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Corresponding author: Wesley O. de Sousa ( entomoi@hotmail.com ) Academic editor: Gabriel L. F. Mejdalani
© 2019 Wesley O. de Sousa, Lincey E. Sousa, Fátima R.J. da Silva, Wildio I. da Graça Santos, Rodrigo Aranda.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
de Sousa WO, Sousa LE, da Silva FRJ, da Graça Santos WI, Aranda R (2019) Composition and structure of the frugivorous butterfly community (Lepidoptera: Nymphalidae) at the Serra Azul State Park (PESA), Mato Grosso, Brazil. Zoologia 36: 1-10. https://doi.org/10.3897/zoologia.36.e27708
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Due to the important ecological role of Nymphalidae as consumers of fermented fruits, excrement, exudates of decomposed plants and animals, as well as bioindicators of environmental quality that attract the interest of the general public, this study aimed to characterize the fauna of frugivorous butterflies at the Serra Azul State Park – PESA (Mato Grosso, Brazil) with regards to composition, taxonomic richness and spatial distribution. Collections were carried out in 2014 from six 250 m plots in a RAPELD module (5x5 km). We defined five sampling points in each plot and placed a Van Someren-Rydon trap (VSR), with a bait made from banana fermented in cane juice, positioned 1 m above the ground for 24 hours. We collected 204 specimens of Nymphalidae from five subfamilies, 22 genera, and 40 species. Satyrinae was the most abundant and species-rich subfamily. The community structure varied spatially, with the gallery forest presenting the greatest richness, diversity, and equitability, while ‘cerrado ralo’ presented higher abundance and less diversity and equitability. Therefore, according to the pattern of abundance in the PESA, species were best adapted to the log series model. Yphthimoides renata (Stoll, 1780) (Satyrinae), Hamadryas feronia (Linnaeus, 1758), and Callicore sorana (Godart, 1824) (Biblidinae) were the most abundant species, 19 species were singletons, and eight were doubletons. Richness estimators showed that 63% of all species were sampled. Our results indicate that the frugivorous butterfly community is structured according to phytophysiognomies, and the dominance of species that are tolerant to disturbances indicates landscape fragmentation within the PESA, which interferes with species substitution pattern and their abundances in different environments of the park.
Cerrado, conservation, inventory, Nymphalidae, Phytophysiognomy
Research about conservation monitoring and planning is most effective when supported by prior knowledge about the distribution of organisms and patterns of occurrence within an area. Such information is collected through biodiversity inventories, which provide important information for restoration, composition maintenance, and structure and function of biological communities (
Arthropods are useful ecological indicators due to their great diversity and abundance, ease of collection, and rapid responses to environmental changes (
Furthermore, frugivorous Nymphalidae butterflies stand out in environmental monitoring and evaluation studies due to their biological and ecological characteristics, since they depend on specific micro-habitats and adequate resources to survive (
Using frugivorous butterflies in ecological studies has methodological and sampling advantages, since simple traps, which are easily made and maintained, are used in field collections (
The state of Mato Grosso is potentially highly biodiverse because three of the main Brazilian biomes are present within its borders: Amazon tropical rainforest, Cerrado, and Pantanal. However, the frugivorous butterfly fauna in Brazil is still poorly contemplated in most inventories (
Furthermore, the ecological importance and status of frugivorous butterflies as bioindicators were so far poorly considered in studies carried out in the region (
In this context, this study aims to increase knowledge and fuel the discussion about the importance of services provided by Serra Azul State Park (PESA) in preservation and public use by maintaining the ecological functions and high biological diversity of the Cerrado. In addition, there is a lack of knowledge about the Cerrado biodiversity, which highlights the importance of understanding the biology and taxonomy of terrestrial invertebrates, especially for groups of poorly studied arthropods, helping future studies that aim to select criteria and biological models for conservation of this biome. Herein, we (1) inventoried the frugivorous butterfly fauna at PESA, (2) described the ecological metrics of the communities, and (3) analyzed the community composition in relation to the phytophysiognomies in the study area.
