Oecologia DOI 10.1007/s00442-013-2718-4
Plant-microbe-animal interactions - Original research
Reduced seed predation after invasion supports enemy release in a broad biogeographical survey
Eva Castells · Maria Morante · José M. Blanco-Moreno · F. Xavier Sans · Roser Vilatersana · Anabel Blasco-Moreno
Received: 13 December 2012 / Accepted: 13 June 2013 © Springer-Verlag Berlin Heidelberg 2013
Abstract the Enemy Release (ER) hypothesis pre- suffered lower seed predation compared to those from the dicts an increase in the plant invasive capacity after being native populations, as expected under the ER hypothesis, released from their associated herbivores or pathogens in and this release was more pronounced in the region with their area of origin. Despite the large number of studies on the most recent introduction (Europe 0.2 % vs. Australia biological invasions addressing this hypothesis, tests evalu- 15 %). The insect communities feeding on S. pterophorus ating changes in herbivory on native and introduced popu- in Australia and Europe differed from those found in South lations and their effects on plant reproductive potential at a Africa, suggesting that the plants were released from their biogeographical level are relatively rare. Here, we tested the associated fauna after invasion and later established new ER hypothesis on the South African species Senecio ptero- associations with local herbivore communities in the novel phorus (Asteraceae), which is native to the Eastern Cape, habitats. Our study is the first to provide strong evidence of has expanded into the Western Cape, and was introduced enemy release in a biogeographical survey across the entire into Australia (>70–100 years ago) and Europe (>30 years known distribution of a species. ago). Insect seed predation was evaluated to determine whether plants in the introduced areas were released from Keywords enemy release hypothesis · Herbivory · herbivores compared to plants from the native range. In Insects · Senecio · Reproductive potential South Africa, 25 % of the seedheads of sampled plants were damaged. Plants from the introduced populations Introduction
Communicated by John Lill. Biological invasions are one of the major causes affecting biodiversity worldwide (Pimentel et al. 2000). The intro- E. Castells (*) · M. Morante Facultat de Veterinària, Unitat de Toxicologia, Departament de duction of an exotic plant into a new habitat can strongly Farmacologia, Terapèutica i Toxicologia, Universitat Autònoma affect the composition, structure and functioning of the de Barcelona, 08193 Bellaterra, Catalonia, Spain invaded ecosystem (Vitousek et al. 1996; Pimentel et al. e-mail: [email protected] 2000) and may drive evolutionary changes in the native J. M. Blanco‑Moreno · F. X. Sans species (Maron and Vilà 2001; Siemann et al. 2006). Not all Facultat de Biologia, Departament de Biologia Vegetal, species introduced into new habitats become invasive, how- Universitat de Barcelona, Avda. Diagonal 643, 08028 Barcelona, ever (Richards et al. 2006). Of the many hypotheses that Catalonia, Spain attempt to unravel the factors affecting potentially invasive R. Vilatersana alien species, those involving the role of herbivores in con- Botanic Institute of Barcelona (IBB-CSIC-ICUB), Passeig de trolling plant populations predominate (Colautti et al. 2004; Migdia s/n, 08038 Barcelona, Catalonia, Spain Hierro et al. 2005; Gurevitch et al. 2011). The most frequently invoked hypothesis for the success A. Blasco‑Moreno Servei d’Estadística Aplicada, Universitat Autònoma de of invasive species is the Enemy Release (ER) hypothesis Barcelona, 08193 Bellaterra, Catalonia, Spain (Elton 1958). This hypothesis predicts that alien plants will
1 3 Oecologia be more successful when colonizing a new environment appropriate to determine realized (not merely potential) due to being released from herbivores and pathogens in herbivore-induced selective pressures. Due to the high spa- their area of origin. The ER hypothesis is based on three tial variation in the interactions between plants and herbi- components (Keane and Crawley 2002): (1) plant popula- vores (Kolb et al. 2007), comprehensive tests of the enemy tions are regulated by their associated enemies in the indig- release hypothesis should cover large distribution areas of enous area; (2) herbivore pressure decreases after introduc- the plant species both in the native and the invasive range. tion into a novel range; and (3) the individual-level benefits Several authors have stressed the importance of bio- of enemy release to exotic plants translate into increased geographical comparisons when testing major hypothe- population size, geographic distribution, and overall inva- ses related to biological invasions (Maron and Vilà 2001; sive ability. Plants that are strongly regulated by herbivores Hierro et al. 2005), but this area of research has advanced in their areas of origin can experience immediate benefits little in recent years. We found 13 studies published to date after enemy release, with increased growth, reproductive that quantified in situ herbivory between native and intro- capacity, and survival (Colautti et al. 2004). duced populations in a replicated biogeographical survey A decrease in herbivore pressure on exotic plants, as pre- (Sheppard et al. 1996; Memmott et al. 2000; Fenner and dicted by the ER hypothesis, is not determined exclusively Lee 2001; Wolfe 2002; DeWalt et al. 2004; Prati and Boss- by the plants’ escape from the natural enemies left behind dorf 2004; Vilà et al. 2005; Cripps et al. 2006, 2010; Ebe- during an invasion. Once in the introduced range, alien ling et al. 2008; Adams et al. 2009; Williams et al. 2010; plants may be colonized by native herbivores from the novel Hinz et al. 2012). Of those, only four (Fenner and Lee habitat, a process known as Native Enemy Host