Seasonal climatic effects on the Lepidoptera diversity in a peri-urban patch of “restinga” in Brazil

doi:10.21203/rs.3.rs-3998336/v1

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Seasonal climatic effects on the Lepidoptera diversity in a peri-urban patch of “restinga” in Brazil

https://doi.org/10.21203/rs.3.rs-3998336/v1

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Global climate change and the accelerated urbanization process of coastal habitats have resulted in a drastic reduction in biodiversity, including lepidopteran fauna. In the Atlantic Forest, “restingas” are among the most threatened phytophysiognomies because they are located on the coastal strip, where high demographic densities are concentrated. Therefore, restinga areas have been strongly affected by actions of urbanization, but data on species composition, endemism, or extinction risks, mainly for its entomofauna, remains scarce. In this work, we evaluated whether the abundance and richness of butterfly and diurnal moth species respond to seasonal variations at the Restinga of Barreto Municipal Natural Park (PNMRB) in Macaé, Rio de Janeiro, Brazil. We actively searched for butterflies and diurnal moths between 2019 and 2020 and captured them using an entomological net. We tested whether species richness and abundance varied between different periods of the day (morning and afternoon) and seasons (dry and rainy season). We sampled a total of 236 individuals representing 40 butterflies and diurnal moth from eight families. Species abundance and richness were higher during the dry season, when average temperature, relative humidity and rainfall are lower. We observed two peaks of species abundance during the day, one at ~ 10:00 am and the other at ~ 2:00 pm. Nymphalidae was the family with the greatest richness and abundance and the most abundant species were Ascia monuste orseis (Godart, 1819), Heliconius sara apseudes (Hubner, 1813) and Dryas iulia alcionea (Cramer, 1779). The lepidopteran fauna of PNMRB presented a clear seasonal pattern, showing that climatic fluctuations related to variations in average temperature and rainfall can negatively affect this important group of pollinating insects. Studies involving Lepidoptera communities are fundamental to management and conservation plans of insect fauna and the ecosystem services. In this sense, the survey of Lepidoptera diversity in the PNMRB can be relevant information for the maintenance or expansion of protected areas. Also generate data that can increase the knowledge about climatic effects on the temporal distribution and conservation of Neotropical Lepidoptera.

Atlantic Forest

conservation

Nymphalidae

seasonality

urbanization

The Atlantic Forest is one of the most diverse biomes in the Neotropical region (Myers et al., 2000; Santos et al., 2017) and is also considered a hotspot of world diversity (Laurance & Vasconcelos, 2009; Mittermeier et al., 2011). Moreover, this biome is identified as one of the most threatened on Earth, as only 11–16% of its original coverage remains (Ribeiro et al., 2009; SOS Mata Atlântica & INPE, 2017). Rezende et al. (2018), in a comprehensive high-resolution remote sensing study, suggested in Atlantic Forest a high prevalence of secondary vegetation and fragmented vegetation.

Restinga is one of the phytophysiognomies of the Atlantic Forest present in the coastal regions, where the highest demographic densities in Brazil are concentrated (Rocha et al., 2007). Restinga areas have been strongly affected by actions of urbanization, but data on species composition, endemism, or extinction risks, mainly for its entomofauna, remains scarce (Silva, 1999; Rocha et al., 2007; Kamke et al., 2011). Restinga is recent geological formations, during the Quaternary, and were formed by the deposition of sandy sediments (Assumpção & Nascimento, 2000). Adjacent to the Brazilian coast, its vegetation is composed of plants adapted to constant exposure to high temperatures, light incidence and high levels of radiation and salinity. They also need to respond with adaptations to survive the scarcity of nutrients and water in the soil, mobility of the dunes and action of the winds (Dillenburg et al., 1992).

Most tropical organisms respond to the effects of seasonality, which can be observed through variations in population frequencies throughout the year (Kishimoto-Yamada & Itioka, 2015; Lourenço et al., 2019). The biotic and abiotic variables during the dry and rainy seasons alter the availability of resources and the regulation of natural enemies, directly affecting the abundance and richness of tropical insects (Wolda, 1989; Grotan et al., 2012). Temperature and rainfall are predictors that influence the development cycle of butterfly fauna (Hamer et al., 2006; Ribeiro et al., 2010).

