Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid

Biological Control 35 (2005) 55–67 www.elsevier.com/locate/ybcon

Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid T. Haye a, H. Goulet b, P.G. Mason b, U. Kuhlmann a,¤ a

b

CABI Bioscience Centre, Agricultural Pest Research, Rue des Grillons 1, CH-2800 Delémont, Switzerland Agriculture and Agri-Food Canada, Research Centre, K.W. Neatby Building, Ottawa, Ont., Canada K1A 0C6 Received 15 March 2005; accepted 21 June 2005 Available online 10 August 2005

Abstract Using the retrospective case study of Peristenus digoneutis (Hymenoptera: Braconidae) introduced in the United States for biological control of native Lygus plant bugs (Hemiptera: Miridae), laboratory and Weld studies were conducted in the area of origin to evaluate whether the fundamental host range of P. digoneutis matches its ecological host range. Furthermore, it was determined whether these approaches would have been indicative of the post-introduction host range of P. digoneutis in North America [Day, W.H., 1999. Host preference of introduced and native parasites (Hymenoptera: Braconidae) of phytophagous plant bugs (Hemiptera: Miridae) in alfalfa-grass Welds in the north-eastern USA, BioControl 44, 249–261.]. Seven non-target mirid species were selected to deWne the fundamental host range of P. digoneutis in the area of origin in Europe. Laboratory choice and no-choice tests demonstrated that all selected non-target species were attacked by P. digoneutis and were largely suitable for parasitoid development. To conWrm the validity of the fundamental host range, the ecological host range of P. digoneutis in the area of origin was investigated. Peristenus digoneutis was reared from 10 hosts, including three Lygus species and seven non-target hosts from the subfamily Mirinae. Despite the fact that laboratory tests demonstrated a high parasitism level in non-targets, ecological assessments in both North America (Day, 1999) and Europe suggest a much lower impact of P. digoneutis on non-target mirids, with low levels of parasitism (below 1% in Europe). Therefore, ecological host range studies in the area of origin provide useful supplementary data for interpreting pre-release laboratory host range testing.  2005 Elsevier Inc. All rights reserved. Keywords: Biological control; Fundamental host range; Ecological host range; Non-target eVects; Risk assessment; Lygus plant bugs; Parasitoids; Braconidae; Peristenus digoneutis

1. Introduction Within the last twenty years, concerns regarding the safety of arthropod biological control using invertebrates have increasingly been discussed (e.g., Howarth, 1983, 1991; SimberloV and Stiling, 1996; Follett et al., 2000; Lynch et al., 2001; Stiling, 2004). It has been stressed that classical biological control could have major environmental costs if introduced natural enemies colonize and disrupt

*

Corresponding author. Fax: +41 32 421 4871. E-mail address: [email protected] (U. Kuhlmann).

1049-9644/$ - see front matter  2005 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2005.06.008

native systems (Hawkins and Marino, 1997). The main areas of concern include the irreversibility of exotic introductions, the dispersal of non-indigenous natural enemies to new habitats, and the potential host range expansion of the agent to include native or beneWcial insects, thereby causing harm to such non-target hosts (non-target eVects), (e.g., Howarth, 1983, 1991; Secord and Kareiva, 1996; SimberloV and Stiling, 1996; Follett et al., 2000; Lockwood, 2000; Michaud, 2002; Kuris, 2003; Louda et al., 2003a; Stiling, 2004). However, despite the relatively large number of exotic natural enemies introduced for biological control of insects and mites (Greathead, 1995; Wratten and Gurr, 2000), negative environmental eVects from such releases

56

T. Haye et al. / Biological Control 35 (2005) 55–67

have rarely been reported (Onstad and McManus, 1996; van Lenteren et al., 2003). Many publications focusing on non-target eVects of exotic natural enemies consider target speciWcity as the key to safety in biological control (Nechols et al., 1992; Onstad and McManus, 1996; Secord and Kareiva, 1996; Strand and Obrycki, 1996; Sands, 1997; Keller, 1999; Knight, 2001; van Lenteren et al., 2003). Host speciWcity can be deWned as the degree to which a species restricts its diet (Nechols et al., 1992). In the context of a natural enemy, this can refer to the species host range, broadly deWned as the set of species that can support development of a parasitoid or serve as prey for a predator (Strand and Obrycki, 1996). In addition to collecting available information from the literature (De Nardo and Hopper, 2004; Sands and van Driesche, 2004), a Wrst essential step in host range assessment is to conduct laboratory tests to investigate whether non-target species are attacked under a variety of test conditions (van Driesche and Hoddle, 1997; van Lenteren et al., 2003). The set of species that can support development of a parasitoid or serve as prey for a predator—observed under laboratory conditions exclusively—is deWned as the fundamental (syn. physiological) host range of a potential agent (Onstad and McManus, 1996). In contrast, the ecological host range is deWned as the current and evolving set of host species actually used for successful reproduction in the Weld (Nechols et al., 1992; Onstad and McManus, 1996). Estimating a species’ host range is often linked with various practical problems, such as lack of knowledge on the ecology of non-targets hosts (host plants, habitats, behavior etc.), their phylogentic relatedness to the target host, suitable rearing protocols, availability of desired non-target hosts or large numbers of potential non-target species to be tested (van Driesche, 2004). Therefore, several diVerent approaches have been used in the past by biological control practitioners to assess host speciWcity of biological control agents. These approaches primarily included reviews of scientiWc literature (De Nardo and Hopper, 2004), laboratory tests (e.g., Sands and Coombs, 1999; Porter, 1979; Babendreier et al., 2003) or Weld surveys in the area of origin (Fuester et al., 2001; Haye and Kenis, 2004). However, each approach has inherent strengths and weaknesses (De Nardo and Hopper, 2004; van Driesche and Reardon, 2004). In particular, many studies have shown that the fundamental host range of a biological control agent is often greater than its ecological host range (Cameron and Walker, 1997; Morehead and Feener, 2000; Froud and Stevens, 2003); this is likely due to diYculty in accurately reproducing the factors that inXuence host searching and assessment behaviour of a parasitoid in its natural environment (Nechols et al., 1992; Sands, 1993). Furthermore, it has been stated that laboratory observations should be combined with Weld observations to provide a

