Springer 2005
Biological Invasions (2005) 7: 509–530
Behavioral constancy for interspecies dependency enables Nearctic Chymomyza amoena (Loew) (Diptera: Drosophilidae) to spread in orchards and forests in Central and Southern Europe Henretta Trent Band1,, Gerhard Ba¨chli2 & Rudolph Neal Band1 1
Zoology Department, Michigan State University, East Lansing, MI 48824, USA; 2Zoological Museum, Winterthurerstrasse 190, University of Zu¨rich-Irchel, 8057, Zu¨rich, Switzerland; *Author for correspondence (e-mail:
[email protected]; fax: +1-517-432-5478)
Received 24 September 2002; accepted in revised form 9 April 2004
Key words: apples, behavioral constancy, chestnuts, Chymomyza amoena, facilitation, female oviposition behavior, indirect effects, interspecies dependency, Italy and Switzerland, parasitized substrates, vacant niches Abstract Nearctic Chymomyza amoena, an eastern US forest drosophilid, was initially known only to breed in damaged or parasitized nuts and had been little studied. It has been spreading in Europe since its discovery in the former Czechoslovakia in 1975. By the time it arrived in Switzerland’s Canton Ticino in 1988, research in the United States revealed it had long been in domestic habitats, overwinters in the third instar larval stage in endemic substrates (black walnut husks Juglans nigra, native crabapples Malus coronaria), domestic [imported] apples Malus domestica and ornamental fruits (crabapples) and uses these plus other substrates for breeding from spring and summer through autumn. Female oviposition in firm substrates in Michigan and the mid-South (North Carolina, Virginia) as fallen unripe and ripe frassy apples, acorns, black walnut husks, native and ornamental crabapples is mediated by prior insect attack. Although large numbers of C. amoena coming to banana bait in Canton Ticino suggested that founder effects involving attraction to fermenting substrates might have occurred, experimental studies with European flies in Michigan and continuing research in Zu¨rich and Canton Ticino revealed that behavioral constancy had been maintained. This enabled prediction that C. amoena would spread into apple orchards in northern Switzerland and into Italy. Research in July 2000 established that it is in apple orchards on the German border and in the chestnut forests and in old orchard apples in Italy’s Valtellina region, Lombardy Province. Other European drosophilids have not exploited parasitized fruits and nuts, indicating C. amoena entered a vacant niche. Facilitation provided by pest species attacking fruit and nut substrates parallel those in North America. Chymomyza amoena has maintained behavioral constancy for interspecies dependency and continues to be the principal drosophilid breeding in parasitized fruits and nuts in both North America and Europe.
Introduction ‘Individuals make up populations which are geographically distributed in the habitats to which they become evolutionary adapted through time.
The behaviour of an organism, like other aspects of the phenotype, will be a product of evolution in this geographically and temporally structured context’ (Hewitt and Bultin 1997). However, a biological invader typically replaces its evolved
510 ecobehavioral constraints with a new set of challenges when it arrives on a new Continent: establishment and spread vs failure due to a variety of causes including invasion resistance from existing species richness (Simberloff 1989; Lodge 1993; Niemala¨ and Mattson 1996; Williamson 1996; Stachowicz et al. 1999; D’Antonio and Kark 2002; Shea and Chesson 2002; Bruno et al. 2003). On the other hand, Lohrer et al. (2000) have shown that resource use by a biological invader may remain comparable to that in its native habitat. We report another case in which the behavior of a biological invader at ‘home’ and ‘abroad’
remains similar, enabling predictions that it has entered commercial orchards in Switzerland and has become established in yet another country, Italy. Facilitation (Bruno et al. 2003) in the form of indirect interactions with primary pest insects is crucial to the behavioral constancy (Schowalter 2000) maintained by Chymomyza amoena in the European environment. When Chymomyza amoena, a little drosophilid with black banded wings, was first collected in 1975 in the former Czechoslovakia and began to spread rapidly in Eastern Europe (Burla and Ba¨chli 1992; Ma´ca and Ba¨chli 1994) (see Fig-
Figure 1. The spread of Nearctic Chymomyza amoena (Loew) in Central Europe (exclusive of one collection each in Russia and the Caucauses) between its first capture in 1975 in the former Czechoslovakia (denoted by 1) and 1993. Adapted from Ma´ca and Ba¨chli (1994). The individual collecting sites in each country, latitude, longitude, year and reference are given in Table 1 of that paper. X marks the region of northern Italy in which field work was done in late July/early August 2000.
511 ure 1), this North American species had been subject to few contemporary investigations (Sabath and Jones 1973; Sabath 1974, 1975). Ba¨chli and Rocha Pite´ (1981) suggested it might be either a recent colonizer or else have a Holarctic distribution. Past work in the United States had shown that it was a member of the eastern
forest drosophilid community (Spieth 1957) and bred in a variety of nuts (acorns Quercus sp.: Sturtevant 1921; Winston 1956; Dorsey et al. 1962; black walnut husks Juglans nigra: Sturtevant 1921; butternut hulls Juglans cinera: Sturtevant 1921). No Chymomyza were known to breed in apples (Ferrar 1987).
Table 1. (a) Chymomyza amoena larvae in or adults emerging from domestic apples Malus domestica (a) in Michigan: Northern Lower Peninsula (NLP), mid-MI, Upper Peninsula (UP), 1978–1993; (b) in North Carolina (Piedmont area) and Virginia (Eastern, Piedmont and Western areas), 1984–1992. State/region
Month(s)
Place
Panel a: Michigan NLP 1978 1978 1979 Mid 1979 1980/1981 Mid 1981 NLP 1981 Mid 1981 Mid 1982 1982 1982/1983 1984 1985 1987 1991 UP 1993
Mar.–May Jul.–Oct. April Nov./Dec. March April August Jul./Aug. July Sept.-Nov. Dec.–Feb. Sept. Oct. Jul./Aug. July Aug./Sept.
Panel b: North Carolina Pied. 1984 Virginia West.
East. Pied. West.
East. West. a
Year
1985 1985 1986 1986 1986 1986 1986 1987 1987 1987 1988 1989 1990 1991 1992
Season
Stage
Number
Reference
E. Jordan Overwintered E. Jordan Summer/fall E. Jordan Overwintered St. Johns Fall/winter St. Johns Overwintered E. Lansing Overwintered E. Jordan Summer Lansing Summer E. Lansing Summer E. Lansing Fall E. Lansing Winter E. Lansing Fall Lansing Fall E. Lansing Summer E. Lansing Summer Iron Mountain Summer
Adult Adult Adult Adult Adult Adult Adult Adult Adult Larval Larval Adult Adult Adult Adult Adult
12 35 21 67 12 11 46a 218 25b 36 35 44 1c 130 15 90d
Band Band Band Band Band Band Band Band Band Band Band Band Band Band Band Band
June
Eden
Summer
Adult
22e
Band (1988a, 1995a)
Jul./Aug. Jul. July July June June July July July July July July July July July
Rt. 700 Mt. Lake Rt. 700 Mt. Lake Pamplin Danville Blacksburg Blacksburg Rt. 700 Mt. Lake Rt. 700 Rt. 700 Rt. 700 Pamplin Rt. 700
Summer Summer Summer Summer Summer Summer Summer Summer Summer Summer Summer Summer Summer Summer Summer
Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult
48f 41 36 16 39 68 15 36 146 35 59 114 38g 9h 14
Band Band Band Band Band Band Band Band Band Band Band Band Band Band Band
Also 46 D. melanogaster, 42 D. algonquin. Also 4 D. melanogaster, 6 D. affinis. c Also 17 D. melanogaster + D. simulans, 3 D. immigrans. d Also 5 D. melanogaster. e Also 3 D. affinis, 4 D. melanogaster, 40 D. busckii, 1 D. immigrans. f Also 35 D. affinis, 6 D.melanogaster, 14 D. immigrans. g Also 4 D. immigrans. h Also 9 D. immigrans, 5 D. melanogaster. b
and Band (1988a) and Band and Band (1988a) (1988a) (1988a) (1988a) (1995a) and Band and Band (1988a) (1995a) (1988a) (1995a) (1995b)
(1980) (1980) (1980)
(1984) (1984)
(1988a, 1995a) (1988a) (1988a, 1995a) (1988a) (1988c) (1988c) (1988a, c) (1988c) (1988c) (1988c) (1996) (1996) (1995a) (1995a) (1995a)
512 Table 2. Records of Chymomyza amoena larvae in or adults emerging from native crabapples Malus coronaria, ornamental crabapples Malus pyramidus and domestic plums Prunus domestica, 1982–1995 (Wmston=Williamston, MI, a town east of East Lansing). Year
Month(s)
Place
Substrate
Season
Stage
Number
Reference
Michigan 1981 1982 1982 1982/1983 1985 1986 1982 1982 1982/1983 1985 1987 1992
Oct. May May Dec.–Feb. May May Oct. Oct. Dec.–Feb. Oct. June June
Wmston Wmston Wmston Wmston Wmston Wmston E. Lansing E. Lansing E. Lansing E. Lansing E. Lansing E. Lansing
M. coronaria M. coronaria M. coronariaa M. coronaria M. coronaria M. coronaria Ornam. crab. Ornam. crabb Ornam. crab. Ornam. crab.c Plums Plums
Fall Overwintered Spring Winter Spring Spring Fall Fall Winter Fall Summer Summer
Adult Larval Adult Larval Adult Adult Larval Adult Larval Adult Adult Adult
2 16 48+ 24 122 176 12 5 30 1 25 22
Band Band Band Band Band Band Band Band Band Band Band Band
Virginia 1995
May
Monticellod
M. coronariae Overwintered Adult
95
Unpublished
and Band and Band (1988a) and Band (1988a) (1988a) and Band (1995a) and Band (1995a) (1995a) (1995a)
(1984) (1984) (1984)
(1984) (1984)
a
5 Drosophila affinis group females emerged. b 21 D. melanogaster + D. simulans. c 28 D. melanogaster + D. simulans. d At Charlottesville, VA. e Also included M. angustifolia; 8 D. melanogaster and 7 D. affinis also emerged.
