Arthropod gut symbionts from the Balearic Islands: Majorca and Cabrera. Diversity and biogeography

A h opod gu symbion s om he Balea ic Islands: Majo ca and Cab e a. Di e si y and biogeog aphy by Laia Guà dia Valle1& Se gi San ama ia Uni a de Bo ànica, Dep . Biol. Animal, Biol. Vege al i Ecologia, Facul a de Ciències, Uni e si a Au ònoma de Ba celona (UAB), E-08193 Bella e a, Spain 1Co esponding Au ho : [email p o ec ed] Resumen Guà dia Valle, L. & San ama ia, S. 2009. Simbion es del in es i- no de a ópodos de las islas Balea es de Mallo ca y Cab e a. Di- e sidad y biogeog a ía. Anales Ja d. Bo . Mad id 66S1: 109- 120 (en inglés). El p esen e es udio incluye una ecopilación de odos los da os conce nien es al conocimien o de los icomice os (sensu la o) en las islas Balea es de Mallo ca y Cab e a, incluyendo un ca á- logo de especies y no as sob e la biología, ecología e implicacio- nes biogeog á icas de su insula idad. De las 13 especies ci adas, 10 son nue as pa a las Balea es, incluyendo 4 Mesomyce ozoos, de los cuales 3 Ecc inales (As ep onema gamma i, Ecc inidus lexilis, Pa a aeniella dila a a), 1 Amoebidiales (Pa amoebidium cu um) y 6 Ha pellales (kixckellomyco ina) (Genis ellospo a ho- mo hallica, Ha pella melusinae, Smi ium culise ae, S. simulii, S achylina g andispo a y S . nana); aunque las 3 especies es- an es: Asella ia ligiae (Asllea iales), Lege iomyces a us y S ipe- lla igilans (Ha pellales) ue on ci adas an e io men e, se inclu- yen aquí b e emen e como pa e del ca álogo. Palab as cla e: biogeog a ía, simbiosis, hongos in es inales, insula idad, Kickxellomyco in, Mesomyce ozoa, axonomía, Zy- gomyco a. Anales del Ja dín Bo ánico de Mad id Vol. 66S1: 109-120, 2009 ISSN: 0211-1322 doi: 10.3989/ajbm.2216 In oduc ion The ichomyce es a e euka io ic, ilamen ous a h opod- ela ed obliga e gu symbion s. This g ouping comp ises o ganisms ha ha e pa allelly e ol ed es ablishing hei ecological niche in he a h opod gu whe e hey nou ish wi h he ejec ed ood pa icles ha pass h ough he in es ine o be ex- pulsed h ough he anus (Lich wa d & al., 2001; Mis- a, 2001). The s ic limi a ions o he gu a mosphe e ha e shaped a con e gen mo phology, whe e he op- ions a e es ic ed by he space, he mol ing cycle o he hos and he physical-chemical condi ions o he en i- onmen . This mo phologic con e gence has been e- sponsible o he adi ional concep ion o he Class coun ing ou O de s. Today, we unde s and he i- chomyce es as an ecologically cohe en g oup (Lich - wa d , 1986), al hough being mani es ly polyphyle ic Abs ac Guà dia Valle, L. & San ama ia, S. 2009. A h opod gu sym- bion s om he Balea ic Islands: Majo ca and Cab e a. Di e si y and biogeog aphy. Anales Ja d. Bo . Mad id 66S1: 109-120. This s udy includes a ca alogue wi h all he cu en da a con- ce ning he p esence o ichomyce es (sensu la o) in Majo ca and Cab e a, as well as in o ma ion on he biology, ecology and biogeog aphic implica ions o he insula i y o each axon o hese a h opod-gu symbion s. O he 13 species he e epo ed, 10 a e new o he Balea ic Islands, including 4 Mesomyce o- zoan, o which 3 Ecc inales (As ep onema gamma i, Ecc inidus lexilis, Pa a aeniella dila a a), 1 Amoebidiales (Pa amoebidium cu um) and 6 kixckellomyco ina Ha pellales (Genis ellospo a homo hallica, Ha pella melusinae, Smi ium culise ae, S. simulii, S achylina g andispo a and S . nana); he addi ional 3 we e p e- iously epo ed elsewhe e: Asella ia ligiae (Asllea iales), Lege i- omyces a us and S ipella igilans (Ha pellales), bu a e he e in- cluded as indissoluble pa o he p esen Balea ic ca alogue. All axa a e commen ed, illus a ed and hei biogeog aphic impli- ca ions a e discussed. Keywo ds: biogeog aphy, symbiosis, gu ungi, insula i y, Kick- xellomyco ina, Mesomyce ozoa, axonomy, Zygomyco a. 