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Pollinator assemblage response to nutrient enrichment in grasslands
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Abstract(s)
Os insetos polinizadores estão globalmente em declínio, sendo a intensificação da agricultura um dos principais fatores promotores desse declínio. Além das alterações no uso do solo (incluindo a simplificação da paisagem e dos ecossistemas) e do uso massivo de pesticidas, a intensificação da agricultura também está associada a uma elevada adição de nutrientes, ou enriquecimento em nutrientes, a qual constitui uma grande ameaça para a biodiversidade global. Nas últimas décadas, estudos principalmente nas regiões temperadas do hemisfério norte possibilitaram conhecer os efeitos do enriquecimento em nutrientes em comunidades de plantas, identificando várias tendências como o aumento de produtividade, redução da riqueza de plantas e as mudanças na química destas. Não obstante, regiões como a ecorregião Mediterrânica (sul da Europa) e várias regiões tropicais e subtropicais da América do Sul não têm recebido suficiente atenção sobre o efeito do enriquecimento em nutrientes nas plantas. Além disso, existe uma lacuna no conhecimento do efeito em cascata do enriquecimento em nutrientes em níveis tróficos superiores, como os polinizadores.
O objetivo principal desta tese é avaliar os efeitos simultâneos de vários tratamentos de enriquecimento em nutrientes nos polinizadores, relacionando-os com as alterações na composição das comunidades de plantas, na abundância de flores e nos recursos florais (qualidade e quantidade de pólen). Contribuindo para colmatar as atuais lacunas de conhecimento, usámos locais experimentais da Nutrient Network (NutNet – uma rede de investigação coordenada de pradarias que implementam tratamentos estandardizados de adição de nutrientes) e combinámos:
i)
uma abordagem local (usando uma experiência de campo de manipulação de nutrientes que está a ser desenvolvido numa pradaria Mediterrânica em Portugal) para avaliar os efeitos do enriquecimento em nutrientes nos recursos florais e seu efeito nos polinizadores e nos patrões de interação planta-polinizador.
ii)
uma abordagem a larga escala (com dados de 14 experiências de campo de manipulação de nutrientes) para compreender os efeitos do enriquecimento em nutrientes em diferentes comunidades de plantas e polinizadores em três continentes (Europa e América do Norte e do Sul) e avaliar o efeito da fertilidade do solo e da temperatura no efeito do enriquecimento em nutrientes
nas plantas e polinizadores.
Com a abordagem local, detetámos efeitos contrastantes na abundância de flores de três espécies dominantes coexistentes (Crepis capillaris, Raphanus raphanistrum e Echium plantagineum), ou seja, o enriquecimento em NP aumentou a abundância de flores enquanto o enriquecimento em P diminuiu-a. Os efeitos do enriquecimento em nutrientes na qualidade (em termos dos aminoácidos) e quantidade do pólen foi específica para cada espécie, tendo-se observado efeito forte, médio e fraco no conjunto das três espécies. Nenhum tratamento teve efeito negativo sobre a taxa de visitação dos polinizadores (total ou nos grupos de polinizadores), o que foi explicado por compensações na qualidade e quantidade de pólen ao nível da flor e da parcela. O enriquecimento em P teve um efeito positivo na taxa de visitação de Raphanus devido ao aumento da concentração de aminoácidos no pólen, mas teve um efeito negativo na taxa de visitação da comunidade de plantas ao nível de parcela, devido a uma redução da abundância de flores. Finalmente, o enriquecimento em NP e em P afetou os padrões de procura de alimento, e consequentemente, as redes de interação: i) enriquecimento em NP aumentou a diversidade de polinizadores e a generalidade de plantas, resultando numa maior generalização da rede; e ii) o enriquecimento em P diminuiu a diversidade de polinizadores, sendo estes mais especializados na procura de alimento, o que aumentou a especialização da rede.
