Invertebrate Zoology, 1(1): 29–51 © INVERTEBRATE ZOOLOGY, 2004

Exclusion of the Polyarthra from Harpacticoida and its reallocation as an underived branch of the Copepoda (Arthropoda, Crustacea)

Hans-Uwe Dahms

Hong Kong University of Science and Technology/ Dept. Biology — Coastal Marine Lab/ Kowloon — Clearwater Bay/ Hong Kong/ SAR China. e-mail: [email protected]

ABSTRACT: There is no reasonable autapomorphy, either from the naupliar or the adult organization, which justifies a monophylum Harpacticoida (sensu Lang, 1948). This implies a paraphyletic situation of this taxon, comprising two independent monophyletic taxa, the Polyarthra and the Oligoarthra. To solve this problem, the present study will provide justifying arguments for the exclusion of the taxon Polyarthra from the Harpacti- coida, which then is exclusively represented by the monophylum Oligoarthra. When Polyarthra are excluded from the Harpacticoida, than Oligoarthra share the following naupliar synapomorphies: postmaxillar limbs widely spaced, antennal coxa with strong gnathobase, antennal endopodite elongate, mandibular endopodite an elongate process. Based on naupliar characters, Polyarthra are allocated as an underived taxon of the Copepoda, sharing with all other Copepoda the following naupliar characters: antennule 5- segmented, antennal exopodal segments increase from 6 at N I to a final number of 9 at N IV, antennal endopodite is 1-segmented, maxilla absent, swimming performance and life history, dorsocaudal process, antennule segment homologues, larger number of segments in naupliar antennal endo- and exopodites.

KEYWORDS: nauplii, development, phylogenetic systematics, ß-systematics, evolution, Polyarthra, Harpacticoida, Copepoda. Èñêëþ÷åíèå ãðóïïû Polyarthra èç Harpacticoida è âûäåëåíèå åå â ïðèìèòèâíóþ âåòâü Copepoda (Arthropoda, Crustacea)

Ã.-Ó. Äàìñ

Hong Kong University of Science and Technology/ Dept. Biology — Coastal Marine Lab/ Kowloon — Clearwater Bay/ Hong Kong/ SAR China. e-mail: [email protected]

ÐÅÇÞÌÅ: Îñîáåííîñòè îðãàíèçàöèè íè íàóïëèàëüíûõ, íè, â òàêîé æå ìåðå, âçðîñ- ëûõ ñòàäèé íå ïîçâîëÿþò âûäåëèòü íàäåæíûå àóòàïîìîðôèè, êîòîðûå áû ïîäòâåð- æäàëè ìîíîôèëåòè÷íîñòü Harpacticoida (sensu Lang, 1948). Ýòî óêàçûâàåò íà ïàðàôè- ëåòè÷íîñòü äàííîãî òàêñîíà, âêëþ÷àþùåãî äâå íåçàâèñèìûå ìîíîôèëåòè÷åñêèå ãðóïïû: Polyarthra è Oligoarthra. ×òîáû ðåøèòü ïðîáëåìó, â äàííîé ðàáîòå ïðèâåäå- íû äîêàçàòåëüñòâà, óêàçûâàþùèå íà íåîáõîäèìîñòü èñêëþ÷åíèÿ Polyarthra èç îòðÿäà Harpacticoida, êîòîðûé â òàêîì ñëó÷àå áóäåò ïðåäñòàâëåí èñêëþ÷èòåëüíî ìîíîôèëå- 30 H.-U. Dahms

òè÷åñêîé ãðóïïîé Oligoarthra. Ïðè èñêëþ÷åíèè Polyarthra èç Harpacticoida íàóïëèñû Oligoarthra õàðàêòåðèçóåòñÿ ñëåäóþùèìè ñèíàïîìîðôíûìè ïðèçíàêàìè: ïîñòìàê- ñèëëÿðíûå êîíå÷íîñòè ðàññòàâëåíû øèðîêî, êîêñà àíòåíí ñ õîðîøî ðàçâèòîé ãíàòî- áàçîé, ýíäîïîäèò àíòåíí óäëèíåí, ýíäîïîäèò ìàíäèáóë èìååò óäëèíåííûé âûðîñò. Íà îñíîâàíèè ïðèçíàêîâ íàóïëèàëüíûõ ñòàäèé Polyarthra âûäåëÿåòñÿ â ïðèìèòèâíûé òàêñîí Copepoda, íàóïëèóñû êîòîðîãî õàðàêòåðèçóþòñÿ, êàê è ó âñåõ äðóãèõ Copepoda, ñëåäóþùèìè ïðèçíàêàìè: àíòåííóëû ïÿòè÷ëåíèêîâûå, ÷ëåíåíèå ýêçîïîäèòà àíòåíí âîçðàñòàåò ñ 6 íà ñòàäèè N I (íàóïëèóñ ïåðâîé ñòàäèè) äî 9 íà íàóïëèàëüíîé ñòàäèè N VI, ýíäîïîäèò àíòåíí îäíî÷ëåíèêîâûé, ìàêñèëëà îòñóòñòâóåò, ïëàâàòåëüíîå äâè- æåíèå è æèçíåííûé öèêë, äîðçîêàóäàëüíûé âûðîñò, ãîìîëîãèÿ ÷ëåíèêîâ àíòåííóë, áîëüøîå ÷èñëî ÷ëåíèêîâ ýêçîïîäèòà è ýíäîïîäèòà àíòåíí.

ÊËÞ×ÅÂÛÅ ÑËÎÂÀ: Íàóïëèñû, ðàçâèòèå, ôèëîãåíåòèêà, ß-ñèñòåìàòèêà, ýâîëþ- öèÿ, Polyarthra, Harpacticoida, Copepoda.

Introduction Diogenidae and the Parapaguridae as distinct families resulted largely from considerations of In organisms with larval development, both, larval characters (Williamson, 1982). Rice early and late developmental stages show char- (1986) gave an outline of the evidence drawn acters of the same genotype. However, in most from the zoea-stage for the phylogeny of the cases only the adults have so far been used for Brachyura. Dahms (1990) has demonstrated the the reconstruction of phylogenetic relationships, usefulness of naupliar characters in phylogenet- although larvae may provide a rich source of ic hypotheses among the Harpacticoida. additional morphological, behavioural, and eco- Walossek (1993) and Maas et al. (2003) dem- logical characters. Evidence from postembryonic onstrated that larval characters are also useful in stages should complement that gained from the reconstruction of the phylogeny of Crusta- adult characters for an individual exhibits dif- cea considering also or exclusively fossil taxa. ferent and significant characters at all phases of Several other colleagues have used naupliar its ontogeny which can be used as species- characters for phylogenetic considerations and specific character patterns of evolutionary spe- their results will be discussed where appropriate cies (Ax, 1987). Often a larva is as valuable for phylogenetic and taxonomic investigations as throughout this study (cf. Ferrari, Ivanenko, the adult and much more valuable in cases 2001). where the adult is highly specialized and recent- Polyarthran harpacticoid nauplii differ strik- ly has been altered. In phylogenetic investiga- ingly in a number of characters from those of the tions an uncritical use of larval characters is just Oligoarthra and they do not share a single nau- as unadmissible as a similar use of the charac- pliar character with them. The monophyletic ters of the adults (Jägersten, 1972). status of the Harpacticoida, hitherto comprising Larval characters have been used for phylo- Polyarthra and Oligoarthra, is therefore ques- genetic studies of Crustacea. Schminke (1981) tioned. The present contribution aims to pro- demonstrated the origin of Bathynellacea by vide phylogenetic inferences for the realloca- neotenous processes from a zoea-like ancestor. tion of the Polyarthra, and will use naupliar Gurney (1942) showed that larval characters are characters for phylogenetic reconsiderations. useful for separating decapods at various taxo- Consequences for the reallocation of the Pol- nomic categories. Within the Paguroidea (Ano- yarthra will be discussed in the light of the mura), the widely accepted recognition of the evolution of the Maxillopoda. Reallocation of the Polyarthra 31