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 109 (Benny & O’Donnell, 2000; Us ino a & al., 2000; Lu zoni & al., 2004; Tanabe & al., 2004; Adl & al., 2005; Ca a o, 2005; Whi e & al., 2006a), wi h wo o de s, he Ecc inales and Amoebidiales cu en ly placed wi hin he P o ozoan Mesomyce ozoa (Benny & O’Donnell, 2000; Ca a o, 2005), plus Ha pellales and Asella iales, placed wi hin he zygomico an Kick- xellomyco ina (Hibbe & al., 2007). Anyway, his o i- cal and p ac ical mo i a ions p omo e hei main e- nance wi hin ichomyce es (wi h “ ” o designa e his polyphyle ic condi ion o “sensu la o” ea men ). The in ec i e capaci y o Ha pellales, he mos di- e se o de o gu ungi, is es ic ed o he la al phas- es o he a h opod hos s usually associa ed in a com- mensalis ic ela ionship. Howe e , some dip e ans can ca y ungic cys s in he o a ian eggs o emale adul s (Labey ie & al., 1996; Moss & Descals, 1986; Yeboah & al., 1984; Whi e & al., 2006b). Du ing his phase, gu ungi ope a e as pa asi es, since he ep oduc i e capaci y o he in ec ed emale (Simuliidae and Chi- onomidae) is a ec ed by he ina bili y o gene a e o - sp ing om ungal-occupied eggs. A e being o ipo - si ed, ungal cys s (o Ha pella melusinae Lége & Du- boscq and Genis ellospo a homo hallica Lich w.) will ge mina e o in ec new la al hos s (Labey ie & al., 1996; Moss & Descals, 1986; Yeboah & al., 1984). Since he dispe si e capaci y o gu - ungi is mainly e- s ic ed o he dispe si e capaci y o hei hos s, co o- logical s udies ega ding he p esence o his o gan- isms in isola ed en i onmen s as islands, is a good ap- p oach o in e dispe sal and specia ion p ocesses. P e iously published da a abou Balea ic icho - myce e include he ci a ion o h ee species (Valle, 2006; Valle & San ama ia, 2004; Valle, 2007) which a e also ecompiled he e (as a b ie no e in axa lis ) as pa o he ca alogue o Majo ca. Be o e hese s u- dies, knowledge o ichomyce es was inexis en o he whole Medi e anean Islands. Ma e ials and Me hods P ospec ed a ea The Balea ic a chipelago is placed in on o he Va- lencian and Ca alan coas (Eas e n Spain) and in- cludes h ee main islands: Majo ca, Mino ca and Ibiza, he o me being he la ge one (3640 km2); Fo men e a (nex o Ibiza) and Cab e a (nex o Ma- jo ca) a e smalle inhabi ed islands (nowadays e- s ic ed o he Na ional Na u al Pa k wo ke s and isi o s in he case o Cab e a), ha oge he wi h ano- he 250 isle s con o m he whole a chipelago. The no h coas o Majo ca is sepa a ed abou 180 km om Ba celona seapo . The Balea ic a chipelago L. Guà dia Valle & S. San ama ia comp ises he mos isola ed islands in he Occiden al Medi e anean. The p esen s udy is cen ed in Ma- jo ca, wi h a ichomyce e ci a ion om he mino is- land o Cab e a. The subs a e is p edominan ly cal- ca eous limes one o bo h p ospec ed islands. The highes poin in Majo ca is Puig Majo Peak (1445 m), se led in cen al zone o he moun ain idge called “Se a de T amun ana”, which ex ends h ough a lon- gi ude o 90 km nex o he no he n coas . Mos o he i e s and s eams p esen an i egula low cycle, and a e o en supe icially d ied du ing he Medi e - anean summe . Du ing hese appa en ly d y seasons, s eams main ain a ea ic ac i i y which may p o ide he equi ed humidi y o he subsis ence o eshwa- e -dependan in e eb a es. Expe imen al me hodology The s udy o a h opod- ela ed gu symbion s e- qui es a combina ion o bo h en omological and mi- c obiological me hodology. The en omologic me hods ha e o be applied when collec ing and iden i ying he hos s, while a mic obiologis p o ile will be necessa y o he ex ac ion, p ocessing and s udy o icho - myce e inquilines. The me hodology is explained in de ail in Lich wa d & al., 2001. Fo collec ing he aqua ic hos s o Ha pellales, mos ly imma u e s ages o Plecop e a, Epheme op e a, Nema oce an Dip e a (mainly Simuliidae, Chi onomidae, Culicidae, Thau- maleidae and Ce a opogonidae), T ichop e a, and adul aqua ic Isopodes (mos ly wi h Asella ian and Ec- c inid inquilines) limnology ne s a e equi ed. When hese hos s a e ound in lo ic habi a s, he subs a e, ocks and ege a ion a e gen ly mo ed o inco po a e he a h opods in o he low o be e ained by he ne , which is placed downs eam. In len ic habi a s he ne has o be used mo e dynamically o cap u e he swim- ming hos s and hose a ached o di e en subs a es. The po en ial hos s a e selec ed using o ceps and pipe es and