Tewksbury Joshua J, Levey Douglas J, Huizinga Meribeth, Haak David C, Traveset Anna
Department of Biology, 106 Kincaid Hall, Box 351800, University of Washington, Seattle, Washington 98195, USA
Ecology. 2008 Jan;89(1):107-17. doi: 10.1890/07-0445.1.
A fundamental way in which animal-dispersed plants can influence the viability and distribution of dispersed seeds is through control of retention time in the guts of dispersers. Using two species of wild chilies and their dispersers, we examined how chemical and physical properties of fruits and seeds mediate this interaction. Capsicum chacoense is polymorphic for pungency, occurs in Bolivia, and is dispersed mostly by elaenias. Capsicum annuum is not polymorphic, occurs in Arizona (USA), and is dispersed mostly by thrashers. We first tested whether capsaicin, the substance responsible for the pungency of chilies, affects gut retention time of seeds in primary dispersers. Capsaicin slowed gut passage of seeds but did so in a manner that differed greatly between bird species because the constipative effects of capsaicin occurred only after an 80-minute time lag. Elaenias in Bolivia held only 6% of C. chacoense seeds for > 80 minutes, whereas thrashers in Arizona held 78% of C. annuum seeds for > 80 minutes. Next we examined the effects of retention time on seed viability and germination. Increased retention resulted in a greater proportion of seeds germinating in C. annuum, had no effects on non-pungent C. chacoense, and had negative effects on pungent C. chacoense. These divergent effects are explained by differences in seed coat morphology: seed coats of pungent C. chacoense are 10-12% thinner than those of the other two types of seeds. Thus, longer retention times damaged seeds with the thinnest seed coats. In C. annuum, seed viability remained high regardless of retention time, but germination increased with retention, suggesting a role for scarification. Thus, in C. annuum, fruit chemistry appears well matched with seed morphology and disperser physiology: capsaicin extends gut retention for most seeds, resulting in greater seed scarification and higher germination rates. Increased retention of pungent C. chacoense seeds is detrimental, but because the primary consumers have short retention times, capsaicin slows only a small proportion of seeds, minimizing negative effects. These results illustrate the importance of context in studies of fruit secondary metabolites. The same chemical can have different impacts on plant fitness depending on its morphological, physiological, and ecological context.
动物传播的植物影响传播种子的活力和分布的一种基本方式是通过控制种子在传播者肠道中的停留时间。我们使用两种野生辣椒及其传播者，研究了果实和种子的化学和物理特性如何介导这种相互作用。查科辣椒（Capsicum chacoense）的辣味具有多态性，生长在玻利维亚，主要由艾氏雀鹎传播。一年生辣椒（Capsicum annuum）没有多态性，生长在美国亚利桑那州，主要由嘲鸫传播。我们首先测试了导致辣椒辣味的辣椒素是否会影响种子在主要传播者肠道中的停留时间。辣椒素减缓了种子在肠道中的通过速度，但不同鸟类物种的反应差异很大，因为辣椒素的致便秘作用仅在80分钟的时间滞后才出现。玻利维亚的艾氏雀鹎只有6%的查科辣椒种子停留超过80分钟，而亚利桑那州的嘲鸫有78%的一年生辣椒种子停留超过80分钟。接下来，我们研究了停留时间对种子活力和发芽的影响。停留时间增加导致一年生辣椒中有更大比例的种子发芽，对不辣的查科辣椒没有影响，而对辣的查科辣椒有负面影响。这些不同的影响可以通过种皮形态的差异来解释：辣的查科辣椒的种皮比其他两种种子的种皮薄10 - 12%。因此，较长的停留时间会损坏种皮最薄的种子。在一年生辣椒中，无论停留时间如何，种子活力都保持较高，但发芽率随停留时间增加，这表明存在擦伤作用。因此，在一年生辣椒中，果实化学似乎与种子形态和传播者生理学非常匹配：辣椒素延长了大多数种子在肠道中的停留时间，导致更大程度的种子擦伤和更高的发芽率。辣的查科辣椒种子停留时间增加是有害的，但由于主要消费者的停留时间短，辣椒素只会减缓一小部分种子的速度，将负面影响降至最低。这些结果说明了背景在果实次生代谢物研究中的重要性。相同的化学物质根据其形态、生理和生态背景，对植物适合度可能有不同的影响。
