Table Of ContentBijdragentot deDierkunde, 63 (3) 149-161 (1993)
SPBAcademie Publishingbv, The Hague
Phylogeny and biogeography of the Niphargus transitivus group of species
(Crustacea, Amphipoda)
Boris Sket & Jos Notenboom
of Biology, BiotechnicalFaculty, University ofLjubljana, Askerceva 12, 61000Ljubljana,
Slovenia; 2NationalInstitute ofPublicHealth andEnvironmentalProtection, P.O. Box 1,
3720BA Bilthoven, TheNetherlands
Keywords: Amphipoda, Niphargus, phylogeny, zoogeography
Abstract 1. Introduction
The Niphargus transitivus group includes 12 groundwater- TheNiphargustransitivusgroupwas introducedby
dwellingspecies. Itisdefinedbyanuprightbodypositionduring Sket(1971) to delimitate fourspecies ofNiphargus
locomotion,a small,stoutbodywithshortappendages, except Schiödte, 1849,whichontheonehandwereallvery
forlongcoxaeanddactyli,coxaeV-VIequilobateorposterolo-
aberrant, but on the other hand intermediatein
bate,accessory flagellumsubjecttoreduction,andthebody en-
dowed with adaptationsfor volvation (=abilityto enroll into somecharactersbetweenN. kochianusBate, 1859,
a ball). and KaramaniellaSket, 1962.Thelattergenuswas
The biogeography of this southeastern Europeangroup of erected for K. pupettaSket, 1962,aspecies which
speciesisdiscussed and acladistic analysis ofthe groupispre- didnot fit withinthe Niphargus diversity spectrum
sented. Some cases ofparallel character evolution in ground-
at thetime. At presentKaramaniellais considered
wateramphipodsarementioned. Theinference ofbiogeograph-
ic and phylogeneticinformation inelucidatingtheevolutionary synonymous with Niphargus, and K. pupetta has
history ofthe group is hamperedby inconsistency ofthe data. beenincorporated intotheN. transitivusgroup(cf.
One ofthe hypotheses about the evolutionary history of the Sket, 1972: 106, 111; Karaman, 1975). For the
groupis thoughttobe the mostparsimonious. relatedbut morphologically very distinctK. para-
doxa(Sket, 1964) thegenusCarinurellaSket, 1971,
Résumé hasbeen established.
SinceestablishmentoftheN. transitivusgroup,
Le groupe transitivus du genreNipharguscomprend12espèces several additional taxa have been described by
souterrains. Ilestdéfini surtoutparlapositionverticale du corps
Dancàu (1971), Karaman (1972, 1984a, 1989), and
pendantledéplacement,par uncorps petitettrapuauxappen-
dices courts (àl’exceptiondes longuescoxaeetdactyli),par les Karaman& Sket(1991). Moreover,afterreanalysis
coxaeV-VIequilobésouposterolobés,parleflagelleaccessoire of the previously known but insufficiently de-
sujetà uneréduction accusée, etpar le corps doué d’adaptions scribedN. kochianus longidactylus Ruffo, 1937, it
permettantlavolvation. appeared to belong to theN. transitivus groupas
Labiogéographiedecegrouped’espècesd’EuropeduS.E.est
well (cf. Sket, 1971; Karaman, 1981).
discutée et uneanalyse cladistique est présentée. Sont men-
tionnéscertainscasd’évolution parallèledes caractèreschez des
Amphipodessouterraines. L’utilisation de l’information bio- Altogether 12 nominal species are now consid-
géographiqueetphylogénétiquedans le but del’élucidation de eredas theN. transitivusgroup,andwedecidedto
l’histoireévolutive du groupeestrendue difficileparlecaractère
treatthesystematics, phylogeny, andbiogeography
contradictoire des données. Une des hypothèses sur l’histoire
évolutive du groupe est considérée comme étant la plus par- ofthisgroupofNiphargusspecies moreproperly as
cimonieuse. a whole.
150 B. Sket & J. Notenboom - Phytogeny andbiogeography of theNiphargus transitivusgroup
2. Definition and peculiarities of the Niphargus west Bosnia(Ruffo, 1937; D'Ancona, 1942a& b;
transitivus group Benedetti, 1942; Karaman, 1981; Sket &
Velkovrh, 1981).
