THE LARVAE The names used t o describe the larvae of euphausiids are nauplius, metanauplius, calyptopis and furcilia. These types of larvae and their nomenclature are discussed and defined in Mauchline and Fisher (1969). Williamson (1969) suggests that the terms nauplius, zoea, megalopa and juvenile be used but this is liable to cause confusion rather than simplification. Mauchline and Fisher (1 969) divide the development of the furciliae into phases as a means of classifying larvae. The larvae in each phase are then examined to determine the number of moults, that is larval stages, in each phase. The stages are numbered sequentially so detailing the number of moults in the developmental sequence. A similar scheme of stages is used by Endo and Komaki (1979) to describe the development of Thysanoessa Zongipes. Casanova ( 1974).proposes calling phases of development furciliae I t o 111; her system of presentation of the results of an analysis of the larval development of a species is useful in making comparisons with other species. Silas and Mathew (1977) review the various approaches used in studies of larval euphausiids. Mauchline and Fisher (1969) have reviewed the anatomy and histology of the male and female genital systems. Reference t o the androgenic gland described by Zerbib (1967) in Meganyctiphanes norvegica was omitted; this endocrine gland occurs close to the external opening of the vas deferens and is responsible for the differentiation of the primary and secondary sexual characteristics of the male. Hollingshead and Corey (1974) and Kulka and Corey (1978) have provided further figures of developmental stages of eggs within the ovary of M . norvegica and Thysanoessa inermis along with comparable figures of lobes of the testes. The ovaries a t different stages of maturation were dissected from the animals and photographed by Roger (19738).
Species in Group A of the genus Euphausia usually produce spermatophores in the left urn deferens, the lobes of the testes on the right side being markedly less developed (Mauchline and Fisher, 1979). Sebastian (1966) h d s that only one spermatophore is carried in Thysanopoda
tricuspidata whereas the normal two are carried by T . orientalis and Stylocheiron longicorne. The spermatophore is normally transferred by the male and attached to the thelycum of the female. It usually remains attached there for some time after the spermatozoa have discharged from it into the spermathecum and is probably not lost by the female until she moults. The four Euphausia species in the “gibba” group, namely E . hemigibba, E. pseudogibba, E. paragibba and E. gibba, appear to be exceptional in that the discharged spermatophores are not retained by the females. James (1977) believes that males of the latter three species transfer the spermatophores briefly to the structural elements of the thelycum present in the seventh thoracic segment of the females so that the spermatozoa can discharge into the spermathecum. The thelycum of E. hemigibba is the least specialized and in this species the male may hold the spermatophore briefly on or close to the spermathecum t o effect discharge of the spermatozoa. Brinton (1978) reports nine occurrences of spermatophores attached to the first pair of pleopods, one occurrence on the second pair of pleopods, and three instances of attachment to the gills of males. The species involved were Thysanopoda aequalis, Euphausia pacijica, E . similis, Thysanoessa gregaria, Nemtoscelis dificilis and N. microps but these were extremely rare occurrences. The seasonal changes in the percentage of males and females in populations of Meganyctiphunes norvegica and Thysanoksa raschi carrying spermatophores is shown in Mauchline and Fisher (1969). Transference of the spermatophores from the males to the females in a population takes place some considerable time before egg laying. Wiborg (1971), examining populations of Meganyctiphanes mrvegica in the Byfjord and Hardangerfjord in Norway, and Hollingshead and Corey (1974), examining populations of the same species in Passamaquoddy Bay in eastern Canada, confirm that transference takes place over a period of about three months. Similar results were obtained by Kulka and Corey (1978) in a study of Thysanoksa inermis. Berkes’ (1976) data are insufficient to draw any conclusions about the length of the transfer period. It is not known why spermatophores should be transferred to the females when the ovaries are still in an early stage of maturation. Mauchline (1972), in considering the breeding strategies of oceanic and deep sea pelagic organisms, suggests that early mating may be necessary for the initiation of the final stages of ovarian maturation. It is not a single act of mating that is being discussed here because the females are usually actively growing in body size and consequently they are moulting and have t o be remated. The frequency of moulting is once every two or three days up to
THE BIOLOGY O F EUPHAUSIlDS
about once every twenty or thirty days, depending upon the species, its body size and the environment. Thus, there is opportunity for complex working of endocrine systems stimulated by the mating processes. Brinton (1978) points out that fertilization is always accomplished by one spermatophore in Euphausia pacijka. This also seems to be true in Meganyctiphanes norvegica. ThysanoGsa species are fertilized by either one or two spermatophores while Brinton states that Nematoscelis species appear to require two spermatophores. Examples of the ranges in sizes of the eggs of different species are given in Mauchline and Fisher (1969). Ponomareva (1969) found that eggs of Euphmusia diomedeae from' the Indian Ocean ranged in diameter from 0-30 t o 0.42 mm with a perivitelline space of 0.04 mm. She obtained large eggs, 0-71-0-87 mm in diameter, which she considers are those of Thysanopoda tricuspidata. Ponomareva (1969) examined the development time of the eggs of Ewphausia diomedeae and found that they require 16 h to develop from the stage of cleavage into two blastomeres to a fully developed nauplius. The series of early larval stages in species that lay their eggs freely in the sea consists of a nauplius, that emerges from the egg, a subsequent second nauplius, a metanauplius and three calyptopes. Species in some genera carry their eggs attached to the thoracic legs; these eggs hatch a t a later stage, the second nauplius, which develops into a metanauplius. The abdomen and stalked eyes develop in the three successive calyptopes. All species of euphausiids pass through this developmental sequence of stages (Mauchline and Fisher, 1969).
