JOURNAL OF CRUSTACEAN BIOLOGY, 21(1): 288–303, 2001
A MORPHOMETRIC ANALYSIS OF REGIONAL VARIATION IN CARCINUS
LEACH, 1814 (BRACHYURA: PORTUNIDAE: CARCININAE) WITH
PARTICULAR REFERENCE TO THE STATUS OF THE TWO SPECIES
C. MAENAS (LINNAEUS, 1758) AND C. AESTUARII NARDO, 1847
Paul F. Clark, Michael Neale, and Philip S. Rainbow
(PFC, PSR) Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD,
England (e-mail: [email protected], [email protected]); (MN) School of Biological Sciences,
Queen Mary and Westfield College, London E1 4NS, England; present address: Environment Agency,
Rivers House, Threshelfords Business Park, Inworth Road, Feering, Colchester, Essex CO5 9SE, England
(e-mail: [email protected])
A B S T R A C T
Biometrical analyses have been carried out on 26 population samples of Carcinus from the Pacific (1), Atlantic (17), and Mediterranean (8), to investigate the validity of the taxonomic division
of the genus into C. maenas (Atlantic) and C. aestuarii (Mediterranean). Consideration of carapace
width to carapace length and carapace width to carapace depth ratios, and a set of 10 biometric
characters by canonical variates analysis, showed that there were two different statistical populations in the European data set apparently corresponding to Atlantic and Mediterranean specimens
of Carcinus. There was still overlap of individuals between the Atlantic and Mediterranean data sets,
such that individual crabs could not be assigned unequivocally to one group or the other on the basis of shape. The presence or absence of setae on the frontal distal margin of the cheliped carpus
varied geographically. Mediterranean crabs possessed prominent setal brushes, while crabs from
the Atlantic north of (and including) Porto in Portugal lacked these setae. Crabs from the other
Portuguese sites, from the Palmones estuary in southern Spain, and from Gibraltar did, however,
sometimes have a few setae on the cheliped carpus. This observation indicates lack of complete
genetic separation of the Atlantic and Mediterranean populations of Carcinus, with the potential
existence of a hybrid zone between them. The morphological data do not support the separation of
European Carcinus into two taxa distinct at the species level, but additional genetic data are needed
to verify the presence of any real gene flow and a hybrid zone between Atlantic and Mediterranean
crab populations.
Leach (1814) established Carcinus as a
monotypic genus for Cancer maenas Linnaeus, 1758, and this species was considered
to be widely distributed throughout the NE
Atlantic and Mediterranean Sea (e.g., Rathbun, 1930). Carcinus maenas has an extensive geographical range from Southern Iceland and Norway (Christiansen, 1969) in the
northeast Atlantic (70°N latitude) to Mauritania (Monod, 1956) in the southeast Atlantic
(21°S latitude), and Almaça (1961) records
this species from Ceuta, North Africa, Strait
of Gibraltar. This species commonly occurs
from intertidally (Yonge, 1949) to depths of
62 m (Bouvier, 1940). The Atlantic species
has been introduced into a number of regions
where populations are now established, including the east coast of America from Nova
Scotia (Welch, 1968; Bousfield and Laubitz,
1975) to Virginia (Holthuis and Gottlieb,
1958; Williams, 1984), the west coast of
America, San Francisco (Cohen et al., 1995;
Grosholz and Ruiz, 1995), the Bay of Panama
(Rathbun, 1930), Madagascar (Crosnier,
1962), Table Bay, Cape Town, South Africa
(Le Roux et al., 1990), Ceylon (Alcock,
1899), Maungmagan, Burma (Boschma,
1972), and Australia (Fulton and Grant,
1900). Specimens have also been recorded
from Pernambuco, Brazil (Rathbun, 1930;
doubtful according to Almaça, 1962) and
Hawaii (Streets, 1877; doubtful according to
Edmondson, 1954), although the legitimacy
of these sightings is unknown, as populations
in these two localities have not become established.
Carcinus continued to be considered monotypic until Demeusy and Veillet (1953) examined populations of C. maenas from Sète
in the Mediterranean and Roscoff and Loc
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CLARK ET AL.: BIOMETRIC ANALYSES OF CARCINUS
289
Table 1. A list of characters considered by Demeusy and Veillet (1953) that separated populations of Carcinus
maenas (Linnaeus, 1758) from Sète (Mediterranean Sea) and Roscoff and Luc (English Channel, Atlantic Ocean).