Global climate change and habitat loss caused a decline in the abundance of terrestrial arthropods (Van Klink et al., 2020). Lepidoptera is the second largest order of insects and approximately 60% of all the diversity of the Neotropical region, nearly 26.000 species distributed in 71 families is concentrated in Brazil (Brown Jr. & Freitas, 1999; Prado & Zukovski, 2018). Lepidopterans exploit a wide range of resources, which make them fundamental to ecological balance (Lourenço et al., 2019). Pollinating species allow gene flow between plant populations and maintain the stability and regulation of plant communities (Fonseca et al., 2006). Additionally, these insects participate in natural biological control when preyed on or parasitized during their different life stages (Duarte et al., 2009). Butterflies can also be involved in management and conservation plans as they are considered excellent models for studying the structure and temporal variation in communities, therefore, potentially being a proxy of environmental changes (Bonebrake et al., 2010; Devries et al., 2016; Lourenço et al., 2019; Kuussaari et al., 2020).

Fragmentation and habitat loss are factors that have threatened lepidopteran fauna (Paz et al. 2014). Populations of some butterfly species manage to establish themselves in small urban fragments, making these areas important for conservation (Brown Jr. & Freitas, 2002; Alvey, 2006; Uehara-Prado et al., 2007; Nilon, 2011). According to the Red Book of Endangered Brazilian Fauna (ICMBio, 2018), 50 species of Lepidoptera are assigned to some threat category, 33 of them recorded in Rio de Janeiro state.

Considering that climatic variation drives seasonal changes in butterfly populations, this work aimed to explore the fauna of butterflies in a peri-urban fragment to answer the following questions: Do richness and abundance of lepidopterans vary between seasons? Are species richness and abundance positively related to temperature, rainfall, and relative humidity?

Study area - The Restinga of Barreto Municipal Natural Park (PNMRB) is located in the urban region of Macaé municipality, Rio de Janeiro (22º20.367' S, 41º44.467' W) and occupies an area of 320,000 m² of “restinga” (Fig. 1). The Park is located in a region threatened by accelerated urbanization, and most of the areas with natural vegetation have been either wiped out or are severely fragmented. The phytophysiognomy is characterized by creeping vegetation, thickets, shrubs, and typical restinga vegetation, composed mainly of species from the Myrtaceae, Convolvulaceae, Cactaceae, Bignoniaceae, and Fabaceae families (Araújo 1992). The climate is tropical, classified as Aw (Köppen & Geiger, 1928). The average temperature is 22.9° C, and the average annual rainfall is 1126 mm, with most of the rains concentrated during the tropical summer (INMET, 2020).

Sampling - Sampling was carried out from May 2019 to March 2020 along a 1,800 meter transect, with six sampling sites located 300 meters apart from each other. Two collectors captured all the butterflies and diurnal moths in flight or visiting flowers using an entomological net in each sampling event, alternating between the 6 sites from 8:00 am to 4:00 pm at intervals of 30 minutes (Fig. 1). We visited the area five times during both dry and rainy seasons. The months from October to March were considered the rainy season, and the dry season was considered from May to September. All captured butterflies and diurnal moths were placed in entomological envelopes for later assembly and taxonomic identification. We identified individuals based on previously published taxonomic literature (Brown Jr., 1992; Penz & Devries, 2002; Willmott, 2003; Uehara-Prado et al., 2004; D'Abrera, 2005; Santos et al., 2011), as well as the illustrated list of South American butterflies (Warren et al., 2017). We vouchered and stored the collected specimens at the Integrated Invertebrate Laboratory of the Biodiversity and Sustainability Institute, Federal University of Rio de Janeiro, Brazil. Temperature, rainfall, and air humidity records were obtained from the website of “Instituto Nacional de Meteorologia” (INMET, 2020).

Statistical analyzes - The species occurrence frequency was assessed based on the number of individuals defined as singletons (a single individual was sampled throughout the study period) and doubletons (two individuals sampled) (sensu Ferraz et al., 2009). We then perfomed an analysis of variance and subsequently a Tukey’s posthoc test at p < 0.05 significance level (Sigmaplot version 12.5) to test whether species richness and abundance vary between different periods of the day (morning and afternoon) and season (dry and rainy). We used a non-linear regression model with a sine-squared function to test whether the abundance of butterflies varies between periods of the day and between the rainy and dry seasons.