The study area is located in the Serra Azul State Park (PESA) in the municipality of Barra do Garças, eastern region of the state of Mato Grosso (15°51’S, 51°16’W), with an area of approximately 11,000 ha and an altitude between 350 m and 750 m above sea level (
Geographic coordinates and phytophysiognomies of the plots in the RAPELD module installed in the Serra Azul State Park (PESA), Barra do Garças, Mato Grosso, Brazil.
| Plots | Coordinates | Phytophysiognomy |
| 1 | 15°50’58,7”S; 52°15’47”W | Cerrado sensu stricto |
| 3 | 15°50’22,2”S; 52°14’49”W | Gallery forest |
| 5 | 15°49’42,5”S; 52°13’49”W | Cerrado ralo – open savanna |
| 6 | 15°51’07,6”S; 52°14’49”W | Deciduous forest |
| 8 | 15°50’33,5”S; 52°13’56”W | Cerrado sensu stricto |
| 10 | 15°49’53,8”S; 52°13’05”W | Cerrado ralo – open savanna |
The PESA plots were characterized according to their vegetation type (phytophysiognomy) following the protocol from the Research Program on Biodiversity (PPBio) with standardized adaptations by the ComCerrado Network. Of our six plots, four presented Cerrado phytophysiognomies, Cerrado sensu stricto, and ‘cerrado ralo’ (open savannah with sparse trees), with different tree densities (356 to 1,463 individuals (∆) Ha-1). The other two plots were characterized as gallery forest (684 ∆ Ha-1) and deciduous forest (586 ∆ Ha-1) (Table
For the collections, we defined five sampling points (100 m2) in each plot spaced 50 m apart from each other. At each sampling point we installed a Van Someren-Rydon (VSR) trap (
All specimens were individually wrapped in silk paper envelopes, labeled, and mounted on a wooden stretcher with entomological pins. Specimens were then dried in an oven at 40°C for three days, labeled, and deposited at the Entomological Reference Collection of the Departmento de Biologia, Universidade Federal de Mato Grosso, Campus Universitário de Rondonópolis (DBFR). Identifications were made based on specific literature (
We calculated the absolute richness and relative frequency of each species in each phytophysiognomy. To describe the community of frugivorous butterflies in the sampled areas, we used the diversity indices of Shannon-Wiener (H’), Pielou equitability (J), and Chao species richness estimator, as well as a rarefaction curve. Shannon-Wiener index was compared using t-test. The pattern of species abundance was tested in relation to the four predictive models (broken-stick, log normal, log series, and geometric). To verify if species composition differed with the phytophysiognomies, we performed a non-metrical dimensional scaling (NMDS – Bray Curtis similarity index). Similarity percentage (SIMPER) was used to assess which taxa were most responsible for the similarity between samples. Seriation test was used to order the species in the localities, presuming the faunal gradient for reorganizing the data matrix when the presences of the species are concentrated along the diagonal gradient, with the ‘Monte Carlo’ simulation. All analyses were performed in the Past® program and Sigmaplot® was used for graphic construction.
We obtained a total of 204 individuals of Nymphalidae, distributed in five subfamilies, 22 genera, and 40 species. Satyrinae presented the highest abundance, number of genera, and number of species, and Biblidinae presented the second largest abundance. The most dominant species were Yphthimoides renata (Stoll, 1780) (N = 77, 37.75%), Hamadryas feronia (Linnaeus, 1758) (N = 30, 14.71%), and Callicore sorana (Godart, 1824) (N = 10, 4.9%) (Table
Abundance (N) and relative frequency (%) of the subfamilies and species of Nymphalidae sampled from the four phytophysiognomies in the Serra Azul State Park (PESA), Barra do Garças, Mato Grosso, Brazil.
