Proceedings of the XIV International Symposium on Biological Control of Weeds, pp 105-111. F.A.C. Impson, C.A. Kleinjan and J.H. Hoffmann (eds). 2-7 March 2014, Kruger National Park, South Africa.

Ecological traps and weed biological control

R.A. Casagrande*1, F.S. Chew2 and R.G. Van Driesche3

1Department of Plant Sciences and Entomology, University of Rhode Island, Kingston, RI 02881 USA 2Department of Biology, Tufts University, Medford, MA 02155 USA 3Department of Environmental Conservation, University of Massachusetts, Amherst, MA 01003 USA

Keywords: , Monarch , swallow-worts, milkweeds, garlic mustard

Abstract

In a phenomenon sometimes called an ecological trap, native may select an invasive plant as a suitable oviposition site even though their larvae may perish on these non-hosts. Two North American native ( oleracea and . : Pieridae) readily oviposit on garlic mustard (, ), and monarch butterflies (Danaus plexippus, Lepidoptera: Nymphalidae) readily oviposit on non-host swallow-worts (Vincetoxicum nigrum and Vincetoxicum rossicum, Apocynaceae: Asclepiadoideae) where these non-host plants coexist with milkweeds. Oviposition on swallow-worts is not generally listed among the major factors in the extensive decline of monarch populations. However, milkweeds are increasingly being eliminated through agricultural practices and are being displaced by swallow-worts in unmanaged areas. The balance between suitable hosts and ecological traps is therefore shifting and this may result in further decline of monarchs in future. An effective swallow-wort biological control program might assist in efforts to restore monarch populations. Garlic mustard is widely distributed throughout the range of P. virginiensis which is a habitat specialist of forests. Females lay more readily on garlic mustard than on the normal hosts even though there are no signs of adaptation to the adopted host and P. virginiensis populations are in decline. This native butterfly might benefit from a garlic mustard biological control program but since North American garlic mustard populations are now known to decline on their own, the outcome of a potential biocontrol release is uncertain. In a third case, garlic mustard biocontrol appears to be unnecessary to protect populations of P. oleracea. A population of this butterfly in western Massachusetts, USA appears to be avoiding this potential ecological trap by being able to survive and develop on garlic mustard. This adaptation, combined with escape from attack from the parasitioid Cotesia glomerata (Hymenoptera: Braconidae) and the introduction and spread of a new host plant, the exotic cuckoo flower ( pratensis, Brassicaceae) may allow populations to recover to historical levels. Although difficult to assess on a regional population scale, the negative impacts of exotic plants on native insects should be considered in developing, evaluating, and regulating weed biological control programs.

1. Introduction they give an example of mayflies ovipositing on an asphalt road that had the same reflective properties as a pond. This In environments subjected to rapid anthropogenic concept is expanded to include introduced species as change, organisms may become ‘trapped’ by responses to ecological traps in a subsequent paper where Schlaepfer et environmental cues that had served them well through al. (2005) describe inappropriate oviposition by three evolutionary time. A newly introduced element can mimic butterfly species on exotic non-host plants that mimic the a stimulus used by an organism in selecting a suitable olfactory stimuli of their traditional hosts. The North habitat, thus inducing an inappropriate response. American native monarch butterfly Danaus plexippus (L.) Schlaepfer et al. (2002) termed this an evolutionary trap and

*Corresponding author: [email protected] 105 Casagrande et al.

