Shell Growth and Ecology of Recent Brachiopods from Scotland and New Zealand

SHELL GROWTH AND ECOLOGY OF RECENT BRACHIOPODS FROM SCOTLAND AND NEW ZEALAND

GORDON BARRETT CURRY, B.A.(Mod.); (T.C.D.).

September 1979

A thesis submitted for the degree of Doctor of Philosophy of the University of London and for the Diploma of Membership of the Imperial College.

Department of Geology, Royal School of Mines, Imperial College, London, SW7. 1

SHELL GROWTH AND ECOLOGY OF RECENT BRACHIOPODS FROM SCOTLAND AND NEW ZEALAND

by Gordon B. Curry.

ABSTRACT

The ecology, growth rate, and population structure of the Recent articulate brachiopod Terebratulina retusa (Linnaeus) are described. The specimens studied are predominantly attached to the mussel Modiolus modiolus, (Linnaeus), which occur in dense beds around the margins of a deep (220 metres) depression off the west coast of Scotland. Length-frequency histograms prepared from large representative samples collected at regular intervals during 1977 - 1979 are unimodal and right-skewed. Prominent modes within the overall unimodal length-frequency histograms correspond to biannual settlement cohorts. Spawning occurs regularly in late spring and late autumn, and is initiated at temperatures of 10°C - 11°C; the available evidence indicates that the entire reproductive cycle, from spawning to settlement, occurs within 3 weeks. Newly-settled specimens grow rapidly to a length of 2.75mm within 3 months; the animals grow (initially by 4mm per year) throughout life at a progressively reduced rate. Growth slows or ceases during winter in all but recently settled specimens. The maximum life-span is 7 years. Mortality rate remains constant from the first year of life onwards; the causes of death are not apparent. Growth-lines form biannually, at times of pronounced environmental disturbance. In Part II the results of growth-line analyses of numerous Recent and fossil brachiopod populations are described. In temperate-latitude, shallow-water habitats growth-lines form biannually or annually - alternate large and small increments representing 'summer' and 'winter' growth are diagnostic of the former strategy; the latter is a special case of the former due to the cessation of growth in winter because of unfavourable conditions. Regularly- spaced growth-lines in brachiopod populations from polar and abyssal habitats are thought to form annually; the reduced growth-rate in such habitats is attributed primarily to the lower temperatures and reduced food availability. Preliminary growth-line analyses of fossil brachiopod populations are encouraging; the great potential of growth- line analysis as a source of precise palaeoecological data is discussed. 2

ACKNOWLEDGEMENTS

I am greatly indebted to my joint supervisors, Dr. C.H.C.Brunton, Dept. of Palaeontology, British Museum (Natural History), London, and Dr.P.Wallace, Dept. of Geology, Imperial College, London, for their advice, guid- ance, and encouragement; their willingness to discuss the subject at all times was greatly appreciated. Dr. H.W.Ball kindly granted me space and use of facilities within the Dept. of Palaeontology; many other members of this Dep- artment also contributed greatly by discussing various problems and giving freely of their academic and technical expertise, in particular Dr. R. Cocks, Mr. E. Owen, Mr. A. Rissone, Dr. M. Howarth, and Mrs.P.P. Hamilton-Waters. Miss L. Cody kindly helped with the typing, and arranged for German translations by Mrs. 0. Ferguson. I also gratefully acknowledge the help of Mr. D.Claugher and the technical staff of the Electron Microscopy Unit, B.M.(N.H.), for instruction in the techniques of specimen preparation and the use of the Scanning Electron Microscopes. Dr. A. Fincham, Dept. of Zoology, B.M.(N.H.), kindly agreed to the installation of an aquarium system within a constant temperature room under his charge. Mr. J. Hoar of the Photographic Studios, B.M.(N.H.), expertly re-photographed the plates. I am very grateful to many members of staff of the Dunstaffnage Marine Research Laboratory, Oban, Scotland, for their willing co-operation, and for the collection of regular samples during my absence in New Zealand and USA; in 3

particular I would like to thank the Director, Mr R.Currie, for granting me space and use of facilities, Dr.A.Ansell, Mr. C.Comely, Mrs. L.Robb, Miss F.Newman, Mr.. S.Knight, and the Captains and crews of the R/V 'Calanus' and 'Seol Mara'. My visit to New Zealand and USA would not have been possible without the co-operation and encouragement of Dr. G.A.Cooper, Dept. of Paleobiology, N.M.N.H., Washington, DC, and Dr. D.I.Mackinnon, Dept. of Geology, Univ. of Canterbury, Christchurch; their consideration and academic expertise greatly alleviated the many problems associated with such a venture. Professor R.Crawford, Christchurch, and Dr, P. Kerr, Washington, kindly granted me space and the use of facilities during my visits. I also wish to acknowledge the help of Dr.P.Andrews, N.Z. Geological Survey; Professor J.Jellitt, and the Captain and Crew of R/V 'Munida', Portobello Marine Research Laboratory, Dunedin; Dr J.Richardson, N.Z. Oceanographic Institute, Wellington; and Dr.P.Redfern, N.Z. Dept. of Agriculture and Fisheries, Wellington. Dr. A. Williams, Principal's Lodgings, Univ. of Glasgow, suggested the topic of this thesis, and his continuing interest, support, and encouragement is a great stimulus, and is gratefully acknowledged. Finally, I wish to express my appreciation to the Dept. of Education, (Northern Ireland), for a Postgraduate Studentship, and to the British Council for a Commonwealth University Interchange Scholarship which provided the travel funds for the trips to New Zealand and USA.

CONTENTS PAGE ABSTRACT . . . . 1 ACKNOWLEDGEMENTS . . 2 LIST OF CONTENTS ...... 4 LIST OF TABLES ...... 7 LIST OF TEXT-FIGURES . . 8 FRONTISPIECE . . 10 PART I ASPECTS OF THE ECOLOGY AND BIOLOGY OF TEREBRATULINA RETUSA (LINNAEUS) CHAPTER I.1. Introduction . . . . 11 I.2. Materials . . . 16 Section I.2.1. Collection . . . 16 1.2.2. Aquaria . . . 19 CHAPTER I.3. Ecology of T.retusa . . . . 26 Section I.3.1. Distribution . . 26 1.3.2. Depth . . . . 30 1.3.3. Temperature . . 33 1.3.4. Substrate . . . 42 1.3.5. Current . . . . 47 I.3.6. Salinity . . . . 49 I.3.7. Associated fauna . . • 51 CHAPTER 1.4. Population structure and dynamics of T.retusa . . . 53 Section I.4.1. Introduction . . . 53 I.4.2. Size-frequency diagrams . . . 54 I.4.3. Growth rate . . . . . 71 I.4.4. Mortality . . 88

Section I.4.5. Life-history . . . . 92 I.4.6. Comparison with theoretical model. 96 I.4.7. Comparison with other studies . 99 CHAPTER I.5. Biology of T.retusa . . . . 113 Section I.5.1. Lophophore and feeding . . . 113 I.5.2. Reproduction . . . . . 124 Subsection 1.5.2.1. Introduction . . . 124 1.5.2.2. Gonad development . 125 1.5.2.3. Spawning season . . 132 1.5.2.4. Fertilisation 138 1.5.2.5. Larval development • 140 I.5.2.6. Settlement . . . 143 PART II GROWTH OF RECENT AND FOSSIL BRACHIOPODS CHAPTER II.1. Introduction . . . . . 149 I1.2. Materials . . . . . 151 II.3. Methods . . . 152 Section 11.3.1. Electron microscopy . . 152 11.3.2. Growth-line measurement techniques 154 CHAPTER II.4. Microscopic growth-lines . . 171 CHAPTER I1.5. Analysis of Macroscopic growth-lines 181 Section II.5.1. Recent temperate latitude brachiopods - N.Hemisphere . . 181 Subsection II.5.1.1. Terebratulina septentrionalis (Couthouy). 181 II.5.1.2. Laqueus californicus (Koch) . . . 185 Section 1I.5.2. Recent temperate latitude brachiopods - $.Hemisphere . . 190 Subsection 1I.5.2.1. Terebratella inconspicua (Sowerby) . 190 ▪•

Subsection I2.5.2.2. Notosaria nigricans (Sowerby) . . . . 199 I2.5.2.3. Neothvris lenticularis (Deshayes) . . . . 204 II.5.2.4. Liothvrella neozelanica, Thomson . . . . 207 11.5.2.5. Magellania venosa (Solander) . . . . 211 I2.5.2.6. Gvrothvris mawson& antipodesensis, Foster . 214 Section II.5.3. Recent polar brachiopods . 217 Subsection IL5.3.1. Liothvrella uva notorcadensis (Jackson) 217 1I.5.3.2. Magellania fragilis, Smith . . . . . 223 Section II.5.4. Recent abyssal brachiopods . 226 Subsection II.5.4.1. Macandrevia baveri, Cooper . . . . 226 Section II.5.5. Fossil brachiopods . . . 230 Subsection II.5.5.1. Magadina sp. . . 230 1I.5.5.2. Bouchardia antarctica, Buckman . . . . 233 I1.5.5.3. Pachvmagas sp. . . 237 CHAPTER II.6. Discussion . . . . . 239

PART III. Appendices 243 Appendix I. The N.Atlantic species of Terebratulina 243 II.Free-lying brachiopods - the evolutionary implications 246 III.Comments on the function of Caeca 250 IV.BRITISH BRACHIOPODS (with C.H.C. Brunton) . . 252 PART IV. REFERENCES . • . • . 253

PART V. PLATES 1 - 17 • . . 264 7

TABLES PAGE I - SAMPLE STATIONS . • 27 II - SUBSTRATE OF ATTACHMENT . 41 III - ANALYSIS OF MARCH 1977 LENGTH-FREQUENCY HISTOGRAM 68 IV - AGE-GROUPS IN MARCH 1977 SAMPLE . . 70 V - ANNUAL GROWTH RATE OF T.RETUSA . 73 VI - MODE PROGRESSION - 4th and 5th YEAR-GROUPS. 75 VII - MODE PROGRESSION - JUVENILES 75 VIII - GROWTH-LINE ANALYSIS - T.RETUSA . . 76 IX - GROWTH RATE ANALYSIS OF R.ROSTRATA 110 X - GROWTH RATE ANALYSIS OF T.SEPTENTRIONALIS . . 181 XI - GROWTH RATE ANALYSIS OF T.INCONSPICUA . 191 XII - GROWTH RATE ANALYSIS OF T.INCONSPICUA . 194 XIII - GROWTH RATE ANALYSIS OF G. MAWSONI

ANTIPODESENSIS . • . • • 214 XIV - GROWTH RATE ANALYSIS OF MAGADINA SP . • 230

FIGURES

PAGE 1 - Internal and external shell features of T.retusa 15 2 - Distribution Map . . . . 28 3 - Brachiopod aquaria ...... 32 4 - Temperature graphs - Firth of Lorne and aquaria . 35 5 - (A) % of mussels with attached brachiopods; (B) correlation of modes in length-frequency and width-frequency histograms- March 1977 . . 45 6 - Population structure - March 1977 -T-. . 60 7 - Length-frequency histograms - May, July, August, 1977 . . . . 64 8 - Length-frequency histogram - January 1979,(A); Age pyramid (B.); Growth curve (C); Survivorship curve (D)...... 67 9 - Sexual dimorphism in growth rate . . . 80 10 - Stylised growth rate, survivorship, and size-frequency curves . . . . 104 11 - Development of brachial loop in T.retusa . 115 12 - Mode appearance v number of measurements; Laqueus californicus (Koch) 161 13 - Umbonal erosion in Liothyrella uva notorcadensis (Jackson) . 164 14 - Stylised representation of the effect of umbonal erosion on growth-line measurements . . 167 15 - Growth-line frequency diagram - Terebratulina septentrionalis (Couthouy) . . . . 183 16 - Growth-line frequency diagram - Laqueus californicus (Koch). . . . . 187 17 - Growth-line spacing in Laqueus californicus (Koch) ...... 189 18 - Length-frequency diagram - Terebratella inconspicua (Sowerby) - rockpool . . . . 193 19 - Growth-line frequency diagram - Terebratella inconspicua (Sowerby) - Paterson Inlet . . . 195 •

20 - Growth-line frequency diagram-Terebratella inconspicua (Sowerby) - rockpool and beach . • 198 21 - Length-frequency histogram - Notosaria nigricans (Sowerby) - rockpool ▪ 201 22 - Growth-line frequency diagram - Notosaria nigricans (Sowerby) - rockpool and beach .203 23 - Growth-line frequency diagram - Neothyris lenticularis (Deshayes) . • 206 24 - Growth-line frequency diagram - Liothyrella neozelanica, Thomson .209 25 - Growth-line frequency diagrams -(A) Pachymagas sp. (B) Magellania venosa (Solander) . 213 26 - Growth-line frequency diagram - Gvrothyris mawsoni antpodesensis, Foster . . .216 27 - Growth-line frequency diagram - Liothyrella uva notorcadensis (Jackson) . .219 28 - Growth-line frequency diagram - Liothyrella uva notorcadensis (Jackson) - compensated . .222 29 - Growth-line frequency diagram - Magellania fragilis, Smith . • .224 30 - Growth-line frequency diagram - Macandrevia bayeri, Cooper. . . . • • 228 31 - Growth-line frequency diagram - Magadina sp . • 232 32 - (A) growth-line spacing in two populations of $ouchardia antarctica, Buckman; (B) growth curves of the two populations. 235 33 - Length-height and length-width scatter diagrams of Terebratulina retusa (Linnaeus) and Terebratulina septentrionalis, (Couthouy) . 245 FRONTISPIECE

Terebratulina retusa (Linnaeus) from the Firth of Lorne, attached to Modiolus modiolus (Linnaeus). PART I,

ASPECTS OF THE ECOLOGY AND BIOLOGY OF

TEREBRATULINA RETUSA (LINNAEUS) 11

I.1. INTRODUCTION

Brachiopods are far from being as rare a component of Recent marine faunas as is commonly believed. Representat- ives of the phylum are found in all oceans, from intertidal to abyssal depths, and in some areas they dominate the epifauna much as they did during their heyday in the Palaeozoic. There are approximately 300 extant species, 21 of which have been recorded from around the British Isles (Brunton and Curry, in press). Living brachiopods are primarily of interest to palaeontologists seeking a framework for the reconstruction of the life-habits and habitats of fossil brachiopods. For obvious reasons, previous studies of Rec- ent brachiopods have dealt predominantly with those readily- accessible populations from intertidal or shallow-subtidal habitats. Unfortunately, organisms from such habitats are rarely preserved in the fossil record, and consequently the results of previous studies have not always been readily applicable to the study of fossil populations, especially as environmental conditions vary considerably between intertidal and deeper subtidal habitats. The aim of this project was to carry out the first long term ecological and growth-rate study of an abundant brachiopod population from depths similar to those at which the majority of fossil brachiopods are presumed to have lived. The fortuitous circumstances in the Firth of Lorne proved ideal for such a study, and preliminary comparisons with fossil populations have illustrated the great potential of the analytical methods used in this study as a source of 12 precise palaeoecological and palaeoenvironmental data. The species under investigation was Terebratulina, retusa (Linnaeus). The genus Terebratulina (d'Orbigny, 1847) first evolved in the Upper Jurassic of Europe and India, colonising the margins of the Tethys Ocean. During the Jurassic, Terebratulina migrated through the recently- opened Straits of Gibraltar to the margins of the Atlantic Ocean, and representatives have been found in the Cretaceous of England and North America. Subsequently the genus under- went tremendous radiation, and had a cosmopolitan distribution throughout the Tertiary. Terebratulina survives as one of the most common and geographically widespread of Recent brachiopod genera, although it is no longer found around New Zealand despite being a common constituent of Tertiary faunas in that region. Terebratulina retusa (Linnaeus) has been known to be abundant in some regions of the north-eastern North Atlantic for over 100 years, but the ecology of the species has never been studied. It was first described, as Anomia retusa, by Carl Linnaeus in 1758; due to some confusion in the original diagnosis, however, specimens were commonly identified as Terebratulina caputserpentis. This confusion was finally resolved by Brunton and Cocks who, having examined the Linnaean collections, selected lectotypes of both A. retusa and A. caputserpentis, and proposed that the type-species of Terebratulina should be re-designated as Anomia retusa, Linnaeus, 1758 (Brunton, Cocks and Dance, 1967). This proposal was upheld by the International Commission on Zoological Nomenclature. Detailed diagnoses of 13

Terebratulina retusa (Linnaeus) have been given by several authors (Brunton, Cocks,and Dance (1967); Davidson (1886); Thomson (1927)) , and criteria for the field identification of this species are described in Brunton and Curry (in press) . From its first appearance in the Upper Jurassic, Terebratulina has been a morphologically-conservative genus, and certainly the two living species found in the N.Atlantic are very similar and have often been confused (Appendix I). A complete revision of the taxonomy of fossil and Recent representatives of this genus is urgently required, as its conservatism has undoubtedly resulted in the sub-division of valid species because of their widespread distribution and longevity. 14

EXPLANATION OF TEXT-FIG. 1.

Internal and external shell features of Terebratulina retusa (Linnaeus); Recent; Firth of Lorne; Scotland.

A,B. Internal features of the ventral and dorsal valve (respectively) of an adult specimen showing a complete brachial loop.

C,D. Dorsal and lateral views (respectively) of the external shell features of an adult specimen, showing orientation of the principal shell parameters. (L = length; W = width; H = height). 15

Pedicle aperture

Deltidiai plates

Outer socket ridge

Brachidium (=Brachial loop)

5MM 1 1

Posterior Ventral Valve Pedicle Dorsal Valve BrachialC )

5MM

Anterior C ' -- - w— - D 16

I.2. MATERIALS

I.2.1. COLLECTION. Dredging is the only practical method of sampling the brachiopod populations which occur off the west coast of Scotland. There are a few shallow-water localities where appreciable numbers of specimens can be collected by divers (i.e. Stn.2 in Table I and Fig.2), but such populations are unlikely to survive frequent sampling; the abundant populations occur at depths of 100 to 180 metres, and are beyond the range of SCUBA divers. Large numbers of T.retusa were known to occur in the Sound of Mull (Fig.2), and it was originally intended to collect regular samples from this area. However during an exploratory cruise in March 1977 a large brachiopod population, ideally situated for regular sampling, was discovered around the margins of a fault-deepened depression in the Firth of Lorne, close to the south-west coast of the Island of Mull (Stn.l in Table I and Fig.2 - grid ref. 745 265, O.S. Sheet 49, 1:50,000 First Series). The brachiopods are predominantly attached to the horse-mussel Modiolus modiolus (Linnaeus) which occurs in dense beds around the margins of this depression (see frontispiece). The samples were collected using a conventional 'clam-dredge', (1.2 metres wide by 2 metres long), the body of which consists of an outer framework of interlocking iron chain, and an inner nylon meshwork with a maximum aperture of 15mm (Plate 2,B,C). This dredge proved particularily efficient at sampling the mussel-beds, as clumps of mussels 17

were easily detached from their substrate, and all but the most juvenile specimens are retained by the inner nylon meshwork. This locality is particularily suitable for dredging operations as the margins of the depression are relatively smooth, with few obstructions which would damage or entangle the dredge. Fortunately such deep depressions are not common in this region and, using the vessel's depth sounding equipment, it was possible to collect all samples from the same population. Because of the density and abundance of brachiopods and mussels, and the efficency of the clam-dredge, all attempts to sample the Firth of Lorne population were successful. For each sample the dredge was trawled along the bottom for between 5 and 10 minutes, with the vessel moving slowly in either a north-easterly or south-westerly direction; trawling either with or directly against the prevailing current reduces the risk of the cables fouling the vessel's propellers. On average winching of the dredge back to the surface was accomplished within 5 minutes. Once landed on deck (Plate 2,D,E), the sample was washed with fresh sea- water to remove adherent sediment (Plate 3,A-F), and then placed in a plastic bath through which fresh sea-water was continually being pumped. On many occasions the brachiopods and mussels had become acclimatised and were feeding within 30 minutes of arriving on deck. Obviously the dredging process does involve considerable physiological disturbance, but very few of the specimens suffered any mechanical damage. The mussels occur in dense clumps, firmly attached to one another by 18

byssus threads, and the fact that these clumps were collected intact confirms that the dredging operation does not cause significant mechanical disruption. In one sample, of 811 specimens, it was calculated that only 7 specimens had been destroyed during the collection process; even if the shell and body of a specimen is removed, the pedicle and its strong adjustor muscles remain in position. (The peduncular attachment of T.retusa is strong, and the pedicle cuticle is slightly flexible and extremely resilient; attempts to remove a specimen from its substrate by force will result in the pedicle and attached adjustor muscles being ripped from the shell and remaining attached to the substrate). All samples were kept immersed in constantly-flowing fresh sea-water., During the preparation of the samples the surfaces of all potential brachiopod substrates were examined using a high-powered binocular microscope to ensure that as many as possible of the smaller specimens were picked out. Once each specimen was detected it was removed from its substrate by severing its pedicle with a sharp scalpel; specimens were then measured, using either_. dial calipers or a vernier microscope scale, and preserved in either 70% alcohol or 10% formalin. All samples collected during this study are housed in the Dept. of Palaeontology, British Museum (Natural History), London; the registration numbers quoted in the text ( with the prefix ZB-) refer to the Recent brachiopod collections in that Museum. 19

I.2.2. AQUARIA

An aquarium system was set up at the Dunstaffnage Lab- oratory to ensure that living specimens were always available for study when required. This consists of a circular black plastic bath (approx. 80cros. in diameter by lm deep) which has an outlet close to the upper rim (Fig.3,A). Fresh sea-water, at a rate of 450 litres per hour, is pumped in through plastic tubing, the nozzle of which is firmly attached to the base of the bath diagonally opposite the outlet. Initially, introduced specimens were simply placed on the bottom of this bath, but this proved unsatisfactory as the water circulation in such a position was inadequate; in addition large quantities of particulate matter settled on, and threatened to smother,the specimens. Consequently the brachiopods were placed in cages constructed from large- mesh rigid nylon netting, which were suspended well above the base of the bath, and in a position to receive maximum current (Fig.3,A). Air is pumped in through an air-stone positioned close to the inlet nozzle - the upward movement of air-bubbles enhances the circulation within the tank, and helps carry potential food particles up to the surface (Fig. 3,A). The bath is covered with a thick black P.V.C. sheet, thereby ensuring total darkness and inhibiting algal growth. This open-ended system is virtually maintenance-free and there is no need to add food or vitamins as both are adequately provided by the Laboratory's sea-water supply, which is pumped directly from the sea with only the larger grades of particulate matter filtered out . Occasionally 20 the sea-water input flow causes problems, as the pressure varies slightly depending on the demand and the state of the tide; the Laboratory's sea-water is- pumped in from below low-tide level on the seaward side of Dunstaffnage Penin- sula and, having passed once through the aquaria, is pumped out into Dunstaffnage Bay on the landward side of the peninsula. This fluctuation in sea-water pressure may have caused some disturbance to the brachiopods in the tank, and certainly on one occasion, when the flow had decreased to a mere trickle, all brachiopods had ceased feeding and closed their shells. However the flow rate is regularily monitored by members of staff, and such stagnant conditions are infrequent and rarely persist for more than 24 hours. This aquarium was used as a holding-tank for the regular samples colleeted from the Firth of Lorne, and also for long-term ecological and growth-rate studies. The aquarium is situated in an outside embayment of the Laboratory, protected from the environment only by a roof, and is therefore susceptible to air-temperature fluctuations. It is this feature which is thought to be the main cause of the failure of the growth-rate study, as all the metabolic activities of marine organisms are known to be greatly affected by temperature fluctuations in the surrounding sea-water (Section I.3.3). A daily temperature range equivalent to the normal annual range was measured in this aquarium on a sunny winter day.(Fig.4,B). Organisms can adapt to gradual temperature changes but rapid short-term fluctuations are a source of stress, the most noticeable manifestation of which, in brachiopods, being the slowing or cessation of the processes 21

of feeding and shell-growth. Specimens held in this tank for more than a year failed to grow, although they still survive and appear to be in good health; undoubtedly,had it been possible to supress these temperature fluctuations, conditions within this aquarium would have been more conducive for brachiopod growth. The majority of the time spent at the Dunstaffnage Laboratory during this study (14 weeks in total) was occup- ied by the collection and preparation of the samples from the Firth of Lorne, with the result that the full potential of the aquarium as a source of ecological information was not exploited. For this reason it was decided to set up a separate aquarium in one of the Constant Temperature rooms in the Zoology Dept., British Museum (Natural History), London. In such a location a closed-system aquarium (i.e. with recirculation of the sea-water) was the only feasible alternative and, as fresh sea-water is difficult to obtain .. in London, 'artificial' sea-water was used. This was prepared by diluting the required quantity of 'INSTANT OCEAN' synthetic sea-salts with tap water. The manufacturers of these salts do not attempt to include all chemical compounds found in natural sea-water, but only those which are thought to be essential for the maintenance of life (i.e. Cl, Na, Mg, Ca, etc.); important trace elements (such as Zn, Cu, Fe, etc) are introduced by adding a specified quantity of a 'Trace- Element Solution' provided with the synthetic sea-salts. Natural sea-water is impossible to duplicate in the laboratory as virtually all naturally occurring elements are present in concentrations which vary depending on the location, 22 season, etc. Synthetic sea-salts have been used with great success in the study of many marine organisms, and are to be preferred in a closed-system aquarium as natural sea-water, once enclosed in such a system, is liable to undergo undesirable chemical changes which are difficult to control due to the great complexity and variety of the chemical constituents present. In this study a small rectangular glass tank (91cros x 45cros x 25cms) was filled with synthetic sea-water, which was agitated vigorously to ensure that all of the sea-salts were completely dissolved. At this stage the specific gravity was measured using a hydrometer, and either additional sea-salts or tap water added if the value was outside the accepted range (the aquarium was maintained at a temperature of 12°C, and the specific gravity of sea-water at such a temperature should be between 1.025 and 1.026). A chelating agent is present in the sea-salts to remove potentially- harmful compounds present in tap water. Circulation within this aquarium was maintained by means of an air-lift system as described by King and Spotte (1974). This consists of a vertical plastic tube connected to a sub-gravel filter; air is pumped down to an air-stone situated at the bottom of the air-lift tube, and as air-bubbles rise to the surface through this tube they draw water down through the gravel substrate into perforations in the sub-gravel filter, and thereby promote circulation (Fig.3,B). Specimens were transported from the Dunstaffnage Laboratory in vacuum-flasks, as described in Appendix IV. A closed-system marine aquarium has one major 23 disadvantage, namely that all the waste products of feeding and decay are retained within the system, and the sea-water quality progressively decays as these products accumulate. Ammonia, the principal waste material of most aquatic animals, is extremely toxic to all aquatic life-forms in concentrations as low as 0.006 parts per million. To prevent the build-up of toxic ammonia several species of bacteria must be introduced into the aquaria. These bacteria derive their energy from the oxidation of ammonia (NH4) to the less toxic nitrite (NO2); this in turn is utilised by other species of bacteria which oxidise nitrite to relatively harmless nitrate (NO3). Nitrifying bacteria are ubiquitous in nature and, having been introduced to the aquarium attached to the surfaces of living animals, will multiply rapidly in the presence of ammonia ,. and will colonise the walls of the aquarium and the surfaces of the substrate. This complex biological filter of nitrifying bacteria must be well established before the bulk of the animals are introduced, to prevent the sudden build-up of toxic ammonia. The recommended procedure is to introduce one or two hardy animals which are then fed, (in this case the mussel Mytilus edulis Gray), thereby initiating the nitrogen oxidation cycle. The duration of this 'run-in' period depends on the sea-water temperature; in this case, at a temperature of 12°C, a five-week 'run- in' period was desirable (King and Spotte, 1970. The grain-size of the substrate is an important criterion, as it has been determined that the most efficient and evenly- distributed biological filters develop on grains which are 2 - 5 mm in diameter. In this study non-toxic synthetic 24

grains of this size were used; suitably-sized substrate gravels are available from aquaria supply stores. In the open sea the nitrate ion concentration is low due to the activity of denitrifying bacteria and direct assimilation by certain planktonic organisms. In a closed- system aquarium, however, the net effect of the nitrogen oxidation cycle described above is a gradual increase in the nitrate ion concentration. High nitrate ion concentrations, whilst not toxic, are nevertheless undesirable, and are one of the primary causes of the gradual decrease of pH value which is a feature of all closed-system marine aquaria (the others main causes being respiratory activity and the oxidation process). Normal sea-water has a pH of between 8.2 and 8.4, and many marine organisms are known to be adversely affected by values of less than 8.0. In this study crushed oyster-shell was added to the aquarium as this material, unlike pure calcium carbonate, is soluble in sea-water (containing at least 4% magnesium, oyster-shell, dolomite rock, and coral rock, are all soluble in sea-water, and are therefore suitable additives). The progressive dissolution of the oyster-shell helps maintain an optimum pH value. In addition, regular partial water changes helped to maintain a pH value of at least 8.0 in this aquarium (the pH was measured at regular intervals using a pH meter). Regular replenishment of the sea-water reduces the concentration of nitrate ions and other undesirable compounds; at least 50% of the sea-water was replaced each month. The brachiopods in this aquarium were fed on dissolved nutrients prepared from minced beef-heart blended with sea- 25

water (see McCammon, 1972). Initially algal cultures mere considered as a potential food-stuff, but there is no indication as to which species of algae, if indeed any, T.retusa will feed on. It was considered preferable to use dissolved nutrients, which had already proved an acceptable food for other species of living brachiopods held in closed-system aquaria (McCammon,1972). Minced beef-heart is used as a food-stuff for many marine organisms, and can be obtained frozen from aquaria-supply stores, or fresh from a butcher. Frozen beef-heart is provided in thin slices which were particularily convenient for this study as only small quantities of food were required; small pieces can be broken off as needed, defrosted, and then blended with sea-water, whilst the remainder can be stored in the ice-making compartment of a fridge. The brachiopods were fed twice per week, and multi-vitamins were added to the aquarium once per week, as recommended by McCammon (1972). Specimens held in this aquarium survived for several months, although once again growth was inhibited due to the abnormal conditions. Some of the specimens died because of fungal infection, which is a common feature in closed-system aquaria. This fungal infection, which caused portions of the periostracum of infected specimens to turn black, was successfully treated with 'LIQUITOX' fungicide. This aquarium provided a very valuable opportunity to observe living brachiopods in life-positions, and much useful information on the environmental requirements for brachiopod survival. 26

I.3. ECOLOGY OF T.RETUSA

1.3.1. DISTRIBUTION

T.retusa is the most abundant of the 21 species of Recent brachiopods found around the British Isles (Brunton and Curry, in press). It is also common off the coast of Norway (Da11,1920), and has been recorded as far west as the east coast of Greenland (Wesenberg-Lund,l940), and as far south as the Mediterranean (Davidson,1886-1888; Dall, 1920). The precise geographic limits of the distribution of this species are unknown, as there are at least two morphologically similar species of Terebratulina in the N.Atlantic which have often been confused, with the result that some previous records may be based on misidentified specimens. Whilst there are distinct morphological differences between the Scottish T.retusa and specimens of Terebratulina septentrionalis (Couthouy) from the Bay of Fundy, Canada (see Appendix I), it is possible that they are members of a Terebratulina cline within the North Atlantic; a detailed study of representatives of this genus from the mid North Atlantic may reveal morphological features intermediatory between these two species. The available information on the distribution of T.retusa in the study area off the west coast of Scotland has been summarised in Table I and Fig.2. This data represents the results of numerous dredging operations carried out by the R/V 'CALANUS' during 1977 - 1979. Dredging, whilst being the only practical method of collecting samples of 27 TABLE I Results of the dredging operations of the R/V 'Calanus', west coast of Scotland, 1977 - 1979. (a = abundant, c = common, r = rare, X = absent).

