HYM. RES. J. Vol. 14(1), 2005, pp. 69-77 The North American Invasion of the Giant Resin Bee (Hymenoptera: Megachilidae) Ismael A. Hinojosa-Diaz, Olivia YAnez-Ordonez, Guojun Chen, A. Townsend Peterson, and Michael S. Engel (IAH, MSE) Division of Entomology, Natural History Museum, and Department of Ecology & Evolutionary Biology, 1460 Jayhawk Boulevard, Snow Hall, University of Kansas, Lawrence, Kansas 66045-7523, USA; (OY) Museo de Zoologia "Alfonso L. Herrera," Departamento de Biologia Evolutiva, Facultad de Ciencias, Universidad Nacional Autonoma de Mexico, Apdo. postal 70-399 CP 04510 Mexico D.F., Mexico; (GC, ATP) Division of Ornithology, Natural History Museum, 1345 Jayhawk Boulevard, Dyche Hall, University of Kansas, Lawrence, Kansas 66045-7561, USA — Abstract. The giant resin bee, Megachile sculpturalis Smith (Megachilidae: Megachilinae), is a species originally ofAsia recently adventive in NorthAmerica. This largeandconspicuousspecies was first recorded at a few localities in the mid-Atlantic states of the United States, but is now found from southeastern Canada (Ontario) to Georgia, and as far west as western Pennsylvania and northwestern Alabama. Known occurrences of this species in its native distributional areas were used to generate an ecological niche model for the species, which can be used to anticipate the geographic potential for species in novel landscapes. Thenichemodel wastested on thenative range of the species for robustness in predicting independent suites of occurrence points. The nic—he model was then used to predict the potential distribution ofM. sculpturalis in North Amer- ica our results indicate that this species has the potential eventually to occupy theentireeastern half of the continent, as far west as the Great Plains. The model also predicts that the species would find appropriate conditions along the Pacific Coast, in Mexico, and in the West Indies. Impacts of M. sculpturalis on native Megachile species are entirely unknown. As the most significant and efficientpol- lifera Linnaeus native to Africa, Europe, linators of flowering plants, bees are crit- the Middle East, and northwestern Asia ical for many aspects of the diversity and (Ruttner 1988), now globally distributed stability of both natural and agricultural as human colonists have transported bee ecosystems; in addition, honey bees have colonies. A famous episode in the pres- long been appreciated for their products ence of honey bees in the Americas was (e.g., honey and wax; Michener 2000). the experimental introduction in 1957 of These beneficial features make it difficult the African A. mellifera scutellata Lepeletier to think of bees as threats when intro- de Saint Fargeau ("Africanized" honey duced into areas outside their native rang- bees) into Brazil, and the later establish- es, despite the widely known negative ef- ment of feral populations throughout fect of exotic species in general (Goulson South and Central America, reaching the 2003, Lawton and Brown 1986, William- southern United States (Kerr 1957, 1967, son 1999, NAS 2002, Perrings ct al. 2002). Michener 1975, Taylor 1977, Sheppard and Several bee species have been intro- Smith 2000). Goulson (2003) mentioned duced into novel regions by man, either other bee introductions carried out to im- deliberately or not. The most famous ex- prove pollination, among the most signif- ample is the western honey bee Apis niel- icant, species of the genera Bombus, Me- 70 Journalof Hymenoptera Research gachile, Osmia and Nomia. Ascher (2001) polylectic (Mangum and Brooks 1997). mentioned the presence of 17 adventive Combining the records reported by Batra bee species in North America, providing (1998), Ascher (2001), and Mangum and taxonomic, geographic and biological in- Sumner (2003), in North America, M. formation for Hylaeus (Spatulariella) hyali- sculpturalis has been recorded foraging on natus Smith, and occurrence notes for Au- flowers of at least 16 plants of 12 families, thidium (Anthidium) manicatum (Linnaeus), the most commonly visited being ever- A. (Proanthidium) oblongatwu (Illiger), Hop- lasting pea, Lathyrus latifolius