Switch- 2001; Wolfe 2002; Prati and Bossdorf 2004; Cripps et al. ing (Keane and Crawley 2002; Agosta 2006). The diver- 2010) evaluated seed predation, which is more closely sity of consumers in each novel location limits the types related to plant fitness and population success (Kolb et al. and strengths of the interactions that are ultimately estab- 2007), and none covered a large distributional area across lished. For example, Lepidum draba, a herbaceous perennial the native and invasive ranges. These numbers contrast mustard, is associated with 16 phytophagous species in its markedly with the nearly 500 papers published in the last native range, 18 in its extended range, and 11 in its intro- 10 years that explicitly address the ER and its evolution- duced range; only 4 of these species are common to all three ary extension, the Evolution of increased Competitive Abil- regions (Cripps et al. 2006). When novel interactions as a ity (EICA) hypotheses (ISI Web of Science). Clearly, more result of host switching are quantitatively significant, exotic biogeographical studies of enemy release are needed. plants may never be released from herbivore pressure but Here, we conducted a biogeographical test of the second may merely exchange the species involved. The process of component of the ER hypothesis using Senecio pteropho- enemy release can be understood as the net effect of the loss rus DC (Asteraceae) as a model species. This species is a of associated enemies from the native range and the acquisi- perennial shrub native to the Eastern Cape and southern tion of fewer new enemies in the introduced range (Colautti KwaZulu-Natal provinces in South Africa (Hilliard 1977). et al. 2004; Verhoeven et al. 2009). Its range expanded to the Western Cape during the early The fact that an important element of the ER hypothesis twentieth century (Levyns 1950). Introduced into Australia (i.e., host switching) strongly depends upon the biotic com- in 1908, S. pterophorus currently forms persistent popu- munity and the characteristics of the receiver ecosystem lations along the southeastern coast from Port Lincoln to (Graves and Shapiro 2003; Tallamy et al. 2010) highlights Melbourne and around Sydney and Newcastle in New the importance of studies that account for this geographic South Wales (The Council of Heads of Australasian Her- mosaic of species assemblages. Commonly performed baria 1999–2012). In continental Europe, S. pterophorus experiments addressing the ER hypothesis include labora- was first found in 1982 near Barcelona in the northeastern tory bioassays, which determine the preference and perfor- Iberian Peninsula (Casasayas 1989), and additional popula- mance of selected phytophagous species feeding on plants tions in the Mediterranean basin were found in 1990 on the from the native and introduced ranges (Caño et al. 2008; Ligurian coast in northwestern Italy (Barberis et al. 1998). Schaffner et al. 2011), and common-garden experiments Preliminary studies using neutral markers have shown that performed in a single area, usually in the invasive range populations from Australia and Europe are not geneti- (Agrawal and Kotanen 2003; but see Maron et al. 2004). cally related; thus, the colonization of the two continents Although these experiments can help to determine levels occurred independently (Vilatersana et al., unpublished). of plant resistance against certain herbivores, they do not We performed a biogeographical survey designed to inform on the actual plant–herbivore interactions estab- cover a substantial portion of the distribution of S. ptero- lished under field conditions. Biogeographical surveys phorus and to adequately compare seed predation between comparing in situ herbivory on native and alien plant popu- native and introduced populations. The relatively restricted lations in areas where the plants naturally occur are more worldwide distribution of S. pterophorus enabled us to
1 3 Oecologia conduct a complete biogeographical survey, determining populations have been recorded in Sydney and Newcastle, in situ herbivory on S. pterophorus in its native, expanded, New South Wales, since 1987 (The Council of Heads of and invaded ranges. The different colonization histories Australasian Herbaria 1999) (Fig. 1). In South Australia, in Australia (>70–100 years) and Europe (>30 years) and S. pterophorus causes heavy productivity losses in agri- the native versus expanded ranges in South Africa allowed cultural areas, and it is a strong competitor that excludes us to explore the effects of time since introduction and of native species in natural communities and interbreeds with distance from the source on herbivore release. We aimed several related native species, thus reducing the diversity to answer the following question: are S. pterophorus plants of the invaded areas (Parsons and Cuthbertson 1992). In from the extended and introduced ranges released from her- 1994, S. pterophorus was classified as a Declared Noxious bivore predation compared to plants from the native range, Weed subject to eradication by the Department of Primary resulting in greater reproductive potential? Industries, Victoria (Australia). The first European populations of S. pterophorus were found around wool mills in the United Kingdom in 1913 Materials and methods (Preston et al. 2002), but its presence was erratic and infre- quent, with only eight records from 1913 to 1986. After Studied species being absent from the UK for 30 years, S. pterophorus is now considered extinct in that country. The introduction Senecio pterophorus is a perennial shrub between 0.4 and of S. pterophorus into continental Europe is comparatively 2 m in height. The capitula, which are up to 1.5 cm in diam- recent. First recorded in 1982 near Barcelona, northeast- eter with c.13 female ligulate florets measuring from 2 to ern