Larval and Early Post-Larval Stages in the Abbreviated Development of Heterosquilla Tricarinata (Claus, 1871) (Crustacea, Stomatopoda)

Journal of Plankton Research Volume 6 Number 4 1984

Larval and early post-larval stages in the abbreviated development of Heterosquilla tricarinata (Claus, 1871) (Crustacea, Stomatopoda)

J.G. Greenwood* and Barbara G. Williams Portobello Marine Laboratory, University of Otago, Portobello, Otago, New Zealand (Received September 1983; accepted March 1984)

Abstract. Heterosquilla tricarinata was laboratory-cultured through its complete larval development and found to have one propelagic and two pelagic larval stages prior to metamorphosis to the Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 juvenile. These larval stages, the first juvenile, and relevant portions of the second juvenile stage, are described and figured. Individual larvae do not change in size during intermoult periods. Larvae occurring in the plankton show a progressive decrease in mean size between early (September) and late (November) springtime. Reasons for this are suggested. The first pelagic stage of H. tricarinata is anatomically very advanced in development, and the number of pelagic stages very few, in comparison with other known stomatopod life-histories. Ecological implications of this are discussed in relation to the high-latitude distribution of the species. Comparison is made between the final pelagic stage of H. tricarinata and that of its congenor H. brazieri.

Introduction Larvae of only two species of stomatopod have been recorded from New Zealand waters. Wear (1965) captured larvae of Heterosquilla tricarinata (as H. spinosa) and Pterygosquilla armata schizodonta (Milne Edwards) (as Squilla armata) from plankton in Wellington Harbour, which he identified by rearing through to the juvenile stage. Although no description of rearing stages was given, Wear (1965) figured a dorsal view of a 'stage five larva' of H. tricarinata. It is not clear how Wear determined the stage of his larva, and from the characters figured it appears to have been a first pelagic stage. The only other account, and the only previous complete description, of NZ stomatopod larvae is Pyne's (1972) description of the two propelagic and nine pelagic stages of 5. armata. The present paper describes the single propelagic stage, both pelagic stages, and the early post pelagic development of H. tricarinata. H. tricarinata (Claus) is an inhabitant of burrows which it creates commonly in the lower intertidal region of sheltered sandy shores in New Zealand and adjacent Islands (Manning, 1966; Fussell, 1979) between -34°-55°S. Egg masses are deposited within these burrows where they remain until larvae are hatched and emerge. During the main emergence period these larvae are one of the major macroplankters in waters of Otago Harbour and adjacent regions. In a companion paper to the present one (Williams et al., 1984) we report the successful multiple laboratory rearing of H. tricarinata, development times for each larval stage, the seasonality and distribution of the larvae in the plankton off Otago, and the unusual eye development which occurs in the transition from

•Permanent address: Zoology Department, University of Queensland, Brisbane, Australia

© IRL Press Limited, Oxford, England 615 J.G. Greenwood and B.G. Williams planktonic larva to benthic juvenile. Three larval stages occur prior to transition to the postlarval form: a single propelagic stage occurs within the parent burrow and occupies —30 days from hatching. Following a moult to the first pelagic stage, larvae emerge from the burrows and become planktonic. After -15 days these first pelagic larvae moult to the second pelagic stage, and 20 days later moult again to the first postlarval stage, which itself has a duration of ~ 16 days. (All the above times are based on rearing at 15°C.) Overall development time from hatching to 1st post larva is therefore -60 — 70 days. Methods Procedures used to obtain egg masses and to culture larvae are given elsewhere

(Williams, et al., 1984). Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 Descriptions given here are based on larvae from laboratory culture with, in all cases, both moulted larvae and cast exuviae being available for verification of stages. Further specimens for dissection, measurement and study of temporal changes in size, were obtained from plankton samples taken within Otago Har- bour. Samples were generally fixed in 5% neutral formalin then transferred to 70% ethyl alcohol for storage. Whole animal measurements and drawings were based on animals from alcohol storage. Specimens for dissection and drawing of appendages were first warmed gently in ~5°7o KOH to remove tissues, washed and lightly stained with chlorazol black and/or lignin pink, then stored in 70% ethanol. Dissections and slide preparations were made in glycerol and/or lactic acid. Drawings were made with the aid of camera lucida drawing tube attachments. Each drawing is based upon one specimen. Descriptions given in the text result from equally detailed examination of at least 10 more specimens of the same stage, and partial examination of many more. All measurements were made microscopically with the aid of ocular micro- meters. Dimensions were measured as follows: total length, from tip of rostrum to posteromedial cleft of telson; rostral length, from tip of rostrum to midpoint of a transverse line between posterior borders of orbits; carapace length, medially from the same posterior orbit line to the posteromedial border of carapace (not including spine); telson length, along its midline; telson width, greatest width; protopod of second maxilliped, maximum length of that segment. Terminology of setal types is based on that used by Factor (1978). Results Larval colouration Propelagic larvae are conspicuously bright orange in general appearance because of the abundance of residual yolk material retained in the hepato- pancTeatic region. This mass occupies most of the cephalothorax. The abdomen is transparent. The orange yolk mass is progressively reduced through the non- trophic propelagic development. The pelagic stages are basically transparent with a slight blue-green tinge due to pigment in the buccal region, mero-carpular and propodo-dactylar junctions of the second maxilliped, distally in the protopod of

