Contributions to Zoology, 67 (2) 125-141 (1997)
SPB Academic Publishing bv, The Hague
Phylogeny of the Anomura (Decapoda, Crustacea): Spermatozoa and
spermatophore morphological evidence
Christopher+C. Tudge
Crustacean Laboratory, Museum of Victoria, 71 Victoria Crescent, Abbotsford, Vic. 3067, Australia
Keywords: Anomura, phylogeny, spermatozoa, spermatophore, ultrastructure, hermit crabs
le Abstract un taxon monophylétique: genre lomoïde Lomis est exclu de
ce tandis le groupe, que genre thalassinide Thalassina y est
La indu. -synapomorphie pour la des taxons conven- A of majorité phylogenetic analysis selected anomuran, thalassinidean, tionnels d’Anomures.(Lomis exclu) est l’origine cytoplasmique and other decapod crustacean taxa, based on spermatozoal des branches microtubulaires. Si des représentants des ultrastructural characters and spermatophore morphological Palinurides des Thalassinoïdes et sont séparément désignés characters, was performed and the following relationships of comme “outgroups”, les Astacidea + the Brachyura forment un taxa are elucidated from the trees produced. The Anomura groupe-frère pour les Anomura. Les superfamilles Thalassi- are not a monophyletic assemblage, with the lomoid Lomis
noidea, Paguroidea et Galatheoideane sont des exclusive of pas groupes being the remainderof the anomurantaxa, and the monophylétiques. Les montrent thalassinid analyses que les familles Thalassina included in the anomuran clade. The d’Anomures Coenobitidae et Porcellanidae sont des the groupes synapomorphy joining majority of the conventional ano- monophylétiques. La famille de Paguroïdes Diogenidae est muran taxa (Lomis excluded) is the cytoplasmic origin of the paraphylétique, les Clibanarius et Cancellus devant être microtubular genres arms. When the palinurid and thalassinoid du clade contenant le des Les séparés reste genres diogenides. representatives are separately designated as outgroups, the et familles Paguridae Parapaguridae forment un mono- Astacidea clade and Brachyura jointly formed a sister group to the
- à du phylétique l’exception genre Porcellanopagurus. Les Anomura. The superfamilies Thalassinoidea, Paguroidea, and deux représentants de la famille Chirostylidae Eummida et Galatheoidea not In all the ( are monophyletic groups. analyses Uroptychus) ne peuvent pas être associés avec les autres anomuran families Coenobitidaeand Porcellanidae each form a espèces des Galatheoidea. Les taxons de la familleGalatheidae The is monophyletic group. paguroid family Diogenidae para-
ne forment pas un groupe monophylétique. Le seul with the Clibanarius and Cancellus Hippoïde phyletic, genera separate étudié. Hippa, est considéré comme groupe-frère des autres from a the single clade containing remaining diogenid genera. taxons d’Anomures Lomis The (. excepté). families Paguridae and Parapaguridae form a mono- phyletic clade with the exception of Porcellanopagurus. The two representatives of the family Chirostylidae ( Eumunida and
Uroptychus ) fail to associate with the other species in the Introduction
Galatheoidea. taxa The in the family Galatheidae are not a monophyletic assemblage. The only investigated hippoid The of use spermatozoal ultrastructure in tax- is sister the remainder of the Hippa portrayed as the group to and is onomy phylogeny now firmly established anomuran taxa (with the exception ofLomis).
as a valid means of investigating phylogenetic
in various animal There relationships groups. are
Résumé many phyla in which advances have been made in
phylogenetic studies by using spermatozoal ultra-
Une Recent include studies analyse phylogénétique d’une sélection de taxons d’Ano- structure. examples in the mures, de Thalassinides d’autres et Décapodes, basée sur des Platyhelminthes (Ehlers, 1985; Justine, 1991); caractères ultrastructuraux des des spermatozoïdes et sur Polychaeta (Jamieson & Rouse, 1989); Oligo- caractères morphologiques du spermatophore, a été entreprise, chaeta (Jamieson, 1981, 1983); Mollusca et les arbres (Healy, produits permettent d’élucider plusieurs aspects fish 1991b; Mattel, and concernant la entre taxons. Les Anomures 1988); (Jamieson, 1991), parenté ne sont pas
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Amniota (Healy & Jamieson, 1992; Jamieson & have been the subject of several investigations at
Healy, 1992; Jamieson, 1995a, b). the morphological and molecular level. Of note
Within the Crustacea, studies on spermatozoal are the phylogenetic analyses of the constituent ultrastructure in representatives of the Penta- families of the Anomura using adult and larval stomida (Wingstrand, 1972; Storch & Jamieson, somatic morphology (McLaughlin, 1983b; Martin
1992) have confirmed that the pentastomids are & Abele, 1986; Richter & Scholtz, 1994; Scholtz
view crustaceans, a endorsed by molecular biol- & Richter, 1995) and the analyses of several
based ogy (Abele et al., 1989). Similarly, spermatozoal members of the Anomura on 18S rRNA
nucleotide Abele ultrastructure has been shown (Jamieson & sequences by Spears & (1988)
Tudge, 1990; Jamieson, 1991a, 1994; Jamieson et and Spears et al. (1992), 16S rRNA by al., 1995) to support Guinofs re-classification of Cunningham et al. (1992), and 16S rRNA and the Brachyura (Guinot, 1977, 1978) into cytochrome oxidase I genes by Tam et al. (1996).
Podotremata, Heterotremata (sensu lato), and Richter & Scholtz (1994: 197) state that “the
Thoracotremata, based on differential location of phylogenetic relationships (within the asymmetri-
cal hermit unresolved and be the male and female gonopores. crabs) are seem to
of While the of The phylogenetic significance crustacean very complex". recognizing validity spermatozoa had been recognized by Koltzoff the taxon “Anómala”, particularly as used by
(1906) and later, Wielgus (1973). Koltzoff (1906: Scholtz & Richter (1995), and not wishing to
424) was one of the first workers to construct a enter into debate over terminology, I prefer to use phylogeny of crustaceans based on spermatozoal the term “Anomura” for the infraorder containing structure at the light microscope level. To the the superfamilies Galatheoidea, Paguroidea, Hip-
encountered he and different sperm types assigned a poidea, Lomoidea, as argued by McLaughlin binomen consisting of the “generic” name & Holthuis (1985).
and and The value of such Spermia a descriptive “species” name computer programs, as placed this binomen on the nodes and branches of PAUP (Phylogenetic Analysis Using Parsimony) his phylogenetic tree. The crustacean taxa in- (Swofford, 1993), for phylogenetic analysis of cluded in his study were Mysis, Euphausia, spermatozoal and molecular characters has been
well demonstrated in animal Natantia, Galatheidea, Paguridea, Thalassinidea, many groups (Jamie-
& Astacus, Loricata, Brachyura, Oxystomata, and son et al., 1987; Kim Abele, 1990; Abele,
Dromiidea. Some of the significant relationships 1991; Jamieson, 1991b, 1993, 1994, 1995a, b; apparent in Koltzoff s phylogenetic tree were the Spears et al., 1992; Jamieson & Grier, 1993; separation of Mysis from the decapods at the Jamieson et al., 1995). The present study investi-
42 node Spermia flagellifera, recognizing the pres- gates the interrelationships of species of ence of what is now termed a pseudoflagellum anomuran crab, three species of thalassinidean
(Jamieson, 1987) in the spermatozoa of Mysis. shrimp, and six species of other decapods using
The Galatheidea and similar and anomuran groups Paguridea parsimony analysis procedures em-
in 26 were designated Spermia erecta, recognition of ploys spermatozoal and 6 spermatophore char- the superiorly positioned, generally elongate acters. acrosome vesicle. The Brachyura, Oxystomata, and Dromiidea were labelled Spermia cepha- lacantha. The latter binomen probably refers to Materials and methods the nuclear and that many arms spikes project
The taxa included in this analysis, with sources of character laterally from around the acrosome vesicle of the
information, are displayed in Table I. Appendices A & B spermatozoa in these groups. describe the characters used in the parsimony analysis and the The relationships among the families in the complete data matrix, respectively. Of the 32 characters infraorder Anomura “Anomala” of Boas, (the employed in the analysis only one (character 19) is considered and within uninformative. 1880), among representatives families, at present phylogenetically
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Table I. Taxa included in the analysis. [ ] = source of character information.
