RESEARCH NOTES 293 about the nature of muscle tissue changes in 3. MOMMSEN, T.P., BALLANTYNE, J-, MACDONALD, Photololigo sp. during senescence. Dying squid (eg. D., C-OSUNE, J. & HOCHACHKA, P.W. 1981. Moroteuthis ingens) can undergo very dramatic Proc NatL Acad. ScL USA, 78: 3274-3278. changes in muscle tissue in which the muscle fibres 4. MOLTSCHANIWSKYJ, N.A. 1993. Can. J. Fish. are completely absent and just the collagen structure AquaL Sci., 51: 830-835. remains.13 Likewise, the muscle fibres of senescent 5. PECL, G. 1994. BSc(Hons.) Thesis, James Cook Octopus vulgaris break down leaving spaces in the University of North Queensland. 12 tissue. This phenomenon was not present in any of 6. O'DOR, R.K. & WELLS, M J. 1978. /. exp. Bioi, the Photololigo sp. tissue samples examined. Fur- 77:15-31.

thermore, the relatively poor relationship between 7. POLLERO, RJ. & IRIBARNE, O.O. 1988. Comp. Downloaded from https://academic.oup.com/mollus/article/63/2/293/1056896 by guest on 29 September 2021 size, reproductive status and amount of disorganisa- Biochem. PhysioL, 90B: 317-320. tion suggests that this phenomenon may not be 8. MOLTSCHANIWSKYJ, N.A. 1995. Mar. Biot, V2A: directly due to either senescence or reproductive 127-135. activities. 9. HATFIELD, E.M.C., RODHOUSE, P.G. & BARBER, The presence of disorganised muscle fibres in the D.L. 1992. /. mar. bioL Ass. U.K., 72: 281-291. mantle muscle may affect the swimming abilities of 10. RODHOUSE, P.G. & HATFIELD, E.M.C. 1992. /. the squid. Circular muscle fibres are responsible for mar. bioL Ass. U.K., 72: 293-300. providing the power stroke in the flight response, by 11. GUERRA, A. & CASTRO, B.G. 1994. Antarctic forcing water out of the siphon.1 The radial fibres Sci., 6:175-178. provide the force to restore the mantle back to the 12. TAIT, R.W. 1986. PhD Thesis University of Paris resting shape.1 It may be envisaged that co-ordina- VI. tion of the muscle fibres to provide the force for the 13. JACKSON, G.D. & MLADENOV, P.V. 1994. J. jet propulsion may be impaired by a breakdown in ZooL Lond,, 234:189-201. the organisation of the fibres. 14. HOCHACHKA, P.W., MOON, T.W., MUSTAFA, T. J. Yeatman and C.C. Lu assisted with the identifi- & STOREY, K.B. 1975. Comp. Biochem. PhysioL, cation of adult and juvenile Photololigo sp. speci- S2B: 151-158. mens. PJ. Doherty allowed me access to juvenile 15. O'DOR, R.K. & WEBBER, D.M. 1986. Can. J. cephalopods caught using light-traps. B. Molony, ZooL, 64:1591-1605. J.H. Choat, G.D. Jackson, L. Winsor. B. Kier and 16. JACKSON, G.D. 1990. Veliger, 33: 389-393. the reviewers provided constructive comments and 17. JACKSON, G.D. & CHOAT, J.H. 1992. Can. J. discussion. This work was supported by a Merit Fish. AquaL Sci., 49: 218-228. Research Grant from James Cook University and 18. YEATMAN, J. 1993. PhD Thesis, James Cook was carried out whilst the author was a Common- University of North Queensland. wealth Scholar at James Cook University. 19. MOLTSCHANIWSKYJ, N.A. & DOHERTY, PJ. 1993. Fish. BulL, 92:109-119. 20. TABACHNICK, B.G. & FIDELL, L.S. 1989. Using REFERENCES multivariate statistics. Harper & Row, New York. 1. WARD, D.V. & WAINWRIGHT, S.A. 1972. J. 21. MARTINEZ, P. 1996. MSc Thesis, James Cook ZooL, Lond., 167: 437-449. University of North Queensland. 2. HANSON, J. & LOWY, J. 1957. Nature, 180: 906- 909.

/. Moll. Stud. (1997), 63,293-296 © The Malacological Society of London 1997

Effect of temperature on embryonic development of two freshwater pulmonates, comeus (L.) and planorbis (L.)

