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-
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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 -
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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.
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Balea ic ichomyce es 113
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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
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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-
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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-
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