Characters
CARAPACE
anterolateral teeth
pilosity of anterolateral margins
width/length ratio
length/depth ratio
frontal region
hepatic, branchial, and
cardiac regions
color of juveniles
color of adult
ANTENNULE
segments
flagellum segments
ANTENNA
number of segments
total length of antenna
teeth on outer basal segment
CHELIPED
dactylus
propodus
distal outer margin of the carpus
ABDOMEN
young female
Sète
pointed and with the posterolateral
tooth more oblique
denser
narrower
deeper
setose with 3 size classes of setae
Roscoff/Luc
separated by deeper furrows and
dorsal carapace more rugose
white spots which disappear
rapidly during development
dark green
blunter and with the posterolateral tooth directed forward
less marked
broader
shallower
generally smooth and frontal
teeth finely festooned
no obvious furrows present
and dorsal carapace smooth
extremely rich in various tones
which are preserved to puberty
violet-blue or green
longer and slightly narrower
4
shorter and a little broader
5–6
significantly more
longer
present on the outer lateral
margin of dorsal face
outer lateral margin of ventral
face smooth
less
shorter
outer lateral margin of
dorsal face smooth
outer lateral margin of
ventral face spinose
with accentuated crests
with crests, granules and setae
setose
not distinct
not distinct
not setose
more enlarged
less enlarged
from the English Channel. They considered
that these two populations were distinct and
separated by a number of characters including the presence or absence of setae on the
frontal distal margin of the cheliped carpus
(see Table 1). According to their study the two
populations could be interbred using females
from the English Channel and males from the
Mediterranean, and the eggs hatched. Furthermore, crabs from the English Channel
survived and grew in Mediterranean conditions, whilst retaining their morphological
features (Demeusy and Veillet, 1953). Forest
(1957) reported on a meeting of carcinologists in Barcelona during July 1957 at which
Zariquiey Álvarez discussed differences between populations of C. maenas from
Cataluna (Mediterranean) and Galicia (Atlantic). A year later the type locality for Atlantic Carcinus was established as the west
coast of Sweden (Marstrand, North Göteborg)
by Holthuis and Gottlieb (1958), and they resurrected the name C. mediterraneus Czerniavsky, 1884, for the Mediterranean form. A
key separating the Atlantic and Mediterranean
Carcinus forms, based on the characters of
Demeusy and Veillet (1953), was produced
by Zariquiey Álvarez (1968). The latter also
noted that there were differences in the structure of the male pleopod. The first pleopod
was described as strongly curved in C. maenas but rectilinear in C. aestuarii (as C.
mediterraneus; see Zariquiey Álvarez, 1968,
Fig. 115). Pleopod differences between the
two proposed Carcinus species were also illustrated by T. Sakai (1986, Pl. 2). Later,
Manning and Holthuis (1981) found a senior
synonym for the Mediterranean species, C.
aestuarii Nardo, 1847, and this name has now
become established in the literature. Carcinus
aestuarii has an extensive distribution around
the Mediterranean Sea to a depth of 26 m
(Abelló et al., 1988) and has been reported
from outside this area in the Canaries (Almaça, 1961) and Tokyo Bay, Japan (Sakai,
1986). The Red Sea Carcinus specimen reported by A. Milne Edwards (1860) may have
been either species, but Klunzinger (1913)
considered this introduction to be unique because he had not collected any material from
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this locality. However, recently Cottiglia
(1983) questioned the validity of the name
C. aestuarii of Nardo (1847); he considered
it to be a nomen nudum and consequently
used C. mediterraneus (Czerniavsky) in his
“Crostacei Decapodi Lagunari”.
Since the studies of Demeusy and Veillet
(1953) and Zariquiey Álvarez (1968), there
have been other attempts at separating the two
possible Carcinus species using morphometric data. Almaça (1961) examined 176 specimens from Portugal, the Canaries, Spain, and
France. Carapace width and length ratios
were calculated for crabs from the English
Channel and Mediterranean by Rice and Ingle (1975). In their study, Carcinus maenas
specimens from Brighton and Plymouth (English Channel) scored 1.32 and 1.29 respectively, compared with C. aestuarii (as C.
mediterraneus) material from Salammbo,
Tunisia, with a ratio of 1.25 (see Rice and
Ingle, 1975, Table 1, Plate 1A, B, D, E). More
recently Noël (1992) wrote a key to identify
the decapod crustaceans of France which also
included distinguishing features of the Carcinus species and cited a carapace width/length
ratio for C. maenas (1.29–1.32), compared
to C. aestuarii (1.25–1.29). All these studies
supported the separation of Carcinus into two
species. However in their work, Rice and Ingle (1975) also described the larval development of both Carcinus species from laboratory-reared material, and apart from the dimensions of the zoea, they considered the two
forms to be very similar. Therefore according
to them, there was no good larval evidence
to support the specific separation of C. maenas and the Mediterranean species, despite
the existence of consistent differences between the adults. There is still little quantitative evidence to support or reject the establishment of the two species of Carcinus on
morphological characters. In fact Carcinus
specimens are probably identified by locality rather than on morphology, conveniently
avoiding any overlap of the two species. The
morphometric studies conducted by Demeusy
and Veillet (1953), Almaça (1961), Rice and
Ingle (1975), and Noël (1992) were limited
to small samples from discrete areas and did
not account for the full geographical distribution of both putative Carcinus species.
The aim of this paper is to review the
nomenclature of the Mediterranean form of
Carcinus and to support or reject the validity of the taxonomic division of the genus into
the two proposed species by morphometric
analysis. An analysis was conducted using a
large number of specimens from a wide range
of sites representative of known distributions.
A further analysis attempted to duplicate the
work of Demeusy and Veillet (1953) by comparing two populations, one from the English
Channel and the other from the French
Mediterranean Coast. Also investigated was
the presence or absence of setae on the frontal
distal margin of the cheliped carpus. Moreover, the pleopod structure of both putative
Carcinus species was examined using Scanning Electron Microscopy.
NOMENCLATURE
The two publications of Nardo dated 1847
were re-examined in order to establish the
availability of the name Carcinus aestuarii.
The figures of Cherreghini cited by Nardo
(1847a, b) have not been published (see footnote, Cottiglia, 1983: 102). Nardo (1847a) is
just a list of names and consequently is not
a valid indication, but, although the description by Nardo (1847b) in his tabulation of
“Classe de Crostacei” may be considered to
be superficial and brief, it appears to make
the name available. Therefore, the present
study follows Manning and Holthuis (1981:
75) and accepts C. aestuarii Nardo, 1847, as
senior synonym of C. mediterraneus Czerniavsky, 1884.
MATERIALS AND METHODS
Material
A total of 1,737 Carcinus specimens of both putative
species was included in the present study. The samples
were provided from various sources, including deposits
at the Museu Nacional de História Natural, Lisboa
(MNHN), Natural History Museum, London (NHM), and
the Smithsonian Institution, Washington (USNM), as well
as more recent samples which were specifically collected
for the purposes of this project (deposited in the NHM).
