BIOLOGICALCONTROL Habitat Diversification for Improving Biological Control: Abundance of Anagrus epos (Hymenoptera: Mymaridae) in Grape Vineyards BROOK C. MURPHY, JAY A. ROSENHEIM, ANDJEFFREY GRANETT Department of Entomology, Universityof California, Davis, CA 95616 Environ. Entomol. 25(2): 495-504 (1996) ABSTRACT A frequently cited habitat diversificationtactic is the use of prune tree refuges that support overwintering populations of Anagrus epos (Girault), a mymarid egg parasite of the western grape leafhopper, Erythroneura elegantula Osborn, in vineyards.Here we test the effect of prune trees on early-season abundance of adult A. epos in vineyards. A. epos was found in vineyards downwind of prune trees at more than twice the densities of vineyards lackingpnllle trees, despite significantvariation in A. epos immigration from sources outside the pnme tree-vineyard system. Densities of A. epos overwintering within prune trees ex- plained a significantamount of the variationin A. epos trap capture in vineyards.Furthermore, another factor associated with prune trees was found to influence A. epos abundance in vine- yards: a windbreak effect created by the prune trees concentrated dispersing A. epos on the leeward side of the prune trees, tllereby further enhancing A. epos numbers. KEY WORnS Anagrus epos, Erythroneura elegantula, habitat diversification,conservation biologicalcontrol, grape HABITATDIVERSIFICATIONHASlong been promot- Altieri 1992), most studies have been qualitative ed as a tactic to conserve natural enemies and en- rather than quantitative in nature. Furthermore, hance biological control of insect pests and as a there are no current tactics that have been widely integrated method of developing sustainable pest adopted for pest control in production agriculture. control systems in production agriculture. Both ap- Here, we test and examine the ecological mecha- proaches argue that habitat diversification can pro- nisms associated with prune tree habitats planted vide essential resources for natural enemies, such adjacent to grape vineyards on a key natural enemy as feeding sites, alternate hosts or prey, or over- species. wintering sites, that can enhance their abundance Anagrus epos-Erythroneura elegantula System. in the surrounding environment and help prevent A frequently cited example used to illustrate the pest outbreaks (Herzog and Funderburk 1985, Na- effect of habitat diversification on natural enemy tional Research Council 1989, van Emden 1990, effectiveness is the planting of overwintering hab- Altieri 1992). itats for Anagrus epos (Girault) near grape vine- Whether viewed as a biological control tactic or yards to enhance biological control of the western as an integrated approach to sustainable pest con- grape leafhopper, Erythroneura elegantula Os- trol, habitat diversification in or around crop fields born. can have a profound effect on how insect herbivore Erythroneura elegantula is a major pest of and nahlral enemy populations interact. An under- grapes in many regions of the western United standing of the ecological mechanisms involved States. High leafhopper numbers result in eco- will also provide a rich resource for the develop- nomic losses caused by cosmetic damage to grape lIlent of pest management tactics in production ag- berries from leafhopper frass, reduced vine vigor riculture (Herzog and Funderburk 1985). from heavy leaf feeding and leaf loss, and fruit One of the key hypotheses underlying the con- damage from sun exposure. Furthermore, high cept of habitat diversification is that many pest densities of adult leafhoppers can disrupt harvest problems are the result of a loss of habitat critical by flying into the eyes, nose, and mouth of field for supporting natural enemy populations (Letour- laborers. neau 1987, Russell 1989, Andow 1991). Although A key natural enemy of the grape leafhopper is the ecological basis behind habitat diversification A. epos, an important egg parasite of E. elegantula and natural enemy effectiveness has been dis- as well as other leafhopper species (Gordh and cllssed for many years, and many proposed systems Dunbar 1977, Williams 1984). A. epos has been have been evaluated in a preliminary way (re- reported to parasitize a significant proportion of E. viewed by Flint and Roberts 1988, Russell 1989, elegantula eggs within commercial vineyards 0046-225X196/0495-0504$02.00/0 © 1996 Entomolngical Society of America 496 ENVIRONMENTAL ENTOMOLOCY Vol. 25, no. 2 (Doutt and Nakata 1973). A major h1ctor hypoth- A. epos in vineyards or by examining E. elegantula esized to be associated with the abundance and eggs and comparing rates of egg parasitism. Col- effectiveness of A. epos is the presence of nearby onization appeared to be enhanced in vineyards