Fatal attraction: Male spider mites prefer females killed by the mite-pathogenic fungus Neozygites floridana

Abstract

Exploring prospective mates can be risky. Males of the spider mite Tetranychus urticae approach and guard immobile (quiescent) female nymphs to increase their chances of fathering offspring, this being a first-male sperm priority species. We investigated the behaviour of male T. urticae towards females killed by the mite pathogenic fungus Neozygites floridana, letting them choose between a fungal killed and a healthy quiescent female. The dead female (called cadaver) was in one of three stages: (1) non-sporulating; (2) sporulating with primary conidia (non-infective); (3) surrounded/partly covered by secondary capilliconidia (infective). When the cadaver was in stage 1 or 2, males were significantly more often observed near the cadaver than near the healthy female. When the cadaver was in stage 3 (infective capilliconidia), males preferred the vicinity of healthy females. The frequency of two male behaviours, touching and guarding, was also recorded. Touching the cadaver tended to decrease as cadaver developed, whereas touching the healthy females increased. Guarding of non-sporulating cadavers and healthy females was equally common, while guarding of sporulating cadavers was only observed once (stage 2) or not at all (stage 3). To differentiate between the effect of fungal infection and sex, we also let males choose between a non-sporulating cadaver of each sex. Males then preferred to approach the female cadaver. Touching behaviour followed the same pattern, and guarding of male cadavers was not observed. Our results indicate that T. urticae males are more attracted to non-infective female cadavers than to healthy females, only detecting their mistake when very close. Moreover, males approach and explore cadavers surrounded by infective conidia. Whether the results of host manipulation by the pathogen or just sensory constraints in the host, this inability to detect unsuitable and indeed infective mates promotes transmission of the pathogen.

Keywords: Behaviour; Mate choice; Neozygites floridana; Pathogen transmission; Tetranychus urticae; Two-spotted spider mite.