Biol Invasions (2015) 17:1683–1695 DOI 10.1007/s10530-014-0826-7 ORIGINAL PAPER Modeling the decline and potential recovery of a native butterfly following serial invasions by exotic species Tegan A. L. Morton • Alexandra Thorn • J. Michael Reed • Roy G. Van Driesche • Richard A. Casagrande • Frances S. Chew Received: 14 November 2013 / Accepted: 9 December 2014 / Published online: 27 December 2014 Ó Springer International Publishing Switzerland 2014 Abstract Population sizes and range of the native enabled P. oleracea to adapt to A. petiolata.We butterfly Pieris oleracea declined after habitat loss and simulated scenarios of trait proliferation via sponta- parasitism by an exotic braconid wasp (Cotesia neous mutation or immigration of the trait, and glomerata) introduced to control the exotic invasive residual variation in the trait following the butterfly’s butterfly Pieris rapae. Further declines are attributed isolation in North America. Results indicate that the to the invasive exotic weed garlic mustard (Alliaria most likely scenario for the population that has petiolata), an oviposition sensory trap on which adapted to garlic mustard includes (1) a change in P. oleracea larval survival and growth are very poor. selection following garlic mustard invasion to favor But a population of P. oleracea has adapted to garlic previously neutral residual variation in the population, mustard over the past several decades, coincident with (2) release from parasitism, and (3) evolution of the introduction of a second parasitoid, C. rubecula,a improved larval survival on garlic mustard, which specialist on P. rapae that is competitively dominant allowed an increased host range, and potentially, to C. glomerata. We used stochastic simulation population size. models to assess the plausibility of a hypothesis that reduced parasitoid pressure over this time period Keywords Enemy-free space Á Pieris Á Tri-trophic interaction Á Novel host Á Alliaria petiolata T. A. L. Morton Á A. Thorn Á J. M. Reed Á F. S. Chew (&) Department of Biology, Tufts University, Medford, MA 02155, USA Introduction e-mail: [email protected] A. Thorn The spread of exotic species into an ecosystem can Institute for the Study of Earth, Oceans, and Space, shift selection pressures for native species (e.g., Lau University of New Hampshire, Durham, NH 03824, USA 2006). In insect herbivore-plant associations, these shifts might be predicted from knowledge of the R. G. Van Driesche Department of Entomology, Plant, Soil and Insect phylogenetic constraints of the herbivore-plant sys- Sciences, University of Massachusetts, Amherst, tems involved (Pearse and Altermatt 2013), may incur MA 01002, USA fitness costs for native herbivores (Nakajima et al. 2014), may have effects that span trophic levels R. A. Casagrande Department of Plant Science and Entomology, University (Harvey et al. 2010a, b), and can involve both of Rhode Island, Kingston, RI 02881, USA ecological and evolutionary processes in communities 123 1684 T. A. L. Morton et al. (Strauss et al. 2006; Forister and Wilson 2013). We competitively dominant to C. glomerata (Laing and hypothesize here that sequential introductions of two Corrigan 1987; Herlihy et al. 2012), greatly lowering exotic species exerting negative top-down and bot- the abundance of C. glomerata from habitats where it tom-up effects on a native herbivorous insect were was abundant previously (Van Driesche 2008; Herlihy responsible for the native’s decline, but a third et al. 2012), and potentially creating enemy-free space introduction released top-down pressure, creating for the native butterfly. This enemy-free space would opportunity for proliferation of an allele that allows allow slow-growing individuals on garlic mustard, successful dietary expansion by the herbivore, with which would otherwise experience increased exposure positive consequences for its population size. to parasitism and almost certainly be parasitized, to The native butterfly Pieris oleracea Harris (Lepi- survive to pupation and contribute their genetic doptera: Pieridae) decreased in abundance and range material to future generations. in eastern and central North America in the late 1800s The serial invasions described above, in tandem (Scudder 1889; Longstaff 1912; Klots 1951; Opler and with variation among butterfly maternal families in Krizek 1984) and is now listed as threatened in parts of larval ability to develop on garlic mustard (Keeler and its range (Massachusetts Natural Heritage and Endan- Chew 2008), could potentially permit P. oleracea to gered Species Program 2010). Declines are attributed expand its host range to include garlic mustard by to decreased native host availability caused by habitat permitting persistence and proliferation of adapted loss (Chew 