616 Larval stages of Heterosquilla all pleopods, and in the anal region. Eye colour is lime-green peripherally, black centrally. Description of larval stages Larval dimensions are given in Table I, and some aspects of setation in Table II. Propelagic stage (Figures 1A, 2). Rostrum relatively short, ventrally deflected, without ornamentation, not reaching beyond antennular flagella. Eyes sessile, fused to rounded anterolateral margins of carapace. Carapace rounded dorsally over prominent yolk-mass, covering all except last thoracic somite. Postero- lateral carapace spines simple, curved dorsolaterally, not extending beyond level

of first abdominal segment when viewed dorsally. Dorsal carapace spine present Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 posteromedially. Last abdominal somite (6th) with pair of small submedian spines posterodorsally. Antennule (Figure 2A) triramous. Inner flagellum of three segments; distal segment with long terminal seta, 2 small subterminal setae; other segments each with

Table I. Dimensions of larvae in four developmental stages (September samples) - measurements in mm.

Dimension Developmental stage Propelagi( Pelagic 1 Pelagic 2 Postlarval

n X SD n X SD n X SD n X SD

Total length 8 5.88 (0.28) 10 10.26 (0.18) 7 13.24 (0.48) 7 13.7 (0.74) Rostral length 8 0.7 (0.03) 10 2.48 (0.13) 7 2.7 (0.22) 7 1.03 (0.05) Carapace length 8 2.08 (0.15) 47 2.51 (0.11) 29 2.86 (0.12) 16 2.75 (0.13) Telson length 8 0.75 (0.06) 10 1.22 (0.07) 7 1.46 (0.07) 7 1.46 (0.07) Telson width 8 1.0 (0.05) 47 1.57 (0.08) 29 1.87 (0.08) 18 2.34 (0.10) Mxpd 2 propod. 8 1.15 (0.07) 47 2.08 (0.09) 29 2.54 (0.10) 18 2.68 (0.09)

Table n. Number of peripheral setae on the distal segments of pleopods and uropods in the four developmental stages

Pleopod Developmental stage Propelagic Pelagic 1 Pelagic 2 Postlarval 1

exopod 12-13 26-27 28-33 36-38 endopod 10 18-20 20-21 -18 , exopod 12-13 29-31 32-36 43-44 endopod 10-11 18-21 20-23 -23 exopod 14-15 29-32 34-39 -43 endopod 8-10 19-22 21-23 22-23 exopod 11-12 28-32 30-35 -42 endopod 9-10 19-21 21-23 -23 exopod 10-11 23-28 30-32 34-38 endopod 8- 9 19-21 19-21 20-22 ,, . exopod 2 4-10 13-15 -25 UrOpOd endopod 2 5-7 6-9 -30

617 J.G. Greenwood and B.G. Williams

B Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021

Fig. 1. H. tricarinata developmental stages, dorsal view. A, propelagic; B, first pelagic; C, second pelagic; D, first postlarval.

1 longer 2 shorter setae distally. Outer flagella pair shorter than inner, comprises 3-segmented median flagellum and much broader outer branch, the latter with 5 groups of aesthetes along length proximal to distal, formula being 2,3,3,2,2; 2 small setae proximally. Antenna (Figure 2B) biramous; exopod (scale) with —12 — 13 biplumose setae on distolateral margins; endopod rudimentary, clearly 2-segmented with indications of further segmentation, 2 small distal setae. Mandible (Figures 2C, 6A) with incisor and molar regions differentiated; incisor ridge very simple, with ~3 incipient denticles; molar region almost smooth. Maxillule (Figure 2D) with ~ 11 cuspidate setae on flattened medial border of coxal endite, 2 small setae on inner face; basal endite continuing into large distal spine, with longer stout seta and setal bud more distally; palp a distinct segment with 2 simple setae. Maxilla (Figure 2E) indistinctly divided into 5 endites having 2, 3, 4, 5, 4 setae proximal to distal.

618 Larval stages of Heterosquilla Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021

1-0mm 0-5 mm

Fig. 2. H. tricarinata propelagic stage appendages. A, antennule; B, antenna; C, mandible; D maxillule; E, maxilla; F —J, maxillipeds 1—5 respectively; K,L,M, pereiopods 1, 2, 3; N —R, pleopods 1 —5 respectively; S, uropod, ventral view; T, telson, dorsal view.

