Displacement of Aphytis chrysomphali by Aphytis melinus, parasitoids of the California red scale, in the Iberian Peninsula

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1 Instituto Ncionl de Investigción y Tecnologí Agrri y Alimentri (INIA) Spnish Journl of Agriculturl Reserch (1): Avilble online t ISSN: X eissn: Displcement of Aphytis chrysomphli by Aphytis melinus, prsitoids of the Cliforni red scle, in the Iberin Peninsul Jun Rmon Boyero 1, Jose Miguel Vel 1, Ev Wong 1, Crlos Grci-Ripoll 2, Mri Jesus Verdu 2, Alberto Urbnej 2 nd Pilr Vncloch 2 * 1 Unidd de Entomologí. Centro IFAPA de Churrin. Cortijo de l Cruz Málg, Spin. 2 Unidd de Entomologí. Centro de Protección Vegetl y Biotecnologí. Instituto Vlencino de Investigciones Agrris (IVIA). Ctr. Moncd-Náquer, km 4, Moncd (Vlenci), Spin Abstrct Prsitoids re the min nturl enemies of the Cliforni red scle, Aonidiell urntii (Mskell) nd on occsion cn regulte their popultions. To increse their effectiveness, inocultive or ugmenttive releses of prsitoids re promoted. Previous to the implementtion of ny relese strtegy n importnt nd necessry step is to cquire knowledge on the prsitoid fun ssocited with this key phytophgous pest. Prsitoids were surveyed nd quntified in Spnish citrus orchrds between nd. Aphytis melinus DeBch (87.1%) resulted s the dominnt species, followed by Aphytis chrysomphli (Mercet) (15.9%), Encrsi perniciosi (Tower) (2.4%) nd Aphycus hederceus (Westwood) (0.004%). Overll, higher levels of prsitism were recorded in fruit thn in twigs. Scles in fruit were prsitized t similr levels by the different prsitoid species wheres E. perniciosi ws more ctive in twigs. Dt eventully revel the recent displcement of A. chrysomphli by A. melinus. The implictions of these results on the biologicl control of A. urntii re discussed nd this informtion will be useful in the decision of IPM strtegies for this pest. Additionl key words: biologicl control; Aonidiell urntii; climtic conditions; Encrsi perniciosi. Introduction * Corresponding uthor: pilrvncloch@gmil.com Received: Accepted: Hymenoptern prsitoids of the genus Aphelinide re the min nturl enemies of rmoured scle insects, prticulrly the ectoprsitoids of the genus Aphytis (Rosen, 1994) nd the endoprsitoids of the genus Encrsi (Viggini, 1990). Severl species of these gener hve been widely used in the regultion of Cliforni red scle (CRS), Aonidiell urntii (Mskell) (Hemipter: Dispidide) popultions (Viggini, 1990; Rosen, 1994). This phytophgous pest, CRS, cn cuse the commercil deprecition of fruit nd due to its unstisfctory control is considered key pest in lmost ll citrus-growing res worldwide (Jcs & Urbnej, 20). Nturl occurring CRS prsitoid guilds re insufficient to keep pest popultions under economic injury levels (Viggini, 1994). Hence, to increse the benefits provided by these nturl enemies, biologicl control (BC) progrms, bsed on inocultive or ugmenttive releses of CRS prsitoids s well s conservtion mesures ddressed to mintin nturlly occurring prsitoid guilds, re being promoted (Jcs & Urbnej, 20; Ten et l., 2013b; Vncloch et l., 2013; Urbnej et l., 2014). Previous to the implementtion of ny of these mesures n importnt nd necessry step is to cquire knowledge on the prsitoid fun ssocited with this phytophge, such s guild composition, ecology nd ctivity in the res where they re going to be implemented. Previous studies hve been conducted on A. urntii prsitoids in Spnish citrus orchrds (Rodrigo et l., 1996; Pin et l., 2003; Sorribs et l., ). Unfortuntely, ll of them were performed in the sme citrus growing re, the Vlenci region. In these studies, the prsitoids ssocited with A. urntii were the ectoprsitoids Aphytis chrysomphli (Mercet), Aphytis melinus De- Bch, Aphytis lingnnensis Compere, Aphytis hispnicus (Mercet) nd the endoprsitoid Encrsi perniciosi Tower. Aphytis chrysomphli nd A. hispnicus re considered ntive species in Spin. Aphytis chrysomphli ws found to be the prevlent prsitoid in erlier studies (Rodrigo et l., 1996; Pin et l.,