InfraorderInfraorder Thalassinidea Strigopagurus boreonotusboreonotus Forest, 19951995 [Tudge, 1995a, 1996] Axiidae: Axius glyptocercus Von Martens, 1868 [Tudge, Galatheidae: Allogalathea eleganselegans (Adams & White, 1848)1848)
1995a, b] [Jamieson, 1991a;1991a;Tudge,Tudge, 1995a]
Callianassidae: australiensis Munida Trypaea (Dana, 1852) [Tudge,[Tudge, sp. [Tudge, 1995a, b]
1995a] Munidopsis sp.sp. [Tudge, 1995a] Thalassinidae: ThalassinaThalassina squamifera De Man, 1915 [Tudge,[Tudge, Hippidae; Hippa pacifica (Dana, 1852) [Matthews, 1956; 1995a, b]b] Tudge,Tudge, 1995a,b]
Lomidae:Lomidae: Lomis hirta (Lamarck, 1810) [Tudge, 1995a, b,
Infraorder Anomura 1997]1997]
Chirostylidae: Eumunida sternomaculata St. Laurent & Paguridae;Paguridae; Pagurus bernhardus (Linnaeus, 1758) [Tudge,[Tudge,
Macpherson, 1990 [Tudge, 1995a, b] 1995a]1995a]
chevreuxi Uroptychus sp.sp. [Tudge, 1995a] Pagurus chevreuxi (Bouvier,(Bouvier, 1896) [Tudge,[Tudge, 1995a,1995a, b]
Coenobitidae: Birgus latro (Linnaeus, 1758) [Tudge[Tudge & Pagurus hirtimanusMiers, 1880 [Tudge, 1991, 1995a]
Jamieson, 1991;Tudge,Tudge, 1991, 1995a] Pagurus prideaux Leach, 1815 [Tudge, 1995a]
18521852 Coenobitabrevimanus Dana, [Tudge, 1991, 1995a] Porcellanopagurus sp. [Tudge, 1995a,b]
* Coenobita H. 1837 * perlatus Milne Edwards, [Tudge, 1991, Xylopagurus sp.sp. nov.nov. [Tudge,[Tudge, 1995a, b]
1995a, b] Parapaguridae: Sympagurus sp. [Tudge, 1995a,1995a,b]
Coenobita 1858 purpureuspurpureas Stimpson, [Tudge, 1995a] Porcellanidae: Aliaporcellana suluensis (Dana,(Dana, 1852) [Tudge,
Coenobita rugosusrugosas H. Milne Edwards, 1837 [Tudge, 1991, 1995a,1995a, b; Tudge & Jamieson, 1996a]
1995a] PetrolisthesPetrolisthes armatus (Gibbes, 1850) [Tudge, 1995a; Tudge&
Coenobita variabilisvariabilis McCulloch, 1909 [Tudge,[Tudge, 1991, 1992, Jamieson, 1996b]
1995a] Petrolisthes lamarckii (Leach,(Leach, 1820)1820) [Jamieson,[Jamieson, 1991a;
Diogenidae: Calcinus gaimardii (H. Milne Edwards, 1848) Tudge, 1995a; Tudge & Jamieson, 1996b] Pisidia [Tudge, 1995a] longicornis (Linnaeus,{ Linnaeus, 1767)1767) [Retzius, 1909; Mouchet,
Calcinus laevimanus(Randall, 1840) [Tudge, 1995a] 1931;Tudge,Tudge, 1995a; Tudge & Jamieson,Jamieson, 1996a] Calcinus minutus Buitendijk, 1937 [Tudge, 1991, 1995a,1995a,b]b] Polyonyx transversustransversas (Haswell, 1882) [Tudge, 1995a,1995a, b; Cancellus & sp. [Tudge, 1995a, b]b] Tudge Jamieson, 1996b] Clibanarius corallinus (H. Milne Edwards, 1848) [Jamieson, Infraorder Astacidea 1991a;1991a; Tudge, 1991,1991, 1992, 1995a] Astacidae:Astacidae; Pacifastacus leniusculus Dana, 1852 Clibanarius [Dudenhausen erythropus (Latreille, 1818) [Tudge, 1995a] & Talbot, 1982,1982, 1983] Clibanarius longilarsus (De Haan, 1849) [Tudge, 1995a, b] Homaridae: Homarus americanusamericanas Milne Edwards, 1837 [Tal- Clibanariustaeniatus (H. MilneEdwards,Edwards, 1848) [Tudge, 1992, bot & Chanmanon, 1980a,b] 1995a]1995a]
Clibanarius virescens 1991, 1992, (Krauss,(Krauss, 1843) [Tudge,[Tudge, 1991, Infraorder Palinura 1995a]1995a] Palinuridae: Panulirus argus (Latreille,(Latreille, 1804) [Talbot & Dardanus arrosor ((Herbst,Herbst, 1995a, b] 1796)1796) [Tudge,[Tudge, Summers, 1978] Dardanus crassimanuscrassimanus (H.(H. Milne Edwards, 1836) [Tudge, Scyllaridae; Thenus orientalis (Lund, 1793) [Burton, 1995; 1992, 1995a] Jamieson, pers. comm.] Dardanus lagopodes {Forsk&l,Forskäl, 1775)1775) [Tudge, 1991, 1995a]
Dardanus scutellatus (H. Milne Edwards, 1848) [Tudge, Infraorder Brachyura
1995a]1995a] Majidae: Menaethius monoceros (Latreille,(Latreille, 1825) [Jamieson,[Jamieson, Dardanus * sp. nov. [Tudge, 1995a] 1991a, pers.pers. comm.]comm.]
Diogenes custoscusios (Fabricius, 1798) [Tudge, 1992, 1995a] Portunidae: FortunasPortunus pelagicuspelágicas (Linnaeus, 1766)1766) [Jamieson,
Diogenes pallescens Whitelegge, 1897 [Tudge, 1995a, b] 1989;1989; Jamieson & Tudge,Tudge, 1990]
* Probable from the western Pacific Ocean; in the MNHN, Dardanus new species currently lodged Paris, awaiting identification ( sp.
nov. - - Pg 5468, Xylopagurus sp. nov. Pg 5337).
Phylogenetic analysis branch-swapping performed; MULPARS option in effect; stee-
pest descent option not in effect; branches having maximum The phylogenetic analysis was performed using PAUP version length zero collapsed to yield polytomies; topological con- 3 1.1 multi-state (Swofford, 1993), utilizing a data matrix originally set up straints not enforced; trees unrooted; taxa inter-
in MacClade version 3 (Maddison & Maddison, 1992). Heuris- preted as polymorphism; character-state optimization: accele- tic search analyses were performed with the following options rated transformation (ACCTRAN). All characters unordered applied. Addition held each and unsealed. sequence; simple; one tree at step during stepwise addition; tree-bisection-reconnection (TBR) As suggested by Hillis (1991) and demonstrated in Hillis &
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Huelsenbeck (1992), the strength of the phylogenetic signal higher taxonomic groupings, relevant characters
of information content) for a given data set can be (measure and contentious clades and taxa are indicated. interpreted from the skewness (or otherwise) ofthe distribution The cladogram of the same consensus tree is of all the given trees. A symmetrical (bell-curve) distribution shown in Fig. 2, with clades not supported by indicates that the data are random, and the most parsimonious 100% indicated. tree obtained from these data would not necessarily reflect the of trees phylogenetic history of the taxa used. Notwithstanding recent Heuristic analyses (with identical parameters
criticism ofthe skewness criterion as a measure of phylogenetic above the astacid as the analysis), using two gen- signal (Kallersjo et al., 1992), it is applied in the present study. era Homarus and Pacifastacus and, separately, Using the exhaustive search setting the distribution of all three the thalassinoid genera Axius, Thalassina, trees can be obtained from a given data set. An alternative
method ofestimating the skewness oftree distributionis to use and Trypaea as outgroups, each produced a 50%
size of 1000 random trees the random trees option. A sample majority rule consensus tree of nearly identical
was chosen as it is the minimum number needed to obtain a topology to Figs. 1 and 2. Each of the consensus reasonably accurate estimate of skewness (Jamieson, 1994). trees was 136 steps long and was calculated from Two palinurids, two astacids, and three thalassinoids were 26 trees. For these the The taxa Panulirus and equally parsimonious brevity variably used as outgroup. palinurid
Thenus were used as the outgroup in the principle analysis be- trees have not been illustrated.
