Michael Heethoff

Molecular phylogeny of oribatid mites (Oribatida, Acari): evidence for multiple radiations of parthenogenetic lineages

Nucleotide sequences of the D3 expansion segment and its flanking regions of the 28S rDNA gene were used to evaluate phylogenetic relationships among representative sexual and asexual oribatid mites (Oribatida, Acariformes). The aim of this study was to investigate the hypothesis that oribatid mites consist of species rich clusters of asexual species that may have radiated while being parthenogenetic. Furthermore, the systematic position of the astigmate mites (Astigmata, Acariformes) which have been hypothesised to represent a paedomorphic lineage within the oribatid mites, is investigated. This is the first phylogenetic tree for oribatid mites s.1. (incl. Astigmata) based on nucleotide sequences. Intraspecific genetic variation in the D3 region was very low, confirming the hypothesis that this region is a good species marker. Results from neighbour joining (NJ) and maximum parsimony (MP) algorithms indicate that several species rich parthenogenetic groups like Camisiidae, Nanhermanniidae and Malaconothridae are monophyletic, consistent with the hypothesis that some oribatid mite groups diversified despite being parthenogenetic. The MP and maximum likelihood (ML) method indicated that the D3 region is a good tool for elucidating the relationship of oribatid mite species on a small scale (genera, families) but is not reliable for large scale taxonomy because branches from the NJ algorithm collapsed in the MP and ML tree. In all trees calculated by different algorithms the Astigmata clustered within the oribatid mites, as proposed earlier.

Radiation in sexual and parthenogenetic oribatid mites (Oribatida, Acari) as indicated by genetic divergence of closely related species

The D3 domain and its flanking regions of 28S rRNA of four pairs of closely related sexual species (Eupelops hirtus and E. torulosus; Oribatella calcarata and O. quadricornuta; Chamobates voigtsi and Ch. borealis; Liacarus coracinus and L. subterraneus) and four pairs of closely related parthenogenetic species (Nanhermannia nana and Na. coronata; Nothrus silvestris and No. palustris; Tectocepheus sarekensis and T. minor; Camisia spinifer and Ca. segnis) of oribatid mites were sequenced to investigate (1) if the D3 region can be used as a species marker and (2) if there is genetic variation among closely related species pairs and if its magnitude is related to reproductive mode. Furthermore, we investigated the world-wide genetic variation of the D3 region from the oribatid mite species Platynothrus peltifer. There was no intraspecific genetic variation in the D3 region in any of the species studied; it was even identical in two closely related parthenogenetic species (Na. nana and Na. coronata) and two closely related sexual species (E. hirtus and E. torulosus). The genetic differences of the other species pairs indicated that both parthenogenetic and sexual lineages have various ages. On average, however, the differences between the closely related parthenogenetic species were larger than those between closely related sexual species, indicating that parthenogenetic lineages exist historically and may radiate slower than sexual species. The findings of this study support the hypothesis that some of the parthenogenetic oribatid mite taxa (Tectocepheus, Nothrus) are ‘ancient asexuals’. The absence of intraspecific or intra-individual variation in the D3 region of parthenogenetic species is consistent with the presence of concerted evolution in the 28S rRNA gene. From this we infer the existence of a meiotic process, which is consistent with the automixy known from several other parthenogenetic oribatid species.

Tasty but Protected—First Evidence of Chemical Defense in Oribatid Mites

Oribatid mites (Acari, Oribatida) represent one of the most abundant and speciose groups of microarthropods in the decomposer food webs of soils, but little is known of their top-down regulation by predators. Oribatids are relatively long-lived and have numerous morphological defensive adaptations, and so have been proposed to live in ‘enemy-free space’. Most also possess a pair of large exocrine oil glands that produce species-specific mixtures of hydrocarbons, terpenes, aromatics, and alkaloids with presumably allomonal functions, although their adaptive value has never been tested empirically. We developed a protocol that discharges the oil glands of the model oribatid species, Archegozetes longisetosus. and offered ‘disarmed’ individuals as prey to polyphagous Stenus beetles (Staphylinidae), using untreated mites as controls. Stenus juno fed on disarmed mites with behavioral sequences and success rates similar to those observed when they prey on springtails, a common prey. In contrast, mites from the control group with full glands were almost completely rejected; contact with the gland region elicited a strong reaction and cleaning behavior in the beetle. This is the first evidence of an adaptive value of oribatid mite oil gland secretions for chemical defense. The protocol of discharging oil glands should facilitate future studies on top-down control of oribatid mites that aim to differentiate between morphological and chemical aspects of defensive strategies.

Oribatid mites and skin alkaloids in poison frogs

A recent publication in Biology Letters added a new family, Eleutherodacytlidae, to the list of frogs known to possess defensive, toxic alkaloids in their skin—the so-called ‘poison frogs’ [[1][1]]. The alkaloids have attracted much attention since they are not synthesized by frogs de novo,

Expanding the ‘enemy-free space’ for oribatid mites: evidence for chemical defense of juvenile Archegozetes longisetosus against the rove beetle Stenus juno

Adult oribatid mites are thought to live functionally in ‘enemy-free space’ due to numerous morphological and chemical defensive strategies. Most juvenile oribatid mites, however, lack hardened cuticles and are thus thought to be under stronger predation pressure. On the other hand, the majority of oribatids have exocrine oil glands in all developmental stages, possibly rendering chemical defense the crucial survival strategy in juvenile Oribatida. We manipulated tritonymphs of the model oribatid mite Archegozetes longisetosus to completely discharge their oil glands and offered these chemically disarmed specimens to the polyphagous rove beetle Stenus juno. Disarmed specimens were easily consumed. By contrast, specimens with filled oil glands were significantly protected, being rejected by the beetles. This is the first direct evidence that oil gland secretions provide soft-bodied juvenile oribatids with chemical protection against large arthropod predators.

