A scanning electron microscopic study on the appendage morphology of Astacus leptodactylus (Eschscholtz, 1823) and Pacifastacus leniusculus (Dana, 1852) (Crustacea: Decapoda: Astacoidea)/ Estudio en microscopio electronico de barrido sobre el apendice morfologico del Astacus leptodactylus (Eschscholtz, 1823) y Pacifastacus leniusculus (Dana, 1852) (Crustacea: Decapoda: Astacoidea).
The signal crayfish, Pacifastacus leniusculus (Dana, 1852), is native to north-western North America inhabiting lakes, streams and rivers (Lowery & Holdich, 1988) as well as saline waters (Henry & Wheatly, 1988; Holdich et al., 1997). It is also tolerant to environmental extremes such as temperature and various pollutants (Firkins, 1993). Pacifastacus leniusculus is similar in many ways to Astacus astacus (Linnaeus, 1758) and consequently has proved popular alternative since the decline of the latter species due to the introduction crayfish plague into many Europe catchments (Holdich, 1999). The signal crayfish is identified by its red colour, and large robust chela including a white to turquoise patch on the claw gives this crayfish its common name. This North American crayfish has been introduced into many European watersheds.
The narrow-clawed crayfish, Astacus leptodactylus (Eschscoltz, 1823) is a native of Turkey and near East Europe. It occupies a similar niche to that of P. leniusculus. However, in addition to streams, rivers, lakes, and ponds, it also inhabits swamps. Thus, it is sometimes called the swamp crayfish (Cherkashina, 1975; Koksal 1988, Harlioglu & Harlioglu, 2004). Astacus leptodactylus is commercially exploited either as imports or from introduced populations distributed widely across Europe, exception of the Iberian Peninsula and Nordic countries (Harlioglu & Holdich, 2001; Holdich 2002; Skurdal & Taugbol, 2002). This species is identified by its long claws (mainly typical for males) and is commonly named the narrow-clawed or Turkish crayfish (Harlioglu, 1996).
Pacificastacus leniusculus and A. leptodactylus have become popular experimental animals. The Turkish crayfish has been subjected to biochemical, physiological and ecological studies where as physiology, ecology, reproduction and distribution have been subjects for P. leniusculus (Duvic & Soderhall, 1990; Firkins, 1993; Guan, 1995; Warner & Green, 1995; Harlioglu, 1996). The main reason for these researches is because the signal crayfish has been introduced into most European countries for aquacultural and wild-stocking purposes (Lowery & Holdich). However, in recent years there has been an increase in the number of studies concerning aquaculture and immunology of P. leniusculus as the species carries crayfish plague. Consequently, many investigators have concentrated on its immune system (e.g. Persson et al., 1987; Duvic & Soderhall; Aspan & Soderhall, 1991; Kopacek et al., 1993) and the implications for susceptible crayfish when this species has been translocated (Holdich & Reeve, 1991).
Descriptions of P. leniusculus and A. leptodactylus have been given in a few keys (Curra, 1967; Pennack, 1978; Laurent & Forest, 1979; Brodski, 1983; Gledhill et al., 1993; Vigneux et al., 1993) and Andrews (1907) illustrated the appendage structure of the signal crayfish. Recently, P. leniusculus was chosen as a model in the description of functional morphology of crayfish by Holdich & Reeve (1988), and Holdich (1992) also reviewed the early post-embryonic development of astacid, cambarid and parastacid crayfish. However, to date no scanning electron microscopic studies have highlighted the morphology and appendage structure of these two species in any detail.
Differences in the morphology and structure of mouthparts and pereiopods of crayfish are useful in classifying them for systematic purposes. For example, variations in the rostra, chelae, mandibles and third maxillipeds were used by Hobbs (1987) to classify species of Astacoides. Variations in chelae were also considered to determine taxonomic differences between Orconectes propinquus and O. obscurus by Tierney (1982). Morphological differences of the western North American crayfish species of Pacifastacus have been used to assign species into the subgenera Pacifastacus and Hobbsastacus (Bouchard, 1977).