(Lepidoptera: Nymphalidae), which normally reproduces 2.1. Monarch decline on milkweed species, also oviposits (and their larvae perish) Populations of eastern monarch butterflies have on exotic swallow-worts (Haribal and Renwick, 1998; experienced population increases and declines in the past, Casagrande and Dacey, 2007). Similarly, the native North particularly related to weather conditions in overwintering American butterflies Harris and Pieris sites and during migratory periods, but since the 1976 virginiensis W.H. Edwards (Lepidoptera: Pieridae), which discovery of overwintering populations in Mexico, these traditionally oviposit on native Brassicaceae, are stimulated populations have greatly declined (Brower, 1995). In the to oviposit on garlic mustard, Alliaria petiolata (M. Bieb.) past decade, an estimated winter population covering 11.12 Cavara & Grande (Brassicaceae), which is toxic to their ha in 2003/4 was reduced to a mere 1.29 ha in 2012/13. larvae (Courant et al., 1994; Porter, 1994). In addressing This population shrank to 0.67 ha in 2013/14 (Wines, 2014) management issues related to ecological traps, Schlaepfer et following the precipitous decline (near absence) of al. (2005) suggest novel approaches that assist organisms in monarchs throughout the upper Midwest and northeast parts adapting to the novel environment instead of pursuing of the United States in the 2013 season (Robbins, 2013). “futile attempts to restore ‘pristine’ or ‘ancestral’ conditions.” Biological control programs under There are no good historical data on abundance of development for both garlic mustard and swallow-worts are North American monarch butterflies. Brower (1995) unlikely to restore a pristine environment, but they may mentions several reports of enormous migratory flights of reduce the impact of these invasive plants on butterfly monarchs in the midwestern United State before 1880. The populations, perhaps allowing time for them to adapt to subsequent spread of A. syriaca throughout the Midwest these plants and other environmental constraints. and into the previously forested, eastern states certainly expanded the range of the monarchs, but it is unknown what In the United States it currently takes a decade or more effect this had on the overall size of the North American of research and regulatory consideration before a novel monarch population. There is some (disputed) evidence biological control agent for an invasive plant is permitted that larger monarch populations in North America resulted for introduction. The continuing vulnerability of in colonization of distant islands and continents around P. virginiensis populations and precipitous decline of 1880 (Brower, 1995). The most widely accepted counts are monarchs argue for population-level assessments of the provided by estimates of overwintering colonies1. impacts of these and other ecological traps and possible reconsideration of regulatory processes. A reduction in size of the fir forest and thinning of trees in some monarch overwintering sites in Mexico has exposed monarchs to unfavorable weather conditions, resulting in winter mortality as high as 42% in 1981 and 80% in 1992 2. Monarch butterflies (Brower, 1995). Brower also reported surprisingly high The monarch butterfly, native to North America, is overwintering predation by birds and mice on adult well known for its seasonal migrations. Eastern populations butterflies that should have been protected by cardiac exhibit the longest flights, overwintering in Mexico. glycosides accumulated as larvae. He attributes this to Western populations fly shorter distances to overwintering production of these overwintering adults on A. syriaca with sites in coastal California, and Florida populations do not variable levels of cardiac glycosides instead of more toxic migrate at all (Altizier et al., 2000). The eastern monarch prairie milkweeds that were their primary hosts over a population primarily overwinters in Mexico and migrates century ago (Brower, 1995). Recent factors considered north in early spring. Before large-scale conversion of the important to the decline of eastern monarch populations plains grassland ecosystems to agricultural lands, monarchs include the loss of farm conservation land to corn reproduced on native Asclepias species, with successive production for biofuels and the widespread use of herbicides generations moving northward as host plants senesced and on corn and soybeans (Robbins, 2013). These factors have then retreating in great mass flights to Mexico for the winter resulted in 60-90% loss of milkweed in a decade in Iowa (Brower, 1995). The late 1800s witnessed two changes in (Hartzler, 2010; Brower et al., 2012). An increased monarch behavior – both related to native common incidence of the protozoan Ophryocystis elektroscirrha milkweed (Asclepias syriaca L., Asclepiadaceae). As the McLaughlin and Myers (Neogregarinida: Ophryocystidae) plains were farmed, native milkweeds were largely in overwintering colonies in recent years might also be eliminated and replaced by the weedy A. syriaca which also contributing to the decline of eastern monarchs and to a moved into eastern farm fields newly created from forest. male-skewed shift in sex ratios in overwintering sites and Monarchs switched to A. syriaca in the midwestern United throughout the breeding range of these butterflies (Davis States and followed this host plant into the eastern states and Rendón-Salinas, 2010). In addition to these problems, where the first large-scale migrations were noted in the which have gradually increased in severity over the past 1880s (Brower, 1995). decade, poor weather early in the spring migration was a