K. Costil Laboratoire de Zoologie et Ecophysiologie (U.A. INRA & U.M.R. du C.N.R.S. 6553), University de Rennes 1, Campus de Beaulieu, Av. du Ciniral Leclerc, 35042 Rennes Cedex, France

In freshwater Pulmonates, the embryonic develop- planorbis are freshwater snails commonly found in ment is direct and takes place in eggs. Eggs, which Brittany (France) where they belong to relatively comprise a zygote surrounded by perivitelline fluid rich communities.1 In our region, P. planorbis shows and membrane, are embedded in jelly and enclosed an annual life cycle with two generations per year, in a common egg capsule. The juveniles leave the whereas the P. corneus cycle tends to be longer egg capsule using their radula to gnaw the surround- and more variable according to year.2 In experimen- ing membranes. Planorbarius comeus and Planorbis tal populations of these , we already showed 294 RESEARCH NOTES the importance of temperature on behaviour - mean embryonic development duration is the (unpublished data), survival and growth,3 and mean time elapsing between the egg mass deposition 4 reproduction. We also verified the ability of self- and the emergence of the first juvenile: Dm; fertilization in these planorbid species and examined - minimum and maximum embryonic development the influence of the temperature on this mode of durations: respectively, D,^ and Dm; reproduction.5 In the present paper, we are inter- - hatching time is for a given egg mass the time ested in the impact of temperature on the embryonic elapsing between the hatchings of the first juvenile development of both species. and the last juvenile: Tb. Adult snails of both species were collected from A complete embryonic development followed by

two ponds located near Rennes (Brittany, France). the hatching of juveniles occurred between 10 and Downloaded from https://academic.oup.com/mollus/article/63/2/293/1056896 by guest on 29 September 2021 Brought to the laboratory, they produced snails 25°C for P. comeus, and between 15 and 25°C for P. which, grouped and reared at 20°C, grew and then planorbis (Table 1). In contrast to P. planorbis, P. laid egg capsules. These latter were used for the comeus developed but did not lay eggs at 10°C,4 experiments. The egg masses were individually which could seem illogical. However, in the present placed in little jars filled with 13 ml of pond water. study all the eggs placed in incubation were previ- During the experiments, the water was periodically ously laid at 20°C and it is possible that the tempera- agitated (to supply oxygen) but not changed or only ture at which the eggs were produced is also partly changed (when the development was long), important for the future development. At the tem- because the micro-organisms which then proliferate perature of 5°C, the embryos of both species did not tend to favour the opening of the egg masses and the develop. At 10°C, the hatching of P. comeus juve- hatching of juveniles.6 The effects of five constant niles was observed in only 28% of the egg masses, temperatures (5, 10, 15, 20 and 25°C) were tested and the mean hatching rate was low (37.3%). These and the photoperiod was L/D: 12/12 h. At each tem- results reflected the development difficulties at 10°C perature, the embryonic development was studied in which appeared close to the minimum threshold. 75 egg masses (total number of eggs ranging from The eggs of Lymnaea truncatula (Muller) laid at 5°C 1186 to 1205) for P. comeus, and in 30 egg masses did not develop.7 The embryonic development (total number of eggs ranging from 581 to 591) for P. requires a minimum temperature below which planorbis. Every day, the egg capsules were exam- anabolic reactions cannot be normally carried out; ined, the newly-hatched snails counted and then the thermic thresholds recorded for the embryonic removed. At each temperature, the following development can be related to the thresholds of bio- parameters were computed: chemical reactions, especially enzymatic ones.8 In - percentage of egg capsules in which eggs develop the present study, the upper limit of temperature until hatching: Pe, (at least one juvenile hatched); allowing the embryonic development was not reached. This is probably below the threshold of - mean hatching rate (in %): Hm = 100 1 (N/N )/N,. where N is the number of newly- 35°C found for the species adapted to tropical con- e m D ditions: Indoplanorbis exustus (Deshayes)9 and hatched snails issued from a given egg mass, Nc is the 10 total number of eggs contained in this egg mass, and Biomphalaria glabrata (Say ). The upper limit for No,, is the total number of egg masses investigated; the development of the lymnaeid of New Zealand, Lymnaea tomentosa (Pfeiffer), was 30°C." The eggs - minimum and maximum hatching rates: respec- of temperate species such as Lymnaea stagnalis (L.) tively, Hnt, and Hw;

Table 1. Total number of studied eggs and hatching rates in Planorbarius comeus and Planorbis planorbis reared at five constant temperatures ranging from 5 to 25°C.

Species 5°C 10°C 15°C 20°C 25°C

Total number of P. comeus 1189 1205 1197 1186 1190 studied eggs (75 capsules) P. planorbis 581 585 589 587 591 (30 capsules) P.,, (%) P. comeus 0 28 100 100 100 P. planorbis 0 0 98 100 100

Hm (% ± S.D.) P. comeus 37.3 ± 26.6 91.8 ± 10.8 93.6 ± 9.6 94.1 ±7.6 P. planorbis 0 88.7 ± 19.4 86.3 ± 18.2 89.7 ± 15.8 Hmi™ (%) P. comeus 4.8 55.5 52.6 74.2 P. planorbis 28.6 25 50 H™» (%) P. corneus 76.2 100 100 100 P. planorbis 100 100 100 RESEARCH NOTES 295

Table 2. Embryonic development durations (D) and mean hatching time (Th) in individuals of and Planorbis planorbis reared at four temperatures ranging from 10 and 25°C.

