Bulletin of the Japanese Society of Scientific Fisheries 50(12), 1969-1973 (1984)

Egg Laying and Egg Mass Nursing Behaviour in the Japanese Mantis *1

Tatsuo HAMANO*2 and Shuhei MATSUURA*2 (Accepted December 5, 1983)

The spawning and egg mass nursing behaviour, together with the change in external appearance of the egg mass, of the mud-dwelling Japanese Oratosquilla oratoria were studied using artificial burrows in aquaria.

This usually spawns in a supine posture in the burrow maintaining this posture with the back of abdomen and exopods of uropods against the wall of burrow for almost 3 h. The newly extruded egg mass is amorphous, but the female shrimp compacts it and then shapes it into a thick disc within 1 h and to a thin disc having a marginal turnup within 24 h of spawning. All maxillipeds excluding the raptorial claw are used for the nursing behaviour, i.e. spreading and folding the egg mass, so it is teased out and becomes a tuft shape after 3 days or so. The second egg laying occurred in 2 females about 40 days after the first spawning of each individual at 25•Ž, and this fact suggests that O. oratoria may spawn more than once in a spawn ing season in natural warm waters.

The Japanese mantis shrimp Oratosquilla ora mm in diameter and 600 mm in length,8) on the

toria (DE HAAN) lives in burrows in the mud bot grit bed at the Fishery Research Laboratory of tom of bays and inlets. Although this species is Kyushu University, Tsuyazaki (Fig. 1). Six ani much used for edible meat in Japan, there is no mals in the first catch were reared in flowing, fresh detailed report of its behaviour. seawater where the temperature fell to 11.0•Ž in With many species of other orders, January, 1983 under natural photoperiod until the egg laying behaviour has been studied in detail. February 5 in 1983, and then the water tempera In Stomatopoda, however, an account of spawning ture was raised to 25•Ž and photoperiod was fixed behaviour has not been published notwithstanding at 15L9D. In addition, the 37 individuals from the known behaviour nursing the egg mass1-4) and the second catch were reared under natural sea embryonic development.1,5 water conditions and the temperature reached ) The present authors induced egg laying of the 30.2•Ž in August from 16.2•Ž in April, 1983. mantis shrimp by rearing in artificial burrows which made observation in aquarium of the be haviour of mud-dwelling mantis shrimp possible.8) The present paper contains the first description of spawning behaviour in Stomatopoda and detailed observations of nursing in relation to change in external appearance of the egg mass of the mantis shrimp.

Materials and Methods

Adult female mantis , more than 30mm in carapace length, were captured with a tow net in the waters of Hakata Bay, firstly 6 on September 28, 1982 and secondly 37 on April 26, Fig. 1. Aquarium arrayed in artificial burrows for 1983. They were kept in large aquaria, 102 x rearing of mantis shrimp. Rod on the right is 103x114cm, provided with artificial burrows, 56 an electric thermometer sensor.

*1 Ecological Studies on the Japanese Mantis Shrimp, Oratosquilla oratorio (DE HAAN)-‡U. *2 Department of Fisheries, Faculty of Agriculture, Kyushu University 46-04, Hakozaki, Higashi, Fuku

oka 812, Japan (ûM–ì—´•v•E•¼‰Y•C•½:‹ã•B‘åŠw”_Šw•”). 1970 HAMANO and MATSUURA

Fig. 2. Diagrammatic lateral view of mantis shrimp O. oratoria illustrating terms used in descrip tions.