1 There are annual observational counts of migrants made at two sites (Cape May, NJ and Peninsula Point, Mich.) which lead Davis (2012) to question whether monarch populations are actually declining. However this analysis was based on counts through 2010 before the Cape May counts declined from 183.15/hr. over the 2012 season to12.74/hr in 2013 http://www.monarchmonitoringproject.com/mmptwo.html 106

Ecological traps and weed biological control

major contribution to population decline in 2012 and 2013 New York, Ontario, and the upper midwestern United (Wines, 2014). States. There are no data on the extent of monarch oviposition in these areas, and, unless monarch populations Large migratory flights of monarchs on the North rebound considerably, such studies will be impossible. American Pacific coast date back to at least 1864. (While spending a substantial part of the summer of 2013 in Butterflies overwinter in several coastal locations, primarily the field, our research team saw only a single monarch in California before dispersing to summer breeding sites butterfly and that was in a large patch of swallow-wort.) west of the Rocky Mountains (Brower and Malcolm, 1991). These populations are even more difficult to enumerate than The role of swallow-worts in the decline of monarch those that migrate to Mexico because they overwinter in butterflies has not been studied and these plants are not relatively small numbers in hundreds of locations, but they among those factors most commonly discussed. However, too, have apparently declined in recent decades – possibly as milkweed populations decline in agricultural land, the due to O. elektroscirrha (Brower, 1995), which infests 30% displacement of milkweeds by swallow-worts in of sampled western populations (Altizer et al., 2000). unmanaged lands becomes more significant and an ever- greater percentage of monarch eggs will be deposited on 2.2. Monarch/swallow-wort interactions these non-host plants although these eggs may be too rare to find. Two swallow-worts are widely distributed in the United States. Black swallow-wort, Vincetoxicum nigrum

(L.) Moench (Apocynaceae: Asclepiadoideae) (synonyms = Cynanchum nigrum, Cynanchum louiseae Kartesz & 3. Pieris Butterflies Gandhi), ranges from Maine through Kansas and also Two species of native North American butterflies that occurs in California. This European perennial herbaceous traditionally reproduce on native spring ephemeral crucifer vine is most common in disturbed areas, pastures, roadsides, hosts also oviposit on exotic garlic mustard (Huang et al., and forest understories (DiTommaso and Losey, 2003). 1995). The primary native hosts of P. oleracea and Pale swallow-wort, Vincetoxicum rossicum (Klepow) P. virginiensis are found in the same mesic deciduous Barbar (Apocynaceae: Asclepiadoideae) (synonym = forests that are now invaded by garlic mustard. Both Cyanchum rossicum (Kleopow) Borhidi), also known as butterfly species have been adversely impacted by garlic dog-strangling vine, is native to Ukraine and Russia. Its mustard in recent decades but they have responded very growth habit is similar to V. nigrum, and it is found in differently to these and other environmental perturbations. disturbed areas from the Great Lakes through New England and the Mid-Atlantic States. Both swallow-wort species are 3.1. Garlic mustard. highly invasive in North America, causing serious problems in pasture management because of livestock toxicity and This biennial European crucifer was first found in aggressive competition with native plants, including North America in 1868 (Nuzzo, 1993). It is one of the few milkweeds (Haribal and Renwick, 1998; DiTommaso and non-indigenous herbs to dominate the forest understory, Losey, 2003). Vincetoxicum nigrum was first reported in where its displacement of native species may be facilitated Massachusetts in 1854 and V. rossicum was recorded in by production of phytotoxic chemicals and overgrazing by New York in 1897. Thus monarchs have been exposed to deer (Blossey et al., 2002; 2005). This species is largely swallow-worts in the northeastern United States since these avoided by deer which have increased in abundance in butterflies expanded their range into this area in the late recent decades and are exerting increasing pressure on the 1800s. native plants. First year garlic mustard plants develop In addition to anecdotal notes, there are published sizeable rosette foliage and a large root system that allow second-year plants to quickly grow taller with greater floral reports of monarch oviposition on swallow-worts in the masses than the native cruciferous hosts of the pierid field (Mattila and Otis, 2003; Casagrande and Dacey, 2007) butterflies. The current range of garlic mustard overlaps and several laboratory studies have been conducted on this phenomenon (Harribal and Renwick, 1998; Mattila and with much of the ranges of P. virginiensis and P. oleracea. Otis, 2003; DiTommaso and Losey, 2003; Casagrande and Dacey, 2007). While laboratory studies provide disparate 3.2. Pieris virginiensis. results on monarch oviposition on swallow-wort, field The West Virginia White is found in mature, mesic results show that monarch butterflies can lay a significant hardwood forests from Vermont south through the percentage of their eggs on this non-host. In pastures where Appalachian Mountains to Alabama and west to Wisconsin. milkweed cover was triple that of black swallow-wort, The primary larval host is two-leafed toothwort Cardamine monarchs laid 15.4% of their eggs on swallow-wort. In diphylla (Michx.), and lesser hosts include Cardamine nearly pure stands of swallow-wort with only a few concatenata (Michx.), Cardamine dissecta (Leavenw.) and milkweed stems present, monarchs still preferentially rock mustard laevigata (Muhl. ex Willd.) (all oviposited on milkweed. However, egg density on Brassicaceae). Adults emerge from overwintering pupae in swallow-worts was five-fold higher than in the pastures early spring before trees are fully foliated and oviposit on (Casagrande and Dacey, 2007). Large, almost pure sands their ephemeral host plants, which typically bloom at that of black swallow-wort are now common in southern New time. Larvae complete a single generation before host plants England and pale swallow-wort is even more common in 107