The sample sizes from each site varied considerably, ranging from just 12 individuals to 251 individuals. Material
from various geographic areas was examined, and a good
cross-section of individuals of many sizes, including both
sexes, was obtained from different regions. Specimens
were taken from different depths, ranging from the intertidal zone to a depth of fourteen metres, and at different times of year. Specimens of Carcinus were collected
from 17 different sites across the North-East Atlantic
down to and including the Strait of Gibraltar (one site,
Estuario do Mira, Portugal, being sampled on two different occasions), six sites from the Mediterranean (two sites
CLARK ET AL.: BIOMETRIC ANALYSES OF CARCINUS
sampled twice), and one from the west coast of the United
States, as follows:
16.
1. Carcinus maenas: 38 specimens; Bodega Harbour,
Bodega Bay, California, United States; Pacific Ocean;
coll. Ted Grosholz, Paul Clark, and Roni Robbins, 21
March 1999; det. Ted Grosholz, NHM reg.
2000.166–199.
2. Carcinus maenas: 54 specimens; Islesburgh Voe, grid
ref. HU 336688, Mainland, Shetland, Scotland; NE
Atlantic Ocean; coll. A. P. Buckle, and R. G. Oates,
Royal Holloway College, 8 July 1969; det. Elizabeth Allen, NHM reg. 1969: 1044.
3. Carcinus maenas: 90 specimens; Alligin, grid ref.
NG 845575, Upper Loch Torridon, Scotland; NE Atlantic Ocean; coll. Tony Rice, 21 September 1968;
det. D. M. U., NHM reg. 1968: 329.
4. Carcinus maenas: 39 specimens; Helnoes, Fjord Fyn
(Funen), 55°09′N, 10°05′E, Denmark; Kattegat,
North Sea, NE Atlantic Ocean; coll. Poul Bjerregaard, November 1996; det. Poul Bjerregaard, NHM
reg. 1997: 1006–1015.
5. Carcinus maenas: 164 specimens; Menai Bridge,
North Wales; Irish Sea, NE Atlantic Ocean; coll. Norman Sloan, 20 May 1970; det. Elizabeth Allen, NHM
reg. 1970: 436.
6. Carcinus maenas: 178 specimens; Coulagh Bay,
County Cork, Ireland; NE Atlantic Ocean; coll. C. R.
Boyden and M. J. Daniel, Summer 1970, Queen
Mary College; det. Elizabeth Allen, NHM reg. 1970:
435.
7. Carcinus maenas: 20 specimens; the wreck of the
Teddington, 14 m, 2 miles east of Cromer, off Overstrand, Norfolk, England; North Sea, NE Atlantic
Ocean; coll. David Davis, 21 November 1996; det.
Paul Clark, NHM reg. 2000.200–255.
8. Carcinus maenas: 56 specimens; West Runton, Norfolk, England; North Sea, NE Atlantic Ocean; coll.
Nick Evans, Paul Clark, and Brian Pitkin, NHM Diving Unit, 29 September 1996; det. Paul Clark, NHM
reg. 1996: 1413–1422.
9. Carcinus maenas: 251 specimens; Power Station intake, Fawley, Hampshire, England; Southampton Water, The Solent, English Channel, NE Atlantic Ocean;
coll. R. S. K. Barnes, Central Electricity Generating
Board, May–June 1970; det. Elizabeth Allen, NHM
reg. 1970: 437.
10. Carcinus maenas: 78 specimens; Fort Euek, pointe
de Fouras, 46°00.2′N, 01°07.5′W, Rés de Rochefort,
Charente-Maritime, France; NE Atlantic Ocean; coll.
Pierre Noël, 2 March 1997; det. Pierre Noël, NHM
reg. 1997.730–739.
11. Carcinus maenas: 90 specimens; Porto, Portugal; NE
Atlantic Ocean; coll. April 1977; det. Ray Ingle,
NHM reg. 1978: 130 and 1978: 131.
12. Carcinus maenas: 141 specimens; canal de Mira, Ria
de Aveiro, Portugal; NE Atlantic Ocean; coll. Henrique Queiroga; det. Henrique Queiroga, NHM reg.
1997: 740–749.
13. Carcinus maenas: 22 specimens, Estuario do Mira,
Portugal; NE Atlantic Ocean; coll. José Paula, 22 October 1986; det. José Paula, MNHN reg. 847CD.
14. Carcinus maenas: 20 specimens, Estuario do Mira,
Portugal; NE Atlantic Ocean; coll. José Paula, May
1986; det. José Paula, NHM reg. 1989: 246.
15. Carcinus maenas: 34 specimens; Vila Nova de Milfontes, Portugal; NE Atlantic Ocean; coll. A. J.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
291
Almeida, 26 February 1984; det. A. J. Almeida,
MNHN reg. 1384CD.
Carcinus maenas: 24 specimens; Palmones Estuary,
36°10′N, 5°27′W, Algeciras Bay, Cadiz Province,
Spain; coll. Darren Fa and Paul Clark, 14 September 1997; det. Paul Clark, NHM reg. 2000: 4–13.
Carcinus maenas: 18 specimens; Europa Point,
Gibraltar; coll. Awantha Dissanayake, 15 September
1997; det. Paul Clark, NHM reg. 2000.148–165.
Carcinus maenas: 22 specimens; Sandy Bay, Gibraltar; coll. Awantha Dissanayake, 18 August 1997; det.
Paul Clark, NHM reg. 2000.128–147.
