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Current state of knowledge on Virilastacus species (Crustacea, Decapoda, Parastacidae)/Estado de conocimiento de las especies de Virilastacus (Crustacea, Decapoda, Parastacidae).

INTRODUCTION

At the beginning of the XX century, 10 species of the family Parastacidae had been described for South America, all grouped within one genus: Parastacus. Riek (1971) separated them into the genera Samastacus and Parastacus; he assigned two species [Parastacus spinifrons (Philippi, 1882) and Parastacus araucanius Faxon, 1914] to the genus Samastacus, in view of the following characteristics: P1 dactyls moving horizontally and phallic papillae being relatively long, articulated tubular projections. The other species, whose dactyls move vertically and phallic papillae are only small non-articulated protuberances, remained within Parastacus. Additionally, Riek (1971) characterized these genera in ecological terms: the Parastacus species as burrowers and inhabitants of underground waters, while the Samastacus species were characterized as weak burrowers, inhabiting rivers and lakes. After a period of 69 years, during which the only knowledge about Samastacus araucanius (Faxon, 1914) was based on the type specimen, Jara (1983) collected a second specimen, a male captured in the Botanical Gardens of the Universidad Austral de Chile (Valdivia), cohabitating with Parastacus nicoleti (Philippi, 1882). Rudolph & Rivas (1988) collected the third representative of this species, also a male in Hualqui (Concepcion) cohabiting with Parastacus pugnax (Poeppig, 1835). These discoveries provided sufficient evidence to exclude the occurrence of S. araucanius in open waters, as had been suggested in Faxon's (1914) description of the location where the type material was obtained: "in a waterfall in Corral". Based on this evidence, as well as on morphological differences [which were already mentioned by Jara (1983) and Rudolph & Rivas (1988)], Hobbs (1991) separated these two species into the genera Samastacus (S. spinifrons) and Virilastacus (V. araucanius); this author also provided diagnoses of the three South American genera of Parastacidae. Crandall et al. (2000) validated these three genera, based on the sequencing of 500 nucleotides of the 16S mitochondrial DNA gene in seven of the ten species of South American parastacids. Rudolph & Crandall (2005, 2007, 2012) described three new species of Virilastacus, extended their geographic range, and confirmed that all the species of this genus were burrowers. In the present review, the scarce information published on the Virilastacus species is compiled and systematized, together with other data available to the author, with the aim to update the biological knowledge about this species and, in turn, to promote effective conservation measures.

Family Parastacidae Huxley, 1879

Genus Virilastacus Hobbs, 1991

Diagnosis

Rostrum short. Carapace lacking spines, tubercules and postorbital ridges; anterolateral portion of branchio-cardiac groove clearly separated from the portion subparallel to cervical groove, which is located close to upper third portion of cephalothorax. Viewed dorsally, cervical groove V-shaped, except in V. retamali. Pleon lacking spines and tubercles; pleura of first abdominal segment distinct from and partly overlapped by that of the second abdominal segment. Telson without transverse suture and wholly calcified; posterior half with dorsomedian longitudinal groove. Ventral surface of ischipodite of third maxilliped bearing a median longitudinal band of tubercules; inside half of this surface with tufts of rigid setae; distolateral end of podomere rounded, except in V. jarai; merus lacking spines or tubercules; exopodite reaches distal end of merus. Caudal molar process of mandible quadricuspid in V. araucanius and V. jarai; tricuspid in V. rucapihuelensis and V. retamali; nodular cusp on proximal margin of cuspidal triangle. P1 chelae dimorphic, with almost completely tuberculated palms, but lacking spines or large tubercules; ventrolateral borders tuberculated to slightly subtoothed; carpus lacking large tubercules medially or ventrally, when upper surface held in a horizontal plane, dactyl moving obliquely in V. rucapihuelensis and V. jarai, and subhorizontally in V. araucanius and V. retamali. No occurrence of male and female gonopores in the same individual, except in V. rucapihuelensis. Male genitalia with a semi-rigid, tubular, thin, articulated, and very long phallic papilla extending forward from coxae in very close proximity to each other; lacking male cuticle partition, except in V. rucapihuelensis. Sternite XIII with an anterior medial plate, and posterior orifice. Viewed caudally, lateral processes of sternite XIV separated by a pronounced vertical fissure.

Type species. Parastacus araucanius Faxon, 1914: 553

Gender: Male

Etymology. From the Latin virilis = masculine; so-called because of its comparatively long phallic papilla (Hobbs, 1991; Rudolph & Crandall, 2012).

