T A N E (1967) 1 3 : 33 - 4 2 33

T H E E A R L Y S T A G E S O F S O M E NEW Z E A L A N D S H O R E B A R N A C L E S . by B . A . F o s t e r *

I N T R O D U C T I O N Barnac l e larvae or n a u p l i i are d i s t ingu ished from the l a r v a l

stages of other Crustacea by the posse s s i on of the pecu l iar f ronto- lateral horns of the carapace . Dur ing the l i f e c y c l e there are s i x naupl iar stages, which are fo l lowed by the cypr i s stage wh ich ac t i ve l y seeks su i tab l e se t t l ing s i t es for permanent attachment and metamorphosis into the adult . Barnac le naup l i i are most ly ident i f i ed for descr ip t ion by rear ing them in i so la t i on from the f i rst naup l ius stage, wh ich can be readi ly hatched from the ripe ovigerous lamel lae wh i ch are the deposited egg masses i n the mantle cav i ty of the parent and there develop to the f i rs t naup l ius stage within the egg membrane. D i f f i cu l t y can be exper ienced i n s u c c e s s f u l l y rearing plankton larvae about wh i ch very l i t t l e i s known of the ir environ­mental and food requirements. Some s u c c e s s has been ach ieved by us ing plunge-jar systems ( B a s s i n d a l e , 1936) or more soph i s t i ca t ed c i r cu l a t i n g sea water apparatus (Wise l y , 1960). In most cases the n a u p l i i must be fed, usua l l y on cu l tures of phytoplanktonic a lgae. There i s ev idence that there are spec i f i c a l ga l preferences for the var ious spec i e s of barnac l es (Moyse , 1963). If the optimum of food spec i es can be found then reason­able success in l a r v a l development can be ach ieved , e. g. cypr ids of Elminius modestus can be reared from jus t hatched n a u p l i i i n s i x days on a diet of Skeletonema costatum whereas re la t i ve l y fewer cypr ids can be obtained on a diet of Phaeodactylum closterium in at l eas t ten days . A l te rnat i ve ly , barnacle n a u p l i i may be captured from the p lankton and s i z e frequency d i s t r ibut i ons used to ind ica te the stages present ( e . g. Knight-Jones and Waugh, 1949 ), although such a procedure i s of l im i t ed use when more than one barnac le spec i e s has unknown larvae i n the plankton at the same t ime.

The naupl iar stages of European barnac les have been descr ibed by var ious authors ( B a s s i n d a l e , 1936; Pye f inch , 1949; Jones and C r i s p , 1953; Norr is and C r i s p , 1953; Moyes, 1961; C r i s p , 1962), and pre l iminary invest igat ions of the l i f e history of seven barnacle spec i e s from South A f r i c a have been made by Sandison ( 1951 ) . The l i fe h i s to r i es of New Zea land barnacles have rece ived scant attention: Batham (1946) has descr ibed the larvae of Pollicipes spinosus, wh ich do not feed, and Knight -Jones and Waugh (1949) have descr ibed the stages of Elminius modestus from spec imens that have become es tab l i shed in European waters .

The l a r va l stages of most New Zea land barnacles s t i l l await descr ip t ion . T h i s paper does not descr ibe the l i fe h i s t o r i e s , but on the bas is of observat ion of early stage n a u p l i i of seven known spec i e s out­l ines what may be use fu l characters for the ident i f i ca t i on of barnacle ' D e p a r t m e n t o f Z o o l o g y , U n i v e r s i t y o f A u c k l a n d

P r e s e n t A d d r e s s : M a r i n e S c i e n c e L a b o r a t o r i e s , H e n a i B r i d g e , A n g l e s e y , U . K .

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F I G . 1 N a u p l i i of Elminius plicatus: I, the f irst stage naup l ius ; II, the second stage naup l ius ; a, the entire naupl ius from dorsal and ventral aspec ts for naup l i i I and II r espec t i ve ly ; b, the antennule; c, the antenna; d, the mandible; e, the abdominal and cauda l process of naupl ius II.

