From seed dispersal service to reproductive collapse: density-dependent outcome of a palm-mammal interaction

Interspecific ecological interactions are inherently context-dependent. They may vary in both magnitude and sign depending on the biotic and abiotic conditions, depicting a mutualism-antagonism continuum. However, how population abundances and the activity of interacting species modulate these interactions remains underexplored. Here, we chose the interaction between the Mediterranean palm Chamaerops humilis and the feral goat Capra hircus in Mallorca (Balearic Islands, Spain). We selected three study plots with low, intermediate and high intensities of goat activity where we characterized palm distribution, seed rain, seed predation, and early palm recruitment during two consecutive years. Since goats can cause both costs (e.g. florivory) and benefits (e.g. seed dispersal) to C. humilis performance, we investigated the following three questions: (1) Does the spatial distribution of adult palms vary depending on the intensity of goat activity? (2) Does the intensity of goat activity influence seed rain and its potential spatial association with adult palms? (3) To what extent does the intensity of goat activity determine post-dispersal events such as seed predation and seedling emergence? We found that adult palms showed a more clumped and complex distribution (double-cluster process) in plots with low and intermediate goat activity compared to that with high goat activity (simple-cluster process). In the low goat activity plot, dispersed seeds were spatially aggregated around adult palms, showing twice insect-seed predation and nearly three times lower seed germination success than those in the intermediate goat activity plot. Palm seed dispersal and recruitment were almost nil in the high goat activity plot due to heavy consumption of palm inflorescences and developing fruits by goats. Our findings demonstrate how the net outcome of plant-animal interactions can change from mutualism to antagonism, from reproductive service to reproductive collapse, depending on the abundance and the activity of the interacting species.

Methods
To evaluate the hypothesis that the outcome of the palm-goat interaction depends on the intensity of goat activity, we first described the spatial distribution of C. humilis by geo-referencing in 2019 (with a Garmin GPSMAP) all adult palms within each study plot. Then, we searched for dispersed seeds in two consecutive years (2019 and 2020) from September to December, which covered the entire seed dispersal seasons of C. humilis. Every dispersed unit (defined as one dispersed seed or a group of dispersed seeds) was geo-referenced as an independent point and covered with a wire 1-cm mesh cage (10 x 10 x 9 cm) to prevent seed predation, seed removal and seedling trampling by vertebrates. (e.g. Fedriani and Wiegand 2014). GPS coordinates were then imported into a geographic information system (Quantum GIS Team 2023). Caged dispersed seeds were checked every two months up to January 2022 (i.e. two years after the end of the first sampling season) to record seed predation by scolytine beetles, seed germination, seedling emergence, and seedling survival. Then, we used recent extensions of spatial point pattern analyses (SPPA, hereafter; Wiegand and Moloney 2014, Velázquez et al. 2016, Ben-Said 2021) to explore the data. Specifically, to characterize the spatial distribution of adult palms and seed rain (question 1) we fitted univariate cluster point process models to the data, whereas to analyze the spatial association between adult palms and dispersed units (question 2) we employed bivariate pair correlation functions together with realizations of the spatial independence null model. Finally, to detect spatial patterns of seed predation and to test the Janzen-Connell hypothesis (question 3) we used mark connection functions and trivariate mark correlation functions together with the random labeling null model.

种间生态相互作用本质上依赖于环境背景，其强度与作用性质（即互利或拮抗）会随生物和非生物条件发生变化，构成了互利-拮抗连续体。然而，种群丰度与互作物种的活动如何调控这类相互作用，目前仍未得到充分研究。
本研究以西班牙巴利阿里群岛马略卡岛上的地中海矮棕（Chamaerops humilis）与野山羊（Capra hircus）的互作关系为研究对象。我们选取了3个野山羊活动强度分别为低、中、高的研究样地，在连续两年间对棕榈的空间分布、种子雨、种子捕食以及棕榈早期定植情况进行了调查。鉴于野山羊既能对矮棕产生生存代价（如花食行为），也能带来生存益处（如种子传播），我们围绕以下三个问题展开研究：（1）成年矮棕的空间分布是否随野山羊活动强度的变化而改变？（2）野山羊活动强度是否会影响种子雨及其与成年矮棕的潜在空间关联？（3）野山羊活动强度在多大程度上调控扩散后事件，如种子捕食与幼苗出土？
研究结果显示，与高野山羊活动强度样地的单簇空间分布模式相比，低、中活动强度样地内的成年矮棕呈现出更聚集且复杂的双簇空间分布模式。在低活动强度样地中，扩散的种子在成年矮棕周围呈空间聚集状态，其昆虫种子捕食率是中活动强度样地的2倍，种子萌发成功率则比中活动强度样地低近2/3。在高活动强度样地中，由于野山羊大量取食矮棕的花序与发育中的果实，其种子传播与定植过程几乎完全终止。本研究结果证实，动植物互作的净效应可随互作物种的丰度与活动强度发生变化，从互利转向拮抗，从繁殖服务走向繁殖崩溃。

研究方法
为验证“棕榈与野山羊的互作结果依赖于野山羊活动强度”这一假说，我们首先于2019年使用佳明（Garmin）GPSMAP手持GPS对每个研究样地内的所有成年矮棕进行地理定位，以刻画其空间分布特征。随后，在2019年与2020年连续两年的9月至12月（覆盖矮棕完整的种子扩散季）开展种子收集调查。每一个扩散单元（定义为1粒分散种子或一簇分散种子）均被作为独立点位进行地理定位，并使用1 cm网孔的金属笼（10 × 10 × 9 cm）进行覆盖，以防止脊椎动物对种子的捕食、移除以及幼苗被踩踏（改编自Fedriani与Wiegand 2014）。随后将GPS坐标导入地理信息系统（Quantum GIS Team 2023）。从首次采样季结束后至2022年1月，我们每两个月对笼内的扩散种子进行1次检查，以记录小蠹虫对种子的捕食、种子萌发、幼苗出土以及幼苗存活情况。
我们采用近年发展的空间点格局分析（SPPA，以下简称SPPA；Wiegand与Moloney 2014，Velázquez等2016，Ben-Said 2021）方法对数据进行处理。具体而言，针对问题1（成年矮棕与种子雨的空间分布），我们对数据拟合单变量簇状点过程模型；针对问题2（成年矮棕与扩散单元的空间关联），我们采用双变量成对相关函数结合空间独立零模型的随机模拟结果进行分析；针对问题3（检测种子捕食的空间模式并检验詹森-康奈尔（Janzen-Connell）假说），我们使用标记连接函数与三元标记相关函数，并结合随机标记零模型开展检验。