Virilastacus araucanius (Faxon, 1914) (Fig. 1a)

Common name: Dwarf crayfish

Synonymy

Parastacus araucanius Faxon, 1914: 353, pp. 4, Figs. 1-3; Van Straelen, 1942: 9; Holthuis, 1952: 84; Bahamonde & Lopez, 1963: 126 and 127, maps 1 and 2; Jara, 1983: R-163.

Samastacus araucanius Riek, 1971: 135; Manning & Hobbs, 1977: 159; Rudolph & Rivas, 1988: 73, Fig. 1; Hobbs, 1989: 80, Fig. 374; Buckup & Rossi, 1993: 167, Figs 11-13; Martinez et al., 1994: 9, Figs. 1-11.

Distinctive morphological characteristics

Cephalothorax smooth, coloration: olive green. Small eyes. Rostrum short, reaching distal end of middle podomere of antennal flagellum; dorsally excavated. Rostral carina long and slightly prominent. Cervical groove weakly "V" shaped. Areola narrow and extended. Antennal scale short with one small distolateral spine. Basal podomere of antennula lacking spines. Opposable margin of propodite without pilosity, bearing 11 to 18 teeth; dactyl moving sub horizontally, opposable margin bearing nine to 15 teeth. Individuals with female or male gonopores. Elongated phallic papilla reaches base of lateral process of XII body segment. In males, P5 coxae lack cuticle partition. Pleon coloration light brown. Telson subrectangular, dorsomedian longitudinal groove, and prominent spine on each lateral border (Faxon, 1914; Riek, 1971; Hobbs, 1991; Rudolph & Crandall, 2012). Species relatively small. The largest specimen caught is a female, measuring 28.7 mm cephalothorax length (CL) (74.8 mm total length). The smallest specimen collected is also a female, 18.3 mm CL (Martinez et al., 1994). In the case of males, maximum and minimum sizes recorded are 26.0 and 19.0 mm CL respectively (Faxon, 1914; Jara, 1983). A summary of distinctive morphological features of the four species of Virilastacus is provided in Table 1.

Geographic distribution

V, araucanius has been recorded from areas surrounding Concepcion (36[degrees]46'22"S, 73[degrees]03'47"W), Valdivia (39[degrees]48'30"S, 73[degrees]14'30"W), and Maicolpue (40[degrees]36'27,74"S, 73[degrees]44'01,44"W) (Faxon, 1914; Jara, 1983; Rudolph & Rivas, 1988; Hobbs, 1991; Martinez et al., 1994; Bahamonde et al., 1998). This discontinuous distribution may only be apparent, since it coincides with the presence of university research centers in these three areas (Jara et al., 2006). Nevertheless, recordings of V. araucanius in Maicolpue (Bahamonde et al., 1998) should be reviewed, given that they may correspond to specimens of either V. rucapihuelensis or V. retamali, described after the studies of Bahamonde et al. (1998), in a location (Rucapihuel) situated only 15 km from Maicolpue. Finally, recordings of V. araucanius suggest that it is distributed between the coast and the Coastal Cordillera mountain range; the extent of occurrence is estimated at 11.571,64 [km.sup.2] (Ministerio del Medio Ambiente, 2013 a).

Habitat

V. araucanius inhabits underground waters in topographic basins with evergreen lowland forest associations. Almost all recordings of this species occur in these biotopes, commonly referred to as "vegas" or "hualves" (Fig. 1b). Only the discovery of V. araucanius in the Botanical Gardens of the Universidad Austral de Chile in Valdivia (Jara, 1983; Hobbs, 1991) indicates its presence in flatter zones, subject to considerable anthropic intervention. Specimens of this species have also been found coexisting with P. nicoleti (Jara, 1994; Jara et al., 2006) in the same Botanical Gardens. A similar situation occurs in the locality of Hualqui (46[degrees]56'S, 72[degrees]55'W), where specimens of V. araucanius have been found cohabiting with P. pugnax (Rudolph & Rivas, 1988).

Burrow morphology

The burrows constructed by V. araucanius are shallow (<1 m), but quite complex, with multiple ramifications, many of them almost parallel to the surface, which complicates their capture, whether manually or by suction methods. In winter, V. araucanius constructs mud "chimneys" 2.0-6.0 cm high, located around the entrance orifices of their burrows (Jara, 1994) (Fig. 1c). According to the classification of burrowing crayfish proposed by Hobbs (1942), V. araucanius would be a primary burrower, since it builds complex burrows are not connected to permanent water bodies, and the entire life cycle of this species occurs inside the burrows.