ofthe basal ofthe Palinura cause relatively undisputed position The distribution of 1000 random trees for the fossil mole- within the Reptantia, based on (Glaessner, 1969), analysis gave a gl value of-0.43. The negative cular (Vaughn & Traeger, 1976) and somatic morphological value indicates that the data are not random in (Scholtz & Richter, 1995) evidence. As with the Palinura, the terms of the table in Hillis & Huelsenbeck Astacidea previously have been designated a basal or stem given position within the evolution of the reptantian decapods. (1992), and therefore the phylogenetic signal is
“ Makarov 1962: stated The from which all Anomura ( 23) group significant. originated was that of the Astacura, ...” and Glaessner (1969)
indicated that the fossil record of the Astacidea is as old, ifnot
older than, that of the Palinura (excluding the Glypheoidea).
The relationship of the infraorder Thalassinideato the other Discussion
decapod infraorders has long been the subject of debate. The
crustacean workers thalassinoids are considered by some Infraorder Anomura (Burkenroad, 1963; Bauer, 1986) to have important links with
the other decapod infraorders and to have played an integral The Anomura is not shown to be a monophyletic role in the evolution of the Decapoda. They have previously One been linked with the infraorder Anomura on both larval assemblage (Fig. 1, point B). excluded taxon
MacDonald et and adult (Gurney, 1942; al., 1957) morphologi- is Lomis hirta (Lomidae), which is depicted in a cal (de Saint Laurent, 1973; Martin & Abele, 1986) evidence. very basal position, reflecting a plesiomorphic In recent cladistic analyses of adult somatic characters the (Tudge, 1997). Also, of the spermatozoal morphology thalassinoids are depicted as the sister group Anomura \ the of the thalassinid, (Poore, 1994; Scholtz & Richter, 1995). questionable placement Thalassina squamifera, with the hippoid, Hippa
pacifica, within the “anomuran” clade makes the
Results Anomura paraphyletic. For both Lomis and Tha-
lassina the spermatozoal and spermatophore mor-
An heuristic analysis of 51 decapod taxa using 32 phology is not fully known or is contentious
further alter spermatozoal and spermatophore characters (us- (Tudge, 1995a, b), and study may
the listed 26 these ing options above) gave equally relationships.
of the parsimonious trees using the outgroup method. The clade containing the vast majority
The phylogram of the 50% majority rule consen- anomuran taxa (Fig. 1, point B) is primarily char-
acterized the character state sus tree of the 26 trees is shown in Fig. 1. The by unambiguous
Thenus and Panulirus were des- from microtubular arms of palinurid genera change spermatozoa!
ignated as the outgroup. Tree length =136 steps; nuclear origin to such arms being cytoplasmic in
consistency index (Cl) = 0.493; homoplasy index origin (see character 1, Appendix A). This char-
(HI) = 0.603; retention index (RI) = 0.768; re- acter is equivocal in Lomis and Thalassina (see
= and scaled consistency index (RC) 0.378. Some data matrix, Appendix B) may go some way
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towards explaining their contentious placement been disputed by Gurney (1942) and de Saint
(Figs. 1 & 2). Laurent (1973). This latter view of paraphyly of
the Thalassinidea would here appear to receive
Infraorders Palinura, Astacidea, and Brachyura support from spermatozoal ultrastructure.
The six in these taxa decapod categories were Superfamily Paguroidea added to the further analyses to provide compari- The members of the superfamily Paguroidea son with the The Anomura. paraphyletic relation- (comprising the families Coenobitidae, Dioge- ship of the to the 1 and Brachyura Anomura (Figs. & nidae, Paguridae, Parapaguridae) are not
2) conforms with shown to be a only partially previous opinion monophyletic group (Figs. 1 & 2).
& (see Glaessner, 1969; Scholtz Richter, The inclusion of some members of the 1995). super-
The of the Astacidea sister-group relationship to family Galatheoidea within the same clade indi- the I Anomura (Figs. & 2) is more contentious cates paraphyly for both superfamilies. This is in but is of with the supportive a sister-group relationship contrast monophyletic Paguroidea sug- between Astacidea (“Astacida”) and Anomura/ gested by McLaughlin (1983b) and Richter &
Brachyura (“Meiura”) proposed by Scholtz & Scholtz (1994) using adult somatic morphological Richter (1995) and the derivation of the Anomura characters in their analyses. Admittedly though, from the Astacidea Makarov the of the is (as “Astacura”) by monophyly Paguroidea only compro-
(1962). The very basal position of the palinurid mised spermatologically by the inclusion of the representatives (when not used as an outgroup), investigated galatheids and chirostylids, both previously supported by fossil (Glaessner, 1969) sharing the apomorphic possession of three and & molecular (Vaughn Traeger, 1976) evi- microtubular arms with the spermatozoa of the dence, and their association with the thalassinoid paguroids (Fig. 1, point D). The separation of the
Trypaea (Figs. 1 & 2), are of considerable inter- Paguroidea into the traditional “right” and “left- This latter association est. is supported by the handed” hermit crabs is not upheld. The inclusion shared absence of the chamber in of the Clibanarius perforatorial clade (Fig. 1, point E), dio- the spermatozoa (Fig. 1, point A). genid or “left-handed” hermit crabs, within the
clade containing the members of the Paguridae,
Thalassinidea which considered Infraorder are “right-handed”, marts this
classical dichotomy. The general placement of
The three in this were des- the representatives taxon major genera in the Paguroidea is consistent ignated as the one outgroup for analysis based on with the intuitive phylogenetic trees previously previous indications of their sister-group relation- suggested by the author (Tudge, 1991, 1992). ship with the Anomura & (Martin Abele, 1986; Family Coenobitidae. The six species in the
Foore, The was unable to be re- in this 1994). outgroup two genera investigated family, Birgus and tained as a clade as both Thalassina monophyletic Coenobita, consistently form a monophyletic and shifted the them- Trypaea to ingroup, allying group, and, interestingly, this is a subclade of the selves with Hippa and Panulirus, respectively majority of the diogenid members (Figs. 1 & 2).
(these latter associations were maintained in the This close association between members of the analysis shown 1 In in Figs. & 2). all analyses, Coenobitidae and Diogenidae has previously been the Thalassinoidea were never retained as a suggested (McLaughlin, 1983b; Tudge, 1991, monophyletic group. Paraphyly of these thalassi- 1992; Richter & Scholtz, 1994). Monophyly of noids reflects the diverse the Coenobitidae is very spermatozoal supported on somatic mor-
exhibited the morphologies by three representa- phological grounds by McLaughlin (1983b), Mar- tives 1995a, (Tudge, b), each from a separate tin & Abele (1986), and Richter & Scholtz (1994) superfamily (Poore, 1994). Monophyly of the and now strongly supported spermatologically. Thalassinidea has been proposed by Poore (1994) Family Diogenidae. The investigated members and Scholtz & Richter but has of this (1995) previously morphologically diverse family did not
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Fig. I. Phylogram of 50% majority rule consensus tree of 26 equally parsimonious trees obtained from an heuristic analysis of 51 taxa using 32 combined spermatozoal and spermatophore characters, using the outgroup method. Tree length = 136; consistency index (Cl)
= 0.493; homoplasy index (HI) =0.603; retention index (RI) =0.768; rescaled consistency index (RC) = 0.378. Some highertaxonomic
indicated character contentious categories are (brackets) along with relevant, unambiguous, apomorphic changes (numerals), taxa
(species names in bold), and nodes of specific interest (bold capitals). Point A = characters associated with the developmentof the perforatorial chamber in the spermatozoa.Point B = the “Anomura” characterized by the shift ofmicrotubular arms from the nucleus
Point = = to the cytoplasm. C the appearance ofthe pedunculate spermatophore. Point D the restriction of the numberof microtubular arms to three. Point E = the Clibanarius species clade separated from the other traditional diogenids.
