J. Zool., Lond. (1968) 156, 137-153 Reproduction, growth and bionomics of Dynamene bidentata (Crustacea: Isopoda) D. M. HOLDICH Department of Zoology, University College of Swansea" (Accepted 13 February 1968) (With 12 figures in the text) Laboratory and field investigations show that there are five distinct marsupial stages and eight post-marsupial stages in the development of the isopod Dynamene bidentutu (Adams). Extensive sexual dimorphism is apparent, beginning at stage 6, and females undergo extensive tissue reduction at the moult to the eighth stage. Young stages inhabit and feed on intertidal algae, and the non-feeding adults (stage 7 and 8 females, and stage 8 males) shelter in crevices or empty barnacle tests. Average brood numbers are fairly high (c. 90) and the average marsupial mortality rate is about 36%. Release of young takes place in May/June, after which the females die, and a resident population of males remains in the crevices to be joined by newly maturing females and males from August onwards each year. The occurrence of two breeding seasons in males, but not in females, explains how the sex ratio of males to females as they leave the algal habitat (1 :9) is about half the ratio of males to females in the reproductive habitat (1 :4). Contents Page Introduction ...................... 137 Marsupial development .................. 138 Post-marsupial development ................ 142 Field investigations .................... 149 Discussion ...................... 151 References ...................... 152 Introduction Dynamene (= Naesa) bidentata (Adams) is a sexually dimorphic sphaeromid isopod occurring between tide-marks (Colman, 1940; Glynne-Williams & Hobart, 1952; Wieser, 1952; Morton, 1954; Kensler, 1967) in south-west Britain (Omer-Cooper & Rawson, 1934). Recent reports of the unusual life-cycle of this species have been given independently by Naylor & Qdnisset (1964) and Bourdon (1964), who have described how young, free- swimming, algal-feeding, stages change their habitat to shelter in crevices or barnacle sheIls at the onset of the breeding condition. This paper considers in detail the develop- ment, growth and bionomics of Dynamene bidentata to determine the precise stage at which the habitat change takes place. It describes the structural features associated with the development of sexual dimorphism, and compares development in this isopod with more typical forms. * Present address: Department of Zoology, The University, Nottingham. 11 137
Transcript
J. Zool., Lond. (1968) 156, 137-153
Reproduction, growth and bionomics of Dynamene bidentata (Crustacea: Isopoda)
D. M. HOLDICH
Department of Zoology, University College of Swansea"
(Accepted 13 February 1968)
(With 12 figures in the text)
Laboratory and field investigations show that there are five distinct marsupial stages and eight post-marsupial stages in the development of the isopod Dynamene bidentutu (Adams). Extensive sexual dimorphism is apparent, beginning at stage 6, and females undergo extensive tissue reduction at the moult to the eighth stage. Young stages inhabit and feed on intertidal algae, and the non-feeding adults (stage 7 and 8 females, and stage 8 males) shelter in crevices or empty barnacle tests. Average brood numbers are fairly high (c. 90) and the average marsupial mortality rate is about 36%. Release of young takes place in May/June, after which the females die, and a resident population of males remains in the crevices to be joined by newly maturing females and males from August onwards each year. The occurrence of two breeding seasons in males, but not in females, explains how the sex ratio of males to females as they leave the algal habitat (1 :9) is about half the ratio of males to females in the reproductive habitat (1 :4).
Introduction Dynamene (= Naesa) bidentata (Adams) is a sexually dimorphic sphaeromid isopod
occurring between tide-marks (Colman, 1940; Glynne-Williams & Hobart, 1952; Wieser, 1952; Morton, 1954; Kensler, 1967) in south-west Britain (Omer-Cooper & Rawson, 1934). Recent reports of the unusual life-cycle of this species have been given independently by Naylor & Qdnisset (1964) and Bourdon (1964), who have described how young, free- swimming, algal-feeding, stages change their habitat to shelter in crevices or barnacle sheIls at the onset of the breeding condition. This paper considers in detail the develop- ment, growth and bionomics of Dynamene bidentata to determine the precise stage at which the habitat change takes place. It describes the structural features associated with the development of sexual dimorphism, and compares development in this isopod with more typical forms.
