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Postembryonic development in freshwater crayfish (Decapoda: Astacidea) in an evolutionary context

Abstract

Detailed morphology of the first three postembryonic developmental stages (Stages I-III juvenile) in representatives from all four crayfish families, Austropotamobius torrentium (von Paula Schrank, 1803) (Astacidae), Procambarus virginalis Lyko, 2017 (Cambaridae), Cambaroides japonicus (De Haan, 1841 [in De Haan, 1833-1850]) (Cambaroididae) and Cherax destructor Clark, 1936 (Parastacidae) are described and the diagnostic characters for each family are indicated. A phylogenetic tree of freshwater Astacidea, based on these new diagnostic juvenile characters is constructed to suborder, superfamily and family levels, and compared with a molecular phylogenetic tree. The evolutionary history of maternal care in freshwater crayfish is discussed based on particular features of the postembryonic stages of each family. Using comparisons between the phylogenetic tree and global geo-history, the location and timing of the early evolution of maternal care in postembryonic development and the extension of this care are estimated.

Keywords:
Adaptation; Astacoidea; juvenile; morphology; Parastacoidea

INTRODUCTION

The infraorder Astacidea Latreille, 1802Latreille, P.A. 1802. Histoire naturelle, générale et particulière des Crustacés et des Insectes. Ouvrage faisant suite à l’histoire naturelle générale et particulière, composée par Leclerc de Buffon, et rédigée par C.S. Sonnini, membre de plusieurs Sociétés savantes, Vol. 3. Paris, F. DuFart, 467p. has two freshwater (Astacoidea Latreille, 1802 and Parastacoidea Huxley, 1879Huxley, T.H. 1879. On the classification and the distribution of the crayfishes. Proceedings of the Zoological Society of London, 1878: 752-788.) and two marine superfamilies (Nephropoidea Dana, 1852Dana, J.D. 1852. United States Exploring Expedition during the years 1838, 1839, 1840, 1841, 1842, under the Command of Charles Wilkes, U.S.N. Vol 13, Crustacea. Part I, [Atlas, pls. 1-96 (1855)]. Philadelphia, C. Sherman. and Enoplometopoidea De Saint Laurent, 1988De Saint Laurent, M. 1988. Enoplometopoidea, nouvelle superfamille de crustacés décapodes Astacidea. Comptes Rendus hebdomadaires de l'Académie des Sciences, Paris, 3 sér. 307: 59-62.) (De Grave et al., 2009De Grave, S.; Pentcheff, N.D.; Ahyong, S. T.; Chan, T-Y.; Crandall, K.A.; Dworschak, P.C.; Felder, D.L.; Feldmann, R.M.; Fransen, C.H.J.M.; Goulding, L.Y.D.; Lemaitre, R.; Low, M.E.Y.; Martin, Joel W.; Ng, P.K.L.; Schweitzer, C.E.; Tan, S.H.; Tshudy, D. and Wetzer, R. 2009. A classification of living and fossil genera of decapod crustaceans. Raffles Bulletin of Zoology, Supplement 21: 1-109.). The superfamily Astacoidea includes three families, Astacidae Latreille, 1802, Cambaridae Hobbs, 1942Hobbs, H.H. Jr. 1942. A generic revision of the crayfishes of the subfamily Cambarinae (Decapoda, Astacidae) with the description of a new genus and species. American Midland Naturalist, 28: 334-357., and Cambaroididae Villalobos, 1955Villalobos, A. 1955. Cambarinos de la fauna mexicana: Crustacea Decapoda. Ciudad de México, Departamento de Biología, Universidad Nacional Autónoma de Mexico, 276p. [translated by Hobbs, H. H. Jr. 1983. Crayfishes of Mexico (Crustacea: Decapoda). Washington D.C., Smithsonian Institution Libraries and National Science Foundation]., all native to the Northern Hemisphere. The superfamily Parastacoidea Huxley, 1879 contains a single family, the Parastacidae, whose members are all native to the Southern Hemisphere (Hobbs, 1974Hobbs, H.H. Jr. 1974. Synopsis of the families and genera of crayfishes (Crustacea: Decapoda). Smithsonian Contributions to Zoology, 164: 1-32.; 1988Hobbs, H.H. Jr. 1988. Crayfish distribution, adaptation, and evolution. p. 52-82. In: D.M. Holdich and D.M. Lowery (eds), Freshwater Crayfish: Biology, Management and Exploitation. London, Croom Helm.; Crandall and De Grave, 2017Crandall, K.A. and De Grave, S. 2017. An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. Journal of Crustacean Biology, 37: 615-653.). All crayfish live in freshwater throughout their entire lives. Females carry eggs and early juvenile stages remained attached to the female. Offspring do not have larval planktonic stages (Scholtz, 1999Scholtz, G. 1999. Freshwater crayfish evolution. Freshwater Crayfish, 12 : 37-48.) and cannot disperse via the sea. Their world distribution is noticeably disjunct. The Cambaridae are found on the Atlantic coasts of North and Central America (440 extant species); the known range of Cambaroididae (6 species) embraces far-eastern Asia; Parastacidae (184 species) are found in Oceania, as well as New Guinea, Madagascar and southern South America (Hobbs, 1974Hobbs, H.H. Jr. 1974. Synopsis of the families and genera of crayfishes (Crustacea: Decapoda). Smithsonian Contributions to Zoology, 164: 1-32.; 1988Hobbs, H.H. Jr. 1988. Crayfish distribution, adaptation, and evolution. p. 52-82. In: D.M. Holdich and D.M. Lowery (eds), Freshwater Crayfish: Biology, Management and Exploitation. London, Croom Helm.; Scholtz, 1999Scholtz, G. 1999. Freshwater crayfish evolution. Freshwater Crayfish, 12 : 37-48.). The range of European Astacidae (16 species) is disjunct from that of American Astacidae (5 species) inhabiting the Pacific drainages of western North America (Larson and Olden, 2011Larson, E. and Olden, J. 2011. The State of Crayfish in the Pacific Northwest. Fisheries, 36: 60-73.; Ďuriš, 2015Ďuriš, Z. 2015. Systematic and distribution of crayfish. p. 15-36. In: P. Kozák, Z. Ďuriš, A. Petrusek, M. Buřič, I. Horká, A. Kouba, E. Kozubíková-Balcarová and T. Policar(eds), Crayfish Biology and Culture. Vodňany, Czech Republic, University of South Bohemia.; Füreder, 2015Füreder, L. 2015. Crayfish in Europe: Biogeography, ecology and conservation. p. 594-627. In: T. Kawai, Z. Faulkes and G. Scholtz (eds), Freshwater Crayfish: A Global Overview. Boca Raton, FL, CRC Press .; Souty-Grosset and Fetzner, 2016Souty-Grosset, C. and Fetzner, J.W. 2016. Taxonomy and identification. p. 1-30. In: M. Longshaw and P. Stebbing (eds), Biology and Ecology of Crayfish. Boca Raton, FL, CRC Press .; Crandall and De Grave, 2017Crandall, K.A. and De Grave, S. 2017. An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. Journal of Crustacean Biology, 37: 615-653.; Pârvulescu, 2019Pârvulescu, L. 2019. Introducing a new Austropotamobius crayfish species (Crustacea, Decapoda, Astacidae): A Miocene endemism of the Apuseni Mountains, Romania. Zoologischer Anzeiger, 279: 94-102.).

Juvenile Astacidae and Cambaroididae become independent from their mothers in Stage II, while juvenile Cambaridae and Parastacidae only become independent in Stage III. The latter taxa thus exhibit extended maternal care, which has been suggested as a contributing factor in the remarkably high species richness (Albrecht, 1982Albrecht, H. 1982. Das System der europäischen Flußkrebse (Decapoda, Astacidae): Vorschlag und Begrün dung. Mitteilungen des Hamburgischen Zoologischen Museum und Institut, 79: 187-210.; Kawai and Scholtz, 2002Kawai, T. and Scholtz, G. 2002. Behavior of juvenile of the Japanese endemic species Cambaroides japonicus (Decapoda: Astacidea: Cambaridae), with observations on the position of the spermatophore attachment on adult females. Journal of Crustacean Biology, 22: 532-537.; Scholtz and Kawai, 2002Scholtz, G. and Kawai, T. 2002. Aspects of embryonic and postembryonic development of the Japanese freshwater crayfish Cambaroides japonicus (Crustacea, Decapoda) including a hypothesis on the evolutional maternal care in the Astacida. Acta Zoologica, 83: 203-12.) of these families. In two Tasmanian crayfishes, Engaeus leptorhyncusClark, 1939Clark, E. 1939. Tasmanian Parastacidae. Papers and Proceedings of the Royal Society of Tasmania, 1938: 117-127, pls. 12-13. and Ombracoides leptomerus (Riek, 1951Riek, E.F. 1951. The freshwater crayfish (family Parastacidae) of Queensland. Records of the Australian Museum, 22: 368-388.), long associations between mother and juvenile crayfish in burrows have been recorded (Horwitz and Richardson, 1985Horwitz, P.H.J.; Richardson, A.M.M. and Cramp, P. 1985. Aspects of the life history of the burrowing freshwater crayfish, Engaeus leptorhynchus at Rattrays Marshes, north east Tasmania. Tasmanian Naturalist, 82: 1-5.; Hamr and Richardson, 1994Hamr, P. and Richardson, A.M.M. 1994. The life history of Parastacoides tasmanicus tasmanicus Clark, a burrowing freshwater crayfish from South-west Tasmania. Australian Journal of Marine and Freshwater Research, 45: 455-470.).