Casagrande et al. senesce. Adults seldom venture out of the forest and have experience over 70% survival on garlic mustard (F.S. Chew, been greatly affected by deforestation and forest unpublished data). It appears that the ‘innate tolerance” fragmentation (Cappuccino and Kareiva, 1985). may represent residual genetic variation in P oleracea populations because their close relatives in Europe Pieris Surveys conducted in the past two decades indicate napi napi L. (Lepidoptera: Pieridae), commonly use garlic that this butterfly is now rare in many areas where it was mustard as a larval host (Chew, pers. comm.; Bowden, once common (Shuey and Peacock, 1989; Davis and 1971). Cipollini, 2014a), due in part to the invasion of its habitat by garlic mustard, which poses “an imminent threat to the 3.4. Cotesia rubecula (Marshall) (Hymenoptera: long-term survival of this species throughout much of its Braconidae) historic range” (Bess, 2005). Past authors have noted oviposition by P. virginiensis on garlic mustard (Courant et This parasitoid, introduced in New England in 1988 al., 1994; Porter, 1994). Davis and Cipollini (2014a) found against P. rapae (Van Driesche and Nunn, 2002), has P. virginiensis ‘prefers’ garlic mustard over C. diphylla as substantially changed the outlook for survival of an oviposition site in both field observations and laboratory P. oleracea. The host-specific C. rubecula has spread tests. In field sites, they found twice as many P. virginiensis throughout the northeastern United States, displacing or eggs on garlic mustard as on C. diphylla but they found no greatly suppressing C. glomerata in all locations in larval survival on garlic mustard – results consistent with 20 Massachusetts (Herlihy et al., 2012). Since this parasitoid years of rearing attempts by F.S. Chew (unpublished). does not attack P. oleracea, the butterfly no longer needs the protection offered by the forest and it can, once again, 3.3. Pieris oleracea reproduce on crucifers growing in full sun. This species recovery is being facilitated by a newly established exotic The veined white was historically common in New plant, Cardamine pratensis (L.)(Brassicaceae) (cuckoo England and New York, where it occurred on many flower). cruciferous host plants growing in sunny disturbed habitats. However, the distribution and abundance of this butterfly 3.5. Cardamine pratensis have greatly diminished since the 1880s, due in part to habitat loss (Chew, 1981). Another major factor in this Cuckoo flower has been present for at least 30 years in decline has been the parasitoid Cotesia glomerata (L.) the site near Lenox, Massachusetts studied by F. Chew and (Hymenoptera: Braconidae), an exotic wasp introduced in her students, and P. oleracea was infrequently seen on this the 1880s for biological control of the exotic pest Pieris host plant. Before 2008 it was possible to see a dozen rapae (L.) (Lepidoptera: Pieridae), which invaded Quebec P. oleracea on a good day in the forested site. However, about 1860 (Scudder, 1889; Clausen, 1978). In open areas around this time amateur lepidopterists began reporting this parasitoid preferentially attacks the native P. oleracea large populations of this butterfly in an open area across the over P. rapae, but it generally does not attack hosts located Housatonic River within 1 km of her research site. These in the shade of forests (Van Driesche et al., 2004). It thus butterflies were found to be reproducing on exotic effectively eliminated the native pierid from open areas, C. pratensis. By 2010 it was possible to see hundreds of leaving forest populations of the shade-growing toothwort these butterflies in a short walk along the river and in nearby (C. diphylla) as its primary host (Benson et al., 2003). pastures and these populations have persisted in subsequent Unfortunately for these butterflies, these same wooded years. At this site there are at least four generations in a refuges that protect them from the parasitoid have also warm season (Van Driesche, pers. observation). Garlic become common habitat for garlic mustard, which induces mustard is abundant along the river and the butterflies are them to oviposit on this non-host. commonly seen nectaring on these flowers in early spring. These butterflies appear to have escaped a century of Garlic mustard provides oviposition cues that are parasitism, adapted to garlic mustard, and they are thriving similar to those of the native host C. diphylla (Huang, on a new invasive host plant. Their future seems secure – Renwick and Chew 1995) but P. oleracea larvae grow at least at one site in western Massachusetts. slowly, if at all, on garlic mustard (Courant et al. 1994). More recently, Keeler and Chew (2008) discovered that some populations of P. oleracea have an innate tolerance to 4. Considerations for biological control A. petiolata, with up to 7% of the larvae in a population 4.1. Pieris oleracea never previously exposed to A. petiolata surviving to pupation. In that same paper, they described another Populations of P. oleracea poised to rebound. Not population near Lenox, Massachusetts with roughly 60-100 many sites have been sampled for tolerance to garlic generations of exposure to garlic mustard where an average mustard, but it is clear that the Lenox, Massachusetts of 17% of larvae survived to pupation on garlic mustard and population has adapted to this exotic plant and the presence some adults had a marked oviposition preference for garlic of low-level tolerance to garlic mustard in an unexposed mustard over C. diphylla. Their suggestion that this population in northern Vermont demonstrates the potential particular population may be escaping the ecological trap of for adaptation at additional sites. The widespread garlic mustard has been borne out by recent research displacement of the parasitoid C. glomerata by the showing that in the intervening decade the larval offspring specialist C. rubecula allows this butterfly to return to the of some individual females of these butterflies now open-field sites where new exotic crucifers such as 108

