''
BULLETIN DE L'INSTITUT RO YAL DES SCIENCES NAT URELLES DE BELGIQ UE,
BULLETIN VAN HET KONINKLIJK BELGISCH lNSTITUUT VOO R NATUURWETENSCHAPPEN,
BIOLOG fE , 76: 5-26, 2006
BIOLOG IE, 76: 5-26, 2006
The remarkable diversity of subterranean Cirolanidae (Crustacea: Isopoda) in
the peri -Caribbean and Mexican Realm
by Thomas M. ILIFFE & Lazare BOTOSANEANU
We dedicate this paper to the memory of Jan H. Stock, indef atigable promoter of
stygobiological research in the West Indies, almost ten years aft er his untimely death.
Abstract
With 42 ende mic spec ies (o ne of them with two subspecies) described to this day, most of th em belo nging to 11 ende mic genera,
the peri-Caribbea n -Mex ican zone has definitely the richest fa un a
of stygobitic (entirely subterranean-adapted) cirolanids of the
world . After a succinct prese ntation of th e various habitats fo r
stygobitic cirolanids in the zone, the species are grouped together
(Table I) accordin g to the ir affili atio n to habitats of fres hwater or of
marine wate r - water salinity being considered th e most reliable
common denominator. A check-list in alphabeti cal order follows,
including references, know n distribution , informati o n on habitats,
etc. That this is a case of very hi gh biodi versity of stygobitic
Ci ro lanidae res ults from comparison with the situati on in th e rest of
the wo rld. Some aspects of morph ology in relation to sys te mati cs
are reviewed (i. a. : evoluti ve significan ce of some morphological
adaptations; monophyly of stygobitic genera). Attempts are made to
reply to ques ti ons like: what can we kn ow about ancestors of
stygobitic species? Can age of stygobitic taxa, or lineages, be appreciated with some degree of reliability? What can we guess about the
roots of prese nt-day di versity (two types of habitat requ iring di ffe rent ex pl anati on fo r time and mode of groundw ater coloni zati o n being recog ni zed)? How deep are these roots? What is the legacy of
Tethys? This case of hi gh biodi versity could be explained th rough
the rich , turbule nt history of this vast and frag mented area; th rough
the abundance and ex traordin ary di ve rsity of habitats propitious for
stygoevolution; and thro ugh the (s upposed) abundance and hi gh diversity of pote ntial marin e ancestors. A final part of the paper is
devoted to endangered or already destroyed habitats and fa un a, with
a plea for protecti on.
Key words: stygobitic C irol anidae, Caribbean-Mex ican area, subte rranean aqu atic habitats, biodi vers ity, stygoevo lution
Resume
Avec 42 especes ende miques ac tu elle me nt decrites (un e de celles ci avec deux sous-especes), appartenant pour Ia plupart a 11 ge nres
e ndemiq ues, Ia zone Cara"ibe-Mex icaine possede sans doute Ia
fa un e de cirolani des stygobies Ia plus ric he du mo nde. Apres une
prese ntatio n succincte des divers habitats peupl es par des
ciro lanides stygo bies dans Ia zo ne, les especes sont groupees (Tableau 1) d'apres ces habi tats: eau do uce o u eau marine- Ia sa linite
de l' ea u etant conside ree com me denominate ur commun le plus digne de confiance. Une li ste des taxo ns e n ordre alphabetique presente les references, Ia distribu tion connue, des info rmati ons sur les
habitats, etc. Une comparaiso n avec Ia situati o n pour le reste du
globe montre qu ' il s ' agit ici d ' un cas de biodive rsite remarqu ablement grande. Sont passes en revue plusieurs aspects concern ant des
relati ons e ntre morphologie et systematique (signi ficatio n evoluti ve
de certaines adaptations morphologiques; monophylie des ge nres
stygobies). On essaie de fo urnir des reponses a des questions
comme: qu ' est-ce que peut etre connu sur les ancetres des especes
stygobies? Est-ce que !'age des taxo ns (ou des lignees) stygobies
peut etre apprecie avec un certain degre de certitude? Qu ' es t-ce
qu ' on peut supposer concern ant les rac ines de Ia di versite actuelle
(deux ty pes d ' habitat de mandant des explications di ffe rentes pour
le te mps et Ia modalite de Ia colonisati on des eaux soute rraines etant
distingues)? Combien profo ndes so nt ces rac ines? Que! est, dans
ce cas co ncret, I' heritage de Ia Tethys? Ce cas de biodiversite pourrait etre ex plique par l'hi stoire ric he et mouve mentee de cette zone
vaste et frag mentee; par l' abond ance et l'extraordinaire diversite
des habitats propices a Ia stygoevolutio n; ainsi que par l'abond ance
et Ia di versite (s upposees) des a ncetres marins potentiels. Une secti on fin ale du trava il es t consacree aux habitats et a Ia faun e menaces OU deja detruits.
Mots-cJes: Cirolanidae stygobies, zone Cara1be-Mex icaine, habitats aquatiques so uterrains, biodiversite, stygoevolution.
Introduction
Although the first subterranean cirolanid isopod of the Caribbean -Mexican zone was di_scovered more than one century
ago, it was only during the last half of the previous century
that research on this group of stygobitic crustaceans has assumed large proportions, thanks to increas ing interest in speleology and stygobiology and to improving techniques for
exploration and zoological sampling. This has led to discovery and description of a remarkable large number of species
entirely bound to subterranean aquatic habitats of various
kinds, making this zone the most extraordinary " hot spot" of
the world for stygobitic Cirol anidae. The time seems to be
ripe fo r attempting a sy nthetic presentation of know n fac ts,
foc using on diversity and its poss ible explanation, in a naturalistic spirit, and limiting to a minimum reasonable speculati on not dictated by fashions. In order to avoid this paper taking exaggerated proportions, almost no reference to
stygobionts other than Cirolanidae and to "generalized
tracks" will be made. Also reference to publications not directly dea ling with Cirolanidae has been limited to some of
II
6
T.
M.
ILIFFE & LAZARE BOTOSANEANU
those shedding more light on aspects directly concerning the
present paper.
The stage
The zone dealt with in this paper is called "Caribbean-Mexican basin" by ARGANO (1972), "The (sub) tropical Atlantic"
by STOCK (1994), " the Central American/Caribbean intermediary areas" by BANARESCU ( 1995), or "Western Atlantic" by
BRIGGS ( 1995) - who distinguishes here a "West Indian
Province" and a "Caribbean Province". The wording used in
the title is from Stygofauna Mundi (BOTOSANEANU, 1986).
Stygobitic cirolanids of the peri-Caribbean - Mexican zone
inhabit wholly or partially submerged caves and
groundwater of varying salinity, all situated in karstic limestone. Due to locally characteristic differences in habitat
type, each area within the zone will be considered separately.
Generalized descriptions of habitat, geological setting, hydrology, water quality, and cirolanid stygofauna will be presented. Distribution of cirolanid species within the zone is
illustrated in Fig. 1.
Bermuda is a mid-Atlantic volcanic seamount, capped with
Pleistocene aeolian and marine limestone. Karstic caves in
Bermuda are concentrated in a small area of the island where
the oldest limestone outcrops. Tidal , sea level pool s occur at
entrances and in the dark interior of the caves. Although the
upper (dry and shallow submerged) portions of Bermuda
caves are dominated by collapse features, extensive horizontal passage development typically occurs at 18m de pth. The
presence of large speleothems (stalactites, stalagmites, etc.)
in all parts of the underwater caves indicates that the entire
known portions were completely dry and air-filled for long
times during glacial periods of lowered sea level. While surface waters in Bermuda's cave pool s range from slightly
brack ish to nearly fully marine, deeper waters below about 35 m depths approach fully marine salinities. One stygobitic
cirolanid, Arubalana arubaides, is known from Bermuda.
The Bahamas archipelago consists of a series of shallow
banks made up of a continuous, up to 5700 m thick, sequence
of carbonates of shallow water origin which began depositing during the Jurassic. As the banks gradually subsided, carbonate deposition has kept pace, mai ntaining a shallow water
environment. The banks are separated from one another by
deep water channels reac hing 2,000 m de pths. Water-filled
caves in the Bahamas are locally referred to as " blue holes".