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Fig. 2. Cladogram of same 50% majority rule consensustree as Fig. 1. Clades are supported by 100% of trees unless otherwise indicated.
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and Rich- form a single clade but were split between two & Scotto (1983), McLaughlin (1983b), clades 1 & the Clibanarius ter & Scholtz and is intimated in the (Figs. 2), genera (Fig. (1994)
1, point E) and Cancellus being separated from present analysis. the remainder. The single representative of the Family Parapaguridae. The single investigated
Cancellus exhibits several unusual lies within the genus sperma- parapagurid. Sympagurus sp., tozoal features (Tudge, 1995a, b) that separate it clade containing the members of the family Pagu- from the Diogenidae (of which it is convention- ridae in this analysis (Figs. 1 & 2). The presence
in ally a member) and place it in a basal position of an accessory ampulla (character 29) and, less
stalk relation to the other paguroids. The heterogeneity so, the form of the spermatophore (character
link members of the of the genera within the family Diogenidae and 31) some family Paguridae the difficulty in determining their affinities has with the investigated parapagurids. Similarly, the been expressed by Forest (1984, 1995), but he perforatorial chamber shape (character 5), and considers the family to be an ancient mono- absence of microvillar projections (character 6)
Scholtz have phyletic group. Richter & (1994) are synapomorphies (Tudge, 1995a, b). suggested that the Diogenidae are most likely paraphyletic (as indicated in the present study), Superfamily Lomoidea but they presented no supporting evidence. Family Lomidae. The single representative of this
Family Paguridae. The representatives of the superfamily, Lomis hirta, is considered to have a
retained that in- family Paguridae are not as a mono- very primitive spermatozoal morphology
The inclusion of the dicates basal for this crab within the phylctic group. parapagurid a position
in the clade and the Anomura The of Sympagurus sp. Pagurus (Tudge, 1997). spermatozoon
Lomis exclusion of Porcellanopagurus sp. make the hirta shares many plesiomorphic charac-
with other the family paraphyletic, at least in terms of sperma- ters decapods (notably complete
in tological features (Figs. 1 & 2). The pagurid clade embedding the cytoplasm of the small acro-
(with the exception of Porcellanopagurus) is somal vesicle, the possible nuclear origin of the characterized by the presence of one or more microtubular arms, and the inconsistent number reticulated acrosome zones (character 18) in the of microtubular arms). The above characters, spermatozoa (Fig. 1), although the exact homol- combined with an imperfectly known spermato-
this character between all the inclusive Lomis the base of all ogy of phore morphology, place at
is uncertain. The the with the of genera Pagurus-Sympagurus investigated decapods, exception clade is defined by the presence of the accessory the thalassinoids Trypaea and Axius and the ampulla (character 29) in the spermatophore of palinurids (Figs. 1 & 2). Previous morphological the examined species (Fig. 1). Further investiga- studies (Pilgrim, 1965; McLaughlin, 1983a, b;
of Martin & tion of the occurrence the accessory ampulla Abele, 1986) have not agreed on the throughout representatives in the Paguridae and relationship of Lomis hirta to the other anomu- related families may confirm the validity of this rans. Richter & Scholtz (1994), supporting the character for phylogenetic analysis. The exclu- view of Pilgrim (1965), have suggested that the sion of hirtimanus from the clade Lomidae is the sister the Pagurus con- group to Paguroidea. taining the remainder of the species of the genus
Pagurus reflects the difference in sperinatozoal Superfamily Galatheoidea morphology that exists between this Indo-Pacific Family Chirostylidae. The chirostylids, Eumunida species and its European relatives P. bernhardus. sternomaculata and Uroptychus sp., are widely
in P. chevreuxi and P. prideaux (Tudge, 1995a, b). placed the analysis and are more closely asso-
The 150 ciated with a of very speciose genus Pagurus (with over (spermatologically) variety
than The taxa) is a heterogeneous assemblage with, as yet, paguroids to any galatheoids (Fig. 1). ill-defined affinities in with a rapidly growing num- chirostylids investigated may represent part a ber of sister A link between these genera. paraphyletic assemblage two major superfamilies. Mar-
Paguridae has been suggested previously by Gore tin & Abele (1986) previously noted the differ-
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between the and The ences members of Chirostylidae perfectly known (Tudge, 1995a, b). super- other galatheoids. family Hippoidea usually is considered to be a
Family Galatheidae. Allogalathea elegans and distinct evolutionary line within the Anomura
Munida sp. form a small clade at the base of a with its closest links to the Galatbeoidea
Scholtz & and larger clade containing the pagurids, parapa- (Makarov, 1962; Richter, 1995),
and the evidence this gurids, chirostylids, diogenid genus independent neurological supports
Clibanarius (Figs. 1 & 2). The third genus inves- (Paul, 1989). Spermatologically, Hippa pacifica tigated in the Galatheidae, Munidopsis (consid- is distinct from the other anomurans here investi-
with certain of its ered a very heterogeneous genus by McLaughlin gated aspects perforatorial
with the former chamber 8 & (1983b)), never grouped two gen- (characters 9) being diagnostic (Fig. era and is shown as the sister group to them and 1)- Hippa shares the possession of a cytoplasmic
clade. The of the microtubular to the above-mentioned larger family origin sperm arms (character
Galatheidae did form with the remainder of the not a separate monophyletic 1) anomuran repre- clade (Figs. 1 & 2). sentatives (with the possible exception of Lomis)
Family Porcellanidae. The representatives in (Fig. I, point B), but it separated from the same
virtue this family form a monophyletic group in this representatives by of not developing the analysis (Figs. 1 & 2). The porcellanid clade pedunculate spermatophore (Fig. 1, point C). comprised two sister clades containing the two Other hjppoids are reported to have pedunculate representatives in the genus Petrolisthes in one, spermatophores (Subramoniam, 1984) and so the
Alia- addition of further this and the three remaining porcellanid genera, hippoid taxa may change porcellana, Pisidia and Polyonyx, in the other. current result.
This dichotomy, based on spermatological and There is a lack of comparable studies of ano-
spermatophore data (Tudge, 1995a, b; Tudge & muran phylogeny in the literature except for the
Jamieson, 1996a, b), is consistent with larval morphological analyses of McLaughlin (1983b)
(Sankolli, 1965; Gore, 1971; Van Dover et al., and Martin & Abele (1986), and at present there
and adult somatic molecular studies. The 1982) morphology (Haig, are no comparable papers
al. 1965). The Porcellanidae are depicted as a basal, of Spears & Abele (1988) and Cunningham et
sister the and the molecular data on the group to Paguroidea remaining (1992) provide relationship
galatheoids (Fig. 1, point D), and this dichotomy of only a few anomuran genera. In general, the
indicates the point on the tree where the number phylogenetic analysis presented here, using
of microtubular arms changes from the plesio- purely spermatological and spermatophoral evi-
number of four fixed of the results of morphic or more, being at dence, supports most McLaugh-
lin & three arms for the remaining terminal taxa. (1983b) and, less so, Martin Abele (1986).
