Life History Plasticity Magnifies the Ecological Effects of a Social Wasp Invasion
Total Page：16
File Type：pdf, Size：1020Kb
Life history plasticity magnifies the ecological effects of a social wasp invasion Erin E. Wilsona,1, Lynne M. Mullenb, and David A. Holwaya aSection of Ecology, Behavior, and Evolution, Division of Biological Sciences, University of California, San Diego, Mail Code 0116, 9500 Gilman Drive, La Jolla, CA 92093; and bMuseum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, MCZ Labs 215, 26 Oxford Street, Cambridge, MA 02138 Edited by Mary Jane West-Eberhard, Smithsonian Tropical Research Institute, Costa Rica, and approved June 23, 2009 (received for review March 17, 2009) An unresolved question in ecology concerns why the ecological Vespula (yellowjacket wasps) includes some of the world’s effects of invasions vary in magnitude. Many introduced species most ecologically damaging invasive insects (13, 14). Less well fail to interact strongly with the recipient biota, whereas others known than its congeners (e.g., V. germanica and V. vulgaris), V. profoundly disrupt the ecosystems they invade through predation, pensylvanica became established about 30 years ago in Hawaii competition, and other mechanisms. In the context of ecological (15), where it is now a major pest (16). The invasion of natural impacts, research on biological invasions seldom considers pheno- areas by western yellowjackets has reduced densities of certain typic or microevolutionary changes that occur following introduc- endemic taxa [e.g., Hawaiian picture-wing flies (17)], but the full tion. Here, we show how plasticity in key life history traits (colony ecological effects of this invasion remain incompletely studied. size and longevity), together with omnivory, magnifies the pred- Furthermore, shifts in colony structure (18) may amplify eco- atory impacts of an invasive social wasp (Vespula pensylvanica)on logical effects. Relative to native populations of V. pensylvanica, a largely endemic arthropod fauna in Hawaii. Using a combination up to 20% of colonies in introduced populations become pe- of molecular, experimental, and behavioral approaches, we dem- rennial (19). Plasticity in colony structure commonly occurs in onstrate (i) that yellowjackets consume an astonishing diversity of introduced populations despite the likelihood of low effective arthropod resources and depress prey populations in invaded population sizes associated with eusociality and decreased ge- Hawaiian ecosystems and (ii) that their impact as predators in this netic diversity from founder effects. Perennial V. pensylvanica ECOLOGY region increases when they shift from small annual colonies to colonies in Hawaii can have orders of magnitude more wasps large perennial colonies. Such trait plasticity may influence inva- compared with colonies in the western United States, which are sion success and the degree of disruption that invaded ecosystems annual and contain a few thousand individuals (20, 21). The experience. Moreover, postintroduction phenotypic changes may largest perennial colony of any Vespula species ever reported was help invaders to compensate for reductions in adaptive potential a V. pensylvanica colony on Maui with nearly 600,000 individuals resulting from founder events and small population sizes. The (21). Shifts in colony structure occur in other Vespula introduc- dynamic nature of biological invasions necessitates a more quan- tions, but little is known about the ecological significance of this titative understanding of how postintroduction changes in invader transition. traits affect invasion processes. We studied western yellowjackets in 2 national parks: Hawaii Volcanoes (HAVO) on Hawaii and Haleakala (HALE) on biological invasions ͉ predation Maui; both parks support large populations of V. pensylvanica and diverse arthropod assemblages. Study sites were located in pecies introductions disrupt ecosystems and can threaten open Metrosideros polymorpha (ohia) woodland between 1,000 biodiversity (1–3). Predicting the magnitude of these effects, and 1,200 m (HAVO) and in subalpine shrubland between 2,500 S and 3,000 m (HALE). We used molecular analyses to identify however, has proved difficult (4), in part because invaders and Ϸ members of the recipient biota may undergo microevolutionary masticated diet items collected from 50 returning foragers at each of 10 colonies (5 in HAVO and 5 in HALE). We identified changes or display phenotypic plasticity following introduction diet items by sequencing the 16S rDNA and COI genes following events (5–7). For invaders, postintroduction modifications in Kasper et al. (22) and Magnacca and Danforth (23). We behavior, morphology, or life history traits may influence inva- extracted DNA from 93% of samples (n ϭ 465), 90% of which sion