Scanning electron microscopy has been used to study the external morphology of mouthparts, pereiopods and pleopods in a variety of decapod crustaceans. For example, the functional morphology of mouthparts and pereiopods has been observed in the Norway lobster Nephrops norvegicus by Farmer (1974) and the shrimp Atya innocous by Felgenhauer & Abele (1983); in the prawn Panaeus merguiensis by Hindley & Alexander (1978) and Alexander et al. (1980). Moreover, observations on the morphology and structure of feeding apparatus and distribution of setae in lobsters have mainly reported for Homarus americanus and H. gammarus (Solon & Cobb, 1980). In addition to these, there are also some studies on anostracan crustaceans. For example, Mura & Caldo (1993) have studied the structure of the molar surface of the mandibles in the shrimp Branchinella spinosa. A similar study has been carried out on brine shrimp by Tyson & Sullivan (1981).
The aim of the present study is to compare the differences and similarities in the morphology of appendages (rostrum, carapace, first pereiopod, second pereiopod, fourth pereiopod) and mouthparts (third maxilliped, second maxilliped, first maxilliped, mandible, maxillule and maxilla) of A. leptodactylus and P. leniusculus under the scanning electron microscope. In addition, the development of mouthparts in stage 1, 2 and 3 juveniles of the two species was also evaluated.
MATERIAL AND METHOD
Juveniles of different stages (first, second and third) and juveniles 12 mm in carapace length (CL) of P. leniusculus and A. leptodactylus were scanned. The samples were reared under laboratory conditions in clean containers instead of keeping them in concrete tanks which have a muddy floor would therefore make them dirty and unsuitable for photography. After individuals had moulted, they were sacrificed when their body became hard enough to dissect and before they lost any appendages. To sacrifice the samples, they were placed in a freezer for ten minutes. Then they were preserved in 70 percent alcohol.
Mouthparts and appendages were removed under a light microscope. After dissection, the selected body parts of 12 mm length (carapace) juveniles were air dried for approximately 12 hours at room temperature (18 [+ or -] 1 0C). Because the stage 1, 2 and 3 juveniles were too delicate to apply air drying technique, the critical-point drying technique was applied for them.
Then, the selected appendages were attached to aluminum stubs with silver colloidal paint and coated with gold using a Polaron Sputter Coating Unit E5100. Finally, to view the body parts the stubs were set up in a JSM-840 scanning electron microscope operated at either 10, 15 or 25 KV.
The terminology used is taken from Holdich & Reeve (1988). The segments of the appendages are named from attachment point as: coxa, basis, ischium, merus, carpus, propodus, and dactylus with a terminal unguis.
To show differences and similarities in the rostrum, carapace, second pereiopod, fourth pereiopod, third maxilliped, second maxilliped, first maxilliped and mandible between P. leniusculus and A. leptodactylus, 12 mm (carapace length) juveniles were compared. Third stage juveniles were also used to show differences in the first pereiopod (cheliped) between the two species. The development of stage 1, 2, 3 and 12 mm (CL) juveniles was also evaluated within and between the two species (except the maxilla of stage 1 juveniles).
Due to the delicate nature of the mouthparts and appendages of juveniles it proved sometimes very difficult to prepare them for scanning electron microscopy. Consequently, some of the photographs exhibit charging (brightness). In the description below only the differences and similarities which were apparent between the two species are described.
Differences and similarities in the morphology of appendages and mouthparts: Differences and similarities in the morphology of appendages and mouthparts were found between the species.
Rostrum and carapace. In general, the shape of the rostra in the two species is very similar. They taper to a point, but near the apex a sharp spine occurs on either side (long arrows in Fig. 1 for P. leniusculus and Fig. 2 for A. leptodactylus).
The sides of the rostrum of A. leptodactylus are bordered by a regular row of setae. This row of setae on the rostrum of P. leniusculus is not as regular as that of A. leptodactylus. (see short arrows in Fig. 1 for P. leniusculus and Figure 2 for A. leptodactylus).
Although both species have pairs of post-orbital ridges on each side of the rostrum, A. leptodactylus also has a prominet tubercle on shoulder of carapace (see arrow in Fig. 4); this is absent in P. leniusculus (Fig. 3).
Mandible. There are more teeth on the incisor lobe of the mandible of P. leniusculus (see arrow in Fig. 39 for P. leniusculus and Fig. 40 for A. leptodactylus).
Maxillue. The length of setea on the protopod of P. leniusculus is greater than that of A. leptodactylus. In addition, unlike P. leniusculus, in A. leptodactylus the tip of the protopod of the maxillule has long setae (arrows in Fig. 47 for P. leniusculus and Fig. 48 for A. leptodactylus).