Carcinus aestuarii: 12 specimens; saltmarsh, UTM
4412145/31508245, Albupereta de pollença, Alcudia,
Mallorca, Balearic Islands, Spain; Mediterranean
Sea; coll. Damián Jaume, January 1997; det. Paul
Clark, NHM reg. 1999: 640–649.
Carcinus aestuarii: 21 specimens; saltmarsh, UTM
4412145/31508246, Albupereta de pollença, Alcudia,
Mallorca, Balearic Islands, Spain; Mediterranean
Sea; coll. Damián Jaume and Paul Clark, 13 March
1999; det. Paul Clark, NHM reg. 1999: 630–639.
Carcinus aestuarii: 69 specimens; Ebro Delta, Alfacs
Bay, Spain; Mediterranean Sea; coll. Pere Abelló,
15 October 1998; det. Pere Abelló, NHM reg. 1999:
8–17 and 1999: 18–27.
Carcinus aestuarii: 88 specimens; Marseille, France;
Mediterranean Sea; coll. H. C. Kellers, August 1922;
det. Mary J. Rathbun as Carcinus maenas, USNM
reg. 57416.
Carcinus aestuarii: 70 specimens; Carthage Harbour,
Carthage, Tunisia; Mediterranean Sea; coll. Paul
Clark and Tom Aldridge, 5 September 1974; det. Ray
Ingle, NHM reg. 1978: 129.
Carcinus aestuarii: 78 specimens; Marano Lagoon,
Italy; Adriatic Sea, Mediterranean Sea; coll. Carlo
Froglia and M. E. Gramitto, 19 September 1997; det.
Carlo Froglia, NHM reg. 1999: 28–37 and 1999:
38–47.
Carcinus aestuarii: 30 specimens; Istanbul, Turkey;
Sea of Marmara, Mediterranean Sea; coll. H. C.
Kellers, March 1923; det. Mary J. Rathbun as Carcinus maenas, USNM reg. 57420.
Carcinus aestuarii: 30 specimens; Istanbul, Turkey;
Sea of Marmara, Mediterranean Sea; coll. H. C.
Kellers, September–October 1923; det. Mary J. Rathbun as Carcinus maenas, USNM reg. 57428.
Methods
Measurements.—Various morphological traits were identified, based predominantly on the distinguishing features
described by Demeusy and Veillet (1953), Zariquiey
Álvarez (1968), Rice and Ingle (1975), and Noël (1992),
to differentiate between the species. A total of ten different linear distances, including those traits in the literature, along with other important taxonomic features, was
taken on each individual (see Fig. 1). Distance measurements were taken with callipers to the nearest 0.1 mm.
Additionally to this, the presence or absence of setae on
the frontal distal margin of the cheliped carpus was
recorded using a Wild M5 microscope. The morphological measurements used were 1. Carapace Width; 2. Carapace Length; 3. Carapace Depth (not shown); 4. Optical
Groove Width; 5. Length of Right Chela; 6. Depth of
Right Chela; 7. Length of Propodus of Right Chela, excluding Pollex; 8. Length of Left Chela; 9. Depth of Left
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Fig. 1. Carcinus; locations of measurements taken on the dorsal surface of each crab.
Chela; 10. Length of Propodus of Left Chela, excluding
Pollex.
To reduce further the influence of size on the crab’s
morphology, some of the data obtained were converted to
appropriate ratios. Thus, carapace width was divided by
carapace length, as it has been suggested (Noël, 1992)
that there is a noticeable difference in values of this ratio between populations of C. maenas and C. aestuarii.
Statistical Analyses.—Before the statistical analysis, all
measurements were log transformed, and ratios were
transformed using the arcsine transformation. The analyses involved comparisons of mean ratios by Analysis of
Variance (ANOVA), regression coefficients by Analysis
of Covariance (ANCOVA), and Canonical Analysis for
multiple group discrimination. The choice of canonical
analysis for taxonomic analysis followed the recommendation of Thorpe (1980), and the example of Bamber
(1982).
Scanning Electron Microscopy.— The tips of the male
pleopods are often used in distinguishing species of crabs
(Serène, 1984; Clark and Galil, 1993). The populations
chosen for the SEM study were the population from West
Runton, Norfolk (putatively C. maenas) and the one from
the Ebro Delta, Spain (putatively C. aestuarii). The right
first pleopod was removed from each of two male specimens from each population and prepared on the basis
of the method of Felgenhauer (1987). The pleopods, preserved in 70% alcohol, were rehydrated in a descending
ethanol series, from 60% ethanol to distilled water,
washed in distilled water, and placed in the anionic surfactant TWEEN–20 (one drop of concentrate to 50 ml dis-
tilled water) for 15 min, before sonication to remove debris in a Dawe Instruments Ltd. sonicator for 10 sec. The
material was washed again in distilled water and dehydrated in an ascending acetone series from 25% acetone
to 100% acetone. Dehydration was completed in a Balzers CPD030 Critical Point Drier. The pleopods were
mounted on stubs using Araldite, cured in an oven for
16 h, sputter coated with a 20-nm thick layer of gold in
a Cressington sputter coater, and examined using a Hitachi S2500 Scanning Electron Microscope.
