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ABBREVIATED LARVAL DEVELOPMENT IN CARIDEAN SHRIMPS AND ITS SIGNIFICANCE IN THE ARTIFICIAL CULTURE OF THESE ANIMALS

by

S. DOBKIN
Department of Biological Sciences
Florida Atlantic University
Boca Raton, Florida 33432, U.S.A.

Abstract

The author's studies on the larval development of one penaeid and more than 40 caridean shrimps have produced information applicable to the development of successful culture techniques. Among these species, Palaemonetes paludosus, Synalpheus brooksi, Glyphocrangon spinicauda, Glyphocrangon sp., Systellaspis debilis, and Thor sp. had abbreviated or direct development. Comparison of survival to metamorphosis in the laboratory between Thor floridanus, with a typical long pelagic larval life, and Thor sp., with abbreviated development, shows that many more of the latter attain the postlarval stage despite the greater fecundity of the former. These data indicate that the artificial culture of animals with abbreviated or direct development will achieve the best results. Among the shrimps thus far studied, the large fresh and brackish water shrimp of the genera Macrobrachium and Cryphiops appear best suited to culture from a commercial standpoint. Experiments on the culture of M. carcinus, M. rosenbergii, M. acanthurus, M. ohione, and others have been inconclusive. It is significant that these species all have a long larval life. Pond-culture experiments on forms with abbreviated development such as M. jelskii, M. quelchi, M. borellii, M. potiuna, M. brasiliense, and M. iheringi, all of which are found in Central and South America, are recommended. Forms with similar developmental patterns can be found in other parts of the world.

LE DEVELOPPEMENT LARVAIRE COURT DES Caridea ET SON IMPORTANCE DANS I'ELEVAGE DE CES ANIMAUX

Résumé

Les études de l'auteur sur le développement larvaire d'une espèce de Penaeidea et de plus de quarante appartenant aux Caridea ont fourni des informations applicables à la mise au point de techniques efficaces d'élevage. Parmi les espèces examinées, Palaemonetes paludosus, Synalpheus brooksi, Glyphocrangon spinicauda, Glyphocrangon sp., Systellaspis debilis et Thor sp. connaissent un développement court ou direct. La comparaison in vitro du taux de survie jusqu'à la métamorphose entre Thor floridanus, dont la larve a une vie pélagique particulièrement longue, et Thor sp., à développement direct, révèle qu'un beaucoup plus grand nombre de cette dernière espèce parviennent au stade postlarvaire, bien que la première soit plus féconde. Ces données indiquent que c'est avec l'élevage des animaux à développement court ou direct que l'on obtiendra les meilleurs résultats. Parmi les crevettes étudiées jusqu'ici, les grands animaux d'eau douce ou d'eau saumâtre des genres Macrobrachium et Cryphiops paraissent être ceux qui se prêtent le mieux à l'élevage commercial. Les expériences conduites en matière de culture de M. carcinus, M. rosenbergii, M. acanthurus, M. chione, etc., n'ont pas été concluantes. Il est significatif que toutes ces espèces ont une longue vie larvaire. Il est recommandé de procéder à des expériences d'élevage en étangs de formes à développement court telles que M. jelskii, M. quelchi, M. borellii, M. potiuna, M. brasiliense et M. iheringi, qui se trouvent toutes en Amérique centrale et en Amérique du Sud. Il existe dans d'autres parties du monde, des formes présentant des caractéristiques analogues du point de vue du développement larvaire.

DESARROLLO LARVAL ABREVIADO DE LOS CAMARONES CARIDIFORMES Y SU IMPORTANCIA EN EL CULTIVO ARTIFICIAL DE ESTOS ANIMALES

Extracto

Los estudios del autor sobre el desarrollo larval de un peneido y de más de 40 camarones caridiformes han proporcionado información aplicable al desarrollo de técnicas de cultivo favorables. Entre estas especies, Palaemonetes paludosus, Synalpheus brooksi, Glyphocrangon spinicauda, Glyphocrangon sp., Systellaspis debilis y Thor sp. tenían un desarrollo reducido o directo. La comparación en el laboratorio de la supervivencia a la metaformosis entre Thor floridanus, con una típica y larga vida pelágica larval, y Thor sp. con desarrollo abreviado, indica que de estos últimos son muchos más los que llegan a la fase postlarval, a pesar de la mayor fecundidad de los primeros. Estos datos muestran que el cultivo artificial de animales con desarrollo abreviado o directo conseguirá los mejores resultados. Entre los camarones estudiados hasta ahora los que mejor se adaptan al cultivo, desde el punto de vista comercial, son los grandes camarones de aguas dulces y salobres de los géneros Macrobrachium y Cryphiops. No han sido concluyentes los experimentos sobre el cultivo de M. carcinus, M. rosenbergii, M. acanthurus, M. ohione y otros. Es interesnte observar que todas estas especies tienen una prolongada vida larval. Se recomiendan experimentos de cultivo en estanques con formas de desarrollo abreviado tales como M. jelskii, M. quelchi, M. borellii, M. potiuna, M. brasiliense y M. iheringi, todos los cuales se encuentran en América del Sur y Central. En otras partes del mundo se pueden encontrar formas con tipos de desarrollo similar.