Sexual system

Descriptions of external sexual characteristics, together with some anatomical analyses of gonads and gonoducts, suggest that V. araucanius is a gonochoric species. Adult females have ellipsoidal gonopores, partially surrounded by setae and covered by a non-calcified membrane. These characteristics, suggesting the occurrence of functional gonopores, are very similar to those observed in V. rucapihuelensis adult females (Rudolph et al., 2007). Males have an elongated, calcified phallic papilla ([bar.X] = 3.1 [+ or -] 0.4 mm; n = 12) and the respective gonopore opens at the apical end (Rudolph & Rivas, 1988; Hobbs, 1991; Martinez et al., 1994; Rudolph & Almeida, 2000).

Conservation status

Bahamonde et al. (1998) categorized V. araucanius as Insufficiently Known throughout its entire geographic range. Nevertheless, they warned that water pollution and substrate modification within its distribution area could cause negative effects on the conservation of these populations. Rudolph & Crandall (2007) classified the species as Vulnerable through its geographic distribution range, based on the B1ab (iii) criteria of the IUCN Red List (2001). Buckup (2010a) classified it as Data Deficient. The Ministerio de Medio Ambiente (2013a) described it as Vulnerable, in accordance with the B1ab (iii) + 2ab (iii) criteria of the IUCN Red List (2001). Finally, Almerao et al. (2014) also endorsed this latter categorization.

Virilastacus rucapihuelensis Rudolph & Crandall, 2005 (Fig. 2a)

Common name: Vega crayfish

Synonym: Virilastacus araucanius Rudolph & Rojas, 2003: 835, Figs. 1-8

Distinctive morphological characteristics

Cephalothorax with small tubercles only in anteroventral regions of branchiostegites. Small eyes. Rostrum short, reaching distal margin of basal podomere of antennal flagellum; dorsally concave. Rostral carina long and prominent. Epistome antero-median lobe resembles a triangle. Cervical groove "V" shaped. Basal podomere of antennula with small spine. Dorsal surface of P1 carpus with faint median groove, opposable margin of propodite bearing 5 to 9 teeth with pilosity on both sides, but only of their proximal group, dactyl moving obliquely. Abdominal pleura ventral margins almost straight. Individuals with supernumerary gonopores. In adult females, pleura of second pleomere with wide anteroventral flap, weakly calcified. Males with slightly elongated phallic papillae that reach the base of the P4 coxae. In males, P5 coxae with cuticle partition. Telson subrectangular, lateral margins almost parallel, each of them with a small, blunt spine. Light brown body coloration (Rudolph & Crandall, 2005, 2012). This species is slightly larger than V. araucanius. The largest specimen collected (33.6 mm CL) is an intersex individual in female phase and the smallest, a primary female with 4.4 mm CL (Rudolph et al., 2007) (Table 1).

Geographic distribution

This species has been reported from five nearby sites in the Coastal Cordillera of the province of Osorno, southern Chile: Rucapihuel (40[degrees]35'00.64"S, 73[degrees]34'42. 96"W), Coigueria (40[degrees]35'17.62"S, 73[degrees]32'10.00"W), Carrico (40[degrees]35'34.14"S, 73[degrees]31'19.70"W), Contaco (40[degrees]36'01.50"S, 73[degrees]31'00.97"W), and Loma de la Piedra (40[degrees]40'13.59"S, 73[degrees]30'51.42"W) (Rudolph & Crandall, 2005; Grosso & Peralta, 2009). The extent of their occurrence covers 39.3 [km.sup.2] (Ministerio de Medio Ambiente, 2013b).

Habitat

V. rucapihuelensis inhabits underground waters in biotopes locally called "vegas" or "hualves" (Rudolph & Crandall, 2005) (Fig. 2b). The soil profile of the "vegas" located in Rucapihuel includes two layers composed of fine clay sand. The upper layer comprises abundant iron oxides, the lower layer (80 cm below the soil surface) is of sandy gravel. In the winter, the phreatic level is close to or above the surface, and in summer, it descends as far as 1.0 or 1.5 m below the surface (Bedatou et al., 2010). After carrying out year-round monthly recordings of some physicochemical parameters of the water inside the burrows, Martinez (2005) verified that temperature fluctuated between 11 y 19[degrees]C, pH between 4.1 and 5.3, and dissolved oxygen between 2.6 and 6.5 mg [L.sup.-1]; on the other hand, total hardness remained constant at 17.8 ppm de CaC[O.sub.3].

