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Egg Maturation, Oviposition, and Longevity of the Gall Midge Rhopalomyia Californica (Diptera: Cecidomyiidae)

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Egg Maturation, Oviposition, and Longevity of the Gall Midge Rhopalomyia Californica (Diptera: Cecidomyiidae) ARTHROPOD BIOLOGY Portrait of an Ephemeral Adult Stage: Egg Maturation, Oviposition, and Longevity of the Gall Midge Rhopalomyia californica (Diptera: Cecidomyiidae) JAY A. ROSENHEIM,1 SARINA J. JEPSEN, CHRISTOPHER E. MATTHEWS, DAVID SOLANCE SMITH, AND MICAH R. ROSENHEIM Department of Entomology, University of California, Davis, CA 95616 Ann. Entomol. Soc. Am. 100(4): 549Ð561 (2007) ABSTRACT Insect reproduction is typically spread out in time and space, making estimates of lifetime reproductive success quite difÞcult under natural Þeld conditions. Such estimates are, however, critical to providing rigorous tests of theory for reproductive behavior. One approach to circumventing this problem is to study insects whose lifetime reproduction is compressed in space and time, and whose ovarian dynamics (oogenesis, oosorption, and oviposition) are simpliÞed. We investigated the gall midge Rhopalomyia californica Felt (Diptera: Cecidomyiidae) as a possible candidate for an herbivore with such a simpliÞed pattern of lifetime reproduction. We demonstrate here that R. californica matures all of its eggs before adult eclosion (it is strictly proovigenic), and it does not resorb eggs, even when deprived of oviposition sites. Observational and experimental studies in the Þeld demonstrate that this midge typically completes its entire lifetime reproduction in a single day: females usually emerge at dawn, mate, and after a posteclosion period of resting, they initiate a sustained period of active oviposition during which most eggs are laid over a 4Ð5-h period. Mean longevity of adult females is very short, consistently Ͻ1 d and only 5Ð6 h on clear and warm days. Two key aspects of senescence are experimentally demonstrated: an increase in mortality rates and a decrease in oviposition rates with age. The life history traits associated with the ephemeral adult stage of R. californica are consistent with a syndrome that has been characterized recently for many proovigenic herbivorous and parasitic insects. Proovigenic species, including R. californica, may be particularly valuable as model systems for studies of lifetime reproductive success in nature. KEY WORDS life history, proovigeny, oosorption, oviposition, senescence Insect herbivores and parasitoids have been used ex- Asplen and Byrne 2006). Ongoing oogenesis can be tensively as model systems for developing theory in fueled by an array of foods available to ovipositing behavioral and evolutionary ecology, in part because adults, including feeding on nectar, pollen, honeydew, they are relatively easy to study in the laboratory fruit juices, and, for parasitoids, their hosts (“host (Price 1980, Godfray 1994, Wajnberg 2006). Often, feeding”; OÕBrien et al. 2002; Casas et al. 2003, 2005). however, rigorous tests of theoretical predictions re- Oviposition and oosorption have very different impli- quire estimates of reproductive costs and beneÞts in cations for female Þtness increments, despite produc- nature, rather than in the artiÞcial laboratory envi- ing identical changes in the oocyte inventory. These ronment. Such estimates have proven to be difÞcult to ovarian dynamics mean that for most insects it is not obtain (for reviews, see Casas 2000, Casas et al. 2004) possible to estimate lifetime reproductive success for at least two reasons. First, reproduction by indi- from simple dissections. Point estimates of oviposition vidual female herbivores and parasitoids is usually rates may be possible in some cases (e.g., Tatar 1991, spread out over time and space, making it difÞcult to Visser 1994, Casas et al. 2000), but only for insects that sum across an individualÕs lifetime. Second, many do not demonstrate senescence (accelerating mortal- adult insects have relatively complex processes of ity rates or decelerating oviposition rates with age; ovarian dynamics, with mature egg inventories in- Tatar 2001) can point estimates easily be translated creasing through ongoing oogenesis, which may occur into lifetime estimates of reproduction. at highly variable rates (Papaj 2000, 2005), and with One possible means of ameliorating these problems inventories decreasing through either oviposition or is to study insects that exhibit the traits that typify oosorption (Bell and Bohm 1975, Rivero-Lynch and herbivores or parasitoids, but whose range of repro- Godfray 1997, Papaj 2000, Rosenheim et al. 2000, ductive activity is compressed in time and space, mak- ing lifetime estimates more tractable. Insects with 1 Corresponding author, e-mail: [email protected]. temporally compressed reproduction are, further- 0013-8746/07/0549Ð0561$04.00/0 ᭧ 2007 Entomological