Table 3. Records of Chymomyza amoena larvae in or adults emerging from black walnut hulls Juglans nigra, acorns Quercus rubra (red) and Quercus alba (white) and oriental chestnuts Castanea mollisima in Michigan and Virginia, 1983–1992. Month, year Michigan Jan. 1983 Jan. 1983 Nov. 1983 Nov. 1984 Dec. 1984 Jan. 1985 Feb. 1985 Nov. 1984 Oct. 1985 Oct. 1989 Nov. 1989 Virginia July 1989 Sept. 1989 July 1990 July 1990 Oct. 1992
Substrate
Stage
Season
Number
Reference
Juglans nigra J. nigra J. nigra J. nigra J. nigra J. nigra J. nigra J. nigra J. nigra Quercus rubra Q. rubra
Larval Adult Adult Larval Larval Larval Larval Adult Adult Larval Larval
Winter Winter Fall Fall Winter Winter Winter Fall Fall Fall Fall
7 17 12 32 16 28 41 125 2a 4b 5
Band Band Band Band Band Band Band Band Band Band Band
and Band (1988a) (1988a) and Band and Band and Band and Band (1988a) (1994) (1991) (1991)
Quercus alba Q. alba Q. alba Q. alba Castanea mollisima
Adult Larvae Adult Eggs Pupae
Summer Fall Summer Summer Fall
74 28c 41 103 10d
Band Band Band Band Band
(1991, 1995a, 1996) (1991, 1995a, 1996) (1995a) (1996) (1996)
(1984)
(1987) (1987) (1897) (1987)
a
Also 4 Drosophila busckii, 3 D. immigrans emerged. Also 1 Drosophila larva. c 7 C. amoena emerged, 5 Drosophila larvae present, 4 D. melanogaster emerged. d 1 C. amoena adult emerged. b
Papp and Pecsenye (1987) asked if North American and European C. amoena were the same species. Schumann (1987) published draw-
ings of C. amoena’s conspicuously banded wings and eggs obtained from specimens captured in Berlin which indicated that European and North
513 American species were the same. Meanwhile discovery that C. amoena was breeding in and overwintering in apples in East Jordan, Michigan (on Michigan’s Lake Charlevoix) led to studies on larval overwintering in mid-Michigan (Band and Band 1984, 1987) and breeding season studies in both Michigan and the mid-South (Virginia, North Carolina), where research was conducted using the facilities at the University of Virginia’s Mt. Lake Biological Station in Virginia’s Allegheny Mountains (Band 1988a–d, 1989, 1991, 1994, 1995a, 1996). Nearctic C. amoena could breed in and overwinter in a variety of fruits and nuts (see Tables 1a, b, 2, 3) demonstrating that it was a broad-niched species, as suggested by Sabath (1974), and preadapted to survive the seasonal European climate, as noted by Schumann (1987). It was first recorded emerging from domestic apples along with codling moth Cydia pomonella in East Lansing, Michigan in 1891 by G.C. Davis of Michigan Agricultural College and most likely was the Drosophila apple fly whose larvae entered early apples in Massachusetts via codling moth tunnels or curculio scars as noted by Packard in 1869 (Band 1994). Chymomyza amoena’s widespread undetected invasion of the domestic environment while continuing to persist in eastern forests in the United States (Winston 1956; Dorsey and Carson 1956; Dorsey et al. 1962) also hinted the species might have a Holarctic distribution (Band 1989). However, two centuries of European forest entomology (Schwerdtfeger 1973) failed to disclose any record in Europe prior to 1975. Drosophilid collecting in Switzerland netted over 250,000 specimens from 1946 to 1984 representing the 34 most frequent species (Burla and Ba¨chli 1991a) and C. amoena was not present until 1988 when it was captured in three places in Canton Ticino. Two additional samplings in Canton Ticino also support the evidence that C. amoena is a recent invader: in 1970, 32,812 drosophilids were netted in forests some 10 km south of Maggia and in 1981, 22,385 flies were netted in 10 places between Bellinzona and All’Acqua also in Canton Ticino; C. amoena was in neither sample (Burla and Ba¨chli 1992). By 1991 it had become well established in the Maggia Valley, Canton Ticino, had reentered the forest habitat and was reared from parasitized (having an exit hole made by a depart-
ing pest larva) European chestnuts Castanea sativa, parasitized acorns Quercus robur and wild sweet cherries Prunus avium in addition to domestic apples (Burla and Ba¨chli 1991b, 1992). Studies conducted at Michigan State University on C. amoena cultures from the Maggia Valley showed they were just as variable in mating behavioral traits as Michigan and Virginia populations and interfertile with them (Band 1995b). However, new questions arose. Had oviposition behavior changed due to founder effects (Hewitt and Bultin 1997; Holway and Suarez 1999), a fact that seemed likely given the large numbers coming to fermented banana bait in Canton Ticino (Burla and Ba¨chli 1992; Band et al. 1998), or did C. amoena still oviposit in firm fruits as well as nuts via reliance on primary pests for oviposition access as in the United States? Whereas few C. amoena came to a variety of baits in the United States over 4 decades of collecting (see Table 17, Band 1996), Burla and Ba¨chli (1992) were able to collect 117 C. amoena among 7677 drosophilids representing 20 species in the Maggia Valley in a twoday period in September 1991. In 1995 Ba¨chli netted five times that number of C. amoena in the Bolle di Magadino, a protected forest preserve near Gordola, in late June (Band et al. 1998). Parsons and Stanley (1981) and Parsons (1983) argued that for a drosophilid species to become a successful colonizer, it has to be tolerant to physical stresses, fruit baitable and able to breed in a variety of substrates. This characterized Drosophila pseudoobscura, a widespread forest species on the west coast of North America which colonized New Zealand (Millar and Lambert 1985), and D. subobscura, the most widely distributed European drosophilid which colonized Chile in 1978 and the west coast of North America in 1982 (Ayala et al. 1989). Dobzhansky (1965) noted that D. pseudoobscura was moving from forests into orchards in California; Coyne et al. (1984) reared it from a variety of California fruits. Drosophila subobscura was already known to breed in a variety of fruit substrates and other substrates (Schatzmann 1977; Shorrocks 1982). Chymomyza amoena, a distant relative of Drosophila (see Powell 1997) had entered eastern Europe on apples (Burla and Ba¨chli 1992). The hypothesis of a shift in preference for fermenting fruits as the species moved westward was not
514
Figure 2. A map of Switzerland indicating where fruit and/or nuts were collected in July 1998 and where work was done near the Swiss/German border in July 2000. Zurich – Hotel Zu¨richberg; H – Ho¨nggberg; M – Ma¨genwil; C – Corzoneso; R – Castelrotto; P – Purasca; S – Castel San Pietro; B – Bolle di Magadino; MRD – Marthalen, Rheinau and Dachsen; DP – Dettighofen and Pfyn.
unreasonable. Icelandic fulmars Fulmarus glacialis shifted feeding and breeding site behaviors as they moved east and south from Foula in the Shetland Islands (Williamson 1996). Palearctic Drosophila subobscura shows regional ecological differences between the European Continent, where it breeds largely in soft or decaying fruits and vegetables, and England, where it breeds in mushrooms and rotting rowan berries (Shorrocks 1982; Burla et al. 1987, 1991; Burla and Ba¨chli 1991b, 1993). Band (1996), however, argued that C. amoena females continued to oviposit in parasitized fruit and nut substrates in Switzerland as in North America, a fact subsequently substantiated (Band et al. 1999) (see Figure 2 and Table 4). Consequently, could behavioral constancy (Schowalter 2000) for oviposition in parasitized fruits and nuts in the United States and in Zu¨rich and Canton Ticino be used to predict the presence of C. amoena in apple orchards of northern Switzerland and in the chestnut forests of northern Italy? Although the ‘vacant niche hypothesis’ has generated controversy (Herbold and Moyle 1986; Colwell 1992; Griesemer 1992; Simberloff 1995; Brandon 1996; Williamson 1996; Mack et al. 2002; Shea and Chesson 2002), there was no record of any Palearctic drosophilid consistently
breeding in nuts or parasitized fruit/nut substrates (Ba¨chli and Roche-Pite´ 1982; Burla and Ba¨chli 1991b, 1993; Powell 1997) prior to the arrival of C. amoena. Hence Nearctic Chymomyza amoena is a ‘missing drosophilid’ that was accidently introduced into the European Continent. Oviposition behavior of Chymomyza amoena in North America Drosophila oviposition sites are typically described as soft or rotting: rotting fruits, rotting vegetation, fleshy fungi, slime fluxes, rotting bark (Powell 1997). Temperate zone Chymomyza are mostly forest species and breed under bark of recently damaged trees or cut wood (Wheeler 1952; Spieth 1957; Ba¨chli and Burla 1985; Burla 1995a, b, 1997; Band 1996). Nearctic Chymomyza amoena is an exception. It does not breed under bark and it does not necessarily depend upon rotting (fermenting) substrates. Table 1a presents data on C. amoena larvae in or adults emerging from domestic apples in Michigan, 1978–1993; Table 1b presents data on C. amoena adults emerging from domestic apples in North Carolina and Virginia, 1984– 1992. Table 2 presents data on C. amoena larvae
515 Table 4. Parasitized substrates with Chymomyza amoena eggs at places in Canton Zu¨rich, Canton Aargau and Canton Ticino, Switzerland in July 1998. Adapted from Band et al. (1999). Place
Fruit/nut
Total parasitized substrates
No. with C. amoena eggs
No. eggs
Canton Zu¨rich Ho¨nggerberg Hotel Zu¨richberg
Apples Apples
29 27
5 4
13 7
Canton Aargau Ma¨genwil I, II
Apples
79
7
34
Canton Ticino Corzoneso Castelrotto Castelrotto Purasca Purasca Castel San Pietro Bolle di Magadino
Chestnuts Apples Plumsc Chestnuts Apples Apples Acorns
53 13 18 99 22 36 13
1 3 1 1 5 21 4
3a 28b 1 4d 37 154b 13e
a
l larva, 2 pupae. 1 larva. c Not parasitized. d 4 larvae. e 3 pupae cases. b
in or adults emerging from other fruit substrates in mid-Michigan and from native crabapples in Virginia, 1981–1995. Table 3 presents data on C. amoena larvae in or adults emerging from mostly black walnut hulls in mid-Michigan and acorns in Virginia, 1983–1992. Based on studies in the two states, the following composite picture emerges: Chymomyza amoena overwinters as a third instar larva in a variety of substrates in mid-Michigan (native crabapples Malus coronaria and black walnut hulls Juglans nigra as well as domestic apples and ornamental crabapples). Diapause is not obligate; adults will emerge in about 15 days when overwintering substrates are held in the laboratory at 22 C. In the natural environment pupation is in the spring with emergence in May. The breeding season begins about mid-May; a generation takes about 30 days, although the species is polymorphic for developmental time. Females from all overwintering substrates prefer to oviposit in soften overwintered native crabapples (Band 1988a). Overwintered native crabapples, if available at all, disappear in summer when they become dry. A succession of oviposition substrates is required during the breeding season which can extend into October: overwintered native crabapples (May), fallen parasitized plums (June), early fallen parasitized unripe apples (late June, early July), ripen-
ing parasitized fallen and unfallen apples (late July, early August). Parasitized apples and pears may continue to be used in fall but females also switch to nuts, especially parasitized black walnut hulls, to nut-like native crabapples and softer ornamental crabapples which can/will serve as overwintering sites for the developing larvae. In early fallen and ripening apples, females oviposit in scars, codling moth tunnels or frass (insect excreta); females will also feed on frass in apples still on the trees. In mid-Michigan in May in addition to C. amoena, 12 Drosophila will also come to fruit and/or mushroom bait (Band 1993a). Chymomyza amoena is the only or the predominant drosophilid to emerge from the various substrates, May–August; in August–October sometimes D. affinis, D. immigrans, D. melanogaster and D. simulans have also emerged from apples and ornamental crabapples. The latter three Drosophila are among a small group called ‘cosmopolitan’ or domestic since they are commensal with man and have world-wide distribution (Dobzhansky 1965). Drosophila affinis group species, D. immigrans, D. melanogaster and D. simulans have a shorter developmental time and emerge before C. amoena if present in a substrate. Studies in Virginia confirmed C. amoena’s oviposition in fallen and unfallen parasitized apples, aggregated oviposition, preference for parasitized
516 rather than just damaged acorns and use of native crabapples as a breeding substrate. Parasitized apples are shared with other Drosophila earlier in summer, but the fruit growing season also begins earlier in the mid-South than in Michigan. In Virginia’s Allegheny Mountains, C. amoena is sympatric with other Chymomyza and may be collected with them on damaged trees/cut wood (Band 1988d, 1996) but none share breeding substrates (acorns, apples) with C. amoena. Dorsey et al. (1962) called C. amoena a secondary invader in acorns because acorns had to be damaged or parasitized for females to gain oviposition access. However, preference for parasitized rather than damaged acorns accorded with its preference for parasitized early fallen apples in July and frass-breeding nature in general. Band (1988b, c, 1996) suggested interspecies dependency enabled females to access firm substrates for oviposition. Band (1996) argued that species cohesion was maintained by female oviposition. Interfertility of Swiss and American C. amoena was in agreement (Band 1995b).