2.1.List ofspecies and distribution • N. transitivus transitivus Sket, 1971; found
directlyininterstitialwaters andinwellsalongPi-
The following taxa compose the N. transitivus aveandTorreinnortheastItaly, occasionally also
group: in caves at the karst margins in the same area
• N. carcerariusG. Karaman,1989;only two speci- (Sket, 1971; Karaman, 1975, 1984a, 1985).
mens (!)found inasmallcave lakenear Pljevlja • N. transitivusdissonusG. Karaman, 1984; found
(caveofSljivanski potoknearDjurdjevica Tara), in wells in the Bergamo region, northern Italy
northernMontenegro (Karaman, 1989). (Karaman, 1984a, 1985). Sket (1971) opened the
• N. asper G. Karaman, 1972; only one specimen question ofapossible conspecifity ofN. transiti-
(!) foundina wellnear Podgorica (= Titograd), vus withN.pupetta,according to thegreatvaria-
Montenegro(Karaman, 1972). bility of someN. transitivuspopulations. Kara-
• N. factorG.Karaman&Sket, 1991; inhabitantof man (1975) deniedthis possibility sincehe found
small cave lakes inlower parts ofPopovo polje no intermediatespecimens in mixedpopulations,
(Vjetrenica at Zavala; Baba pecina at Strujici), but we think that more materialshould be ex-
southeastHercegovina (Karaman & Sket, 1991). aminedbeforethe last decision is conclusive.
This species is very similar to N. asper,bothmay • N. pupettapupetta (Sket, 1962) (syn.: Karama-
be varietiesof a single species. niella pupetta Sket, 1962); found in interstitial
• N. brevirostris Sket, 1971; only two specimens (!) waters and wells in Bergamo and probably in
foundininterstitialwaters oftheGacko polje (at Bellunoregions in northand northeast Italy, as
Licko Lesee) in Lika, southwest Croatia(Sket, well as innorthwest (Bovec, new data), central,
1971). andeastern Slovenia(Sket, 1962,1972; Karaman,
• N. numerus G. Karaman& Sket, 1991;only one 1975, 1984a).
specimen (!) foundin asmallresiduallake ofan • N.pupettaparapupettaG. Karaman, 1984(syn.:
active cave near Zrmanja River (Cavlinska peci- N. parapupetta in Karaman, 1984a, and Kara-
na), near Obrovac, northern Dalmacija (Kara- maniellapupetta in Dancâu, 1972); foundin in-
man& Sket, 1991). N.brevirostrisandN. numer- terstitial waters and wells near Zagreb, western
usalso show many similarities pointing to their Croatia, and near the river Dunarea-Dunav
possible conspecifity. (Danube) in southwestRumania.This taxon was
• N.pectinicauda Sket, 1971; inhabitantofintersti- describedas aseparatespecies. Sinceit seems to
tial waters of theSavaRiverbetween Bohinj and becompletely allopatric to N.p.pupetta,andthe
Ljubljana, northwest Slovenia(Sket, 1971; Sket differencesare extremely small, we now suggest
& Velkovrh, 1981). that both taxa are conspecific.
• N. rostratusSket, 1971;foundin smalllakesofa • Carinurellaparadoxa (Sket, 1964) (syn.: Kara-
cave near Cetina River (Dragica pecina at Malj- maniellaparadoxa■Sket, 1964); found inintersti-
kovo), centralDalmacija, Croatia(Sket, 1971). tial waters of the lower reaches of Soca-Isonzo
• N. alutensis Dancâu, 1971; probably an inhabi- and its tributaries: Vipava, Torre-Ter, and
tant of interstitialwaters of the Olt River valley Nadiza-Natisone, all on both sides of the Slo-
(found in wells, village Jilbea), south-central veno-Italianboundary (Sket, 1964, 1971, 1972).
Rumania(Dancâu, 1971). Although attributedto aseparategenus, thisspe-
• N. longidactylus Ruffo, 1937;inhabitantof inter- cies has drawn much concern. The acceptability
stitial waters, ableto buildlarge populations in ofmakingthegenus(Niphargus) paraphyletic has
open wells near rivers outside karst areas, in been discussed elsewhere (Sket, 1990).
northeast Italy, and in central and northeast
Slovenia, northwest Croatia, central and north- Inconclusion, therepresentatives oftheN. transiti-
Bijdragen tot deDierkunde, 63 (3) - 1993 151
vus group are not all sufficiently characterized, 2.2. Characterization ofthe N. transitivus group
primarilybecauseoflack ofmaterial. Information
aboutmorphological variationwithinandbetween 2.2.1. Analysis ofcharacters. - Themostconstant
adjacent populations is lacking and the possibility characters of the Niphargus transitivus group
that some of the nominal species are merely in- (some apparently synapomorphies) are: body size
traspecific varieties must be considered. smallto verysmall, stoutand upright-walking; cox-
Thegroupincludestaxa that areevidently mem- aeofpereiopods II—III very deep, atleasttwiceas
bers of the benthos in larger water bodies of the deep as wide; coxa of pereiopod V equilobate or
karst; a quite remarkable feature, since in the posterolobate, thatof VI posterolobate; bases of
Dinarickarst such anecology is mostlyexhibitedby posterior pereiopods broad, with widely rounded
larger niphargids of a centimetreor larger. Other distoposterior lobes; dactyli of pereiopods very
membersof thegroupinhabitinterstitialwaters in slender and long; gnathopods basically of theN.