Linnaeus litis (Hoplitis) anthocopoides (Schenck), Che- (Leguminosae); Japanese pagoda, Sophora lostoma (Gyrodromclla) rapunculi (Lepeletier japouica Linnaeus (Leguminosae); privet, de Saint Fargeau)1, C. (Fovcosmin) campan- Ligustrum lucidum W. T. Aiton (Oleaceae); ularum (Kirby), and (our subject herein) and golden-rain tree, Koelreuteria panicu- Megachile (Callomegachile) sculpturalis lata Laxmann (Sapindaceae), the first na- Smith. tive to Europe and the remainder to Asia. The giant resin bee, M. sculpturalis, is a FemaleM. sculpturalis leave a trace oftheir robust bee widely distributed in eastern foraging activity on flowers of everlasting Asia (China, Japan, Taiwan, and Korea). pea and Japanese pagoda by puncturing The species is easily differentiated from the standard petal (Mangum and Sumner native North Ammermican Megachile bymimts 2003). elongate (14-19 in males, 22-27 In the last decade, M. sculpturalis hasap- in females) parallel-sided body, black peared in eastern North America, with head, and dark mesosoma with fulvous populations established and spreading setae (Mangum and Brooks 1997) (Fig. 1). from their initial areas of appearance Imtinneistmsumpreoffe0r.e5ntmialalbyovien tshheadgyrouplnadc,esi,n aa t(rpordoubcaebdl,y vnieaarcaBraglotifmorroem,JaacpcaindenotralClhyinian;- variety of cavities, e.g., dry, hollow hori- Batra 1998, Mangum and Brooks 1997). zaonndtaelmsptteymsb(ubrarmobwosomiandites nbaytivoethrearnghey)-, MNeogratchhiAlmeesrciulcpaturianli1s99w4asonfirtshteccolalmepctuesd oinf mcleundoipntgeraabnasnd(oInwaetdaw19o3o3,dObkuardraow1s99o5f),cairn-- N19o9r6thwaCsarowliidneaspSrtaetaedUinnivNerosritthy,Caarnodlibnya piAoemrnethreairscbaaelnerseap(doPyipebulelea19nt3i3do)on.csTuhm(iesMnatlaentdtgeurinmbNeoharantvdh- (DeMlaanwgaurem (anMdanBgruoomksan1d997S)u,manlesorr2e0a0c3)h.inIgt Brooks 1997). Brood cells are made of res- has since spread over much of eastern in from conifers (Iwata 1933) and maple North America, with records as far west gum (Piel 1933), from which the name "gi- as Athens, Limestone Co., Alabama, as far ant resin bee" derives (Batra 1998). In Ja- south as Auburn, Lee Co., Alabama (Kon- Jpuann,eittshrpoeurgiohdSoefpatdeumlbtearct(iIvwiatytais1f9r33o)m,lcaot-e ddaogcat aClo..,200N0e),wanYdoraks (fAarscnhoerrth20a0s1)O,noann-d inciding with the blooming of kudzu Ontario, Canada (Mangum and Sumner [Pueraria lobata (Willdenow) Ohwi (Legu- 2003). Records also exist from Georgia, minosae)], its principal source of pollen South Carolina, Virginia, Maryland, Penn- (Batra 1998), although it is known to be sylvania, West Virginia, Ohio, Washing- ton D.C., Tennessee, and Connecticut (Mangum and Sumner 2003). Batra (1998) 1 Thisspecieshas oftenbeenreferred tobytheold- predicted, based on its Asian range, that e(ra,jbuuntioprrpeorcicmuapriyedh,onmaomneymofiCn.Afpuils)i,giwnohsiucmh(wPaanszerre)- M. sculpturalis would come to inhabit the placed by C. nigricorne (Nylander), but this itselfis a humid, subtropical to temperate climates synonym ofC. rapunculi. of the southeastern and mid-Atlantic Unit- Volume 14, Number 1, 2005 71 Fig. 1. Megachile sbulpturalis Smith, female from Japan, above dorsal habitus, below lateral habitus. ed States, from eastern Texas and Florida, range ecological characteristics provide north to southern New England. excellent predictivity regarding invaded- Herein we have applied methods ofeco- range ecological and geographic potential logical niche modeling. Extensive previ- of species (Scott and Panetta 1993, Suth- ous studies have indicated that native- erst et al. 1999, Skov 2000, Zalba ct al. 2000, 72 Journalof Hymenoptera Research Peterson et al. 2003). Although this ap- mental Panel on Climate Change, native proach does not provide comprehensive resolution 50 x 50 km: http://www.ipcc. predictions of geographic range because ch/). To minimize conflicts in scale be- of other complicating factors (Peterson et tween topographic and climatic data, we al. 2003), the resulting predictions never- conducted analyses at an intermediate res- theless offer an excellent summary of spe- olution (10 X 10 km). — cies' invasive