Collembola om Hundide o-Ga o Ca e in Sou he n
Spain, wi h he desc ip ion o a new species o
En omob ya Rondani, 1861 (Collembola, En omob yidae)
Ja ie I. A bea1, Vi ginia Ga cía López2, F ancisco Ja ie So ia2, Ped o Abellán2
1C/ Ría de Solía 3, ch 39, 39610, As ille o, Spain 2Labo a o io de En omología Aplicada, Depa amen o de
Zoología, Facul ad de Biología. A da. Reina Me cedes, 6, 41012, Se illa, Spain
Co esponding au ho : Ja ie I. A bea ([email p o ec ed])
Academic edi o : Ľubomí Ko áč|Recei ed 21 Ma ch 2021|Accep ed 14 Ap il 2021|Published 19 Ap il 2021
h p://zoobank.o g/4B29C24B-8715-4620-88E9-B4D0086F98FB
Ci a ion: A bea JI, López VG, So ia FJ, Abellán P (2021) Collembola om Hundide o-Ga o Ca e in Sou he n Spain,
wi h he desc ip ion o a new species o En omob ya Rondani, 1861 (Collembola, En omob yidae). Sub e anean
Biology 38: 77–90. h ps://doi.o g/10.3897/sub biol.38.66254
Abs ac
This pape deals wi h some Collembola om a ca e a La Sie a de G azalema (Málaga). In o al, eigh spe-
cies o sp ing ails we e ound. Two may ep esen new species bu he e is insu icien ma e ial a ailable o
p epa e ull desc ip ions (one species in he genus Ce a ophysella, one in Hypogas u a), one species (Folso-
mides c . ayllonensis) is iden i ied o species, bu di e ences om he nominal species sugges u he s udies
may indica e he G azalema popula ions ep esen a dis inc o m, and one o he is desc ibed as new o
science, En omob ya i giniae A bea, sp. no . The new species is cha ac e ized by no sexual dimo phism in
colou pa e n, 5 cen al mac ochae ae on Abd II and 4 mac ochae ae on Abd III. Fo he iden i ica ion
and desc ip ion o he new species, he se o cha ac e s p oposed by Jo dana and Baque o (2005) was used.
Keywo ds
A h opoda, biospeleology, En omob yidae, En omob ya, axonomy
In oduc ion
The Hundide o-Ga o sys em, wi hin he Subbae ic Moun ain ange (Sou he n Spain),
is a hyd ogeological sys em composed by mo e han 10 km o galle ies. This ca e, loca -
ed be ween he municipali ies o Mon ejaque and Benaoján in he p o ince o Málaga
Sub e anean Biology 38: 77–90 (2021)
doi: 10.3897/sub biol.38.66254
h ps://sub biol.penso .ne
Copy igh Ja ie I. A bea e al. This is an open access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License (CC
BY 4.0), which pe mi s un es ic ed use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal au ho and sou ce a e c edi ed.
RESEARCH ARTICLE
Sub e anean
Biology Published by
The In e na ional Socie y
o Sub e anean Biology
A pee - e iewed open-access jou nal
Ja ie I. A bea e al. / Sub e anean Biology 38: 77–90 (2021)
78
(Andalusia, Spain), has wo mou hs: he i s one is Hundide o, which ac s as a sink,
and he o he one, which is called Ga o, whe e he complex d ains. The sys em ha -
bou s a wide a ie y o sub e anean en i onmen s, including an old sub e anean i e
cou se, sub e anean lakes, b oad chambe s and galle ies (Gue e o Sánchez 2015).
The in o ma ion abou he sub e anean biology in his sys em is sca ce and ag-
men ed (Ga cía-López e al. 2020). The i s s udies we e ca ied ou in 1865 by Lucas
on Heyden, a Ge man en omologis who wan ed o ind blind coleop e ans. Subse-
quen ly, he abbo Hen i B euil, in 1914, could see he p esence o wa m guano inside
he ca e bu did no cap u e anyone. Yea s la e , in he 1970s, some speci ic su eys
we e ca ied ou by ce ain speleological g oups, such as he GE Tele ónica o Mad id,
GEOS o Se illa and he E.R.E om C.E.C. om Ba celona, among o he s. In 1978, a
Du ch speleological g oup desc ibed he spide Ibe one a nasewoa Deeleman-Reinhold,
1984, he aqua ic amphipod Pseudonipha gus s ockin No enboom, 1987, and he gas-
opod Ibe ho a ia ga oa (Boe e s, 1980) (Boe e s 1980; Deeleman-Reinhold 1984;
No enboom 1987). Despi e he in e es o many esea che s h oughou decades, he
deepes and mos ex ended s udies did no begin un il Ma ch o 2016 (He nando and
Ga cía-López 2016), which e ealed a new endemic species, he oglobi ic s aphyli-
nid Phloeocha is manu He nando & Ga cía-López, 2016. Mo e ecen ly, wel e spide
species ha e been eco ded o his ca e, which belong o nine amilies: Agelenidae,
A aneidae, Dysde idae, Hahniidae, Linyphiidae, Lioc anidae, Seges iiadae, Te ag-
na hidae and Ulobo idae) (Ba ien os e al. 2019).