Burrow morphology and burrowing behavior

The burrow morphology is variable. Some have several relatively complex entrance orifices (diameter 2.5-3.5 cm) with multiple ramifications in the subsoil. Some of these connected to a terminal chamber with a slightly larger diameter than the tunnel, situated between 1 and 1.2 m below the surface. Others are blind tunnels (Type 1 burrow, Fig. 3a). Other burrows have only one subvertical tunnel (3 to 4.5 cm diameter and up to 66 cm depth) with a few blind tunnels emerging from the uppermost section. The lower terminal section of this system is a sub-horizontal chamber with a slightly wider diameter than the tunnel (Bedatou et al., 2010) (Type 2 burrow, Fig. 3b). V. rucapihuelensis forms small pellets (8-10 mm maximum diameter) from the excavated material, and these pellets are deposited in the winter around the entry orifices of the burrows, forming "chimneys" of up to 12 cm height (Rudolph & Crandall, 2005) (Fig. 3c), these burrows are usually inhabited by one specimen; nevertheless, in spring-summer, it may be possible to find a female with a variable number of recently released juveniles in some of these burrows. According to Hobbs' (1942) classification, aspects such as excavating complex burrows, distanced from permanent water bodies, together with no recordings of specimens outside the burrows, suggest that this species can be considered as a primary burrower.

Sexual system

V. rucapihuelensis presents partial protandric hermaphroditism with primary males and females (Rudolph et al., 2007). Depending on the presence or absence of gonopores in the P3 and P5 coxae; externally, six sexual forms may be distinguished. Anatomical analyses of the gonads and gonoducts of these sexual forms enabled us to ascertain the presence of three basic sexual types: primary males, primary females, and intersex specimens. These latter comprise one malephase and two female-phase forms, that would originate from male-phase intersex individuals (Rudolph et al., 2007).

Fecundity

The species produced up to 74 eggs, incubated by a primary female of 27.9 mm CL. The lowest fecundity (three eggs) observed was in a primary female of 23.1 mm CL (Rudolph et al., 2007).

Conservation status

Rudolph & Crandall (2007), based on the B1 ab (iii) criteria of the IUCN Red List (2001), classified V. rucapihuelensis as Endangered in its entire distribution range, while Buckup (2010b) classified it as Data Deficient. The Ministerio de Medio Ambiente (2013b) classified it as Endangered, maintaining that it meets the B1 ab (iii) + 2ab (iii) criteria of the IUCN Red List (2001). Finally, Almerao et al. (2014) suggested that V. rucapihuelensis is Critically Endangered, considering that it falls within the B1 ab (iii) criteria associated with this category.

Virilastacus retamali Rudolph & Crandall, 2007 (Fig. 4a)

Common name: Peatland crayfish

Distinctive morphological characteristics

Precervical cephalothorax with four smooth ridges. Eyes comparatively large. Rostrum short reaches distal margin of middle podomere of antennal flagellum; dorsally concave. Rostral carina short and prominent. Cervical groove "U" shaped. Areola wide and short. Antennal scale long with large distolateral spine. Epistome anteromedian lobe resembling a rhombus. Basal podomere of antennula with large spine. Opposable margin of P1 propodite bearing 13 to 17 teeth, with pilosity on both sides of the row of teeth. Dactyl moving subhorizontally. Abdominal pleura with rounded ventral margins. Telson with converging lateral margins resembling a triangle, with prominent, sharp marginal spines. Individuals with female or male gonopores. Phallic papillae very elongated, reaching as far as the base of the P3 coxae. Males without cuticular partition in P5 coxae. Cephalothorax dark-olive green and pleon light olive green (Rudolph & Crandall, 2007, 2012). Species is small (17.9-30.0 nun CL; [bar.X] = 21.1 [+ or -] 3.0 mm CL; n = 21), but the only size data available derives from the type series specimen (Rudolph & Crandall, 2007) (see Table 1).

Geographic distribution

This parastacid, recorded in two Coastal Cordillera localities in the provinces of Osorno and Llanquihue, southern Chile: Rucapihuel (40[degrees]35'00.08"S, 73[degrees]34' 44.3"W), and Estaquilla (41[degrees]25'15.93"S, 73[degrees]46'51. 74"W) (Rudolph & Crandall, 2007) extends its occurrence approximately 3.200 [km.sup.2] (Rudolph, 2010).