Iberian Peninsula (Casasayas 1989), S. pterophorus is 4 mm around the periphery, are grouped into terminal cor- mainly found in disturbed riverbeds and eutrophic waste ymbose synflorescences (Hilliard 1977). The seeds (techni- areas, where it can form very dense populations of approx- cally achenes or cypselae) are approximately 1.5 mm long, imately three individuals/m2 (Sans et al. 2004). The larg- cylindrical, somewhat angular and minutely hairy over the est populations occur at the Ripoll River in Sabadell, the surface. The flowering period may extend from late spring most significant textile-manufacturing area in Spain during to mid-autumn (Levyns 1950) but peaks during 2–3 weeks the nineteenth and twentieth centuries. From 1951 to 1986, in early summer, when all plants in a population bloom Spanish companies processed 208 metric tons of unwashed synchronously (Morante et al., unpublished). This spe- wool imported from South Africa and Australia (Dirección cies produces a large number of seeds (up to 1,200 heads/ General de Aduanas de España 1951–1986), suggesting individual; Morante et al., unpublished), but its population that S. pterophorus may have been accidentally introduced viability is strongly limited by low seedling emergence and to Spain via sheep wool used in the textile industry. Since establishment (Sans et al. 2004). 1995, this species has been widely reported at numerous localities in the northeastern Iberian Peninsula (Chamorro Distributional area and invasion history et al. 2006) (Fig. 1). At present, S. pterophorus grows in natural and semi-natural areas, including open forests, Senecio pterophorus is indigenous to an area extend- road margins, and abandoned fields in Sant Llorenç de ing from the eastern parts of the Eastern Cape Province Munt i l’Obac Natural Park (E.C., personal observation) to the southernmost part of the KwaZulu-Natal Province and Montseny Natural Park (Morante et al., unpublished). (Hilliard 1977) (Fig. 1). In its native range, S. pteropho- This species has also been found in western Liguria, north- rus forms scattered populations in forest margins, grass- western Italy, since 1990 (Barberis et al. 1998). The known lands, and fynbos, but it also grows in ruderal habitats, distribution of S. pterophorus in Italy extends from Savone, such as roadsides. This species was introduced into the 45 km south of Genova, to Ventimiglia, near the French Western Cape Province around 1918 (Levyns 1950). The border (Barberis et al. 1998) (Fig. 1). Although its geo- earliest records of S. pterophorus in Australia date to graphical range in Europe remains limited, S. pterophorus 1908 and 1909 in Melbourne, Victoria, but the absence is most likely expanding there, slowly spreading into less- of herbarium records during the following three decades disturbed communities, such as grasslands, shrublands, and suggests that the species may have failed to establish suc- forests (Chamorro et al. 2006). cessful populations in that area. In 1935, S. pterophorus was found in Port Lincoln, South Australia. From there, Biogeographical survey it spread to Adelaide Hills and southeast to Melbourne, Victoria, where it reached high levels of infestation dur- The survey was planned with two purposes: (1) to cover the ing the 1970s (Parsons and Cuthbertson 1992; The Council entire known distribution of S. pterophorus, including its of Heads of Australasian Herbaria 1999–2012). Scattered native, expanded, and introduced ranges; and (2) to target
1 3 Oecologia
SOUTH AFRICA KZN Durban 17 16 19 14 15 18 13
12 ECP 100 Km 10 11
7 6 8 9 5 1 WCP Port Elizabeth 2 3 Cape 4 Town
AUSTRALIA
SA NSW 2
6 1 Sydney 3 9 8 4 Adelaide 5 7 200 Km VIC
13 10 11 Melbourne 12 1 Sampled localities
Distribution based on literature
EUROPE
LIG Genova
6 CAT 2 1
5 10 3 6 12 11 3 2 4 9 7 5 4 8 Barcelona 1
50 Km 25 Km
Fig. 1 Locations of populations of S. pterophorus surveyed in the regions or states: in South Africa, ECP Eastern Cape, WCP Western native range (South Africa, populations 6–19), the expanded range Cape, KZN KwaZulu-Natal; in Australia, NSW New South Whales, (South Africa, populations 1–5), and the two invasive ranges (Aus- SA South Australia, VIC Victoria; in Europe, CAT Catalonia (Spain), tralia and Europe). All populations had reproductive individuals to LIG Liguria (Italy). The shaded area indicates S. pterophorus distri- which damage of herbivores on seedheads and seeds could be evalu- bution based on herbaria databases and literature. Population numbers ated, except for populations 1 and 13 in Australia. Abbreviations for correspond to the codes in Table 1
1 3 Oecologia the plants’ blooming period to evaluate herbivore damage reproductive individuals for which seed predation could to reproductive plant parts. Distributional data for S. ptero- be assessed. In each population, we evaluated the habitat phorus were first obtained from the herbarium records of type, the sampled patch size, the level of disturbance (low, the South African National Biodiversity Institute, the Aus- medium, high), the number of S. pterophorus individuals tralian National Herbarium (The Council of Heads of Aus- (<25, 25–100, 100–500, and >500 individuals), the percent tralasian Herbaria 1999–2012), the Biodiversity Data Bank cover of S. pterophorus (<5, 5–25, 25–50, 50–75, and 75– of Catalonia (Font 2012), and the literature (Hilliard 1977; 100 %), and the percentage of individuals at the seedling Barberis et al. 1998; Chamorro et al. 2006; Caño et al. stage as an estimate of population recruitment (<1, 1–5, 2008; Morante et al., unpublished). The consulted sources 5–25, 25–50, 50–75, and 75–100 %) (Table 1). Climate provided contradictory information on the native area of S. data (mean annual temperature and precipitation) for each pterophorus in South Africa. While Hilliard (1977) stated location were obtained