Climatic conditions and functional traits affect spider diets in agricultural and non-agricultural habitats worldwide

Spiders are dominant predators in terrestrial ecosystems and feed on prey from the herbivore and detritivore subsystem (dual subsystem omnivory) as well as on other predators (intraguild predation). Little is known about how global change potentially affects the importance of different prey groups in predator diets. In this meta-analysis we identify the impact of climatic conditions, land-use types and functional traits of spider species on the relative importance of Hemiptera, Araneae and Collembola prey in spider diets. We use a dataset including 78 publications with 149 observational records of the diet composition of 96 spider species in agricultural and non-agricultural habitats in 24 countries worldwide. The importance of Hemiptera prey was not affected by climatic conditions and was particularily high in smaller spider species in agricultural habitats. Araneae prey was most important for actively hunting, larger spider species in non-agricultural habitats. Collembola prey was most important for small, actively hunting spider species in regions with higher temperature seasonality. Spider species with a higher importance of Araneae prey for their diet also had higher importances of Collembola and lower importances of Hemiptera prey. Future increases of temperature seasonality predicted for several regions worldwide may go along with an increasing importance of Collembola prey which also related to a higher importance of intraguild prey here. Two global change drivers predicted for many regions of the world (increasing climatic seasonality and ongoing conversion of non-agricultural to agricultural land) both hold the potential to increase the importance of Collembola prey in spider diets. The importance of Hemiptera and Araneae prey may however show contrasting responses to these two drivers. These complex potential effects of global change components and their impact on functional traits in spider communities highlight the importance to simultaneously consider multiple drivers of global change to better understand future predator-prey interactions.

Methods
This study is based on a global database about the diet composition of hunting and web-building spider species in natural ecosystems used in Birkhofer and Wolters (2012) with the addition of data from agricultural ecsoystems and updates from Diehl et al. (2013b), Michalko & Pekár (2015a), Arvidsson et al. (2020) and Mezőfi et al. (2020). All data in the original publications are derived by direct visual records of prey or prey remains in spider species in field studies, not including data from molecular or experimental studies. Note that only subsets of data from the original database from non-agricultural (82 cursorial and web-building spider species in natural habitats: Birkhofer & Wolters 2012) or only for web-building spiders (63 spider species in agricultural, natural and forest habitats: Birkhofer et al. 2018) were previously published. The database includes 118 unique publications that reported 310 datasets about diet compositions in individual spider species worldwide. All datasets that were based on fewer than 20 recorded prey items per spider species in individual studies or did address spider species in forest habitats were excluded for this study. The selection of a minimum of 20 records was based on the fact that spiders in each study could theoretically reach the maximum diet breadth, including prey from all 20 prey orders that were originally recorded across datasets (see Birkhofer & Wolters 2012). The selection of non-forest habitats was based on the aim to compare habitats that share a major structural characteristic by not being dominated by dense, natural tree cover. Forests further have a very different invertebrate community compared to grasslands and arable fields (e.g. Birkhofer et al. 2015), which would limit a comparison of diets between major habitat types. The remaining 78 publications provided 149 datasets on the diet composition of 96 spider species worldwide (Figure 1). This database was used to calculate the relative contribution of each prey order to the overall diet in each dataset as percentage value. The percentages of Hemiptera, Collembola and Araneae prey were then extracted to reflect the relative contribution of these prey orders to the diet of individual spider species.

蜘蛛是陆地生态系统中的优势捕食类群，其取食对象既涵盖植食性与腐食性亚系统（双亚系统杂食性）的猎物，也包括其他捕食者（集团内捕食（intraguild predation））。目前学界对全球变化如何影响不同猎物类群在捕食者食谱中的相对重要性仍知之甚少。本元分析（meta-analysis）旨在厘清气候条件、土地利用类型以及蜘蛛物种功能性状，对半翅目（Hemiptera）、蜘蛛目（Araneae）和弹尾目（Collembola）三类猎物在蜘蛛食谱中的相对重要性的影响。本研究整合了全球24个国家农业与非农业生境中96种蜘蛛的食谱组成数据，共包含78项已发表研究、149条观测记录。

半翅目猎物的重要性不受气候条件影响，且在农业生境中的小型蜘蛛物种中尤为突出。蜘蛛目猎物对非农业生境中主动猎食的大型蜘蛛物种而言最为重要。弹尾目猎物在温度季节性更高区域的小型主动猎食蜘蛛物种的食谱中占比最高。食谱中蜘蛛目猎物占比更高的蜘蛛物种，其弹尾目猎物占比也更高，而半翅目猎物占比则更低。

未来全球多个区域预计出现的温度季节性升高现象，可能伴随弹尾目猎物在蜘蛛食谱中重要性的提升，而这类区域的集团内捕食猎物的重要性也会相应升高。全球变化的两大驱动因子——日益增强的气候季节性与非农业生境向农业生境的持续转化——均有可能提升弹尾目猎物在蜘蛛食谱中的重要性。但半翅目与蜘蛛目猎物的重要性对这两类驱动因子的响应可能截然相反。全球变化各组分的潜在复杂效应及其对蜘蛛群落功能性状的影响，凸显了同时考量多重全球变化驱动因子的必要性，以更深入地理解未来捕食者-猎物相互作用。

方法
本研究基于伯克霍夫与沃尔特斯（Birkhofer and Wolters, 2012）中使用的、关于自然生态系统中狩猎型与结网型蜘蛛物种食谱组成的全球数据库，并补充了来自农业生态系统的数据，以及迪尔等人（Diehl et al., 2013b）、米哈尔科与佩卡尔（Michalko & Pekár, 2015a）、阿尔维德松等人（Arvidsson et al., 2020）和梅佐菲等人（Mezőfi et al., 2020）的更新数据。原始已发表研究中的所有数据均来自野外研究中对蜘蛛体内猎物或猎物残体的直接目视记录，未纳入分子或实验研究的数据。需注意的是，原始数据库中仅部分数据曾被发表：要么来自非农业生境（自然生境中的82种游走型与结网型蜘蛛物种，Birkhofer & Wolters 2012），要么仅针对结网型蜘蛛（农业、自然与森林生境中的63种蜘蛛物种，Birkhofer et al. 2018）。本数据库共包含118篇已发表文献，报道了全球范围内310组关于单个蜘蛛物种食谱组成的数据集。本研究排除了两类数据集：单篇研究中单个蜘蛛物种的记录猎物数量少于20项的数据集，以及针对森林生境蜘蛛物种的数据集。设定20项记录的下限，是基于理论上每项研究中的蜘蛛可覆盖所有20个曾在各数据集记录的猎物目级类群的最大食谱宽度（详见Birkhofer & Wolters 2012）。排除森林生境则是为了比较具有主要结构特征共性的生境，即不受密集自然林木覆盖主导的生境。相较于草原与耕地，森林的无脊椎动物群落组成差异极大（例如Birkhofer et al. 2015），若纳入森林生境将限制主要生境类型间的食谱对比。最终筛选得到的78项已发表研究，共提供了全球范围内96种蜘蛛的149组食谱组成数据集（图1）。本数据库被用于计算各猎物目在单组数据集总食谱中的相对占比（以百分比计）。随后提取半翅目、弹尾目与蜘蛛目猎物的百分比占比，以反映这三类猎物在单个蜘蛛物种食谱中的相对贡献。