19
Revised for Journal of Shellfish Research September 6, 2001
Field identification
of
the European Green crab species:
Carcinus maenas (Linnaeus, 1758)
and
C. aestuarii Nardo, 1847
Sylvia Behrens Yamada
and
Laura Hauck,
Zoology Department,
Oregon State University
Corvallis, Oregon 97331-2914
U.S.A.
Telephone: 541-737-5345
FAX: 541-737-0501
e-mail:
ABSTRACT. Adults of the global invaders, Carcinus maenas (Linnaeus, 1758) and C. aestuarii Nardo, 1847, can generally be distinguished in the field by three diagnostic characteristics: the shape of the copulatory appendages (pleopods) in the male, the shape of the frontal area between the eyes and the carapace width to length ratio. The pleopods of male C. maenas are crescent–shaped and curve outward with the center of the crescents touching; those of C. aestuarii are straight and parallel to one another. The frontal area of C. maenas does not protrude and is bordered by three scalloped-shaped lobes with distinct bumps. The frontal area of C. aestuarii is flat without distinct bumps and protrudes beyond the eyes. The carapace width to length ratio of adult crabs is typically > 1.29 for C. maenas and < 1.27 for C. aestuarii.
KEY WORDS: Carcinus maenas, Carcinus aestuarii, sibling species, invasive species, green crab.
Introduction
The European green crab, a native to Europe and North Africa, is receiving much attention lately because of its success as a global invader. Established breeding populations outside its native range are currently found in Japan, South Africa, Australia, Tasmania and on both the east and west coasts of North America (Le Roux et al. 1990, Grosholz and Ruiz 1995, Cohen et al. 1995, Furota et al. 1999).
Two forms of the green crab are now recognized: the Atlantic Carcinus maenas and the Mediterranean C. aestuarii, (old name Carcinus mediterraneus Czerniavsky, 1884) (Demeusy and Veillet 1953, Demeusy 1958, Holthuis and Gottlieb 1958, Almaça 1961, Zariquiey Alvarez 1968, Bulheim and Bahns 1996 and Geller et al. 1997). The Strait of Gibraltar, with its high sill, acts as a partial barrier to larval and gene exchange. Consequently, Mediterranean populations of many marine organisms, including the green crab, diverged from their Atlantic counterparts (Demeusy and Veillet 1953, Barsotti and Meluzzi 1968, Almaça 1989, Quesada et al.1995, Saavedra et al.1995, Bulnheim and Bahns 1996, d’Udekem d’Acoz 1999). There is evidence, however, of some mixing of Carcinus populations near the Strait of Gibraltar (Almaça 1961, Clark et al. 2001, Armand Kuris, unpublished observation).
Within the last two centuries, Carcinus has been accidentally introduced to several regions outside its native range as a result of maritime commerce and ballast transport: Carcinus maenas to the east and west coast of North America, Australia, Tasmania and South Africa; and C. aestuarii to Japan (Almaça 1962, Geller et al. 1997). Since Carcinus spp. tolerate air exposure, starvation and wide ranges in temperature and salinity, they are well adapted to survive ocean voyages and plane rides. Furthermore, the free-swimming larvae have the potential to survive within the ballast tanks of cargo ships. Once released into a new environment, these ecological generalists can subsist on a variety of food organisms including marsh vegetation, algae, crustaceans, mollusks and fish (Cohen et al. 1995). Under favorable conditions both species can reach sexual maturity within one year (Grosholz and Ruiz 1995, Furota et al. 1999, Behrens Yamada and Hunt 2000). The planktonic larvae produced by colonists can travel on ocean currents and “seed” new breeding populations elsewhere (Behrens Yamada and Hunt 2000). Marine scientists, resource managers, shellfish growers and members of the general public are concerned that these invaders may adversely affect marine communities by altering food webs, disturbing habitats, displacing native species and preying on commercially important clams, mussels, oysters and juvenile native crabs.
When a green crab is sighted in a new geographical area, it is important to rapidly confirm its identity, its source and mode of introduction. Once a vector has been identified, steps can be taken to prevent further individuals from arriving. If the numbers of a new invader can be kept below a critical threshold, a self-perpetuating population may not establish itself. Time is thus paramount in identifying the invader’s origin. While it may be possible to identify the most likely source of a new green crab invader with genetic tools (Bulnheim and Bahns 1996, Geller et al. 1997, Bagley and Geller 2000), these procedures take time and resources to implement. We propose that a fast, simple field identification method be used to identify which Carcinus species is actually invading.
Green crabs can be distinguished from other crabs in Europe and North America by their fan-like shaped carapace, five prominent, sharp anterio-lateral teeth behind the eyes and three lobes between the eye sockets (Figure 1, Crothers and Crothers 1988). Distinguishing the Atlantic from the Mediterranean species, however, takes closer inspection. Various studies have focused on green crab species identification, but these references are not readily available to most English-speaking scientists and resource managers because they are dated and/or published in Spanish, French and Portuguese journals. Our goals are: 1) to list all the distinguishing characteristics described in the literature and 2) to evaluate the usefulness of each in a field setting. The latter was accomplished by examining preserved museum specimens from collection sites in the Mediterranean and Atlantic and fresh specimens from Oregon.
