Department of Entomology, University of Arizona, Tucson, AZ, United States of America.
Department of Science, University of Roma Tre, Rome, Italy.
PLoS One. 2019 Jan 16;14(1):e0209790. doi: 10.1371/journal.pone.0209790. eCollection 2019.
The carabid subfamily Paussinae contains many species known to be obligately associated with ants during at least one stage of their life history. Myrmecophilous larvae have been documented for members of the tribe Paussini as well as several genera in the tribes Ozaenini, including Physea and Eustra. Here we describe the first instar larva of Ozaena lemoulti, and find it to be the most highly modified ozaenine larva that we have examined to date. Many structures of the larva suggest that it is a myrmecophile. Unlike all other described ozaenine larvae, which live in burrows that they construct and seal with their terminal disk, the completely unique larval morphology suggests Ozaena has adapted to living without the protection of a burrow and therefore must have a completely different feeding strategy than the typical ambush strategy of burrow dwelling larvae. We hypothesize that Ozaena larvae live in association with ants and use their long legs for running within the nest, and modifications of the mouthparts suggest the larva feeds on soft lightly sclerotized prey, such as ant brood. Our findings support an earlier hypothesis that Ozaena is mymecophilous during the adult stage. Comparisons of the functional anatomy of the eggs, larvae and adult between Ozaena lemoulti and the closely related, non-myrmecophilous general arthropod predator, Goniotropis kuntzeni, provide complementary, yet independent, evidence suggestive of this shift in lifestyle. We also examine and molecularly identify gut contents, providing direct evidence that adult Ozaena exclusively eat Camponotus ants. We conclude that Ozaena represents an independent shift to adopting a life of myrmecophily among beetles classified within the carabid subfamily Paussinae and document the morphological changes at each life history stage associated with the shift to a nest parasite lifestyle.
步甲亚科 Paussinae 包含许多种已知在其生命史的至少一个阶段与蚂蚁强制性相关联的物种。有记录表明,在 Paussini 部落以及 Ozaenini 部落的几个属中,包括 Physea 和 Eustra,都存在拟蚁幼虫。在这里,我们描述了 Ozaena lemoulti 的第一龄幼虫,并发现它是我们迄今为止研究过的最高度特化的拟蚁幼虫。幼虫的许多结构表明它是一种拟蚁。与所有其他描述的拟蚁幼虫不同,后者生活在它们用末端盘密封的挖掘洞穴中,而完全独特的幼虫形态表明 Ozaena 已经适应了没有洞穴保护的生活,因此必须具有与典型的洞穴居住幼虫的伏击策略完全不同的喂养策略。我们假设 Ozaena 幼虫与蚂蚁生活在一起,并利用它们的长腿在蚁巢内奔跑,而口器的修改表明幼虫以软而轻度硬化的猎物为食,例如蚂蚁幼虫。我们的发现支持了早期的假设,即 Ozaena 在成虫阶段是拟蚁。Ozaena lemoulti 与密切相关的非拟蚁性一般节肢动物捕食者 Goniotropis kuntzeni 之间的卵、幼虫和成虫的功能解剖比较提供了互补但独立的证据,表明这种生活方式的转变。我们还检查并分子鉴定了肠道内容物,提供了直接证据表明成年 Ozaena 只吃 Camponotus 蚂蚁。我们得出结论,Ozaena 代表了在分类为步甲亚科的甲虫中独立转变为拟蚁生活方式的一个例子,并记录了与转变为巢寄生生活方式相关的每个生命史阶段的形态变化。