* Present address: Department of Zoology, The University, Nottingham.
11 137
138 D . M . H O L D I C H
Most of the material used in the investigation was collected at St Brides Haven in south- west Pembrokeshire (OS.802112). Juveniles and immature adults were collected from Fucus serratus L., from Ascophyllum nodosum L. bearing the epiphyte Polysiphonia lanosa (L.), and from Himanthalia elongata L., while mature adults were obtained from shale, limestone, and old red sandstone crevices, and from empty tests of Balanus pevforatus Brugihe.
TABLE I
Average brood numbers and range, with statistical analysis of the difference between consecutive stages
Brood number &
Stage Av. Range Diff. S.D. Comparison t
A 90 63-137 15.7 AIB B 86 53-112 4 15.7 B/C C 80 45-120 -6 17.15 ClD D 65 36-108 -1 5 15.7 DIE E 57 25-86 -8 16.05 A/E
The isopods reproduced successfully in aerated aquaria in which the sea-water was changed weekly. As in the field, juveniles fed on fucoid algae, and later settled in the bar- nacle tests or artificial rock crevices provided. Post-marsupial development was observed by frequent examination of growing juveniles in the laboratory and the instars, thus determined, were confirmed by regular examination of field material over a period of three years.
Marsupial development Brood stages
The mature female moults into the ovigerous condition and releases its eggs into the marsupium through the oviducal openings adjacent to the fifth pair of peraeopods. The initial number of eggs present in the marsupium is usually about 90 (Table I) and they are so compacted as to remain in placed when the ventilating water current, effected by the maxillipedes, passes through the marsupium. If they are fewer than about 50 the eggs tend to be moved by the current and may be lost. On the other hand, if the number of eggs is greater than about 140 the oostegites are often forced apart and the eggs may again escape. Marsupial development was also observed to be arrested in broods found to be infected with the epicardian isopod Ancyroniscus bonnieri Caullery & Mesnil (Caullery & Mesnil, 1919, 1920) or a saprolegnid fungus closely resembling Plectospira dubia Atkins (Atkins, 1954).
Normal development takes place over winter and spring when five stages, A-E, are recognizable.
DEVELOPMENT OF D Y N A M E N E B I D E N T A T A
0.5 rnrn
139
V.
L
Stage A The newly released egg is oval, measuring approximately 0.5 x 0.4 mm. The colour of
the yolk in any one brood is uniform, being either orange, yellow or green. At first two transparent egg membranes are visible (m.l and m.2) with fluid between them and between the inner membrane and the yolk (Fig. l(A)). Whilst in the ovary the yolk is in close contact with the inner membrane and the space between them only appears after fertiliza- tion. Towards the end of stage A the outer membrane becomes wrinkled and split, being shed in one piece usually before the onset of stage B.
U.
d. d. V,
PI.
FIG. I. Marsupial stages A to C. y., Yolk mass; m.l, first egg membrane; m.2, second egg membrane; v., ventral body surface; d., dorsal body
Stage B Initially (Fig. l(Bl)) this stage differs from A by having only a single membrane (m.&
surrounding the yolk mass. After a few days two rows of limb buds appear between the yolk and inner membrane (Fig. l(BJ). Later a cleft appears on the dorsal surface of the egg and eventually penetrates to the centre, when the precursors of the eyes also appear (Fig. I(B&). The stage is completed when the remaimng egg membrane is split and shed in a single piece.
140 D. M . H O L D I C H
Stage C This stage becomes comma shaped by unfolding from the cleft; it has eyes which are
still unpigmented, distinct cephalic and peraeonal appendages and is enveloped in a newly developed first embryonic membrane (Fig. l(CJ). At this stage C, the embryo straightens (Fig. l(C&), the eyes become pigmented and the embryonic membrane becomes wrinkled dorsally, before it is split into two pieces and shed by active movements of the embryo.
(D) (El
FIG. 2. Marsupial stages D showing single limb, antennule and antenna, and E with antennule and antenna of
hp.. Hepatopancreas; h., heart: s.. setae; g., gut; 7, seventh peraeonal somite; m.4, final membrane; y.. yolk. left side only.