river valleys, some also in hilly country (N. lon- kochianus type(synapomorphy ofawidergroup?).
gidactylus), butall species maybuild denserpopu- However, there exists a number of characters,
lationsin openwells - eitherinresponseto greater present in some of thetaxa, that are functionally
space or to richer food supplies that are usually connected by the above-mentionedcharacters and
present there.Therefore, the groupas a whole, as absent in other niphargids.
wellas someofthespecies, appearsas quite ubiqui- Wewilltrytoevaluateall specific characterstates
tous stygobiontic animals. Some species (N. bre- appearing in the N. transitivus group. Character
virostris, N. numerus, andN. asper) were found in state polarity is determinedmainly by comparison
so few numbers that their ecology remains un- withspeciesoftheN. kochianuscomplex which ap-
certain. parently is the most closely related totheTV. tran-
Theknown distributionareaofthegroupreaches sitivus groupand consideredas a sister group.
from Bergamo in northernItaly to theOlt Riverin Habitus: The body is small to extremely small,
Rumania; below the southern slopes of the Alps short and broad, not depressed; the stout appear-
andalongthesouthernpartsoftheDanubesystem, ance is emphasized by deep coxae and short distal
aswellas intheDinarickarst. Whilecave species of parts ofappendages.N. carcerarius, with alength
the Dinarickarst seem verylimitedin distribution, of 11mmormore, isby farthelargest member,but
rangesofinterstitialspecies maybeextraordinarily its taxonomieposition within the groupis uncer-
extended. Comparable zoogeographical connec- tain. All other taxa are only 2-6 mm long, being
tionsbetweennortheasternItalyandsouthernparts amongthesmallestoftheniphargids. Theurosome
ofthe Danube system have already been notedin hasbeengreatly modifiedinCarinurellaparadoxa.
othergroups(e.g., Sket, 1972, and inprep.). They Rostrum: Some species ofthis groupare excep-
obviously originated under influence of cor- tionsamongniphargids, having aconspicuous ros-
responding paleogeographical events. trum. In most taxa it is only slightly indicated. In
Thereexists anumberoftaxaintheJV.kochianus N. brevirostris itis well developed, anditisexceed-
group, showing somesimilarities withmembersof ingly long (equalto lateralcephalic lobes) inN.ros-
theN. transitivus group(e.g., slender dactyli, see tratus. As this featurewas neglected untilthe dis-
TV. wolfiSchellenberg, 1933,andN. “kochianus” coveryofthisgroup, itis impossible toestablishits
melticensis Dancâu & Andreev, 1973). Supposedly condition inother niphargids.
thesimilaritiesofthesetaxa are homoplasies, since Epimera: The ventroposterior angles of the
a high probability exists for convergent character epimera in niphargids are rounded or obtuse, to
evolution in niphargids (mosaic evolution). Of acute. Either ofthese shapes seem to have devel-
course,prior to a detailedanalysis ofthe wholege- oped convergently, butitisoftenquiteconstant for
nus itisimpossible toknow whethertheN. transiti- larger groups of taxa. In the groupstudied, only
vusgroupis delimitedcorrectly (i.e., ifthegroupis N. carcerariusexhibitsrectangular angles, whereas
monophyletic). epimeral plates in all other species end in acute
152 B. Sket & J. Notenboom - Phytogeny andbiogeography of the Niphargus transitivusgroup
angles. Withtheabove-mentionedexception, inall of maxillaI is variablein niphargids. Most mem-
species oftheN. transitivusgrouptheventral (i.e. bers ofthe groupstudied exhibit alownumberof
apical) parts of epimera II—III (sometimes I—III) setae, with exception ofN. carcerarius which has
are strongly produced in ventrocaudal direction. more than fivesetae.
