J. HYM. RES. Vol. 10(1), 2001, pp. 91-100

Natural Alternative Hosts of Eulophidae (Hymenoptera: Chalcidoidea) Parasitoids of the Citrus Leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) in the Mediterranean Basin

Bruno Massa, Maria Concetta Rizzo, and Virgilio Caleca

Istituto di Entomologia agraria, Universita degli Studi di Palermo, Viale delle Scienze 13, 90128 Palermo, Italy. E-mail: [email protected]

Abstract. —The entomofauna linked to native flora in and around citrus groves was studied in Italy and Jordan in order to find alternative hosts of eulophid parasitoids of the Citrus Leafminer (CLM), Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae). Twenty new associations (12 in Italy, 8 in Jordan) among native and exotic CLM parasitoids and leafminers were found. Two new alternative hosts were recorded for Citrostichus piln/llociiistoides (Narayanan) (an unidentified Nepticulidae on Pistacia lentiscus L. and Stigmella sp. on Rubus ulmifolius Schott, in Sicily and Jordan respectively) and 1 for Cirrospiliis iiigenuus Gahan (Agromyzidae on Salix sp., in Jordan). Five new alternative hosts were recorded for Semielacher petiolatus (Girault) (in Sicily Liriomyza sp. on Mcrciirialis annua L., Chromatomyia horticola (Goureau) on Sonchiis spp., Cosvioptcrix pulchrimella Chambers on Parictaria diffusa M. et K., and Stigmella aurcUa (Fabr.) on Rubus ulmifolius Schott; in Jordan, Dialcctica scalariella Zeller on Echium sp.). The other 12 new associations of CLM parasitoids with leafminers found in both countries include NeochrysocJiaris formosa (Westwood) (4 new hosts),

Cirrospilus variegatus (Masi) (5 new hosts), Ratzeburgiola incompleta Boucek (1 new host), Rntzcbur- giola cristata (Ratzeburg) (1 new host), and Asccodcs dclucchii (Boucek) (1 new host). Data reported here suggest that native vegetation harbours alternative hosts for both native and exohc parasit- oids. They also underline that more attention should be paid to the understanding of ecology and biology of parasitoid in order to use appropriate exotic enemies in biological control, preserving at the same time indigenous parasitoid communities.

The Citrus Leafminer (CLM), Phyllocnis- CLM in many countries and in some case tis citrella Stainton (Lepidoptera: Gracillar- also have been recovered in neighbouring iidae), is presently considered to be a se- countries (Schauff et al. 1998). rious threat to young citrus trees in the Native are an important source of Mediterranean region and other countries, biological diversity in agroecosystems and w^here it has expanded its range in the last are known to harbour natural enemies of seven years. The CLM attacks new phytophagous pests of cultivated plants, causing a loss of photosynthetic area. Seni- supplying alternative food, refuges and ielacher petiolatus (Girault), Citrostichus hosts (McMurtry and Johnson 1965, Pow- phyllociiistoides (Narayanan) and Cirrospi- ell 1986, Altieri 1991, Ragusa Di Chiara lus ingenuus Gahan (Hymenoptera: Eulo- 1991). They provide a diverse source of phidae) are considered among dominant food for many species of polyphagous nat- natural enemies of CLM in its original ural enemies, which in turn may parasit- range (India and South Asia) and in Aus- ize phytophagous insects of cultivated tralia (Smith et al 1997, Schauff et al. 1998). plants in seasons when they are abundant. Eulophid parasitoids have been selected Studies of phytophagous insects are of- for biological control programmes against ten directed at species attacking cultivated 92 Journal of Hymenoptera Research

plants and, less so, species feeding on na- following localities: Al Bahhath (Amman), tive ones; thus our knowledge of the hosts Aqaba and Dana Village. of parasitoids on cultivated plants is ex- RESULTS tensive, whereas we have only scattered data on the alternative hosts available to In Sicily, 40 host-parasitoid associations these parasitoids on native plants. Preser- involving phytophages of native plants vation of these reservoirs of antagonists and antagonists of CLM were already may prove valuable when parasitoids uti- known (Caleca et al. 1997, Mineo et al. lize hosts that are not pests of cultivated 1997a, 1997b, Caleca 1998, Caleca et al. plants, and when biological control de- 1998, Mineo and Sinacori 1998, Rizzo et al. pends on multiple natural enemy species, 1999, Massa and Rizzo 2000). They are list- as in the case of the CLM. ed in Fig. 1 together with the 12 (Italy) and The present study is part of a research 8 (Jordan) associations, previously unno- project examining the entomofauna of na- ticed, recorded in the present paper. Data tive flora carried out in 11 citrus orchards for new records are reported in Table 1. of Sicily (Italy), the results of which were The parasitoids we found on indige-