STATION Nod LOCATION. DEPTH. SEDIMENT. T.rrtu"t C.anomala ASSOCIATED FAUNA. abund.:attachment. abund.,attachment.

1 Firth of Lorne 146-183m. fine mud a uvoAin)1,1 a j Modm7ug see text. 2 Rabbit Island 13m. -- c ,rocks r ! rocks Pe^ten 3 Garbh Reisa 20m. -- X ! -- X I -- PACISII I 4 Sound of Jura 73-128m. -- X . -- X -- MAlin)ug and (north-east) 1 I hydrozoans 5 Sound of Jura 110m. -- r 1vesicular X I -- large no. of di.- basalt , articulated Modiolus 6 Sound of Jura 37m. -- X I -- X a -- pecten. gnus. (south) I 1 7 E. of Colonsay 37m. sand X I -- X ( -- d. crabs. 8 North-east of 55m. -- C ,rocks and c I rocks and -- Colonsay 'clinker I clinker 9 Torran Rocks 91-110m. -- X 1 -- X I -- -- 10 North-west of 73-110m -- r 'rocks X ~ -- -- Iona I 11 North of Iona 73-128m. sand X ; -- X 1 -- -- 12 Treshnish Is. 29-55m. -- X I -- X ' -- Balani, serpulida I I on rocks 13 Lunga 37m. -- I ; -- X I -- Ulan= on rocks 14 North-west of 37.46m. -- X I -- X 1 -- Par-tan, schinoids Mull I I 15 East of Coll 146-183m. -- X 1 -- c I rocks -- 16 Ardmore Point. 73-213m. mud I . -- I 1 -- -- Mull I I 17 Mingary Bay, 37m. mud X I -- c ' rocks -- Ardnamurchan I 18 Tobermory Bay, 73m. mud c / clinker a 1 clinker and /Hodio)ua Mull I I rocks 19 Sound of Mull 110m. mud c ',rocks a I rocks -- (north) I 20 Sound of Mull 91m. mud a IModio)ug c d olus -- (north) 1 I 21 Sound of Mull 91m. mud X : -- c I rocks -- (north) 22 Sound of Mull 91m. mud a IModiolu:! a I Modiolus -- (north) i i 23 Sound of Mull 91-146m. mud r 1 Nodiclua r 1 Modiolus -- (north) I I 24 Sound of Mull 18- 37m. -- c 'shell X I -- -- (north) I fragments 25 Sound of Mull 110-128m. mud a ~Mndialua a I Modiolus -- (south) 26 Sound of Mull 128-146m. mud c /clinker r 1 clinker -- (south) 1 1 27 Sound of Mull 18-37m. mud c / clinker r I clinker -- (south) I 23 Lismore Island 37m. -- r 'vesicular r I vesicular -- I basalt I basalt 29 Lismore Island 15-26m. -- r I rocks X I -- --

EXPLANATION OF TEXT-FIG. 2

Map showing the locations of the R/V 'Calanus' sample stations off the west coast of Scotland, (see Table I above). 28 29

T.retusa in this locality (Section I.2.1.), is a rather unsatisfactory method of determining the geographic range and habitats of sessile marine organisms. Dredges are extremely selective, and will only collect free-lying or loosely- attached material within a rather restricted size range. The limitations of dredging have been well illustrated in the present study as dredging operations in the Sound of Jura (Stns.4 - 6 in Table I and Fig.2) indicated that brachiopods are rare, and yet divers have reported large numbers of T.retusa attached to large boulders and rock-faces in this area (R.Harvey, pers comm. 1979). Despite these limitations, there is no doubt that T.retusa has a patchy distribution off the west coast of Scotland. This is particularily evident from the results of numerous dredged samples collected in the Sound of Mull (Stns. 18 - 29 in Table I and Fig.2). Brachiopods can be extremely abundant in some areas of the Sound of Mull (i.e. Stn.20, 22 in Table I and Fig.2), and either rare or absent in nearby localities (i.e. Stn.21,23)._As far as could be ascertained the environmental conditions were similar at all these localities, and certainly suitable substrate for attachment was available in those localities where brachiopods were either rare or absent. Undoubtedly localised variations in environmental conditions will affect the survival of brachiopods, and patchy distribution is certainly a common feature in Recent and fossil brachiopod populations (Rudwick,1970). This patchiness may be indicative of a relatively short pelagic larval stage, which would result in the larvae settling close to the parents rather than spreading to nearby areas. 30

Direct observations on the populations in the Sound of Mull (using underwater television), combined with detailed measurements of localised variations in important factors such as current velocity, sedimentation rate,etc., may help determine whether this patchy distribution pattern is indeed an inherent characteristic of the T.retusa populations.

I.3.2. DEPTH

Off the west coast of Scotland the most abundant populations of T.retusa are found at depths of between 130m. and 200m. (Table I). The species has however been collected at much shallower depths in this region, notably at a locality close to Rabbit Island (Stn.2 in Table I and Fig.2), where it is commonly attached to boulders. On one occasion specimens of this species have been collected in the Sound of Raasey, at an estimated depth of less than 3 metres (M. Howarth, oral comm., 1978). Despite these records, T.retusa is not a common constituent of the shallow subtidal ecosystem , and there is no record of any brachiopod ever being washed up on a beach in this region. The known depth-range of T.retusa is from 3 - 1478 metres, although it is most commonly found between 100m and 500m. Environmental conditions vary considerably with depth, and it is the tolerance of an organism to such variations which determines its depth range; depth in itself is not considered to be a controlling factor. Presumably T.retusa 31

EXPLANATION OF TEXT-FIG. 3.

A. A diagrammatic view of the outside aquarium at the Dunstaffnage Laboratory used as a holding tank for the regular samples, and for ecological and growth rate studies.

B. A diagrammatic view of the closed-system aquarium set up in the Dept. of Zoology, B.M(N.H.), London, using synthetic sea-water and an airlift system for circulation.

In both A and B arrows demonstate the direction of flow. 32 outflow brachiopocl /';;::!=== .-. cage air

o •• : ••• 0 • •• • • • • ~,. .. . • , , J------~::

o ••·· • f • • • • •

..air input airlift brachiopods

- substrate 33

is prevented from colonising intertidal or shallow subtidal habitats by the combined effect of certain biological and physico-chemical factors characteristic of such habitats, such as competition from other organisms, rapid daily temperature fluctuations, the possibility of dessication, salinity fluctuations , wave turbulence, and perhaps damage by ultraviolet light (which causes the rapid breakdown of vitamins). Factors likely to be of significance in controlling the maximum depth inhabited by T.retusa include reduced food supply, increasing hydrostatic pressure, and the increased solubility of calcium carbonate (which results in the organism having great difficulty in extracting this essential component from the surrounding sea-water).

1.3.3. TEMPERATURE

Samples of bottom-water from the vicinity of the brachiopod population in the Firth of Lorne were brought to the surface in an insulated sampling bottle. The temperature of this water was measured at the surface using a standard mercury thermometer; as the time taken for the bottle to reach the surface was less than 4 minutes, the measured temperatures are within 0.1°C of the actual bottom temperatures. Readings were taken throughout the year to determine the seasonal temperature variations, and the results are plotted in Fig.4,A; for comparative purposes the surface- water temperatures were measured at the same time and are 314,

EXPLANATION OF TEXT-FIG. 4.

A. Annual temperature curves for the surface and bottom (approx. 150 metres depth) waters in the Firth of Lorne, west coast of Scotland.

B. A plot of the temperatures measured in the outside aquarium at the Dunstaffnage Laboratory during 1977 and 1978, showing the overall similarity with A, but with superimposed short-term fluctuations. 35 15

14 • 13 - .• 12

T 11

S. [°C] 1 . . I • 9 I \ I / 8 /

JAN FEB MAR APR MAY JUNE JULY AUG SEPT OCT NOV DEC

• SURFACE ♦ BOTTOM A

15—

14—

..• .. . . • . . • . • . . . . • . . . a . . •S • • . • . . . .• •:• . • . • .a f-. . • . . . . • Of . •• ••••~ • • • :• • • •

6— . . JAN FEB MAR APR MAY JUNE 1 JULY AUG SEPT OCT NOV DEC 1

B 36 also included in Fig.4,A. The bottom-water temperatures vary from a February minimum of 6.5°C to a maximum of 13°C in August (annual range = 6.5°C). The annual range of surface-water is slightly greater (i.e. 8°C) with a ,January minimum of 6°C, and a maximum of 14°C in August. It is apparent that bottom and surface conditions are virtually never isothermal, and can differ by as much as 2.5°C. This vertical stratification of the water column (the thermocline) is a common feature of Scottish sea-lochs, and is primarily due to the fact that surface-waters are much more affected by air temperature than bottom-waters, with the result that surface-waters are warmer in summer and cooler in winter. (Fig.4,A). Other factors which enhance this vertical stratification are salinity and density gradients produced by the high surface run-off of fresh water from the surrounding land. It is apparent, therefore, that throughout most of the year there are at least two distinct water bodies in the Firth of Lorne. Mixing of these vertically-stratified water bodies occurs in February/March, because of the reduced vertical temperature gradient and the pronounced stirring effect of the frequent and severe winter storms. At this time the entire water column becomes saturated with oxygen; the bottom-waters subsequently become progressively less saturated with oxygen, reaching a minimum immediately prior to the breakdown of the summer thermocline during September/October. At this time the Firth of Lorne waters once again become isothermal and uniformly saturated with oxygen. The seasonal temperature variations of bottom- and 37

surface-waters are very similar, and it seems unlikely that a difference of only 1.5°C is a significant factor in limiting the dispersal of T.retusa into shallow-water.habitats. However the fact that surface waters are subjected to rapid daily temperature fluctuations will certainly be a limiting factor. The extent to which such fluctuations cause stress to T.retusa is well illustrated by the results of the growth studies carried out in the outside aquarium at the Dunstaffrage Laboratory. The temperature of the sea-water in this tank was measured at regular intervals (Fig.4,B), and significant daily temperature fluctuations are apparent. It was not surprising, therefore, that specimens in this aquarium did not grow under such stress-inducing conditions. A fluctuating temperature is considered to be the biological • equivalent of a constant temperature higher than the mean of the fluctuating one (Margalef, 1977); therefore the rapid daily temperature fluctuations in this aquarium may have been equivalent to subjecting the specimens to temperatures outside their tolerance range. However it is much more likely that it was the rapidity of the temperature fluctuations which was the main cause of stress, rather than the maximum or minimum temperatures experienced in the aquarium, which were not significantly different to those in the natural environment (Compare figs.4,A and 4,B). In its natural habitats, T.retusa will be subjected to very gradual temperature changes, which will be either uniformly increasing or decreasing; in the aquarium, however, the specimens were occasionally subjected to a daily temperature range equivalent to the normal annual range. 38

Temperature is one of the most important factors controlling the distribution of marine organisms. T.retusa is predominantly a temperate-latitude species, with the northern and southern limits of its distribution being determined by the onset of polar and tropical conditions respectively. The upper and lower lethal temperature limits of marine organisms are determined by the temperature sensitivity of the cellular membranes. These membranes consist primarily of chains of phospholipids which are held in place by weak Van der Waal forces. Temperature variations affect both the chemical constituents of the membranes and their binding forces. Decreasing temperatures, for instance, cause an increase in the viscosity of the membrane, thereby reducing its porosity, and disturbing many of its essential functions (Somero and Hochachka, 1976). However temperature becomes a limiting factor well below the maximum and minimum lethal temperatures for a species are reached. Thus T.retusa may survive for some time if transposed north into a polar habitat, or south into a tropical habitat, but under such atypical conditions gonad development is almost certain to cease . and the population would not survive. There is a non- breeding margin at the limits of the geographic distribution of some marine invertebrates, maintained by the influx of highly mobile larvae from the central areas where gametogenesis does occur. The extent to which such a phenomenon is discernible at the margins of living brachiopod populations will depend on the length of the pelagic larval stage; the available information suggests that it is not a significant feature in T.retusa because of the short duration of 39

its larval stage (Subsection I.5.2.5). However temperature is more than a limiting factor in distribution, as it has a pronounced effect on all aspects of the life-functions of an organism. This is due to the fact that the rate at which any chemical reaction proceeds is governed by ambient temperature conditions; the rate of a reaction increases with increasing temperature, and slows with decreasing temperature. This phemomenon is known as Van't Hoff's rule. All the life-processes of an organism: depend on complex sequential interactions between biochemical compounds called enzymes, which obey Van't Hoff's rule. Therefore, the rate at which these vital enzyme reactions proceed (and hence the rate of growth, feeding , and respir- ation) is determined by the temperatures within the tissues of the organism. T.retusa is cold-blooded and does not regulate its body temperature, with the result that the annual range of body temperature is identical to that of the surrounding sea-water. Van't Hoff's rule is often defined quantitatively as the 410 coefficient:- the 410 of a particular reaction is the factor by which the rate of that reaction is increased by a rise of 10°C. In general, the metabolic reactions of an organism have a 6110 of between 2 and 2.5 (with a Q10 of 2.5 the reaction rate will increase by 2.5 times per 10°C rise in temperature (Prosser, 1973), which is equivalent to 9.6% per degree ). Therefore, in theory, the annual temperature range of 6°C in the Firth of Lorne will result in a difference of 57.6% in the activity rate of T.retusa between maximum and minimum temperature conditions. However such a 40 conclusion is of little practical significance as enzyme reactions are complex and commonly involve several steps and a great number of compounds, each of which is affected to a greater or lesser extent by temperature. In addition the Q10 coefficient of an organism can vary between periods of activity and quiescence - the Q10of the bivalve Cardium, when active, is 1.84; when resting it drops to 1.2 (Prosser, 1973). Virtually nothing is known about the rates of metabolic activity in brachiopods, although it has often been assumed, but never proved, that they have a lower metabolic rate than bivalves. Direct measurements of temperature - related metabolic activity rates in brachiopods are necessary if the precise effects of temperature on their life-functions are to be determined. Such direct measurements are all the more desirable when the phenomenon of physiological adaption is considered. The measured difference in activity rates is considerably smaller in some species than would be expected in response to the temperature change experienced, and it is clear that these species are capable of modifying certain aspects of their enzyme reactions to allow metabolic compensation for the temperature change. Possible mechanisms for such a process are to change the enzyme concentrations, to modify the functions of certain enzymes, or to develop new enzyme variants (Somero and Hotchachka, 1976). Time is a critical factor in this adaptive strategy as organisms can adapt to gradual temperature changes, but their adaptive mechanisms are unable to cope with rapid temperature fluctuations. 41

TABLE II Substrate of attachment of 786 specimens of T.retusa collected 5th May 1977 from the Firth of Lorne.

No.of No.of 5 of SUBSTRATE OCCURRENCES BRACHS TOTAL Living mussel 166 591 75 Dead mussel 27 53 7 Mussel frags. 33 63 9 Hydrozoan 10 13 2 Dead gastropod 5 14 2 Dead brachiopod 4 10 1 Living and dead bivalve 4 8 1 Sponge/ascidian 4 16 2 Unattached 4 8 1 Rock 2 9 1 Tube-worm 1 1 0.1 42

1.3.4. SUBSTRATE

In the Firth of Lorne and Sound of Mull T.retusa is most commonly found attached to the external shell surface of the horse-mussel Modiolus modiolus (Linnaeus). The predominance of this form of attachment (see frontispiece) is to some extent due to the fact that the majority of samples were collected from the Firth of Lorne mussel-beds because of the suitability of such substrate for dredging operations. Divers have reported large numbers of T.retusa attached to rock faces and large boulders at depths of 20-40 miles in the Sound of Jura (R. Harvey, pers.comm.,1979), and this form of attachment is to be expected in other areas where suitable rock surfaces are free of sediment (because of high inclination or high current velocity). Nevertheless it is clear that mussels are a very common substrate for T.retusa, as is well illustrated by the following analysis of the substrate of the 786 brachiopods collected on 5th May 1977, (Table II ) . The sample contained 204 living mussels, 81% of which had attached brachiopods (i.e. 166 mussels). The predominant use of mussels as a substrate is not surprising, as they are the dominant constituent of the epifauna in this area in terms of bulk, and are certainly ideal brachiopod substrate. They present a large and relatively easily- bored surface for attachment, and attached brachiopods are unlikely to be smothered by accumulations of sediment. Mussels are a stable substrate, rarely altering their position or orientation, and having a much longer lifespan than 43

brachiopods (at least 20 years(Comely, 1978), as compared with a maximum of 7 years for T.retusa - Section I.4.3.). Being relatively smooth, there are few obstructions to prevent the rotation of brachiopods around their pedicles, a procedure which enables them to move away from local disturbances and- to take up preferred feeding positions. The majority of brachiopods are attached anteriorly, close to the inhalent and exhalent feeding currents of the mussels, and are likely to benefit from the increased flow of nutrient- carrying water in such regions. Apart from the substrates listed in Table II, T.retusa has also been found attached to pieces of clinker, cobbles, and other assorted pieces of debris (Table I). On rare occasions living specimens unattached to any substrate have been collected. It is possible that these specimens became detached during the dredging operation, but laboratory observations have proved that T.retusa could survive unattached provided the commissural gape was unobstructed. Specimens will continue to feed and excrete faecal pellets whilst free-lying, and will even continue to rotate their pedicles when disturbed, indicating that they are unaware that they are no longer attached. The weight of the body tissues posteriorly results in detached specimens settling with the anterior slightly elevated, an ideal feeding position, whether the animals are lying on their dorsal or ventral valve. McCammon (1972) kept large numbers of living, but unattached, brachiopods in aquaria by placing them posterior- downwards in suitably sized perforations in a plastic sheet. There is good evidence that brachiopods which have been 44

EXPLANATION OF TEXT-FIG. 5.

A. % of the total number of specimens of Modiolus modiolus (Linnaeus) collected on 24th May 1977 from the Firth of Lorne which had brachiopods from each of the 7 year classes attached. The sample yielded 127 mussels and 554 brachiopods; a total of 21 mussels (= 16.5%) had no attached brachiopods.

B. Correlation between the modes in the length-frequency and width-frequency histograms prepared from 811 specimens of T.retusa collected in March 1977 from the Firth of Lorne. The width-frequency histogram was divided into nine groups on the basis of prominent modes (Fig.6,C) and the length of all specimens in each group determined from the original data. The small degree of overlap in the length-frequency distribution of each group (i.e. B) confirms the precise relationship between shell length, width, and age. 45

::I• ] 'a o ~ 'ii.. 25 ..o "-o ~

Vear Clall A

40 8 ," , , ,, ,., ~ , ~ '"I: I C ...r

5 10 20 Length (mm) B 46 detached from their substrate in their natural habitat can survive for some time, and an apparent ability to modify peduncular morphology (Rudwick, 1961; Appendix II) may result in unattached specimens forming a considerable proportion of the population if the environmental conditions are suitable. Some usually -attached specimens have been observed free-lying on the sea-bed in various New Zealand brachiopod populations (Doherty, 1976; Richardson, oral. comm., 1978). T.retusa is most common in areas where the sediment is fine-grained glauconitic mud, and was absent from Southern areas of the Firth of Lorne where the dominant sediment is sand (Table II). However this feature does not necessarily indicate that T.retusa has a restricted tolerance to sediment grain-size, as few samples were collected in the areas of predominantly sand deposition. The absence of suitable substrate for attachment will certainly limit the distribution of pedunculate brachiopods although,as already mentioned, divers have observed large numbers of T.retusa attached to boulders and rock-faces in the Sound of Jura (where sand is the main sediment type) - a substrate which cannot be sampled by benthic dredge. Therefore the apparent absence of T.retusa from areas of sand deposition is undoubtedly due to the selectivity of the dredge, rather than an indication of preference for fine-grained sediments. In fact sediment type will only become a limiting factor when sedimentation is rapid, or when water conditions are so turbulent that clouds of suspended particles interfere with the feeding process. Sedimentation rates appear to be low in the Firth of 47

Lorne, and the bulk of the sediment which settles on the marginal mussel beds is moved by the currents down into the central depression - the only area where significant thick- nesses of sediment are known to be accumulating in the vicinity of the brachiopod population. It is clear, from Table II, that T.retusa prefers hard substrates. What is not clear ,however, is whether brachiopod larvae are capable of recognising a suitable substrate for attachment. Studies on the larvae of other marine invertebrates have shown that some will prolong the duration of their pelagic stage until a suitable substrate is found. The extent to which such a phenomenon determines the settlement pattern of T.retusa is unknown; a possible mechanism for substrate recognition is described in Subsection I.5.2.6.

1.3.5. CURRENT

A strong and constantly-flowing water current is a necessity for sessile benthic invertebrates such as T.retusa, which feed primarily on food particles carried in suspension in the surrounding sea-water. Laboratory observations have indicated that there is a maximum and a minimum threshold for survival, as high current velocities are likely to damage the rather delicate food-gathering lophophore, whilst low current velocities result in starvation. Current velocity, therefore, has the most noticeable effect on the feeding 48

process; the pedicle attachment of T.retusa is extremely strong, and the shell robust, and mechanical damage due to high current velocities is, therefore, unlikely. However when current velocities are outside the tolerance limits of T.retusa, the valves remain closed and feeding ceases. The nature of current flow may also be a limiting factor. A sudden increase or decrease in current velocity causes the cessation of feeding in T.retusa (Section 1.5.1.) - such disturbances if frequent in the natural environment, would certainly seriously affect the feeding process. Therefore, under ideal conditions, the currents would be constant and uniform, with no sudden surges or periods of stagnation. Unfortunately, nothing is known about the prevailing current conditions in the bottom-waters of the Firth of Lorne. The only data available for the area comes from the Admiralty Pilot (West Coast of Scotland, 1974, 2nd Ed.) and from nav- igation charts, both of which deal solely with surface currents. The main oceanic current which affects the west coast of Scotland is the North Atlantic Current, which is a continuation of the north-easterly flowing Gulf Stream. However the most pronounced surface currents within the Firth of Lorne are associated with the tidal ebb and flow. These tidal currents are usually of the order of 0.5 - 1 knot, although tidal streams of over 4 knots have been measured. As described in Section 1.3.3., there are at least two distinct water bodies in the Firth of Lorne, and it is unlikely that current conditions on the sea-floor are comparable to those prevailing at the surface. Certainly the tidal effects are unlikely to be discernible at the depths 49

inhabited by the T.retusa population in the Firth of Lorne (i.e. 180 metres). It is perhaps reasonable to assume that a steady north-easterly current of relatively uniform velocity flows past the mussels beds in the Firth of Lorne, but such a conclusion is highly speculative.

I.3.6. SALINITY

In general, the percentage salt content of the cells of marine organisms is similar to that of average sea-water (Moore, 1958). Therefore, under constant salinity conditions, marine organisms have little difficulty in maintaining a desirable salt concentration within their body tissues. However significant salinity fluctuations do occur in some habitats (i.e. intertidally , in estuaries, and in shallow enclosed seas such as the Black Sea), and under brackish or freshwater conditions organisms must devise some osmoregul- atory mechanism to ensure that the salt concentration of their body tissues remains within the tolerance limits of the species. Methods of osmoregulation vary from simply isolating the body tissues from the surrounding sea-water for the duration of the period of undesirable salinity conditions (by burrowing, closing their shells, or clamping down tightly against the substrate), to complex modifications of the cellular membranes to regulate the rate of osmotic diffusion. Significant salinity fluctuations occur in the surface 50 waters of Scottish sea-lochs because of the run-off of fresh water from the surrounding land. T.retusa has never been collected from such areas of reduced salinity, and this species would appear to be relatively intolerant of salinity fluctuations (i.e. stenohaline). As far as can be ascertained, all articulate brachiopods are stenohaline. There are, however, many other factors which are likely to inhibit the settlement and survival of T.retusa in shallow water environments (Section I.3.2.), and low salinity may not be a primary limiting factor. Many stenohaline organisms do have a small but significant tolerance range to salinity fluctuations despite being incapable of modifying their cellular membranes; the salt content of the body tissues will increase or decrease in response to similar changes in sea-water salinity without any of the life functions being impaired. However the inarticulate burrowing brachiopod Glottidia pyramidata (Stimpson) is known to be tolerant of salinities between 19.9% and 30.6% in its natural habitat (Paine, 1963), as compared with an average normal sea-water salinity of 36%. Such a wide tolerance range is partially due to the fact that burrowing brachiopods are able to isolate themselves by withdrawing to the bottom of their burrows, although laboratory experiments have proved that G.pyramidata is also capable of osmoregulation (Paine, 1963). Abnormal salinities are known to affect the growth-rates of many marine organisms, and it may be that dwarf faunas in the fossil record reflect brackish or reduced salinity conditions. 51

1.3.7. ASSOCIATED FAUNA

The dredged samples from the Firth of Lorne commonly contain:- the asteroids Crossaster, Solaster and Asterias; the ophiuroids Ophiothrix and Ophiura; the echinoid Echinus; the decapods Galathea and Munida. Apart from the horse- mussel Modiolus modiolus (Linnaeus), bivalves are rare, and only dead gastropod shells have been found. Ili terms of bulk the mussels and ophiuroids dominate the fauna (Plate 3A-F). The external surfaces of the mussels are used as substrate by a wide range of animals and plants, the most abundant of these being the inarticulate brachiopod Crania anomala (Miller), hydroids, sponges, chitons, Foraminifera, and bryozoans. However T.retusa is by far the most common epifauna on the mussel shells. The external surfaces of T.retusa are themselves used as substrate by a wide range of smaller organisms, in particular hydroids and sponges. A number of these epifaunal organisms bore into the shell of T.retusa, but these borings are not predatory, and rarely penetrate beyond the primary shell layer. On several occasions small nematoid worms have been found within the brachial cavity of T.retusa. Whether these are in fact parasitic, or have simply been drawn in by the feeding currents, is unknown. A few specimens of T.retusa, collected during the spawning season, had no gonadal tissues, perhaps because of disease or fungal infection. As far as can be ascertained none of the predators in this fauna commonly feed on T.retusa. In comparison with shallow-water faunas in this region this deep-water fauna is relatively impoverished; apart from 52 a few strongly-ribbed, and presumably burrowing, bivalves, and the mussels, the molluscs form a much smaller proportion of the total population. Barnacles, apart from a few extremely large solitary specimens, are absent in the deep- water fauna, which may be a contributory factor in the great success of the brachiopod population. Barnacles and brachiopods are both sessile epifaunal organisms feeding from particulate matter in the surrounding sea-water, and comp- ete directly with one another for the available substrate and nutrients. There is no indication of crowding amongst the epifaunal organisms collected from the deep-water fauna in the Firth of Lorne, and competition for space is clearly not a limiting factor. However some deep-water brachiopods were re-introduced into the shallow marine environment on the west coast of Scotland, and were killed within 3 months by a dense spat-fall of fast growing barnacles which smothered them. Clearly the brachiopods are at a disadvantage in habitats where suitable substrates are rare, and competition for space is probably a limiting factor restricting the occurrence of T.retusa in shallow-water habitats. It has been pointed out that the death of these specimens may have implications for the interpretation of the evolutionary history of brachiopods, as the appearance of barnacles coinc- ides with the widespread dis=appearance of brachiopod stocks from shallow marine habitats (Dr. G.Adams, oral comm. 1979). In the light of this suggestion it is worth pointing out that apart from the advantage gained by rapid growth, the barnacles appeared to be of greater morphological flexibility, becoming grossly deformed, and growing over and around substrate irregularities. 53

I.4. POPULATION STRUCTURE AND DYNAMICS OF T.RETUSA.

I.4.1. INTRODUCTION

The structure of any population is the result of a balance between natality (birth-rate), mortality (death-rate) and the rate of growth. All of these factors are affected to a greater or lesser extent by biological and physico- chemical conditions within the organism and within the environment it inhabits. The reproductive activity of any organism is geared to producing sufficent offspring to ensure the survival of the population, thereby fulfilling the requirements of the underlying driving force in nature, namely the survival of its genetic identity. The basic strategy varies considerably - mammals produce very few offspring which are carefully protected and nurtured until they become self-sufficient, whilst spawning invertebrates, such as T.retusa, produce many thousands of offspring in a single reproductive event, very few of which survive to maturity. In the case of T.retusa the latter strategy is obviously highly satisfactory; biannual spawning events are equally successful, and the population appears to be highly stable both in space and time. 54

I.4.2. SIZE-FREQUENCY DIAGRAMS

The population structure and dynamics of T.retusa have been determined from the size-frequency histograms prepared from regular samples collected from the large population in the Firth of Lorne. Before describing the results, and the other evidence which supports the conclusions reached, it is appropriate to discuss the problems associated with the compilation and interpretation of size-frequency diagrams. There are many pitfalls associated with this method of population analysis, even in the study of living populations; in fossil populations the problems are increased by factors such as post-mortem transportation and selective preservation. Attempts to interpret the population structure and dynamics of fossil brachiopod populations have been hampered by the inconclusive and often contradictory data available from living populations. Whilst the results of the present study certainly provide a basis for the interpretation of the population structure and dynamics of fossil and living brachiopods, it is important that the limitations of size- frequency diagrams as analytical tools are fully realised. The fundamental problem is that it is often difficult to collect a representative sample of a particular population,

and even difficult to determine if the collected sample is. indeed representative. By definition, a representative sample must include all components of the population in their natural proportions (i.e. an increase in the size of the sample would not result in a significant change in the population structure as determined from the original sample). 55

The problem is that many sampling techniques are selective, and further bias can be introduced during the preparation and measurement of the sample. The bias introduced by selective sampling techniques is of particular significance for the study of both fossil and Recent brachiopod populations. For living populations, the suitable substrate for attachment in any one locality may vary in size from large boulders and solid rock-faces, to small shell fragments and pebbles. Sampling of living brachiopods is usally by means of benthic dredges, which are strictly limited as to the size of the material they will collect. Therefore, unless it is clear that the predominant brachiopod substrate in the sample area is of a size and nature which can be adequately sampled by the benthic dredge used (such as the mussels in the Firth of Lorne), analyses of population structure based on dredged samples may well be inaccurate. Even when divers collect the samples inadvertent bias is a distinct possibility; substrates of manageable size, and with large and clearly- visible specimens attached, will be collected in preference to those with only smaller and less-noticeable juvenile specimens. Another factor which may be critical is the area, or volume, of substrate which has been sampled. Once again this factor is of particular relevance for the study of brachiopod populations, many of which have patchy distributions. The problems associated with an inadequate sample area have been well illustrated by the contrasting results of Percival (1944) and Rudwick (1962) who both collected samples of the Recent New Zealand brachiopod Terebratella 56

inconspicua (Sowerby) from Lyttelton Harbour, near Christchurch, New Zealand. In this locality the brachiopods are predominantly attached to large boulders, and the samples were collected by transferring a number of these boulders back to the laboratory where all attached specimens were removed and measured. Rudwick attributed the difference between the shape of his size-frequency distribution and that of Percival to the inadequate area of substrate sampled by the latter. Brachiopods are known to be gregarious, and quite obviously larvae of each generation do not settle evenly on all available boulders. Therefore even when brachiopods can be sampled directly, bias can still be introduced (subsequent studies have indicated that fludwick's results were indeed more representative). The total number of specimens in a sample is another important criterion, as small samples are much more likely to be unrepresentative than large samples. In this study it was considered desirable to have samples of at least 400 specimens. To illustrate the undesirable effect of a small sample, a length-frequency histogram was prepared from a collection of only 65 specimens (Fig.7,C)-• The overall shape of this histogram is very different to those prepared from much larger samples (i.e.Fig.7,A), and it would be impossible to determine the population structure of T.retusa from the data available in Fig.7,C. Unfortunately this fact has often been overlooked in previous studies of brachiopod population structure, and many of the conclusions reached in such studies cannot be justified on the basis of the available data. 57

The other main type of bias, that introduced by the observer, can occur at all stages of the preparation and measurement of the samples, and subsequently during the compilation and analysis of the data. Juvenile specimens can easily be overlooked because of the size. Despite the fact that all samples collected in this study were prepared at the laboratory using a binocular microscope, there is evidence to suggest that the number of newly-settled brachiopods which were picked out was much less than the total number present (Fig.5,A). Bias can also be introduced during the measurement of the specimens, either because of ambiguity in the definition of the parameters to be measured, or by personal bias in estimating the last digit of a reading by eye on a vernier scale. Ansell and Parulekar , (1969), commenting on previously published size-frequency histograms, suggested that regularly spaced modes were in fact artificially introduced by inadvertent bias of the observer towards certain final digits. Such a problem, whilst only of significance in the study of populations of small specimens in which increments of 0.1mm are critical, has been avoided in the present study by using dial calipers. It is impossible to state desirable minimum values for either sample size or sample area which are widely applicable, as conditions vary considerably from population to population. Even within a single brachiopod population it is impossible to state desirable minima for these critical parameters. A good example is the question of sample size in studies of T.inconspicua fron Lyttelton Harbour - whilst Rudwick criticised Percival for his small sample area, the 58 author obtained a representative sample identical to Rudwick's from a single small boulder, which was a much smaller area than sampled by Percival. Rudwick's representative sample was only of 200 specimens, whilst Percival's less representative collection contained over 700 specimens. Ultimately, therefore, it is a matter of 'trial and error'; if conditions permit, a number of large samples should be collected, and if the resultant size-frequency histograms are similar then it is reasonably safe to assume that the samples are indeed representative. As a further check, the results can be compared with theoretical models of population structure, such as those of Craig and Oertel, (1966). Despite all these problems, size-frequency diagrams are an invaluable source of information on population structure and dynamics, and, with due consideration to the potential haz- ards, it is possible to extract from them a wealth of information on natality, mortality, growth-rate, and environmental conditions.