1981), and especially to parasitism by genotypes. Indeed the population in one locality has Cotesia glomerata (L.) (Benson et al. 2003), an exotic already begun to include garlic mustard in its diet and braconid parasitoid introduced in the 1880s as biolog- its population size is apparently recovering (Chew ical control for the exotic pest Pieris rapae (Clausen et al. 2012). We used a stochastic simulation model to 1978). Invasion by garlic mustard (Alliaria petiolata investigate plausibility of our hypothesized scenario in [Bieb.] Cavara & Grande) following habitat loss and enabling the spread of adaptation to garlic mustard. disturbance likely exacerbated the decline (Courant Specifically, we sought to evaluate the likelihood that et al. 1994; Keeler et al. 2006). Garlic mustard is an (1) observed adapted individuals arose from: a spon- exotic invasive plant first documented in North taneous dominant mutation producing heterozygotes America in 1868 (Nuzzo 1993). It is a sensory trap in the population (or a dominant allele introduced via for P. oleracea. Its aliphatic glucosinolates are cues immigration); or residual variation from dissected for egg laying by P. oleracea (Huang et al. 1995; polymorphism (Bowden 1979) in the Holarctic species Chew and Renwick 1995), and are similar to those of a complex P. napi. We examined the likelihood that the native host Cardamine (=Dentaria) diphylla (Feeny number of such adapted individuals in a population of and Rosenberry 1982). However, P. oleracea larvae mostly wild-type (non-adapted) individuals would did not survive on garlic mustard (Bowden 1971)or increase and persist. Scenarios evaluating the ecolog- survived poorly and grew slowly (Courant et al. 1994; ical context of such proliferation and persistence of Courant 1996). The ability to use garlic mustard adapted individuals included (2) whether top-down behaves as a dominant, autosomal trait in European regulation in the form of the exotic, generalist P. napi L. (Bowden 1971), a related species in the parasitoid C. glomerata could limit proliferation of Holarctic Pieris napi complex (Bowden 1979; Chew an allele introduced through the scenarios above; and and Watt 2006). F1 hybrid larvae of crosses between (3) whether release from parasitism via introduction of the adapted P. napi with North American P. oleracea the competitively dominant, specialist parasitoid develop on garlic mustard (Bowden 1971). C. rubecula could allow for allele proliferation. Further complicating our expectations about poten- tial proliferation of a trait allowing P. oleracea to develop on garlic mustard is another parasitoid wasp, Methods Cotesia rubecula (Marshall), which was introduced in 1988 as another biological control agent for P. rapae Model overview and parameters (Van Driesche and Nunn 2002). This parasitoid does not attack P. oleracea (Brodeur et al. 1996; Van For our analyses we modified the published stochastic Driesche et al. 2003). Interestingly, C. rubecula is population simulation model of Keeler et al. (2006; 123 Modeling the decline and potential recovery of a native butterfly 1685 Fig. 1 A graphical representation of the life cycle of the native community parameters affecting abundance of each life cycle butterfly P. oleracea modified from Keeler et al. (2006), stage are depicted on each side, along with the corresponding including variables that decrease or potentially decrease equation numbers that describe the relationships of the variables survivorship of individuals. Surviving individuals were tracked to determine survivorship among life-history stages. Survivor- by genotype in separate, but identical models, which interacted ship on garlic mustard Alliaria petiolata (shaded) differs among between generations with random mating. Life history and genotypes Fig. 1). This model simulates females only. All parasitoid, C. rubecula, so we included this in some parameter values are specified below, and, unless scenarios of our model. Thus, the first significant otherwise noted, are the same as those used in the modification to the existing model was to capture the original model (Keeler et al. 2006; see therein for effect of decreased C. glomerata parasitism as references). The model was built and modified using C. rubecula invades (Brodeur et al. 1996). We also STELLA software (version 8, isee systems, Inc., New increased the number of instars that are separately Hampshire, USA). The original model included top- modeled in the second generation (Fig. 1) to allow us down regulation by the exotic braconid parasitoid, to model decreasing risk with increasing larval instar C. glomerata. Although in the original model, Keeler because susceptibility is size-dependent (Brodeur et al. (2006) concluded that parasitism by C. glomerata et