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First record of the leaf-gall inductor Cystiphora sonchi (Vallot, 1827) (Diptera: Cecidomyiidae) for Portugal and some notes about its Iberian distribution

López-Núñez, Francisco A.,Marchante, Hélia,Marchante, Elizabete

Abstract

FCT and COMPETE/FEDER, through project “INVADER-IV – INnoVating Approaches to Detect invasive spEcies and biocontRol agents” (PTDC/AAG-REC/4896/2014).

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G aellsia, 74(1): e068 ene o-junio 2018 ISSN-L: 0367-5041 h p://dx.doi.o g/10.3989/g aellsia.2017. 74.192 Fi s eco d o he lea -gall induc o Cys ipho a sonchi (Vallo , 1827) (Dip e a: Cecidomyiidae) o Po ugal and some no es abou i s Ibe ian dis ibu ion F ancisco A. López-Núñez1,*, Hélia Ma chan e2 & Elizabe e Ma chan e3 ¹Cen e o Func ional Ecology, Depa men o Li e Sciences, Uni e si y o Coimb a. Calçada Ma im de F ei as, 3000-456 Coimb a, Po ugal. ORCID iD: h p://o cid.o g/0000-0003-0773-9134 2Escola Supe io Ag á ia, Ins i u o Poli écnico de Coimb a. Bencan a, 3045-601 Coimb a, Po ugal. Cen e o Func ional Ecology, Depa men o Li e Sciences, Uni e si y o Coimb a. Calçada Ma im de F ei as, 3000-456 Coimb a, Po ugal. ORCID ID: h p://o cid.o g/0000-0002-3247-5663 3Cen e o Func ional Ecology, Depa men o Li e Sciences, Uni e si y o Coimb a. Calçada Ma im de F ei as, 3000-456 Coimb a, Po ugal. ORCID: h p://o cid.o g/0000-0003-1303-7489 *Au ho o co espondence: [email p o ec ed] ABSTRACT One equen limi a ion in zoology and ecology s udies is ha he cu en spa ial dis ibu ion o se e al species is only pa ially assessed, based on museum o ama eu s’ eco ds, unde es ima ing he eal dis ibu ion o he species. Al hough his limi a ion could be pa ially sol ed by di e en ools (e.g., species dis ibu ion models), he co ec unc ioning o many o such ools is ela ed o he numbe o occu ences, equi ing a minimum numbe o occu ences o be co ec ly alida ed. The genus Cys ipho a Kie e , 1892 (Dip e a: Cecidomyiidae) has h ee species in he Ibe ian Peninsula and is mainly cha ac e ized by he induc ion o galls in species o sow- his le (Sonchus spp.); his genus has an added alue since some species a e used as biocon ol agains in asi e sow- his les in he Nea c ic and Aus alasian egions. Howe e , li le is known abou i s ac ual dis ibu ion in Ibe ia. Cys ipho a sonchi (Vallo , 1827) is a Palea c ic species whose p esence in Ibe ia Peninsula was un il now es ic ed o ou eco ds in he Eas o Peninsula and in he Balea ic Islands. We ound h ee new popula- ions o his species in Coimb a, cen al Po ugal, adding a new species o he Po uguese auna. Addi ionally, in o de o comple e as much as possible i s cu en spa ial dis ibu ion, a me hodical sea ch was ca ied in di - e en Biodi e si y Da abases. These wo app oaches, expanded he dis ibu ion a ea o C. sonchi in he Ibe ian Peninsula, wi h i e new occu ences ( h ee o Po ugal, one o Galicia and one o Andalusia) and es ablishing a new wes limi in he cu en dis ibu ion o C. sonchi in he Palea c ic egion. Key wo ds: Dip e a; Cecidomyiidae; Cys ipho a; Sonchus; Po ugal; Ibe ia; gall; spa ial dis ibu ion. RESUMEN P ime os egis os pa a Po ugal del induc o de agallas olia es Cys ipho a sonchi (Vallo , 1827) (Dip e a: Cecidomyiidae) y algunas no as sob e su dis ibución en la Península Ibé ica Un p oblema habi ual en los es udios de zoología y ecología es la e aluación pa cial de la dis ibución espacial ac ual de muchas especies, pues subes ima su dis ibución eal al es a basada en los egis os de na u alis as y de museos. Aunque es a limi ación