The e a e ew e e ences on he ca e-dwelling Collembola in he Subbae ic Sys-
em. Only nine species ha e been eco ded in some ca es om Sie a de las Nie es,
Sie a de Almija a and Sie a de Tejeda (A bea and Baena 2003; A bea e al. 2011;
A bea 2012): Ce a ophysella engadinensis (Gisin, 1949), Deu e apho u a cebenna ia
(Gisin, 1956), Onychiu us ge o um A bea, 2012, En omob ya paza is ei Denis, 1937,
Lepidocy us lexicollis Gisin, 1965, Pseudosinella in equens Gisin & Gama, 1969,
Pseudiso oma monochae a (Kos, 1942), He e omu us ni idus (Temple on, 1835) and
T oglopede es absoloni Bone , 1931. This is he i s s udy in which a ca e om he
Sie a de G azalema ha e been sampled o Collembola cap u e. The biospeleological
wo k has been de eloped in he Hundide o-Ga o sys em. A o al o 597 specimens
ha e been cap u ed, belonging o 8 di e en species. Among hem he e is one new
species, belonging o he genus En omob ya.
Ma e ial and me hods
Ca e desc ip ion
The Hundide o-Ga o sys em is loca ed in he no heas ex eme o Sie a de Líba ,
wi hin he moun ain ange o Ronda, in he no hwes o he p o ince o Málaga. In
his ca e we can ind h ee cha ac e is ic ypes o ka s i ica ion: he i s loo co e-
sponds o a i s s age, while he lowe loo is always looded; he middle loo is he
mos ele an as i co esponds wi h he speleological ek and i is he mos de eloped.
Collembola om Hundide o-Ga o 79
Due o he ex ension o he sys em, we ha e limi ed he s udy a ea o he mos acces-
sible pa a he en ance. The coo dina es o Hundide o a e 36°43'39"N, 5°14'19"W,
abou 558 m abo e he sea le el. The en ance o he ca e has a wid h o 10 m and a
heigh o app oxima ely 60 m, and 400 m o dep h accessible on oo .
Sampling
We used bai ed pi all aps o collec in e eb a es, which we e placed in some a eas
o he ca e ha we e suscep ible o ha bo auna. Fo he pi all aps we used clinical
analysis cans ( olume 150 ml), which we e bu ied and illed wi h a modi ica ion o
Tu quin´s liquid (Domingo-Que o and Alonso-Za azaga 2010). The aps we e bai ed
wi h Majo can sausage (cu ed sausage om Balea ic Islands made wi h po k, pap ika,
sal and o he spices) as a ac an (Belda-Ga cía e al. 2014). All collec ed specimens
we e p ese ed in 70% e hanol.
Two a eas we e sampled: he en ance o he ca e, which co e s abou 400 m om
he mou h o he i s lake, and he a ea called galle y, a ledge loca ed a e abou 20 m
om he lake, abou 20 m in he e ical o he wall, co esponding o he deepes a ea
ha was sampled. In o al, six een pi all aps we e placed: ou in semi-da kness ( wi-
ligh ) and ou in o al da kness in he en ance a ea; and i e aps in soil wi h guano
and h ee in soil wi hou guano in galle y. The sampling was ca ied ou in 2016 (bo h
he en ance and galle y) and 2018 (only he en ance), and he aps we e placed in he
da es ha he Na u al Pa k o Sie a he G azallema allowed us. The aps we e in he
ca e o one week. The en y seasons es ablished by he Pa k was go e ned by he ac i i y
o he ba s, allowing us access om mid-Ma ch o mid-Ap il and la e om mid-Augus
o mid-No embe , in o de o no dis u b he b eeding and win e ing pe iods o he ba s.
P epa a ion and analysis
Some specimens we e clea ed in Nesbi ’s luid and we e moun ed in Hoye ’s medium
o compound mic oscope obse a ion in phase cons as . Figu es we e d awn wi h a
came a lucida.