Inland blue holes occur in the interior of islands, while ocean
blue holes are s ituated offshore, in shallow water. While
many inland and ocean blue holes are karstic sinkhol es with
no passage developme nt, others are parts of an extensive network fo rmed either by limestone di ssolution at the fresh/saltwate r inte1face (flank margin caves) or by slump faulting occurring along the platform marg in s (fault line caves). Ocean
holes typica ll y have reversi ng, high velocity, tidal currents
which flush the caves with seawater, while inland caves lack
perceptible currents and have a fresh to brackish water le ns
overl y ing fully marine waters. Stygobitic fa una of the Bahamas includes seven species of cirolanids from three gene ra,
Bahalana, Ciralana (subgenu s Ciralana) and Exumalana.
The northern coast of the Yucatan Peninsula is composed of
Pleistocene and Holocene limestone, while Miocene to
Eocene age rocks are exposed in the interior. Northern
Yucatan is generally low, with little relief, and smface rivers
or streams are absent. Water-filled caves are locally referred
to as cenotes, a Spanish corruption of the Mayan word
"dzonot". The most exte nsive underwater cave systems in
the world are located along the eastern Caribbean coastline,
with Systema Ox B-::1Ha at 130 km being the world's longest.
In the interior of the Peninsula, a well defined semicircle of
cenotes, mostly in the form of deep sinkholes, outlines the
deeply buried rim of the 65 million year old Chicxulub impact crater. Groundwater throughout the Peninsula consists
of a fresh water lens of varying thickness, floating on top of
denser seawater. The depth of the halocline boundary between fresh and saltwater varies from 10 m depth along the
coast to more than 60 m in the interior. The stygobitic fauna
of Yucatan thus includes both freshwater and marine species.
Seven species of stygobitic cirolanids from five genera,
Metaciralana,
Cirolana
(subgenus
Anapsilana),
Creaseriella, Haptalana and Yucatalana , have been described from the Yucatan Penin sula (including Cozumel and
Belize).
The Greater Antilles consist of the four large islands of
Pue rto Rico, Hispaniola (with Haiti and the Dominican Republic), Cuba, and Jamaica. They are part of a lower Cretaceous to Holocene island arc chain making up a submerged
mountain range extending from Central America eastwards
through the Caribbean. Each of the four islands is encircled
by a coastal plain, backed on the north coast of Cuba, Jamaica, and Hispaniola by Pleistocene-raised shorelines that
reach heights of 300 m. The extensive limestone outcrops on
these islands have given rise to a tropical karst landscape,
characterized by subterranean drainage, well developed
cockpit and tower karst, and numerous caves including large
river caves, deep sinkholes and long horizontal caves near
the coast that formed under the influence of palaeo-sea levels. Two species each of stygobitic cirolanids are known
from Cuba (Haptalana and Cirolana, subgenus Anapsilana),
Jamaica (Aruba/ana and Ciralana, subgenus Anapsilana)
and Hi spaniola (both Cirolana, subgenus Anapsilana).
The Netherlands Antilles include the islands of Aruba,
Bonai re and Cura<;ao _i n the southern Caribbean. The islands
formed as a result of volcanic activity 90-95 million years
ago, but half of the present day surface consists of Neogene
or Quaternary limestone. Caves are generally small , but
stygobitic fauna is also found in karstic springs, wells,
anchialine pools and the marine interstitial. One stygobitic
ciroland (Aruba/ana) is known from Aruba.
The Cayman Islands are co mposed of two distinct limeston_e
formations; dense and highly karstified Oligocene-Mioce ne
limestone forms the central core of each island, and is surrounded by a coastal limestone terrace of Pleistocene age
ca lled " ironshore". The island of Cayman Brae, due to its
greater elevation , has more numerous and larger caves. One
speci es of stygobiti c cirolanid ( Cirolana, subgenus
An.apsilana) is known from Grand Cayman.
One stygobitic cirolanid, Zulialana caalescens, is described
from the Sierra de Perija in northwestern Venezuela. This regio n is a tropical rainforest with well developed karst in Cretaceous limestone.
I I
Caribbean stygobitic Cirolanidae
The stygobitic cirolanid, Antrolana lira, is restricted to the
Shenandoah Valley including caves in Augusta County, Virginia and Jefferson County, West Virginia. This isopod inhabits pools that intersect the groundwater table. Limestone
in this area is Upper Cambrian in age.
Caves and groundwater habitats in Central and West Texas
including the Balcones Escarpment and Edwards Plateau are
inhabited by two stygobitic cirolanids, Speocirolana hardeni
and Cirolanides texensis texensis. The Edwards Aquifer
which underlies this area has the highest diversity of
stygobites in the United States (LONGLEY, 1986). The
Edwards limestone which outcrops over most of this area
was deposited in a shallow sea starting in the early Cretaceous. The receding shoreline passed through this area in the
early Tertiary.
The Sierra Madre Oriental of northeastern Mexico contains a
wide variety of groundwater habitats (e.g., caves, thermal
springs, wells, mines, and spring-fed pools) and an exceptionally diverse assortment of stygobitic cirolanids including
16 species from 4 genera (Cirolanides, Mexilana ,
Speocirolana and Sphaerolana). All of these systems contain
freshwater, although water in thermal springs can be highly
mineralized. During the Mesozoic, a thick layer of limestone
was laid down in the shallow sea extending from south central Texas, across Mexico and Belize, and into Guatemala. In
the late Cretaceous and early Tertiary, a series of mountainbuilding events known as the Laramide Orogeny uplifted,
distorted and compressed these rocks creating the coastal
ranges of the Sierra Madre Oriental.
Water salinity apparently being the best possible "common
denominator", we make an attempt to group together the species considered in this paper according to their affiliation to
either freshwater or marine habitats. Needless to say, in
rather many cases, it is difficult to appreciate correctly the
situation, owing to problems with obtaining reliable data during difficult exploration, or brought about by sampling quite
near Uust above or just below) haloclines. Moreover, some
species are certainly more or less euryhaline. For a few species - included or not in Table 1 - the situation is at present
rather problematic (Arubolana imula and parvioculata,
Bahalana cardiopus, Speocirola.na thermydronis, Yuca.tala.na robustispina.: see explanatory notes under "The actors").
7
Genus Antrolana BOWMAN, 1964
I. Antrolana lira
BOWMAN, 1964
Fig. 7
COLLINS & HOLSINGER, 1981 ; HOLSINGER et a.l. , 1994;
HOLSINGER, 2005
o,S?
Phreatic water in ten caves in the Shenandoah Valley karst
region of northwestern Virginia and eastern West Virginia,
USA
Freshwater
Genus Arubolana BOTOSANEANU & STOCK, 1979
2. Arubolana aruboides
(BOWMAN & ILIFFE, 1983)
Originally described in Bermuda/ana n.g. ; transferred by
NOTENBOOM, 1984, Bennudalana being synonymized with
Arubola.na..
NOTENBOOM, 1984; BOTOSANEANU & ILIFFE, 1997
o,S?
Bermuda, Hamilton Parish: Church Cave (Paynter's Vale
Cave), Wonderland Cave (Whitby Cave, Fantasy Cave), Bitumen Cave, Wilkinson Quarry Cave (this last cave: new
record)
Salt water; salinity variable with depth but species found
only in deeper, salt water
3. Arubola.na imula
BOTOSANEANU & STOCK, 1979
Fig. 16
NOTENBOOM, 1984
o,S?
Aruba by Lago Colony: Mangel Cora Tunnel
Fully marine water(?), although in original description " . ..
brackish (chlorinity 3600 mg/1)"
4. Arubola.na parvioculata.
NOTENBOOM, 1984
o,S?
The actors
Here follows a concise presentation of all 42 described
stygobitic species (one of them with two subspecies) of the
peri-Caribbean and Mexican realm, in alphabetical order.
For each species: publications, other than that containing the
original description, bringing some relevant additional information ; male/female described; known distribution; habitats
of freshwater/saline water; some additional information. To
these 42 species, two more should be added: that, from Cuba,
mentioned in the "Appendix to the check-list" and described
as Bahalana bowman.i; and a new species of Bahala.na from
Abaco, the Bahamas, described by BOTOSANEANU & JLJ FFE
in a separate paper in this same volume of the Bulletin (pp.
27-31).
Jamaica, Discovery Bay: interstitial in dry bed of Rio Secco
near sea shore (possibly also in marine interstitial)
Water salinity very different in various holes dug in sediment
Microoculate
Genus Baiza/ana CARPENTER, 1981
5. Bahalana. ca.icosa.na.
BOTOSANEANU & ILIFFE, 2003a
Plate I (a)
o,S?