from the WorldClim database (Hij- that the plant “is found in the eastern parts of the Transkei mans et al. 2005) (Table 1). and just enters Natal across its Southern border”, the distri- Ten individual plants at reproductive stage were sampled bution of S. pterophorus obtained from herbarium records from each population to evaluate herbivore damage. The exceeded these limits. Moreover, some records identified as selected individuals were scattered across the plant patch in S. pterophorus in the South African National Biodiversity order to cover the maximum area of distribution and maxi- Institute herbarium may correspond to other Senecio spe- mize the distance between individuals. A total of 465 plants cies with coincident flowering times and similar morpholo- were surveyed. We collected 20 seedheads from each plant gies (e.g., S. polyanthemoides Sch. Bip. and S. juniperinus to quantify the proportion damaged by insect herbivores. L.f.) (M. Welman, South African National Herbarium in To ensure homogeneous sampling across populations and Pretoria, personal communication). To ensure that we cov- regions, ripe seedheads were chosen when possible. Seed- ered the entire native range of S. pterophorus, we searched heads were dissected on the day of collection by opening outside the limits cited by Hilliard (1977), including the area them longitudinally through the receptacle, spreading the from Cape Town (Western Cape Province) to Port Elizabeth seeds on a surface, and recording the presence of seed-eat- (Eastern Cape Province) and up to 225 km north of Durban ing insects therein. A seedhead was recorded as “damaged” (KwaZulu-Natal Province). Sampling was conducted during when predated by phytophagous insects, regardless of their the flowering period of S. pterophorus, in December 2009 number and developmental stage. We calculated the per- and January 2010 in the southern hemisphere (South Africa centage of damaged heads per individual plant. Insects were and Australia) and in July 2010 and July 2011 in the northern raised to adults for identification when possible.T axonomic hemisphere (Catalonia and Liguria). identification was performed by Jordi Dantart (Societat Cata- Senecio pterophorus populations were sought near loca- lana de Lepidopterologia, Spain) (Lepidoptera) and Bernhard tions where the species had been previously reported. We Merz (Muséum d’Histoire Naturelle, Switzerland) (Diptera). attempted to choose populations that were spread across Other species collected at immature stages (larvae) that were the territory, including populations from the distributional not successfully raised to adults during the collecting trip limits. We located the species in most of the searched areas were classified at the lowest possible taxonomic level. (Fig. 1). In South Africa, S. pterophorus was absent from To determine the frequency of predated seeds within Cape Town to Port Elizabeth (Eastern Cape) and north of capitula, five heads from each of five individuals per popu- Port Shepstone (KwaZulu-Natal), confirming the distribu- lation (8 populations from South Africa, 5 from the West- tion proposed by Hilliard (1977). The plant was not found ern Cape, 12 from Australia, and 12 from Europe) were in some dry areas in South Australia, including York Pen- collected and stored in separate envelopes. Only healthy, insula and Murray Bridge. In the State of Victoria, where ripe heads with no external damage were collected. These S. pterophorus is declared a noxious weed, the plant was samples could not be processed during the collecting trip; extremely difficult to find, possibly due to the control therefore, the heads were frozen for 24 h to prevent fur- efforts by local authorities. ther herbivore damage. In the laboratory, the heads were A population was defined as a cluster of 15 or more dissected, and the total number of seeds (achenes) was adult individuals. In South Africa and Australia, we chose recorded. Each seed was assigned to one of the follow- populations at least 30 km apart; in Catalonia and Liguria, ing categories: damaged, showing signs of predation; where the plant is more localized, we choose populations at aborted, having an undeveloped embryo; and filled, having least 5 km apart. A total of 50 populations were surveyed, an undamaged, well-developed embryo. A total of 68,621 including 14 native (Eastern Cape and KwaZulu-Natal, achenes (23,610 from South Africa, 21,035 from Australia, South Africa), 5 expanded (Western Cape, South Africa), and 23,976 from Europe) were analyzed. The seeds were and 31 introduced (13 in Australia and 18 in Europe) categorized by inspection under a stereomicroscope at (Fig. 1). Of these populations, a total of 48 contained 10–60 magnification (SMZ800; Nikon). The proportion × 1 3 Oecologia e 0 7 2 0 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 N o. sampled ind. 10 10 10 10 10 10 10 10 10 A frica) and intro - M M M M M H M M M M H M M M M M H M H Disturb. Disturb. L evel M L , M M L H , M L M M L L H H M d 1–5 n/a <1 <1 1–5 1–5 <1 5–25 n/a n/a <1 <1 n/a 1-5 1–5 1–5 <1 1–5 25–50 S eedlings (%) <1 1–5 <1 <1 50–75 <1 50–75 5–25 <1 5-25 75–100 <1 <1 c over S P C over (%) 5–25 5–25 5–25 25–50 25–50 5–25 5–25 50–75 50–75 75–100 75–100 5–25 5–25 5–25 5–25 5–25 5–25 25–50 5–25 5–25 5–25 50–75 25–50 5–25 <5 50–75 <5 <5 <5 5–25 25–50 <5 Pop. S ize ( N o. ind.) 25–100 >500 25–100 100–500 25–100 25–100 25–100 >500 >500 >500 25–100 25–100 25–100 25–100 <25 25–100 100–500 100–500 100–500 25–100 >500 >500 >500 <25 100–500 25–100 25–100 100–500 100–500 25–100 <25 25–100 frica), the expanded range (Western C ape, S outh range (Western A frica), the expanded 50 10 50 75 25 35 10 50 25 50 75 30 30 30 20 25 30 15 15 10 400 100 100 125 150 200 125 100 200 125 600 Patch size Patch (m) 4700 H abitat type Perennial grassland M eadow G rassland G rassland Perennial