Biological Journal of the Linnean Society, 2017, 121, 200–222. With 16 figures.

One hundred years of carcinization – the evolution of the

crab-like habitus in Anomura (Arthropoda: Crustacea)
JONAS KEILER,* CHRISTIAN S. WIRKNER and STEFAN RICHTER
Universitat Rostock, Institut fur Biowissenschaften, Allgemeine & Spezielle Zoologie

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Received 10 July 2016; revised 3 November 2016; accepted for publication 1 December 2016

Within decapod crustaceans, Anomura is the phenotypically most disparate taxon, ranging from hermit crabs to
squat lobsters to crab-like representatives. Curiously, not only did the crab-like habitus evolve independently from
the ‘true’ crabs (Brachyura), it also evolved three times independently within anomurans. This process has been
called ‘carcinization’ by the English zoologist Lancelot Alexander Borradaile in 1916. In this paper we summarize
the results of our recent studies into the evolution of the crab-like morphotype (i.e. carcinization) and into possible
structural dependences (i.e. coherences) between the external morphology of a crab-like habitus and inner organs.
A micro-computer tomography and computer-aided 3D reconstruction-based comparison between the various crab-
like taxa shows that amazingly similar structural coherences exist across all these lineages between the external
characters of the crab-like habitus and internal characters. We were even able to trace complex coherence concat-
enations, or ‘coherence chains’, between various structures. These new findings greatly enhance our knowledge and
understanding of the evolutionary transformation into a ‘crab’, particularly in the context of causal and coherence
morphology. Although enormous morphological disparity is observed in the internal anatomy of the crab-like taxa,
reflecting the fact that the evolution of the crab-like habitus was indeed convergent, various corresponding depend-
ences are found across the different lineages between the external characters of a crab-like habitus/morphotype and
inner structures. In other words, as a result of carcinization certain structural coherences led to the specific internal
anatomical patterns found in crab-like forms. There is no reason to assume that ‘evolutionary tendencies’ or any such
vague concept played a role.

ADDITIONAL KEYWORDS: Brachyura – character transformation – circulatory system – coherence chains;

Decapoda – endophragmal system – evolutionary morphology – morphotype evolution – structural coherence –
ventral nerve cord

DISPARITY AND PHYLOGENY OF ANOMURA Reimann, Richter & Scholtz, 2011; Schnabel, Ahyong
& Maas, 2011; Tsang et al., 2011; Bracken-Grissom
Within decapod crustaceans, Anomura MacLeay,
et al., 2013; see also Lemaitre & McLaughlin, 2009),
1838 (or Anomala Boas, 1880; see McLaughlin &
the monophyly of Anomura has been convincingly
Holthuis, 1985) is the taxon with the highest mor-
shown (Scholtz & Richter, 1995; Ahyong & O’Meally,
phological disparity (Tsang et al., 2011). It com-
2004; Schram & Dixon, 2004; Porter, Pérez-Losada &
prises forms (morphotypes sensu Haug et al., 2016)
Crandall, 2005; Tsang et al., 2008; Chu et al., 2009;
as distinctly varied as symmetrical and asymmetri-
Toon et al., 2009; Shen, Braband & Scholtz, 2013).
cal hermit crabs, squat lobsters and representa-
Controversy still surrounds the relationships within
tives with a crab-like habitus. It is likely that none
Decapoda Reptantia Boas, 1880, but most studies
of these groups constitutes a monophyletic unit but
assume Anomura and Brachyura Linnaeus, 1758
rather that they form para- or polyphyletic assem-
to be sister taxa, together forming Meiura Scholtz
blages (Fig. 1). Although the phylogenetic relation-
& Richter, 1995 (Dixon, Ahyong & Schram, 2003;
ships between the higher anomuran taxa are still
Ahyong & O’Meally, 2004; Schram & Dixon, 2004;
largely unresolved (Ahyong, Schnabel & Maas, 2009;
Tsang et al., 2008; Chu et al., 2009; Kim et al., 2012;
Shen et al., 2013; but see also, e.g., Porter et al., 2005;
*Corresponding author. E-mail: [email protected] Toon et al., 2009).

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, 121, 200–222 200
 HUNDRED YEARS OF CARCINIZATION 201

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Figure 1. Different hypotheses of anomuran phylogeny based on molecular + morphological (A) and molecular (B + C) data.
[(A) Schnabel, Ahyong & Maas, 2011, (B) Tsang et al., 2011 and (C) Bracken-Grissom et al., 2013]. Coloured circles represent
the general habitus in the ground pattern of the respective taxon. Underlined taxa contain crab-like forms (additionally
represented by green stars). All phylogenies shown imply the evolution of a crab-like habitus which appeared three times
independently within Anomura.

Tsang et al. (2011) suggested that all representatives a crab-like habitus did not evolve solely in ‘true’ crabs but
of Anomura can be traced back to the symmetrical her- also several times independently in the Anomura makes
mit crab morphotype and stem from an ancestor resem- this process ideal for evolutionary research. The emer-
bling extant Pylochelidae Bate, 1888. Bracken-Grissom gence of a crab-like habitus is probably the most-noticed
et al. (2013), on the other hand, proposed that the ground evolutionary process within reptant decapods. Following
pattern of Meiura comprises a crab-like morphotype. the English zoologist Lancelot Alexander Borradaile
The oldest fossil which can be assigned to Anomura, (1916), we term this process carcinization.
Platykotta akaina, however, shows a squat lobster mor-
photype and dates from the upper Triassic (Chablais,
Feldmann & Schweitzer, 2011) ‘shortly’ after the time
CARCINIZATION
of the split leading to Anomura and Brachyura approxi-
mately 260 Mya (Bracken-Grissom et al., 2013). Due to Borradaile (1916: 121) used the term carcinization not
its degree of similarity to stem lineage representatives of only to describe the evolution of the crab-like habitus in
the closely related Brachyura, it is likely that this habi- Brachyura but also to refer to the repeated formation
tus actually represents the ground pattern of Anomura of a ‘general habit of body of a crab’ in the evolutionary
(Haug & Haug, 2014), an interpretation which also hap- lineages of Anomura which resemble ‘true’ crabs.
pens to be more congruent with recently suggested phy- Studies into the evolutionary processes which led to
logenies (Schnabel et al., 2011; Bracken-Grissom et al., a crab-like habitus can be traced as far back as the sec-
2013). ond half of the 19th century. Decapod crustaceans with
A crab-like habitus must have evolved at least three a crab-like habitus (Table 1) were initially recognized
times within Anomura, each time independently from as ‘crabs’ and taxonomically categorized accordingly
the other instances and independently from the evolution (Lamarck, 1818; Milne Edwards, 1837). A more inten-
of the ‘true’ crabs (Brachyura) (Borradaile, 1916; Wolff, sive examination of the origin of the crab-like habitus
1959; Morrison et al., 2002; see also Fig. 1). The crab-like and related evolutionary processes began with the stud-
taxa in Anomura are the porcelain crabs (Porcellanidae ies by Boas (1880a, b) and Bouvier (1895). Since then,
Haworth, 1825), the king crabs (Hapalogastridae Brandt, the phenomenon of carcinization has repeatedly formed
1850 + Lithodidae Samouelle, 1819) and Lomis hirta the focus of morphological and phylogenetic studies
(Lamarck, 1818) (Lomisidae Bouvier, 1895). The fact that (Wolff, 1959; McLaughlin, Lemaitre & Tudge, 2004;

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202 J. KEILER ET AL.