sites at Ma¨genwil in Canton Aargau, and at multiple locations in the Malcantone and Bolle di Magadino areas of Canton Ticino. In the Val Blenio and Malcantone regions, C. amoena larvae were found in chestnuts while netting results established that C. amoena was present in low frequency in the Val Blenio (Band et al. 1999). In this investigation parasitized substrates were inspected individually, the occurrence of C. amoena eggs and larvae recorded, removed from substrates, transferred to vials containing Lakovaara’s modified malt medium, mailed back to East Lansing, and held for emergence. Thus it was possible to assert that no behavioral changes had occurred in the ability of European C. amoena females to seek out and to oviposit in frassy fruits as well as nuts. It also indicated that interactions with primary pests attacking substrates first had been maintained. Table 5 lists the primary pests attacking fruit and nut substrates prior to C. amoena oviposition. Only domestic apples and codling moth occur in both Europe and the USA, where they were imported by the colonists.
Oviposition in parasitized apples and chestnuts in Switzerland, July 1998 In Switzerland C. amoena has been present in low numbers in the greater Zu¨rich area since 1989 (191 C. amoena collected among 116,180 non-domestic drosophilids in two wooded locations). Studies undertaken in July 1997 failed to substantiate that C. amoena was using parasitized unripe apples for a breeding substrate. In the Maggia Valley research did reveal that C. amoena was also breeding in damaged hazelnuts, wild apples and continuing to use soften damaged apples (Band et al. 1998). Flies netted in Lodano (Maggia Valley) and Zu¨rich in August 1997, were mailed to East Lansing, established as laboratory cultures and used to test the propensity of females to oviposit in parasitized unripe Michigan apples in July 1988 when early fallen parasitized apples became available. They did. In July 1998 in Switzerland studies were undertaken in Canton Zu¨rich and Canton Aargau in northern Switzerland and Canton Ticino, as shown in Table 4 and Figure 2. Chymomyza amoena was found to be breeding in parasitized fallen apples at two sites in/near Zu¨rich, at two
Can the spread of Chymomyza amoena into orchard apples in northern Switzerland and into Italy be predicted? The challenge now is to make invasion biology a predictive science (Kareiva 1996; Vermeij 1996; D’Antonio and Kark 2002; Mack et al. 2002), a subject raised earlier by Simberloff (1985). Attention recently has focused on plant invasiveness (Kolar and Lodge 2001; Sakai et al. 2001; Heger and Trepi 2003) and range expansion in birds (Kolar and Lodge 2001; Sakai et al. 2001). Sakai et al. (2001) also review traits associated with colonists in general and with specific groups as fish and vertebrates. Mack et al. (2002) target plant pests–plants, pathogens and insects. Lodge (1993) also raised the question about predicting the outcome of a species colonization and noted that Simberloff (1991) had declared that for successful prediction, the potential invader and target community had to be studied intensively. However, Lodge (1993), Kolar and Lodge (2001) and Heger and Trepi (2003) note that some ecologists are pessimistic about predicting
517 Table 5. Primary pests attacking fruit and nut substrates first in which Chymomyza amoena females later oviposit in the eastern USA and in Switzerland. Substrate
Common name
Primary pest, USA
Primary pest, Switzerland
Malus domestica
Domestic apples
Malus coronaria Ornamental crabapples Juglans nigra hulls Quercus sp.
Native crabapples
Rhynchites weevils Cydia pomonella Not present
Black walnuts Oaks (acorns)
Castanea sativaa
European chestnut
Conotrachelus nenuphar Cydia pomonella As above Ragoletis pomonella Rhagoletis suavis Curculio sp. Filbert moth Blight susceptible
Castanea mollissima
Oriental chestnut
Curculio sp.
a
Not present Curculio nucum Cydia splendana Curculio elephas Cydia splendana Not present
Also imported into the United States.
the identity of non-indigeneous species. Gilpin (1990) declared there is no way to predict which species will invade or succeed as an invader, a view reiterated by Stiling (1996). Acknowledging Giplin’s pessimism, Williamson (1996) outlined several factors determining a species’ invasion success: abundant and widespread in its original habitat, climatic matching and entry into a vacant niche. Holway and Suarez (1999) declared that animal behavior is an essential component of invasion biology. Lohrer et al.’s (2000) study of the widely distributed Asian shore crab Hemigrapsus sanguineus in Tanabe Bay, Japan and in Long Island Sound, which it invaded in the 1990s, emphasized behavior and also validated Williamson. The species invaded a vacant niche, and maintains behavioral constancy for resource use in invaded vs native habitats. The finding that Nearctic Chymomyza amoena also retains behavioral constancy in exploitation of parasitized firm substrates (nuts, unripe and ripening fruits) in Switzerland indicated that its spread elsewhere might be predicted. The area north of Zu¨rich to the German border is a prime apple orchard region. Commercial orchards with older large trees grow apples for cider production. Since there is only one generation of codling moth per year (Mani et al. 1997), no spraying is done, making it feasible to gather dropped apples in mid-summer. Italy was the first country in which recovery from the chestnut blight fungus was observed near Genoa, beginning in 1950. Blight had been discovered there in 1934 and spread throughout the country. Healing progressed northeast toward
Austria and the now Slovenia border and south toward Naples by 1978 (Mittempergher 1978). Chestnut forests now cover the north face of the Orobie Alps. The fact that Nearctic C. amoena has been found in Canton Ticino close to the Italian border in both chestnuts and apples raises the possibility that it invaded Italy. At the time this prediction was made (Band et al. 1999) only one specimen had been collected in Italy in May in Veneto (Ba¨chli et al. 1999). Our objective in July 2000 was to determine if C. amoena is present in fallen parasitized orchard apples north of Zu¨rich and if it can be found in chestnut forests as well as in apples in the Valtellina region of Lombardy Province, Italy. Success would again support Williamson (1996), Simberloff (1985, 1991) that predicting the spread of a biological invader is possible, and Holway and Suarez (1999) that behavior is important to invasion success.