placed in o ja s o plas ic esealable bags o be anspo ed o he lab, keeping he hos s ali e in- side an ice-coole . Te es ial hos s o Ecc inales and Asella iales (sp ing ails, isopods and millipedes) a e di- ec ly picked by hand, using o ceps, en omologic aspi- a o s and ja s. All hos s may be e be examined ali e, o eco e he gu symbion s in he bes condi ions. The hos s a e dissec ed unde a s e eobinocula mic oscope wi h he help o ine o ceps and needles, cleaned and sepa a ed om he gu whe e he ichomyce es a e a - ached (Lich wa d & al., 2001). Once he symbion s a e sepa a ed and se led in a clean slide wi h wa e , can be co e ed and obse ed in he scope o iden i y he ichomyce e specimen. Pho og aphs we e aken om wa e -moun ed slides and lac ophenol-co on- 110 Anales del Ja dín Bo ánico de Mad id 66S1: 109-120, 2009. ISSN: 0211-1322. doi: 10.3989/ajbm. 2216 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 110 blue ixed slides, wi h an analogical came a adap ed o Zeiss Hena al compound scope. Resul s New eco ds o he Balea ic Islands The s udy o ichomyce es in Majo ca and Cab e a has p o ided ele en axa o which 8 a e new o he Balea ic Islands. Among he dissec ed a h opods, he p e alence o gu symbion s was e y low, especially in he case o Ha pellales, wi h mos di e si y ound in aqua ic Dip e ans. The pe cen age o in ec ed hos s (coun ing aqua ic and e es ial a h opods) was 3%. We expose i s ly he lis wi h commen s on he new Majo can ichomyce es eco ds. O. Ha pellales Genis ellospo a homo hallica Lich w., Mycologia 64: 167. 1972 Habi a . In he pe i ophic ma ix o aqua ic Si - muliidae (Dip e a) la ae. Known dis ibu ion. Spain, England, USA, Pue o Rico, Cos a Rica, Chile and A gen ina. Ma e ial examined SPAIN. Mallo ca:Valldemossa (To en d’A all), 31SDD69 [E2º37’30” N39º42’25”], p epa ed om Simulium sp., 3-VIII- 2007, mic oscope slides BCB-T 1976-1979. This species was epo ed om he Ibe ian Penin- sula (Gi bal & San ama ia, 1998; Valle, 2004), al- hough emained unknown om any Medi e anean island. The specimens collec ed show ypical cha ac- e is ics in ichospo es [25-38 × 9-11 µm (x –= 31 × 9.7 µm)], wi h 6 appendages. The species was o igina- lly desc ibed om he USA (Lich wa d , 1972); od- dly, i has no been epo ed o F ance. Genis ellospo- a homo hallica is no common in Majo ca, al hough is a wide-sp ead species in many di e en egions, being one o he mo e cha ac e is ic species om Simuliidae hos s, e en in he neighbo Peninsula. Ha pella melusinae Lége & Duboscq, Comp . Rend. Hebd. Acad. Sci. Pa is 188: 951. 1929 (Figs. 1-5) Habi a . In he pe i ophic ma ix o aqua ic Simu - liidae (Dip e a) la ae. Known dis ibu ion. A menia, China, Dominican Republic (unpublished), F ance, India, Japan, Mexi- co (unpublished), New Zealand, No way, Pue o Rico, Spain, USA. Ma e ial examined SPAIN. Mallo ca: Valldemossa (To en d’A all), 31SDD69 Balea ic ichomyce es [E2º37’30” N39º42’25”], p epa ed om Simulium sp. la ae, 29-V- 2006, mic oscope slides BCB-T 1817-1819. Espo les, To en d’Es- po les, 31SDD69 [E2º37’30” N39º42’25”], p epa ed om Simu - lium sp. la ae, 5-VI-2006, wi hou numbe . This p obably a cosmopoli an species, equen ly p esen in mos aqua ic en i onmen s whe e black lies (Simuliidae) a e a ailable, li ing a ached o hei midgu pe i h ophic ma ix. Among he species o he genus, H. melusinae is he mos equen ly epo ed, anging om he Ca ibbean (Whi e & al., 2000) o he Caucasus (Nelde & al., 2005), wi h ecen no ices o i om he Rocky Moun ains (Whi e & al., 2006c). I was o iginally desc ibed om F ench dip e ans (Lége & Duboscq, 1929) and epo ed again in F ance by di- e se au ho s (Lége & Gau hie , 1935; Manie , 1950, 1970; Tuze & Manie , 1955). The species was ob- se ed in No way (Whi e & Lich wa d , 2004) and is known om he con inen al Spain (San ama ia & Gi - bal, 1998), whe e he species has a high p e alence as- socia ed wi h i s hos . All s udied specimens a e in con o mi y wi h he desc ip ion o H. melusinae,a species ypically a iable in he spo e size [60-155 × 4- 10 µm (x –= 87 × 7 µm) in ou specimens] and shape, om coiled (Figs. 2, 4-5) o almos s aigh . The key cha ac e ha allows i s iden i ica ion is he hold as cell (small, discoid in he p esen species), ha di e - en ia es i om o he species o Ha pella. Smi ium culise ae Lich w., Ame . J. Bo . 