North Caicos Island, Sandy Point: Cottage Pond (anchialine
cave). Middle Caicos Island , Conch Bar: Conch Bar Cave
Fully marine salinity
''
8
T. M. ILLFFE & LAZARE BOTOSANEANU
-2
)
30°
30°
37, 38,
39,40
30
20°
->g_)
41
31
29
28, 33
26, 27,
34, 35,
36
J2
~9:
7 , ~\
~6?
16, 20
)6- 5
~
11
.... . .
20°
-4
CJ..: -:_·
?
'\
If>;
~
\)
km
1"""'1
0
1"""'1
400
Figure 1: Map of the peri-Caribbean- Mexican zone illustrating the distribution of endemic stygobitic Cirolanidae. Numbers refer to the
species presented in that order under the section entitled "The actors": l. Antra/ana lira, 2. Aruba/ana arubaides, 3. Aruba/ana imula, 4.
Aruba/ana parviaculata, 5. Bahalana caicasana, 6. Bahalana cardiapus, 7. Bahalana exumina, 8. Bahalana geracei, 9. Bahalana
yagerae, LO. Ciralana (Anapsilana) acanthura, II. Ciralana (Anapsilana) crenata, 12. Ciralana (Anapsilana) cubensis, 13. Ciralana
(Anapsilana) pleascissa , 14. Ciralana (Anapsilana) radicicala, 15. Ciralana (Anapsilana) yucatani:l, 16. Ciralana (Ciralana) traglexuma,
17. Ciralanides texensis texensis, 18. Ciralanides texensis rnexicensis , 19. Creaseriella anaps, 20. Exumalana replans , 21. Haptalana
belizana, 22. Haptalana bawmani, 23 . Haptalana trichastama, 24. Hapta lana yunca, 25. Metaciralana mayana, 26. Mexilana salupasi,
27. Speaciralana bafivari, 28. Speaciralana disparicarnis, 29. Speaciralana endeca, 30. Speacirolanajustiura , 31. Speacirolana guerrai ,
32. Speaciralana hardeni, 33. Speaciralana lapenita, 34. Speacirolana pelaezi, 35. Speacirolana prima, 36. Speaciralana pubens , 37.
Speaciralana thermydranis , 38. Speaciralana zumbadara , 39. Sphaeralana affinis , 40. Sphaeralana interstitia/is, 41. Sphaerolana
karenae, 42. Yucata!ana rabustispina, 43. Zulialana caalescens
,,
Caribbean stygobitic Cirolanidae
9
Plate 1: Digital photographs of live stygobitic cirolanids: (a) Bahalana caicosana, (b) Cirolana (C.) trog lexuma, (c) Creaseriella anops,
(d) Exumalana reptans, (e) Yucatalana robustispina and (f) Metacirolana mayana.
''
10
T. M. ILIFFE
& LAZARE BOTOSANEANU
4
3
6
Figure 2: Speocirolana thermydronis, male (red rawn from BOTOSANEANU et al. 1998). Figure 3: S. pubens (redrawn from BOWMAN
198 1). Figure 4: S. prima, male (redrawn from SCHOTIE 2002). Figure 5 : S. pelaezi, fema le (redrawn from BOLIVAR y PI ELTA IN 1950).
Figure 6: S. zwnbadora, female (redrawn fro m BOTOSANEANU et a!. 1998)
II
Caribbean stygobitic Cirolanidae
7
9
\
Figure 7: An.trolana lira (redrawn f rom BOWMAN 1964). Figure 8: Yucatalana robustispina, female (ori ginal drawing). Figure 9:
Cirolanides texensis texensis (redrawn f rom BOWMAN 1964). Figure 10: Bahalana yagerae, male (redrawn from CARPENTER 1994).
Figure 11: B. exumina, male (redrawn from BOTOSANEANU & l LI FFE 2002).
11
11
T. M. ILIFFE & LAZARE BOTOSANEANU
12
12
13
Figure 12: Exumalana replans, fema le (redrawn from BOTOS ANEANU & lLI FFE 2003). Figure 13: Zulialana coalescens (redrawn fro m
& VILORI A 1993). Figure14: Creaseriella anops , fe male (ori ginal drawing). Figure 15: Sphaerolana interstitia/is, male
(orig inal drawin g).
B OTOSANEANU
I I
Caribbean stygobitic Cirolanidae
-·---------________ .......... - ....
17
18
,~
Figure 16: Arubolana imula, male (redrawn fro m BOTOSANEANU & STOCK 1979). Figure 17: Cirolana (Anopsilana) radicicola, male
(redrawn from NOTENBOOM 1981). Figure 18: Mexilana saluposi, fema le (redrawn from BOWMAN 1975). Figure 19: Cirolana
(Cirolana) troglexuma, female (original drawing).
13
14
T. M. ILIFFE & LAZARE BOTOSANEANU
Closely related to B. geracei and B. cardiopus, not to B.
yagerae or B. exumina
10. Cirolana (Anopsilana) acanrhura
(NOTENBOOM, 198 1)
6. Bahalana cardiopus
NOTENBOOM, 1981
Origi nall y described in Hairilana n.g. Transfen ed to
Anopsilana in BOTOSANEANU er al., 1986, Haiti/ana being
synonymized with Anopsilana in that publication.
BOTOSANEANU & ILI FFE, 1999
0,9
Bahamas. Mayaguana Island, Little Bay: Mount Mi sery
Cave; AckJins Island: Duncan Pond Cave.
Water salinity, according to NOTENBOOM, 1981, only ca. 10
g/1 (but this is highly improbable)
Only very slight differences from B. geracei.
9
Haiti : well at Marigot, southern coast 'of Departement de
!' Ouest.
Freshwater
11 . Cirolana (Anopsilana) crenata
(BOWMAN & FRANZ, 1982)
Origi nally described in g. Anopsilana
0,9
7. Bahalana exwnina
BOTOSANEANU & ILIFFE, 2002(a)
Fig. II
Grand Cayman Island, NW end: West Bay Cave.
Weak ly brackish water
12. Cirolana (Anopsilana) cubensis
HAY, 1903
0
Bahamas, Exumas, Great Guana Cay: Oven Rock Cave
Fully marine salinity
Maybe not far from B. geracei and B. cardiopus
8. Bahalana geracei
CARPENTER, 1981
BOLiVAR Y PIELTAIN, 1950; RIOJA, 1953, 1956 (i n this last
publication as n. g. Troglocirolana) ; SILVA TABOADA, 1974.
Transferred to Anopsilana in BOTOSANEANU et al., 1986,
Troglocirolana being synonymized with Anopsilana in that
publication.
Bahamas, San Salvador Island : Dixon Hill Lighthouse Cave
Fully marine salinity (but cave ca. 1 km di stant from ocean)
Cuba. Pinar del Rio: Caverna en San Isidro ; Habana: Cueva
between Madruga and Aguacate, Cueva del Quintana!,
Cueva de Ia Yagruma. Matanzas: Cueva de Suarez. Isla de
Pinos: Cueva de los Camarones, Cueva de los Murcielagos.
Freshwater
NOTENBOOM, 1981
o,s>
o,s>
9. Bahalana yagerae
(CARPENTER, 1994)
Fig. 10
Originally described in Dodecalana n.g.; transferred by
BOTOSANEANU & ILIFFE, 1997, Dodecalana being
synonymized with Bahalana.
BOTOSA NEANU & Iliffe, ] 997, 2002a, 2003a
0,9
Grand Bahama Island: Bahama Cement Cave, Old Freetown
Cave, Lucayan Cavern; Sweetings Cay (adjacent to Grand
Bahama Island): Janet Pyfrom's Blue Hole, Asgard Cave,
Virgo Blue Hole, Sagittarius Blue Hole, Lucy's Cave; Great
Ex uma Island: Basil Minn's Blue Hole ; Andros Island :
Conch Sound Blue Hole.
Fully marine salinity
Species distinct from all others by absence of pereiopods VII
in mature specimens.
Genus Cirolana LEACH, 1818
(sg. Anopsilana PA ULIA N &
DELAMARE DEBOUTEV ILLE, 1956)
Most species in this subgenus are marine/epigean, some of
them stygophilic.
13. Cirolana (Anopsilana) pleoscissa
(BOTOSANEANU & ILIFFE, 1997)
Originally described in Jamaica/ana n.g. Transferred by
BOTOSANEANU & lLIFFE, 2000, Jamaica/ana being
synonymized with Cirolana (Anopsilana) in that publication.