Some agreement with previous morphological
Superfamily Hippoidea and molecular analyses emerges in many areas of
Family Hippidae. The single representative of the current tree (Figs. 1 and 2). Agreement is seen
this family and superfamily investigated, Hippa in the close relationship between the Coeno- pacifica is linked to the base of the anomuran bitidae and the of the members in the , majority
clade and paired with the thalassinid Thalassina Diogenidae (McLaughlin, 1983b; Martin &
squamifera (Figs. 1 & 2). This relationship pro- Abele, 1986; Spears & Abele, 1988; Cunningham
vides for the Richter & and simi- some support suggestion that, among et al., 1992; Scholtz, 1994) a the anomurans, the hippoids are the more closely lar relationship between the Paguridae and related group to the thalassinoids (Martin & Parapaguridae (McLaughlin, 1983b; Martin &
Abele, 1986). However, caution should be exer- Abele, 1986). Interestingly, a close link between
cised when interpreting the close relationship the Paguridae (in particular the genus Pagurus) between Thalassina and Hippa indicated in this and the Lithodidae (see Makarov, 1962;
analysis as the spermatozoal and spermatophore McLaughlin, 1983b; Cunningham et al., 1992)
morphologies of Thalassina squamifera are im- has been recently supported by new spermatozoa!
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and spermatophore evidence by the author attention from researchers using these spermato-
These (Tudge et ah, 1998), but this new data set has yet logical or other available techniques. prob-
be included in The lems include the of the Anomura as a to any phylogenetic analysis. validity
essentially basal position of Lomis hirta (Figs. 1 coherent taxon (considering the exhibited differ-
in of such the and 2), when compared to the other anomurans, ences placement groups as Hip- supports the results of McLaughlin (1983b). The poidea and Lomoidea), the heterogeneity of the distinct position of the Hippoidea (Makarov, Thalassinoidea, the monophyly of the Galatheo-
1962; McLaughlin, 1983b; Martin & Abele, idea (in particular the inclusion of the Porcellani-
1986) and the plesiomorphic position of the dae), the true affinities of the Chirostylidae, and
the Thalassinoidea (Martin & Abele, 1986) are also divergent placement of the genus Clibanarius supported by the current spermatological phylo- from their supposedly nearest diogenid relatives.
An consideration for future research geny. important
disa- is that However, certain aspects of my analysis specimens (particularly rare or pivotal
for the Anomura. be for different gree with previous phylogenies taxa) differentially preserved
of This study suggests a closer relationship between methods evaluation (spermatological, neuro- the Galatheoidea (in particular the Galatheidae logical, molecular) rather than treated to the and Chirostylidae) and the Paguroidea than that standard formalin and ethanol fixation for mor- suggested by McLaughlin (1983b) from morpho- phological studies. This latter practice (albeit the logical evidence. Conflict also occurs with the most common) effectively precludes the use of phylogeny of Martin & Abele (1986) in their specimens from the vast museum collections placement of Lomis between the Galatheoidea around the world for these alternative research and Paguroidea, with a much more basal position projects, which would otherwise have the capa- being suggested here by the spermatological evi- bility to provide useful and additional information dence (Figs. 1 and 2). Comparisons with the to resolve phylogenetic questions. broader decapod phylogeny of Scholtz & Rich-
harder ter (1995) are much to draw and the spermatological results presented here would ap- Conclusions
the pear to simply preclude a close relationship of
Thalassinoidea with the Anomura and Brachyura While recognizing that addition of further taxa
(their “Meiura”). may alter some of the groupings obtained, the
The current analysis deals with only 9 of the 13 present analysis, based solely on spermatozoal anomuran families, thus it seems obvious that and spermatophore evidence, indicates that the investigation of the spermatozoa and spermato- Anomura and two of its constituent superfamilies, phores of representatives from the missing fami- the Paguroidea and Galatheoidea, are not mono- lies (the Aeglidae, Albuneidae, Lithodidae, and phyletic assemblages. The infraorders Astacidea
Pylochelidae) is required to complete the survey. and Brachyura appear to be paraphyletic to most
there is Similarly, a need to sample more repre- of the Anomura. The Anomura (with the possible sentatives from of the and often of share the some rarer exception Lomis) unique synapo-
families of microtubular of poorly sampled and genera. Some exam- morphy having arms cytoplas-
The ples include more hippoids, chirostylids, and mic origin. superfamily Thalassinoidea is not parapagurids, and species from genera such as a monophyletic taxon (even when they are desig-
Cancellus, Porcellanopagurus, and Xylopagurus. nated as the outgroup). The only monophyletic
Spermatozoal or spermatophoral autapomorphies anomuran families are the Coenobitidae and Por- for taxa might be confirmed through repetitive cellanidae, while the Diogenidae, Paguridae,
of different within and Galatheidae to be sampling genera a family or Chirostylidae, appear para- multiple species within a genus. phyletic. The paguroid families Paguridae and
Some salient problems in anomuran phylogeny Parapaguridae together form a monophyletic that arise from this analysis will require further clade with the exception of Porcellanopagurus.
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The two representatives in the family Chirosty- leniusculus Dana, Int. J. Invert. Reprod. Devel., 5: 149-
lidae and 159. (Eumunida Uroptychus) do not group Dudenhausen, E.E. & P. Talbot, 1983. An ultrastructural with the other galatheoids investigated. The comparison of soft and hardened spermatophores from hippoid Hippa forms the sister group to the re- the crayfish Pacifastacus leniusculus Dana. Can. J. Zool.,
mainderof the taxa the anomuran (with exception 61: 182-194. of Lomis). Lomis occurs as a separate (basal) sis- Ehlers, U., 1985. Phylogenetic relationships within the
In: S.C. J.D. ter taxon to the remainder of the Anomura and Platyhelminthes. Morris, George, R. Gibson
& H.M. Platt (eds.). The origin and relationships of lower the Astacidea and Brachyura. invertebrates: 143-158 (Clarendon Press, Oxford),
1984. Revision du Forest, J., genre Aniculus (Decapoda
Diogenidae). Crustaceana, Suppl. 8: 1-91.
Acknowledgments Forest, J., 1995. Crustacea Decapoda Anomura: Revision du
1952 genre Trizopagurus Forest, (Diogenidae), avec
I’etablissement de deux In: A. Crosnier The author has benefited from frequent conversations with, and genres nouveaux.
(ed.), Resultats des Campagnes MUSORSTOM, 13. Mem. the sound advice of, Prof. Barrie Jamieson (Zoology Dept., The Mus. natn. Hist, nat., 163: 9-149. University of Queensland, Australia), Dr. Cliff Cunningham Glaessner, M.F., 1969. In: R.C. Moore (Zoology Dept., Duke University, USA) and Dr. Rafael Decapoda. (ed.), Treatise on invertebrate Arthropoda 4. Part Lemaitre (Dept, of Invertebrate Zoology, NMNH, USA). The paleontology, R, vol. 2: R399-R533 of America author also wishes to thank the helpful staff of the Zoology (Geological Society & University of Kansas Press, Department, The University of Queensland, Australia where Lawrence). Gore, R.H., 1971. The complete larval of this project had its beginnings and the Department of development Porcellana sigsbeiana (Crustacea: Decapoda) under labo- Invertebrate Zoology, National Museum of Natural History, ratory conditions. Mar. Biol., 11: 344-355. Smithsonian Institution, Washington D.C., USA, where it was
Gore, R.H. & L.E. Scotto, 1983. This the Studies on decapod completed. paper was improved by suggestions and Crustacea from the Indian River region ofFlorida XXVII. comments of an anonymous reviewer. During the writing of holthuisi this the Phimochirus (Provenzano, paper author was funded from a Smithsonian Institution 1961) (Anomura:
Postdoctoral Paguridae): The complete larval development under labo- Fellowship (1995-96) and an Australian Research ratory conditions, and the of its Council Postdoctoral Research Fellowship (1996). systematic relationships larvae. J. crust. Biol., 3: 93-116.
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Tudge, C.C., 1992. Comparative ultrastructure of hermit crab Appendix A, Spermatozoal characters
spermatozoa (Decapoda: Anomura: Paguroidea). J. crust.