grassland G rassland M eadow M eadow M eadow M eadow G rassland M eadow Perennial grassland Perennial grassland S hrubland Perennial grassland A nnual grassland A nnual grassland A nnual grassland Perennial grassland Perennial grassland A nnual grassland S hrubland A nnual grassland S chubland Forest Forest Plantation Forest S hrubland Perennial grassland Perennial grassland b 440 741 548 595 593 802 713 912 827 907 856 787 927 834 786 825 996 589 509 531 516 399 801 616 867 757 785 960 873 1,086 ainfall R ainfall (mm) 1,092 1,101 b emp. 16.4 18.5 16.1 18.2 18.2 17.9 17.4 16.0 15.9 15.6 15.6 16.0 15.6 15.5 16.9 16.4 14.7 16.2 16.5 17.9 16.0 16.2 16.2 16.4 14.6 13.0 14.9 13.3 12.9 14.5 13.7 17.2 T (° C ) 6 6 b 61 26 23 13 13 15 84 15 48 668 124 535 471 716 884 176 326 114 262 602 257 171 223 121 1116 1076 1242 1261 1141 1200 A lt. (m) S 150º52 ′ E 33º41 ′ S 25º49 E 33º19 ′ S 26º32 E 33º36 ′ S 26º24 E 33º36 ′ S 26º52 E 32º47 ′ S 26º52 E 32º40 ′ S 28º00 E 31º51 ′ S 28º30 E 31º11 ′ S 29º26 E 30º50 ′ S 29º15 E 30º50 ′ S 29º35 E 30º57 ′ S 28º57 E 30º42 ′ S 28º51 E 30º31 ′ S 29º46 E 30º23 ′ S 29º38 E 33º47 ′ S 18º52 E 34º07 ′ S 18º23 E 34º09 ′ S 19º01 E 34º24 ′ S 19º11 E 33º56 ′ S 18º26 E 33º45 ′ 32º52 ′ S 151º41 E 34º33 ′ S 135º49 E 34º30 ′ S 135º25 E 34º48 ′ S 135º46 E 33º55 ′ S 136º14 E 35º20 ′ S 138º36 E 34º57 ′ S 138º42 E 34º40 ′ S 138º51 E 37º35 ′ S 140º28 E 37º55 ′ S 142º02 E 38º17 ′ S 145º11 E 38º04 ′ S 145º39 E C oordinates N N N N N N N N N N N N N N E E E E E I I I I I I I I I I I I I Origin a S 06 C ode S 07 S 08 S 09 S 10 S 11 S 12 S 13 S 14 S 15 S 18 S 19 S 16 S 17 S 01 S 02 S 03 S 04 S 05 A 01 A 02 A 03 A 04 A 05 A 06 A 07 A 08 A 09 A 10 A 11 A 12 A 13 own own yliff C olchester Population G rahamstown A lexandria Port A lfred H are Fort C ourtlands Umtentu Flargstaff M t. A B izana M ount Frere A ntioch Post S tafford’s Franklin G roenfonteinkop C ape T E lgin H ermanus C ape T Doonside N ewcastle Port L incoln Wangary L incoln N P H incks N P M t. C ompass C leland N P C P Warren M t. B urr M t. N apier P H astings G umbaya Park populations surveyed in the native range ( S outh in the native populations surveyed L ocations and habitat characterization of Senecio pterophorus EC P EC P EC P EC P EC P EC P EC P EC P EC P EC P EC P EC P KZ N KZ N W C P W C P W C P W C P W C P NS W NS W SA SA SA SA SA SA SA SA VI C VI C VI C 1 Table duced ranges ( A ustralia and E urope) L ocation S outh A frica A ustralia
1 3 Oecologia e 5 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 N o. sampled ind. H H M H M H H H M M L L H H H H M M Disturb. Disturb. L evel C atalonia ( S pain), LIG L igu - d n/a 50–75 5–25 <1 n/a n/a 5–25 <1 <1 <1 n/a n/a 1–5 25–50 25–50 <1 <1 <1 S eedlings (%) c over S P C over (%) 5–25 25–50 75–100 <5 5–25 50–75 5–25 <5 25–50 5–25 25–50 25–50 5–25 5–25 50–75 50–75 5–25 <5 Pop. S ize ( N o. ind.) 25–100 >500 >500 25–100 25–100 25–100 25–100 25–100 100–500 <25 <25 25–100 100–500 25–100 100–500 100–500 <25 <25 75 40 50 50 30 50 50 30 25 25 75 80 50 100 100 100 100 500 Patch size Patch (m) H abitat type iver bed R iver Forest S hrubland bed R iver A nnual grassland Wasteland A nnual grassland Wasteland bed R iver G rassland, Forest Forest Forest G rassland A nnual grassland A nnual grassland bed R iver A nnual grassland A nnual grassland b 549 722 717 589 631 667 594 599 662 654 798 822 846 807 794 812 804 884 ainfall R ainfall (mm) b new south whales, SA australia, VIC victoria; in E urope: CATA ustralia: NSW new emp. 16.3 15.6 15.6 16.3 15.3 15.1 16.1 16.3 14.5 14.9 14.2 13.0 14.7 14.2 14.4 15.7 15.7 14.5 T (° C ) b 20 66 51 61 10 14 21 30 144 288 295 124 413 332 519 622 172 283 A lt. (m) 41º04 ′ N 1º04 E 41º39 ′ N 2º42 E 41º37 ′ N 2º39 E 41º27 ′ N 1º59 E 41º36 ′ N 2º04 E 41º41 ′ N 2º12 E 41º31 ′ N 2º07 E 41º29 ′ N 2º10 E 41º35 ′ N 2º01 E 41º36 ′ N 2º05 E 41º43 ′ N 2º28 E 41º43 ′ N 2º24 E 44º08 ′ N 8º16 E 44º06 ′ N 8º07 E 43º56 ′ N 8º00 E 43º50 ′ N 7º51 E 43º49 ′ N 7º35 E 44º16 ′ N 8º25 E C oordinates I I I I I I I I I I I I I I I I I I Origin a C ode C 01 C 02 C 03 C 04 C 05 C 06 C 07 C 08 C 09 C 10 C 11 C 12 L 01 L 02 L 03 L 04 L 05 L 06 aggia kwazulu-natal; in ECP eastern cape, WCP western KZN kwazulu-natal; Population C ambrils Palafolls C alella C astellbisbal C astellar V. B igues i R iells S abadell R ipollet M atadepera S ant L lorenç N P C ampins N P M ontseny Pietra L igure Zucarello Pontedassio A rma di T Ventimiglia L igure Vado continued S outh A frica: CAT CAT CAT CAT CAT CAT CAT CAT CAT CAT CAT CAT L I G L I G L I G L I G L I G L I G a ltitude, mean annual temperature and rainfall seedlings in the population, n/a data not available of S. pterophorus abundance r elative c ode assigned to each population. Population number corresponds Fig. 1 in the sampling area of S. pterophorus cover r elative on capitula and seeds that were sampled to assess herbivory individuals n umber of reproductive L ocation E urope 1 Table low, M medium, H high L low, I introduced; Disturbance level: E expanded, ria (Italy), Origin: N native, In a b c d e
