Abstract The defense strategy of an insect toward natural enemies can include a trait that appears at first sight to contradict its defensive function. We explored phylogeny, chemistry, and defense efficiency of a peculiar group of hymenopteran sawfly larvae where this contradiction is obvious. Pseudodineurini larvae live in leaf mines that protect them from some enemies. Disturbed larvae also emit a clearly perceptible lemon-like odor produced by ventral glands, although the mine hampers the evaporation of the secretion. The mine could also lead to autointoxication of a larva by its own emitted volatiles. Citral was the major component in all Pseudodineurini species, and it efficiently repels ants. We conclude that full-grown larvae that leave their mine to pupate in the soil benefit from citral by avoiding attacks from ground-dwelling arthropods such as ants. In some species, we also detected biosynthetically related compounds, two 8-oxocitral diastereomers (i.e., (2E,6E)- and (2E,6Z)-2,6-dimethylocta-2,6-dienedial). Synthetic 8-oxocitral proved to be a potent fungicide, but not an ant repellent. The discrete distribution of 8-oxocitral was unrelated to species grouping in the phylogenetic tree. In contrast, we discovered that its presence was associated with species from humid and cold zones but absent in species favoring warm and dry environments. The former should be protected by 8-oxocitral when faced with a fungal infestation while crawling into the soil. Our work shows the importance of integrating knowledge about behavior, morphology, and life history stages for understanding the complex evolution of insects and especially their defense strategies.
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Subterranean ecosystem biodiversity is characterized by a unique combination of four features that may account for its patterns and fluctuations at a global scale: (1) a low number of lineages due to environmental harshness, (2) a high proportion of endemic species as a result of habitat fragmentation and isolation, (3) a high level of relict taxa, best explained by the relative stability and antiquity of the habitat compared with most superficial habitats, and (4) food webs that are truncated at both the bottom (no primary producers) and the top (few or no predators and no specialized ones). In this review, we present a synthesis of the current state of knowledge of groundwater oligochaetes, and we investigate in what extent their biodiversity meets these criteria. The present knowledge is strongly biased in favour of the West-Palaearctic region, in particular the karst of Southern Europe. While our understanding of groundwater biodiversity in Europe and the United States has gained much during these last decades, many areas are undersampled in the world. To date, more than 300 nominal species have been found in ground waters all over the world (on about 1,700 and 1,100 aquatic and freshwater oligochaete species, respectively). Most of these species should be considered as incidentals or waifs; however, about one-third of them are found exclusively in this environment (stygobionts). Among the 21 families that are fully aquatic or include species occurring in aquatic habitats, 16 families are present in ground water. Stygobiont species belong to only 7 different families, harbouring 42 genera among which 17 are represented by a single species. Thirty-four per cent of the species are representatives of only two genera: Trichodrilus (Lumbriculidae) and Rhyacodrilus (Naididae). With 9 species, all being stygobiont, the Parvidrilidae is unique in being the only family, worldwide, comprising taxa that are restricted to groundwater habitats. Data on the distribution of stygobiont oligochaetes suggest pronounced endemism, nearly 60% of the species being known only from their type locality. The origins of subterranean oligochaete biodiversity probably involve multiple and successive colonization processes, both from marine and freshwater environments. The current distribution of Parvidrilidae, Rhyacodriloides (Rhyacodriloidinae), Delaya (Haplotaxidae), or species belonging to primarily marine genera, may be explained when assuming that these species are palaeoendemics or relicts, namely survivors of an old fauna that has long since become extinct in the surrounding areas. Aquatic oligochaetes appear to be pre-adapted to live in the subterranean environment. In the absence of genuine troglomorphic characters, their stygobiotic status can only be inferred from their exclusive presence in the subterranean environment. Valuable studies to enhance knowledge of subterranean aquatic oligochaetes will probably take more advantage of investigating adaptations that enable them to face scarceness of food and oxygen in groundwater, rather than focussing on an uncertain quest for morphological adaptations. Promising approaches would be to compare related hypogean and epigean species within the same genus, such as in Trichodrilus and Rhyacodrilus, or ecosystems the most similar to the underground such as lake hypolimnia and the deep sea. Keywords: ground water, Clitellata, biodiversity, patterns, endemism, relictuality, adaptation.
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