Materials and methods Adult C. amoena have conspicuously black banded wings; adults wingwave, a characteristic of Chymomyza in general. Eggs, larvae and pupal cases are readily distinguished from other Drosophila or drosophilids which may sometimes share fruit substrates (Sturtevant 1921; Patterson 1943; Throckmorton 1962; Schumann 1987). To determine if C. amoena could be found in substrates in northern Switzerland and in Italy, work was carried out as in summer 1998. Small vials containing Lakovaara’s malt medium were prepared at Michigan State University in early
518 July 2000, airmailed to the University of Zu¨richIrchel, and kept under refrigeration until needed. All work in northern Switzerland made use of the laboratory facilities in the Zoological Museum, University of Zu¨rich-Irchel. All work in northern Italy was done under field conditions and media vials transported for use were kept in Styrofoam coolers. Global positioning was used to define sites where substrates were collected. Northern Switzerland: Fallen apples were collected in open orchards at Marthalen on 17 July 2000; Dachsen and Rheinau in the northern part of Canton Zu¨rich on 18 July 2000; Pfyn and Dettighofen in Canton Thurgau on 19 July 2000 (see Figure 2). Attempts were made to collect primarily parasitized fallen apples. All apples were transported to the laboratory and inspected under a binocular dissecting microscope. If there were no hole (and no C. amoena eggs on the surface), the apple was discarded. Parasitized apples were inspected for the presence of frass (insect excreta) and C. amoena eggs on the surface, and the position of the egg recorded (stem, calyx, side). Otherwise, the apple was dissected along the tunnel made by a former pest larva in the apple; the absence or presence and number of C. amoena eggs and larvae in the tunnel were recorded. All eggs and larvae per apple were transferred to a vial with medium; the vial was numbered and holes punched in the plastic cap to provide an exchange of air. The number of Drosophila eggs and larvae in the apples, if any, was also noted, transferred to medium and the vial numbered. If the Drosophila and C. amoena eggs and larvae shared the same apple, all were
transferred into the same vial. Codling moth larvae were still in some apples with C. amoena preadults and their presence was also recorded. Vials with C. amoena eggs and larvae were kept under room temperature conditions prior to mailing to Michigan State University to record emergence. Altitude, latitude and longitude for northern Switzerland sites are given in Table 6. Northern Italy: The Valtellina region in Lombardy is characterized by an agricultural valley between two alpine ranges. Vineyards dominate on the south facing slopes of the Rhaetian Alps which are shared with Switzerland. Chestnut forests (Castanea sativa, the European chestnut) cover the north facing slopes of the Orobie Alps, which are totally within Italy. Between Tirano and Sondrio, commercial apple orchards consisting largely of dwarf colunmar apple trees are abundant in the valley. Beyond Sondrio, apples give way to maize. Here and there, especially around Tirano, old but still producing apple trees can be found. Sites sampled in the Valtellina region (apples, 1; chestnuts, 4; adults netted over fermented banana bait, 3) were named according to the nearest map location. GPS coordinates are in Table 6, the area by X in Figure 1. Apple collections were made under several trees at a small village called Calcarola on 28 and 30 July 2000. Apples were handled as previously. Calcarola is slightly west of Tirano. The major focus was on chestnut collections in the chestnut forests at four locations and on drosophilids netted over banana bait at three locations: between the Swiss/Italian border and
Table 6. Global positioning coordinates for sites sampled in northern Switzerland for fallen parasitized apples and in the Valtellina region, Lombardy Province, Italy, for fallen parasitized apples and chestnuts in July and August 2000. Country
Site
Altitude
Latitude (N)
Longitude (E)
Switzerland
Marthalen Dachsen/Rheinau Pfyn Dettighofen
405 ~405 ~405 ~405
m m m m
4737.18¢ 4739.76¢ 4735.62¢ 4736.87¢
838.93¢ 832.40¢ 856.89¢ 857.13¢
Italy
Border/Tirano Calcarola San Sebastiano (A) San Sebastiano (B) Castel dell’Acqua #417 trail marker Bormio
495 m ~495 m 500 m 496 m 554 m 509 m 1193 m
4613.58¢ 4609.96¢ 4608.84¢ 4608.86¢ 4608.99¢ 4612.31¢ 4628.51¢
1008.82¢ 1006.48¢ 1002.45¢ 1002.37¢ 1000.54¢ 1009.90¢ 1023.02¢
519 Tirano at 495 m, San Sebastiano (B) at 496 m in the chestnut forest, and Bormio at 1193 m. At the first site where drosophilids were netted there were relatively young Robinia pseudoacacia (black locust) trees and a single chestnut tree. There were many chestnut trees on the eastern slope of the mountain but they were separated from the collecting site by the railway line and the main highway. At San Sebastiano (B) the chestnut forest also contained some beeches. At Bormio, the woods were more or less homogeneous larches Larix decidua surrounding a small garbage dump for garden refuse. The nearest bait was set in the woods at a distance of about 50 m from the garbage dump. Fallen chestnuts were collected in the mixed chestnut/beech forest under trees at an area just above San Sebastiano at 500 m (designated A) on 30 July 2000, in the forest at San Sebastiano (B) at 496 m also on 30 July 2000, west of San Sebastiano near Castel dell’Acqua at 554 m on 31 July 2000 and east of Tirano near #417 trail marker at 509 m altitude on 2 August 2000. Attempts were made to collect parasitized nuts (i.e. with hole) that had not been reduced to shells over time. All chestnuts were dissected under a binocular microscope and searched for the presence of C. amoena eggs, larvae and pupae. The presence of pest larvae remaining in the chestnuts (Bovey et al. 1975), if any, was also noted. No other drosophilid preadults were in the chestnuts. Flies were netted over banana bait evening and morning at a site between the Swiss/Italian border and Tirano from 29 July to 3 August 2000, at the San Sebastiano (B) site from 31 July to 2 August, and evenings only at the Bormio site from 29 July to 2 August. Oviposition studies, Italian Chymomyza amoena, November 2000 To determine if oviposition preferences existed among the apple derived and chestnut associated Italian C. amoena, cultures were established at Michigan State University from emergents from the two different substrates; C. amoena netted at San Sebastiano were added to the chestnutderived stock. Chestnuts used in the experiments were cut with an X to pierce the outer shell, placed in a plastic bag, sprinkled with distilled
water to keep them moist, and kept in a refrigerator until used. One chestnut and one slice of commercial apple (Red Delicious variety) were placed together in a pint-sized glass population bottle containing a small population of C. amoena, either Calcarola (apple) or San Sebastiano (chestnut). Substrates were left in each bottle 2– 3 days. Experiments were repeated three times for each locality. A second group of imported chestnuts was purchased because one showed an exit hole made by a departing pest larva. This chestnut was used to verify that females would enter the hole and oviposit inside the nut. It was soaked in distilled water for several days prior to placing it in a population bottle of San Sebastiano flies together with a dish of C. amoena medium. It remained in the population bottle for 3 days. Oviposition studies, commercial chestnuts, 2002 In December 2001 commercial chestnuts were again purchased locally. Nuts were slit on one side and soaked in distilled water for varying periods of time, 3–30 days. Individual nuts were transferred to population bottles of flies from different localities which were allowed to oviposit on/in them for 2–3 days. Each nut was then transferred to a population bottle with moistened tissue. Distilled water was used to moisten each nut and tissue every 3 days. Nuts were monitored for egg hatchability, larval development, pupation and adult emergence.
Results Northern Switzerland As shown in Table 7, 516 fallen apples were gathered from five locations. Of these 367 were parasitized (had a hole to the exterior) and were inspected for the presence of C. amoena eggs and larvae. In northern Switzerland only a few parasitized apples at each location in mid-July contained C. amoena eggs. The incidence of fallen parasitized apples with C. amoena eggs (3%) was very significantly lower than in the Zu¨rch/ Ma¨genwil area (12%) in 1998 (v2 ¼ 14.93; df ¼ 1; P ¼ 0.0001). All C. amoena eggs were in tunnels inside the parasitized apples. Codling moth
520 Table 7. Existence of Chymomyza amoena eggs (e) and larvae (l) in fallen parasitized apples in July 2000 in five places in northern Switzerland. Place
Total no. apples
Parasitized apples
No. C. amoena
%
Emerged
Marthalen Dachsen Rheinau Pfyn Dettighofen Totals
82 120 103 107 104 516
No C. amoena With C. amoena 43 3 63 3 84 1 64 2 103 1 357 10
(e, l) 7 (5, 2) 6 (1, 5) 1 (0, 1) 3 (1, 2) 1 (0, 1) 18 (7, 11)
3.7 2.5 1.0 2.8 1.0 2.0
1 3 4
The % apples with C. amoena eggs and larvae is calculated by dividing the number of apples with C. amoena in the sample by the total number of apples collected at that place.
larvae were in apples at each location except Marthalen. At Pfyn, a C. amoena egg and a codling moth larva shared the same tunnel. At Marthalen one C. amoena egg, one C. amoena larva and one Drosophila eggs were in the same tunnel; one apple had four Drosophila eggs and another a Drosophila larva in frass. At Dettighofen one apple had a Drosophila larva. The Drosophila which emerged were D. subobscura. Thus, while 10 apples out of 367 parasitized apples had a total of 18 C. amoena preadults, only 3 apples had a total of exclusively 6 Drosophila preadults. No Drosophila preadults were in parasitized apples collected at the Ho¨nggerberg and Hotel Zu¨rich orchards in Canton Zurich or at the Ma¨genwil sites in Canton Aargau in July 1998 (Band et al. 1999; Table 4). However, Schatzmann (1977) reported D. subobscura emer-ged from soft juicy fruits as wild strawberries Fragaria vesca in June, wild sweet cherries Prunus avium and raspberries Rubus idaeus in July in the Aarau region of Canton Aargau. The percentage of C. amoena imagoes from the total number of eggs and larvae taken from the apples, 22.2%, is in agreement with past findings in both the United States and Switzerland. Not
all C. amoena eggs hatch, not all larvae successfully develop into adults. Valtellina Region, Lombardy Province, Italy As shown in Table 8, 94 fallen apples, 71 of them parasitized, were collected near the small village of Calcarola and inspected for the presence of C. amoena eggs and larvae. Two collections were made under the same tree. A total of 17 parasitized apples contained C. amoena eggs and larvae. Infestation rate is significantly higher than in northern Switzerland, as shown in Table 9. This agrees with the results obtained in July 1998 when the numbers of fallen parasitized apples containing C. amoena eggs and larvae in the greater Zu¨rich and Ma¨genwil areas were compared with the numbers obtained in southern Ticino. Results in both years also reflect the fact that some varieties of parasitized apples are more attractive to ovipositing C. amoena females than others. However, the incidence of apples with C. amoena eggs and larvae was significantly higher in July 1998 in southern Ticino (41%) (Band et al. 1999; Table 4) compared to the rate at Calcarola (24%) (v2 ¼ 3.89; df ¼ 1; P ¼ 0.05).
Table 8. Existence of Chymomyza amoena eggs (e) and larvae (l) in fallen parasitized apples in July 2000 in collections made at Calcarola in the Valtellina region of Italy. Collection 28 July 28 July 30 July Totals
Total no. apples
Parasitized apples
7, green 63, red 24, green 94
No C. amoena 2 43 9 54
With C. amoena 1 14 2 17
No. C. amoena
%
Emerged
(e, l) 3 (3, 0) 40 (38, 2) 3 (3, 0) 46 (44, 2)
14.7 22.2 8.3 18.1
1 5 6
The % apples with C. amoena eggs and larvae is calculated by dividing the number of apples with C. amoena in the sample by the total number of apples collected.