potential. As such, we use Ecological niche modeling. Ecological this technique to predict the potential ex- niches are herein defined as the set ofcon- tent of M. sculpturalis' invasive range in ditions under which a species is able to North America. maintain populations without immigra- METHODS tion (Grinnell 1917, 1924). Our approach — consisted of three steps. (1) Model ecolog- Input data. Collections with specimens ical niche requirements of the species of M. sculpturalis were studied to obtain based on known occurrences in the native native-range occurrence data suitable for distribution area ofthe species. (2) Testthe retrospective georeferencing. Specimen accuracy of the native-range predictions data were taken from the Snow Entomo- based on spatially structured subsets of logical Collection, Division of Entomolo- the available information. (3) Project the gy, University of Kansas Natural History niche model onto North America to iden- Museum, Lawrence, KS, USA; Kyushu tify areas predicted tobe susceptible to in- University, Japan; Institute of Zoology, vasion. Chinese Academy of Sciences, People's The software tool used for niche mod- Republic of China; and the Natural His- eling was the Genetic Algorithm for Rule- tory Museum, London, UK; as well as set Prediction (GARP) (Stockwell and No- data from Huan-li Xu personal collection ble 1992, Stockwell and Peters 1999). (People's Republic of China). Occurrences GARP uses an evolutionary-computing of the species on its invaded range in approach to carry out a flexible and pow- North America were gathered from the erful search for non-random associations Snow Entomological Collection, Universi- between environmental variables and ty of Kansas Natural History Museum, known occurrences of species, as contrast- Lawrence, KS, USA, and from recent pub- ed with the environmental characteristics lished reports (Mangum and Brooks 1997, of the overall study area. Batra 1998, Kondo et al. 2000, Ascher 2001, Specifically, available occurrence points Mangum and Sumner 2003). are resampled with replacement to create To summarize ecological variation a population of 1250 presence points; an across the native and introduced geo- equivalent number of points is resampled graphic distributions of the species, we from the population of grid squares ('pix- used 15 raster grid data sets ('coverages'). els') from which the species has not been These coverages summarized aspects of recorded. These 2500 points are divided topography (elevation, topographic index, equally into training (for creating models) slope, and aspect, from the US Geological and testing (for evaluating model quality) Survey's Hydro-IK data set, native reso- data sets. Models are composed of a set of lution 1 X 1 km: http://edcdaac.usgs. conditional rules developed through an it- gov/gtopo30/hydro/) and climate (an- erative process of rule selection, evalua- nual means of diurnal temperature range; tion, testing, and incorporation or rejec- frost days; precipitation; maximum, mini- tion. First, a method is chosen from a set mum and mean monthly temperatures; of possibilities (e.g. logistic regression, solar radiation; wet days; and vapor pres- bioclimatic rules, etc), and applied to the sure; for 1960-1990 from the Intergovern- training data set. Then, a rule is developed Volume 14, Number 1, 2005 73 by a number of means (mimicking DNA expected under random models. Because evolution: point mutations, deletions, test results depend critically on how oc- crossing over, etc.) to maximize predictive currence points are divided into training accuracy. Rule accuracy is evaluated via and testing data sets (Fielding and Bell the testing data, as a significance param- 1997), we used a 2 X 2 checkerboard ap- eter based on the percentage ofpoints cor- proach (splitting available points into rectly predicted as present or absent by quadrants above and below median lati- the rule. The change in predictive accura- tude and median longitude) that pr—esents cy from one iteration to the next is used a maximum challenge to the model pre- to evaluate whether a particular rule diction intobroad areas