZACCA & BRAVO, 2012; LIMA & ZACCA, 2014; KERPEL et al., 2014; RAFAEL et al., 2017). New records for the Northeast region were obtained from the inventories available in scientific literature (CARDOSO, 1949; KESSELRING & EBERT, 1982; NOBRE et al., 2008; ZACCA et al., 2011; PALUCH et al., 2011; ZACCA & BRAVO, 2012; LIMA & ZACCA, 2014; KERPEL et al., 2014; PALUCH et al., 2016; RAFAEL et al., 2017; MARTINS et al., 2017; PEREIRA et al., 2018; MELO et al., 2019).

Results and Discussion

Eighty-one (81) butterfly species were recorded distributed in 30 species of Hesperiidae (37%), 26 of Nymphalidae (32%), 13 of Pieridae (16%), eight of Lycaenidae (10%), three of Papilionidae (4%) and one species of Riodinidae (1%) (Table I). The list of species was complemented by adding nine more species, mostly Hesperiidae, from anterior and posterior collections to the sampling period, constituting a total of 90 species: Historis acheronta (Fabricius, 1775) (Nymphalidae); Anteos clorinde (Godart, [1824]) (Pieridae); Electrostrymon endymion (Fabricius, 1775), Strymon crambusa (Hewitson, 1874), Pseudolycaena marsyas (Linnaeus, 1758) (Lycaenidae); Aguna megaeles (Mabille, 1888), Staphylus sp., Staphylus melangon epicaste Mabille, 1903, Heliopetes arsalte (Linnaeus, 1758) (Hesperiidae) (Table I).

Table I.
List of butterfly species sampled at the Health and Rural Technology Center (CSTR), Patos, Paraíba, Brazil, between February 2011 and December 2011, except October, and total frequencies. Legend: S = richness, N = abundance, AF = absolute frequency, RF = relative frequency; D = dominance of species, EU = eudominant, DO = dominant, SU = subdominant, RE = recessive, RA = rare; C = species constancy, CON = constant, ACE = accessory, ACI = accidental; RAI = rainy season (Feb-Jun), DRY = dry season (Jul-Dec); species that have been also recorded for at least one of the works described for the biomes and the apostrophe (’) means records of different subspecies or just the same species for the 1 = Caatinga (NOBRE et al., 2008; PALUCH et al., 2011; ZACCA & BRAVO, 2012; LIMA & ZACCA, 2014; KERPEL et al., 2014; RAFAEL et al., 2017), 2 = Atlantic Forest (CARDOSO, 1949; KESSELRING & EBERT, 1982; ZACCA et al., 2011; PALUCH et al., 2016; MELO et al., 2019), 3 = Cerrado (EMERY et al., 2006; PINHEIRO & EMERY, 2006; MARTINS et al., 2017), 4 = Amazon (MIELKE et al., 2010; MARTINS et al., 2017; PEREIRA et al., 2018); * = butterfly species out of sampling and with records for the CSTR; ** = new records for the Northeast region of Brazil.
List of butterfly species sampled at the Health and Rural Technology Center (CSTR), Patos, Paraíba, Brazil, between February 2011 and December 2011, except October, and total frequencies. Legend: S = richness, N = abundance, AF = absolute frequency, RF = relative frequency; D = dominance of species, EU = eudominant, DO = dominant, SU = subdominant, RE = recessive, RA = rare; C = species constancy, CON = constant, ACE = accessory, ACI = accidental; RAI = rainy season (Feb-Jun), DRY = dry season (Jul-Dec); species that have been also recorded for at least one of the works described for the biomes and the apostrophe (’) means records of different subspecies or just the same species for the 1 = Caatinga (NOBRE et al., 2008; PALUCH et al., 2011; ZACCA & BRAVO, 2012; LIMA & ZACCA, 2014; KERPEL et al., 2014; RAFAEL et al., 2017), 2 = Atlantic Forest (CARDOSO, 1949; KESSELRING & EBERT, 1982; ZACCA et al., 2011; PALUCH et al., 2016; MELO et al., 2019), 3 = Cerrado (EMERY et al., 2006; PINHEIRO & EMERY, 2006; MARTINS et al., 2017), 4 = Amazon (MIELKE et al., 2010; MARTINS et al., 2017; PEREIRA et al., 2018); * = butterfly species out of sampling and with records for the CSTR; ** = new records for the Northeast region of Brazil.

Table I.
List of butterfly species sampled at the Health and Rural Technology Center (Cont...)
List of butterfly species sampled at the Health and Rural Technology Center (Cont...)

Table I.
List of butterfly species sampled at the Health and Rural Technology Center (Cont...)
List of butterfly species sampled at the Health and Rural Technology Center (Cont...)

Table I.
List of butterfly species sampled at the Health and Rural Technology Center (Cont...)