First maxilliped (Figure 2F) chelate. Ischium without setae; merus with 3 setae distally; carpus with -10 setae in distal third; propodus with -12 weakly serrulate setae in 4 groups (3, 4, 3, 2), terminal border with 3 peripheral and 3 inner denticles; dactylus with 5 peripheral and 2 central denticles. Epipod present basal-

Second maxilliped (Figure 2G) subchelate, with dactylus - 0.8 x length of pro-

619 J.G. Greenwood and B.G. Williams

podus. No setae on basis, ischium, merus, or carpus; menus with posterior flang- ed groove into which portions of carpus and propodus can recess; propodus with stout arcuate spine proximally near depression into which tip of dactyl can recess, — 20 complex denticles spaced along inner margin ridge together with -20 minute setae lateral to the denticles. Dactylus with simple margins, 6 — 8 minute setae along length. Epipod present basally. Third, fourth and fifth maxillipeds (Figure 2H, I, J) fully segmented; third and fourth subchelate, but subchela of fifth poorly developed; setation as illustrated; third maxilliped the largest, fifth the smallest; each with epipod present basally. Pereiopods (Figure 2K, L, M) unsegmented, bud-like but distinctly biramous. Of similar size. All 5 pairs of biramous pleopods present (Figure 2N —R); appendix interna Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 distinct and bearing 3-6 minute hook-like setae; each ramus indistinctly divided into 2 segments, distal segment fringed with biplumose setae, the numbers of which for this and subsequent stages are summarised in Table II. Presumptive swelling of gill-bud evident on proxo-medial margin of exopod. Uropods (Figure 2S) with basal prolongation of two processes; outer process (spine) very robust and elongate, extending -1/3 length beyond exopod, much smaller inner process (spine) arising at point approximately central to endopod. No proximal spine. Endopod 2/3 length of exopod; 1 —2 minute setae distally. Exopod a single flattened ovoid segment with stout spine-like process continuing from disto-lateral border, 1—2 simple setae distally. Telson (Figure 2T) breadth -1.14 x length (see Table I) greatest width in posterior third; single distinct lateral, 2 intermediate and one elongate posterolateral spine on each side; posterior margin indented medially, bearing 10-11 sub-median denticles on each side, those nearest midline being smallest; margin between denticles minutely denticulate. First pelagic stage (Figures IB, 3). Rostrum elongate, length similar to that of carapace, extending forward in line of body beyond antennular flagella and with slight ventral curvature to mid-length. Anterolateral carapace margins now forming prominent supraorbital spines; posterolateral carapace spines now directed approximately in line with body and reaching to about posterior border of second abdominal segment, each spine with a carinate ridge which extends onto posterior third of carapace. Dorsal carapace spine extending to about posterior border of last thoracic segment. Eyes mobile, corneal region large. Antennule (Figure 3A) now with flagella more elongated and increased setation on peduncle segments. Cluster of small setae proximally on basal segment of peduncle. Inner flagellum of 5 segments, each with a distal seta, terminal segment with 1 long and 1 short seta. Median flagellum still of 3 segments; outer flagellum extending to midpoint of second segment and with setation and aesthetes distributed as previously. Antenna (Figure 3B) with endopod now longer than scale and divided into 3 — 4 segments, second with about 5 minute setae distally, last with 2-3 minute terminal setae as previously. Exopod fringed by about 29 - 30 biplumose setae. Mandible (Figures 3C, 6B) incisor ridge now with 7-8 acute denticles; molar 620 Larval stages of Heterosquilla Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021

0-5mm

Fig. 3. H, tricarinata first pelagic stage appendages. A, antennulc; B, antenna; C, mandible; D, maxillule; E, maxilla; F, first maxilliped with enlargement of distal region; G-J, maxillipeds 2 — 5; K —M, pereiopods 1 —3; N, first pleopod; O, fifth pleopod; P, uropod, dorsal view; Q, tdson, dorsal view. 621 J.G. Greenwood and B.G. Wlllbuns plate with peripheral obtuse denticles and transverse ridges. Maxillule (Figure 3D) as in previous stage but the basal endite now with terminal spine and two fully developed cuspidate setae; coxal endite now with about 13 cuspidate setae medially, 3 setae on inner face. Maxilla (Figure 3E) morphology as previously, setation of endites (proximal to distal) now 3, 3-5, 6-7, 8-9, 5-8. First maxilliped (Figure 3F) with increased setation. Carpus with about 23 setae in distal half; propodus with about 20 serrulate setae in 4 groups and two strong serrate setae sub-terminally on 'thumb' of chela; denticles of chela as shown in enlargement in Figure 3F. Epipod present basally. Second maxilliped (Figure 3G) with dactylus now relatively longer ( — 0.9 x