Several studies of the morphology of the postembryonic developmental stages of crayfish have been conducted, specifically in the following families: Astacidae (e.g., Zehnder, 1934Zehnder, H, 1934. Über die Embryonalentwicklung des Flusskrebses. Acta Zoologica, 15: 261-408.; Kawai and Kouba, 2020Kawai, T. and Kouba, A. 2020. A description of postembryonic development of Astacus astacus and Pontastacus leptodactylus. Freshwater Crayfish, 25: 103-116.), Cambaridae (e.g., Van Deventer, 1937Van Deventer, W.C. 1937. Studies on the biology of the crayfish Cambarus propinquus Girard. Illinois Biological Monographs, 15(3): 1-67.; Suko, 1953Suko, T. 1953. Studies on the development of the crayfish. I. The development of secondary sex characters in appendages. Science Reports of Saitama University B, 1: 77-96.; Payne, 1972Payne, J.F. 1972. The life history of Procambarus hayi. American Midland Naturalist, 87: 25-35.; Vogt, 2008Vogt, G. 2008. Investigation of hatching and early post-embryonic life of freshwater crayfish by in vitro culture, behavioral analysis, and light and electron microscopy. Journal of Morphology, 269: 790-811.), Cambaroididae (e.g., Ko and Kawai, 2001Ko, H.S. and Kawai, T. 2001. Postembryonic development of the Korean crayfish, Cambaroides similis (Decapoda, Cambaridae) reared in the laboratory. The Korean Journal of Systematic Zoology, 17: 35-47.; Scholtz and Kawai, 2002Scholtz, G. and Kawai, T. 2002. Aspects of embryonic and postembryonic development of the Japanese freshwater crayfish Cambaroides japonicus (Crustacea, Decapoda) including a hypothesis on the evolutional maternal care in the Astacida. Acta Zoologica, 83: 203-12.) and Parastacidae (e.g., Wood-Mason, 1876Wood-Mason, J. 1876. On the mode in which the young of the New Zealand Astacidae attach themselves to the mother. The Annals and Magazine of Natural History, Series 4, 18: 306-307.; Rudolph and Zapata, 1986Rudolph, E. and Zapata, L.A. 1986. Desarrollo embriosario y postlarval del camaron de las vegas Parastacus nicoleti (Phillipi, 1882 ), en condiciones de laboratorio. Biota, Chile, 2: 37-50.; Ribeiro et al., 2019Ribeiro, F.B.; Gomez, K.M.; Huber, A.F. and Araujo, P.B. 2019. Description of the second juvenile stage of the blue-fingered burrowing crayfish Parastacus caeruleodactylus (Decapoda: Astacidea: Parastacidae). Zootaxa, 4686: 581-592 .). All of the studied crayfish species hatch as Stage I juveniles that are temporarily attached to their mothers via the so-called “telson thread” connecting the terminal part of the juvenile telson to the inner lining of the egg capsule, which is joined to the female pleopod. Hatchlings have an unsegmented telson (only the telson is present and no uropods). After moulting from Stage I to Stage II, the unsegmented tail-fan is retained but the telson thread disappears. After the moult to Stage III, juveniles have the same features as adults, including a fully developed tail-fan and a pair of biramous uropods (Scholtz, 1995Scholtz, G. 1995. The attachment of the young in the New Zealand freshwater crayfish Paranephrops zealandicus (White, 1847) (Decapoda, Astacida, Parastacidae). New Zealand Natural Science, 22: 81-89.; 1999Scholtz, G. 1999. Freshwater crayfish evolution. Freshwater Crayfish, 12 : 37-48.). The presence of recurved hooks only on the tip of pereiopod 1 (cheliped) in Stage I juveniles is an apomorphy of the superfamily Astacoidea. Stage I Parastacoidea juveniles, on the other hand, have recurved hooks on the tips of pereiopods 4 and 5 (Gurney, 1935Gurney, R. 1935. The mode of attachment of the young in the crayfishes of the families Astacidae and Parastacidae. The Annals and Magazine of Natural History, Series 10, 16: 553-555.; Rudolph and Iracabal, 1994Rudolph, E.H. and Iracabal, J.C. 1994. Desarrollo embrionario y postembrionario del camaron de rio Samastacus spinifrons (Philippi, 1882 ) (Decapoda, Parastacidae), en condiciones de laboratorio. Boletin de la Sociedad de Biologia de Concepción, Chile, 55: 43-49.; Burton et al., 2007Burton, T.B.; Knot, D.; Judge, P.; Vercoe, A. and Brearley, A. 2007. Embryonic and juvenile attachment structures in Cherax cainii (Decapoda: Parastacidae): Implications for maternal care. American Midland Naturalist, 157: 127-136.). Although Astacidae and Cambaroididae have a rounded telson in Stages I and II (Huxley, 1880Huxley, T.H. 1880. The crayfish. An Introduction to the Study of Zoology. London, C. Kegan Paul and Co., 371p.; Kurata, 1962Kurata, H. 1962. Studies on the age and growth of Crustacea. Bulletin of Hokkaido Region Fisheries Research Laboratory, 24: 1-115.; Köksal, 1988Köksal, G. 1988. Astacus leptodactylus in Europe. p. 365-400. In: D. Holdich and I.D. Reeve (eds), Freshwater Crayfish. London, Croom Helm .), no other family-level diagnostic character has yet been described. The present study describes new diagnostic characters in postembryonic stages at the suborder and superfamily levels, as well as certain family-level diagnostic characters. These diagnostic early juvenile morphological features were used to explore crayfish phylogeny, with special emphasis placed on the evolution of maternal care in this animal group.

MATERIAL AND METHODS

Early developmental stages of Austropotamobius torrentium (von Paula Schrank, 1803von Paula Schrank, F. 1803. Fauna Boica: durchgedachte Gechichte der in Baiern einheimischen und zahmen Thiere. Vol. 3, part 1. Nürnberg, Germany, 382 p.) (Astacidae), Procambarus virginalisLyko, 2017Lyko, F. 2017. The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa, 4363: 544-552. (Cambaridae), Cambaroides japonicus (De Haan, 1841 [in De Haan, 1833-1850]De Haan, W. 1833-1850. Crustacea. In: Fauna Japonica sive Descriptio nimalium, quae in Itinere per Japoniam, Jußu et Auspiciis Superiorum, qui Summum in India Batava Imperium Tenent, Suscepto, Annis 1823-1830 Collegit, Notis, Observationibus et Adumbrationibus Illustravit (P.F. von Siebold, ed.). Lugduni-Batavorum [= Leiden].) (Cambaroididae), and Cherax destructorClark, 1936Clark, E. 1936. The freshwater and land crayfishes of Australia. Memoirs of the National Museum, Melbourne, 10: 5-57, pls. 1-11. (Parastacidae) were obtained from ovigerous females kept in culture at the Faculty of Fisheries and Protection of Waters, University of South Bohemia in České Budějovice, Czech Republic, and the Central Fisheries Research Institution, Hokkaido Research Organization, Japan. Juveniles were preserved in 10 % formalin for seven days to preserve their pigmentation and then in 70 % ethanol to allow for the dissection of their body parts. For each species, five individuals from Stages I, II, and III were examined using a digital camera (Sony MEX-5R, Tokyo) coupled to a microscope (Nikon TI-SM, Tokyo) to observe the setae on their appendages, or using a stereomicroscope (Olympus, SZ61, Tokyo) to describe the appendages and body. The morphological terminology used in this paper is adopted from Thomas (1970Thomas, W. 1970. The seta of Austropotamobius pallipes (Decapoda, Astacidae). Journal of Zoology, London, 160: 91-142.; 1973Thomas, W.J. 1973. The hatchling setae of Austropotamobius pallipes (Lereboulet) (Decapoda, Astacidae). Crustaceana, 24: 77-89.) and Noro et al. (2005Noro, C.K.; Buckup, L. and Bond-Buckup, G. 2005. The juvenile stages of Parastacus brasliensis (von Martens, 1869) (Crustacea, Decapoda, Parastacidae). Journal of Natural History, 39: 1831-1873. ).

RESULTS

Austropotamobius torrentium

Stage I (Figs. 1, 2)

Figure 1.
Juvenile Stage I of Austropotamobius torrentium. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D-H) pereiopods 1-5, dorsal view or lateral view; (I-M) distal segments of pereiopods 1-5, dorsal view or lateral view. Scale bars: 0.25 mm.

Figure 2.
Juvenile Stage I of Austropotamobius torrentium. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. bsg, basal segment of peduncle; bsp, basipodite; c, carpopodite; cxp, coxopodite; d, dactylopodite; de, distal endite; dsg, distal segment of peduncle; ed, endopodite; en, endite; ep, epipodite; exp, exopodite; exf, external flagellum; i, ischiopodite; in, incisor ridge; inf, internal flagellum; m, meropodite; mp, mandibular palp; mr, molar ridge; msg, intermediate segment of peduncle; p, propodite; pe, proximal endite; tc, toothed crest. Scale bars: 0.25 mm.

Globular carapace filled with yolk (hepatopancreas for storing nutrients), red pigment present on lateral and anterior parts of carapace, antenna 1 elongated and situated above antenna 2 (Fig. 1A), down-curved rostrum and sessile (no peduncle) eyes (Fig. 1B).

Telson rounded with notched posterior margin (Fig. 1C), uropods undeveloped, cephalic margin of telson with row of cuspidate setae, caudal margin with hook-like curved cuspidate setae. Freshly hatched juveniles remain attached to inner lining of egg capsule by telson thread connected to posterior margin of the telson; telson thread formed by twisting of inner egg-capsule lining. Juveniles remain attach to mother’s long pleopodal setae using specialized recurved spines on the tips of their chelipeds (dactylopodite and propodite) (Fig. 1D, I). Second (Fig. 1E, J) and third (Fig. 1F, K) pereiopods with curved spines on tips of small claws (dactylopodites and propodites). Fourth (Fig. 1G, L) and fifth (Fig. 1H, M) pereiopods with slightly curved spines at apex of dactylopodites (Fig. 1L, M); all pereiopods often with rudimentary setae or setal precursors (Fig. 1D-H).

Antenna 1 (Fig. 2A): four segments on internal and external flagellum. Setae only on distal segments, bearing few minute precursor setae. Mesial margin of antennal scale (Fig. 2B) bearing several long setal precursors. Antenna 2 (Fig. 2C): flagellum consisting of approximately 50 segments with 3-4 setal precursors at apex of final segment.

Mandible (Fig. 2D): no setae, processes or teeth on cutting edge of incisor ridge and molar ridge; mandibular palp 3-segmented, distal margin of terminal segment with 1 setal precursor. Maxilla 1 (Fig. 2E) with coxopodite, basipodite, and endite, and plumose setae on proximal endite; maxilla 2 (Fig. 2F) with biramous coxopodite and basipodite (distal endite and proximal endite), endite and exopodite.

First maxilliped (Fig. 2G) bearing coxopodite, basipodite, endite, expodite, and epipodite. Proximal-external margin of exopodite with pappose setae. Second maxilliped (Fig. 2H) biramous, with 5-segmented endopodite (dactylopodite, propodite, carpodite, meropodite, ischiopodite) and unsegmented expodite. Terminal margin of dactylopodite with one setal precursor; external margin of propodite, internal margin of meropodite, ischiopodite and basipodite with small-toothed crest. Expodite with setal precursors on apical region. Third maxilliped (Fig. 2I) biramous; 5-segmented endopodite and unsegmented exopodite. Terminal margin of dactylopodite with sub-apical setal precursors; internal margin of ischiopodite with small-toothed crest; terminal tip of exopodite with no setal precursors.

All pleopods (representative second pleopod depicted in Fig. 2J) with setal precursor on endopod and on exopod.

Stage II (Figs. 3, 4)

Figure 3.
Juvenile Stage II of Austropotamobius torrentium. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D-H) pereiopods 1-5, dorsal or lateral view; (I-M) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 4.
Juvenile Stage II of Austropotamobius torrentium. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) flagellum of antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view, (J) pleopod. cd, caudal process; cp, cephalic process; in, incisor ridge. Scale bars: 0.25 mm.

