Feeding and oviposition tests refute host–herbivore relationship between Fragaria spp. and Abia sericea, a candidate for biological control of Dipsacus spp.
B.G. Rector,1 V. Harizanova2 and A. Stoeva2
Summary Two species of teasels, Dipsacus fullonum L. and Dipsacus laciniatus L. (Dipsacales: Dipsacaceae), have become invasive in the USA and are targets of a classical biological control programme. The sawfly, Abia sericea (L.) (Hymenoptera: Cimbicidae), was identified as a teasel biological control candidate, but reports in the literature raised concerns about the possibility of non-target effects on members of the genus Fragaria L. Oviposition tests and multiple- and no-choice feeding tests were conducted on A. sericea to test the suitability of three Fragaria spp. (Fragaria ´ ananassa Duchesne, Fragaria vesca L. and Fragaria viridis Duchesne) as host plants. In oviposition tests, males were paired with females in cages containing a D. laciniatus plant and plants of the three Fragaria spp. In 16 replicates, all eggs were laid in D. laciniatus leaves, except in one replication in which two eggs were laid in a leaf of F. viridis (vs >100 eggs in D. laciniatus leaves by the same female and >1000 eggs by all females). From these two eggs, one larva hatched, which fed only on D. laciniatus in a choice test and died before pupating. In no-choice feeding tests on the three Fragaria spp., larvae of first, second, third and fourth instars were infested in separate tests, and no feeding, tasting or damage was observed on any Fragaria spp. in any replicate; all larvae died. In multiple-choice feeding tests, first, second, third and fourth instar larvae were reared to pupation. Larvae of all instars fed exclusively on D. laciniatus, while no feeding attempts, tastes or feeding damage was observed on any Fragaria spp. plant. Entomology and agricultural literature were thoroughly reviewed, and the connection between Fragaria and A. sericea was traced to two brief anecdotal mentions that were widely repeated but never supported by collection or bioassay data. The tests and other evidence presented in this paper refute the idea that Fragaria spp. are suitable hosts for A. sericea.
Keywords: teasel, invasive plants, strawberry.
Introduction as affecting natural areas in 14 states and four national parks (USDI-NPS, 2005). This combined status and Two invasive teasels of European origin, Dipsacus other factors led to the initiation of a US-government- fullonum L. and Dipsacus laciniatus L., are emerging sponsored biological control programme targeting Dip- as problem weeds in various parts of North America, sacus spp. in 2003. particularly in non-agricultural habitats (Sforza, 2004). The genus Dipsacus L. is in the family Dipsacaceae, Either or both species occur in 43 states (Singhurst and an exclusively Old World family with no species native Holmes, 2001; USDA, 2005; Rector et al., 2006) and in to the Western Hemisphere (Verlaque, 1985) and no several Canadian provinces (Werner, 1975). Five states members of significant economic importance (Bailey, (Colorado, Iowa, Missouri, New Mexico and Oregon) 1951). Thus, in selecting biological control candidates have declared teasels noxious (USDA-NRCS, 2005). (BCCs) to combat invasive teasels in North America, They are also listed as invasive by 11 other states and those restricted to feeding on hosts within the family Dipsacaceae should be specific enough to avoid non- 1 USDA-ARS, European Biological Control Laboratory, Campus Inter- target concerns (Wapshere, 1974; Rector et al., 2006). national de Baillarguet, Montferrier-sur-Lez, France. However, for any teasel BCC, the list of plants tested 2 Agricultural University, Faculty of Plant Protection, Department of En- tomology, 12 Mendeleev St., 4000 Plovdiv, Bulgaria. will include many species outside the family Dip- Corresponding author: B.G. Rector