RESULTS
Statistical Analysis.—Following Noël (1992),
particular attention was paid to the ratio between carapace width and carapace length
(CW/CL). Figure 2 shows the mean CW/CL
ratio for each population in the order listed
in materials examined (Fig. 2a). There does
appear to be a discontinuity in the distribution of the data between samples 18 (Gibraltar) and 19 (Mallorca), corresponding to the
proposed split between C. maenas in the Atlantic Ocean and C. aestuarii in the Mediterranean Sea. Indeed statistical comparison of
transformed data by ANOVA does show a significant difference between the CW/CL ratios
for the Atlantic (2 to 18) and Mediterranean
(19 to 26) populations (Fs = 865; 1,692 d.f.;
P < 0.001). However, considerable overlap
CLARK ET AL.: BIOMETRIC ANALYSES OF CARCINUS
293
Fig. 2. Mean ratios (± 1 standard deviation, SD) of carapace width (CW) to carapace length (CL) of: (a) 26 samples of populations of Carcinus spp. as described in the
text. Sample 1 is from the Pacific Ocean, samples 2 to 18
from the NE Atlantic Ocean, and samples 19 to 26 from
the Mediterranean Sea; (b) populations of Carcinus
grouped as Pacific, Atlantic, or Mediterranean in origin.
is apparent in the ratios of different populations in the two regions (Fig. 2a), and indeed
there are significant differences between the
ratios of populations within both the Atlantic
(Fs = 15.5; 1,280 d.f.; P < 0.001) and Mediterranean (Fs = 9.57; 389 d.f.; P < 0.001) regions. Figure 2b shows the mean ratios for
combined populations from the Atlantic and
Mediterranean, together with that for the
single Pacific population examined. Although
there is considerable overlap between the data
for Pacific and Atlantic crabs (Fig. 2a, b),
there is a significant difference between the
mean CW/CL ratios for the Atlantic and Pacific crabs (ANOVA of transformed data, Fs
= 17.2; 1,333 d.f.; P < 0.001). More expectedly from Figs. 2a and 2b, there is also a significant difference between CW/CL ratios for
Mediterranean and Pacific crabs (Fs = 219;
433 d.f.; P < 0.001).
In order to make allowance for any possible effect of size of individual crabs on the
CW/CL ratio, Analysis of Covariance (AN-
Fig. 3. Regressions of carapace width against carapace
length of individual crabs from (a) the Atlantic Ocean,
(b) the Mediterranean Sea, (c) the Pacific Ocean, and (d)
the Atlantic and Mediterranean together. Lines shown are
best-fit lines by least squares regression with equation and
correlation coefficient (r).
COVA) was used to compare regressions of
Carapace Width (CW) against Carapace
Length (CL) for the same three categories of
crab populations (Fig. 3). There is a significant difference between the regression coefficients of Atlantic (Fig. 3a) and Mediter-
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Fig. 4. Canonical analysis. A plot of the first discriminant function (Root 1) against the second (Root 2), depicting
any discrimination by biometric measurements of Carcinus grouped into the Pacific Ocean, Atlantic Ocean, and
Mediterranean Sea regions.
ranean (Fig. 3b) combined data sets (ANCOVA: Fs = 853; 1,691 d.f.; P < 0.001), and
between each of these and that of the Pacific
population (Fig. 3b) (Fs = 13.7; 1,332 d.f.; P
< 0.001 for Atlantic; Fs = 175; 432 d.f.; P <
0.001 for Mediterranean comparisons). Figure 3d shows the data sets for the Atlantic and
the Mediterranean on the same graph, emphasizing that, even though the regression coefficients differ significantly, individuals from
the Atlantic and Mediterranean populations
are not well separated by consideration of the
relationship between carapace width and carapace length alone.
A discriminant function analysis was therefore carried out using all the biometric data
collected in order to discover whether the
crab populations of the three areas could be
distinguished morphometrically. All data
were transformed logarithmically to increase
their fit to normal distributions, and the data
set was subjected to canonical analysis. Results of the canonical analysis of the sample
data grouped into the three areas Pacific, Atlantic, and Mediterranean are shown in Fig.
4. Discrimination between the groups was
very highly significant (Wilks’ lambda 0.31,
Fs = 111; 20, 2,800 d.f.; P < 0.001). The variables in the order in which they entered the
model are listed in Table 2; two discriminant
functions (roots) account for 100% of the explained variance. The first discriminant function (root 1) accounted for 95% of the explained variance and was weighted most
Table 2. Standardized coefficients for canonical variables of the multiple group discriminant analysis of biometric data for Carcinus grouped into Pacific, Atlantic,
and Mediterranean regions.
Variable
Carapace Width
Carapace Depth
Length of Left Chela
Optical Groove Width
Length of Right Chela
Length of Propodus of
Left Chela
Depth of Right Chela
Length of Propodus of
Right Chela
Carapace Length
Depth of Left Chela
Eigenvalue
Cumulative Proportion
Root 1
Root 2
–17.356
8.451
1.882
1.792
–2.032
2.464
–9.937
0.279
–2.056
2.368
7.319
5.873
2.243
–1.096
–2.161
1.578
4.550
–0.931
1.906
0.947
–3.647
0.089
0.107
1.000
CLARK ET AL.: BIOMETRIC ANALYSES OF CARCINUS
295
Fig. 5. Canonical analysis. A plot of the first discriminant function (Root 1) against the second (Root 2), depicting
any discrimination by biometric measurements of Carcinus from Southampton Water (Atlantic Ocean), Marseille
(Mediterranean Sea), and Pacific Ocean.
heavily by carapace width, followed by carapace depth, then carapace length (Table 2).
A plot of discriminant function (root) 1
against discriminant function (root) 2 (Fig. 4)
shows that Atlantic and Mediterranean crabs
are separated by root 1, while root 2 separates
Pacific from Atlantic and Mediterranean
crabs. Despite the significant differences between the statistical populations of data representing the three geographical areas, there
is still some overlap of individual crabs. Thus,
no individual crab can be assigned unambiguously to a particular geographical area on
the basis of these linear measurements alone.
Earlier authors have compared populations
of crabs from the Atlantic and Mediterranean,
taken from sites very far apart geographically.