9
Jamaica, Westmoreland
Freshwater
~arish:
Revival Water Pump Cave
14. Cirolana (Anopsilana) radicicola
(NOTENBOOM, 1981 )
Fig. 17
Originally described in Haitilana n. g. Transferred in
BOTOSANEANU et al., 1986, Haitilana being sy nonymized
with Anopsilana in that publication.
0,9
Haiti, southern peninsula, near Jerem ie: "Source Debarasse",
large karstic spring flowing from cave.
Freshwater
15. Cirolana (Anopsilana) yucatana
BOTOSANEANU & ILI FFE, 2000
9
Mexico, Yucatan , Mucuyche: Cenote Dzonotila.
''
Caribbean stygobitic Cirolanidae
Freshwater
Genus Cirolana LEACH, 181 8
(sg. Cirolana)
Almost all described species are marine/epigean.
16. Cirolana (Cirolana) troglexuma
BOTOSANEANU & ILIFFE, 1997
Fig. 19, Plate l (b)
15
Mexico, Yucatan Peninsula: numerous caves (some of them
true cenotes) in the states Quintana Roo or Yucatan. To those
in the various publications above mentioned should be added
the following new records: from Quintana Roo - Cenote
Kaape Ha (Del Mar), Systema Ox Bel Ha, Tulum; from
Yucatan- Cenote San Miguel and Cenote Chean Kab, both at
Huhi, and Cenote San Antonio at Homun.
Freshwater
Genus Exumalana BOTOSANEANU & lLIFFE, 2003(b)
BOTOSANEANU & lLIFFE, 1999, 2003b. The species has been
rediscovered (2003, 2004) both in the type locality and in a
new one (Basil Minn 's Blue Hole); these records not published.
S?
Bahamas. Exuma Cays, Great Guana Cay: Oven Rock Cave;
Great Exuma Island: Basil Minn 's Blue Hole; Cat Island: Big
Fountain Blue Hole (this last record not yet published).
Fully marine salinity
S?
Bahamas, Exumas, Norman's Pond Cay: Norman's Pond
Cave ("inland blue hole").
Water fully marine
Additional note: in BOTOSANEANU & ILIFFE, 1997, two
subgenera are recognized in g. Cirolana.
Genus Haptolana BOWMAN, 1966
Genus Cirolanides BENEDICT, 1896
21. Haptolana belizana
BOTOSANEANU & lLIFFE, 1997
17. Cirolanides texensis texensis
BENEDICT, 1896
Fig. 9
20. Exumalana reptans
BOTOSANEANU & ILIFFE, 2003(b)
Fig. 12, Plate l (d)
0
Belize: Inland Blue Hole, Caves Branch.
Freshwater
BOWMAN, 1964, 1972, ] 992; BOTOSANEANU & lLIFFE,
2002b (here, inter alia: updated distribution)
22. Haptolana bowmani
BOTOSANEANU & ILIFFE, 1997
o,S?
36 records (caves, phreatic waters, springs) all from Texas
(counties Bexar, Burnet, Coma!, Crockett, Edwards, Hays,
Kendall, Kerr, Medina, Real, Schleicher, Terrell, Uvalde, Val
Verde) all in the southern part of Edward's Plateau.
Freshwater
18. Cirolanides texensis mexicensis
BOTOSANEANU & ILIFFE, 2002b
o,S?
Mexico, Yucatan: Grutas de Tzab-Nah (Dzab Nah) 2 km S of
Tecoh on road to Telchaquillo; immatures probably of the
same species from three other Yucatan localities: Cenote
Kambul (published as Noc Ac), Cenote Mucuyche, Cenote
Yuncu.
Freshwater, at least in type locality
BOTOSANEANU et al., 1998; BOTOSANEANU & ILIFFE 1999.
o,S?
N. Mexico. Nuevo Leon, Lampazos: Cueva de El Tule,
Cueva de La Espantosa; Coahuila, west and north from
Ciudad Acuna: S6tano de Amezcua.
Freshwater
Genus Creaseriella RIOJA, 1953
19. Creaseriella anops
(CREASER, 1936)
Fig. 14, Plate l(c)
Originally described in Cirolana; transferred by RIOJA, 1953
to Creaseriella n.g.
Creaser, 1938 ; BOLIVAR Y PI ELTAlN, 1950; RIOJA, 1953;
REDDELL, 1977; PEREZ ARANDA, 1984; BOTOSANEANU &
ILIFFE, 1997, 1999, 2002a; ESCOBAR et al. , 2002.
o,S?
23. Haptolanrt trichostoma
BOWMAN, 1966
SILVA TABOADA, 1974
0
Cuba, Province Camaguey, Sierra de Cubita: Cueva Bonita,
Cueva de Ia Lechuza.
Freshwater
Cons idered by BOTOSANEANU & ILIFFE, 2000 as not being
closely related to H. belizana, H. bowmani and H. yunca
which could have a common marine ancestor.
24. Haptolana yunca
BOTOSANEANU & ILIFFE, 2000
S?
Mexico, Yucatan, Yuncu: (deep) Cenote Sabakha.
Caught in freshwater near halocline
II
16
T. M. ILIFFE & LAZARE BOTOSANEANU
28. Speocirolana disparicomis
BOTOSANEANU & IUFFE, 1999
Genus Metacirolana NIERSTRASZ, 1931
The bulk of species in this genus are marine/epigean.
3,9
25. Metacirolana mayana
(BOWMAN, 1987)
Plate 1(f)
Originally described as Bahalana; transferred by
BOTOSANEANU & ILIFFE, 2002a.
BOTOSANEANU & lL!FFE, 1997, 1999, 2002a; CARPENTER,
1994.
3,9
Mexico, Yucatan, Quintana Roo. Isla Cozumel: Cueva
Quebrada, Cenote Aero! ito, Cenote Tres Potrillos. Other loca]jties in Quintana Roo: Cenote Temple of Doom Cave
(near Tulum), Cenote Crustacea, originally published as
Aayin Aak (Puerto Morelos), Cenote 27 Steps (Akumal).
One additional known locality in Quintana Roo has never
been published: Cenote Chac Moo! (Puerto Aventuras).
Fully marine water
Genus Mexilana BOWMAN, 1975
26. Mexilana saluposi
BOWMAN, 1975
Fig. 18
3,9
Mexico, Tamaulipas, Jaumave: Guayatejo spring
Freshwater
29. Speocirolana endeca
BOWMAN, 1981
3,9
Mexico, Tamaulipas, NW of Ciudad Victoria: S6tano de las
Calenturas (Yerbabuena); Cueva del Tecolote (Los San
Pedro).
Probably freshwater
30. Speocirolana just iura
BOTOSANEANU & ILIFFE, 1999
c)
Mex ico, Nuevo Le6n, Potreritos: Sima Chupacab1e
Freshwater
31. Speocirolana guerrai
CONTRERAS-BALDERAS & PURATA-VELARDE, 1982
3,9
Mex ico, Nuevo Leon, Linares: Cueva de Ia Chon-era
Freshwater
Considered as more closely related to S. pubens
Mexico, San Luis Potosf, 4 km NW Micos: Cueva del
Hui sache
Probably freshwater
32. Speocirolana hardeni
BOWMAN, 1992
c)' 9
Genu s Speocirolana BOLiVAR Y PIELTAIN, 1950
Origi nally described as sg. of Cirolana LEACH. Elevated to
generi c rank by BOWM AN, 1964.
S. Texas: several wells, artesian wells, or springs in the COUI1ties Bexar and Val Verde
Freshwater
Considered as most closely related to S. thermydronis
33 . Speocirolana lapenita
BOTOSANEANU & ILIFFE, 1999
27. Speocirolana bolivari
(RIOJA , 1953)
Originally described in sg. Speocirolana of Cirolana.
REDDELL & MITCHELL 1971a,b; BOWMAN 1981 ; BOTOSANEANU & ILIFFE, 1999; BOTOSANEANU et al., 1998.
3,9
Mexico. Tamaulipas: Cueva (Grutas) de Quintero (Sierra de
El Abra); "Bee Cave" (S ierra de Guatemala); Cueva del
Nacimiento del Rfo Frio (Municipio Gomez Farias, Ej ido El
Nacimiento) ; Ojo Encantado (Jaumave, Canon Trejo). San
Luis Potosf: spring at La Laja. Nuevo Leon: Sima
Chupacable (Potreritos).
