Abstract: The diversity of hawkmoths (Lepidoptera: Sphingidae) is poorly known in the biomes of the Bahia state. However, studies were carried out in other states of the northeastern region with species inventories in the Atlantic Forest, Caatinga and Cerrado. In order to bro aden the knowledge on of the richness and diversity of hawkmoths in the Atlantic Forest of the state of Bahia, six monthly sampling sessions were carried out in the State Ecological Station of Wenceslau Guimarães. Hawkmoths were captured using a 250-watt mercury-vapor light trap set against a white cloth panel, for two nights a month, between 6:00 p.m. and 6:00 a.m. A total of 266 specimens were collected, distributed across 17 genera and 41 species. The most abundant and dominant species were Isognathus swainsoni C. Felder, 1862, with a relative abundance of 12.41%, and Xylophanes amadis (Cramer, 1782) and Xylophanes anubus (Cramer, 1777), both with 7.9%. Our study represents the second inventory of hawkmoths for the state, totaling 59 species known for the Atlantic Forest of Bahia. Isognathus excelsior (Boisduval, [1875]) and Manduca lucetius (Cramer, 1780) represented new records for the biome. The accumulated number of species indicates the need for further sampling in order to safely reach the curve asymptote.
Keywords: hawkmoths, neotropical, conservation, richness, Atlantic Forest.
Zoologia
Sphingidae (Lepidoptera: Bombycoidea) assemblage in the State Ecological Station of Wenceslau Guimarães, Bahia, Brazil
Eduarda Mendes Malheiros eduarda_malheiros@hotmail.com
Recepción: 13 Diciembre 2020
Aprobación: 23 Abril 2021
Sphingidae (hawkmoths) is worldwide acknowledged for its important role in pollination, interactions with plants and as bioindicators (Camargo, Camargo, Corrêa, Vilela, & Amorim, 2018). They are found in all continents except for Antarctica and Greenland (D’Abrera, 1986;Kitching & Cadiou, 2000; Hilty & Merenlender, 2000; Darrault & Schlindwein, 2002;Motta & Xavier-Filho, 2005; Duarte, Marconato, Specht, & Casagrande, 2012; Amorim, Wyatt, & Sazima, 2014; Lourido, Motta, Graça, & Rafael, 2018; Conceição & Teston, 2020).
Worldwide, the hawkmoths are a family comprising approximately 1,608 species, distributed across 213 genera, grouped in three subfamilies: Sphinginae, Macroglossinae and Smerinthinae (Camargo et al., 2018). An analysis of their phylogeny based on 5 nuclear genes revealed a strongly supported monophyly of the family, although the position of Smerinthinae sensu lato within the family deserves further investigation, because some of its genera remain incertae sedis (Kawahara, Mignault, Regier, Kitching, & Mitter, 2009).
Approximately 302 species are estimated for South America and among those, 196 occur in Brazil (Haxaire & Mielke, 2019). They are mainly nocturnal, except for some genera, such as Aellopos, Hübner [1819], and Eupyrrhoglossum, Grote 1865, which show diurnal and crepuscular activity (Marinoni, Dutra, & Mielke, 1999; Kitching & Cadiou, 2000).
In northeastern Brazil, the hawkmoths are known chiefly by species inventories, distributed in the biomes Caatinga, Atlantic Forest and Cerrado (Cardoso, 1949; Silva, 1967; Duarte Jr, Motta, & Varela-Freire, 2001; Darrault & Schlindwein, 2002; Gusmão & Creão-Duarte, 2004; Duarte Jr & Schlindwein, 2005a, 2005b, 2008; Lopes, Medeiros, Aguiar-Neto, & Machado, 2005; Primo, Duarte, & Machado, 2013; Mielke & Haxaire, 2013; Rafael et al., 2017; Câmara, Rocha, & Pereira, 2018; Vila-Verde & Paluch, 2019).
Although Sphingidae is considered to be the best-inventoried family among nocturnal moths (Kitching & Cadiou, 2000), very little is known about them in Bahia, a priority state for lepidopterans inventories in the Northeast (Freitas & Marini-Filho, 2011).