Material and methods Olesen, 2001); Ostracoda (Keslingm, 1951); Nauplii were reared from individual females Thecostraca (Bassindale, 1936; Itô, 1986a,b; to ensure reliable species identification. The Grygier, 1987a,b); Harpacticoida (Dahms, 1990, original ovigerous females which provided the 1991); Cyclopoida (Koga, 1984; Dahms, Fernan- developmental stages were collected from va- do, 1992; Ferrari, 2000; Ferrari, Ivanenko, rious areas (Dahms, 1990). Substrate from field 2001); Poecilostomatoida (Izawa, 1986); and samples was stirred in a beaker, and subsequently Calanoida (Song, Jinchuan, 1990; Dahms, decanted over a screen (100m m mesh-size). The Fernando, 1993). The following contributions residue containing adults was rinsed into small- were used for general information about crusta- er bowls for transport to the laboratory. The cean nauplii or maxillopodan phylogeny: Koga developmental stages used were the offspring (1984), Björnberg (1986), Izawa (1986), Schram exclusively of single-female cultures. Female (1986), Grygier (1987a,b), and Boxshall and identity was determined after successful cultu- Huys (1989). Nauplii are defined as those onto- ring. For culturing procedures see Dahms (1990). genetic stages which still bear the antennal en- Stages were selected individually under a ditic process, while metanauplii have more than dissecting microscope and fixed in 5% buffered the 3 appendages of A1, A2, and Md developed, formaldehyde and embedded in W 15 (C. Zeiss if only as limb buds. Company). This clarifies nonexuvial material within a few weeks and provides information on Abbreviations used: hidden posterior structures when observed by A1 — first antenna (=antennule); A2 — sec- phase-contrast. Unfortunately, the natural co- ond antenna (=antenna); Abd — abdomen; lour of nauplii, e.g. colour and shape of the red Ae — aesthetasc; CI, II — copepodid I, II etc.; nauplius-eye, was lost quite rapidly and the eye Cs — cephalic shield; Dcsp — dorsocaudal is, therefore, not figured. Nauplii, exuviae and spine dorsal to anus; End — endite (setiferous copepodids were mounted whole, and broken lobes of limb corm); Enp — endopodite; Exp — glass-fibres were added to prevent compression exopodite; Cur — caudal ramus; La — labrum; and to facilitate specimen movement to allow M — mouth; Md — mandible; Msp — masti- inspection from all sides. Abnormalities occa- catory spine of mandibular basipod; Mx1 — sionally were observed but not been figured. first maxilla; Mx2 — second maxilla; NI, II — Body lengths were measured from the anterior nauplius I, II etc.; Ne — nauplius eye; Pgn — to the posterior end of the naupliar body; body paragnaths; Som (Som 4) — somite (the 4th width is given as the widest part of the nauplius. somite); Set — seta(e); Setat — setation; Thp — Drawings were made from individual speci- thoracopods (trunk legs); Ths — Thoracic mens; others were checked for variability. The somites; Vcp — ventrocaudal process (pair of nauplius sensu stricto is an orthonauplius (with processes at ventrocaudal margin of telson). 3 limb-bearing segments). If a nauplius has developed another pair of limbs. Naupliar Îáîçíà÷åíèÿ: somites are difficult to determine], it is called A1 — ïåðâàÿ àíòåííà (=àíòåííóëà); metanauplius. The general term “nauplius” re- A2 — âòîðàÿ àíòåííà (=àíòåííà); Abd — àá- fers in the present contribution to all larval äîìåí; Ae — ýñòåòàñê; CI, II — êîïåïîäèò- stages throughout the naupliar phase (being íàÿ ñòàäèÿ I, II è ò.ä.; Cs — ãîëîâíîé ùèò; characterized e.g. by the presence of antennal Dcsp — äîðçîêàóäàëüíûé øèï íàä àíóñîì; gnathobases). End — ýíäèò (ùåòèíèñòûå ëîïàñòè â îñíî- Characters were assembled from personal âàíèè êîíå÷íîñòåé); Enp — ýíäîïîäèò; observations and various sources in the litera- Exp — ýêçîïîäèò; Cur — êàóäàëüíàÿ âåòâü; ture: Cephalocarida (Sanders, 1963 a,b); Bran- La — ëàáðóì; M — ðîò; Md — ìàíäèáóëà; chiopoda (Walossek, 1993; Olesen, 1999); My- Msp — æåâàòåëüíûé øèï áàçèïîäèòà ìàí- stacocarida (Delamare Deboutteville, 1954; äèáóë; Mx1 — ïåðâîÿ ìàêñèëëà; Mx2 — âòî- 32 H.-U. Dahms

Fig. 1. First naupliar stages (NI) of Polyarthra. (A) Longipedia minor (Longipediidae). (B) Canuella perplexa (Canuellidae). Scale bars 50 mm (after Dahms, 1991). Ðèñ. 1. Íàóïëèñû ïåðâîé ñòàäèè (NI) Polyarthra. (A) Longipedia minor (Longipediidae). (B) Canuella perplexa (Canuellidae). Ìàñøòàá 50 ìêì (ïî Dahms, 1991).

Fig. 2. Structural changes in Longipedia minor. Habitus of NI — scale bar 100 mm (A). Abdomen of NI (B) and NII (C) in ventral view; development of maxillule at NII — scale bar 50mm (B, C) (after Dahms, 1991). Ðèñ. 2. Èçìåíåíèÿ â ñòðîåíèè Longipedia minor. Îáùèé âèä ñòàäèè NI, ìàñøòàá 100 mkm (A). Àáäîìåí íà ñòàäèÿõ NI (B) è NII (C), âèä ñíèçó; ðàçâèòèå ìàêñèëëóë íà ñòàäèè NII; ìàñøòàá 50 ìêì (B, C) (ïî Dahms, 1991). Reallocation of the Polyarthra 33

Fig. 3. Antennule segment homologues among copepod taxa. (A, B) Longipedia minor at NI (A) and NII (B); (C) Canuella perplexa at NVI; (D) representative of Diaptomidae at NVI; (E) Euterpina acutifrons at NVI; (F) representative of Lernaeidae at NVI. Scale bars 50 mm. Ðèñ. 3. Ãîìîëîãèÿ ÷ëåíèêîâ àíòåííóë êîïåïîä ðàçíûõ òàêñîíîâ. (A, B) Longipedia minor íà ñòàäèÿõ NI (A) è NII (B); (C) Canuella perplexa íà ñòàäèè NVI; (D) ïðåäñòàâèòåëü Diaptomidae íà ñòàäèè NVI; (E) Euterpina acutifrons íà ñòàäèè NVI; (F) ïðåäñòàâèòåëü Lernaeidae íà ñòàäèè NVI. Ìàñøòàá 50 ìêì.

ðàÿ ìàêñèëëà; NI, II — íàóïëèàëüíàÿ ñòàäèÿ íèå; Thp — òîðàêîïîäû (ãðóäíûå íîãè); I, II è ò.ä.; Ne — íàóïëèàëüíûé ãëàç; Pgn — Ths — ãðóäíîé ñåãìåíò (= ñîìèò); Vcp — ïàðàãíàòû; Som (Som 4) — ñåãìåíò (4-é ñåã- âåíòðîêàóäàëüíûé âûðîñò (ïàðà âûðîñòîâ ìåíò); Set — ùåòèíêà(è); Setat — âîîðóæå- íà âåíòðîêàóäàëüíîì êðàå òåëüñîíà). 34 H.-U. Dahms

Fig. 4. Antennule development in Polyarthra and Oligoarthra. (A) Longipedia minor at NVI and CI. (B) First segment of Ectinosoma melaniceps at CI and CII; (C) First segment of Macrosetella gracilis at CII, CIII and CIV. (D) Distal segment of Thalestris longimana at CI and CII. (E) Distal segment of Tegastes clausi at CI and CII. (F) Heterolaophonte minuta at NVI, CI and CII (I–III, a–c: indicating the three setae of the 2nd segment of a 3-segmented oligoarthran naupliar antennule; arrowheads in B–F pointing at structures which are reduced in the subsequent stages). Scale bar 50 mm (after Dahms, 1991). Ðèñ. 4. Ðàçâèòèå àíòåííóë â Polyarthra è Oligoarthra. (A) Longipedia minor íà ñòàäèÿõ NVI è CI. (B) Ïåðâûé ÷ëåíèê Ectinosoma melaniceps íà ñòàäèÿõ CI è CII; (C) Ïåðâûå ÷ëåíèê Macrosetella gracilis íà ñòàäèÿõ CII, CIII è CIV. (D) Äèñòàëüíûé ÷ëåíèê Thalestris longimana íà ñòàäèÿõ CI è CII. (E) Äèñòàëüíûé ÷ëåíèê Tegastes clausi íà ñòàäèÿõ CI è CII. (F) Heterolaophonte minuta íà ñòàäèÿõ NVI, CI è CII (I–III, a–c: óêàçûâàþò íà òðè ùåòèíêè íà 2-ì ÷ëåíèêå òðåõ÷ëåíèêîâûõ àíòåííóë íàóïëèñîâ Oligoarthra; ñòðåëêè íà ðèñ. B–F óêàçûâàþò íà ñòðóêòóðû, ðåäóöèðóþùèåñÿ íà áîëåå ïîçäíèõ ñòàäèÿõ). Ìàñøòàá 50 ìêì (ïî Dahms, 1991). Reallocation of the Polyarthra 35