partly published (Caleca et al. 1997, Mineo nous leafminers belong to two quite dif-

et al. 1997a, 1997b, Caleca 1998, Caleca et ferent kinds: exotic CLM biological control

al. 1998, Mineo and Sinacori 1998, Rizzo et agents (i.e., Semielacher petiolatus, Citrosti-

al. 1999, Massa and Rizzo 2000). Some chiis phyllocnistoides and Cirrospilus iiigen- new findings are presented that highlight uus), which possibly have switched over interesting relationships between CLM onto indigenous hosts after their introduc- parasitoids and their non-pest hosts ex- tion or immigration, and native parasit- ploiting native plants. oids, which in turn have switched over onto the invading CLM. Among the latter, MATERIALS AND METHODS some (i.e., Neocluysocharis formosa (West- wood), Ratzeburgiola iucompleta Boucek Native floras associated with citrus and P}iigalio soeDiius (Walker)) are quite groves in Sicily (Italy) have been studied common on indigenous hosts in Sicily in detail by Raimondo et al. (1979); they (Fig. la), while three of them (i.e., Digly- amount to about 200 species involving phiis isaea (Walker), Ratzeburgiola cristata mainly and shrubs. During the four (Ratzeburg) and Cirrospilus variegatus years of our research project (1997-2000), (Masi)) have not yet been recorded on we collected about 40 of the most common CLM in the island, although they have species belonging to this flora, and about been reported on this host in other coun- 10 belonging to riverine flora sometimes tries (Schauff et al. 1998). It should be occurring in the neighbouring of cit- areas pointed out that, even if their parasitiza- rus orchards in Sicily. About 250 g of each tion does not always reach relevant val- species were collected monthly ues, most CLM parasitoids engage in host- along at least two perpendicular transects feeding which contributes additional mor- inside 11 citrus groves and along their pe- tality. For example in Algeria Guenaoui rimeter. Leaves infested by miners were and Dahliz (1997) attributed as much as placed in Petri dishes with wet paper at 20-50% of CLM larval mortality to host- 25° C, 65% r.h. and L14:D10. All phytoph- feeding and in Sicily it may approach 15% agous species and parasitoids that (pers. obs.). emerged were mounted and identified. Among the eight new host-parasitoid as- Further samples were gathered by the se- sociations reported from Jordan (Fig. lb), nior author during a research trip to Jor- five concern eulophids (S. petiolatus, N. for- dan between 21 and 29 May 1999 in the fuosa, C. phyllocnistoides and C. iugeiiuus) Volume 10, Number I, 2001 93

Plants Phytophagous insects Eulophids known to attack Phvllocnislis cilrella a) Sicily

Sonchiis ( 3 spp ) 94 Journal of Hymenopthra Research this pest in Sicily (Caleca et al. 1998, Mineo Cirrospilus ingenuus Gahan and Mineo 1999a). The five new hosts hst- Also known as its synonym C. quadris- ed in this paper (Table 1), comprising triatiis (Subba Rao and Ramamani), this (Cosmopterigidae, Nep- three Lepidoptera species has been recorded from Austra- ticulidae and Gracillariidae) and two Dip- lia, China, India, Indonesia, Japan, Ma- (Agromyzidae), are widespread in the tera laysia, Oman, Taiwan, Thailand (Smith Mediterranean region. et al. 1997, Schauff et al. 1998), and intro- It should be noted that this species ap- duced to Cyprus, Turkey, Israel, Syria, Sicily on Chromatomyia horticola peared in Egypt, Tunisia, Morocco, Florida and (Goureau) (Diptera: Agromyzidae) about Mexico (Argov and Rossler 1996, FAO one year after its release in 1996 in Tunisia 1996, Perales-Gutierrez et al. 1996, Ha- (FAO 1996). The availability of alternative med et al. 1999, LaSalle et al. 1999). It has hosts that provide refuge and food for S. also spread to Jordan and North Egypt, petioJatus during seasons of low CLM pop- probably from other countries of the ulation density, could partly explain the Mediterranean Basin (Schauff et al. 1998). quick spread and establishment of this It is generally considered to be a domi- species, both in countries where it has nant parasitoid of P. citrella (e.g., Thai- been released and in neighbouring sites land, Taiwan and Japan: Ujiye et al. (Caleca et al. 1998, Schauff et al. 1998, Mi- 1996), but also has been recorded as a neo and Mineo 1999a). parasitoid of Rhynchaeiuis maugiferae Marshall (Coleoptera: Curculionidae) in Citrostichus phyllociiistoides (Narayanan) India (Peter and Balasubramanian 1984). This species is known from Afghani- Agromyzidae previously has not been stan, China, India, Indonesia, Japan, recorded as a host for this parasitoid. Oman, Pakistan, Taiwan, Thailand,