This study aimed to contribute to the knowledge of Sphingidae assemblage within a protected area located to the northwest of the central corridor of the Atlantic Forest in the Bahia state, known as Estação Ecológica Estadual de Wenceslau Guimarães (State Ecological Station of Wenceslau Guimarães), in order to improve the understanding of diversity and distribution of hawkmoths in northeastern Brazil.
The State Ecological Station of Wenceslau Guimarães. (SESWG) (13°35’43’’S and 39°43’10’’W) located in the municipality of Wenceslau Guimarães, Bahia is a priority area for conservation in the full protection category (SNUC Law 9985/2000 and Decree 4340/2002). Currently, it comprises a total area of 2,418 ha of protected forests. It was created by the State Decree 6228/1997 and later expanded by the Decree 7791/2000. It is inserted in the Atlantic Forest biome, and it is composed exclusively of the Submontane Ombrophilous Dense Forest phytophysiognomy (Figure 1) (Rigueira et al., 2012).
The region presents a humid and sub-humid climate. Climatology of the municipality, based on 30 years of observation, shows precipitation varying from 103 mm to 153 mm, maximum temperature from 27 to 29ºC and the minimum temperature from 19 to 20ºC, between October and March (Rigueira et al., 2012; Climatempo, 2020).
One sampling event per month consisting of two consecutive nights was carried out from October 2013 to March 2014. We made a total of 12 nights and 144 hours of sampling in two seasons: spring and summer. Sampling was carried out in the waning or new moon phases, between 6:00 p.m. and 6:00 a.m. (12 hours). The sampling period (October-March) was determined based on the fact that the richness and abundance of Sphingidae respond positively to the increase in rainfall after the driest period (Amorim, Ávila Jr, Camargo, Vieira, & Oliveira, 2009; Duarte Jr & Schlindwein, 2005a, 2005b). The pluriannual precipitation of Wenceslau Guimarães shows September (108 mm) and October (103 mm) with the lowest averages of the year, with a increase in November (136 mm), reaching the highest summer average in March (153 mm) (Climatempo, 2020).
We used a light trap consisting of a rectangle of white cotton cloth measuring 1.5x2.0 m, illuminated by a 250 watts mercury vapor mixed light lamp. Hawkmoths were collected manually or using an entomological net. The specimens were then sacrificed by lethal injection composed of ethyl ether 35% (v v-1), through a fine needle ventrally inserted between the thorax and abdomen, and then put in individual entomological envelopes with the specimen information. In the laboratory, the collected specimens were numbered and identified, and their sampling date was entered in a database. The specimens were prepared and deposited in the collection of the Laboratório de Sistemática e Conservação de Insetos, Setor de Ciências Biológicas, Centro de Ciências Agrárias, Ambientais e Biológicas, Universidade Federal do Recôncavo da Bahia, Cruz das Almas, Bahia. Duplicates were deposited in the Embrapa Cerrados entomological collection, Planaltina, Distrito Federal.
Sphingidae nomenclature and classification followed Carcasson and Heppner (1996), Camargo et al. (2018) and Haxaire and Mielke (2019). The species were identified based on information and illustrations obtained in Martin, Soares, and Bizarro (2011), Camargo et al. (2018) and through consultation to the insect Embrapa Cerrados entomological collection, Planaltina, Distrito Federal.
Following Santos, Casagrande, and Mielke (2015), the richness and dominance were chosen to describe and depict the structure of the Sphingidae assemblage that was also qualitatively compared with other areas from Northeast Brazil, using only data from works with species level identification. These areas belong to the states of Maranhão, Ceará, Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, and Bahia. For richness estimates based on abundance, we chose to use Chao1 estimator, which also considers the relationship between the number of singletons (rare species) and doubletons, and the ACE estimator that uses species with ten or less individuals per sample (Lee & Chao, 1994; Ferraz, Gadelha, & Aguiar-Coelho, 2009). We also used the Bootstrap estimator, which is based on species incidence, using data from all collected species (Ferraz et al., 2009). To obtain an estimated species richness, and in order to provide an accumulation curve, we used the statistical software EstimateS version 9.1 (Colwell, 2013).
During the study, 266 specimens (N) were collected, distributed across 17 genera and 41 species (S). The average number of captures per hour was 1.85 individuals (Table 1).