basis for correctly interpreting fundamental host range estimations (Onstad and McManus, 1996; Hopper, 2001; Kuhlmann and Mason, 2003). Here, we present a retrospective case study on Peristenus digoneutis (Hymenoptera: Braconidae), a European parasitoid of Lygus spp. that was introduced in the early 1980s in the United States for biological control of the native plant bug Lygus lineolaris (Palisot de Beauvois) (Day et al., 1990, 2003). Laboratory and Weld studies were conducted in the area of origin of the parasitoid to evaluate whether the fundamental host range matches the ecological host range of P. digoneutis in Europe, and determine whether these approaches would have been indicative for the post-introduction host range of P. digoneutis in North America, as reported by Day (1999).

2. Material and methods 2.1. Fundamental host range 2.1.1. Selection of non-target hosts In accordance with Kuhlmann and Mason (2003), the selection of non-target hosts for laboratory testing was based on phylogenetic criteria, availability, spatial and temporal overlap of potential non-target hosts and Lygus hosts in their natural habitats in the area of investigation (Schleswig-Holstein, northern Germany). According to the maximum Wt cladogram of Lygus and its outgroup taxa (Schwartz and Foottit, 1998), two Mirini species, Lygocoris pabulinus (L.) and Liocoris tripustulatus (Fabricius), were chosen as test candidates following a centrifugal phylogenetic approach (Wapshere, 1974). Another candidate chosen from the tribe Mirini (to which Lygus belongs) was the potato bug, Closterotomus norwegicus (Gmelin), which is the most abundant mirid found in spring in northern Germany (Afscharpour, 1960) and occurs at the same time and habitat as Lygus species. To include less closely related mirid species into the testing procedure, four grass bugs from the tribe Stenodemini were selected, including Leptopterna dolobrata L., Stenodema calcarata (Fallén), Notostira elongata (GeoVroy), and Megaloceraea recticornis (GeoVroy). In the present study, L. rugulipennis Poppius represented the target host instead of the congeneric North American Lygus species. To investigate if variations in acceptance and parasitoid development occur when diVerent Lygus target hosts are oVered, Lygus maritimus Wagner, which in contrast to the former species occurs primarily in coastal habitats, was included in the testing procedures. 2.1.2. Source and rearing of parasitoids, Lygus hosts, and potential non-target hosts Peristenus adults were reared from parasitized nymphs of the Wrst and second generation of

T. Haye et al. / Biological Control 35 (2005) 55–67

L. rugulipennis collected in clover and camomile habitats in northern Germany. Parasitoids were kept in a subterranean insectary at temperatures of 15–18 °C and provided with honey and water. Before each test, parasitoids were allowed to adapt to the laboratory temperature (25 °C) for at least 1 h. Nymphs of L. rugulipennis, L. maritimus, and L. tripustulatus were reared from overwintered adults, and nymphs of L. pabulinus were reared from newly emerged adults from the spring generation; for all species above, the adults were collected in their natural habitats and brought to the laboratory for egg laying. Adults were kept at 20 °C and 16 h photoperiod and provided with lettuce and sprouting potatoes as oviposition substrates. Nymphs were produced following a combination of rearing methods described for L. lineolaris by Stevenson and Roberts (1973) and Snodgrass and McWilliams (1992). To establish a culture of S. calcarata, grass ears in which adults had previously oviposited before were collected in the Weld to obtain freshly emerged nymphs. To obtain nymphs of univoltine non-target mirids that overwinter in the egg stage, such as C. norwegicus, L. dolobrata, and M. recticornis, Wrst and second instar nymphs were Weld-collected in early spring. Small instar nymphs of N. elongata were collected in early July when the second nymphal generation started to emerge. In the very early period of nymphal emergence, the risk that nymphs have already been parasitized in the Weld is generally low. However, as an additional control, subsamples of small non-target nymphs were always reared and dissected for parasitism. Nymphs of Lygus, Closterotomus, Lygocoris, and Liocoris that were attacked during exposure to P. digoneutis females in laboratory tests were reared individually in small plastic vials to investigate whether observed oviposition by female parasitoids was successful and whether hosts were suitable for parasitoid development. Although nymphs of most of the species tested were provided with Romaine lettuce and potato sprouts as a food source, grass bug nymphs were placed on grass ears or leaves instead. A thin layer of moistened vermiculite covered the bottom of the vials to oVer emerging parasitoid larvae a pupation site. 2.1.3. Small arena no-choice test The aim of the test was to determine whether P. digoneutis accepts non-target nymphs consistently and whether non-target nymphs are suitable hosts for parasitoid development. Three day old, mated, naïve females were Wrst exposed to a single second or third instar nymph of the target L. rugulipennis. As P. digoneutis has no pre-oviposition period (Haye, 2004), females that did not react to Lygus nymphs were presumably unWt for use and thus, were excluded from the testing procedure. In the subsequent no-choice tests, females that were presumed ready for oviposition were individually placed into a clear plastic vial of 30 £ 55 mm each containing a