51: 836. 1964 (Fig. 8) = Rube ella inopina a Manie , Rioux & Whisle , Vie e Milieu 12: 167. 1961 [nom. in al.] ⬅Smi ium inopina um (Manie , Rioux & Whisle ) Manie , Ann. Sci. Na . Bo . Pa is 10: 565. 1970 Habi a . In he hindgu lining o aqua ic Culicidae (Nema oce a, Dip e a) la ae. Known dis ibu ion. Cosmopoli an, including: F ance, Spain, Aus alia, New Zealand, Japan, USA, A gen ina, B azil. Ma e ial examined SPAIN. Mallo ca: Esco ca, Mo i x s eam, 31SDD91 [E2º55’00” N39º53’10”], p epa ed om Culicis sp. la ae, 27-VI- 2003, mic oscope slides BCBT 1804-1806. This is a cosmopoli an species ecod ed om USA, B azil, A gen ina, Aus alia, New Zealand, F ance, Japan (Lich wa d & al., 2001), and con inen al Spain (San ama ia & Gi bal, 1997). The species was o igi- nally epo ed om Culicidae (mosqui o) la ae, bu he e a e e e ences indica ing he p esence o he species wi hin Simuliidae and Ce a opogonidae (Lich - 111 Anales del Ja dín Bo ánico de Mad id 66S1: 109-120, 2009. ISSN: 0211-1322. doi: 10.3989/ajbm. 2216 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 111 wa d , 1986). The species is cha ac e ized by he o a e- ellipsoidal ichospo es [14-17.5 × 2.5-4 µm (x –= 16.2 × 3.3 µm) in ou samples] wi h a sho (ca. 1.5-2 µm) ou - la ed colla . The whole hallus can become e ile, wi h he delimi a ion o gene a i e cells h oughou all he b anches and e en main axial hypha. Smi ium culise- ae can be seg ega ed om S. culicis by ichospo e mo phology, he o me ha ing he la ges diame e be- low he middle egion o he spo e, he la e app oxi- ma ely in he middle egion (Manie , 1970). Smi ium simulii Lich w., Ame . J. Bo . 51: 836. 1964 (Fig. 9) ⬅Rube ella simulii Manie , Ann. Sci. Na ., Bo ., Pa- is 4: 737. 1963 [nom. in al.] Habi a . In he hindgu lining o aqua ic Chi ono- midae, Simuliidae, and a ely Culicidae and Tipulidae (Nema oce a, Dip e a) la ae. Known dis ibu ion. Cosmopoli an. Ma e ial examined SPAIN. Mallo ca: Randa, oun ain and pool, 31S DD97 [E2º55’00” N39º31’10”], p epa ed om Chi onomidae la ae, 9- IV-2006, mic oscope slides BCB-T 1919-1823. This species, ini ially named Rube ella simuilii Manie (nom. in al), was desc ibed om F ance in Simuliidae la ae (Manie , 1963). R.W. Lich wa d obse ed la e ha i was in ac a species o he genus Smi ium (Lich wa d , 1964), epo ed om dis an locali ies o he globe: om Japan, whe e i was ob- se ed in Simuliidae and Chi onomidae (Lich wa d & al., 1987), om Aus alia and New Zealand in en- demic Aus osimulium (Lich wa d & Williams, 1992), om No way (Whi e & al., 2004) and om con inen al Spain (Gi bal & San ama ia, 1998). The p e alence o he species is lowe han expec ed; he Balea ic specimens we e ob ained om Culicidae and Chi onomidae la ae. These specimens had elonga e- ellipsoidal ichospo es measu ing 19-27 × 5-5.5 µm (x –= 23.2 × 5.3 µm), wi h a colla 1.5-3.5 × 2-3 µm (x – =2.6 × 2.4 µm) o pa allel o con e gen ma gins. S achylina g andispo a Lich w., Mycologia 64: 193. 1972 (Fig. 6) Habi a . In he pe i ophic ma ix o aqua ic Chi- onomidae (Dip e a) la ae. Known dis ibu ion. England, Spain, Sweden, Aus- alia, Hawaii, New Zealand, India, USA. Ma e ial examined SPAIN. Mallo ca: Randa, Foun ain and s eam, 31S DD97 [E2º55’00” N39º31’10”], p epa ed om he hindgu lining o Diamesiinae la ae (Dip e a: Chi onomidae), 9-IV-2006, mic o- scope slides BCB-T 1819-1823. L. Guà dia Valle & S. San ama ia This cosmopoli an species associa ed wi h he di- ges i e ac o Chi onomidae (Lich wa d & al., 2001), is epo ed om di e se Ibe ian locali ies (Valle, 2007), om endemic species o Chi onomidae in New Zealand and Hawaii (Lich wa d , 1986), showing i s abili y o long-dis ance dispe sal and adap abili y o new en i onmen s. Some o he spe - cimens examined had sligh ly smalle ichospo es [27-42 × 6-8 µm (x –= 35 × 7 µm)] han usual. Ac ual- ly, he species shows me ic a ia ions, especially e- ga ding ichospo e leng h (Lich wa d & al., 2001). None heless, he shape o ichospo es, colla [2.5-3.5 × ca. 2 µm in ou samples], appendage and basal cell (Fig. 6) a e e y cons an e en among di e en popu- la ions. S achylina nana Lich w., Myco axon 19: 529. 