The hawkmoth assemblage consists of the three subfamilies: Macroglossinae, Smerinthinae and Sphinginae. Macroglossinae was represented by two tribes: Dilophonotini, distributed across 20 species of 11 genera, represented 39.5% of the individuals collected (N = 105), and Macroglossini with 10 species of two genera accounted for 29.7% of the individuals collected (N = 79). Smerinthinae was represented by the only tribe that occurs in the Neotropical region, Ambulycini, with four species of two genera that represented 12.8% of the individuals collected (N = 34). Sphinginae was represented by the tribe Sphingini with seven species of two genera, which amounted to 18% of the individuals collected (N = 48) (Table 2).
Comparison of the SESWG species richness with that of published inventories in the northeastern Brazil indicated that SESWG occupies the third place in the ranking, after Balsas (BLS) and Feira Nova of Maranhão (FNM), two localities in the state of Maranhão that added 48 species to the region (Mielke & Haxaire, 2013). The Private Natural Heritage Reserve Frei Caneca (PNHRFC), Jaqueira, Pernambuco, with 50 species (Duarte Jr & Schlindwein, 2008), remains as the locality with the greatest species richness in northeastern Brazil (Table 3).
Among the species recorded in SESWG, seven were the most abundant with a total of ten or more individuals: Isognathus swainsoni Felder & Felder, 1862, Pachylia darceta Druce, 1881, Xylophanes amadis (Stoll, 1782), Xylophanes anubus (Cramer, 1777), Protambulyx strigilis (Linnaeus, 1771), Manduca florestan (Cramer, 1782) and Manduca lucetius (Cramer, 1780). Together they corresponded to 47.4% of the abundance and 17.1% of the richness. Seven species were represented by a single individual (singleton) and four by two individuals (doubletons) accounting for 26.8% of the richness in the SESWG (Table 1). Novotný and Basset (2000) state that these species may appear to be rare in inventories due to inadequate sampling. However, they can also represent transient species or specialists with genuinely low population levels. Among the collected singletons, five species were recorded previously in two or three northeastern biomes. Thus, we might conclude that they are common species widely distributed and that their low abundance in the SESWG was probably affected by the sampling technique (Table 1). Seasonality studies including the four seasons may elucidate the real abundance of these species in the SESWG.
Seven species were collected exclusively in spring (October to December) and 14 only in summer (January to March). Thirteen species (31.7% of the richness and 8.3% of the abundance) occurred in a single month. Nineteen species were recorded in at least three months of sampling, of these ten species contributed with approximately 56% of abundance and 24.4% of richness: Callionima nomius (Walker, 1856) (N = 7; RA = 2.63%), Isognathus leachii (Swainson, 1823) (N = 8; RA = 3%), Isognathus swainsoni (N = 33; RA = 12.41%), Pachylia darceta (N = 10; RA = 3.76%), Xylophanes amadis (N = 21; RA = 7.9%), Xylophanes anubus (N = 21; RA = 7.9%), Xylophanes tersa tersa (Linnaeus, 1771) (N = 8; RA = 3%), Protambulyx strigilis (N = 15; RA = 5.64%), Manduca florestan (N = 14; RA = 5.26%) and Manduca lucetius (N = 12; RA = 4.5%) (Table 1).
Among the hawkmoths of SESWG, Isognathus swainsoni (N = 33), Xylophanes amadis (N = 21), Xylophanes anubus (N = 21) and Manduca florestan (N = 14) scored the highest abundance throughout the sample period. In the spring (October-December) we recorded 29 species of which Isognathus swainsoni (N = 19) and Manduca florestan (N = 10) had the highest dominance. One hundred and fourteen individuals were collected during the season, which corresponds to 43% of the specimens sampled. In summer (January-March) 35 species were found, of which three were dominant: Isognathus swainsoni (N=14), Xylophanes amadis (N = 13), and Xylophanes anubus (N = 13). One hundred and fifty two individuals were collected during the season, representing 57% of the total sampled. However, these species are not frequently recorded in northeastern Brazil. Cardoso (1949) collected Manduca florestan in the Atlantic Forest of Alagoas state; Duarte Jr and Schlindwein (2008) recorded the four species in the PNHRFC, Mielke and Haxaire (2013) collected Xylophanes anubus and Manduca florestan in BLS-FNM and Vila-Verde and Paluch (2019) collected Isognathus swainsoni, Xylophanes anubus in the Campus Sosígenes Costa (CSC), Porto Seguro, Bahia (Table 1 and 3).