Submarginal spines along the ventral margins of The denticulationofspines on the outer lobeof
the epimera, present in a modest numberin most maxilla I seems to be a quite variable character,
niphargids, may completely disappear. perhaps enabling even populations (subspecies) of
Telson: The telson is always longer than wide, somespecies to adaptthemselvesto particularfeed-
witha deep incisionand narrow lobes, usually pro- ing conditions.Intheanalyzed group usually none
videdwith distalspines and dorsalpairs ofpennate or only the innermost spine is comb-like, but in
setae. Insomespecies, thetelsonis extremely elon- some taxa (N. longidactylus, C. paradoxa) there
gate, with very short spines (e.g., N. transitivus); may bethree or more such spines.
dorsalsetae are sometimesmovedto anearly distal Pereiopods I—IV: Coxae ofanterior pereiopods
position. N. longidactylus, an exception in this (particularly II-III) areinmost niphargids only up
group, has comparatively long dorsal spines; we to 50percent as long as wide. In all species of the
suggestthis isofsecondary appearance,andthere- N. transitivusgroup,they areatleast twice as long
fore an autapomorphy. as wide.Theprobably primarilywideneddistalpart
AntennaI: The basal articleof antenna I tends of coxa IV (in N. alutensis, N. rostratus, and N.
toextend dorsodistally forming a"visor". Such a carcerarius) is in this group mostly only slightly
visorseems tobelacking insometaxa(e.g.,N.pec- widened(in N. asperandN. longidactylus) orbow-
tinicauda, N. asper), while only slightly markedin shaped andparallel-sided (in remaining species).
others (e.g., N. alutensis, N. rostratus), and ex- Gnathopods :Article6 isoriginally elongatedand
tremely developed inN. pupettaandC.paradoxa. subrectangular, with subparallel anterior and
Incertain populations ofN. transitivus (from the posterior margins. InsometaxaoftheN. transiti-
Piave River; cf. Sket, 1971; Karaman, 1985), the vus group,themargins convergeinproximal direc-
antenna I is highly variable. The antenna I also tion, givingthearticleatriangularshape. Thenum-
tendsto shortenits flagellum, resulting inareduced berof transverse posterior rows of setae isreduced
numberofarticles. insuch cases, mostlyto onlytwo. Thepalmar mar-
Allniphargid amphipods exhibitareducedacces- ginof gnathopod IImakeswiththeanteriormargin
sory flagellum, generally withtwoarticles. Thedis- of the articlein most niphargids an acute orright
tal articlemaybe very shortinseveralspecies, such angle, which angle maybecomeobtuse by bulging
as in N. carcerarius and particularly in N. pec- of thecentraland/orposterior ( = angular)part of
tinicauda, N. longidactylus, andin NJ . asper. In the palma in distal direction.
brevirostris, it is shorter than the diameterof the Insome species, thelength ofarticle5 increased
proximal article. InN.factor, itis presentor miss- in relationto article 6 and may become even re-
ing. In.N.rostratus,N. transitivus, andTV.pupetta, markably longer than article 6. The originally
the accessory flagellum seemstobealways uniartic- higher numberofsetae on thedactyli(= article 5)
ulateand sometimesvery short. is in this group(and in many other small species)
AntennaII\N. rostratusandN. brevirostris seem usually reduced to 1-3.
to be an exception among niphargids, having aes- Pereiopods V- VI, coxae: The coxae of the
thetascs on both antennae I and II. posterior pereiopods are innearlyallotherniphar-
Mandibularpalp: Article3is longerthanarticle gids anterolobate.Inthetaxaincludedhere, coxaV
2 in most niphargids. In this group,it tendstobe- is equilobate or posterolobate, whilecoxa VI is al-
come shorter with reduced setation. This is not ways posterolobate. Theanterior lobeincoxa VIis
foundinN. rostratus, N. pectinicauda, andN. car- usually lacking.
cerarius. Pereiopods V- VII, bases: These articles have a
MaxillaI: Thenumberofsetaeon theinnerlobe rounded distoposterior lobe in many niphargids.
Bijdragen tot deDierkunde, 63 (3) - 1993 153
Some members of this group, however, have at lutionary "trend" ofthis groupof species, are re-
leastpereiopod Vdeveloped withanadditionalan- latedto theupright poise and the following ability
terodistallobe, resulting in an almost rectangular to enrol moreor less into anirregular ball (volva-
basis. Whilethe posteriormargins ofbases VI—VII tion). This upright position seems to be a general
are sometimesbroadly rounded as well, in N. lon- trait ofthis groupof species.
gidactylusthebases V-VII are almostrectangular. Inniphargids, thetransitionfromtheusualloco-
Pereiopods V—VII, distal articles: Article 4, motionon theflankto theupright poiseis connect-
originally narrow androd-shaped or withamoder- ed by widening ofthe previously laterally flattened
ate posterior bulge, may develop alarge posterior body. IntheN. transitivusgroup,theupright poise
lobe, making thearticle very broad. In some spe- is facilitatedalso byashortening oftheentirebody.