We recorded 236 individuals comprising a total of 40 lepidopteran species (Fig. 2) distributed among eight families. The Nymphalidae was the richest (S = 18 spp; 45%) and most abundant (n = 130 individuals; 55.08%) family, followed by Pieridae (S = 6 spp; 15%; n = 73 individuals; 30.93%), and Hesperiidae (S = 4 spp; 10%; n = 12 individuals; 5.08%). The families Erebidae, Geometridae, Lycaenidae, Papilionidae, and Ridionidae were less frequent (Fig. 2, Fig. 3).

The most abundant species were Ascia monuste orseis (Godart, 1819) (n = 52), Heliconius sara apseudes (Hubner, 1813) (n = 50), and Dryas iulia alcionea (Cramer, 1779) (n = 19), which were sampled mainly in the dry season (Fig. 2) and represented more than half of the individuals sampled (n = 121; 51.27%). We recorded 15 species (37.5%) exclusively during the dry season, six (15%) exclusively in the rainy season, and 19 species (47.5%) occurred in both seasons, showing a clear difference in species composition between these seasons (Fig. 2). Most species had low population density, and 11 species were singletons (Fig. 2).

The richness and abundance of species varied between the dry and rainy seasons (richness: F1; 64 = 7.91; P = 0.0065 and abundance: F1; 64 = 23.13; P < 0.0001; Fig. 3), between families (richness: F7; 64 = 16.58; P < 0.0001 and abundance: F7; 64 = 19.46; P < 0.0001; Fig. 3) and in the interaction between the seasons and families (richness: F7; 64 = 2.79; P = 0.0135 and abundance: F7; 64 = 9.15; P < 0.001; Fig. 3).

The richness and abundance of Lepidoptera species were higher in the dry season when average temperature and rainfall are lower (richness: F1; 16 = 15.46; P = 0.0012 and abundance: F1; 16 = 8.30; P = 0.0109; Fig. 4). We did not find an effect of the interaction between the seasons and the periods of the day on butterfly richness and abundance (richness: F1; 16 = 0.37; P = 0.5494 and abundance: F1; 16 = 0.01; P = 0.9335). We observed two peaks of species abundance during the day, one at ~ 10:00 am and the other at ~ 2:00 pm (F2; 45 = 17.06; P < 0.001; Fig. 5).

The abundance and richness of Lepidoptera in the PNMRB varied seasonally and were higher in the dry season. The species composition may indicate how habitat fragmentation impacts the structure of habitats and the response of butterfly communities to changes, such as resource availability, food guilds, patterns of occurrence, and species composition (Pignataro et al., 2020). In addition to reducing the availability of host plants for larval stages, fragmentation of the restinga can reduce the availability of native fruit trees, affecting the butterflies throughout the year (Ramírez-Restrepo & MacGregor-Fors, 2017).

This temporal pattern with greater richness and abundance in the dry season can also be an escape strategy from natural enemies mainly because, during the rainy season, the availability of plant resources increases and, consequently, higher rates of parasitism and predation on the larvae as well (Morais et al., 1999). Despite the importance of natural enemies as biotic pressure, the sandbank has severe physical characteristics, due to open vegetation and sandy soil, which increases the incidence of solar radiation. During the rainy season, which corresponds to the summer in the tropics, the average temperature is higher, and there is more intense insolation, factors that increase the risk of desiccating eggs and interfering with the physiology of insects (Monteiro et al., 2007).

The higher number of species restricted to the dry season (n = 15) suggests they may be sensitive to increased temperature. Patterns of the temporal distribution of Lepidoptera were found in some areas of restinga, with higher peaks of abundance between March and April (end of the rainy season) and in the dry season, between July and September (Flinte et al., 2006; Monteiro et al., 2007), a period that precedes the growth of new leaves of host plants. However, most studies indicate that the butterfly species richness and abundance are higher in the rainy season (Brown Jr. & Freitas, 2000; Silva et al., 2007; Iserhard et al., 2013; Carneiro et al., 2014; Kishimoto-Yamada & Itioka, 2015), mainly due to a greater supply of food resources and oviposition sites and host plants with new and soft leaves, and greater nutritional value (Wolda, 1989; Grotan et al., 2012; Iserhard et al., 2013). The rainy season increases the availability of resources, but climate change has raised average temperatures in recent decades. Climate change can alter the interaction between butterfly species and their host plants and affect ecosystem functions (Ferro et al., 2014; Sousa et al., 2019). Changes in the temporal distribution of species include a shift in synchronization between larvae, host plants, butterflies, flowers, and natural enemies between dry and rainy seasons (Logan et al., 2003; Carneiro et al., 2014; Lourenço et al., 2019; Sousa et al., 2019).