Stage D At this stage the embryo is capable of moving its appendages but not of swimming or
crawling. Unlike previous stages it is enclosed in a membrane which covers all the append- ages individually and beneath which the developing setae are clearly visible. Chromato- phores become apparent at this stage and are scattered over the dorsal body wall. The heart, hepatopancreas and gut, with a mass of surrounding yolk, are clearly visible, and the tel- sonic channel appears widely open (Fig. 2(D)). The membrane is actively shed in two parts at the end of this stage.
D E V E L O P M E N T OF D Y N A M E N E B I D E N T A T A 141
25
Stage E A juvenile with all its appendages and setae uncovered is released by the stage D/E
moult (Fig. 2(E)). This has a soft exoskeleton, the yolk mass has disappeared and the background pigment is poorly developed, the animal appearing pink with a scattering of chromatophores. The posterior tips of the telsonic channel are now closer together, the antennule has a flagellum of four articles, the distal two of which bear a single aesthetasc (Fig. 5), and the antenna1 flagellum has seven articles, Juveniles of this stage differ from later post-marsupial stages in that the seventh peraeonal segment is very small and lacks peraeopoda. Soon after the hardening of the cuticle the juveniles emerge, often in pairs, from the posterior margins of the fourth pair of oostegites and eventually swim away.
No stage D/E exuvia have been found in the marsupia of empty females and it seems likely that they are eaten by the juveniles.
- -
0
.
l 0 l I I I I I I I I I I I I I I I I I 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 I l l l l l l l l l l l l l l l l l I I
60 70 80 90 100 I10 Egg number
FIG. 3. Numbers of newly deposited eggs in the brood pouches of 85 females of various stages (area = length x breadth). The trend line derived by linear regression analysis has the foimula y = 13.86+0.07~.
Brood numbers In general the number of newly deposited eggs in any single marsupium is directly
related to the area of the ovigerous femaIe (Fig. 3), but numbers decreased in any female during development (Table I). There is no significant difference in the average number of embryos between stages A and B, and B and C, but the fall in numbers between stages C and D is significant at the 0.1 % level and the fall between D and E is significant at the 5 % level (Table I). The total fall in numbers between stages A and E indicates an overall marsupial mortality rate of 36.4 %, which is highly significant (Table I).
In approximately 75% of ovigerous females the embryos are all at the same stage of development and among the remainder one stage always predominates.
142 D. M . H O L D I C H
Duration of embryonic stages Marsupial development takes place throughout winter and spring in south-west Britain.
In South Wales, during the years 1964-1967 it averaged between 90 and 110 days over a period when sea-water temperatures ranged from 7-10°C. In the laboratory at an average temperature of 15°C the average incubation period was 48 (44-59) days, and at 17.5"C it was 36 (30-40) days. Broods did not develop in females kept at 5°C and 25°C in the laboratory.
T I t 5 -z u
3 4 2
f I
€
i I i I I I I I I I I I I I I
0 1 2 3 4 5 Se 66 7P 7d 8% 8fl Stage
FIG. 4. Mean and range of body length for each post-marsupial stage of development.
Post-marsupial development
Combining the methods of Howes (1939), Forsman (1944), Kjennerud (1950), and Matsakis (1956) eight distinct instars have been distinguished in the post-marsupial devel- opment of D. bidentata. The main criteria used are body length (Fig. 4), number of articles and aesthetascs on the antennular flagellum (Fig. 5) and external sexual characteristics (Figs 6 and 7).
Stage 1 This is marsupial stage E (Fig. 2) and individuals averaged 1.4 mm in body length.
% Such newly released animals are positively phototactic and dispersed by swimming for up to 24 hours. They then become negatively phototactic and settle to feed.
Stage 2 At this stage the body length averages 1.7 mm and the two small buds of the seventh
pair of peraeonal limbs are diagnostic. The antennular flagellum has five articles, the distal three each having a single aesthetasc (Fig. 5).