| Nymphalidae | Cerrado sensu stricto | Gallery forest | Deciduous forest | Cerrado ralo | Total | |||||||||
| (N) | (%) | (N) | (%) | (N) | (%) | (N) | (%) | (N) | (%) | |||||
| Biblidinae | 33 | 16.17 | 4 | 1.96 | 2 | 0.98 | 13 | 6.37 | 52 | 25.49 | ||||
| Callicore sorana (Godart, 1824) | 8 | 3.92 | 0 | 0.00 | 2 | 0.98 | 0 | 0.00 | 10 | 4.90 | ||||
| Catonephele acontius (Linnaeus, 1771) | 1 | 0.49 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 2 | 0.98 | ||||
| Hamadryas amphinome (Linnaeus,1767) | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 1 | 0.49 | ||||
| Hamadryas februa (Hubner, 1823) | 3 | 1.47 | 0 | 0.00 | 0 | 0.00 | 2 | 0.98 | 5 | 2.45 | ||||
| Hamadryas feronia (Linnaeus, 1758) | 21 | 10.29 | 0 | 0.00 | 0 | 0.00 | 9 | 4.41 | 30 | 14.71 | ||||
| Nica flavilla (Godart, 1824) | 0 | 0.00 | 3 | 1.47 | 0 | 0.00 | 0 | 0.00 | 3 | 1.47 | ||||
| Temenis laothoe (Cramer, 1777) | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 1 | 0.49 | ||||
| Charaxinae | 5 | 2.45 | 6 | 2.94 | 2 | 0.98 | 2 | 0.98 | 15 | 7.35 | ||||
| Archaeoprepona demophon (Linnaeus, 1758) | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Archaeoprepona sp. | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Archeoprepona amphimachus (Fabricius, 1775) | 0 | 0.00 | 1 | 0.49 | 1 | 0.49 | 0 | 0.00 | 2 | 0.98 | ||||
| Memphis moruus (Fabricius, 1775) | 1 | 0.49 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 2 | 0.98 | ||||
| Prepona laertes (Hübner, 1811) | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 1 | 0.49 | 2 | 0.98 | ||||
| Prepona pheridamas (Cramer, 1777) | 0 | 0.00 | 1 | 0.49 | 1 | 0.49 | 0 | 0.00 | 2 | 0.98 | ||||
| Siderone galanthis (Cramer, 1775) | 4 | 1.96 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 5 | 2.45 | ||||
| Heliconiinae | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Heliconiinae sp. | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Nymphalinae | 0 | 0.00 | 2 | 0.98 | 0 | 0.00 | 0 | 0.00 | 2 | 0.98 | ||||
| Colobura dirce (Linnaeus, 1758) | 0 | 0.00 | 2 | 0.98 | 0 | 0.00 | 0 | 0.00 | 2 | 0.98 | ||||
| Satyrinae | 23 | 11.27 | 17 | 8.33 | 17 | 8.33 | 77 | 37.75 | 134 | 65.68 | ||||
| Amphidecta calliomma (Felder &Felder, 1862) | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 1 | 0.49 | ||||
| Amphidecta reynoldsi (Sharpe, 1890) | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 1 | 0.49 | ||||
| Caligo brasiliensis (Felder 1862) | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Chloreuptychia arnaca (Fabricius, 1776) | 0 | 0.00 | 3 | 1.47 | 0 | 0.00 | 0 | 0.00 | 3 | 1.47 | ||||
| Cissia myncea (Cramer, 1780) | 0 | 0.00 | 4 | 1.96 | 2 | 0.98 | 1 | 0.49 | 7 | 3.43 | ||||
| Cissia sp. | 0 | 0.00 | 2 | 0.98 | 0 | 0.00 | 0 | 0.00 | 2 | 0.98 | ||||
| Hermeuptychia hermes (Fabricius, 1775) | 3 | 1.47 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 4 | 1.96 | ||||