2 Prsitoids of Aonidiell urntii ), but t present, A. melinus hs displced the ntive one becoming the most bundnt species ssocited with CRS (Vncloch et l., ; Sorribs et l., 20; Ten et l., 2013). Aphytis melinus ws first introduced in the Vlenci region in 1976 (Meliá & Blsco, 1980). Aphytis lingnnensis nd E. perniciosi were lso introduced in this region, but their estblishment ws not successful (Rodrigo et l., 1996; Pin et l., 2003; Sorribs et l., 20). Prsitoids of CRS re usully found s species guilds tht my vry in their composition t different sites nd different substrtes of the plnt due to different environmentl condition requirements s well s host stge preferences (Yu et l., 1990; Rodrigo et l., 1996). For their ecologicl success, prsitoids must dpt to rnge of environmentl conditions similr to the ones required by their host. However, when two or more species compete in the sme ecologicl niche, smll vritions on ny environmentl vrible my chnge the dominnce hierrchy within the guild (Chpin et l., 2000; Hnce et l., ). As result, reduction in the reltive bundnce of some species or even their extinction could result (Hnce et l., ). The effect of environmentl vribles on prsitoid guilds cn be followed through geogrphicl or temporl studies. Ares under different climtic conditions my present different guild compositions. Temporl series in which these vribles chnge my explin the ecologicl succession from pst to present guild. Thus, climte chnge is recognised s n importnt fctor ffecting the distribution of wide rnge of orgnisms (Pimm, 2001; Prmesn, ; Hnce et l., ). Met-nlysis estimtes n verge displcement per decde of northern nd ltitudinl species distribution boundries of 6.1 km nd 6.1 m northwrd nd upwrd respectively (Prmesn & Yohe, 2003). In ddition to the more predictble effects of biotic fctors on single species, species idiosyncrtic phenologicl responses to chnges in environmentl vribles re expected to trigger cscde of chnges on species interctions t ll ecologicl levels with unpredictble consequences (Dvis et l., 1998; Chpin et l., 2000; Vn Nouhuys & Lei, 2004). In the present work, comprehensive study describing CRS prsitoid ssemblges in the min Spnish citrus growing res hs been conducted. The species composition nd their reltive bundnce hve been determined for ech ssemblge nd correlted to the CRS prsitism rtios found. Results obtined were compred with those of previous study done on more locl scle (Sorribs et l., 20). The informtion compiled provides better understnding of the mechnisms determining the CRS prsitoid hierrchy under most of the climtic conditions found on the Iberin Peninsul, nd help to predict potentil chnges in the hierrchy with regrd to globl wrming scenrio. The informtion herein provided my be used in the design of Integrted Pest Mngement (IPM) strtegies dpted to more locl conditions. Mteril nd methods Study sites nd smpling methods Aonidiell urntii-infested fruit nd twigs of citrus trees (sweet ornge nd clementine mndrin) were smpled between nd, from August to November, in 21 orchrds locted throughout the min citrus-growing res of Spin (Tble 1 nd Fig. 1). During this period, twig nd fruit smples were rndomly collected from ech plot t lest once per month nd tken to the lbortory, where leves were removed. The first genertion of the scle (My-June) ws not smpled since fruit ws not vilble for prsitism comprison with twigs. Twigs of pproximtely 20 cm were exmined under binoculr microscope. From ech smple, both twig nd fruit, irrespective of the number of scles present, up to ten individuls were checked to stndrdise the smpling. One hundred susceptible scles of A. urntii per smpling site nd dte for prsitism (second nymphl stge, young femles nd prepup nd pup mles), were checked. Prsitoid species were determined ccording to their pup pigmenttion pttern nd, when necessry, pupe were trnsferred into geltine cpsules for further development. Adults emerged from pupe were determined to species level. Dt nlysis Active prsitism rte, given s n verge ± stndrd error, ws clculted s the number of live prsitized CRS over the totl number of scles susceptible to being prsitized. According to the prsitoids obtined, percentges of ctive prsitism were clssified in four different ssemblge combintions found in the smpled orchrds: 1) orchrds where A. melinus ws predominnt (> 95% of the prsitoids found)