521 Table 9. Comparison of numbers of parasitized apples without and with Chymomyza amoena eggs and larvae in collections from northern Switzerland and at Calcarola, Italy in July 2000. Country
Parasitized apples
Northern Switzerland Calcarola, Italy Total
No C. amoena 357 54 411
Total With C. amoena 10 17 27
367 71 438
v2 = 42.71; df = 1; P < 0.0001.
In northern Switzerland, all C. amoena eggs and larvae were found in tunnels inside fallen apples. At Calcarola, 32 of the 38 C. amoena eggs were on the outside of the apple in frass (insect excreta) which had been deposited by the primary pest larva inside. Oviposition in frass is characteristic of C. amoena females (Band 1988a– d, 1996). More codling moth larvae were also observed in the apples, and one apple with four C. amoena eggs in frass at the stem had a codling moth larva inside. Three apples each had from one to four Drosophila subobscura eggs or larvae (for a total of eight D. subobscura) in addition to C. amoena. As shown in Table 10, chestnut collections in late July/early August at four different sites had parasitized chestnuts with C. amoena preadults inside. These were nuts that had presumably fallen the previous autumn from which at least one pest larva inside then exited. Multiple Curculio elephas weevil larvae can complete development, exit from a nut, burrow into the soil and pupate. However, if there are multiple Cydia splendana larvae, only one can complete development in a chestnut, exit and form a cocoon; the others remain in a larval state (Bovey et al. 1975). As shown in Table 11, in the 13 parasitized chestnuts lacking pest larva inside, there were 26 C. amoena larvae and 6 pupae; in the 7
chestnuts containing pest larvae in arrested development there were 22 C. amoena third instar larvae and 2 pupae, (v2 ¼ 2.51; df ¼ 2; P ¼ 0.28). The continued presence of pest larvae may not hamper C. amoena development. The supply of parasitized nuts indicates that chestnuts may be a more readily available breeding substrate for this species in the Valtellina region than apples. The total number of parasitized nuts with C. amoena preadults inside (20) was comparable to the total number of parasitized apples containing C. amoena preadults (17). However, stages within the substrates differed significantly as indicated in Table 12. Significantly more eggs were found in apples, indicating recent ovipositions, whereas the chestnuts contained more larvae and in some cases empty pupal cases. Minimum generation time during the breeding season is approximately one month for this developmentally polymorphic species (Band 1988a). No other drosophilids were present inside the parasitized chestnuts in contrast to finding a few D. subobscura in the fallen apples. Some 300 nuts over all sites were found to be merely shells, too old to be attractive to ovipositing C. amoena; many contained ants. They have not been included in the table. Table 13 lists the drosophilids collected over banana bait near Tirano, at San Sebastiano (B)
Table 10. Existence of Chymomyza amoena eggs (e), larvae (l) and pupae (p) in parasitized chestnuts Castanea sativa in collections made in July/August 2000 in four regions of chestnut forests in the Orobie Alps, Valtellina region of Italy. Place San Sebastiano (A) San Sebastiano (B) Castel dell’Acqua #417 trail marker Totals
No hole
Parasitized nuts
19 9 18 19 65
No C. amoena 47 40 48 55 190
No. C. amoena Emerged (e,l,p) With C. amoena 2 5 5 8 20
% 2.9 9.3 7.0 9.8 7.3
3 (0,3,0) 22 (1,17,4) 12 (0,11,1) 20 (0,17,3) 57 (1,48,8)
1 1 2
The % is calculated by dividing the number of parasitized nuts with C. amoena in the sample by the total number of nuts collected.
522 Table 11. Chymomyza amoena preadults in parasitized chestnuts without and with pest larvae-Valtellina region, Italy, 2000. No pest larvae Location Eggs San Sebastiano A San Sebastiano B Castel dell’Acqua #417 trail marker Totals
With pest larvae
Larvae 3 11 12 26
Eggs
Larvae
Pupae
Eggs
2 1 3 6
1
6 11 5 22
2
1
2
1
1
Table 12. Comparison of preadult Chymomyza amoena stages in parasitized apples vs parasitized chestnuts, Valtellina region, Italy, July/August 2000. Substrate
Eggs
Parasitized apples 44 Parasitized chestnuts 1
Totals
Pupae
Larvae
Pupae
Total
2 48
0 8
46 57
v2 = 91.28; df = 2; P < 0.00001.
and at Bormio. Eighteen adult C. amoena were netted at San Sebastiano, confirming the presence of this species in the Orobie chestnut forests. One
Larvae 3 17 11 17 48
Pupae 4 1 3 8
C. amoena specimen was also netted among the 1894 individuals representing 19 drosophilid species near Tirano. It was not captured at Bormio; nor had we sampled substrates for its presence there. Although more collections were made in the mixed chestnut forest at San Sebastiano than at higher altitude Bormio, fewer individuals were netted despite similar numbers of species. Two cosmopolitan species were netted in all three areas: D. funebris and D. immigrans. Five Palearctic species were netted in all areas: D. kuntzei,
Table 13. Drosophilids netted over fermented banana bait at three locations in the Valtellina region of Italy, July/August 2000. Location
Tirano
San Sebastiano
Bormio
Altitude Dates Species D. alpina D. andalusiaca D. bifasciata D. deflexa D. fenestrarum D. funebris D. helvetica D. histrio D. hydei D. immigrans D. kuntzei D. limbata D. littoralis D. obscura D. phalerata D. repleta D. simulans D. subobscura D. testacea D. transversa D. tristis C. amoena S. pallida
495 m 29 July–3 August
496 m 31 July–3 August
1193 m 29 July–2 August
1 5
18
Totals
1894
598
1333
3825
No. species
19
12
13
23
1 1 1 1 17 1 4 342 56 501 4 1 18 421 1 87 428 4
2
2 5 52 14 325 1 8 58 3 42 70
1
1 16 2
164 12 1 1122 5 4 2
Totals
1 1 3 1 17 4 9 394 1 86 828 5 1 190 491 3 2 1251 503 8 2 19 5
At Tirano and San Sebastiano collections were made morning and evening. At Bormio in the evening only.
523 D. obscura, D. phalerata, D. subobscura and D. testacea. Drosophila histrio, D. kuntzei, D. phalerata and D. testacea are mushroom breeders (Shorrocks 1982). They comprise some 1700 of the nearly 1900 individuals collected in/near Tirano and 500 of the nearly 600 individuals netted at San Sebastiano. Drosophila obscura and D. subobscura have also been bred from sap fluxes and decaying vegetation as has also D. phalerata (Shorrocks 1982); D. immigrans, D. simulans, D. obscura and D. subobscura have been reared from wild and domestic fruits (Schatzmann 1977; Shrorrocks 1982; Burla and Ba¨chli 1991b). Drosophila subobscura, the most common nondomestic European species, dominates the collection at Bormio and comprises almost a third of the total numbers of drosophilids, 3825, netted over bait in the three sampling areas. At higher altitude Bormio, D. alpina was present, as in the 600–1100 altitudes in Canton Ticino (Ba¨chli and Burla 1992). There have been few studies on species’ distributions in Italy; D. alpina represents a new record for the Italian fauna.
position site in laboratory tests is in agreement with past findings for North American C. amoena (Band 1988a). Nevertheless, Band (ibid.) used domestic (commercial) apple in the laboratory to demonstrate that prolonged emergence of C. amoena from immature/ripe parasitized apple collections in the USA in summer reflected a developmental polymorphism. The low number of eggs in a 72 h period is also in agreement with the low number of eggs laid by one replicate of a 1997 Zu¨rich culture (40 eggs) on unripe Michigan apples in July 1998, also over a three-day period (Band et al. 1999). Oviposition in a parasitized chestnut, November 2000: Females laid 23 eggs inside the hole, four around the rim. A small knife was used to open up the hole to count the eggs within the opening. Band (1993b) showed that Virginia C. amoena would oviposit in oriental chestnuts Castanea mollissima from which weevil larvae had emerged. C. amoena may use oriental chestnuts as an overwintering/breeding site niche at a farm near Mt. Lake Biological Station (Band 1996; Table 3).
Laboratory oviposition studies
Oviposition and emergence from commercial chestnuts, January–March 2002 Table 14 shows the results of paired tests using chestnuts soaked for varying periods of time in distilled water. All small populations of C. amoena laid eggs on the moist chestnuts. This included East Lansing, MI, and Zu¨rich females. Neither population encounters chestnuts in the natural environment. Despite periodic wetting following removal of the adults, only nuts soaked for 30 days remained soft enough to sustain larval growth. Calcarola females laid 51 eggs in the nut
Italian Chymomyza amoena, chestnut vs apple: Both Calcarola and San Sebastiano females prefer to oviposit in chestnuts rather than in domestic apple. The Calcarola flies laid no eggs on apple, despite having emerged from apple. Females laid a total of 43 eggs on chestnuts. The San Sebastiano females laid 35 eggs on chestnuts, 6 on apple (v2 ¼ 21.98; df ¼ 1; P < 0.005). That Italian C. amoena from apples and chestnuts discriminate against ripe domestic apple as an ovi-
Table 14. Laboratory oviposition and emergence records in commercial chestnuts, January through March 2002 using various laboratory Chymomyza amoena stocks. In distilled water
Stock
No. eggs laid
No. days
Emergence
3 days
00SSa 92EL 00SS 97Zu¨rich 00SS 00Cal
>70 >40 21 49 25 51
3 3 3 3 2 2
Noneb Noneb Noneb Noneb 15 30
2 weeks 1 month
Individual nuts placed on tissue and wetted every 3 days. a Parasitized nut. b Dried. SS = San Sebastiano, Italy; EL = East Lansing, MI; Zu¨rich, Switzerland; Cal = Calcarola, Italy. 00 = 2000; 92 = 1992; 97 = 1997.
524 provided, 30 adults emerged; San Sebastiano females laid 25 eggs, 15 adults emerged. Adults emerging were small due to larval crowding. Burla and Ba¨chli (1992) reported 1–14 C. amoena adults emerged from individual chestnuts and acorns collected in the Maggia Valley, Canton Ticino in 1990 and 1991. Aggregated oviposition characterizes the species (Band 1989).
