Received: 16 January 2019 Revised: 15 April 2019 Accepted: 30 May 2019 DOI: 10.1111/1440-1703.12035

ORIGINAL ARTICLE

Invasive facilitates use of a native food plant by other native and invasive

Jeffrey A. Harvey1,2 | Rieta Gols3 | Brittany Smith4 | Paul J. Ode4

1Department of Terrestrial Ecology, Netherlands Institute of Ecology, Abstract Wageningen, The Netherlands Organisms that invade new habitats exploit new resources or niches and influence 2Department of Ecological Sciences, native species. Here, we examine how an invasive moth, the webworm Section Ecology, VU University ( radiella, formerly D. pastinacella), facilitates interactions with other Amsterdam, Amsterdam, The Netherlands arthropods in spatially separated populations of native cow parsnip (Heracleum 3Laboratory of , Wageningen University, Wageningen, The Netherlands maximum) in the Rocky Mountains (New Mexico and Colorado). We compare this 4Department of Bioagricultural Sciences and with results on small hogweed () in the Netherlands, where Pest Management/Graduate Degree Program both the plant and herbivore are native. Larvae of D. radiella feed in webs on rip- in Ecology, Colorado State University, Fort Collins, Colorado ening fruits of their food plants. Mature caterpillars descend the hollow stems into which they chew a hole, enter the stem and pupate. Other arthropods enter the Correspondence stems through these holes. Plants in all populations of cow parsnip/hogweed con- Jeffrey A. Harvey, Department of Terrestrial Ecology, Netherlands Institute of Ecology, tained either moth pupae and/or webworms mummified by their main parasitoid, Droevendaalsesteeg 10, 6700 EH Copidosoma sosares that also been introduced into parts of the United States. In Wageningen, The Netherlands. both countries, earwigs (Forficula auricularia), which are also invasive in the Email: [email protected] United States, were the dominant to utilize webworm-perforated stems, although there was more within-site variability in abundance of earwigs in the United States than in the Netherlands. The woodlouse, Porcelio scaber, which is native to Eurasia but also established in the United States, was abundant in stems of Dutch hogweeds but absent in stems of American cow . Other native herbivores (e.g., mirid bugs), were collected in stems at sites in both continents. Moreover, the number of various arthropods found in perforated stems correlate positively with the number of holes found in these stems.

KEYWORDS cow parsnip, ecosystem engineer, facilitation, invasive moth, small hogweed

1 | INTRODUCTION in their new range. The field of invasion ecology has tradi- tionally focused on how invasive plants and/or Over the past several centuries, humans have moved many become established and affect native trophic interactions and species from their native habitats to non-native ecosystems food webs with recommendation for ways of controlling or across the biosphere. Although most introductions fail to even eradicating them (Bezemer, Harvey, & Cronin, 2014; establish or the invader remains rare and unobtrusive in its Keane & Crawley, 2002; Parker, Burkepile, & Hay, 2006). new home, a small number of species become invasive pests Most authorities believe that the net costs of invasive species

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. © 2019 The Authors. Ecological Research published by John Wiley & Sons Australia, Ltd on behalf of The Ecological Society of Japan