length propodus) and more acutely tapered than previously. Propodus with ma- Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 jor longitudinal ridge now bearing about 33 'denticles' (setae of complex structure Figure 6E); a second parallel minor ridge also now developed with about 9 small setae along its length; the two ridges continue proximally to form the borders of the depression into which the tip of the dactyl recesses. Dactylus with anterior margin (= inner of subchela) simple but with about 8 minute submarginal setae. Epipod present basally. Third, fourth and fifth maxillipeds (Figure 3H, I, J) with propodi relatively more expanded than previously, setation increased, and dactylus of fifth more differentiated. Each with epipod present basally. Pereiopods, (Figure 3K, L, M) considerably longer than those of propelagic stage, almost visible in dorsal view of animal, but segmentation still incomplete. Pleopods (Figure 3N, O) with peripheral setation considerably increased (see Table II). Gill buds now large and bilobed; appendix interna with 4—6 hook-like setae. Uropods (Figure 3P). Basal process with outer and inner spines as previously. Both exopod and endopod with increased numbers of peripheral setae (see Table II); exopod with additional small stout spine developing proximolateral to previous one resulting in 2 distolateral spines being present. The additional small spine is readily seen in cleared specimens, uncleared specimens must be oriented appropriately to make the spine visible. Telson (Figure 3Q) slightly broader than previously (breadth about 1.25 x length, see Table I), greatest width about midlength. Lateral spination as in propelagic stage. Number of submedian denticles on posterior now 10 — 12 each side of median notch; some asymmetry is found in this feature. Second pelagic stage (Figures 1C, 4). General appearance and morphology similar to that of first pelagic stage, but size generally increased (see Table I). Eyes show beginnings of swelling on proximo-medial surface of coraeal region which is presumptive development of the adult eye (see Williams, et al., 1984). Antennule (Figure 4A) with outer branch of outer flagellum relatively longer, now reaching beyond second segment of median flagellum. Swelling beneath setal cluster on proximal peduncle segment. Setation and aesthetes generally similar to previous stage. Antennal endopod (Figure 4B) now of 5 — 6 segments, each segment with distal

622 Larval stages of Heterosquilla Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021

1-0 mm

Fig. 4. H. tricarinata second pelagic stage appendages. A, antennule; B, antenna; C, mandible; D, maxillule; E, maxilla; F-J, maxillipeds 1-5; K-M, peieiopods 1-3; N, first pleopod; O, second pleopod; P, uropod, ventral view; Q, tdson, dorsal view.

623 J.G. Greenwood and B.C. Williams seta, 3rd and 4th with additional setae. Exopod with 28-31 peripheral biplumose setae. Mandible (Figures 4C, 6Q and maxillule (Figure 4D) essentially unchanged. Maxilla (Figure 4E) now with increased setation on endites, there being (proximal to distal) 5-7, 6, 8-10, 11-13, 10. First maxilliped (Figure 4F) with increased setation, there being -3—4 distally on the ischium, 10-12 on the merus, 27-30 on the carpus, 24-26 on the propodus these being arranged in 6 transverse rows of 3 — 5 setae each; many of these setae have finely serrulate margins. The number of serrate setae on the thumb is now 3. Propodus 'thumb' with four peripheral denticles, dactylus with 6 forming chela; ~7 setae near base of dactylus. Epipod present basally.

Second maxilliped (Figure 4G) similar to previous except that: denticulate ridge Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 of propodus now bears >40 'denticles'; anterior (inner) margin of dactylus now slightly sinuate and with — 8 — 9 minute submarginal setae. Epipod present basally. Third, fourth and fifth maxillipeds (Figure 4H, I, J) further developed and fifth now clearly subchelate. Propodus of third and fourth almost as broad as long. Setation of these appendages now as figured. Basal epipods now relatively large. Pereiopods (Figure 4K, L, M) greatly enlarged beyond previous stage; first smallest, third longest; segmental nodes clear. Exopod a single segment, endopod of 2 segments. No setae present. Pleopod (Figure 4N, O) with further increase in setation, especially on both proximal and distal segments of exopods and endopods (see Table II). Gills now obvious multiramous structures. Uropod morphology (Figure 4P) basically as previously but with two changes in ornamentation: peripheral setation of exopod and endopod is increased (Table II); most notably, the number of disto-lateral spines is further increased so that in addition to the major (propelagic) one there are 2 or 3 smaller ones. As with the previous stage, observation of the smaller of these spines (most proximal) may re- quire correct orientation or clearing of the specimen. Telson (Figure 4Q) breadth -1.13 x length (see Table I), greatest width in anterior third. Ornamentation of lateral margins is notably changed toward that of adult: on each side, the lateral (most proximal) spine and the more proximal of the two intermediate spines each has a small second spine developed immediately anterolateral to it so that a paired structure is produced with the original (propelagic/first pelagic) spine now arising within a concavity between the new outgrowth and the telson margin. On each side of the telson there are therefore 2 paired and 2 single spines. Some slight variability in the extent of this new development was noted, especially in the degree of development of the 'new' lateral spine and careful examination of specimens may be needed. In 101 specimens closely examined by the authors, 2 were found in which although the individual was otherwise clearly in the second pelagic stage, the telson was in- determinate, having only some of the appropriate spines actually paired. Posterior margin of telson with -11 — 13 submedian denticles each side of the median notch. 624 Larval stages of Heterosquilla