Mantis shrimps were fed with short-necked clam, from the genital openings at the centre, ventrally and sardine. The mature ovary of mantis of the sixth somite, being linked each other by an shrimp can be seen through the ventral face of adhesive substance forming a string (Fig. 5). Then telson, so its shape was observed periodically to the eggs formed an adhesive mass of uncertain detect the degree of ovarian development. shape (Figs. 5 and 6-1) which dangled from the Terms used in this text are shown in Fig. 2, and edge of thoracic somites since during the progress size measurement follows MATSUURA and HAMA of egg extrusion the body always leaned to one NO. 8) side (Fig. 4-1). The kept this inclined posture, scarcely moving excepting the pleopods, Results until the end of spawning. The time required for egg laying was an average of 167 min for 5 spawn The Japanese mantis shrimp never laid eggs out ings; ranging from 125 to 217 min. of the artificial burrow. The shrimp always The female stretched her body out straight in the spawned within a week after the ovarian shape on supine posture after spawning, and then she form the ventral side of telson had assumed the shape of ed the egg mass compacting it by rotation of all an isoceles triangle (Fig. 3). the maxillipeds excluding the second, raptorial Egg laying took place in all of the 6 females claw. This compacting behaviour usually con reared in warmed water during the period from tinued for a quarter hour or so, to give the egg April 17 to June 1 in 1983 and in 22 of the 37 mass a globe shape. Following this compaction, females reared under natural water temperatures shaping behaviour was observed; the mantis shrimp during the period from May 14 to July 8 in 1983. alternately stretched and rotated the egg mass The Mann-Whitney U test showed that heated with the right and left portions of the meri to the water significantly promoted ovarian maturation in this species (U=5, P<0.001). Mantis shrimp started laying eggs during daylight hours in 15 of the 19 spawnings observed in aquaria. The entire process of egg laying was clearly observed in 5 cases and the spawning posture was observed in 11 cases. The female adopted a supine posture, firmly supporting the body on the inner wall of the bur row using dorsal portions of the first to the fourth abdominal somites and both exopods of uropods (Fig. 4). The pleopods were slightly elevated, but other parts, antennae, maxillipeds and pereopods, remained at rest, Animal intermittently adopted Fig. 3. Ventral surface of telson of well matured fe this posture for several hours before spawning. male of 0. oratoria. Arrow represents ovary Eggs were freely extruded onto the thoracic somites site. Scale 1 mm. Egg Laying Behaviour in Mantis Shrimp 1971

Fig. 4. Egg laying posture of mantis shrimp in artificial burrow . View from front (1) and view from behind (2). Identifying number is drawn on telson (2) . a: egg mass, b: the second maxilliped, c: the fifth maxilliped, d: the sixth abdominal somite, e: exopod of uropods.

Fig. 5. Lateral view of spawning posture of mantis shrimp, which was forcibly removed out of burrow to take photos during egg laving. Arrow represents egg mass. dactyli of the third to the fifth maxillipeds, so the was teased out by the maxillipeds and came to re egg mass was given a shape similar to a thick disc semble a tuft after 3 days or so, succeeding to within about I h after spawning (Fig. 6-2). Sub spawning (Fig. 6-4). At first, spawned female sequently the female continued shaping the egg always kept the egg mass with devoting almost half mass until it became a thin disc having a marginal of her time to nursing it; feeding occurred rarely turnup, about 10 cm in diameter, which was only and at times of emergence from the burrow the slightly adhesive (Fig. 6-3). The egg mass was egg mass was carried by the maxillipeds though usually given this form within 24 h after spawning. emergence seldom occurred. Finally, just before Then the animal commenced to nurse the egg mass, hatching, the female tended to neglect the egg mass which was alternately advanced and retracted or to a large extent, i.e. by laying it down in the bur spread and folded with the maxillipeds excluding row, to feed more frequently and by emerging, leav the second (Fig. 7). This nursing behaviour was ing it in the burrow, and not necessarily returning. continued until hatching though the frequency was However, any abandoned egg masses were eaten decreased gradually, and, therefore, the egg mass by other individuals, or became addled and never 1972 HAMANO and MATSUURA

Fig. 6. Reshaping of egg mass of mantis shrimp. Undefined shape during spawning at the same time as Fig. 5 (1), thick disc shape at 1 h following spawning (2), thin disc shape having marginal turnup at 28 h (3), tuft shape at 3 days later (4). Scale 1 mm.

sparent.

Two females which lost the egg mass during the

nursing period then resumed feeding and rapid

ovarian development again and the second egg laying occurred about 40 days at 25•Ž after the

first spawning.

On May 16, 1983 one female showed a different

spawning sequence and posture, which was very

similar to the usual compacting behaviour but dif fered in the extrusion of eggs. The female ap

peared to extrude the eggs directly into a shape similar to a ball of knitting yarn while in a standing

posture and this egg laying accompanied with egg compaction was continued for 22 min after the