RESULTS. All specimens in each of the regular samples were measured to an accuracy of 0.1mm using dial calipers. Of the three principal shell dimensions, (length, width and height - see fig.l), the anterior-posterior length is the most suitable measurement to use in the present study, as the maximum incremental increase in shell size occurs anteriorly throughout ontogeny. It can be demonstrated (Fig.5,B) that the width-frequency histogram (Fig.6,C), and to a lesser extent the height-frequency histogram (Fig.6,B), 59

EXPLANATION OF TEXT-FIG. 6.

Population structure of T.retusa as determined from 811 specimens collected March 1977 from the Firth of Lorne. In A,B, and C the modes corresponding to age-groups have been labelled. (ZB 3727 - ZB 3736)

A. Length-frequency histogram.

B. Height-frequency histogram

C. Width-frequency histogram.

D. Length'- height scatter diagram, illustrating the tendancy for height to increase relative to length in later life.

E. Length - width scatter diagram, demonstrating a precise linear relationship throughout life.

In D and E linear regression equations have been calculated; 'r' is the correlation coefficient, and these values indicate a good correlation between the plotted coordinates and the regression line. (r = 1 indicates a straight line). 60

Firth el lorry March 1977 1 N•811 a

100- Pork of Lorne March 1977 N•811

40— 80-

2 2

b 60- ~ f - 3 3

4 20- 40- 3

5 4 S 10- 20- 7 6 7 7 r 1 fl IS 1 Is 10 20 10 A L.ngth (mm B Height (mm)

Y • 0 52X-0-3 1 r • 0 983 70- a • ' n • 811

Folk of lam March 1977 E E 60- N=811

b O 5 I

50-

10 15 20 1 glh [mm

2 Y ■080X.0-03 a r •0994 n a 811

15 30—

3 4

9 5

10- 6

m 1s C s 10 15 10 20 Width (mm) Length [mm) 61 yield essentially the same results as the length-frequency histogram (Fig.6,A). However the smaller absolute values of the width and height increments result in the all-important modes in the histogram being closer together, with a conse- quent loss of detail because of the more pronounced overlap of different age-classes. Throughout this study, the overall shape of a size- frequency histogram is described as being either 'right- skewed', 'left-skewed ', or 'bimodal'. Bimodal is self- explanatory (Fig.10,F) but there has been some confusion in the use of the term 'skewed' as applied to unimodal size- frequency distributions. In conventional statistical usage 'skewed' refers to the gradually sloping 'tail' of the distribution (Simpson, Roe, and Lewontin, 1960) and therefore a unimodal skewed distribution which slopes away gradually on the right-hand side would be described as right- skewed, (Fig.l0,C) or positively-skewed. A left-skewed, or negatively-skewed, distribution would have a tail on the left-hand side, and a mode on the right-hand side. However this convention has been reversed by some authors (i.e.Raup and Stanley, 1978; Thayer, 1975) who obviously relate 'skewed' to the steeply sloping mode rather than the tail. Throughout this study the more conventional usage has been adopted. A living brachiopod population will have a high percentage of juvenile specimens, and therefore the fact that all size-frequency histograms prepared during this study were right-skewed and unimodal (i.e. with a high proportion of juveniles) confirms that all samples collected 62

during this study were indeed representative of the living population in the Firth of Lorne. When examined in greater detail it is apparent that, within the overall unimodal shape, all of the -size-frequency distributions are multimodal. Once the biannual spawning seasons of T.retusa, and their timing, had been confirmed (Subsection I.5.2.3.), it was then possible to establish the significance of the individual modes. The majority of these modes can be recognised in all of the length-frequency histograms, but the March 1977 sample has been selected as the standard, and will be described in detail. The underlying principle on which this analysis is based is that each of the modes represents a cohort of brachiopods which settled on the mussel beds after one of the reproductive events. Such a technique has been widely used, and is a logical feature providing the growth-rate of the animal is such that successive modes do not merge, and that the animal has a sharply defined breeding season. The modes in the March 1977 length-frequency histogram were defined numerically by the mid-point of the modal group i.e. 2.75mm, 4.25mm, etc. (see Table III). As described in Subsection I.5.2.3., T.retusa spawns twice per year, with the result that larvae settle on the Firth of Lorne mussel beds during two short periods in late Spring (April/May) and late Autumn (November/December). Therefore the March 1977 sample was collected before the Spring 1977 spawning period, as was confirmed by the examination of the state of gonad development in this and subsequent samples (Subsection I.5.2.2.), and by the fact that spawning actually occurred 63

EXPLANATION OF TEXT-FIG. 7.

Length-frequency histograms prepared from samples of T.retusa collected during Spring and Summer 1977.

A. Collected 5th May 1977; N = 786. (ZB 3737 - ZB 3746)

B. Collected 24th May 1977; N = 554. (ZB 3747 - ZB 3756)

C. Collected 6th May 1977; N = 65.

D. Collected July 1977; N = 209. (ZB 3757 - ZB 3766)

E. Collected August 1977; N = 830. (ZB 3767 - ZB 3776) 64

70— 70--

finh af Lam* Firth of lam 5th May 1977 24th Moy 1977 60— N. 786 60— N. 554

50— 50--

40— 40—

30—

i 20—

10— 10—

r 15 A 10 20 10 15 B Length (men Length (mm)

Sowd d Mull 6N' May 1977 N. 65

firth of Lam* August 1977 60— N 0830

50—

nn 40— 15 1 20 10 length (mm)

30— RAI of tam 30— July 1977 33. N=209 C •

•

20—

10— 10—

T 1r Tim n n -n n Is 15 D Length (mm) 20 E 10 20 Length (mm) 65

between 5th and 24th May 1977 (Subsection 1.5.2.3.). Consequently the most recently-settled brachiopods collected in March 1977 will have been spawned during Autumn 1976, and are represented by the first discernible mode on the left-hand side of the length-frequency distribution, namely at 2.75mm (labelled 1(a) in Fig.6,A). The next discernible mode, at 4.25mm (1(b) in Fig.6,A) must therefore represent the cohort which settled after the Spring 1976 spawning season. Similarly, modes corresponding to the biannual spawnings in 1975 (6.75mm - 2(a), 8.25mm - 2(b), in Fig.6,A), and 1974 (10.25mm - 3(a), 11.75mm - 3(b), in Fig. 6,A), can be recognised. There are two further clearly defined modes in Fig.6,A, at 14.75mm and 17.25mm, with a less obvious grouping of only two specimens at 21.5mm. It is clear from the spacing of these modes that biannual cohorts can no longer be distinguished; as described in Section I.4.3., a slight reduction• in growth-rate at this stage of life results in the merging of the biannual modes into a single mode representing all specimens which settled within one calendar year. Thus the 14.75mm mode (4 in Fig.6,A) represents the cohorts which settled during 1973, and 17.25mm (5 in Fig.6,A) represents the settlement during 1972. The mode at 14.75mm is broad, which suggests that it does indeed represent the two cohorts which settled during 1973. There is no mode representing the settlement in 1971 in the March 1977 sample, but the spacing of the other modes indicates that such a mode is to be expected at approximately 20mm (? in Fig.6,A). In the 5th May 1977 sample however, there is a mode at 19.75mm 66

EXPLANATION OF TEXT-FIG. 8.

A. Length-frequency histogram prepared from 472 specimens of T.retusa collected in January 1979. (ZB 3717 - ZB 3726).

B. Age pyramid prepared for the 811 specimens of T.retusa collected from the Firth of Lorne in March 1977.

C. Growth curve for T.retusa as determined from the analysis of modes in Fig.6,A.

D. Survivorship curve for T.retusa as determined from the age-groups in the March 1977 sample.

In C and D the curves have been fitted by eye. 67

40- F,rrh of le.. lm.nrr 1979 N. 472

n $11 1 1 II I 1 l 10- 1 1 I 40 30 20 10 0 T ,,, X B 5 IS 20 K1 Length ki.'.) A

LENGTH (mm)

AGE (yrs) c

6—

m' 5- m 0 4- • N Q 3-

2— cie • N 1 — •

1 I I 1 Z 3 4I 7

AGE (yrs) D 68

corresponding to the 1971 cohorts (Fig.7,A). As discussed in Section I.4.3., specimens of this age-group do not grow during the winter months, and therefore 19.75mm is almost certainly the position of such an age-group in the March 1977 histogram; its absence is not surprising as there are so few specimens in the older age-groups (Table IV). The mode at 21.5mm is poorly defined, but similarly sized specimens are present in other samples, and its interpretation as a 7th year-class can also be justified on the basis of the spacing between previous modes in the histogram. The striking features of this analysis are the obvious success of each reproductive event, and the extreme regularity of the spacing between the modes. This latter feature is best illustrated diagrammatically, as in Table III :-

TABLE III Analysis of the March 1977 length-frequency histogram (see Fig.6,A). All measurements are in mm.

ANNUAL BIANNUAL DATE OF YEAR- INCREMENT MODE INCREMENT SETTLEMENT CLASS 2.7 Autumn 1976 1(a) /4.25 Spring 1976 1(b) 4 j6.75 Autumn 1975 2(a) 1.5 3.5 /8.25 Spring 1975 2(b) 3.5 10.25 Autumn 1974 3(a) 11.75 Spring 1974 3(b) 3~ 14.75 1973 4 2.5 17.25 1972 5 2.5 19.75 1971 6 1.75 21.50 1970 7 69

Where they can be distinguished, the separation between the modes corresponding to the biannual cohorts (i.e. the 'biannual increment' in Table III) is identical, namely 1.5mm. This regularity suggests a constant rate of growth during the first three years of life, which is confirmed by the estimations of annual growth-increments from modes corresponding to cohorts whose date of settlement was separated by one year; for instance Autumn 1975 - Autumn 1976 = 4mm, and Spring 1975 - Spring 1976 = 4mm (column 1 in Table III). The regularity of mode spacing is all the more remarkable when it is considered that the numerical value assigned to each mode is an average value, and that individuals in a particular age-group grow at varying rates depending on local environmental conditions. The clarity of the modes can perhaps be partly explained by the fact that the March 1977 sample was collected at a time of year when growth-rates seem to be at their lowest, and indeed many older specimens do not grow at all during the winter months (Section I.4.3.). However modes corresponding to annual or biannual cohorts can be recognised in samples collected throughout the year, and all the evidence suggests that the T.retusa population is not subjected to the disturbances caused by fluctuating environmental conditions which are known to adversely affect the stability of marine benthic populations in shallow-water habitats. The procedure of assigning modes to year-classes (i.e. 1(a), 1(b), etc., in • Table II1 and Fig.6,A) has only been used in describing the March 1977 histograms, as the presence of newly-settled specimens in subsequent samples can lead to confusion. For example in the 24th May 1977 histogram the 1(b) prefix would 70 be assigned to specimens spawned in Spring 1977 (on average 0.25mm in length - Fig.7,B), whilst 1(b) in the March 1977 histogram refers to specimens spawned one year earlier during Spring 1976, and which are, on average, 4.25mm in length (Fig. 6,A). Using the data from Table III the March sample can be divided into age-groups (i.e. year-classes). The boundaries of the age-groups are somewhat arbitrary, and undoubtedly the higher and lower values in each grouping include specimens which rightly belong in the age-groups on either side. However, it is considered unlikely that this feature results in significant distortion of the relative proportions of the animals in each age-group. The resulting data (Table IV) was used to construct an age pyramid (Fig.8,B).

TABLE IV Age-groups in the March 1977 sample (N=811); 'size range' refers to maximum shell length measured in MUG

AGE- YEAR OF SIZE No.of % of GROUP SETTLEMENT RANGE SPECIMENS TOTAL 1 1976 up to 5.5 365 45 2 1975 5.6 - 9.5 213 26 3 1974 9.6 - 13.5 121 15 4 1973 13.6 - 15.5 56 7 5 1972 15.6 - 18.5 47 6 6 1971 18.6 - 20.0 7 1 7 1970 over 20.0 2 0.5 71

I.4.3. GROWTH-RATE

The rate of growth of T.retusa, as represented by the increase in shell length, can be calculated from the data in Table III. Having determined the significance of the modes in terms of settlement cohorts, it is then possible to use the mid-point of a particular mode as a measure of the average growth achieved by specimens in that cohort since settlement. For instance, the specimens which settled in Spring 1976 had grown,on average, to a length of 4.25mm by March 1977. Having applied similar logic to all modes in the March 1977 histogram (Fig.6,A), the resultant data can be illustrated diagrammatically in the form of a growth-curve Fig.8,C). The significant feature of the growth-curve of T.retusa is its approximate linearity, indicating that growth continues throughout the life of the animal. Apart from a gradual slowing of growth in later life, the only significant depar- ture from linearity occurs in a short period following settlement when growth is relatively rapid (Fig.8,C). By observing the progression of modes representing newly-settled cohorts in successive samples, it is possible to determine the duration of this period of rapid growth with reasonable accuracy. Thus the specimens which settled in Autumn 1976 had attained a length of 2.75mm by March 1977 (1(a) in Fig. 6,A), and were on average 1.5mm smaller than those spawned during Spring 1976 (1(b) in Fig.6,A). This is the expected separation between modes corresponding to biannual spawnings (i.e. 'biannual increment' in Table III), and further rapid 72 growth of the Autumn 1976 cohort would result in the 2.75mm mode closing on, or merging with, the Spring 1976 mode (i.e. 4.25mm), which obviously does not happen. Therefore the Autumn 1976 cohort has completed its period of relatively rapid growth by March 1977, approximately 3 months after settlement. Similarly, the specimens which settled in May 1977 (Fig.7,B) were on average 1.25mm in length in July 1977 (Fig.7,D), and 2.75mm in length in August 1977 (Fig.7,E). The possibility of further rapid growth is precluded by the fact that these specimens are a mere 3.75mm in length in January (Fig.8,A), and 4.25mm in March (Table VII). It is interesting, therefore, that in all specimens, whether they undergo their early development in winter or summer, the initial period of relatively rapid growth is of similar duration (i.e. approximately 3 months). As all specimens are on average 2.75mm in length at the end of this 3 month period, it is quite obvious that the growth- of post- settlement specimens is unaffected by variable seasonal conditions which, as discussed below, are thought to affect the growth-rate of older specimens. The ovum of T.retusa, has a large nutrient-filled. yolk-sac, and probably the developing larvae are not dependant on planktonic food supplies during their pelagic stage. It is generally accepted that it is the reduced availability of nutrients which inhibits many temperate-latitude invertebrates from spawning in the winter months. However brachiopods do develop short stubby lophophore filaments and an alimentary and digestive system shortly after settlement, and feeding has been observed in some recently-settled specimens (Morse, 1871). There 73

seems little doubt that such specimens are dependant on external food supplies. Thus the ability of newly-settled specimens of T.retusa to grow rapidly in either winter or summer is somewhat unexpected, although it may be that the low nutrient requirements of juveniles are adequately satis- fied by even the reduced food supply in winter months. The growth history of T.retusa can be summarised as follows, (data, in mm, is from the March 1977 sample as interpretated in Table III) :-

TABLE V Annual growth-rate of T.retusa

YEAR AVERAGE OF LIFE GROWTH 1 4.5 2 4.0 3 3.5 4 3.0 5 3.0 6 2.75 7 1.75

It is quite clear that the maximum age of T.retusa is seven years. Indeed the 7th year-class is represented by only two specimens out of a total of 811 collected in March 1977 (Fig. 6,A), by seven out of 786 collected on 5th May 1977 (Fig.7,A), and by seven out of 830 collected in August 1977 (Fig.7,E). Occasionally one of these specimens exhibits an unusual 74

degree of globosity, and a number of closely-spaced anterior growth-lines, (two features which are characteristic of gerontic growth), suggesting that these specimens may have survived for slightly longer than seven years. Craig and Oertel (1966) believe that high-to-low growth strategy (i.e. rapid early growth, slowing progressively throughout life but never ceasing) is especially characteristic of invertebrates, and an approximately linear growth-rate, similar to that of T.retusa, has been recognised in some bivalves (Kirstensen, 1959). (The differentiation between high-to-low and approximately linear growth-curves is obviously rather arbitrary. A high-to-low growth- curve, as illustrated be Craig and Oertel (1966), is much more highly curved than the growth-curve of T.retusa which, therefore, is more accurately described as approximately linear.) The growth history of the mussels utilised by T.retusa as substrate in the Firth of Lorne has been analysed by Comely (1978), who described a high-to-low growth strategy. Comely also studied shallow water populations of the same species and found that, whilst the annual growth increment was larger in shallow-water habitats, the growth strategy was similar to that of the deep-water population. This suggests that, whilst environmental factors affect the absolute growth-rate, the overall growth strategy is probably genetically controlled. Observation of the progression of the modes in successive samples can be used to determine whether T.retusa grows continuously throughout the year, or only at certain seasons. The modes corresponding to the fourth and fifth year-classes 75 in the March 1977 length-frequency histogram have been recognised in subsequent samples collected in May, August, October, and January, as indicated in Table VI (measurements are in mm, and refer to the maximum shell length) s-

TABLE VI EXPECTED MAR MAY AUG OCT JAN IN MAR

4th YEAR 14.75 14.75 16.25 17.25 17.25 17.25 5th YEAR 17.25 17.25 18.25 18.75 19.75 19.75

In both cases, there is no noticeable movement of the modes between the March and May samples. The 4th year mode has attained its expected position after one years growth (i.e. to 17.25mm) by October, and the 5th year mode (to 19.75mm) by January. Thus it is apparent that,in later life specimens grow predominantly during the summer months. However the pattern of seasonal growth is different in juveniles, and the movement of the modes corresponding to recently-settled cohorts has been observed in similar fashion :-

TABLE VII

DATE OF EXPECTED SETTLEMENT MAR MAY AUG JAN IN MAR AUTUMN 2.75 2.75 - 5.75 6.75 SPRING - 0.25 2.75 3.75 4.25 76

TABLE VIII

Analysis of growth-lines on specimen No. ZB 3717.

DATE OF INCREMENT GROWTH-LINE FORMATION -2.0 Autumn 1975 Winter 1.4 3.4 Spring 1976 Summer 2.9 6.3 Autumn 1976 Winter 1.6 7.9 Spring 1977 Summer 2.9 10.8 Autumn 1977 Winter 2.0 12.8 Spring 1978 Summer 1.4 14.2 Autumn 1978 Winter 1.3 15.5* Spring 1979

(* this is actually the length of the shell and not a growth- line; it is clear that shell growth virtually ceases during Winter, and therefore this value is an acceptable approximation of the position of the Spring 1979 growth-line) 77

The significant feature is that these specimens quite obviously continue to grow throughout most of the winter months when the older specimens do not, a phenomenon which is apparent not only in the three month period of rapid growth immediately following settlement. There is some indication that the growth of these younger specimens does slow or even halt between March and May (i.e. the lack of movement of the Autumn 1976 mode between the March and May sample - Table VII) although the evidence for this from the analysis of length-frequency histograms is certainly not conclusive. However further evidence of a reduced growth-rate during winter comes from the analysis of growth-lines. Whilst the analysis of brachiopod growth-lines is the main topic of Part II of this thesis, a sample analysis of the growth-lines on a single specimen is included at this stage to illustrate that such an analysis confirms the conclusions reached above. The specimen (ZB3717) was collected from the Firth of Lorne on the 1st January 1979, at an approximate depth of 165 metres. The measurements refer to the distance from the posterior margin of the shell to each growth-line, measured (in mm) along the anterior-posterior axis on the ventral valve. (Table VIII). The analysis in Table VIII indicates that this specimen was spawned in Spring 1975, and would have been approximately 15.5mm in length by the Spring of 1979, which is within the size range for 4 year old specimens predicted by the analysis of length-frequency histograms.(Specimens of this age are, on average, 14.75mm in length - see Table IV). Clearly growth- 78

lines are formed biannually, presumably during the autumn and spring as a direct result of the pronounced disturbances associated with the mixing of the water column at such times (Section I.3.3.). Spawing activity, whilst occurring virtually synchronously, cannot be a primary cause of the formation of growth-lines, which are present during the first two years of life when the animals are sexually immature. Progressive erosion of the posterior portion of the ventral valve (due to abrasion against the substrate as the specimens rotate around their pedicle) results in some of the growth-line measurements, particularly of earliest- formed growth-lines, not being an accurate indication of the size of the animal when the growth-line was formed (Section II.3.2.); such a phenomenon, however, does not affect the validity of the growth-line increment as a measure of the growth achieved within a certain period. This analysis confirms that growth is faster in summer than in winter (i.e. column 1 in Table VIII). In general, approximately two-thirds of the annual increase in shell length appears to have occurred during summer. As the 'summer' and 'winter' periods do seem to be of equal length (Section I.3.3.), summer growth must, therefore, proceed at twice the rate of winter growth. During the fourth year of life the growth rate of the specimen analysed in Table VIII seems to have been identical in winter and summer, although this may have been due to some localised disturbance which adversely affected the growth of this animal between Spring and Autumn 1978. A more likely explanation however, is that the growth-check (i.e. the physiological disturbance caused 79 by changing environmental conditions) may have been delayed in Spring 1978, with the result that the animal's growth rate had already increased before the growth-line formed; the fact that the previous winter increment is unusually large (i.e. between Autumn 1977 and Spring 1978 - Table VIII) seems to confirm such a conclusion. Whilst the reducing growth-rate results in the later formed growth-lines being progressively closer together and consequently more difficult to interpret, it does seem from the analysis of the growth-lines on other specimens that growth occurs predominantly in the summer throughout the lifespan of T.retusa. The regularity of the inter growth-line increments, and the fact that such increments are as predicted by the analysis of the length-frequency histograms, is a further indication of the remarkably stable and disturbance-free environment inhabited by these animals, and of the great potential of size-frequency histogram analysis and growth-line studies. A further feature which must be considered is differential growth-rates between males and females in a population. Gonads were well-developed in all sexually- mature specimens of T. retusa in a sample ccllēcted_from the Firth of Lorne on the 28th October 1977, and it was therefore possible to determine the sex of each specimen. A separate length-frequency distribution was then prepared for each sex (Fig.9). It is clear from Fig.9 that males and females do have slightly different growth strategies; there is some indication that females greater than 15mm in length have a slightly slower growth-rate than similarly sized males, perhaps due to the relatively greater stress 80

25- --A.— FEMALE (N=161) - -v- -MALE (N =181) • COMBINED

20—

15-

10 15 20 Length [mm]

EXPLANATION OF TEXT-FIG. 9.

Sexual dimorphism in shell growth as determined from 342 sexually-mature specimens collected 26th October 1977 from the Firth of Lorne. The fact that the male and female curves are out of phase suggests slightly different growth rates in males and females. 81 associated with the development of ova rather than sperm. However, the modes in fig.9 are rather confused and ambiguous and further data is required before the significance of such a sexual dimorphism can be assessed. In the context of the present study the effect of sexual dimorphism on growth-rates is not discernible in the length-frequency diagrams and need not,therefore, be considered further. A slowing of the rate of growth is in fact a characteristic feature of the growth strategy of many temperate- latitude marine invertebrates during winter, and can be directly related to seasonal variations in biological and physico-chemical factors which affect the growth process. Temperature and food supply are the two main seasonally variable factors which are likely to affect the_grawncth-rate`` of T.retusa. The effect of seasonal temperature variations on the growth of cold blooded marine invertebrates has been discussed in detail in Section I.3.3. Changing temperatures affect the rate of chemical reactions (Van't Hoff's rule), and therby affect the rates of metabolic activities, including those which control the process of shell secretion. On average the metabolic activities of marine invertebrates are thought to be affected at the rate of 9.6% for every 1°_C change in sea-water temperature (Prosser, 1973). The problem is that nothing is known about the rates of metabolic processes within T.retusa, or to what extent they are affected by changing temperature, and it is therefore difficult to assess the quantitative effect of the annual temperature range of 6°C in the Firth of Lorne (Fig.4,A). Using the average value described above, the rate of metabolic activity of T.retusel would be expected to vary by as much as 60% 82

between maximum and minimum temperature conditions; a figure very similar to the 50% reduction in growth-rate which is apparent from the analysis of modes in the length-frequency histograms (see above). However other factors are known to affect the rate of growth and, furthermore, many invertebrates are known to be capable of physiological adaptation to seasonal temperature variations, a process that would reduce the effect of changing temperatures or metabolic rate. The analysis of the progression of modes in the length- frequency histograms does not yield sufficiently precise data to allow the slowing of growth in winter to be assessed quantitatively, apart from the rough estimation of 50% (see above). However there can be no doubt that the apparent slowing or cessation of growth during winter months is related to low ambient temperatures. It is likely that growth becomes progressively slower during autumn as sea-water temperatures fall, and reaches a minimum or ceases during periods of minimum temperature. The annual temperature range (6°C) experienced by T.retusa in the Firth of Lorne is much less than would be expected at such latitudes, due to the warming effect of the North Atlantic Current (Section I.3.5.). Terebratulina septentrionalis (Couthouy), at equivalent latitudes on the east coast of N.America, experiences similar maximum summer temperatures as T.retusa, but experiences an annual range more than double that of T.retusa because of much lower winter temperatures (Noble, Logan, and Webb, 1976). During winter months the quantity of food available to T.retusa is reduced. As nutrients, primarily derived from ingested food particles, provide the fuel for all metabolic 83 activity, it is to be expected that the rate of growth is reduced in direct proportion to the quantity of food available. However, as discussed in Appendix III, it is possible that during winter months T.retusa obtains nutrients both from food particles carried in suspension in the surrounding sea-water, and also from storage centers within the caeca. which are stocked with nutrients during seasons when they are abundant. Such a nutrient storage capability would reduce the effect of the reduced availability of food during winter months, and may well be a crucial factor, allowing juveniles to continue growing at such times. However the winter cessation of growth in older specimens must then be explained. Such specimens have a large well-developed lophophore, a proportionately greater storage capacity than smaller specimens, and there is no reason to suggest that they are incapable of collection and storing the quantity of nutrients necessary to allow all metabolic activities to proceed at the rate dictated by the prevailing biological and environmental conditions. Similarly, temperature conditions are undoubtedly not age-specific, or size-specific, in their effect. The winter cessation of growth in adults may, of course, simply be a feature of the ageing process but, if so, then the first signs of senility are apparent at a surprisingly early stage of ontogeny (i.e. during the third year of life). However an additional factor which must be be considered is the process of gonad development., which is first discernible in specimens of approximately 8mm in length, although spawning does not occur until the third year of life. It is at this stage (i.e. 10 - 12mm in length) that 84

the first noticeable slowing of growth-rate is apparent (Table V). Thus it is possible that, in sexually mature specimens, winter growth ceases because the bulk of available nutrients, whether from external or internal sources, is required for gametogenesis. Unfortunately the data available from the analysis of the length-frequency histograms is not sufficiently detailed to determine if there is a precise correlation between the winter cessation of growth and the first major development of gonadal tissues. However this would seem a logical strategy, with the emphasis being on ___- -shell growth in juveniles; subsequently, with the attainment of sexual maturity, the developing gonads receive priority in terms of available nutrients. As discussed in Section I.4.5. there are other physiological and morphological changes associated with the onset of sexual maturity. It is perhaps doubtful that the solubility of calcium carbonate is a factor which has any significant effect on the growth of T.retusa. The solubility of calcium carbonate is known to increase with decreasing temperature, with the result that organisms have progressively greater difficulty in extracting this vital skeletal component from the surrounding sea-water as temperature decreases. However the change of solubility resulting from an annual range of 6°C is unlikely to be significant in inhibiting the winter growth of T.retusa, and indeed this factor is unlikely to be important in temperate latitude shallow-water habitats. The solubility of calcium carbonate also increases with increasing hydrostatic pressure and increasing partial pressure of carbon dioxide. As a result the calcareous skeletal 85 components of organisms from deep water are demonstrably thinner than those of equivalent shallow water organisms. Some preliminary work on the ultrastructure of Recent deep- water brachiopods has suggested that modifications of the shell secretory regime, producing strengthening 'struts' within the primary shell layer (Plate 10,A,B), are necessary to compensate for the greatly reduced availability of calcium carbonate. Structural modifications of this nature have not been recognised in shallow water brachiopods, and undoubtedly are restricted to specimens from abyssal habitats. Ideally the conclusions described above would be confirmed by the measurement of the rate of growth of living specimens in their natural environment. In practice this is often very difficult because of the life-habits or habitat of the animals; even when conditions are suitable, measuring and marking specimens can cause significant disturbance to the growth process. However Chuang (1961) used this technique with considerable success in studying the growth-rate of the readily-accessible intertidal brachiopod Lingula unguis (Linnaeus) from Singapore. This species grows by as much as 20mm per year, and therefore the proportionate effect of notching the anterior margin on the annual growth-rate is less significant than if a similar technique was used in studying the relatively slow-growing T.retusa. In any event it was impossible to measure and mark in-situ specimens in the Firth of Lorne at a depth of 180m, which is well beyond the range of SCUBA divers. An alternative method, often used in growth-rate studies of benthic invertebrates, is to measure and mark dredged 86

specimens which are then retured to their natural habitat in recoverable cages. Such a technique was used in the study of the growth-rates of Norwegian brachiopods (Schumann, pers. comm., 1976) but_as the cages were either destroyed or moved by strong currents, the results were disappointing. Obvio- usly such a procedure involves considerable disturbance to the animals, and ideally such ā study should continue for several years, with only infrequent recovery of the cages to measure the enclosed specimens. A suitable recoverable- cage system for the Firth of Lorne would have required exp- enditure beyond the scope of this study; in addition there were many logistical problems, not the least of which being the navigational hazard caused by buoys (with approximately 300m of attached cable) moving with the tidal currents close to the entrance of Oban Harbour. However attempts were made to measure the growth-rate of T.retusa in aquaria (Chapter I.2.) and by reintroducing measured and marked specimens to the more natural shallow marine environment of Dunstaffnage Bay. These latter specimens were killed by a dense settlement of fast-growing barnacles before any increase in length was discernible. The aquaria attempts also failed - the outside aquarium at the Dunstaffnage Laboratory was very susceptible to changes of air-temperature, with the result that a daily temperature range close to the normal annual range in the Firth of Lorne was measured in this aquarium on some sunny winter days, (Fig.4,B.). No growth was discernible in the specimens living in such stress-inducing conditions for over a year. The conditions in the London aquarium were even more 87

artificial than in the Dunstaffnage aquarium, and once again no increase in shell length was discernible. Whilst the available data on the growth-rates of living brachiopods is described in Part II of this report, it is worth pointing out at this stage that the inferred growth- rate of T.retusa is very similar to the growth-rates of many other temperate-latitude brachiopods of comparable maximum size. Whilst the inability to measure the growth of T.retusa in its natural habitat was disappointing, there is no doubt as to the accuracy of the determination of growth-rate based on the analysis of length-frequency histograms. Because of the stable and relatively disturbance-free environment inhabited by T.retusa, and the fortuitous circumstances which allow regular representative samples to be collected, the frequency histograms provide sufficiently detailed information to allow the growth-rate to be determined with more accuracy than is often possible with frequency histograms of shallower-water populations which are prone to frequent environmental disturbances. The growth strategy of the organisms within a population has a pronounced effect on the shape of representative size-frequency diagrams. In many invertebrates, including some brachiopods, the growth curve levels off in later life (i.e. Fig.10,D.), with growth virtually ceasing. In effect, the older specimens are surviving for varying lengths of time after attaining their maximum size. Such a growth strategy (known as determinate growth) has been recognised in one living brachiopod species (Doherty,1976), and is apparent in other Recent and fossil species because of the 88

effect of this phenomenon on the overall shape of the size- frequency diagrams and on the shape of individual shells. As described in Section I.4.7. the overall shape of size- frequency diagrams depends on several factors, and determinate growth strategy results in the merging of older age- groups into a mode on the right-hand side o the size- frequency diagram, thereby forming a bimodal distribution (the other being the juvenile mode as recognised in T.retusa, - see Fig.10, A-F, for comparison of these two types of frequency distribution). The effect of determinate growth strategy on shell morphology is equally apparent, as many specimens, whilst ceasing to grow in length and width at the determinate shell size, commonly continue to grow in height and become extremely globose with numerous closely-spaced anterior growth-lines.