Carapace more elongated and containing less yolk (Fig. 3A), eye peduncle developed, rostrum straighter than in previous stage, longer and down-curved, acumen with single pair of small tubercles and spines derived from first pair of postorbital ridges (Fig. 3B). Telson large, rounded (Fig. 3C), with 2 kinds of setae; about 51-53 long plumose setae and 15-18 simple setae on posterior margin.

Juvenile with prominent, slightly curved spine at tip and teeth along mesial margin of fingers of cheliped (Fig. 3D, I), second (Fig. 3E, J), and third (Fig. 3F, K) pereiopods. Fourth (Fig. 3G, L) and fifth (Fig. 3H, M) pereiopods with slightly curved ungues on dactylopodite. Large spine on tip and long simple setae on dorsal and ventral sides of dactylopodite of fourth and fifth pereiopods (Fig. 3L, M). Long simple setae cover all pereiopods.

Antenna 1 (Fig. 4A): 5-7 segments on external and 4-7 segments on internal flagellum; both flagella having simple setae on apical region, lateral and mesial margins. Antennal scale (Fig. 4B) with long plumose setae on mesial margin. Antenna 2 (Fig. 4C): flagellum consisting of approximately 42-49 segments and 2-3 simple setae at apex of final segment on lateral and medial sides of joints.

Mandible (Fig. 4D): dentition consisting of large tubercles on margin of incisor ridge with cornified caudal processes and cephalic processes on molar ridge. Coxopodite, basipodite, and endopodite of maxilla 1 (Fig. 4E) with developing segmentation, bearing long simple setae. Outer margin of exopodite of maxilla 2 (Fig. 4F) with single longer multidenticulate setae on caudal margin.

First maxilliped (Fig. 4G): internal margin of basiopodite with cuspidate setae and internal margin of coxopodite with pappose setae; endite elongated with pappose setae; distal margin of exopodite with plumose setae. Second maxilliped (Fig. 4H): terminal margin of dactylopodite of endopodite with cuspid setae, and external margin of basipodite and internal margin of meropodite and ischiopodite and basipodite with plumose setae; end of endopodite with plumose setae. Third maxilliped (Fig. 4I): terminal margin of dactylopodite of endopodite with long pappose setae, external and internal margins of propodite and internal margin of meropodite, ischiopodite, and basipodite with pappose setae, mesial margin of ischiopodite with pappose setae and row of toothed crests; exopodite with plumose setae on apical region.

All pleopods (representative second pleopod depicted in Fig. 4J) with long plumose setae on distal margin of endopod and exopod.

Stage III (Figs. 5, 6)

Figure 5.
Juvenile Stage III of Austropotamobius torrentium. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D-H), pereiopods 1-5, dorsal or lateral view; (I-M) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 6.
Juvenile Stage III of Austropotamobius torrentium. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) flagellum of antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bars: 0.25 mm, C: 1.0 mm.

Overall appearance similar to adults. Remains of yolk still present in carapace (Fig. 5A) and rostrum with acumen and spines derived from first pair of postorbital ridges on head (Fig. 5B).

Biramous uropods developed and telson forming 5-part tail-fan. Uropods same length as telson, with heavily setose edges; exopods of uropod having single spine on lateral side (Fig. 5C).

Pereiopods 1-3 having slightly curved terminal spines on dactylopodites and propodites (Fig. 5D-F, I-K). Fourth (Fig. 5G, L) and fifth (Fig. 5H, M) pereiopods with slightly curved spines at apex of dactylopodites. Long simple setae on dorsal and ventral sides of all pereiopods (Fig. 5D-M).

Antenna 1 (Fig. 6A): 5-segmented external and internal flagellae, both with simple setae in apical region and lateral and mesial margins. Antennal scale (Fig. 6B) with long plumose setae along mesial margins. Antenna 2 (Fig. 6C): flagellum of approximately 54-59 segments and 2-3 simple setae at apex of the last segment on lateral and medial sides of joint.

Mandible (Fig. 6D): dentition consisting of large tubercles on margin of incisor ridge with cornified caudal processes and cephalic processes on molar ridge. Coxopodite, basipodite and endopodite of maxilla 1 (Fig. 6E) with developing segmentation bearing plumose setae. Maxilla 2 (Fig. 6F): single longer multidenticulate setae on caudal margin of exopodite.

First maxilliped (Fig. 6G) bilobed; distal margin of exopodite with group of plumose setae. Second maxilliped (Fig. 6H) biramous; exopodite with plumose setae on terminal tip, endopodite with long setae along lateral and terminal margins. Third maxilliped (Fig. 6I) biramous; terminal margin of exopodite with plumose setae.

All pleopods (representative second pleopod depicted in Fig. 6J) having long plumose setae on distal margin of endopods and exopods.

Procambarus virginalis

Stage I (Figs. 7, 8)

Figure 7.
Juvenile Stage I of Procambarus virginalis. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan and telson thread, dorsal view; (D) posterior edge of the tail fan and telson thread; (E-I), pereiopods 1-5, dorsal or lateral view; (J-N) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 8.
Juvenile Stage I of Procambarus virginalis. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bars: 0.25 mm.

Globular carapace filled with yolk, red pigment on lateral and anterior parts of carapace; antenna 1 elongated and situated above antenna 2 (Fig. 7A), down-curved rostrum and sessile eyes (Fig. 6B).

Telson undifferentiated and elongated with notched terminal margin (Fig. 7C); telson margin with inner row of cuspidate setae, caudal margin with 23-29 curved, hook-like cuspidate setae (Fig. 7D). Freshly emerged juvenile remaining attached to inner lining of egg capsule by telson thread via terminal margin of its telson. Juveniles are attached to mother’s long pleopodal setae by specialized recurved spines on tips of their chelipeds (dactylopodites and propodites) (Fig. 7E, J). Second (Fig. 7F, K) and third (Fig. 7G, L) pereiopods with curved spines on terminal tips of dactylopodites and propodites. Fourth (Fig. 7H, M) and fifth (Fig. 7I, N) pereiopods having slightly curved spines at apex of dactylopodites. Dactylopodites of fourth and fifth pereiopod with slightly curved spines (Fig. 7M, N). Pereiopods often having setal precursors (Fig. 7E-I).

Antenna 1 (Fig. 8A): internal and external flagellae bearing four segments; no setae except on distal segments; distal segments bearing few minute setal precursors. Mesial margin of antennal scale (Fig. 8B) with several long setal precursors. Antenna 2 (Fig. 8C): flagellum consisting of approximately 21 segments, with setal precursors at apex of final segment.

Mandibles (Fig. 8D) lacking setae, processes and teeth on cutting edge of incisor ridge and molar ridge; mandibular palp 3-segmented; distal margin of terminal segment with connate setae. Coxopodites, basipodites, and endites of maxilla 1 (Fig. 8E) at beginning of segmentation; setal precursors on distal margin of basipodite and coxopodite. Maxilla 2 (Fig. 8F): biramous basipodites and coxopodites, endites and leafy exopodites.

First maxilliped (Fig. 8G): coxopodite and basipodite, endite, exopodite and epipodite. Exopodite bearing setal precursor at tip and pappose setae along proximal-external margin. Second maxilliped (Fig. 8H) biramous; terminal margin of dactylopodite with sub-apical setal precursor, external margin of propodite, internal margin of meropodite, ischiopodite, propodite with small-toothed crest, exopodite with setal precursors on apical region. Third maxilliped (Fig. 8I) biramous; dactylopodite of coxopodite with sub-apical setal precursor, internal margin of propodite and ischiopodite bearing single row of small teeth; exopodite with no setal precursors.

All pleopods (representative second pleopod depicted in Fig. 8J) have setal precursors on endopod and on exopod.

Stage II (Figs. 9, 10)

Figure 9.
Juvenile Stage II of Procambarus virginalis. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D-H) pereiopods 1-5, dorsal or lateral view; (I-M) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 10.
Juvenile Stage II of Procambarus virginalis. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) flagellum of antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bar: 0.25 mm.

Carapace more elongated and containing less yolk (Fig. 9A), eye peduncle developed, rostrum straighter than in previous stage, longer and down-curved, acumen with single pair of small tubercles and spines derived from the first pair of postorbital ridges (Fig. 8B). Telson elongated (Fig. 9C) and margin with 15-20 plumose setae and 4-8 simple setae. Simple setae all over body and appendage surfaces.

Curved spines at tips of chelipeds (Fig. 9D, I), slightly curved spine on second (Fig. 9E, J) and third pereiopods of dactylopodite and propodite (Fig. 9F, K). Fourth (Fig. 9G, L) and fifth (Fig. 9H, M) pereiopods with large spines at apex of dactylopodite, row of long simple setae along the cephalo-ventral margin of the dactylopodite of fourth and fifth pereiopods (Fig. 9L, M). Low density long simple spines cover all pereiopods.

Antenna 1 (Fig. 10A): 5-6 segments of exopodite and endopodite, both with long simple setae on apical region, and on lateral and mesial sides of joint. Antennal scale (Fig. 10B) with long plumose setae on mesial margin. Antenna 2 (Fig. 10C): flagellum consisting of approximately 26-29 segments with 2-3 simple setae at apex of final segment and on lateral and mesial sides of joint of segment; terminal segment thinner.

Mandible (Fig. 10D): dentation with large tubercles on margin of incisor ridge, caudal process and cephalic process on molar ridge. Coxopodite, basipodite, and endite on maxilla 1 (Fig. 10E) having developing segmentation bearing long simple setae. Maxilla 2 (Fig. 10F): no long setae on margin of exopodite.

First maxilliped (Fig. 10G): internal margin of basiopodite with cuspid setae and internal margin of coxopodite with pappose setae; endite elongated without setae; exopodite segmented, plumose setae at tip of distal segment; pappose setae on external and internal margins. Second maxilliped (Fig. 10H): weak setation on endopodite; terminal margin of dactylopodite and mesial margin of meropodite having pappose setae; internal margin of ischiopodite with simple setae and row of tubercles; exopodite with segmentation on distal and proximal halves; end of distal half with long plumose setae. Third maxilliped (Fig. 10I): no dense setation on endopodite; tip of dactylopodite and mesial margin of meropodite with pappose setae; inner margin of ischiopodite with toothed crest; exopodite having segmented terminal half and unsegmented proximal half, apical tip of terminal half with group of long plumose setae.

All pleopods (representative second pleopod depicted in Fig. 10J) with setal precursor at tip of endopod and exopod.

Stage III (Figs. 11, 12)

Figure 11.
Juvenile Stage III of Procambarus virginalis. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D-H) pereiopods 1-5, dorsal or lateral view; (I-M) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 12.
Juvenile Stage III of Procambarus virginalis. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) flagellum of antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bars: 0.25 mm.