South Africa, Sudan, Swaziland (Boucek Cirrospilus variegatus (Masi) 1988, FAO 1996, Schauff et al. 1998), and Also known as its synonym Zagrammo- has been introduced to Cyprus, Greece soffia variegatum, it occurs in the Mediter- and Italy (Sicily) (Michelakis 1997, FAO ranean Region, North and East Africa, 1996, Mineo and Mineo 1999b), and Aus- Central and South Asia, West Indies (Bar- tralia and Israel (where it is not consid- bados), Australia and New Zealand (Bou- ered established) (Smith et al. 1997, Ar- cek 1988; Yefremova 1996). This species gov and Rossler 1996). It probably described from Italy by Masi spread to Jordan from Israel (Mineo was (1907), as parasitoid of Metriochroa latifoliella (Mil- 1999). Although recorded as a parasitoid liere) (Lepidoptera: Gracillariidae). It is of the CLM (Boucek 1988, Ujiye and also known to parasitize many species of Adachi 1995, Wu and Lin 1998), it also -mining Lepidoptera (Boucek has been reported to parasitize the small and the in nymphs of Trioza obsoleta Buckton (Ho- 1988, Yefremova 1996) CLM (Schauff et al. moptera: Psyllidae) a gall former on Di- Libya, Spain and Turkey this study it found on ospijros nielanoxylon (Roxb.) (Dash and 1998). During was three Das 1997). Our records concern two ad- two Nepticulidae leafminers and on Diptera (one Tephritidae and two Agro- ditional Lepidoptera (Table 1); according all previously unre- to Nieukerken (pers. comm.) the mines myzidae) (Table 1), cognised as hosts. on Rubus ulmifolius Schott found in Jor- dan belong to a Stii^tfiella species (Nep- Ratzeburgiola incompleta Boucek ticulidae), possibly Stigmella aurella (Fabr.), a previously unrecorded host for Recorded from central Europe and this parasitoid. many countries of the Mediterranean Ba- )

Volume 10, Number 1, 2001 95

Table 1. List of new host records for Eulophidae emerged from leafminers reared from native plants collected in Italy and Jordan.

l.ulophid I lost spri ir Host plant

Sciiiiclachcr pctiolntu Chnvimtoim/in horticoln Soiichiis spp. Ital}, Parco d'Orleans 26 (Girault) (Goureau) (Diptera: (Palermo) 3.V.97, Agromyzidae) 21.in.99

Lirioiin/za sp. (Diptera: Mcrcurialis annua L. Italy, Borgo Molara 1 9 Agromyzidae) (Palermo) 29.XI.98 Cosiiioptcrix piilchriincl- Parictaria diffusa M. Italy, Zucco (Palermo) 49

la Chambers (Lepi- and K. 6.VI.00, Borgo Mo- doptera: Cosmopter- lara 26.1.99, 14.III.99 igidae)

Stiginclla nurclla {Fnbr.) Rubus uhiufolius Schott Borgo Molara 1 9 (Lepidoptera; Nepti- 17.VIII.99, Parco culidae) d'Orleans 20.IX.99

Dialectica scaliviclln Echiuni sp. Jordan, Dana Village 1 9 Zeller (Lepidoptera: 25.V.99 Gracillariidae) Lepidoptera: Nepticu- Pistacm Iciitiscus L. Zucco 4.IV.00

ides (Narayanan) lidae StigiucIIa sp. (Lepidop- R. uhiiifolius

tera: Nepticulidae)

Cirrospilus iiigcniiiis Diptera: Agromyzidae Salix sp. Gahan Cirrospiliis varicgntiis C. horticoln Rcichardia picroidcs (L.) (Masi) Lirionn/za coiigcsta Lathyrus pratcnsis L. (Becker) (Diptera: Agromyzidae) Eulcia hcradci (L.) Snn/rniuin pcrfoUatuni (Diptera: Tephriti- (L.) dae) Lepidoptera: Nepticu- P. Icutiscus lidae Lepidoptera: Nepticu- Chrozophora ti}U'toria lidae (L.)

