Oviposition strategies of conifer seed chalcids in relation to host phenology

Abstract

Insects are considered the most important predators of seed cones, the female reproductive structures of conifers, prior to seed dispersal. Slightly more than 100 genera of insects are known to parasitize conifer seed cones. The most diverse (i.e., number of species) of these genera is Megastigmus (Hymenoptera: Torymidae), which comprises many important seed pests of native and exotic conifers. Seed chalcids, Megastigmus spp., lay eggs inside the developing ovules of host conifers and, until recently, oviposition was believed to occur only in fertilized ovules. Ovule development begins just after pollination, but stops if cells are not fertilized. The morphological stage of cone development at the time of oviposition by seed chalcids has been established for many species; however, knowledge of ovule development at that time has been documented for only one species, M. spermotrophus. Megastigmus spermotrophus oviposits in Douglas-fir ovules after pollination but before fertilization. Unlike the unfertilized ovules, those containing a M. spermotrophus larva continue to develop, whether fertilized or not, stressing the need to broaden our understanding of the insect-plant interactions for this entire genus. To achieve this task, we reviewed the scientific literature and assembled information pertaining to the timing of oviposition and to the pollination and fertilization periods of their respective host(s). More specifically, we were searching for circumstantial evidence that other species of Megastigmus associated with conifers could behave (i.e., oviposit before ovule fertilization) and impact on female gametophyte (i.e., prevent abortion) like M. spermotrophus. The evidence from our compilation suggests that seed chalcids infesting Pinaceae may also oviposit before ovule fertilization, just like M. spermotrophus, whereas those infesting Cupressaceae seemingly oviposit after ovule fertilization. Based on this evidence, we hypothesize that all species of Megastigmus associated with Pinaceae can oviposit in unfertilized ovules, whereas those exploiting Cupressaceae cannot, and thus oviposit only in already fully developed fertilized seeds. Furthermore, we predict that the presence of a larva in unfertilized ovules of all Pinaceae will influence the development of the female gametophyte by preventing its abortion. This influence on the Pinaceae can be interpreted as an ability to parasitize any of the potential seeds present in a seed cone, and as such represents a much more efficient oviposition strategy than searching and locating only fertilized seeds. Concomitantly, this ability has likely led to an overestimation of the impact of the species of seed chalcid infesting Pinaceae on seed production.

Selective oviposition in fertilized seed of Ilex integra by the wasp Macrodasyceras hirsutum (Hymenoptera: Torymidae)

“…In gymnosperms (conifers), such as Abies balsamea (L.) Miller, Juniperus phoenicea L. and Pinus contorta Douglas ex Loudon, it takes from one month to one year for pollen to fertilize ovules after pollination. Therefore, parasitoid wasps may oviposit into both pollinated and unpollinated ovules that cannot be distinguished from one another at the time of oviposition (Rouault et al, 2004). Once fertilization has occurred, unpollinated ovules usually quickly degenerate but if they contain wasp larva they do not degenerate and even accumulate energy reserves, as is the case when Megastigmus spermotrophus Wachtl (Hymenoptera: Torymidae) larvae are present in unfertilized ovules of Douglas fir (Pseudotsuga menziesii (Mirbel) Franco) (von Aderkas et al, 2005a, b).…”

“…Once fertilization has occurred, unpollinated ovules usually quickly degenerate but if they contain wasp larva they do not degenerate and even accumulate energy reserves, as is the case when Megastigmus spermotrophus Wachtl (Hymenoptera: Torymidae) larvae are present in unfertilized ovules of Douglas fir (Pseudotsuga menziesii (Mirbel) Franco) (von Aderkas et al, 2005a, b). However, when the seed wasp lays its eggs after the seeds are fertilized they may differentiate between fertilized and unfertilized megagametophytes (Rouault et al, 2004). Rouault et al (2004) hypothesized that selective oviposition and host manipulation by wasps is closely associated with when in a season wasps lay their eggs relative to host reproductive phenology.…”

“…However, when the seed wasp lays its eggs after the seeds are fertilized they may differentiate between fertilized and unfertilized megagametophytes (Rouault et al, 2004). Rouault et al (2004) hypothesized that selective oviposition and host manipulation by wasps is closely associated with when in a season wasps lay their eggs relative to host reproductive phenology. On the other hand, some angiosperms, although costly in terms of resources, have non-viable seeds and/or fruits containing non-viable seeds, which serve as a decoy for seed predators or as a sink for eggs deposited by them, resulting in the increased likelihood of viable seeds surviving to seed dispersal (Zangerl et al, 1991;Traveset, 1993;Ghazoul & Satake, 2009).…”

“…Third, female wasps only oviposit into fertilized seeds. To determine which hypothesis explains the concentra-tion of wasp larvae in developing seeds and in particular to test Rouault et al (2004) hypothesis, the distribution of eggs between fertilized and unfertilized seeds in the field and laboratory immediately after the first period of oviposition, and whether they would oviposit into unfertilized seeds obtained by means of the use of pollen exclusion bags in the field, were investigated. Possible reasons for retaining berries with unfertilized seeds are also discussed.…”

Variation of selfing rate and inbreeding depression among individuals and across generations within an admixed Cedrus population

“…larvae, were observed. As this insect is suspected, in some cases, to induce the development of full seeds from non-pollinated ovules (Rouault et al, 2004), these full sized but infected seeds could not be assigned to either the pollinated or un-pollinated ovule groups. Therefore, we computed the germination rate as the ratio between germinated seeds and the total number of 'healthy' seeds, removing all empty and infected seeds.…”