311 XII International Symposium on Biological Control of Weeds niches, those sharing similar life histories, plant archi- in northern Bulgaria at two locations in the vicinity tecture and secondary chemistry, and those with pub- of Pleven (43°24.26¢N, 24°28.76¢E and 43°14.16¢N, lished associations with the BCC (Rector et al., 2006). 24°18.24¢E) and one location near Lovech (43°04.12¢N, Abia sericea (L.) (Hymenoptera: Cimbicidae) is a 14°44.09¢E). All larvae from these three sites were sawfly that is native to Europe and is a candidate for grouped together and reared to pupation under ambient biological control of invasive teasels in the USA. The climatic conditions near Plovdiv, Bulgaria (42°08.64¢N, most recent, comprehensive host-range records for A. 24°43.81¢E). On 29 June 2006, adult females were col- sericea (Liston, 1995, 1997; Taeger et al., 1998) list lected from D. laciniatus plants in the field near Sofia two host species in the family Dipsacaceae [Knautia ar- (42°3757 N, 23°303427 E). Oviposition tests and feed- vensis (L.) Coult. and Succisa pratensis Moench], plus ing tests were conducted using all of these insects and the genus Fragaria L., which is in the family Rosaceae their progeny. and includes cultivated and wild strawberries. In assessing A. sericea as a BCC of teasels, it was nec- Test plants essary to start by testing the suitability of Fragaria as a host, to either confirm or refute the existing herbivore– The D. laciniatus plants used in host-specificity host records. Any amount of A. sericea larval feeding on testing were either grown from seed gathered from Fragaria plants, particularly on cultivated strawberry wild plants in Bulgaria or were transplanted from fal- (Fragaria ´ ananassa Duchesne), would immediately low fields near Plovdiv (42°08.64¢N, 24°43.81¢E). disqualify it as a BCC of teasel. It was also necessary The test plants of the wild Fragaria spp. (Fragaria vesca from the start to confirm the use of D. laciniatus as L. and Fragaria viridis Duchesne) were dug up from a host plant suitable for complete development by A. the wild on a mountainside near Plovdiv (41°53.80¢N, sericea, as this relationship had only previously been 25°20.07¢E), transferred to pots and identified to spe- observed in the field without further testing (Rector et cies with a key (Markova, 1973). Cultivated strawberry al., 2006; Rector et al., unpublished data). (F. ´ ananassa) plants were vegetatively propagated The purpose of this paper is to report the successful from 6-year-old plants. rearing of A. sericea on D. laciniatus and to refute the published herbivore–host relationship between A. seri- Oviposition tests cea and Fragaria spp. Test 1: On 11 Oct 2005, a male and three female A. sericea adults were put in a large cage (40 ´ 20 ´ 40 cm, made from clear, plastic panels with fine nylon mesh Materials and methods tops) with two D. laciniatus and two F. ´ ananassa plants. At 8:30 a.m. on 12 October, the teasel plants Literature survey were removed from the cages, leaving only the straw- An intensive literature search was conducted to berry plants. At 4:30 p.m. on the same day, the teasel determine the origin(s) of reports of a herbivore–host plants were returned to the cages. The insects were then relationship between A. sericea and Fragaria spp. An left in the cage with both plant species until they died. attempt was made to identify the original source lit- A 5% sugar solution was provided for the insects with erature behind this alleged association and to gauge a cotton wick from which to feed. its plausibility. Literature surveyed included various Test 2: Pairs of newly emerged adults were released entomological texts, articles and monographs. Most of into small plastic cages (20 ´ 20 ´ 30cm) with one pot- these were on the subject of basic sawfly (Hymenop- ted plant each of D. laciniatus, F. ´ ananassa, F. vesca tera: Symphyta) biology and taxonomy (e.g. André, and F. viridis. Cages were kept in an insectary at ap- 1879; Stein, 1883; Cameron, 1890; Dalla Torre, 1894; proximately 22/15°C, day/night, and 16 h daylight. Konow, 1901; Enslin, 1917; Berland, 1947; Lorenz and The adults were kept in the cages until they died, af- Kraus, 1957; Ermolenko, 1972; Vasilev, 1978; Wright, ter which the plants were removed from the cages and 1990; Magis, 2001). Other sources included sawfly examined with a magnifying glass for eggs laid, and host-range compendia (Liston, 1995, 1997; Taeger et this number was recorded for each plant species. A total al., 1998), work specific to Abia spp. (Kangas, 1946) of 16 replications were conducted during the period 1 and a general entomology text (Krishtal, 1959). In ad- April to 1 Aug 2006. dition, pest management literature for cultivated straw- berries was surveyed to determine whether A. sericea is No-choice larval feeding tests considered a pest to commercial strawberry growers in its native range in Europe. No-choice feeding tests were conducted in small plastic cages. In each cage, one plant of each of the three Fragaria spp.—F. vesca, F. viridis and F. ´ anan- Insect material assa—were exposed to six larvae of first instar of A. On 4 September 2005, 29 late-instar larvae of A. sericea. Four replications were carried out, while one sericea were collected from the wild on D. laciniatus cage with only D. laciniatus plants and six larvae of the