from which no oc- should be incorporated into the final rule- currence information was available (Peter- set. The algorithm runs either 1000 itera- son and Shaw 2003). Ecological niche tions or until addition of new rules has no models based on localities in two of the effect on predictive accuracy. The final quadrants ("on-diagonal") were used to rule-set (the ecological niche model) is predict the distribution of the occurrences then projected onto a digital map ofnative in the other two quadrants ("off-diago- or potentially invaded areas to identify a nal"), and vice versa. Models were vali- potential geographic distribution. Al- dated via chi-square tests that incorporate though these environmental variables can- dimensions of correct prediction of both not represent all possible ecological-niche presences (based on independent test dimensions, they likely represent (or are data) and absences (based onexpected fre- correlated with) many influential ones in quencies) (Peterson and Shaw 2003). Ran- delineating the species' potential distri- dom expectations were calculated as the bution. product of the proportional area (within Spatial predictions of presence and ab- 500 km of known occurrences) predicted sence can hold two types of error: omis- present and the number of test presence sion (areas of known presence predicted points. Observed frequencies of correct absent) and commission (areas of known and incorrect predictions ofpresence were absence predicted present) (Fielding and then compared with expectations using a Bell 1997). Because GARP does not pro- x2 test (1 df). duce unique solutions, we followed re- KtbUL b cently published best practicesapproaches to identifying an optimal subset of result- The native-range predictions based on ing replicate models (Anderson et al. the two independent spatial subsets of the 2003). For each analysis, we developed 100 available occurrence data were closely replicate models; of these models, we re- similar to one another (Fig. 2), with the tained the 20 with lowest omission error, exception that the model based on on-di- Finally, from these 20, we retained the 10 agonal quadrants was somewhat more ex- with moderate commission error (i.e., we tensive in the north and the south. Both discarded the 10 models with area pre- predicted areas in the 'other' quadrants dieted present showing greatest devia- (from which occurrence data were with- tions from the overall median area pre- held from the modeling exercise) that co- dieted present across all models). This incided well with the test points in those 'best subset' of models was summed to areas (both x; * 23.90, both P < 10 "!"")- produce final predictions of potential dis- Although the two reciprocal predictions tributions. are not identical, their substantial signifi- To validate our model predictions, we cance nonetheless indicates clear predic- evaluated their ability to predict indepen- tive ability of our models for distribution- dent sets of test points compared with that al phenomena related to this species. 74 Journal of Hymenoptera Research Fig. 2. Predictions of native geographic distribution of Megachile sculpturalis Smith, based on two distinct subsets (here depicted as squares versus circles) of the available data-on-diagonal quadrants predict off- diagonal quadrants (top), and vice versa (bottom). Volume 14, Number 1, 2005 75 Fig. 3. Projection of native-distribution ecological niche model for Megachilesculptumlis Smith to theUnited States, identifying areas putatively suitable for the species (top); observed pattern of advance (year of first detection) of invading populations (bottom): X's = 1994-1997, light grav circles = 1998-1999, and dark gnu circles = 2000-2001. Thus, we combined all native-range oc- These areas included the entire eastern currences to build a single model for pro- half of the continent, west as far as the jection to North America. Great Plains. The models also identified Projecting our native-range ecological disjunct areas of potential distribution niche model to North America, broad ar- along the Pacific Coast; in western, cen- eas were identified