Biol., 12: 397-409. 1. Origin ofmicrotubular arms. The bundles ofmicrotubules,
Tudge, 1995a. The ultrastructure and of the of the C.C., phylogeny representing bases microtubular arms, can be
anomuran crab 1-346 Zool- either nuclear in and from the spermatozoa: (Ph.D. Thesis, origin, or develop emerge
ogy Department, The University of Queensland, Brisbane, cytoplasm. The hairy stone crab Lomis hirta has micro-
Australia). tubules in both the nucleus and the cytoplasm but because
Tudge, C.C., 1995b. Ultrastructure and phylogeny of the spermiogenesis has not been studied their origin remains
spermatozoa of the infraorders Thalassinidea and Ano- The crabs do equivocal. brachyuran not possess micro-
mura In: B.G.M. (Decapoda, Crustacea), Jamieson, J. tubular arms and so the character has been scored as
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secondarily absent. (Nuclear origin =0, cytoplasmic origin Hippa pacifica, the perforatorial chamber divaricates into
or = 1, secondarily absent =2.) two or more perforatorial points fingers. (Perforatorial
microtubular number of microtubu- chamber absent = 0, anterior end of chamber 2. Numberof arms. The perforatorial
= mature of the entire = into two or more or lar arms in the spermatozoa thalassinoids, 1, separated points fingers
while porcellanids, and hippoids is four or more repre- 2.)
chamber Where is the sentatives from the Paguroidea and Galatheoidea(with the 9. Perforatorial contents. one present,
does not exception of the Porcellanidae) always have only three. perforatorial chamber in the majority of taxa
structures but has hetero- The exact number of microtubular arms is not known for contain any a homogeneous or
and Pisidia matrix. are the of Thalassina squamifera, Lomis hirta, longi- geneous granular Exceptions presence
tortuous tubules cornis. As above, this character has been scored as sec- perforatorial or a longitudinal septum
chamber ondarily absent in Portunus pelagicus. (More than 3 arms which ‘hangs’ inside the chamber. (Perforatorial
= = = without tubules = chamber contents 0, 3 arms 1, secondarily absent 2.) absent 0, perforatorial
vesicle that the or = 1, tubules = 2, 3. Proportion of the acrosome cytoplasm septum prominent prominent dividing
The vesicle be = envelops. acrosomal may totally embedded septum 3.)
vesicle in the cytoplasm (except for the opercular region), sig- 10. Acrosome vesicle dimensions. The acrosome
exhibited the various taxa are into four nificantly embedded, or the acrosomal vesicle may be shapes by arranged
with to superior to the cytoplasm with only its most posterior categories. (1) Subspheroidal acrosome length portion embedded. (All of the acrosomal vesicle width ratios less than 1.0. (2) Spherical to ovoid acrosome,
of = width ratios embedded [except operculum] 0, half or more than half encompassing the acrosome length to 1.0-
of the acrosomal vesicle embedded = !, posterior portion 1.5. (3) Ovoid to oblong-ovoid acrosome with length to
only embedded = 2.) width ratios of 1.6-2.5. (4) Oblong-ovoid to elongate
with width ratios of 2.6- 4. Presence and extent ofperforatorial chamber. A distinct cylindrical acrosome length to
chamber be in the 5.0, vesicle to width ratios < 1,0 = 0, perforatorial appears to absent (Acrosomal length
= Panulirus 1.0-1.5 = 1.6-2.5 = 2.6-5.0 spermatozoa of Trypaea australiensis, argus, 1, 2, 3.)
11. Acrosome vesicle The of Axius and Thenus orientalis but present in the remaining species contents. spermatozoa australiensis, Panulirus studied. In the species with a perforatorial chamber, this glyptocercus, Trypaea argus,
Thenus and Lomis exhibit structure can extend from the base ofthe acrosome vesicle orientalis, less so hirta no
concentric zonation of the acrosome vesicle contents, to a subterminal position below the operculum (post- the while the show distinct concentric equatorial) or terminate at or below the mid-point of remaining taxa
chamber zonation. zonation absent =0, = 1.) acrosome vesicle (pre-equatorial). (Perforatorial (Concentric present
= = 12. The electron-dense be absent = 0, post-equatorial 1, pre-equatorial 2.) Operculum form. operculum may hirta 5. Perforatorial chamber shape. For those species with a centrally perforate or entire. In Lomis there is more
than and the inter- perforatorial chamber, it can assume one of three forms: one perforation operculum appears
section with The condition of the is unknown in (1) a bulbous posterior a thin, tapering rupted. operculum
Thenus orientalis. = anterior projection, (2) a columnar or basically uniform (Operculum imperforate 0, perforate
= cylindrical perforatorial chamber, or (3) entirely bulbous 1.) crabs have anterior swollen into bulbous area. 13. Thickened The brachyuran a dense ring at or having the region a ring.
(Perforatorial chamber absent = 0, perforatorial chamber the posterior end ofthe acrosome vesicle surrounding the
= A dense bulbous posteriorly and tapering anteriorly 1, columnar perforatorial chamberbase (see Jamieson, 1991a).
= = of similar in 2, bulbous or bulbous anteriorly ring is present the same position or cylindrical entirely ( appearance Thalassina 3.) in the spermatozoa of squamifera. (Thickened
absent = 6. Presence andform of microvillarprojections. Microvillar ring 0, present =1.)
small structures that extend 14. Acrosome The is a modified projections are finger-like ray zone. acrosome ray zone
that the laterally from the perforatorial chamber wall into the zone within the acrosome vesicle has appearance,
posterior region of the perforatorial chamber in some ano- in transverse section, of dark and light radiating bands.
the of the muran representatives. When the microvillar projections This zone may occupy majority acrosome
taxa short and tuberculous or vesicle contents or be smaller in extent. Some are present, they are either longer may
= Cancellus and and filamentous. (Microvillar projections absent 0, short (Calcinus laevimanus, sp., Pagurus pri-
and tuberculous = 1, long and filamentous =2.) deaux] have a similar-looking zone but the homology is
= = 7. Ornamentation ofperforatorial chamber walls. The walls uncertain. (Acrosome ray zone absent 0, present 1.)
of chamber is or 15. zone.The zone the perforatorial (if one present) may may Subopercular subopercular (when present)
ornamented with that is not be longitudinal grooves or septa. is an homogeneous, coarsely granular region
= the (Perforatorial chamber absent 0, perforatorial chamber directly below or often fills the concavity of operculum
= = shallow extend for distance down the walls smooth 1, longitudinal corrugations 2, and may some acrosome
= vesicle. This be divided into prominent longitudinal septa 3.) zone may two or more
= = 8. Form of the anterior tip of the perforatorial chamber. In separate regions. (Subopercular zone absent 0, entire
of the anterior end divided into two or more = divided into three the majority species or apex of the 1, regions 2,
perforatorial chamber (if one is present) is entire but in or more regions =3.)
from the Calcinus and the 16. Dense The dense is representatives genus hippid. perforatorial ring. perforatorial ring
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an electron-dense zone that occurs around the posterior 25. Opercular ridge. The opercular ridge is a lateral extension
bulbous of the chamber in the the external ofthe in region perforatorial repre- on surface electron-dense operculum
sentatives ofthe Clibanarius the two of the genus only. (Dense perfora- investigated species genus Petrolisthes.
= = = torial ring absent 0, present 1.) (Opercular ridge absent 0, present = I.)