DEVELOPMENT OF D Y N A M E N E B I D E N T A T A 143
Stage 3 The body length averages 2.0mm. The seventh pair of peraeopoda are partially developed
with setae not yet released, and they lie folded across each other beneath the body. The antennular flagellum has six articles, with a single aesthetasc arising from each of the four distal ones (Fig. 5).
FIG. 5. Antennules of post-marsupial stages 1 to 8. p., Peduncle; f., flagellum; s.as., single aesthetasc; pas., pair of aesthetascs.
Stage 4 Body length averages 2.8 qm and in this and later stages the size range overlaps with
the previous and subsequent stage (Fig. 4). The seventh pair of peraeopoda are fully formed and the background pigmentation of the animal becomes dark green or yellow. The antennular flagellum has seven articles, with single aesthetascs arising from the five distal joints (Fig. 5 ) and, for the first time, the antenna1 flagellum shows an increased number of articles, to eight or nine.
Stage 5 Body length averages 3.7 mm. External sexual characters are not yet present but on
dissection a number of incipient females are found to possess small ovaries with immature
144 D. M. H O L D I C H
oocytes. The antennular flagellum has eight articles (Fig. 5), the most distal four of which each bear a single aesthetasc, and the fifth a pair. The antennal flagellum has nine or ten articles.
Stage 6 At this stage males are recognizable, having two small projections on the posterior
margin of the sixth peraeonal segment, one on each side of the mid-dorsal line (Fig. 6). The average body length of the male is 4.3 mm and that of the female 4.5 mm. In males and females the antennular flagellum has nine articles, the distal four bearing single aes- thetascs and the fifth and sixth each a pair (Fig. 5). The antennal flagellum has 11 or 12 articles.
FIG. 6. Dorsal views of the pleotelson of a and 8 (lower).
stage 5 juvenile; female stages 6, 7 and 8 (upper); male stages 6, 7
Stage 7 The male averages 5.3 mm in body length and is characterized by an enlarged bidentate
process on the hind margin of the sixth peraeonal segment (Figs 6 and 7). Leach (1818) named this stage Dynarnene rnontagui. The pleon has a small double tubercle, and its
145 DEVELOPMENT OF D Y N A M E N E B I D E N T A T A
posterior edge dips down sharply to the telsonic channel which is slightly occluded in the mid-dorsal line. Near the point of insertion of each uropod the telsonic shelf has a small tubercle, and the tips of the inner endites of the uropoda are slightly flattened. The penes appear at this stage and they average 0.06 mm in length.
The females (Fig. 7) average 5.24 mm in body length and oostegite buds, near the bases of the first four pairs of peraeopods, are diagnostic. The ovaries enlarge throughout this stage during which the female ceases feeding, leaves the algal habitat and enters the repro- ductive habitat.
FIG. 7. Dorsal view of stage 8 male (a), and of stage 7 female (b).
In both male and female the antennular flagellum has tea articles, the four distal with single aesthetascs and the following three with pairs (Fig. 5). The antenna1 flagellum has 12 or 13 articles.
Stage 8
ously classified the male as a separate genus, Nesaea. Sexual dimorphism is extremely pronounced and because of this, Leach (1814) errons
146 D. M . H O L D I C H
Male. Body length averages 6.1 mm and the thorax is more convex than that of previous stages and of females. The body colour is usually green or yellow, mottled with orange and purple and white. The antennular flagellum has eleven articles, the distal four each with an aesthetasc and the following four each with a pair (Fig. 5). The antenna1 flagellum has 13 or 14 articles. The peraeon has pleura fringed with fine setae, segment six overlaps seven and the large bidentate posterior median process reaches the pleotelson (Figs 6 and 7). The penes averages 0.12 mm in length and, unlike most isopods, appendix masculina are absent. The pleotelson is rugose, with a large double tubercle on the posterior border.
The telsonic channel is triangular and closed postero-ventrally. The uropods are rugose and setose, with the exopod longer than in stage 7 and at right-angles to the endopod, the hind margin of which is fringed with long setae (Fig. 7). Other appendages remain, as in juvenile stages, except for an increase in size. At this stage males cease feeding and enter the reproductive habitat.