| Morpho helenor achillides Felder & Felder 1867 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Opsiphanes invirae (Hübner, 1808) | 4 | 1.96 | 0 | 0.00 | 0 | 0.00 | 2 | 0.98 | 6 | 2.94 | ||||
| Paryphthimoides undulata (Butler, 1867) | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Posttaygetis penelea (Cramer, 1777) | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 1 | 0.49 | ||||
| Satyrini sp. 1 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Satyrini sp. 2 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Satyrini sp. 3 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 1 | 0.49 | ||||
| Taygetina oreba (Butler, 1870) | 0 | 0.00 | 0 | 0.00 | 2 | 0.98 | 2 | 0.98 | 4 | 1.96 | ||||
| Taygetis acuta Wetmer, 1910 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 1 | 0.49 | 2 | 0.98 | ||||
| Taygetis cleopatra Felder & Felder, 1867 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Taygetis mermeria (Cremer, 1776) | 0 | 0.00 | 0 | 0.00 | 4 | 1.96 | 1 | 0.49 | 5 | 2.45 | ||||
| Taygetis rufomarginata Staudinger, 1888 | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Taygetis sp. | 0 | 0.00 | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | ||||
| Taygetis virgilia (Cramer, 1776) | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 1 | 0.49 | ||||
| Yphthimoides pacta (Weymer, 1911) | 1 | 0.49 | 0 | 0.00 | 0 | 0.00 | 6 | 2.94 | 7 | 3.43 | ||||
| Yphthimoides renata (Stoll, 1780) | 12 | 5.88 | 1 | 0.49 | 5 | 2.45 | 59 | 28.92 | 77 | 37.75 | ||||
| Yphthimoides sp. | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 1 | 0.49 | 1 | 0.49 | ||||
| Total | 61 | 30.00 | 30 | 15.00 | 21 | 10.00 | 92 | 45.00 | 204 | 100.00 | ||||
The species abundance pattern was best fit to the log series model (alpha = 14.9, χ2 = 111, p < 0.001; Broken stick: χ2 = 185.4, p =0.003; Geometric: χ2 = 541.8, p =0.009; log-normal distribution: χ2 = 2.25, p =0.32) (Fig.
Ecological metrics of Nymphalidae in phytophysiognomies of the Serra Azul State Park (PESA), Barra do Garças, Mato Grosso, Brazil. Richness (S), Abundance (N), Shannon index (H’), Pielou equitability (J), and species richness estimator (Chao-2). Shannon diversity t test index (H’) comparison among phytophysiognomies. Blank cell: t-test result. Bold: p values.
| Phytophysiognomies | S | N | H’ | J | Chao-2 |
| Cerrado sensu stricto | 12 | 61 | 1.945 | 0.7826 | 22 |
| Cerrado ralo | 16 | 91 | 1.469 | 0.5299 | 27 |
| Deciduous forest | 11 | 22 | 2.199 | 0.9171 | 15 |
| Gallery forest | 21 | 30 | 2.904 | 0.9539 | 61 |
| Shannon diversity t | t/p | CR | C | GF | DF |
| CR | – | 0.29 | 0.250 | 0.18 | |
| C | 1.06 | – | 0.03* | 0.77 | |
| GF | -1.16 | 2.19 | – | 0.02* | |
| DF | 1.35 | -0.29 | 2.47 | – |
Individual and cumulative contribution of species to the similarity of Nymphalidae community composition in the Serra Azul State Park (PESA), Barra do Garças, Mato Grosso, Brazil.