Fig. 7. Egg mass nursing behaviour of mantis shrimp. present authors chanced upon it. The egg mass was eventually shaped into a thick disc shape (Fig. Arabic numerals represent orders of maxillipeds. 6-2) in only 13 min and the compacting behaviour developed. The period of the embryonic life re after spawning was omitted. All of the reared females with carapace lengths quired until hatching was about 14 days at 25•Ž. At the time of hatching the eggs became semitran exceeding 30 mm died by September 3, 1983 whe Egg Laying Behaviour in Mantis Shrimp 1973 ther the animal spawned or not, and most deaths subsequent shapes from Fig. 6-3 to 6-4. occurred in relation to ecdyses. The spawning season and the seasonal dynamics of the group gonadal index of O. oratoria have Discussion been studied well in Japan,8.11-1a) but those studies do not show the spawning frequency of a female in The egg laying behaviour of Oratosquilla oratoria a spawning season. The present study in aquaria is similar to that of one of the American showed that warm water promoted spawning of Pacifastacus trowbridgii7) and the Norwegian female of this species and that the ovary of indivi .e) All of these are duals which lost the egg mass developed rapidly mud or/and sand dwellers and spawn onto the again. These observations indicate the possibility ventral side of the body while supine. Although that the mantis shrimp may spawn more than once this posture may be essential to prevent sediment during a spawning season in natural warm waters. from attaching to the adhesive eggs in the case of animals which spawn in exposed places such as Acknowledgment on the surface of a fiat muddy bottom, this posture must involve large risks for the successful comple The authors are indebted to the following who tion of spawning without interference. Extruded have greatly contributed toward this study: Dr. eggs and even the female parent shrimp herself N. M. MORRISSY, Western Australian Marine may be injured and killed by other individuals or Research Laboratories, made so kind inspection carnivorous animals. Spawning in a burrow large of the manuscript; Prof. Y. ITAZAWAand Prof. Y. ly eliminates these dangers. The present species YONE, Kyushu University, advised and aided us never laid eggs outside the burrow, and the female throughout the study; Mr. M. IWAMIZU,a graduate ceased spawning when she was removed forcibly student of Kyushu University, assisted the trans from the burrow during the process of spawning. portation of the animals examined. In addition, this mantis shrimp strongly held itself in the burrow during spawning by pressing the References back of abdomen and the exopods of uropods againstthe wall of burrow (Fig. 4). These observa 1) T. KOMAI: Mem. Coll. Sci., Kyoto Imp. Univ., tions and inferences lead to the conclusion that O. Ser. B, 1, 273-283 (1924). oratoria in nature is adapted to a burrowing life 2) T. TAKAMATSU,T. MIMURA, and T. SHIOYA: and requires a burrow of compatible size, not only Aquicult., 14, 1-7 (1966). for every day living as described by MATSUURA 3) T. SHIOYA: Cult., No. 43, 92-94 (1967). and HAMANO,81but also for reproduction. 4) H. DINGLE and R. L. CALDWELL: Biol. Bull., 142, 417-426 (1972). The present authors think another spawning 5) S. M. SHTINO: Mem. Coll. Sci., Kyoto Imp. style, standing posture, was a result of the female Univ., Ser. B, 17, 77-174 (1942). beinginterrupted during the egg laying perhaps due 6) S. MATSUURAand T. HAMANO: Bull. Japan. Soc . to interference by other individuals. The egg Sci. Fish., 50, 1963-1968 (1984). handling behaviour during egg extrusion well 7) J. C. MASON: Crustaceana, 19, 37-44 (1970). resembledthe compacting behaviour which usually 8) A. S. D. FARMER: J. Zool., Lond., 174, 161- commenced after spawning. The shaping of the 183 (1974). egg mass was faster than normally observed, be 9) T. YORITA: Hokusuishi Geppo, No. 916, 2-14 cause the compaction after laying the eggs was (1972). omitted. 10) N. NATSUYAGiand M. IMAi: Kanagawa-suishi The shape of the egg mass of O. oratoria changed Kanazawa-bunjo Jiho, No. 9, 20-32 (1968). 11) I. Kuuo, S. HORI, M. KUMEMURA,M. NAGANAWA, with time (Fig. 6). KOMAII)and YORITA8)describ and J. SOEDJONO:J. Tokyo Univ. Fish., 45, ed it as a disc. On the other hand, TAKAMATSU 1-25 (1959). et al,2) SHIOYA3)and NATSUYAGIand IMAI10)gave 12) T. SENTA, A. SHIMIZUand T. HARADA: Bull. it as of undefinable form and looking like a piece Fish. Exp. St., Okayama Pref., 1968, 20-29 (1969). of yellow cloth. The former description cor 13) Y, HAYASHIand K. TSUJINO: Bull. Osaka Pref. responds to Figs. 6-2 and 6-3, and the latter to the Fish. Exp. St., No. 5,116-135 (1978).