Habitat

Both of these V. retamali populations inhabit geogenous peatlands, i.e., depend on rainwater and superficial underground waters to supply hydric needs (Kulzer & Cook, 2001). These peatlands originated in a small endorreic basin generated by the holocenic deglacialization where, over the course of time, organic matter has been deposited (Grignola & Ordonez, 2002). This organic material originated from the partially decomposed, loosely compacted vegetal remains of the genus Sphagnum, mixed with woody fragments, gramineous and humus particles, accumulated in an anoxic environment, highly saturated with water all year round (Grignola & Ordonez, 2002) (Fig. 4b). On capturing the type series, (17 December 2002), the water analyzed inside the burrows had a pH of 4.7, dissolved oxygen of 2.8 mg [L.sup.-1], constant hardness of 17.8 ppm of CaC[O.sub.3], and a temperature of 12.5[degrees]C (Rudolph & Crandall, 2007).

Burrow morphology

Virilastacus retamali excavates shallow burrows (45 cm depth approximately) with few ramifications. A mold made with polyester resin (Bedatou et al., 2010) revealed six main entrances, with diameters ranging from 3.0 to 3.5 cm. Fifteen centimeters below the surface, three of these entrances converged into a short, subhorizontal tunnel; one of its ends projected slightly upwards to form a short blind tunnel; the other extreme is connected to a main sub-horizontal tunnel. The remaining three entrances converged at a depth of 30 cm, at the other end of the main tunnel. In the winter, the species constructs "chimneys" reaching an average height of 3.9 cm (SD = [+ or -] 0.729; n = 8) (Fig. 4c). Unlike the other species of the genus, V. retamali has been observed and captured outside its burrows, in nearby surface pools. Based on these observations and according to Hobbs's criteria (1942), V. retamali can be categorized as a secondary burrowing species (Rudolph & Crandall, 2007).

Sexual system

No external morphological evidence of intersexuality has been detected in the type series (Rudolph & Crandall, 2007), suggesting that this species is gonochoric. Females smaller than 20.0 mm CL have strongly calcified semi-ellipsoidal gonopores, while females larger than 20.0 mm CL have apparently functional ellipsoidal gonopores, given that they are only partially calcified and surrounded by abundant pilosity. Males have a very elongated phallic papilla ([bar.X] = 3.5 [+ or -] 0.5 mm) (Rudolph & Crandall, 2007).

Conservation status

Rudolph & Crandall (2007) classified V. retamali as an Endangered throughout its entire geographic range, given that it would meet the B1 ab(iii) criteria of the IUCN (2001) Red List for this category. Nevertheless, Buckup (2010c) classified it as Data Deficient, while Almerao et al. (2014) supported the endangered species classification of Rudolph & Crandall (2007).

Virilastacus jarai Rudolph & Crandall, 2012 (Fig. 5a)

Common name: Angeline crayfish

Distinctive morphological characteristics

Precervical cephalothorax with four, two or lacking smooth dorsal ridges. Eyes small. Rostrum short, reaching distal margin of the middle podomere of antennal flagellum; dorsally concave. Rostral carina short, weakly prominent. Epistome anteromedial lobe resembling a rhombus. Cervical groove "V" shaped. Areola wide and extended. Opposable margin of P1 propodite bearing 11 to 22 teeth with pilosity along the length of dorsal side, while only on basal part of ventral side. Dactyl moving obliquely. Abdominal pleura with straight ventral margins. Telson subtriangular with a small, sharp spine in each lateral margin. Individuals with female or male gonopores. Phallic papillae elongated, reaching base of lateral process of XII body segment. Males lacking cuticular partition in P5 coxae. Cephalothorax and P1 chelipeds olive green. Pleon and caudal fan light brown (Rudolph & Crandall, 2012). It is a small species; size in the type series ranges from 6.7 to 24.8 mm CL ([bar.X] = 17.5[+ or -] 6.1 mm) (Rudolph & Crandall, 2012) (see Table 1).

Geographic distribution

Virilastacus jarai has only been recorded in the type locality, a fragment of wetland situated in the "El Porvenir" sector (37[degrees]26'39.84"S, 72[degrees]18'37.12"W), 1.5 km northwest of the town of Los Angeles in centralsouthern Chile (Rudolph & Crandall, 2012).

Habitat

The species inhabits the underground waters of a fragment of semi-marshland, located in a topographic basin of 861 [m.sup.2] at 152 m above sea level. This area is flooded for six months of the year (May to October) and the phreatic level remains below the surface in spring-summer (Fig. 5b). The soil, characterized by a large accumulation of organic material, in addition to the high percentage of moisture originating from partially decomposed vegetal remains. On capturing the type series (13 June 2010), analysis of the water inside the burrows was as follows: dissolved oxygen = 4.9 mg [L.sup.-1], temperature = 14.1[degrees]C, pH = 6.5, and constant hardness of 53.4 ppm of CaC[O.sub.3] (Rudolph & Crandall, 2012).