Erinnyis ello ello (Linnaeus, 1758), Protambulyx strigilis and Xylophanes tersa tersa are quite common in northeastern Brazil, occurring in the Caatinga, Atlantic Forest and Cerrado biomes (Table 1). Pollination studies found 22 pollen types in mouth parts of Erinnyis ello ello and ten types in Xylophanes tersa tersa, which shows that these subspecies visit several plants and have great ecological importance (Darrault & Schlindwein, 2002).
The estimated richness was very close to the one observed with the estimators based on abundance Chao1 = 47.1 and ACE = 44.5 and also in the species incidence with Bootstrap = 46.23 (Figure 2). The highest estimate was obtained with Chao 1, probably as a function of the number of singletons and doubletons that represented 26.8% of the richness in the SESWG (Ferraz et al., 2009). The sampling efficiency was 87% with Chao1; 92.1% with ACE; and 88.7% with Bootstrap.
The total of hawkmoths species collected was considered high for the sampling effort. The SESWG showed a significantly higher species richness than the localities where one year or more of sampling effort with luminous attraction was carried out, as for example, two areas of Atlantic Forest in Pernambuco with records of 23 species in the Gurjaú Biological Reserve (GBR), Cabo de Santo Agostinho (Duarte Jr & Schlindwein, 2005b) and 31 species in the Tapacurá Ecological Station (TES), São Lourenço da Mata (Primo et al., 2013). The estimate of 47.1 species (Chao 1) for SESWG is consistent with the highest richness known for northeastern Brazil, with 50 species in the PNHRFC, a reservation that harbors one of the best-preserved Atlantic Forest fragments of Pernambuco state (Duarte Jr & Schlindwein, 2008) (Table 3).
The accumulated number of species throughout the six sampling periods in SESWG resulted in a curve close to the asymptote (Figure 3). In other areas of Atlantic Forest in northeastern Brazil, as the GBR, the species accumulation curve showed stabilization as of the sixth sampling (six months) (Duarte Jr & Schlindwein, 2005b). However, in PNHRFC, the curve reached the asymptote point and stabilization in the tenth sampling (ten months) (Duarte Jr & Schlindwein, 2008). Similarly, in TES, the curve showed an apparent stabilization after the fourteenth sampling (14 months) effort, but there was an increment of 11 species at the end of the sampling (total of 27 months) (Primo et al., 2013).
Analyzing geographic distribution of the species recorded in the SESWG, 19 species have only been sampled in the Atlantic Forest and one species in the Caatinga, three species were collected in the Caatinga and Atlantic Forest biomes, three species in the Atlantic Forest and Cerrado, and fifteen species are broadly distributed across the three biomes (Table 1 and 3).
In the SESWG the genera with highest species richness were Xylophanes Hübner, [1819], Manduca Hübner, [1807], Isognathus Felder & Felder, 1862 and Eumorpha Hübner, [1807]. This result is probably a direct function of the number of species in each genus, since these are the richest of them. The same pattern was also observed in the PNHRFC; in this area however, the genera Callionima Lucas, 1857, Erinnyis Hübner, [1819] and Eumorpha together correspond to 30% of the richness, with a total of 15 species (Duarte Jr & Schlindwein, 2008).
Five species, Eumorpha phorbas (Cramer, 1775), Isognathus excelsior (Boisduval, [1875]), Oryba kadeni (Schaufuss, 1870), Pachylia darceta and Manduca leucospila (Rothschild & Jordan, 1903) are recorded for the first time in the northeastern region. These species were recorded previously mainly in the Amazon biome (Motta, Ferreira, & Aguiar, 1991; Motta, Aguilera-Peralta, & Andreazze, 1998; Motta & Andreazze, 2001; Motta & Xavier-Filho, 2005; Lourido et al., 2018; Conceição & Teston, 2020). Martin et al. (2011) also recorded Oryba kadeni, Eumorpha phorbas and Manduca leucospila in the Atlantic Forest of Serra dos Órgãos, Rio de Janeiro State; Camargo et al. (2018) recorded Pachylia darceta in the Cerrado in the states of Maranhão and Minas Gerais, and according to Haxaire and Mielke (2019) this species also occur in the state of Santa Catarina.