A phylogenetic problem — the paraphyl- Cyclopoida or the Calanoida are regarded as etic status of the Harpacticoida and the un- plesiomorphic. Otherwise, it appears that the settled position of the Polyarthra. naupliar characters of Polyarthra are the most Nauplii of the two only polyarthran families plesiomorphic naupliar copepod characters com- Longipediidae and Canuellidae, usingLongipe- pared to copepodan as well as to other maxil- dia minor and Canuella perplexa as examples, lopodan taxa. Polyarthran naupliar characters figured at NI (Fig. 1) appear quite dissimilar. also agree with those of other maxillopodan This is mainly due to the long caudal spine of groups, especially with the Cirripedia. Longipedia causing the pear-shaped body form If Polyarthra were excluded from the Har- of the nauplii. However, the two families show pacticoida, the remaining monophylumOligoar- several structural as well as meristic similari- thra is characterized by the following four ties, some of which are assumed to be autapo- autapomorphies (illustrations are provided by morphic on the basis of outgroup comparison Dahms, 1990, 2004): suggesting the monophyletic status of both fam- 1) Postmaxillar limbs widely spaced in ilies, which have a sister taxon relationship later metanauplii: In Cephalocarida (Sanders, with each other — see below. As for the life- 1963a,b), Branchiopoda (Olesen, 1999), and cycle of the Polyarthra — both taxa show a Mystacocarida (Olesen, 2001) the postmaxillar habitat transition from substrate bound adults to appendages are separated medially, probably to planktic nauplii (Dahms, 2000). Here, I will provide space for a medial food grove where enumerate only meristic synapomorphies for food is transported frontally. This character is polyarthran taxa (see also Dahms, 1990), they: not available from the Thecostraca for their lack 1) bear 5-segmented antennules (from NII– of appendages caudal to the maxillules. Post- VI) with the same number and pattern of setae maxillar appendages are juxtaposed medially in from NI–III (Figs. 1, 2); Cyclopoida, Polyarthra and Calanoida, whereas 2) have 6-segmented antennal exopodites they are widely spaced in the Oligoarthra. This that increase their segment number by 3 at NIV, positional peculiarity indicates a striking differ- when the final number of 9 segments with an ence between copepod antennules to the second identical setal pattern is reached (Fig. 5); maxillae (= cephalic) and postmaxillary (= tho- 3) have a similar structure of the post- racic) appendages. As indicated from this plesi- mandibular appendages and the same stage at omorphic condition — taking non-thecostracan which they appear (see below); Maxillopoda as an outgroup, where the post- 4) have a pair of caudal setae at NI with maxillar appendages of copepod nauplii are specific spinular ornamentation and reduction juxtaposed medially (also in Polyarthra), the of size at NII (Fig. 6) position of these limbs becomes lateroventral 5) have 6 caudal setae on either side at NVI among the Oligoarthra-Maxillipedasphalea (Fig. 6). (Lang, 1948), and even more widely spaced and Therefore, the Polyarthra (i.e. Longipe- laterally located among the Oligoarthra. How- diidae and Canuellidae, Figs. 1–7) share a num- ever, limb buds of thoracopods 3–6 of presumed ber of naupliar autapomorphies characterizing derived calanoids are located laterally (Ferrari, them as a monophylum. Polyarthran nauplii Steinberg, 1993; Ferrari, Markhaseva, 1996) differ strikingly in a number of characters from relative to the ventral position of presumed the nauplii of Oligoarthra and they do not share older calanoids (Ferrari, 1985, 1996). There- a single naupliar character with the Oligoarthra fore, it is not unlikely that this character seems (as for the autapomorphies of the Oligoarthra — to have evolved independently several times. see below). The monophyletic status of the 2) Antennal coxa with strong gnathobase Harpacticoida, comprising Polyarthra and Oli- throughout the naupliar phase: Whereas the goarthra until now, is therefore questioned. All antennal coxa of all major copepod taxa con- characters Polyarthra share with for instance the sists of just an inner protuberance with some 36 H.-U. Dahms

Fig. 5. Antennal development in the Harpacticoida. (A — Polyarthra; B, C — Oligoarthra.). (A) Longipedia minor at NI and its basis, endopodite and exopodite at NVI; (B) Phyllognathopus viguieri at NI and NVI. (C) Scutellidium hippolytes at NVI (arrowheads pointing at structures which are indicative of former segment borders). Scale bar 50 mm (after Dahms, 1991). Ðèñ. 5. Ðàçâèòèå àíòåíí Harpacticoida. (A — Polyarthra; B, C — Oligoarthra.). (A) Longipedia minor íà ñòàäèè NI; áàçèñ, ýíäîïîäèò è ýêçîïîäèò íà ñòàäèè NVI; (B) Phyllognathopus viguieri íà ñòàäèÿõ NI è NVI. (C) Scutellidium hippolytes íà ñòàäèè NVI (ñòðåëêà óêàçûâàåò íà ñòðóêòóðû, ïîêàçûâàþùèå ïðåæíèå ãðàíèöû ÷ëåíèêîâ). Ìàñøòàá 50 ìêêì (ïî Dahms, 1991). strong setal armature, there is a pronounced 3) Antennal endopodite elongate throug- masticatory process already indicated at NI (see hout the naupliar phase: The 1-segmented Fig. 5C), and this is strongly developed from antennal endopodite is lobe-like otherwise in NII onwards in the Oligoarthra. copepod taxa, whereas it is 1-segmented and Reallocation of the Polyarthra 37