cies, the posterior pereiopods tendto shortentheir Shortening ofthe distalpartsof some appendages,
distalparts(we expressed thesestates intherelation likeantennae andposterior pereiopods, seems tobe
between lengths ofarticles 2and4+5 +6 inpereio- the next step in this direction, achieved only by
pod VII). However, most taxaof this grouphave somemembersofthegroup.Probably, thedeep an-
particularly thin dactyli, mostly due to elongation terior coxaeand theparticularly slender dactyliof
ofnailsinrelationto socles. Theelongation ofdac- the posterior pereiopods are apartofthistendency
tyliinrelationto article6 is probably only aresult as well.
ofthenailelongation. Dactylihave only inN. pec- Posterolobateposterior coxae are extremelyrare
tinicaudaandN. brevirostrisastronginnerspine or characters in niphargids. Supposedly they allow
spine-like seta; in most species it is reduced to a anotherdirectionofthepereiopod movement than
fragile seta. is possible inthe anterolobateones. However, this
Uropods I—II: Only inN. pectinicauda theorigi- supposition must be experimentally confirmed.
nally moderatenumberofspines along each ramus Bousfield (1983) considers posterolobate coxae
has increased. plesiomorphous, asupposition which maybe cor-
Uropods III: Originally they are moderately rectfor Amphipoda ingeneral, butwithinthegenus
long, but they tend to become particularly short, Niphargus it is correlated with so many other
resulting also ina reduced numberoflateralspine peculiarities (see below), thatitevidently has been
groups. Seemingly, the exopodite developed its achieved secondarily. The next step in the same
shape by progressing from flattenedthrough rod- directionhas obviously beenan "inversion"ofthe
shaped to subcorneal; unfortunately, thedegree of pereiopod V, or/and VI, carried out by the de-
flatness is sometimesdifficulttoassess. This limb velopment of a distallobeon the anterior side of
underwent an extreme shortening, connected by theirbases. In this context, wemayalsoexplain the
further reduction of the terminal article, in convexity ofthe anterior margin and straightening
Carinurellaparadoxa. ofthe posterior one.
The above-mentionedmorphological modifica-
2.2.2.Functional relation of characters. - Some tions enablesometaxa torollintoamoreor less ir-
characters, like pectinate spines on maxilla I and regular ball. This volvation is in fact occasionally
aesthetascs onantenna II, areprobably theresultof recorded inN.alutensis(cf. Dancâu, 1972). Volva-
special adaptations. Others, like the reductionof tionhasbeen developedfurtherinN.pupettaby the
accessory flagella on antenna Iandreductionofin- characteristic transformationof theproximal arti-
ner spines on dactyli, couldbethe resultofneutral cle inantenna I, as wellas by widening ofproximal
mutations.Someparticularities in the shape ofthe articles and shortening of distal ones (except for
gnathopods as well as reductive processes in the dactyli) in hind pereiopods. The niphargids' last
mandibular palp's terminal article might be ex- achievementinthisdirectionis C.paradoxa withits
plained by paedomorphosis, and this is supported completely modifiedposteriorpartofthebody and
by the morphology of juvenile niphargids. The the strongerincrustation oftheintegument. Unfor-
mostextraordinary characters, designatingtheevo- tunately, the ethology of other species is virtually
154 B. Sket& J. Notenboom - Phylogeny andbiogeography ofthe Niphargus transitivusgroup
TableI.Charactersusedforphylogeneticanalysis oftheNiphargustransitivusgroupandtheir plesiomorphousand apomorphousstates
(forfurtherexplanation,seetext): 0 =plesiomorphousstate, 1 =apomorphousstate.
1. Bodylength:
a.(0): > 10mm;(1): < 8mm.
b. (0): > 3mm; (1): < 3mm.
2. Rostrum:
(0):indistinct or very small;(1)longer than 50°7o oflateral head lobe.
3. EpimeronIII, angle:
(0)right;(1)acute.
Intheconstruction ofthe cladogramit hasbeen supposedthatthe seeminglyplesiomorphousstatein Carinurellaihasbeenachieved
secondarily;this suppositionis supportedby anextensive remodelingofthe entire abdominal partin this species.
4. Epimera:
(0)normal;(1) extended in ventrocaudal direction. For Carinurella asin "3".
5. SpinesofventralmarginsofepimeronIII:
(0) 2-3 spines;(1)0-1 spine.
6. Urosome:
(0)normal;(1) greatlymodified.
7. Spinulationoftelson:
(0) dorsal spineslacking; (1) dorsal spinespresent.
8. Pennate setae ontelson:
(0)in ornearthe middle ofthe telson length;(1)apicallyorsubapically.
9. Antenna I, basal article:
(0)without or with small "visor"; (1)visor longer than diameterof article,orvariable.
10. Antenna I,number of flagellararticles:
(0) 9or more; (1)8 orless.