Table 1. Overview of the taxa with crab-like representatives

Taxon Porcellanidae Hapalogastridae Lithodidae Lomis hirta Brachyura

Number of 277 8 121 1 6599

described (Osawa & McLaughlin, (McLaughlin, (McLaughlin (De Grave et al.,
species* 2010) Lemaitre & et al., 2010) 2009)
Crandall, 2010)
Geographical Worldwide North Pacific Worldwide Bass Strait Worldwide
distribution (Rodríguez, Hernández (Hall & Thatje, (Hall & Thatje, (southern
& Felder, 2005) 2009) 2009) Australia)
(Poore, 2004)

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Natural habi- Marine Marine Marine Marine Marine, freshwater,
tat (milieu) (Rodríguez et al., 2005) (Hall & Thatje, (Hall &Thatje, (Poore, 2004) semiterrestrial,
2009) 2009) terrestrial
(Ng, Guinot &
Davie, 2008)
Vertical Intertidal and subtidal Intertidal to 200 m Intertidal to deep Intertidal Intertidal to deep
distribution (Rodríguez et al., 2005), (Hall & Thatje, sea (Poore, 2004) sea
occasionally deep sea 2009) (Hall & Thatje, (Ng et al., 2008)
(Osawa, 2014a, b) 2009)
Fossil record† 163–145 Mya Missing 12–5 Mya Missing 200–170 Mya
(Schweitzer & (Feldmann, (Schweitzer &
Feldmann, 2010a) 1998) Feldmann, 2010b)

Note: *Anomura comprise about 2500 described species (De Grave et al., 2009). †The oldest fossil assigned to Decapoda was found in the late Devonian
(360 Mya) (Schram & Dixon, 2004); the oldest fossil assigned to Anomura was found in the upper Triassic (230–200 Mya) (Chablais et al., 2011).

Bracken-Grissom et al., 2013; Haug & Haug, 2014), and Wägele, 1989, 1992; Feldmann & Schweitzer, 2010).
the adaptive value linked to the origination of a crab-like Although the ability to walk sideways is not restricted
habitus has been debated at length (Glaessner, 1960; to crab-like forms (Chasserat & Clarac, 1983; Faulkes &
Števčić, 1971; Guinot, 1979; Förster, 1985; Wägele, 1989, Paul, 1997), ‘crabs’ seem to be better adapted for it than
1992; Cunningham, Blackstone & Buss, 1992; Richter & macruran forms (Vidal-Gadea et al., 2008). Ultimately,
Scholtz, 1994; McLaughlin & Lemaitre, 1997; Morrison a crab-like habitus is not any more intrinsically advan-
et al., 2002; Vidal-Gadea, Rinehart & Belanger, 2008; tageous than the habitus of other morphotypes since
Hiller, Viviani & Werding, 2010; Feldmann & Schweitzer, the ecological and functional circumstances are crucial
2010; Tsang et al., 2011; Scholtz, 2014). (Scholtz, 2014).
We consider carcinization as the evolutionary pro-
cesses leading to a crab-like habitus without arguing
what the exact adaptive value of this habitus is. One Evolutionary scenarios explaining
important aspect seems to have been the need to pro- carcinization in anomura
tect the pleon against predators by folding it under the The crab-like habitus within Anomura evolved in three
ventral side of the body (Števčić, 1971; Wägele, 1989, independent lineages. The scenarios forming the basis
1992). The folding of the pleon might also constitute of these independent events are presented in the fol-
a prerequisite for higher mobility. Some authors pro- lowing. For better readability, genus names represent
pose that the crab-like habitus confers a general selec- the species previously mentioned.
tive benefit over the macruran habitus by enhancing
mobility in benthic habitats (Glaessner, 1960; Števčić,
1971; Förster, 1985; Hiller et al., 2010) and increasing The evolution of porcelain crabs (Porcellanidae)
success during predation or escape. While the large The close relationship between porcelain crabs
pleon in macruran forms might have prevented rapid (Porcellanidae) and squat lobsters sensu stricto
locomotion (Förster, 1985; for walking speeds in vari- (Munidopsidae, Munididae and Galatheidae) has been
ous Reptantia see Burrows & Hoyle, 1973; Chasserat & recognized since the beginning of the 19th century (Leach,
Clarac, 1983), a flattened crab-like form made it possi- 1820). Borradaile (1907) was the first to note that porce-
ble not only to move more rapidly, but to hide in crevices lain crabs evolved from squat lobster-like ancestors – a
and under stones to avoid predators (Glaessner, 1960; hypothesis supported by subsequent studies (Glaessner,

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, 121, 200–222
 HUNDRED YEARS OF CARCINIZATION 203

subsequent analyses failed to include Hapalogastridae,

a taxon which in several respects probably represents
the morphologically plesiomorphic condition within king
crabs (Richter & Scholtz, 1994). The strongest evidence
for this hypothesis is the soft and sparsely calcified pleon
in Hapalogastridae which, despite the missing uropods,
resembles the pleon in Paguridae (Brandt, 1850). This
notwithstanding, several analyses have shown that
Lithodidae and Paguridae are closely related to each
Figure 2. Phylogenies of Galatheoidea based on molecu- other (Morrison et al., 2002), and Lithodidae have even
lar + morphological (A) and morphological data (B). A. been seen to cluster within paraphyletic Paguridae

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Schnabel et al., 2011. B. Reimann et al., 2011. (Cunningham et al., 1992; Richter & Scholtz, 1994;
Tsang et al., 2008, 2011; Chu et al., 2009). Subsequent
1960; Martin & Abele, 1986; McLaughlin & Lemaitre, studies which did take Hapalogastridae into account
1997; Tudge, 1997; Schram, 2001; Morrison et al., 2002; have confirmed that Paguridae are paraphyletic and
Dixon et al., 2003; McLaughlin, Lemaitre & Sorhannus, enclose a monophylum comprising Hapalogastridae and
2007; Chu et al., 2009). Recent cladistic analyses suggest Lithodidae (Fig. 3; Ahyong et al., 2009; Schnabel et al.,
that porcelain crabs cluster within squat lobsters (Fig. 2011; Bracken-Grissom et al., 2013).
2; Schnabel et al., 2011; Bracken-Grissom et al., 2013),
and probably even within paraphyletic Galatheidae
(Reimann et al., 2011), meaning that they are likely to The evolution of Lomis hirta (Lomisidae)
be derived from an ancestor similar to extant squat lob- Lomis hirta, the only representative of the Lomisoidea
sters sensu stricto. Bouvier, 1895, is endemic to the intertidal on both sides
With a pleon incompletely bent under the cepha- of the southern Australian Bass Strait and lives on stony
lothorax, squat lobsters can be interpreted either as coasts (Poore, 2004). The phylogenetic position of Lomis
morphologically intermediate forms between macruran has been a matter of debate since the species was first
and crab-like forms, or as being half-carcinized (Keiler, alleged by Lamarck (1818) to be a representative of por-
Richter & Wirkner, 2015a; but see Scholtz, 2014). celain crabs. Subsequently, discussed as a close relative
of hermit crabs (Bouvier, 1895; Boas, 1926; Balss, 1957;
Pilgrim, 1965; Richter & Scholtz, 1994), or of king crabs
The evolution of king crabs (Hapalogastridae and (Milne Edwards, 1837; Stimpson, 1858; Martin & Abele,
Lithodidae) 1986; see also McLaughlin, 1983), more recent studies
The evolutionary transformation from hermit crabs into suggest that Lomis is actually more closely related to
king crabs is probably the most familiar and impressive the freshwater Aegloidea Dana, 1852 – they are either
example of carcinization. King crabs are representa- sister groups (Morrison et al., 2002; Tudge & Scheltinga,
tives of the monophylum comprising Hapalogastridae 2002; Schnabel et al., 2011; Tsang et al., 2011; Keiler &
and Lithodidae (Hall & Thatje, 2009; Keiler, Richter & Richter, 2011) or members of a taxon which also includes
Wirkner, 2015b). Superficially regarded, king crabs and deep sea Chirostyloidea Ortmann, 1892 (Bracken-
hermit crabs possess few morphological correspond- Grissom et al., 2013; but see also Reimann et al., 2011).
ences, but it was suggested as early as the 19th century
(Brandt, 1850) that they may be closely related. The
Danish zoologist Johan Erik Vesti Boas (1880a, b) then
suggested that king crabs are not only closely related
to hermit crabs but even derived from a Pagurus-like
ancestor. Morphological characters such as the left-sided,
unpaired pleopods and the asymmetrically arranged ter-
gite plates in female king crabs were interpreted as rem-
nants from a hermit crab-like ancestor (Boas, 1880a, b,
1924; Bouvier, 1895). More recent morphological studies
also support a close relationship between Paguridae and Figure 3. Phylogenetic relationship between Paguridae
king crabs (Richter & Scholtz, 1994; Keiler & Richter, and king crabs. Paraphyletic Paguridae implies that king
2011; Reimann et al., 2011; Keiler, Richter & Wirkner, crabs (Hapalogastridae + Lithodidae) are derived from a
2013, 2015b; Jaszkowiak et al., 2015). The first molecu- pagurid-like ancestor. Phylogeny supported by cladistic
lar analyses aimed at shedding light on the relationship analyses based on molecular (Ahyong et al., 2009; Schnabel
between hermit crabs and king crabs were performed by et al., 2011; Bracken-Grissom et al., 2013) and morphologi-
Cunningham et al. (1992). However, both these and most cal data (Reimann et al., 2011).