Fig. 6. Development of abdomen and caudal armature in copepod nauplii; showing a caudal process, or a symmetrical/asymmetrical abdomen. Only one prospective caudal ramus is shown for NVI of Longipedia minor (C) and Canuella perplexa (D). Scale bar 50 mm. Ðèñ. 6. Ðàçâèòèå àáäîìåíà è êàóäàëüíîãî âîîðóæåíèÿ ó íàóïëèñîâ êîïåïîä; ïîêàçàíû êàóäàëüíûé âûðîñò èëè ñèììåòðè÷íûé/àñèììåòðè÷íûé àáäîìåí. Äëÿ ñòàäèè NVI Longipedia minor (C) è Canuella perplexa (D) ïîêàçàí òîëüêî îäèí çà÷àòîê êàóäàëüíîé âåòâè. Ìàñøòàá 50 ìêì. 38 H.-U. Dahms becomes elongate in Oligoarthra. Its reduced sent in nauplii of Cyclopoida, Oligoarthra, Cala- state is apparent from the 1 to 4 setae situated at noida and Notodelphyoida (Dudley, 1966) and in the inner margin midlength representing the the Facetotecta (Itô, 1986b) throughout the nau- armature of the remnant first of a former 2- pliar phase but in no other maxillopodan taxon. segmented endopodite. 2) 6-segmented antennal exopodites in later 4) Mandibular endopodite an elongate pro- naupliar stages: A maximum number of 6 seg- cess: The endopodal process of the mandible is ments for the antennal exopodite at later stages lobe-like and bears 4 or more setae usually of the is characteristic for nauplii of the Calanoida and same size at later stages in all major copepod taxa. of free-living Cyclopoida (Gurney, 1932), but In Oligoarthra there is an elongate, rectangular for no other maxillopodan group. Segment num- process with1 (Harpacticidae, Thalestridae, Me- ber is lower in other groups of the Copepoda, tidae) or 2 stout spiniform setae terminally, be- including the Oligoarthra. sides some smaller setae (cf. Dahms, 1990). 3) Presence of the maxillae at later met- If Polyarthra are excluded from the Harpacti- anauplii: The presence of a maxilla is, however, coida (with the Oligoarthra as the only remaining not strong evidence because its absence in Pol- taxon), a sister-group relationship of the Poly- yarthra is a reduction which could have evolved arthra with the Copepoda-Podoplea or a subset several times independently. of this group is unlikely because Polyarthra share 4) 1-segmented antennal endopodites only a single rather unspecific naupliar character throughout the naupliar phase: The antennal with the remaining podopleans (Podoplea, ortho- endopodite throughout the naupliar phase is 2- and metanauplii are known from the Monstril- segmented in the Cephalocarida and in the Fac- loida, Misophrioida, Cyclopoida, Poecilosto- etotecta, but 3-segmented in Mystacocarida, matoida, and Siphonostomatoida): Cirripedia, and Ascothoracida of Thecostraca. 1)Mandibular endopodite 2-segmented: The Therefore, a 1-segmented naupliar antennal mandibular endopodite is indistinctly 2-seg- endopodite, which is present without exception mented in Cephalocarida, 3-segmented in the among copepod nauplii, is a strong apomorphy Mystacocarida and Cirripedia, 1-segmented in for the Copepoda. The presence of one spinule Ascothoracida, and 2-segmented in “Facetotec- row (or more in later naupliar stages) on this ta” and Podoplea. The mandibular endopodite ramus of the polyarthran Longipedia minor T. is present in all representatives of the Pol- & A. Scott, 1893 (Dahms, 1991), may indicate yarthra, Cyclopoida, Poecilostomatoida, Sipho- an ancestral 2-segmented state (or even 4-seg- nostomatoida, Misophrioida. In gymnopleans mented state in later naupliar stages). one or more arthrodial membranes fail to form, 5) Legs 1, 2 present at NVI: The external resulting in a single segment. A 2-segmented appearance of the second and third thoracic condition is clearly present in the Polyarthra, appendages as limb buds at NVI in all major but it is difficult to observe in some Cyclopoida copepod taxa is a unique character compared to and most Oligoarthra. In many representatives other crustacean nauplii (cf. Walossek, 1993) of Oligoarthra, also a reduction to a 1-segment- and, provides a strong autapomorphy for the ed state or an “endopodal field”, fused to the Copepoda. It is unlikely that a more posterior basis takes place (Dahms, 1990). limb bud will be developed in copepod nauplii If, on the other hand, Polyarthra were kept as proposed by Izawa (1987), who cited the as a sister-taxon of all the remainingCopepoda , presence of leg 3 at NVI in the descriptions of the remaining taxa of the Copepoda share the various authors. This pair of limbs belongs to following six naupliar synapomorphies (using the first copepodid, although it may become other maxillopodan nauplii as an outgroup) (cf. visible through the naupliar cuticle on the inter- Dahms, 2004): moult first copepodid (cf. Dahms, 1992). Ex- 1) 3-segmented antennules throughout the ceptions in the form of reductions are provided naupliar phase: A 3-segmented antennule is pre- by certain Harpacticoida-Oligoarthra (e.g.Mac- Reallocation of the Polyarthra 39 rosetella gracilis) where naupliar postma- 4) Postmandibular appendages juxtaposed xillulary limb formation is absent (Dahms, 1990). medially in later metanauplii: In Cephalocari- 6) Six caudal setae at later metanauplii da, Branchiopoda und Mystacocarida there is a (Fig. 6): The caudal armature of non-copepod medial gap between contralateral pairs of meta- nauplii is difficult to ascertain, because spini- naupliar postmandibular appendages. This char- form processes found on some non-copepod acter is not known from Thecostraca. Post- nauplii may or may not have setal precursors. mandibular appendages are juxtaposed medial- However, Cephalocarida, Branchiopoda, Mys- ly in Cyclopoida, Polyarthra and Calanoida, tacocarida, and Thecostraca have fewer than 6 whereas they are widely spaced secondarily in caudal elements on each prospective caudal the Oligoarthra. This positional peculiarity in- ramus. Six setae are widespread and this is the dicates a striking difference between copepod maximum number among all major copepod cephalic and thoracic appendages. taxa. Six setae are present in the underived 5) Six caudal setae: see above (synapomo- Oligoarthra-Maxillipedasphalea, but there is a rphies of Polyarthra and Copepoda). A sister- lower number in some other harpacticoid taxa. group relationship of Polyarthra + remaining Caudal setae are reduced in number and the Copepoda provides a reasonable hypothesis, number may be contralaterally asymmetrical in where the Polyarthra exhibit the most plesio- many Calanoida. Six caudal setae cannot be an morphic character states. This is also indicated apomorphy of Poecilostomatoida, as suggested by nine plesiomorphic character states Poly- by Izawa (1987), because this is shared charac- arthra share with other groups of the Maxillo- ter state of all late copepod metanauplii. poda which lack, however, among all known If these characters are accepted as common nauplii belonging to non-polyarthran Copepo- characters of non-polyarthran Copepoda, then da. Although the author is aware of the fact that the Polyarthra would become the sister-taxon plesiomorphies do not provide direct evidence of the remaining taxa of the Copepoda with of relationships, they do restrict the number of which they share the followingfive synapomor- states which than can express an apomorphy. phies (which are naupliar autapomorphies of 1) Antennule with 5 segments throughout the Copepoda as a whole as deduced from the phase (Fig. 3): (6 segments for Longipedia outgroup-comparison with other maxillopodan minor — for NI still showing a 5-segmented groups — cf. Dahms, 2004): state cf. Fig. 2) is unique insofar as there are no 1) Two antennal coxal setae: In addition to more than 3 segments in non-polyarthran Cope- the antennal enditic process of the coxa which is poda. Six antennular segments are characteris- present throughout the naupliar phase (although tic for Cephalocarida (Sanders, 1963a) and le- rudimentary at NI), there is a peculiar strong padid Cirripedia (Grygier, 1987b), whereas a 5- seta at the base of this process developed at NIII segmented antennule is common in other groups stage in Calanoida and Cyclopoida (Dahms and of Cirripedia (Izawa, 1987). There seems to be Fernando, 1993). In some species of Oligoar- no functional necessity for the acquisition of thra a presumably homologous seta is present additional segments of the antennule as an adap- throughout the naupliar phase. Presence of this tation to pelagic performance (so secondary seta is a weak naupliar apomorphy for the Cope- acquisition of segments to a presumed 3-seg- poda because its presence has not been well- mented antennule would be expected to have no studied among all Maxillopoda. adaptive value). Swimming is performed suc- 2) 1-segmented antennal endopodite cessfully also by a 3-segmented antennule of throughout the naupliar phase: see above (syn- calanoid nauplii. It is more likely that an anten- apomorphies of Polyarthra and Copepoda). nule of more than 3 segments is a plesiomorphic 3) Thoracopods 1 (=Mxp), 2 (=leg 1) and 3 character state, retained from maxillopodan an- (=leg 2) present at NVI stage: see above (syn- cestry. This view is supported by Grygier (1987b) apomorphies of Polyarthra and Copepoda). who postulated that an 8-segmented antennule 40 H.-U. Dahms is a ground pattern state of nauplii belonging to ner, performing circles while swimming on their the Maxillopoda. backs as most nauplii of the Cirripedia do. This, 2) The exopodal segments of the antenna of besides other characters made Gurney (1930) Polyarthra increase from 6 at NI to a final and Nicholls (1935) emphasize the “resemb- number of 9 at NIV (Fig. 5): An increase of lance”of the nauplii of Longipedia and the Cir- segments is unknown from non-polyarthran ripedia. Lauterbach (1980) argued that the creep- Copepoda. Throughout the naupliar phase there ing behaviour of nauplii is a plesiomorphic are 6 segments in Cyclopoida and Calanoida character within Harpacticoida and used this as and 9 in Mystacocarida and Cirripedia. InChtha- a model to claim that the ancestral Crustacean malus stellatus (Cirripedia) there are 2 setae on larva (i.e. the nauplius) was also substrate-dwell- the first seta-bearing segment, 1 seta on each of ing and non-planktic. Consequently, swimming the following and 3 setae on the terminal seg- ability and multi-segmented exopodites of the ment (Egan, Anderson, 1989) as it is the case in second antennae and mandibles must have de- the Polyarthra. veloped secondarily (reversing the usually pro- 3) Multisegmented state of antennal en- posed reduction sequence). This is incompatible dopodite (Fig. 5): The antennal endopodite is 2- not only with the proposed maxillopodan ances- segmented in Cephalocarida and Facetotecta, 4- try of the Copepoda and the finding that Oli- segmented in Mystacocarida (or 3-segmented if goarthra and the Polyarthra as a rule develop the distal portion is interpreted as a complex through nauplii that are excellent swimmers. seta), 3-segmented in Cirripedia (this may often Nicholls (1935) admitted that at least the appear 1-segmented in Cirripedia, due to fusion particular jerky swimming motion may be only of segment 1 to the basis and segments 2 and 3 a mechanical effect and attributed this to the to each other partially — (M. Grygier, pers. long posterior spine present in both groups — comm.), and 3-segmented in Ascothoracida. As the Polyarthra and the Cirripedia. It has to be for the Copepoda, the only exception with a 2- emphasized that a caudal process is of impor- segmented endopodite is the taxon Cyclopoida. tance in swimming, probably as a balancing In the polyarthran Longipedia minor, there are organ. This may explain its widespread occur- spinule rows which may indicate the position of rence among underived Crustacean taxa with an arthrodial membrane of a former 2-segment- planktic nauplii (except the benthic Mystaco- ed [or even a 4-segmented state at later develop- carida). Among holoplanktic calanoid nauplii mental stages] of the antennal endopodite. there are many cases where one of the two 4) Lack of maxilla: The maxilla does not closely set longer caudal setae and its rami are become visible externally nor are there traces reduced in size whereas the other is enlarged discernible internally in the Polyarthra. This (Faber, 1966; Koga, 1984; Björnberg, 1986), contradicts all studies of the nauplii of the Pol- thus, probably achieving the functional effect of yarthra to date which find the presence of a only one long caudal seta. In this context, NI of maxilla. This may be due to a misinterpretation the oligoarthran Euterpina acutifrons (a plank- of outer parts of the medial maxilliped anlage. If tic species of Tachidiidae) is remarkable. It the maxilla does not develop externally in the does not bear a caudal spine but rather the nauplius, this would be a secondary loss the prominent, arched ventral portion of the abdo- Polyarthra have in common with the Thecostra- men is furnished with a semilunar-shaped row ca (Cirripedia, Facetotecta and Ascothoracida). of long spinules, which may function in the same Among non-polyarthran Copepoda (except in way as do the caudal setae at NI and the maxil- some parasitic forms and some Oligoarthra lule from NII onwards in Polyarthra. where it is lacking) the maxilla appears at NIV As for the life history of Oligoarthra and or NV stage. Polyarthra, Dahms & Qian (2003, 2004) specu- 5) Swimming performance and life history: late that because these larvae share the same Polyarthran nauplii swim in a slow, jerky man- realm as the adults and no costly habitat transi- Reallocation of the Polyarthra 41 tion is necessary. This contradicts conventional 6) 4th pair of appendages (fig. 1): A much wisdom that there is an adaptive advantage for disputed and important question concerns the species in which larvae and juveniles or adults presence at NI stage of the Polyarthra of the do not share the same habitat. Furthermore, anlage of the maxillule. Gurney (1930) de- Dahms (2000) observed that Leptastacidae de- scribed the NI of Longipedia (Longipedia, ge- velop nauplii and copepodids which are inter- nus II) with 2 long spinulose setae posterior to stitial dwellers of marine coastal sands. Even if the mandibles which he interpreted as the max- planktonic, both phases may share the same illules. This interpretation implied that no furcal habitat: e.g., Macrosetella gracilis (Miracidae) setae are present. Lang (1948) also described clasping cyanobacterial Trichodesmium fila- the more caudal setae of NI of Sunaristes paguri ments; nauplii and copepodids ofDrescheriella as the maxillules and he declared the presence of glacialis living in the interstices of Antarctic the maxillule at NI as a constitutive character of pack ice. The only exception is the Polyarthra. the Polyarthra separating this taxon from the In both taxa, Longipediidae and Canuellidae rest of Harpacticoida (and Copepoda as a whole). (cf. Dahms, 2000, fig. 7), copepodids are al- This interpretation has been followed by Nicholls ways close to the substratum, it may be sediment (1935), Onbé (1984) and Izawa (1987). The or invertebrate host. The nauplii, however, are presence of the maxillules at NI would be highly planktonic suspension feeders with good swim- unexpected for the fact that this stage is sup- ming abilities. This holds for free-living Canue- posed to be an orthonauplius in the Copepoda. llidae (Dahms, 1990) as well as for symbiotic The only authors interpreting the caudal setae of taxa where nauplii have not been found at/in the NI as belonging to the hind-body and not as the host and, therefore, are suspected to constitute maxillule are Vincx & Heip (1979), although the planktonic infecting and dispersal phase (cf. they provided no explanation. Huys, 1995). According to Huys (1995) Canuel- Nevertheless, the similarity of the presence lidae inhabit a wide range of sediments from of 2 stout setae at NI and 2 pairs of stout setae flocculent muds to coralline debris, and they are at NII within Longipedia and Canuella (Figs. primarily found in the intertidal and shallow 1, 2) is so remarkable that these cannot but be subtidal areas of the continental shelves. Some homologous and it is more than likely that a genera such as Canuella and Canuellopsis ha ve maxillule is developed not earlier than from been reported from deeper muds. Interpreting NII onwards in Longipediidae as well. The these as exceptions, the family has been unsuc- erroneous interpretation confuses the caudal cessful in invading the deep sea realm. The setae with the maxillules at NI among Pol- absence of suspended food items in deeper yarthra and of the planktonic representatives waters suitable for nauplii of the Polyarthra of Ectinosomatidae (Hirakawa, 1974; Diaz, might be the main ecological reason for both Evans, 1983), and may be due to the fact that polyarthran taxa, being restricted with few excep- these setae are longer than the caudal setae of tions to shallow waters (see Huys, 1995). NII. In this respect they resemble the maxil- A swimming naupliar locomotion seems to lules. However, the fact that the caudal setae be the underived state for the Crustacea. Functio- are so short at NII can be viewed as a functional nal reconstructions revealed that, as in feeding shift (of balancing and stability) provided by nauplii of extant Crustacea, the nauplius of long setae from the caudal setae at NI to the Rehbachiella kinnekullensis (Branchiopoda) maxillules at NII. This is demonstrated by the may have fed while swimming. Since this can be epibenthic species of the Ectinosomatidae, in applied also to the maxillopodan larva ofBredo- which the morphology of both the caudal setae caris admirabilis(Müller, Walossek, 1988), the and the maxillules are different from that of the speculations of Lauterbach (1980) concering a planktic representatives, but similar to that of all creeping ancestral larval type for Crustacea other representatives of Oligoarthra studied (cf. must be rejected (cf. Dahms, 1990). Dahms, 1990). 42 H.-U. Dahms