11. Antenna I,accessory flagellum:
(0)regularlywith 2articles; (1) 1 article orvariable.
12. Antenna II, aesthetascs:
(0)absent;(1)present.
13. Mandibular palp article3:
(0)length > article 2; (1)length < article 2.
14. Maxilla I,inner lobe:
(0) 1-3 apicalsetae; (1) 5 ormoreapicalsetae.
15. Maxilla 1, outerlobe:
(0)noneoronly innermost spinecomblike; (1) 3or morecomblike spines.
16. Coxae II—III:
(0)twice aslongaswide;(1)morethan twice aslongaswide.
17. Coxa IV:
(0) distoposteriorlobe large; (1)coxaonly slightly wider in its distal part orparallel-sided.
18. Gnathopods,article 6:
(0)subrectangular,withsubparallelanteriorand posteriormargins;(1)marginsconvergeproximally,givingthearticle atriangular
shape.
19. GnathopodII, article 5:
(0)upto 110% oflength ofarticle 6; (1)longer.
20. Gnathopods,dactyli:
(0)morethan 5outersetae; (1) 1-3 outersetae.
21. GnathopodII,palmarmargin:
(0)makes withanteriormarginofarticleanacuteorrightangle;(1) mentionedangleobtuseby bulgingofthecentral orposterior
(= angular)part ofpalmain distal direction.
22. CoxaV:
(0)equilobate;(1)posterolobate.
23. PereiopodV, article 2:
(0) without ananterodistal lobe; (1)with anterodistal lobe.
24. PereiopodV, article 2:
(0)posteriormarginconvex; (1)posteriormarginstraight.
Bijdragen tot de Dierkunde, 63 (3) - 1993 155
Table I. Continued.
25. PereiopodVII, article2:
(0)posterior marginconvex; (1)posteriormarginstraight.
26. PereiopodV-VII,article 4:
(0)narrow; (1)with aposterior lobe, makingitswidth equaltoor largerthan Vj ofthe length.
27. PereiopodsVII,relation betweenlengthsofarticles 2 and 4+5+6:
(0)art.2 < (art. 4+5+6);(1)art. 2 > (art. 4+5+6).
28. PereiopodsV-VII,dactyli:
(0)nail shorterthan socle;(1) nail equaltoor longerthan socle.
29. PereiopodsV-VII, dactyli:
(0)with inner spineorspine-like seta;(1)with tender seta.
30. PereiopodVII,dactylus:
(0)article 7 shorterthan 'A ofarticle 6; (1)it is longer.
31. UropodI,endopodite:
(0)with 5 orless spinesalong itsupper side;(1)with 6ormore ofsuch spines.
32. UropodIII, proximal articleof exopodite:
(0)number of lateral spinegroups ononeside morethan 3; (1)number ofsuch groups is 3or less.
unknown, exceptforN. longidactylus, whichis not to N. pupetta or even to C. paradoxa.
ableto volvate. Theonlypartial parallel withinthegenus Niphar-
It seems plausible that Carinurella developed gus has been observed in the N. steueri Schellen-
from aN. pupetta-like ancestor by somenew aut- berg, 1935 "Rassenkreis". N. steueri probably
apomorphies and character reversals (characters 3 belongs to thewiderN. orcinusJoseph, 1869aggre-
and4, seeTableI), whichinthemodifiedbody ap- gate. All its races are characterized by compara-
parently received another function. tivelyshort antennaeandpereiopods, deepanterior
coxae, wide bases of posterior pereiopods, and
2.2.3. Some analogies. - There are a number of rather narrow gnathopod article 6; making this
amphipod taxathat haveconverged ontheN. tran- comparatively large species resembleplesiomorphic
sitivusgroupeitherby retaining orregaining some speciesoftheN. transitivusgroup.Insomeraces of
characters in connection with similar movement N.steueri, however, the coxaeV-VIareequilobate
techniques. A good representative of them is the orposterolobate andthebasisofpereiopod VIpos-
Synurella ambulans (F. Miiller, 1846) "Rassen- sesses a small anterodistal lobe (cf. Karaman,
kreis" withasimilarbody shape, long anteriorand 1984b). In N. steueri liburnicus G. Karaman &
posterolobate posterior coxae, shortened uropods Sket, 1989,theanterodistallobeisdeveloped onall
III, and in some populations also shortened arti- posterior pereiopods (V-VII) and uropod III is
cles4-6and long dactyli of posterior pereiopods. shorterthaninanyotherknown population ofthe
An interesting convergencewith the N. transitivus species (Karaman & Sket, 1989).Thisvariablespe-
groupisalso shown by Parapseudoniphargus bae- cies of the centimetre category will be the most
tis Notenboom, 1988 in the Pseudoniphargus- suitable subject for experimentation, which could
Parapseudoniphargus complex and particularly by show us the functional nature of the transforma-
Parasalentinella rouchi Bou, 1971 (Bou, 1971; tions in posterior pereiopods.