1 3 Oecologia of damaged seeds within a head was expressed relative to introduced regions (Australia, 140.7 m; Europe, 192.5 m) the total number of achenes after excluding the aborted (South Africa–Western Cape t 4.19; South Africa–Aus- = ones. tralia t 5.60; South Africa–Europe t 5.54; P < 0.001 for = = all paired-comparisons, ANOVA) (Table 1). Mean annual Data analyses temperature was significantly higher in the native range in South Africa (16.6 °C) than the introduced ranges in Aus- Differences among regions were tested using an ANOVA tralia (15.1 °C) and Europe (15.1 °C) (South Africa–Aus- for continuous variables (altitude, temperature, and pre- tralia t 3.25, P 0.011; South Africa–Europe t 3.52, = = = cipitation) and a likelihood-ratio test for categorical vari- P 0.005, ANOVA) but did not differ between the native = ables (population size, percent cover of S. pterophorus, and extended ranges (16.1 °C) (South Africa–Western Cape percentage of seedlings, and disturbance level). To evalu- t 0.80, P 0.85, ANOVA). Mean annual rainfall, S. pter- = = ate differences among regions in seedhead predation, a ophorus population size, percent cover, and seedling rela- zero-inflated negative binomial (ZINB) mixed model was tive abundance were similar across all four regions (data calculated considering damage as the response variable, not shown). Disturbance level differed significantly among region as a fixed explanatory variable, and population as regions (χ2 18.36, P 0.005, likelihood ratio test), with = = a random factor. We used this type of model due to the the highest levels found in European populations (Table 1). large number of zero values in the data (Hall 2000). A Plants in the native range had an average of 25.2 % of ZINB is a mixture model for count data that incorporates their seedheads damaged by herbivores (Fig. 2). In the two sources of zero values: a negative-binomial distribu- expanded range, herbivores attacked 33.4 % of the heads tion for the process generating the counts (NB, seedhead per plant, but this value did not differ significantly com- damage 0) and a zero-inflation process that separately pared to the native area (NB: F 1.54, P 0.221; ZI: ≥ = = models the occurrence of extra zero values not accounted F 2.98, P 0.091). In Australia, where S. pteropho- = = for by the process generating the counts (ZI, extra undam- rus has coexisted 70–100 years with the native fauna, aged seedheads). Accordingly, each comparison between herbivory levels were lower than in the native area (NB: regions resulted in two P values, one for the average seed- F 5.81, P 0.020; ZI: F 4.69, P 0.035), with an = = = = head damage and one for the zero inflation. Next, a gener- average of 15.4 % of the seedheads damaged (Fig. 2). alized linear model (GLM) was calculated separately for In Europe, where S. pterophorus was introduced more each region to compare the populations therein. A Levene recently compared to Australia (>30 years ago), only 0.2 % test was conducted to identify differences in the variance of the seedheads per plant were damaged by herbivores, across regions. significantly lower than in South Africa (NB: F 13.43, = Differences among regions in the frequency of her- P 0.001; ZI: F 110.62, P < 0.001) or Australia (NB: = = bivore-damaged seeds within heads were assessed by a F 6.72, P 0.013; ZI: F 85.13, P < 0.001) (Fig. 2). = = = GLMM (generalized linear mixed model). Region and Cross-regional comparison of the extra occurrence of zero population nested within region were considered fixed values (ZI), which indicates the absence of plant–herbivore factors, and the individual plant was considered a random associations, showed that the South African populations factor. A negative binomial distribution was used to model had significantly fewer predation-free seedheads compared the total number of seeds, and a binomial distribution was to the Australian and European populations. The variances used to model the percentage of aborted seeds and the per- of the frequency of damaged seedheads differed signifi- centage of filled seeds.T he percentage of damaged seeds cantly among regions (F 27.02, P < 0.0001, Levene test). = was modeled using the variance-transformation proposal of The highest variability, as estimated by the standard devia- McCullagh and Nelder (1989), which enabled us to control tion (SD), was found in the native and extended ranges the variability in these data. The statistical analyses were (SD 19.73; SD 20.03), followed by South Africa = Western Cape = performed using SAS System® v.9.2 (SAS Institute, Cary, the introduced ranges (SD 14.96; SD 1.29). Australia = Europe = NC, USA). For all statistical tests, a nominal significance The number of achenes per head varied across regions, level of 5 % (p < 0.05) was applied. A Tukey adjustment but these differences were not related to the native or inva- was performed for multiple tests. sive status of the populations (Fig. 3a). The seed predation pattern was similar to the head predation pattern (Fig. 3b). Plants from the native populations (South Africa) showed Results significantly higher seed predation compared to plants from the introduced populations (South Africa–Australia Populations of S. pterophorus in the native region (South t 14.90, P < 0.001; South Africa-Europe t 99.94, = = Africa) were located at a higher altitude (750 m a.s.l.) P < 0.001, GLMM) (Fig. 3b). However, in contrast to compared to populations in the extended (133 m) and the results found at the head level, achene predation was
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40 Native a 60 Expanded 35 Introduced 30 a 50 25
20 b
40 15 10
5 30 c 0
20 Damaged heads (%) Europe S.Africa Australia
10
0 L0 1 L0 2 L0 3 L0 4 L0 5 L0 6 S0 6 S0 7 S0 8 S0 9 S1 0 S1 1 S1 2 S1 3 S1 4 S1 5 S1 6 S1 7 S1 8 S1 9 S0 1 S0 2 S0 3 S0 4 S0 5 A0 2 A0 3 A0 4 A0 5 A0 6 A0 7 A0 8 A0 9 A1 0 A1 1 A1 2 C0 1 C0 2 C0 3 C0 4 C0 5 C0 6 C0 7 C0 8 C0 9 C1 0 C1 1 C1 2
South Africa Australia Europe