as suitable for this spe- tral, and southern Mexico; and in the West cies to maintain populations (Fig. 3). Indies. As such, the potential distribution Journal of Hymenoptera Research 76 of M. sculpturalis in North America ap- become established and widespread on pears to be quite extensive. these islands. The growing number of collection re- DISCUSSION cords of the bee in North America so far confirms the predictions presented here. The potential invaded distribution in Indeed, plotting known North American North America predicted by our ecologi- occurrences by year (Fig. 3) shows the cal niche model for M. sculpturalis consid- broadening spatial pattern of occurrence erably exceeds the earlier prediction of Ba- of the species through time. Continued tra (1998). Both predictions agree that the surveying of this species over time will species will come to occupy the humid provide much more concrete tests of our eastern United States; our model, howev- in states such as predictions, particularly er, also shows a broader potential to the Kentucky, Illinois, Indiana, Missouri, and west and north of the area outlined by Ba- Mississippi as well as more western local- tra (1998). In other words, instead of ex- ities in Tennessee. Such surveys will be tending only west to eastern Texas, the important for documenting the spread of species will likely reach northwesternTex- M. sculpturalis. Surveying for M. sculptur- as and western Kansas. Similarly, instead alis is not difficult, given its impressive of ending in southern New England, the size; even indirect records can be accu- species will likely reach north to Nova mulated via the marks it leaves on flowers Scotia, Canada (Fig. 3). while foraging (Mangum and Sumner Projection of our model onto all of 2003). Possible impacts of M. sculpturalis North America identified additional po- on native Megachile species, other native tential areas of invaded distribution for bees, or as a pollinator, are entirely un- the bee outside the present eastern range known. Although it has been seen using discussed above. These areas are along the abandoned nests of native carpenter bees Pacific Coast of the United States, portions (Mangum and Sumner 2003), its foraging of Idaho, and parts of Mexico and the activities have so far been recorded prin- Wes—t Indies (Fig. 3). These p—redictions cipally on exotic plants. For the moment are it should be remembered of poten- there is little reason to a priori suspect any tial distributions only; as such, the species barriers to the bee's continued westward would likely establish populations only if invasion of the North American continent. presented with dispersal opportunities ACKNOWLEDGMENTS that would place them in or close to those areas. Given the potential ecological suit- Wewould liketothankWan-ru Yu (ChineseAcad- ability identified and high import traffic emy ofSciences, People's RepublicofChina),Osamu from Asia along the western seaboard Tadauchi (Kyushu University, Japan), Huan-li Xu, pthreorbeabwioluiltdy, hoofweavneri,nadpeppeeanrdteonbteNaohritghh aLinnondAdsCoihnar.,isWUtKie)n,earTaelalyglorfoartwe(hfTuohlemtoNparWtoyuvraiatdltedHMioasctncogurryurmeMnucfseoerduaamtd,a- American introduction of this species into ditional information on M. sculpturalis. Support was northern California, and eastern Oregon partially provided by NSF DBI-0096905 (toJ. S. Ashe and Washington. The West Indies also and M. S. Engel). This is contribution 3401 of the Di- sMe.emsscultpotubrealiascrmeidgihbtleirnevgaidoen. inAtorwehlaitcehd vBiisoidoinveorfsiEtnytRoemsoelaorgcyh,CNeanttuerr,alUnHiivsetrosriytyMuofseKaunmsaasn.d species, M. (Callomegachile) rufipennis (Fa- LITERATURE CITED bricius) from Africa, is already adventive in the West Indies (e.g., Mitchell 1980, AndeErvsaolnu,atRi.ngP.,prDe.dicLteiwv,e amnoddeAl.sTo.fPsepteecriseosn'.di2s0t0r3i.- Genaro 1997), reinforcing the notion that, butions: Criteria for selecting optimal models. if introduced, M. sculpturalis could easily Ecological Modeling 162: 211-232. Volume 14, Number 1, 2005 77 Ascher, J. S. 2001. 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