Brazilian Journal of Development 47275 ISSN: 2525-8761 Leaf changes in Avicennia schaueriana following a massive herbivory event by Hyblaea puera (Lepidoptera) in South Brazil Mudanças foliares em Avicennia schaueriana após um grande evento de herbivoria por Hyblaea puera (Lepidoptera) no Sul do Brasil DOI:10.34117/bjdv7n5-233 Recebimento dos originais: 07/04/2021 Aceitação para publicação: 12/05/2021 Amanda Martins Ruthes Laboratory of Plant Morphology and Ecology, Post-graduate Program in Health and Environmental, University of Joinville Region, R. Paulo Maschitzki 10, 89219-710, Joinville, SC, Brazil Maiara Matilde da Silva Post-graduate Program in Ecology and Conservation, Federak University of Paraná, Box 19031, 81531-990 Curitiba, PR, Brazil João Carlos Ferreira de Melo Júnior Laboratory of Plant Morphology and Ecology, Post-graduate Program in Health and Environmental, University of Joinville Region, R. Paulo Maschitzki 10, 89219-710, Joinville, SC, Brazil E-mail: [email protected] ABSTRACT (Leaf changes in Avicennia schaueriana following a massive herbivory event by Hyblaea puera (Lepidoptera) in South Brazil) Herbivory is an interaction that can change the structure of plant communities in two main ways: by causing death and reducing plant populations; and by changing leaf characteristics of plants that, secondarily, changes interactions of plants with the biotic and abiotic environment. Leaf defense and nutritional attributes of Avicennia schaueriana were comparatively evaluated after a massive herbivory event by the exotic species Hyblaea puera (Lepidoptera: Hyblaeidae) in the mangrove of Babitonga Bay, Joinville, SC, Brazil. The leaf attributes differed between the A. schaueriana control group and group that suffered a massive herbivory attack. The specific leaf area (SLA) was smaller in the group that suffered the injury from herbivory and, thus, the leaves were harder. In addition, there was a reduction in water content that made the leaves less nutritious. Secondary compounds were present in more mesophyll tissues in the plants that suffered herbivory compared to the control group. These results suggest that the plants respond to herbivory through changes in the leaves that reduce the preference of the insects. Keywords: plant herbivory, tropical mangrove, environmental quality RESUMO A herbivoria é uma interação que pode mudar a estrutura das comunidades de plantas de duas maneiras principais: causando a morte e reduzindo as sua populações; ou alterando as características das folhas das plantas que, secundariamente, alteram as interações das Brazilian Journal of Development, Curitiba, v.7, n.5, p. 47275-47286 may. 2021 Brazilian Journal of Development 47276 ISSN: 2525-8761 plantas com o ambiente biótico e abiótico. A defesa foliar e os atributos nutricionais de Avicennia schaueriana foram avaliados comparativamente após um evento de herbivoria massiva pela espécie exótica Hyblaea puera (Lepidoptera: Hyblaeidae) no manguezal da baía Babitonga, Joinville, SC, Brasil. Os atributos foliares diferiram entre o grupo controle de A. schaueriana e o grupo que sofreu um ataque massivo de herbivoria. A área foliar específica (SLA) foi menor no grupo que sofreu o dano por herbivoria e, portanto, as folhas ficaram mais duras. Além disso, houve redução do teor de água que tornou as folhas menos nutritivas. Compostos secundários estiveram presentes em mais tecidos do mesofilo nas plantas que sofreram herbivoria em comparação ao grupo controle. Esses resultados sugerem que as plantas respondem à herbivoria por meio de mudanças nas folhas que reduzem a preferência dos insetos. Palavras-chave: herbivoria vegetal, manguezal tropical, qualidade ambiental 1 INTRODUCTION Herbivory is one of the most common interactions in natural environments due to the high diversity of extant plants and insects. Rates of herbivory are controlled by leaf characteristics, such as presence of epidermal appendages (Abdala-Roberts & Parra- Tabla 2005), presence of a thick cuticle of varying chemical composition (Eigenbrode & Espelie 1995), amount of calcium oxalate crystals (Franceschi & Nakata 2005), and chemical compounds in cells that repel or are toxic to insects (Kursar & Coley 2003). Plants that occupy shaded habitats on soils with high water availability and high concentrations of nutrients develop more nutritious palatable leaves and, consequently, are damaged more by herbivores (Muth et al. 2008; LoPresti 2017). On the other hand, plants that occur in environments with scarce resources or conditions of stress develop tissues of low nutritional quality and palatability. A mangrove is an example of an ecosystem with plant species that are characterized by sclerophyllous leaves, with subepidermal layers with calcium oxalate crystals