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C. pratensis and Cardamine impatiens L. (F.S. Chew, northern portions of their summer range where swallow- unpublished data) provide additional potential. Biological worts out-compete native host plants and induce control of garlic mustard does not appear necessary to inappropriate oviposition. preserve P. oleracea. European exploration in 2006 identified several promising natural enemies of swallow-worts (Weed, 2010), 4.2. Pieris virgiensis including Hypena opulenta Christoph (Lepidoptera: The West Virginia white has a less-promising future. Noctuidae). This agent is monophagous on swallow-wort Parasitism by C. glomerata was never an issue because this species and has the potential to substantially damage these butterfly does not venture from the forest (Benson et al., plants (Weed and Casagrande, 2010; Weed et al., 2011). A 2003). Although it actively prefers the non-host garlic release petition submitted in 2011 required additional mustard over its native host plants, P. virginiensis shows no testing before receiving TAG approval in 2013. It is ability to survive on this plant. Thus a case can be made for presently in the post-TAG regulatory process with a biological control of garlic mustard to preserve populations possibility of approval for field release in 2014 or 2015. By of P. virginiensis. The recent discovery that garlic mustard then, these moths may have flown to the United States from populations decline several years after establishment (B. a September, 2013 release in Ottawa, which has a Blossey, pers. comm.) as evidenced in Mayer et al. (2011) more streamlined process following a favourable TAG provides some hope for these butterflies, but garlic mustard ruling. tends to become abundant before it declines and it is possible that some populations of P. virginiensis will be 5. Regulatory process extirpated as reported by Davis and Cipollini (2014b). Programs of biological control against swallow-worts Biological control research on garlic mustard was and garlic mustard could possibly reduce the impacts of initiated in 1998 (Blossey et al. 2002) and in 2008, a release these ecological traps on the monarch and West Virginia petition for a garlic mustard biological control agent, white butterflies. It is not clear how much this would help Ceutorhynchus scrobiocollis Nerensheimer and Wagner since both species are subject to many adverse (Curculionidae: Coleoptera) was submitted to the U.S. environmental influences, but this approach might help Department of Agriculture’s and Plant Health maintain or even restore some populations of these Inspection Service (APHIS) - the agency that regulates butterflies. Unfortunately, the cumbersome regulatory biological control releases in the United States. In 2009, the process is delaying these programs. The seven-year interval TAG (Technical Advisory Group, reporting to APHIS on between discovery and (Canadian) release of H. opulenta is biological control introduction petitions) requested reasonably quick (especially when compared to the garlic additional testing. Results of this testing and supplemental mustard program), but like many other biological control information were added to a renewed release request in projects, it has been funded by competitive grants that are 2011. In 2013, the TAG requested further testing because of supplemented by grower and conservation groups. Funding test plant taxonomic revisions and the addition of more organizations rightly demand timely results. It is difficult threatened/endangered species to the test list. If a proposed to explain to a New England grower that biological control species test list is agreed upon and successful tests are progress on a northern plant is held up due to the conducted over the next one to two years, it will be at least unavailability of a threatened tropical test plant on the list another year before TAG might recommend approval and of 75 or so needed for host range testing. Canadian perhaps another year of regulatory hurdles before a field biological control practitioners might wonder why the release2. If the release permit clears these steps, then United States has such an arduous regulatory process after APHIS-PPQ (Plant Protection and Quarantine) should an agent receives a TAG recommendation for release. TAG approve the agent for field release – about 2018. How many Membership includes a representative each of five agencies P. virginiensis populations will have perished during these of the USDA, six agencies of the U.S. Department of the 20 years of research and deliberation? Interior, as well as the U.S. EPA, the Army Corps of Engineers, and invited participants from professional 4.3. Monarch butterfly organizations and other federal agencies (APHIS, 2014). In evaluating release petitions, members are charged with Monarch restoration efforts include protecting representing their employer’s interests and identifying and overwintering sites and increasing food sources throughout consulting with subject-matter specialists who are familiar their range (Brower et al., 2012). These efforts could be augmented by reducing swallow-wort populations in the