1984 (Fig. 7) Habi a . In he pe i ophic ma ix o aqua ic Chi- onomidae (Dip e a) la ae. Known dis ibu ion. F ance, Spain, Sweden, Japan, New Zealand, Cos a Rica, USA. Ma e ial examined SPAIN. Mallo ca: Valldemossa, o en de Valldemossa (To - en d’A all), 31SDD69 [E2º37’30” N39º42’25”], p epa ed om he hindgu lining o Diamesiinae la ae (Dip e a: Chi onomidae), 29-V-2003, mic oscope slides BCB-T 1822-1823. Species desc ibed om ma e ial ob ained in F ench midges (Chi onomidae) (Lich wa d , 1984). I has been epo ed om Japan (Lich wa d & al., 1987), New Zealand (Williams & Lich wa d , 1990), Cos a Rica (Lich wa d , 1997), Sweden (Lich wa d , 1984) and di e se locali ies o USA (Lich wa d , 1984). San- ama ia & Gi bal ( 1997) also eco ded i om con i- nen al Spain. S achylina nana has a ela i ely sho and usi o m hallus, which gi es ise o a maximum o 4 ichospo es. Al hough he ichospo es o his species do no ha e an appa en colla , clea eminiscences o he gene a i e cell can be obse ed a he p oximal end o he spo e. The appendage is wide a he base and a enua es o he ex eme. We ha e widened he ichospo e leng h ange, wi h some smalle i- chospo es [18-35 × 6-8.5 µm (x –= 25.2 × 7.6 µm)]. One specimen showed a pa icula ly small hallus which esembles S . minima M.C. Williams & Lich w.; his species has a basal cell ha pene a ed he pe i h ophic ma ix (Williams & Lich wa d , 1990), and he specimen in slide T 1822 seems o ha e a sim- ila base. Anyway, spo e mo phology is mo e p oximal o S . nana so i ’s p obable ha he pa icula basal cell may be an anomaly, as i is no e y clea i s pene a- ions o he ma ix. 112 Anales del Ja dín Bo ánico de Mad id 66S1: 109-120, 2009. ISSN: 0211-1322. doi: 10.3989/ajbm. 2216 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 112 Balea ic ichomyce es 113 Anales del Ja dín Bo ánico de Mad id 66S1: 109-120, 2009. ISSN: 0211-1322. doi: 10.3989/ajbm. 2216 Figs.1-5. Ha pella melusinae. 1. Gene a i e cell showing he coiled ichospo e appendages inside (a ow). 2. Released icho- spo e wi h appendages (a ow). 3. Basal po ion o he halli wi h he ypical hold as (a ow). 4. Coiled ichospo e. 5. Di e se halli wi hin he simulid pe i ophic ma ix, he a ows poin ing a conjuga ion. Fig. 6. S achylina g andispo a. Thalli wi h ichospo es (a owheads) and basal cell (a ow). Fig. 7. S achylina nana. Ma u e hallus wi h ichospo es. Scale ba s = 25 µm, Figs. 1-4,7; 50 µm, Figs. 5, 6. 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 113 O. Ecc inales (Mesomyce ozoea) Fam. ECCRINACEAE As ep onema gamma i (Lége & Duboscq) Manie , Ann. Sci. Na . Bo . Pa is 5: 767. 1964 (Fig. 10) ⬅Ecc inella gamma i Lége & Duboscq, A ch. Zoo. Exp. Gen. 75: 284. 1933 Habi a . A ached o he he hindgu lining o Gam- ma us sp. (Gamma idae, C us acea). Known dis ibu ion. Spain; F ance, Ge many, Eng- land, USA. Ma e ial examined SPAIN. Mallo ca: Pollença, S’Albu e e a, o en 31SEE01 [E3º05’20” N39º51’30”], p epa ed om he hindgu lining o Gamma us sp., 25-V-2003, mic oscope slides BCB-T 1795-1796. This is he i s epo o an Ecc inal species om he Balea ic Islands. The specimens collec ed p o i- ded ma e ial wi h all he spo e ypes. This Ecc inid was epo ed om F ance (Lége & Duboscq, 1906, 1933; Poisson, 1929; Manie , 1950), Ge many (Maessen, 1955), England (Moss, 1972) and USA (Lich wa d , 1973). Lége & Duboscq ga e he name Ecc inella gamma i (basionym) o his axon (Lége & Duboscq, 1906, 1933), bu he au ho s did no p o- ide a desc ip ion un il 1933. Finally, Manie changed he name o As ep onema gamma i Manie (1964) based on spo angiospo e and hallial cha ac e s. The specimens o Majo ca we e ound in Gamma us. Mi- c o halli, a a e s age o his species (Manie , 1964, 1970; Lich wa d , 1986), we e obse ed in specimens L. Guà dia Valle & S. San ama ia o A. gamma i. These hin halli (300 × 1.5-2 µm) ge - mina