Materials and Methods
We compiled the literature on green crab species identification and created a list of characters that could potentially be useful for distinguishing Carinus maenas and C. aestuarii (Table 1). In addition, Dr. Toshio Furota kindly sent us his unpublished observations on the physical characteristics of C. aestuarii from Shinhama lagoon in Tokyo Bay Japan.
In order to evaluate the usefulness of each morphological feature in field identification, we obtained preserved specimens of similar size male Carcinus maenas and C. aestuarii from the Smithsonian Museum of Natural History. Collection sites included Vlissingen, Netherlands, Chausey Islands in the English Channel, Rabat, Morocco, Tunis, Tunisia and Marsala, Sicily (Figure 2, Table 3). To supplement these samples, we collected live specimens from Yaquina Bay, Oregon using baited and pitfall traps. For each specimen we prepared a data sheet and noted which of the characteristics in Table 1, could be used as a diagnostic tool in a field setting. For a feature to be useful, it had to be visible to the naked eye (or through a hand lens) and measurable with vernier calipers.
Table 1. Morphological features useful for distinguishing Carcinus maenas and C. aestuarii in the field. 1=Demeusey and Veillet 1953, 2=Demeusy 1953, 3=Demeusy 1958, 4=Almaça 1961, 5=Zariquiey Alvarez 1968, 6=Almaça 1972, 7=Rice and Ingle 1975, 8=Rasmussen 1973, 9=Noël 1992, 10=Furota 1999, 11=G. Jensen and C. Hieb, unpublished data, 12=Clark et al. 2001, 13=this study.
Feature
/ Carcinus maenas / Carcinus aestuarii / CommentsNative Distribution
4, 5 / Western Baltic, North Sea, Atlantic from Norway and Iceland to Morocco and Mauritania / Mediterranean, Black Sea, Asow Sea / Yes, for specimens within native range, (some mixing near Strait of Gibraltar).
Male pleopods
(copulatory appendages)
4, 5, 9, / Crescent-shaped, touch at the bend / Parallel and straight, don’t touch / Yes, Figure 1
(Fig. 115 in 5)
Posterior (5th) pair of teeth of anterio-lateral region of carapace
3, 5, 7, 13 / Appear to point forward / Appear to slant outward, tooth and central rib are elevated / Mostly, Figure 2,
Teeth of some Atlantic specimens also slants outward (4)
Posterior-lateral margin of carapace
13 / Straight or convex /
Concave
/ Mostly, Figure 2,But margin was concave in Atlantic specimen from Rabat, Morocco.
Carapace width to length ratio (CW/CL) for crabs ³ 20 mm
5, 6, 7, 9, 12, 13 / Wider carapace
1.29 – 1.36 / Narrower carapace
1.22 – 1.27 / Yes, Figure 2,
Tables 2, 3
Carapace width to depth ratio (CW/CD)
6, 12 / Thinner carapace
2.32 – 2.50 / Deeper carapace
2.19 – 2.26 /
Shows great promise as a discriminator
Appearance of dorsal surface of carapace1, 3 / Smooth and uniform / Cardiac, hepatic and branchial regions divided by deep furrows; rough with hairy projections / Not noticeable for preserved specimens
(13)
Margin of frontal area (between the eyes)
3 / Few or no bristles / Three size classes of bristles line the border of the frontal area / No (4, 7)
Not noticeable for preserved specimens
(13)
Shape of three lobes in frontal area (between the eye sockets)
5, 7, 13 / 3 distinct “bumps”, margin scalloped, frontal area does not protrude / Flatter, “bumps” not as distinct, frontal area protrudes beyond eyes / Yes, Figure 2
(Figure 115 in 5, Plate 1 in 7)
Toshio Furota, un-published data
Segmentation of first antennae
3 / 5-6 segments / 4 segments /
No, feature varies with size of animal (4)
Second antennae3 / Fewer segments / Longer, more segments / No (4)
Orientation of teeth at the base of the second antennae
3 / On ventral side / On dorsal side / No (4)
Outer margin of claws 3 / Smooth / Hairy with bumps / No (13)
Tooth on inside of carpal
5 / Blunt / Sharp / No, (7, 13)
Presence of a fringe of long hair on the carpal (“wrist”segment) of claw.
3 / No / Yes / No, some Atlantic specimens also possess this feature (4)
Length of legs / Shorter / Longer and more slender / Possibly, Figure 2,
(Figure 115 in 5)
No (4)
Abdomen of same sized immature females
2 / Narrower / Wider (mature at a smaller size) / No, would be difficult to quantify
Carapace width of female in last pre-puberty stage
2 / 22.5 mm / 14 mm / No, great variability
(d’Udekem d’Acoz, unpublished data)
Carapace width of females after puberty molt
2 (estimate based on 35% growth increment with molt) / 28-30 mm / 16-19 mm / No, in Portugal ovigerous female C. maenas can be 15 mm and smaller (Kuris, unpublished data)
Maximum carapace width
5, 8, 10, 11 / > 90 mm / 65 mm / No, maximum size is not reached in many locations.