312 Feeding and oviposition tests refute host–herbivore relationship between Fragaria spp. and Abia sericea same instar from the same cohort was set up as a con- host–plants list for A. sericea. The Krishtal (1959) in- trol. Larvae were checked every 48 h whereupon the formation in particular has been characterized as ‘unre- number of dead larvae was recorded. The same proce- liable’ (A. Taeger, personal communication). dure was followed with four replicates each of second, In addition, if A. sericea were in fact a herbivore of third and fourth instar larvae that had been reared on D. Fragaria spp., it is likely that it would be of concern laciniatus to that stage. to commercial strawberry (F. ´ ananassa) production within its native range. However, A. sericea is not listed Multiple-choice larval feeding tests as a pest of strawberry in current pest management lit- erature in Bulgaria (Harizanov and Harizanova, 1998), The tests were carried out by placing six A. sericea England (Marks, 2008) or France (Lamarque and Bos- larvae of the same instar into a small cage with one sennec, 2001), three strawberry-producing nations potted plant each of D. laciniatus, F. vesca, F. viridis within the native range of A. sericea. Taken together, and F. ´ ananassa whose leaves were all touching. To these various lines of evidence provide no support begin the test, two larvae were placed on each of the whatsoever to the records by Konow (1901) and Krish- three Fragaria spp. plants, after which they were free tal (1959) suggesting that Fragaria spp. are host plants to move to other plants. The experiment was repeated for A. sericea. three times: from 24 April to 16 May 2006 with seven replications each of larvae from second, third and fourth instars; from 17 May to 15 June with seven replications Oviposition tests each of larvae from first to fourth instars and from 7 Test 1: A total of 64 eggs were laid on D. laciniatus July to 5 August with eight replications each of larvae plants by the three A. sericea females before the teasel from first to fourth instars. The larvae were monitored plants were removed from the cage (Figs. 1 and 2). No daily, and the number of dead larvae was recorded. The eggs were laid on the strawberry plants, neither in the experiment was terminated after the pupation of the last presence of the teasel plants nor in their absence. After larva. D. laciniatus plants were replaced as needed. the teasel plants were returned to the cage, an additional 26 eggs were laid on them. Results Literature survey There appear to have been only two direct reports of Fragaria spp. recorded as a host plant for A. sericea, with all other such reports in the literature referring ei- ther to one of these two original reports or to others that have, in turn, cited the original two. The first re- port (Konow, 1901) simply lists A. sericea as occurring “on S. pratensis and F. vesca” while including neither a reference nor any specific collection data nor any in- formation regarding feeding nor rearing experiments. The second independent report alleging an association between A. sericea and Fragaria comes from a Ukrai- nian general entomology text by Krishtal (1959) that covers all insects in all orders occurring in that country. This book declares that A. sericea is ‘polyphagous’, although the only food plants listed are two Fragaria spp. that are native to Ukraine: F. vesca and F. viridis, and there is no collection or feeding/rearing informa- tion provided. This alleged host–herbivore connection has been repeated many times throughout the entomo- logical literature, particularly in literature pertaining to Symphyta in general (e.g. Enslin, 1917; Ermolenko, 1972; Liston, 1995, 1997; Taeger et al., 1998) or the genus Abia in particular (e.g. Kangas, 1946). However, recent reports have cast doubt on this connection. In- deed, Taeger et al. (1998) stated explicitly “Fragaria is surely not a food plant [for Abia sericea] under field conditions.” However, they presented no reference or Figure 1. Abia sericea female ovipositing into the leaf data to support this statement and left Fragaria on their margin of a D. laciniatus plant.