Notenboom, 1988a). The latterhas obviously de-
scended from a Salentinella-like ancestor, which
resembled some taxa of the groupanalyzed here 2.3. Cladisticanalysis
in a numberof characters. In P. rouchi, in con-
nection withvolvation, there are also "visors" on 2.3.1. Selectionof character states. - An attempt
the proximal articles of antenna I, and extremely was made to establish phylogenetic relationships
shortened caudal appendages, making it similar withinthegroupby cladisticanalysis. According to
156 B. Sket& J. Notenboom - Phytogeny and biogeography of theNiphargus transitivusgroup
TableII.Distribution ofcharacterstatesintheNiphargustransitivus group(for descriptionand definition ofcharactersandtheir states,
seeTable I and text):0 =plesiomorphousstate, 1 =apomorphousstate,? = character stateunknown.
la lb 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
CA N. carcerarius 00000000000000100
AS N. asper 1001 1000000000001
FA N. factor 101 1 1000000101001
RO N. rostratus 11 111100100110001
PE N.pectinicauda 1001 1 100000000001
LO N. longidactylus 1001 1 101000001010
AL N. alutensis 11011100101000000
NU N. numerus 10011100001100001
BR N. brevirostris 10111100001010001
TR N. transitivus 17011100010101001
PU N. pupetta 11011100011101001
CP C. paradoxa 10011110011101011
17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32
CA N. carcerarius 0000000000001000
AS N. asper 0001001 100001001
FA N. factor 1001001000001101
RO N.rostratus 0001 10000001 1 100
PE N.pectinicauda 1001001 100000010
LO N. longidactylus 0011117110011100
AL N. alutensis 0111001100011701
NU N. numerus 1001001101111101
BR N. brevirostris 1001101100110101
TR N. transitivus 1111010100111101
PU N. pupetta 111111110 111110 1
CP C. paradoxa 1111110 11111110 1
thediscussionintheabovesections,asetofcharac- characterstatechanges inorder to explain the pat-
ters was chosen and we tried to definetheir most ternof characterstate distributionamongthetaxa.
representative and exactly measurable states. The The most parsimonious cladograms found under
selectedcharactersare giveninTableIandtheirdis- similarpremises wereevaluatedby comparing their
tribution over the species inTableII. topologies andthedistributionofsynapomorphies.
The consistency index is used as a tool for clado-
2.3.2. Numerical cladistic analysis. - The data gram comparison; it is defined by the theoretical
matrix of theN. transitivus group(Table II) with minimumnumberofcharacter statechanges divid-
theexclusionofautapomorphous (6, 7, 14,31) and edbytheactualnumberofchanges. Theconsisten-
doubtful(la, 15, 20, 29) characters has been ana- cy index is 1 in case cladograms containno homo-
lyzed with the MIX, PENNY, and CLIQUE pro- plasies. Rooting of cladograms is doneby specify-
gramsofthePHYLIPphylogeny inferencepackage ing the ancestral states for each character. Strict
(Felsenstein, 1987) version 3.01. Cladograms were consensus cladograms are constructed onthebasis
constructed under Wagner (Eck & Dayhoff, 1966; of PHYLIP CONSENSE. Compatibility analysis
Kluge & Farris, 1969)and Camin-Sokal(Camin & (Le Quesne, 1969) is performed by PHYLIP
Sokal, 1965)parsimony options. UndertheCamin- CLIQUE. Thismethodsearches forthelargest col-
Sokalcriterion, characterreversals are not permit- of mutually compatible characters
ted. Theparsimonyorientatedprograms(MIXand (clique(s)).
PENNY) attempt to minimize the number of Compatibility analysis ofthe datashows a high
Bijdragen tot deDierkunde, 63 (3) - 1993 157
To facilitate discussion, the third subset is
consideredthe N. transitivus group s. str.
Parsimony analysis of all data leads to a large
number(+ 100)ofequally parsimonious cladistic
solutions. The consistency indices of the clado-
gramsconstructedwiththeWagnermethodis0.45,
and0.40when the Camin-Sokalmethodis chosen.
The differentsolutionsshow littleagreementinthe
monophyletic groups they support.