Te minology
Chae o axy schemes in En omob ya ollow Szep ycki (1979), Jo dana and Baque o
(2005) and Jo dana (2012). Symbols used in do sal chae o axy schemes a e: open ci cle
in he igu es s ands o he p esence o la ge mesochae ae o mac ochae ae ha could
be absen in male and ju enile specimens bu p esen in emales, closed ci cle s ands
o mac ochae ae ha a e always p esen , black chae ae-like d awings o sensilla, la ge
black ci cles wi h a c oss line o pseudopo es, long chae ae o bo h io icha.
Abb e ia ions used: Abd = abdominal segmen ; An = an ennal segmen ; as = sen-
silla; mc = mesochae a(e); Mc = mac ochae a(e); psp = pseudopo e; Th = ho acic seg-
men ; MNCN = Na ional Museum o Na u al Sciences a Mad id, Spain; MZUN =
Museum o Zoology, Uni e si y o Na a a, Spain.
Ja ie I. A bea e al. / Sub e anean Biology 38: 77–90 (2021)
80
Resul s
Family Hypogas u idae Bö ne , 1906
Ce a ophysella sp.
Ma e ial s udied. Cue a del Ga o, wiligh zone, 27-III-2016, 1 ♀
The single indi idual collec ed appa en ly ep esen s an undesc ibed species simila
o C. no ensis Cassagnau, 1965, cha ac e ized by A- ype o chae o axy (p1 chae a sho -
e han p2 chae a on Abd IV), dens wi h 6 chae ae, he basal chae a mo e han wice as
long as he o he s, e inaculum wi h 4+4 ee h, ibio a si wi h one poin ed enen hai ,
claw wi h one in e nal oo h and wo la e al ee h, ilamen o empodium 2/3 as long
as he inne edge o claw, An IV wi h ilobed apical bulb and 7 hin sensilla, slende
anal spines 1.5 imes he long o he claws and 1.8 mm leng h. The species is da k blue
and does no show cha ac e s ypically p esen in ca e-adap ed species.
Addi ional ma e ial is needed o con i m he iden i y o he species.
Hypogas u a sp.
Ma e ial s udied. Cue a del Ga o, wiligh zone, 27-III-2016, 1 ju .
The single indi idual collec ed appea s o ep esen a new species simila o H. e -
nalis (Ca l, 1901), cha ac e ized by ibio a si wi h one sligh ly knobbed enen hai ,
empodium wi h b oad basal lamella, do so-la e al pa s o Th II–III wi h m6 chae a,
An IV wi h ilobed apical bulb and 7 sensillae, dens wi h 6–7 chae ae, 2.7 imes as
long as muc o, PAO nea ly he same size as an omma idium, anal spines minu e, on
high papillae, coa se body g anula ion (8 g anules be ween he p1 chae ae o Abd V)
and 1 mm leng h. The species is g ey-blue and does no show cha ac e s ypically p e-
sen in ca e adap ed species.
Addi ional ma e ial is needed o con i m he iden i y o he species.
Mesogas u a ojco iensis (S ach, 1919)
New Sie a de G azalema (Málaga) eco d.
Ma e ial s udied. Cue a del Ga o, wiligh zone, 27-III-2016, 16 ex; da k zone, 14-
IV-2016, 1 ex, 13-XI-2016, 2 ex, 4-X-2018, 25 ex; ca e galle ies, 14-IV-2016, 1 ex,
30-IX-2016, 1 ex.
Edaphic and oglophilous, guanophilous species. This is a common Eu opean
species in he ca es o he Ibe ian Peninsula (Spain and Po ugal) and he Balea ic
Islands (Jo dana e al. 1997).
Collembola om Hundide o-Ga o 81
Figu e 1. Topog aphy o Hundide o-Ga o sys em and loca ions whe e he Collembola we e sampled.
Modi ied om Gue e o Sánchez (2015). In b own, he wiligh pi all aps, in blue, he da kness pi all
aps and in ed, galle y aps ( i e on guano and h ee on g ound wi hou guano). The di e en species
ha appea in each a ea a e ep esen ed wi h hei own symbol in he legend.
Xenylla ma i ima Tullbe g, 1869
New Sie a de G azalema (Málaga) eco d.
Ma e ial s udied. Cue a del Ga o, wiligh zone, 27-III-2016, 3 ex, 16-VIII-2018, 1 ex.