Society of America 550 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 100, no. 4 more, more likely to exhibit simpliÞed ovarian dynam- suggesting that female longevity is generally Ͻ2Ð3 d ics. Both empirical and theoretical analyses suggest and that females are weak ßyers (Hopper 1984, Ehler that very short-lived arthropods are more likely to be and Kinsey 1993, Palmer et al. 1993, Latto and Briggs strictly proovigenic, with egg maturation occurring 1995, Miller and Weis 1999, Briggs and Latto 2000). during the pupal stage rather than the adult stage. The Tilden (1951) furthermore observed that the mouth- ability to resorb mature oocytes also may often be parts and gut are reduced and may be nonfunctional, lacking in species with short-lived adults (Jervis et al. and no authors have recorded feeding behavior by the 2005). When egg maturation and resorption are adults. Field experiments have demonstrated that known to be absent, we can estimate realized indi- most reproduction occurs within a few meters of the vidual lifetime reproduction from a simple dissection site of female emergence (Briggs and Latto 2000). R. of females at the end of their lives (Jepsen et al. 2007). californica, like many cecidomyiid midges, does seem, The goal of this study was to develop a quantitative therefore, to concentrate its lifetime reproduction in picture of the behavior, longevity, and oocyte dynam- a small time and space. Although nothing has been ics (egg maturation, resorption, and oviposition) for reported on egg maturation by this midge, or egg the gall midge Rhopalomyia californica Felt (Diptera: resorption for this or any other midge, the suggestion Cecidomyiidae), to determine whether this species that adults may not feed makes it more likely that egg might be valuable as a model organism for studies of maturation might occur before adult eclosion (Jervis lifetime reproductive success in nature. We also et al. 2005). sought to evaluate what we considered an unlikely The speciÞc questions that we addressed were as possibility, namely, that there are no age-dependent follows. What is the timing of R. californica reproduc- increases in mortality rates or decreases in oviposition tion on a seasonal and daily basis? Does R. californica rates, to see whether point estimates of reproductive mature or resorb eggs during the adult stage? How success could be projected directly to lifetime esti- long does R. californica live in the Þeld? What is the mates. R. californica induces terminal multichamber daily pattern of R. californica behavior in nature? Does bud galls on its sole host plant Baccharis pilularis De R. californica feed during the adult stage? and Does R. Candolle (Asteraceae), a dominant native shrub dis- californica show accelerating mortality rates or decel- tributed along coastal California and Oregon, with erating oviposition rates as they age (two aspects of some inland populations extending across CaliforniaÕs senescence)? Central Valley and into the foothills of the Sierra Nevada (Gagne and Boldt 1995). R. californica seemed ´ Materials and Methods to be a good candidate for several reasons. First, R. californica is a member of the family Cecidomyiidae, Study Site. Our main study site was located just many of whose members are known to be extremely north of the University of California G. Ledyard Steb- short-lived (Gagne´ 1989, 1994; Yukawa and Rohfritsch bins Cold Canyon Preserve and just east and south of 2005). For example, several Rhopalomyia spp. associ- the conßuence of Cold Creek and Putah Creek (38Њ ated with sagebrush, Artemisia tridentata Nutt., seem 30.71Ј N, 122Њ 5.76Ј W). The site, Ϸ50 by 200 m, was to have Þeld longevities of Ͻ1 d, emerging at dawn and subject to both natural and anthropogenic distur- becoming difÞcult to Þnd by mid-day (Jones et al. bance, and it was characterized by a broken pine and 1983). The family Cecidomyiidae includes some spe- oak overstory and a shrubby understory dominated by cies whose egg maturation seems to occur gradually Baccharis pilularis and Toxicodendron diversilobum during the adult stage (“synovigeny”), including both (Torr. & Gray Greene). gall-inducing herbivores (Pivnick and Labbe´ 1993) Phenology. Although coastal populations of R. cali- and predatory taxa (Havelka and Zemek 1999, Mo and fornica reproduce actively year-round, inland popu- Liu 2006). Nevertheless, most gall inducers are de- lations like the population that we studied are asso- scribed as proovigenic (Miller and Borden 1984, Har- ciated with host plants that may cease vegetative ris and Rose 1989, Hinz 1998, Harris et al. 2003, Yukawa growth during the dry and very hot summer; inland and Rohfritsch 2005), although in most cases rigorous midge populations therefore seem to peak in density demonstrations are lacking. Oosorption has, to our during the late winter and early spring, when rainfall knowledge, never
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