Species 10°C 15°C 20°C 25°C

Dm P. corneus 67.1 ± 7.6 25.7 ± 1.1 13.9 ± 0.8 8.5 ± 0.6 (days ± S.D.) P. planorbis 20.4 ± 3.7 9.2 + 0.8 7.0 ± 0.5

D^n (days) P. corneus 54 25 12 8 Downloaded from https://academic.oup.com/mollus/article/63/2/293/1056896 by guest on 29 September 2021 P. planorbis 17 8 6 Dm« (days) P. corneus 76 32 17 10 P. planorbis 29 11 8

Th (days) P. corneus 10.8 ± 8.9 3.5 ± 1.1 2.9 ± 1.4 2.7 ± 0.9 P. planorbis 2.8 ± 1.0 2.2 + 0.9 1.9 + 0.7 and Lymnoea peregra (MUller) develop when the the numerous biochemical processes occurring in the embryos. In two Egyptian freshwater snails, El Has- rearing temperature respectively ranges from 9.9 to 17 28°C12 and 7.5 to 30°C.i:! A normal development sen found similar results: between 15 and 30°C, until the trochophore stage is not always followed by hatching rates showed no considerable differences the-hatching of juveniles. An hypothesis to explain but embryonic development was accelerated and the this phenomenon is a lack of energy required for incubation period shortened as the water tempera- radular movements, after the fast utilization of ture was raised. In Physella cubensis, hatching energy stores during embryonic development.12 In occurred in 36, 13 and 9 days at 10, 20 and 30°C, respectively.18 Acceleration of development with the present study, it is possible that in a given egg 91013 mass some eggs did not develop because they had temperature has been reported by other authors. not been fertilized previously. From 15°C upwards, The best overall results in terms of innate capacity of the minimum hatching rate was never below 50% for increase and net reproduction for three South P. corneus, but dropped to 25% for P. planorbis. African snails were recorded at the higher fluctuat- ing temperature regime (18-28°C) compared to 5°C Percentages of 100% were not rare for both species. 20 At the three highest temperatures, the mean hatch- fluctuation and constant temperature."' As regards ing rates of both species did not vary significantly in the hatching time and hatching percentage, no signif- relation to temperature (Kruskal and Wallis tests, H icant differences were found between these three = 3.41 and p = 0.19 for P. planorbis; H = 2.51 and p different temperature regimes. In the field, L. stag- = 0.29 for P. corneus). They were of 92-94% for P. nalis eggs laid early during the season took a longer corneus, and close to 87-89% for P. planorbis, the time to develop than those which were laid later, probably because of the differences in water temper- greatest variation (reflecting by highest standard 21 deviations) having been observed in the case of the ature. In Egypt, the hatching time for eggs of Buli- latter species. Closely similar hatching rates have nus truncatus (Audouin) varied from 8 days in the hot month of July to 20 days in the cold month of been determined for different species: 94% in Physa 22 pomilia Conrad;'4 94.1% in L. stagnalis,'2 95.5% in January. Irrespective of temperature, the embry- 3 3 onic development of P. planorbis was faster than L. peregra.' For the latter species, Calow' and par- 23 ticularly Lambert16 found lower rates (ranging from that of P. corneus. According to Piechocki, the 62 to 73% and from 12-5 to 58.4%, respectively). It development of P. planorbis needs from 11 to 14 days at 20°C, that of P. corneus from 17 to 18 days. appears that the embryonic development depends 24 on the geographical origin of the individuals and is At 20°C, Alyakrinskaya has reported an embryonic part of demographic strategy. development lasting 11 to 13 days for P. comeus and Arakelova25 an incubation period of 17 days for P. The period of embryonic development was in- planorbis. This latter period corresponds to the versely proportional to temperature in both studied longest embryonic development which we observed species (Table 2). Significant differences were then at this temperature, but this concerns P. corneus and found between all temperatures: Kruskal and Wallis not P. planorbis. tests, H = 79.94 and p = 0.001 for P. planorbis; H = 227.53 and p = 0.001 for P. corneus. Development In our experiments, the development of embryos became particularly faster when rearing temperature located in a same capsule was not synchronous. The was 15°C compared to 10°C for