Freshwater
Disc ussion of variability, characters enab ling or not di stinction from the closely related and so metimes coexisting S.
pelaezi, possibility of hybridi zation, relative abundance of
these two spec ies: RIOJA , 1953 ; COLE & MrNCKLEY, 1966;
MINCKLEY & COLE, 1968; BOWMAN, 198 1; BOTOSANEANU
& lLI FFE, 1999; BOTOSANEANU et al., 1998.
3,9
Mex ico, Tamaulipas, Ciudad Victoria: Manantial La Penita
Freshwater
Apparently related to S. guerrai and S. pubens.
34. Speocirolana pelaezi
(BOLiVAR Y PIELTAIN, 1950)
Fig. 5
Originally described in sg. Speocirolana of Cirolana.
RIOJA, 1953; REDDELL & MITCHELL, 1971 a, b; BOTOSANEANU et al., 1998; BOTOSANEANU & lLIFFE, 1999.
3,9
Mex ico. San Luis Potosf: Cueva de los Sabinos, Sotano de
Pichijumo, Sotano de las Piedras, S6tano del Tigre, Sotano
de Ia Tinaja, S6tano del Arroyo, Cueva Chica, Cueva de Ia
Curva, Sotaruto de Montecillos. Tamauli pas, Sierra de El
Abra: Cueva de Ia Florida, Cueva de El Pachon, Grutas
Caribbean stygobitic Cirolanidae
(Cueva) de Quintero; Tamaulipas, Sierra de Guatemala:
Cueva de Ia Mina; also in Tamaulipas are: Cueva del
Nacimiento de l Rfo Frfo (Municipio Gomez Farias, Ejido El
Nacimiento) and Ojo Encantado (Jaumave, Canon Trejo).
Freshwater
For various observations: see last paragraph of text for S.
bolivari
35. Speocirolana prima
SCHOTIE, 2002
Fig. 4
o,<i'
Mexico, Tamaulipas: Nacimiento de R fo Mante just south of
Ciudad Mante
Freshwater
" .. . most like S. pubens ... "
36. Speocirolana pubens
BOWMAN, 1981
Fig. 3
o,<i'
Cuatro Cienegas; Cueva La Zumbadora (Municipio La Madrid). Nuevo Leon: flooded mine near Cueva de Ia Boca
(Villa Santiago)
Freshwater
40. Sphaerolana interstitialis
COLE & M!NCKLEY, 1970
Fig. 15
COLE, 1984; BOTOSANEANU et al., 1998
o , <i'
Mexico. Coahuila: small springs and " pozos" near Cuatro
Cienegas. Tamaulipas: Manantial de San Rafael de los
Castro (Municipio Ciudad Mante).
Freshwater
41. Sphaerolana karenae
RODRIGUEZ-ALMARAZ & BOWMAN, 1995
0
Mex ico, Nuevo Leon: small spring adjacent to Pilon River,
Montemorelos; mine near Cueva de Ia Boca, (Villa) Santiago
Freshwater
Mexico. San Luis Potosf, San Nicolas de los Montes: Cueva
de Ia Bonita; Tamaulipas, 14 km of Ocampo: Cueva de l Ojo
de Agua de Manantiales
Freshwater
Considered as more closely related to S. guerrai
37. Speocirolana thermydronis
COLE & MINCKLEY, 1966
Fig. 2
MlNCKLEY & COLE, 1968; COLE, 1984; BOWMAN 1992;
BOTOSANEANU et al., 1998.
o,<i'
Mexico, Coahuila: several " pozos" (thermal springs and associated habitats - marshes) SW of C uatro Cienegas, for instance Pozos de Ia Becerra and El Majarral; El Potrero 1 and
E l Potrero 2 (Municipio Melchor Muzquiz).
Thermal , possibly rather highly mineralized water
Considered as closely related to S. hardeni.
38. Speocirolana zumbadora
BOTOSANEANU et al. , 1998
Fig. 6
<jl
Mexico, Coahuila, M unicipio La Madrid: Cueva La
Z umbado ra
Freshwater
Genus Sphaerolana COLE & MINCKLEY, 1970
39. Sphaerolana affinis
COLE & M !NCKLEY, 1970
COLE 1984; BOTOSANEANU et al., 1998.
o,<i'
Mexico. Coahuil a: vario us " pozos" ("springfed wells") near
17
Genus Yucata/ana BOTOSANEAN U & ILIFFE, 1999
42. Yucatalana robustispina
BOTOSANEANU & IUFFE, 1999
Fig. 8, Plate l (e)
BOTOSANEANU & lLIFFE, 2000, 2002a
o,<i'
Mexico, Yucatan: Cenote Pabakal (Eknakan); Cenote
Kankirixche, Cenote Kakuel , Cenote Chuih-Hol Dos (all
three: Mucuyche); Cenote Xacha, Huhi, Cenote San
Geronimo, Sotuta (these latte r two records not yet published).
Probably caught both above or below the halocline
Genus Zulialana BOTOSANEANU & VILORIA, 1993
43. Zulialana coalescens
BOTOSANEANU & .VILORIA, 1993
Fig. 13
o,<i'
NW Venezuela, Estado Zu lia, Sierra de Perija: Cueva de
Toromo, near hacie nda Medellfn. A second population of
this species has been recently discovered by Francesco F.
Herrera (IVIC, Caracas) in a cave about 100 km distant fro m
the type locality, but still in Sierra de Perija: Mara 2 Cave,
Guasare river basin.
Freshwater
Appendix to the check-list
In ORTIZ et al. (1997), the blind and depigme nted ci.rolanicl
Bahalana bowmani is desc ribed fro m "Cue va de l Humo,
Playa Giron , Provi ncia de Matanzas, C uba" (fully mar ine
II
18
T. M. ILLFFE & LAZARE BOTOSANEANU
water). This species is certrunly not a Bahalana, lacking the
distinctive characters of this genus. Moreover, information
on some relevant morphological detruls is lacking from its
description and illustration. Being unable to decide about the
genus to which it belongs, we could not place it in the checklist. In the same publication, Anopsilana magna n. sp. is described from a cave with fully marine water near the locality
of "Bahalana bowmani". Although depigmented, this species has very large facetted eyes; being quite probably not a
stygobiont, it will not be taken into consideration in this paper.
The case of the extremely poorly described and unrecognizable Coni/era stygia PACKARD, 1894 from Monterrey,
Nuevo Leon, Mexico, has been discussed in several publications; it is considered as probably being a species of
Speocirolana.
***
Several cases of coexistence of two species at one site are
documented at present: Bahalana exumina and Cirolan.a (C.)
troglexuma in Oven Rock Cave; B. yagerae and C. (C.)
troglexuma in Basil Minn 's Blue Hole; Speocirolana bolivari
and S. pelaezi in Cueva de Quintero, Cueva del Nacimiento
de Rfo Frfo, and Ojo Encantado; S. bolivari and S.fustiura in
Sima Chupacable; S. zumbadora and Sphaerolana affinis in
Cueva La Zumbadora; Sphaerolana affinis and S.
interstitia/is in springs and "pozos" near Cuatro Cienegas.
Moreover, there is very probably coexistence of Cirolanides
texensis texensis and of Speocirolana hardeni at some Texan
sites. Likewise, coexistence will possibly be discovered also
for Speocirolana thermydronis and · Sphaerolana (affin.is?
interstitia/is?) at some sites in the neighbourhood of Cuatro
Cienegas.
lana RACOVITZA - Turcolana ARGANO & PESCE - Marocolana BOULANOUAR et al. There are about 20 species described in this complex (possibly not all will prove to be
valid, whereas additional species will be described); together
with fi ve species described in Sphaeromides DOLLFUS (one
with one subspecies, one with two), one in Faucheria
DOLLFUS & VIRE, one in Kens/eya J?RUCE & HERRANDOPEREZ, and one in Metacirolana, this would give a total of
slightly more than L.5 endemic species in seven genera. There
is, too, an ecological difference between the stygobitic
cirolanid fauna of the two zones: genuine anchialine species
are very poorly represented in the Mediterranean - possibly as
result of the hypersalinity/drying-up crisis during the late
Miocene (Messinian) having forced ancestors of the
stygobitic taxa directly into near-littoral subterranean freshwater habitats (STOCK, 1981 ).
The contrast becomes very impressive when we reach nonMediterranean Africa (one species of Cirolana (Anopsilana)
known from Madagascar; two of Skotobaena FERRARA &
MONOD and one of Haptolana known from the Horn of Africa), to the enormous mass of Pacific islands (3 species of
Cirolana (Anopsilana) described from Sulawesi, the Philippines, and Palau Islands), and to Australia (only one species
of Haptolana described; but - information in litt. from N.L.