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204 J. KEILER ET AL.

We have suggested the taxon name Australopoda for the specific morphological transformations are discussed
monophylum Lomisoidea + Aegloidea + Chirostyloidea within the framework of what we have called ‘coher-
(Keiler, Wirkner & Richter, 2016). All representatives of ence morphology’ (Richter, 2007; Richter & Wirkner,
Aegloidea and Chirostyloidea possess a squat lobster- 2014). A comparison of the crab-like forms which
like habitus, although in some cases it is more distinct evolved convergently enables us to reveal correspond-
than in others. Lomis can therefore be regarded to be ences and differences in the structural dependences
derived from an ancestor that had a squat lobster-like between external features of the crab-like habitus and
habitus (Fig. 1). internal anatomical features in the four independent
lineages that led to the crab-like morphotype.
The majority of morphological studies into decapods
Carcinization in the context of coherence and are concerned with external morphological features.

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causal morphology Studies into the anatomy of inner organs and struc-
Previous studies into carcinization have concentrated tures, especially the ventral nerve cord and the haemo-
almost exclusively on external morphological characters lymph vascular system, are few in number and often
(e.g. bent pleon, broad carapace, etc.) in their exploration based on just a few or even one single species of mostly
of convergent transformations in anomurans and brachy- species-rich taxa. The spatial relationships between
urans (Glaessner, 1960; McLaughlin & Lemaitre, 1997; organs and other inner structures within the body are,
Scholtz, 2014). Decapod anatomical studies, however, with a few exceptions (Pearson, 1908; Jackson, 1913;
have revealed internal differences between crab-like Pike, 1947; Young, 1959), largely undescribed.
forms and their macruran relatives, for example in the In the light of this, we recently carried out a comprehen-
pattern and arrangement of the ganglia (Bouvier, 1888a, sive survey using micro-computer tomography of repre-
1889; Scholtz & Richter, 1995) and in the course of the sentatives of the three crab-like anomuran taxa and their
artery systems (Bouvier, 1891; Pearson, 1908; McGaw & closest non-crab-like relatives (Keiler et al., 2013, 2015a,
Reiber, 2002; McGaw & Duff, 2008). b, 2016). Our aim was to discover which internal features
This present study focuses on the questions of how evolved convergently as part of the crab-like morphotype.
the evolution of a crab-like habitus (i.e. carcinization)
influenced internal anatomical structures and spa-
General characteristics of the crab-like
tial relationships [especially with regard to the ven-
habitus/morphotype
tral nerve cord and the arterial system (haemolymph
vascular system)], and in what way, if at all, internal The term carcinization sensu Borradaile (1916) is com-
morphology is structurally dependent on external monly used to describe the evolutionary processes
morphology (Fig. 4). In addition, the possible causes of which led to a crab-like habitus. Borradaile’s (1916:
121) definition of carcinization reads as follows: ‘[…]
carcinization […] consists essentially in a reduction of
the abdomen of a macrurous crustacean, together with
a depression and broadening of its cephalothorax, so
that the animal assumes the general habit of body of
a crab.’ Although this describes the evolutionary–mor-
phological transformations which led to a crab-like
habitus, the crab-like habitus itself is not defined pre-
cisely enough.
While carcinization is the evolutionary process
which resulted in a crab-like habitus, the actual
objects of transformation are individual characters (in
the sense of Hennig’s concept of ‘character as transfor-
mation series’; Hennig, 1966). Starting with their last
common ancestor, all the taxa studied herein under-
went morphological changes on the same evolutionary
timescale. This means that while individual charac-
ter states can be ancestral (plesiomorphic) or derived
(apomorphic), whole organisms cannot (see Hennig,
Figure 4. Schematic representation of initial hypothesis. 1966; Scholtz, 2010; Keiler et al., 2015b).
Changes in external characters that led to a crab-like habi- To answer the question of whether structural coher-
tus also resulted in transformations of internal anatomical ence exists between a crab-like habitus and internal
characters. Thus, carcinization has an indirect impact on morphology, the external features which characterize a
internal anatomy. crab-like habitus must first be defined precisely. Unlike

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, 121, 200–222
 HUNDRED YEARS OF CARCINIZATION 205

the evolutionary process (carcinization) which led to this ‘half-carcinized’ forms. These forms do not possess a
combination of character states, a crab-like habitus or crab-like habitus sensu stricto, but exhibit certain mor-
morphotype is a typological concept. Without going into phological similarities with the crab-like morphotype
detail on which species are recognized as ‘crabs’ by the (‘degrees of carcinization’ in Feldmann & Schweitzer,
human brain (see Reindl et al., 2015), brachyurans such 2010; but see Scholtz, 2014). Some species might even
as Cancer pagurus Linnaeus, 1758 and Carcinus mae- show ‘hypercarcinization’ (see Hiller et al., 2010).
nas (Linnaeus, 1758) would seem to be the quintessential Borradaile (1916) was stretching the concept of a
‘crabs’ (see also Scholtz, 2014). For the purposes of this ‘crab’ when he suggested half-carcinized hermit crabs
paper, we define the crab-like habitus/morphotype as the such as Porcellanopagurus Filhol, 1885, Ostraconotus A.
morphological overlap between these brachyuran repre- Milne-Edwards, 1880 and Tylaspis Henderson, 1885 to
sentatives and porcelain crabs, king crabs and Lomis: be crab-like representatives. Other species exist within

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Meiura which some authors have described as crab-
• The carapace is flatter than it is broad and pos-
like but which do not match the criteria for a crab-like
sesses lateral margins (Fig. 5A).
habitus proposed herein. The robber crab Birgus latro
• The sternites are fused into a wide sternal plastron
(Linnaeus, 1767), for example, resembles a crab and
which possesses a distinct emargination on its pos-
possesses a strongly bent pleon as an adult, but the
terior margin (Figs 5C and 8B).
sternites of the fourth pereiopods are not completely
• The pleon is flattened and strongly bent, in dorsal
fused with the preceding sternal plate. Furthermore,
view completely hiding the tergites of the fourth
the anterior part of the carapace, the so-called shield,
pleonal segment (Fig. 6B, D, E, H), and partially or
does not possess lateral margins. Some authors regard
completely covers the plastron (Figs 5B and 7A).
representatives of Hippoidea Latreille, 1825 to be forms
The above criteria in combination provide a defini- with a crab-like habitus (Borradaile, 1916; Morrison
tion which allows us to differentiate the crab-like et al., 2002; Tsang et al., 2011; Bracken-Grissom et al.,
habitus/morphotype from other habitus/morphotypes, 2013), but Hippoidea do not possess a plastron and have
something which is essential for the following discus- slender, separated sternites. Moreover, either the pleon
sion on carcinization. The crab-like habitus, which is is only moderately bent (in Blepharipodidae Boyko, 2002
a combination of all the above criteria, is understood and Albuneidae Stimpson, 1858) or the carapace does
herein as the result of ‘complete’ carcinization – not possess lateral margins (Hippidae Latreille, 1825).
something which took place only in the four meiuran Even within Brachyura, especially within the rep-
lineages mentioned. Other forms which possess some resentatives of ‘Podotremata’ suggested to reflect the
but not all of the features listed above might be called ancestral condition (Scholtz & McLay, 2009), forms exist
half (or partly) carcinized (but see Scholtz, 2014). which do not match all criteria for a crab-like habitus
The term ‘carcinization’ has often been used, and (Scholtz, 2014). In Raninidae De Haan, 1839 (Brachyura:
indeed was even used originally (Borradaile, 1916), Raninoidea De Haan, 1839), the posterior part of the
to include evolutionary alterations which resulted in plastron is reduced, resulting in the absence of a posterior