success and alter the capacity of these species to disrupt the were identified at least to the family level using a combination ecosystems they invade. In this way, trait plasticity may permit of BLAST searches, comparisons with voucher specimens col- individuals to compensate for reduced genetic diversity (8) and lected on site, and phylogenetic analyses. the subsequent loss of adaptive potential that is assumed to result Molecular analyses revealed that V. pensylvanica exhibits an from translocation to new environments (9). extraordinarily broad diet on both islands (Fig. 1A and Table 1). Trait plasticity may be especially important for invasive social The yellowjacket diet spans 14 taxonomic orders of invertebrates insects, because small behavioral changes at the individual level and vertebrates. Vespula pensylvanica collected endemic and can scale up to produce dramatic and unexpected changes at the introduced taxa in relatively equal numbers (Fig. 1B), but orders colony level (e.g., the formation of supercolonies) (10). In this differed in the proportion of endemic or introduced taxa con- sense, the phenotypic envelope of the social superorganism can sumed. Endemic Hawaiian arthropod genera commonly con- encompass a larger set of potential morphotypes compared with that of a typical solitary organism. Here, we quantify the ecological effects of trait plasticity in an omnivorous social insect Author contributions: E.E.W. and D.A.H. designed research; E.E.W. and L.M.M. performed invader (the western yellowjacket, Vespula pensylvanica) that is research; E.E.W. analyzed data; and E.E.W. and D.A.H. wrote the paper. shaping Hawaiian arthropod assemblages through top-down The authors declare no conflict of interest. effects on multiple trophic levels. In part because Hawaii lacks This article is a PNAS Direct Submission. native eusocial insects (11), yellowjacket invasions pose a po- Data deposition: The sequences reported in this paper have been deposited in the GenBank tentially devastating threat to endemic taxa. This study illustrates database (accession nos. FJ821513, FJ849062–3, and GQ254018–21). how postintroduction shifts in invader traits shape ecological 1To whom correspondence should be addressed. E-mail: [email protected]. interactions between native and invasive taxa (12) and helps to This article contains supporting information online at www.pnas.org/cgi/content/full/ explain why some species become problematic invaders. 0902979106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0902979106 PNAS Early Edition ͉ 1of5 Downloaded by guest on October 1, 2021 hydrate resources (Fig. 3D). Perennial colonies depressed spider A 100 Hawaii Volcanoes National Park (HAVO) densities 30% more than did annual colonies; this disparity 75 Haleakala National Park (HALE) presumably reflected higher resource requirements of perennial 50 colonies. We likely underestimated the ecological effects of 25 perenniality because we sampled within 40 m of nests. Because 0 the size of perennial colonies can vastly exceed that of typical annual colonies (18, 19, 21), one would expect the effects of Number of diet items perennial colonies per unit area to be much greater than the Diptera Araneae Rodentia phora Squamata Hemiptera Orthoptera summed effects of multiple annual colonies. Foragers from Coleoptera Dictyoptera Psocoptera Galliformes Lepidoptera Stylommato- Hymenoptera B Passeriformes perennial colonies may quickly deplete resources near their 50 nests, forcing them to forage at greater distances; thus, the total 40 Endemic Introduced predatory effect of a perennial colony will be greater in mag- 30 nitude close to the nest, and the radius of the depleted zone will 20 be larger compared with that of annual colonies. 10 Seasonal differences in colony activity further accentuate disparities in resource consumption between annual and peren- 0 Number of diet items Araneae Hemiptera Hymenoptera Lepidoptera nial colonies (Fig. 3). Perennial colonies forage actively in early Yellowjacket diet by taxon spring when the annual colonies are being founded and also remain active later in the season compared with annual colonies Fig. 1. (A) Molecular analysis of 412 diet items collected from foragers in 2 (21, 24). In November, when the annual colony cycle is nearing Hawaiian national parks. Invertebrates comprised the majority of the Vespula its end, perennial colonies exhibited a mean entrance rate of 94.7 diet; vertebrate samples were scavenged carrion. (B) We classified diet items wasps/min, whereas annual colonies exhibited a mean 16.1 in the 4 most common orders of endemic arthropods at our field sites as incoming wasps/min (t ϭ 2.53, P ϭ 0.022). ϭ 16 endemic to Hawaii or introduced (n 133 items shown). The transition to colony perenniality occurs in multiple Vespula species,