Ratzcburgioln iiicoiiiplcta Diptera: Agromyzidae Salix sp. Boucek

Ratzcbiirgioln cristata L. coiigcstn L. pratcnsis (Ratzeburg) Neochrx/socharis foiiiwsn D. scalariclla Borago officinalis L. (Westwood

Lt'ticoptcrn nialifoliclln Crataegus inonogifna (Costa) (Lepidop- Jacq. tera: Gracillariidae)

Lirionn/zti bn/oninc Mattlnola uicana (L.) (Kaltenbach) Lepidoptera: Nepticu- C. tinctoria lidae Asccodcs dclucchii l~>iptera: Agromyzidae Salix sp. (Boucek) 96 Journal of Hymenoptera Research sin (Boucek 1969, 1970, Schauff et al. 1998), pers. comm.), but has not been previously this species is known to parasitize Holo- recorded in Jordan. It is known to attack cacista rivillei Stainton (Lepidoptera: He- P. citrella in Italy and Japan (Ujiye and liozelidae) (Boucek, 1969), Phyllouonjcter Adachi 1995, Ujiye et al. 1996, Mineo corylifoUclla Hiibner (Lepidoptera: Gracil- 1999), and has also been recorded as a par- lariidae) (Mineo and Sinacori 1998), Cos- asitoid of Caliroa cerasi L. (Hymenoptera: mopterix pulchrimella Chambers (Lepidop- Tenthredinidae) and Phyllonorycter messan- tera: Cosmopterigidae) (Rizzo and Mineo iella (Zeller) (Lepidoptera: Gracillariidae)

1997), Liriomyza trifolii (Burgess) (Diptera: (J. LaSalle, pers. comm.). Agromyzidae Agromyzidae) (Freidberg and Gijswijt previously has not been recorded as a host 1983), Urioviyza sp. (Diptera: Agromyzi- for this parasitoid. dae) (Rizzo and Mineo 1997), and Agro- DISCUSSION myza hiennilis (Massa and Rizzo 2000). It is also recorded as CLM parasitoid (Azawi The introduction of exotic polyphagous

1997, Schauff et al. 1998), and as the most parasitoids could decrease native parasit- abundant native CLM parasitoid in Tur- oids competing for the same food resource key (Uygun et al. 1997) and Israel (Rossler (Bennett 1993, Duan et al. 1996); thus, due and Argov 1997). to the naturally low density of their pop- ulations, native polyphagous parasitoids Ratzeburgiola cristata (Ratzeburg) may undergo dramatic decrease to be- Known from the whole Europe (Boucek come locally extinct (LaSalle 1993). For and Askew 1968, Rizzo and Mineo 1997, these reasons, to find the best control

Schauff et al. 1998) parasitizing Plnjllono- agent of a noxious insect before using it in rycter nigrescentella Logan (Lepidoptera: biological control programs LaSalle (1993) Gracillariidae) and Cosmia trapezina L. suggested carrying out research on the bi- (Lepidoptera: Noctuidae) (Boucek and ology and ecology of species of parasit- Askew 1968), Chrysoesthia sexguttella oids that are considered antagonists of the (Thunberg) (Lepidoptera: Gelechiidae), host.

Cosuiopterix pulchrimella and Stigjiiella aii- Since 1993, when P. citrella colonised rella (Rizzo and Mineo 1997), and the CLM Mediterranean citrus groves, endemic bi-

in Spain (Schauff et al. 1998). Agromyzidae ological diversity represented the poten- previously has not been recorded as a host tial resource for biological control (cf. for this parasitoid. LaSalle 1993). A dozen native polypha-

gous eulophids were found to parasite it. Neochrysocharis foiiiiosa (Westwood) These species constituted the parasitoid This species is known from the Palearc- community living on leaf-miners of the tic, Asia and Africa (Boucek and Askew native flora. Research carried out in Sicily 1968). It develops as a primary endopar- listed a total of 47 associations involving asitoid of larvae, and rarely eggs, of leaf- native eulophids that parasitize the CLM

miners (Hansson 1990), and is known as (Caleca et al. 1997, Mineo et al. 1997a,

parasitoid of P. citrella in Cyprus, Greece, 1997b, Caleca 1998, Caleca et al. 1998, Mi-

