Climate seasonality drives ant–plant–herbivore interactions via plant phenology in an extrafloral nectary‐bearing plant community

• Published in: The Journal of ecology Vol. 109; no. 2; pp. 639 - 651
• Main Authors: Calixto, Eduardo Soares, Novaes, Letícia Rodrigues, Santos, Danilo Ferreira Borges, Lange, Denise, Moreira, Xoaquín, Del‐Claro, Kleber, Züst, Tobias
• Format: Journal Article
• Language: English
• Published: Oxford Blackwell Publishing Ltd 01.02.2021
• Subjects: Abiotic factors; Abundance; Ants; ant–plant interactions; biotic defence; Brazilian Cerrado; Carbohydrates; Climate; Extrafloral nectaries; Flowers; Herbivores; herbivory; indirect defence; Leaves; Mutualism; Nectar; Phenology; phenophases; Plant communities; Plant species; Plants; Rain; Rainfall; Rainy season; seasonal environment; Seasonal variations; Seasonality; Secretion; Symbiosis; Temperature effects; Temporal variations; Wet season
• ISSN: 0022-0477; 1365-2745
• DOI: 10.1111/1365-2745.13492

Interactions between ants and plants bearing extrafloral nectaries (EFNs) are among the most common mutualisms in Neotropical regions. Plants secrete extrafloral nectar, a carbohydrate‐rich food that attracts ants, which in return protect plants against herbivores. This ant–plant mutualism is subjected to temporal variation, in which abiotic factors can drive the establishment and frequency of such mutualistic interaction. However, studies investigating how abiotic factors (e.g. climate) directly and indirectly influence ant–plant–herbivore interactions are incipient. In this study, we investigated direct and indirect (via plant phenology) effects of temperature and rainfall on ant–plant–herbivore interactions. To address these goals, each month we estimated six plant phenophases (newly flushed leaves, fully expanded leaves, deciduousness, floral buds, flowers and fruits), the activity of EFNs and abundance of ants and herbivores in 18 EFN‐bearing plant species growing in a markedly seasonal region (the Brazilian Cerrado) during a complete growing season. Our results showed that (a) there were marked seasonal patterns in all plant phenophases, EFN activity and the abundance of ants and herbivores; (b) the peak of EFN activity and ant and herbivore abundance simultaneously occurred at the beginning of the rainy season, when new leaves flushed and (c) rainfall directly and indirectly (via changes in the production of new leaves) influenced EFN activity and this in turn provoked changes in ant abundance (but not on herbivores). Synthesis. Overall, our results build towards a better understanding of how climate drives seasonal patterns in ant–plant–herbivore interactions, explicitly considering plant phenology over time. Resumo Interações entre formigas e plantas portadoras de nectários extraflorais (NEFs) estão entre os mutualismos mais comuns nas regiões Neotropicais. As plantas secretam néctar extrafloral, um alimento rico em carboidratos que atrai formigas, que em troca protegem as plantas contra herbívoros. Esse mutualismo formiga‐planta está sujeito à variação temporal, na qual fatores abióticos podem conduzir o estabelecimento e a frequência de tal interação mutualística. No entanto, estudos que investigam como esses fatores (por exemplo, clima) influenciam direta e indiretamente as interações formiga‐planta‐herbívoro são incipientes. Neste estudo, investigamos os efeitos diretos e indiretos (via fenologia das plantas) da temperatura e da precipitação nas interações formiga‐planta‐herbívoro. Para atingir esses objetivos, a cada mês estimamos seis fenofases das plantas (folhas recém‐lavadas, folhas totalmente expandidas, caducifólia, botões florais, flores e frutos), a atividade dos NEFs e abundância de formigas e herbívoros em 18 espécies de plantas portadoras de NEF de uma região marcadamente sazonal (o Cerrado brasileiro) durante uma estação de crescimento completa. Nossos resultados mostraram que (i) havia padrões sazonais marcados em todas as fenofases da planta, na atividade dos NEFs e na abundância de formigas e herbívoros; (ii) o pico de atividade dos NEFs e abundância de formigas e herbívoros ocorreram simultaneamente no início da estação chuvosa, quando novas folhas surgiram; e (iii) a chuva direta e indiretamente (via mudanças na produção de novas folhas) influenciou a atividade dos NEFs e isso por sua vez provocou mudanças na abundância de formigas (mas não nos herbívoros). Síntese. No geral, nossos resultados fornecem um melhor entendimento de como o clima impulsiona os padrões sazonais nas interações formiga‐planta‐herbívoro, considerando explicitamente a fenologia da planta ao longo do tempo. Palavras‐chave. Interações Formiga‐Planta, Mutualismo, Defesa Indireta, Defesa Biótica, Herbivoria, Cerrado Brasileiro, Ambiente Sazonal, Fenofases. Overall, our results build towards a better understanding of how climate drives seasonal patterns in ant–plant–herbivore interactions, explicitly considering plant phenology over time. We present an Structural Equation Modelling diagram showing direct and indirect effects of climatic variables (rainfall and temperature) on newly flushed leaves, EFN activity, and the abundance of ants and herbivores.