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Factors Regulating the Reproductive Cycles of Some Uest Coast Invertebrates

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Factors Regulating the Reproductive Cycles of Some Uest Coast Invertebrates FACTORS REGULATING THE REPRODUCTIVE CYCLES OF SOME UEST COAST INVERTEBRATES by John H. Himmelman B.Sc, Acadia University, 1967 M.Sc, Memorial University of Newfoundland, 1969 A thesis submitted in partial fulfillment of the requirements for the degree of DOCTOB OF PHILOSOPHY in the Department cf Zoology We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA June 1976 (<T) John H. Himmelman, 1976 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the Head of my Department or by his representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Zoology- Department of The University of British Columbia 2075 Wesbrook Place Vancouver, Canada V6T 1W5 July 9, 1976 Date ii ABSTRACT Annual reproductive cycles are found in many marine invertebrates. There is a vast literature on the subject, but the mechanisms involved have seldom been demonstrated. In the present study, 8 species of chitons and one sea urchin were studied for 3-5 years in southwestern British Columbia, at Vancouver and Porteau in the Strait of Georgia estuary, and at Botanical Beach on the outer coast of Vancouver Island. Reproductive condition was assessed mainly by the gonadal index method (percentage gonadal weight). There was a distinct annual cycle in the mean gonadal index of the urchin, Strongylocentrot- us droebachiensis Miiller, and the chitons, Tonicella lineata Wood, Tonicella insignis Reeve, Mogalia hindsii Reeve, Mo£alia laevior Pilsbry, Mogalia ciliata Sowerby, and Katharina tunicata Wood. In S. droebachiensis, T. lineata, T. insignis, M. laevior, and M. ciliata an abrupt spawning occurred in the spring, usually in April, and in M. hindsii there was usually an earlier spawning. K. tunicata sometimes spawned in April but the main spawning period was June. In M. laevior, K. tunicata, and probably M. hindsii, the gonads remained small during the summer and rapid gonadal growth occurred in the autumn and winter. In contrast, in S. droebachiensis, T. lineata, T, insignis, and !• Siliata gonadal growth started shortly after spawning. The data on reproduction in Mogalia ii9.H2§§ Gould were less clear. Mature animals were found in several seasons and drops in the mean gonadal index occurred in late winter-spring as well as in the summer. In Mo£alia luscosa Gould animals in ripe and spent condition were found throughout the year. Consideration was given to the possible factors controlling gonadal growth. In a number of species, particularly species of warm water origin, it has been clearly demonstrated that gonadal development in the spring and summer is stimulated by increased temperatures. If temperature affects gonadal development in the species in the present study, it must act in several ways, since gonadal growth occurs through 2-3 periods of steadily increasing or decreasing temperature. The initiation of gonadal growth in K. tunicata and T. lineata in California and Oregon occurred at the same time as in the present study, although temperatures in the southern localities were fluctuating due to upwelling, in contrast to the regular temperature changes which occurred in British Columbia. This would suggest that temperature was not important, at least during the early stages of gonadal growth in K. tunicata and T. lineata. There are distinct annual photoperiod changes throughout the geographical ranges of the species in the present study, and in S. droebachiensis, 1.' lineata, T. insignis, and M. ciliata most gonadal growth occurred during the period of decreasing day length. Food conditions are known to affect the number of gametes produced in a number of species, including S. droebachiensis and K. tunicata, but there is no evidence that the timing of gonadal growth in the species in my study is controlled by a change in food conditions. iii The importance of temperature in stimulating spawning has been stressed by many authors, but I know of no instance where it has been demonstrated that a temperature change, sufficient to induce animals to spawn in the laboratory, actually occurred at the time of natural spawning. At First Narrows, there was usually a major spawning when the temperature reached 7-8 °C in the spring. However, in 1971, S. droebachiensis spawned when the temperature was about 6.3 °C» and temperature differences would not account for an abrupt spawning in 1973 In: Perspectives in Marine Biology, A. A. Buzzati-Traverso (Ed.), University of California Press, Berkeley, pp. 67-36. Compared to the prolonged spawning in 1974. At