This is a cosmopoli an species known o occu in d y habi a s, su ace lea li e o
lichens on ocks (Thibaud e al. 2004). May appea in he meso oid shallow subs a-
um o in ca es acciden ally.
Family Iso omidae Schä e , 1896
Folsomides c . ayllonensis Simón & Luciáñez, 1990
New Sie a de G azalema (Málaga) eco d.
Ma e ial s udied. Cue a del Ga o, da k zone, 30-IX-2016, 1 ex.
The species lacks pigmen , bu has 5+5 eyes. The ju enile (0.5 mm) examined
di e om F. ayllonensis, as o iginal desc ip ion (Simón and Luciáñez 1990) and
no es made by Fjellbe g (1993), in ha ing an o al pos an ennal o gan, 1.7–1.8 as
long as omma (>2 in F. ayllonensis), and in ha ing h ee pos e io chae ae on dens
( wo in F. ayllonensis).

Ja ie I. A bea e al. / Sub e anean Biology 38: 77–90 (2021)
82
Figu e 2. Hundide o Ga o ca e a ex e io iew om Hundide o b Hundide o en ance c, d da k zone,
making di ec cap u es (Pho o by Miguel de Felipe).
The physical dis ance (≈690 km) and mo phological di e ences be ween he
G azalema and Ayllón popula ions sugges hey may ep esen dis inc species, bu
addi ional ma e ial om Sie a de G azalema will be needed o de e mine i he mo -
phological di e ences no ed he e a e ixed.
Collembola om Hundide o-Ga o 83
Family En omob yidae Schä e , 1896
En omob ya i giniae A bea, sp. no .
h p://zoobank.o g/0391BA36-456A-44BE-84BA-5C82C944D00A
Figs 3–15, Tables 1, 2
Type locali y. Sis ema Hundide o-Ga o, Benaoján-Mon ejaque, Málaga (Sie a de
G azalema Na u al Pa k, Spain), 36°43'39"N, 5°14'19"W, 558 m a.s.l.
Type ma e ial. Holo ype emale on slide, Sis ema Hundide o-Ga o, Benaoján-
Mon ejaque, Málaga (Spain), da k zone, 23-VIII-2018, leg. Vi ginia Ga cía López;
80 pa a ypes, same da a as holo ype: 12 emales, 4 males and 4 ju eniles on slide (11
om wiligh and 9 om da k zone) and 60 ex. in a ube wi h e hyl alcohol (20 om
wiligh and 40 om da k zone). Deposi ed in MNCN (holo ype and pa a ypes in
slides) and MZUN (pa a ypes in alcohol).
E ymology. The name is dedica ed o Vi ginia Ga cía López, who cap u ed he
specimens.
Desc ip ion. Body leng h 1.80 mm, excluding an ennae (mean 16 ex., Table 1).
Wi hou dimo phism in colou ; g ound colou whi e o e y ligh blue, wi h blue pig-
men on la e al body (all segmen s), do sola e al segmen s Th II o Abd V, as wo no
comple e s ipes wide on pos e io e gi es, a cen al pa ch on Abd III wi h a un-
ca ed cone shape, o he cen al pa ches on Abd I–II, and ans e sal bands on pos e io
e gi es Th II–Abd III in many specimens; head wi h pigmen on pos e io la e al eyes
and a do sal V-shaped pa ch; on legs, pigmen on dis al emu and la e al ibio a sus;
an ennae wi h pigmen on An I ip and whole An II–IV (Fig. 3). Simpli ied Mc
o mula (Jo dana and Baque o 2005) H1-H2-H3-H4-H5/T1-T2/A1-A2/A3-A4-A5/
A6-A7-A8-A9-A10 in adul emales: 3-2-0-3-2/2-4/2-3/1-2-1/0-4-3-2-2.
Head. Eigh eyes, GH smalle han EF. An ennae leng h 1.08 mm, 3.13 imes he
leng h o he head (n = 16, Table 1); An IV wi h apical esicle simple (Fig. 10) (sligh -
ly bilobed in some specimens); ela i e leng h o An I/II/III/IV = 1/2.38/2.42/2.43
(Table 1). Lab um wi h 4/5,5,4 chae ae; p elab al chae ae cilia ed, and lab al chae ae
smoo h. The labium has MR*ELL cilia ed Mc; R* hal as long as M; he emaining
labial Mc a e smoo h. The maxilla y palp has h ee sublobal chae ae. The papilla E
has a la e al p ocess eaching he end o he papilla (Fig. 9). In he do sal head chae o-
axy (Fig. 4), he H1 a ea has h ee Mc: An2, An3e1 and An3, and he H2 a ea wi h
wo Mc: A5 and A6 (some imes absen o as mc in male and ju enile specimens); Mc
se ies M wi h M1–M4; he H3 a ea wi hou Mc S’0; he H4 a ea wi h S1, S3 and
S4 Mc, and he H5 a ea wi h Ps2 and Ps5 Mc. The e a e ou chae ae on he ocula
well: p, q, and s.