The presence of maxillules at NI of Poly- ment but the two distal setae are both situated on arthra would be the first case for the suppression the then demarcated 3rd segment at NII (cf. of an orthonauplius among the Copepoda, Cir- Ferrari and Benforado 1998). Here, the anten- ripedia and Ascothoracida (cf. Izawa, 1987), nule of NI of L. minor shows a cylindrical distal and would result in the reduction of the number segment at NI which becomes flattened during of metanaupliar stages to five. An early appear- subsequent moults until it is paddle-like in the ance of the maxillule at NI would be of phyloge- last naupliar stage. The armature is confined to netic importance because it has been regarded the lateral and terminal edges. Judging from its both historically and recently as a primitive reduced size and disc-like appearance, the sub- state. Lang (1946) argued that the protaspis distal segment (representing segments III–V) larva with 4 pairs of appendages of the trilobites probably serves as a joint for the paddle-strokes is not already “a specialized larval stage”, but a of the terminal segment — similar to segment 2 primitive one, and that the first nauplius stage of of calanoid nauplii called the “Wirbel” by Oberg crustaceans is a protaspis stage which is arrested (1906). In Oligoarthra, the number of segments and delayed in its development. Garstang and of the antennule never exceeds 3, and all seg- Gurney (1938) among others attempted to de- ments are cylindrical throughout the phase. rive crustaceans from trilobites and the crusta- Judging from setal composition and devel- cean nauplius from the protaspis larva of trilo- opment, the unarmed 1st segment of oligoar- bites. They interpreted the nauplius as a special- thran antennules is homologous to that of Poly- ized (or modified) protaspis. However, as point- arthra. Segment 2 with 3 setae is homologous to ed out by Fryer (1992), little is known about the segments 2–4 of polyarthran metanauplii which supposedly five appendages (vide Garstang and also together bear 3 setae. Segment 3 is equiv- Gurney, 1938) of the trilobite protaspis. Cisne alent to the 5th of Polyarthra which also bears 3 (1974) observes there are only four appendages. elements at NI and also increases its armature Fortey and Morris (1978) described a larval throughout the naupliar phase. The segment stage of trilobites that precedes the protaspis (or number of the antennule can be 1–3 in the anaprotaspis as the first protaspis is often called). Oligoarthra (cf. Dahms, 1990). For species in They identified this larva as a crustacean naup- which it is 3-segmented, the 1st segment is lius. The fossils, however, show no appendages always unarmed and the 2nd segment always and therefore, little about naupliar affinities can bears 3 setae, of which the distalmost is by far be inferred (cf. Fryer, 1992). Maas et al. (2003) the longest. Homologues of these 3 setae (I–III) give arguments that the Crustacean (ortho-) are assumed in the Polyarthra based on their nauplius, as a larva having exactly three limb- position. Therefore, the unarmed segment of the bearing segments, cannot be derived from a 1st nauplius of the Polyarthra and Oligoarthra larva with four limb-bearing segments as having should be homologous; segments 2 and 3 of L. just reduced the segment number. minor correspond to segment 2 in the Oligoar- 7) Antennule segment homologues of Pol- thra, and the distal segments of L. minor are yarthra and other Copepoda (Fig. 3): In Longi- homologous to the 3rd segments in the Oligoar- pedia minor the antennule is 6-segmented at NI thra. and 5-segmented from NII to NVI (cf. Dahms, An antennule of 5 segments in the nauplii of 1990). From NI to NII a new, unarmed segment Polyarthra (6 segments at NI of Longipedia develops which subsequently is reduced in size minor, cf. Dahms, 1990) is unusual; there are no to a mere disc at NVI, at which stage it probably more than 3 segments in the other taxa of the functions as a joint for the paddle-like distal Copepoda. On the other hand, six antennular segment. At NI the antennule bears 1 long, segments are characteristic throughout the nau- spinulose seta each anteriorly on distal out- pliar phase for the Cephalocarida (Sanders, growths of the 2nd, 3rd and 5th segments. The 1963b), lepadid Cirripedia and Ascothoracida proximal seta remains situated on the 2nd seg- (Grygier, 1987a). Reallocation of the Polyarthra 43

