Biol Invasions DOI 10.1007/s10530-006-9010-z ORIGINAL PAPER Morphological and ecological traits promoting aphid colonization of the Hawaiian Islands Edward B. Mondor Æ Michelle N. Tremblay Æ Russell H. Messing Received: 13 March 2006 / Accepted: 22 March 2006 Ó Springer Science+Business Media B.V. 2006 Abstract Species introductions into novel habi- well suited to the Hawaiian subtropical climate, tats, especially island ecosystems, can have dev- thereby eliminating the need for sexual phases astating effects on ecosystem function and and egg-laying for overwintering. By under- stability. Though none are native, at least 96 standing the traits that enable aphids to success- aphid species can now be found on one or more of fully colonize remote islands, it is our hope that the Hawaiian Islands. As aphids cause direct plant protection efforts may be enhanced, thereby feeding damage and transmit plant viruses, it is reducing damage to native ecosystems. important to identify the traits that have enabled these particular species to successfully colonize Keywords Aphid Æ Aphididae Æ Congener Æ the archipelago. To address this question, nine Hawaii Æ Homoptera Æ Introduced species Æ morphological and ecological traits that may Invasive species Æ Life history Æ Non-indigenous contribute to successful colonization were as- species sessed for aphids present in Hawaii. As a com- parative null model, we assessed the same traits for heterospecific congeners which are not pres- Introduction ent in the archipelago, but are present elsewhere in the world. Here we report that traits with The introduction of, or colonization by, species higher frequencies among colonizing aphid spe- into regions that they did not previously occupy is cies are: small apterae size, broad host range, increasingly recognized as a key threat to biodi- anholocycly (i.e., permanent parthenogenesis), versity (Mack et al. 2000; Clavero and Garcia- and presence in continental USA. Small aphids Berthou 2005). Free from natural enemies, fun- arriving from the mainland US and capable of damental life history variables such as population feeding on numerous plant species may be inter- growth rate and survivorship are often enhanced, cepted less often by plant protection agents. It is resulting in dynamics unlike those observed in the also likely that asexually reproducing species are species’ native ranges (Jeffries and Lawton 1984; Torchin et al. 2003; Stastny et al. 2005). As a re- sult, organisms intentionally or unintentionally E. B. Mondor (&) Æ M. N. Tremblay Æ R. H. Messing transferred from one area to another may become Kaua’i Agricultural Research Center, University of invasive, thereby causing large-scale economic Hawai’i at Ma¯noa, 7370 Kuamo’o Road, Kapa’a, Hawai’i 96746, USA and (or) ecological damage (Elton 1958; Sim- e-mail: [email protected] berloff 1996; Vitousek et al. 1996). 123 Biol Invasions The negative effects of species invasions are traits among this diverse group of aphids that even more pronounced in small and isolated re- have enabled them to successfully colonize the gions, such as island habitats (Loope et al. 1988; archipelago? In this case, it is not possible to Nafus 1993; Gillespie and Roderick 2002). In compare the differences and similarities between these dispersal-limited systems, the population native and introduced species (e.g., Williamson growth of invading species can result in high and Fitter 1996), as there are no native aphids in levels of abundance and, hence, increased dam- the Islands (Zimmerman 1948). It can also be age. On the Hawaiian Islands, for example, spe- difficult to objectively determine which species cies introductions have devastated the native are invasive versus non-invasive introduced spe- fauna and flora (Vitousek et al. 1987; Sax et al. cies (e.g., Kolar and Lodge 2001), as this can 2002). It is estimated that these introductions differ both spatially and temporally. One power- have caused the extinction of 10% of the native ful comparative approach, however, is to directly flora (Vitousek et al. 1987) and half of the native contrast trait values for introduced species with bird species (Banko et al. 2001; Scott et al. 2001). trait values of non-colonizing congeners (National Over 3,000 arthropod species are believed to have Research Council 2002). By contrasting intro- been introduced into Hawaii (Howarth and duced species trait values to those of a ‘‘conge- Ramsay 1991; Miller and Eldredge 1996). neric baseline’’, it is possible to determine specific Approximately 20 arthropods species are intro- characteristics which may enhance the ability of duced into the Islands each year, with about half particular species to colonize novel habitats becoming invasive (Beardsley 1979). (National Research Council 2002). Plant-feeding Homoptera, such as aphids, can To identify the traits that have enabled some be highly problematic when introduced into is- aphid species to colonize the Hawaiian Islands, land habitats (Pike et al. 2000; Teulon and Stuf- we compiled a list of nine morphological and kens 2002). Even though not a single aphid