Ecological Research. 2019;34:659–666. wileyonlinelibrary.com/journal/ere 659 660 HARVEY ET AL. on the global economy are enormous (Pejchar & Mooney, (Figure 1c). When they are mature, webworm larvae crawl 2009; Pimentel, Zuniga, & Morrison, 2005). However, in down the stems of their food plants, chew a hole in them and some situations, a small number of invasive species are able enter the hollow stems where they pupate. Some of the larvae, to integrate well into their new habitats with negligible or however, are parasitized during the egg stage by the polyem- even positive impacts. For example, some species have been bryonic parasitoid, Copidosoma sosares (Figure 1d) that pro- deliberately introduced because they perform a vital ecosys- duce distinctive mummies (Figure 1e) inside the stems. The tem service, such as pollination or biological control of pests adult or parasitoids emerge from the stems through the (Kenis et al., 2009; Liebhold & Tobin, 2008). Moreover, holes within a few weeks and overwinter in the surrounding some invasive plants sustain populations of rare butterflies vegetation or leaf litter until the following spring. However, when their native food plants became rare because of agri- other arthropods, such as the woodlouse Porcelio scaber,the cultural or urban expansion (Brown, Breed, Severns, & earwig Forficula auricularia, and spiders, especially Clubiona Crone, 2017; Jahner, Bonilla, Badik, Shapiro, & Forister, phragmitis, that are known to perform important ecological 2011; Shapiro, 2002). roles (i.e., as decomposers or predators), also use the holes to Some organisms, called “ecosystem engineers” (Jones, enter the stems, often in large numbers. They may use these Lawton, & Shachak, 1997), are known to directly or indi- stems for several months and occasionally even a year or rectly influence the behavior, development and survival of more, depending on how long the plant stem remains intact, other species by physically altering certain characteristics of but long after D. radiella or C. sosares have terminated their their habitat (Gribben et al., 2009; Hastings et al., 2007). For relationship with the plant. Some individual plants may be example, dams constructed by beavers create wetlands attacked by more than a single D. radiella caterpillar (up to that provision many other species of plants and animals 20), and we have found plants containing five or more holes (Wright, Jones, & Flecker, 2002). The abandoned bur- in the stems. rows of mammals like armadillos, prairie dogs and mar- has been introduced from its native mots provide vital refuges for a large range of other European range to many other countries including vertebrates, and the excavated soil can profoundly affect nutri- New Zealand and the United States, where, as a seed preda- ent cycling (Desbiez & Kluyber, 2013; Reichman & tor, it is a major natural enemy of invasive umbelliferous Seabloom, 2002). Social invertebrates, such as ants and ter- weeds like wild parsnip (Pastinaca sativa) or giant hogweed mites, build large mounds or create a labyrinthine network of (Heracleum mantegazzianum) (Berenbaum & Zangerl, tunnels in their nests that also facilitate other invertebrates and 2006; Hansen et al., 2006). In North America, however, influence nutrient cycles that enhance the colonization and D. radiella also attacks related native umbellifers, including growth of plants (Esmaeili & Hemami, 2013; Jouquet, Dauber, the cow parsnip H. maximum (Figure 1b) which is the only Lagerlöf, Lavelle, & Lepage, 2006). In spring, larvae of native species of Heracleum found across much of North Pseudotelphusa sp. use silk to “tie” overlapping leaves on America. Heracleum maximum is closely related to the pre- trees that act as shelters during feeding. After pupating, the ferred plant host of D. radiella in its native European range, abandoned shelters are used by a diverse range of other the small hogweed, H. sphondylium; indeed, until recently it as protection against rain and desiccation. Some trees may was considered a subspecies of the latter. Interactions contain many hundreds of these tied leaves (Lill & Marquis, between webworms and cow parsnips are virtually identical 2003, 2004). to those with hogweeds. In the United States, moreover, Many other organisms alter the physical habitats at C. sosares has also been introduced and become established smaller or more local scales, such as in small plants (forbs), in parts of the western United States where D. radiella is and thus may not fill an ecological role as true engineers but abundant. as “facilitators.” Nevertheless, facilitators may influence Here, we examine interactions between D. radiella, its par- other species that do perform vital functions in their habitats. asitoid C. sosares, and other insects in both hogweeds and For example, Tischler (1973) showed that feeding damage cow parsnips in eight spatially separated plant populations in by deer opens the hollow stems of reeds and thistles and that the native and invasive ranges (The Netherlands and Col- these stems are then colonized by insects. Other studies have orado/New Mexico, United States, respectively). The Dutch found variable temporal occupancy by arthropods in hollow populations of H. sphondylium grow at elevations close to sea plant structures including thorns and bracts (Rathet & level, whereas the American populations of H. maximum grow Bronstein, 1987; Rathke, 1976; Seifert, 1982). Harvey, Ode, between 2,000 and 3,000 m above sea level, predominantly in Malcicka, and Gols (2016) found that many small hogweed river valleys or passes in the Rocky Mountains. First, we com- Heracleum sphondylium plants (Figure 1a) were infested by pared numbers of D. radiella pupae and C. sosares mummies larvae of the parsnip webworm. Depressaria radiella (for- per attacked plant in both its native and invasive ranges; sec- merly D. pastinacella) that feed in webs of the ripening fruits ond, we compared the abundance and diversity of other HARVEY ET AL. 661