First postlarval stage (Figures ID, 5). General morphology radically different from that of previous stages, particularly due to changes in the carapace and its spines, the rostrum, second maxilliped, pereiopods, uropods and telson. Body size increased (total length 12-13 mm). Rostrum (Figure ID) movable, triangular, as long as wide, rounded proximally tapering to acutely rounded tip. Reaches to midlength of proximal antennular peduncle segment. Antennular somite with acute antero-lateral process visible either side of rostrum. Carapace without spines or carinae; abbreviated, no longer covering last 3 thoracic somites; anterolateral and posterolateral borders rounded; slight increase in width to posterior third.

Last 3 thoracic somites (6th — 8th) smooth dorsally, convex laterally, narrow- Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 ing anteriorly and with obtuse posterolateral projection. Walking legs extended laterally, large obtuse spine visible on proximal segment of each. Abdominal segments with sinusoidal posterior margin leading to moderately acute posterolateral corners, those of last two segments being the most acute. Pair of submedian spines posterodorsally on last segment as in earlier stages. Eyes still of larval form, but presumptive bud of adult eye prominent. Antennule (Figure 5A) peduncle with proximal setose (14 — 20) papilla; all peduncle segments with distal setae (~ 10 —14, 15 — 20, 4 — 5, respectively). Inner flagellum of ~ 9 segments each bearing 3 — 8 distal setae; median flagellum of 8 segments each with 3 — 5 distal setae; outer flagellum of 5 segments bearing aesthetes in 5 groups (2, 3, 3, 2, 2 proximal to distal) as previously. Antennal scale (Figure 5B) 0.43 x length of carapace, fringed with -35 biplumose setae. Flagellum, including peduncle, with 11 segments, proximal 2 setose as indicated, remainder with -6 — 11 small setae distally on each. Mandible (Figures 5C, 6D) similar to previous stages; palp not apparent. Maxillule (Figure 5D) with additional small seta on basal endite; several small setae on surface of coxal endite, medial surface now with -16 major cuspidate setae. Maxilla (Figure 5E) with setation of endites (proximal to distal) now 9-10, 3, 11-12, 13-15, 9-11. First maxilliped (Figure 5F) with increased setation, especially ventrally on the ischium and merus. Epipod present basally. Second maxilliped (Figure 5G) basis with prominent spine projecting disto- medially. Propodus with one large and two smaller spines proximally bordering depression into which dactyl tip recesses; denticulate (pectinate) ridge with 48 — 50 complex denticles; parallel simple ridge with 12 small setae. Dactylus considerably modified; inner margin with 10 'teeth', most proximal smallest, distal one formed by tip of dactyl; small seta near base of most teeth. Epipod present. Maxillipeds 3 — 5 (Figure 5H, I, J) markedly more hirsute on all segments (as figured). Propodus width of 3rd and 4th maxillipeds ^length. Epipods present. Pereiopods (Figure 5K, L, M) now fully segmented and setose. Proximal segment with two obtuse spines, one medial, one distal. Exopods flattened and fringed 45-50 weakly biplumose setae. Endopods of 2 segments; first longer, reaching beyond exopod, ~ 6 - 8 distal setae; second truncated convexly ventrally 625 J.G. Greenwood and B.G. Williams Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021

Fig. 5. H. tricarinata first postlarval stage appendages. A, antennule; B, antenna; C, mandible; D, maxillule; E, maxilla; F-J, maxillipeds 1-5; K-M, pereiopods 1-3; N, uropod, dorsal view; O, first pleopod; P, fifth pleopod; Q, telson, dorsal view.

626 Larvml stages of Heterosquilla with dense tuft of -25 simple setae arising. Pleopods (Figure 5O,P) with further increased fringing setation (see Table II) and branching of gills. Uropod (Figure 5N) with basal process having outer and inner spines as previously (outer now only just extending beyond exopod) and additional proximal spine near articulation point of endopod. Endopod with weakly plumose peripheral setae (Table II). Exopod now of two segments; proximal segment longer, with small fringe of setae on medial border, and 6 distolateral spines, distal spine longest extending beyond midpoint of second segment, proximal spine very small; distal segment about ovoid with weakly plumose peripheral setae distolaterally (Table II).