I.4.4. MORTALITY

Mortality-rate is a measure of the percentage of specimens in each year-olass which die per year. In all samples of T.retusa the proportion of specimens in each age- class is virtually identical, and the March 1977 sample, (which has been divided into year-classes in Table IV), can be considered representative. Unfortunately there is no practical method of estimating the number of specimens which settle from each spatfall, and therefore it is impossible to 89

determine the mortality-rate of specimens less than one year old. Data on mortality is plotted, by convention, in the form of a survivorship curve, as in Fig.8,D. As the vertical scale of this diagram is logarithmic, the linear plot of points indicates that the rate of mortality remains remarkably constant from the first year of life onwards. The anomalously low value of the 6th and 7th age- classes is not thought to be an accurate reflection of the mortality affecting older age-classes - the 6th and 7th year- classes are poorly represented in the March 1977 sample (Sec- tion I.4.2.), but are more clearly defined in other samples (i.e. Fig.7,A). If more representative values were used, these last two points would be much closer to the plotted line, although a slight increase in the mortality-rate amongst old specimens would not be unexpected. Examining the data in Table IV it is apparent that approximately 50% of the specimens in each year class die per year. The un- determined mortality-rate amongst sessile specimens less than one year old is almost certainly much greater than 50%, whilst amongst pre-settlement larvae estimations of more than 99% mortality would not be unrealistic. High larval mortality, as a result of predation by zoo- plankton and other organisms, is a common and understandable feature of spawning invertebrates. However it is much more difficult to determine the cause of death of post-settlement specimens. The shells of dead specimens provide no indication as to the cause of death, although few empty shells were collected by the dredge and it is possible that the examination of larger numbers of dead specimens may throw 90 some light on the cause of death. Shallow borings are common, but these are essentially restricted to the primary shell layer, and are unlikely to cause significant mortality; there are considerable numbers of living and apparently healthy specimens with highly bored shells. These shallow borings are not predatory, but merely function as habitats for a variety of organisms which cause little disturbance to their brachiopod 'host'. The characteristic circular borings caused by predatory gastropods and sponges, which penetrate through to the coelomic cavity, were not observed. It is not known whether other carnivores in the Firth of Lorne, such as starfish, commonly feed on T.retusa, but it is considered unlikely as the small quantity of heavily- spiculated brachiopod body tissue will yield much less nour- ishment than the mussels and other bivalves which form tha usual diet of such carnivores. Other possible causes of death include diseases, infections, etc.; several aquaria specimens did indeed die because of fungal infection. Just how common diseases and infections are in nature is unknown; the only possible indication of disease in T.retusa is the occurrence of a few specimens with undeveloped gonads at a time when all other specimens are fully developed. Some small, and possibly parasitic, worms were observed in the mantle cavity of a few specimens. Probably a large proportion of the annual mortality occurs during winter, as a direct result of the increased stress caused by environmental conditions. There is good evidence that the mortality-rate of many invertebrates is directly related to the severity and duration of winter 91

conditions. There was, for instance, a pronounced increase in mortality amongst some marine invertebrates in the Firth of Lorne as a result of the prolonged and severe winter in 1979. However the population structure of T.retusa as determined from the January 1979 sample (Fig.8,A) is essentially similar to that determined from samples collected at various seasons throughout the preceding two years, indicating that, at such depths (approximately 180m), T.retusa is effectively shielded from the most severe effects of abnormal winter conditions. This is also indicated by the fact that the mortality-rate remains constant, despite winters of varying severity in recent years. The Firth of Lorne depression may provide an ideal opportunity to study the taphonomy of a brachiopod population. The fact that so few dead specimens have been collected along the margins of the depression confirms that the majority are moved, by current and gravity, down into the deep central region of the depression ( more than 220m deep). Thick accumulations of sediment and other debris are known to be present in this area. The short distance that shells are moved from the marginal mussel beds to the central depression will preclude significant mechanical disintigration; in addition, dredged samples from the central area of this depression reveal an impoverished fauna, suggesting that shells will not be subjected to significant biological degradation. Therefore there is a distinct possibility that large corer-type samples from the central depression can be used to determine to what extent the 'fossil' population structure, as determined from the 92

potentially fossilisable dead shells, is an accurate reflection of the actual living population structure. Craig and Oertel (1966) produced computer simulations of size- frequency histograms (Section I.4.6.) which indicate that constant growth-rate and constant mortality will result in the fossil population structure being identical to that of the living population. As the preservation potential of T.retusa in the Firth of Lorne appears to be good, it would be interesting to determine if this theoretical conclusion is correct. Large corer-type samples from the central depression, which are logistically possible with the equipment available on the R.R.S. CHALLENGER, may also help to determine the cause of death of some specimens of T.retusa.

I.4.5. LIFE-HISTORY

The life of T.retusa can conveniently be divided into three distinct stages :- (a) the larval pre-settlement stage; (b) the post-settlement, pre-sexual maturity stage; (c) the sexual maturity stage. The larval pre-settlement stage is of the shortest duration (approximately 3 weeks or less), and is poorly known. Larval T.retusa do not secrete a protective calcareous skeleton, and are therefore very vunerable to predation; they may well be brooded within the mantle cavity of the parent (Subsection I.5.2.5.) in an attempt to reduce the detrimental effect of such predation. Once 93

released from the parent, the larvae become free-swimming, moving rapidly and erratically above the substrate in search of a suitable settlement site. Shortly before settlement the movements of the larvae become sluggish, and initial attachment to the substrate is thought to be achieved by means of a sticky substance secreted from the posterior tip of the pedicle. T.retusa begins to secrete a calcareous exo-skeleton soon after entering the post-larval, pre-sexual maturity stage. The first formed shell - the protegulum (Plate 10, C - E) - is secreted synchronously and uniformly on both ventral and dorsal surfaces, and can be easily distinguished from subsequent shell growth, which proceeds by peripheral accretion. The first formed shell is thin and transparent, but becomes progressively more opaque as the shell material thickens. A variable proportion of the posterior-most ventral valve, including the protegular plate, is progressively eroded throughout the life of the animal due to abrasion against the substrate (Section II.3.2.). With the exception of this eroded portion, the external valves are preserved in their entirety throughout the life of the animal, and provide a record of the post-larval growth history. Internally the various calcareous processes such as the crura, the brachidium, and the articulatory teeth and sockets (Fig.1), are developed at an early stage (Fig.11), and throughout the life of the animal they are subjected to a variable amount of resorption to accommodate ontogenetic changes in the size and disposition of body and lophophoral tissues. The valves of the shell grow faster in the 3 month period immediately 94

following settlement than at any other stage of life (Sect- ion I.4.3.), and throughout the post-settlement, pre-sexual maturity stage it is growth of both shell and body which receives priority; during this stage growth continues at all seasons (Section 2.4.3.). In its earliest development stages the pedicle is un-. _ able to support the weight of the shell and body, and the animal lies flat against the substrate, with the pedicle functioning simply as a tether rather than a supportive 'stalk'. Progressively the pedicle cuticle becomes more rigid, the developing rootlets (Plate 4,B) begin to bore into the substrate, and the shell is supported above the substrate. Strong pedicle adjustor muscles develop at an early stage, and juvenile specimens move around their pedicles as freely as adults. Internally, feeding and digestive organs develop shortly after settlement, and feeding commences. The anterior feeding gape in juveniles is extremely wide, forming an angle of at least 45 degrees. As the teeth and sockets become progressively larger and more robust the commissural gape decreases, and is approximately 15 - 20 degrees in adult specimens. The lophophore development proceeds rapidly through the four development stages (Section I.5.1.; Plate 5, E-F; Plate 6, A-C.), with the 'adult' plectolophe present in specimens less than one year old, although in these specimens the median spiral of the lophophore will continue to develop for some time (Plate 6, A). Lophophore filaments, which in recently-settled specimens extend well beyond the shell margin when the animal is feeding, become 95

proportionately shorter as development proceeds, and at the plectolophe stage they barely project beyond the shell margin when feeding. The setae are initially much longer than the valves of the shell, but they also become proportionately shorter as growth proceeds. Gonadal tissues first appear towards the end of the post-settlement, pre-sexual maturity stage, but they remain immature. The initiation of sexual maturity, defining the onset of the third stage, is distinguished by profound physiological and morphological changes. Specimens become sexually mature during their third year of life (approximately 10 - 12mm in length), and for the remainder of their life-span gametogenesis receives priority over shell growth._ A significant change in relative shell proportions occurs at sexual maturity, as height begins to increase at a proportionately greater rate than width or length (Fig.6,D). This is probably linked to the achievement of the fully developed median spiral of the lophophore; by the third year of life , the lophophore has reached its final development stage, and future changes involve increasing size without significant alteration of its proportions. One of the most significant features of the sexual maturity stage is the gradual slowing of the growth-rate (Fig.8,C), and the restriction of growth to the summer season (Section I.4.3.). The gonads, in complete contrast, become larger as the space available for their development increases in direct proportion to increasing shell dimensions. The gradual slowing of shell growth may be directly related to the progressively larger gonads which require an increasing proportion of the available nutrients (Section I.4.3•)• 96

Death occurs before any obvious signs of senility are apparent; the slowing growth-rate is thought to be due primarily to a reduction in the energy input into the secretory processes because of increasing gonadal requirements. However less efficient food-gathering and/or util- isation may indeed be a feature of the ageing process. Whatever the cause, (Section I.4.4.), the mortality of approximately half of each age-group per year results in few specimens in the older age-groups. Specimens never exceed 23mm in length, and only rarely survive for more than 7 years.

I.4.6. COMPARISON WITH THEORETICAL MODEL

The overall shape of a size-frequency diagram is determined by the somewhat complex interrelationship of the various biological and environmental factors which affect the population in question. Craig and Oertel (1966), using computer simulations, attempted to provide a detailed theoretical background for the analysis of size-frequency diagrams. They identified five main factors which influence the shape of a size-frequency diagram, and produced a series of histograms using various combinations of these five factors. Craig and Oertel's first factor - recruitment strategy - had five possible categories. T.retusa clearly falls within the 'boreal' recruitment strategy, which was defined 97

as two short spawning periods in spring and autumn (Subsect- ion•I.5.2.3.). The second factor was growth-rate, and T.retusa has an approximately linear growth-rate (Section I.4.3.), which was the first of the three categories defined by Craig and Oertel. The third factor, the 'coefficient of variation of growth-rate', was an attempt to allow for the effect of varying growth-rates within a single cohort. There is no indication as to the extent of such variation in T.retusa, but in the histograms relevant for this comparison Craig and Oertel use a coefficient of variation of 2, which they believed was an acceptable average value. Mortality- rate was the fourth factor, and T.retusa obviously falls within Craig and Oertel's third category, namely constant mortality-rate (Section I.4.4.). The fifth factor, 'cessation of growth', had only two categories:- (a) a winter stoppage of three months duration; (b) an artificial stoppage of growth for two months in summer. The second category was only used in conjuction with 'tropical' recruitment strategy, and all age-groups of T.retusa certainly grow in summer. As described in Section I.4.3., the growth strategy of T.retusa varies between juveniles and adults, but in either case a slowing or cessation of growth occurs during winter, and obviously the above-mentioned category (a) applies. Therefore the relevant criteria ares- boreal recruitment, linear growth-rate, constant mortality, and winter cessation of growth. These criteria were combined in Craig and Oertel's experiment number 34, and the resulting size- frequency histogram is strikingly similar to the length- 98

frequency histograms prepared from samples of T.retusa collected from the Firth of Lorne (i.e. Fig.6,A; Fig.7,A,B,E.). The overall shape of these distributions is identical, both being unimodal and right-skewed. In Craig and Oertel's histogram the evenly-spaced modes corresponding to the biannual spawning season are discernible, and they merge into a single annual mode in later life exactly as in the natural population. Craig and Oertel describe experiment number 34 as follows:- "Boreal recruitment, three winter months cessation of growth with doubling of mortality, coefficient of variation 2 growth-rate linear mortality constant. Boreal recruitment consists of two equal waves in late spring and early autumn, separated by a short summer interval and a long winter interval This forms twin peaks in the living population the groups of twin peaks are equidistant, and the twins have identical intervals. This peak spacing is diagnostic for linear growth." Significantly the winter cessation of growth has been linked with a doubling of the mortality-rate (constant mortality refers to the rate of mortality from year to year, rather than from season to season). Predominant winter mortality is considered a distinct possibility in the T.retusa population (Section I.4.4.). For each combination of variables Craig and Oertel produced histograms for both living and dead populations; the striking similarity between the theoretical and the actual living population structure would suggest there is good reason to expect the predicted form of the dead population to be correct (i.e. for the dead population structure to be identical to the living population). It remains to be seen if this prediction can be confirmed by collecting large samples of dead specimens of T.retusa from the central depression in the Firth of Lorne. 99

I.4.7. COMPARISON WITH SIZE-FREQUENCY DIAGRAMS OF LIVING AND FOSSIL BRACHIOPODS

There have been many attempts to determine the population structure of both fossil and Recent brachiopods from size-frequency diagrams. Collections of fossil populations are even more liable to bias than living populations as, not only can specimens be destroyed or overlooked during their removal from the rock, but a proportion of the original population may not even have been preserved. Certain age-classes may be more susceptible to various mechanical and biological processes which cause the disintigration of shells before, during, and indeed after, they become fossilised. Thus a detailed knowledge of the population structure of living brachiopods is an essential prerequisite for any palaeontological reconstructions. Theoretical exercises, such as those of Craig and Oertel (1966) - see Section I.4.6. - are important, allowing the effects of various parameters to be assessed; ultimately, however, it is the direct observation of the actual population structure which is conclusive. The fortuitous circumstances in the Firth of Lorne have allowed the first detailed study of a relatively deep-water living brachiopod population, and over a much greater length of time than has previously been possible. The possibility of being able to determine how this population will be represented in the 'fossil' record is an added bonus (Section I.4.4.), allowing the proportionate effect of mechanical and biological disintigration on various age-groups to be assessed. The population structure of the Recent N.American 100

brachiopod Terebratulina septentrionalis (Couthouy) is very similar to that of T.retusa. Whilst the published length- frequency diagrams (Noble, Logan, and Webb, 1976) are plotted as curves in which age-classes cannot be distinguished, all of these curves (a total of nine) are unimodal and right- skewed. Noble, Logan, and Webb (1976) believed that recruitment of juveniles continues throughout the year, and cited as evidence the finding of "females with eggs throughout the year". However the danger of using such a criterion as an indication of the date of spawning has been discussed in Subsection I.5.2.3, and an examination of the T.septentrionalis length-frequency diagrams suggests that such a conclusion may indeed be inaccurate. In two of their samples, collected in April and September, newly-settled brachiopods predominate (Fig.9 in Noble,,Logan, and Webb, 1976), and as a result the mode of the distribution is very close to the vertical axis on the left-hand side of the graph. In the seven other samples, which were collected at other months of the year, the main mode of the distribution is further away from the vertical axis, indicating that no recently- settled specimens were collected. This is identical to the seasonal movements of the main mode in the T.retusa histograms, which has been correlated with the biannual spawning events (Subsection I.5.2.3.). Therefore it seems likely that T.septentrionalis also spawns during spring and autumn, and many other aspects of the growth strategy of this species appear to be very similar to those determined for T.retusa. Terebratella inconspicua (Sowerby) is the most studied Recent brachiopod species. Samples of an intertidal 101

population of this species from a rockpool in Lyttelton Harbour, near Christchurch, New Zealand, have been collected on many occasions (i.e. Percival, 1944; Rudwick, 1962; Rickwood, 1977; and by the author in Nov.1977), and Doherty (1976) carried out a detailed survey of the abundant subtidal and intertidal populations of this species in the Hauraki Gulf, near Auckland, New Zealand. Populations of this species from Paterson Inlet, Stewart Island (southernmost New Zealand) are under investigation by a team from the New Zealand Oceanographic Institute, (Richardson, oral comm., 1978), and the growth history of a large sample from this locality has been analysed by the author (Subsection II.5.2.1). Rickwood collected this species from the Hauraki Gulf, Otago Harbour, Stewart Island, as well as Lyttelton Harbour. Whilst some of the early studies yielded contrasting results (for discussion see Section I.4.2.), there is now a general consensus of opinion that the characteristic size-frequency diagram of this species is bimodal. The left-hand mode corresponds to the juvenile mode as recognised in the T.retusa histograms, whilst the right-hand mode is caused by the merging of several of the older age-classes because of the survival of older specimens after attaining their determinate size. In the majority of cases, representative samples of living, temperate-latitude, brachiopod populations will yield either bimodal or right-skewed unimodal size-frequency distributions. These two basic forms are primarily controlled by the interplay of growth-rate and mortality-rate (Craig and Oertel, 1966) :- (a) linear growth-rate (Fig.lO,A), combined with constant mortality (Fig.lO,B) results in a 102

unimodal right-skewed size-frequency diagram (Fig.10,0); (b) high-to-low or high-to-zero growth strategy (Fig.l0,D), combined with increasing mortality (Fig.10,E), results in a bimodal size-frequency diagram (Fig.l0,F). It is virtually certain that the bimodal size-frequency distribution of T.inconspicua is characteristic , rather than, as Rudwick (1962) suggested, an atypical situation caused by the failure of certain spatfalls. In some organisms the overall shape of the size- frequency distribution varies from season to season (e.g. Craig and Hallam, 1963). This effect is most pronounced in short-lived species with high growth-rates; as described in Section I.4.3. the modes in the length-frequency histograms of T.retusa do vary in position depending on the season of collection, although the overall shape of the distribution remains constant throughout the year. As described below, the fossilised reprepresentation of a living population may differ from the living population structure, and obviously all these factors must be considered in studying fossil or Recent species for which only one sample is available. Unfortunately in some studies of living populations the available data is insufficient to justify the conclusions reached. Very different results were described from two separate growth-rate studies of the brachiopod Terebratalia transversa (Sowerby) from two localities separated by only 160 km on the west coast of N.America (Paine, 1969; Thayer,

1977). It is possible that this difference is in part due to inadequate samples. However the growth-rate of a species 103

EXPLANATION OF TEXT-FIG. 10.

Stylised growth rate, survivorship, and size-frequency curves illustrating the controlling influence of the first two on the overall shape of the latter.

Linear growth rate (A) combined with constant mortality (B) result in a unimodal right-skewed size-frequency distribution.

High-to-low or high-to-zero growth rate (D) combined with increasing mortality (E) result in bimodal size- frequency distributions. 104

... N lit

AGE---~' AGE----. A D t t -m• -m• oS .2 lita.: -a.:lit 0 0 ~. > a.:> > ;:, •;:, lit 1ft

AGE---~" AGE---_" B E.

1 ,.1 u Z... ;:,a ...a.: ~

SIZE----I SIZE----' c F 105 depends to a large extent on prevailing environmental conditions, especially temperature (Section I.3.3.), and representatives of a species from different habitats may well have significantly different growth-rates. Such environmentally- related variations have been recognised in the growth-line study of Terebratella inconspicua (Sowerby) from different localities along the New Zealand coast (Subsection II.5.2.1). This phenomenon is discernible at two levels, local and world- wide, and in both fossil and Recent brachiopod populations, and may be one of the most fruitful of the potential applications envisaged for the growth-line analysis techniques described in Part II of this report. Thayer (1975) attempted to determine the population structure and growth-rate of four species of brachiopods from size-frequency histograms prepared from dredged samples. In one species, Hemithiris psittacea (Gmelin), Thayer considered that a bimodal distribution,(derived from two samples which yielded a total of only 220 specimens), was indicative of the specimens attaining their maximum length of 20mm in two years; however a preliminary examination of the growth- lines on this species indicates that such a conclusion is erroneous, and that H.psittacea appears to have a much longer life-span than suggested by Thayer. There can be no doubt that, without other data, such attempts are highly speculative, especially as many of the samples are unacceptably small. Sample size is the main pitfall and, as described in Section I.4.2., a small sample cannot be used to determine the population structure of T.retusa from the Firth of Lorne, although large samples are extremely informative. 106

The problem of sample size is also apparent in several studies of fossil brachiopod populations. Admittedly there are often great difficulties associated with collecting a large representative sample from a living or fossil population, but this does not justify the use of small samples in population structure analysis, and all such attempts must be regarded as unproved until further data are available. Neall (1970) collected a sample of 48 specimens from a living population of Neothyris lenticularis (Deshayes) by dredging in Forveaux Strait, New Zealand, and another sample, once again of 48 specimens, of fossil Neothyris 'ovalis' (Hutton) from Pleistocene limestones. The fact that both of these samples yielded unimodal left-skewed size-frequency distributions was thought to indicate that the fossil population had not been subjected to selective post-mortem sorting or disintigration. Neall suggested two possible reasons for the lack of juveniles in his dredged sample:- (a) that the free-lying adult N.lenticularis are moved by the strong Forveaux Strait currents and clumped into age-groups; (b) that the larvae settle in clumps and grow to maturity in an area in which subsequent larvae do not settle. Richardson and Watson (1975) observed specimens of Magadina cumingi (Davidson) being moved along the bottom by strong currents, and certainly gregarious settlement behaviour seems to be characteristic of many brachiopod populations. Therefore Neall's two suggestions are indeed possibilities, although it does seem premature to invoke such factors on the basis of a single sample of only 48 specimens, especially as dredging is a notoriously selective method of sampling marine 107 benthos. No population can survive without regular recruitment of juveniles, and any stable living population will include a high proportion of juveniles. It is important to remember, therefore, that whilst post-mortem sorting and/ or gregarious settlement behaviour may indeed affect the - local distribution of age-groups within a population, these factors do not affect the overall population structure. A unimodal left-skewed size-frequency distribution is a common feature of many fossil populations, (Olsen (1957) , in a study of 200 samples of fossil animals, found that 75% were unimodal and left-skewed), and there has been considerable debate as to the significance of such distributions. Formerly it had been considered that such a distribution was indicative of post-mortem transportation, although this simplistic explanation has now been discounted; as described above certain benthic organisms are characterised by a gregarious settlement behaviour with clumps of similarly sized specimens yielding a unimodal left-skewed size-frequency distribution. Whilst this distribution can__not be considered representative of the entire living population, it is nevertheless certain that in some instances a fossil left- skewed unimodal distribution will be representative. Whilst none of Craig and Oertel's computer simulated size-frequency histograms of living populations can be described as unimodal and left-skewed, their results clearly show that a decreasing growth-rate combined with constant mortality may lead to such a distribution in the derived dead population because older age-classes are concentrated in a small size range. In addition a constant growth-rate combined with 108 increasing mortality may also result in a unimodal left- skewed distribution. As a result of these combinations of factors, therefore, the fossil size-frequency distribution can be different from, but still representative of, the living population structure, in contrast to the situation in the T.retusa population where linear growth-rate combined with constant mortality will, in theory, result in the fossil population structure being a mirror image of the living population structure. A unimodal left-skewed distribution can also represent the right-hand mode of a bimodal distribution in which the juvenile mode is poorly represented or absent because of post-mortem transportation or selective preservation. In extreme situations, when even medium-sized specimens are moved or destroyed, a unimodal distribution may even be the representation of a unimodal right-skewed living population distribution, such as that characteristic of T.retusa. With such a wide range of possibilities, it would seem to be virtually impossible to determine the significance of a fossil unimodal left-skewed distribution in terms of the population structure and dynamics of the livin& population from which it was derived. However the all-important growth strategy of a brachiopod, which can be determined in those species with well-developed growth-lines (see Part II), can distinguish between those brachiopod populations which have a determinate growth strategy (i.e. high-to-low or high-to-zero growth-rate) and those which have a linear growth-rate. The former are characterised by gerontic growth which results in adults becoming relatively globose 109

with a number of closely-spaced anterior growth-lines. Further evidence is provided by the modes corresponding to age-classes in a size-frequency diagram, as such modes are equidistant when the growth-rate is linear, but become progressively closer and eventually merge as a result of high- to-low or high-to-zero growth-rate. Once the growth strategy of a species is known, it is then possible to interpret its size-frequency diagram with greater confidence and accuracy. The fact that modes are discernible in a size-frequency diagram is informative. Modes will only appear in a fossil population if they originally existed in the living population, and will only be transmitted to the fossil population if there is a seasonal 'brake', such as cessation of growth, seasonal increase of mortality, or a combination of both (Craig and Oertel, 1966). Therefore, in general multimodal size-frequency diagrams can be considered as characteristic of animals inhabiting temperate and polar latitudes. In theory distinctive modes corresponding to age-groups would be absent from size-frequency diagrams prepared from samples of tropical brachiopods because there is no seasonal 'brake'. The available evidence does indicate that growth and juvenile recruitment continues throughout the year (Chuang, 1959, 1961; Paine, 1963). Unfortunately virtually nothing is known of the population structure and dynamics of tropical brachiopods - data which is an essential prerequisite for any comprehensive analysis of the population structure of fossil brachiopods. Quite obviously the full potential of size-frequency diagrams as a source of palaeoecological

110

information has yet to be realised, and further studies on living populations, which are far from being as rare as many palaeontologists believe, will provide the basis for much. more precise reconstructions of the palaeoecological setting of fossil brachiopods than has been possible to date, as is apparent from the following preliminary discussion. Walker and Parker (1976) collected samples of the brachiopod Rostricellula rostrata, Ulrich and Cooper, from the middle Ordovician of Tennessee. The width-frequency histograms prepared from a sample of R.rostrata has four distinct modes, three of which are bimodal. Walker and Parker used the identical histogram grouping as used in the study of T.retusa (i.e. 0.5mm), and therefore the modes can be analysed in a similar manners-

TABLE IX Analysis of the modes in width-frequency histogram of Rostricellula rostrata, Ulrich and Cooper. (data, in mm, is from Walker and Parker, 1976)

ANNUAL BIANNUAL YEAR INCREMENT MODE INCREMENT CLASS

2.75 1(a) 1.5 5.0 /4.2 1(b) 5.0 /7.75 2(a) 1.5 3.5 /9.25 2(b) 3.5 3(a) 3.0 12.7 3(b) 14.25 4 111

The similarity between the population structure of R.rostrata and T.retusa is remarkable. The separation between modes thought to represent the biannual settlement cohorts remains constant (column 3 in Table IX), and is identical to that determined for T.retusa (column 3 in Table III). The annual growth increment decreases gradually throughout life (column 1 in Table IX) just as in T.retusa (column 1 in Table III), although the increments involved are slightly different, and R.rostrata has a shorter life-span (4 years as compared to 7 years for T.retusa). R.rostrata is a species in which the maximum incremental increase in shell dimensions occurs laterally (i.e. in width), and therefore it is appropriate to the analyse the data from the width-frequency diagram plotted by Walker and Parker, as the resolution between modes is maximised. However the most significant feature of this comparison is the overall similarity in growth strategy and in the pattern and regularity of modes; the absolute increments involved are less significant as they are often controlled by environmental conditions and can vary considerably in neighbouring habitats (Subsection II.5.2.1.). Walker and Parker plotted a growth-curve for R.rostrata which, as in T.retusa, is most accurately described as approximately linear. Significantly Walker and Parker consider R.rostrata to be a 'later-stage' species (i.e. a well- established, stabilised species in equilibrium with its environment). All the available evidence suggests that the T.retusa population in the Firth of Lorne is also highly stable. Without more data it is not clear to what extent 112

Ordovician and Recent populations can be compared. However biannual reproductive_ strategy is generally accepted as being characteristic of marine invertebrates inhabiting temperate latitudes (so, as described above, is the fact that modes are discernible in the size-frequency diagrams). The paleogeographic reconstructions of Smith, Briden and Drewry .(1973) suggest that in the Cambrian/L.Ordovician the area from which R.rostrata was collected was situated between 25° and 30°S. of the equator, and was moving further south. Therefore it is certainly possible that the present conditions in the Firth of Lorne are similar to those prevailing at the time when R.rostrata was living, and that season variations similar to those recognised in the Firth of Lorne (temperature, food-supply, etc.) can be inferred. Such conclusions, however, can only be justified when more data are available, but it is certainly encouraging that such significant similarities can be demonstrated between Ordovician and Recent populations, separated as they are by perhaps 450 million years. The geophysical basis for Palaeozoic palaeogeographical reconstruction is generally accepted as being imprecise and unreliable, and it may be that widespread study of brachiopod growth strategies will prove a much more accurate method of delineating the extent of palaeoclimatic zones, especially if the differences between tropical and temperate-latitude growth strategies are as apparent from growth-line analysis as seems likely (Part II). 113

I.5. BIOLOGY OF T.RETUSA

I.5.1. LOPHOPHORE AND FEEDING

The lophophore, the food-gathering organ of brachiopods, is situated within the mantle cavity (Fig.l(a) in Appendix IV). The area enclosed by the brachiopod shell is divided into separate body and mantle cavities by mantle epithelium, with the only connection between them being via the mouth and the ducts of the mstaepbridia (Fig.l(a) in Appendix IV). Brachiopods feed by filtering food particles from sea-water drawn into the mantle cavity when the valves are open (and also, perhaps, by direct assimilation of dissolved nutrients). This filtering is carried out by the filaments of the lophophore which, when extended in the feeding position, divide the mantle cavity into discrete inhalent and exhalent chambers (Plate 6,A). All brachiopods are dependant on external currents for a constant supply of potential food particles, but the feeding currents within the mantle cavity are primarily caused by the beating of lateral cilia situated along the lophophore filaments (Williams, 1965). Food particles, having been trapped by the frontal cilia on the filaments as they are drawn from the inhalent to the exhalent chamber, are moved down to the food-groove (Fig.l(b) in Appendix IV) and transferred to the mouth in mucus-bound strands (Plate 5,A). Disarticulation of the valves of living specimens of T.retusa can be accomplished without damaging the lophophore, thereby allowing detailed observations on the feeding process as the lophophore of a disarticulated specimen soon starts 114

EXPLANATION OF TEXT-FIG. 11.