Israel, Italy, Japan, Jordan, Spain, Tunisia neo and Sinacori 1998, Rizzo et al. 1999, and Turkey (Caleca et al. 1996, FAO 1996, Massa and Rizzo 2000, present study) (cf. Ujiye et al. 1996, Schauff et al. 1998). Fig. la). Among CLM parasitoids, the ge- nus Cirrospilus (Hymenoptera: Eulophi- Asecodes delucchii (Boucek) dae) played a dominant role, particularly Asecodes delucchii (= Teleopterus deluc- C. pictus (Nees) in Sicily, Algeria and

chii) is known throughout the Palearctic Spain (Caleca et al. 1998, Guenaoui and

Region from England to Japan (J. LaSalle, Dahlis 1997, Vercher et al. 1997). Due to Volume 10, Number 1, 2001 97 the spread of CLM, many researchers significant quantitative analysis, from the planned the introduction of its specific qualitative point of view it seems that the control agents; in the Mediterranean Basin community structure of parasitoids did today at least 6 exotic species, known as not change after the introduction of exotic dominant parasitoids of P. citrella, have species (Caleca et nl. 1997, Mineo et nl. been introduced (Argov and Rossler 1997a, 1997b, Caleca 1998, Caleca et nl.

1996). Among them S. petiolntus sponta- 1998, Mineo and Sinacori 1998, Rizzo et nl. neously colonised Sicily (Mineo et al. 1999, Massa and Rizzo 2000). The number 1998), probably from N Africa, where it of individuals of S. petiolntus and C. phyl- had been introduced, while Ageniaspiis ci- locnistoides found parasitizing native hosts tricola Logvinovskaya (Hymenoptera: En- indeed is still low, compared with the cyrtidae) and the eulophids Qundrnstichus whole number of parasitoids (564) ob- sp. and C. pJn/Uociiistoides were here ac- tained during our research (Massa and tively introduced (Siscaro et al. 1997, Mi- Rizzo in press). neo and Mineo 1999b). Finally, our results point out that native Our research led us to find 5 alternative flora within and at the edge of citrus new native hosts of S. petiolntus and 2 of groves strengthens the biological control C. phyllocnistoides, as well as another new of P. citrelln, providing alternative hosts to host of C. ingenuus, eulophids previously its parasitoids, native as well exotic, main- known as dominant or specialist CLM ly in the winter-spring seasons when P. parasitoids. We believe that alternative citrelln density is very low. Additionally, hosts, leaf-miners of native flora, contrib- they stress the importance of knowledge uted to acclimatation of S. petiolntus and of parasitoid biology and ecology to opti- C. phyllocnistoides in Sicily, providing al- mise their use in biological control pro- ternative food and shelter, mainly in win- grams, as well the conservation of native ter and spring, when CLM populations parasitoid communities. decrease very much (Massa and Rizzo in press). As regards the interference deter- ACKNOWLEDGMENTS

mined on native CLM parasitoids by ex- The authors thank Prof. Pietro Mazzola and Dr. otic ones, S. petiolntus in 1998 represented Lorenzo Gianguzzi (Dipartimento di Scienze Botani- che, Palermo) for plant identification; Prof. Luciano as much as 38% of all the parasitoids in Siiss (Istituto di Entomologia agraria, Milan), Dr. Pa- an orange grove, with an average parasit- olo Triberti (Museo di Storia Naturale, Verona), Dr. ization rate of 6.9%, peaking to 87.5% in Erik Van Nieukerken (Rijksmuseum van Naturlijke September (Caleca et nl. 1998), while in Historic, Leiden) and Dr. John LaSalle (CABI Biosci-

1999 it represented 89% of all the parasit- ence UK Centre, Biology Dept., Ascot) for the iden- Agromyzidae, Gracillariidae, Nepticuli- oids in a lemon grove, with a peak of par- tification of dae and some Eulophidae, respectively; Prof. Ahmad asitization rate of 69.6% (Mineo and Mi- Katbeh-Bader (Horticulture and Plant Protection neo 1999b), playing a dominant role in the Dept., Jordan Univ., Amman), Dr. Salvatore Blando, CLM control. C. pJn/llocfiistoides on the Rocco Lo Duca, Dr. Gabriella Lo Verde and Dr. Val- agraria, Pa- contrary seems to be still sporadic in Sicily entina Lo Verde (Istituto di Entomologia help in the field; and Prof. At- (Mineo and Mineo 1999b). lermo Univ.) for their tilio Carapezza (Palermo University) for improving Among native CLM parasitoids in Sici- English. Paper funded by C.N.R. and M.U.R.S.T. ly, in 1998 C. pictus reached 7.9% of par- asitization rate, while all the other para- LITERATURE CITED sitoids did not exceed 2% (Caleca et nl. Altieri, M. A. 1987. A^roccolo^/. Intermediate Tech- 1998), values already known before the in- nology Publications, London. 227 pp. re- troduction of exotic parasitoids. As Argov, Y. and Y. Rossler. l'^)96. Introduction, release gards the parasitization on hosts of native and recovery of several exotic natural enemies

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