Results
Demeusy and Veillet (1953) and Demeusy (1953, 1958) draw attention to a suite of characters that distinguish green crabs from the Atlantic and Mediterranean coasts of France (Table 1). They obtained specimens from Sète in the Mediterranean and from La Manche (the English Channel) and Roscoff on the Atlantic (Figure 2). They note that Mediterranean crabs are generally smaller, hairier and possess a narrower and thicker carapace than Atlantic crabs. Almaça (1961) expands this comparative study by adding populations from the Spanish Mediterranean and the Spanish, Portuguese and French Atlantic coasts (Figure 2). While some of the characteristics were conserved across the larger sampling area, others, such as the distribution of hair on the carapace, frontal areas and claws, carapace texture and the number of segments on the antennae, were not (Table 1). Almaça (1972) observed carapace shape of Carcinus specimens from his former study areas as well as specimens from Australia and Maine and confirms that, in general, Atlantic specimens have wider and flatter carapaces than Mediterranean ones. He quantified these features as the carapace width to carapace length ratio (CW/CL) and the carapace width to depth ration (CW/CD). For example, CW/CL is defined as the distance between the tips of the 5th anterio-lateral teeth divided by the distance between the central lobe of the frontal area and the posterior border of the carapace. CW/CL in C. maenas (³ 20 mm) varied from 1.27 to 1.35 while that in C. aestuarii, from 1.24 to 1.27. The CW/CD for males ³ 20 mm was 2.27 – 2.57 for C. maenas and 2.25 – 2.31 for C. aestuarii (Table 5).
Zariquiey Alvarez (1968) provides a key for distinguishing the two species and includes photos of carapace shapes and male pleopods and a table of CW/CL for various size classes of both species and sexes (Table 2). The shape of the male pleopods is very diagnostic in separating adult Mediterranean from the Atlantic specimens (Figure 1, Tables 1, 3). When the abdomen of a male crab is lifted, the copulatory appendages, formed from the first two pairs of pleopods, become visible. The pleopods of C. maenas curve outward in a crescent shape with the centers of the crescents touching each other. Those of C. aestuarii form straight, parallel lines and don’t touch. While size and sex appears to affect relative carapace width, the difference in the CW/CL between the species (for crabs ³20mm) is significant: 1.30 – 1.35 for C. maenas and 1.23 – 1.27 for C. aestuarii (Table 2). Rice and Ingle (1975) confirm these species difference in CW/CL. The ratios for two female C. maenas from Plymouth, U.K. are 1.29 and 1.32 while that for a female C. aestuarii from Tunis, Tunisia is 1.25 (Table 5).
Table 2. Mean carapace width to length ratios (CW/CL) for male and female Carcinus maenas and C. aestuarii of various size categories. Numbers in brackets give sample size. Data taken from Zariquiey Alvarez 1968.
Carapace width / Male C. maenas / Female C. maenas /Male C. aestuarii
/ Female C. aestuarii0 – 10 mm / 1.200 (1) / 1.187 (5) / 1.176 (5)
10 – 20 mm / 1.272 (1) / 1.224 (2) / 1.281 (7)
20 – 30 mm / 1.354 (2) / 1.317 (5) / 1.252 (11) / 1.252 (9)
30 – 40 mm / 1.323 (10) / 1.304 (2) / 1.266 (16) / 1.259 (12)
40 – 50 mm / 1.348 (9) / 1.307 (1) / 1.247 (7) / 1.259 (1)
50 – 60 mm / 1.327 (2) / 1.298 (1) / 1.264 (1) / 1.227 (1)
Mean
(CW>20mm)
Range (CW>20mm) / 1.336
1.323 – 1.354 / 1.305
1.298 – 1.317 / 1.256
1.247 – 1.266 / 1.249
1.227 – 1.259
Clark et al. (2001) carried out the most statistically sound and geographically extensive study of carapace shape in Carcinus. They sampled 17 populations from the Atlantic, one from California and 8 from the Mediterranean and measured carapace width, length and depth for a total of 1,737 specimens. While the carapaces of the Atlantic and California populations were significantly wider and thinner than those of from the Mediterranean, there was also great variation between and within populations of a region. For example, the mean carapace width to depth ratio for Atlantic populations varied from 1.27 to 1.32 and that for Mediterranean populations from 1.23 to 1.27. Standard deviations around the population means were over 0.02 (Table 5). The authors point out that it may not always be possible to correctly assign any one specimen to a species. They found less overlap in the mean carapace width to depth ratio: Atlantic populations varied from 2.32 to 2.50 and Mediterranean populations from 2.19 to 2.26 (Table 5).