Discussion When Nearctic C. amoena entered the former Czechoslovakia in 1975 and began to spread (see Figure 1), it entered a Continent where domestic apples had been under cultivation since before Roman times, where English oaks are widespread, where European chestnuts have staged a comeback from the chestnut blight which devastated North American chestnut forests, and where primary pest insects attack developing fruits and nuts. European drosophilids had also been under intensive study during the 20th century (Ba¨chli and Roche-Pite´ 1982) and there was no nut breeding drosophilid until the arrival of C. amoena. Niemala¨ and Mattson (1996) argued that European forests were largely closed to insect invaders (34 phytophagous insects from North America vs 266 from Europe to North America in the past 500 years, Mattson et al. 1994). However, C. amoena was preadapted to invading the forests and exploiting the parasitized nut breeding niche. The fact that Swiss females from cultures maintained in Michigan would oviposit and larvae develop in parasitized unripe Michigan apples (oviposition: 209 eggs in five such apples; emergence: seven adults from one apple with 14 eggs) showed that the species could continue to exploit parasitized apples also. Can the spread of Chymomyza amoena be predicted? As hypothesized by Simberloff (1985, 1991) sufficient information about a biological invader and the target community enables its spread into that community to be predicted. In northern Switzerland the fact that (1) C. amoena has been present at low frequencies for at least a decade in the greater Zu¨rich area, (2) that Swiss females still
exploit parasitized apples as a breeding substrate and (3) populations in the greater Zu¨rich area and Canton Aargau were breeding in parasitized fallen apples in summer 1998 enabled predicting and subsequently finding that the species has spread northward into commercial orchards along the German borders in Cantons Zu¨rich and Thurgau. The 3% infestation rate among parasitized apples is the lowest realized in Switzerland and probably reflects a very low C. amoena population density in that region. Where else C. amoena may be breeding in northern communities remains unknown. It has been consistently netted among non-domestic drosophilid species in two locations in the greater Zu¨rich area, but nut producing trees as oaks were not present. Apples and apple orchards represent a domestic environment. In Canton Ticino, C. amoena is now widespread especially in the southern region. It has been found in the mixed chestnut forests in and above the Maggia Valley (Burla and Ba¨chli 1992; Band et al. 1998), in the Val Blenio, in the Malcantone region in southern Ticino and very near the Italian border (Band et al. 1999). Its significantly higher incidence among parasitized apples in southern Switzerland (Band et al. 1999) probably reflects both the longer growing season and variety of nut and other fruit substrates available to the species there. Predicted to have entered Italy, C. amoena in fact seems well established in northern Italy’s Valtellina region. Parasitized chestnuts may provide overwintering and breeding season substrates for the species until the new season’s fallen parasitized apple crop is available. Significantly more eggs were found in apples, whereas third instar larvae and some pupae were in chestnuts. Few apples in both northern Switzerland and at Calcarola had Drosophila eggs; none of the chestnuts contained Drosophila. Nevertheless, 11 Drosophila species were netted with C. amoena in the mixed chestnut forest at the San Sebastiano (B) site where parasitized chestnuts contained 17 C. amoena larvae, four pupae and one egg. Similar results were obtained in the Torre Pellice area in the northwestern section of Piedmont Province in northern Italy in July 2002. Thirty-five C. amoena adults were netted in the chestnut woods among over 10,000 drosophilids representing 20 species, but only C. amoena
525 larvae were in parasitized chestnuts while females had just begun to oviposit in available fallen parasitized apples (Band et al. 2003). In July 2001 we determined if this species could predictably be found in the chestnut woods of southern Austria, having spread south from Vienna where it was found in 1990. As expected, 28 C. amoena adults were netted among over 10,300 drosophilids representing 26 species in the chestnut woods. However, chestnuts were dry and females were ovipositing in frassy apples and also English walnuts J. regia. Again, few Drosophila shared substrates with C. amoena (Band et al. 2003). Chymomyza amoena has consistently been netted among 11–26 drosophilid species in northern Italy, Austria and Canton Ticino (Band et al. 1999, 2003), and among 16–24 species in the greater Zu¨rich area (Band et al. 1998). Drosophilid species richness has not impeded the entry of C. amoena into the established drosophilid community. The role of species richness in impeding invasions remains controversial (Stachowicz et al. 1999; Levine 2000). Shorrocks et al. (1984) argued that, among Drosophila, interspecific competition is not a factor influencing drosophilid community organization in nature although Burla and Ba¨chli (1993) found negative dissociations among fruit breeding species, and both studies apply to species reared from soft rotting fruits, not fallen unripe and ripening apples. Vacant niches Williamson (1996) included entry into vacant niches among the factors promoting invasion success. Because ‘vacant niche’ is controversial, Mack et al. (2002) suggested instead that invaders enter unused or underused niches. Williamson (1996) and Shea and Chesson (2002) argued it is how resources are used that define niche opportunities for a biological invader, not the number of already existing species. Lohrer et al. (2000) showed that resources used by the Asian shore crab Hemigrapsus sanguineus, which is now established in southern New England, are quite different from resources used by resident crabs in the invaded habitat. It entered ‘an unused niche’, according to Mack et al. (2002). Chymomyza amoena clearly is not using unused substrates; drosophilids require damaged surfaces for ovipo-
sition. In a study of acorn decay Winston (1956) showed C. amoena females oviposted in acorns in stage II or III decay, which could extend longer than a year under appropriate conditions. One could argue that C. amoena exploits underused niches, according to Mack et al. (2000). However, the vacant niche controversy arises from Hutchinson’s claim that the niche is a property of the species (Schoener 1989; Griesemer 1992). Hewitt and Bultin’s (1997) statement linking behavior and physiology of an organism to its native habitat adopts a view similar to Hutchinson’s although Hutchinson stressed species-level properties. An organism that retains exactly the same properties and uses comparable resources in the invaded habitat as in the home environment, which sympatric species in the invaded habitat do not use, signifies that the niche was vacant and a missing species has been introduced. Herbold and Moyle (1986) made introducing (accidently) ‘the missing species’ the criterion for defining that the niche had been vacant. Lohrer et al.’s (2000) finding that the Asian shore crab introduced into Long Island Sound and the northeast coast of North America uses similar resources in the invaded LIS habitat and Tanabe Bay, Japan, and does not overlap with crabs in the invaded habitat shows that its evolved behavior has been retained in the new environment (Hewitt and Bultin 1997), and constitutes a ‘missing species’ (Herbold and Moyle 1986). Williamson (1996) provides two other examples of entry into vacant niches: the pox virus producing myxomatosis in rabbits and the introduction of muskrats into Europe since previously there was no large aquatic vole in Europe. Introduction of placental mammals into Australia where only marsupials had evolved was a large scale entry into vacant niches. The prickly pear cactus moth Cactoblastis cactorum is native to Argentina, was brought into the Caribbean for biological control in 1957, has now invaded Florida where it is already attacking Opuntia cacti and has spread to South Carolina. It is viewed as an immediate threat to endemic cacti in the southwestern United States and to wild and cultivated Opuntia in Mexico (Stiling 2002). Ironically, a population of Monarch butterflies Danaus plexippus that appeared in Australia in 1870/1871 and subsequently spread (Clarke and Zalucki 2004) was also an entry into a vacant niche since its
526 main host plant Asclepias curassavica (Bloodflower, a tropical milkweed) was already available. Ma´ca and Ba¨chli (1994) argued that the success of Nearctic C. amoena in Europe was due to its entry into open ecological niches. As the only parasitized fruit/nut breeding drosophilid on the European Continent, this appears to be the case. Interspecies dependency as an example of facilitation via indirect effects Chymomyza amoena is actually a member of the fruit and nut breeding insect communities. However it is neither among the primary insects attacking either substrate first nor among the end stage users. Shea and Chesson (2002) state that community ecology theory is relevant to the study of biological invasions. Schowalter (2000) noted that indirect effects among species have only recently begun to receive attention in community ecology. Indirect effects are defined by Miller and Travis (1996) as ‘the effect of one species on another that occurs through the mutual interaction with a third species’ and can include positive and negative effects. Stiling (1996) also states that indirect effects typically involve three species, lists apparent competition, facilitation, some mutualisms, cascading effects, tri-trophic interactions and non-additive effects among the different types of indirect effects, and provides examples. Bruno et al. (2003) stress that facilitation, i.e. positive interactions between species, needs to be included in modern ecological theory. They recognize that positive interactions between species can be both direct and indirect. They do not specifically mention interspecies dependency as a category of facilitation. As a concept it seems to have emerged initially in conservation biology and spans the biological gamut (Band 1988b). Examples there implicate no biological invaders. However Simberloff and Von Holle (1999) document many positive interactions between exotic species. Interspecies dependency results when the activities of one species create the habitat exploited by other species. In the United States, C. amoena interacts with native insect species in utilizing nuts including oriental chestnuts. Domestic fruits and codling moth were imported from Europe by
the colonists while attacking curculio weevils as Conotrachelus nenuphar represent host switchers. In Europe, Rhynchites weevils replace curculios in attacking apples, and acorns and chestnuts are initially attacked by insects not present in the United States as shown in Table 5. However, the effect is the same: a primary pest larva inside the substrate cuts a hole to the outside both to deposit frass (i.e. codling moth) and to exit at the completion of larval development. This enables a C. amoena female to lay eggs either inside in a tunnel or outside primarily in frass. Parasitized nuts are available in autumn, spring and summer (and possibly for a year after their fall, Winston 1956) unless they become too dry; parasitized apples and other fruits become available in summer. Grapholitica prunivora, the lesser apple worm, is considered a pest but frequently oviposits in apples parasitized by codling moth. In Michigan, it follows C. amoena in oviposition; in Virginia and North Carolina, the two overlap. Present in Europe, it was in frassy apples in Calcarola, Italy. Ant colonies inside chestnut shells represent end stage users. Other drosophilids may also manifest interspecies dependency. In North America trees felled by beavers which then begin to rot in water attract species of the D. virilis group for oviposition (Powell 1997). Band (1988b) noted that Lachaise (1977) found that African lissocephalids preferentially oviposit around holes made by fig weevil larvae, if available, while Barker (1982) reported that D. buzzatti and D. aldrichii relied on the Cactoblastis cactorum moth to attack Opuntia cactus in Australia. To date, however, C. amoena seems to be the only drosophilid invader which has relied on interspecies dependency for establishment and spread in central and southern Europe. Frass breeding and Drosophila evolutionary potential Oviposition by C. amoena females in frass or adults feeding on frass indicates an adaptation to a nitrogenous environment. Frass as insect excreta is rich in uric acid/urea. Carson (1974) reported three species of drosophilids living in association with land crabs, whose larvae occupy
527 the nephritic grooves during all or part of their prepupal development. Wallace (1978) was able to adapt a D. virilis strain to a high urea environment (artificial crab). In the American South (Virginia, North Carolina) Band (1995a) showed that Drosophila cosmopolitan species – D. melanogaster, D. immigrans, D. busckii – and native species D. affinis frequently emerged from frassy apples in June and July along with C. amoena; four D. melanogaster emerged from acorns with C. amoena in autumn 1989. In Michigan cosmopolitan D. melanogaster, D. simulans and D. immigrans exploit frassy fruits (apples, pears, ornamental crabapples) in autumn. There was one incidence of cosmopolitan D. busckii and D. immigrans emerging from black walnut hulls in October. Pears had been parasitized by codling moth, ornamental crabapples by Rhagolettis pomonella and black walnut hulls by Rhagoletis suavis. Among cosmopolitan species it appears there is sufficient genetic diversity to move into soft frassy substrates, but Band (1995a) suggested that frass breeding was a relatively new niche for the North American Drosophila, possibly associated with the further disappearance of farms and orchards. In Europe currently there appear to be few Drosophila following C. amoena in frassy apples. Fallen damaged apples gathered in the Maggia Valley in July 1998 that yielded D. subobscura, D. simulans and D. immigrans along with C. amoena were already soft and none were found to have codling moth tunnels (Band et al. 1998). However Parsons and Hoffman (1986) showed that fruit odors will attract Drosophila; D. subobscura (Burla and Ba¨chli 1993) and D. melanogaster (Del Solar and Palomino 1966) females lay eggs where others of their species also lay eggs, while D. melanogaster also prefers oviposition substrates already containing larvae, even if these are of a different species (Del Solar and Palomino 1966). Hence facilitation and appropriate genetic variability may eventually lead to Drosophila species in Europe sharing frassy apples with C. amoena as has been found in the United States.