This stage is similar to the adult. Body and all appendages covered with numerous small setae, remains of yolk still present in carapace (Fig. 11A). Rostrum with 1 pair of spines and postorbital ridges (Fig. 11B).

Biramous uropods developed, and with telson, form 5-part tail fan (Fig. 11C).

Slightly curved spines on tips of dactylopodite and propodite of pereiopods 1-3 (Fig. 11D-F, I-K). Fourth (Fig. 11G, L) and fifth (Fig. 11H, M) pereiopods with slightly curved spines at apex of dactylopodite. Long simple setae appearing on dorsal and ventral pereiopods 1-5 (Fig. 11D-M).

Antenna 1 (Fig. 12A): 5-8 exopodite and endopodite segments, both with long simple setation on apical region and on lateral and mesial sides of joint. Antennal scale (Fig. 12B) with long plumose setae on mesial margin. Antenna 2 (Fig. 12C): not bent downward, flagellum consisting of approximately 26-29 segments with 2-3 simple setae at apex of last segment and on lateral and mesial sides of segment joint.

Mandible (Fig. 12D): dentition with large tubercles on margin of incisor ridge with caudal process and cephalic process on single lip of molar ridge. Coxopodite, basipodite, and endite of maxilla 1 (Fig. 12E) with developing segmentation; distal margin of coxopodite and basiopodite with short cuspidate setae and plumose setae; endite elongated with simple setae on distal margin. Maxilla 2 (Fig. 12F) biramous, appendages consisting of the basiopodite with endites, and exopodite. Distal margin of basiopodite with pappose setae, terminal margin of distal and proximal endite with simple setae. Exopodite elongated with pappose setae along outer margin.

First maxilliped (Fig. 12G): bilobed; internal margin of basiopodite with cuspid setae; internal margin of coxopodite with pappose setae; endite elongated with no setae; exopodite with plumose setae on end of distal segment; external margin of proximal segment with pappose setae. Second maxilliped (Fig. 12H): biramous appendage; endopodite and exopodite with pappose and simple setae, respectively; end of distal half with long pappose setae. Third maxilliped (Fig. 12I): biramous appendage; both appendages having long pappose setae and long simple setae; end of exopodite with plumose setae.

All pleopods (representative second pleopod depicted in Fig. 12J) with setal precursor at end of endopod and exopod.

Cambaroides japonicus

Stage I (Figs. 13, 14)

Figure 13.
Juvenile Stage I of Cambaroides japonicus. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan and telson thread, dorsal view; (D) posterior edge of the telson and telson thread; (E-I), pereiopods 1-5, dorsal or lateral view; (J-N) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 14.
Juvenile Stage I of Cambaroides japonicus. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view, (J) pleopod. Scale bars: 0.25 mm.

Globular carapace filled with yolk, red pigment on lateral and anterior parts of carapace; antenna 1 elongated and situated above antenna 2 (Fig. 13A), rostrum down-curved, eyes sessile (Fig. 13B).

Telson rounded, with terminal notch (Fig. 13C), tail-fan consisting of telson only and undifferentiated; telson margin with approximately 60 sub-terminal cuspidate setae and terminal curved hook-like cuspidate setae (Fig. 13D). Recurved spines on tips of chelipeds (dactylopodite and propodite) (Fig. 13E, J). Second (Fig. 13F, K) and third (Fig. 13G, L) pereiopods with curved spines on tips of dactylopodite and propodite. Fourth (Fig. 13H, M) and fifth (Fig. 13I, N) pereiopods having slightly curved spines at apex of dactylopodite. Pereiopods often having setae precursors (Fig. 13E, F).

Antenna 1 (Fig. 14A): 4 or 5 segments on internal and external flagella, distal segments bear a few setal precursors. Mesial margin of antennal scale (Fig. 14B) with several long setal precursors. Antenna 2 (Fig. 14C): flagellum with approximately 21 segments, setae precursors on segmental joints and connate setal precursor at apex of terminal segment.

Mandible (Fig. 14D) lacking setae, processes and teeth along incisor edge and molar ridge; mandibular with 3-segmented palp; distal margin of terminal segment with connate setae. Coxopodite, basipodite, and endite of maxilla 1 (Fig. 14E) with beginning of segmentation; long setae on proximal part of endite. Maxilla 2 (Fig. 14F) with biramous basipodite and coxopodite, endite and elongated exopodite. Exopodite elongated with pappose setae along margin.

First maxilliped (Fig. 14G): 5-segmented endopodite and segmented exopodite, coxopodite and basipodite; internal margins with setal precursors, endite elongated with no setal precursors, distal margin of exopodite with setal precursors, proximal-lateral margin having pappose setae; epipodite, leaf-like, elongated. Second maxilliped (Fig. 14H): biramous; internal and external margins, terminal margin of dactylopodite with sub-apical setal precursors; external margin of propodite, internal margin of meropodite, ischiopodite and propodite with small-toothed crests; exopodite having setal precursors on apical region. Third maxilliped (Fig. 14I): biramous; no setae, exopodite reaching meropodite; terminal margin of dactylopodite with sub-apical setal precursors, internal margin of propodite and meropodite with setal precursors and ischiopodite bearing row of teeth along mesial margin.

All pleopods (representative second pleopod depicted in Fig. 14J) with setal precursors at tip of endopod and on exopod.

Stage II (Figs. 15, 16)

Figure 15.
Juvenile Stage II of Cambaroides japonicus. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D) posterior edge of tail fan; (E-I) pereiopods 1-5, dorsal or lateral view; (J-N) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 16.
Juvenile Stage II of Cambaroides japonicus. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bars: 0.25 mm.

Carapace more elongated and yolk scarce (Fig. 15A), eyes with developed peduncle, triangular-shaped rostrum straighter than in previous stage, down-curved with no spines or ridges (Fig. 15B). Telson rounded with notched posterior margin (Fig. 15C), caudal margin with approximate 54 plumose setae and 23 simple setae. Simple setae distributed all over the surface of body and appendages.

Prominent spines at tips of chelipeds (Fig. 15D, I); second (Fig. 15E, J) and third (Fig. 15F, K) pereiopods possessing slightly curved spines on tips of dactylopodite and propodite. Fourth (Fig. 15G, L) and fifth (Fig. 15H, M) pereiopods with slightly curved spines at apex of dactylopodite. Long simple spines cover all pereiopods.

Antenna 1 (Fig. 16A): 4-segmented internal and external flagellae, both with long simple setae at apical region and on lateral and mesial margins. Antennal scale (Fig. 16B) with long plumose setae on mesial margin. Antenna 2 (Fig. 16C): straight, flagellum consisting of approximately 26-29 segments with 2-3 simple setae at the apex of terminal segment and on lateral and mesial sides of joint.

Mandible (Fig. 16D): dentition with large tubercles on margin of incisor ridge, cornified caudal process and cephalic process on molar ridge. Coxopodite, basipodite, and endite of maxilla 1 (Fig. 16E) with developing segmentation bearing plumose setae. Exopodite of maxilla 2 (Fig. 16F) with pappose setae along outer margin and 2 longer multidenticulate setae on caudal margin.

First maxilliped (Fig. 16G): bilobed; internal margin of basiopodite with cuspid setae, internal margin of coxopodite with pappose setae, elongated endite, segmented exopodite, plumose setae on terminal end of distal segment; external and internal margin of proximal segment with pappose setae. Second maxilliped (Fig. 16H): biramous; terminal and internal margins of endopodite with pappose setae, segmented exopodite on distal and proximal half, terminal region of distal half with long pappose setae. Third maxilliped (Fig. 16I): biramous; tip and mesial margin of endopodite with pappose setae; exopodite with plumose setae at tip.

All pleopods (representative second pleopod shown in Fig. 16J) with long plumose setae at tip of endopod and exopod.

Stage III (Figs. 17, 18)

Figure 17.
Juvenile Stage III of Cambaroides japonicus. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D) posterior edge of tail fan; (E-I) pereiopods 1-5, dorsal or lateral view; (J-N) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.5 mm in A-C, 0.25 mm in D-M.

Figure 18.
Juvenile Stage III of Cambaroides japonicus. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bars: 0.25 mm.

The adult stage. Body and all appendages covered with numerous small setae, remains of yolk still present (Fig. 17A), triangular rostrum and postorbital ridge similar to adult (Fig. 17B). Antenna 2 with 2-3 simple setae at apex of final segment and on lateral and medial sides of joint (Fig. 17A).

Biramous uropods developed and telson forming 5-part tail-fan (Fig. 17C).

Juvenile with slightly curved spines on terminal parts of dactylopodite and propodite of pereiopods 1-3 (Fig. 17D-F, I-K). Fourth (Fig. 17G, L) and fifth (Fig. 17H, M) pereiopods with slightly curved spines at apex of dactylopodite. Long simple setae on dorsal and ventral pereiopods 1-5 (Fig. 17D-M).

Antenna 1 (Fig. 18A): 6 segments on internal and 5 segments on external flagellum, both with long simple setae on apical region and lateral and mesial margins. Antennal scale (Fig. 18B) with long plumose setae on mesial margin. Antenna 2 (Fig. 18C): flagellum consisting of approximately 51-57 segments with 2-3 simple setae at apex of terminal segment and on lateral and mesial sides of segment joint.

Mandible (Fig. 18D): dentition consists of large tubercles on margin of incisor ridge with cornified caudal processes and cephalic process on molar ridge. Coxopodite, basipodite, and endite of maxilla 1 (Fig. 18E) with developing segmentation bearing plumose setae. Exopodite of maxilla 2 (Fig. 18F) with 2 long multidenticulate setae on caudal margin.

First maxilliped (Fig. 18G): bilobed; cuspid setae, endite with no setae, terminal end of exopodite with plumose setae. Second maxilliped (Fig. 18H): biramous; terminal margin and internal margin of endopodite with pappose setae, exopodite segmented on distal and proximal half, end of distal half with long plumose setae. Third maxilliped (Fig. 18H): biramous; tip region and mesial margin of endopodite with pappose setae; exopodite having plumose setae at tip.

All pleopods (representative second pleopod depicted in Fig. 18J) with long plumose setae at tip of endopod and exopod.

Cherax destructor

Stage I (Figs. 19, 20)

Figure 19.
Juvenile Stage I of Cherax destructor. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D) posterior edge of tail fan; (E-I) pereiopods 1-5, dorsal or lateral view; (J-N) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 20.
Juvenile Stage I of Cherax destructor. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bars: 0.25 mm.

Globular carapace filled with yolk; red pigment present on lateral and anterior parts of carapace, antenna 1 elongated and situated above antenna 2 (Fig. 19A), down-curved rostrum and sessile eyes (Fig. 19B).

Telson undifferentiated with sub-rectangular rounded border, devoid of setae (Fig. 19C); sub-terminal row of small tubercles (Fig. 19D).