1 INTRODUCTION

In the course of nine years of study concerning the larval development of penaeidean, caridean, and stenopodidean shrimps of South Florida, some 40-odd species, the great majority belonging to the Caridea, have been investigated. Larval development within the Suborder Natantia is quite varied. At one end of the spectrum are the Penaeidea, in which the primitive developmental sequence begins with a series of free-swimming naupliar stages and includes up to twenty planktonic stages (Heldt, 1938). At the opposite end are certain species of the Caridea and Stenopodidea in which direct development occurs, i.e. the newly-hatched individual is similar to the adult in form and therefore undergoes no metamorphosis.

The vast majority of the Natantia have developmental patterns lying somewhere between these extremes. The development of all of the Caridea and Stenopodidea thus far investigated is abbreviated when compared with that of the Penaeidea in that none of these has been observed to have a free-swimming nauplius; none the less, development within these two groups is extremely variable.

In the Caridea, species of which occupied most of the author's attention, abbreviated and direct development occur largely in forms from cold water (both deep sea and high latitudes), fresh water, and those living inquilinistically. Of approximately 40 species of Caridea studied, six showed abbreviated or direct development: Palaemonetes paludosus, a common freshwater form in South Florida (Dobkin, 1963); Synalpheus brooksi, an inquiline of the loggerhead sponge (Dobkin, 1965 a); Glyphocrangon spinicauda, Glyphocrangon sp., and Systellaspis debilis, deep water forms from off the Florida Coast (Dobkin, 1965 b); and Thor sp., an inhabitant of turtle grass in shallow water marine areas (Dobkin, 1962 and 1968). Several others, however, appeared to be evolving toward abbreviated development, and a review of the literature on caridean development uncovered many more species characterized by a decreased number of planktonic larval stages (abbreviated development) or complete suppression of planktonic larvae (direct development).

While the studies were being pursued, the author became interested in the prospects for pond culture of shrimps and prawns. In particular, the fresh and brackish-water shrimps of the genera Macrobrachium and Cryphiops held great interest. It became obvious that as the early developmental stages of most organisms are the most sensitive to environmental stresses, and that as it is at this time in the life history of most organisms that the greatest mortality takes place, that shrimp undergoing abbreviated or direct development might be more successfully cultured than those with a longer developmental sequence. This then, in brief, is the thesis of this paper.

2 EXPERIMENTAL EVIDENCE

Evidence to support this thesis was obtained from laboratory rearing of larvae. The methods used are reported in detail in the literature cited above, but briefly, larvae were reared in plastic compartmented boxes, one larva per compartment, in 50 to 75 cc, of filtered water. The water was changed every day or every other day, at which time the larvae were fed the newly-hatched nauplii of the brine shrimp Artemia salina. In the species having abbreviated development, the larvae were generally not fed at all.

Although it was not possible to rear the larvae of any species of Cryphiops or Macrobrachium with abbreviated or direct development because of the absence of such forms in the area under study, it was possible to compare survival to metamorphosis in two species of Thor, two species of Palaemonetes, and two species of Synalpheus. In each of these genera a species having abbreviated or direct development as well as one having a longer developmental sequence were studied and compared.

The members of the genus Palaemonetes that were studied were P. intermedius, a brackish-water and marine form found in salinities of 6 to 38‰ (Tabb and Manning, 1961), and P. paludosus, a fresh to brackish-water species living in 0 to 10‰ (Tabb and Manning, ibid.). Of 25 specimens of P. intermedius reared, none attained the postlarval stage after six or seven instars. This cannot be considered a valid statistical sample, but additional data are provided by Broad (1957) who worked on P. vulgaris and P. pugio. Of 100 larvae of P. pugio fed Artemia nauplii, 65 reached the postlarva stage generally after seven instars, and of 390 P. vulgaris fed the same food, 131 became postlarvae after about the same number of larval stages. P. intermedius, P. pugio, and P. vulgaris appear to be evolving in the direction of abbreviated development, which is very common in fresh and brackish-water species of the family Palaemonidae. Palaemonetes paludosus has abbreviated development, passing through three larval stages before attaining the postlarva. Of 302 larvae reared, 200 reached the postlarva in five to ten days without being fed. Much less care was required to rear the larvae of P. paludosus than those of P. intermedius, and yet 66 percent of the larvae of the former successfully completed metamorphosis compared with 36 percent of the latter.