Burrowing behavior

The species excavates shallow (<1 m), but complex burrows, not connected to lothic or lenthic waters (Rudolph & Crandall, 2012). In winter, it also constructs "chimneys" around the entrance orifices of the burrows (Fig. 5c). Outside the burrows, no specimens have been found, which suggest that the entire life cycle of V. jarai occurs inside the burrows. According to the Hobbs's (1942) criteria, the species can be considered as a primary burrower.

Sexual system

The revision of the type series revealed the occurrence of an intersex individual; however, this is not sufficient evidence to maintain that this is a transitional stage of an eventual sex change or, even less likely, that the species presents some form of hermaphroditism. Consequently, the evidence available suggests that V. jarai would be a gonochoric species (Rudolph & Crandall, 2012).

Conservation status

Rudolph & Crandall (2012) categorized V. jarai as Critically Endangered. This conclusion was based on the B1ab (ii) criteria of the IUCN Red List (2001) for this category, i.e., an estimated extent of occurrence of less than 100 [km.sup.2], only known recording in one location, and a projected decline in habitat quality. The V. jarai habitat has been subject to deforestation in the recent past to clear land for agricultural purposes. At present, this land has been divided up and the topography modified to accommodate building development projects resulting from the rapid expansion of the town of Los Angeles. Almerao et al. (2014) endorsed categorizing V. jarai as a critically endangered species.

REMARKS

The four Virilastacus species are endemic to Chile and have a restricted geographic range, distributed between the coastline and the Coastal Cordillera, from Concepcion (36[degrees]46'S) to Estaquilla (41[degrees]25'S), except for V. jarai, whose presence has only been recorded in one location, to the east of the coastal Cordillera (Fig. 6). Furthermore, within this coastal fringe, populations present a clearly discontinuous distribution, associated with wetlands. These species are burrowers, and although their burrows are shallow (<1.5 m), have multiple ramifications and are much elaborated (Bedatou et al., 2010). The most significant morphological adaptations to this life style include the following aspects: (1) body without large protuberances, facilitating their movement inside the tunnels; (2) highly developed cephalothorax, in comparison to the scarcely developed pleon; (3) cephalothorax taller than broad, which increases the volume of the branchial chamber and makes it possible to house larger branchia than those species that inhabit open waters; (4) P1 chelae relatively large and vertically orientated, and (5) reduced eye size (Rudolph, 1997; Reynolds et al., 2013). They also share some biological characteristics of all freshwater astacids (Families Astacidae, Cambaridae and Parastacidae) such as: low fecundity, direct development with hatching in the juvenile stage, extended parental care up to the second juvenile stage, as well as omnivorous feeding habits (Rudolph & Rojas, 2003; Rudolph, 2013). Like the other species of these three families, they are very important functional elements in the linmic ecosystems, both as prey and as consumers (Jara et al., 2006; Almerao et al., 2014). Nevertheless, biological knowledge about these species is limited mainly to taxonomic and distributional aspects, with some information about their sexual system. Three of the four species have separate sexes while V. rucapihuelensis presents partial protandric hermaphroditism, with primary males and females (Rudolph et al., 2007). Similarly, some information has been acquired about their phylogenetic affinities (Rudolph & Crandall, 2007, 2012). Reconstruction of phylogenetic relationships revealed the monophyly of the Virilastacus genus and of each one of its species. Furthermore, they showed that there is clear genetic differentiation between V. jarai and the other species of the genus. Virilastacus jarai is situated in a different basal clade with respect to the clade of the other three species, with V. araucanius being the species phylogenetically closest to V. jarai. Moreover, the incubation period of V. rucapihuelensis and probably that of the other three species extends from mid-winter to mid-summer (from July to February) (Rudolph et al., 2007). Recently, the Ministerio del Medio Ambiente (2013a, 2013b) and Almerao et al. (2014), based on the IUCN (2001) Red List criteria, have reevaluated and updated the state of conservation of Chilean and South American parastacids, respectively. Notwithstanding these updates, no effective measures for their protection have been implemented yet and, as a result, the conservation of the Virilastacus species is still under threat. Included among these threats are: (1) drainage of the "vegas" for forestry, farming and livestock development; (2) use of chemicals (agricultural fertilizers and pesticides); (3) clearing of vegetation and subsequent replacement of vegetation coverage; (4) free-range pig farming, which removes the original vegetation and compacts the soil, and (5) cattle farming, with trampling and destruction of the burrows. These threats are degrading, fragmenting, and ultimately decreasing the geographical extension of their habitat. Furthermore, certain intrinsic characteristics of parastacids [i.e., slow growth, low fecundity, delayed sexual maturity and long periods of embryonic and early post-embryonic development (Holdich, 1993; Rudolph, 2013)], together with the restricted geographic range and scarce mobility of the Virilastacus species, render them particularly vulnerable to the aforementioned threats. At present, the Chilean parastacids in general, and the Virilastacus species in particular, are not threatened by invasive exotic species (Rudolph, 2013). However, this threat could materialize in the near future, if we consider that Procambarus clarkii (Girard, 1852), a species native to North America and with considerable adaptive plasticity, has been introduced successfully to almost all continents, and has already been recorded in Colombia, Ecuador and Brazil (Valencia-Lopez et al., 2012; Almerao et al., 2014). Furthermore, recent studies revealed numerous areas in the southern cone of South America (Argentina, Paraguay, Uruguay, and Chile) suitable for P. clarkii occupation (Palaoro et al., 2013). Fortunately, these four species are not under threat from fishery activities for human consumption, because they are small species whose edible part (the pleon) is underdeveloped, thus, meat yield is very meager; these species also construct very complex burrows and considerable effort is required to capture them. Finally, part of their geographic range is located to the south of the Tolten River (39[degrees]S), where the local inhabitants have no tradition of consuming these types of crustaceans. Could this lack of socio-economic significance account for the lack of legislation regulating their protection? Probably not considering that other Chilean parastacids exposed to elevated extraction pressure for human consumption purposes (i.e., Samastacus spinifrons and Parastacus pugnax) and neither is protected. Minimum biological knowledge (distribution range, habitat type, life style, size, incubation period, and state of conservation) necessary to establish regulations is now available. Legislation in this respect, together with regulating compliance with the law, would greatly contribute towards the conservation of Chilean parastacids. It is believed that protection of these species can be achieved, considering that the Ministry of Environment has announced a series of measures in both the National Plan of Action on Climate Change and the draft law for the creation of a Biodiversity and Protected Areas Service.