| Species | Contribution (%) | |
| Individual | Cumulative | |
| Yphthimoides renata | 28.94 | 28.94 |
| Hamadryas feronia | 14.17 | 43.11 |
| Callicore sorana | 5.99 | 49.10 |
| Cissia myncea | 5.21 | 54.31 |
| Taygetis mermeria | 3.40 | 57.71 |
| Chloreuptychia arnaca | 3.04 | 60.75 |
| Opsiphanes invirae | 2.87 | 63.62 |
| Yphthimoides pacta | 2.64 | 66.26 |
| Siderone galanthis | 2.46 | 68.72 |
| Taygetina oreba | 2.24 | 70.96 |
| Hermeuptychia hermes | 2.08 | 73.04 |
| Hamadryas februa | 1.82 | 74.86 |
| Archeoprepona amphimachus | 1.72 | 76.58 |
| Prepona pheridamas | 1.69 | 78.28 |
| Cissia sp. | 1.57 | 79.85 |
| Catonephele acontius | 1.51 | 81.36 |
Regarding richness and abundance, the most dominant subfamilies of frugivorous butterflies in the PESA were Satyrinae and Biblidinae. Furthermore, these taxa showed higher abundance and species richness in other studies from the Neotropical region (
The diversity of Satyrinae is related to its biology. They have diurnal habits, feed on fruits in different stages of decomposition and with fungi, have low dispersal capacity, fly near the ground, and prefer shaded areas. They are dominant members of the butterfly communities in different Neotropical (
The complexity of interspecific or biotic interactions is considered the main reason for diversity in tropical environments, and the intimate relationships between butterflies and their host plants could help clarify the origin of butterfly megadiversity in the tropics (
Our results indicate that the association of Satyrinae with monocotyledons may explain the higher abundance and dominance of certain species in the Cerrado areas, as the cerrado ralo, which is typically more open and has more monocotyledons as compared to forested areas. This was observed for Yphthimoides Forst, 1964, as Y. renata was the most abundant of the three species of Yphthimoides recorded in PESA. Yphthimoides is a Neotropical genus associated with Poaceae (
The abundance of Biblidinae, explained by the dominance of H. feronia in the Cerrado sensu stricto, also reinforces the previous hypothesis since this species is associated with anthropogenically impacted areas (e.g.,
In this way, the log-series distribution found may be indicative of the disturbed environment in the PESA, which has a large amount of grasses, due to the region’s fire history. The two most abundant species in the frugivorous butterfly community were the ones considered tolerant to anthropogenic effects, which contributed to the abundance model and to the low diversity and equitability indexes registered for the Cerrado physiognomies of the PESA. In this sense, both Y. renata and H. feronia can be considered indicators of disturbances and/or landscape fragmentation within the PESA, as observed by
The occurrence of species with low abundance and the 27 rare species recorded in the PESA can be considered high when compared to inventories carried out in the areas with marginal influences of savannah, Chaco, and Pantanal (e.g.,
The observed richness was well below the estimated richness for the frugivorous butterfly community distributed in the PESA, demonstrating that other species could still be collected with a larger sampling effort. When compared to other studies developed in the Cerrado (
While it is difficult to compare richness and diversity of frugivorous butterflies from different studies due to the peculiarities of each study, especially regarding differences in collection methods, sample effort and size, and disturbed and undisturbed areas (
Our results demonstrate that the community of frugivorous butterflies at the PESA is spatially structured, with the highest richness, diversity, and equitability in the gallery forest. However, the second largest richness and lower diversity and equitability were found in the cerrado ralo. Cerrado sensu stricto and deciduous forest showed similar ecological metrics. Such pattern may be related to periodic disturbances, such as the frequency and intensity of fires (e.g.,
In this study, we found a significantly higher number of species in the forest with higher frequency of burning (
The frugivorous butterfly community in the cerrado ralo and gallery forest indicates that these phytophysiognomies are subsets of the butterfly communities in the deciduous forest, since, in terms of composition and dominance, they share the same species. Furthermore, authors such as
Our results confirm that frugivorous butterfly guilds are promising biological models for developing future environmental monitoring studies, and that patterns of species richness, abundance, and distribution can be used to make conservation and management decisions in the PESA and other areas. The spatial and temporal monitoring of the butterflies can be used in the selection of species for indicating the degree of degradation of the habitat.
This initial inventory can serve as a starting point for long-term monitoring of the PESA butterfly community, which could provide data to support decisions about area management. In addition, our data highlights the need for more studies in areas that have not yet been inventoried. Finally, as more species are recorded and/or discovered, information is increased and can be used for Neotropical biodiversity conservation.
We thank the Rede ComCerrado, the SISBIOTA Project, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq process 563134/2010-0) and the PPBIO Project (CNPq process 457497/2012-2) for financial support. We thank also all teams linked to PPBio – Rede ComCerrado of the Federal University of Mato Grosso, Campus do Araguaia, who contributed directly and indirectly to the logistic support, collections, and/or mounting of the butterflies. We also thank Amabílio José A. de Camargo (EMBRAPA Cerrado, Brasília, DF) for identifying the frugivorous butterflies.