puede se pa cialmen e esuel a po medio de di e en- es he amien as (p.e. modelos de dis ibución de especies), el co ec o uncionamien o de dichas he a- mien as es á condicionado po el núme o de localizaciones disponibles, necesi ando además de un núme o mínimo de ellas pa a que los modelos puedan se alidados. El géne o Cys ipho a Kie e , 1892 (Dip e a: Cecidomyiidae), con es especies en la Península Ibé ica, es á ca ac e izado p incipalmen e po la o mación de agallas en las especies de ce ajas (Sonchus spp.); sin emba go, poco se sabe ace ca de su dis ibución ac ual en Ibe ia. Además, como alo añadido, a ias de las especies que pe enecen a es e géne o son u iliza- das como agen es de lucha de con ol biológico con a las ce ajas in aso as en las egiones del Neá ico y de Aus alasia. Cys ipho a sonchi (Vallo , 1827) es una especie paleá ica cuya p esencia en la Península Ibé ica es aba es ingida has a hoy a cua o ci as en el Es e de la Península y en las Islas Balea es. Se encon a on No as / No es 2 No as / No es G aellsia, 74(1), junio 2018, e068 — ISSN-L: 0367-5041 – h p://dx.doi.o g/10.3989/g aellsia.2017. 74.192 es nue as poblaciones de es a especie en Coimb a (Po ugal cen o), añadiendo una nue a especie a la auna po uguesa. Además, con el obje i o de comple a lo máximo posible su dis ibución, se ealizó una búsqueda sis emá ica en di e en es bases de da os de biodi e sidad. Con esos dos en oques, se es ableció un nue o lími e occiden al del á ea de dis ibución de C. sonchi y se expandió su á ea de dis ibución ac ual en la Península Ibé ica con cinco nue os egis os ( es pa a Po ugal, uno pa a Galicia y uno pa a Andalucía). Palab as cla e: Dip e a; Cecidomyiidae; Cys ipho a; Sonchus; Po ugal; Ibe ia; agalla; dis ibución espacial. Recibido/Recei ed: 14/11/2017; Acep ado/Accep ed: 8/03/2018; Publicado en línea/Published online: 20/04/2018 Cómo ci a es e a ículo/Ci a ion: López-Núñez, F. A., Ma chan e, H. & Ma chan e, E. 2018. Fi s eco d o he lea -gall induc o Cys ipho a sonchi (Vallo , 1827) (Dip e a: Cecidomyiidae) o Po ugal and some no es abou i s Ibe ian dis ibu ion. G aellsia, 74(1): e068. h p://dx.doi.o g/10.3989/g aellsia.2018. 74.192 Copy igh : © 2018 SAM y CSIC. This is an open-access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion 4.0 In e na ional (CC BY 4.0) License. Se e al s udies highligh he impo ance o he Medi e anean basin as one o he hi y- ou biodi- e si y ho spo s in he wo ld (Mi e meie e al., 2004; Fonseca, 2009; Hewi , 2011), p obably because i was a clima ic e ugia du ing he Qua e na y glacial cycles (Rand, 1948). Consequen ly, he auna and lo a o he Ibe ian Peninsula a e qui e well s udied, bu pa adoxically, Fon aine e al. (2012) ema k ha Old Wo ld, and because o ha , Ibe ian Peninsula, can be conside ed as an impo an ese oi o unknown species. Despi e he impo ance o desc ibing new species and imp o ing knowledge on he spa ial dis- ibu ion o exis ing species, hese aspec s a e o en o go en. The spa ial dis ibu ion o se e al species in Old Wo ld is o en only pa ially assessed, based on museum o ama eu s’ eco ds, unde es ima ing he eal dis ibu ion o he species. Cecidomyiidae is he second mos species ich amily o h ead-ho ns (Dip e a: Nema oce a) in he wo ld wi h pa icula impo ance in he Ibe ia whe e 292 species (ou o he o al 6200 epo ed species) occu (Gagné & Jaschho , 2014; Ca les-Tol á, 2002; Sánchez e al., 2012; Sánchez, 2016). This amily is mainly cha ac e ized by he es ablishmen o a highly speci ic ophic ela ionship be ween a ly and a plan species: he induc ion o a gall. This ype o