P. corneus (factor of mean hatching time (Tb) was negatively related to 2.5), and 20°C compared to 15°C for P. planorbis temperature. Indeed, in P. corneus a significant neg- (factor of 2.2). The earliest hatching (at 6 days) was ative correlation was computed between the hatch- observed for P. planorbis eggs maintained at 25°C, ing time and the four tested temperatures: Kendall the latest (76 days) for P. corneus eggs at 10°C. Up rank correlation, t = -0.26, z = -6.03 and p = to a certain limit, raising the temperature accelerates 0.0001. For the individuals reared at 10°C a mean of 10.8 days separated the earliest hatching from the 296 RESEARCH NOTES last Between 15 and 25°C, the difference observed (Mollusque, Gastiropodc, ). Doc- between the two planorbid species was slightly less toral thesis, University of MontpeUier II than one day. In the case of P. planorbis, the mean (France), 185 pp. hatching time ranged between 1.9 at 25°C and 2.8 7. HODASI, J.K.M. 1976. Z. Parasitenk., 48: 281- days at 15°C. Oldham26 has reported time gaps up to 286. 12 days between the earliest hatching of P. comeus 8. HOFFMANN, K.H. 1983. Metabolic and enzyme and the last. Inter-individual variability increased as adaptation to temperature and pressure. In: The temperature decreased. Indeed, this variation was , 2: Environmental Biochemistry and more pronounced when embryonic development Physiology, 219-255. Academic Press, London. was longer. 9. VAIDYA, D.P. & NAGABHUSHANAM, R. 1978. Downloaded from https://academic.oup.com/mollus/article/63/2/293/1056896 by guest on 29 September 2021 At 10°C, P. comeus eggs develop with difficulty Hydrobiologia, 61: 267-271. and P. planorbis eggs do not develop at all. From 10. STURROCK, R.F. & STURROCK, B.M. 1972. Ann, 15°C, temperature has no effect on hatching rates, Trop. Med. Parasit, 66: 385-390. which illustrates the suitability of this temperature to 11. HARRIS, R.E. & CHARLESTON, W.A.G. 1977. induce the reproduction of these planorbid species New Zeal J., 41:45-49. and then the embryonic development Such a tem- 12. VAUGHN, CM. 1953. Am. Midi Nat, 49: perature is generally recorded from the end of April 214-228. in the ponds of our region, and the reproduction 13. AL HABBIB, O.A. & GRAINGER, J.N.R. 1981. /. period begins in mid-May in Breton populations of Therm. BioL, 6: 35-36. both species.2 On the other hand, temperature 14. DE WITT, R.M. 1967. Malacologia, 5: 445-453. strongly affects the embryonic development duration 15. CALOW, P. 1981. Malacologia, 21: 5-13. which decreases when temperature increases. Tem- 16. LAMBERT, M.C. 1990. Contribution a la biologie perature then has a pronounced influence on the et d Vtcophysiologie d'un Lymnaeidae armori- life cycle of P. comeus and P. planorbis and on cain: Lymnaea peregra (MUller) (Mollusque, the whole of their life history traits studied in the Gasttropode, Pulmoni, Basommatophorc). Ph laboratory: behaviour, survival, reproduction, post- D Thesis, University of Rennes (France), 317 pp. embryonic development and also embryonic devel- 17. EL HASSAN, A.A. 1974. Folia Parasit., 21: 181- opment as described in the present paper. So, 187. temperature appears to be one of the major abiotic 18. THOMAS, D.L. & MCCLINTOCK, J.M. 1990. factors controlling the populations of these temper- Invert Reprod. DeveL, 17: 65-71. ate freshwater snails. 19. DE KOCK, K.N. 1985. J. LimnoL Soc. Sth. Afr., Thanks are due to Stacy Payne for linguistic help. 11: 71-74. 20. DE KOCK, K.N. & VAN EEDEN, J.A. 1986. 5. Afr. J.ZooL, 21: 28-32. 21. BOAG, D.A. & PEARSTONE, S.M. 1979. Can. J. REFERENCES ZooL, 57: 353-362. 22. DAZO, B.G., HAIRSTON, N.G. & DAWOOD, I.K. 1. COSTIL, K. 1994. J. Moll Stud., 60: 467-471. 1966. Bull. Wld Hlth Org., 35: 339-356. 2. COSTIL K. & DAGUZAN, J. 1995. Malacologia, 23. PiECHOCKi, A. 1979. Fauna Slodkowodna 37: 53-68. Polski. Panstwowe Wydawnictwo Naukowe, 3. COSTIL, K. 1994. J. MolL Stud., 60,223-235. Poznan. 4. COSTIL, K. & DAGUZAN, J. 1994. Malacologia, 24. ALYAKRINSKAYA, I.O. 1981. Dokl Biol. ScL, 36: 79-89. 260: 472^74. 5. COSTIL, K. & DAGUZAN, J. 1995. Veliger, 37: 25. ARAKELOVA, E.S. 1982. Zh. Obshch. Biol, 43: 252-258. 553-559. 6. VIANEY-LIAUD, M. 1990. Biologie dt la repro- 26. OLDHAM, C. 1930. Naturalist, 801:177-178. duction de Biomphalaria glabrata (Say, 1818)