e appa en ly om seconda y spo angiospo es (2-8 nuclea ed, cylind ical, 25-50 × 8-10 µm) p o- duced by mac o halli, 1-2 mm × 8-18 µm (x –= 1.4 × 15.2 µm), a leas i was deduced om a ailable ma e- ial. Mo he cell o hese mic o halli is pe sis en (as in mac o halli) un il iso diame ic mic ospo es (2 × 2 µm, uninuclea ed) a e o med. The samples ob ained in Majo can show consis en spo e mo phology, coinci- den wi h he o iginal desc ip ion o he species. The uni o mi y is ema kable also in p ima y in es a ions spo es, 22-32 × 7-10 µm (x –= 25.8 × 8.4 µm), 4-nuclea - ed, o al wi h pola appendages. Size a ia ion is mo e equen in seconda y in es a ion spo es. Manie (1950, 1970) desc ibed he p esence o o al spo es longe han ypical p ima y in es a ion spo es, no obliquely a anged bu longi udinally disposed in he hallus. Howe e , we ha e no obse ed hese spo es, conside ed esis an s uc u es (Manie , 1950, 1964, 1970; Lich wa d , 1986). Ecc inidus lexilis (Lége & Duboscq) Manie , Ann. Sci. Na . Bo . Pa is 10: 469. 1970 (Fig. 11) ⬅Ecc ina lexilis Lége & Duboscq, Comp . Rend. Hebd. Acad. Sci. Pa is 142: 590. 1906 Habi a . A ached o he hindgu lining o e es i- al Glome is sp. (Glome idae, Diplopoda). Known dis ibu ion. F ance, Spain. Ma e ial examined SPAIN. Mallo ca: A à, ma i ime slopes o Talaia Mo eia, 31SED39 [E3º21’35” N39º46’40”], p epa ed om he hindgu 114 Anales del Ja dín Bo ánico de Mad id 66S1: 109-120, 2009. ISSN: 0211-1322. doi: 10.3989/ajbm. 2216 Fig. 8. Smi ium culise ae. Thalli wi h ichospo es. Fig. 9. Smi ium simulii. Thalli wi h ichospo es. Scale ba s = 25 µm. 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 114 lining o e es ial Glome is sp. (My iapoda), 4-VI-2001, mic o- scope slides BCB-T 1185-1187. This species may be dis ibu ed h oughou mos Balea ic en i onmen s, ollowing he dis ibu ion o i s hos Glome idae (Millipede). We couldn’ obse e he o ma ion o p ima y in es a ion spo angiospo es, o esis an spo es, which usually a ise jus be o e he hos s a s he mol ing p ocess (Lich wa d & al., 2001), e en we kep some o he hos s in a e a ium un il hey s a ed o mol , and he exu iae we e exam- ined wi h no success. None heless, we obse ed sec- onda y in es a ion spo angiospo es (10-22 µm diame- e ) which p o ide enough da a o a consis en iden i- ica ion, wi h ypically oblique o pe pendicula sep a inside he hallial cell wall, bo h kinds o sep a wi hin he same indi idual. Hold as mo phology, cha ac e- is ically wi h a columna sec ion (17-35 × 13-17 µm) (x –= 29.7 × 15.2 µm), expanded in he p oximal end in o a basal disc 16-25 µm diame e , is also o axo- nomic alue. The b eak up o he hold as disc du ing he manipula ion o he gu is no a e, and he disc can emain a ached o he chi inous lining, showing i s igh adhesion. Thalli we e a ached mos ly a he an e io sec ion o he hindgu lining, nea he midgu sec ion. Fam. PARATAENIELLACEAE Pa a aeniella dila a a Poisson, A ch. Zool. Exp. Gén. 69: 205. 1929 (Fig. 12) ⬅Pa a aeniella binuclea a Poisson, A ch. Zool. Exp. Gén. 69: 207. 1929 Habi a . A ached o he hindgu lining o e es i- al isopoda Oniscidae. Known dis ibu ion. Spain, Ge many, F ance, USA. Ma e ial examined SPAIN. Mallo ca: Palma, Bell e Cas le Pa k, 31S DD78 [E2º37’35” N39º33’50”], p epa ed om A madillo spp., 18-IV- 2001, mic oscope slides [T 0695-0698]; 4-VI-2003, mic oscope slide BCB-T 0684-0685. Cab e a: Cap de Llebeig, 31SDD93 [E2º55’08” N39º09’30”], p epa ed om Po cellio sp., 14-VIII- 2004, mic oscope slide BCB-T 1913-1914. In he o iginal publica ion, Poisson epo ed h ee di e en species: P. dila a a in he gu o A madillo o - icinalis, P. in e media wi hin T ichoniscus oseus and P. binuclea a in Po cellio lae is hindgu (Poisson, 1929). La e on, di e se au ho s conside ed ha di - e ences in hese h ee species we e no signi ican and Manie (1970) synonymized P. in e media wi h P. dila a a. Lich wa d (1986) also included P. binuclea a in o his axon. The scan and a iable cha ac e s in he species do no allow a na ow desc ip ion, pa ic- ula ly ega ding spo e ea u es, widely inconsis en Balea ic ichomyce es e en wi hin