In the genus Synalpheus, S. apioceros and S. brooksi were the two species most carefully studied. Development is direct in S. brooksi and all specimens are postlarval on hatching. By contrast, of 72 specimens of S. apioceros reared, not a single one reached metamorphosis or even approached it. The most advanced specimens reached the fifth larval stage and it was estimated that they required several more molts before attaining the postlarva.

Studies were made on Thor floridanus and Thor sp., the former with a long pelagic life and the latter with abbreviated development. Specimens of Thor sp. generally attained the postlarval stage after 48 hours without being fed. Mortality of the larvae was extremely low, only 10 out of 356, or less than three percent, succumbing prior to metamorphosis. It was possible to rear four generations of this species during 1963 and 1964 in running sea water in small aquariums with very little care other than occasional feeding. Siblings bred freely within these tanks. Generation time during the summer was about two months. Of 161 specimens of Thor floridanus reared, 28 became postlarvae. These 28 were bred further and three generations of this species were achieved, but with significantly more effort, and with fewer adults resulting from these efforts.

Initial attempts to rear larvae of Cryphiops caementarius from Peruvian waters and and Macrobrachium acanthurus from Florida have resulted in all specimens of both species succumbing prior to metamorphosis. Both of these forms have a long planktonic larval life, C. caementarius in fact having been reared through ten instars without attaining the postlarva.

3 CARIDEANS WITH ABBREVIATED OR DIRECT DEVELOPMENT

Tables I and II are the result of a fairly complete literature survey extending through the early part of 1964, and indicate carideans which have been reported to undergo abbreviated or direct development. The information on many of these species is admittedly very limited and may be based on as little evidence as a very large egg or a late embryo removed from the egg membranes and examined. Nevertheless, they will probably be of some value in regard to the problem under consideration.

To this list should be added Macrobrachium jelskii, M. quelchi, and M. brasiliense which have large eggs indicative of abbreviated development. All three are found in Latin America. Future investigations will undoubtedly add many more species to this list.

4 DISCUSSION AND RECOMMENDATIONS

The most successful experiments in the aquiculture of shrimps have been those of Fujinaga and his associates (personal communication) with Penaeus japonicus. This success has been accomplished in spite of the large number of larval stages in this species, and is the result of great technological skill employed by these workers. It is obvious, however, that this venture would not have been a commercial success if it were not for the fact that Fujinaga could sell his shrimp at an extremely high price while keeping his rearing costs relatively low. This favorable price/cost ratio does not exist in most areas.

TABLE I

Members of the Subfamily Palaemoninae reported to undergo abbreviated development

* Indicates species for which only a late embryo was examined

TABLE II

Carideans (exclusive of Subfamily Palaemoninae) reported to undergo abbreviated development

* Only late embryos examined

Attempts at the aquiculture of species of Macrobrachium and Cryphiops have for the most part been inconclusive. Among the species studied have been Macrobrachium carcinus (Lewis, 1961), M. acanthurus and M. ohione (Schmittou, personal communication), M. rosenbergii (Ling, 1962; Ling and Merican, 1961), and Cryphiops caementarius (Boza, personal communication). The work on M. rosenbergii in Malaysia has been the most promising.

It is significant that all of these species have a relatively long planktonic life. To the author's knowledge, no species of Macrobrachium or Cryphiops exhibiting abbreviated or direct development has been the subject of pond culture experiments. It is the author's recommendation that these species be used in such experiments and his belief that the results will be well worth the effort. Based on the experimental evidence described above, forms with abbreviated or direct development attain the postlarval stage in greater numbers than those with a longer larval life, despite a lower fecundity. Elimination of the necessity for feeding and caring for large numbers of planktonic larvae would be a significant factor in lowering the costs of culture operations. The cost of providing large numbers of Artemia nauplii to the young stages of Penaeus japonicus in large measure prevented an earlier financial success of shrimp farming operations in Japan.

In many parts of the world the large fresh and brackish-water species of the genera Macrobrachium and Cryphiops are untapped fishery resources. In this day of expanding world population we cannot afford to allow such resources to remain unexploited. Building on the technological advances that have already been achieved we must accelerate our efforts in the field of aquiculture of commercially important species not only of shrimp, but of other fish and shellfish so as to help meet the nutritional requirements of future generations.

