Tales from the crypt: a parasitoid manipulates the behaviour of its parasite host

Abstract

There are many examples of apparent manipulation of host phenotype by parasites, yet few examples of hypermanipulation—where a phenotype-manipulating parasite is itself manipulated by a parasite. Moreover, few studies confirm manipulation is occurring by quantifying whether the host's changed phenotype increases parasite fitness. Here we describe a novel case of hypermanipulation, in which the crypt gall wasp Bassettia pallida (a phenotypic manipulator of its tree host) is manipulated by the parasitoid crypt-keeper wasp Euderus set, and show that the host's changed behaviour increases parasitoid fitness. Bassettia pallida parasitizes sand live oaks and induces the formation of a ‘crypt’ within developing stems. When parasitized by E. set, B. pallida adults excavate an emergence hole in the crypt wall, plug the hole with their head and die. We show experimentally that this phenomenon benefits E. set, as E. set that need to excavate an emergence hole themselves are about three times more likely to die trapped in the crypt. In addition, we discuss museum and field data to explore the distribution of the crypt-keeping phenomena.

A keeper of many crypts: a behaviour-manipulating parasite attacks a taxonomically diverse array of oak gall wasp species

“…Two recent papers [5,6] describe the discovery and life history of the parasitoid stem, where the developing larval wasp will then feed and grow. Unparasitized adult B. pallida later chew a small exit hole in their gall-made of woody plant material-and then fly away.…”

A keeper of many crypts: the parasitoidEuderus setmanipulates the behavior of a taxonomically diverse array of oak gall wasp species

“…These examples were from museum specimens, which were not destructively sampled to confirm the presence of Euderus within the gall. They also report evidence of head-plugging in an unidentified cynipid on Q. nigra in southeast Texas [17], that has since been keyed to genus Bassettia (possibly B. aquaticae; A.A.F. unpublished data).…”

“…For the five other non-Bassettia gall wasp species from which Euderus emerged in the lab, we inspected post-emergence galls for evidence of head plugs, chewed heads, or other signs of hypermanipulation previously described in the B. pallida / E. set interaction [17].…”

“…Two recent papers [16,17] describe the discovery and life history of the parasitoid "crypt keeper wasp" (Euderus set), so named because of its parasitism and behavioral manipulation of the "crypt-gall wasp" (Bassettia pallida) in live oaks (Quercus virginiana & Q. geminata). Oviposition by a B. pallida female into a young stem induces the formation of a swollen internal gall (known as a "crypt") inside the stem, where the developing larval wasp will then feed and grow.…”

“…The parasitoid communities of most oak gall wasps are understudied or unknown such that it is premature to assert that the manipulation of B. pallida by E. set is a unique relationship. Indeed, Weinersmith et al [17] report additional examples of "head plugging" in the gall wasp Bassettia ligni on the host plants Q. lobata and Q. douglasii. These examples were from museum specimens, which were not destructively sampled to confirm the presence of Euderus within the gall.…”