ophic specialism can be conside ed as an in e media e si u- a ion be ween pa asi ism and he bi o y (Red e n & Shi ley, 2011) because he gall is a eac ion o he hos - plan o he o iposi ion by he galle insec in hei inne issues. This eac ion causes he g ow h o an abno mal plan s uc u e ha esul s om hype ophy ollowed by hype plasia o he ege al cells, p o iding a nu i i e issue ha eeds he galle la ae; simul ane- ously, he insec la ae induces a physiological cascade o p omo e he g ow h o he nu i ional issue by he hos -plan (Nie es-Ald ey, 1998). In many cases, he speci ici y o he ela ionship is so high ha he gall is conside ed as he ex ended pheno ype o he induc o genes (S e n, 1995; C espi e al., 1997), allowing pos- sible o iden i y he galle insec only by he p esence o he gall and by i s mo phology. Some species wi hin his amily a e o conce n o ag icul u e because hey a e conside ed pes s o se e al c ops (i.e. Con a inia nas u ii (Kei e , 1888) on b occoli, S enodiplosis so ghicola (Coquille , 1899) on so ghum, Con a inia maculipennis Fel , 1933 on o chids, e c.). On he o he hand, he high speci ici y be ween galle s and hos - plan s suppo s he use o galle s as biological con- ol agen s agains in asi e plan species, dec easing he p obabili y o unwan ed di ec non- a ge e ec s on non- a ge species (Pea son & Callaway, 2003; Thomas e al., 2004; López-Núñez e al., 2017). The genus Cys ipho a Kie e , 1892 belongs o Cecidomyiidae and includes six species in Eu ope, h ee o hose eco ded in Spain: C. sanguinea (B emi, 1847), C. schmid i (Rübsaamen, 1914) and C. sonchi (Vallo , 1827). All membe s o his genus a e gall induc o s on he lea es o se e al species o Cicho ieae (As e aceae) and some o hem we e in oduced in o Nea c ic and Aus alasian Regions as biological con- ol agen s o in oduced As e aceae weeds (Ca les- Tol á, 2002; Skuh a á & Skuh a ý, 2009; Gagné & Jaschho , 2014); o example: C. sonchi and C. a ax- aci (Kie e , 1888) we e in oduced in o Canada o con ol Sonchus a ensis L. and Ta axacum o icinale (L.) Webe ex F.H. Wigg espec i ely; and C. schmid i was in oduced in Aus alia, Cali o nia and A gen ina agains Chond illa juncea L. (Gagné & Jaschho , 2014). The midge C. sonchi is a lea -gall induc o in species o sow- his le (Sonchus a ensis L., S. aspe (L.) Hill, S. ole aceus L., S. ma i imus L. and S. ene imus L.), and in spo adic si ua ions in bulbous hawksbea d (Ae heo hiza bulbosa Cass.) (Peschken, 1982; Peschken e al., 1989). This is he single gall species induced by a midge desc ibed in sow- his le; he gall is a da k ed blo ch wi h abou 5 mm in diame e , loca ed on he lea es. The la - ae eed be ween he uppe and lowe epide mis o he lea . In many cases, one lea can ha bo se - e al blo ch galls, dis ibu ed in ows h oughou he lea leng h. Depending on he season, he la ae can pupa e in he lea (in sp ing gene a ions) o in he No as / No es 3 G aellsia, 74(1), junio 2018, e068 — ISSN-L: 0367-5041 – h p://dx.doi.o g/10.3989/g aellsia.2017. 74.192 g ound (in win e gene a ions); he adul s eme ge and a e ma ing emales lay he eggs on he unde side o ma u e lea es, a oiding he younges and oldes lea es (Peschken, 1982). This species was eleased o he i s ime in Canada, om 1981 o 2008, as a bio- logical con ol agen agains S. a ensis, which was acciden ally in oduced wi h impo ed seeds o od- de , p omo ing losses in c ops p oduc ion (Peschken, 1982). The occu ence o his species is mos ly sca ce, wi h some eco ds o locally abundan , bu i has an Eu o-Sibe ian dis ibu ion, being eco ded in almos 30 Eu opean and in i e Asian coun ies (Peschken, 1982; M. Skuh a á, comm. pe s., 2017). The p esence o C. sonchi in Ibe ian Peninsula is only con i med in Spain (Skuh a á e al., 2006) on h ee locali ies in he Basque Coun y (in 1901), Ca alonia (in 1902) and in Balea ic Islands (in 1997; Fig. 1) (T o e , 1902; Cogolludo, 1921; Skuh a á & Skuh a ý, 2004; Blanes-Dalmau e al., 2017). F om Po ugal he e is only one dubious ci e in Ta a es (1907) pag. 129: “[…] Cecidomyia, p obably new […]” in S. ole a- ceus; bu his ma e ial was no p ese ed and is no a ailable o be con i med. We epo o he i s ime C. sonchi o Po ugal mainland, expanding i s known dis ibu ion o he u - he wes co ne o Eu ope. Th ee popula ions we e spo ed in Coimb a (Po ugal) (Figs. 1-2): (1) López-Núñez, FA, 2017; 40.19868333333333, -8.408333333333333; 10/X/2017; Rua A onso Albuque que, Bai o No on de Ma os, Coimb a, Po ugal; 57 m a.s.l.; be ween 3 and 5 blo ches on lea es o isola ed indi iduals o S. ole aceus in he edges o he s ee sidewalk, (2) López-Núñez, FA, 2017; 40.211288888888895, -8.452769444444444; 10/X/2017; main build- ing o Escola Supe io Ag á ia (ESAC), Ins i u o Poli écnico de Coimb a. Bencan a, Coimb a, Po ugal; 43 m a.s.l.; 6 blo ches on lea es on iso- la e indi idual o S. ole aceus in he le co ne o he pa king and (3) López-Núñez, FA, 2017; 40.216825, -8.45023 8888888888; 10/X/2017; Rua do F eixo s/n, g een- house o ESAC, Ins i u o Poli écnico de Coimb a, Coimb a, Po ugal; 18 m a.s.l.; se e al blo ches on lea es on se e al indi iduals o S. ene imus Fig. 1.— Upda ed dis ibu ion o Cys ipho a sonchi (Vallo , 1827) in Ibe ian Peninsula based on li e a u e, biodi e si y da abases and ield obse a ions du ing he pe iod 1901-2017; some occu ences a e oughly posi ioned due o he lack o accu a e loca ion (see Table 1 o mo e de ails). The inse ame shows a zoom o he occu ences eco ded in Coimb a (Po ugal). Fig. 1.— Dis ibución ac ualizada de Cys ipho a sonchi (Vallo , 1827) en la Península Ibé ica du an e el pe iodo 1901-2017, basada en los egis os en la li e a u a, bases de da os de biodi e sidad y obse aciones de campo; algunas localidades es án oscamen e ubicadas debido a la al a de da os de localización más p ecisos ( e Tabla 1 pa a más de alles). El ecuad o mues a una ampliación de las ci as egis adas en Coimb a (Po ugal). 4 No as / No es G aellsia, 74(1), junio 2018, e068 — ISSN-L: 0367-5041 – h p://dx.doi.o g/10.3989/g aellsia.2017. 74.192 in he open a ea nea he wa e well. Galls we e iden i ied ollowing Dauphin (2012) and Chine y (2013) and con i med o be C. sonchi. Assuming ha he h ee eco ds o C. sonchi in Spain and he new eco ds now con i med in Po ugal we e mos p obably no ep esen a i e o he eal dis ibu ion o he species in he Ibe ian Peninsula, we did an addi ional sea ch o inc ease dis ibu ion eco ds. A sys ema ic sea ch was pe o med h ough he Global Biodi e si y In o ma ion Facili y (GBIF) (www.gbi .o g) and a se o di e en ci izen science biodi e si y da abases: iNa u alis (www.ina u al- is .o g), Na u da a (na u da a.com), Biodi e si y4all (www.biodi e si y4all.o g) and Biodi e sidad Vi ual (BV; www.biodi e sidad i ual.o g). iNa u alis and GBIF a e global biodi e si y da abases, while he o h- e s a e de eloped and ocused in Po ugal (Na u da a and Biodi e si y4all) and in Spain (BV). In hese da a- bases, any egis e ed ci izen can upload a pho og aph o a species and a communi y o specialis s can ei he iden i y he species o alida e he iden i ica ion made by he ci izen. Al hough such ci izen science da abase can ca y some iden i ica ion unce ain y by lacking o specimens o