Tho ax (Fig. 5). Th II has wo Mc: m1 and m2i, on he T1 a ea; he T2 a ea has
ou Mc: m4, m4i, a5 and a5’ (some imes absen o as mc in male o ju enile speci-
mens). Th III has comple e basal chae o axy: a1–a7, p1–p6, m6–m7.
Abdomen (Figs 6, 7). The Abd II has wo Mc on a ea A1: a2 and a3 (some imes
absen o as mc in male o ju enile specimens) and h ee Mc on a ea A2: m3, m3ep and
m3e. Abd. III has 1, 2 and 1 Mc on a eas A3, A4 and A5, espec i ely: a1, a2, a3 (some-
Ja ie I. A bea e al. / Sub e anean Biology 38: 77–90 (2021)
84
Figu e 3. En omob ya i giniae A bea, sp. no . Habi us.
Figu es 4–7. En omob ya i giniae A bea, sp. no . 4 head chae o axy 5 Th II chae o axy 6 Abd II–III
chae o axy 7 Abd IV chae o axy. Symbols: open ci cle = Mc ha could be absen in male and ju enile
specimens bu p esen in emales; closed ci cle = Mc ha a e always p esen ; black chae ae-like = sensilla;
black ci cles wi h a c oss line = pseudopo es; long chae ae = bo h io icha.
imes absen o as mc in male o ju enile specimens) and m3. Abd. IV wi h 11+11 cen-
al Mc: A3–A6, B3–B6, C1 (some imes absen ), C2a and E1 (Fig. 7). The ichobo h-
ia on Abd IV a he le els T2 and T4. Leng h a io o Abd IV/III = 3.78 (n=16, Table
1). Leng h o manub ium and dens 0.35 and 0.43 mm, espec i ely (n=16, Table 1).
Manub ial pla e wi h ou chae ae and wo pseudopo es (Fig.13). Muc o wi h ee h
simila in size, muc onal spine eaching ip o subapical oo h (Fig.12).
Collembola om Hundide o-Ga o 85
Figu es 8–15. En omob ya i giniae A bea, sp. no . 8 lab um 9 labial papilla E 10 ip o An IV
11lab al papillae 12 ip o dens and muc o 13 manub ial pla e (open ci cles = Mc; g ay ci cles = pseu-
dopo es) 14 ochan e al o gan 15 claw and empodium o leg III; Scale ba s: 0.02 mm (8, 12–15),
0.01 mm (9–11).
Legs. T ochan e al o gan wi h 15–16 smoo h chae ae in V-shaped and 7–8 la -
e al smoo h chae ae (Fig. 14). Tibio a sus no subsegmen ed, wi hou smoo h chae ae,
excep o smoo h e minal chae a on legs III. Claw wi h ou inne ee h: pai ed a
53–58% (one o hem la ge and o wa d), i s unpai ed a 70% om basis, and he
las one close han 90%; do sal ee h a he le el o la e al ee h (Fig. 15). Empodium
lanceola e, wi h se a ed ex e nal lamella in leg III. Tenen hai cla a e, longe han claw.
Rema ks. Fo he iden i ica ion o he species o En omob ya we mus conside a com-
bina ion o colou pa e n and do sal mac ochae o axy. I has been shown ha species wi h
he same colou pa e n can ha e a di e en chae o axy (Jo dana and Baque o 2005). On
he o he hand, species wi h di e ences in colo pa e n can co espond wi h species-le el
gene ic di e gence wi hou any ob ious di e ences in chae o axy (Ka z e al. 2015b).I he
mac ochae o axy o Th II/Abd II/Abd III is conside ed simul aneously, wel e species o
he genus sha e a simila simpli ied o mula o hese e gi es: 2-3/2-3/1-2-1 in E. a ocinc a
Schö , 1896, E. ma occana Baque o & Jo dana, 2008, E. meli ensis S ach, 1963, E. nu-
midica Baque o, Ham a-K oua & Jo dana, 2009, E. e ga ensis Baque o, A bea & Jo dana,