BRUCE - two or possibly three more cirolanids recently discovered from the extraordinarily productive "calcretes" of
Northwestern Australia).
Genera Annina BUDDE-LUND and Sahara/ana MONOD,
whose species cannot be considered as clearly stygobitic,
have been omitted from these considerations. In our opinion,
the future will not bring drastic changes in the situation as
here sketched.
Some aspects of morphology in relation
to systematics
A uniquely high biodiversity of stygobitic
Cirolanidae
The peri-Caribbean and Mexican Realm is the most extraordinary area of the world in this respect, with 42 endemic species (one of them with two subspecies) described to this day,
most of them belonging to 11 genera endemic for the area some of these morphologically very remarkable. Exceptional cases of specific diversification are offered by
Speocirolana, Bahalana, or Cirolana (Anopsilana), and
those of Sphaerolana, Haptolana, or Arubolana are, too,
highly interesting. The tropics of the Western Atlantic have
been for stygobitic Cirolanidae a centre of strong evo lutionary radiation (B RIGGS, 1995: 238-242 discusses the contrast
with the comparatively poor faunal area represented by the
tropics of the Eastern Atlantic). Undoubtedly, more discoveries can be expected , especially in Mexico, and maybe also
in the practically unexplored smaller Central American COUI1tries, when their anchialine habitats are explored by diving.
T here is a clear contrast even with the zone of the globe second in biodi versity: the European Mediterranean sensu lato.
It is not possible to offer really exact f igures of stygobitic
species for this zone, because there are still some sub j udice
taxonomk problems with the generic complex Typhlociro-
The vast array of morphological (and other) adaptations of
Cirolanidae to hypogean life has been summarized by
BOTOSANEANU (2001). Only two facts of paramount importance in the evolution of stygobiont Cirolanidae will be
evoked here. First: the highly diversified pereiopodal morphology with more or less strongly raptorial structures affecting various groups of pereiopods, is, possibly, grosso modo,
a result of partly abandoning feedi ng by scavenging (raptorial
pereiopods are an exception in epigean-marine cirolanids) for
an actively prey-grasping mode of life. Second: the occurrence in possibly phylogenetically widely distant taxa, of
highly modified tailfans and especially uropod , having completely lost their natatory fu nction (a result of abandoning
active sw imming for creeping in smaller bodies of water). It
may be suspected that drastic remoulding of the tailfan has
had a mechanical impact on the pleonal type of segmentation
- considered by BOWMAN (1975) as being of prime importance for grouping cirolanid genera, as well as for realization
of a morphology making more or less complete rolling into a
ball possible. We believe that characters resulting from these
major evolutionary events and shared by congeneric species
can be considered as synapomorphies; whereas much caution
is recommended when making use of them fo r deciding about
I I
Caribbean stygobitic Cirolanidae
kinship between genera (BOTOSANEANU & VILORIA,
1993:169). As aptly worded by CAVALLI-SFORZA et al.
(1994:372) "Natural selection causes convergence, or divergence in ways and directions that have nothing to do with
coancestry".
Characters from almost all parts of the cirolanid body have
been successfully used in systematics - a partial exception
being the mouthparts. Different morphological characters
may have quite different evolutive (phylogenetic) strength
and significance- a field for future research in cirolanid syste matics. For the time being, experience shows that, besides
characters mentioned above, good tools for syste matics are
those offered by: rostrum-lamina frontalis-clypeolabrum ;
pleopodal morphology and setation ; the penes.
19
lifeline carrying . .. genetic reinforcement for a thriving tropical community across some 1200 km of ocean").
All this does not mean that generic attribution of some species will not be questioned in the future, as it has been in the
past for other species. We can only hope that authors atte mpting revisions in the future will take into account the ele mentary fact, often neglected by cladists, that subterranean
life has generated characteristics strongly blurring the image
of phylogenetic relationships.
The questions
What can we know about ancestors of stygobitic
species?
About possible monophyly of some stygobitic
genera
This is a study of biodiversity, and by no means one of
cladistics. Nevertheless, here are succinct remarks on the
possible monophylg of some genera represented in the area.
There were difficulties with Anopsilana (discussion of various aspects: MONOD, 1976; BOWMAN & FRANZ, 1982;
BRUCE, 1981, 1992; BRUSCA etal., 1995; BOTOSANEANU &
ILIFFE, 1997) considered as morphologically not sharply distinct from Cirolana (a problem having received a provisional
solution by distinction of two subgenera: BOTOSANEANU &
ILTFFE, 1997) or as a polyphyletic taxon- conclusion drawn,
probably, from the geographical distribution, because we
have not seen morphological arguments. In our opinion
these difficulties have been exaggerated; we can very well
imagine the origin of various members of Anopsilana across
the globe either from various marine-epigean species of
Cirolana (which, of course, would displace the question to: is
Cirolana monophyletic, or not?) ; or, in some cases, even
polytopically from various populations of one epigean
Cirolana - which would be a case similar to those of
Astyana.x fasciatus/Anoptichthys in Central Mexico (i.a. :
WILKENS, 1981) or of Asellus aquaticus with its various
"cave forms".
Despite impressive diversity of habitus in various species,
Speocirolana also is very probably monophyletic,
monophyly being supported by a good number of shared
morphological details (for instance: BOTOSANEANU et al.,
1998) and also by the remarkable compact distribution of
most species in northeastern Mexico (SCHOTIE, 2002: fig.
4), a fine example of speciation by geographic isolation.
Shared characte rs for various species of Haptolana are summarized in BRUCE & HUMPHREYS, 1993 and in
BOTOSANEANU & ILTFFE (1 997, 2000), and at least some of
the m are probably synapomorphic.
Bahalana is an example of a monophyletic genus
(BOTOSANEANU & ILIFFE, 2003a) not needing much discussion; and a fine example of speciation by insular isolation.
As to Arubolana, despite the re markable disjunct distribution
of its species, there can be no doubt about monophyly (BowMAN & IL!FFE, 1983; see also B RIGGS, 1995 :238 for discussion of the role played by the Gu lf Stream as "Bermuda's
There is a consensus between various authors that all
stygobitic Cirolanidae in the area are of marine origin. There
has been some discussion around Antra/ana lira, not questioning its marine origin but considering it as an exceptional
case: the only taxon found in an area unexposed to marine
water since the Paleozoic (detailed discussion in BOWMAN,
1964; see also COLLINS & HOLSINGER, 1981 ). However, recently published evide nce (KOENEMANN & HOLSINGER,
2001: fig . 26) shows that du ring middle to late Cretaceous,
the localities of A. lira in Virginia were flooded by a continental marine e mbayment: which confirms the marine origin
of this species. The alternative "shallow water ancestors"
versus " deep sea ancestors" has been discussed in several
publications not specifically devoted to Cirolanidae (i.e.:
lLIFFE et al., 1983; HART et al., 1985; MANNING et al., 1986;
STOCK, 1986a; ANKER & ILIFFE, 2000). Origin from taxa of
shallow marine water seems clearly more plausible if the anoxia crisis with its catastrophic consequences in the Atlantic
waters deeper than 200 mat the Mesozoic/Tertiary boundary,
as well as at the Oligocene/Miocene boundary, are taken into
consideration. Nevertheless, the proble m cannot be considered as definitely settled. That the immediate ancestors were
animals well preadapted to hypogean life seems to be a
strongly fo unded opinion (importance of preadaptation in the
case of Cirolanidae has been stressed by BOTOSANEANU,
2001).
Ve ry little concrete e vidence can be gathered, without falling
into wild speculation, about the actual ancestors. It should be
kept in mind that " the subte rranean ofte n convergent evolution of characters might obscure the phylogenetic relationships between marine epigean and stygobiont taxa"
(GALASSI, 1997); and the possibility of speciation, in some
cases, from already stygobitic ancestors (HOLSINGER, 2004)
should not be excluded. The re is more solid evide nce fo r the
species of sg. Anopsilana, very probably derived from marine-epigean Cirolana spp., and for the subterranean
Metacirolana, fo r which descent from congeneric marine/
epigean species is qu ite plausible (according to KENSLEY &
SCHOTIE, 1989, fro m epigean marine waters of the Cari bbean, not including the G ulf of Mexico, two species of
Anopsilana, five of Cirolana, and four of Metacirolana are
known).
20
T. M. IUFFE & LAZARE BOTOSANEANU
Can the age of stygobitic taxa and lineages be
appreciated with some degree of reliability?