Telson shape changed (Figure 5Q) (Table II). Width now 1.45 x length and Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 widest region in anterior third. Arrangement of spines on the lateral surfaces is as in the second pelagic stage but by virtue of the changed telson shape these spines now occupy a more posterolateral position. Posterior margin with —13 — 14 submedian denticles each side of the median notch. Second postlarval stage (in part) (Figure 6F, G) The most notable changes occurring in the moult from the first postlarval stage concern the telson and uropods. Description here is limited to those structures. Telson (Figure 6F) now very broad ( — 1.8 x length) with an elevated central region leading to an acute tooth, situated just anterior to the posteromedial telson margin, with similar submedial tooth placed each side and slightly more anteriorly. Three pairs of major lateral teeth (elaborations of those developed in the second pelagic stage) — fixed laterals and intermediate, moveable posterolateral (= submedian). The first pelagic lateral and 2 intermediate spines remain as denticles between these new teeth. Posterior margin with 11-14 submedial teeth either side of the medial notch. Uropod (Figure 6G) similar to previous stage, but the basal process now with a conspicuously developed ventral carina running the length of the distal spine; inner spine much shorter than outer (— 0.2) and with similar sized and obvious proximal spine. Variation in dimensions of larvae Larval dimensions and the general change in size that occurs between moult stages have been given in Table I for specimens collected in September. There is no apparent change in body dimensions of individuals within at least the first pelagic stage: eight laboratory-reared 1st pelagic larvae (at 24 h old) were repeatedly measured during December after 2, 6 and 9 day intervals, and no significant differences in individual dimensions were found. There are however indications that absolute size of each pelagic stage differs at different times in the breeding season. In Table III measurements of three characters are given for groups of first pelagic larvae taken in plankton samples from Otago Harbour in three con- secutive months during the major period of abundance (17 September, 13 Oc-

627 J.G. Greenwood and B.C. Williams A Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021

Fig. 6. H. tricahnata A - D mandibles of A, propelagic (x 240); B, first pelagic (x 120); C, second pelagic (x 120); and D, first postlarval (x 120) stages; E, spines of denticulate ridge on first pelagic maxilliped 2 propodus (x 720); F, telson and uropod; G, uropod of second postlarval stage, ventral view (Scale line = 2 mm). 628 Lanrml stages of Heterosquilla

Table III. Dimensions of three structures in first pelagic stage larvae from three monthly plankton samples, (measurements in mm).