Tip of dactylopodite and propodite of first (Fig. 19E, J), second (Fig. 19F, K), and third pereiopod (Fig. 19G, L) with slightly curved spines. Fourth pereiopod (Fig. 19H, M) and fifth pereiopod (Fig. 19I, N) with recurved hooked spines on tip of propodite. Juvenile attached to mother’s long pleopodal setae by specialized recurved spines. Pereiopods often having setal precursors (Fig. 19E-N).

Antenna 1 (Fig. 19A): 8 segments on internal and external flagellum, no visible setae except on distal segments that bear 2-3 minute setal precursors. Mesial margin of antennal scale (Fig. 19B) with several apical setal precursors. Antenna 2 (Fig. 19C): flagellum consisting of approximately 26-28 segments with 3-4 setal precursors at apex of terminal segment.

Mandible (Fig. 19D): no setae, processes or teeth on cutting edge of incisor ridge; mandibular palp 3-segmented and distal margin of terminal segment with connate setae. Coxopodite, basipodite and endite of maxilla 1 (Fig. 19E) with incipient segmentation; setal precursors on distal margin of basipodite and coxopodite. Maxilla 2 (Fig. 19F): biramous, 3 long multidenticulate setae situated on caudal margin of exopodite.

First maxilliped (Fig. 19G): medial coxopodite and basipodite, endite, exopodite and epipodite. Distal margin of the exopodite with setal precursors and proximal-external margin with pappose setae. Second maxilliped (Fig. 19H): biramous; 5-segmented endopodite and unsegmented exopodite. Dactylopodite with setal precursors on apical marginal; exopodite having setal precursors on apical region and internal and external margins. Third maxilliped (Fig. 19I): biramous; 5-segmented endopodite and segmented exopodite. Endopodite with almost no setal precursors and setae; exopodite with setal precursors on apical region.

All pleopods (representative second pleopod depicted in Fig. 19J) with setal precursors on endopod and exopod.

Stage II (Figs. 21, 22)

Figure 21.
Juvenile Stage II of Cherax destructor. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D) posterior edge of tail fan; (E-I) pereiopods 1-5, dorsal or lateral view; (J-N) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 22.
Juvenile Stage II of Cherax destructor. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bars: 0.25 mm.

Carapace more elongated, containing less yolk (Fig. 21A), developed eye peduncle, rostrum down-curved and longer straighter than in previous stage, and triangle-shaped with no spines or setae (Fig. 21B). Sub-rectangular telson (Fig. 21C); caudal margin with single row of approximately 20 tubercles (Fig. 21D).

Juvenile with slightly curved spines at tips of chelipeds (Fig. 21E, J), second (Fig. 21F, K) and third (Fig. 21G, L) pereiopods. Curved spines on tips of dactylopodite of fourth (Fig. 21H, M) and fifth (Fig. 21I, N) pereiopods. Row of longer aesthetasc setae on ventral margin of dactylopodite of fourth and fifth pereiopod (Fig. 21M, N). Most pereiopods having almost no setae; long and simple spines on tip of pereiopods 1-3.

Antenna 1 (Fig. 22A): external and internal flagellae with 8-9 segments; external flagellum with setal precursors on mesial margins of distal segment. Antennal scale (Fig. 22B) with single row of setal precursors on mesial margin. Antenna 2 (Fig. 22C): not bent downwards, with flagellum consisting of approximately 39-41 segments with 2-3 simple setal precursors at apex of final segment.

Mandible: distal edge bearing large dentition along incisor ridge, small proximal processes on molar ridge, and external margin of terminal segment of mandibular palp with long simple setae (Fig. 22D). Coxopodite, basipodite, and endite of maxilla 1 (Fig. 22E) with developing segmentation bearing plumose setae. Expodite of maxilla 2 (Fig. 22F) having pappose setae along its outer margin, with 3 long multidenticulate setae on caudal margin.

First maxilliped (Fig. 22G): bilobed; internal margin of basipodite and coxopodite with pappose setae, endite elongated with simple setae, exopodite with setal precursors at tip, external margin of proximal segment with pappose setae. Second maxilliped (Fig. 22H): biramous; 5-segmented endopodite and exopodite, terminal margin of dactylopodite with cuspid setae, and external margin of protopodite and internal margins of meropodite and ischiopodite with pappose setae; lateral margin of proximal half of exopodite with pappose setae and tip of distal half with setal precursors. Third maxilliped (Fig. 22I): biramous; 5-segmented endopodite and segmented exopodite, terminal region and inner margin of endopodite with pappose setae; tip of exopodite having setal precursors on apex region.

All pleopods (representative second pleopod depicted in Fig. 22J) having setal precursors in terminal region of endopod and exopod.

Stage III (Figs. 23, 24)

Figure 23.
Juvenile Stage III of Cherax destructor. (A) Habitus, lateral view; (B) eyes and rostrum, dorsal view; (C) tail fan, dorsal view; (D-H) pereiopods 1-5, dorsal or lateral view; (I-M) distal segments of pereiopods 1-5, dorsal or lateral view. Scale bars: 0.25 mm.

Figure 24.
Juvenile Stage III of Cherax destructor. (A) Antenna 1, dorsal view; (B) antennal scale, dorsal view; (C) flagellum of antenna 2, dorsal view; (D) mandible, view of inside of mouth; (E) maxilla 1, oral view; (F) maxilla 2, oral view; (G) first maxilliped, oral view; (H) second maxilliped, oral view; (I) third maxilliped, oral view; (J) pleopod. Scale bars: 0.25 mm.

Similar in appearance to adults. Remains of yolk still present (Fig. 23A); rostrum with short setae (Fig. 23B).

Biramous uropods developed; telson forming 5-part tail-fan. Uropods with heavily setose edges (Fig. 23C).

Pereiopods 1-3 with slightly curved spines at tip of dactylopodite and propodite (Fig. 23D-F, I-K). Fourth (Fig. 23G, L) and fifth (Fig. 23H, M) pereiopods with slightly curved spines at apex of dactylopodite. Long simple setae on dorsal and ventral sides of all pereiopods (Fig. 23E-M).

Antenna 1 (Fig. 24A): 11-segment internal and external flagella; external flagellum with simple setae on mesial margins of most distal segments. Antennal scale (Fig. 24B) having row of plumose setae on mesial margin. Antenna 2 (Fig. 24C): flagellum consisting of approximately 68-73 segments with 2-3 simple setae at apex of last segment.

Mandible: distal edge bearing large dentition along incisor ridge; molar ridge with two proximal cornified processes (Fig. 24D). Coxopodite, basipodite, and endite of maxilla 1 (Fig. 24E) with developing segmentation bearing plumose setae. Exopodite of maxilla 2 having 3 long multidenticulate setae on caudal margin (Fig. 24F).

First maxilliped (Fig. 24G): bilobed; tip and external margin of proximal segment of exopodite with plumose setae. Second maxilliped: (Fig. 24H) biramous; exopodite having segmented distal and proximal halves; terminal end and distal margin of distal half segment bearing plumose setae. Third maxilliped: (Fig. 24I) biramous; terminal end of exopodite with plumose setae.

All pleopods (representative second pleopod depicted in Fig. 24J) having plumose setae on terminal region and on distal half of outer margin of endopod and exopod.

DISCUSSION

This article is a contribution to previous studies of the morphology of early juvenile stages of freshwater Astacidae species and confirms earlier published work (for categorization by families, see Tabs. 1 - 4). The morphology of the postembryonic developmental stages of all crayfish families is summarized in Tab. 5. This accumulation of knowledge now allows us to identify new diagnostic features in juveniles at the suborder (freshwater crayfish: Astacidea), superfamily (Astacoidea and Parastacoidea) and family (Astacidae, Cambaridae, Cambaroididae, and Parastacidae) levels. The following characteristics were found to be common to all Astacidea (Tab. 5): sessile eyes in Stage I and eye stalks developing from Stage II onwards; globular carapace in Stage I and carapace more similar to adults in Stage II; teeth and processes of mandible absent in Stage I but developed in Stage II; setae on pereiopod absent in Stage I but long setae present in Stage II. To these can be added three characters (telson, telson thread, terminal tip of pereiopod) previously known to be diagnostic at the subordinal level (Scholtz, 1995Scholtz, G. 1995. The attachment of the young in the New Zealand freshwater crayfish Paranephrops zealandicus (White, 1847) (Decapoda, Astacida, Parastacidae). New Zealand Natural Science, 22: 81-89.; 1999Scholtz, G. 1999. Freshwater crayfish evolution. Freshwater Crayfish, 12 : 37-48.).

Table 1.
Comparison of the morphology of postembryonic stages of European Astacidae and American Astacidae.
Table 2.
Comparison of the morphology of postembryonic stages of Cambaridae
Table 3.
Comparison of the morphology of postembryonic stages of Cambaroididae members.
Table 4.
Comparison of the morphology of each postembryonic stage of Parastacidae members.
Table 5.
Comparison of morphology and seta on appendages of each postembryonic stage in all four families of freshwater crayfish.

At the superfamily level, additional new apomorphic features include: i) the presence of developed plumose setae on antenna 1 and 2, with an antennal scale in Stage II in Astacoidea; conversely, Parastacoidea lack setae on antenna 1-2; ii) the presence of plumose setae on the exopodite of maxilliped segments 1-3 in Astacoidea in Stage II but not in Parastacoidea, which lack these setae at this stage (Tab. 5).

Apomorphies at the family level include the single long multidenticulate seta on the distal part of maxilla 2 in Astacidae, the absence of any long multidenticulate setae on the distal part of maxilla 2 in Cambaridae, two long multidenticulate setae on the distal part of maxilla 2 in Cambaroididae, and 1 or 3 long multi-denticulate setae on the distal part of maxilla 2 in Parastacidae (Tab. 5). Previous studies have failed to reveal any family-level diagnostic characters (Andrews, 1907aAndrews, E.A. 1907a. The young crayfishes of the Astacus and Cambarus. Smithsonian Contributions to Knowledge, 35: 1-79.; Hamr, 1992Hamr, P. 1992. Embryonic and postembryonic development in the Tasmanian freshwater crayfishes Astacopsis gouldi, Astacopsis franklinii and Parastacoides tasmanicus tasmanicus (Decapoda: Parastacidae). Australian Journal of Marine and Freshwater Research, 43: 861-878.; Ko and Kawai, 2001Ko, H.S. and Kawai, T. 2001. Postembryonic development of the Korean crayfish, Cambaroides similis (Decapoda, Cambaridae) reared in the laboratory. The Korean Journal of Systematic Zoology, 17: 35-47.) in the postembryonic developmental stages of crayfish.