A further canonical analysis was therefore
carried out on the biometric data of the
Southampton Water population (sample 9)
representing the Atlantic against the Marseille
population (sample 22) representing the
Mediterranean, with the Pacific population
(sample 1) also included. As shown in Fig.
5, there is still overlap between Atlantic and
Mediterranean crabs, confirming that even
geographically well-separated populations of
Atlantic and Mediterranean crabs cannot be
unequivocally separated by biometric analysis.
Given that in the canonical analysis of the
data grouped into the three regions (Fig. 4),
carapace depth was given more weight in the
first discriminant function than carapace
length (both after carapace width), it was decided to plot carapace width against carapace
depth in an attempt to seek better discrimination between Atlantic and Mediterranean
populations than seen in Fig. 3. Figure 6
therefore shows these regressions for data for
crabs from the Atlantic (Fig. 6a), the Mediterranean (Fig. 6b), and the Pacific (Fig. 6c). The
regression coefficients for carapace width
against carapace depth for Atlantic and
Mediterranean crabs differ significantly (ANCOVA Fs = 1,808; 1,693 d.f.; P < 0.001), and
Fig. 6d shows better, but by no means complete, separation of these crabs than did Fig.
3d. The same regression coefficient for Pacific crabs (Fig. 6c) differs significantly from
that for both Atlantic (Fs = 36.5; 1,333 d.f.;
P < 0.001), and Mediterranean crabs (Fs =
532; 433 d.f.; P < 0.001).
Figure 7 shows the carapace width/cara-
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 1, 2001
Fig. 7. Mean ratios (± 1 standard deviation, SD) of carapace width (CW) to carapace depth (CD) of: (a) 26 samples of populations of Carcinus spp. as described in the
text. Sample 1 is from the Pacific Ocean, samples 2 to 18
from the NE Atlantic Ocean, and samples 19 to 26 from
the Mediterranean Sea; (b) of populations of Carcinus
grouped as Pacific, Atlantic, or Mediterranean in origin.
Fig. 6. Regressions of carapace width against carapace
depth of individual crabs from (a) the Atlantic Ocean,
(b) the Mediterranean Sea, (c) the Pacific Ocean, and (d)
the Atlantic and Mediterranean together. Lines shown are
best-fit lines by least squares regression with equation and
correlation coefficient (r).
pace depth ratio for each separate population
(Fig. 7a), and for the three combined populations (Fig. 7b). The pattern of ratios in Fig.
7b is similar to that in Fig. 2b, with an even
greater discontinuity apparent between Atlantic (2 to 18) and Mediterranean (19 to 26)
populations. The CW/CD ratios for Atlantic
and Mediterranean crabs are significantly different (ANOVA of log-transformed data: Fs
= 1,695; 1,694 d.f.; P < 0.001), but the ratio
also differs significantly between the separate
populations of Atlantic crabs (Fs = 11.8;
1,282 d.f.; P < 0.001) and between populations of the Mediterranean crabs (Fs = 6.13;
390 d.f.; P < 0.001). The CW/CD ratio for
Pacific crabs is also significantly different
from the Atlantic (Fs = 22.0; 1,334 d.f.; P <
0.001) and Mediterranean (Fs = 572; 434 d.f.;
P < 0.001) ratios (Fig. 7b).
Cheliped Setae.—The presence or absence of
setae on the frontal distal margin of the cheliped carpus was first described as a character for separating English Channel and
Mediterranean Carcinus specimens by Demeusy and Veillet (1953). This character was
CLARK ET AL.: BIOMETRIC ANALYSES OF CARCINUS
297
Fig. 8. Putative Carcinus maenas (Linnaeus, 1758); right cheliped a, c, e; left cheliped b, d, f; a, b—Bodega Bay,
United States, East Pacific Ocean, male cw = 48.9 mm, NHM reg. 2000.166–199; c, d—West Runton, England,
North Sea, NE Atlantic Ocean, male cw = 43.2 mm, NHM reg. 1996: 1413–1422; e, f—Estuario do Mira, Portugal;
NE Atlantic Ocean; male cw = 51.4 mm, NHM reg. 1989: 246.
illustrated by Rice and Ingle (1975, pl. 1C, F)
when they compared chelipeds of crabs from
Brighton, England, and from Salammbo,
Tunisia. These cheliped setae were studied
during the present study (Figs. 8a–f, 9a–f).
All crabs examined from Mallorca, Spain;
Marseille, France; Carthage Harbour, Ebro
delta, Spain; Tunisia; Marano Lagoon, Italy;
and Istanbul, Turkey, possessed prominent setal brushes along the carpodal/propodal margin of the cheliped. Setal brushes were also
observed in NHM-registered specimens from
Tokyo, Japan. These cheliped setae were absent in all crabs from the following locations:
Bodega Bay, United States; Shetland, Scotland; Upper Loch Torridon, Scotland; Fjord
Fyn, Denmark; Menai Bridge, North Wales;
County Cork, Ireland; Norfolk, England;
Fawley, England; Rés de Rochefort, France;
and Porto, Portugal. However, a small number of Carcinus specimens from Ria de
Aveiro, Portugal; Estuario do Mira, Portugal
(see Fig. 9e, f); Vila Nova de Milfontes, Portugal; Palmones Estuary, Spain; Europa Point,
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 1, 2001
Fig. 9. Putative Carcinus aestuarii Nardo, 1847; right cheliped a, c, e; left cheliped b, d, f; a, b—Ebro Delta, Spain,
Mediterranean Sea, male cw = 49.6 mm, NHM reg. 1999: 18–27; c, d—Istanbul, Turkey, Sea of Marmara, Mediterranean Sea, male cw = 47.6 mm, USNM reg. 57416; e, f—Tokyo Bay, Tokyo, Japan, West Pacific Ocean, male cw
= 40.3 mm, NHM reg. 1995: 854–856.