Structure Month sampled September October November n X SD n X SD n X SD

Carapace length 47 2.51 (0.11) 20 2.25 (0.06) Mxpd 2 propod. 47 2.08 (0.09) 34 1.96 (0.12) 20 1.81 (0.06) Telson width 47 1.57 (0.08) 27 1.52 (0.05) 20 1.41 (0.05) tobeT, 18 November 1981). A progressive decrease in larval size was evident during that period, the size differences between all pairs of months for each of the three structures measured being very highly significant (Mest, p< 0.001 except Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 for telson width September/October where p=0.02). Discussion Knowledge concerning larval development of stomatopods has been summarised by several authors. In some cases these have been regional summaries, and many planktonic larvae of unknown parentage have been included in a larval classification (e.g. Townsley, 1953; Shanbhogue, 1975). Manning and Proven- zano (1963), and Pyne (1972) provided lists of those species for which larval stages have been positively identified either by hatching eggs or by rearing late stage planktonic larvae to an identifiable juvenile stage. Those lists were updated by Provenzano and Manning (1978), and a further two species added by Morgan and Provenzano (1979). Larvae of 11 species are known from hatchings, and a further 25 by rearing through metamorphosis, making 36 validated species in total. Only one of these species has been reared from hatching to metamorphosis Gonodactylus oerstedii Hansen (Manning and Provenzano, 1963; Provenzano and Manning, 1978). H. tricarinata is the second species whose complete larval development is known. Most notable amongst many interesting features of the development of H. tricarinata are the extreme abbreviation of the larval life history, the advanced stage of development at which larvae hatch, and variability both within stages and between seasons in some features of larval morphology. These three phenomena are interrelated. Abbreviation of development Reduced duration of the planktonic phase in a crustacean life-history may result from a reduction in either the number of larval stages, or in the duration of each stage, (but see Gore et al., 1981 for an exception). Such abbreviation is usually viewed as an advanced evolutionary feature (Lebour, 1928; Scotto, 1979) and/or resulting from specialised ecological adaptation (e.g. Makarov, 1968; Lam, 1969; Forbes, 1973; Glaister, 1976; Greenwood et al., 1976; Gore et al., 1981; Andryszak and Gore, 1981). Ecological advantages suggested include reduced vulnerability to variation in adequacy of food supply (Sulkin, 1978), reduced planktonic predation (Boschi and Scelzo, 1968), reduced population loss 629 J.G. Greenwood and B.G. Williams by larval transport away from suitable adult habitats (Makarov, 1968; Wear, 1968; Gore et al. ,1981), inherited variability (Sandifer and Smith, 1979). Any advantages accruing from these phenomena must be balanced against the effects of reduced dispersal and genetic interchange between populations, and probable decreased ability to re-invade local areas devastated by disturbance (Reaka, 1980; Reaka and Manning, 1981). The number of pelagic stages found in the eight stomatopod species whose larval development is either fully known or presumed to be near complete (but lack- ing confirmation either from propelagic or postlarval moults) were summarised by Michel and Manning (1972), and updated by Williams et al. (1984). Four species have nine pelagic stages, two have eight stages, the remaining two species having six and four stages. H. tricarinata has achieved relative abbreviation of its pelagic life history by having only two pelagic stages. Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 Few data are available on either the duration of larval development in stomatopods or on egg size and embryological development (Reaka, 1979; Williams et al., 1984). It is not surprising that a relatively very high-latitude stomatopod such as H. tricarinata has few pelagic larval stages and large egg size with prolonged embryological development, for the phenomenon is well known (Thorson, 1950), and there are many crustacean examples where these correlations with latitude apply (see e.g. Barnes and Barnes, 1965; Vance, 1973; Reaka, 1979), though it is not true of all (Underwood, 1974; Jones and Simons, 1983). Reaka (1979) in her examination of coral-reef-dwelling stomatopod life-history patterns did not examine the number or duration of planktonic stages in the life histories, but she did examine relationships between latitude, egg size, body size and clutch size, and from this inferred duration of the pelagic phase. She found that although there was no overall correlation between either body size and latitude or egg number and latitude within this group of coral-dwelling stomatopods, for a given body size egg numbers per reproductive effort and percentage clutch volume did decrease with increasing latitude. In more recent studies (Reaka, personal com- munication) on other and larger groups of stomatopods a correlation between body size and latitude has been found. The occurrence of a relatively small number of large eggs in H. tricarinata (Williams et al., 1984) agrees with those findings. Reaka (1979, 1980) also found that within coral-dwelling stomatopods there was a positive correlation between egg size and the geographical range of a species. From this she concluded that larger egg size does not result in a decreased planktonic phase, but rather in an increased size at settlement and hence greater ability to capture prey and avoid predators (see also Reaka and Manning, 1981). These latter conclusions are only partially true for H. tricarinata. Large egg size is accompanied by a compressed larval development, but the result is that duration of the pelagic phase is similar to that found in more tropical species (Williams et al., 1984). Size at settlement in H. tricarinata is -13.7 mm total length (Table I). In comparison with the 16 species of postlarvae whose measurements were tabulated by Alikunhi (1967), those of H. tricarinata are toward the small end of the spectrum, there being only five species with smaller postlarvae. Similarly the range of post-larval sizes given by Reaka (1979) for 27

630 Larral stages of Heterosquilla species was from 7 mm to 45 mm, there being 13 species with postlarvae larger than those ofH. tricarinata. Large egg size does not appear to have resulted in increased size at settlement in this species. Interestingly, the stomatopod Pterygo- squilla armata schizodonta, whose geographical range overlaps that ofH. tricarinata (though not extending beyond about 45 °S), shows no abbreviation of its pelagic life-history, passing through nine pelgic stages in an estimated -260 days (Pyne, 1972). Size of the postlarva is not known for that species, but the 9th pelagic stage is large (20-21.5 mm in length). There are therefore no apparent similarities in high-latitude-related life-history specialisations of these two sympatric stomatopods. It appears then that the reduced number of pelagic stages in the life-history of H. tricarinata is not part of a latitudinal trend in stomatopods, nor has it resulted Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 in increased absolute size and hence offensive/defensive abilities at settlement. It may however compensate for reduced development rates at lower environmental temperatures, maintaining overall exposure times in the vulnerable planktonic phase to a period similar to that of its more tropical relatives. In so doing H. tricarinata achieves ecological advantages over the sympatric P. armata in reduced planktonic predation, reduced losses from transport in offshore currents, and optimised nutritional conditions for larvae by restriction of larval emergence and the planktonic phase to the spring period when potential planktonic food is abun- dant (Jillett, 1976; Williams et a!., 1984). Advanced stage of development Newly hatched larvae of H. tricarinata are anatomically very advanced when compared with other species, and cannot be fitted into the generally accepted scheme of larval types. As noted by Pyne (1972), derived from Giesbrecht (1910), and based on the limited data previously available, lysiosquillids 'normally' hatch at an antizoeal stage and develop into an erichthus larva. The propelagic stage of H. tricarinata conforms to the antizoal type in having sessile eyes, but in no other features. Rather it is already at the synzoeal stage, having all five pairs of maxillipeds, three pairs of legs, five pairs of pleopods, and uropods. In other stomatopods this stage is not normally attained until the 5th or 6th pelagic stage. Foxon's (1969) view was that it is more appropriate to adopt a larval classification based mainly on adult characters which appear late in larval life. Such a system seems more appropriate for species like H. tricarinata where much of the early development is compressed into embryological stages. On this basis the pelagic stages of H. tricarinata are of the Lysioerichthus type (Foxon, 1939). Differentiation of stages The four developmental stages of H. tricarinata described here are readily distinguished from each other. The propelagic and postlarval stages differ radically from the pelagic stages in most respects, including rostral development, carapace shape and spines, telson, uropod and eye morphology. The second pelagic stage is most readily distinguished from the first by the duplication of the more anterior two pairs of lateral telson spines, and a greater number of