3 246 J. R. Boyero et l. / Spn J Agric Res (2014) 12(1): Tble 1. Reltive bundnce of prsitoid species observed in 21 citrus groves for the smpled period -. The different citrus groves smpled were locted through the Spin citrus re. AL: Almerí; CA: Cádiz; CS: Cstellón; IB: Isls Bleres; HU: Huelv; MA: Málg; MU: Murci; VL: Vlenci Code Loction Citrus species nd cultivr Yer Prsitoids A. melinus A. chyrsomphli E. perniciosi A. hederceus (n) (%) (%) (%) (%) Almenr (CS) Benifiró de l Vlldingn Llíri Béter Moncd L Pobl de Vllbon Inc (PM) Bellregurd Cstellonet L Alcúdi de Crespins El Mirdor (MU) Mondujr (AL) Mojoner (AL) Churrin (MA) Alhurín de l Torre (MA) Pizrr (MA) Csrbonel (MA) Citrus clementin Hort. Ex Tn. cv. Oronules Citrus clementin Hort. ex Tn. cv. Clemenules cv. Nvelin cv. Lne Lte Citrus clementin Hort. ex Tn. cv. Esbl cv. Nvelin Citrus clementin Hort. ex Tn. cv. Orogrnde cv. Lne Lte cv. Cstelln 1, ,

4 Prsitoids of Aonidiell urntii 247 Tble 1 (cont.). Reltive bundnce of prsitoid species observed in 21 citrus groves for the smpled period -. The different citrus groves smpled were locted through the Spin citrus re, AL: Almerí; CA: Cádiz; CS: Cstellón; IB: Isls Bleres; HU: Huelv; MA: Málg; MU: Murci; VL: Vlenci Code Loction Citrus species nd cultivr Yer Prsitoids A. melinus A. chyrsomphli E. perniciosi A. hederceus (n) (%) (%) (%) (%) Sn Enrique (CA) Moguer (HU) Crty (HU) Nerv (HU) Sub-totl Totl cv. Newhll Citrus clementin Hort. ex Tn. cv. Clemenpons ,656 1, , (6.9 1 ) % in loclities with presence of Encrsi perniciosi. (Am); 2) orchrds where E. perniciosi ws present (< 95% of the prsitoids were A. melinus nd 5-0% were E. perniciosi) (Am + Ep); 3) coexistence of A. melinus nd A. chrysomphli, but predominnce of A. melinus (51-95% A. melinus nd 5-49% A. chrysomphli) (Am + Ac) nd 4) coexistence of A. melinus nd A. chrysomphli but predominnce of A. chrysomphli ( 50% A. melinus nd 50% A. chrysomphli) (Ac + Am). Prsitism percentges were subjected to two-wy nlysis of vrince (fctors: substrte nd prsitoid ssemblge) nd the Bonferroni-test ws used for men seprtion t p < Dt underwent ngulr trnsformtion before the nlysis to meet the ssumption of normlity nd homogeneity of vrince. Results Four species of prsitoids were found ssocited with A. urntii: Aphytis melinus, A. chrysomphli, E. perniciosi nd Aphycus hederceus (Westwood) (Encyrtide). Aphytis melinus ws the most widespred nd the predominnt species in the mjority of the study loctions ccounting for 81.7% of A. urntii prsitism. Aphytis chrysomphli nd E. perniciosi ccounted for 15.9% nd 2.4% of CRS prsitism (Tble 1). The incidence of A. hederceus ws negligible, with only three specimens found in the south of Spin in. Aphytis melinus ws present throughout ll the study re, while A. chrysomphli nd E. perniciosi hd more restricted nd rther lloptric distributions. Aphytis chrysomphli spred in the estern citrus res situted t round 37º 50 N ltitude (loctions 1 to in Tble 1 nd Fig. 1); conversely, E. perniciosi ws distributed south of tht ltitude, in the Andlusi region (loctions 12 to 21 in Tble 1 nd Fig. 1). In the symptric re encompssing A. melinus nd A. chrysomphli (Vlenci region nd Bleric Islnds), the incidence of the ltter dropped from 55.5% in to 8.7% in. In its distribution re, E. perniciosi reched on verge, reltive bundnce of 6.9%. No ssocition between prsitoid reltive bundnces nd citrus species ws observed (Tble 1). Prsitism of scles ws significntly higher in fruit thn in twigs (fruit: 21.2 ± 8.3%; twigs: 15.7 ± 8.7%) (F 1,140 =13.2; p =0.0004) (Fig. 2). Different prsitism levels were recorded for the different species ssemblges in twigs, nd were sttisticlly higher where E. perniciosi ws present (F 3,77 =6.5; p =0.0006) (Fig. 2).