Female. The body length averages 5-32 mm and width is increased (Fig. 8). The colour is white, due to the loss of background pigment, but sparsely speckled with chromatophores. Body tissues are markedly reduced as are some external features. The antennules degenerate
D E V E L O P M E N T O F D Y N A M E N E B I D E N T A T A 147
with reduced numbers of articles and aesthetascs, but the antennae remain unaltered from stage 7. The mouth parts are strongly metamorphosed, with mandibles losing the asymmetrical chitinized incisor processes add becoming fringed with h e setae (Fig. 9). The mandibular palp remains large and bears comb setae which serve to clean the antenna1 flagellum. The maxillules, maxillae and maxillipedes are reduced, the last appendage developing, on the inner border of the basal article, a bilobed flexible, setose plate which creates a forward-flowing water current through the marsupium. The dorsal surface of
FIG. 9. Mouthparts of preovigerous (stage 7) and ovigerous (stage 8 ) females. Female stage 7; (a) mandibles; (c) maxillule; (d) tip of outer endite of maxillule enlarged; (f) maxilla; (h) maxil-
lipede; (j) coupling hooks of right and left maxillipedes enlarged.
the peraeon is covered with small spines, and segments one to four have oostegites, which constitute the marsupium (Fig. 8). Peraeopods 1 to 7 have long setae on the inner surface of the ischium, which serve to support the marsupium. The telsonic channel closes over postero-ventrally .
The female is fertilized by the male when in the half moulted condition from stage 7-8 which may last from one to five days before the oostegites are released. When the oostegites
148 D . M . H O L D I C H
are released by the shedding of the anterior half of the cuticle, the marsupium may remain empty for two to seven days before the female deposits the eggs. Normally the eggs are prevented from escaping anteriorly by the T-shaped first pair of oostegites which are linked posteriorly and by the upturned edges of the saucer-shaped fourth pair of oostegites.
Duration of post-marsupial stages In the field, post-marsupial growth up to the moult of the eighth stage takes about 150
days in males, and up to 240 days in females. This occurs from May until December, when mean sea temperatures range from 16°C down to 5°C. At an overall mean sea temperature of 17.5"C in the laboratory, growth is more rapid and males and females
Days
FIG. 10. Cumulative percentage curves for Dynamene attaining successive growth stages. Based upon 800 labora- tory-reared specimens.
reached stage 8 in an average of 118 days. This is illustrated in Fig. 10 which gives the cumulative percentage curves for the numbers of animals ieaching each growth stage, timed from the day of intial release from the brood pouch. The distance between the 50 % points on successive curves indicates the average duration of each stage, which at 17~5°C was 33, 13, 11, 13, 8 and 6 days, respectively, for stages 1 to 6. The steep S-shaped curves representing the moults to stages 2 to 7 indicate that development proceeds at a fairly similar rate for all specimens. The shallow slope representing animals moulting to stage 8 is the result of differences in the development and behaviour of males and females at stage 7. Stage 7 lasts for 10 to 12 days in males, which remain in the juvenile habitat among algae. Females, on the other hand, leave the algal habitat at that stage and settle in the reproductive habitat among crevices and barnacles. In the field they do not moult to stage 8 until after three months, though this is shortened to an average of 32 days, at 17-5"C, in animals kept in the laboratory.
Males moult to stage 8 while still among algae and only then move into the reproductive habitat, where specimens have survived for up to 500 days without feeding in the laboratory. Females of this stage live for a much shorter period, on average 90 days without feeding.
DEVELOPMENT OF D Y N A M E N E B I D E N T A T A 149
Field investigations
Monthly samples of a population of Dynamene bidentata were taken over the two-year period from November 1964 to October 1966 at St Brides Haven. Standard 3O-minute collections were made from among Ascophyllum nodosum, Fucus serratus, and Himanthalia elongata and also from dead shells of Balanus perforatus, to ensure samples of all available stages in the life cycle. Material was staged according to the characters determined from laboratory-reared specimens, the number of animals at each growth stage being thus determined (Figs 11 and 12).
r n Stage
n !- I I I I
t I h
0
50 6oE n
1965 Month 1966
FIG. 11. Total numbers in standard 30-min. samples of post-marsupial stages 1-8 occurring on intertidal algae at St Brides Haven over a period of 24 months. Black portions represent males.