57

small instar nymph of a non-target host (Fig. 1). Each parasitoid was given a maximum time period of 20 min to Wnd and parasitize the nymph. The same procedure was repeated 24 h later, but oVering a L. rugulipennis nymph in order to exclude false-negatives in case females had not reacted to the non-target host (control, Fig. 1). When the parasitoid was observed to insert the ovipositor into the nymph, the host was recorded as attacked (“Attacks on hosts”, Fig. 1). A host was further counted as accepted when either a parasitoid larva was found in the dissection or a parasitoid cocoon was found in the rearing vial (“Host acceptance”, Fig. 1). Encapsulated eggs or larvae were never observed in dissections of attacked mirid hosts and have never been reported in the literature and thus, they did not inXuence the measure of host acceptance. A mirid host was classiWed as suitable when parasitoid larvae successfully completed their development and formed a cocoon outside their hosts (“Host suitability”, Fig. 1). 2.1.4. Small arena behavioral choice test To investigate whether the behavioral threshold for attacks on non-target hosts can be changed in the presence of the target host (“Host preference”, Fig. 1), choice tests were conducted in which parasitoids were oVered Lygus nymphs and non-target nymphs simultaneously (Fig. 1). For these tests, six to eight day old experienced female parasitoids (n D 20/non-target species) were used. Parasitoid experience was acquired in the no-choice tests (as outlined in Fig. 1). Individual female wasps were oVered three second or third instar Lygus nymphs and three second or third instar non-target nymphs at the same time in a Petri dish (diameter 5 cm). Following observed attack, potentially parasitized nymphs were immediately removed with a mouth aspirator and replaced by new, non-parasitized ones to maintain a constant number of each mirid species at all times. Tests lasted for 5 min, and the number of attacks on each mirid species was recorded. 2.1.5. Statistical analysis The
-square test after McNemar was used to analyze the data sets obtained from each mirid species tested in small arena no-choice tests. For comparing the levels of host acceptance, only data obtained from parasitoids which had attacked Lygus and non-target nymphs in the no-choice tests were used. Consequently, the number of replicates was automatically reduced. Some of the attacked nymphs died and dried out during the rearing process and thus, could not be dissected for parasitism. In these cases the complete test series was excluded from the analysis (Fig. 1) and consequently, the number of replicates was further reduced. Data sets of small arena behavioral choice test were analyzed using the Wilcoxon pairedsample test. All statistical analyses were carried out with the SPSS 10.0 software package (SPSS Inc., 1999).

58

T. Haye et al. / Biological Control 35 (2005) 55–67

Fig. 1. General procedure for assessing the fundamental host range of P. digoneutis.

2.2. Ecological host range 2.2.1. Selection of non-target hosts According to Wagner (1952), approximately 2000 species belonging to the family Miridae occur in the Palaearctic region (307 in Germany) and thus, the number of potential non-target hosts of P. digoneutis is immense. The aim of collections in various habitats in northern Germany (e.g., stinging nettle stands, fallow Welds, and grasslands) was to obtain samples from a broad range of common and rare mirid species considered as potential non-target hosts of P. digoneutis. In order to investigate whether these parasitoids are actually speciWc to the subfamily Mirinae, collections were also focused on other mirid subfamilies, such as Bryocorinae, Orthotylinae, and Phylinae. 2.2.2. Source and rearing of potential non-target hosts Potential non-target mirid nymphs were collected from various host plants (Table 1) in natural or agricultural habitats using a standard sweep net. As parasitoid larvae are known to emerge from late nymphal instars or rarely from teneral adults (Loan, 1980), mirid nymphs