Porteau, water temperatures showed a slow rise of only 0.8 °C during a two week period in which there was a complete spawning in To nice 11a lineata, Tonicella in sign, is, and Hop_alia laevior. At Botanical Beach, temperatures were a few °C warmer than at First Narrows when T. lineata, 3. droeDachien- sis, and H. hindsii spawned, and the temperature at the time of spawning of T. lineata and K. tunicata varied several °C in different years. These observations suggest that spawning did not occur in response to a physiological threshold temperature, or to a sudden change in temperature. In 1973, S. droebachiensis and T. lineata were collected at First Narrows in late March, prior to spawning, and maintained under various temperature and light conditions: at 5.5 and 14 °C in darkness, and at 5.5 and 14 °C in light conditions similar to those in the field. These animals did not spawn whan spawning occurred in the field. Similarly, S. drcjsbachiensis, T. lineata, and T. insig[nis collected prior to spawning in 1974 and maintained in the laboratory did not spawn. However, animals returned to the field from the laboratory did spawn. This suggested that some condition in the field, which was not present in the laboratory, stimulated spawning, and tnis factor did not appear to be light or temperature. An abrupt spawning at First Narrows and Porteau in 1973 occurred at the time of the spring phytoplankton outburst, but in 1974 spawning at First Narrows was less abrupt corresponding to the slow development of the phytoplankton bloom in that year. In the laboratory, a large proportion of S. droebachiensis, !• and T. insianis spawned when they were exposed to natural phytoplankton collected during the bloom with a 50 u mesh net. This suggested that some substance bound to or released by phytoplankton stimulated spawning. For species with planktotrophic larvae the synchronization of spawaing with the phytoplankton bloom increases the probability of bota favourable food and temperature conditions for development or eggs, larvae, and juveniles. Gonadal growth during the coldest part of the year and spawning at the time of the spring phytoplankton uloom was found in S. droebachiensis, T. lineata, T. insignis, M. ciiiata, and probanly K. tunicat a. This pattern is characteristic* of marine invertebrates with pelagic larvae living in cold waters. iv TABLE OF CONTENTS INTRODUCTION ... .............. 1 STUDY -&JKJEAS •*•«•••• • ^ •••*:••••••••••#••''•»••* y * • 6 RESULTS Relation of Gonad Size to Animal Size ................. 17 Reproductive cycles Katharina tunicata ........,...... ................ 27 Mojgalia hindsii 32 Mopalia ciliata .................................. , 35 Mogalia lianosa 38 MO£aiia laevior .................................. 40 Mopalia muscosa 43 Tonicella lineata 46 22si£sii§ issiasis 51 Strong;y.iocentrotus droebachiensis ................ 54 Observations and Experiments on Spawning Temperature and Spawning in the Field ............. 59 Effect of Light and Temperature on spawning in the Laboratory 67 Phytoplankton Observations in the Field 74 Experiments on the Effect of Phytoplankton on Spci%rni.ii•••*••••••••••••••«•**•*«••••••••'•*•• 3.2 V DISCUSSION The JBegulation of Reproductive Cycles , .. 86 possible factors Regulating Gonadal Growth ............ 87 Temperature ...................................... 89 Photoperiod ....................................... , 92 Nutrition ........................................ 95 Possible Factors Regulating Spawning ..................101 Temperature .........,,.,....,*.*. ,•...... 102 light 110 Chemical Factors ................................. 110 Phytoplankton 112 Internal Considerations ............................... 118 Evolutionary and Geographic Considerations ............. 121 fiEFERENCES ................................................. 127 vi TABLES Table I, Live weight (g) of animals at sexual maturity, and weight range collected for the study of the reproductive cycle, for each of the species in the present study. ......,y, ............................ 26 Table II. Density (millions of cells/m3) of common species of phytoplankton at Stations 1, 2 and 6 before and during the bloom in 1973. (Dr John Stockner, pers. comm.) 77 Table' III., Density (millions of celis/m3) of Thalassi- sp. and Skeletonema costatum at Stations 1 and 2 from 6th March to 3rd May 1974 (Dr John Stockner, Table IV. Density (millions ox cells/m3) of diatoms at Stations A and B in the Strait of Georgia, and for Station C in Juan de Fuca Strait, during winter and spring 1973 (Mr Jae Shim, pers. , comm.),....,.....,...,. 79 Table V,, Density (millions of cells/m3) of diatom species at Stations A, B, and C
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