Gibraltar and Sandy Bay, Gibraltar, had chelipeds where the carpodal/propodal margin
was slightly setose. This setation varied both
within and between these latter populations
but was never as dense as the brushes observed from Mediterranean specimens from
Mallorca or east of Mallorca.
Pleopod Morphology.—Scanning electron
micrographs of the tips of the pleopods of
male crabs from West Runton, England, and
Tunisia are depicted in Fig. 10a, b. As can
be seen, there are no clear distinguishing features between the two.
DISCUSSION
Biometric analyses have shown that there
is a negligible probability (P < 0.05) that the
measurements from crabs grouped into Atlantic, Mediterranean, and Pacific areas were
CLARK ET AL.: BIOMETRIC ANALYSES OF CARCINUS
299
Fig. 10. Carcinus male pleopod tips. Ventral view: a) putative Carcinus maenas (Linnaeus, 1758); cw = 40.3 mm,
NHM reg. 1996: 1413–1422, West Runton, England, North Sea, NE Atlantic Ocean; b) putative Carcinus aestuarii
Nardo, 1847; cw = 40.6 mm, NHM reg. 1999.18–27, Ebro Delta, Alfacs Bay, Spain. Dorsal view: c) putative Carcinus maenas (Linnaeus, 1758); cw = 50.5 mm, NHM reg. 1996: 1413–1422, West Runton, England, North Sea, NE
Atlantic Ocean; d) putative Carcinus aestuarii Nardo, 1847; cw = 50.2 mm, NHM reg. 1999.18–27, Ebro Delta, Alfacs Bay, Spain.
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 1, 2001
drawn from the same statistical population.
Thus, in the specific comparison of the data
sets from the Atlantic and Mediterranean
crabs, there are two different statistical populations and these are apparently partitioned to
the two geographically defined areas.
Data for individual crabs from the Atlantic
and Mediterranean do overlap, both when
considering the ratios of carapace width to
carapace length and carapace width to carapace depth, and when analysing the biometric data sets as a whole. It is not possible,
therefore, to assign unambiguously an individual crab to either the Atlantic or Mediterranean populations on the basis of biometric
measurements.
Morphometric differences between populations of the same species are not unexpected
even when the organism concerned has a
planktonic larval stage, as is the case for
Carcinus. Henderson et al. (1990), for example, used a morphometric analysis to identify six distinct populations of the decapod
crustacean Crangon crangon (Linnaeus,
1758) in English and Welsh waters, suggesting that the populations are to some degree
isolated by the reduced dispersal of planktonic larvae across fronts. The morphometric differences did not, however, constitute a
case for the erection of different species.
Atlantic and Mediterranean specimens of
Carcinus could not be separated on the structure of the male pleopod. The presence or absence of setae on the frontal distal margin of
the cheliped carpus did, however, vary geographically. Crabs from the Mediterranean
possessed prominent setal brushes in this position, whereas crabs from the Atlantic north
of (and including) Porto in Portugal lacked
any such cheliped setae. Crabs from the other
Portuguese sites, from the Palmones estuary
in southern Spain, and from Gibraltar did,
however, sometimes have a few setae (never
a dense brush) on the cheliped carpus. This
observation indicates a lack of complete genetic separation of the Atlantic and Mediterranean populations of Carcinus.
The remark by Rice and Ingle (1975: 118)
“that there is no very good larval evidence
to support the separation of maenas and
mediterraneus as distinct species” requires
comment. Christiansen (1973) and Clark
(1983, 1984) found that chaetotaxy of congeneric species is identical. Furthermore,
Clark (1983) and Ng and Clark (2000) have
shown that incongruences in setal patterns
within taxa are indicative of systematic misplacement. Therefore, the expectation that
differences in zoeal morphology provide support for species-level discrimination is unfounded.
Since setting out on this morphometric
analysis, the authors of this study have become aware of the work of Bulnheim and
Bahns (1996) and Geller et al. (1997).
Bulnheim and Bahns (1996) addressed the
same question using starch gel electrophoresis for 19 allozyme loci in specimens of
Carcinus from nine sites covering a similar
geographical range to those in this study.
These authors found that there was full identity between Atlantic C. maenas and Mediterranean C. aestuarii for the banding patterns
of all but two loci. The genetic identity was
about 0.89; Bulnheim and Bahns (1996) concluded that the Atlantic and Mediterranean
crabs should not be designated as separate
species of Carcinus but that a taxonomic classification of subspecies is appropriate. Geller
et al. (1997), using molecular techniques,
found distinct mitochondrial 16S rDNA haplotypes corresponding to Atlantic and
Mediterranean populations of Carcinus. By
comparison with the degree of molecular differences between established species of the
crabs Menippe and Callinectes, Geller et al.
(1997), on the other hand, concluded that the
genetic differences observed in Carcinus were
sufficient to support the specific separation of
C. maenas in the Atlantic and C. aestuarii in
the Mediterranean. The Spanish sites investigated, Rio de Batanzos and Cadiz, are just
to the west of Gibraltar, and crabs from these
sites were clearly of the Atlantic type; the two
Mediterranean sites, Banyul-sur-mer (France)
and Naples (Italy) are well into the Mediterranean itself. Geller et al. (1997) noted that
their data were consistent with other data for
the bivalve molluscs Mytilus galloprovincialis Lamark, 1819 (see Quesada et al.,
1995) and Ostrea edulis Linnaeus, 1758 (see
Saavedra et al., 1995), indicating phylogeographic breaks in both cases near Almeria in
Mediterranean Spain, near the point where intruding Atlantic water is deflected offshore at
Cabo de Gata (Hopkins, 1985).