were collected exclusively in the fourth or Wfth instar. From each collection, subsamples of 20–50 nymphs were taken randomly and dissected to assess percent parasitism. However, mirid species that were found in low numbers were exclusively used for rearing out parasitoids, as dissection provides no information pertaining to parasitoid species. The rearing system for samples up to 50 nymphs consisted of 1.2 L plastic containers Wtted with removable Petri dishes on the bottom. The Petri dishes were Wlled with moist vermiculite and separated from the rest of the container by a round piece of gauze (width 1.20 £ 1.38 mm) which allowed larval parasitoids gain access to the Petri dish for pupation (Drea et al., 1973). Larger samples of a maximum of 500 nymphs were kept in plastic buckets with the bottoms removed and replaced with gauze. Plastic funnels terminating in vermiculite-Wlled Petri dishes were attached to the bottom of the buckets in order to collect emerging parasitoid larvae that fall through the gauze. Mirids belonging to the genus’ Lygus, Adelphocoris, Closterotomus, and Calocoris were fed with organically grown beans and lettuce. For all other mirid species the host plants they were

Table 1 Ecological host range of P. digoneutis: Mirid species, host plants, and details regarding collection and rearing of mirid nymphs collected in Schleswig–Holstein, northern Germany to assess presence and parasitism by P. digoneutis in target and non-target mirids No. of No. of No. of nymphs taken mirid adults cocoons into rearing reared received

No. of No. of sites No. of sites parasitoids sampled with P. digoneutis emerged present

Parasitoid species composition (%)

Overall % Parasitism % Parasitism parasitism by P. digoneutis by P. digoneutis (%) in the Weld in the laboratory

Host Plantsa

Bryocorinae Dicyphus globulifer (Fallén)

Sv

274

100

69

38

1

0

0

100

0

35.5

0

—

Ml

568

336

59

35

11

0

0

97

3

14.9

0

—

1114

466

155

86

13

1

2

72

26

25

0.3

—

U

186

120

25

21

8

1

5

91

4

17.2

0.8

—

A

14

6

2

2

2

0

0

100

0

25.0

0

—

15,149

7639

1828

1357

29

9

4

89

7

19.3

0.7

100

U

4217

1197

839

409

31

4

1

79

20

41.2

0.6

73

U

1955

1127

141

74

27

2

3

54

43

11.1

0.3

21

Mr

1243

877

80

62

6

2

10

86

4

8.4

0.6

96

488 39,851

363 22,154

67 7296

65 5556

13 20

8 19

34 58

52 37

14 5

15.6 24.8

5.3 14.4

— 91

A Q

97 23

64 11

4 8

1 8

4 2

0 0

0 0

100 100

0 0

5.9 42.1

0 0

— —

G

911

351

252

200

9

0

0

85

15

41.8

0

—

G

3285

1218

529

375

23

0

0

70

30

30.3

0

G

37

25

6

4

1

0

0

100

0

19.4

0

G

2450

1772

75

43

14

0

0

91

9

4.1

0

11

G

7872

4014

757

603

23

0

0

82

18

15.9

0

83

G

1970

1038

458

269

25

1

<1

69

30

30.6

0.1

42

Mirinae: Mirini Adelphocoris lineolatus (Goeze) Apolygus lucorum (Meyer-Dür) Calocoris aYnis (Herrich-SchaeVer) Calocoris roseomaculatus (De Geer) Closterotomus norwegicus (Gmelin) Liocoris tripustulatus (Fabricius) Lygocoris pabulinus (L.) Lygus maritimus Wagner Lygus pratensis (L.) Lygus rugulipennis Poppius Orthops kalmii (L.) Rhabdomiris striatellus (Fabricius) Stenotus binotatus (Fabricius) Mirinae: Stenodemini Leptopterna dolobrata (L.) Leptopterna ferrugata (Fallén) Megaloceraea recticornis (GeoVroy) Notostira elongata (GeoVroy) Stenodema calcarata (Fallén)

U, Av

Tp, Mr, G, Pt, U

Mr, Tp Mr, Tp

Peristenus Peristenus Mesochorus spp.c digoneutis spp.b

T. Haye et al. / Biological Control 35 (2005) 55–67

Mirid host species

62 —

59

(continued on next page)

60

Table 1 (continued) Mirid host species

Orthotylinae Orthotylus moncreaY (Douglas and Scott) Orthotylus marginalis Reuter Phylinae Europiella artemisiae (Becker) Lopus decolor (Fallén) Plagiognathus chrysanthemi (WolV) Plagiognathus arbustorum (Fabricius) Amblytylus nasutus (Kirschbaum)

G

486

318

93

80

3

1

<1

93

6

22.6

0.3

—

G

371

224

33

19

13

0

0

100

0

12.8

0

—

G

102

61

7

3

5

0

0

33

67

10.3

0

—

G

341

189

68

48

9

0

0

94

6

26.5

0

—

Al

24

20

1

1

1

0

0

0

0

4.8

0

—

U

25

13

6

5

1

0

0

100

0

31.6

0

—

Av

54

5

18

12

1

0

0

58

42

78.3

0

—

U Cv

137 195

25 104

3 64

1 25

1 3

0 0

0 0

0 96

0 4

10.7 38.1

0 0

— —

U

3141

1076

601

375

22

0

0

81

19

35.8

0

—

G

1225

820

46

38

8

0

0

97

3

5.3

0

—

a A, Apiaceae; Al, Atriplex lacinata L.; Av, Artemisia vulgaris L.; Cv, Chrysanthemum vulgare (L.); G, Gramineae; Ml, Medicago lupulina L.; Mr, Matricaria recutita (L.); Pt, Phacelia tanacetifolia Bentham; Q, Quercus spp.; Sv, Silene vulgare (Moench) Garcke; Tp, Trifolium pratense L.; U, Urtica spp. b All Peristenus species, except P. digoneutis. c Hyperparasitoids.

