Maternal effects in zooplankton consumers are not only mediated by direct but also by indirect effects of phosphorus limitation

Nutrient limitation of primary producers has repeatedly been shown to negatively affect consumers, directly through stoichiometric mismatch and indirectly via alterations in the producer's biochemical quality or palatability. In this study, we assessed whether direct and indirect impacts of phosphorus-limitation on a planktonic consumer are transferred to the next generation via maternal effects and whether these effects reflect an anticipatory adaptive strategy. For this, we subjected cultures of the algivorous monogonont rotifer Brachionus calyciflorus to three food quality treatments, i.e. P-limited (LP), P-replete (HP) and P-enriched LP algae (i.e. algae with an LP-growth history but with molar C:P ratios equal to those of HP-algae). After two generations, we subjected offspring of these cultures to each of the three food quality treatments and monitored life history traits. In addition, we tested starvation resistance. Our results showed very strong negative maternal effects of low P food on offspring performance. These negative effects prevailed irrespective of contemporary diets, suggesting transmissive and selfish maternal effects rather than anticipatory adaptive effects. The relative strength of direct and indirect maternal P-limitation effects varied among different traits. Adult body size was predominantly determined by direct effects of P-shortage in maternal as well as contemporary food (LP < LP+P and LP+P = HP). In contrast, whereas egg size was negatively affected by direct effects of P-limitation in the maternal diet, a contemporary diet of LP and LP+P algae resulted in larger eggs than HP algae. Animals born from such larger eggs showed no higher growth rates, but they were more resistant to starvation, likely as the result of higher maternal allocation of energy rich molecules to the eggs. The present study shows that maternal food conditions represent an important factor that should be taken into account in studies of stoichiometric mismatch between producers and consumers.

初级生产者（primary producers）的养分限制已被反复证实会对消费者（consumers）产生负面影响，既通过化学计量错配（stoichiometric mismatch）直接施加作用，也可通过改变初级生产者的生化品质（biochemical quality）或适口性（palatability）间接产生效应。本研究旨在探究磷限制对浮游消费者（planktonic consumer）的直接与间接影响是否可通过母体效应（maternal effects）传递至子代，以及此类效应是否属于预期性适应策略。为此，我们将食藻单巢轮虫萼花臂尾轮虫（Brachionus calyciflorus）的培养种群设置3种食物质量处理组：磷限制组（LP）、磷充足组（HP），以及磷富集的磷限制藻类组（即具备磷限制生长历史，但摩尔碳磷比与磷充足藻类相当的藻类）。经过两代培养后，将各处理组的子代种群分别暴露于3种食物质量处理环境中，监测其生活史特征（life history traits），并检测抗饥饿能力（starvation resistance）。研究结果显示，低磷食物对子代适合度存在极强的负面母体效应。此类负面效应不受当代食物环境的影响，表明其属于传递性且自私的母体效应，而非预期性适应效应。直接与间接的母体磷限制效应的相对强度因不同性状而异：成体体型主要由母体及当代食物中的磷缺乏直接决定（LP组 < LP+P组，且LP+P组与HP组无显著差异）。与之相反，尽管卵大小会因母体食物的磷限制直接作用而减小，但当代投喂LP与LP+P藻类时，子代卵的尺寸反而大于HP组。由大卵孵化出的个体并未表现出更高的生长速率，但其抗饥饿能力更强，这可能源于母体向卵中投入了更多富含能量的分子。本研究表明，母体的食物环境是生产者与消费者间化学计量错配研究中不可忽视的重要因素。