The pattern of growth was similar in 1964,1965 and 1966, with release of stage 1 juveniles occurring in May to July, and frequent observations during 1967 showed that the same pattern was continuing. Specimens grew rapidly from June to September and in October they began to disappear from the algal samples (Fig. 11). From Fig. 12 it can be seen that autumn was the time when stage 7 females and new stage 8 males first began to appear in the reproductive habitat. The stage 7 females showed peak abundance in the reproductive
150 D. M . H O L D I C H
habitat in September and October when they first settled from the algae and their numbers gradually decreased as they moulted to stage 8 throughout the winter and spring. Ovigerous females (stage 8) reached their peak in the following April to June and then their numbers gradually fell off, specimens dying after releasing their broods.
Owing to their more widespread distribution, numbers of individuals collected from algae were lower than those collected from aggregations in crevices in the standard collecting
50_Id( O O N D J F
IF i
1965
T I
1 r
A J J A S O N D J F M A M Month 1966
Month 1966 L
FIG. 12. Total numbers in standard 30-min. samples of stage 8 male (a), stage 7 female (b), and stage 8 females (c) occurring in the empty tests of dead Bulunusperforutus at St Brides Haven over a period of 24 months.
time. However, the data (Fig. 11) are sufficient to indicate that the ratio of stage 8 males to stage 7 females, at the time when both sexes were about to leave algae and enter the reproductive habitat, was about 1 :9. In contrast, the data in Fig. 12 shows that the ratio of males to females recorded in the reproductive habitat is about 1 :4, and field observa- tions showed that a single male was usually found with a " harem " of females, averaging four in number. The apparent discrepancy between the actual and potential ratios of males to females in crevices is accounted for since males survive to breed for a second year whereas females die at the end of their single breeding season (Fig. 12).
151 DEVELOPMENT O F D Y N A M E N E B I D E N T A T A
Discussion
Present results confirm and extend the preliminary observations of Naylor & Quknisset (1964) and Bourdon (1964), who first reported the change in habitat which occurs during development in Dynamene bidentata. The work also successfully categorizes the number of antennule articles and the number and arrangement of aesthetascs to designate the various instars. The method has previously been fairly successful in categorizing instars of Jaera albifrons (Forsman, 1944), Sphaeroma hookeri (Kinne, 1954), Mancasellus macrourus (Markus, 1930) Ligia italica (Matsakis, 1955), Idotea chelipes (= viridis) (Howes, 1939), and Idotea neglecta (Kjennerud, 1950), but has been less successful with other Idotea species (Naylor, 1955; Matsakis, 1956) and Eurydice spp. (Jones & Naylor, 1967). The instars in D. bidentata appear to be more readily definable than in any other isopod species reported on so far.
The change of habitat which occurs during development in D. biderttata, whereby adults come to occupy a cryptic habitat and do not feed, is associated with a considerable meta- morphosis and loss of function of the female mouthparts. This type of life cycle in isopods is intermediate between normal free living forms and forms such as Gnathia, in which the young stages (pranizae) are quite different from the crevice dwelling adults (Monod, 1926). In the Sphaeromatidae, to which D. bidentata belongs, Hansen (1905) correlates the meta- morphosis of female mouthparts with the development of a dorsal tubelike telsonic channel. One is inclined to agree with Hansen when he suggests that, in their cryptic and often muddy habitat, forms with an upturned telsonic channel are better able to take in clean water across the pleopods and through the brood pouch.
There are four pairs of oostegites forming the marsupium in D. bidentata as there are in Campecopea hirsuta (Tetart, 1962), not three as reported by Hansen (1905), and not five as in many other isopod species (Kjennerud, 1950; Kinne, 1954; Naylor, 1955). As in many species (Verhoeff, 1920; Vandel, 1924) oostegites will develop in females kept in isolation and do not require the stimulus of fertilization as suggested by Schobl (1880) and Loyola e Silva (1963). Once developed, the oostegites remain until death of the females there are no subsequent non-breeding stages with reduced oostegites as have been reported in Sphaeroma hookeri (Kinne, 1954) and Limnoria (Menzies, 1954). The eggs are carried in the marsupium, but there are finger-like projections from the marsupium into the head region, a condition which seems to be an intermediate stage towards those sphaeromid isopods which carry eggs in internal pockets opening from the marsupium (Hansen, 1905; Kinne, 1954).