FIGURE 1 Photographs of plant species and invertebrates associated with them. (a) Small hogweed, Heracelum sphondylium (the Netherlands). (b) Cow parsnip, Heracleum maximum (United States). (c) Umbels and seeds of H. sphondylium infested with larvae of parsnip webworm, Depressaria radiella. (d) Larval entrance and adult emergence hole chewed by mature caterpillar of D. radiella in stem of H. maximum. (e) Mummy of larva of D. radiella parasitized by the polyembryonic parasitoid, Copidosoma sosares. (f) Adult female of C. sosares. (g) Adult male of European earwig, Forficula auricularia. (h) Adult woodlouse, Porcelio scaber

arthropods that use plants previously attacked by D. radiella were: Veenhuizen, Drenthe: 532038.8200N, 623011.9500E; in the Dutch and American populations of H. sphondylium Wageningen, Gelderland: 5159016.2500N, 540014.7700E; and H. maximum, respectively. We hypothesize that in both Kekerdom, Gelderland: 5151056.8700N, 61021.2200E; Zoelen, the native and the invasive range holes chewed by mature Gelderland: 5154050.0800N, 523017.1500E. Elevation at all sites D. radiella caterpillars in the stems for pupation facilitate the was <10 m asl. The United States locations were: New Mexico use of the plant stems by other arthropods. (Santa Fe National Forest, elevation 2,477 m asl): 35.768217N, 105.698517W; Colorado (Rio Blanco Basin, Spring Creek, ele- vation 2,483 m asl): 39.507133N, 106.7519W; Colorado 2 | MATERIALS AND METHODS (Cebolla Creek, 2,585 m asl) 38.183683N, 107.053867W; Col- orado (McClure Pass, 2,671 m asl) 39.1287N, 107.286667W. 2.1 | Locations The United States locations were scattered over a far wider area Plants were sampled at eight locations in The Netherlands than the Dutch populations, as H. maxima is much more and western United States (four in each country) between scattered and less common in the western United States mid-August and September of 2017. The Dutch locations than H. sphondylium is in the Netherlands. 662 HARVEY ET AL.