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naup l i i from the p lankton.

T H E E A R L Y N A U P L I I

When mature ovigerous lamel lae are extracted from the adult and placed in fresh sea water the f irst stage naup l i i (naupl i i I) readi ly hatch and become ac t i ve . The pronounced pos i t i ve phototaxis of barnacle naup l i i convenient ly aggregates the naup l i i i n regions of maximum l ight in tens i ty , and samples can then be withdrawn and transferred to further containers or preserved. Within a few hours the f irst moult occurs to y i e l d the second stage naup l i i (naupl i i II). The requirements for cont inued growth and moult­ing then become more exact ing and no stage III n a u p l i i were obta ined . The naup l i i were preserved in 70% ethy l a l coho l or 5% formalin in s e a water, and then examined on a covered g lass s l i d e with the a id of a b inocular and a compound microscope.

Naupl ius I The f irst naupl ius ( F i g . I) carr ies three pairs of l imbs - the antennules , antennae, and mandibles - a l l of which have unfeathered setae . The fronto-latera l horns are projected in a latero-posterior d i rec t ion , and the c a u d a l . appendage i s short. The frontal f i laments are usua l l y inconsp i cuous . The first naupl ius i s a locomotory stage and thought not to feed (Pye f inch , 1949) and moults w i th in a few hours. Interspeci f ic di f ferences of stage I naup l i i are hard to f ind, and no readi ly ascerta inable characters can be sugges ted . The labrum i s nearly a lways inconsp icuous . A s i z e dif ference occurs (Table I), but the ranges of s i z e s are not mutually e x c lus i v e . Stage I naup l i i may make up some temporary part of inshore plankton, but as the moult occurs within a few hours they are probably of l e s s importance in the offshore plankton. L i v e n a u p l i i cou ld be retained un t i l metamorphosis, when s l i gh t l y better chances of ident i f i ca t i on preva i l .

Table I. D imens ions of stage I naup l i i of s i x barnacle s p e c i e s .

Species Carapace width To t a l length Length/width m. m. m. m.

C . brunnea 0. 12 0. 27 2. 25 C. columna 0. 10 0. 23 2. 30 T . purpurascens 0. 15 0. 33 2. 20 E . p l i ca tus 0. 16 0. 35 2. 19 E . modestus Q. 12 0. 25 2. 08 B . vest i tus 0. 17 0. 30 1. 76

Naupl ius II The second naupl ius ( F i g . 2) differs from the f irst stage in i t s greater s i z e ,

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Balanus vestitus

F I G . 2 Out l ines of the carapace and labrum of stage II barnacle naup l i i ; a l l drawn to the same s c a l e .

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the more forwardly swept fronto-lateral horns, the sometimes appearance of the frontal f i laments , the extens ion of the caudal spine on the carapace ( F i g . 1, He), the pronounced labrum, and the increased se ta t ion of the antennules, antennae and mandibles . The l imb setae may or may not be feathered. Outl ine drawings of the stage II naup l i i of seven barnacle spec i es are g iven in F i g . 2. These drawings are from the ventral sur faces and show the shape of the labrum. A number of se tat ion formulae have been dev i sed to summarize the setat ion charac t e r i s t i c s of each l imb of each stage of each spec ies (Bass inda le , 1936; Jones and C r i s p , 1954; and Newman, 1965). However, the procedure of check ing the number and nature of the setae of the naup l i i from a plankton sample makes such a scheme of l i t t l e p rac t i c a l va lue . The setat ion, which a lways increases from one stage to the next, i s a develop­mental as we l l as a spec i f i c feature, and i s use fu l mainly for separat ing stages wi th in the s p e c i e s . The nature of the sp ine armature and re lat ive proportions of the abdominal process of naup l i i can be used to separate many of the stages (e. g. Knight- Jones and Waugh, 1949); these characters might be useful for in terspec i f i c d i s t inc t i on as w e l l . Sandison (1951) found that " . . . no one character can be used to determine both spec i e s and stage i n naup l i i . A cons iderat ion must be made f i r s t l y of the carapace shape, the form of the labrum and of the cauda l appendages to ind ica te the spec i es , and secondly of the s i z e of the naupl ius and the se ta t ion formula to deter­mine the s t a g e " .