There is no functional neccessity as an adap- the dorsodistal corner of the 1st segment and tation to a pelagic life for the acquisition of only the more proximal setae are lost. additional antennular segments (i.e. a second- The same phenomenon of setal loss occurs ary addition of segments to a presumed 3-seg- on the distal antennular segments. Often, 1 tiny mented antennule). Calanoid nauplii swim suc- seta on the terminal segment ventral to the cessfully with 3-segmented antennules which aesthetasc is lost from CI to CII (e.g. Tegastes have a flattened distal antennular segment sim- clausi) (Dahms, 1989). Even a second seta, ilar to that in polyarthran nauplii. However, due proximal to the terminal setae/aesthetasc comp- to functional improvements, this has probably lex, disappears inThalestris longimana (Dahms evolved independently in the nauplii of the two 1989, 1990). The setae which become lost here groups. An antennule of more than three seg- are homologous to those of the naupliar distal ments may be a plesiomorphic character re- antennular segment. This is supported by iden- tained from a maxillopodan ancestor. This in- tical seta numbers in, for instance, Longipedia ference is supported by Grygier (1987a), who minor and Heterolaophonte minuta (14 setae/ postulates an 8-segmented antennule as a con- aesthetasc at both, NVI and CI). stitutive feature of the Maxillopoda. The loss of setae on the antennules of early In L. minor the 3 proximal setae are retained copepodids is interpreted as evidence for a on the 1st segment of the antennule of copepo- higher ancestral number of antennular segments did I while the 1st segment of the nauplius either within the Polyarthra and Oligoarthra and other becomes reduced or is fused to the former 2nd taxa by Dahms (1989). Dahms has suggested segment (cf. Fig. 3). The same holds for oligoar- that the presence of additional setae on the 1st thran antennules: the naupliar 1st segment is lost and most distal segments of the antennules of and the 2nd naupliar segment gives rise to the the copepodids is a palingenetic recapitulation 1st segment of the copepodid antennule. This (or „haeckelian“ in the sense of De Beer, 1940); becomes particularly evident when the 1st seg- i.e. they indicate that stem line taxa of the ment of CI still bears 3 setae, as in the oligoar- Harpacticoida must have had more than 1 seta thran Ectinosoma melaniceps, Parathalestris on their proximal segments as a ground pattern clausi, Tigriopus brevicornis and Amonardia and additional setae on the distal segment at CI normani (Dahms, 1989).Heterolaophonte minu- at least. Gurney (1931) as well as others have ta, also belonging to the Oligoarthra, shows this interpreted the presence of more setae than best because its proximal setae have different usual on a segment as an indication of a fusion morphologies and can thus be traced individual- of segments, and Dahms (1989) suggested that ly. Seta I is minute at NVI and is lost at CI. Seta stem line (juvenile/adult) Harpacticoida had II with its peculiar spinulous ornamentation is antennules with more segments than crown group retained in its subdistal position and the large representatives. That the setae which are lost seta III in the most distal position. Seta II be- among copepodids are actually those homolo- comes lost at CII. As in other species (e.g. gous to naupliar setae, and not those added Ectinosoma melaniceps), the largest and most during copepodid development, has not been distal seta (seta III) is retained in later copepo- stated previously. Dahms (1989) showed that an dids. Reductions confined to the most proximal increase of seta number and segments during segment are also observed in Scutellidium hip- copepodid development takes place only in the polytes andTisbe , where 2 of the 3 setae become middle of the appendage, leaving the most pro- reduced from CI to CII (unpublished obser- ximal and distal segments and presumably naup- vations). With the exception of Macrosetella liar homologues conservatively unchanged. gracilis, where a seta at the dorsodistal corner of This supports the notion that the naupliar setal CI and CII is replaced by a row of spinules at number is retained proximally and distally in CIII, and with spinules lost at CIV, all the early copepodids at least in some of the species harpacticoids studied, retain the large seta III on studied. 44 H.-U. Dahms