Showing progressive development and eventual unification of the descending branches of the lophophore-supporting brachidium in juvenile specimens of T.retusa. At a much later stage of life ascending branches develop from the crura and unite medianly to form a complete brachial 'loop', (see Fig.1,B). 115 116

to feed when placed in a dish of sea-water (Plate 5,D-F; Plate 6,A-C). With the exception of those formed during the earliest stage of lophophore development (the trocholophe - see Plate 5, D-E), the filaments occur in pairs, and a single row consists of alternate inner (adlabial) and outer (ablabial) filaments. The trocholophous filaments are un- paired. The adult lophophore of T.retusa is a plectolophe (Plate 6,A) and consists of two distinct lateral lobes composed of two parallel rows of paired filaments (Fig. 1(a) in Appendix IV), and a well developed median spiral with a single row of paired filaments (Plate 6,A). Inhalent feeding currents occur along both lateral margins of the shell; the exhalent current is situated antero-medianly. Rapid inward flexures of the tips of the filaments enhance the current produced by the lateral cilia, and presumably direct the potential food particles onto the frontal cilia. T.retusa, in common with all brachiopods, is incapable of distinguishing between nutritious and non-nutritious particles, and indiscriminately traps all suitably sized particles. -Large particles such as sand grains will, however, be detected and rejected. Once a large particle impinges on a filament the frontal cilia reverse their direction of beat, moving the particle to the tip of the filament rather than to the food- groove. The rejected particle, often enmeshed in mucus strands (Plate 5,B,C), is then passed from filament to filament towards the margins of the shell where it is eventually ejected, as a pseudofaecal pellet, by the snapping of the valves. The fact that the feeding activity of the lophophore is dependent on some form of circulation in the surrounding 11? sea-water can be demonstrated by allowing the water in the dish containing the disarticulated specimens to become stagnant. Under such conditions the lophophore will cease feeding and curl up. Such a reaction indicates an ability to detect the presence or absence of particulate matter, which is confirmed by the fact that after several hours in a dish of constantly circulating sea-water the brachiopods will cease feeding, presumably as the majority of the available particulate material has been ingested. When circulation is resumed, or fresh sea-water added, feeding immediately recommences. The movement of faecal and pseudofaecal pellets along the filaments is rapid and highly co-ordinated, which would seem to imply that there is good nervous control of the activities and movements of the filaments. However the nervous control of the lophophore is in fact very tenuous, as was clearly demonstrated by the fact that a lophophore, when separated from the rest of the body tissues during a laboratory experiment, continued to feed for over 52 hours despite the fact that the brachial nerves had been severed. This indicates that the filtering activity is 'instinctive', and even the cilia along a filament will continue to beat for several hours when separated from the lophophore. Non- innervated ciliary activity has been recognised in many invertebrates; it is thought that the cells are themselves electrically coupled to one another, and that stimuli pass from cell to cell without the need for nervous conduction (Prosser,

1973). Digestion occurs within the lobes of the digestive 118

diverticula (plate 4,C). These finger-like lobes are situated around the stomach of T.retusa, and are connected to it by a series of ducts. The alimentary canal is a simple U-shaped tube, with the oesophagus connecting the mouth to the relatively inflated stomach, which opens into the blind intestine (Fig.1(a) in Appendix IV). Particulate matter is drawn back and forth from the stomach into the lobes of the digestive diverticula, by the rhythmic muscular pulsations of the lobes themselves. The periodicity of these pulsations has been shown to vary at different stages of the feeding cycle of the inarticulate brachiopod Lingula unguis (Linnaeus), (Chuang, 1959). Even within the stomach there is no sorting of nutritious from non-nutritious particles, and all ingested material is sucked into the lobes of the diverticula whether it is digestible or not (Chuang, 1959; Owen, pers comm.,in Steele-Petrovic, 1976). Digestion is accomplished both by the absorption of particulate material and direct assimilation of nutrient-rich fluids produced by enzyme activity within the digestive diverticula (Owen, pers comm., in Steele- Petrovic, 1976). Once digestion has occurred, waste materials are ejected back into the stomach, and are moved by peristalsis into the blind intestine. During a laboratory experiment some sand grains were inadvertantly dropped into the mouth of a disarticulated specimen of T.retusa. These grains were clearly visible through the walls of the blind intestine approximately 45 minutes later. The grains were being rapidly rotated in an anticlockwise direction by ciliary action. This seems to confirm the belief that the waste products of digestion 119

are moved by peristalsis into the blind intestine, where they are rotated into mucus-bound faecal-rods (Rudwick, 1970). Whilst not visible in T.retusa because of the surrounding digestive diverticula (Fig.l(a) in Appendix IV), faecal rods are also thought to form within the stomach (Steele-Petrovic, 1976). Feeding and digestion will therefore continue until the stomach and blind intestine are clogged by waste materials in the form of mucus-bound faecal-rods. As T.retusa has no anus, feeding and digestion must obviously cease at this stage, and the faecal rods are moved by anti-peristalsis back up the oesophagus, into the mantle cavity via the mouth, and ejected from the shell margin. The feeding and digestion cycle can, therefore, be summarised as follows:- (1) shell opens; (2) particulate material is trapped by the lophophore and moved to the mouth; (3) digestion commences as particulate matter reaches the stomach and is sucked into the diverticula; (4) as digestion proceeds, the waste material is moved into the blind intestine and rotated into faecal-rods; (5) feeding, digestion, and faecal-rod formation continue simultaneously until blind intestine and stomach are clogged by waste material; (6) feeding and digestion cease, faecal rods moved by anti- peristalsis back up the oesophagus and into the mantle cavity; (7) movement of faecal pellets to shell margin by filaments; (8) ejection of faecal pellets by snapping of the valves, often associated with the rotation of the brachiopod around its pedicle; (9) shell re-opens, and a new feeding cycle

begins. Rudwick (1970), and Gurr and Penn (1971), observing 120

living brachiopods in aquaria, noted feeding cycles with an average duration of approximately 15 minutes. A slightly longer duration was recorded by Savage (1972). In practice, however, there are so many variables affecting the rates of feeding and digestion processes, that these values are virtually meaningless. Obviously the duration of the feeding cycle will depend on the current velocity, and on the amount of particulate material carried in suspension. In addition changes in temperature are known to affect the rate of all metabolic activities (Section I.3.3.), which will obviously affect the duration of both the feeding and digestive processes. The rate of feeding and digestion may vary in specimens of different size, and perhaps even in specimens from slightly different habitats. These factors will vary from season to season, and perhaps even from day to day - so, therefore, will the duration of the feeding and digestive cycles. A direct comparison of the feeding cycle duration of both adults and juveniles under identical environmental conditions would be possible both in aquaria and in nature (using underwater television to observe the deep-water population in the Firth of Lorne; or by direct observations by divers on the shallow- water population near Rabbit Island--Stn.2 in Table I and Fig.2). It seems likely that the duration of an individual's feeding cycle is extremely variable, depending on the severity and frequency of various localised disturbances, and on prevailing environmental conditions. McCammon and Reynolds (1972), using radioactive glucose, demonstrated that Terebratalia transversa (Sowerby) can absorb dissolved nutrients through the lophophoral tissue. Whilst 121

many other brachiopods may have a similar ability, it is unlikely that direct assimilation of dissolved nutrients represents more than a minor proportion of the total amount of nutrients utilised by a brachiopod in nature. Brachiopods can be maintained in aquaria by feeding them on dissolved nutrients (McCammon, 1972; this study - Section I.2.2.), although under such unnatural conditions T.retusa did not grow. The lophophore may also have an important respiratory function, as Rudwick (1970) suggests, and gaseous exchange_ between coelomic fluid and the surrounding sea-water is likely to occur via the lophophoral tissues, and indeed via most body tissues which are in contact with the sea-water. The nature of the food utilised by T.retusa remains unknown. As all brachiopods indiscriminately ingest all suitably sized particles, the content of their intestine will not necessarily indicate the nature of brachiopod food, and those particles which can be identified are more likely to be undigestible waste. Apart from organic particles and dissolved nutrients, it has been suggested that brachiopods feed on (a) colloidal particles absorbed onto the surface of ingested silt particles; (b) bacteria; and (c) algae. Attempts to determine the enzymes present in the intestines of brachiopods (and thereby to determine the nature of the food utilised by brachiopods on the basis of the substrates that these enzymes will act upon), have not proved conclusive. It is likely that brachiopods feed both on a wide range of organic particulate material and also by direct assimilation of dissolved nutrients (Zezina, 1976). When feeding in aquaria, the anterior-posterior axis 122

(A-P axis) of T.retusa was commonly aligned parallel to the current direction (i.e. A-P angle = 0). The preferred feeding orientation in nature is unknown. The advantage of the A-P = 0 orientation is that the current will enhance the exhalent feeding current of the brachiopod, thereby ensuring that previously filtered sea-water is not recycled by the inhalent feeding current. However LaBarbera (1977) pointed out that in such an orientation the inhalent currents are in fact opposed by the effect of viscous entrainment (i.e. the water within the inhalent chambers tends to be sucked out of the shell by the drag-effect of the current moving past the lateral margins of the shell). LaBarbara suggests that it would be more beneficial for brachiopods to be orientated with the A-P axis at 90° to the flow direction of the prevailing water current, as both the exhalent feeding current and one of the lateral inhalent feeding currents will be directly enhanced. LaBarbera claims to have observed such an orientation both in aquaria and in nature. However it seems likely that the orientation of brachiopods whilst feeding is dependant on the velocity of the prevailing water current. This fact seems to be confirmed by experiments with disarticulated specimens of T.retusa in aquaria. When a current of relatively high velocity was directed laterally (equivalent to an A-P angle of 90° to the water current) the filaments on the exposed lateral lobe of the lophophore were disturbed, ceased feeding, and curled up. The effect of a current of similar strength directed parellel to the A-P axis was less pronounced, and the majority of the lateral filaments continued to function normally . 123

although some of the ventral filaments of the median spiral of the lophophore were disturbed (in non-disarticulated specimens these would be protected by the ventral valve). Therefore under low current conditions the A-P = 90° orientation may be preferred, whilst at higher current velocities the A-P = 0 orientation combined with a reduced anterior gape may allow the brachiopod to continue feeding without risking damage to the filaments. T.retusa, when re- opening its valves, does so cautiously, as if 'testing' the prevailing current strength and turbulence before taking up a feeding position. However there is no preferred orientation of the brachiopods attached to the boulders in Lyttelton Harbour (New Zealand), presumably because the specimens are so closely packed; under such conditions it is the orientat-, ion of the neighbouring brachiopods which determines the feeding orientation of an individual, rather than the current direction or velocity. 124

I.5.2. REPRODUCTION

I.5.2.1. INTRODUCTION

The long-term success of any animal population ultimately depends on the success of its reproductive activities. In most brachiopods the sexes are separate, and reproduction is achieved by synchronised release of sperm and ova. When fully developed, the gonads represent a considerable proportion of the total body weight of a brachiopod, and a single female can release as many as 20,000 ova during a single spawning period, and several hundreds of thousands throughout its entire reproductive life. Fertilisation and cleavage is followed by a pelagic larval stage which represents the only significant means of geographical dispersion. During the pelagic stage the danger of predation is great, and only a minute proportion of fertilised ova survive to the post-larval stage. The effect of this predation is somewhat reduced, in articulate brachiopods, by restricting the duration of the pelagic stage, thereby limiting the dispersal range of a single generation. The duration of the pelagic stage may be further restricted by the brooding of embryos to an advanced stage of development within the mantle cavity, and such a phenomenon may be more common in living brachiopods than is generally realised,

The pelagic larval stage of some inarticulate brachiopods is of much longer duration than that of articulates; this difference is almost certainly due to the fact that inarticulates, unlike the articulates, begin to secrete a 125 protective skeleton whilst still in the pelagic larval stage. T.retusa is dioeceous, although the determination of sex is only possible in specimens which are greater than 8mm in length, and in which the gonad tissues are well developed. The female gonad is normally orange, yellow or reddish in colour, and other body tissues, especially those of the lophophore, are commonly similarly coloured when the gonads are well-developed. In contrast, male gonadal tissues are white or cream in colour. The texture of the gonadal tissues is another useful criterion in attempting to distinguish between the sexes as the sperm occurs in undifferentiated cloudy masses, whilst individual ova can be distinguished from a relatively early stage of their development. The ratio of males to females is approximately 1:1; a total of 342 adult specimens could be sexed in a sample collected on 26th October 1977, 181 of which were male and 161 were female (M:F = 1.12:1).

I.5.2.2. GONAD DEVELOPMENT

The developmental state of the gonads in specimens of T.retusa can readily be determined by separating the valves; gonads develop primarily within the mantle canals, and are clearly visible through the mantle epithelium (Plate 4,F). For some time prior to spawning the outline and colouration 126

of the gonad can be seen even through the shell (see frontispiece) allowing determination of sex and of the state of gonad development without separating the valves, which can only be accomplished by severing the adductor and diductor muscles. In T.retusa the gonads develop within the lateral portions of the mantle canals (the vascula genitalia) of both valves, and also extend posteriorly into the body cavity. The individual gametes develop along narrow, interconnecting genital canals (Plate 4,F), which are anchored to the outer epithelium by membranes. Columns of tissue, situated in the interstices between the genital canals and attached to both inner and outer epithelium, prevent the gonad from being damaged or crushed between the two layers of tissue. Fur- ther protection for the gametes is provided by calcareous spicules which, although present in many areas of the body wall of T.retusa, are particularly numerous and well- developed above the gonads (Plate 4,F). The gonadal pits which have been recognised on the internal shell surfaces of some fossil brachiopods are likely to represent the points of attachment of the supportive columns of tissue (which separate the inner and outer epithelium) rather than the points at which the gonad itself is attached (as Rudwick (1970) suggested). It is not known if these columnar tissues are capable of rhythmic contractions, but if so this feature would facilitate the movement of gametes to the metanephridia during the spawning season. The nature of these genital canals is in some doubt. Hancock (1859) considered them to be connected posteriorly 127 to the 'heart' (see Fig.1 in Appendix IV), and to be the arteries of a circulatory system. This in effect would represent a secondary circulatory system, apparently open- ended, within the main circulation of the body cavity. The advantages of such a system would be that the flow of essential nutrients and oxygen to the developing gametes would be enhanced. In T.retusa the gametes are seeded along the length of the genital canals, and remain attached to them until released during the spawning period. However Morse (1902) challenged Hancock's conclusions, stating that even after prolonged observations he was unable to detect any rhythmic contractions of the so-called 'heart', and concl- uded that the 'secondary circulatory system' was not linked to gonad development. Morse believed that the genital canals were extensions of the ilio-parietal mesentery. Preliminary microscopic examination of the genital canals suggested that they were hollow, but precise determination of their form and function must await a detailed anatomical and histological study. One of the difficulties of studying the brachiopod circulatory systems is that it is necessary to separate the valves to examine the body tissues, and such a process results in the rupture of the body wall and the draining of the coelomic fluids. This may well explain the apparent lack of contractile movements in the 'hearts' examined by Morse. Initially it was hoped to develop a quantitative method of comparing the gonadal development stages of specimens from different samples. However it became apparent that in any one specimen the size of the ova and sperm was often 128 very variable, as some portions of the gonad were at a more advanced development stage than others. The situation was further complicated by the presence of some mature unspawned gametes from a previous development cycle (Plate 4,F). For these reasons neither the maximum or minimum size of the gametes within an individual provides a meaningful measure of the state of the gonad for comparative purposes. Many of the first seeded gametes achieve a size close to their maximum size well in advance of the actual spawning season, which effectively rules out any size measurements as a useful indication of the state of gonad development. The less desirable, but nevertheless widely used, practice of using arbitrary terms to describe_vārious_dēvelopment stages was adopted. The terms selected in this study were undeveloped (ā spent), partially-developed, well-developed, and fully-developed; they are rather loosely based on the quantity of gonad tissue present. Undeveloped and fully- developed, the two extremes, are the most easily defined, as in undeveloped gonad the genital canals are bare (Fig.4,F), whilst when fully-developed the interstices between the genital canals are almost completely filled with gametes. The intermediatory stages, partially-developed and well- developed, are less easily defined, and indeed the boundaries between the four stages are gradational and their definition will vary from person to person. However these terms do allow the stage of gonad development to be described in simple, widely-understood terms, and are therefore valuable. Individual ova and sperm were described as being mature (i.e. capable of being fertilised or of fertilising) or 129 immature. The criterion used was absolute size; the average maximum diameter of ova being 180 microns, and the maximum length of sperm (including tail) being on average 30-40 microns. It is not clear if maximum size necessarily indicates that the gametes are mature in the strict sense of the word. The apparently mature gametes which are discernible at an early stage of the development cycle may well undergo significant internal development for some time after reaching their maximum size. A detailed histological study, which was beyond the scope of this project, would be the only method of determining the precise stage at which gametes become mature. Indirect evidence does suggest however, that maturity is achieved well in advance of spawning. Mature sperms can be recognised as they are motile, but in nature this condition is of very short duration, and is only initiated immediately prior to spawning. Non-motile sperm, which by definition were mature, were removed from several specimens at different times of year. On several occasions, when observed under a high-powered microscope, these sperm became motile, presumably because of the heat from the microscope light. The fact that this feature was observed well in advance of the natural spawning season, indicates that sperm become mature at an early stage and lie dormant within the gonad until activated by a certain critical temperature in the surrounding sea-water. The gonads of T.retusa pass through two full developmental cycles per year, the culmination of each being one of the biannual spawning events. It is an interesting feature that the development cycle initiated during the winter months 130

appears to be of shorter duration than that initiated during the summer. However this feature is not thought to be of great significance, as the precise timing of spawning is controlled by environmental conditions rather than the time of maturation of the gonads. There is no readily discernible difference in the number of gametes produced in each of the biannual development cycles. It is possible that the longer summer development period may result in the number of gametes released in autumn being greater than in spring, but there is no practical method of checking this. The data on gonad development has been derived from the examination of the gonadal tissues in at least 20 specimens from each of the samples collected between March 197? and March 1979. There is considerable variation in the gonadal development stage of specimens from a single sample; in a sample collected in March 1977 the gonads of those specimens examined were either undeveloped, partially developed, or well-developed, and some specimens had mature ova. One of the most interesting aspects of these gonadal development cycles is that T.retusa can apparently build up gonadal tissues in both winter and summer with equal ease. In many other benthic invertebrates the development of gametes can be directly related to the increased availability of food during spring and summer months (in temperate latitudes). The fact that gonad development in T.retusa in not restricted to these two seasons can be explained in two ways. Either the quantity of food available during the winter months is not significantly lower than during the summer months, or T.retusa can store nutrients when they are abundant for 131

future use. The first explanation would seem to be untenable, especially at the temperate latitudes at which T.retusa lives. In such locations the planktonic bloom in spring is widely- recognised and generally accepted as being characteristic of temperate latitudes, (a secondary, though less pronounced, planktonic bloom occurs insautumn). Admittedly the exact nature of the food utilised by brachiopods remains in some doubt, and it is possible, though highly unlikely, that there is less seasonal variation in the abundance of other potential brachiopod food materials than in the abundance of plankton. However the plankton bloom has a pronounced effect on the productivity of the entire marine biosphere, and it is almost certain that the increased biomass during spring and autumn will result in a distinct seasonal variation in the quantity of the food available to T.retusa. It seems likely, therefore, that T.retusa is indeed capable of storing nutrients during the spring and summer when they are abundant, and of utilising them during the winter as required. In many bivalves surplus nutrients are stored in the form of body tissue, and certain organs become distented during spring and summer, and shrink during autumn and winter as the tissue is converted back into nutrients. This process is analagous to the storage of excess food in the form of fat in the mammals. Such a system can only be of limited application in brachiopods, however, as the body occupies such a small proportion of the volume enclosed by the valves of the shell (the mantle cavity occupies approx-

imately 80% of the internal volume of T.retusa). However 132

T.retusa has numerous fine evaginations of mantle tissue, called caeca, which occupy hollow cylindrical tubes (the endopunctae) within its shell, and these are the most likely storage centres, as has been suggested by Owen and Williams (1969). The implications of such a function, both for all brachiopods possessing endopunctae and for those which do not, are discussed in Appendix III. As mentioned above there are only two short periods when developing gonads are absent from the gonads of T.retusa. This fact underlines the danger of attempting to interpret the annual breeding behaviour of any brachiopod species on the basis of the examination of the state of gonad development from few samples. Such an interpretation is impossible until the entire gonad development cycle has been observed. Without this information the relative stage of development cannot be determined - what one observer describes as a well- developed gonad may in fact be a relatively early stage. In addition the very significant feature of biannual spawning would obviously be impossible to recognise by examining the gonads of the specimens from a single sample.

1.5.2.3. SPAWNING SEASON

The timing of the natural spawning seasons of T.retusa is evident from the gonad development cycles described above. Further confirmatory evidence for the biannual spawning strategy was obtained from the regular dredged samples, as 133

the surfaces of all potential brachiopod substrates were examined in great detail to determine if newly-settled brachiopods were present (i.e. less than lmm in length). There is no doubt that T.retusa spawns during late autumn and late spring. Benthic sampling contined for over two years, encompassing four spawning seasons, and the regularity of all aspects of the biannual spawning events is striking. The actual spawning process of T.retusa has been observed in the laboratory. A number of specimens with fully- developed gonads were selected from a sample collected in early December,1978, and placed in a dish of sea-water. Spawning was induced by rapid controlled variations of the sea-water temperature, and by the addition of motile sperm to the sea-water in the dish. Rapid temperature fluctuation-is- one of the most widely used methods of inducing laboratory spawning in invertebrates (P. Redfern, oral comm. 1978). Motile sperm were added because it was suspected that their presence had the effect of stimulating brachiopods to spawn. This had become apparent during experimentation with Terebratella inconspicua (Sowerby) in New Zealand, when it was noticed that males were the first to spawn, and that nearby specimens commenced spawning shortly after the sperm had been drawn into their mantle cavities by the feeding currents. This reaction is presumably due to a chemical stimulus, perhaps from hormones secreted along with the sperm. In T.retusa the ejection of gametes from the mantle cavity is accomplished by rapid snapping movements of the valves, often associated with rapid rotational movements of 134 the brachiopod around its pedicle. Sperm is ejected in a mucus-bound cloud, which remains in suspension in the sea- water. The sperm cloud is apparently of viscous consist- ancy, will retain its shape for some time, and will adhere to brachiopod setae or other substances with which it comes into contact. The sperm, although motile, cannot swim against the current, and are carried along by it. The ova, once ejected, settle in dense clusters on the substrate close to the parent. Only a few of the specimens in this laboratory experiment actually spawned. The spawning behaviour of many invertebrates in aquaria is known to be atypical, and it is not known to what extent the spawning activity observed in this experiment was a response to the stress imposed by the rapid temperature fluctuations and the other abnormal conditions experienced under laboratory conditions. The spawning event in nature is of relatively short duration. This is evident from the fact that the majority of specimens collected on 5th May 1977 (Fig.7,A) had fully- developed gonads, whilst in a sample collected approximately 3 weeks later (Fig.7,B) the gonads were predominantly undeveloped. The large number of newly-settled brachiopods in the latter sample confirms that larvae had settled during the previous 3 weeks. This implies that the reproductive process, from spawning through to spatfall, is accomplished within 3 weeks. To check such a conclusion motile sperm and mature ova were teased from specimens of T.retusa in the laboratory, and mixed in a dish of sea-water. Several of the ova became fertilised, and free-swimming larvae were 135 observed within 5 days. These pelagic larvae were at an advanced stage of development, and the presence of a third segment indicated that settlement was imminent. Unfortun- ately, it was impossible to maintain a desirably low and constant temperature during this experiment. Increasing temperature is known to cause an increase in the rate of larval development in many other invertebrates, such as bivalves and echinoderms, and undoubtedly brachiopod larvae will be similarly affected. However in the experiment with T.retusa it is unlikely that the rate of larval development was affected by a factor of more than 50% (temperatures were never more than 5°C above natural temperatures). This suggests that the time for development from fertilised ova to settled larvae in nature is of the order of 7 days. It is clear that the timing and duration of the spawning seasons of T.retusa can be directly related to ambient sea-water temperatures. In both spring and autumn spawning is initiated at temperatures of between 10°C and 11°C (Fig. 4., A) . Both of the biannual spawning seasons occur at times when the sea-water temperature is changing relatively rapidly when compared with other times of the year, and this would explain the short duration of the spawning events. The spawning of T.retusa is obviously inhibited by temperatures which are either higher or lower than the critical temperature. There is therefore a relatively short period of time during which the sea-water temperature is within what appears to be the narrow range within which spawning is initiated. Because of this the precise timing of the spawning season will obviously vary slightly from year to 136 year, depending on the temperature conditions. For example the unusually prolonged cold winter of 1979 resulted in the March sea-water temperature being much lower than indicated in Fig.4,A (6°C in 1979 as compared with approximately 8°C in 1977 and 1978), and it seems probable that the spring spawning will occur slightly later in 1979 than in previous years. Published accounts of the spawning seasons of other Recent brachiopods are often based on few samples, and are frequently imprecise or even contradictory. However biannual spawning strategy has been recognised in two other species from the N.Atlanticg- Terebratulina septentrionalis(Couthouy) spawns in the spring and autumn in the Bay of Fundy, Canada, (based on length-frequency curves in Noble, Logan, and Webb, 1976), and Crania anomala (Miler), an inarticulate brachiopod commonly found along with T.retusa in the Firth of Lorne mussel beds,_ spawns in April and November (Rowell, 1960). Specimens of C.anomala collected from the Mediterranean also had developed gonads in November and May (Joubin, 1886). Platidia davidsoni (Eudes-Deslongchamps) collected from off the coast of N. France, had well-developed gonads in July/ August and February (Atkins, 1959). In the temperate latitudes of the Southern Hemisphere a similar biannual reproductive strategy has been recognised in a living brachiopod. A detailed study of Terebratella inconspicua (Sowerby) from New Zealand by Doherty (1976;1979) showed that spawning occurred during the southern spring and autumn. The failure to recognise this feature in previous studies of a population of T.inconspicua from an intertidal 137 rock-pool near Christchurch (i.e. Percival, 1944) may indicate that the conditions within this pool are so atypical as to restrict the reproductive activity to a single event per year; alternatively it is possible that the larvae of T.inconspicua and Pumilus antiquatus, Atkins, have been confused. P.antiquatus also occurs in the rock pool, and it has been thought to spawn during the southern spring (Rickwood, 1968), whilst T.inconspicua was formerly believed to spawn only in the autumn (Percival, 1944; Rickwood, 1968). However it has been pointed out that it is impossible to distinguish between juvenile specimens of T.inconspicua and P.antiquatus (Atkins, 1958), and it seems likely that their larvae are also indistinguishable. It is possible, therefore, that both species spawn biannually, and certainly specimens of P.antiquatus collected in autumn had well- developed gonads (Atkins, 1958). Virtually nothing is known of the spawning activity of articulate brachiopods from tropical or polar regions, where seasonal variations in environmental conditions are either less pronounced than in temperate regions, or totally absent. However the breeding seasons of two predominantly tropical inarticulate burrowing brachiopods have been accurately determined. The study of these two brachiopods - Lingula unguis (Linnaeus) by Chuang (1959) and Yatsu (1902), and Glottidia pyramidata (Stimpson) by Paine (1963) - has clearly illustrated the effect of latitudinal variations in environmental factors on the breeding behaviour. Spawning continues throughout the year in populations of L.unguis from Singapore (Chuang, 1959) at a latitude of 1°N.; the same species has 138

a summer spawning season of between two and three months around Japan (Yatsu, 1902) at a latitude of approximately 35°N. G.pyramidata also spawns throughout the year off the coast of southern Florida, but further to the north breeding is restricted to a nine month period (Paine, 1963). As with many other marine organisms, sea-water temperature is thought to be the main environmental factor which controls the duration of brachiopod spawning periods. It has been determined that spawning is initiated in G.pyramidata at temperatures of between 20°C and 22°C, and the shorter spawning season of the northernmost populations of this species has been attributed to the fact that the sea-water temperatures drop below this critical value for three months during winter (Paine, 1963). Similarly there is a good correlation between spawning and temperature in the articulate brachiopod Pumilus antiquatus, Atkins, which spawned at temperatures of between 8°C and 9°C in Otago Harbour, New Zealand (Rickwood, 1968).

I.5.2.4. FERTILISATION

For successful reproduction, mature ova and sperm must be brought into close proximity, in order that the former may be fertilised by the latter. The sperm of T.retusa are motile but, as described above, laboratory experiments indicate that they are weak swimmers, and are carried along by the prevailing current. The ova are entirely non-motile.