631 J.G. Greenwood and B.G. Williams distolateral spines on the uropod exopod. In the present rearing program larvae were kept in individual containers so that exuviae could be observed, but no indication was found of any supplementary moults within instars, as are found for example in Chorisquilla tuberculata (Michel and Manning, 1972). Variability in larval stages Although the four stages are distinct and their number rigidly fixed, some variability was found within stages in details of setation and size. Where setation varied, an indication of the range encountered has been included in the descriptions above. Similarly, variation was noted in the degree of development of the paired lateral tclson spines in the second pelagic and postpelagic stages, and in the submedial telson spines of all stages (including some left/right asymmetry). Many factors may contribute to these variations, particularly the influence of Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 temperature and food availability on metabolism and growth (Boyd and Johnson, 1963; Costlow, 1965; Michel, 1968; Heegaard, 1971; Knowlton, 1974; Scotto, 1979). Costlow (1965) has shown that moulting and growth may be under independent endocrine control so that some independent variability in rate of development and duration of intermoult may be expected. Hartnoll and Dalley (1981) have shown that in longer larval developments, such as that of Palaemon elegans, the coefficient of variation for body size increased through a number of instars (to the 6th and the first postlarval) then abruptly decreased due to a regulatory negative feedback growth relationship at the preceding moult. Such variations in within-instar growth, independence of moult and growth cycles, and accumulative variation between regulatory moults may be reflected in minor mor- phological differences within an instar, even in an abbreviated development such as that of H. tricarinata. A further aspect of variation in larval morphology of H. tricarinata is the apparent decrease in average body size found in natural planktonic populations during the spring - summer period. Similar trends are found in other crustaceans (Barnes and Barnes, 1965; Greenwood and Jones, in preparation) and correlate with the fact that as temperatures rise through springtime the first maturing females in a population are the larger ones, which in turn produce larger eggs and hence larger larvae than those which mature later in the reproductive season under the influence of higher temperatures. In the case of H. tricarinata the first released larvae are possibly from subtidal populations not subjected to intertidal temperature extremes (Williams et al., 1984). Comparison with other stomatopod larvae Because of the advanced stage of development of H. tricarinata even at the first pelagic stage, it is not useful to compare these larvae with those of most other stomatopods. Comparison is therefore made only with the two known stages of a congenor as described by Michel (1969). Michel captured a final pelagic stage larva off New Caledonia which was maintained until it moulted to the postpelagic stage and was then identified as belonging to Heterosquilla brazieri (Miers, 1880). The two larval stages were described.

632 Larval stages of Heterosquilla

The final pelagic stage carapace of H. brazieri differs from that of H. tricarinata in being expanded posterolaterally near the origins of the posterolateral spines, and in having an accessory spinule near the base of each spine. Michel (1969) also suggested that the posterolateral spines may extend beyond the telson, but there is doubt about this, for his description of this stage was based upon an exuvium. The arrangement of telson spines is similar in the two species, but the development of paired lateral and anterolateral spines is much more pronounced in H. brazieri, the original (propelagic/first pelagic) member of each pair being dwarfed by the new (presumptive postpelagic) lateral member. The telson is also relatively much broader in H. brazieri. Differences in uropod armature include six outer spines on the exopod (cf. 3-4), and the inner spine of the basal process is subequal in length with the outer (cf. much smaller, -0.2). Downloaded from https://academic.oup.com/plankt/article/6/4/615/1440969 by guest on 01 October 2021 General morphology of the postlarvae in the two species is similar, but H. brazieri differs in having: a much more acuminate rostrum; only 6 dactylar teeth on the second maxilliped (cf. 10); 7 dorsal spines on the telson (cf. 3), and an additional marginal spine between the intermediate and moveable posterolateral spines; and most notably, the inner spine of the uropod basal process is longer than the outer (cf. 0.2 x in H. tricarinata). No other larvae of Heterosquilla species have been described. Acknowledgements We thank Beverley Dickson and Carolyn Munro for their willing assistance during this study, and Dr. Marjorie Reaka for the many helpful comments she made when reviewing the initial manuscript.

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