8) Dorsocaudal process (Fig. 6): A caudal the cone-like caudal spine of NI is reduced in spine is probably of functional importance for size at NII and completely lost at NIII (Koga, the swimming behaviour as a balancing organ. 1984). Its early appearance and later reduction This would explain why it is developed only in probably indicates its plesiomorphic larval char- the Polyarthra and planktonic larvae of the Oli- acter state. goarthra, and is widespread among supposedly A dorsocaudal spine is probably of functional underived Crustacean groups with planktonic importance during swimming which may explain nauplii. Among other Copepoda a caudal pro- why it is developed only in planktonic larvae of cess is known also from some Poecilostoma- the Harpacticoida, such as in all known species of toida. Longipediidae (Polyarthra) and in Microsetella A short dorsocaudal spine is further present norvegica, a planktonic representative of Ecti- in nauplii of Mystacocarida, Ascothoracida, nosomatidae. Nauplii of Longipediidae are cha- Facetotecta, and could grow out to a long pro- racterized by a dorsocaudal process and a similar cess in some Cirripedia. In view of its important structure is also present in later copepodids. functional role it is not unlikely to assume that a This spine, decreases in relative length dur- caudal process has evolved independently for ing development. The furcal setae arise from a more than once, even among the “Maxillopo- ventrodistal bulge and, with the caudal process, da”. The 1st stage nauplius of Euterpina acuti- form a tri-partite unit probably functionally frons, a planktonic harpacticoid belonging to important for balancing. The furcal setae are the Tachidiidae (Harpacticoida — Oligoarthra, very stout at NI. At NII they become drastically cf. Dahms, 1990) does not bear a caudal spine reduced in size and lose their spinular ornamen- but a replacement structure. This is a remark- tations. Then they bear long spinules on the ably prominent and arched ventral portion of the outer edge of the distal third. The balancing abdomen, furnished with a semi-lunar-shaped function is probably taken over by the newly row of long spinules, probably forming a coun- developed maxillules which are nearly as strong terweight for balancing purpose as the caudal and spinulose as the caudal setae of NI. At NIII setae at early and the maxillules at later stages of there are 3, and at NIV and NV 4 caudal setae. the Polyarthra. A caudal process is present in At NVI, 6 setae are present (Fig. 6). some Cyclopoida and Polyarthra, whereas there The spine/total body length ratio decreases in is no indication of such a median structure in any Longipedia minor (present study), L. americana representative of the Calanoida (however, there (Onbé, 1984), L. brevispinosa (Koga, 1984) and is a functional replacement-complex in most L. scotti (Nicholls, 1935) throughout the phase, calanoid taxa — see below). but it decreases from NI – NIV until it is com- The naupliar dorsocaudal process of the pletely lost at NV and NVI in L. weberi (Koga, Poecilostomatoida is interpreted by Izawa (1987) 1984). In M. norvegica the cone-like caudal as homologous to that of Cirripedia, Ascotho- spine of NI is reduced in size at NII and is racida, Facetotecta, and Mystacocarida. Izawa completely lost at NIII (Diaz, Evans, 1983; Koga, (1987) states that the caudal process is a part of 1984). According to Hirakawa (1974) this spine the general plan of naupliar development among is reduced already at NII and Björnberg (1972) Cyclopoida s. l., although an unpaired caudal does not mention it at all for M. rosea. process is present only in the taeniacanthiform This spine is widespread in the nauplii of group of the Poecilostomatoida. It has to be other Copepoda and „Maxillopoda“. In his de- emphasized that the spine/total body length scription of the development of the parasitic ratio in Longipedia minor, L. americana (cf. Taeniacanthus lagocephali (Taeniacanthidae), Onbé, 1984), L. brevispinosa (cf. Koga, 1984) Izawa (1986b) states that the two naupliar stag- and L. scotti (cf. Nicholls, 1935) decreases from es present in this species have short caudal NI to NIV and is completely lost at NV and NVI spines. Izawa (1986a) describes a caudal pro- in L. weberi (cf. Koga, 1984). In M. norvegica cess for the nauplii of 4 families of poecilostome Reallocation of the Polyarthra 45 cyclopoids: Anchistrotos pleuronichthydis fringing ornamentation of formerly separate (Taeniacanthidae), Tegobomolochus nasicola segments, 4 segments may have been present in (Tegobomolochidae), Doridicola sepiae and the ancestral endopodite. However, a 4-seg- Nasomolgus firmus (Lichomolgidae). Izawa mented antennal endopodite is unknown from (1987) considers the caudal process to be a part nauplii of extant Crustacea. of the general plan of naupliar development among The exopodal segments of Polyarthra in- Cyclopoida although an unpaired caudal process crease from 6 at NI to 7 at NII, 8 at NIII and the is present only in certain species of this group. final number of 9 at NIV–VI (Dahms, 1990). In Delamare-Debouteville (1954) described a the Oligoarthra, there is no increase in segment shorter caudal spine from at least the first eight number of the antennal exopodite except for developmental instars of the benthicDerocheilo- Phyllognathopus viguieri (Phyllognathopodi- caris remanei (Mystacocarida — cf. also Oles- dae), where a new 2nd segment is added at NIII en, 2001). The caudal process is also common in to the 4-segmented exopodite of NII; at NVI the Ascothoracida (Grygier, 1987a), „Facetotecta“ exopodite is indistinctly 5–6 segmented, be- (e.g. Itô, 1986a) and Cirripedia (e.g. Hansen, cause another unarmed disc-shaped segment 1899). The same holds for fossil Crustacea (cf. develops distal to the outer margin of the 2nd Walossek, 1993). Among other characters, it is segment (Dahms, 1990). In other oligoarthran the caudal process which makes Gurney (1930) taxa the segment number is 1–5 constantly and Nicholls (1935) stress the resemblance be- throughout the naupliar phase. However, the tween the nauplii of Longipedia and that of setae on the proximal and distal segments which cirripedes. The dorsocaudal spine is most likely are formed in the course of naupliar develop- an autapomorphy of Eucrustacea — and there- ment (e.g. those indicated by arrowheads in fore a plesiomorphy in any in-group taxon Scutellidium hippolytes) probably are indica- (Waloszek, pers. comm.). tive of a larger number of segments of this 9) Evidence for larger numbers of segments ramus. Apart from the 6 to 9 segments seen at in ancestral naupliar antennal endo- and ex- various naupliar instars in L. minor, there are opodites: In Longipedia minor the naupliar an- spinule rows on the 2nd segment at NVI, suggest- tennal endopodite is 1-segmented and bears 2 ing former segment borderlines. The proximal transverse rows of spinules in addition to the spinule row of the 2nd segment at NVI and its setae on the inner edge; 1 row is found at subdistal 2nd seta, however, may indicate 2 fur- midlength and the other more irregular one on ther segments, thus providing a segment number the distal edge (Fig. 5 — cf. Dahms, 1991). The of 11. Additionally, it can be argued that the 3 setae at midlength and its associated spinule setae on the terminal segment indicate another 2 row may indicate the location of armature and segments (if one seta per segment is the rule for arthrodial membrane of the first of an ancestral the underived state, cf. Gurney, 1931; Vaupel- 2-segmented endopodite. Spinule rows often Klein, 1984), giving rise to an ancestral number accompany segments which are separated by of 13 segments for the naupliar antennal ex- arthrodial membranes in many Copepoda and in opodite ofL. minor. It seems more reasonable to the Polyarthra (see Figs. 5A, B). In the Oligoar- assume, however, that a crown group of 3 setae thra only the seta(e) at midlength remain as represents the groundpattern in the Copepoda, observed in the primitivePhyllognathopus vigu- leaving a number of 11 segments for the naupli- ieri and the more derived Scutellidium hippoly- ar antennal exopodite as the ground-pattern of tes. A transverse spinule row has never been the Polyarthra. observed at midlength in nauplii of the Oligoar- The antennal exopodite is 13-segmented in thra. At NVI of Longipedia minor there are 2 Cephalocarida, 9-segmented in Mystacocarida additional rows of spinules on the endopodite — and Cirripedia, 8-segmented in most Asco- one proximal to the row at midlength and one thoracida. However, there are up to 13 segments distal to it. Assuming that these are the distal in planktotrophic, late metanaupliar ascothora- 46 H.-U. Dahms cidans (cf. Boxshall, Böttger-Schnack, 1988). tacocarida (Olesen, 2001) bear a 3-segmented Most nauplii of the Facetotecta are described as one. Boxshall and Böttger-Schnack (1988) de- having 4–5-segmented antennal exopodites. scribed a 3-segmented antennal endopodite also According to Itô (1990) they are 6-segmented. from a late metanauplius of the Ascothoracida. Among copepod nauplii 6-segmented exopodites In Cirripedia a formerly 3-segmented endopodite are widespread, and copepod nauplii do not might be present (Grygier, pers. comm.). A 2- show a higher segment number (with the excep- segmented condition may be indicated by an tion of later stages of Polyarthra and certain indentation of the inner middle portion which Cyclopoida belonging to Oncaeidae and Cory- bears a bundle of setae. In nauplii of the cirriped caeidae, the latter with 7 segments at later nau- Chthamalus stellatus (Bassindale, 1936) there pliar stages; cf. Koga, 1984). However, in some are 4 medial setae, as there are in later stages of species the 6-segmented state is acquired only at both taxa belonging to the Polyarthra (Dahms, later stages (at NIII in some representatives of 1990). Cyclopoida; cf. Dahms, Fernando, 1993). Re- duction of segment number takes place inde- Phylogenetic affinities within the pendently especially in parasitic taxa of the Maxillopoda Cyclopoida and Harpacticoida (Dahms, 1992). The increase in segment number of the an- Dahl (1956) included the Ascothoracida, tennal exopodite in the Polyarthra (from 6 seg- Branchiura, Cirripedia, Copepoda and Mysta- ments at NI to 9 at NIV) is unknown in other cocarida into the taxon Maxillopoda. Later, the groups of Copepoda or Maxillopoda. In the Ostracoda, Facetotecta, and Pentastomida were Cyclopoida and Calanoida there are 6 segments included as extant taxa, as well as the fossil among all nauplii, whereas there are 9 in the species Bredocaris (Orstenocarida) and Skara Mystacocarida and Cirripedia. In Chthamalus (Skaracarida) (Walossek, 1993). On the other stellatus (Cirripedia), for instance, there are 2 hand Abele et al. (1992) do not allocate the setae on the 1st seta-bearing segment, 1 seta on Branchiura and Mystacocarida to the Maxil- each of the following segments, and 3 setae on lopoda. the terminal segment (Bassindale, 1936), as is Branchiura, Tantulocarida and Pentastomi- the case in the Polyarthra. However, there might da appear to lack naupliar stages, and data on be an increase of segments during the naupliar ostracod nauplii are limited so that not all max- development of some Cirripedia as this has been illopodan taxa considered in the present study. reported for Ascothoracida (Itô, Grygier, 1990). Because the Maxillopoda show several features Although neither a reconstructed 13-segmented in reduced states (cf. Dahl, 1956), there is a nor an observed 9-segmented naupliar antennal question concerning the process effecting these exopodite is known from any other copepod features. Progenetic paedomorphosis is one pro- taxon, a 12-segmented antennal exopodite was cess which explains these features. Since the shown for an ascothoracid metanauplius type I ancestral condition among the Crustacea in gen- by Boxshall and Böttger-Schnack (1988). eral comprises anamorphic development, it was No indication of a 2nd segment on the endo- inferred that a reduction in the number of larval podite of the second antenna has been reported instars was achieved by progenetic paedomor- from any other copepod group except the Cyclo- phosis, precocious maturity of a larval form. poida (e.g. Gurney, 1932), where the endopodites However, paedomorphosis may merely be an are 2-segmented. But 2 and even 3 segments are convenient mechanism to explain a reduction in common for other taxa of the Maxillopoda and number of somites or appendages, when a bi- the Cephalocarida. Ascothoracida (Grygier, ramous mandibular palp is retained in the adult. 