Figure 5. Character states/conditions of a crab-like habitus. (A) Flattened carapace with lateral margins (arrow). Hyas
araneus (Brachyura: Majidae), oblique anterior view. (B) Wide sternal plastron (double arrow) and pleon strongly bent below
the plastron (arrow). H. araneus in ventral view. Fourth pleonal segment indicated by asterisk. (C) Posterior emargination
(arrow) of the plastron. Bathypluma forficula Saint Laurent, 1989 (Brachyura: Retroplumidae Gill, 1894), based on Guinot
& Quenette, 2005.

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, 121, 200–222
206 J. KEILER ET AL.

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Figure 6. Habitus and proportions. Schematic drawings of representatives of studied taxa in dorsal view. Proportions
relative to carapace width (= 1.0; green): overall habitus (blue), carapace length (red; exclusive of rostrum). (A) Galatheidae
(Galathea). (B) Porcellanidae (Petrolisthes). (C) Paguridae (Pagurus). (D) Hapalogastridae (Hapalogaster). (E) Lithodidae
(Paralomis). (F) Aeglidae (Aegla). (G) Kiwaidae (Kiwa). (H) Lomisidae (Lomis). Abbreviations: pl2, second pleonal segment.

emargination. Furthermore, the pleon is less strongly Crab-like morphotype

bent than in crab-like forms and the carapace is elon- (Porcellanidae, Lomisidae, Hapalogastridae and
gated. This secondary loss of the features of a crab-like Lithodidae): The carapace (excluding the rostrum) of
habitus has been termed decarcinization (Scholtz, 2014). all the crab-like anomurans studied herein (Fig. 6B, D,
E, H) is slightly broader than it is long and broader
than it is high. The overall habitus (carapace includ-
ing rostrum and bent pleon) is slightly longer than
EXTERNAL MORPHOLOGY
it is broad. The width-length ratio of the cephalo-
The external morphology of the different morphotypes thorax plus pleon varies between taxa. In the spe-
in Anomura is characterized by the following features: cies of Hapalogaster (Hapalogastridae) and Lomis

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, 121, 200–222
 HUNDRED YEARS OF CARCINIZATION 207

proportions, being dorsoventrally flattened in the sequel

in crab-like forms (Fig. 13). Broad chelipeds and a reduc-
tion of the rostrum also contribute to a compact crab-like
habitus, but were not investigated in this study.

Squat lobster morphotype

(Galatheidae, Munididae, Munidopsidae, Aeglidae and
Kiwaidae): The carapace (excluding the rostrum) is
slightly longer than it is broad and broader than it is
high. The overall habitus (carapace including rostrum

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and bent pleon) is significantly longer than it is broad,
resembling an elongated oval (Fig. 6A, F, G). The pleon is
bent, hiding the fifth and sixth pleonal segments in dor-
sal view (Fig. 6A, F, G). In Kiwaidae, the pleon is strongly
bent, also hiding the third and fourth pleonal segments
(Fig. 6G). In Galatheidae, Munididae and Munidopsidae
the pleon covers most of the sternal plastron (Fig. 7B); in
Aeglidae and Kiwaidae the plastron remains uncovered
(Fig. 8A). The plastron is formed by the fused sternites
of thoracic segments 3–7. The sternites of the eighth tho-
racic segment are separated from the plastron by a thin
section of cuticle. In Aeglidae, Galatheidae, Munididae
and Munidopsidae, the posterior margin of the plastron
is almost straight; in Kiwaidae, a triangular posterior
emargination is present (Fig. 8A).

Asymmetrical hermit crab morphotype

Figure 7. Bent pleon (green) hiding sternal plastron (blue) (Paguridae): The carapace is significantly longer
in (A) crab-like forms (Lomis hirta, king crab Hapalogaster
than it is broad (Fig. 6C), while width and height are
mertensii, porcelain crab Pachycheles rudis) and (B) gala-
roughly equal. The thoracic sternites, which are partly
theoid squat lobsters (Munida sarsi). Volume rendering.
movable, are relatively slender and separated between
Sixth pleonal segment (or the tergites thereof) indicated by
the fifth, sixth, seventh and eighth thoracic segments
asterisk. Abbreviations: p1-p4, pereiopods; pl4-pl5, pleonal
tergite plates (left); t, telson.
by sutures or thin sections of cuticle (Fig. 8A).

(Lomisidae), the overall habitus is elongated by the

large tergite plates of the second pleonal segment,
SELECTED INTERNAL ANATOMICAL
while in the species of Petrolisthes (Porcellanidae) and
FEATURES
Paralomis (Lithodidae), the tergite plate is smaller and
the pleon more strongly bent. In all species with a crab- The general internal composition of the anomurans
like habitus, the pleon is strongly bent, partially or studied herein largely resembles that in other stud-
completely hiding the third pleonal segment (Fig. 6B, ied decapods, although the anatomical systems differ
D, E, H). The sternal plastron is fully or partially cov- between the taxa in position, extension and shape [see
ered by the bent pleon and is formed by the fused following references (descriptions of internal anatomi-
sternites of thoracic segments 3–7 (Porcellanidae) or cal structures in anomurans are marked with an *):
4–7 (Lomisidae, Hapalogastridae and Lithodidae). The Audouin & Milne Edwards, 1827, 1829; Grobben, 1878;
sternites of the eighth thoracic segment are separated Claus, 1884*; Bouvier, 1888a*, b, c, d, e*, 1889*, 1890*,
from the plastron by a thin section of cuticle. On its 1891*; Marchal, 1892; Coutière, 1899; Thompson, 1903*;
posterior margin, the plastron possesses a distinct tri- Doflein, 1904; Pearson, 1908; Herrick, 1911; Fasten,
angular or semicircular emargination (Fig. 8B). 1917*; Baumann, 1921; Brody & Perkins, 1930; Young,
Basically, the overall habitus of crab-like anomurans is 1959; Chacko, 1967; Sandeman, 1967; Vuillemin, 1968;
more squat (length to width <1.5) than in the non-crab- Pilgrim, 1973*; Belman, 1975; Burnett, 1984; Sillar
like anomurans studied herein (length to width >1.7). & Heitler, 1985*; Keim, 1915; Schmidt, 1915; Huxley,
The strongly bent pleon is the main contributor to these 1920; Pillai, 1965; Paterson, 1968; McLaughlin, 1980*;

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208 J. KEILER ET AL.

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Figure 8. Sternal plastron (blue) in (A) Pagurus hirsutiusculus, Aegla cholchol, Kiwa puravida and galatheoid squat lob-
sters (Munida sarsi) and (B) crab-like forms (porcelain crab Porcellana platycheles, king crab Hapalogaster mertensii and
Lomis hirta). Volume rendering. Pleon coloured green, eighth thoracic sternites purple. Arrows in (A) and (B) indicate pos-
terior emargination of plastron. Sixth pleonal segment (or the tergites thereof) indicated by asterisk. Abbreviations: p1-p5,
pereiopods; st3-st8, thoracic sternites; t, telson.