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was observed on D. laciniatus during daylight hours. There appeared to be a stimulus to this oviposition- associated behaviour that was linked to the presence of D. laciniatus plants and a lack of such stimulus from the strawberry plants. Oviposition occurred along the margins of the D. laciniatus leaves, with the eggs deposited just beneath the epidermal layer of either the upper or lower leaf surface (Figs. 1 and 2). None of the adults were ob- served feeding on the sugar solution, consistent with the observation by Vasilev (1978) that most Cimbici- dae adults do not require such food. Test 2: The presence of D. laciniatus plants did not stimulate oviposition on adjacent strawberry plants or on other surfaces such as the walls of the cage, with only one exception. A total of 16 females laid 936 eggs, 934 of which were laid in D. laciniatus leaves (99.8%), while two were laid by one female in a F. viridis leaf (0.2%). This same female also laid >100 eggs in D. la- ciniatus leaves during the same trial. Only one of the eggs laid in the F. viridis leaf hatched, and the larva died before pupation after feeding exclusively on D. lacini- atus leaves despite hatching from a F. viridis leaf and always having all three Fragaria spp. available as food options. There were no eggs laid on any of the F. vesca or F. ´ ananassa leaves in any of the replications.
Figure 2. Abia sericea eggs (along leaf margins) and neo- nate larvae on a leaf of Dipsacus laciniatus. No-choice larval feeding tests No feeding, feeding attempts or evidence of feed- ing was observed on any of the F. vesca, F. viridis or A difference in female A. sericea behaviour was F. ´ ananassa leaves in any of the cages (Table 1). Most observed that coincided with the presence or absence of the first-instar larvae died after 1 or 2 days, appar- of the teasel plants in the cage. The females moved ently of starvation. The second-instar larvae died 1 to restlessly over the surface of the D. laciniatus leaves, 4 days after their release into the cage. As the instar raising and lowering their abdomens and periodically of the larvae at the beginning of the test increased, the piercing the leaf epidermis with their ovipositors. survival period to death also increased. The third-instar This behaviour was not observed when they were on larvae died within 5 days (most after 3 to 4 days), and strawberry leaves. When the teasel plants were absent, the fourth-instar larvae were all dead by the eighth day leaving only the three Fragaria spp. plants, the females (most after 4 or 5 days) without access to D. lacini- were no longer active at all. This indifferent behav atus plants as food. In contrast, only one second-instar iour did not appear to correlate with their only spend larva died feeding on D. laciniatus in a control cage. ing daylight hours alone with the strawberry plants, as All other control larvae of all instars (23 in total) fed oviposition by A. sericea and its associated behaviour normally and survived to pupation.
Table 1. Summary of oviposition and choice and no-choice feeding experiments of Abia A. sericea on Dipsacus laciniatus, Fragaria ´ ananassa, F. vesca and F. viridis. Test type Number of No. eggs laid/larvae feeding on each host plant replicates D. laciniatus F. ´ ananassa F. vesca F. viridis Oviposition, Test 1 1 90 0 0 0 Oviposition, Test 2 16 934 0 0 2 Larval feeding, 16 96 0 0 0 no-choice Larval feeding, 81 486 0 0 0 free-choice
314 Feeding and oviposition tests refute host–herbivore relationship between Fragaria spp. and Abia sericea
Multiple-choice larval feeding were feeding exclusively on D. laciniatus, 23 of 24 de- veloped to pupation. A total of 486 A. sericea larvae fed exclusively on Given that the purported associations between A. the teasel plants until they either pupated or died. They sericea and Fragaria spp. have been shown in this study did not feed at all on the F. viridis, F. vesca, or F. ´ to be invalid and given that all confirmed hosts of A. ananassa plants, and no tasting attempts were observed. sericea belong to the family Dipsacaceae, there is no Most of the larvae feeding on D. laciniatus developed reason to suspect that A. sericea will be a threat to F. normally and pupated (88.6%). Of the larvae that died ´ ananassa. The absence of concern for A. sericea in while feeding on D. laciniatus, some showed symp- European strawberry pest management literature sup- toms of virus infection (Lacey