2 Once APHIS gets an approval recommendation from TAG, APHIS then has to develop an Environmental Assessment (for compliance with the National Environmental Policy Act – NEPA), a biological assessment (BA) with input from US Fish and Wildlife Service (for compliance with the Endangered Species Act), hopefully a Finding of No Significant Impact (FONSI) by APHIS, and then posting the proposed action in the Federal Register for public comment. If during the BA process the USFWS believes that the agent under consideration poses a threat to some threatened/endangered species or their habitats, then Section 7 Consultation kicks in and more discussions and time will be involved to address their concerns (R. Nowierski, pers. comm.)

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Casagrande et al. with the , biology, ecology, and other aspects of Brower, L.P., 1995. Understanding and misunderstanding the organisms being considered (TAG Charter). the migration of the monarch butterfly (Nymphalidae) in North America: 1857-1995. Journal of the It is not clear that the benefits of the post-TAG Lepidopterists Society 49, 304-385. regulatory process outweigh the benefits of a timely release. However, it is clear that ecological traps such as garlic Brower, L.P., Malcolm, S.B., 1991. Animal migrations: mustard and swallow-worts continue to pose threats to endangered phenomena. American Zoologist 31, 265- native and that this issue warrants the attention 276. of biological control scientists who better start while still Brower, L.P., O.R. Taylor, E.H. Williams, D.A. Slayback, young! R.R. Zuieta, Ramirez, M.I., 2012. Decline of monarch butterflies overwintering in Mexico: is the migratory Acknowledgments phenomenon at risk? Conservation and The authors acknowledge the contributions of many Diversity 5, 95-100. graduate students who have contributed to this body of Cappuccino N, Kareiva, P., 1985. Coping with a capricious knowledge over several decades as well as financial support environment: a population study of a rare pierid by Hatch funding (RAC and RGV-D) and funding by Tufts butterfly. Ecology 66, 152–161. University and the Arabis Fund (FSC). Casagrande, R.A., Dacey, J., 2007. Monarch butterfly oviposition on swallow-wort (Vincetoxicum spp.). References Environmental Entomology 36, 631-636. Altizer, S.M., Oberhauser, K.S., Brower, L.P., 2000. Chew, F.S., 1981. Coexistence and local extinction in two Associations between host migration and the Pieris butterflies. American. Naturalist 118, 655-672. prevalence of a protozoan parasite in natural populations of adult monarch butterflies. Ecological Clausen C. 1978. Introduced Parasites and Predators of Entomology 25, 125-139. Pests and Weeds: A World Review. United States Department of Agriculture, Washington, DC, APHIS, 