5 REFERENCES

Bate, C.S. 1888 Report on the Crustacea Macrura collected by H.M.S. CHALLENGER during the years 1873–76. Rep.Voyage Challenger(Zool.), 24: 1–942

Boone, L., 1935 Scientific results of the world cruise of the yacht ALVA 1931, William K. Vanderbilt, Commanding. Crustacea. Bull.Vanderbilt mar.Mus., (6): 1–264

Boschi, E.E., 1961 Sobre el primer estadio larval de dos especies de camarones de agua dulce (Crustacea, Decapoda). In Actas y Trabajos, 1° Congr. Sudam.Zool, La Plata, 12–24 Octubre 1959, vol. 2:69–77

Bourdillon-Casanova, L., 1960 Le meroplancton du golfe de Marseille: les larves de crustacés decapodes. Recl.Trav.Stn mar.Endoume, 30(18): 286 p.

Broad, A.C., 1957 Larval development of Palaemonetes pugio Holthuis. Biol.Bull.mar.biol. Lab., Woods Hole, 112(2): 144–61

Brooks, W.K. and F.H. Herrick, 1892 The embryology and metamorphosis of the Macroura. Mem.natn Acad.Sci., 5: 321–576

Burkenroad, M.D., 1942 The development and relationships of Glyphocrangon (Crustacea, Decapoda, Caridea). Am.Naturalist, 76: 421–5

Calman, W.T., Decapoda. 1907 Rep.natn.Antarct.Exp.(Zool.) 1901–1904, (2): 1–7

Coutière, H., 1898 Note sur le développement de Synalpheus laevimanus, Heller. Bull.Soc. ent.Fr., 1898: 220–2

Coutière, H., 1899 Les Alphéidae. Annls Sci.nat.(Zool.), (8)9: 1–560

Dobkin, S., 1962 Abbreviated larval development in a species of Thor (Decapoda: Caridea). Am.Zoologist, 2(3): 404–5

Dobkin, S., 1963 The larval development of Palaemonetes paludosus (Gibbes) (Decapoda, Palaemonidae), reared in the laboratory. Crustaceana, 6(1): 21–41

Dobkin, S., 1965a The first post-embryonic stage of Synalpheus brooksi Coutière. Bull.mar. Sci., 15(2): 450–62

Dobkin, S., 1965b The early larval stages of Glyphocrangon spinicauda A. Milne-Edwards. Bull.mar.Sci., 15(4): 872–84

Dobkin, S., 1968 The larval development of a species of Thor (Decapoda: Caridea) from South Florida, U.S.A. Crustaceana, Suppl.2: 1–18

Edmondson, C.H., 1929 Hawaiian Atyidae. 1929 Bull.Bernice P.Bishop Mus., (66): 1–36

Elofsson, R., 1961 The larvae of Pasiphaea multidentata (Esmark) and Pasiphaea tarda (Krøyer). Sarsia, 4: 43–53

Gurney, R., 1937 Larvae of Decapod Crustacea. Part 4. Hippolytidae. “Discovery” Rep., 14: 351–404

Gurney, R., 1949 The larval stages of the snapping-shrimp, Synalpheus goodei Courtière. Proc.zool.Soc.Lond., 119(2): 293–5

Gurney, R. and M.V. Lebour, 1941 On the larvae of certain Crustacea Macrura, mainly from Bermuda. J.Linn.Soc.(Zool.), 41(227): 89–181

Heldt, J.H., 1938 La reproduction chez les Crustacés Decapodes de la famille des Peneides. Annls Inst.oceanogr., Monaco, 18(2): 31–206

Henderson, J.R. and G. Matthai, 1910 On certain species of Palaemon from South India. Rec. Indian Mus., 5(4): 277–305

Kemp, S.W., 1910 The Decapoda Natantia of the coast of Ireland. Scient.Invest.Fish.Brch.Ire., 1908 (1): 190 p.

Koelbel, C., 1886 Crustacea, Pycnogonida und Arachnida von Jan Mayen. Die Internat. Polarforschung 1882–1883. Die österreichische Polarstation Jan Mayen. Beob.Ergebn., 3: 38–57

Kurata, H., 1955 The post-embryonic development of the prawn, Pandalus kessleri. Bull. Hokkaido reg.Fish.Res.Lab., (12): 1–15

Lewis, J.B., 1961 Preliminary experiments on the rearing of the freshwater shrimp, Macrobrachium carcinus (L.). Proc.Gulf.Caribb.Fish.Inst., 14: 199–201

Ling, S.W., 1962 Studies on the rearing of larvae and juveniles and culturing of adults of Macrobrachium rosenbergii (De Man). Curr.Aff.Bull., Indo-Pacif.Fish.Coun. 35:1–11