Table I in Mauchline and Fisher (1969) contains measurements of the early larval stages of 36 species of euphausiids and lists the relevant literature. Detailed descriptions of the individual larvae can be obtained from that literature. Additional information is now available on 14 of these species and is presented in Table I11 along with data on a further 13 species. Consequently, information on the early development of 49 species has now been published. Le Roux (1976) has demonstrated marked annual variations in the body sizes of the three calyptopes of Meganyctiphanes norvegica and Nyctiphanes couchi in the Gulf of Morbihan, France. This is probably a general feature of larvae of most species and so the measurements given in Mauchline and Fisher (1969) and in Table 111 are presented primarily as ranges in size. Mathew (197 I ) describes the larvae of Euphausia distinguenda from the northern Indian Ocean but Brinton (1975) has re-named these populations E . sibogae; Bhe name E . sibogae is used in Table 111.
TABLE111. RANGEIN S m (mm) OF EARLYLARV~LL STAGES
Naupliua Speciea Thysanopoda T . rnonacantha T . tricwpidata T . a.eqwlis T . pectinata; Meganyctiphanes M . norvegica Nyctiphanw N . couchi Euphausia E. krohni E . brevis E. diontedeae E . crystallorophias E . sibogae E . fallax E. gibboidw E . sanzoi E . hmnigibba E . hanseni ThysanoZsaa T . gregaria T . longipea
2.90 2-50-2.74 1.70-1.90
0.90-1.40 0.88-1 *03 1.161.23 1.35-1.50 0.96-1.15 1.17-1.35 1.09-1.27 1.01-1.23
III 3.40 2.90-3.40 2.20-2.30 4-00 (2-40)
7 1, 5 6, 7 7 1, 6, 11
1, 4, 6, 11
1, 6 1, 6
1.50-1.70 2.25-2-80 1.49-1.58 1.80-2.14 1366-1.98 1'68- 1'92 1.60 1.70-2.10
1.80-2.80 1.70-2.40 2.14-2.28 3.66-4.45 1.9%2*00 2.48-3.07 2.34-2.7 1 2.18-2.79 2.00-2-60 2.90-3.60
1.40- 1.80 1.43-1'93
1, 6 15
2, 7 12 2 14 9
TABLEIII-contd. Nauplius Species Nematoscelis N. di&ilis N. megalops N. tenella N. microps N. atlanticu N. gracilis Stylocheiron S. carinatum S. suhrni S. longicorne S. abbreviatum S. maximum
I1 0.60 0.53-0.57
1.30-1.60 0.80-1.70 1.20-1-30 1.30-1-40 1.40-1.50 1.30-1.40
1.80-2-10 1.60-2.50 1.60-1.90 1.80-2.10 2.1Cb2.30 2-00-2-20
2.00-2.80 2.20-3.30 2.40-2-70 2-60-2.80 2.60-2.90 2-50-2.70
1.60-1’75 1.20-1.28 1-30 1.80-2.24 2.47-2.70
1.80-1.96 1.70-1.76 1.70-1-90 2.66-2,75 3.92(?)
2.08-2.59 2.00-2.50 2.30-2.40 2.40-2.87 3.85
1, 8 1, 6, 8 1, 8 1, 8 8 8 1, 3, 7
1, 6, 7 1, 4, 6
Mean sizes are shown in brackets, single measurements not in brackets are of doubtful accuracy. This is additional information to that of Table I in Mauchline and Fisher (1969). References: 1, Mauchline and Fisher, 1969; 2, Mathew, 1971, 1975; 3, Mathew, 1972; 4, Casanova, 1972; 5, Knight, 1973; 6, Casanova, 1974; 7, Brinton, 1975; 8, Gopalekrishnan, 1975; 9, Knight, 1975; 10, Knight, 1976; 11, Le Roux, 1976; 12, Pertzova, 1976; 13, WeigmannHaass, 1977; 14, Knight, 1978; 15, Endo and Komaki, 1979.