In the Catálogo dos Lepidoptera Cearenses, Silva (1967) cited the only reference of the Manduca lucetius (Cramer, 1780) in the Northeast. The state of Ceará has most of its territory in the Caatinga phytogeographical domain. Thus, two species, Isognathus excelsior and Manduca lucetius found mainly in the Amazonian rainforest (Haxaire & Mielke, 2019) represent new records for the Atlantic Forest biome.
The present study is the second Sphingidae inventory undertaken in the state of Bahia. Among the 41 species recorded in the SESWG, 22 species were also recorded in the Tabuleiro Forest of the Campus Sosígenes Costa (CSC), Porto Seguro, Bahia, that now holds the fourth place in hawkmoths richness in northeastern Brazil with 40 species. Together, SESWG and CSC add up to a total of 59 species for the Atlantic Forest of Bahia. The following species were recorded only in the CSC: Callionima inuus (Rothschild & Jordan, 1903), Enyo gorgon (Cramer, 1777), Enyo ocypete (Linnaeus, 1758), Erinnyis obscura obscura (Fabricius, 1775), Eumorpha fasciatus fasciatus (Sulzer, 1776), Isognathus australis Clark, 1917, Isognathus menechus (Boisduval, [1875]), Madoryx plutonius (Hübner, [1819]), Nyceryx coffaeae (Walker, 1856), Perigonia lusca (Fabricius, 1777), Phryxus caicus (Cramer, 1777) (Macroglossinae: Dilophonotini); Adhemarius daphne daphne (Boisduval, 1875, Adhemarius gagarini (Zikán, 1935), Protambulyx eurycles (Herrich-Schäffer, [1854]) (Smerinthinae: Ambulycini); Cocytius lucifer Rothschild & Jordan, 1903, Cocytius duponchel (Poey, 1832), Neococytius cluentius (Cramer, 1775) (Sphinginae: Sphingini); Agrius cingulata (Fabricius, 1775) (Sphinginae: Acherontiini) (Vila-Verde & Paluch, 2019; Haxaire & Mielke, 2019).
The results obtained in this study after six months of samplings corroborate the high species richness expected for the Atlantic Forest and encourage new studies in SESWG, including other taxonomic groups. Species Inventories are important tools for assessing the local diversity and for allowing the promotion of conservation actions and policies (Santos, Mielke, & Casagrande, 2008; Freitas & Marini-Filho, 2011).
The richness found in the SESWG evidences the need for further studies in order to increase the sampling effort. It is important to note that most inventories carried out in the northeastern Atlantic Forest lasted a year or more, but the richness recorded was lesser or similar than the richness found in the SESWG after a six month sampling period.
The sampling efficiency obtained with the estimators Chao1= 87%, ACE= 92.1% and Bootstrap= 88.7% was higher than 80%. Notwithstanding, the accumulated number of species collected demonstrates the need for further sampling, including seasonality studies in order to better approach the curve asymptote.
The present study contributes to broaden the knowledge on richness and distribution of Sphingidae in northeastern Brazil. Together, SESWG and CSC add up a checklist of 59 species for the Atlantic Forest of Bahia. Isognathus excelsior and Manduca lucetius represented new records for the Atlantic Forest biome.
The Instituto do Meio Ambiente e Recursos Hídricos (INEMA) for the collection license. The Programa de Pós-Graduação em Ciências Agrárias (PPGCAGR) of the Universidade Federal do Recôncavo da Bahia (UFRB) and staff of the SESWG for their support. The researcher Alexandre Soares (MNRJ-Brazil) for the assisting in the Manduca species identification. The first author thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship. This publication is part of the Rede Nacional de Pesquisa e Conservação de Lepidópteros – RedeLep (SISBIOTA-Brasil/CNPq - 563332/2010-7).
eduarda_malheiros@hotmail.com