5 248 J. R. Boyero et l. / Spn J Agric Res (2014) 12(1): Discussion Aphytis melinus Aphytis chrysomphli Encrsi perniciosi Aphycus hederceus Figure 1. Smpling loctions nd distribution of species of prsitoids founded ssocited to Aonidiell urntii long the min citrus growing res in Spin. Ech number indictes the loction. 1, Almenr (CS); 2, Benifiró de l Vlldign ; 3, Llíri ; 4, Béter ; 5, Moncd ; 6, L Pobl de Vllbon ; 7, Inc (PM); 8, Bellregurd ; 9, Cstellonet ;, L Alcúdi de Crespins ;, El Mirdor (MU); 12, Mondujr (AL); 13, Mojoner (AL); 14, Churrin (MA); 15, Alhurín de l Torre (MA); 16, Pizrr (MA); 17, Csrbonel (MA); 18, Sn Enrique (CA); 19, Moguer (HU); 20, Crty (HU); 21, Nerv (HU). AL: Almerí; CA: Cádiz; CS: Cstellón; PM: Plm de Mllorc; HU: Huelv; MA: Málg; MU: Murci; VL: Vlenci. However, no significnt differences between ssemblges were found in fruit (F 3,62 = 1.0; p = 0.39) (Fig. 2b). Aphytis melinus nd A. chrysomphli were found in similr percentges in both twigs nd fruit wheres 96% of E. perniciosi prsitoids were found in twigs. Aphytis melinus nd A. chrysomphli re widespred biologicl gents of CRS worldwide (Dhms & Smith, 1994; Viggini, 1994; Noyes, 2003). In Spin A. melinus ws first relesed in the Vlenci region in 1976 s prt of BC progrm; lter it ws lso relesed in Andlusi in 1987 (Pin & Verdú, ). According to our results, A. melinus hs been estblished very successfully in ll citrus-growing res of Spin. Aphytis chrysomphli is considered n indigenous species. It ws first found in Spin on Chrysomphlus dictyospermi (Morgn) (Hemipter: Dispidide) in Andlusi, the Vlenci region nd the Bleric Islnds by Grcí-Mercet (1912). Lter, this ectoprsitoid ws found on both C. dictyospermi nd CRS in Andlusi (Grcí-Mercet, 1930) nd the Vlenci region (Limón et l., 1976; Rodrigo et l., 1996). The results here obtined demonstrte tht A. melinus hs become the dominnt CRS prsitoid species in Spnish citrus nd seems to be progressively displcing A. chrysomphli, t lest in the hottest nd driest loctions s suggested by Sorribs et l. (20) in Vlencin citrus. This displcement hs lso been observed in other Mediterrnen regions (Siscro et l., 1999). The endoprsitoid E. perniciosi is common CRS prsitoid widely distributed round the world (Furness et l., 1983; Herty et l., ). To our knowledge, this species hs only been previously recorded in estern Spin (Pin & Verdú, b; Sorribs et l., ) where some inocultive releses were crried out (Pin & Verdú, b). Aphicus hederceus is widespred cross Europe (Noyes, 2003), nd hs lredy been recorded in Spin (Grcí-Mercet, 1921). In ) b) b b b % Prsitism % Prsitism 0 0 Am Am + Ep Am + Ac Ac + Am Am Am + Ep Am + Ac Ac + Am Figure 2. Prsitism percentges in twigs () nd in fruit (b) for the different prsitoid ssemblges. Am: > 95% Aphytis melinus; Am + Ep: < 95% Aphytis melinus nd 5-0% Encrsi perniciosi; Am + Ac: 51-95% Aphytis melinus nd 5-49% Aphytis chrysomphli; Ac + Am: 50% Aphytis melinus nd 50% Aphytis chrysomphli.