Tab le 2. D imens ions of stage II naup l i i of seven barnacle s p e c i e s .

Spec ies Carapace width To ta l length Length/width m. m. m. m.

C . brunnea 0. 19 0. 35 1. 89 C . columna 0. 17 0. 30 1. 76 T . purpurascens 0. 20 0. 47 2. 37 E . p l i ca tus 0. 20 0. 49 2. 50 E . modestus 0. 15 0. 36 2. 36 B . trigonus 0. 19 0. 37 2. 00 B . vest i tus 0. 20 0. 55 2. 75

On cons iderat ion of the characters shown i n F i g . 2 a d i s t inc t i on can be made between the Chthamal idae (Chamaesipho) and the Ba lan idae (Balanus, Tetraclita and Elminius). The squar i sh carapace (with a ratio of total length to carapace width of l e s s than two) and the almost s ingle labrum with two pronounced teeth on the d i s t a l border separates the genus Chamaesipho. The presence of the toothed labrum has been demonstrated for Octomeris angulosa and Chthamalus dentata by Sand ison (1951) and for

Chthamalus stellatus by B a s s i n d a l e (1936); but neither worker has suggested that th is may be a fami ly charac te r i s t i c .

P I G . 3 The percentage of adult barnacle populat ions at L e i g h with mature ( shaded ) and immature (unshaded) larvae as ovigerous lamel lae wi th in the mantle cav i t y . Samplings arranged i n quarter monthly per iods. B l o c k s below the ax is ind icate populat ions sampled but no lamel lae found.

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The two spec i e s of Chamaesipho are not eas i l y d i s t ingu i shed except on the bas i s of s i z e , C . brunnea being the larger . T h i s c l o s e l y para l l e l s the s im i l a r i t y of the adults where the d i s t i nc t i on i s one of s i z e and a number of minor cons idera t ions of mouthparts and c i r r a l se ta t ion . Jones and C r i s p (1954) d i s t i ngu i sh Elminius modestus and Balanus improvisus pr imari ly by the labrum which i n the former spec i e s " t h e middle lobe protrudes by a d is tance greater than one third of i t s w id th ; th is i s not true for any other known spec i es of Balanus". A l though Jones and C r i s p suggest th is as a generic charac te r i s t i c , Elminius plicatus ( F i g . 1) does not show a protruding middle lobe of the labrum. The genera Elminius and Tetraclita differ from Balanus by the straighter anterior margin of the carapace and the more forwardly swept fronto-lateral horns. E. modestus may be separated from E. plicatus and T. purpurascens by the protruding middle lobe of the labrum. The carapace of E. plicatus i s more of a " t h i s t l e " shape than the s lender " w i n e - g l a s s " shape of that of T. purpur­ascens but otherwise these two spec i es are very s im i l a r . Bo th spec i es of

Balanus i n F i g . 2 show a rounded anterior margin of the carapace , and la tera l ly directed fronto- lateral horns. Bass inda l e (1936, p. 69) recognized the s imi la r i t y of the naup l i i of the spec i e s of Balanus. In the present case , B. vestitus differs from B. trigonus by i t s more s lender shape and greater total length.