Rodrigues, 1984; Secretan, 1998*; McGaw & Reiber, In the following, we compile findings from our previ-
2002; Secretan-Rey, 2002; Kronenberger et al., 2004*; ous studies (Keiler et al., 2013, 2015a, b, 2016) which
McGaw, 2005; Hobbs, Harvey & Hobbs, 2007; McGaw contribute to the discussion on carcinization and
& Duff, 2008*; McGaw & Stillman, 2010]. coherence morphology.

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Figure 9. Ventral vessel system, sella turcica and median phragma. (A) Hyas araneus. (B) Carcinus maenas. (C, D) Kiwa
puravida. (E, F) Petrolisthes eriomerus. Ascending arteries are indicated by asterisks. Abbreviations: da, descending artery;
es, endosternites; mph, median phragma; p1-p5, pereiopods; p1a-p5a, leg arteries; pvv, posterior ventral vessel; st, sella
turcica; vv, ventral vessel.

Endophragmal system The median distance between the endosternites var-

The endophragmal system (= endoskeleton) is basi- ies between the taxa (Fig. 12). In Paguridae, endos-
cally formed by integumental invaginations of the ternites 4/5, 5/6 and 6/7 are close together medially
thoracic sternites and pleurites of two consecutive forming relatively narrow channel-like passages
body segments. These invaginations, properly termed (Keiler et al., 2013). In all other forms (Galatheidae,
‘endosternites’ and ‘endopleurites’, extend into the Munididae, Munidopsidae, Porcellanidae, Aeglidae,
body (Fig. 9E). Kiwaidae, Lomisidae, Hapalogastridae and Lithodidae)

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210 J. KEILER ET AL.

the median distance between the endosternites is sig- of the hemineuromeres of thoracic segments th4–
nificantly larger (Fig. 9E). th8 (tn4–tn8) are distinctly separated medially. The
In Porcellanidae, Lomisidae and Kiwaidae the paired neuropils of the first pleonal neuromere (pn1)
median distance between endosternites 7/8 is smaller are close together medially and may be confluent with
than between endosternites 4/5, 5/6 and 6/7 (Fig. 9C, each other.
E). Furthermore, the plastron in these three taxa pos- The cephalothoracic ganglions of the studied species
sesses mediosagittal invaginations at its posterior differ from each other in terms of their extension along
end. These take the form of several small phragmata the longitudinal axis of the body and the distances
in Lomisidae (Keiler et al., 2016) and a single large between the thoracic neuropils (Fig. 12). The neuro-
phragma in Kiwaidae (Fig. 9D) and Porcellanidae pils are closest together in king crabs (Fig. 11A) and
(Fig. 9F). porcelain crabs (Fig. 11C). In squat lobsters (Fig. 10B),

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Lomis (Fig. 11B) and Pagurus (Keiler et al., 2015b), the
neuropils are more distinctly separate from each other
Ventral nerve cord
and the cephalothoracic ganglion is more elongated.
Cephalothoracic ganglion
The brain is connected to the cephalothoracic ganglion
Pleonal ganglia
(cg) via the paired circumesophageal connectives. The
cephalothoracic ganglion lies ventrally in the midline The cephalothoracic ganglion is connected with ple-
of the cephalothorax above the ventral vessel and onal neuromeres pn2–pn6 via paired connectives. The
is formed by a coalescence of the neuromeres of the neuropils of the pleonal neuromeres are closely spaced
mandible segment, the two maxillar and eight tho- medially and in some species can actually be confluent
racic segments and the first pleonal segment (Fig. 10). with each other.
Although in some species the neuropils of the hem- The arrangement of the pleonal neuromeres dif-
ineuromeres of the mandible (mdn), maxillar (mxn1, fers significantly between the studied taxa. In squat
mxn2) and of thoracic segments th1–th3 (tn1–tn3) lobsters, Paguridae and Pisidia, neuromeres pn2–
can each be identified individually, they form a com- pn6 form distinctly separated ganglia (Fig. 10A)
pact cluster in all studied species (Fig. 10B). By con- which are arranged segmentally within the pleon.
trast, with the exception of thoracic neuromeres tn7 Pleonal neuromeres pn2–pn6 in Hapalogaster
and tn8 in Pagurus (Keiler et al., 2015b), the neuropils (Fig. 11A), Lomis (Fig. 11B), Porcellana (Fig. 11C) and

Figure 10. Central nervous system. Possible ground pattern in Galatheoidea (also representative of the ground pattern
in Chirostyloidea and Aegloidea). (A) Central nervous system of Munida sarsi. (B) Cephalothoracic ganglion of Munidopsis
serricornis. Each fused neuromere represented by paired neuropils. Neuromere of first pleonal segment (pn1) fused with
cephalothoracic ganglion. Abbreviations: mdn, neuropil of mandible segment; mxn, neuropiles of maxillar segments; pn1,
neuropil of first pleonal segment; tn, neuropiles of thoracic segments.

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Figure 11. Pleonal ganglia attached to cephalothoracic ganglion in crab-like representatives. Neuropils of neuromers
are indicated by arrows. (A) Hapalogaster mertensii. (B) Lomis hirta. (C) Porcellana platycheles. (D) Dromia personata
(Linnaeus, 1758) (Brachyura: Dromiidae De Haan, 1833); based on Bouvier 1896). (E) Corystes cassivelaunus (Pennant,
1777) (Brachyura: Corystidae Samouelle, 1819); based on Bouvier, 1889. Abbreviations: tn4-tn7, thoracic neuromeres
(neuropils).

Pachycheles are distinctly reduced and lie within the the descending artery and the position of its junc-
seventh to eighth thoracic segment, closely attached tion with the ventral vessel vary between the taxa.
to each other and to the cephalothoracic ganglion The descending artery merges with the ventral ves-
(see schemes in Fig. 12). sel between the branches of the second and third leg
arteries (Fig. 12). In Kiwa (Fig. 9D) and porcelain
crabs (Fig. 9F), the ventral vessel runs above the
Haemolymph vascular system median phragma which protrudes from the posterior
The circulatory system is formed by the haemolymph part of the sternal plastron.
vascular system (heart and artery systems) and the In all anomurans, the leg arteries which run into
haemolymph lacunar system (sinuses and lacunae) the pereiopods and the arteries which supply the
(Wirkner, Tögel & Pass, 2013). The circulatory system mouthparts branch off from both sides of the ventral
in the studied anomurans matches the basic set-up in vessel. The angles and relative distances between the
other decapods: a compact (globular) heart positioned leg arteries vary between the taxa (Fig. 12). In Aegla
dorsomedially supplies the body with haemolymph and Hapalogaster, the fourth and fifth leg arteries
via seven artery systems which emanate from it. (p4a, p5a) have a common branch emanating from the
Haemolymph is channelled back via a system formed ventral vessel. Similarly, the second, third and fourth
by tissue spaces (lacunae) between the organs and leg arteries (p2a, p3a and p4a) have a common branch
distinct channels (sinuses). It passes the gills and the in Lithodidae. Before entering their respective perei-
pericard and finally enters the heart through three opod, the leg arteries in all the studied species run
pairs of ostia. between the cuticular walls formed by the endoster-
The ventral vessel system is formed by the descend- nites and endopleurites of the endophragmal system
ing artery (da), and the ventral vessel (vv) and its side (Fig. 9C, E). The ventral vessel supplies the ventral
branches (Fig. 9C–F), and mainly supplies the ventral nerve cord via ascending arteries (stars in Fig. 9D, F)
nerve cord and the muscles of the mouthparts and legs which protrude between the neuromeres of the cepha-
(pereiopods). lothoracic ganglion. In terms of position the branches
The descending artery emanates posteroven- of the ascending arteries largely correlate with the
trally from the heart and runs ventrally, skirting branches of the leg arteries.
the gut either to the left or the right depending
on the taxon. It continues ventrally and, except in
Lithodidae, pierces the cephalothoracic ganglion Pleonal muscles
between the sixth and seventh thoracic neuromeres The pleonal muscles can be categorized into lateral,
before merging with the ventral vessel, which runs ventral and dorsal muscles depending on their position
below the ventral nerve cord (Fig. 12). The course of (Fig. 13). The dorsal muscles belong to the extensor,

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212 J. KEILER ET AL.

