Compensatory growth and costs of molluscivory in Gambusia holbrooki

Some prey are exceptionally difficult to digest, and yet even non-specialized animals may consume them—why? Durophagy, the consumption of hard-shelled prey, is thought to require special adaptations for crushing or digesting the hard shells to avoid the many potential costs of this prey type. But many animals lacking specializations nevertheless include hard-bodied prey in their diets. We describe several non-mutually exclusive adaptive mechanisms that could explain such a pattern, and point to optimal foraging and compensatory growth as potentially having widespread importance in explaining costly-prey consumption. We first conducted a literature survey to quantify the regularity with which non-specialized teleost fishes consume hard-shelled prey: stomach-content data from 325 teleost fish species spanning 82 families (57,233 stomach samples) demonstrated that non-specialized species comprise approximately 75% of the total species exhibiting durophagy, commonly consuming hard-shelled prey at low to moderate levels (~10–40% as much as specialists). We then performed a diet survey to assess the frequency of molluscivory across the native latitudinal range of a small livebearing fish, Gambusia holbrooki, lacking durophagy specializations. Molluscivory was regionally widespread, spanning their entire native latitudinal range (> 14° latitude). Third, we tested for a higher frequency of molluscivory under conditions of higher intraspecific resource competition in Bahamian mosquitofish (Gambusia spp.). Examining over 5,300 individuals, we found that molluscivory was more common in populations with higher population density, suggesting that food limitation is important in eliciting molluscivory. Finally, we experimentally tested in G. holbrooki whether molluscivory reduces growth rate and whether compensatory growth follows a period of molluscivory. We found that consumption of hard-shelled gastropods results in significantly reduced growth rate, but compensatory growth following prior snail consumption can quickly mitigate growth costs. Our results suggest that the widespread phenomenon of costly-prey consumption may be partially explained by its relative benefits when few alternative prey options exist, combined with compensatory growth that alleviates temporary costs.

Methods
Laboratory experiment examining growth rate of Gambusia holbrooki over a 17-day period, including a snail-feeding period (hard [with shells] and soft [without shells] treatments) and a flake-feeding (recovery) period to test for growth costs of consuming hard-shelled molluscs, as well as compensatory growth following the period of molluscivory.

部分猎物极难消化，但即便非特化动物亦会取食此类猎物——其背后的原因是什么？硬食性（Durophagy），即取食带硬壳的猎物，通常被认为需要特化的适应结构以压碎或消化硬壳，从而规避这类猎物带来的诸多潜在代价。但许多缺乏此类特化结构的动物仍会将硬体猎物纳入自身食谱。我们阐述了数种非互斥的适应性机制，可解释这一现象，并指出最优觅食与补偿性生长或许在解释“取食高代价猎物”的现象中具有广泛的重要性。
我们首先开展了一项文献调研，以量化非特化硬骨鱼类取食硬壳猎物的普遍程度：涵盖82个科的325种硬骨鱼类的胃容物数据（共57233份胃样本）显示，非特化物种约占表现出硬食性行为的物种总数的75%，它们通常以低至中等的水平取食硬壳猎物，其取食量约为特化物种的10%~40%。
随后我们开展了一项食谱调研，以评估一种缺乏硬食性特化结构的小型胎生鱼类——食蚊鱼（Gambusia holbrooki）——在其自然分布纬度范围内的食软体动物性（Molluscivory）发生频率。结果显示食软体动物性行为在区域内广泛分布，覆盖了其整个自然纬度范围（跨度超过14°纬度）。
第三，我们在巴哈马食蚊鱼（Gambusia spp.）中测试了在种内资源竞争更高的条件下，食软体动物性的发生频率是否更高。通过对超过5300条个体的检测，我们发现种群密度更高的群体中食软体动物性行为更为常见，这表明食物限制在诱发食软体动物性行为中发挥了重要作用。
最后，我们对食蚊鱼（G. holbrooki）开展了实验，以验证取食硬壳猎物是否会降低生长速率，以及食软体动物行为之后是否会出现补偿性生长。我们发现，取食带壳腹足类动物会显著降低生长速率，但此前取食螺类后的补偿性生长可快速缓解生长代价。我们的研究结果表明，取食高代价猎物的广泛现象，或许可部分通过“当缺乏其他替代猎物时取食此类猎物的相对收益”，结合缓解临时代价的补偿性生长来解释。

研究方法
实验室实验：对食蚊鱼（Gambusia holbrooki）开展为期17天的生长速率观测实验，设置螺类取食阶段（分硬壳[带壳]与软质[去壳]处理组）以及薄片饲料（flake）恢复期，以验证取食硬壳软体动物的生长代价，以及食软体动物行为后的补偿性生长。