Eggs are aerated entirely by movements of the modified maxillipedes and not by the raising and lowering of the oostegites as occurs in Asellus aquaticus (Unwin, 1920), Mancasellus macrourus (Markus, 1930), Idotea neglecta (Kjennerud, 1950) and Asellus intermedius (Ellis, 1961).
The pattern of development of the brood follows that described for other isopods except that, as in Asellus intermedius (Ellis, 1961) there are five embryonic stages, not four as described for Jaera albifons (Forsman, 1944), Idotea spp. (Kjennerud, 1950; Naylor, 1955), Sphaeroma hookeri (Jensen, 1954; Kinne, 1954), and Eurydice spp. (Salvat, 1966).
The number of eggs in a marsupium tends to be higher in females of large size but this is better expressed in relation to surface area rather than length as was suggested by Bourdon (1964). The brood numbers in general in isopods seem to be most intimately
152 D. M . H O L D I C H
related to factors such as ecology and behaviour, which influence the survival rate (Menzies, 1954). Species such as Limmoria which remain in burrows throughout their life-cycle have a high survival rate and produce few eggs, whereas parasitic forms, producing young subject to predation in plankton, often have several thousand eggs. D. bidentata with its habitat change from algae to crevices appears to be in an intermediate condition in this respect.
Brood number decreases owing to mortality during the period of incubation in D. bidentata, as it does in Idotea chelipes (= viridis) and Asellus aquaticus (Jancke, 1926), and Sphaeromu hookeri (Kinne, 1954). There is, too, some variation in the stage of development of embryos in about 25 % of brood pouches, with embryos at the posterior end often being more advanced than the others. This differs from the general rule among isopods that the brood is uniform (Green, 1965), but agrees with exceptional species such as Idotea (Howes, 1939; Kjennerud, 1950), and Limnoria (Eltringham & Hockley, 1961).
Copulation in D. bidentata has never been observed but isolated females cannot produce viable broods, nor have they been observed to have a sperm-storage organ. Menzies (1954) has correlated the absence of a sperm-storage organ in isopods with long term association of the sexes, and this seems to apply well for crevice and burrow-dwelling forms such as Limnoria (Menzies, 1954), Sphaeroma (Leichmann, 1891) and D. bidentata. Menzies (1954) states that although Limnoria tripunctata has appendix masculinae they bear no grooves or bristles and that it is difficult to imagine how these are able to transfer sperms to the female, although he admits that in the majority of the Flabellifera they are probably long enough to act as intromittent organs. Complete lack of the appendix masculinae is rare. Recorded examples are Dynamene (Hansen, 1905), Ancinus (Hansen, 1905) and Dyna- meniscus (Richardson, 1905) and it is not known how copulation is effected in these forms.
Finally it has been shown that male D. bidentutu are able to survive very long periods without food. It seems probable that in the field they survive for two breeding seasons, ejecting the females from the reproductive habitat when they have released their brood. The survival of males for two breeding seasons explains how the ratio of males to females leaving the algal habitat is about half the ratio of males to females in the reproductive habitat (see p. 149).
I am indebted to Dr E. Naylor for advice and criticism, to Professor E. W. Knight-Jones for provision of working facilities, and to the Science Research Council for a grant which made this work possible.
REFERENCES
Adams, J. (1800). Description of some marine animals found on the coast of Wales. Trans. Linn. SOC. Lond. 5 : 7-13. Atkins, D. (1954). A marine fungus Plectospira dubiu n.sp. (Saprolegniaceae), infecting crustacean eggs and small
Bourdon, R. (1964). Notes sur la biologie de Dynamene bidentata Adams (Isopode, Sphaeromatidae). Bull. trimest.
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