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Figure 12. Spatial relationships of anatomical systems in the ventral cephalothorax. Schematic drawings of the ventral
systems in the cephalothorax. Colour code: pink, ventral thoracic muscles; bright blue, sterna plastron and eighth tho-
racic sternites; dark blue, endosternites; red, ventral vessel system; yellow, ventral nerve cord (translucent) with neuropil
areas. *The composition of the ventral systems in Galathea essentially corresponds with that in Munida and Munidopsis.
Abbreviations: da, descending artery; cn1-3, cephalic neuropils (neuromeres of mandible and maxillar segments); es4-8,
endosternites; p1-5, pereiopods; pn1-6, pleonal neuropils; pvv, posterior ventral vessel; tn1-8, thoracic neuropils.

the ventral muscles to the flexor system of the pleon. Hepatopancreas

Squat lobsters have the greatest proportion of ple- The hepatopancreas is formed by two bundles of tubu-
onal muscle of all studied morphotypes. In porcelain lar diverticles which are each connected to the pylorus
crabs, the proportion of pleonal muscle is significantly via a broad duct. In Paguridae and king crabs, the
smaller; in Lomis it is drastically reduced (Fig. 13). hepatopancreas is almost completely restricted to the
In Paguridae and king crabs, the proportion of dorsal pleon. In the other taxa, the hepatopancreas fills most
muscle is significantly reduced (Keiler et al., 2013); the of the cephalothorax and the degree to which it extends
proportion of ventral muscle in king crabs is also sig- into the pleon varies from taxon to taxon (Fig. 15).
nificantly reduced (Keiler et al., 2015b).

Ovaries TRANSFORMATIONS AND STRUCTURAL

COHERENCE
The ovaries are situated on the hepatopancreas. In
Paguridae and king crabs, the ovaries (like the testes) The transformations of the pleonal muscles, ventral
are completely restricted to the pleon and only asso- nerve cord and haemolymph vascular system dis-
ciated with the thorax via the oviducts. In the other cussed herein can be assigned to – and are structurally
taxa, the largest portion of the ovaries is located in the dependent on – external changes in either the cepha-
cephalothorax. The degree to which they extend into lothorax or the pleon brought about by the process of
the pleon varies from taxon to taxon (Fig. 14). carcinization.

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 HUNDRED YEARS OF CARCINIZATION 213

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Figure 13. Schematic transverse section through the fourth pleonal segment. Abbreviations: ce, cecum; dpm, dorsal pleonal
muscles; g, gut; lpa, left pleonal artery; lpm, lateral pleonal muscles; pa, posterior aorta; plr; pleurites; rpa, right pleonal
artery; vnc, ventral nerve cord; vpm, ventral pleonal muscles.

Transformations in the cephalothorax Noteworthy, most decapod taxa exhibit separated

The impact of the endophragmal skeleton neuromeres. Fused thoracic neuromeres are found in
representatives of slipper lobsters (Achelata Scholtz
The median distance between the endosternites
& Richter, 1995) and caridean shrimps (Pike, 1947).
and endopleurites is determined by the width of the
A cephalothoracic ganglion formed by a coalescence
plastron and the sternites, respectively. In taxa with
of the neuromeres of the mandible segment, the two
narrow sternites, which probably constitutes the ple-
maxillar and eight thoracic segments and the first ple-
siomorphic condition within Decapoda (Secretan,
onal segment, however, is exclusively found in Meiura
1998), median distances between endosternites are,
(Brachyura + Anomura) and therefore might represent
accordingly, small, and the separation of the segmen-
its ground pattern. The distinct separation of the tho-
tal thoracic neuromeres is pronounced, as in crayfish
racic neuromeres in Hippidae (mole crabs) (Paul, 2004;
(Keim, 1915) and Paguridae (Jackson, 1913; Keiler
own unpublished data) must then be interpreted as
et al., 2013). The same applies to the leg arteries,
secondary.
which are separated from each other by the endoster-
The posterior emargination caused the last pair
nites. In contrast, the endosternites of a broad sternal
of sternites (es 7/8) to shift closer together medi-
plastron, which is present in the crab-like morphotype,
ally, which in turn led to a narrowing of the passage
are further apart, which in turn allows a shorter dis-
between the cephalothorax and the pleon. This led,
tance between the neuromeres and changes the course
in Lomis and porcelain crabs, to the fifth leg arteries
and common branches of the leg arteries (Keiler et al.,
(p5a) being separated by leg arteries p1a–p4a, which
2013, 2015a, b, 2016).
had moved together and shifted anteriorly. In king
crabs such effect is not as distinct.
The impact of the posterior emargination
The posterior emargination of the plastron is a result Neuro-arterial coupling
of the complete bending of the pleon. The posterior The reduced distances between the branches of the leg
emargination leads to a shortening of the median arteries p1a–p4a are presumably related to the more
midline of the ventral cephalothorax. This resulted, pronounced fusion of the neuropils of the cephalotho-
to some degree, in shorter distances between the neu- racic ganglion. The ascending arteries of the ventral ves-
romeres of the cephalothoracic ganglion. sel secure supply to the ganglion and at the same time

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214 J. KEILER ET AL.

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Figure 14. Differences in expansion of the ovaries. Schematic illustration with pleon artificially unfolded. Abbreviations:
pl6, sixth pleonal segment; pl4, fourth pleonal segment.

Figure 15. Differences in expansion of the hepatopancreas. Schematic illustration with pleon artificially unfolded.
Abbreviations: pl3, third pleonal segment; pl4, fourth pleonal segment.

are structurally coupled with the origins of leg arteries

The emergence of the sternal plastron and
p1a–p4a (Fig. 9D, F), with both having been displaced
its posterior emargination – both associated
by the anterior shift in the cephalothoracic ganglion.
with the evolution of the crab-like habitus –
The shift in the leg arteries may have been driven by
led to alterations in the cephalothoracic gan-
a shift in the descending artery, too. In Lithodidae, and
glion and the ventral vessel system.
especially in Lithodes, the distances between the ori-
gins of leg arteries p2a–p4a are small to such an extent Functional differences in the ventral nerve cord between
due to the relatively small size of the cephalothoracic taxa with separated ganglia and those with one larger
ganglion. The narrowing of the space between these fused ganglion are yet to be studied. Complex neuronal
three arteries constitutes a predisposition for the emer- interconnection between walking legs (interleg cou-
gence of a shared origin. Similarly to the situation in pling), however, has been observed in several reptant
Lithodidae, the common branch of the last two pairs decapods (Cruse, Clarac & Chasserat, 1983; Faulkes &
of leg arteries (p4a + p5a) in Hapalogaster was made Paul, 1997). Shorter distances between neuropil areas
possible by a reduction in the distances between the are possibly a prerequisite for enhanced movement coor-
arterial origins and a lateral shift in the endosternites. dination and more complex movement behaviour.