T.retusa is therefore dependant on the prevailing current 139 to carry the cloudy suspensions of sperm to the ova. An unfertilised ovum is a strongly flattened sphere with a translucent outer membrane through which the large centrally- situated yolk sac is clearly visible (Plate 4,E). A newly fertilised ovum can be recognised by its almost perfect spherical shape, and by its opaque outer membrane. During the spawning process the gametes, having been released from the genital canals, are moved by ciliary action through the body cavity to the metanephridia (Fig.1,A in Appendix IV). These organs function as gonadophores, eject- ing the gametes from the body cavity to the mantle cavity. Observations on some specimens of T.retusa collected during the natural spawning period showed none of the ova found within the metanephridia were fertilised and,.furthermore, there is no indication of sperm entering the body cavities of females, allowing fertilisation prior to the ejection of ova into the mantle cavity. Fertilisation must, therefore, occur either within the mantle cavity, or in the sea-water surrounding the specimens. In the laboratory spawning experiments described above it was impossible to determine if fertilisation did indeed occur within the mantle, or when the ova where lying on the bottom of the dish. It would seem likely that a proportion of ova are fertilised within the mantle cavity, and that others are fertilised as they lie on the sea-floor. The proportion of the total number of spawned ova which are actually fertilised is probably small; only three pelagic larvae developed from the thousands of ova shed in the laboratory experiments. 140

I.5.2.5. LARVAL DEVELOPMENT

Attempts to collect the naturally-occurring pelagic larvae of T.retusa were unsuccessful. Plankton samples were collected using a fine mesh plankton net, at both the surface and at a depth of approximately 100 metres. Deeper trawls were impossible because of the danger of the net becoming entangled with one of the rock pinnacles which are common in the Firth of Lorne. As described above the pelagic larval stage is of short duration, and the highly-synchronised spawning event occurs within a three week period. It is possible, therefore, that the plankton samples were collected at a time when pelagic larvae were not present in significant numbers, although without large daily samples throughout the expected spawning period it is impossible to determine the exact timing of the natural spawning event. Logistics and possible over-sampling of the population precluded any comprehensive plankton sampling. Alternative explanations for the absence of pelagic larvae in the plankton samples are that they remain close to the sea-floor, or that they are brooded. The implications of brooding are discussed below. As so few of the ova spawned in the laboratory became fertilised, it was considered undesirable to subject them to further stress by studying their development for long periods of time as the increased temperatures, from the microscope light, would be likely to disturb the development process. It was thought to be more important, in the context of the present study, to become familiar with the gross external morphology of the larvae of T.retusa, rather than risk 141 killing the embryos by prolonged study of their development stages under the microscope. In the event only three embryos survived the abnormal laboratory conditions, and even these died before settling. The experiment did show that larvae can be reared in the laboratory, and that the embryology of T.retusa can be readily studied if care is taken to control any fluctuations in environmental factors such as temperature, current velocity, etc. When first observed, cleavage of the fertilised ova was already well advanced. As sperm had been added on several occasions, in an attempt to obtain a greater number of fertilised ova, it was not known how long these ova had been fertilised. The actively swimming larvae of T.retusa are mushroom-shaped, with one transversely-oval segment (the future mantle) and one longitudinally-oval segment (the future body). The connection between these two segments is not rigid and while swimming the transversely-oval segment pivots actively from side to side about the other. Shortly before settlement a third segment develops (the future pedicle). From the few observations possible it seems that the larval development stages of T.retusa are essentially similar to those described in T.septentrionalis by Morse (1873). Certainly the pelagic larvae of the two species are very similar in size, shape, and activity. The possibility that developing embryos are brooded within the mantle cavity of T.retusa cannot be discounted, especially in the light of the results from a recent study of the ecology of T.septentrionalis from the Bay of Fundy,

Canada, (Webb, Logan, and Noble, 1976), which indicated that 142

the brooding of embryos to an advanced stage of development is common practice in this species. This brooding behaviour is of particular significance as no special brood pouches are developed to house the embryos, and for this reason the brooding activity of T.septentrionalis has been overlooked in previous studies (i.e. Morse, 1873). In T.septentrionalis the brooded embryos are held between the dorsal filaments of the median spiral of the lophophore and the body wall, within the mantle cavity. The difficulty in recognising this form of brooding activity is partially due to the great dist-

urbance caused by the collection methods; brooded larvae., if present within the mantle cavity of T.retusa, would almost certainly be released from the shell because of the disturbance caused by the dredging operations, and by the subsequent transportation to the marine laboratory. The advantage of brooding is that a greater number of the embryos will survive to the settlement stage. Webb, Logan, and Noble (1976) found that the brooded larvae in T.septentrionalis were at an advanced stage of development, with well-developed pedicle segments, indicating that settlement was imminent. It is worth pointing out that the volume available for brooded larvae in the mantle cavity of T.retusa (i.e. between the body wall and the dorsal filaments of the median spiral of the lophophore) would be insufficient to hold all the ova shed by an individual. Obviously, therefore, even if brooding is common practice, a proportion of the released ova must be ejected into the surrounding sea-water. It will be difficult to determine if brooding is common 143

in the deep-water populations of T.retusa in the Firth of Lorne, which can only be sampled by dredging. However the shallow-water population (20 metres) discovered close to Rabbit Island (Stn.2 in Table I and Fig.2) would be ideal for such a study. Divers would be able to collect specimens in sealed containers, and even if brooded larvae were released because of disturbance, they would be retained within the containers.

I.5.2.6. SETTLEMENT

It is not clear to what extent brachiopod larvae are successful in distinguishing between favourable and unfavourable localities for settlement. A wide variety of substrates are utilised by T.retusa (Table II), and apparently the environmental setting of the potential substrate is more critical for the survival of the brachiopod than the composition or texture of the substrate. The mortality rate amongst recently settled brachiopods is known to be high (Doherty, 1979), and the settlement of larvae in unfavourable localities is likely to be a contributory factor. However, like many sessile invertebrates, the pelagic larvae of brachiopods may be able to delay settlement until a suitable substrate is found. It was once considered that the presence of an organic film on the surface of potential substrate was an essential prerequisite for settlement, but it is now known that some 144

larvae prefer a 'clean' surface. Perhaps brachiopod larvae can recognise suitable locations for settlement by analysing critical parameters; for instance the larvae may be sensitive to current velocity. The survival of a sessile invertebrate such as T.retusa is dependant on being situated in a current from which the vital food particles can be extracted, and it would certainly be advantageous if the larvae were able to recognise unsuitable locations where current velocities were either too low or too high. However brachiopod larvae do not appear to develop the complex sensory organs necessary for such a precise analysis of environmental conditions. Despite the overall dense settlement of brachiopods on the Firth of Lorne mussel beds, gregarious settlement of larvae is apparent, and individual mussels may have as many as 30 attached brachiopods. Some interesting work on the larvae of other gregarious sessile invertebrates suggests that larvae settle. in direct response to a chemical compound secreted by adults of that species. Crisp and Meadows (1962; 1963) were able to extract a compound called 'arthropodin' from the cuticle of barnacles which, when smeared on previously unattractive substrates, caused large numbers of barnacle larvae to settle. Therefore it is possible that the brachiopod do not actively analyse the environment, and that the gregarious settlement behaviour is the result of a similar chemical recognition mechanism. Larvae would settle when they recognise the diagnostic chemical compound which is unique to T.retusa; this chemical may be present both in the body tissues of T.retusa and on the surface of the substrate (after having been released from the pedicle tissues). 145

It has been demonstrated that 'arthropodin' will only act as a stimulus for barnacle settlement when it is bound by physico-chemical forces to a surface such as body tissue or substrate. Solutions of 'arthropodin' are entirely ineffect- ive - an important characteristic in a compound whose main function is to promote settlement. Such a feature is not surprising, as a compound will have a similar orientation no matter what substance it is bound to, and yet may have completely different characteristics when in solution. Simil- arly, the ability to recognise a diagnostic chemical compound is not necessarily an advanced phenomenon, and the recognition process may be analogous to the mechanism by which antibodies are capable of recognising the precise antigen they are des- igned to neutralise, (Crisp, 1976). Such a settlement promoting system is both simple and efficient - simple because there is no need for the development of complex sensory mechanisms to analyse the environment, and efficient because the larvae are more likely to settle on substrates already colonised by many brachiopods, and which, presumably, are ideally- suited for brachiopods. The result of such a process in the Firth of Lorne would be the settlement of a large proportion of the T.retusa, larvae close to the already-attached post-larval specimens, with a much smaller proportion settling on uncolonised mussels (perhaps after failing to recognise the chemical stimulus for settlement within the time limits of the pelagic stage). This latter phenomenon must occur, as the mussels have a life-span of approximately 20 years, and juvenile mussels must be colonised as they grow to maturity and replace dead 146

specimens. Such a feature would result in a proportion of the larvae settling on unsuitable substrate and dying, but this is of little significance as the proportion of the total number of larvae which perish as a result is likely to be small, and it is obviously vital for the survival of the population that new substrates are colonised. The colonisation of new substrates is, of course, an important feature in the process of geographical migration. Some intertidal brachiopod species appear to sensitive to light intensity during their pelagic stage (i.e. Paine, 1963) and, being photonegative shortly before settlement, they tend to settle in shaded locations, such as the under- surfaces of the boulders in the Lyttelton Harbour rockpool. Such a phenomenon is common in many groups, such as sponges, corals, and bryozoans; the larvae of the bivalve mollusc Mytilus edulis, Gray, which is also photonegative immediately prior to settlement, usually settles with its anterior pointing away from the light (Crisp, 1976). Such a strategy is desirable in intertidal and shallow subtidal habitats as it reduces the risk of dessication or over-heating due to direct exposure to sunlight. Adult brachiopods from intertidal habitats also tend to be photo-sensitive, and will snap their valves shut in response to sudden changes in light intensity (Rudwick, 1970). In complete contrast, however, T.retusa is completely insensitive to light, presumably because light intensities are low at the depths inhabited by the specimens observed during this study (i.e. 180 metres). It would seem unlikely, therefore, that light intensity is an important factor in controlling the larval settlement 147

behaviour of T.retusa. Newly-settled T.retusa are thought to become attached to their substrate by means of a sticky substance secreted from the tip of the pedicle. As development proceeds the distal portion of the pedicle divides into a variable number of rootlets which bore into the surface of the substrate (Plate 4,B). The boring capability is presumably due to a chemical compound secreted by pedicle tissues, although the nature of this compound has yet to be determined. It has been suggested that the boring of the rootlets into a living molluscan substrate is a two stage process:- firstly an initial stage during which organic compound(s) are secreted to attack the organic matrix of the molluscan shell, and a secondary stage during which different compounds are secreted to dissolve the inorganic residues (Mackay and Hewitt, 1978). The density of settlement of brachiopod larvae on the Firth of Lorne mussel beds is striking. The number and lengths of all brachiopods attached to each mussel in the 24th May 1977 sample was recorded. The brachiopods were assigned to year-classes as in Table IV, with newly-settled brachiopods (i.e. less than 1mm in length) representing the first year-class. The percentage of the total number of mussels in the sample which had brachiopods of each year- class attached was then calculated. First and second year- class brachiopods were attached to more than 50% of the muss-

els (Fig.5,A). The fact that fewer mussels has first year- class brachiopods attached than second year-class is almost certainly due to the fact that it is difficult to pick out minute brachiopods. From the trend of the curve in Fig.5,A 148 it is to be expected that 70% or more of the mussels actually had first year-class brachiopods attached to them. This represents an even greater proportion of the available mussel substrate, as they occur in dense clumps with the lower- most presumably less accessible to brachiopod larvae. The fact that the peaks representing successive settlement cohorts can be recognised in all samples collected during this study suggests that dense settlements are the rule rather than the exception. Large brachiopod populations occur nearby in the Sound of Mull (Fig. 2), but the prevailing currents will prevent a significant number of the larvae produced by this population from settling on the Firth of Lorne mussel beds, or vice versa. PART II

GROWTH OF RECENT AND FOSSIL BRACHIOPODS 149

īI.1. INTRODUCTION

Brachiopods grow by the accretion of new shell material secreted by peripheral mantle epithelium. At various stages throughout life the shell secretory processes are interrupted by environmental disturbances which are either localised or population-wide in their effect. The result of such a disturbance is a mantle regression, and ultimately the formation of a growth-line when normal shell growth is resumed. Growth-lines are preserved within the shell fabric and provide a record of the ontogenetic development. In addition, several brachiopod workers have considered it likely that growth-lines with various'periodicities develop predominantly as a result of regular disturbances (i.e. diurnal, annual - Williams, 1968; Rudwick, 1970), but the lack of any 'control data' on the growth rate and periodicity of growth-line formation in living' brachiopods has prevented the development of growth-line analysis into what is potentially one of the most precise and informative methods of palaeoecological reconstruction. Previous attempts to analyse the significance of brachiopod growth-lines were often disappointing because of the difficulty in distinguishing between growth-lines caused by irregular localised disturbances, and those formed as a result of regular disturbances affecting the entire population (see Section II.3.2.). Furthermore, virtually nothing was known of the mechanism of brachiopod growth prior to the comprehensive studies of Williams (see Chapter II.4.) who, using both scanning and transmission electron 150 microscopy, unravelled the complex sequential secretory activity of the epithelial cells, and developed a widely- applicable model of the brachiopod growth process. The Williams model of brachiopod growth strategy, combined with the results of the T.retusa study described in Part I of this report, has provided a basis for the detailed analysis of growth-lines in other living and fossil brachiopod species. In Part I it has been demonstrated that the analysis of growth-lines and size-frequency histograms provides detailed information on many aspects of the ecology and habitat of T.retusa. The logical extension of these results is to use growth-line and size-frequency histogram analysis in the study of living and fossil brachiopod populations which cannot be studied in their natural environment. Undoubtedly the analysis of brachiopod growth-lines has greater palaeontological potential, as size-frequency histograms, although very useful, are often problematical because of factors such as post-mortem transportation and preservational bias. The great potential of growth-line studies lies in the fact that growth-lines are a common feature in even the most ancient of brachiopods, and that the achievement of significant results does not depend on the near-perfect preservation of a population; this latter feature is the major disadvantage of size-frequency histogram analysis. 151

II.2. MATERIALS

In attempting a comprehensive survey of the periodicity of growth-line formation in Recent brachiopods it was essential to study as many different species as possible, from geographically widespread localities, and from a diverse range of habitats and environments. In this respect the comprehensive Recent brachiopod collections in the Dep ārt- ment of Palaeontology, British Museum (Natural History), London, were invaluable. The widening of the scope of the study to include analysis of the abundant brachiopod faunas in the Southern Hemisphere was possible as a result of a British Council travel grant, which enabled the author to collect from the abundant intertidal brachiopod populations around New Zealand, and to study other brachiopod collections housed in various museums, universities, and research instit- utes in that country. Further large collections, from Antarctica, North and South America, and Africa, were studied in the Department of Paleobiology, National Museum of Natural History, Washington DC, USA. All the available information on the locality and habitat of each population studied is described at the beg- inning of the relevant section. Some of the populations are, however, poorly localised and lacking in environmental data, but such precise information, though desirable, is not a vital prerequisite for growth-line analysis. 152

II.3. METHODS

II.3.1. ELECTRON MICROSCOPY - TECHNIQUES OF SPECIMEN PREPARATION

A 'CAMBRIDGE S-600' ('STEREOSCAN') scanning electron microscope was used to examine the microscopic growth banding in several species of Recent Brachiopoda. Fragments of shell were prepared for S.E.M. study by first immersing them in concentrated 'MILTON' solution (essentially sodium hypo-

chlorite) for approximately i hour, to remove any adherent soft tissue - a longer immersion period is undesirable because the dissolution of the organic matrix significantly reduces the structural integrity of the shell. A gentle scouring of the shell surface using a soft paint-brush was sufficient to remove any adherent tissue remaining after such treatment. The shell fragments were then thoroughly washed in a mild solution of 'TEEPOL' detergent, and subsequently in deionised water. When sections through the shell were required the fragments were embedded in either 'EM301-PA' polyester resin or fine industrial casting plaster. A diamond blade was used to section the embedded fragment in the required orientation. The exposed surfaces were first smoothed on a band- faced grinder, and then polished using successively finer grades of 'ALOXITE' carborundum powder (grades 600, 800, and 1000). A completely smooth and scratch-free surface was achieved using a jeweller's polishing disc impregnated with 'SERRI-ROUGE' (cerium oxide). The embedded shell fragments were then washed in deionised water and ultrasonically 153 cleaned in acetone. Other non-embedded fragments intended for the study of external or internal surface features were cleaned in similar fashion. Fragments embedded in casting plaster, having been sectioned and polished, can then be freed from the plaster matrix prior to attachment to the S.E.M. stub, allowing the examination of the microscopic growth bands both in polished section,and, in the same fragment, their manifestation on the external surface. The surfaces and sections of prepared fragments were gently etched in a 2% solution of E.D.T.A. (Ethylenediamine- tetra-acetic acid) in the hope of emphasising the growth banding; the immersion times varied from 5 to 30 minutes. Prepared specimens were attached to the aluminium stubs using 'EPON ARALDITE' epoxy resin, and were left overnight in a low-temperature oven to set. A thin coating of cond- uctive gold/palladium, between 10 and 20 nanometres thick, was deposited on the specimens using a modified 'POLARON E5000' sputter coating unit (which used a cold stage, and an annular, rather than discoidal, target). All important 'Stereoscan' observations were recorded photographically, using either a 'POLAROID' or 'ROLLEX' camera. 154

II.3.2. GROWTH-LINE MEASUREMENT TECHNIQUES

The primary complicating factor in growth-line analysis is the difficulty in distinguishing between growth-lines and 'disturbance-lines'. Growth-lines are formed at regular intervals on the majority of specimens in a population, whilst disturbance-lines are caused by aperiodic localised disturbances which only affect a small proportion of the specimens. However these complications can be overcome by measuring the growth-lines on a large number of specimens from each population (rather than attempting to determine the growth strategy of individual specimens), and by using suitable cumulative methods of data analysis. It is of paramount importance to avoid techniques or procedures which involve or depend upon personal prejudice or selectivity (as regards the validity or significance of a particular growth-line or series of growth-lines); any preconceived notion as to the probable or expected result will almost certainly affect the final results if the methods of data collection and analysis are susceptible to distortion by the many forms of insidious personal bias. All methods of growth-line measurement and the subsequent procedures of data analysis must be standardised; the pattern of growth- line formation must be allowed to emerge from the accumulated data, rather than be moulded to conform to the observer's beliefs and expectations. With these considerations in mind it was decided that, throughout this study, all discernible growth-lines would be measured, even when it was apparent that damage to the shell 155 margin had been the primary cause of growth-line formation. Particular care was taken to include all juvenile growth- lines, which are often faint because the juvenile shell is thin. (The formation of a pronounced growth-line terrace - a common feature in adults - is undesirable in juveniles as it would significantly reduce the structural integrity and strength of the shell,:and, in addition, would disturb the normal ontogenetic development of the shell profile.) It was considered desirable to measure growth-lines on at least 50 specimens from each population studies; however in some cases, when the number of specimens available was limited, and the population of particular interest in the context of the present study, measurements were taken from fewer than 50 specimens. A standard preliminary familiarisation procedure was adopted in the study of each population. Before any growth- lines were measured a number of specimens were examined vis- ually under high-powered illumination to determine the state of development of external growth-lines. Some species exh- ibit well-developed growth-lines which have considerable surface relief, whilst in others growth-lines are generally faint and of low relief. The familiarisation process was facilitated, when necessary, by using low-level illumination, by dusting the shell surfaces with chalk dust, or by wetting the specimens with water. In some instances the shell surfaces were examines using a microscope, although only during the familiarisation process; only those growth-lines discernible with the naked eye were measured. Despite the wide variety in the state of growth-line development between 156

different species (and indeed between specimens from a single population), it proved possible to measure growth-lines on all specimens examined during this study; the familiarisation process is thought to have been a major contributory factor in the success of these studies, and should be regarded as an essential prerequisite for this method of growth-line analysis. For the purposes of the present study the most appropriate method of growth-line measurement was to measure the distance to each growth-line on the ventral valve from the posterior margin of the shell. This method of measurement, and the ensuing cumulative method of data analysis (see_. below) , was= f` -C p-^=posed by Cr .ig- ānd Hallam (1963) for the analysis of bivalve growth-lines. The measurements are linear approximations of a more or less curvate growth increment, but such approximations are adequate for the purposes of this study. It is customary, and indeed logical, to measure these increments in the direction of maximum dimensional increase, thereby maximising the resolution between successive growth-lines. The growth-lines on all brachiopods examined during this study were measured (to the nearest 0.1mm) along the anterior-posterior axis of the shell as, with one exception, the maximum incremental increase in shell dimensions occurred anteriorly in all species investigated. (The only exception being adult specimens of Notosaria nigricans (Sowerby), in which the maximum increase occurs laterally (i.e. in width). However this factor does not discernibly affect the analysis of the growth history of this species based on anterior-posterior measurements (Subsection 157

II.5.2.2.). Growth-line studies of other brachiopod species, in which length is not the primary shell dimension, are likely to involve modification of this measurement technique.) The accumulated data from each population was then combined graphically in the form of a growth-line frequency diagram (i.e. Fig. 15;16). The rationale_ behind this procedure is logical - the regularly formed growth-lines will be represented by a large number of measurements and will therefore stand out as a mode in the frequency distribution; disturbance-lines, in direct contrast, are irregularly spaced and variably developed, and such measurements will form part of the background 'noise' of the frequency distribution rather than prominent modes. The pattern of growth-line formation can be determined from the mode spacing. The grouping used in the preparation of the frequency diagrams is critical; for most species examined during this study a grouping of 0.5mm yielded optimum results. Using a grouping which is either too large or too small results in frequency distributions which, respectively, are lacking in detail, or uninterpretable because of the great confusion of modes present. The optimum grouping clearly depends on the maximum size of the specimens and the spacing between the growth-lines; in the study of the micromorphic Magadina sp (Subsection II.5.5.1.) a grouping of 0.2mm was found to be most appropriate. The relative merits of the various group- ings are discussed in Subsection II.5.2.4. One of the major advantages of this method of growth- line analysis is that each measurement is a close approximation of the length of the specimen when that growth-line was 158

formed (the accuracy of the approximation depends on the degree of umbonal erosion - see below). Having adopted this method of analysis as standard procedure for each population, the results of all analyses are therefore directly comparable with each other and with the results of the growth- rate study of T.retusa (based on length-frequency histograms - Section I.4.3.). When suitable numbers of specimens were available both a length-frequency distribution and a growth- line frequency distribution were prepared. Each of these graphical representations yields precise and detailed information on the growth history and habitat of the population; taken in conjunction they complement each other, by supplem- enting and confirming the conclusions reached, and by compen- sating for aspects which are lacking or difficult to interpret in the other. For instance the growth-line frequency diagrams rarely provide detailed information on the earliest- formed growth-lines or on the gerontic growth strategy, whilst length-frequency diagrams are often much more informative on these topics. In a few studies the average spacing between the growth- lines on each specimen was calculated (by subtracting the measured distance to each growth-line from that measured to the succeeding growth-line). In one instance (Subsection I1.5.5.2.) the spacing between growth-lines was measured directly from the specimens. The calculated average growth- line spacing for each specimen was then plotted as a single data point in a frequency diagram, the main mode of which represents the mean average growth-line spacing for the entire sample. This method is useful when comparison between two 159

or more populations are required (Subsection II.5.5.2.). However the information provided by this method of analysis is limited, and certainly the diagnostic pattern of alternating summer and winter growth increments will be lost during the averaging process. A further complication is that the success of this method depends upon near perfect growth-line formation and preservation; 'missing' growth-lines will increase the calculated average value and distort the results. In certain circumstances this method can be applied to great advantage, either as the main method of analysis (Subsection II.5.5.2.) or to supplement the results of the more precise analytical procedure described above (i.e. Subsection II.5.1.2.). The success of either method of growth-line analysis depends upon an adequate 'sample' of measurements; below a certain number of data points a size-frequency diagram will yield incomplete, inconclusive or uninterpretable information. As discussed in Section I.4.2., it is impossible to state meaningful minimum values for the size of an acceptable sample; the only conclusive method of determining this is to collect several large samples and check that the results from each are comparable. In this study it was often impossible to study more than one population of each species because of a lack of suitable material and time restrictions, and a few of the analyses are undesirably imprecise and lacking in detail as a direct result. In retrospect, it would seem that for temperate latilude species a rough guide to the desirable number of growth-line measurements is to double the maximum shell length (in mm) and multiply by 10 - thus for a species 160

EXPLANATION OF TEXT-FIG. 12.

Diagram illustrating the desirability of large numbers of growth-line measurements for analysis. The black circles correspond to modes discernible at 100 measurement intervals and the progressively greater resolution, detail, and comp- leteness is apparent.

Data from the analysis of growth-lines on Laqueus californicus (Koch); Recent; Catalina Island, west coast of USA. (see Section II.5.1.2.) 500-

NTS •

E 400-

UREM 300- AS

200- OF ME No. 100-

r r 1 10 1'5 20 2'5 30 35 40 415

LENGTH (mm) 162

of maximum length 20mm, at least 400 measurements would be desirable. The progressively greater resolution and detail attain- able with increasing numbers of growth-line measurements was apparent in the study of Laqueus californicus (Koch) - (Sub- section II.5.1.2.). After each 100 growth-line measurements (taken from adult specimens selected at random from the available sample) a growth-line frequency distribution was prepared and the prominent modes recorded. As indicated in Fig.12, out of the final total of 22 modes discernible at the 500 measurement stage, only 8 were present after the first 100 measurements (= 36%), 12 after 200 measurements (= 55%), 15 after 300 measurements (= 68%), and 16 after 400 measurements (= 73%). Apart from the increasing number of modes, their slight realignment, and the more comprehensive data, the significant feature of this progression iš the fact that twin modes, an extremely important diagnostic feature, are clearly discernible at the 500 measurement stage, but are only sporadically developed with fewer measurements. The phenomenon of umbonal erosion must be considered in the context of growth-line analyses based on measurements from the posterior margin to growth-lines on the ventral valve. In most living articulate brachiopods the shape and position of the pedicle aperture (Fig.l) is modified, to a greater or lesser extent, throughout ontogeny (Williams, 1965). These modifications are the result of a number of processes, such as shell resorption (to accommodate increasing pedicle diameter), and the progressive secretion of deltidial plates

(Fig.l). The effect of such ontogenetic changes on the 163

EXPLANATION OF TEXT-FIG. 13.

Scatter diagram of the length of shell removed by umbonal erosion (as determined from the width of the posterior-most growth-line - see Section II.3.2.) versus total shell length in specimens of Liothyrella uva notorcadensis (Jackson); Recent; Antarctic Peninsula; Antarctica, (Subsection 11.5.3.1.). 11- • 10-

M) 9- • • •• M • • • • ( • •

8- N • •• • • ••• • 7- • • • •• ••• •_ 6- • • • • • • • • 5- • • • • • • • 4- • • • • UMBONAL EROSIO • • 3- • • • • • • • • 2- • 1- • • • • I I 15 10 20 25 30 35

Length (mm) 165 ventral umbo is enhanced in those species which are held close to the substrate by their pedicles; many living articulate brachiopods frequently rotate around their pedicle when disturbed or when re-orientating into preferred feeding positions, and as a result portions of the ventral umbo are eroded by abrasion against the substrate (Plate 10,E,F). The net effect is the gradual removal of portions of the ventral umbo (i.e. umbonal erosion). Therefore in adult specimens the measured distance from the posterior margin to each growth-line is not an exact measure of the length of the shell when that growth-line was formed, In some species the degree of umbonal erosion is insignificant; in others, however, as much as two years growth has been removed. Umbonal erosion occurs throughout life (Fig.13), and can be considered as a negative component of the annual growth increment. Fig.14 illustrated diagrammatically the effect of umbonal erosion on the measured growth-line increments:- in (A) the first growth-line has just formed; in (B) the second growth-line has formed at a length of 25mm, and gradual erosion of the ventral umbo has reduced the measured distance to growth-line 1 from 12mm in (A) to 10mm in (B); in (C) the third growth-line has formed at a length of 35mm - by this stage the first growth-line is only 8mm from the posterior margin, and the second growth-line, similarly affected by umbonal erosion but to a lesser extent, is at a distance of 24mm; in (D) the fourth growth-line is forming at a distance of 45mm from the ventral margin, and by this stage the first growth-line is a mere 6mm from the posterior margin, 166

EXPLANATION OF TEXT-FIG. 14.