Traditional phylogenetic relationships based on the morphology of genital organs (first male pleopod, hook on ischia of male pereiopod, female annulus ventralis) suggest that Cambaridae comprise both American Cambaridae and Asian freshwater crayfish of the genus CambaroidesFaxon, 1884Faxon, W. 1884. Descriptions of new species of Cambarus, to which is added a synonymical list of the known species of Cambarus and Astacus. Proceedings of the American Academy of Arts and Sciences, 20: 107-158. (Hobbs, 1988Hobbs, H.H. Jr. 1988. Crayfish distribution, adaptation, and evolution. p. 52-82. In: D.M. Holdich and D.M. Lowery (eds), Freshwater Crayfish: Biology, Management and Exploitation. London, Croom Helm.). This disjunct distribution of these two freshwater crayfish groups does not agree with the zoogeographic evidence. Recent studies have cast doubts on this view and suggest, instead, that American Cambaridae and Cambaroides are two distinct families (Braband et al., 2006Braband, A.; Kawai, T. and Scholtz, G. 2006. The phylogenetic position of the East Asian freshwater crayfish Cambaroides within the Northern Hemisphere Astacoidea (Crustacea, Decapoda, Astacida) based on molecular data. Journal of Zoological Systematics and Evolutionary Research, 44: 17-24.; Crandall and De Grave, 2017Crandall, K.A. and De Grave, S. 2017. An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. Journal of Crustacean Biology, 37: 615-653.; Grandjean et al., 2017Grandjean, F.; Mun, H.T.; Han, M.G.; Yin, P.L.; Kawai, T.; Distefano, R.J.; Martin, B.; Roles, A.J. and Austin, C.M. 2017. Rapid recovery of nuclear and mitochondrial genes by genome skimming from Northern Hemisphere freshwater crayfish, Zoologica Scripta, 46: 718-728.). Postembryonic development in Asian Cambaroididae shows unique characters in its four crayfish families: antenna 2 has 25-39 segments in Stage I, the telson is rounded and has approximately 55 setae in Stage I; and there are two long multidenticulate setae present on the distal part of maxilla 2 in Stage II (Tab. 3). A phylogenetic tree based on apomorphic characters of juveniles according to their families matches the phylogenetic tree based on molecular data (Fig. 25).

Figure 25.
Phylogenetic tree of freshwater crayfish, Astacidea, with diagnostic morphological features in postembryonic stages. Basic phylogenetic tree constructed using recent molecular studies (Crandall et al., 2000Crandall, K.A. Harris, D.J. and Fetzner, J.W. 2000. The monophyletic origin of freshwater crayfish estimated from nuclear and mitochondrial DNA sequences. Proceedings of the Royal Society B, 267(1453): 1679-1686.; Porter et al., 2005Porter, M.L.; Pérez-Losada, M. and Crandall, K.A. 2005. Model-based multi-locus estimation of decapod phylogeny and divergence times. Molecular Phylogenetics and Evolution, 37: 355-369.; Bracken et al., 2009Bracken, H.D.; Toon, A.; Felder, D.L.; Martin, J.W.; Finley, M.; Rasmussen, J.; Palero, F. and Crandall, K.A. 2009. The Decapod tree of life: compiling the data and moving toward a consensus of Decapod evolution. Arthropod Systematics & Phylogeny, 67: 99-116.; Breinholt et al., 2009Breinholt, J.; Pérez-Losada, M. and Crandall, K.A. 2009. The timing of the diversification of the freshwater crayfishes. p. 343-355. In: J.W. Martin; K.A. Crandall and D.L. Felder (eds), Decapod Crustacean Phylogenetics. Crustacean Issues 18, Boca Raton, FL, CRC Press.; Pérez-Losada et al., 2010Pérez-Losada, A.M.; Schweitzer, C.E.; Feldmann, R.M.; Carlson, M. and Crandall, K.A. 2010. Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules. Journal of Biogeography, 37(12): 2275e2290.; Toon et al., 2010Toon, A.; Pérez-Losada, M.; Schweitzer, C.E.; Feldmann, R.M.; Carlson, M. and Crandall, K.A. 2010. Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules. Journal of Biogeography, 37: 2275-2290. ; Stern and Crandall, 2016Stern, D. and Crandall, K.A. 2016. Phylogenetic estimate of the freshwater crayfish (Decapoda: Astacidea) using morphology and molecules. p. 298-309. In: T. Kawai; Z. Faulkes and G. Scholtz (eds), Freshwater Crayfish: a Global Overview. Boca Raton, FL, CRC Press .; Crandall and De Grave, 2017Crandall, K.A. and De Grave, S. 2017. An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. Journal of Crustacean Biology, 37: 615-653.; Grandjean et al., 2017Grandjean, F.; Mun, H.T.; Han, M.G.; Yin, P.L.; Kawai, T.; Distefano, R.J.; Martin, B.; Roles, A.J. and Austin, C.M. 2017. Rapid recovery of nuclear and mitochondrial genes by genome skimming from Northern Hemisphere freshwater crayfish, Zoologica Scripta, 46: 718-728.; Wolfe et al., 2019Wolfe, J.M.; Breinholt, J.W.; Crandall, K.A.; Lemmon, A.R.; Lemmon, E.M.; Timm, L.E.; Siddall, M.E. and Bracken-Grissom, H.D. 2019. A phylogenomic framework, evolutionary timeline and genomic resources for comparative studies of decapod crustaceans. Proceedings of the Royal Society B: Biological Sciences, 286: 20190079. https://doi.org/10.1098/rspb.2019.0079.
https://doi.org/10.1098/rspb.2019.0079...
). The bars on the tree represent the juvenile morphology as given in Tab. 1; a solid bar means presence and an open vertical bar absence. Numbers on the bar: 1: compound sessile eye in Stage I and developed eye stalk in Stage II; globular carapace in Stage I lost in Stage II; teeth and processes absent in Stage I but present in Stage II; setae absent on pereiopod in Stage I and long setae present in Stage II; 2: setae absent on antenna 1 and 2 with antennal scale in Stage I, and seta present in Stage II; no setae at tip of the exopodite of the maxilliped in Stage I; the plumose setae appear in Stage II; curved hook on terminal end of the pereiopod absent in Stage II; telson with plumose setae along cephalic margin; 3: maxilla 2 with 1 or 3 long setae in Stage II; 4: maxilla 2 with 2 long setae in Stage II; 5: maxilla 2 with 1 long setae in Stage II; 6: maxilla 2 with no long setae in Stage II.

The morphology of the juveniles of freshwater decapods occasionally reflects the evolutionary history of their adaptations to freshwater ecosystems (Anger, 2001Anger, K. 2001. The Biology of Decapod Crustacean Larvae. Crustacean Issues series 14. Netherland, A.A. Balkema, 419p.; Vogt, 2008Vogt, G. 2008. Investigation of hatching and early post-embryonic life of freshwater crayfish by in vitro culture, behavioral analysis, and light and electron microscopy. Journal of Morphology, 269: 790-811.). The abbreviation of embryonic development (or direct development), i.e., the hatching of larger and more advanced individuals lacking larval stages, reduces the risk of being washed away and/or predated (Hancock, 1998Hancock, M.A. 1998. The relationship between egg size and embryonic and larval development in the freshwater shrimp Paratya australiensis Kemp (Decapoda: Atyidae). Freshwater Biology, 39: 715-723.). Maternal care increases the survival of early juveniles (Mohamed et al., 2015Mohamed, A.; Awaad, E.S.; Samir, Z.; Kalid, A.D. and Mohammed, G. 2015. Egg incubation and post-embryonic development in the red swamp crayfish Procambarus clarkii from the River Nile, Egypt. International Journal of Advanced Research, 3(8): 281-289. ). Juveniles are attached to their mother’s pleopod by means of the telson thread and recurved hooks on the tip of the pereiopod 1 (cheliped) in Astacoidea, and recurved hooks on the tip of pereiopods 4-5 in Parastacoidea (Huxley, 1880Huxley, T.H. 1880. The crayfish. An Introduction to the Study of Zoology. London, C. Kegan Paul and Co., 371p.; Scholtz, 1995Scholtz, G. 1995. The attachment of the young in the New Zealand freshwater crayfish Paranephrops zealandicus (White, 1847) (Decapoda, Astacida, Parastacidae). New Zealand Natural Science, 22: 81-89.; Vogt, 2012Vogt, G. 2012. Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda. Biological Reviews, 88: 81-116.). Independent juveniles develop toothed mouthparts for manipulating prey (Kawai, 2012Kawai, T. 2012. Morphology of the mandible and gill of the Asian freshwater crayfish Cambaroides (Decapoda: Cambaridae) with implications for their phylogeny. Journal of Crustacean Biology, 32: 15-23.) and sensory organs for searching for food and for escaping from larger predators (Vogt, 2002Vogt, G. 2002. Functional anatomy. p. 53-151. In: D.M. Holdich (ed.), Biology of Freshwater Crayfish. Oxford, Blackwell Science.). The compound eye in independent juveniles is essential for searching for a shelter or burrow and fleeing from predators (Vogt, 2002Vogt, G. 2002. Functional anatomy. p. 53-151. In: D.M. Holdich (ed.), Biology of Freshwater Crayfish. Oxford, Blackwell Science.). Crustaceans receive external sensory input through cuticular hair organs known as setae (Laverack, 1988Laverack, M.S. 1988. The nervous system of Crustacea with special reference to the organization of the sensory system. p. 323-351. In: M.A. Ali (ed), Nervous Systems in Invertebrates. NY, Platinum Press.; Derby, 1989Derby, C.D. 1989. Physiology of sensory neurons in morphologically identified cuticular sensilla of crustaceans, p. 27-47. In: B. Felgenhauer; L. Watling and A.B. Thistle (eds), Functional Morphology of Feeding and Grooming in Crustacea. Crustacean Issues, 6. Rotterdam, A.A. Balkema Publishers.), which are found all over their body surfaces, including the antenna, pereiopods and telson, and provide a wide range of chemosensory functions (Felgenhauer and Abele, 1983Felgenhauer, B.E. and Abele, L.G. 1983. Ultrastructure and functional morphology of feeding and associated appendages in the tropical freshwater shrimp Atya innocuous (Herbst) with notes on its ecology. Journal of Crustacean Biology, 3: 336-363.; Watling, 1989Watling, L. 1989. A classification system for crustacean setae based on the homology concept. p. 15-26. In: B. Felgenhauer; L. Watling and A.B. Thistle (eds), Functional Morphology of Feeding and Grooming in Crustacea. Crustacean Issues, 6. Rotterdam, A.A. Balkema Publishers .) and hydrodynamic reception (Vogt, 2002). Chemosensors are needed to forage for food, while hydrodynamic stimuli provide an important source of information such as the presence and movement of predators and prey (Vogt, 2002Vogt, G. 2002. Functional anatomy. p. 53-151. In: D.M. Holdich (ed.), Biology of Freshwater Crayfish. Oxford, Blackwell Science.; Vogt and Tolley, 2004Vogt, G. and Tolley, L. 2004. Brood care in freshwater crayfish and relationship components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. Journal of Morphology, 262: 286-311.; Vogt et al., 2004Vogt, G; Tolley, L. and Scholtz, G. 2004. Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. Journal of Morphology, 261: 286-311.).