and Brooks, 1997). A ports this assertion. virus was identified from some of these A. sericea ca- davers as belonging to the family Iridoviridae. These same symptoms were not observed in any of the larvae Conclusions that died on Fragaria spp. in the no-choice tests. There was no evidence to support a herbivore–host relationship between A. sericea and any Fragaria spp. These results, combined with evidence from the ento- Discussion mological and strawberry pest management literature and the lack of any comparable data or evidence in Fragaria vesca and F. viridis, two species of wild the literature supporting such an insect–plant associa- strawberry, have been recorded in the entomological tion, strongly suggest that existing records of such a literature as hosts for the European sawfly A. sericea relationship are erroneous. At the least, it can be confi- (Konow, 1901; Krishtal, 1959). Doubt has been cast dently stated that the populations of A. sericea inhabit- on this insect–plant association (Taeger et al., 1998; A. ing the region of northern Bulgaria from whence the Taeger, personal communication), but to date, there have test insects for these studies came do not attack the been no data to either confirm or refute these reports. two species implicated by Konow (1901) and Krishtal The phylogenetic evidence suggests that such a con- (1959), F. vesca and F. viridis, nor do they pose any nection is unlikely. If the inclusion of Fragaria as a threat to the cultivated strawberry, F. ´ ananassa. For host of A. sericea were accurate, this would represent the purpose of ensuring host fidelity in a weed BCC the only known host plants outside the closely related such as A. sericea, this is a satisfactory conclusion, as families Caprifoliaceae and Dipsacaceae for any spe- biological control agents are selected on a population- cies in the genus Abia (Taeger et al., 1998). Fragaria specific basis due to the need for absolute certainty in is in the family Rosaceae, which is not at all closely avoidance of non-target effects. The studies presented related to Dipsacaceae (APG II, 2003). Although host in this paper also confirm the use of D. laciniatus as relationships among herbivores do not always follow food plant for A. sericea. plant phylogeny, this evidence is not trivial. Cultivated strawberry, F. ´ ananassa, is a hybrid of two New World species, Fragaria chiloensis (L.) P. Acknowledgements Mill. and Fragaria virginiana Duschene (Hokanson et al., 2006), and thus neither the hybrid plant nor its pro- The authors would like to thank Dr. D. Smith of USDA- genitors would have had any exposure to A. sericea be- ARL-SEL, Washington, DC and Dr. A. Taeger of DEI, fore the introduction of the two progenitor species into Münester, Germany for their assistance in locating lit- Europe in the 19th century and the subsequent creation erature and for specimen identification. Thanks also to of the hybrid (Hokanson et al., 2006). Dr. Taeger, Dr. R. Sobhian of USDA-ARS-EBCL, In an oviposition test with three gravid females, France and Dr. M. Volkovich of the Zoological Institute eggs were laid on only D. laciniatus. In a second ovipo- of St. Petersburg, Russia for translation of literature. sition test with 16 females, a total of 934 eggs (99.8%) Thanks to Dr. W.G. Meikle of USDA-ARS-EBCL for were laid in the leaves of D. laciniatus plants, while his comments on the manuscript. Blagodarya to Dr. K. two eggs were laid in a F. viridis leaf (0.2%). Possible Kojuharova of the Dept. of Botany, Agricultural Univer- explanations for the laying of these two eggs on a non- sity, Plovdiv, Bulgaria who provided identification of host plant are central nervous system excitation or sen- wild strawberry species, Dr. M. Velichkova-Kojuharova sitation, as described by Marohasy (1998), or the lack of The Plant Protection Institute, Kostinbrod, Bulgaria of appropriate leaf-edge oviposition sites available on for virus identification, and to O. Todorov for technical the D. laciniatus plant in the cage (whose leaves were assistance. more or less lined with eggs by the end of the trial). In no-choice feeding studies presented in this paper, all References insects died without leaving any trace of feeding or at- tempted feeding. In control cages in which larvae from André, E. (1879) Species des Hyménoptères d’Europe et the same cohorts as the insects tested on Fragaria spp. d’Algérie, vol. 1. Beaune, France, pp. 29–32.
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