This is a ticklish question. To correlate age with the geological age of the rock in whkh the habitat of the stygobiont is
developed , would be simply absurd (MONOD, 1975). It
would be equally wrong to correlate it with the supposed
time of emergence above sea level of its habitat, because it is
quite possible (and in some cases quite probable) that a long
period of stygoevolution below sea level has preceded this
emergence. Several authors have published ideas in this context (HART et al., 1985; STOCK, 1986a, 1994; ILIFFE, 1990;
ANKER & lLIFFE, 2000; KORNICKER & ILIFFE, 2000; and interestingly, some additional evidence seems to come from
palaeontology: LOZOUET, 2004). This idea is aptly worded,
for instance, in STOCK (1994:109-110): " ... stygobionts did
not need subaerial edifices to evolve, their marine ancestors
could have Jived on shallow submerged banks or sea mounts
and then adapted to subaerial conditions after such banks
arose above sea-level" .
Can the age of a taxon or lineage be correctly inferred from
morphology? If unconditionally answering with "yes", this
would imply that we believe that rates of stygoevolution are
identical in all lineages - something which cannot be accepted. Nevertheless, a morphological diversification like
that seen in Speocirolana could be evidence for long-lasting
evolution. Genera in the fauna of the zone, with morphology
most radically moulded by subterranean life, are
Sphaerolana, Zulialana, Exumalana , and Yucatalana: are
they all very o ld/ the oldest? In some cases possibly yes
(Sphaerolana , Zulialana), in some. others possibly not
(Exumalana, Yucatalana); if such speculation can be made, it
is because morphological evidence seems to be supported by
evidence from habitat and distribution . At the opposite end
of the spectrum we have the least radically transformed taxa:
still macro-oculate like Anopsilana magna, or, for instance,
micro-oculate like Arubolana parvioculata: in such cases
and possibly also in that of Cirolana (Cirolana) troglexuma
there is serious evidence for relatively recent stygobitization.
What can we guess about the roots of pr·esent day
diversity?
Various authors have expressed opinions (sometimes contradictory- even in publications by the same author!) about time
of g roundwater colonization in various parts of the peri-Caribbean/Mexican Realm . Here follows an incomplete list of
such publications.
• Concerning more than one geographic unit belonging to
our zone: ALVAREZ et al. , 2005; HART et al. , 1985 ;
HOLSI NGER, 2000 ; HUMPHREYS , 2000 ; lLIFFE, 1992a,
2000, 2005 ; MONOD, 1975 ; NOTENBOOM , 1984; SK ET,
1996, 2005 ; STOCK, 1986a, 1994.
• Bermuda: ANKER & lUFFE, 2000; BOWMAN & IUFFE,
1983; BRlGGS, 1995 ; lLIFFE, 1994, 2003 , 2004; lLIFFE et
al. , 1983 ; HART eta!., 1985; MANNING eta!. , 1986; SKET
& lLI FFE, 1980; STERRER, 1998.
• Texas: HEN DRICKSON & KREJCA , 2000 ; HOLSINGER &
LONGLEY, 1980 ; LONGLEY, 1986, 2004; MITCHELL &
REDDELL, 1971.
• Mainland of Mexico: ARGANO, 1972; BOTOSANEANU et
a!., 1998; COLE, 1984; COLE & MINCKLEY, 1966, 1970;
HENDRICKSON & KREJCA , 2000; VILLALOBOS eta!., 1999.
• Yucatan Peninsula: lLIFFE, 1992b, 1993; REDDELL, 1977;
SCHMITTER-SOTO et a!. , 2002; SUAREZ-MORALES et a!. ,
2004; WILKENS, 1982.
• Bahamas, Turks and Caicos: ALVAREZ et a/., 2004;
BOTOSANEANU & lLIFFE, 2003a,b; FOSSHAGEN & lLIFFE,
2004a,b; KOENEMANN et al. , 2003 , 2004; KORNICKER et
al. , 2002.
• Greater Antilles: BRIGGS, 1984; KORNICKER & lLIFFE,
1992; JAUME, 2001; JUARRERO & ORTIZ, 2000; STOCK,
] 977, 1981, 1986b.
• Aruba: BOTOSANEANU & STOCK, 1979.
• Sierra de Perija (Venezuela): BOTOSANEANU & VJLORlA ,
1993.
1\vo types of habitat requiring different explanations for
·
time and mode of groundwater colonization
Despite differences in interpretation of known facts by various authors, most situations may be reduced to two main
types of habitat and groundwater colonization history. The
author having most consistently considered this problem, offering solid generalizations is STOCK (l986a, 1986b, 1994),
and we shall mainly borrow ideas from these publications.
STOCK (1986a:929-930) criticizes the idea that "all stygobionts, be they high-salinity or low-salinity ones, have supposedly evolved to an identical evolutionary scenario and
time-scale". Zones of two distinct types can be distinguished
in the peri-Caribbean and Mexican Realm:
a). Lower ("sinking", or "subsiding") zones more or less recently emerged form the sea, habitats with fully or nearly
fu lly marine water and still in (indirect) contact with the sea:
Bahamas and Turks and Caicos, Cayman Islands , YucatanBelize-Cozumel , near-shore localities of some greater Antilles. For such zones a "passive" (" regression") model of
colonization of relatively recent date is proposed , with
shorter periods available for stygoevolution.
b). Higher ("emerging", or " rising") zones, since long/very
long time not flooded ·by the sea, habitats generally with
freshwater (possibly sometimes slightly brackish), and without contact with the sea: mainland of Mexico, Virginia,
Texas , more or Jess inland localities on some Greater Antilles, Sierra de Perija. For such zones, an " active" model of
colonization is proposed, having started long ago either by
geotectonic positive movements or by eustatic regressive sea .
level movements. This has allowed deeper penetration of the
colonized territories (with , in some cases , impressive "climbing" of stygobionts in the mountains: Zulialana coalescens
to 400 m. a.s.l. , Speocirolana thermydronis to about 600 m. ,
S. pubens to about 800 m., S. endeca to 1460 m., S.fustiura to
more than 1500 m. a.s.l.) .
In other words: the most reliable element for inferring time
and mode of stygoevolution see ms to be the transition from
marine to freshwater. Table 1 summarizes what we know
about stygobitic species belonging to one of the two categori es. The situation of Cirolana (A nopsi/ana ) spp. 1s seem-
,,
Caribbean stygobitic Cirolanidae
Table I
SPECIES BOUND TO
FRESHWATER OR NEARLY
FRESHWATER
SPECIES BOUND TO FULLY
OR NEARLY FULLY MARINE
WATER
Antra/ana lira
Cira/ana (Anopsi/ana) acantlwra
Cira/ana (Anapsilana) crenata
Ciralana ( An a p.~ilan)
cubensis
Cirolana (Anapsilana) pleascissa
Cirolana (Anopsilana) radicicala
Cirolana (Anapsilana) yucatana
Ciralanides texensis texensis
Ciralanides texensis mexicensis
Creaseriel/a a naps
Haptalana belizana
Haptalana bawmani
Haptalana tric/w stama
Haptalana yunca
Mexilana sa/uposi
Speaciralana balivari
Speacira/ana disparicamis
Speocirolana endeca
Speaciralana Just iura
Speaciralana guerrai
Speacirolana hardeni
Speaciralana /apenita
Speacira/ana p e la e~i
Speaciralana prima
Speaciralana pubens
Speaciralana thermydranis
Speaciralana zwnbadara
Sphaerolana affinis
Sphaeralana interstitia/is
Sphaera/ana karenae
Zulialana caa/escens
Aruba/ana arubaides
Aruba/ana imula (?)
Baha/ana caicasana
Baha/ana exu111ina
Baha/ana geracei
Bahalana yagerae
Ciralana (Ciralana) traglexu111a
Exumalana replans
Metaciro/ana 111ayana
" Baha/ana baw111ani"
(~ p ecis
inquirendo)
SPECIES COLLECTED FROM
WATERS OF VARIABLE OR
QUESTIONABLE SALINITY
Aruba/ana parviaculaw
Bahalana cardiapus
ingly contradictory: origin probably not very old, but most
species living in freshwater: a hint to importance of speed of
stygoevolution in different lineages. And, from all points of
view, the situation of Bermuda is a very special one.
How deep are the roots?