Com a abordagem a larga escala, observou-se que a temperatura regional e a fertilidade do solo interagem com o enriquecimento em nutrientes, principalmente em N (mais também em P), modulando o efeito na diversidade de plantas e polinizadores. Em áreas quentes, o efeito do enriquecimento em N foi negativo na diversidade de plantas e polinizadores, mas foi positivo em regiões frias. Adicionalmente, a resposta da riqueza de plantas foi mas forte em locais com solos pobres enquanto a abundância de flores foi a resposta foi mais forte em locais com solos ricos. A resposta dos polinizadores ao enriquecimento em nutrientes foi mais acentuada do que a resposta das plantas.
Os resultados desta tese claramente mostram que o enriquecimento em nutrientes é impulsor de alterações da disponibilidade de recursos florais, com efeitos ascendentes até os polinizadores. Os dados de nossa abordagem local claramente mostram que o enriquecimento em NP pode melhorar os recursos florais (em quantidade e qualidade) numa pradaria Mediterrânica com efeitos positivos na diversidade de polinizadores; enquanto o enriquecimento em P pode ter efeitos negativos na abundância de flores, com efeitos negativos na taxa de visitação dos polinizadores e na sua diversidade. Além do efeito na diversidade, mostrámos que o enriquecimento em nutrientes afetou os padrões de procura de alimento dos polinizadores, para uma generalização (enriquecimento em NP) ou especialização (enriquecimento em P) das redes. Mudanças na generalização da redes poderia afetar a tolerância das comunidades a futuras perturbações. Os dados de nossa abordagem em larga escala mostram que os polinizadores estão em maior risco em regiões quentes, que geralmente são hotspots de biodiversidade e que contribuem para a produção global de alimentos. O aquecimento global em curso e o aumento do uso dessas regiões para a agricultura intensiva podem comprometer a polinização das culturas e o fornecimento de alimentos, caso políticas para controlar a intensidade agrícola (incluindo as quantidades de nutrientes adicionados) não sejam implementadas.
Em geral, esta tese fornece informações cruciais sobre os efeitos do enriquecimento em nutrientes nos polinizadores, por meio do estudo de diferentes vias através das quais as mudanças nas plantas causadas pelo enriquecimento em nutrientes, impactam os polinizadores. Para compreender melhor esses efeitos, as investigações futuras deveriam priorizar regiões pouco estudadas e incluir uma ampla variedade de espécies de plantas e de polinizadores em estudos ao nível da comunidade.
ABSTRACT: Insect pollinators are declining worldwide, with agricultural intensification as one of the main drivers. Besides land-use changes (including landscape and ecosystem simplification), and a massive use of pesticides, agricultural intensification is associated with elevated nutrient inputs or nutrient enrichment, which is a major threat to global biodiversity. In the last decades, studies mostly from temperate northern hemisphere regions enabled understanding the effects of nutrient enrichment on plant communities, identifying general trends such as increased productivity, decreased plant richness, and changes in plant chemistry. However, regions such as the Mediterranean ecoregion (e.g., southern Europe), and several subtropical and tropical parts of South America have not received enough attention in terms of nutrient effect on plants. Furthermore, knowledge on nutrient enrichment cascading effect on higher trophic levels, including on pollinators, is lacking worldwide. This thesis’ main objective is to assess the simultaneous effects of multiple nutrient addition treatments on pollinator assemblages and link them to changes in plant community composition, flower abundance and floral rewards (pollen quantity and quality). To achieve this, we used experimental sites from the Nutrient Network (NutNet – a coordinated research network of grassland sites implementing standardized nutrient addition treatments) and combined: i) a local approach (using an ongoing nutrient manipulation