Most of the collected species showed low population densities, which does not necessarily characterize them as rare species. Low population densities may be an effect of fragment isolation caused by the urbanization process, which affects the availability of food resources, host plants, or alters the microclimate of habitats in restinga (Brown Jr. & Freitas, 2002, De Souza & Guillhermo-Ferreira, 2015). Sousa et al. (2019) suggest that a high incidence of singletons and doubletons species may help explain the high species turnover along urban gradients.

Butterflies are mainly sampled in the hours of greatest activity, with peaks of abundance in the morning and the early hours of the afternoon (Basset et al., 2011; Ritter et al., 2011; Freire & Diniz, 2014; Pignataro et al., 2020). Thermoregulation allows these insects to control body temperature through behavioral or physiological mechanisms (Iserhard et al., 2018), such as selection of microhabitats, adaptations to absorb sunlight, and changes in activity or color patterns (Rossato et al., 2018; Pereira et al., 2020).

Studies point out that the definition of protected areas for biodiversity conservation needs to consider the effects of climate change on species distribution (Hannah, 2010; Mawdsley, 2011; Lemes & Loyola, 2013). Several species have shown migrations to colder regions, both in temperate and tropics regions, as a response to the increase in global temperature (Parmesan et al., 1999; Colwell et al., 2008; Ferro et al., 2014). Some studies have applied modern techniques to predict the distribution of invertebrates (Diniz-Filho et al., 2010; Ferro et al., 2014) and revealed that climate change is modifying species’ phenology patterns, distribution and abundance, including Lepidoptera species (Kocsis & Hufnagel, 2011). For the Arctiinae subfamily, a long-term study conducted from 1968 to 1999 in Great Britain showed an approximately 30% decrease in abundance and proportion of occupied places after 1984, coinciding with an increase in average temperature. Ferro et al. (2014) suggest that climate change should cause contractions of up to 100% in the distribution areas of several Arctiinae species that inhabit the Atlantic Forest. Local extinctions can cause cascades of extinction and consequent disruption of ecosystem services, with consequences for ecological interactions and economic losses due to insect infestation and pestilence (Griffith et al., 2009; Araújo et al., 2011; Ferro et al., 2014).

Urbanization is seen as a strong selective pressure that homogenizes habitats and restricts the geographic distribution and sharing of niches by rare and common species (McDonnell & Hahs, 2015; Iserhard et al., 2018). Urban centers tend to form heat islands, increasing local temperature, affecting the microclimate and the structure of habitats. However, butterfly species respond differently to disturbances, with their abundances dependent on specific distribution patterns and life histories (Ramírez-Restrepo & MacGregor-Fors, 2017; Santos et al., 2019).

The richness and abundance of species in the PNMRB varied between seasons and between Lepidoptera families, as observed in other studies (Ribeiro et al., 2010; Freire and Diniz, 2014; Carreira, 2015; Santos et al. 2017). Nymphalidae was the most frequent family, a pattern commonly reported in Neotropical fauna inventories (Martins et al., 2017; Pérez et al., 2019; Sousa et al., 2019). In Brazil, about 800 species of Nymphalidae have been registered. This family has wide morphological and behavioral variety and rapidly responds to environmental variations, making this group essential for environmental monitoring in the tropics (Bonfantti et al., 2009; Ribeiro et al., 2012; Henriques et al., 2019).