DOI: 10.3856/vol43-issue5-fulltext-1

ACKNOWLEDGEMENTS

The author is grateful to the Research Department of the Universidad de Los Lagos, Osorno, Chile, for financially supporting many of the studies carried out on Virilastacus, in addition to the publication of this article. The collaboration of Susan Angus with the translation of the paper is appreciated.

REFERENCES

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Received: 12 December 2014; Accepted: 15 July 2015

Erich H. Rudolph (1)

(1) Departamento de Ciencias Biologicas y Biodiversidad, Universidad de Los Lagos P.O. Box 933, Osorno, Chile

Corresponding author: Erich H. Rudolph (erudolph@ulagos.cl)

Corresponding editor: Ingo Wehrtmann

Caption: Figure 1. Virilastacus araucanius (Faxon, 1914). a) Dorsal view of male. Scale bar = 17.9 mm, b) partial view of habitat, c) overhead view of chimneys. Photos: E. Rudolph.

Caption: Figure 2. Virilastacus rucapihuelensis Rudolph & Crandall, 2005. a) Dorsal view of specimen. Scale bar = 14.0 mm, b) partial view of habitat. Photos: E. Rudolph.

Caption: Figure 3. Virilastacus rucapihuelensis Rudolph & Crandall, 2005. a) Lateral view of mould type 1 burrow, b) lateral view of mould type 2 burrows, c) overhead view of chimney. Arrowheads = surface entrances. Photos: a) and b) E. Bedatou; c) E. Rudolph.

Caption: Figure 4. Virilastacus retamali Rudolph & Crandall, 2007. a) Dorsal view of specimen. Scale bar = 12.0 mm, b) partial view of habitat, c) lateral view of chimney. Photos: E. Rudolph.

Caption: Figure 5. Virilastacus jarai Rudolph & Crandall, 2012. a) Dorsolateral view of specimen. Scale bar = 9.0 mm, b) partial view of habitat, c) lateral view of chimney. Photos: E. Rudolph.

Caption: Figure 6. Geographical distribution of Virilastacus species. Gray fringe = Virilastacus araucanius; * Virilastacus jarai; ** Virilastacus rucapihuelensis; [??] Virilastacus retamali.
Table 1. Morphological characters useful for distinguish the
four presently identified species of Virilastacus (Modified
from Rudolph & Crandall, 2012).