T. Haye et al. / Biological Control 35 (2005) 55–67

Stenodema holsata (Fabricius) Stenodema laevigata (L.) Stenodema trispinosa Reuter Trigonotylus caelestialium (Kirkaldy)

Host No. of No. of No. of No. of No. of sites No. of sites Parasitoid species composition (%) Overall % Parasitism % Parasitism Plantsa nymphs taken mirid adults cocoons parasitoids sampled with P. digoneutis parasitism by P. digoneutis by P. digoneutis in Peristenus Peristenus Mesochorus into rearing reared received emerged present (%) in the Weld the laboratory spp.c digoneutis spp.b

T. Haye et al. / Biological Control 35 (2005) 55–67

61

collected from were added to the rearing cages, because these species would not accept any other diet. After all nymphs had reached the adult stage or parasitoid larvae had emerged, Petri dishes containing parasitoid cocoons were removed and stored in an outdoor wooden shelter until parasitoid adult emergence. 2.2.3. Estimating the ecological host range of P. digoneutis and its impact on mirid hosts Overall parasitism (%) was estimated by dividing the number of parasitoid cocoons by the sum of the parasitoid cocoons and reared mirid adults, multiplied by 100. For each mirid species, the proportion of each parasitoid species (P. digoneutis, Peristenus spp., and Mesochorus spp.) relative to the total number of emerged parasitoids was calculated.The proportion of P. digoneutis was then expressed as percent parasitism caused by this species (e.g., if overall parasitism of a given mirid species was 60% and the proportion of P. digoneutis in the nymphal parasitoid community was 20%, then the percent parasitism for P. digoneutis was 12%). When hyperparasitoids emerged from the cocoons (primarily Mesochorus curvulus Thomson, K. Zwakhals, pers. commun. 2004), the actual proportion of primary parasitoid could not be estimated precisely due to the fact that during the rearing process, the hyperparasitoid consumes the primary parasitoid. This makes it impossible to determine which species of primary parasitoid had initially attacked the mirid host. Thus, it cannot be excluded that the actual proportion of P. digoneutis in these non-target hosts was higher than estimated by rearing. However, Day (2002) showed that P. digoneutis is not a preferred host of M. curvulus and thus, it is very unlikely that the proportion of P. digoneutis in non-target hosts was strongly inXuenced by the hyperparasitoids.

3. Results 3.1. Fundamental host range 3.1.1. Small arena no-choice test Peristenus digoneutis females only attacked the alternative target L. maritimus and the non-target L. pabulinus with nearly the same frequency as L. rugulipennis (>90%) (Fig. 2A). All other test mirids were signiWcantly less attacked (P < 0.001), particularly the Stenodemini, (minimum of 29% observed for M. recticornis and maximum of 54% observed for L. dolobrata). Although attacks on in L. pabulinus were frequently observed, in comparison to the Lygus control a large proportion of the test nymphs survived and reached the adult stage (P < 0.001; Fig. 2B). When these adults were dissected, no evidence of encapsulated parasitoid eggs or larvae were found. Although the potato bug C. norwegicus, the nettle bug L. tripustulatus, and the grass bugs

Fig. 2. Percentage of P. digoneutis females (A) attacking and (B) accepting two Lygus and seven non-target hosts in small arena nochoice tests. The number of tested females is given in brackets for each mirid species. Bars marked with asterisks indicate a signiWcant diVerence between groups, (
-square test after McNemar; *P < 0.05; **P < 0.01; ***P < 0.001; 1Lygus target nymphs were oVered in both experimental runs).

L. dolobrata and N. elongata were attacked less frequently than Lygus nymphs, acceptance of these nontarget hosts and Lygus hosts did not diVer signiWcantly (Fig. 2B). Only S. calcarata (P D 0.016) and M. recticornis (P D 0.008) were signiWcantly less accepted (<40%). In terms of host suitability for parasitoid development, all non-target hosts were suitable, with the exception of M. recticornis (Fig. 3). In the case of M. recticornis, only one out of 10 attacked nymphs was actually found to be parasitized. This nymph, however, died before the parasitoid larva had left its host. As data on in-host development were limited due to the poor acceptance of some of the non-target hosts, statistical analysis of diVerences between groups were not performed. 3.1.2. Small arena behavioral choice test Within the duration of the test, P. digoneutis attacked on average three nymphs (range: 1–7; n D 140). Correspondingly, all non-target host species attacked by P. digoneutis in no-choice tests, were also attacked when oVered simultaneously with Lygus nymphs in choice tests (Fig. 4). In nearly all trials P. digoneutis showed a signiWcant preference for Lygus target nymphs when oVered simultaneously with non-target hosts; only the