and high concentrations of Na (Lima 2013). In addition to diverse defensive leaf attributes, mangroves are low in plant diversity and have the lowest diversity of resources for insects compared to other vegetation formations. The woody flora of the mangrove in Babitonga Bay (Santa Catarina, Brazil), for example, comprises only Laguncularia racemosa (L.) C.F. Gaertn., Rhizophora mangle (Rhizophoraceae) L. and Avicennia schaueriana (Verbenaceae) Stapf & Leechm. ex Moldenke (Kilca et al. 2011). The average herbivory rate recorded in mangroves is around 10% (Menezes & Peixoto 2009); miners are the most common type of herbivore, followed by gallers and Brazilian Journal of Development, Curitiba, v.7, n.5, p. 47275-47286 may. 2021 Brazilian Journal of Development 47277 ISSN: 2525-8761 chewers (Menezes & Peixoto 2009). Among arboreal mangrove species, those of the genus Avicennia suffer major damage from herbivory and have the highest diversity of associated insect feeding guilds (Kathiresan 2003; Menezes & Peixoto 2009). Unlike the records of plant-herbivore interaction mentioned above, some insects can cause intense damage to plants by consuming massive amounts of plant tissue, resulting in direct and indirect physiological and ecological damage to the plant resource. For example, Hyblaea puera Cramer (Lepidoptera: Hyblaeidae) consumes the entire canopy of Tectona grandis in India and Mexico (Nair 2007; Cibrián-Llanderal 2015), resulting in important economic losses (Nair 2007). Recently, H. puera was registered in India causing severe and extensive damage to mangrove communities (Arun & Mahajan 2012). Similarly, the massive consumption of mangroves by H. puera was reported in Brazil in the states of Pará (Menezes & Mehlig 2005, 2008; Fernandes et al. 2009), Rio de Janeiro (Menezes & Peixoto 2009), Paraná (Faraco et al. 2019) and Santa Catarina (Melo Jr. et al. 2017). Although the caterpillar of H. puera attacks all mangrove species, mass consumption occurs only in Aviccenia species in all studied locations (Menezes & Mehlig 2005, 2208; Fernandes et al. 2009; Menezes & Peixoto 2009; Arun & Mahajan 2012; Faraco et al. 2019). With respect to mangrove herbivory, Fernandes et al. (2009) showed evidence that mass herbivory by H. puera causes an increase in nutrient cycling in the soil and, consequently, increases the productivity in aquatic ecosystems. However, no study has evaluated the impact of herbivory by H. puera on the plant itself. The impacts of herbivory on a plant community can be direct, such as changes in leaf characteristics after the herbivory event and death of the plant specimen consumed (Traw & Dawson 2002), and indirect, such as changes in the plant community structure (Norghauer & Newbery, 2014) and changes in the network of insect-plant interactions (e.g., herbivory interaction or pollination) (Glaum & Kessler 2017; Santangelo et al. 2018). The objective of the present study was to evaluate the direct impact caused by the massive herbivory of A. shaueriana leaves in Babitonga Bay. The hypothesis was that after the herbivory event A. schaueriana would exhibit leaf morphoanatomical changes. We predicted that leaves in the affected mangrove would possess more marked anti- herbivory attributes (more sclerophyllous leaves with lower water content and greater distribution of secondary metabolites) in relation to leaves in a non-affected mangrove. Brazilian Journal of Development, Curitiba, v.7, n.5, p. 47275-47286 may. 2021 Brazilian Journal of Development 47278 ISSN: 2525-8761 2 MATERIAL AND METHODS The study was conducted between February and March 2018 in an area of mangrove forest in the municipality of Joinville (26°17'09.8"S, 48°47'05.4"W; - 26.286068, -48.784824), in the northeastern region of the state of Santa Catarina. The climate of the region falls within the humid climate zone and is predominantly humid mesothermic with hot summers (Cfa of Köeppen). Rainfall is well distributed throughout the year with common south winds bringing oceanic humidity to the atmosphere that results in wet winters. The mean annual temperature is 20.6 °C. The mangrove is associated with Babitonga Bay, which together form the largest estuary in the region (Xavier and Maia, 2008, Kilca et al. 2011). The mangrove cover in the city of Joinville corresponds to 76% of the mangroves in Santa Catarina State (Babitonga Ativa unpublished data). Avicennia schaueriana was selected for the study because it is the taxon most attacked by insects, including Hyblaea puera (Menezes & Mehlig 2005, 2208; Fernandes et al. 2009; Menezes & Peixoto 2009; Arun & Mahajan 2012; Faraco et al. 2019). Popularly known as black mangrove, A. schaueriana is a tree characterized by its smooth, light brown bark, fine, long pneumatophores, and light