2014. USA. http://www.aphis.usda.gov/wps/portal/aphis/ ourfocus/planthealth?1dmy&urile=wcm%3apath%3a Courant, A., Holbrook, A., VanderReijden, E., Chew, F.S., %2Faphis_content_library%2Fsa_our_focus%2Fsa_p 1994. Native pierine butterfly (Pieridae) adapting to lant_health%2Fsa_import%2Fsa_permits%2Fsa_plan naturalized crucifer? Journal of the Lepidopterists t_pests%2Fsa_tag%2Fct_charter. Accessed Society 48, 168–170. 2/14/2014. Davis, A.K., 2012. Are migratory monarchs really declining Benson, J., Van Driesche, R., Pasquale, A., Elkinton, J., in eastern North America? Examining evidence from 2003. Introduced braconid parasitoids and range two fall census programs. Insect Conservation and reduction of a native butterfly in New England. Diversity 5: 101-105. Biological Control 28, 197-213. Davis, S.L., Cipollini, D. 2014a. Do mothers always know best? Oviposition mistakes and resulting larval failure Bess, J., 2005. Conservation Assessment for the West of Pieris virginiensis on Alliaria petiolata, a novel, Virginia White (Pieris virginiensis Edwards). toxic host. Biological Invasions. Published online: 5 http://www.fs.usda.gov/Internet/FSE_DOCUMENTS/ January 2014. fsm91_054237.pdf http://link.springer.com/article/10.1007%2Fs 10530- Blossey, B., Nuzzo, V.A., Hinz, H.L., Gerber, E., 2002. 013-0637-2#page-1 Garlic Mustard. In: Van Driesche, R, Blossey, B., Davis S.L., Cipollini, D., 2014b. How environmental Hoddle, M., Lyon, S., Reardon, R. (eds). Biological conditions and changing landscapes influence the Control of Invasive Plants in the Eastern United States. survival and reproduction of a rare butterfly, Pieris USDA Forest Service Publication FHTET-2002-04. virginiensis (Pieridae). Journal of the Lepidopterists pp. 365-372. Society, in press. Blossey, B., Nuzzo, V.A., J. Maerz, Davalos, A. 2005. Davis, A.K, Rendón-Salinas, E., 2010. Are female monarch Ecosystem impacts of Alliaria petiolata (garlic butterflies declining in eastern North America? mustard). In: Proceedings: Symposium on the Biology, Evidence of a 30-year change in sex ratios at Mexican Ecology, and Management of Garlic Mustard (Alliaria overwintering sites. Biological Letters 6, 45-47. petiolata) and European Buckthorn (Rhamnus DiTommaso, A., Losey, J.E. 2003. Oviposition preference cathartica). St. Paul, MN: USDA Forest Service. pp 1- and larval performance of monarch butterflies (Danaus 3. plexippus) on two invasive swallow-wort species. Entomologia Experimentalis et Applicata 108, 205- Bowden, S.R. 1971. American white butterflies (Pieridae) 209. and English food plants. Journal of the Lepidopterist’s Society 25, 6-12. Haribal, M., Renwick, J.A., 1998. Identification and distribution of oviposition stimulants for monarch

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