62

T. Haye et al. / Biological Control 35 (2005) 55–67

Fig. 3. Host suitability: percentage of P. digoneutis larvae that completed larval development and formed a cocoon outside their host and percentage of larvae that failed to complete development due to host mortality (compare Fig. 1). The number of accepted nymphs is given in brackets for each mirid species ( D 100%).

closely related non-target host L. pabulinus was attacked with the same frequency as the target. 3.2. Ecological host range 3.2.1. Estimating the ecological host range of P. digoneutis and its impact on mirid hosts In northern Germany, P. digoneutis was reared from 10 hosts in the subfamily Mirinae (including three Lygus species and seven non-target hosts). No specimens were obtained from the subfamilies Bryocorinae, Orthotylinae, and Phylinae (Table 1); however, the number of species collected were limited and thus, it cannot be excluded that other species from these subfamilies may be accepted P. digoneutis. Among the three Lygus hosts, P. digoneutis was most frequently recorded from L. rugulipennis (58% of all larval parasitoids obtained

from this host). Accordingly, L. rugulipennis showed the highest overall parasitism by P. digoneutis (14.4%). In stinging nettle habitats the Mirini L. tripustulatus, L. pabulinus, Calocoris aYnis, and Apolygus lucorum were sporadically found to be suitable hosts for P. digoneutis. Among non-target hosts, P. digoneutis was reared most regularly from C. norwegicus, occurring at 31% of all sites where C. norwegicus was sampled (n D 29). Furthermore, single specimens were obtained from the Stenodemini S. calcarata and S. holsata. Although reared from a total of seven non-target mirids, the proportion of P. digoneutis in the larval parasitoid guild of suitable non-target hosts was always less than 5% (Table 1), and overall parasitism in non-target hosts by P. digoneutis alone did not exceed 1%.

4. Discussion Prior to releasing a natural enemy, an essential Wrst step is to conduct laboratory tests to measure whether non-target species are attacked under a variety of test conditions (van Driesche and Hoddle, 1997; van Lenteren et al., 2003). The aim of laboratory tests on host speciWcity is to predict the potential ecological host range of the control agent in the area of release (Barratt et al., 1997). However, laboratory assessment of the host range of a biological control agent in the laboratory often yields a signiWcantly broader fundamental host range in comparison to the ecological host range (Cameron and Walker, 1997; Morehead and Feener, 2000; Froud and Stevens, 2003). As an alternative, Weld tests may help eliminate some of the eVects of the laboratory environment (van Lenteren et al., 2003); however, quarantine considerations prevent these tests from being performed in the area of introduction (van Driesche and Murray, 2004). Consequently, conducting pre-release laboratory tests in the area of intended release is an

Fig. 4. Mean percentage of attacks/5 min on Lygus and non-target nymphs when oVered to P. digoneutis in small arena behavioral choice tests. For each non-target species 20 females were tested. Bars marked with asterisks indicate a signiWcant diVerence between attacks on non-target and Lygus hosts (Wilcoxon paired-sample test; *P < 0.05; **P < 0.01; ***P < 0.001).

T. Haye et al. / Biological Control 35 (2005) 55–67

obvious approach to study the potential impact on nontargets occurring in the area of introduction. However, as the comparison of laboratory and Weld data from the area of release is not possible prior to introduction, in the present study laboratory host range tests were performed on seven potential non-target hosts and compared to the ecological host range of P. digoneutis in its area of origin. The aim of this comparison is to analyze whether laboratory tests would be a reliable predictor of the ecological host range of P. digoneutis in the area of origin, and consequently in the area of release. Both approaches for host range assessment as well as the information from the literature on host range of P. digoneutis in Europe were then used to discuss whether retrospectively these approaches would have been indicative for the post-introduction host range in North America published by Day (1999). Although P. digoneutis has been assumed to be monophagus (Bilewicz-Pawinska, 1982), all seven nontarget hosts oVered in no-choice tests were accepted by P. digoneutis and moreover, six were also suitable for parasitoid development. However, it must be noted that P. digoneutis attacked non-target nymphs signiWcantly less frequently than Lygus nymphs. These trends were conWrmed by the results of the choice tests, which showed that P. digoneutis in most cases had a stronger preference for Lygus hosts. Although the lower response to non-target hosts may result from prior experience of females with the target (Withers and Browne, 2004; van Driesche and Murray, 2004), reduced responsiveness to an unfamiliar host has only been described for Aphidius rosae Haliday (Kitt and Keller, 1998). In that study, naïve females of A. rosae attacked non-target hosts in no-choice tests, whereas females that had previous experience with the target did not attack the non-target hosts. Although the response to non-target host may have been reduced in the present study, it did not prevent P. digoneutis from attacking them regularly. In no-choice and choice tests, L. pabulinus was the only non-target host that was attacked by P. digoneutis with the same frequency as Lygus hosts. Therefore, this study does not conWrm the general expectation that a wider host range will be expressed in no-choice tests than in choice tests (Withers and Browne, 2004; van Driesche and Murray, 2004), but it is in agreement with similar studies in which results from no-choice tests corresponded with results from choice tests (Duan and Messing, 2000; Zilahi-Balogh et al., 2002). However, despite frequent attacks on L. pabulinus in no-choice and choice tests, the host was rarely accepted, even though the oviposition behaviour when attacking L. pabulinus did not diVer signiWcantly. This indicates that L. pabulinus nymphs are less attractive for oviposition than Lygus nymphs. The low rate of acceptance was unexpected, because according to the maximum Wt cladogram of Lygus and its outgroup taxa (Schwartz and Foottit, 1998) L. pabulinus is considered