Stylised representation of the effect of umbonal erosion in reducing the measured distance from the posterior margin of the shell to the earliest formed growth-lines throughout the life of the specimen. Adult growth-lines are essentially unaffected by umbonal erosion, as are the growth-lines on the dorsal valve. 16 - H DISTANCE (mm) WT E

IN VENTRAL DORSAL L GRO I

1 12 10

1 10 10 2 . 25 20

1 8 10 2 24 20 3 35 30

1 6 10 2 23 20 3 35 30 4 45 40 168

whilst the second growth-line increment continues to be slightly affected (now at 23mm) - however by this stage the plane of erosion has rotated around (due to shell curvature) to such an extent that the third growth-line increment is not discernibly affected by umbonal erosion , and subsequent growth-lines remain at a relatively constant distance from the ventral umbo. In effect, therefore, umbonal erosion will only affect the earliest-formed growth-lines, and in many species the degree of umbonal erosion is so small as to have a negligible effect on the growth-line frequency distribution. Even in species subject to considerable umbonal erosion the effect on the growth-line frequency distribution can be min- imised by studying specimens of similar size in which the degree of umbonal erosion will be reasonably comparable (Fig. 13); the only significant effect is the lack of detailed information on the earliest growth stages which does not detract from the success of this method of analysis. Nevertheless, in the study of Liothyrella uva notorcadensis (Subsection II.5.3.1.), a species characterised by considerable umbonal erosion, it was decided to attempt to compensate for the eroded portions of the shell by calculating the length of shell which had been removed from each specimen. The procedure was straightforward, and depended upon the precise linear relationship between the length and width of the shells of many articulate brachiopods, (i.e. in T.retusa - see Fig. 6,E). A good approximation as to the quantity of shell which has been removed can be obtained by measuring the width of the posteriormost growth-line; the length and width of juvenile specimens have a precise linear 169

relationship which can be defined algebraically as the equat- ion of the 'best fit' line calculated from a sample of length and width measurements (i.e. Fig. 6,E). The eroded increment was then added to the measured distance to each growth-line, and the resulting data plotted as a growth-line frequency- distribution as is customary (Fig. 28). The spacing between the earliest-formed growth-lines is much more clearly defined in this distribution that in the non-compensated growth-line frequency distribution prepared from the same specimens (Fig. 27). However it is the pattern and spacing of growth-line formation which is critical and diagnostic, and in this respect the compensatory procedure does not significantly augment the data derived from the non-compensated measurements. This compensation method is therefore considered superfluous in the context of the present study, although further refinement of this growth-line analysis method, perhaps computer- based, may encompass a more meaningful compensatory technique. The problem of umbonal erosion can, of course, be avoided by measuring growth-line increments on the dorsal valves which, in the majority of living brachiopods, are unaffected by umbonal erosion, or by by measuring the width of each growth- line rather than the length. Growth-lines on Bouchardia antarctica (Buckman) were indeed measured on the dorsal valve, primarily because a higher proportion of the rather small number of specimens available had damaged or sediment encrusted ventral valves. However widespread use of dorsal valve measurements was considered undesirable because such measurements are difficult to relate to maximum shell length, and the modes in the growth-line frequency diagrams are liable to amalgamation 170 because of the reduced absolute value of the increments involved. This latter feature is the primary disadvantage of utilising width measurements in growth-line analysis, although in species in which the maximum incremental increase in shell dimensions occurs in width rather than length, measurements of either maximum shell width (for width-frequency diagrams) or maximum width of each growth-line (for growth-line frequency diagrams) are preferable. 171

II.4. MICROSCOPIC GROWTH-LINES

This project on the growth and ecology of Recent brachiopods was initiated in the hope that the results would provide a sound empirical basis for the interpretation of growth- related depositional banding within the brachiopod shell fabric. Growth-lines are discernible both on external surfaces and in polished sections of the brachiopod shell, and at periodicities ranging from less than 1 micron to several mil- limetres; they represent periodic alteration or cessation of the shell secretory process. Macroscopic growth-lines form in response to major disturbances which result in the regression of the mantle epithelium from the peripheral margins of the shell (Brunton, 1969); the results of the present study shows that they are primarily formed at biannual or annual intervals (Sections II.5.1. to II.5.5.). The process by which microscopic growth-lines are formed obviously involves much less drastic disturbance to the mantle epithelium, and has been interpretated as representing a diurnal periodicity (Williams, 1968a; 1971a). In the light of the new evidence on the periodicity of macroscopic growth-line formation, it is appropriate to reconsider the possible significance of microscopic growth-lines, and to briefly summarise the available information on the brachiopod growth process. Clearly both have a great bearing on the interpretation of all growth- related structures within the shell fabric. The advent of the electron microscope heralded significant advances in many fields of brachiopod research. The most significant contribution was that of Williams who, using 172 both scanning and tranmission electron microscopy, interpretated the multi-layered brachiopod exoskeleton in terms of the complex sequential secretory activity of individual cells of the outer mantle_epithelium (Williams, 1956, 1966, 1968a,b, c,d, 1970, 1971a,b, 1973, 1977; Biernat and Williams, 1970, 1971; Mackinnon and Williams, 1974; Williams and Mackay, 1978; Williams and Wright, 1970.) Whilst the applications of Williams' research are manifold, the most significant aspect in the context of the present study was Williams' assimilation of the results of his wide-ranging and taxonomically-comprehensive studies into a simplified, readily-understood, and widely-applicable model of the standard brachiopod shell secretory process. The following brief summary of this model describe the mechanism of shell secretion in a typical articulate brachiopod, and therefore can be applied directly to all species investigated during this study. The calcareous valves of brachiopods are secreted by the cells of the outer mantle epithelium, which proliferate__from a generative zone situated within a peripheral mantle groove. As these cells migrate forwards along the inward-facing surface of the mantle groove, due to the forward growth of the shell margin and subsequent generation of new cells, they begin to secrete the various proteinaceous components of the non- mineralised periostracum. As each cell migrates around the tip of the mantle lobe to face outwards, its secretory regime changes and the outermost layer of the calcareous exoskeleton, the primary layer (Plate 8,A,B), is secreted below the covering periostracum. Williams described the migration of the cells in terms of a conveyor belt system. The migration of 173 each cell, now in a posterior direction along the marginal, inwardly-sloping, growth surface of the primary layer, results in a progressively greater thickness of primary layer between the cell and the outermost periostracum. At a certain distance from the peripheral shell margin there is a major change in the secretory activity of each cell, which begins to secrete a single fibre of calcite-within-a:proteinaceous sheath. The secondary layer of the shell is composed of a variable number of tightly-packed alternating rows of these fibres (Plate 9,E,F; Plate 13), each of which is separated from each other by a proteinaceous sheath. In some species a further shell layer, the tertiary prismatic layer, is formed (Plate 6, D,Er Plate 11). Mackinnon and Williams (1974) have interpretated the change-over from secondary layer.--fibres to tertiary layer prisms (Plate 11,C,D) as representing a further profound change in the secretory activity of individual cells; whilst secreting tertiary layer the cells no longer secrete a proteinaceous membrane, and several cells may combine to secrete a single prism. Therefore at any instant in time the junction between the calcareous exoskeleton and the outer epithelium which is secreting it, is a plane which, in radial section, dips posteriorly inwards from the margins of the shell and passes along the growth surface of each individual secondary layer fibre and tertiary layer prism (when developed). This plane of growth is delineated both by the microscopic growth banding within the shell layers, and by the disposition of the inner margins of the various shell layers in polished sections (representing the position of the growth plane at the moment 174

of death - see Plate 12,13). Growth-lines are discernible in all shell layers, but the primary layer growth banding is the most important in the context of the present study. This is because the secondary layer fibres grow forwards_at an angle to the primary - secondary layer junction (see Mackinnon and Williams, 1974, Text-Fig.l), with the result that the micro-._ scopic growth-lines sporadically developed in individual fibres are progressively more difficult to relate to primary layer growth-lines as the separation between primary layer and the secondary fibre increases. In addition the secondary fibres do not continue to grow forwards in synchrony with the primary layer indefinately; at a certain distance from the shell margin the orientation of the secondary layer fibres alters, a feature recognisable by the variable disposition of the fibres in polished sections (i.e. Plate 6, D-F). This represents a fundamental change in the growth strategy, with the emphasis shifting from peripheral accretion to shell thickening. To accommodate the rotational movements of the secondary layer fibres whilst retaining a tightly packed and therefore struct- urally sound fabric, it is probable that the secretion of individual fibres will be interupted - the rotation of groups of fibres (see Williams, 1968a, Text-Fig. 11) necessitates differential growth of the outer and inner fibres of each group, which may be accommodated by fewer or dimensionally smaller growth bands in the innermost fibres. It is obviously vital that the animal maintains a balance between the forward growth of the shell margins and the thickening of the previously secreted shell; the secretion of tertiary prisms, clearly related to shell thickening, may represent the adoption of a more 175

efficient method of secreting calcite for this purpose. Whilst distinct transverse growth-lines have been recognised in the tertiary layer prisms of several species, (Mackinnon and Williams, 1974; Plate 11), the possibility of non-continuous growth is a major stumbling-block in attempting to determine the significance of growth-lines in shell material secreted during the thickening process. In effect, therefore, only in the primary layer and the outermost secondary fibres can the growth-lines confidently be correlated with the forward growth of the shell margin. The primary layer is relatively thin, and is composed of minute accicular crystalites of calcite inclined at a high angle to . the outer surface of the shell (Plate 7,A). Sections through the shell show that microscopic growth-lines representing the former position of mantle epithelium-primary layer junction dip posteriorly at a low angle to the external surface of the primary layer (on average 16.8° (range 5.5° - 25°) in a specimen of Gryphus vitreus (Born) - see Plate 6,F). These primary layer growth-lines are regularly spaced, with an average periodicity of approximately 0.5 microns (see Williams 1968a, 1971). Variations in the spacing of these microscopic growth- lines may, as Williams (1968a) suggests, reflect differential summer and winter growth rates, or variations in the shell secretion rates of adults and juveniles. Unfortunately these microscopic growth-lines are, at best, sporadically developed (i.e. Plate 7,E), and obviously their interpretation depends upon further refinement of the techniques of specimens preparation for 'stereoscan' analysis, perhaps involving more eff- ective differential etching methods. Perhaps microprobe 176 analysis of compositional variations may supplement the visual evidence; however, whilst seasonal variations in the chemical composition of the primary layer may be discernible (reflecting concomitant variations in the chemical constituents of the surrounding sea-water), the resolution of compositional variations to within 0.5 microns seems unlikely. Perhaps living brachiopods can be induced to feed in tetracycline solution, a method which has been used with some success in determining the significance of growth-lines within the skeletons of other invertebrates. Tetracycline is incorporated biochemically within the shell material, and therefore would mark the synch- ronous growth surface within primary, secondary, and tertiary shell layers; the subsequent growth of the animal could then be correlated with growth-lines formed after the tetracycline marker. However the extreme sensitivity of brachiopods to abnormal chemical compounds in the surrounding sea-water may result in the animals reacting against the tetracycline solution and remaining tightly closed for the duration of the immersion period; under such conditions the incorporation of tetracycline into the shell fabric seems unlikely. Williams (1968a, 1971a) was the first to discover these microscopic growth-lines, and suggested that they were of the right order to have been formed diurnally. Before considering the periodicity of microscopic growth-line formation in the light of the new evidence on the periodicity of macroscopic growth-line formation (Sections II.5.1. - II.5.5.), it is appropriate to outline the simple calculations which form the basis of such discussion. Although the spacing between the microscopic growth-lines is, on average, 0.5 microns, the 177

dimensional significance of each increment in terms of the forward growth of the shell margin is in fact much greater. This is due to the angle of inclination of the depositional surface to the external surface of the primary layer; each microscopic layer grows forward beneath the preceeding layer, and the external surface of the primary layer is characterised by a series of microscopic scarps as a result (Williams 1971a, Fig. 4). The scarps on the external surface of the primary layer of Notasaria nigricans (Sowerby) are approximately 2 microns apart (Williams, 1968a), and a periodicity of 1.21 microns (S.D.=0.41 microns: N'=_44) has been measured on the external surface of a juvenile specimen of T.retusa. Assuming that 2 microns is an acceptable average value for the faīvrārd protrusion of each microlayer, then a diurnal periodicity would result in the accretion of 4 microns of new shell material per day and, assuming a growing season of 8 months is typical for temperate latitude species, an average annual growth rate of lmm. The average growth rate of temperate latitude species is significantly larger than this value, being of the order of 3 - 4 mm per year (Section II.5.1. and 11.5.2.). If the increments measured on the surface of the juvenile specimen of T.retusa are representative, and the microlayers deposited diurnally, then the shell of such specimens would grow by 2.4 microns per day, by approximately 80 microns per month and, even if growth continued throughout the year, by a mere lmm per year. Yet juvenile T.retusa grow, on average, to a length of 2.75mm within the first 3 months of life (Section I.4.3.), a growth rate of approximately 30 microns per day. These simplistic calculations seem to indicate 178

that the microscopic growth-lines do not form diurnally, and that as many as 25 are formed per day during the period of rapid juvenile growth in T.retusa. However it is dangerous to argue such a conclusion purely on the basis of the woefully small number of actual measurements which have been recorded; without measurements of microscopic growth-lines in continuous sections of the primary layer it is not known to what extent their spacing and forward protrusion remains constant. Alternative explanations are that the increased growth rate of juveniles is accommodated by an increase in the thickness of each microlayer, or by a greater forward progression of each microlayer beyond its predecessor (perhaps facilitated by a reduction of the angle of inclination of the depositional plane relative to the external surface). However it seems likely than the degree of overlap of each microlayer is subject to purely mechanical constraints; a calcite microlayer, 0.5 microns thick, will, be vunerable to breakage if exposed at the margins of the shell, and whilst the covering periostracum may support and protect the 'exposed' portion of the microlayer, a forward progression of more than 2 microns may be structur- ally unsound. Ultimately, however, the rate of forward progression of each microlayer will depend upon the rate of prolif- eration of new epithelial cells within the mantle groove, and the rate at which the cells secrete shell material; these two features may occasionally become uncoordinated, and a disprop- ortionate increase in cell production relative to the cellular secretion rate may result in a temporary dimensional increase in the plane along which the primary layer is being secreted. The curvature of some microscopic growth-lines in sections 179

through the shells of juvenile specimens, representing an increased forward progression, and a reduced inclination, of the mantle epithelium, may be the preserved record of such _a phenomenon. Thus the rapid growth of juveniles may, perhaps, be interpretable in terms of an overloaded conveyor belt system. Accepting, however, that the available information does indicate that the microscopic growth-lines do form more frequently than diurnually, it is therefore necessary to speculate on rhythmic behavioural and/or biochemical activity which could explain such a frequency. One possibility is that microscopic growth-line formation is linked to the cyclicity of the feeding and digestion of brachiopods; as described in Section I.5.1., the culmination of each feeding cycle is commonly the closure of the valves. It is not unreasonable to suggest that, just as in bivalves (Lutz and Rhoads, 1977), during p-eriods of shell closure the cellular oxygen levels are reduced, and that at such times brachiopod metabolism proceeds under anaerobic conditions. In bivalves the effect of such a phenomenon is a change in the composition of the extrapallial fluid, and a concomitant compositional change in the deposited exoskeleton (Lutz and Rhoads, 1977). A similar situation in brachiopods, at the culmination of each feeding cycle, may result in a slight compositional or density change in the secreted shell material, and the formation of a microscopic growth- line. Shell secretion may even halt during anaerobiosis. The suggestion of a relationship between the feeding cycle and growth-line formation is obviously highly speculative; the feeding cycle of living brachiopods has never been observed 180 in nature, and in any event the bivalve anaerobiosis develops in response to prolonged periods of shell closure. Altern- ative explanations are that the generation of new cells is periodic rather than continuous, or that the input of metab- olites and energy into the cells is rhythmical. Growth-lines with periodicities of greater than 2 microns have been recognised in the brachiopod shell fabric, notably on the external surface of the primary layer and in sections through the tertiary layer (Plate 11,C). As with all microscopic growth banding within the brachiopod shell, the main difficulty in attempting to determine the significance of these structures is the inability to measure them in long continuous sections. This problem may in part be resolved by more advanced methods of specimen preparation, but it does seem that microscopic growth-lines are, at best, sporadically developed, and their interpretation is likely to remain extremely problematical. Perhaps our understanding of these phenomena may be increased by microprobe analysis of compositional variations, and oxygen-isotope ratio studies. 181

II.5. ANALYSIS OF MACROSCOPIC GROWTH-LINES

II.5.1. RECENT TEMPERATE LATITUDE BRACHIOPODS - N.HEMISPHERE

II.5.1.1. Terebratulina septentrionalis (Couthouy)

MATERIAL: Location - off Cape Cod Light, Massachusetts., U.S.A., (064°T); Collected - 5th December, 1966; Depth - 90 metres (47 fathoms). The collection is housed in the Department of Paleobiology, National Museum of Natural History, Washington, DC, U.S.A. Sixty-two specimens were examined and 441 growth- lines were measured. Terebratulina septentrionalis is morphologically very similar to T.retusa, and it is clear from the analysis of growth-lines that the growth strategy of the two species is identical. In the following table the modes in the growth- line frequency diagram prepared for T.septentrionalis (Fig. 153—al.ec mpared _ iith the standard growth analysis of T.retusa (i.e. Table III).

TABLE X Comparison between T.septentrionalis and T. retusa; data in mm.

T.septentrionalis T.retusa 2.25 2.75 - 1(a) 4.25 4.25 - 1(b) 7.75 6.75 - 2(a) 9.75 8.25 - 2(b) 12.25 10.25 - 3(a) 14.75 11.75 - 3(b) 17.75 14.75 - 4 19.25 - 20.75 17.25 - 5 9 19.75 - 6 21.50 - 7 182

EXPLANATION OF TEXT-FIG. 15.

Growth-line frequency distribution prepared from 441 measurements taken from 62 specimens of Terebratulina peptentrionalis (Couthouy); Recent; off Cape Cod Light, Massachusetts, USA; (Subsection II.5.1.1.). 25

DISTANCE TO GROWTH-LINE (mm) 184

Whilst the growth rate of T.septentrionalis is slightly greater than that of T.retusa, the pattern of growth-line formation is identical in both species - growth-lines for biannually, and alternating periods of fast summer growth and relatively slower winter growth are clearly delineated. Thus, calculating the average growth-line spacing for T.septentrionalis from column 1 in Table X :- 2.0mm (W), 3.5mm (S), 2.0mm (W), 2.5mm (S), 2.5mm (W), 3.0mm (S). Having interpretated the pattern of growth-line formation determined for T.retusa in terms of seasonal variations in certain critical environmental parameters, it is encouraging to recognise a similar pattern in a different species from a transatlantic habitat in which the range, intensity, and duration of the seasonal variations are likely to be very similar to those experienced by T.retusa in the Firth of Lorne. The proportion of the annual growth increment attained during the summer months is identical in both species (64% in T.septentrionalis, and 63% in T.retusa). The slight difference in the growth rate of the two species may be genetically controlled, but it is clear that the absolute growth rate of brachiopods is variable, even within neighbouring populations of the same species (Subsection II.5.2.1.). There- fore it is possible that the difference of growth rate between the two species is a reflection of slightly more conducive conditions for brachiopod growth in the N.American location (i.e. increased food supply, less turbulence, etc.). The growth curve of T.septentrionalis appears to be identical to that of T.retusa, although the growth-line frequency diagram provides sparse information on the growth rates during the later years of life. However the fact that the published 185

length-frequency diagrams of T.septentrionalis are unimodal and right-skewed (Noble, Logan, and Webb, 1976) is diagnostic of high-to-low growth strategy(Section I.4.2.).

II.5.1.2. Laqueus californicus (Koch)

MATERIALS Location - 33° 28' 13" Lat., 118° 29' 47" Long., off Shiprock, East of Catalina Island, California; Collected - 'VALERO' Stn. 11917. The collection is housed in the Dept. of Paleobiology, USNM, Washington, DC. Forty-six specimens were examined and 504 growth-lines measured.

The growth-line frequency diagram of this species (Fig. 16) has prominent modes with an average spacing of 4mm, i.e. - 4.25mm, 8.75mm, 12.75mm, 16.75mm, 19.75mm, 23.75mm, 26.25mm, 30.75mm. Many of these modes have closely-associated subsidiary modes, i.e. at 11.75mm, 17.75mm, 20.75mm, 24.75mm, and _27.25mm. This sequence of 'twin' modes suggests that growth- lines form biannually in this species, and that the pattern of growth-line formation may be interpreted in terms of alternate periods of fast summer growth and extremely slow winter growth. L.californicus may, therefore, be intolerant of winter conditions, resulting in a close proximity of modes corresponding to growth-lines formed during the autumn and the following spring (i.e. the 'twin' modes). The average spacing between growth-lines was calculated for each specimen in the sample, and the resulting data plotted in the form of a frequency distribution (Fig.17,A,B). This analysis indicates that the mean average growth-line 186

EXPLANATION OF TEXT-FIG. 16.

Growth-line frequency distribution prepared from 504 measurements taken from 46 specimens of Laqueus californicus (Koch); Recent; Catalina Island, USA. (Subsection II.5.1.2.). I 10- I JI 5 lb 15 210 25 30 35 40 45

DISTANCE TO GROWTH-LINE (mm) 188

EXPLANATION OF TEXT-FIG. 17.

Growth-line spacing in 46 specimens of Laqueus californicus (Koch); Recent; Catalina Island, USA. (Subsection II.5.1.2).

A. Frequency distribution of average spacing (and Standard Deviation = B) of all growth-line on each specimen.

C. Frequency distribution of average spacing (and Standard Deviation = D) of growth-lines less than 32mm in length.

E. Frequency distribution of average spacing (and Standard Deviation = F) of growth-lines greater than 32mm in length. 20

(J> Z :::JL4A o ~ 10 ~

1 3 4 5 6 7 2 3 4 5

MM. A MM. B

15 > >(J (J Z z L4A ~10 :::J10 o o L4A L4A 0:: 0:: ~ ~

2 3 4 5 6 7 2 3 4 5

MM. C MM. D

> (J (J> Z L4A z . :::J 10 ~10 o o L4A L4A 0:: 0:: ~ ~

2 3 4 5 6 7 1 2 3 4 5

MM. E MM. F 190

spacing is 3.25mm (S.D. = 1.25mm). However a visual inspect- ion of the growth-lines on these specimens indicated that there was a marked slowing of growth rate in later life. Consequently the growth-lines were divided, rather arbitrarily, into two groups, roughly corresponding to the periods of juvenile and early growth (less than 32mm in length) and late adult and gerontic growth (greater than 32mm). The analysis of the former, (Fig.17,C,D), indicates a mean growth-line spacing of 4.25mm (S.D. = 1.25mm) in the early stages of life, whilst in Fig.17,E,F, the analysis of growth-lines greater than 32mm in length, an average spacing of 2.75mm (S.D. = 1.25mm) is apparent. The secondary mode at 3.25mm in Fig.17,C suggests that in some specimens the reduction of growth rate occurs prior to 32mm in length; alternatively this feature may be a reflection of the proportion of the sample which had been subjected to considerable localised disturbances during life. The fact that the distribution in Fig.17,E is right-skewed suggests that a proportion of the specimens maintained a high growth rate at a relatively late stage of life. These analyses suggest that L.californicus, with a maximum length of 50mm in this locality, has a maximum life span of 15 - 16 years.

II.5.2. RECENT TEMPERATE LATITUDE BRACHIOPODS - S.HEMISPHERE

II.5.2.1. Terebratella inconspicua (Sowerby)

MATERIAL: Location A - Intertidal rockpool on the western -191

margin of Shelly Bay, Lyttelton Harbour, nr. Christchurch, S. Island, New Zealand; Grid ref:- 111 450,NZMS 1, Sheet 84, 1:63360; Collected 28th November 1977. A total of 125 specimens were utilised for growth-line analysis yielding 523 growth-line measurements; the total sample contained 445 specimens. Location B - Sandy beach approximately 25 metres south of the Lyttleton Harbour rockpool (Loc.A); Collected Nov./Dec. 1977. A total of 440 growth-lines were measured from the 98 specimens collected. Location C - Paterson Inlet, Stewart Island, off the south coast of the South Island of New Zealand; Depth - 22m (60 ft); Collected by divers 10th Feb. 1977. The collection is housed in the New Zealand Oceanographic Institute, Wellington, New Zealand. Sixty-nine specimens were examined, and 528 growth- lines measured.

A densely populated boulder (with a triangular and roughly planar undersurface of dimensions 28cm x 27cm x 23cm) was collected from the Lyttelton Harbour rockpool (Loc.A), and all attached brachiopods removed. A length-frequency diagram was prepared for the 445 specimens of T.inconspicua recovered (Fig. 18), and the prominent modes in this diagram have been compared with the equivalent data from the length-frequency histograms of T.retusa (as analysed in Table III) :-

TABLE XI Comparison between T.inconspicua and T.retusa; data in mm. T.inconspicua T.retusa 2.75 2.75 - 1(a) 4.25 4.25 - 1(b) 6.75 6.75 - 2(a) 8.50 8.25 - 2(b) 10.25 10.25 - 3(a) 11.25 11.75 - 3(b) 12.75 ? 14.75 - 4 13.75 ? 17.25 - 5 19.75 - 6 21.50 - 7 192

EXPLANATION OF TEXT-FIG. 18.

Length-frequency diagram prepared from 445 specimens of Terebratella inconspicua (Sowerby); Recent; Lyttelton Harbour, nr. Christchurch, New Zealand. (Subsection II.5.2.1.). 30 CY

20 UEN REQ F

r 5 1 10 15

'LENGTH (mm) 194

The similarity between the juvenile and early adult growth strategy of the two species is striking, with evenly spaced modes corresponding to biannual spawning events discernible in the first three years of life. However the overall shape of the length-frequency curve of T.inconspicua is different to that of T.retusa (Fig.6,A); the former is bimodal, whilst the latter is unimodal and right-skewed. This feature reflects a fundamental difference in the adult growth strategy of the two species - the growth rate of T.inconspicua is drastically reduced in later life (i.e. deterministic or high-to-zero growth strategy), whilst T.retusa continues to grow, albeit at a slightly reduced rate, throughout life ( i.e. approximately. linear growth strategy - see Section I.4.3.). The mode at 13.75mm in Fig.18 therefore represents the amalgamation of modes corresponding to several cohorts due to the survival of specimens after reaching the determinate size. Growth-lines were measured on specimens from three localities, and the modes in the plotted growth-line frequency diagrams plotted from these data is compared in the following table:-

TABLE XII Comparison of three populations of T.inconspicua; data in mm. Rockpool Beach Paterson Inlet

3.50 3.75 3.25 - 1(b) 6.25 6.25 6.25 - 2(a) 8.25 8.25 8.25 - 2(b) 10.25 10.25 10.75 - 3(a) 11.25 12.75 12.75 - 3(b) 13.25 14.25 ( ) 15.75 - 4(b) 17.25 - 5(a) 18.75 - 5(b) 21.75 - 6 23.25 - 7 195

15—

5—

5 10 15 20 25

DISTANCE TO GROWTH-LINE (mm)

EXPLANATION OF TEXT-FIG. 19.

Growth-line frequency distribution prepared from 528 measurements taken from 69 specimens of Terebratella inconspicua (Sowerby); Recent; Paterson Inlet, New Zealand. (Subsection 11.5.2.1.). 196

The measurements from the rockpool sample indicate a biannual pattern of growth-line formation (Fig.20; column 1 in Table XII), confirming the interpretation of the modes in the length-frequency diagram prepared from this sample (Fig. 18; column 1 in Table XI). The growth-line analysis of the dead specimens collected from the beach (Loc.B) indicates an identical pattern of growth-line formation (Fig.20; column 2 in Table XII), although the modes corresponding to the 3(b) and 4th year cohorts are at slightly greater absolute values than in the rockpool analysis. This feature is thought to be a reflection of the admixture of intertidal and subtidal specimens in the beach sample; specimens collected from offshore- sub- - tidal habitats. had attained a larger maximum size than the rockpool specimens. The growth-line analysis of the subtidal population of this species from Paterson Inlet (Fig.19; column 3 in Table XII) shows that the biannual pattern of growth-line formation is discernible for the first 5 years of life in this locality, and that 7 year old specimens are, on average, 23.25mm in length. This a similar estimation to that of Doherty (1976; 1979) who, studying subtidal populations of this species from the Hauraki Gulf, determined that specimens which are 20 - 24mm in length were between 5 and 7 years old. The spacing between the biannual modes formed during the first three years of life is virtually identical in all three populations studied, and clearly the smaller maximum size attained by the rockpool specimens is due to the earlier cessation of growth (i.e. during the third year of life) rather than a reduced growth rate. It seems reasonable to interpret such a phenomenon in terms of the stress-inducing conditions prevalent in a rockpool habitat, 197

EXPLANATION OF TEXT-FIG. 20.

Growth-line frequency distribution prepared from 523 measurements taken from 125 specimens of Terebratella inconspicua (Sowerby); Recent; Lyttelton Harbour, nr. Christchurch, New Zealand, (solid curve).

Dashed curve represents growth-line frequency distribution prepared from 440 measurements taken from 98 specimens of . inconspicua collected from a beach approximately 25 metres south of the Lyttelton Harbour locality. All these specimens were dead when collected. (Subsection II.5.2.1.). ... . ' > 1 ': u .:" " , , ..:- , z 20 , w ,. , , ' ," ;. , , ., ::l . , • : I, • " , a ,. , ." w . . '.:, . , .,. , et: , . , , .. . IJ.. , , .. , ··, ,. ", , ...... ·, ,, . : . . ' , , . ".: , .' , " . " ' ..H , ' .' ., ,. . ., , , " " : , ," ' " . 10 . " , ,. ., " , , , .. ~,

,, .. ,I ......

,', , " " , 5 10 15 20

DISTANCE TO GROWTH-LINE (mm) 199

the inhabitants of which will be subjected to daily temperature, food supply, current velocity, and salinity fluctuations. In addition the cessation of growth may be associated with crowding (the available substrate within the rockpool is limited, and the competition for space intense), or with the onset of sexual maturity; this latter feature occurs during the third year of life, and may have a more profound effect on the growth of intertidal specimens than on those from less disturbance-prone subtidal habitats.

II.5.2.2. Notosaria nigricans (Sowerby)

MATERIAL: Location A - Intertidal rockpool on the western margin of Shelly Bay, Lyttelton Harbour, nr. Christchurch, South Island, New Zealand; Grid refs- 111 450, NZMS 1, Sheet 84, 1:63,360. A total of 60 specimens were utilised for growth-line analysis, yielding 276 growth-line measurements; the total sample contained 162 specimens. Location B - Sandy beach approximately 25 metres south of the Lyttelton Harbour rockpool (Loc.A); Collected Nov./Dec. 1977. A total of 91 growth-lines were measured from 24 specimens.

The boulder removed from the Lyttelton Harbour rockpool yielded 162 specimens of Notosaria nigricans (Sowerby). This is a rather smaller sample than would be desirable but N.nigricans is much rarer than T.inconspicua in the rockpool, and it was considered advisable not to threaten the survival of this species in such an important locality by collecting a larger sample. The length-frequency diagram prepared from this sample (Fig.21) has prominent modes at 1.25mm, 3.25mm, 6.25mm, 9.25mm, 200

EXPLANATION OF TEXT-FIG. 21.

Length-frequency diagram prepared from 162 specimens of Notosaria nigricans (Sowerby); Recent; Lyttelton Harbour, nr. Christchurch, New Zealand. (Subsection II.5.2.2.).

1 I 5 I 10 15

LENGTH (mm) 202

EXPLANATION OF TEXT-FIG. 22.

Growth-line frequency distribution prepared from 260 measurements taken fron 60 specimens of Notosaria nigricans (Sowerby); Recent; Lyttelton Harbour, nr. Christchurch, New Zealand, (solid curve).

Dashed curve represents growth-line frequency distribution prepared from 91 measurements taken from 24 dead specimens of N.nigricans collected from a beach approximately 25 metres south of the Lyttelton Harbour locality. (Subsection II.5.2.2.). 20

I 5 15 10

DISTANCE TO GROWTH-LINE (mm) 204

12.25mm, and 13.75mm. The spacing of these modes, and the evidence from growth-line analysis (see below), suggests that it is reasonable to interpret these modes in terms of biannual cohorts; thus each mode listed above corresponds, respectively, to the 1(a),1(b), 2(a), 3(a), 4(a)?, 4(b)?_- cohorts. _ The overall shape of this distribution is bimodal, suggesting that this species has a high-to-zero growth strategy, and that the final two modes in the distribution represents several cohorts. The growth-line frequency diagram prepared from the 276 growth-line measurements is more informative (Fig.22), and the following modes (in mm) are discernible:- 2.25 - 1(a); 3.75 - 1(b); 5.25 & 7.25 ? - 2(a); 8.25 - 2(b); 9.75 - 3(a); 10.75 - 3(b); 12.0 - 4(a); 13.25 - 4(b). The analysis of growth-lines from the beach sample was disappointing, primarily because so few specimens were collected. Nevertheless it seems clear that growth-lines form biannually in this species, and that spawning occurs both in autumn and spring.

II.5.2.3. Neothyris lenticularis (Deshayes)

MATERIAL: Location - 29° 42'S, 178° 43.3'E, Bounty Platform, south-east of New Zealand; Depth - 146 metres (80 fms ). The collection is housed in the New Zealand Oceanographic Institute, Wellington, New Zealand. (NZOI A734). A total of 61 specimens were examined and 464 growth-lines measured.

A periodicity of approximately 4 mm between modes is 205

EXPLANATION OF TEXT-FIG. 23.