From Stage II onwards juvenile freshwater crayfish all have well-developed eyes, mandibles with teeth, and sensory setae on their pereiopods, which suggests that the ancestor of freshwater crayfish also enjoyed maternal care during Stage I, and then became independent in Stage II. Although the long setae on maxilla 1 and plumose setae on the pleopods develop in Stage I in Astacidae and Cambaroididae, long setae do not appear on maxilla 1 until Stage II, or plumose setae on pleopods until Stage III, in both Cambaridae and Parastacidae (Tab. 5). Albeit inconsistent with their phylogenetic relationship, this corresponds to a difference in the stage at which independence is reached: Astacidae and Cambaroididae become independent in Stage II (Albrecht, 1982Albrecht, H. 1982. Das System der europäischen Flußkrebse (Decapoda, Astacidae): Vorschlag und Begrün dung. Mitteilungen des Hamburgischen Zoologischen Museum und Institut, 79: 187-210.; Kawai and Scholtz, 2002Kawai, T. and Scholtz, G. 2002. Behavior of juvenile of the Japanese endemic species Cambaroides japonicus (Decapoda: Astacidea: Cambaridae), with observations on the position of the spermatophore attachment on adult females. Journal of Crustacean Biology, 22: 532-537.), while Cambaridae and Parastacidae are independent in Stage III (Andrews, 1907Andrews, E.A. 1907b. The attached young of the crayfish Cambarus clarkii and Cambarus diogenes. American Midland Naturalist, 41: 253-271, 2 pls.a; 1907bAndrews, E.A. 1907b. The attached young of the crayfish Cambarus clarkii and Cambarus diogenes. American Midland Naturalist, 41: 253-271, 2 pls.; Martin et al., 2010Martin, P.; Dorn, N.J.; Kawai, T.; van der Heiden, C. and Scholtz, G. 2010. The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870). Contributions to Zoology, 79: 107-118.; Price and Payne, 1984Price, J.O. and Payne, J.F. 1984. Postembryonic to adult growth and development in the crayfish Orconectes neglectus chaenodactylus Williams, 1952 (Decapoda, Astacidea). Crustaceana, 46: 176-194.; Rudolph and Rojas, 2003Rudolph, E. and Rojas, C.S. 2003. Embryonic and early postmembryonic development of the burrowing crayfish, Virilastacus araucanius (Faxon, 1914) (Decapoda, Parastacidae) under laboratory conditions. Crustaceana, 76: 835-850.; Scholtz, 1995Scholtz, G. 1995. The attachment of the young in the New Zealand freshwater crayfish Paranephrops zealandicus (White, 1847) (Decapoda, Astacida, Parastacidae). New Zealand Natural Science, 22: 81-89.).

The globular carapace of the earliest postembryonic stages is related to the storage of nutrients and energy reserves prior to the onset of exogenous feeding; this feature is typical of maternally dependent Stage I juveniles in Astacidea. The development of the eyes, mandibles and setae all contribute to independent lifestyles in the postembryonic stages of freshwater crayfish. The onset of independence is closely associated with morphological developments related to the development of exogenous feeding. It has been suggested that the development of these three morphological features provides evidence for the onset of independence in Astacidea juveniles from maternal care in Stage II. These four features can be placed onto a molecular phylogenetic tree and their geological history to examine the timing and place of extended maternal care in freshwater crayfish (Fig. 26).

Figure 26.
Estimate of the evolution of maternal care and accompanying postembryonic development in freshwater crayfish (Astacidea) based on juvenile morphology. The tree is based on other recent molecular phylogenetic trees (Crandall et al., 2000Crandall, K.A. Harris, D.J. and Fetzner, J.W. 2000. The monophyletic origin of freshwater crayfish estimated from nuclear and mitochondrial DNA sequences. Proceedings of the Royal Society B, 267(1453): 1679-1686.; Porter et al., 2005Porter, M.L.; Pérez-Losada, M. and Crandall, K.A. 2005. Model-based multi-locus estimation of decapod phylogeny and divergence times. Molecular Phylogenetics and Evolution, 37: 355-369.; Bracken et al., 2009Bracken, H.D.; Toon, A.; Felder, D.L.; Martin, J.W.; Finley, M.; Rasmussen, J.; Palero, F. and Crandall, K.A. 2009. The Decapod tree of life: compiling the data and moving toward a consensus of Decapod evolution. Arthropod Systematics & Phylogeny, 67: 99-116.; Breinholt et al., 2009Breinholt, J.; Pérez-Losada, M. and Crandall, K.A. 2009. The timing of the diversification of the freshwater crayfishes. p. 343-355. In: J.W. Martin; K.A. Crandall and D.L. Felder (eds), Decapod Crustacean Phylogenetics. Crustacean Issues 18, Boca Raton, FL, CRC Press.; Pérez-Losada et al., 2010Pérez-Losada, A.M.; Schweitzer, C.E.; Feldmann, R.M.; Carlson, M. and Crandall, K.A. 2010. Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules. Journal of Biogeography, 37(12): 2275e2290.; Stern and Crandall, 2016Stern, D. and Crandall, K.A. 2016. Phylogenetic estimate of the freshwater crayfish (Decapoda: Astacidea) using morphology and molecules. p. 298-309. In: T. Kawai; Z. Faulkes and G. Scholtz (eds), Freshwater Crayfish: a Global Overview. Boca Raton, FL, CRC Press .; Crandall and De Grave, 2017; Grandjean et al., 2017Grandjean, F.; Mun, H.T.; Han, M.G.; Yin, P.L.; Kawai, T.; Distefano, R.J.; Martin, B.; Roles, A.J. and Austin, C.M. 2017. Rapid recovery of nuclear and mitochondrial genes by genome skimming from Northern Hemisphere freshwater crayfish, Zoologica Scripta, 46: 718-728.) and molecular clocks (Toon et al., 2010Toon, A.; Pérez-Losada, M.; Schweitzer, C.E.; Feldmann, R.M.; Carlson, M. and Crandall, K.A. 2010. Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules. Journal of Biogeography, 37: 2275-2290. ; Wolfe et al., 2019Wolfe, J.M.; Breinholt, J.W.; Crandall, K.A.; Lemmon, A.R.; Lemmon, E.M.; Timm, L.E.; Siddall, M.E. and Bracken-Grissom, H.D. 2019. A phylogenomic framework, evolutionary timeline and genomic resources for comparative studies of decapod crustaceans. Proceedings of the Royal Society B: Biological Sciences, 286: 20190079. https://doi.org/10.1098/rspb.2019.0079.
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). Juvenile morphology relating to maternal care (Tab. 5) is shown on the tree. The geological ages and formation of the continents is based on Owen (1976Owen, H.G. 1976: Continental displacement and expansion of the earth during the Mesozoic and Cenozoic. Philosophical Transactions of the Royal Society A, 281(1303): 223-291.) and Dercourt et al. (1993Dercourt, J.; Ricou, L. and Vrielynck, B. 1993. Atlas Téthys Palaeoenvironmental Maps: Explanatory Notes. Paris, France, Gauthier-Villars, 307p., 14 maps, 1 pl.). Solid bars indicate presence and blank bars absence. Numbers on the bar: 1: compound sessile eye in Stage I and developed eye stalk in Stage II; 2: globular carapace in Stage I lost in Stage II; 3: teeth and processes on mandible absent in Stage I but present in Stage II; 4: setae absent on pereiopod in Stage I but long setae present in Stage II; 5: no setae on antenna 1-2, with antennal scale in Stage I but seta present in Stage II; 6: no setae at tip of exopodite of maxilliped in Stage I, the plumose setae appear in Stage II; 7: curved hook at tip of the pereiopod present in Stage II; 8: plumose setae on telson in Stage II; 9: setae on maxilla 1 in Stage I; 10: no plumose setae on pleopod in Stage I but present in Stage II. Bold text (Cambaridae and Parastacidae): independent after Stage III; plain text (Astacidae and Cambaroididae): independent after Stage II (Andrews, 1907Andrews, E.A. 1907b. The attached young of the crayfish Cambarus clarkii and Cambarus diogenes. American Midland Naturalist, 41: 253-271, 2 pls.a; Albrecht, 1982Albrecht, H. 1982. Das System der europäischen Flußkrebse (Decapoda, Astacidae): Vorschlag und Begrün dung. Mitteilungen des Hamburgischen Zoologischen Museum und Institut, 79: 187-210.; Scholtz, 1995Scholtz, G. 1995. The attachment of the young in the New Zealand freshwater crayfish Paranephrops zealandicus (White, 1847) (Decapoda, Astacida, Parastacidae). New Zealand Natural Science, 22: 81-89.; Scholtz and Kawai, 2002Scholtz, G. and Kawai, T. 2002. Aspects of embryonic and postembryonic development of the Japanese freshwater crayfish Cambaroides japonicus (Crustacea, Decapoda) including a hypothesis on the evolutional maternal care in the Astacida. Acta Zoologica, 83: 203-12.).

Crayfish live almost entirely in freshwater during the whole of their lives. Only a few species are adapted to the high saline levels found in brackish environments. For example, Pacifastacus leniusculus (Dana, 1952) occupies the saline waters of certain major river deltas (Shimizu and Goldman, 1983Shimizu, S.J., and Goldman, C.R. 1983. Pacifastacus leniusculus (Dana) production in the Sacramento River. Freshwater Crayfish, 5: 210-228.) and Miller (1965Miller, G.C. 1965. Western North American crawfishes (Pacifastacus) in brackish water environments. Fish Commission of Oregon Research Briefs, 11): 42-50.) has noted that this species has been observed copulating, moulting and ovipositing in brackish water. Nevertheless, crayfish have never dispersed across the oceans and the evolutionary invasion of freshwater by the marine ancestor of all extant freshwater crayfish occurred only once (Scholtz, 1995Scholtz, G. 1995. The attachment of the young in the New Zealand freshwater crayfish Paranephrops zealandicus (White, 1847) (Decapoda, Astacida, Parastacidae). New Zealand Natural Science, 22: 81-89.; 1999Scholtz, G. 1999. Freshwater crayfish evolution. Freshwater Crayfish, 12 : 37-48.), which has resulted in a monophyletic group supported by molecular methods (Crandall et al., 2000Crandall, K.A. Harris, D.J. and Fetzner, J.W. 2000. The monophyletic origin of freshwater crayfish estimated from nuclear and mitochondrial DNA sequences. Proceedings of the Royal Society B, 267(1453): 1679-1686.).