ecological traits which could be reasonably ex- species is indigenous to Hawaii (Zimmerman pected to contribute to the successful introduc- 1948), at least 96 species can now be found on one tions. These quantitative and qualitative traits or more of the Islands (Messing, unpubl). Several were assessed for species present on one or more of these introduced species have become invasive, of the Hawaiian Islands, and for congeners which feeding on agricultural plants (e.g., Patchiella have not invaded the archipelago, but are present reaumuri), horticultural plants (e.g., Pentalonia elsewhere in the world (see Materials and meth- nigronervosa), native plants (e.g., Aphis spirae- ods for details regarding the congener selection cola), or all three types (e.g., Aphis gossypii) procedure). By contrasting trait values of intro- (Zimmerman 1948; Messing and Klungness 2001). duced aphid species against trait values of aphids Aphids cause direct feeding damage, but more distributed throughout the world (i.e., a null importantly, they may also transmit both persis- model), it is possible to identify the particular tent and non-persistent plant viruses (Ng and traits leading to colonization success. Once traits Perry 2004). Aphids vector many viral diseases in enhancing colonization have been identified, they Hawaii, such as banana bunchy top virus, may help to focus existing control efforts, as well cucumber mosaic virus, watermelon mosaic virus, as provide insights into fundamental aspects of zucchini yellow mosaic virus, and papaya ring invasion biology. spot virus (Cho et al. 1991; Ullman et al. 1991). This latter virus, for example, decreased papaya production in Hawaii by ca. 40% between 1993 Materials and methods and 1997 (Messing and Klungness 2001). The degree to which viruses impact native Hawaiian Our database consisted of 174 aphid species; 96 plant populations, however, is unknown. introduced species and 78 congeners which are Here, we attempt to identify the traits that not present on the Islands (data set available as have enabled aphids to successfully colonize the Appendix, Table 1). In this paper, we define an Hawaiian Islands. That is, are there common ‘‘introduced’’ species as one that is regularly 123 Biol Invasions present on one or more of the Hawaiian Islands. 2000; Lee 2002; Verlaque et al. 2002). The Heterospecific congeners were selected for the importance of polyploidy and hybridization analysis by randomly choosing (random genera- for the success of animal populations is just tion; JMP IN 5.1, SAS Institute 2005), from gen- starting to be explored (Delmotte et al. eric pools, similar numbers of species occurring 2003; Comai 2005). By assessing both chro- elsewhere in the world for which detailed infor- mosome number and the number of karyo- mation was available. Introduced species were types in different aphid populations, it is not paired with congeners from their native re- possible to make a preliminary assessment gions, due to the lack of available data. Even of the importance of this variable. when using a worldwide distribution, data for an equal number of introduced and non-introduced Information was also compiled for the follow- species were not always possible to obtain be- ing ecological variables: cause: (1) some species present in Hawaii are of (5) Host range [0–5; one species, multiple spe- monospecific genera (e.g., Hysteroneura setariae, cies, one genus, multiple genera, one family, P. reaumuri, Rhodobium porosum), and (2) the and multiple families]. It is plausible that biology of many aphid species, apart from those aphids with wider host ranges could more species of economic importance, is little known easily colonize novel environments (Teulon (Blackman and Eastop 2000). and Stufkens 2002). With wider host ranges, For our analysis, we used information from the newly arriving species would have an in- extensive compilations of Blackman and Eastop creased chance of finding suitable host (1994, 2000). Information was assembled for the plants on which to feed. following morphological variables: (6) Feeding site [0–1; below versus above (1) Average apterae (i.e., unwinged) body size ground]. Aphids may be more likely to enter [0.40–5.40 mm]. Body size has previously the islands if undetected, for example, when been shown to be important for arthropod feeding on inconspicuous plant parts such as colonization of novel environments (Lawton roots. Thus, there may be a larger number of and Brown 1986). For example, ant species root-feeding aphids in Hawaii. with smaller body sizes are more likely to be (7) Anholocycly/holocycly (i.e., degree of par- successful colonists (Passera 1994; Lester thenogenesis) [0–2; strictly anholocyclic (i.e., 2005), possibly because they can occupy permanently parthenogenetic), anholocyclic uninhabited ecological niches (Farji-Brener and holocyclic populations known, strictly et al. 2004). It is also feasible that smaller holocyclic (i.e., an obligate sexual phase)]. sized individuals more frequently escape Sexually reproducing organisms may be detection at points of entry into the Islands.