Ling, S.W. and A.B.O. Merican, 1961 Notes on the life and habits of the adults and larval stages of Macrobrachium rosenbergii (De Man). Proc.Indo-Pacif.Fish.Coun. 9(2): 55–60

Liu, J.Y., 1949 On a freshwater prawn, Leander modestus Heller, and its larval development. Contr.Inst.Zool.natn Acad.Peiping, 5(5): 171–89

Matjasic, J., 1958 Postembrionalni razvoj jamske kozice Troglocaris. Biol.Vest., 6: 76–9

Mayer, P. 1881 Die Metamorphose von Palaemonetes varians. Mitt.zool.Stn Neapel, 2:197–221

Rajyalakshmi, K., 1960 Observations on the embryonic and larval development of some palaemonid prawns. Proc.natn.Inst.Sci.India (B), 26(6): 395–408

Sars, G.O., 1885–6 Crustacea, I-II. Christiania, Grøndahl and Sons, bogtrykkeri 1885–6. 2v. (Den Norske Nordhavs - expedition 1876–78. XIV-XV 6 bd., Zoologi [1–2 Hft.])

Sars, G.O., 1890 Bidrag til kundskaben om Decapodernes Forvandlinger. 3. Crangonidae. Arch.Math.Naturv., 14: 132–95

Sars, G.O., 1912 On the genera Cryptocheles and Bythocaris. Arch.Math.Naturv., 32(5): 19 p.

Shen, C.J., 1939 The larval development of some Peiping Caridea - the Caridina (Atyidae), the Palaemonetes and the Palaemon (Palaemonidae). In 40th Anniversary Papers of the National University of Peking, Vol.1: 169–201

Sollaud, E., 1914 Sur deux nouveaux Palaemonides a développement condensé, vivant dans les eaux douces du Tonkin; Leander mani, n.sp., et Coutierella tonkinensis, n.g., n.sp. Bull.Soc.zool.Fr., 39: 314–24

Sollaud, E., 1923 Le développement larvaire des Palaemoninae.1. Partie descriptive - la condensation progressive de l'ontogenése. Bull.biol.Fr.Belg., 57(4): 509–603

Sollaud, E., 1930 Le légende du “Polymorphisme poecilogenique” du Palaemonetes varians (Leach); distribution de ce Crustacé sur nos Côtes. Bull.Soc.Sci.Bretagne, 7: 1–6

Sollaud, E., 1932 Le développement du Palaemonetes mesopotamicus, Pesta, comparé à celui des autres Palaemonetes circummeditterranéens. C.r.hebd.Seanc.Acad.Sci., Paris, 194: 2233–5

Stephensen, K., 1916 Zoogeographical investigations of certain fjords in southern Greenland with special reference to the Crustacea, Pycnogonida and Echinodermata. Meddr Grønland, 53: 231–378

Stephensen, K., 1935 The Godthaab Expedition, 1928. Crustacea Decapoda. Meddr Grønland, 80 (1): 1–94

Tabb, D. and R.B. Manning, 1961 A checklist of the flora and fauna of northern Florida Bay and adjacent brackish waters of the Florida mainland collected during the period July, 1957 through September, 1960. Bull.mar.Sci., 11(4): 552–649

Williamson, D.I., 1960 Larval stages of Pasiphaea sivado and some other Pasiphaeidae (Decapoda). Crustaceana, 1(4): 331–41

Wollebaek, A., 1906 Le développement du genre Sclerocrangon, G.O. Sars. Bergens Mus.Arb., 1906 (11): 9 p.

Wollebaek, A., 1908 Remarks on the decapod crustaceans of the North Atlantic and the Norwegian fjords. 1 and 2. Bergens Mus.Årb., 1908 (12): 74 p.

ADDENDUM

Since the preparation of this paper in April, 1967, there have been significant advances in the culture of Macrobrachium. Ling's papers included in these Proceedings (Volume 3) showed the feasibility of the commercial rearing of M. rosenbergii, and Fujimura (unpublished data) has established a pilot plant for the production of the same species in Hawaii. M. rosenbergii raised in the latter experiments are being sold in Hawaii at prices advantageous to the shrimp farmer.

In the United States, experiments are underway on the rearing of M. carcinus and M. acanthurus (Dobkin, unpublished; Provenzano, unpublished). The author has reared M. acanthurus to metamorphosis in 43 days at 30°C. Although less success has been achieved in rearing the larval stages of M. carcinus, this animal will probably prove to be the better of the two for culture, because of its larger size and presumed faster growing rate. In Mexico, similar work is being done on M. americanum.