habitat that supports alternate leafhopper hosts downwind from prune orchards or riparian habi- (Doutt and Nakata 1965, 1973). A. epos overwin- tats containing blackberry brambles. They con- ters within leafhopper eggs. E. elegantula overwin- cluded that the greater abundance seen in field ters as an adult, thus, an alternate source of leaf- trials supported the overwintering refuge hypoth- hopper eggs is required to support overwintering esis. However, because these initial experiments A. epos numbers. used unreplicated comparisons, the results, al- Doutt and Nakata (1965) first observed that though consistent with the refuge hypothesis, were vineyards located downwind from riparian habitats preliminary in nature. had higher levels of E. elegantula egg parasitism The interpretation presented by Doutt and Nak- and lower E. elegantula numbers relative to vine- ata (1973) and Kido et a1.(1984) also rested on an yards located distant from these' habitats. They untested assumption; namely, that an increase in found that blackberry brambles, Rubus spp., abun- parasite captures or egg parasitism near refuges dant in riparian habitats, support Dikrella eaZifor- was the direct result of A. epos emergence from niea (Lawson), a year-round host of A. epos. They overwintering sites. A 2nd potential mechanism observed that early spring emergence of A. epos that could explain increased parasite captures from blackberry results in earlier vineyard coloni- downwind of prune trees or trees found in riparian zation by parasites, which coincided with oviposi- habitats is a windbreak effect generated by the tion of overwintered E. elegantula. They also spec- physical structure of these habitats. A windbreak ulated that earlier vineyard colonization at higher effect occurs when a structural barrier creates hlr- densities produced a stronger numerical response bulence in the airflow and a sheltered zone on the and thereby improved biological control (Doutt leeward side of the barrier. The turbulent airflow and Nakata 1973). Unfortunately, field trials deter- may act to increase the probability that a dispers- mined blackberry brambles grown away from ri- ing insect will settle into these sheltered zones, parian habitats did not maintain abundant popu- thereby enhancing colonization. Dispersing insects lations of A. epos, and further attempts were from many families, including wasps in the family abandoned (Flal1erty et al. 1985). Mymaridae, have been shown to accumulate be- Kido et at. (1984) demonstrated that prune trees hind windbreaks (Lewis and Stephenson 1966). support the prune leafhopper, Edwardsiana prun- Wilson et a1. (1989) showed that A. epos reach ieola (Edwards), which overwinters in the egg higher densities in pnmes when artificial wind- stage and serves as an overwintering host for A. breaks are positioned on the upwind side of prune epos. Emergence of overwintering A. epos from trees. Corbett and Rosenheim (in press) have also overwintering E. prunieola eggs laid beneath the recently demonstrated a pattern of A. epos cap- bark of prune twigs also was found to coincide with tures in vineyards downwind of pnme trees that is 1st-generation E. elegantula oviposition in vine- consistent with the operation of a windbreak. Thus, yards, suggesting that pnme trees also serve as an enhanced A. epos abundance could be the result overwintering habitat for A. epos. Studies in both of overwintering populations within the prune commercial and experimental plantings of pnille trees, a windbreak effect, or some combination of trees demonstrated that A. epos populations could those 2 factors. be supported year-round. Williams (1984) and In the current shldy, we tested 2 key hypotheses Kido et al. (1984) also showed that A. epos reared with respect to the effect of overwintering sites on from E. prunieola or D. ealifomiea can parasitize A. epos abundance in vineyards as follows: (1) that E. elegant1.l1aeggs successfully, and vice versa. Fi- prune trees adjacent to vineyards enhance early- nally, it has been shown that elevated A. epos pop- season A. epos numbers in vineyards, and (2) that ulations were associated with higher E. elegant1.l1a differences in abundance are the result of differ- egg parasitism in vineyards near pnme trees (Kido ences in the densities of overwintering A. epos et al. 1984, Pickett et aI. 1990). Although these emerging from pnme trees. In addition to those 2 studies established the basic framework of the hypotheses, we also analyzed capture data for ev- grape leafhopper-A. epos interaction, there have idence of a windbreak effect influencing A. epos been no replicated field trials that assess the effi- abundance downwind of pnme trees. cacy of prune tree habitats or that test the ecolog- ical mechanisms underlying