Fig. 2 Herbivory damage, estimated as the percentage of dam- Inserted graph shows herbivory damage by regions (mean SE). aged seedheads among populations from the native (South Africa), Different letters indicate significant differences between+ regions expanded (Western Cape, South Africa) and introduced regions (Aus- (P < 0.05) based on the Zero-Inflation process for the ZINB model tralia and Europe). Bars represent mean ( SE, n 10 individuals per for count data population). Population codes correspond+ to numbers= given in Fig. 1. higher in the extended range than in the native range (South Discussion Africa–Western Cape t 3.52, P 0.002, GLMM). = − = The percentages of aborted and filled seeds varied across Insect seed predation was significantly lower in S. ptero- regions but showed no pattern related to the native or inva- phorus growing in its introduced ranges (Australia and sive plant origin (Fig. 3c, d). Europe) than in plants in the native range (South Africa), The morphology of the collected insects and the analyses as predicted by the ER hypothesis. This pattern was con- of the damage to the heads and seeds showed that the her- firmed by two complementary measures of herbivore pre- bivores were similar for plants in the native and expanded dation: the frequency of damaged seedheads per plant, ranges but highly distinct in the invaded ranges. In the and the frequency of damaged achenes within a seedhead. native and expanded populations in South Africa, the phy- Similarly, previous biogeographical studies evaluating dif- tophagous insects included monkey beetles (Coleoptera: ferences across native and invaded ranges have mostly Scarabeidae, Hopliini) and other unidentified Lepidoptera, supported the ER hypothesis (Memmott et al. 2000; Fen- Diptera and Coleoptera. In Australia, 30.3 % of the predated ner and Lee 2001; Wolfe 2002; Prati and Bossdorf 2004; heads were damaged by Sphenella ruficeps (Macquart 1851) DeWalt et al. 2004; Vilà et al. 2005; Ebeling et al. 2008; (Diptera: Tephritidae), a species endemic to Australia that is Adams et al. 2009; Cripps et al. 2010), although in some monophagous on Senecio (Hardy and Drew 1996), while an cases this trend was not significant (Sheppard et al. 1996; additional 69.6 % of the damaged heads were attacked by Cripps et al. 2006; Williams et al. 2010; Hinz et al. 2012). various species of microlepidoptera, including members of However, the near complete absence of herbivory in some the family Pyralidae. In Europe, herbivore damage to seed- parts of the invaded range, as we found in Europe, has been heads was caused exclusively by microlepidoptera belong- rarely reported. ing to Pyralidae, such as the oligophagous species Phyci- We also evaluated herbivory levels on S. pteropho- todes albatella (Ragonot 1887), which is native to Eurasia rus in an extended distributional area, the Western Cape and is known to consume three genera within Asteraceae (South Africa). We considered these populations in a sep- (Senecio, Crepis, and Solidago) (Roesler 1973). arate category because S. pterophorus has been recently
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Fig. 3 Comparison of seed pro- 120 40 (a) (b) Native duction and viability in native, b Expanded expanded and introduced range 35 100 Introduced across regions: a total number bc c 30 a of seeds per head, b percentage -1 ab 80 a of damaged seeds within a head, 25 c percentage of aborted seeds, and d percentage of well-devel- 60 20 oped, undamaged, filled seeds 15 within a head. Bars represent 40 c
mean ( SE) for heads within No. seeds head 10 each region+ (n 200 for native Damaged seeds (%) = 20 South Africa, n 125 for West- 5 ern Cape, n 300= for Australia d and Europe).= Different letters 0 0 indicate significant differences between regions (P < 0.05) 80 70 (c) (d) 70 60 ab a 60 b b b 50 50 a a a 40 40 30 30
Filled seeds (%) 20 Aborted seeds (% ) 20
10 10
0 0
Europe Europe S. Africa Australia S. Africa Australia introduced to that area and thus may exhibit some traits natural enemies followed by a reassociation in the new common to cross-continental introductions, even though environment. Some examples of plants that escaped from these populations are relatively close to the area of ori- herbivory after invasion, but later reassociated with their gin. However, the genetic origin of these populations is coevolved specialist herbivores in a novel range, include unknown, and we cannot ignore the possibility that these Pastinaca sativa in Unites States and New Zealand and plants behave differently from their native counterparts. A Conium maculatum in United States. These species recent study analyzing six plant species (Engelkes et al. showed high herbivory in the introduced ranges where 2008) has suggested that species whose range is expand- they had reassociated with their natural enemies (Castells ing (for example, in response to climate change or habi- et al. 2005; Zangerl et al. 2008). tat availability) will experience reduced herbivory, as Predation levels following an invasion depend upon the expected for enemy release in intercontinental introduc- balance between the loss of interactions with herbivores tions. Contrary to these predictions, predation levels on S. native to the area of origin (escape from natural enemies) pterophorus in the Western Cape were higher than those and the establishment of new interactions with herbivores in the indigenous range, although the difference was sig- native to the novel habitat (native–enemy host switching) nificant only for the percentage of damaged achenes and (Colautti et al. 2004; Verhoeven et al. 2009). Novel asso- not for the percentage of damaged heads. The relatively ciations between non-coevolved plants and herbivores small distance between the native range and the extended are frequent in invaded communities (Keane and Crawley range may have facilitated the co-introduction of insect 2002; Graves and Shapiro 2003; Parker and Hay 2005; Tal- species from the native range. Alternatively, if the native lamy et al. 2010) and therefore may be an important com- insect species have a wider spatial distribution overlap- ponent of plant–herbivore networks in the invaded habitat ping with the extended range of S. pterophorus, plants (Colautti et al. 2004). However, very few studies have com- in the Western Cape may have had uninterrupted interac- pared insect identities and abundance between native and tions with herbivores, or experience a release from their invasive locations in a biogeographical survey (Cripps et al.