17. Fibrillar acrosome core. The fibrillar acrosome core is the 26. Tubular ring. The tubular ring is a structure fourfd in the
anterior modification of the inner acrosome zone in the acrosome vesicle ofPetrolisthes armatus and P. lamarckii.
spermatozoa ofDiogenes custos and D. pallescens into an It encircles the perforatorial chamber at the mid-point of
fibrillar which the and is elongate structure spirals apically. (Fibril- acrosome vesicle very electron-dense, but has
lar acrosome core absent =0, present = 1.) somewhat paler electron-lucent tubules lunning concen-
= 18. Reticulated acrosome zones. The reticulated acrosome zo- trically through it. (Tubular ring absent 0, present = 1.)
nes are oneor more concentric zones, towards the centre of
the which have reticulated acrosome vesicle, a appearance
in both transverse and longitudinal section. They are found Spermatophore characters
in most studied representatives of the families Paguridae
and Parapaguridae. (Reticulated acrosome zones absent = 27. Spermatophore form. The spermatophores in the taxa
0, present = I.) investigated can assume one of three forms. (1) A tubular
19. sheath. vesiculated sheath Lacunar The lacunar sheath or spermatophore extruded in the size and shape of the vas
has been observed in the of the deferens. A spermatozoa pagurid (2) pedunculate, tripartite spermatophore con-
and is vesiculated of attached base Porcellanopagurus sp. a thin, or faintly sisting an ampulla to a pedestal or by a
loculated cylinder that tightly surrounds the perforatorial stalk of variable length. (3) A spherical to ovoid capsular
chamber the ofthe vesicle. In Axius at midpoint acrosome (Lacunar spermatophore. glyptocercus, Thalassina squa-
sheath absent =0, present = 1.) mifera, Eumunida sternomaculata, and Polyonyx trans-
20. the Position of microtubular arms. Where they are present, the versus spermatophore morphology is unknown. (Sper-
= from the tubular = = microtubular arms emerge cytoplasm sur- matophores 0, pedunculate 1, capsular 2.)
rounding the acrosome vesicle at the posterior end of the 28. Spermatophore ridge. The spermatophore ridge is a raised
acrosome vesicle in nearly all taxa investigated, except for and thickened area of the spermatophore wall where the
where in anterior two of the Xylopagurus sp., they emerge an posi- halves ampulla split to release the contained
tion. = The (Microtubular arms posteriorly situated 0, spermatozoa. centre of the spermatophore ridge has a
anteriorly situated = 1, secondarily absent = 2.) break in the spermatophore wall structure. (Spermatophore
= 21. Inner The inner when absent 0, = acrosome zone. acrosome zone, ridge present 1.)
is the 29. Presence The of present, generally innermost zone of the concentric of accessory ampullae. spermatophores
series and is of the members the the homogeneous, finely granular and investigated of genus Pagurus (with
moderate electron The be into of P. density. zone may divided possible exception chevreuxi) and the parapagurid
two have smaller distinct regions. The imperfect fixation of Thalassina Sympagurus sp. a accessory ampulla present
does not allow decision to be made at the base ofthe main An squamifera a con- ampulla. accessory ampulla may
the form of inner also be the cerning presence or an acrosome zone. present in chirostylid Uroptychus sp. (Sperma-
absent = = = with = (Inner acrosome zone 0, entire 1, divided 2.) tophores accessory ampulla and main ampulla 0,
22. = Microtubular core. The microtubular core is the large main ampulla only I.)
bundle of longitudinally arranged microtubules that 30. Presence of tubular extension. The spermatophores of
the central axis ofthe in the and P. occupy elongate spermatozoa Petrolisthes lamarckii armatus have a long tubular
porcellanid species Aliaporcellana suluensis, Pisidia extension projecting from the distal end of the ampulla.
longicornis, and Polyonyx transversus. (Microtubular core (Spermatophore ampulla without tubular extension = 0,
absent = 0, present = 1.) with tubular extension = 1.) 23. Dense perforatorial cone. The dense perforatorial cone 31. Form of stalk in pedunculatespermatophores. In the taxa
thin the which the stalk occurs as an electron-dense, layer enveloping possess pedunculate spermatophores can
anterior region of the perforatorial chamber in the assume one ofthree forms. (1) An extremely short, almost
porcellanids and, questionably, the pagurid Porcellano- non-existent, pseudo-stalk. (2) A short, thick stalk. (3) A
It is from the thin stalk. = pagurus sp. usually separated perforatorial long, (Spermatophores tubular or capsular 0,
chamber thin of inner is with small = by a layer acrosome zone, spermatophores pedunculate pseudo-stalk 1,
the = perforate at perforatorial chamber apex, and may pedunculate with short, thick stalk 2, pedunculate with
extend to the base of the perforatorial chamber. (Dense long, thin stalk =3.)
absent = = perforatorial cone 0, present 1.) 32. Spermatophore wall ultrastructure. Where the ultra- 24. Posterior perforatorial ring. The posterior perforatorial structure of the spermatophore wall is known, three
is ring present only in the investigated members of the distinct forms occur. The spermatophore wall can be (1)
Porcellanidae where it occurs as a dense in hetero- family ring homogeneously granular appearance, (2) around the perforatorial chamber in the posterior regionof geneously granular, or (3) fibrillar. (Spermatophore wall
the vesicle. absent = ultrastructure acrosome (Posterior perforatorial ring homogeneously granular = 0, hetero-
= = 0, present 1.) geneously granular 1, fibrillar =2.)
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Appendix B. Data matrix (0/1 = 0/1 or an equivocal character state assignment)
111 1 111 1 1111 1 1 111 1 122222222223331 2 2 2 2 2 2 2 2 2 2 3 3 3
Character no. 123456789011 2 3 4 5 6 7 8 9 0 1 23456789012345678902 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 121 2
Taxon
Axius glyptocercus 00010 0 0 1 2032 0 3 1 1 303 0 100000000000000??????1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 7 7 7 7 7 7
Trypaea australiensisauslraliensis 00000000000000000000000000200 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 1 00?0 0 7
Thalassina squamiferasquamifera 00 ?7 2 11 2 0 11 1 1 111 1 000000 0 0 0 0 000 0 000?0 7 0000 0 0 0 00 7??????7 7 7 7 7
I1 IJ 1
Birgus latro 1122221 i 2 2 2 2 11 1 1 212 1 000 0 120000011 2 0 0 0 0 0 1 000000 0 0 0 0 1 1 11 0220 2 2
Coenobita brevimanushrevimanus 1122221 i 2 2 2 2 1 11 11 313 1 000 0 1120000012 0 0 0 0 0 I 0000000 0 0 0 11 1 1 0220 2 2
CoenobitaCoenobila perlatus 1112222i 2 2 2 2 1 11 11 3311 0000 120000011 2 0 0 0 0 0 1 000000 0 0 0 0 11 1 1 0220 2 2
Coenobita 1122221 2 2 2 2 1 11 1I 313 1 000 0 120000011 2 0 0 0 0 0 1 000000 0 0 0 0 11 1 1 0220 2 2 purpureuspurpureas i
112222i 2 2 1 1 1 313 1 000 120000011 2 0 0 0 0 0 1 000000 0 0 0 0 11 1 I1 0220 2 2 Coenobita rugosusrugosas 1 2 2 1 1 1 0
Coenobita variabilis 1112222i 2 2 2 2 1 1I 11 313 1 0000 1120000012 0 0 0 0 0 1 0000000 0 0 0 I1 1 1 0220 2 2
CalcinasCalcinus gaimardii 11211 i 2 1 3322 1 2 11 II1 1 000010000010 0 1 0 0 0 0 0 1 0000000 0 0 0 11 1 1 0320 3 2
CalcinusCalcinas laevimanus 11211 i 2 1 3 I1 1 2 1 111 1 000 0 0100 1 0 000 0 0010 0 1 000000 0 0 0 0 1 1 I1 0320 3 2
1
CalcinusCalcinas minutusminutas 11211 i 2 1 3 I1 1 222 2 II1 1 00010000010 0 0 1 0 0 0 0 0 1 000000 0 0 0 0 1 1 1 0320 3 2
Cancellus 11211 i 2 1 1011 0 1 I12212 2 1 1001000002000001 0 0 1 0 0 0 0 0 2 0 0 0 0 0 1 1 I1 0220 2 2 sp.