2.2 | Sampling of plants for arthropods as the mean height of the holes did not differ between the two continents (mean number of holes per stem United States: 2.92 Senescing plants of both species with holes created by ±0.37 [mean±SE], the Netherlands 2.85 ± 0.36; F1, D. radiella larvae preparing to pupate were sampled in 5.5 = 0.02, p = 0.89; mean hole height: United States: 55 groups of 9–16 plants per population. A fully grown plant ± 4 cm, the Netherlands 61 ± 4 cm, F1, 5.9 = 1.05, p = 0.35). was defined as one in senescence; all seeds were dried or The number of D. radiella pupae per plant stem also had already fallen from the plant and the outer stem was no did not differ between the two continents (F1, 5.7 = 1.33, longer moist and green in color but dry and brown (pos- p = 0.29, Figure 2a) with a mean number of pupae of 2.8 treproductive stage). Plants in each location infested with ± 0.3 per stem that had holes. The number of C. sosares D. radiella were sampled using a paring knife to cut open mummies was higher in cow parsnips sampled in the the stems along their entire length. Before cutting, the total western United States than in hogweeds sampled in the height of each plant was measured, the number of Netherlands (F1, 5.3 =7.50,p = 0.038, western United D. radiella holes per stem counted, and the height to each States 1.6 ± 0.3, the Netherlands 0.8 ± 0.3, Figure 2b). hole from the ground measured. Each hollow stem contains Woodlice were found in each of the four sampled sites in several chambers that are separated by a thick wall, and all the Netherlands but none of the U.S. sites; in more than of these were opened on the sampled plants. Once a stem half of the sampled stems with holes in the Netherlands, was cut it was carefully split open to avoid crushing any res- woodlice were present (Figure 2c). The highest number ident arthropods and the arthropods found in them were of woodlice was found at the Wageningen site, where identified and counted. Species that were not possible to 5ofthe10sampledstemshadmorethan20woodlicein identify in the field were placed in vials in alcohol and iden- each stem. Earwig numbers were highly variable in the tified later. Counts were made visually in situ. sites visited in the western United States (Figure 2d). For instance, in Santa Fe, 6 out of the 11 stems with holes 2.3 | Data analysis contained earwigs (3 of these stems contained more than 40 earwigs each), whereas at two of the other three sites Data on plant variables (plant height, number of holes per earwigs were present but in small numbers (with none in stem, mean hole height) and arthropod numbers (D. radiella plants sampled at Cebollo Creek). In the Netherlands, the pupae, C. sosares mummies and earwigs) were analyzed distribution of earwigs was more even with more than using a mixed general linear model with continent as a 80% of the perforated stem being occupied with earwigs fixed factor and site as a random factor. Woodlice and (Figure 2d). Overall, the number of earwigs in cow pars- mirid numbers were not statistically analyzed as woodlice nip and hogweed stems did not statistically differ were only found in hogweed stems in the Netherlands and between the western United States and the Netherlands, mirids were found in only 8 of the 91 stems with holes. probably because of high variability between sites (F Data were log-transformed when necessary to meet 1, =3.23,p = 0.12). Native mirids were only found in assumptions of normality and homoscedasticity based on 6.2 low numbers in both the Netherlands (3) and the United visual inspection of the residuals. Spearman's rank- States (8). correlation tests were conducted to reveal whether plant Neither plant height nor mean height of the holes correlated traits and number of holes correlated with arthropod num- with the number of webworms, mummies or woodlice found in bers. Data were analyzed using Genstat 19.1 (VSN Inter- perforated stems (Spearman's rank correlation test, all p-values national Ltd, Hempel Hempstead, UK). >.05). However, the number of webworm pupae, mummified pupae, earwigs and woodlice, respectively, correlated positively

3 | RESULTS with the number of holes per stem (ρ80(webworm pupae) = 0.50, p < .001; ρ80(mummies) = 0.42, p < .001; ρ80(earwigs) = 0.38, 3.1 | Numbers of Depressaria radiella, p < .001; ρ80(woodlice) = 0.27, p = .015). Copidosoma sosares and other arthropods in stems of plants 4 | DISCUSSION In total, we sampled 91 plants with D. radiella holes in their stems, 44 in the western United States and 47 in the Netherlands In this study, we found that all eight sampled populations of over the 8 populations. The two plant species, H. sphondylium the two Heracleum species, D. radiella and its parasitoid in the Netherlands and H. maximum in the western United C. sosares were present in varying abundance. Stems of the

States, were similar in height (F1, 4.9 = 1.10, p = 0.34; United two plants often contained multiple pupae/mummies of the States: 129 ± 9 cm [mean ± SE]; the Netherlands 141 ± 7 cm). host and parasitoid, respectively with multiple holes chewed The mean number of holes made by D. radiella larvae as well by the caterpillars being recorded. The number and average HARVEY ET AL. 663

D. radiella C. sosares FIGURE 2 Mean (±SE) number 12 (a) pupae 4 (b) mummies D. radiella pupae (a), C. sosares mummies (b), woodlice (c) and earwigs 10 3 (d) in perforated stems of Heracleum 8 maximum plants sampled at four sites in the western United States (bars on 6 2 the left) and H. sphondylium sampled at 4 four sites in the Netherlands (bars on 1 the right). At each site, arthropods were 2 counted in the stems of 9–16 plants 0 with holes 0