examine (Ga dine e al., 2012), in his case he clea mo phology o he gall and i s hos -plan speci ici y con e a high con idence o he iden i ica- ion based on pho og aphs. Reco ds we e only ound in GBIF and in BV, in o al o eigh mo e eco ds o Spain, wo o hem being a no el y o Spain and he es con ibu ed o ex end i s dis ibu ion a ea (Table 1, Fig. 1A). Concluding, he h ee new popula ions in Po ugal oge he wi h he new eco ds in Spain expand he dis- ibu ion o C. sonchi in he Ibe ian Peninsula, om he no h-wes (A Co uña, Spain) o he wes (Coimb a, Po ugal) and u he sou h (Se ille, Spain). Acknowledgemen s We hank Ma cela Skuh a á o he help and commen s on he manusc ip , and o Ma ia Blanes-Dalmau o he p o ided da a. The au ho s would like o hank he edi o ial commi ee and he wo anonymous e iewe s o hei aluable commen s and sug- ges ions o imp o e he quali y o his sho no e. This esea ch and FLN was suppo ed by FCT and COMPETE/FEDER, h ough p oj- ec “INVADER-IV – INnoVa ing App oaches o De ec in asi e spEcies and biocon Rol agen s” (PTDC/AAG-REC/4896/2014) Fig. 2.— Example o se e al blo ches o Cys ipho a sonchi ( ed a ow) eco ded on a lea o Sonchus ole aceus L. in ESAC. Fig. 2.— Ejemplo de a ias pús ulas de Cys ipho a sonchi ( lecha oja) egis adas en la hoja de Sonchus ole aceus L. en la ESAC. No as / No es 5 G aellsia, 74(1), junio 2018, e068 — ISSN-L: 0367-5041 – h p://dx.doi.o g/10.3989/g aellsia.2017. 74.192 Table 1.— Summa y desc ip ion o he occu ences o Cys ipho a sonchi (Vallo , 1827) in Ibe ian Peninsula. Tabla 1.— Resumen desc ip i o de los egis os de Cys ipho a sonchi (Vallo , 1827) en la Península Ibé ica. Locali y La i ude Longi ude Al i ude (m a.s.l.) Collec ion da e Habi a Re e ences Rua A onso Albuque que, Coimb a, Po ugal 40.19868333333333 -8.408333333333333 57 10/X/2017 Road ma gin New eco d ESAC, main buidling, Bencan a, Coimb a, Po ugal 40.211288888888895 -8.452769444444444 43 10/X/2017 In a ca pa king, be ween spa se na i e o es and ga dens New eco d ESAC, g eenhouse, Rua do F eixo s/n, Coimb a, Po ugal 40.216825 -8.450238888888888 18 10/X/2017 Nea ude al and ga den plan species be ween meadows and o cha ds New eco d San Sebas ian, Spain VIII/1901 T o e (1902); Cogolludo (1921) Ca alonia, Spain VIII/1901 T o e (1902); Cogolludo (1921) Ped albes, Ca alonia, Spain 27/IX/1920 Blanes-Dalmau e al. (2017) Alcúdia, Cas illo Bendina , Mallo ca, Balea ic Islands, Spain 39.546277777777775 2.578044444444444 50–70 19/VI/1997 Spa se o es wi h Pinus halepensis, P. pinea, Pis acia and Ce a onia siliqua Skuh a á & Skuh a ý (2004) Paseo de las delicias, Se ille, Spain 37.37645 −5.9923 8 08/V/2016 Nea he i e BV (2017b) Lé ida, Ca alonia, Spain 08/VII/2013 Py enaic popula ion BV (2017a) A Co uña, Spain 02/VIII/2012 Road ma gin be ween we meadow and o cha ds BV (2017a) Buñola, Mallo ca, Balea ic Islands, Spain 39.69923333333333 2.694841666666667 192 16/VI/2008 Meadow BV (2017a) Mon oliu, Lé ida, Ca alonia, Spain 41.54461111111111 0.6003888888888889 183 11/V/2010 Small d y hill wi h weeds and small sh ubs BV (2017a) Ba celona, Ca alonia, Spain 21/X/2010 U ban ga den BV (2017a) Can Pica o , Mallo ca, Balea ic Islands, Spain 39.753838888888886 3.1585055555555557 24 20/X/2015 GBIF (2017) Son Bosc, Mallo ca, Balea ic Islands, Spain 39°46’20.15”N 3°7’29.73”E 0 19/X/2015 GBIF (2017) 6 No as / No es G aellsia, 74(1), junio 2018, e068 — ISSN-L: 0367-5041 – h p://dx.doi.o g/10.3989/g aellsia.2017. 74.192 Re e ences Blanes-Dalmau, M., Caballe o-López, B. & Pujade-Villa , J., 2017. 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