1 1
Clibanarius corallinus 11111 i 1 1 1 1 11 1 1 II1 1 000010 0 0 0 1 000010 0 0 0 1 000000 0 0 0 0 11 1 1 0310 3 1
Clibanarius erythropus 11111i 1 1 1 1 1 I1 1 11100011000010000011 0 0 0 1 1 0 0 0 0 1 0 0 0 0 0 1 1I 110310 3 1
Clibanarius longilarsuslongitarsus 11111i 1 1 1 2 1 1 1 111 1 0000010 0 0 1 000010 0 0 0 I 000000 0 0 0 0 1 1 1 0 1111
Clibanarius taeniatus 11111i 1 1 I1 1 1 1I 1I 1100001000010000011 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 1 11 10311 0 3 1
Clibanarius virescensvirescens 11111 i 1 1 1 1 1 1 1 111 1 000010 0 0 0 1 000010 0 0 0 1 000000 0 0 0 0 11 1 1 0310 3 1
110000011 1 0 0 0 0 0 1 1 DardanusBardanas arrosor 112221 i 2 2 2 I1 1 1 I1 2211 000 0 000000 0 0 0 0 11 1 1 0320 3 2
BardanasDardanus crassimanus 112221 i 2 2 2 1 1 1 1 111 1 000 0 1110000011 0 0 0 0 0 1 000000 0 0 0 0 11 1 1 0320 3 2
DardanusBardanas lagopodes 112221 i 2 2 2 I1 1 1 1 212 1 000 0 110000011 1 0 0 0 0 0 1 000000 0 0 0 0 11 1 1 0320 3 2
DardanusBardanas scutellatus 11211 i 2 1 222 2 1 1 1 212 1 000 0 110000011 1 0 0 0 0 0 1 000000 0 0 0 0 11 1 I1 0320 3 2
Dardanus 11211 i 2 1 222 2 I1 1 1 212 1 000 0 1110000011 0 0 0 0 0 1 000000 0 0 0 0 11 1 1 0320 3 2 Bardanas sp. nov.
BiogenesDiogenes custoscusios 11221 i 2 2 1 2 I1 1 1 313 1 000 0 1101 1 0 10002000001 0 0 0 2 0 0 0 0 0 1 11 1 00323 2
DiogenesBiogenes pallescens 11121i 2 1 1 2 1 1 11 313 1 000 0 1101 1 0 10002000001 0 0 0 2 0 0 0 0 0 I1 1 1 0320 3 2
StrigopagurusStrigopagarus boreonotus 1111321 i 1 1 3 2 1 11 11 110002000001000001 1 0 0 0 2 0 0 0 0 0 1 0 0 0 0 0 1 11 10321 0 3 2
PagurusPaguros bernhardus 11111 i 1 1 1 020 2 1I 11 111 1 00000010 0 0 0 0 0 1 00010 1 000000 0 0 0 0 I1 1 000 0 1100
Pagurus chevreuxichevrewd 11111 i 1 1 1 020 2 1 1 II1 1 00000010 0 0 0 0 0 1 0010 0 1 000000 0 0 0 0 1 1003?1 0 0 3 7
1 I\ 1 PagarasPagurus hirtimanushirliptanus 11111301i 1 1 3 0 1 I1 11313 1 0 00000010010000010 0 0 0 1 0 0 1 0 0 0 0 0 1 100101 0 0 1 0
Pagurus prideaux 11121i 2 1 I1 0022 1 1 1111 000000010 0 0 0 0 1 0010 0 1 0000000 0 0 0 1 1 0000 101 0
11
11111 i 1 1 1 030 1 1 212 1 00000000 0 0 0 0 0 0 100000001 0 0 0 0 0 0 0 1 1 1 0 101 0 Porcellanopagurus sp. 3
1
1101 0 1 1 Oil XylopagurusXylopaguras sp. nov. 1 i 0 1 1 0 1 1 1 111 1 00010010 0 0 1 0 0 1 0 1 1 000000 0 0 0 0 I1 1 1 02?0 2 7
11221 i 2 2 1 0 11 1 1I 311 000010010 0 0 0 1 000000000 0 0 0 0 0 0 0 1 1 000 0 10 Sympagurus sp. 3 1 1 0
I
Lomis hirta 0 7? 0 1 1 0 11 I1 1 1100 110000000010 0 0 0 0 0 0 0 I 000000 0 0 0 0 1 ?7 I1 0300 3 0
1
Eumunidasternomaculata 11211 i 2 1 202 0 1 1 2212 2 1 000 0 100000011 0 0 0 0 0 0 1 00000?0 0 0 0 0 7 ?7 ?7 ?7 ??7 7
Uroplychus sp. 11111 i 1 1 303 0 1 I1 1 1II1 000 0 1100000010 0 0 0 0 0 1 000000 0 0 0 0 1 1001 0 0 II1 i
I
AllogalatheaAllogalalhea elegans 11211 i 2 1 2032 0 3 I1 1 313 1 0002000002000000 0 0 2 0 0 0 0 0 2 0 0 0 0 0 1 1 1 0 1100
Munida 11211 i 2 1 3 030 3 1 1 313 1 0002000002000000 0 0 2 0 0 0 0 2 0 0 0 0 1 1 1 021 sp.sp, 0 0 1 1 0 2 1
11211 2 20 Munidopsis sp. i 1 2 0 1 1 3213 2 1 0002000002000000 0 0 2 0 0 0 0 0 2 0 0 0 0 0 1 11 I1 0 1 ]1
2
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Appendix B. Cont.
1 J 1111 111 1 1111 1 1 II1 1 122222222223331 2 2 2 2 2 2 2 2 2 2 3 3 3
Character no. 1123456789012 3 4 5 6 7 8 9 0 1 223456789013 4 5 6 7 8 9 0 1 2345678902 3 4 5 6 7 8 9 0 121 2
Taxon
Aliaporcellana suluensis 10211 0 2 1 2022 0 2 1 I1 111 1 10010000021 0 0 1 0 0 0 0 0 2 1111 1 1 000 0 1 1 1 0200 2 0
Petrolisthes armatus 10211 0 2 1 2032 0 3 1 11 212 1 10010000020111 0 0 1 0 0 0 0 0 2 0 1 1 1 1 1 1 1 1 202 0
Petrolisthes lamarckii 10211 0 2 I 2032 0 3 1 11 212 1 10010000020111 0 0 1 0 0 0 0 0 2 0 1 1 1 1 1 1I 1 1 202 0
7 Pisidia longicornis 17211 ? 2 1 2022 0 2 1 1 212 1 10030000021 0 0 3 0 0 0 0 0 2 1111 1 1 000 0 1 I1 1 0 1?1
Polyonyx transversustransversas 10211 0 2 1 2022 0 2 I1 1 2211 10010000021 0 0 1 0 0 0 0 0 2 1111 1 1 00?????00 0 7 7 7 7 7 0
Hippapacifica 110210 2 1 2200 1 2233 I111 0000100000200000000 0 1 0 0 0 0 0 2 0 0 0 0 0 0 0 i1 00000 0
FortunasPortunus pelagicuspelágicas 22012 2 0 1 2200 I1 1 2 111 1 010 1 110000211 1 0 0 0 0 2 1 00000200 0 0 0 0 2 0 1i 0000 0 0
Menaethius monoceros 21113012 1 1 1 3 0 1 1 1 1111 1101000021000002010001 1 0 1 0 0 0 0 2 1 0 0 0 0 0 2 0 i 0 0 0
Homarus americanusamericanas 0122200 1 2 2 2 0 1 1 1 313 1 10010000011 0 0 1 0 0 0 0 0 1 00000000 0 0 0 0 0 0 i1 00010 1
Panulirus 00000000000000000000000000000 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 i1 000?0 7 argus
Thenus orientalis 0000000000 0 0 0 0 0 0 0 0 10700000000000000201 0 7 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 i1 0000 0 0
Pacifastacus leniusculus 00210 0 2 1 3 0 1 1 1 010 1 10000000011 0 0 0 0 0 0 0 0 1 00000000 0 0 0 0 0 0 i1 0010 0 1
1
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