63

closely related to Lygus. Moreover, Stenodemini hosts that were considered less closely related to Lygus were more often accepted than L. pabulinus. These Wndings correspond with other studies which demonstrated that phylogenetic relatedness may not necessarily be a reliable indicator of host suitability (Barratt and Johnstone, 2001; Babendreier et al., 2003). However, this contradiction challenges the centrifugal phylogenetic approach for host selection (Hoddle, 2004) and a broader range of test species may be required. In general, the ecological host range of P. digoneutis in Europe is likely restricted to the subfamily Mirinae. Furthermore, within the subfamily Mirinae hosts belonging to the tribe Mirini seem to be preferred. Prior to the present study, ecological host range studies of Peristenus species in Europe were primarily restricted to cereal crops and cultivated alfalfa and thus, P. digoneutis was only known to parasitize L. rugulipennis (Loan and Bilewicz-Pawinska, 1973; Bilewicz-Pawinska, 1982) and Adelphocoris lineolatus (Goeze) (Carl and Mason, 1996). The seven non-target hosts and the two additional Lygus hosts (L. pratensis (L.) and L. maritimus) examined in the present study were previously not known to be parasitized by P. digoneutis. Therefore, the present study shows that using a careful literature review to predict the post-introduction host range of a biological control agent (De Nardo and Hopper, 2004) may induce false conclusions if host speciWcity is investigated solely in agricultural ecosystems instead of including natural habitats (Strand and Obrycki, 1996). It has further been stated that conclusions concerning host speciWcity can rarely be based solely on Weld data from the area of origin (van Lenteren et al., 2003). This is because some species that were assumed to be monophagous in the area of origin were later found to attack more than one host in the area of release (Barratt et al., 1997). Partly, this contradiction may result from ecological host range studies that were limited to a relatively small area within the distribution of the control agent. For example, in this study A. lineolatus was not recorded as host of P. digoneutis in northern Germany, where it is scarce, strictly univoltine (Wagner, 1952) and nymphs primarily occur in July when Lygus nymphs are generally not present in the Weld (Haye, 2004). On the other hand, in regions such as the southern German Rhine Valley and Switzerland where A. lineolatus is common, at least partly bivoltine, and Adelphocoris and Lygus nymphs occur simultaneously in lucerne Welds, it has been recorded as host of P. digoneutis (Carl and Mason, 1996). Therefore, the chance of underestimating the ecological host range of a biological control agent can be decreased when studies on the ecological host range are expanded to sympatric populations from diVerent regions within the area of distribution of the biological control agent. Based on the acceptance and suitability of non-target mirids in the laboratory, it was expected that P. digoneutis

64

T. Haye et al. / Biological Control 35 (2005) 55–67

would be found regularly in Weld-collected samples of the mirid species which were used in laboratory tests. However, P. digoneutis was only sporadically reared from non-target hosts, and the fundamental host range of P. digoneutis did not completely match its ecological host range. Leptopterna dolobrata and N. elongata (Mirinae: Stenodemini) were regularly accepted and suitable for parasitoid development in laboratory tests, but were not recorded as suitable hosts in the Weld. The laboratory choice and no-choice tests indicated that P. digoneutis would attack Stenodemini less often than Lygus nymphs, but they did not suggest the total absence in the larval parasitoid guild of these two Stenodemini. Thus, the present study agrees with the Wnding that fundamental host range is often greater than ecological host range, as has also been pointed out by others (Cameron and Walker, 1997; Morehead and Feener, 2000; Hopper, 2001; Froud and Stevens, 2003). Furthermore, parasitism of non-targets in the laboratory was generally high (up to 100% for C. norwegicus), whereas in the Weld overall parasitism by P. digoneutis was always less than 1% (Table 1). This remarkable diVerence between laboratory and Weld data supports the concern that laboratory tests can only identify potential non-target hosts (“Host suitability”), but they cannot reliably predict host searching and assessment behavior of a parasitoid in a natural environment (Benson et al., 2003; Louda et al., 2003b) and, thus the actual impact on non-target host populations. To date no severe non-target eVects have been reported after the release of P. digoneutis in the early 1980s to control Lygus lineolaris in the eastern United States (Day, 1996, 1999, 2005). Day (1999) investigated the post-introduction host range of P. digoneutis and the parasitoid complexes of seven mirid species occurring in alfalfa-grass Welds, including two native, one Holarctic, and four introduced mirid species (Table 2). The absence of P. digoneutis