20 (c) Woodlice 25 (d) Earwigs

20 15 Mean no. individuals per stem Mean no. 15 10 10

5 5

0 0

Country and site height of the holes chewed by D. radiella larvae did not vary and 1919 on the west coast (Seattle, Washington) but it rap- significantly between the American and European Heracleum idly spread inland across the continent primarily via human species. Furthermore, although the number of pupae and/or transport (Wirth et al., 1998). When it first arrived in the mummies did vary between plant populations, this difference Rocky Mountains is unknown, but it clearly has become was not based on whether the insects were of invasive or native well established in isolated populations of cow parsnip, for- status. Clearly, both D. radiella and C. sosares are now well ming a new novel interaction with this plant mediated established in Rocky Mountain populations of H. maximum, through the presence of D. radiella. For instance, large num- although it is not known how long they have been associated bers of F. auricularia occupied stems of cow parsnip plants with this plant there or from which European populations they from the Santa Fe National Forest (New Mexico) location, originate although this is currently under investigation in the with some stems containing up to 60 of these insects. Ode lab. In a previous study with Dutch hogweeds, we found that Holes excavated in plant stems by mature caterpillars of webworm infestations are necessary for other arthropods to D. radiella were utilized by a range of other arthropods to access the interior of the stems; in the absence of webworm- gain access to the interior of the stem. Moreover, there was excavated holes, the stems are “clean” (Harvey et al., 2016). some overlap in the identity of the species colonizing these Once inside the stems, the duration of stem occupancy by stems from the native and new ranges of D. radiella. Ear- D. radiella, C. sosares and other arthropods that subse- wigs (Forficula auricularia), which are native to Europe but quently enter the stems appears to be highly variable. For also exotic in the United States (Tourneur & Meunier, 2019; instance, webworms and C. sosares only remain in the stem Wirth, Le Guellec, Vancassel, & Veuille, 1998), were recov- during their pre-pupal and pupal development (around ered from stems in all of the European H. sphondylium 2–3 weeks; Harvey et al., 2016). Adult moths and parasit- plants and three out of four of the American populations of oids emerge from the holes after eclosion and overwinter in H. maximum plants. Forficula auricularia was first recorded the surrounding vegetation. However, earwigs, woodlice and in the United States in 1912 on the east coast (Rhode Island) other arthropods appear to spend much more variable and 664 HARVEY ET AL. perhaps longer periods inside of the stems, lasting from sev- (n = 4) or because climatic conditions during the season in eral weeks to months, although this has not yet been fully which the insects were sampled in 2017 were less favorable determined. Occupancy of the stems offers the different for the hosts and parasitoid in the Netherlands (i.e., spring arthropods refuge from extreme abiotic conditions (e.g., low was hot and dry). temperatures, drought, heavy rainfall) as well as food, shel- The Heracleum is represented by around 60–70 ter and perhaps escape from a wider range of natural ene- species worldwide, most of which are native to Eurasia mies that occur in the adjacent habitat. Despite that, (Jahodová, Trybush, Pyšek, Wade, & Karpa, 2007). Only mummies of C. sosares as well as woodlice inside of the one, the cow parsnip (H. maximum), is native to North plant stems are occasionally eaten by earwigs, which in turn America. Both the cow parsnip and the small hogweed serve as prey for clubionid spiders. (H. sphondylium) are very closely related plants and until Our results thus show that D. radiella has not only recently were considered as a single species. Despite their become reestablished with its most important specialist natu- morphological and presumably chemical similarity (produc- ral enemy (C. sosares) in parts of the United States, but that ing furanocoumarins; Berenbaum & Zangerl, 2006; Johnson, one of two species that most often colonizes D. radiella- Webster, & Gray, 2013), the habitats in which both species infested stems of hogweeds in Europe, F. auricularia, has grow are often very different. In the Netherlands of which also reestablished its association with webworms