The biometric analysis completed here detected significant differences in the data sets
of measurements assigned to crabs from the
two geographical areas, the Atlantic and the
CLARK ET AL.: BIOMETRIC ANALYSES OF CARCINUS
Mediterranean. The biometric analysis in itself does not allow the conclusion that these
differences in shape are sufficient to conclude
that there are two separate species present,
and indeed individual crabs cannot be assigned unequivocally to one group or the
other on the basis of shape. The data on the
presence or absence of setae on the cheliped
carpus indicate a lack of complete genetic
isolation of Atlantic and Mediterranean populations, in effect the existence of a hybrid
zone between Atlantic and Mediterranean
crabs, as indeed do the results of the electrophoretic study by Bulnheim and Bahns
(1996). Given the geographical area covered,
it is not surprising that gene flow is reduced
and that differences in characters appear between Mediterranean and Atlantic crabs
(Bulnheim and Bahns, 1996). From both the
data presented here and those of Bulnheim
and Bahns (1996), it appears that the major
discontinuity in gene flow lies in the sea region between Gibraltar and Barcelona, possibly at the same point near Almeria for Atlantic and Mediterranean populations of
Mytilus galloprovincialis (see Quesada et al.,
1995) and Ostrea edulis (see Saavedra et al.,
1995). The authors of this present study look
forward to the opportunity to explore this
area in more detail at an entirely appropriate time of year.
The morphological data do not unequivocally support the separation of European
Carcinus into two distinct species, but additional genetic data are needed to verify the
presence of any real gene flow and a hybrid
zone between Atlantic and Mediterranean
crab populations.
ACKNOWLEDGEMENTS
This paper is dedicated to the memory of Arthur
Humes, in acknowledgement of his contribution to The
Crustacean Society and to research into the biology of
copepods associated with marine invertebrates.
We acknowledge a number of good friends who either collected or helped to collect Carcinus material
specifically for this study. These include members of The
Natural History Museum Diving Unit (Nick Evans and
Brian Pitkin), Awantha Dissanayake, Pierre Noël, Darren Fa, Pere Abelló, Ted Grosholz, Poul Bjerregaard,
David Davis, Damián Jaume, Henrique Queiroga, and
Carlo Froglia. We also thank José Paula and Ray Manning for organizing loan material for us to examine. We
thank Philip Tubbs of the International Commission on
Zoological Nomenclature for discussions with regard to
the availability of the name Carcinus aestuarii. We wish
to thank Harry Taylor (Figs. 8, 9) and Kevin Webb (Fig.
10) (both NHM photo unit) for taking the photographs reproduced in this paper, and Roger Bamber and Norman
301
Macleod for advice on statistical analysis. We are also
grateful to Brian Smith for his help and patience with statistical software. Two members of the Electron Microscopy Unit (NHM), Chris Jones and Alex Ball, gave
us considerable support and advice during scanning electron microscopy. We also much appreciate the constructive comments of Ted Grosholz which have much improved the manuscript.
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RECEIVED: 22 May 2000.
ACCEPTED: 6 September 2000.
ANNOUNCEMENT
Summer 2000 Best Student Presentation Awards
The Crustacean Society recognized five student presentations at the Summer Meeting which
was held in Puerto Vallarta, Mexico, during June 26–28, 2000. The award for Best Student
Oral Presentation went to Ms. Lisa Rodrigues from the University of Toronto, Ontario, Canada,
and the Bermuda Biological Station for Research, St. George’s, Bermuda [David Dunham
and Kathryn Coates, co-authors] for her paper entitled, “Shelter preferences in the endemic
Bermudian hermit crab, Calcinus verrillii.” The award for Best Student Poster went to Ms.
Renata Bingi Garcia from the University of São Paulo, Ribeirao Preto campus, Brazil [Fernando Luis Medina Mantelatto, co-author] for her poster entitled, “Shell preference of the
hermit crab, Calcinus tibicen (Anomura: Diogenidae) from Ubatuba Region, Brazil.” Each
of the above award winners will receive a certificate, a free one-year membership in TCS
(which includes a subscription to the Journal of Crustacean Biology), and a cash award of
$50.00 from the society.
In addition, the following three presentations were given honorable mention recognition.
Mr. Cristian Correa from the Universidad Catolica del Norte, Coquimbo, Chile [Juan A. Baeza,
Ivan Hinojosa, and Martin Thiel, co-authors] for his oral presentation entitled, “Mating hierarchy and mating tactics in rock shrimp”; Ms. Adriana Corona from the Universidad Nacional Autonoma de México [= UNAM], México D.F. for her poster entitled, “Mesograsser
selection by the pink shrimp Farfantepenaeus duorarum”; and Ms. Carmen Hernandez also
from UNAM [Fernando Alvarez, co-author] for her poster entitled, “Intertidal crustacean diversity and abundance in Montepio, Veracruz, Mexico.”
In an extremely generous gesture, the Instituto de Biología of UNAM presented to all award
winners and honorable mentions six colored prints of Mexican plants and animals in danger
of extinction by Elvia Esparza as well as the following books: Utilizacion y Conservacion
de los Ecosistemas Terrestres de México by A. Challenger; Los Cangrejos Braquiuros del
Pacífico Mexicano by M. Hendrickx; Anfibios y Reptiles de las Serranías del Distrito Federal, México by Z. Uribe-Peóa et al.; Biodiversidad, Taxonomía y Biogeografía de Artropodos de México by J. Llorente et al.; and Diversidad Biologica de México: Orígenes y Distribucion by T. P. Ramamoorthy et al.