The third calyptopis moults to the first furcilia. This larva has the eyes free of the carapace and is a miniature adult in body form but lacks most of the thoracic legs and pleopods. The successive furciliae are recognized principally through the developmental sequence of the pleopods and abdominal photophores and by the reduction in number of the terminal spines on the telson; there are seven spines in the fist furcilia reducing to one in the adolescent (Mauchline and Fisher, 1969). A pleopod develops first as a non-setose rudiment which becomes setose at the following moult. Anterior pairs of pleopods develop before posterior pairs. Some species follow a strict developmental pathway, e.g. Thysanopoda acutifrons has a furcilia I with hree pairs of rudimentary pleopods (denoted 3’), a furcilia I1 with t ree pairs of setose and two pairs of rudimentary pleopods (denoted 3” 2‘) and a furcilia I11 with five pairs of setose pleopods (denoted 5”). This course of development is written as follows :
+ 3” 2’
Other species have a dominant pathway along which the majority of larvae develop but variations in the development are common (Mauchline and Fisher, 1969). For example, in Meganyctiphanes norvegica most larvae follow the dominant pathway: 3’
+ 3‘’ 2‘
but a notable number, varying between populations and seasons, will follow one of the following: 0’
1’ + 1”2‘
1’ + 1”3‘ + 4” P’ + 5” 1’ ---+
1’’ 4’ + 5”
+ 2” 3‘ +
+ 2“ 2‘ + 4“ 1’ + 5”
3’ + 3” 1’
The forms of early furciliae found in some fifty species are described by Mauchline and Fisher (1969). Additional information is now available on 32 of these species and the development of a further twelve
THE BIOLOGY OF EUPHAUSIIDS
species has been described. All the available information is summarized in Figs 15 and 16. Mathew's (1971) Ewphawia distinguenda has been renamed E . sibogae (see Brinton, 1975). The development of E . recurva described by Sheard and shown in Mauchline and Fisher, Fig. '47, is not that of E . recurva; the larvae described by Sheard belong to another unidentified Euphausia species according to Brinton (1975).
Mauchline and Fisher (1969) discuss a t some length the reasons why developmental pathways may be variable in some species and more or less constant in others. They point out that the dominant pathway of development of a species not only varies between different sea areas but can also vary in the same sea area at different times. This has been demonstrated recently in furciliae of E . pacifica by Endo and Komaki (1979). The developmental pathway is probably influenced by the availability of food but other environmental conditions are no doubt involved. Le Roux (1973a, b ; 1974) has examined the influence of food, environmental temperature and removal of the eyes on the larval development of Meganyctiphanes norvegica and Nyctiphanes couchi. These are difficult experiments t o perform satisfactorily in the laboratory because the general conditions of culturing are themselves likely t o affect the developmental sequence. Zelikman (1968) and Makarov (1971b; 1974a) discuss in full the significance of dominance among larval forms of a species. They stress the point that variant forms are not the result of accidental happenings within the development of a larva but are undoubtedly a direct reflection of the environmental conditions in which the larva is living. Changing environmental conditions, over a more or less extended breeding season, cause a change in the dominant pathway of development; or they may cause the appearance of other pathways of development where only one existed before. A taxonomic group of species probably has a dominant pathway of development which is optimal for these species (Figs 15 and 16) and is used under optimal or near optimal environmental conditions for these species. When environmental FIG.15. Development of the early furciliae of species in the genera Thpanopoda,
Meganyctiphanes. Nyctiphanes, Peeudeuphausia and Euphawia. The blocks are representative of the relative numbers of each type of larva recorded in any one species. Open squares represent most probable types of larvae but not s d c i e n t evidence is available to be categorical. Question marks are doubtful records. (1) Mauchline and Fisher, 1969; (2) Jones, 1969; (3) Ponomareva, 1969; (4) Mathew, 1971; ( 6 )Mathew, 1972; (6) Gopalakrishnan, 1973; (7) Le Roux, 19738; (8) Casanova, 1974; (9) Le Roux, 1974; (10)Makarov,197413; (ll)Talbot, 1974; (12)Brinton, 1975; (13)Gopalakrishnan, 1975; (14) Knight, 1975; (15) Pertzova, 1976; (16) Weigmann-Haaas, 1977; (17) Knight, 1976; (18) Le ROUX,1976; (19) Knight, 1978; (20) Endo and Komaki, 1979.