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 HUNDRED YEARS OF CARCINIZATION 215

Convergences in crab-like forms of Anomura and Transformations in the pleon: function–

Brachyura anatomical relationships between
carcinization and the loss of the caridoid
The patterns of the leg arteries in Brachyura are prob-
escape reaction
ably also based on structural coherences relating to
the endophragmal system and the cephalothoracic Triggered by external stimuli, macruran decapods can
ganglion. The branching pattern of the leg arteries in catapult themselves backwards at high speed to escape
brachyurans seems to be more affected – or constricted – danger by suddenly flipping their pleon with its pro-
by the endophragmal system (Fig. 9A) than that in the nounced tail fan downward (Arnott, Douglas & Ansell,
crab-like forms in Anomura. 1998; Jackson & MacMillan, 2000; Faulkes, 2008). The
so-called ‘caridoid escape reaction’ (or ‘escape reflex’,
The external features of a crab-like habitus
‘backward tail flip’ or ‘tail flicking’) is also present

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which evolved convergently in Brachyura and
in squat lobsters (Wilson & Paul, 1987; Keiler et al.,
within Anomura are reflected to some degree
2015a, 2016). The reaction is triggered by a visual or
by similar changes in internal anatomy.
tactile stimulus which leads to a contraction of all the
As in the crab-like anomuran taxa, the position of the pleonal flexor muscles (Faulkes, 2008). The highly
origins of the leg arteries in Brachyura and the fact specialized Blepharipodidae (Anomura: Hippoidea)
that the rear arteries (p4a and p5a) in some Brachyura do not possess a caridoid escape reaction in the strict
(p3a, p4a and p5a in some Portunidae Rafinesque, sense but use the pleon flip to dig backwards into the
1815; see also McGaw & Reiber, 2002) share a com- sandy sediment. Hippidae (Anomura: Hippoidea) use
mon branch are related to the presence of compacted their modified uropods to swim backwards (Paul, 1989;
thoracic neuromeres and the position of the ascending Faulkes, 2008). The ability of hermit crabs to withdraw
arteries which are coupled with the neuromeres (Fig. rapidly into their gastropod shell is also interpreted
9A). The more pronounced endophragmal system in as a strongly modified caridoid escape reaction, since
Brachyura maintains the separation of the branches the muscle contraction involved is controlled in part by
of the anterior leg arteries. Analogously to Kiwa (Fig. similar neurons to those involved in the escape reac-
9D) and porcelain crabs (Fig. 9F), some Eubrachyura tion in macruran forms (Umbach & Lang, 1981; Paul,
de Saint Laurent, 1980 possess a median phragma 1989, 2003).
which evolved as an additional attachment surface
for muscles and compensates the surface reduction
brought about by the posterior emargination. In some Transformation of the pleonal ganglia
eubrachyurans, the eighth pair of endosternites and The pleon-mediated escape reaction requires differ-
endopleurites (es8/ep8) in the transition zone between entiated muscle control, which is provided by spe-
the cephalothorax and pleon is fused, forming the cific neurons within the pleonal ganglia (Paul, 1989;
endophragmal sella turcica (Fig. 9A, B; see also Guinot, Faulkes, 2008 and citations within). As in macruran
1979; Secretan, 1998; Ng, Guinot & Davie, 2008). The forms, pleonal ganglia pn2–pn6 in squat lobsters,
composition of the sella plays a key role in the branch- Paguridae and Hippoidea are arranged segmentally
ing pattern of the leg arteries in eubrachyurans. The and are distinctly separate from each other (Bouvier,
coxae of the eighth pereiopods in eubrachyurans are 1888a, 1889; Jackson, 1913; Pike, 1947; Chacko, 1967;
located anterior to the sella, constraining the leg arter- Sillar & Heitler, 1985; Paul, 2004). Performing the
ies to branch from the ventral vessel more anteriorly. caridoid escape reaction obviously requires not only
As a consequence, the fifth leg arteries (p5a) have to strong muscles and a tail fan, but corresponding neu-
emanate anterior to the median phragma, which prob- ronal control by segmentally arranged ganglia.
ably led to the development of a common branch in
The most distinct changes resulting from
the rear leg arteries. A common arterial branch is pre-
the evolution of a crab-like habitus affected
vented from evolving in cases where the endosternites
the pleon and led to changes in the pleonal
are tightly spaced one after another and the distance
ganglia.
between them medially is small, as in Hyas araneus
(Linnaeus, 1758) (Fig. 9A), for example. A similar endo- In the course of carcinization, however, the caridoid
phragmal structure (pseudo-sella) likewise constrained escape reaction was lost. As a direct consequence of the
by the posterior emargination of the plastron, but with flattening of the pleon, the proportion of pleonal mus-
a differing endophragmal composition (endosternites culature decreased significantly in the crab-like forms,
es 7/8), evolved in Kiwa (Fig. 9C, D). Only due to its dif- particularly in Lomis (Fig. 13). Moreover, in brachy-
fering endophragmal composition the pseudo-sella in urans, king crabs and Lomis, the tail fan (broad telson
Kiwa does not have such a constraining impact on the + broad uropods), which is essential for the tail flip,
arterial pattern as opposed to Brachyura. also became completely or nearly completely reduced.

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216 J. KEILER ET AL.

In some Porcellanidae (Porcellana spp., Polyonyx muscles, a phenomenon particularly pronounced in

sinensis Stimpson, 1858, Petrolisthes spp.), a rhythmic Lomis (Fig. 13), but also to an expansion of the ovaries,
flipping of the pleon has been observed which allows which, in Lomis and porcelain crabs, run further into
the animals to swim (Števčić, 1971; Hiller et al., 2010; the pleon (Fig. 14). Furthermore, the diverticles of the
Hsuch et al., 1998 cited in Paul, 2003) or to remain hepatopancreas also reach further into the pleon in
stable in the water column while descending after Lomis (Fig. 15) than in its non-crab-like ancestors. In
slipping from vertical surfaces (Paul, 1989, 2003). In contrast, the shift into the pleon of the hepatopancreas
Porcellana platycheles, only freshly moulted individu- and gonads in king crabs occurred prior to the evolu-
als, whose density is lower, are capable of active swim- tion of the crab-like habitus, since in asymmetrical
ming, while individuals with a calcified integument hermit crabs the change in the function and biological
cannot move just by flapping their pleon (Davenport, role of the pleon had already taken place.

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1972). A true caridoid escape reaction is not described The starting point of the evolution of king crabs dif-
for porcelain crabs. Alternative escape strategies fered from that of the other crab-like forms since the
such as the autotomy of the chelipeds are evolved in last non-crab-like ancestor of king crabs had probably
Porcellanidae (Wasson, Lyon & Knope, 2002). already lost or modified the caridoid escape reaction
Unlike in macruran forms, the pleonal ganglia in (Paul, 1989). The result as far as the reduced pleonal
Brachyura, king crabs, Porcellana, Pachycheles and ganglia are concerned, however, is the same, and is
Lomis are small, compact and fused with the cepha- a consequence of the reduction in the activity of the
lothoracic ganglion (Fig. 11; Keiler et al., 2015a, b, pleon brought about by the crab-like habitus.
2016). The reduction of and anterior shift in the ple-
onal ganglia in these crab-like representatives cor-
relates with the loss of the caridoid escape reaction. CARCINIZATION – SIMILAR
Among the studied taxa with a crab-like habitus, PREDISPOSITIONS AS THE CAUSE OF THE
Pisidia and Petrolisthes stand out in terms of the pat- PARALLELISM?
tern of pleonal neuromeres. In Petrolisthes, only the
anterior neuromeres (pln2–pln5) have shifted anteri- The extent of the changes affecting internal structures
orly and have become tightly strung and in Pisidia, which occurred in the course of carcinization is essen-
the anterior shift in the pleonal ganglia is only slight tially dependent on the underlying morphological
(Fig. 12; Keiler et al., 2015a). Taxon-specific differences starting point: the last common (non-crab-like) ances-
in the distance between and position of the pleonal tor of the extant forms in question.
neuromeres are also present in brachyurans. In repre- In this regard, Lomis and porcelain crabs are simi-
sentatives of the podotrematan taxon Dromia Weber, lar since both are probably derived from a squat lobster
1795, the pleonal ganglia are tightly spaced and with a ‘half-carcinized’ habitus presumably reflecting the
arranged in a chain-like formation (Fig. 11D; Bouvier, ground pattern of Anomura (Haug & Haug, 2014; Keiler
1896). In eubrachyurans, the pleonal ganglia are more et al., 2016). Very similar, presumably homologous predis-
distinctly reduced and more strongly fused with each positions (e.g. sternites already fused to a wide plastron;
other (Fig. 11E; Bouvier, 1889; Bethe, 1897). pleon already largely bent) were present in both lineages.
The emergence of the crab-like habitus in porcelain crabs
and Lomis thus represents parallel evolution in the wid-
Change in function and biological role of the pleon est sense (see Desutter-Grandcolas et al., 2005; Pearce,
The changes in the pleonal ganglia described above 2012; but see also Arendt & Reznick, 2008).
were only made possible by transformation into a crab- The lineage of king crabs, in contrast, developed from
like habitus and concomitant morphological and func- a totally different morphological starting point. King
tional changes in the pleon. The loss of the caridoid crabs are derived from asymmetrical hermit crabs, which
escape reaction is probably a prerequisite for the ante- do not possess any of the characteristics of a crab-like
rior shift in the pleonal ganglia, their reduction in size habitus. The morphological changes which took place in
and their attachment to the cephalothoracic ganglion the lineage from the hermit crab-like ancestor to today’s
(Keiler et al., 2015a). We interpret the neuro-anatom- king crabs were, therefore, more dramatic in many ways
ical and neuro-physiological alterations in the pleonal than those which took place in porcelain crabs or Lomis.
ganglia and its circuits as a result of morphological Moreover, selection pressure was presumably also differ-
changes in the pleon and the ethological changes (i.e. ent (Cunningham et al., 1992; Richter & Scholtz, 1994).
changes of the biological role) associated with them, The situation with regard to the evolution of Brachyura
and not vice versa (but see Faulkes, 2008). is not clear and depends on the ground pattern of the
The change in the function and biological role (Bock Meirura. We interpret the oldest known representatives
& von Wahlert, 1965; Richter & Wirkner, 2014) of of Anomura (P. akaina Chablais et al., 2011; see fig. 3 in
the pleon led not only to a reduction of the pleonal Chablais et al., 2011) and Brachyura (Eoprosopon klugi