Character           V. araucanius         V. rucapihuelensis

Rostrum
Dorsodistal         Excavated             Concave
  surface
Rostral carina      Long and not          Long and
                       very prominent       prominent
Eyes                Small                 Small
Antennal scale                            Short.
                                            Distolateral
                                            spine small
Basal Podomere      Spine absent          Small spine
  Antennula
Mandible
Cephalic molar      Molariform            Dentiform
  process
Caudal molar        Quadricuspide         Tricuspide
  process
Epistome
Anteromedial lobe   Resembles a           Resembles a
                      rhombus               triangle
Posterior plate     With                  With
                      anterolateral         anterolateral
                      tubercles             tubercles small
Ischium of
  Maxilliped 3
Ventral surface     With a band of        With a band of
                      small, blunt        small, blunt
                      tubercules and        tubercles and
                      scarce pilosity       scarce pilosity

External            Without extension     Without extension
  distal border
Opposable
  Propo margin
Pilosity            Absent                Only on both
                                            sides of the
                                             proximal group
                                            of teeth

Number of teeth     Between 11            Between 5 and 9
                      and 18
Dactylus
Movement            Subhorizontal         Oblique
Number of teeth     Between 9 and 15      Between 5 and 10
Precervical         Dorsal ridges         Dorsal ridges
  cephalothorax       absent                absent

Areola              Narrow and            Narrow and
                      extended              extended
Cervical groove     Weakly V-shaped       Strongly V-shaped
P4 Coxae            Close together        Widely separated
Gonopores           Female or male        Supernumerary
Phallic Papillae    In close              Widely separated,
                      proximity,            more robust and
                      long and thin         shorter
Male Cuticle        Absent                Present
  Partition
Pleomere pleura
Somite 1            With a small          Anterior lobe
                      anterior lobe,        absent, not
                      partially over        overlapped by
                      lapped by the         S2 pleuron
                      S2 pleuron

Somite 2 of the     Flap absent           Flap present
  adult females
Telson
Form                Subretangular         Subretangular
Lateral spines      Prominent and sharp   Small and blunt

Habitat             Semi-marshland,       Semi-marshland,
                      perennially           perennially
                      green areas           green areas

Character           V. retamali          V. jarai

Rostrum

Dorsodistal         Concave              Concave
  surface
Rostral carina      Short and            Short and little
                      prominent            prominent
Eyes                Large                Small
Antennal scale      Long.                  Short.
                      Distolateral         Distolateral
                      spine small          spine small
Basal Podomere      Large spine          Large spine
  Antennula

Mandible

Cephalic molar      Molariform           Molariform
  process
Caudal molar        Tricuspide           Quadricuspide
  process
Epistome
Anteromedial lobe   Resembles a          Resembles a
                      rhombus              rhombus
Posterior plate     With                 With
                      anterolateral        anterolateral
                      tubercles large      tubercles large
Ischium of
  Maxilliped 3
Ventral surface     With a band of       With a band of
                      large, prominent     small, blunt
                      tubercles and        tubercles and
                      abundant             abundant
                      pilosity             pilosity
External            Without extension    With a large
  distal border                            extension
Opposable
  Propo margin
Pilosity            On both sides of     Throughout the
                      the entire row       dorsal side and
                      of teeth             only on the
                                           basal zone of
                                           the ventral side
Number of teeth     Between 13 and 17    Between 11 and 22

Dactylus
Movement            Subhorizontal        Oblique
Number of teeth     Between 10 and 15    Between 9 and 15
Precervical         With 4, smooth       With 4 smooth
  cephalothorax     dorsal ridges          dorsal ridges,
                                           or with 2,
                                           or absent
Areola              Wide and short       Wide and extended

Cervical groove     U-shaped             Strongly V-shaped
P4 Coxae            Close together       Close together
Gonopores           Female or male       Female or male
Phallic Papillae    Very close           Very close
                      together, very       together, long
                      long and thin        and thin
Male Cuticle        Absent               Absent
  Partition
Pleomere pleura
Somite 1            With a small         With a small
                      anterior lobe,       anterior lobe,
                      partially over       total or
                      lapped by the        partially over
                      S2 pleuron           lapped by
                                           S2 pleuron
Somite 2 of the     Flap absent          Flap absent
  adult females
Telson
Form                Subtriangular        Subtriangular
Lateral spines      Prominent and        Small and sharp
                      sharp
Habitat             Peatlands            Fragment semi-
                                           marshland,
                                           perennially
                                           green areas
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Author:Rudolph, Erich H.
Publication:Latin American Journal of Aquatic Research
Date:Nov 1, 2015
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