THYSANOPODA T monacantha T tricuspidoto 7:aequalis T microphthatma T acutifrons T pmtihato T orientatis T cristata I: egregia 7: mrnuta/spinicaudata
I [email protected]
MEGANYCJtPHANES Ynorvegica NYCTIPHAN€S N oustratis N capensis N couchi N simplex PSEUDEUPHAUSIAI I? totifrons
I? sinica EUPHAUSIA E krohni E mutico E bre vis E diotnedeae E recurva E superba E vattentini E hens E frigida E pocifica E nona E crystaltorophias E tenera E sitnilis E sibogae E gibboides E fatlax E sonzoi E pseudqibba E hemigibba E spinifera E honseni E longirostris E triocontho
1 1 1,12 1,12 1
1,12 4 12,14 12,19 12,17 12
NEMATOSCEL./s N difftciks N megolops N tenella N microps N.otlontica nl. lobato nl.gracilis
srrmxmoiv S mrinatum S . offine S suhmi S efongatm S,longicorne S obbreviatwn S maximum
THE BIOLOGY OF EOPHAUSIIDS
I I m
I1,6,13 1,8,13 1,13 1,13 1,13 1.13 1,13
FIQ. 16. Development of the early furcilia6 in species in the genera Thysanokkaa, Nenzatoscelia and Stylocheiron. Format of figure and references as in Fig. 15.
conditions change, for example, later in the breeding season, and become less optimal for the species, the pathway of development changes in response to these conditions. This “variant” pathway is probably not optimal for the species except possibly under the sub-optimal environmental conditions., Consequently in studying the development of a species sampling should be carried out, not only throughout the geographical range of the species, but also throughout the seasonal period of occurrence of the larvae. The development of the later furciliae is referred to in Mauchline and Fisher ( 1969) and in the papers cited in Figs 15 end 16. Marr (1962) demonstrated an ontogenetic migration of the larvae of Euphausia superba and Mauchline and Fisher (1969) discuss the vertical distributions of euphausiid larvae and their relationships to such migrations and to diurnal vertical migrations performed by some of the later furciliae. Hempel and Hempel (1978) and Nast (1979) examine bhe distribution of larval E . superba in the Atlantic sector
of the Antarctic. Few eggs and no nauplii were taken in the upper 150m of the water column. 'There was evidence of some vertical migration of furciliae I, I1 and I11 into the neuston a t night. Haury (1976a) found that the modal depth of occurrence of euphausiid eggs in the California Current is at about 100 m but he did not identify the species. ,Eggs, probably those of Thysanoessa raschi, were concentrated in the surface 60 m of a water column of total depth 170 m in a northern Norwegian fjord (Hopkins and Gulliksen, 1978). Makarov (197%) found that the eggs, nauplii and metanauplii of Euphausia frigida, E . triacantha and Thysanohsa species occurred deep and that the larvae of these species performed an ontogenetic migration in the sea area off north-eastern South Georgia. The depth at which several species lay their eggs is still unknown. The investigations of populations of the Antarctic Euphusia superba have been relatively inconclusive (Hempel, 1979), although this species, like other epipelagic and shallow living species, probably lays them close t o the sea surface. Information on the depths at which eggs are laid by the bathypelagic Bentheuphausia amblyops and species in the genus Thysanopoda is not available. All euphausiid eggs so far examined are slightly denser than sea water and so sink. The furciliae, however, are primarily phytophagous and live in the surface layers. There will be some advantage in restricting the extent of the ontogenetic migration required to be performed by the earlier larvae, which probably do not feed to any great extent, as discussed below. The only way of doing this is by the females laying the eggs high in the water column so that the nauplii hatch out a t relatively shallow depths. The food of larval euphausiids has received little attention (Mauchline and Fisher, 1969).The mouthparts are not functional in the nauplii and metanauplius but become functional in the first calyptopis. Pavillon (1978) examines the capability of eggs, nauplii, metanauplii and first calyptopes of Euphausia krohni to absorb organic nutrients directly from the sea water. He introduced the following a t concentrations likely t o be encountered in the natural environment : glycine, alanine, serine, cysteine, asparbic acid, glutamic acid, methionine, byrosine, thiamin, riboflavin, pyridoxin, cobelmin and palmitic acid. Amino acids were absorbed in greater quantities by larvae than by eggs. Little cobalamin and pyridoxin was absorbed by the eggs but these were absorbed appreciably by the larvae. The absorption of riboflavin increased with time in both eggs and larvae.