a sole indi idual and phase o he li e cy- cle. Pa a aeniella dila a a in ou collec ions om A - madillidio spp. ha e seconda y in es a ion spo an- giospo es usually long and cylind ical, (20)40-50 × 12- 13 µm (x –= 41.4 × 12.6 µm), 2-5 nuclea ed, o igina ed om long halli, 300 × (8)12-14 µm, wi h a disc e dis- coid hold as . The same halli also o med uninuclea - ed spo angiospo es (15-25 µm long), disposed in a single se ies. Ano he hallial ype, 100-230 × (12)22- 28 µm (x –= 196.3 × 24.2 µm), was p oducing p ima y in es a ion spo angiospo es, 1- o 2- nuclea ed ex- uded by he apex o he holoca pic halli. This species has been also epo ed om Ge many (Schee , 1976) and USA (Lich wa d , 1986). O. Amoebidiales (Mesomyce ozoa) As in he case o he Ecc inales, no ep esen a i es o his o de we e p e iously epo ed om any Medi e - anean Island. We ound di e se mo pho ypes, p oba- bly all belonging o he species Pa amoebidium cu um. This species was ound in di e se may ly hos s and also in black lies, a ached o he hindgu lining. Pa amoe- bidium spp. a e no species-speci ic and mos o hem ha e a cosmopoli an dis ibu ion. I was p esen in al- mos all he explo ed locali ies. P e iously epo ed species om he Balea ic Islands Among he p e iously epo ed species, we include he e a b ie lis o h ee axa, o which he ange dis- ibu ion in Majo ca is ac ualized. Fo u he in o - ma ion abou hese species, as well as o illus a ions, check he bibliog aphic e e ences. O. Ha pellales Lege iomyces a us Lich w. & M.C. Williams, Canad. J. Bo . 71: 1109. 1993. Habi a . In he hindgu linig o aqua ic Caenis luc- uosa (Caenidae, Epheme op e a). Known dis ibu ion. Aus alia, Tasmania, Spain. Ma e ial examined SPAIN. Mallo ca: Sólle , Ba anc de Binia aix (Cases de L’O e), 31SDE70 [E2º45’40” N39º45’50”], p epa ed om Caenis luc uosa la ae, 27-V-2003, mic oscope slides BCB-T 1807-1810. Valldemossa, To en de Valldemossa, p epa ed om Caenis luc u- osa la ae, 30-V-2003, mic oscope slides BCB-T 1813-1816. This species was p e iously epo ed om Majo ca (Valle & San ama ia, 2004). The species was o iginal- ly desc ibed om Aus alia, in an endemic Caenidae (Tasmanocoenis) (Williams & Lich wa d , 1993). In Majo ca he species was ound in he hindgu o Cae- 115 Anales del Ja dín Bo ánico de Mad id 66S1: 109-120, 2009. ISSN: 0211-1322. doi: 10.3989/ajbm. 2216 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 115 L. Guà dia Valle & S. San ama ia116 Anales del Ja dín Bo ánico de Mad id 66S1: 109-120, 2009. ISSN: 0211-1322. doi: 10.3989/ajbm. 2216 Figs. 10-12. Ecc inales. 10. As ep onema gamma i: A, ma u e hallus p oducing seconda y spo angiospo es (2ºsp), some o hem ha e ex uded he con en and appea like emp y cells (ec); B-D, di e se halli p oducing p ima y spo angiospo es (1ºsp) wi h pola appendages (ap); C, D, imma u e o ms. 11. Ecc inidus lexilis: A-C, di e se halli showing he basal cell; h, hold as ; gl, gu lining. 12. Pa a aeniella dila a a: A, hallus wi h uninuclea e spo angiospo es; B, Thalli p oducing p ima y spo angiospo es (1ºsp); C, ma u e hallus p oducing seconda y spo angiospo es (2ºsp). Scale ba s = 50 µm. 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 116 nis luc uosa, a Medi e anean wide-sp ead may ly (Valle & San ama ia, 2004). S ipella igilans Lége & Gau hie , Comp . Rend. Hebd. Acad. Sci. Pa is 194: 2263. 1932 Habi a . In he hindgu lining o aqua ic Simuliidae (Nema oce a, Dip e a) la ae. Known dis ibu ion. F ance, England and Spain. Ma e ial examined SPAIN. Mallo ca: San a Ma ia del Camí, o en de Coaneg e, 31SDD79, p epa ed om Simulium sp, 27-V-2003, mic oscope slide BCB-T 1802. Sólle , Binia aix, o en de l’O e, 31SDE70, p epa ed om Simuliidae, 29-V-2003, mic oscope slides BCB- T 1811-1812. Valldemossa, o en de Valldemossa (To en d’A all), 31SDD69 [E2º37’30” N39º42’25”], p epa ed om Simulium sp, 30-V-2003, mic oscope slides BCB-T 1817-1821, BCB-T 1825. Puigpunyen , Sa Rie a, 31SDD58 [E2º32’25” N39º36’50”], p epa ed om P osimulium sp., 13-IV-2006, mic o- scope slides BCB-T 1927. S ipella igilans was o iginally desc ibed om he F ench Alps in he hindgu o Simuliidae, oge he wi h he p o ozoan Pa amoebidium sp. (Lége & Gau- hie , 1932). This species was also epo ed om he Balea ic Islands (Valle, 2007), and he specimens col- lec ed om Majo ca show basically he same cha ac- e is ics as o o he con inen al Eu opean specimens. O. Asella iales Asella ia ligiae Tuze & Manie ex Manie , Ann. Sci. Na . Bo . Pa is 9: 93. 