Fossil evidence of crayfish burrows suggests that the occurrence of freshwater crayfish extends back to the Pennsylvanian subperiod (340-286 million years ago, MYA) and that their origin was in the Early Carboniferous (350-320 MYA) (Hasiotis, 1999Hasiotis, S.T. 1999. The origin and evolution of freshwater crayfish based on crayfish body and trace fossils. Freshwater Crayfish, 12: 49-70.). The oldest body fossils of freshwater Astacidea are found in the Chine Formation in the Late Triassic 252-213 MYA (Mesozoic 252-66 MYA) from the Petrified Forest National Park, Arizona USA (Miller and Ash, 1988Miller, G.L. and Ash, S.R. 1988. The oldest freshwater decapod crustacean, from the Triassic of Arizona. Palaeontology, 31: 273-291.). As palaeontological evidence (Amati et al., 2004Amati, L.; Feldman, R.M. and Zonneveld, J.P. 2004. A new family of Triassic lobsters (Decapoda: Astacidea) from British Columbia and its phylogenetic context. Journal of Paleontology, 78: 150-168.; Schram and Dixon, 2003Schram, F.R. and Dixon, C. 2003. Fossils and decapod phylogeny. Contributions to Zoology, 72: 169-172.; Porter et al., 2005Porter, M.L.; Pérez-Losada, M. and Crandall, K.A. 2005. Model-based multi-locus estimation of decapod phylogeny and divergence times. Molecular Phylogenetics and Evolution, 37: 355-369.) and molecular analyses (Crandall and Buhay, 2008Crandall, K.A. and Buhay, J.E. 2008. Global diversity of crayfish (Astacidae, Cambaridae, and Parastacidae-Decapoda) in freshwater. Hydrobiologia, 595: 295-301.; Toon et al., 2010Toon, A.; Pérez-Losada, M.; Schweitzer, C.E.; Feldmann, R.M.; Carlson, M. and Crandall, K.A. 2010. Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules. Journal of Biogeography, 37: 2275-2290. ; Wolfe et al., 2019Wolfe, J.M.; Breinholt, J.W.; Crandall, K.A.; Lemmon, A.R.; Lemmon, E.M.; Timm, L.E.; Siddall, M.E. and Bracken-Grissom, H.D. 2019. A phylogenomic framework, evolutionary timeline and genomic resources for comparative studies of decapod crustaceans. Proceedings of the Royal Society B: Biological Sciences, 286: 20190079. https://doi.org/10.1098/rspb.2019.0079.
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) have shown, the ancestor of freshwater crayfish evolved from an ancestor of the marine Nephropoidea during the Permian (299-251 MYA) or Triassic. This reveals an evolutionary dispersal scenario that has led to the present-day distribution of freshwater crayfish (Ďuriš and Petrusek, 2015Ďuriš, Z. and Petrusek, A. 2015. Evolution and histological biogeography of crayfish. p. 39-58. In: B. Felgenhauer; L. Watling and A.B. Thistle (eds), Crayfish Biology and Culture. Vodňany, Czech Republic, University of South Bohemia .; Scholtz, 1995Scholtz, G. 1995. The attachment of the young in the New Zealand freshwater crayfish Paranephrops zealandicus (White, 1847) (Decapoda, Astacida, Parastacidae). New Zealand Natural Science, 22: 81-89.). A single marine ancestor of the freshwater crayfish invaded freshwater habitats during the Permian or Triassic when the five extant continents were aggregated into a single supercontinent, Pangea (Dercourt et al., 1993Dercourt, J.; Ricou, L. and Vrielynck, B. 1993. Atlas Téthys Palaeoenvironmental Maps: Explanatory Notes. Paris, France, Gauthier-Villars, 307p., 14 maps, 1 pl.). Subsequently, during the Jurassic (200-144 MYA) and Cretaceous (145-66 MYA) Pangea broke up into two continents, Laurentia in the northern and Gondwana in the southern hemisphere (Scotese, 2020Scotese, C. 2020. PALOMAP Project. Available at Available at http://www.scotese.com/ . Accessed on 1 April 2020.
http://www.scotese.com/...
). The ancestral distribution of freshwater crayfish was split in two, with the Astacoidea being left in Laurentia and Parastacoidea in Gondwana. During the Cenozoic (65 MYA), Laurentia broke up into the Eurasian and North American continents, and Gondwana broke into Africa, Australia, and South America.

The Cambaroididae, the most primitive Astacoidea family (Braband et al., 2006Braband, A.; Kawai, T. and Scholtz, G. 2006. The phylogenetic position of the East Asian freshwater crayfish Cambaroides within the Northern Hemisphere Astacoidea (Crustacea, Decapoda, Astacida) based on molecular data. Journal of Zoological Systematics and Evolutionary Research, 44: 17-24.), emerged during the Jurassic and Triassic. Astacidae are the second most primitive Astacoidea group and appeared after the emergence of Cambaroididae during the Jurassic and Triassic. The most advanced family, Cambaridae, arose from an ancestor of the Astacidae during the Cenozoic (Crandall and De Grave, 2017Crandall, K.A. and De Grave, S. 2017. An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. Journal of Crustacean Biology, 37: 615-653.; Grandjean et al., 2017Grandjean, F.; Mun, H.T.; Han, M.G.; Yin, P.L.; Kawai, T.; Distefano, R.J.; Martin, B.; Roles, A.J. and Austin, C.M. 2017. Rapid recovery of nuclear and mitochondrial genes by genome skimming from Northern Hemisphere freshwater crayfish, Zoologica Scripta, 46: 718-728.; Wolf et al., 2019Wolfe, J.M.; Breinholt, J.W.; Crandall, K.A.; Lemmon, A.R.; Lemmon, E.M.; Timm, L.E.; Siddall, M.E. and Bracken-Grissom, H.D. 2019. A phylogenomic framework, evolutionary timeline and genomic resources for comparative studies of decapod crustaceans. Proceedings of the Royal Society B: Biological Sciences, 286: 20190079. https://doi.org/10.1098/rspb.2019.0079.
https://doi.org/10.1098/rspb.2019.0079...
). Fossil evidence of PacifastacusBott, 1950Bott, R. 1950. Die Flußkrebse Europas (Decapoda, Astacidae). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 483: 1-36, pls. 1-6. from the Miocene (5-23 MYA) and Pliocene (2.6-5 MYA) has been found in Idaho, USA (Cope, 1871Cope, E.D. 1871. On three extant Astaci from the freshwater Tertiary of Idaho. Proceedings of American Philosophical Society, 11: 605-607.), while fossil material corresponding to European Astacidae and extant species ranges from the Late Jurassic to Pliocene (Bell, 1863Bell, T. 1863. A monograph of the fossil Malacostracous Crustacea of Great Britain. Part II. Crustacea of Gault and Greensand. Monograph of the Paelaeontographical Society, 14: 40 p., 11 pls.; Feldman et al., 2011Feldman, R.M.; Schweitzer, C.E. and Leahy, J. 2011. New Eocene crayfish from the McBee beds in British Columbia: first record of Parastacoidea in the northern Hemisphere. Journal of Crustacean Biology, 31: 320-331.; Toon et al., 2010Toon, A.; Pérez-Losada, M.; Schweitzer, C.E.; Feldmann, R.M.; Carlson, M. and Crandall, K.A. 2010. Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules. Journal of Biogeography, 37: 2275-2290. ; Van Straelen, 1928Van Straelen, V. 1928. On the fossil crayfish from eastern Mongolia. Bulletin of the Geographical Society of China, 7: 133-138.; Via, 1971Via, L. 1971. Crustáceos decápodos del jurásico superior del Montsec (Lérida). Cuadernos Geología Iberica, 2: 607-612.). Fossil evidence is consistent with recent molecular analyses. Of the five extant continents, Astacidae today occur in both the European and Pacific drainages of North America, Cambaridae are found on the Atlantic side of North and Central America, and Cambaroididae thrive in far eastern Asia. Parastacidae are present in South America, Australia, New Zealand, New Guinea, and Madagascar (Fig. 26).

Our study suggests the following evolutionary scenario for the extent of maternal care in freshwater crayfish (Fig. 26). A single primitive freshwater crayfish evolved direct development on the supercontinent Pangea during the Permian or Triassic, with juveniles becoming independent of their mothers in Stage II. Subsequently, the ancestors of Astacoidea and Parastacoidea arose from Astacidea. The ancestral Parastacoidea extended maternal care from Stage II to Stage III on Gondwana during the Jurassic or Cretaceous. Ancestral Astacoidea continued to become independent in Stage II during the Jurassic or Cretaceous. The Cambaridae split from the Astacidae on the North American plate during the Cenozoic, and ancestral Cambaridae extended maternal care into Stage III. Thus, the history of extended maternal care is longer in Parastacidae than in Cambaridae since Parastacidae developed extended maternal care during the Jurassic or Cretaceous, whereas Cambaridae only developed it during the Cenozoic. Cambaridae and Parastacidae, whose juveniles become independent in Stage III, share the absence of setae on maxilla 1 in Stage I and plumose setae at the tip of the pleopods. On the other hand, juvenile Astacidae and Cambaroididae become independent in Stage II and commonly have setae on maxilla 1 in Stage I and plumose setae on their pleopods by Stage II (Fig. 26).

Nevertheless, Parastacoidea have retained recurved hooks at the tips of pereiopods 4-5 in Stage II, whereas Astacoidea lose these hooks on pereiopod 1 in Stage II and they remain in maternal care in Stage II. Parastacoidea do not have plumose setae on the telson in Stage II, unlike Astacoidea, which develop the plumose setae on the telson in Stage II (Tab. 5). Although setae on the pereiopods in Stage II in Parastacoidea are restricted to short setae near the tip, setae cover the pereiopods in Stage II of Cambaridae and these setae are longer and denser (Fig. 9D-M). The setation of the pereiopods is less obvious in Parastacidae than in Cambaridae. The undeveloped setae on the telson and weak setae on the pereiopods of Stage II Parastacoidea suggest better adaptation to maternal care extended until Stage III. Postembryonic stages of Parastacoidea receive the most maternal care of all freshwater crayfishes, which suggests a longer history of extended maternal care in Parastacidae from the Mesozoic; this has led to a progressive evolution of recurved hooks on pereiopods 4-5 in Stage II and retrogressive evolution of the setae on telson and pereiopods in Stage II.

ACKNOWLEDGEMENTS

The authors wish to thank Professor G. Scholtz of Humboldt University, Berlin, Professor A.M.M. Richardson from the University of Tasmania, and Michael Lockwood who all made helpful comments on the draft manuscript. Antonín Kouba is funded by the Ministry of Education, Youth and Sports of the Czech Republic - project “CENAKVA” (No. LM2018099). The authors thank the anonymous reviewers who gave valuable comments.

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Publication Dates

  • Publication in this collection
    28 Feb 2022
  • Date of issue
    2022

History

  • Received
    23 May 2021
  • Accepted
    28 Sept 2021
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
E-mail: editor.nauplius@gmail.com