6 Prsitoids of Aonidiell urntii 249 the pst, uthors considered A. hederceus s prsitoid exclusive of soft scles, but Grcí-Mercet (1921) reveled tht this species lso prsitizes the rmoured scle Aspidiotus hedere (Vllot). Aphytis chrysomphli ws the dominnt species prsitizing CRS in Spin before A. melinus releses strted. In Andlusi, there is no dt bout the time in which the displcement by A. melinus occurred, but it probbly hppened fter the releses ccomplished in 1987 (Pin & Verdú, ). In our study, no A. chrysomphli specimens were found in tht citrus growing re during the three sesons when smples were collected. In reltion to the Vlenci region, in the 90 s, Rodrigo et l. (1996) found tht A. chrysomphli ccounted for 98% of CRS prsitisim. At the end of tht decde the reltive bundnce of this prsitoid declined to 77.7% (Pin et l., 2003), nd lter, it dropped to 50% (Sorribs et l., ). The dt presented in this work confirms this tendency showing decline from 55.5% in to 8.7% in. A similr prsitoid displcement of A. chrysomphli by A. lingnnensis (DeBch & Sisojevic, 1960) nd lter of A. lingnnensis by A. melinus (DeBch et l., 1969) occurred in Cliforni; in Greece, displcement of A. chrysomphli by A. melinus lso took plce (De- Bch & Argyriou, 1967). The very recent displcement of A. chrysomphli by A. melinus in Spin cused either by climtic conditions, persistent use of pesticides, competition with A. melinus or possibly combintion of ll these fctors, implies chnge in the performnce of A. chrysomphli in controlling CRS. The verge high tempertures of the Spnish Mediterrnen climte is fvourble to the presence of A. melinus (Smwys, 1985) while, A. chrysomphli nd E. perniciosi re better dpted to more moderte climtic conditions (Abdelrhmn, 1974; Pin & Verdú, b). Indeed, the rpid displcement which occurred in Andlusi ws probbly prtly due to the significntly wrmer tempertures of this re in comprison to the est cost (Fig. 1). Sorribs et l. (20) observed this phenomenon on smller scle in the Vlenci region, where A. melinus ws super-dominnt in those ssemblges found in wrmer res wheres A. chrysomphli ws ble to coexist vi temporl niche prtitioning in those res with colder springs nd winters. As yet, we cnnot explin why, ccording to the current dt, A. chrysomphli nd E. perniciosi spred in lloptric rnges, the former in northern regions nd the ltter in southern ones. The higher percentges of prsitism in fruit (21.2%) thn in twigs (15.7%) found in this work re similr to those found in other relted studies (Atkinson, 1977; Asplnto & Grcí-Mrí, 2002). We hve shown tht A. melinus nd E. perniciosi re symptric in groves of southern Spin, nd tht the ltter shows preference for twigs. This coincides with the sitution on the Cliforni costs described by Yu et l. (1990), who stted tht this resource prtitioning could explin the coexistence of A. melinus nd E. perniciosi. In this work CRS smpling ws not conducted during the first CRS genertion, My-June, when fruit is not present yet nd therefore, A. melinus nd E. perniciosi re forced to compete for the sme resource. Future studies which focus on this period of yer will help to discern the role plyed by E. perniciosi on CRS suppression nd the importnce of competition between these two prsitoid species in wrmer res. Severl uthors estblished tht prsitism rtes round 20% could control CRS (DeBch et l., 1969). This percentge ws reched in some of the orchrds smpled in our study; however, unfortuntely, prsitoids were unble to keep CRS popultions under economic injury levels. The insufficient nturl BC provided by CRS nturl enemies, nd especilly by prsitoids, plces CRS in the ctegory of key pest in Spin (Jcs & Urbnej, 20; Urbnej et l., 2014). In recent yers, emphsis hs been plced on implementing environmentlly sfe mesures to control A. urntii in Spin, rther thn using trditionl chemicl insecticides (Vcs et l., 2012; Vncloch et l., 2012, 2013b). For this purpose, ugmenttive releses of CRS prsitoids should be one of the lterntives considered for controlling this pest. According to our results, the recommended species to use in such ugmenttive progrms is A. melinus becuse it is clerly well-dpted to Spnish citrus growing conditions. Furthermore, becuse E. perniciosi plys role in controlling CRS in twigs, releses in those res where it cn become estblished should be continued. Acknowledgements The uthors wish to thnk ll the growers of the smpled orchrds for their help nd coopertion. We lso thnk C. Monzó (University of Florid) for helpful comments on erlier versions of the mnuscript nd Judy Frron for her English lnguge expertise. This reserch ws prtilly funded by the Conselleri

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