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, 121, 200–222
 HUNDRED YEARS OF CARCINIZATION 217

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Figure 16. Convergent morphological changes (dotted lines) within Meiura (Anomura + Brachyura) which took place in
the course of carcinization and which led to the same morphological pattern in the crab-like taxa, exemplified by three
selected morphological characters (phylogeny based on Schnabel et al., 2011; character states in italics).

Forster, 1986; see fig. 5 in Haug & Haug, 2014) to have turn probably constitutes a predisposition for the increase
a habitus very similar to that of a squat lobster. If the in density and anterior shift in the segmental thoracic neu-
last common ancestor of Anomura and Brachyura actu- romeres, and for the emergence of shared branches in the
ally possessed a habitus similar to a squat lobster, the rear leg arteries (p3a, p4a and p5a). Thus, structural co-
predispositions in Brachyura would have been similar to herence is present between the plastron and endosternites,
those in porcelain crabs and Lomis. Whatever the case, and also between the endosternites and the neuromeres of
various correspondences are present in the internal the ventral nerve cord, and the laterally branching arteries
anatomy of Brachyura and Anomura (particularly por- of the ventral vessel (i.e. leg arteries).
celain crabs) which can be explained against the back- B) The strongly bent pleon in crab-like forms necessitated
ground of convergent changes which took place in the the formation of a posterior emargination in the plastron,
course of carcinization (Fig. 16). which in turn resulted in a median narrowing of the last
pair of endosternites and probably led to an additional an-
terior shift in the thoracic neuromeres. In eubrachyurans,
the posterior emargination led to the formation of the sella
‘COHERENCE CHAINS’ (COHERENCE
turcica and the median phragma, which latter essentially
CONCATENATION)
constrains the common branch of the rear leg arteries.
The crab-like habitus which evolved convergently in Structural coherence is present between the strongly bent
brachyurans and the three anomuran lineages is a pleon and the posterior emargination of the plastron. The
combination of single characters of the crab-like habi- latter, in turn, is related to the coherences set out in ‘A’.
tus (see criteria above) which emerged in the course of C) The shift in the ascending arteries of the ventral vessel
convergent transformations. The posterior emargina- and the descending artery is coupled with the shift of the
tion of the plastron is a direct result of the strongly thoracic neuromeres and probably resulted in an anterior
bent pleon; apart from that, transformation series are shift in the leg arteries and which, along with the increase
largely independent from each other. in the distance between the endosternites (see ‘A’), consti-
Some of the internal anatomical characters stud- tutes another prerequisite for the emergence of a common
ied herein are structurally dependent on the external branch in the rear leg arteries (p3a, p4a and p5a). Thus,
characters of a crab-like habitus. Since morphologi- structural coherence is present between the neuromeres
cal coherence can also exist between internal ana- of the ventral nerve cord and the ventral vessel system.
tomical structures, the coherence chains which can be Denser neuromeres (and neuropils) are possibly a predis-
traced back to the external characters of a crab-like position for more complex locomotion.
habitus are relatively complex in some cases (indirect D) The strongly bent pleon in crab-like forms inevitably led to
coherences). the loss of the caridoid escape reaction. As a consequence,
The most important morphological and structural- the pleon became flattened to be carried under the cepha-
functional coherence chains associated with a crab-like lothorax and pleonal muscles were reduced. These struc-
habitus can be set out as follows: tural–functional alterations finally resulted in a reduction
of and shift in the pleonal ganglia. Thus, structural–func-
A) A wide plastron is the predisposition for the increase of tional coherence is present between the caridoid escape
the median distance between the endosternites, which in reaction and the pleonal ganglia.

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, 121, 200–222
218 J. KEILER ET AL.

Although enormous morphological disparity is 1. Abteilung 7, Buch 12. Leipzig & Heidelberg: Winter,
observed in the internal anatomy of the crab-like taxa, 1505–1672.
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ing dependences are found across the different line- Zoologie, Abteilung B 118: 246–312.
ages between the external characters of a crab-like Belman BW. 1975. Some aspects of circulatory physiology of
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Bethe A. 1897. Das Nervensystem von Carcinus maenas.
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Boas JEV. 1880a. Lithodes und Pagurus. Zoologischer
assume that ‘evolutionary tendencies’ or any such
Anzeiger 3: 349–352.

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vague concept played a role. B o a s J E V. 1 8 8 0 b . S t u d i e r o v e r D e c a p o d e r n e s
Slaegtskabsforhold. Det Kongelige Danske Videnskabernes
Selskabs Skrifter 6, Naturvidenskabelig og Mathematisk
ACKNOWLEDGEMENTS Afdelinger I 2: 27–210.
Boas JEV. 1924. Die verwandtschaftliche Stellung der
We are grateful to the vast number of colleagues and
Gattung Lithodes. Det Kongelige Danske Videnskabernes
friends who have helped us with collecting speci-
Selskabs, Biologiske Meddelelser IV 4: 1–34.
mens, who have sent us material, or provided techni- Boas JEV. 1926. Zur Kenntnis symmetrischer Paguriden.
cal support. We thank our colleagues at the Zoological Det Kongelige Danske Videnskabernes Selskabs, Biologiske
Institute of the University of Rostock and two anony- Meddelelser V 6: 1–52.
mous reviewers for comments and suggestions which Bock WJ, von Wahlert G. 1965. Adaptation and the form-
improved the manuscript. Lucy Cathrow improved the function complex. Evolution 19: 269–299.
English and helped to clarify our thoughts. The German Borradaile LA. 1907. On the classification of decapods crus-
Science Foundation Deutsche Forschungsgemeinschaft taceans. The Annals and Magazine of Natural History 19:
is thanked for funding our studies (grant numbers WI 457–486.
3334/1–2 and 3334/3-1). MicroCT machines were spon- Borradaile LA. 1916. Crustacea. Part II. Porcellanopagurus:
sored by the Deutsche Forschungsgemeinschaft DFG An instance of carcinization. Natural History Report, Zoology
INST 264/38-1 FUGG (Universitaet Rostock) and DFG 3: 111–126.
INST 292/119-1 FUGG, DFG INST 292/120–1 FUGG Bouvier EL. 1888a. Le système nerveux des Crustacés décap-
(Universitaet Greifswald). odes. Bulletin de la Société Philomatique de Paris 7: 111–114.
Bouvier EL. 1888b. Sur l’appareil circulatoire de l’Ecrevisse.
Bulletin de la Société Philomatique de Paris 7: 52–53.
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