Conclusions Commercial orchards in Europe growing apples for cider production typically do not use sprays
in the orchards. This creates a potentially open invitation for C. amoena invasion because both Rhychitis weevils and codling moth are present and attack developing apples, which tend to fall from the trees early. This is why C. amoena was in fallen parasitized apples gathered in the commercial orchards along the Swiss/German border. Although 70% of the apples gathered from the ground were parasitized, only 3% of those had C. amoena eggs and larvae. The low population density of C. amoena in such a large apple growing region indicates that it may never become as widespread or well established in neighboring Germany as it is in Switzerland. Chymomyza amoena is now widespread in the chestnut forests of southern Europe (Canton Ticino in Switzerland, northern Italy, southern Austria) where it is the only drosophilid using fallen parasitized chestnuts as a breeding substrate. However, females primarily oviposit in available fallen parasitized apples by mid/late July in all three countries. Fallen chestnuts have sometimes been found to dry out by mid/late summer, creating a need for alternate breeding substrates if a population is to become established in an area. Chestnuts in Italy now extend as far south as Naples. Whether C. amoena will continue to expand southward in Italy depends on the availability of alternate breeding substrates in summer in addition to chestnuts. When C. amoena entered Italy remains unknown. It also seems likely that C. amoena once bred in fallen parasitized chestnuts Castanea dentata in the eastern United States.
Acknowledgements We thank all property owners for permission to collect in their orchards and gardens. We thank Dr Deb McCullough, Departments of Entomology and Forestry, Michigan State University, for her critical reading of the manuscript and the editors of Mitteilungen Schweizerischen Entomologischen Gesellschaft for allowing us to reproduce Figure 1. Comments and suggestions of a reviewer have greatly improved the paper. One of us (H.T. Band) is indebted to Dan Simberloff for introducing her to the concept of interspecies dependency during a lecture series at Mt. Lake
528 Biological Station in summer 1987. Statistics used Graphpad Instat.
References Ayala FJ, Serra L and Prevosti A (1989) A grand experiment in evolution: the Drosophila subobscura colonization of the Americas. Genome 31: 246–255 Ba¨chli G and Burla H (1985) Diptera, Drosophilidae. Insecta Helvetica. Vol 7. Zu¨rich, Schweizeriche Entomologische Gesellschaft, 116 pp Ba¨chli G and Burla H (1992) Altitudinal effects in assemblages of Drosophilidae (Diptera) in Ticino, Switzerland. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 65: 177–185 Ba¨chli G and Rocha Pite´ MT (1981) Drosophilidae of the Palearctic region. In: Ashburner M, Carson HL and Thompson, Jr. JN (eds) Genetics and Biology of Drosophila, Vol 3a, pp. 169–196 Ba¨chli G and Rocha Pite´ MT (1982) Annotated bibliography of Palearctic species of Drosophilidae (Diptera). Beitra¨ge zur Entomologie, Berlin 32: 203–392 Ba¨chli G, Papp L and Vanin S (1999) New records of Aulacigastridae and Drosophilidae (Diptera) from Switzerland, Italy and Greece. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 72: 119–122 Band HT (1988a) Host shifts of Chymomyza amoena (Diptera: Drosophilidae). American Midland Naturalist 120: 163– 182 Band HT (1988b) Chymomyza amoena (Diptera: Drosophilidae), an unusual urban drosophilid. Virginia Journal of Science 39: 242–249 Band HT (1988c) Chymomyza amoena (Diptera: Drosophilidae) in Virginia. Virginia Journal of Science 39: 378–392 Band HT (1988d) Behavior and taxonomy of a chymomyzid fly (Chymomyza amoena. International Journal of Comparative Psychology 2: 3–26 Band HT (1989) Aggregated oviposition by Chymomyza amoena (Diptera: Drosophilidae). Experientia 45: 893–895 Band HT (1991) Acorns as breeding sites for Chymomyza amoena (Loew) (Diptera: Drosophilidae) in Virginia and Michigan. Great Lakes Entomologist 24: 45–50 Band HT (1993a) Drosophilidae (Diptera) collected in spring in Michigan. The Great Lakes Entomologist 26: 237–240 Band HT (1993b) Just the right size. Drosophila Information Service 73: 101–102 Band HT (1994) The vine loving pomace fly and the pretty pomace fly. Michigan Academician 27: 95–109 Band HT (1995a) Frassy substrates as oviposition/breeding sites for drosophilids. Virginia Journal of Science 46: 11–23 Band HT (1995b) Is Chymomyza amoena (Loew) (Diptera: Drosophilidae) a versatile, colonizing species? Mitteilungen der Schweizerischen Entomologischen Gesellschaft 68: 23–33 Band HT (1996) Sympatry and niche shift among temperate zone Chymomyza (Diptera: Drosophilidae) and the mate recognition controversy. Evolutionary Biology 29: 151–214
Band HT and Band RN (1980) Overwintering of Chymomyza amoena larvae in apples in Michigan and preliminary studies on the mechanism of cold hardiness. Experientia 36: 1182–1183 Band HT and Band RN (1984) A mild winter delays supercooling point elevation in freeze tolerant Chymomyza amoena larvae (Diptera: Drosophilidae). Experientia 40: 889– 891 Band HT and Band RN (1987) Amino acid and allozyme frequency changes in overwintering Chymomyza amoena (Diptera: Drosophilidae) larvae. Experientia 43: 1027–1029 Band HT, Band RN and Ba¨chli G (1998) Further studies on Nearctic Chymomyza amoena (Loew) (Diptera: Drosophilidae) in Switerland. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 71: 395–405 Band HT, Ba¨chli G and Band RN (1999) Nearctic Chymomyza amoena (Loew) (Diptera: Drosophilidae) remains a domestic species in Switzerland. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 72: 75–82 Band HT, Band RN and Ba¨chli G (2003) Nearctic Chymomyza amoena (Loew) is breeding in parasitized chestnuts and domestic apples in northern Italy and is widespread in Austria. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 76: 307–318 Barker JSF (1982) Population genetics of Opuntia breeding Drosophila in Australia. In: Barker JSF and Starmer WT (eds) Ecological Genetics and Evolution: the Cactus-YeastDrosophila Model System, pp 209–224. Academic Press, New York Bounous G (2002) Situazione in Italia. In: Bounous G (ed) Il Castagno, pp 191–213. Edagricole. Bologna, Italy Bovey P, Linder A and Mu¨ller O (1975) Recherches sur les insectes des chaˆtaignes au Tessin (Suisse). Schweizerische Zeitschrift fu¨r Forstwesen 126: 781–820 Brandon RN (1996) The coevolution of organism and environment. In: Brandon RN (ed) Concepts and Methods in Evolutionary Biology, pp 161–178. Cambridge University Press, Cambridge, UK Bruno JF, Stachowicz JJ and Bertness MD (2003) Inclusion of facilitation into ecological theory Trends in Ecology and Evolution 18: 119–125 Burla H (1995a) Records of Chymomyza (Drosophilidae, Diptera) in Switzerland. Mitteilungen der Schweizerschen Entomologischen Gesellschaft 68: 159–168 Burla H (1995b) Natural breeding sites of Chymomyza species (Diptera, Drosophilidae) in Switzerland. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 68: 251–257 Burla H (1997) Natural breeding sites of Chymomyza species (Diptera, Drosophilidae) in Switzerland. Part II. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 70: 35–41 Burla H and Ba¨chli G (1991a) A search for pattern in faunistical records of drosophilid species in Switzerland. Zeitschrift fu¨r Zoologische Systematik und Evolutionsforschung 29: 176–200 Burla H and Ba¨chli G (1991b) Beitrag zur Kenntnis von Substraten, in denen sich Drosophiliden-Arten entwickeln. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 64: 45–53