To arrive at amoreconsistent picture, thechar-
acters not present inanyoftheten largest cliques,
thus those with a high probability of not being
homologous, are excluded from analysis. The
cladograms constructed with this reduced dataset
are allsimilarintopology andinthe monophyletic
groups they support, whether obtained under
Wagner orCamin-Sokaloptions. They always have
a consistency index of 0.75. However, thereis no
unique dichotomoussolutionindicating that poly-
chotomousbranching patterns exist that couldnot
be resolved. The consensus of the cladograms
generated underbothparsimony options isgiven in
Fig. 1A.
Thereare someargumentsinfavourofgiving the
characters4, 5, 10, 24, 27, and28, a greaterimpor-
Fig. 1. StrictconsensuscladogramsoftheN. transitivus group tance in the phylogeny reconstruction. Therefore
constructedby numerical cladistic analysis (seetext forexplana- all numericalanalyses performed have been exe-
tion). Species name abbreviations are explained in Table II. cutedwithbothweighed andunweighed characters.
Matching synapomorphies indicated only, uniquely derived
However,a weighing procedure has not resultedin
characters underlined, character state reversals indicated by
minus-sign. A, cladogram identical for both Wagner and a different class of cladistic solutions. The whole
Camin-Sokal parsimony analysis; B, cladograminferred by argumentin favourof a greater weight for certain
Wagnerparsimonymethod after secondaryanalysis ofthe N. characters has thereforenot been treatedin more
transitivus group s.str.; C, sameasB, but inferred usingthe detail.
Camin-Sokal parsimony method.
Asecondary analysis oftheN. transitivusgroup
s. str. hasbeen executedwith parsimony methods.
level of inconsistency. Ten largest cliques of 8 The ancestral character states of this group have
characterseachare found.Fivecharacters(3, 4, 12, been estimated using outgroups (other species of
19,30) are intheintersectionofallthesecliques and theN. transitivusgroups.l.)andparsimony, apply-
12 characters (lb, 2, 3, 4, 5, 9, 12, 18, 19, 22, 25, ing rules given by Maddison et al. (1984). The
30) in thejoining ofthem.The charactersininter- Wagneranalysis revealstwo cladograms (consensus
section of the cliques convincingly indicate the treeinFig. IB) andtheCamin-Sokalanalysis asin-
monophyly of the following subsets of species: gle one(Fig. 1C); the consistency index ofallthree
(1) all species withexception ofN. carceraríus, N. cladograms is 0.89. Noteworthy are reversals in
pectinicauda, andN. asper; (2) N. brevirostris and characters 11, 16, 17, and 27 constituting syn-
N. rostratus;and(3) N. longidactylus, N.alutensis, apomorphies forthe sisterspecies N. longidactylus
N. transitivus, N. pupetta, and Cdoxaa. rinurellapara- and N. alutensis.
158 B. Sket& J. Notenboom - Phylogeny andbiogeography of the Niphargus transitivusgroup
Fig. 2. Apomorphyindices ofthe species ofthe N. transitivus
group,comparedwiththeirpositionsinthecladogramand their
ecological and geographicalranges. Species indications as in
Table II; forexplanationoftheuseof“apomorphyindices”,
see text. Habitat: ■ = caves; □ = interstitial; ? = proper Fig. 3. Distribution area ofthe N. transitivus group(for N.
habitat uncertain. Range: whole numbers denote length of alutensis only anapproximateposition could be given). The
ranges inkm; * = speciesknown fromonesinglelocalityonly lowest mapshows localities ofthe Dinaric species and the com-
in the heart ofthe Dinaric karst. posedtrackoftheinterstitial species.Theimportantkarstareas
areindicated only onthe topmostmap.Speciesindications asin
Table II;doublesymbolsforTRandPU fordifferentsubspecies
(see text); in the lowest mapthe letters indicate species known
3. Some biogeographic reflections
fromonesinglelocalityinthe heartoftheDinarickarst:B = N.
brevirostris,N = N. numerus, R = N.rostratus,F= N.fac-
Prior to a biogeographic analysis we decided to tor,C = N. carcerarius,A = N. asper.
establish the relative position of individual taxa
along themainevolutionary path ofthegroup.This It is evident (Fig. 2) that taxa with higher apo-
is done by counting "apomorphy indices" by di- morphyindicesaremostly inhabitantsofinterstitial
viding numbers of apomorphies by numbers of waters outside thekarst regions. As much as they
plesiomorphies. One has to emphasize that those approach karst regions, they always inhabit non-
indices have only arelative significance, only for karstic habitats at their borders (in the fluvio-
the chosen set of characters and species, charac- karst). Cave inhabitants in the Dinaric heartland
terizing mostly the developmental "direction" of exhibitmostlyrelativelylowapomorphy. Insidethe
the group. The indices havenot a single meaning Dinarickarst,theapomorphy indicesareincreasing
for the phylogenetic relationships among taxa. in direction from southeast towards northwest.