Maxilla. Setea on the edge of the protopod lobes are present in A. leptodactylus. These setea are not present on the protopod lobes of P. leniusculus (see arrows in Fig. 55 for P. leniusculus and Fig. 56 for A. leptodactylus).
First maxilliped. A difference occurs in the length of setae on the exopod. Bigger setae are present on the exopod of P. leniusculus (Fig. 31 for P. leniusculus and Fig. 32 for A. leptodactylus).
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Second maxilliped. Compared to A. leptodactylus, more abundant and very close setae are present on the endopod of P. leniusculus (see arrows in Fig. 23 for P. leniusculus and Fig. 24 for A. leptodactylus).
Third maxilliped. A spine is present on the second and third segments of the third maxilliped in A. leptodactylus (see arrows in Fig. 13). These spines are not present in P. leniusculus (Fig. 14).
The number and distribution of teeth are also different on the crista dentata (first segment) of the two species. There are more teeth on the crista dentata of P. leniusculus (see arrows in Fig. 15 for P. leniusculus and Fig. 16 for A. leptodactylus).
Cheliped (first pereiopod). The gap between the dactylus and propodus of the cheliped is wide in A. leptodactylus and the margins are serrated. The gap is narrower in P. leniusculus and the inner edges of the dactylus and propodus are not so serrated (see arrows in Fig. 5 for P. leniusculus and Fig. 6 for A. leptodactylus).
There is a row of setae on the propodus of the cheliped in A. leptodactylus (see long arrows in Fig. 8), but there is no a row of setae on the cheliped in P. leniusculus (Fig. 7).
The carpus of P. leniusculus has setae, but that of A. leptodactylus has not. Also, the shape of the spine on the edge of the carpus is different in the two species, that of A. leptodactylus being much larger (Fig. 7 for P. leniusculus and Fig. 8 for A. leptodactylus, see short arrow).
Second pereiopod. A difference was found regarding the propodus and dactylus between the species. Although A. leptodactylus has an unguis at the tip of propodus and dactylus, this unguis does not appear in P. leniusculus (Fig. 9 for P. leniusculus and Fig. 10 for A. leptodactylus, see arrow).
Fourth pereiopod. More abundant setae are present on the ventral side of the propodus of A. leptodactylus than those of P. leniusculus (see arrow in Fig. 11 for P. leniusculus and Fig. 12 for A. leptodactylus).
Juvenile development of Pacifastacus leniusculus and Astacus leptodactylus: In addition to an increase in size, developmental changes in morphology in the feeding apparatus of P. leniusculus and A. leptodactylus were found between the stages (stage 1, stage 2, stage 3) and 12 mm (CL) juveniles. Differences between the stages were given in Figs. 17-22 for the third maxilliped, in Figs. 25-30 for the second maxilliped, in Figs. 33-38 for the first maxilliped, in Figs. 41-46 for the mandible, in Figs. 49-54 for the maxillae and in Figs. 57-60 for the maxilla of the two species.
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It was observed that differences mainly occur in the length and abundance of setea on the feeding appendages, and in the number and dimension of teeth on the mandibles and the crista dentata of the third maxillipeds.
The increase in the number and dimension of teeth on the mandible of P. leniusculus as the crayfish moults are shown in Figs. 45, 43, 41, 39, and those of A. leptodactylus are given in Figs. 46, 44, 42, 40. Similarly, the increase in the number and dimension of teeth on the crista dentata of P. leniusculus as the crayfish moults are shown in Figs. 21, 19, 17, 15, and those of A. leptodactylus in Figs. 22, 20, 18, 16.
Presence of setae were found in the maxillipeds (first, second and third), mandible, maxillule, and maxilla of the two species (Figs. 37, 29, 21, 45, 53 for P. leniusculus, and Figs. 38, 30, 22, 46, 54 for A. leptodactylus respectively). Although setae were also seen in the maxilla of stage 1 P. leniusculus and A. leptodactylus, because of too much charging, they are not shown.
Pacificastacus leniusculus and A. leptodactylus are assigned to the Astacidae which contains only three genera: Astacus, Austropotamobius and Pacifastacus (Hobbs, 1988). Development in P. leniusculus and A. leptodactylus is epimorphic, i.e., it takes place within the egg, and what hatches out is similar to an adult (Holdich, 1992; Harlioglu, 2002). Consequently, P. leniusculus and A. leptodactylus are similar in their morphology and share many common features (Hobbs, 1988). Indeed, in the present study, similarities were observed in the morphology of appendages and mouthparts and in their setal armature between P. leniusculus and A. leptodactylus. For example, the shape of the rostra in P. leniusculus and A. leptodactylus is similar, and both species have two postorbital spines.