Surface area–volume ratios in insects

Body mass, volume and surface area are important for many aspects of the physiology and performance of species. Whereas body mass scaling received a lot of attention in the literature, surface areas of animals have not been measured explicitly in this context. We quantified surface area–volume (SA/V) ratios for the first time using 3D surface models based on a structured light scanning method for 126 species of pollinating insects from 4 orders (Diptera, Hymenoptera, Lepidoptera, and Coleoptera). Water loss of 67 species was measured gravimetrically at very dry conditions for 2 h at 15 and 30 °C to demonstrate the applicability of the new 3D surface measurements and relevance for predicting the performance of insects. Quantified SA/V ratios significantly explained the variation in water loss across species, both directly or after accounting for isometric scaling (residuals of the SA/V ∼ mass2/3 relationship). Small insects with a proportionally larger surface area had the highest water loss rates. Surface scans of insects to quantify allometric SA/V ratios thus provide a promising method to predict physiological responses, improving the potential of body mass isometry alone that assume geometric similarity.

Storage and release of hydrogen cyanide in a chelicerate (Oribatula tibialis)

Significance Hydrogen cyanide (HCN) is highly volatile and among the most toxic substances known, being lethal to humans at a dosage of 1–2 mg/kg body weight. HCN blocks the respiratory chain and prevents aerobic organisms from using oxygen. In nature, HCN is produced by numerous plants that store it mainly as glycosides. Among animals, cyanogenesis is a defensive strategy that has seemed restricted to a few mandibulate arthropods (certain insects, millipedes, and centipedes), which evolved ways to store HCN in the form of stable and less volatile molecules. We found an instance of cyanogenesis in the phylogenetically distant group Chelicerata (“spider-like” arthropods), involving an aromatic ester for stable HCN storage and two degradation pathways that release HCN. Cyanogenesis denotes a chemical defensive strategy where hydrogen cyanide (HCN, hydrocyanic or prussic acid) is produced, stored, and released toward an attacking enemy. The high toxicity and volatility of HCN requires both chemical stabilization for storage and prevention of accidental self-poisoning. The few known cyanogenic animals are exclusively mandibulate arthropods (certain myriapods and insects) that store HCN as cyanogenic glycosides, lipids, or cyanohydrins. Here, we show that cyanogenesis has also evolved in the speciose Chelicerata. The oribatid mite Oribatula tibialis uses the cyanogenic aromatic ester mandelonitrile hexanoate (MNH) for HCN storage, which degrades via two different pathways, both of which release HCN. MNH is emitted from exocrine opisthonotal oil glands, which are potent organs for chemical defense in most oribatid mites.

Reducible defence: chemical protection alters the dynamics of predator–prey interactions

Morphological and chemical defences are widespread anti-predator mechanisms in most domains of life, and play an important role in understanding predator–prey interactions. Classical concepts of dynamical protection (‘inducible defence’) include the morphological changes in certain crustaceans or the production of chemicals in many plants. Permanently stored defensive secretions are, to our knowledge, ignored in food web ecology. We show that this kind of chemical defence is highly dynamic and may loose its effect over time (‘reducible defence’). Combining experimental and theoretical approaches, we show that chemical defence also changes the time budget of predators and decreases the strength of the functional response. However, this may be counteracted by increasing predator density—an effect we call ‘apparent facilitation’. The interplay of ‘reducible defence’ and ‘apparent facilitation’ may substantially contribute to stability in terrestrial ecosystems.

Triggering chemical defense in an oribatid mite using artificial stimuli

Most oribatid mites are well known for their exocrine oil gland secretions, from which more than a hundred different chemical components (hydrocarbons, terpenes, aromatics and alkaloids) have been described. The biological functions of these secretions have remained enigmatic for most species, but alarm-pheromonal and allomonal functions have been hypothesized, and demonstrated in some cases. Here, we tested different experimental stimuli to induce the release of defensive secretions in the model oribatid mite Archegozetes longisetosus Aoki. Whereas various mechanical stimuli did not result in a reproducible and complete expulsion of oil gland secretions, repeated treatments with hexane led to complete discharge. Life history parameters such as survival, development and reproduction were not influenced by the hexane treatment. Repeated hexane treatments also resulted in a complete depletion of oil glands in Euphthiracarus cribrarius Berlese.

Scent of a mite: origin and chemical characterization of the lemon-like flavor of mite-ripened cheeses.

Cheese infested with cheese mites is usually treated as unpalatable. Nevertheless, some traditional cheese manufactories in Germany and France intentionally use mites for fermentation of special varieties (i.e. Milbenkäse and Mimolette). While their production includes different mite species, both are characterized by a “lemon-like” flavor. However, the chemical nature and origin of this flavor-component is unknown. The cheese mites possess a pair of opisthosomal glands producing blends of hydrocarbons, terpenes and aromatics. Here, we describe the chemical profiles of the astigmatid mite species Tyrolichus casei (Milbenkäse) and Acarus siro (Mimolette). Although the chemical profiles differ in several aspects, both mite species produce neral (a volatile flavor component of lemon oil), which was absent from the headspace of both cheeses without mites. We conclude that the lemon-like flavor of mite cheese is not a consequence of fermentation of the cheese itself but a component from secretions of the cheese mites.