field experiment located in a Mediterranean grassland in Portugal) to assess nutrient enrichment effects on floral rewards, and its effect on pollinators, and on plant-pollinator interacting patterns. ii) a large scale approach (using data from 14 ongoing nutrient manipulation field experiments) to understand the effects of nutrient enrichment on different flowering plant and pollinator communities spread across three continents (in Europe and in North and South America), and to assess the effect of soil fertility and temperature on nutrient enrichment effect on plants and pollinators. Using the local approach, we detected contrasting effects on flower abundance of three co-flowering dominant plant species (Crepis capillaris, Raphanus raphanistrum and Echium plantagineum), with NP enrichment increasing flower abundance while P enrichment decreased it. Nutrient enrichment effects on pollen quantity and quality in terms of amino acids were plant species-specific, with strong, medium and weak effects on the three species. Phosphorus enrichment had a positive effect on Raphanus visitation rate at the flower scale driven by an increase in amino acid concentration, but a negative effect on pollinator visitation rate (considering the whole plant community) at plot level, due to a general reduction in flower abundance. On the other hand, plant-pollinator foraging patterns were affected by NP and P enrichment and the interaction networks: i) NP enrichment was associated with an increase in pollinator diversity and plant generality, resulting in higher network generalization; and ii) P enrichment was associated with a decrease in pollinator diversity, with those visitors showing specialized foraging patterns, increasing network specialization. Using the large-scale approach, we found that regional temperature and soil fertility interacted with nutrient enrichment, mainly N enrichment (and also P enrichment), modulating the effect on plant and on pollinator diversity. In warmer regions, the effect of N enrichment was negative on plant and pollinator diversity, while it was positive in colder regions. Moreover, plant richness response was stronger on poor soils while flower abundance response was stronger on rich soils. Pollinator response to nutrient enrichment was more accentuated than plant response. This thesis’ results clearly show that nutrient enrichment is an important driver of floral resource availability, with bottom-up effects on pollinators. Data from our local approach show that NP enrichment may improve floral resources (flower abundance and pollen quantity and quality) in a Mediterranean grassland with positive effects on pollinator diversity; while the addition of P alone was related to negative effects on floral abundance, which negatively affected pollinator visitation rate and pollinator diversity. Besides affecting plant-pollinator diversity, we showed that nutrient enrichment affected pollinator foraging patterns, promoting network generalization (NP enrichment) or specialization (P enrichment). Changes in network generalization patterns could affect community tolerance to future perturbations. Data from our large-scale approach show that pollinators are particularly at risk in warmer regions, which are usually biodiversity hotspots and contribute greatly to global food production. Ongoing global warming in addition to the increasing use of these regions for intensive agriculture could compromise crop pollination and food supply if policies aiming at controlling farming intensity (including nutrient loads) are not implemented. Overall, this thesis provides crucial information regarding the effects of nutrient enrichment on pollinator assemblages, through the study of the different pathways through which nutrient-driven changes in plants may impact pollinators. In order to better understand the effects of nutrient enrichment on plants, and especially on pollinators, future research should prioritize understudied regions and include a wider range of plant and pollinator species in community-level studies.