The breeding seasons T o gain some idea of the l i k e l y s easona l occurrence of n a u p l i i i n

the p lankton, the breeding state of adult barnacle populat ions was i n v e s t i ­gated. In F i g . 3 the presence of immature and mature ov igerous lamel lae within adults of the f ive commonest barnacles at L e i g h are represented as percentages of the popula t ion . The d i s t i n c t i on between immature (uneyed) and mature (eyed) larvae was made on the bas i s of co lour . T h e s i z e of the samples and the co lours used are g iven i n Tab l e 3. Infrequent sampl ing of Balanus trigonus i nd i ca t es a summer breeding per iod (Table 4), where mature larvae hatched when extracted and p laced in sea water. Large numbers of recent ly set t led B. trigonus were observed on most ava i lab le subl i t tora l surfaces and to some extent In the lower l i t t o r a l during late February and early March of 1965 and 1966. N a u p l i i have been found in the mantle cav i ty of Balanus vestitus i n August , and these hatched when p laced in s e a water. No n a u p l i i have been found i n the summer months. Fo r Pollicipes spinosus Batham (1946) states " s ca t t e r ed Ind iv idua ls show lamel lae from December un t i l J u l y . The main breeding period i s , however, from February to A p r i l , when two thirds of the adults are carry ing embryos " .

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Tab l e 3. Sample s i z e and co lours used i n sampl ing adult barnac l es for the presence of ovigerous l ame l l a e .

Spec ies Sample s i z e Immature Mature

C . brunnea 50 - 120 orange brown C . co lumna 100 - 200 orange/cream grey T . purpurascens 20 - 100 cream grey E . p l i ca tus 50 - 100 cream brown E . modestus 50 - 120 cream grey

Tab l e 4. Records of the presence of ovigerous lame l lae i n adult Balanus trigonus, from L e i g h .

Date Sample s i z e % without % immature % mature lamel lae l ame l l ae lame l lae

19. 12. 64 12 100 0 0 21. 1. 65 54 67 33 0

2. 2. 65 37 81 19 0 3. 2. 65 8 63 37 0

21. 2. 65 82 38 45 17 20. 3. 65 47 98 0 2 29. 8. 65 8 100 0 0

Seasona l var ia t ion in breeding per iods has f a c i l i t a t ed the d i s t i n c ­t ion of n a u p l i i i n European waters because of the r es t r i c t i on to a few spec i es at any one t ime. On l o c a l shores, Elminius modestus, E. plicatus and Chamaesipho columna possess mature n a u p l i i i n at l eas t some ind i v ­idua l s i n a l l months. Others have a predominantly summer breeding period (Chamaesipho brunnea and Balanus trigonus) or a winter breeding period (poss ib ly Balanus vestitus). A l though the presence of r i p e ovigerous lamel lae i n the mantle c a v i t i e s of the adult populat ions does not necess ­ar i l y ind icate the period of spawning and neither ind ica te the se t t l ing season, It i s un l i k e l y that at any one time there would be l e s s than three of the spec i es of barnacles present i n the p lankton as l a rvae . Furthermore, the larvae of other barnacles that ex is t on or near New Z e a l a n d shores are even l e s s known than the ones wi th a brief mention i n th i s paper, e. g. Balanus amphitrite. Balanus decorus and Lepas spp.

The separat ion of the barnacle n a u p l i i .

The s im i l a r i t y of barnacle naup l i i i s at once apparent, which ind ica tes that the ancestor of the Tho rac i c a underwent a metamorphosis s im i l a r to that of the present members of the group (Groom, 1892). The

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s im i l a r i t i e s of the larvae may we l l be use fu l i n deducing the phylogeny of the T h o r a c i c a . The ident i f i ca t i on of n a u p l i i requires f i r s t l y the descr ip t ion of each stage of each spec i e s and secondly the recogni t ion of sets of d iag­nost ic characters which for p lankton ana l y s i s need to be eas i l y ascer ta ined or measured. The use of l imb se ta t ion formulae i s at once d i scarded for the reasons g iven above. The use of s i z e i s of some use , except that as i n a l l b i o l og i ca l samples a range of s i z e i s more appropriate than a s ing le measure­ment. Al though the s i z e range of each stage of a spec i e s may be e x c l u s i v e , overlap with the same or other spec i es occur . The shape of the carapace and labrum, and the arrangement of the ventra l sp ines on the abdominal process are somewhat better and more readi ly observed charac ters . The seasona l occurrence of larvae may be of some use with some s p e c i e s .