1968 ⬅Asella ia ligiae Tuze & Manie , Ann. Sci. Na . Zool. Pa is 12: 15-23. 1950 [nom. in al.] Habi a . In he hindgu lining o ma ine (sea-sho e zone) Ligia i alica (Isopoda, Aseliidae). Known dis ibu ion. Cosmopoli an. Ma e ial examined SPAIN. Mallo ca: Pollença, S’Albu e e a, 31SEE01 [E3º05’20” N39º51’30”], p epa ed om Ligia i alica, 25-V-2003, mic oscope slides BCB-T 1797-1798. Species p e iously epo ed om he Balea ic Is- lands, in he hindgu lining o he sea-sho e isopod Ligia i alica Fab . (Ligidae) (Valle, 2006). The species is wo ld-wide dis ibu ed as mos ma ine gu ungi in- habi ing cosmopoli an hos s. Discussion Among he species epo ed in his p elimina y s udy, i ’s ema kable he p e alence o Ha pellales as- socia ed o Nema oce an (lowe Dip e ans) hos s o he amilies Simuliidae (black- lies), Chi onomidae (midges and blood-wo ms) and Culicidae (mosqui- Balea ic ichomyce es oes). In ac , a sole ha pellid species, Lege iomy - ces a us, was epo ed om a non-dip e an hos , in Caenis luc uosa (Epheme op e a: Caenidae), which is widely dispe sed in Eu ope and No h A ica (Lau asian-Godwanan dis ibu ion; Jacob, 2003). None heless, di e se specimens o may lies (Ephe me - op e a: Bae idae and Caenidae) and s one lies (Ple- cop e a: Leuc idae) we e analyzed in di e en low- land and upland locali ies, showing no ichomyce es in hei gu s. Cu en ly, some wide-sp ead Hola c ic species common in Peninsula locali ies (Valle, 2004), such as Lege iomyces amosus Pouza (in Bae idae), o Simuliomyces mic ospo us Lich w. (bo h in Simulii - dae) ha e no been obse ed om Majo ca, al hough hei hos s a e common in he explo ed Balea ic s eams. All he specimens o he p esen ca alogue can be conside ed among cha ac e is ically wide- sp ead species (a leas wi h Hola c ic dis ibu ion), excep o he case o S ipella igilans, appa en ly e- s ic ed o Wes e n Eu ope (F ance, England, Ibe ian Peninsula and Balea ic Islands), and Lege iomyces a us which shows an Ibe o-Balea ic and Aus alian disjunc dis ibu ion (Williams & Lich wa d , 1993; Valle & San ama ia, 2004). This species was desc ibed om Aus alia, in he diges i e ac o he endemic Caenidae Tasmanocoenis (Williams & Lich wa d , 1993). The dis ibu ion o he species has o be con- side ed cau iously o he scan da a abou i- chomyce es in as egions, showing his appa en ly dis up ed occupancy, when he species is p obably mo e h oughou dis ibu ed (Valle & San ama ia, 2004). The low p e alence o Balea ic Ha pellales as- socia e o Epheme op e a and Plecop e a (compa ed o he neighbou con inen ) may be explained by he low agili y o his insec s added o he absence o gu ungi diaspo es anspo ed by he lying adul s, con- ining he in ec i e capaci y o he ungus o he nymphal phases o he hos s. Then, i an ancien in- ec ion o Ha pellales was no se led wi hin he o igi- na y en omo auna which was aisled abou 150 hou- sand yea s ago (when he Ti enic beaches we e shaped and he ising Medi e anean Sea le el aisled he Balea ic a chipelago), he p obabili y o pos e io Ha pellales coloniza ion om he con inen is e y low, e en conside ing he possibili y o ansoceanic adul may ly mo emen s, as no ed in ecen s udies (Monaghan & al., 2005). E en conside ing ha a ha pellid p e alence compa able o ha in he land- mass was ini ially es ablished, agmen ed islands show a common disha mony conce ning species com- posi ion in ela ion o he p oximal con inen . Disco - dance esul s i s ly om he species sampling ha we e on he mainland landmass p io o sea le el as- cend (Gillespie & Rode ick, 2002). A e agmen a- 117 Anales del Ja dín Bo ánico de Mad id 66S1: 109-120, 2009. ISSN: 0211-1322. doi: 10.3989/ajbm. 2216 2216 T ichomyce es:10-T ichomyce es 10/12/2009 13:24 Página 117