ABSTRACT: Insect pollinators are declining worldwide, with agricultural intensification as one of the main drivers. Besides land-use changes (including landscape and ecosystem simplification), and a massive use of pesticides, agricultural intensification is associated with elevated nutrient inputs or nutrient enrichment, which is a major threat to global biodiversity. In the last decades, studies mostly from temperate northern hemisphere regions enabled understanding the effects of nutrient enrichment on plant communities, identifying general trends such as increased productivity, decreased plant richness, and changes in plant chemistry. However, regions such as the Mediterranean ecoregion (e.g., southern Europe), and several subtropical and tropical parts of South America have not received enough attention in terms of nutrient effect on plants. Furthermore, knowledge on nutrient enrichment cascading effect on higher trophic levels, including on pollinators, is lacking worldwide. This thesis’ main objective is to assess the simultaneous effects of multiple nutrient addition treatments on pollinator assemblages and link them to changes in plant community composition, flower abundance and floral rewards (pollen quantity and quality). To achieve this, we used experimental sites from the Nutrient Network (NutNet – a coordinated research network of grassland sites implementing standardized nutrient addition treatments) and combined: i) a local approach (using an ongoing nutrient manipulation field experiment located in a Mediterranean grassland in Portugal) to assess nutrient enrichment effects on floral rewards, and its effect on pollinators, and on plant-pollinator interacting patterns. ii) a large scale approach (using data from 14 ongoing nutrient manipulation field experiments) to understand the effects of nutrient enrichment on different flowering plant and pollinator communities spread across three continents (in Europe and in North and South America), and to assess the effect of soil fertility and temperature on nutrient enrichment effect on plants and pollinators. Using the local approach, we detected contrasting effects on flower abundance of three co-flowering dominant plant species (Crepis capillaris, Raphanus raphanistrum and Echium plantagineum), with NP enrichment increasing flower abundance while P enrichment decreased it. Nutrient enrichment effects on pollen quantity and quality in terms of amino acids were plant species-specific, with strong, medium and weak effects on the three species. Phosphorus enrichment had a positive effect on Raphanus visitation rate at the flower scale driven by an increase in amino acid concentration, but a negative effect on pollinator visitation rate (considering the whole plant community) at plot level, due to a general reduction in flower abundance. On the other hand, plant-pollinator foraging patterns were affected by NP and P enrichment and the interaction networks: i) NP enrichment was associated with an increase in pollinator diversity and plant generality, resulting in higher network generalization; and ii) P enrichment was associated with a decrease in pollinator diversity, with those visitors showing specialized foraging patterns, increasing network specialization. Using the large-scale approach, we found that regional temperature and soil fertility interacted with nutrient enrichment, mainly N enrichment (and also P enrichment), modulating the effect on plant and on pollinator diversity. In warmer regions, the effect of N enrichment was negative on plant and pollinator diversity, while it was positive in colder regions. Moreover, plant richness response was stronger on poor soils while flower abundance response was stronger on rich soils. Pollinator response to nutrient enrichment was more accentuated than plant response. This thesis’ results clearly show that nutrient enrichment is an important driver of floral resource availability, with bottom-up effects on pollinators. Data from our local approach show that NP enrichment may improve floral resources (flower abundance and pollen quantity and quality) in a Mediterranean grassland with positive effects on pollinator diversity; while the addition of P alone was related to negative effects on floral abundance, which negatively affected pollinator visitation rate and pollinator diversity. Besides affecting plant-pollinator diversity, we showed that nutrient enrichment affected pollinator foraging patterns, promoting network generalization (NP enrichment) or specialization (P enrichment). Changes in network generalization patterns could affect community tolerance to future perturbations. Data from our large-scale approach show that pollinators are particularly at risk in warmer regions, which are usually biodiversity hotspots and contribute greatly to global food production. Ongoing global warming in addition to the increasing use of these regions for intensive agriculture could compromise crop pollination and food supply if policies aiming at controlling farming intensity (including nutrient loads) are not implemented. Overall, this thesis provides crucial information regarding the effects of nutrient enrichment on pollinator assemblages, through the study of the different pathways through which nutrient-driven changes in plants may impact pollinators. In order to better understand the effects of nutrient enrichment on plants, and especially on pollinators, future research should prioritize understudied regions and include a wider range of plant and pollinator species in community-level studies.
Description
Tese de Doutoramento, Biologia, 23 de maio de 2025, Universidade dos Açores.
Keywords
Recursos florais Pradaria Conjunto de insetos polinizadores Enriquecimento em nutrientes Interações planta-polinizador Fertilidade do solo Temperatura
Pedagogical Context
Citation
VALLEJO, Juan Pablo Cancela. (2024). "Pollinator assemblage response to nutrient enrichment in grasslands". Ponta Delgada: Universidade dos Açores, 2024. 169 p. Tese de Doutoramento em Biologia. Disponível em http://hdl.handle.net/10400.3/8762