The toothed s ing l e , or almost s ing l e , labrum may be character is t i c of the Chthamal idae. In New Z e a l a n d the Chamaesipho spec i e s m a y b e separated by the s i z e d i f ference and the expected s easona l occurrence of C . brunnea during mid and late summer. The Ba l an idae have a tr i lobed labrum at a l l stages without prominent d i s t a l teeth. The ident i f i ca t ion of the naup l i i may be attempted on the l i n es already suggested, but obv ious ly awaits further inves t iga t ion into the l i f e h i s to r i es of a l l s p e c i e s .

S U M M A R Y

The f irst and second stage naup l i i of seven spec i e s of New Zea land barnacles are brief ly descr ibed wi th respect to characters that might be used for the ident i f i ca t ion of bulk samples of n a u p l i i co l l ec ted from the plankton. The Chthamal idae may be d i s t ingu i shed from the Ba lan idae by the presence of a s ing le lobed and toothed labrum. Data i s a l so g iven on the breeding seasons of the spec i e s .

R E F E R E N C E S

B a s s i n d a l e R., 1936. The developmental stages of three E n g l i s h barnac les , Balanus balanoides, Chthamalus stellatus and Verruca stroemia. Proc. zool. Soc. Lond., 106; 57 - 74.

Batham E . J . , 1946. Pollicipes spinosus Quoy and Gaimard. II Embryonic and larva l development. Trans. R. soc. N. Z., 75; 405 - 418.

Cr i sp D. J . , 1962. The p lanktonic stages of the C i r r i p e d i a Balanus balan­oides ( L . ) and Balanus balanus ( L . ) from north temperature waters. Crustaceana, 3; 207 - 221.

Groom T . T . , 1892. On the early development of C i r r i p ed i a . Proc. R. Soc. 52; 158 - 162.

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Jones L . W., and C r i s p D. J . , 1954. The l a r v a l stages of the barnacle Balanus improvisus Darw in . Proc. zool. Soc. Lond. 123; 765 - 780.

Kn ight -Jones E . W. and Waugh G . D . , 1949. On the l a r va l development of Elminius modestus Darw in . J. mar. biol. Ass. U. K., 28; 413 - 428.

Moyse J . , 1961. The l a r va l stages of Acasta spongites and Pyrgoma anglicum (C i r r iped ia ) . Proc. zool. Soc. Lond., 137; 371 - 392.

Moyse J . , 1963. A comparison of the va lue of f lage l la tes and diatoms as food for barnacle larvae. J. Cons. int. Explor. Mer., 28; 175 - 187.

Newman W. A . , 1965. P rospec tus on l a r v a l c i rr ipede setat ion formulae. Crus taceana , 9; 51 - 56.

Norr is E . and C r i s p D. J . , 1953. The d is t r ibut ion and p lanktonic stages of the c i r r ipede Balanus perforatus Brug ie re . Proc. zool. Soc. Lond., 123; 393 - 409.

Pye f i n ch K. A . , 1949. The l a r v a l s tages of Balanus crenatus. Proc. zool. Soc. Lond., 118; 916 - 923.

Sandison E . E . , 1954. The ident i f i ca t i on of the naup l i i of some South A f r i can barnacles with notes on their l i f e h i s t o r i e s . Trans. R. Soc. S. Africa., 34; 69 - 101.

Wisely B . , I960. Exper iments on rearing the barnacle Elminius modestus Darwin to the se t t l ing stage i n the laboratory. Aust. J. mar. Freshw. Res., 11; 42 - 54.