1987a), Facetoteca (Itô, 1986b) and Cephalo- The Maxillopoda usually have feeding nau- carida (Sanders, 1963b) bear a 2-segmented plii. The retention of the larval feeding mecha- endopodite throughout the phase, whereas Mys- nism in the adult stage is believed to be the first Reallocation of the Polyarthra 47 step in the evolution of all maxillopodan groups. cladogram includes an unresolved trichotomy, It represents a prerequisite for the specialization with the Tantulocarida as one branch, the Copep- of the thorax as a locomotory center and the oda and its sister-taxon Thecostraca as the sec- head as a center for feeding. Sanders (1963a) ond, and the Branchiura, Mystacocarida plus postulated that the metanauplii of cephalocarids Ostracoda as the third branch. The approach of and mystacocarids are the most plesiomorphic Grygier (1987a), using mainly naupliar and among Crustacea in their retention of a primi- cyprid characters, united the Cirripedia, Asco- tively benthic mode of life and correlated mor- thoracida and Facetotecta as the monophylum phological features. If this is true, one cannot Thecostraca. He suggested that the Branchiura specify apomorphic states unique to maxillopo- is the sister-group of the Thecostraca, and that dan nauplii. Rather, most of their common fea- the Copepoda, exhibiting the most plesiomor- tures would seem to be plesiomorphic for Crus- phic character states, is the sister-group of Bran- tacea in general. chiura plus Thecostraca. Grygier (1987a) could The Thecostraca Gruvel (1905) (compris- not provide any apomorphy for all five taxa ing the Cirripedia, Ascothoracida, Facetoteca together. Boxshall and Huys (1989) also sug- (cf. Grygier, 1987a)) have three naupliar char- gested two main lineages within the Maxillopo- acters in common which are unique among da, one leading to the Copepoda core (compris- crustacean nauplii and provide strong autapo- ing Copepoda, Mystacocarida, Skaracarida) and morphies characterizing this monophyletic tax- the other to the Thecostraca core (comprising on (cf. Dahms, 2004): absence of appendages Thecostraca, Branchiura, Ostracoda) (cf. Dahms, caudal to the maxillule; presence of frontal 2004). filaments; presence of lateral ridges [where are Regarding adult characters, the Polyarthra the lateral ridges]. Dahms (2004) hypothesized fit into the character scenario already depicted a sister-group relationship of the Copepoda and for the ancestral copepod by Boxshall et al. the Thecostraca. This hypothesis can be extend- (1986). This, however, is largely a result of the ed to a sister-group relationship between the underlying assumption that copepod evolution Polyarthra as an underived branch of the has proceeded by oligomerization (cf. Hessler, Copepoda and the Thecostraca based on the Newman, 1975 — for the Crustacea in general). following three synapomorphies (for a phylo- Also, the naupliar synapomorphies Polyarthra genetic diagram cf. Dahms, 2004): six naupliar share with all other Copepoda (see above) leave stages; absence of somite borders throughout no doubt about their affinity to the Copepoda. the naupliar phase; pronounced changes be- Both character sets, however, from naupliar as tween nauplius and subseqient phase. well as from juvenile and adult semaphoronts, provide evidence for the exclusion of the Pol- Discussion yarthra from the Harpacticoida. Polyarthra do not share a single naupliar synapomorphy with Grygier (1983) stated that naupliar charac- Oligoarthra. As for adult characters, Thiemann ters can be dismissed for the characterization of (1984) critically evaluated the diagnostic char- the Maxillopoda as a monophylum because they acters provided by Lang (1948) for the Harpac- either are plesiomorphic or represent conver- ticoida and concluded that no convincing apo- gences. Here naupliar characters are inspected morphies for the Harpacticoida are recogniz- and successfully used as synapomorphies for able. Even a short antennule is plesiomorphic in the subtaxa Thecostraca and Copepoda. The the light of maxillopodan ancestry, providing a phylogenetic relationships within the Thecos- plesiomorphic character in probably reduced traca and the monophyletic status of the Thecos- state. According to Thiemann (1984), the whole traca + Copepoda was previously suggested by question about the phylogenetic allocation of Schram (1986: 538, fig. 43.6), who based his the Podoplea center on the antennular segment conclusions mainly on adult characters. His number, but the derived states cannot be deter- 48 H.-U. Dahms mined because the original segment number is rived clade of the Copepoda together with the not discernable. Thiemann (1984) suggested Gelyelloida and the Mormonilloida. A similar that in order to reduce the number of plesiomor- allocation results from the analysis of Huys and phic diagnostic characters of the Polyarthra, the Boxshall (1991) where the Harpacticoida (Pol- Polyarthra be placed as an underived taxon at yarthra plus Oligoarthra) are the sister taxon of the base of the Copepoda, close to stem-line the Poecilostomatoida-Siphonostomatoida- representatives of the podoplean Cyclopoida. Monstrilloida-clade, which is relatively derived There is no need, however, to establish a new compared to the Platycopioida, Calanoida and taxon name for non-polyarthran Harpacticoida Mormonilloida. for the fact that the Oligoarthra are then the only Are Polyarthra and Oligoarthra sister taxa or taxon left from the Harpacticoida sensu Lang a paraphyletic assemblage? Here we have a case (1948). To summarize, Thiemann (1984) based of conflicting evidence caused by characters his argumentation solely on the adult organiza- derived from two phases of ontogenetic sema- tion, did not provide sufficient reproducible phoronts. If the interpretation of adult charac- character information, yet came to the same ters is correct, one may ask how naupliar char- phylogenetic conclusion as the present study acters fit into this scheme. There are two possi- which used non-overlapping naupliar characters bilities of character interpretation: as a data source for phylogenetic inferences. a) Naupliar characters are conservatively According to Huys and Boxshall (1991), on unchanged: It is possible that both phases of the other hand, there is no reason as far as adult Polyarthra, the naupliar and the copepodid phas- characters are concerned, to exclude the Poly- es leading to the adults, have evolved with arthra from the Harpacticoida. They hypothesize different degrees of evolutionary radiation. the following apomorphies for the Harpacticoida Nauplii, therefore, may be conservatively un- sensu Lang (1948): Fusion of particular segments changed, whereas the juvenile/adult forms have on the female and male antennule, presence of only evolved to their present derived state. 3 setae on the inner margin of exopodal segment 3 b) Plesiomorphic naupliar characters are of second swimming leg, presence of only 1 seta on reaquired: Evolutionary progress in general and the inner margin of endopodal segment 2 of first for Crustacea in particular may be characterized swimming leg, a 2-segmented maxillipedal en- by specialization, often accompanied by reduc- dopodite in which the ancestral segment 5 is tions and simplifications leading from a homon- incorporated into the compound proximal seg- omous and polymeric organization to a heteron- ment, retention of relatively plesiomorphic states omous and oligomeric state of somites and of derived characters given for the Poecilo- appendages. This is the concept of oligomeriza- stomatoida-Siphonostomatoida-Monstrilloida- tion which was probably elaborated best by clade. None of these character states provides a Dogiel (1954), who understood oligomerisa- unique apomorphy. Furthermore, all of these tion as the evolution and specialization of vari- characters are meristic and in reduced state. As ous groups of metazoa accompanied by gradual for the maxilliped of the Oligoarthra, the distal reduction of a number of homologous organs. part of the claw (=subchela) is a 2-segmented This oligomerization of a number of organs endopodite; a very careful analysis of the addi- evolved to different systems of organs and is tion of setae suggests that the endopodite of observed through quite different specializations. Polyarthra is either 4-segmented (in the Longi- However, the reverse could also be true. Why pediidae) or 3-segmented (in the Canuellidae) should a secondary annulation and increase in (see Ferrari, Dahms, 1998). Therefore, the polyar- segments, setae, etc. not have occurred? Sec- thran endopodite does not bear the 6-segmented ondly, Dollo’s law (saying basically that struc- ramus suggested by Huys and Boxshall (1991). tures that had been lost in evolution can never be Ho (1990) did not analyse the Harpacticoida reacquired exactly in the same form) has been in particular but allocated them as a more de- invalidated by genetic analysis, for instance in Reallocation of the Polyarthra 49 fruit flies. These show that changes in the timing thank the technical staff of the department for of gene repression or alteration of repressor assistance and my colleagues for encourage- molecules can restore ancestral gene function ment. Mrs. Julia Delingat, Sophie Martyna, and (cf. Ferrari, 1988). The reappearance of ances- Conny Pfeiffer assisted in the preparation of tral characters, reversals, or, “taxic atavism“ figures and text. This study was funded by the (Stiassny, 1992) represents a major problem for DFG — HUD being the principal investigator phylogenetic reconstructions. When apomor- (Da256/7–1; Da 256/10–1) and DAAD (436 phic character states of a taxon do not differ RUS 17/20/98; A/99/09723). from corresponding plesiomorphic character states, then character polarity becomes obscured. Literature

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