It is true that the idea has been expressed (HART et al., 1985;
MANNING et al., 1986) that "marine caves of Bermuda and
the Caribbean" could have been invaded as early as the
Jurassic by ancestors of stygobitic species, thus before the
opening of the Atlantic, on both sides of the forming ocean
(and STOCK, 1986a, ag rees with this idea.) But it is like ly that
the most propitious time for the starting of a flourishing period of stygoevolution in the area was the Cretaceous, a period coinciding with the opening of the Atlantic. As early as
the Aptian time (ca 124 My ago) a Caribbean Province became distinct as result of the Atlantic Ocean spreading in
such a manner that the Caribbean shallow waters became
geographically isolated, gene flow from the East being interrupted. But it is especially during the Late Cretaceo us, aperiod vividly characterized by BRJGGS (1 995) as a mome ntous
period in the Earth 's history whe n - under a greenho use climate - hig h sea leve l had resulted in the formation of extensive epicontine ntal seas, the epicontinental flooding allowing
rivers to deposit sediments in the shallow sea waters. All this
suggests ideal conditio ns for de ve lopme nt of the deep roots
21
of cirolanid stygoevolution and for making from the Western
Atlantic a centre of evolutionary radiation (in contrast with
the faunistically much poorer Eastern Atlantic) and it seems
plausible that the Palaeocene (a period of djsappearance of
the epicontinental seas, a period of shallow, tropical seas, as
result of the fall of eustatic sea level at the e nd of the Cretaceous) was a period of (generic?) di versificafion and establishment of centres of ende mism; and that the appearance of
most present day species occurred from the Miocene through
the Pleistocene.
What is the legacy of Tethys?
The Tethys Sea, restricted prior to the Cretaceous to Medite rranean Europe and the Indo-Pacific, spread westwards in the
early Cretaceous across the developing North Atlantic to the
New World tropics, to form a circumtropic marine belt (ilisrupted during the M iocene). A vast amount of evidence from
practically all groups of stygofauna has accumulated, pointing to the importance of the Tethys in generating distri butional patterns indubitably inherited from this circumglo bal
sea, and we cannot here refer to the vast bibliography on the
subject.
Concerning Cirolanidae we can, first, distinguish a fine case
of what could be called «a loud echo from Tethys»: that of
Haptolana. From this genus, six species are described: H.
trichostoma from Cuba; H. bowmani, H. belizana, and H.
yunca from Yucatan; H. somata M ESSANA & CHELAZZI,
1984, from northern Somalia; and H. pholeta BRUCE &
HUMPHREYS , 1993, from W. Australja (Barrow Island). This
is an exemplary case of a Tethysian pattern of distribution.
Morphological evidence shows that there is close relationship between the three Yucatan species, all well distinct fro m
the Cuban H. trichostoma (BOTOSANEANU & IUFFE, 2000)
and that there is more simjlarity between the Yucatan species
and those fro m Somalia and from Australia (BOTOSANEANU
& lLI FFE, 1997).
O n the other hand, there are «muffled echoes» of Tethys ian
descent which can be traced from re lationships between
stygobitic genera a). in the Weste rn Atlantic and b). in the
Mediterranean sensu lata. T,able 2 (data mainly from
BOTOSANEANU et al., 1986) summarizes what we can say at
present about these re lationships. It is certajn that these data
will be strongly refined in the future.
How could this high biodiversity be explained?
1). Through the rich, turbule nt history of this vast and fragme nted area, with many phases of marine transgressio ns/regress ions affecting its various parts, and with alte rnatingly
rising and subsiding zones eithe r continental or never having
been part of a continental block. C limatic changes, altho ugh
not particularly severe, have certai nly been very important; a
factor of paramount importance in the passive colonization
of subte rranean habitats by marine ancestors of stygobionts
(see BOTOSANEANU & HOLSINGER, 199 1) has been represented by the strong tro pical storms sweeping the area. With
respect to all thi s, the contrast with, for instance, the eastern
II
22
T. M. ILIFFE & LAZARE BOTOSANEANU
Table 2: Genera of stygobitic Cirolanidae in two geographically disjunct
groups with Tethysian ties.
Mediterranean (sensu Jato)
West Atlantic
"Cirolana-group"
Creaseriella
Haptalana
Haptalana
"Sphaeromides-group"
Antra/ana
Ba/ralana
Cirolanides
Mexilana
Speociralana
Metacirolana
Sphaeromides
"Typhlocirolana-complex":
Typlr/ociro/ana
Turcalana
Maraca/ana
Metacirolana
"Faucheria-group"
Sphaerolana
Faucheria
Kensleya
Skatabaena
N.B. The position of Aruba/ana, Yucatalana , Zulialana, and Exumalana in
such a table is at present uncertain.
Atlantic is considerable.
2). Through the abundance and extraordi nary diversity of
habitats propitious for stygoevolution (see "The stage" for
detruls). This has too, certru nly been of paramount importance in determining the present-day diversity of Cirolanidae
and other stygobionts.
3). Through the supposed abundance and high diversity of
potential marine ancestors. If we consider the present-day
fauna of marine-epigean C irolanidae in the area (KENSLEY &
SCHOTTE, 1989 enumerate only 24 species in five (four) genera for the Caribbean not including the Gulf of Mexico; from
an in litteris information from N.L. BRUCE, we learn that
from the whole western North Atlantic, 35 species in 16 genera are recorded at present) this does not seem particularl y
rich (STOCK, 1994 observes that "the number of stygobiont
taxa is always much higher than the number of marine taxa of
the same genus"). Of course, our exact knowledge about the
ancestors of stygobitic Cirolanidae is extremely limited; nevertheless, there is evidence from palaeontology about the
marine fauna of the area having been particularly rich duri ng
the Cretaceous.
Endangered or already destroyed habitats and fauna:
a plea for protection.
At least three stygobitic ciro lanids are curre ntly on endangered species lists. Arubolana aruboides and 24 othe r
stygobitic taxa from Be rmuda are considered as "critically
endangered" on the IUC N Red List. Creaseriella anops
from Yucatan is listed as threatened in the official Mexican
e ndangered species list - Ia Norma Of icial Mexicana (NOM059-ECOL-2001 ). Antrolana lira from Virginia is designated
as threatened by the U.S. Fish and Wildlife Service.
Futhermore, a number of signjf icant habitats are threate ned .
C uatro C ienegas, or "Four M arshes", located in Mexico 's
C hihuahuan Desert has been set aside as a biological reserve ,
but is still threate ned by mining of gypsum and inc reased rec-
reational use. Bermuda caves inhabited by Arubolana
aruboides are threatened by groundwater pollution, quarrying of limestone and development (lLIFFE et al., 1984; lLIFFE,
2003). Many cenotes along the Caribbean coastline of the
Yucatan Peninsula have been set up for use by recreational
scuba divers. An epigean fish, Asf) anax mexicanus, which is
normally restricted to surface pools• of the cenotes has
learned to follow divers into the caves, feeding off stygobitic
crustaceans illuminated by the diver 's lights. Considering
that some caves are visited by hundreds of divers each week,
the cave fauna of the entire area has been severely impacted
and in places is locally extinct. So-called "deep well injection" (to 30 to 100 m depths) of partially treated sewage and
other waste waters going on in Bermuda and the Yucatan Peninsula, among other areas, is particularly troubling. Cave
and groundwater are naturally depleted in dissolved oxygen
due to limited contact with the atmosphere, long residence
times of the water and absence of photosynthetic oxygen production. Enrichment of subterranean waters with excess organic material in the waste water stimulates growth of bacteria, consumption of the limited oxygen and results in anoxia,
anaerobic hydrogen sulfide production and extermination of
all aerobic organisms.
Acknowledgements
L. BOTOSANEANU traveled to Galveston, Texas, for two
weeks of work with Th. M. ILIFFE, thanks to a grant from the
Netherlands Organization for Scientific Research (NWO).
Dr. N.L. BRUCE (National Institute of Water and Atmospheric Research, New Zealand) kindly replied to several
questions asked by the authors and also offered other useful
suggestions. In addition to a grant from the Biodiversity Surveys and Inventories Program of the National Scie nce Foundation (DEB-03 15903) toT. ILIFFE, other support and assistance with field studies has already been cited in resulting
publications.
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Thomas M. lLIFFE
Department of Marine Biology
Texas A&M University at Galveston
Galveston, TX 77553-1675, USA
E-mail: iliffet@tamug.edu
Lazare BOTOSANEANU
Zoologisch Museum
Universiteit van Amsterdam
Plantage Middenlaan 64
1018 DH Amsterdam
The Netherlands