in the larval parasitoid community of Stenotus binotatus (Fallén) and M. recticornis and the presence of P. digoneutis in Lygus, L. dolobrata, and A. lineolatus in the United States correspond with the ecological host range of P. digoneutis in Europe. However, in the United States P. digoneutis also developed sporadically from the Holarctic Trigonotylus caelestialium (Kirkaldy), which has never been reported as host of P. digoneutis in Europe, although the larval parasitoid community of this species has been investigated in northern Germany (present study), southern Germany and Switzerland (White, 2002), and Poland (Bilewicz-Pawinska, 1982). However, the development of P. digoneutis from T. caelestialium in the area of introduction demonstrates that a biological control agent may behave diVerently when released into a new environment. When only relying on the small cage laboratory experiments of the present study to assess the maximum host range possible (Withers and Browne, 2004), retrospectively, P. digoneutis may have been classiWed as potentially risky, when in fact laboratory tests may have had a poor predictive value in this instance. Moreover, according to Stiling (2004), P. digoneutis has to be categorized as generalist as it has been recorded from a total of 10 genera, including Weld host records from Europe and North America. However, these conclusions remain in contrast to post-release host speciWcity studies by Day (1999). In North America, P. digoneutis showed a similar low level of non-target parasitism (Day, 1999); it primarily attacked Lygus, and sporadically three additional mirid species (Table 2), but the parasitism of non-targets (Table 2) was always low and thus the impact on these species was as insigniWcant as in Europe. Thus, a broad host range may suggest that non-target eVects are more likely (Stiling, 2004), but the example of P. digoneutis shows that even with proof of 13 hosts (including 10 from the present study), it does not necessarily predict severe non-target eVects.

Table 2 Post-introduction host range of P. digoneutis in the United States (Day, 1999) and host records from Europe Mirid species

Lygus spp. Adelphocoris lineolatus (Goeze)a Leptopterna dolobrata (L.)a Trigonotylus caelestialium (Kirkaldy)b Stenotus binotatus (Fallén)a Megaloceraea recticornis (GeoVroy)a Halticus bractatus (Say)c

% Parasitism by P. digoneutis in North America United States (Day, 1999)

Europe Northern Germany (present study)

Southern Germany/ Switzerland (White, 2002)

Poland (Bilewicz-Pawinska, 1982)

X (31.2) X (6.4) X (0.2) X (0.3) — — —

X (14.4) — — — — —

X X Xd — ? ?

X — — — ? ?

Data in brackets represent the overall parasitism by P. digoneutis; for White (2002) and Bilewicz-Pawinska (1982) no data were available. X, present; —, absent; and ?, unknown. a Introduced to North America. b Holoartic. c Native to North America. d Peristenus n.sp. nr. P. digoneutis in White (2002) has later been determined as P. digoneutis (H. Goulet, pers. commun. 2005).

T. Haye et al. / Biological Control 35 (2005) 55–67

As shown in the case of P. digoneutis, ecological host range studies in the area of origin provide a useful supplement to interpret laboratory host range testing to predict the behavior of a biological control agent after introduction. Thus, a complete host range evaluation should combine data from the literature, Weld collections, and laboratory experiments (De Nardo and Hopper, 2004). Combining the three diVerent approaches may also help to prevent false-negatives when selecting promising biological control agents in terms of host speciWcity in the future.

Acknowledgments The authors gratefully acknowledge the support of Dr. Birte von Patay, Dr. Eva-Maria Meyer, Antje Petersen, Christine Gueldenzoph, Kristin Moreth, and Marc Schierding (all University of Kiel, Germany) with the Weld and laboratory work. We also thank Tara Gariepy, University of Saskatchewan, Canada, for reviewing the English text and helping with the experiments. We thank Prof. Oliver Betz, University of Tuebingen, Germany, for statistical support. Thanks to Jay Whistlecraft, AAFC, London, Canada, for valuable comments on rearing parasitoids and mirids, and to Dr. Dave Gillespie, AAFC, Agassiz, Canada, Dr. Bruce Broadbent, AAFC, London, Canada, and Prof. Hans Jürgen Braune, University of Kiel, Germany for their support. We gratefully appreciated the identiWcation of mirids by Dr. Albert Melber, University of Hanover, Germany and Dr. Mike Schwartz, AAFC, Ottawa, Canada. We also thank Kees van Zwakhals, Arkel, Netherlands, and Dr. Reijo Jussila, University of Turku, Finland, for the identiWcation of hyperparasitoids. Agriculture and AgriFood Canada contributed substantial funding for this research through CABI Bioscience, Switzerland, as did the University of Kiel, Germany.

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