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2006), and thus the information available to date is not suf- shifts because time increases the probability of plant–her- ficient to determine whether herbivory levels in a novel bivore encounters and, potentially, the adaptation of local range are mostly explained by partial escape from associ- insects to new hosts (Hawkes 2007; Mitchell et al. 2010). ated insects in the indigenous range, by the establishment For example, invasive populations of the Chinese tallow of new interactions via host switching in the novel habitat, tree (Sapium sebiferum) in the United States were released or by a combination of both mechanisms. These different from herbivores only during the early stages of introduc- scenarios have no small consequences on the plant evolu- tion (Siemann et al. 2006). Similarly, herbivore richness tionary outcomes as new plant–herbivore associations may and abundance have been reported to increase with the alter the herbivore selection regimes, causing plant traits to time since the host plant introduction, reaching levels sim- evolve toward different traits in native and invasive com- ilar to those found on native plant species 30–200 years munities (Thompson 1994). following an invasion (Hawkes 2007; Brändle et al. 2008). Here, based on taxonomic identifications and the mor- Our results are consistent with this hypothesis, but we phology of non-identified insect species in the native and cannot reject the possibility that the higher levels of host introduced populations, we found that insects present in switching in Australia compared to Europe were due to S. pterophorus from Europe and Australia differed from other causes, such as the local composition of the biotic those in South Africa, indicating that plant populations in community. the two introduced areas had escaped from coevolved phy- This biogeographical survey was designed to capture tophagous species and established novel interactions with the spatial variability of the biotic community naturally herbivores from the introduced range. Host switching was encountered by S. pterophorus and its effects on the native particularly intense in Australia, the region with a longest and introduced populations. Our study is the first to show invasion history, compared to Europe. strong evidence of enemy release in a survey covering most Contrary to the assumption that generalist insects are of a species’ distributional area, including two independ- the main component of host shifting in invaded commu- ent areas of introduction. The different patterns of herbi- nities (Keane and Crawley 2002; Hinz et al. 2012), we vore predation in the two introduced areas are consistent found that monophagous species participated in a novel with the longer period of coexistence between S. pteropho- interaction. One of the most abundant insect species feed- rus and the local fauna in Australia compared to Europe. ing on S. pterophorus in Australia was the endemic spe- Whether the reduction of herbivory on the exotic S. ptero- cialist Sphenella rucifeps (Macquart 1851) (Diptera: phorus populations determines a higher invasion success Tephritidae). This fly, which develops and pupates within remains undetermined. Increased seed production due to seedheads, is monophagous on the genus Senecio and has lower herbivore damage is a good estimate of plant fitness, been reported to consume native (Senecio lautus and S. but benefits at the individual level do not necessarily trans- amygdalifolius) and exotic species (S. madagascariensis) late into enhanced population recruitment, growth, density, in Australia (Hardy and Drew 1996). Specialist herbivores and spatial distribution (Kolb et al. 2007). An analysis of that are adapted to feed on native plants may readily estab- the plant population dynamics in the native, expanded, and lish interactions with exotic congeners because they share invaded areas accounting for the time since plant introduc- a similar chemical composition that facilitates recogni- tion is necessary to elucidate the role of enemy release in tion, selection, and resistance (Verhoeven et al. 2009). The invasion success. presence of other native and introduced Senecio species in Australia may have facilitated host switching by the spe- Acknowledgments We thank the collaborators for providing data and helping during the collecting trips: Dr Jaco Le Roux (Stel- cialist S. rucifeps. lenbosch University, South Africa), Christina Potgieter (Univer- In addition to evaluating changes in herbivory after sity of KwaZulu-Natal, South Africa), Dr. Ian Thompson (Royal invasion, our study system also enabled us to test differ- Botanic Gardens, Melbourne, Australia), Tony Dold (Rhodes Uni- ences in seed predation between two cross-continental versity, South Africa), and David Wopula (South Africa). We thank Anna Escolà and Pere Losada for outstanding field and laboratory introductions with independent invasion histories. Plants assistance, Estíbaliz Palma for seed analyses, and Bernhard Merz in both non-native ranges experienced less herbivory (Muséum d’Histoire Naturelle, Switzerland) and Jordi Dantart (Cata- than those in native areas, but this release was more pro- lonia) for identification of insect specimens.M .M. has a FPI predoc- nounced in European individuals than in Australian indi- toral fellowship from Ministerio de Ciencia e Innovación (Spain). This research was conducted thanks to the financial support provided viduals. Higher levels of host switching in Australia com- to E.C. by Ministerio de Ciencia e Innovación (Spain) (GCL2008- pared to Europe may be explained by differences in the 02421/BOS) and Ministerio de Economía y Competitividad (Spain) time since the introduction of S. pterophorus. In Australia, (GCL2011-29205). X.S., E.C., J.M.B.M. and M.M. belong to the this species has coexisted with local fauna for at least 70– Agroecosystems Research group funded by Generalitat de Catalunya (Catalonia) (2009 SGR1058). The experiments comply with the cur- 100 years, approximately 50 years longer than in Europe. rent laws of the countries (Spain, Italy, Australia, and South Africa) A longer time since introduction may lead to more host in which the experiments were performed. The permits required for
1 3 Oecologia sampling were obtained from the corresponding authorities when Fenner M, Lee WG (2001) Lack of pre-dispersal seed predators in necessary. introduced Asteraceae in New Zealand. NZ J Ecol 25:95–99 Font X (2012) Vegetation and flora module. Biodiversity database of Catalonia.
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Prati D, Bossdorf O (2004) A comparison of native and introduced Tallamy DW, Ballard M, D’Amico V (2010) Can alien plants support populations of the South African Ragwort Senecio inaequidens generalist insect herbivores? Biol Invasions 12:2285–2292. doi:1 DC. in the field. In: Breckle SW, Schweizer B, Fandmeier A (eds) 0.1007s10530-009-9639-5 Results of the worldwide ecological studies. Heimbach, Stuttgart, The Council of Heads of Australasian Herbaria (1999–2012). Aus- pp 353–359 tralia’s virtual herbarium.
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