on native most of the land is at sea level, H. sphondylium is abundant cow parsnips. By contrast, the woodlouse Porcelio scaber, and grows in disturbed habitats such as roadsides and on the which is native to Europe but has established in much of the margin of agricultural fields (personal observations). By United States, was nevertheless absent from stems of contrast, H. maximum is more sparsely distributed and grows H. maximum despite being abundant in stems of European at higher elevations in the western United States in well H. sphondylium. This result suggests that elevation and/or shaded and moist forest meadows, often among aspen habitat-related differences between the American and stands. Despite this veritable isolation, and the fact that European locations may be an impediment for the coloniza- populations of cow parsnip are often highly fragmented, tion of P. scaber (but clearly not for F. auricularia or D. radiella, its parasitoid C. sosares and the earwig C. sosares). In addition to earwigs, stems of H. maximum F. auricularia have been able to successfully colonize the and H. sphondylium damaged by D. radiella also contained plant in the Rockies up to at least 2,700 m. Our result illus- smaller numbers of closely related bugs (Miridae) that were trates the ability of some highly specialized invasive native to each continent. Our results also suggest that there species—in this case a herbivore and its parasitoid—to find is some congruence in the utilization of webworm-damaged veritable “needles in haystacks” (i.e., a suitable species of stems in both the native and invasive ranges of D. radiella native food plant) when colonizing new habitats. In turn, for certain arthropod taxa. A previous study in the Nether- organisms associated with them in their native ranges are lands (Harvey et al., 2016) also found that, in addition to also able to pick up where they left off and to recolonize earwigs and woodlice, stems of H. sphondylium damaged by microhabitats provided for them by the invader. D. radiella also harbored moderate numbers of a spider, Previous work has shown that, at least in its native range, Clubiona phragmitis (Clubionidae) that was absent from the F. auricularia is a potentially important biological control samples collected in 2017. However, an unidentified species agent of various pests in orchards including leaf-curling midges of clubionid spider that was very similar to C. phragmitis and aphids (He, Wang, & Xu, 2008; Mueller, Blommers, & was found in stems of H. maximum in two of the American Mols, 1988; Nicholas, Spooner-Hart, & Vickers, 2005). Vari- populations (Cebolla Creek CO, Spring Creek CO). ous methods to augment the overwintering survival of earwigs Copidosoma sosares is probably the most important nat- in orchards have been described (Carroll & Hoyt, 1984). In the ural enemy of D. radiella in Europe. It has been introduced New Mexico location, we found that several cow parsnip plants into parts of the United States as well, although mostly west with holes excavated by webworms the previous year con- of the Mississippi River (Lampert, Zangerl, Berenbaum, & tained several to many earwig adults and nymphs at least Ode, 2008; Ode, Berenbaum, Zangerl, & Hardy, 2004). 12 months later. The ability of intact plants to persist through Here, we found it present in all eight of the Netherlands and winter may be influenced by abiotic factors such as moisture, U.S. plant populations surveyed, although in highly variable wind and temperature. In the Netherlands, which has a mari- abundance. In fact, numbers of C. sosares mummies time climate, hogweeds are primarily transient and the stems appeared to be as high, or even higher, in some of the quickly degrade in early winter and fall during storms. How- U.S. populations of H. maximum than in the Dutch ever, in pilot studies we found that artificial holes perforated populations of H. sphondylium. However, this observation into hogweed stems were also used by earwigs, woodlice and should be interpreted with caution, because it could be due other arthropods in the same way as webworm-chewed holes. to the small number of populations sampled in each country Experiments using hogweed stems with artificially excavated HARVEY ET AL. 665 holes that are externally treated with chemical preservative are REFERENCES planned in which the stems are placed in orchards and moni- Berenbaum, M. R., & Zangerl, A. R. (2006). 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