Fruit secondary metabolites alter the quantity and quality of a seed dispersal mutualism

Plant secondary metabolites are key mechanistic drivers of species interactions. These metabolites have primarily been studied for their role in defense, but they can also have complex consequences for mutualisms, including seed dispersal. Although the primary function of fleshy fruits is to attract seed-dispersing animals, fruits often contain complex mixtures of toxic or deterrent secondary metabolites that can reduce the quantity or quality of seed dispersal mutualisms. Furthermore, because seeds are often dispersed across multiple stages by several dispersers, the net consequences of fruit secondary metabolites for the effectiveness of seed dispersal and ultimately plant fitness are poorly understood. Here, we tested the effects of amides, nitrogen-based defensive compounds common in fruits of the neotropical plant genus Piper (Piperaceae), on seed dispersal effectiveness (SDE) by ants, which are common secondary seed dispersers. We experimentally added amide extracts to Piper fruits both in the field and lab, finding that amides reduced the quantity of secondary seed dispersal by reducing ant recruitment (87%) and fruit removal rates (58% and 66% in the field and lab, respectively). Moreover, amides not only reduced dispersal quantity but also altered seed dispersal quality by shifting the community composition of recruiting ants (notably by reducing the recruitment of the most effective disperser by 90% but having no detectable effect on the recruitment of a cheater species that removes fruit pulp without dispersing seeds). Although amides did not affect the distance ants initially carried seeds, they altered the quality of seed dispersal by reducing the likelihood of ants cleaning seeds (67%) and increasing their likelihood of redispersing seeds outside of the nest (200%). Overall, these results demonstrate that secondary metabolites can alter the effectiveness of plant mutualisms, by both reducing mutualism quantity and altering mutualism quality through multiple mechanisms. These findings present a critical step in understanding the factors mediating the outcomes of seed dispersal and, more broadly, demonstrate the importance of considering how defensive secondary metabolites influence the outcomes of mutualisms surrounding plants.植物次生代谢物（Plant secondary metabolites）是驱动物种相互作用的关键机制驱动因子。既往研究多聚焦于这类代谢物的防御功能，但它们同样会对包括种子传播在内的互利共生关系产生复杂影响。尽管肉质果实的核心功能是吸引传种动物，但果实中往往含有复杂的有毒或驱避性次生代谢物混合物，这类物质会降低种子传播互利共生的规模与质量。此外，由于种子通常会经多个传播者完成多阶段传播，果实次生代谢物对种子传播有效性（seed dispersal effectiveness, SDE）乃至植物适合度（plant fitness）的最终影响仍有待充分阐明。本研究针对新热带植物属胡椒属（Piper，Piperaceae）果实中常见的氮基防御化合物——酰胺类（amides）物质，检验其对作为次级传种者的常见蚂蚁的种子传播有效性的影响。我们在野外与室内实验中向胡椒属植物果实中添加酰胺提取物，结果发现酰胺类物质通过使蚂蚁招募率降低87%、果实移除率分别降低58%与66%（野外与室内实验中），减少了次级种子传播的规模。不仅如此，酰胺类物质不仅降低了传播规模，还通过改变招募蚂蚁的群落组成改变了传播质量：具体而言，其将最高效传播者的招募率降低90%，但对一种会移除果肉却不传播种子的欺骗性物种的招募无显著影响。尽管酰胺类物质未改变蚂蚁初始携带种子的距离，却通过使蚂蚁清理种子的概率降低67%、提升其在巢外再次传播种子的概率200%，改变了种子传播的质量。综上，本研究结果表明，次生代谢物可通过多种机制同时降低互利共生规模与改变互利共生质量，从而影响植物互利共生关系的有效性。该研究为解析介导种子传播结局的关键因子迈出了重要一步，更广泛而言，也凸显了考虑防御性次生代谢物如何影响植物周边互利共生关系的重要性。