529 Burla H and Ba¨chli G (1992) Chymomyza amoena (Diptera: Drosophilidae) reared from chestnuts, acorns and fruits collected in the Canton Ticino, Switzerland. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 65: 25– 32 Burla H and Ba¨chli G (1993) Aggregated breeding dispersion of Drosophila species reared from Cornelian cherries (Cornus mas) and plums (Prunus domestica). Mitteilungen der Schweizerischen Entomologichen Gesellschaft 66: 183– 196 Burla H, Ku¨nzli H and Pfaendler U (1987) Laboratory experiments on natural breeding substrates in Drosophila subobscura. Gene´tica Ibe´ria 39: 269–285 Burla H, Ba¨chli G and Huber H (1991) Drosophila reared from the stinkhorn, Phallus impudicus, near Zurich, Switzerland. Zeitschrift fu¨r Zoologische Systematik und Evolutionsforschung. 29: 97–107 Carson HL (1974) Three flies and three islands: parallel evolution in Drosophila. Proceedings of the National Academy of Science, Washington 71: 3517–3521 Clarke AR and Zalucki MP (2004) Monarch in Australia: on the winds of a storm? Biological Invasions 6: 123–127 Colwell RK (1992) Niche: a bifurcation in the conceptual lineage of the term. In: Keller EF and Lloyd EA (eds) Keywords in Evolutionary Biology, pp 241–248. Harvard University Press, Cambridge, MA Coyne JA, Boussy IA and Bryant S (1984) Is Drosophila pseudoobscura a garbage species? Pan-Pacific Entomologist 60: 16–19 D’Antonio CM and Kark S (2002) Impacts and extent of biotic invasions in terrestrial ecosystems. Trends in Ecology and Evolution 17: 202–204 Del Solar E and Palomino H (1966) Choice of oviposition in Drosophila melanogaster. American Naturalist 100: 127– 133 Dobzhansky T (1965) ‘‘Wild’’ and ‘‘domestic’’ species of Drosophila. In: Baker HG and Stebbins GL (eds) The Genetics of Colonizing Species, pp 533–551. Academic Press, London Dorsey CK and Carson HL (1956) Selective response of wild Drosophilidae to natural and artificial attrahents. Annals of the Entomological Society of America 49: 177–181 Dorsey CK, Tryon EH and Carvel KL (1962) Insect damage to acorns in West Virginia and control studies using granular systemic insecticides. Journal of Economic Entomology 55: 885–888 Ferrar P (1987) A guide to the breeding habits and immature stages of Diptera Cyclorrapha. Entomonograph 8: 1–907 Gilpin M (1990) Ecological prediction. Science 248: 88–89 Griesemer JR (1992) Niche: historical perspectives. In: Keller EF and Lloyd EA (eds) Keywords in Evolutionary Biology, pp 231–240. Harvard University Press, Cambridge, MA Herbold B and Moyle PB (1986) Introduced species and vacant niches. American Naturalist 128: 751–760 Heger T and Trepi L (2003) Predicting biological invasions. Biological Invasions 5: 313–321 Hewitt GM and Bultin RK (1997) Causes and consequences of population structure. In: Krebs JR and Davies NB (eds)
Behavioural Ecology, an Evolutionary Approach, 4th edn, pp 350–372. Blackwell, London Holway DA and Suarez AV (1999) Animal behavior: an essential component of invasion biology. Trends in Ecology and Evolution 14: 328–330 Kareiva P (1996) Developing a predictive ecology for nonindigenous species and ecological invasions. Ecology 77: 1651–1652 Kolar CS and Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends in Ecology and Evolution 16: 199–204 Lachaise D (1977) Niche separation of African Lissocephala within the Ficus drosophilid community. Oecologia 31: 201–214 Levine JM (2000) Species diversity and biological invasions: relating local process to community pattern. Science 288: 852–854 Lodge DM (1993) Biological invasions: lessons for ecology. Trends in Ecology and Evolution 8: 133–137 Lohrer AM, Whitlatch RB, Wada K and Fukui Y (2000) Home and away: comparison of resource utilization by a marine species in native and invaded habitats. Biological Invasions 2: 41–57 Ma´ca J and Ba¨chli G (1994) On the distribution of Chymomyza amoena (Loew), a species recently introduced into Europe. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 67: 183–188 Mack RN, Barrett SCH, DeFur PL, MacDonald WL, Madden LV, Marshall DS, McCullough DG, McEnvoy PB, Nyrop JP, Reichard SEH, Rice KJ and Tolin SA (2002) Predicting Invasions of Nonindigenous Plants and Plant Pests. National Academy Press, Washington, DC, 194 pp Mani E, Wildbolz T, Riggenbach W and Staub H (1997) Populationsschwankungen des Apfelwicklers Cydia pomonella (L.) in ungesto¨rten Apfelbesta¨nden der Ostschweiz. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 70: 117–132 Mattson WJ, Niemela¨ P, Millers I and Inguanzo Y (1994) Immigrant phytophagous insects on woody plants in the United States and Canada: an annotated list. General Technical Report NC-169. US Department of Agriculture, St Paul, MN Millar CD and Lambert DM (1985) The mating behavior of individuals of Drosophila pseudoobscura from New Zealand. Experientia 41: 950–952 Miller TE and Travis J (1996) The evolutionary role of indirect effects in communities. Ecology 77: 1329–1335 Mittempergher L (1978) The present status of chestnut blight in Italy. In: MacDonald WL, Cech FC, Luchok J and Smith C (eds) Proceedings of the American Chestnut Symposium, pp 34–37. West Virginia University, Morgantown, WV Niemala¨ P and Mattson WJ (1996) Invasion of North American forests by European phytophagous insects. BioScience 46: 741–753 Papp L and Pescenye K (1987) Drosophilidae/Diptera/of Hungary. Acta Biologica Debrecina 19: 55–90
530 Parsons PA (1983) The Evolutionary Biology of Colonizing Species. Cambridge Univeristy Press, Cambridge, UK, 262 pp Parsons PA and Hoffman AA (1986) Ecobehavioral genetics: habitat preferences in Drosophila. In: Karlin S and Nevo E (eds) Evolutionary Processes and Theory, pp 535–559. Academic Press, New York Parsons PA and Stanley S (1981) Domesticated and widespread species. In: Ashburner M, Carson HL and Thompson JN, Jr. (eds) Genetics and Biology of Drosophila, Vol. 3a, pp 349–393. Academic Press, London Patterson JT (ed) (1943) Studies in the Genetics of Drosophila. III. The Drosophilidae of the Southwest. University of Texas Publication 4313: 1–216 Powell JR (1997) Progress and Prospects in Evolutionary Biology: The Drosophila Model. Oxford University Press, New York, 562 pp Sabath MD (1974) Niche breadth and genetic variability in sympatric natural populations of drosophilid flies. American Naturalist 108: 533–540 Sabath MD (1975) Enzyme variability in 12 sympatric drosophilid species (genera: Chymomyza, Leucophenga, Scaptomyza and Drosophila). American Midland Naturalist 94: 144–153 Sabath MD and Jones JM (1973) Measurements of niche breadth and overlap: the Colwell–Futuyma method. Ecology 54: 1143–1147 Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN and Weller SG (2001) The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305–332 Schatzmann E (1977) Fru¨chte als natu¨rliche Entwicklungssubstrate von Drosophiliden. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 50: 135–148 Schoener TW (1989) The ecological niche. In: Cherrett JM (ed) Ecological Concepts, The Contributions of Ecology to an Understanding of the Natural World, pp 79–113. Blackwell Scientific, Oxford Schowalter TD (2000) Insect Ecology, An Ecosystem Approach. Academic Press, San Diego, CA, 483 pp Schumann H (1987) Chymomyza amoena (Loew, 1862)-eine fu¨r die Fauna der DDR neue amerikanische Drosophilidenart (Diptera). Entomologische Nachrichten und Berichte, Berlin 31: 125–128 Schwerdtfeger F (1973) Forest entomology. In: Smith RF, Mittler TE and Smith CN (eds) History of Entomology, pp 361–386. Annual Review of the Entomological Society of America, Lanham, MD Shea K and Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends in Ecology and Evolution 17: 170–176 Shorrocks B (1982) The breeding sites of temperate woodland Drosophila. In: Ashburner M, Carson HL and Thompson
JN, Jr. (eds) Genetics and Biology of Drosophila. 3b., pp 385–428. Academic Press, London Shorrocks B, Rosewell J, Edwards K and Atkinson W (1984) Interspecific competition is not a major organizing force in many insect communities. Nature 310: 310–312 Simberloff D (1985) Predicting ecological effects of novel entities: evidence from higher organisms. In: Halvorson HO, Pramer D and Rogul M (eds) Engineered Organisms in the Environment: Scientific Issues, pp 152–161. American Society for Microbiology, Washington, DC Simberloff D (1989) Which insect introductions succeed and which fail? In: Drake JA, Mooney HA, di Castri F, Grove RH, Kruger FJ, Rejma´nek M and Williamson M (eds) Biological Invasions: A Global Perspective, pp 61–75. Wiley, Chichester, UK Simberloff D (1991) Keystone species and community effects of biological introductions. In: Ginzburg LR (ed.) Assessing Ecological Risks of Biotechnology, pp 1–19. Butterworth–Heinemann, Boston, MA Simberloff D (1995) Why do introduced species appear to devastate islands more than mainland areas? Pacific Science 49: 87–97 Simberloff D and Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1: 21–32 Spieth HT (1957) Drosophila of the Itasca Park, Minnesota region. New York Entomological Society 65: 89– 96 Stachowicz JJ, Whitlatch RB and Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286: 1577–1579 Stiling PD (1996) Ecology: Theories and Applications, 2 edn. Prentice Hall, Upper Saddle River, NJ, 539 pp Stiling P (2002) Potential non-target effects of a biological control agent, prickly pear moth, Cactoblastis cactorum (Berg) (Lepidopera: Pyralidae) in North America, and possible management actions. Biological Invasions 4: 273– 281 Sturtevant AF (1921) The North American species of Drosophila. Carnegie Institution of Washington 103: 1–150 Throckmorton LH (1962) The problem of phylogeny in the genus Drosophila. University of Texas Publication 6205: 207–343 Vermeij GJ (1996) An agenda for invasion biology. Biological Conservation 78: 3–9 Wallace B (1978) The adaptation of Drosophila virilis to life on an artificial crab. American Naturalist 112: 971–973 Wheeler MR (1952) The Drosophilidae of the Nearctic region, exclusive of the genus Drosophila. University of Texas Publication 5204: 162–218 Williamson M (1996) Biological Invasions. Chapman and Hall, London, 244 pp Winston PW (1956) The acorn microsere, with special reference to arthropods. Ecology 37: 120–132