However, important differences in the morphology of appendages and mouthparts were found between P. leniusculus and A. leptodactylus. In addition, changes in the morphology in the feeding apparatus and appendages between the developmental stages of the two species were observed. For instance, the observations showed that A. leptodactylus has a prominent tubercle on the shoulder of carapace, which is absent in P. leniusculus. According to Harlioglu (1996) this prominent tubercle is a suitable character distinguish stage 2 juveniles of the two species under the light microscope. This spine is also present in Austropotamobius pallipes (but not in stage 2 of A. pallipes) (NRA, 1994).
It is well known that stage 1 juveniles are not active feeders (Thomas, 1970). Although stage 1 juveniles feed on the yolk, setae were found on all the maxillipeds (first, second and third), mandible, maxillule, and maxilla of the two species. Moreover, the differences in the setal armature of mouthparts as observed in the present study may lead to differences in the feeding behavior between P. leniusculus and A. leptodactylus. It seems that when the juveniles are feed the same diet P. leniusculus might have an advantage over A. leptodactylus because of its long and abundant setae on the second maxilliped, more teeth on the mandibles and crista dentata, and form of dactylus and propodus of the chelipeds. Similarly, from the observations described above it is clear that the increase in the number and dimension of teeth on the mandible and crista dentata of juveniles may enable them to cope with different types of food as they get older.
Food preference of crayfish has been subjected to several studies. The preference of two sizes of juvenile and an adult P. leniusculus in the consumption of aquatic weeds has been reported by Warner & Green. This preference is Spirogyra sp., Ceratophyllum demersum, Elodea canadensis or Groenlandia densa respectively for all three crayfish size groups. Warner et al. (1995) have also found that when different sizes of snails are offerred although larger P. leniusculus (55 and 61 mm CL) show no prefence, smaller P. leniusculus (16-44 mm CL) prefer to eat some sizes of snails more frequently than larger and smaller sizes, and smaller or larger snails are not eaten by the smaller P. leniusculus until prey abundance declines.
Momot (1995) is of the opinion that many crayfish species are primarily carnivorous. He bases this on the fact that they need animal protein to maintain their lifestyle and relatively fast growth rates in the summer months. He maintains that plant food is taken in secondarily or when animal food is not readily available. Indeed Guan found a high proportion of animal food items in the guts of P. leniusculus in his study of a wild population. Others have shown, however, that this species is effective at clearing nuisance weeds in water bodies (Blake & Laurent, 1982). It seems likely therefore that crayfish need to possess an array of setal types to cope with all eventualities. As P. leniusculus and A. leptodactylus are closely related and can occupy si milar environments it is not surprising that the setal armature of their appendages is comparable.
Harlioglu (2000) stated that the incisor ridge modification of mandibles may cause the difference in the food choice of different size crayfish, because different ridge structures of mandible may select different type of food. Harlioglu (2003) also stated that the differences in the crista dentate structure and different tooth number of the ischium of third maxilliped, as observed in the present study, cause a different cutting edge and variations in the food choice of crayfish.
Differences in mouthparts have also been found in penaeid prawns which fed on a wide range of food. It was observed that eleven species show food preferences out of 31 species. Moreover, food preferences were observed in the different stages of the same species due to the fact that they possess different mouthpart structures and setal types in their ontogeny (Hindley & Alexander).
In conclusion, important differences occur in the morphology of appendages and mouthparts between P. leniusculus and A. leptodactylus, and in the developmental stages of the species. The morphological differences in mouthparts may cause a difference in the feeding behavior and food choice of the species.
Many thanks are dedicated to my supervisor, Dr. David Holdich for his support and encourament during the course of this study. Thanks are also dedicated to Tim Smith for helping me learn to use the scanning electron microscope, to Brain Case for developing the photographs.
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Prof. Dr. Muzaffer M. Harlioglu
Fisheries Faculty, Firat University, 23119, Elazig
Tel(work): 0090 424 237 0000 ext: 4054
Fax: 0090 424 238 6287
This study is a part of PhD study of M.M. Harliog lu supported by Firat University Elazig, TURKEY.