In Brazil, patterns with a high richness of Lepidoptera species are registered mainly in large and more conserved fragments of the Atlantic Forest. Approximately 241 species were registered (Monteiro et al., 2004) in the Restinga of Jurubatiba National Park (PNRJ), and 98 species in the Rio Doce State Park (PERD; Lourenço et al., 2019). However, a study carried out on eight urban forest fragments, where fragment size ranged between 1.4 to 103.4 hectares, in Curitiba city, south Brazil, were found 298 species of butterflies but the richness was not directly proportional to the fragment size (Pérez et al., 2019). This work allows us to infer those urban fragments, regardless of size, can serve as a refuge for many species of butterflies, making these areas fundamental for biodiversity conservation (Pérez et al., 2019). However, comparisons between studies need to be considered due to the size of the areas and sampling efforts, collection methods, degree of disturbance, and heterogeneity of the Atlantic Forest (Martins et al., 2017).

The diversity of Lepidoptera depends on the distribution pattern of the host plants (Bonebrake et al., 2010; Sousa et al., 2019). Restingas ecosystems have abiotic specificities such as high insolation, salinity, and endemism of plants that influence the colonization of herbivorous insects (Ferro et al., 2014). Bellaver et al. (2012) registered 64 lepidopteran species in an area of 1,000 hectares of restinga in southern Brazil, connected to forest fragments of Atlantic Forest. In the largest preserved area of restinga in Brazil, the PNRJ, with 14,860 hectares (148,600.000m²), 64 out of the 241 lepidopteran species sampled, were actively collected with a net (Monteiro et al., 2004). The present study was carried out in a small urban fragment of 32 hectares, separated from the PNRJ by a large urbanized area (Fig. 1). In this small and isolated restinga fragment, 40 species of butterflies were actively sampled. Such lower species richness may be related to the smaller area, availability of host plants, and the effects of urbanization that can directly affect the structure of the butterfly community, as has been shown in several studies (Clark et al., 2007; Konvicka & Kadlec, 2011; Lizée et al., 2012; Melliger et al., 2017; Ramírez-Restrepo & MacGregor-Fors, 2017; Merckx & Van Dyck, 2019; Tzortzakaki et al., 2019 Kuussaari et al., 2020). Pérez et al. (2019) highlighted the lack of connectivity and the isolation of the fragments as mechanisms affecting the structure of butterfly communities in urban ecosystems, in addition to demonstrating that small fragments can harbor a high diversity of butterflies.

Lepidoptera diversity in the Restinga of Barreto Municipal Natural Park varied between seasons and Lepidoptera families, and were higher in the dry season. The seasonal pattern reflects that climatic fluctuations related to variations in average temperature and rainfall can negatively affect this important group of pollinating insects.

The species composition indicate how habitat fragmentation impacts the structure of habitats and the response of communities to changes. Studies involving Lepidoptera communities are fundamental to management and conservation plans of insect fauna and the ecosystem services. In this sense, the survey of Lepidoptera diversity in the Restinga of Barreto Municipal Natural Park can be relevant information for the maintenance or expansion of protected areas. Also generate data that can increase the knowledge about climatic effects on the temporal distribution and conservation of Neotropical Lepidoptera.

Life science journals + articles with biological applications

1) Funding (information that explains whether and by whom the research was supported)

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

2) Conflicts of interest/Competing interests (include appropriate disclosures)

The authors declare no competing interests

3) Ethics approval (include appropriate approvals or waivers)

'Not applicable'

4) Consent to participate (include appropriate statements)

'Not applicable'

5) Consent for publication (include appropriate statements)

'Not applicable'

6) Availability of data and material (data transparency)

All data are presented in the results section

7) Code availability (software application or custom code)

'Not applicable'

8) Authors' contributions

- Camila T. B. Guedes =conception, design, data collection, analysis, and writing of the document;

- Amanda S. Miranda =conception, design, data collection, analysis, and writing of the document;

- Alexandre Soares =analysis, and writing of the document;

- Leandro Bacci =analysis, and writing of the document;

- Yasmine Antonini =conception, analysis, and writing of the document;

- Vinícius A. Araújo =conception, design, data collection, analysis, and writing of the document;

Acknowledgements

The authors thank the administration of the Restinga do Barreto Natural Municipal Park for support and structure and the Municipal Environmental Guard of Macaé for security. To Jully da Silva and Juliana Meireles for their help in field collections.

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Seasonal climatic effects on the Lepidoptera diversity in a peri-urban patch of “restinga” in Brazil

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