Growth-line frequency distribution prepared from 464 measurements taken from 61 specimens of Neothyris lenticularis (Deshayes); Recent; Bounty Platform , off New Zealand. (Subsection II.5.2.3.). I I I 10— I I Z LLJ M i -\ LLI re LL 5- n, I / I / I

I n 5 10 15 20 2'5 30 35 40

DISTANCE TO GROWTH-LINE (mm) 207

apparent in the growth-line frequency diagram prepared for this species (Fig.23). There is some suggestion of bimod- ality, with some prominent modes associated with subsidiary modes; i.e. 17.25mm and 18.75mm, 25.25mm and 26.75mm, 35.75mm and 36.75mm. These two features suggest that this species has an annual growth rate of approximately 4 mm per year, and that growth-lines are formed biannually. Certainly the interpretation of the growth history of this species would have been greatly facilitated had a much larger sample been available for study, as the pattern of growth-line formation is discontinuously portrayed by the available data. Neverthe- less it does seem that N.lenticularis has an annual growth rate similar to that determined for other similarly sized temperate latitude brachiopods, and that this species has a maximum life-span of 15 years approximately.

II.5.2.4. Liothyrella neozelanica, Thomson

MATERIAL: Location A - off Farewell Spit, to the north of the South Island of New Zealand; Collected by benthic dredge 7th August 1972; This collection is in the care of Dr. D.I. Mackinnon, Dept. of Geology, University of Canterbury, Christchurch, New Zealand. A total of 68 specimens were examined, and 524 growth-lines measured. Location B - 40° 23.5'S, 117° 12'E, western margin of the Hikurangi Trench, off the west coast of the North Island of New Zealand. Depth - 497 metres (272 fms). This single specimen is housed in the New Zealand Oceanographic Institute, (NZOI E731).

Two growth-line frequency distributions were prepared for this species to determine the most suitable modal grouping. 208

EXPLANATION OF TEXT-FIG. 24.

Growth-line frequency distributions prepared from 524 measurements taken from 68 specimens of Liothyrella neozelanica, Thomson; off Farewell Spit, New Zealand. The solid and dashed curve represent, respectively, distributions prepared using lmm and 0.5mm grouping. (Subsection II.5.2.4.).

30-

/I, ,%

1 I `I ; a `' ,' I 11 ' IS /I 11 ,` / 1 ,1 I 1 a / 1 I I I %, I I I a Iv I , 1` I . 1 1 1,Ir ,, 10- I I 1 I t I 1 i ,~ -- ' ,' 1 / I I a 1/ 1 1. II / 1 11 I 1 1 1 1 a--1 A I I I 1 1 / r 1 1 1 I 'I 1 / 1 i i 1 1 1 1. I 1 I I I 1--1 I 1, /%, 1., / /I I 1 r I /' 1 I % 1 I 1 I 1 , l 1 1/ % 11 /,`~. ~~ r ` 1 1 1 a ` / 1 / I 1 / — — — • / I 1° / 1 I 1/ 1 1/ r 11 I / I • 1 • r I 1 1 l t 5 10 15 20 25 30 315

DISTANCE TO GROWTH-LINE (mm) N O 210

Utilizing a grouping of lmm a periodicity of 3-4mm is apparent between modes (Fig. 24);- 5.5mm, 8.5mm, 11.0mm, 14.5mm, 16.5mm, 21.5mm, 23.5mm, 26.5mm, 30.5mm, and 34.5mm. The frequency distribution prepared from the same data, but using a 0.5mm.grouping, is more informative, and intermediatory modes between those distinguished using the lmm grouping are an important addition to the information provided by the analysis. The resolution of this method of analysis, therefore, is to some extent dependant on the modal grouping used - in the majority of cases a grouping of 0.5 mm will provide optimum results. It seems clear that the growth-line in this species form biannually (i.e. dashed curve in Fig.24), and some closely spaced 'twin' growth-lines were observed on some specimens. The NZOI brachiopod collections contain a single extremely large specimen of this species (66.7mm in length as compared with a maximum of approximately 40mm for the Farewell Spit specimens) collected from a deep water locality off the west coast of the North Island of New Zealand (Loc.B). Over 30 growth-lines were clearly marked on the surface of this specimen, and having compared the spacing of these growth- lines with that determined for the Farewell Spit specimens, it is clear that this specimen was at least 30 years old when collected. The juvenile growth-lines on this specimen have been removed by umbonal erosion, but early adult growth continued, at an identical rate to that of the Farewell Spit specimens, until the specimen was approximately 40mm in length (i.e. 15 years old); the unusual feature of this specimen is that it continued to grow, albeit at a progressively red-

ucing rate, for at least a further 15 years. 211

II.5.2.5. Magellania venosa (Solander)

MATERIAL: Location - 53° 39.1'S, 700 55.3'W, Strait of Magellan, between Tierro del Fuego and Chile, S.America; Depth - 51 - 59 metres; Collected 26th April 1970; 'HERO' cruise no. 702, Stn. 469. The collection is housed in the USNM, Washington, DC. A total of 55 specimens were examined and 776 growth-lines measured.

Prominent modes at 3.75mm, 12.75mm, 17.75mm and 22.25mm, (see Fig.25,B) suggest that this species grows at a faster rate in early life (i.e. approx. 5mmm per year) than other temperate latitude species which have been studied. The 9mm interval between the first and second of these two modes may indicate an even more rapid juvenile growth rate,although such a conclusion is obviously tentative. However many marine invertebrates from the Megallanic province do have an unusually high rate of growth, and therefore such a possibility cannot be discounted. There is some indication of a biannual pattern of growth- line formation, with sporadically defined 'twin' modes, i.e. at 25.75mm and 26.75mm, and 29.25mm and 30.75mm. The spacing of these and subsequent modes suggests that the growth rate slows to approximately 4mm per year in specimens greater than 20mm in length. Well defined modes at 42.25mm, 44.75mm, 46.5mm, 48.75mm, 50.75mm, 53.0mm, and 54.75mm suggest that that the growth rate slows progressively throughout life, and that these specimens (with a maximum length of 65mm) have a life span of approximately 20 years. 212

EXPLANATION OF TEXT-FIG. 25.

A. Growth-line frequency distribution prepared from 714 measurements taken from 113 specimens of Pachymagas sp; Lower Miocene; Southland, New Zealand. (Subsection 11.5.5.3.).

B. Growth-line frequency distribution prepared from 776 measurements taken from 55 specimens of Magellania venosa (Solander); Recent; Strait of Magellan, S.America. (Subsection 1I.5.2.5.). 15- Y C 10- EN FREQU 5-

A AA 15 25 10 20 30 315 40 45 50 DISTANCE TO GROWTH-LINE (mm) A

Ji\t

5 i5 215 35 1 10 20 30 40 45 50 DISTANCE TO GROWTH-LINE (mm) B

214

II.5.2.6. Gyrothyris mawsoni antipodesensis, Foster

MATERIAL: Location - 49° 40'S, 178° 53'E, to 49° 40'S, 178° 54'E, off Antipodes Island; Depth 476 - 540 metres. The collection is housed in the USNIvI, Washington, DC, (USNM 550147). A total of 50 specimens were examined, and 576 growth-lines measured.

The modes in the growth-line frequency diagram prepared for this species (Fig.26) indicate a biannual pattern of growth-line formation, and an annual growth rate very similar to that of T.retusa, as is clear from the following comparison:-

TABLE XIII Comparison between G.mawsoni antipodesensis and T.retusa; data in mm.

G.mawsoni antipodesensis T.retusa 2.75 - 1(a) 2.75 4.75 - 1(b) 4.25 5.75 - 2(a) 6.75 8.25 - 2(b) 8.25 10.75 - 3(a) 10.25 12.25 - 3(b) 11.75 13.25 - 4(a) 14.25i 14.75 15.75 - 4(b) 17.25 - 5(a) .25 18.75 - 5(b) 17 22.25 - 6 19.75 24.25 - 7 21.50 25.75 - 8 ? 28.00 - 9 ? 29.75 - 10 ? 215

EXPLANATION OF TEXT-FIG. 26.

Growth-line frequency distribution prepared from 576 measurements taken from 50 specimens of Gyrothyris mawsoni antipodesensis, Foster; Recent; Antipodes Island. (Subsection II.5.2.6.). 15 U Z LLI M 10 c% LUJ M LL 5

DISTANCE TO GROWTH-LINE (mm) 217

The great similarity between the growth strategy of the two species is a significant feature, bearing in mind the deep-water southern hemisphere habitat of G.mawsoni antipodesensis. The indication that continental shelf conditions, as recognised by their effect on growth strategy, persist to a depth of at least 500 metres confirms a similar conclusion reached from the growth-line analysis of the extremely large specimen of L.neozelanica (Subsection II.5.2.4.). The specimens of G.mawsoni antipodesensis examined during this study appear to have an approximately linear growth strategy, and a life span slightly in excess of 10 years is evident from Table XIII.

II.5.3 RECENT POLAR BRACHIOPODS

II.5.3.1. Liothyrella uva notorcadensis (Jackson)

MATERIAL: Location 64° 46'S, 064° 03'W, OREGON STATE UNIV. Stn. AH4-80, Arthur Harbor, (nr Palmer Station), ANTARCTIC PENINSULA, Antarctica; Depth - 24 metres; The sample was collected by divers on 26th January 1969, and is now housed in the USNM, Washington, DC. A total of 73 specimens were examined and 592 growth-lines measured.

The significant feature of the growth-line frequency diagram prepared for L.uva notorcadensis is the large number of closely spaced modes- a much greater number than in similarly-sized specimens from temperate latitudes (Sections II.5.1. and II.5.2.). Thus the successive spacing between 218

EXPLANATION OF TEXT-FIG. 27.

Growth-line frequency distribution prepared from 592 measurements taken from 73 specimens of Liothyrella uva notorcadensis (Jackson); Recent; Antarctic Peninsula, Antarctica. (Subsection II.5.3.1.).

15 I .;\ / \/\k

5 lb 15 20 2'5 30 315 DISTANCE TO GROWTH-LINE (mm) 220

the modes in this distribution (Fig.27) is as follows (in mm):- 1.5, 1.0, 1.0, 2.25, 1.25, 1.5, 2.5, 2.0, 1.0, 1.5, 1.5, 1.5, 2.0, 2.0, 1.0, 1.0, 1.0, 2.5, 3.25, 1.25, 1.5, (mean = 1.62mm; S.D. = 0.62mm). These modes have a roughly uniform spacing, which is in contrast to the alternating pattern of summer and winter increments determined for many of the temperate latitude species studied. The large number of growth-lines, and their approximately uniform spacing, suggests that growth-lines form annually and that L.uva notorcadensis has a reduced annual growth rate in comparison with equivalent temperate latitude species. A reduced growth rate, often combined with increasing longevity, has long been recognised as characteristic of marine invertebrates from polar habitats. As discussed in Section I.3.3., the rate of metabolic activity, including the processes of shell secretion, feeding, etc., is greatly reduced at low temperatures. Combined with reduced availability of nutrients, the effect of such a phenomenon during the prolonged and severe polar winter will be the total cessation of shell secretion and greatly reduced feeding and digestive activity - a state analogous to hibernation in other groups. The pedicle of L.uva notorcadensis emerges posteriorly from a labiate pedicle foramen, which facilitates reorientation of specimens which are tethered, rather than supported, by their long thick pedicle (see frontispiece in Foster, 1974). As a result there has been considerable resorption of the ventral umbo, with as much as 8mm of shell length having been removed in adult specimens. An attempt to compensate for the shell material removed, by the method described in Section 221

EXPLANATION OF TEXT-FIG. 28.

Compensated growth-line frequency distribution (see Section II.3.2.) prepared from 592 measurements taken from 73 spec- mens of Liothyrella uva notorcadensis (Jackson); Recent; Antarctic Peninsula, Antarctica. (Subsection II .5.3.1.). 70-1 1

1 5- I 4

5 10 15 20 25 30 35 40

DISTANCE TO GROWTH-LINE (mm) 223

II.3.2., did indicate that juvenile growth proceeds at a slightly greater rate than indicated by the mean value of 1.62mm (Fig.28). The available data suggests that L.uva notorcadensis has a maximum life span of 25 years in this locality.

II.5.3.2. Magellania fragilis Smith

MATERIAL: Location - 78° 23.8'S, 169°W, to 78° 23.7'S, 168° 59'W, ROSS SEA,Antarctica; Depth - 562 - 564 metres; Substrate - fine sediment with a few pebbles. The collection is housed in the USNM, Washington, DC, (USNM 550185). A total of 70 specimens were examined and 833 growth-lines measured.

Magellania fragilis, Smith, is the most abundant brachiopod in the Ross Sea (Foster, 1974), and the sample studied was dredged from a deep-water habitat close to the seaward margin of the Ross Ice Shelf. As in L.uva notorcadensis (Subsection 11.5.3.1.) the growth-line frequency diagram prepared from these specimens (Fig.29) is characterised by a large number of closely-spaced modes. The spacing between successive modes, in mm, is as follows:- 1.5, 1.5, 1.5, 1.0, 1.5, 1.5, 2.5, 2.0, 2.0, 1.5, 1.5, 1.0, 1.5, 1.5, 1.0, 1.0, 2.0, 1.5, 2.75, 2.5, 1.5, 1.0, 1.5, (mean = 1.60mm; S.D. _ 0.49mm). The pattern of growth-line formation, and their spacing, is virtually identical to that determined for L.uva notorcadensis, confirming the total cessation of growth during the prolonged antarctic winter (the Ross Sea is ice- 224

EXPLANATION OF TEXT-FIG. 29.

Growth-line frequency distribution prepared from 833 measurements taken from 70 specimens of Magellania fragilis, Smith; Recent; Ross Sea, Antarctica. (Subsection 11.5.3.2.). / I I I 15- I

U Z LIJ J 10- \/\ a / Lt L J 1. / I 1/ 5- I

10 15 20 25 30 35 40

DISTANCE TO GROWTH-LINE (mm) 226 covered for nine months of the year). Growth-lines, therefore, most probably form annually, and the data from Fig.29 suggests that M.fragilis lives for approximately 25 years. Foster (1974),in his comprehensive survey of Recent Antarctic brachiopods, states that Liothyrella blochmanni Jackson, collected at depths of 1058 - 3697 metres off the Ross and Weddell seas, has "numerous very fine growth-lines", and it is clear that many Recent Antarctic species, from both shallow and deep-water habitats, show a similar pattern of closely-spaced growth-lines (i.e. Plate 20,21, in Foster, 1974).

II.5.4. RECENT ABYSSAL BRACHIOPODS

II.5.4.1. Macandrevia bayeri, Cooper_

MATERIAL: Location - 4°58'N, 3° 48'E, to 4° 52'N, 3° 48'E, south-east of Porto Novo, Dahomey, West Africa; Depth - 2268 - 2332 metres; The collection is housed in the USNM, Washington, DC. A total of 46 specimens were examined and 521 growth-lines measured. (Fig.30)

The growth-line frequency diagram prepared for M.bayeri is very similar to that prepared for the two antarctic species studied, i.e. with a large number of closely-spaced modes. The spacing between the modes in the former distribution is as follows (in mm) :- 1.5, 1.0, 1.5, 1.0, 1.0, 2.0, 2.0, 2.0, 1.5, 1.5, 1.5, 1.0, 1.0, 1.5, 1.0, 1.5, (mean = 1.41mm; S.D. = 0.38mm). Clearly there is no pattern of alternate 227

EXPLANATION OF TEXT-FIG. 30.

Growth-line frequency distribution prepared from 521 measurements taken from 46 specimens of Macandrevia bayeri, Cooper; Recent; off Porto Novo, West Africa. (Subsection II.5.4.1.). A I 10 15 20 25

DISTANCE TO GROWTH-LINE (mm)

iv N co 229

summer and winter growth increments, indicating that growth- lines form annually. The obvious similarity between the pattern of growth-line formation in this species and that of the two polar species examined (Section II.5.3.) is not surprising, as the abyssal and high latitude environments have many features in common; in both habitats temperatures are generally low, food supplies commonly impoverished, and the solubility of calcium carbonate is high. The fact that growth-lines are uniformly spaced, even on specimens from 2268 - 2332 metres, indicates that there are regular disturbances even at this great depth. Whether such disturbances are related to food supply fluctuations, periodic breeding, or other factors, is unknown, but some bivalves from similar deep-water habitats also display 'seasonality', despite the fact that pronounced seasonal variations in environmental conditions are almost certainly absent at such depths. It has been suggested that this seasonality may be a reflection of the shallow water origin of some deep sea species which, having moved into deep-water habitats in geological recent times, still retain the seasonal behavioural rhythms although the environmental stimuli for such periodic activity are absent. Despite the fact that this population was collected close to the equator, the above described growth strategy can not be considered as characteristic of tropical brachiopods, because the prevailing environmental conditions are abyssal, rather than tropical, in aspect. 230

Section 1I.5.5. FOSSIL BRACHIOPODS

II.5.5.1. Magadina sp.

MATERIAL: Horizon - Miocene; Location - South Canterbury, South Island, New Zealand. The specimens examined were from the R.S.Allan Collection housed in the Dept. of Geolo , University of Canterbury, Christchurch, New Zealand, UC - 28112). A total of 58 specimens were examined and 244 growth-lines measured.

The specimens of Magadina sp. examined attain a maximum size of approximately 10mm. Growth-lines were measured on the ventral valve as is customary, but because of the small maximum size of these specimens a grouping of 0.2mm was used in the preparation of the growth-line frequency diagram (Fig. 31), rather than the more usual 0.5mm grouping. The modes in Fig.31 have been analysed in the usual manner in the following table:-

TABLE XIV Analysis of the modes in the growth-line frequency diagram of Magadina sp; Miocene, New Zealand; data in mm.

MODES INCREMENT 1.35 1.0 2.35 0.8 3.15 1.0 4.15 0.8 4.95 1.4 6.35 0.6 6.95 1.0 7.95 0.6 8.55 231

EXPLANATION OF TEXT-FIG. 31.

Growth-line frequency distribution prepared from 244 measurements taken from 58 specimens of Magadina sp.; Miocene; South Canterbury, New Zealand. A grouping of 0.2mm was used in the preparation of this distribution (see Subsection 11.5.5.1.). 15

I I I I 2 I I 3 4 5 6 7 8

DISTANCE TO GROWTH-LINE (mm) 233

Unfortunately detailed locational information for these specimens is unavailable, but evidence for a temperate latitude habitat survives enshrined in the pattern of growth-line formation. As described in Sections II.5.1. and II.5.2., many living brachiopods from temperate latitude habitats display a biannual pattern of growth-line formation, with alternate relatively large summer growth increments and smaller winter growth increments. Exactly the same pattern is apparent in Table XIV (i.e. column 2). The available data indicates that Magadina sp had an approximately linear growth strategy, and a life span of 5 years.

II.5.5.2. Bouchardia antarctica, Buckman

MATERIAL: Horizon - La Meseta Formation (Miocene); Location - Seymour Island, Antarctica; The specimens were collected by staff members from the Institute of Polar Studies and Dept. of Geology, The Ohio State University, Columbus, Ohio, (Localities T-30 and IPS-22), and were examined whilst the collections were in the care of Mr. E.F.Owen, Dept. of Palaeontology, British Museum (Natural History), London. A total of 54 specimens were examined from the two localities and 244 growth-lines measured.

All specimens of this species examined display a number of regularly spaced and prominently developed growth-lines. Whilst being generally well preserved, a number of specimens had damaged or sediment-encrusted ventral valves, and consequently it was decided to measure the growth-lines on the dorsal valve. Such a procedure was acceptable as the primary aim of this analysis was to compare the growth history of 234

EXPLANATION OF TEXT-FIG.32.

A. Growth-line spacing in two populations of Bouchardia antarctica, Buckman; Miocene; Seymour Island, Antarctica. A total of 244 growth-lines were measured on the dorsal valves of 54 specimens.

B. Growth curves for the two populations of B.antarctica as determined from growth-line analysis.

(Subsection II.5.5.2.). 235

T-30 - IPS22 ----

5—

1 1 i i i 1 2 3 4 5 A MM.

T-30 ----- IPS-22

1 I I 1 2 3 4I 6

AGE (yrs) B 236

of two populations rather than to rationalise the growth strategy and pattern of growth-line formation in terms of the maximum (i.e. ventral) shell length. The two samples were collected from two horizons within the same section (vertical separation of approx. 120 metres). and are clearly con-specific (E.F.Owen, oral comm, 1979) but the specimens from the upper (T-30) locality were of much greater maximum length than those from IPS-22. The distance between each growth-line on the dorsal valve was measured, and the average growth-line spacing for each specimen was calculated. The resulting data, for each of the populations, was then plotted as a frequency distribution (Fig.32,A). Fig.32,A clearly illustrates that the difference in maximum size between the two collections is due to a significant difference in the annual rate of shell growth (i.e. Fig.32,B) rather than a different growth strategy or life span. Spec- imens from T-30 had an average annual growth rate of 2.75mm, whilst the IPS-22 specimens grew, on average, by 1.75mm.per year (dorsal valve measurements). Both populations had an identical growth strategy, (i.e. approx. linear - Fig.32,B), and an identical life span of 7 - 8 years. The fact that the growth-lines on all specimens of B.antarctica examined are evenly spaced indicates an annual pattern of growth-line formation, similar to that found in present day polar (Section II.5.3.) and abyssal (Section II.5.4.) brachiopod populations. An abyssal habitat for B.antarctica seems unlikely, but a relatively cold, shallow water habitat is a distinct possibility, especially as the progressive cooling of climatic conditions, culminating in 237

the formation of the antarctic ice-cap, was initiated during the Miocene. The difference in growth rate between the two samples is a reflection of the amelioration of the environmental conditions affecting brachiopod growth, which were relatively unfavourable at locality IPS-22, and significantly more conducive at the younger T-30. Possible explanations for such a phenomenon are a decrease in the rate of sedimentation, reduced water turbulence, increased food supplies, or perhaps an increase in the average annual temperature (possibly a localised or short duration oscillation superimposed on the inferred long-term pattern of decreasing temperature) .

11.5.5.3. Pachymagas sp.

MATERIAL: Horizon - Balfour Limestone, Waitakian (Lower Miocene); Locality - Balfour Quarry, Southland, New Zealand. The specimens examined were from the R.S.Allan Collection housed in the Dept. of Geology, University of Canterbury, Christchurch, New Zealand, (UC 26000 to 26124). A total of 113 specimens were examined and 714 growth-lines measured.

Utilizing a lmm grouping in the preparation of the growth-line frequency diagram for this species, prominent modes with an average spacing of 3 - 4mm are apparent, i.e. (in mm) :- 5.5, 8.5, 11.5, 16.5, 20.5, 23.5, 26.5, 30.5, 33.5, 38.5, 42.0, 45.5,48.5, (mean spacing between modes = 3.6mm). Figure 25,A was prepared using a grouping of 0.5mm and a more detailed picture of the pattern of growth-line 238

formation emerges. The following modes are discernible (in mm) in Fig.25,A (the values in brackets correspond to the modes from the lmm grouping listed above) s- 4.75, (5.75), 7.25, (8.25), 10.25, (11.75), 13.75, 15.25, (16.75), 19.75, (20.75), 21.75, (23.75), (26.75), 28.25, (30.75), (33.75), 35.25, 36.25, (38.25), 40.0, (42.25), 44.25, (45.75), 47.75, 50.75, 53.75. Additional modes, intersp- ersed between those listed on the previous page, indicate that growth-lines form bianually, suggesting a shallow-water temperate latitude habitat for these specimens. This is in keeping with the sedimentological,palaeo-latitude, and faunal assemblage data available for the New Zealand Miocene. The consenus of opinion is that marine conditions during the deposition of the fossiliferous New Zealand Miocene were essentially similar to those prevailing on the present day New Zealand continental shelf, although possibly with slightly higher average annual temperatures. Therefore the similarity in the pattern of growth-line formation between Recent New Zealand populations (Section II.5.2.) and the two Miocene populations studied (Section II.5.5.) is not surprising. 239

II.6. DISCUSSION

The major conclusions of this study are that growth- lines form at biannual or annual intervals, and that such a pattern can be recognised using suitable cumulative methods of analysis. In temperate latitudes, down to depths of at least 500 metres, biannual or annual growth-lines form; the latter being, in effect, a special case of the former, due to the total cessation of growth during winter because of unfavourable environmental conditions. In polar latitudes the severity of winter conditions restricts shell growth to a relatively short summer period, resulting in evenly spaced annual growth-lines; the generally low temperatures, reduced food supply, and short growth season, result in a reduced annual growth rate as compared with equivalent temperate latitude species. The latitudinal 'control' on growth strategy breaks down in abyssal habitats, and uniform closely-spaced growth-lines, interpret led as representing an annual periodicity, have been recognised in the one abyssal population studies. Growth-line formation is clearly intimately associated with spawning activity in many species, although it has yet to be determined if biannual growth-lines necessarily prove biannual spawning. Despite this apparent correlation it would be erroneous to consider growth-lines as ' spawning lines' as they form in sexually immature, and therefore non- spawning, juveniles; growth-lines can, however, confidently be correlated with periods of major environmental disturbance in most species studied. The interpretation of growth-line periodicity in terms 240

of prevailing environmental conditions is a reasonable pro- prosition, one which is probably beyond dispute. The major stumbling-block in attempting to make use of such a precise palaeoecological indicator as the pattern of growth-line formation has always been the lack of empirical data on living populations, and the difficulty caused by disturbance- lines. Certainly it was apparent during this study that the pattern of growth-line formation is commonly imperfectly preserved on a single specimen, and that without 'control' data it was impossible to analyse an individual's growth history. However during this study it was possible to carry out a long-term ecological, biological, and growth rate study of an abundant subtidal population, and subsequently to rationalise the pattern of growth-line formation in this species on the basis of precise empirical data on its life history and habitat. The results of this study provided the 'control' data necessary for wide-ranging growth-line analysis of populations for which confirmatory ecological, biological, and growth rate data was often not available. The procedure of utilizing bulk samples for analysis was clearly successful, and the 'frequency diagram' method of graphically compiling the resulting data greatly facilitated the interpretation of growth strategy. Whenever possible, the results of the growth-line analyses were compared with available data on the ecology,biology, and growth rate of the species under investigation; whilst such information is sparse, it was encouraging that the conclusions reached from growth-line analysis were confirmed. Certainly there are many gaps in our understanding of 241 the processes, causes, and significance of growth-line formation; future advances in our knowledge on these topics require detailed and exhaustive research in many fields. The advantages of multi-disciplinary approaches have been well illustrated in many scientific fields; the breakdown of traditional barriers between previously isolated disciplines has been one of the most welcome developments in modern scientific endeavour. Thus the future development of brachiopod growth-line studies will, hopefully, involve physiological experimentation, combined with ecological investigations and growth-line analyses of living and fossil, articulate and inarticulate, species, from all latitudes and habitats. The applications of the results of such a co-ordinated and intensive research programme will be manifold. Williams has shown that, throughout their geological range, the growth of the brachiopod shell, which may vary considerably in ultrastructural composition and complexity, is interpretable in terms of a basic growth model. The relationship between environmental conditions and the pattern of growth- line formation is fundamental, and not just for brachiopods. There are certainly methodological problems to be faced in the analysis of growth-lines from fossil populations, although none should prove unsurmountable. The recovery of specimens from the rock matrix may on occasions prove difficult; however the great potential of this form of analysis may warrant the longitudinal sectioning of a suitable number of embedded specimens - growth-lines are clearly marked within the shell fabric in all but the most distorted and poorly preserved specimens, and therefore can either be measured 242 directly or from cellulose acetate peels. The processes of measurement and data compilation could be automated - digital calipers, yielding an electrically-encoded reading, could be linked, via a foot control, to a mini-computer, and each measurement entered and processed immediately, and the progression of modes monitored. Growth-line analysis, combined when appropriate with data from length-frequency diagrams, is potentially one of the most informative and precise methods of palaeoecological reconstruction, providing data on the ecology and biology of the organism, on its habitat, and on the geographical extent of palaeo-climatic zones. Certainly there can be no more precise reflection of prevailing palaeo-environmental conditions than the organism which experienced them, and which entombed periodic markers in a diagnostic pattern within their shell fabric. 243

APPENDIX I THE N.ATLANTIC SPECIES OF TEREBRATULINA

Representatives of the genus Terebratulina have been present in the N.Atlantic since the Cretaceous, and their gross morphological characteristics have changed little up to the present day, when the genus is found from the Mediterranean to Scandanavia, around Iceland and Greenland, and along the north-east coast of N.America. It became clear when attempting to delineate the geographic range of Terebratulina retusa (Linnaeus), the species under investigation off the west coast of Scotland, that the literature provided no objective criteria for distinguishing between T.retusa and the morphologically- similar T.septentrionalis from the east coast of N.America. Comparison between the available specimens of the two species indicated that such criteria did exist:- T.retusa having diagnostic postero-lateral pustules (Plate 1,B; 10,E), and stat- istically coarser external ribbing (see Appendix IV). In addition there appears to be differences is shell proportions:- T.retusa from the Firth of Lorne (Scotland) being of greater height and width, in relation to length, than specimens of T.septentrionalis from a broadly similar N.American habitat (Fig.33, A-D). Whilst the morphological differentiation between the two species is clear and unequivocal, it seems probable that the difficulty in determining their geographic range within the N.Atlantic is due to a transatlantic gradation of morphological characteristics (i.e. a cline). Certainly the ornamentation and overall shape of the shell are features which are 244 likely to vary depending on prevailing environmental conditions. T.retusa can be considered as a 'warm-water' species, inhabiting regions along the north-east margin of the N.Atlantic which are affected by the warm waters of the North Atlantic Drift Current, whilst there is a good correlation between the distribution of T.septentrionalis along the east coast of N.America and the area affected by the cold-water Labrador Current. Thus the shells of specimens from the northern margin of the N.Atlantic and the Mediterranean, regions subjected to different environmental conditions, will vary in shape and ornamentation, and hence the confusion as to the precj'ce_.geographic range of the two species. 245

Y = 0.43X -0.44 r•0.972 11 n • 179 E Y= 0.49X-0-111 r = 0.988 ia n•206 i 5

10 15 20 25 10 15 A 5 Length [mm] 6 l~n,th [mm]

Y • 0-80X -0-2 r•0.989 20- n•179

15 Y =0.83X-0.25 r = 0.990 n • 206 Ē1 E s 3 5- 5

5 10 15 20 25 5 10 15 C Luth [mm] D Length [mm]

EXPLANATION OF TEXT-FIG. 33.

A,C. Length - height and length - width scatter diagrams •(respectively) of 179 specimens of Terebratulina septentrionalis (Couthouy); Recent; off Nova Scotia, USA.

B,D. Length - height and length - width scatter diagrams (respectively) of 206 specimens of Terebratulina retusa (Linnaeus); Recent; Firth of Lorne, Scotland. 246 APPENDIX II

FREE-LYING BRACHIOPODS - THE EVOLUTIONARY IMPLICATIONS

MATERIAL: Identification - Terebratulina septentrionalis (Couthouy); Horizon - Recent; Location - 43° 34'N, 63° 56' 30"W, (off Nova Scotia), 'ALBATROSS' Stn. 2513; Depth- 241 metres (134 fms); Collected 11th July 1885; Surface temp. 14.4°C (56°F), Bottom temp. 6.4°C (43.6°F); Sediment- 'gray ooze'. This collection, of at least 1,000 specimens, is preserved in alcohol, and housed in the Dept. of Paleo- biology, Smithsonian Institution, Washington, DC, USA. (USNM 551142).

A major problem in palaeoecology is to explain the occurrence of large numbers of undisturbed pedunculate brachiopods in areas where suitable hard substrate for attachment was sparse. No doubt a proportion of these specimens had, in life, been attached to each other or to non- preserved, unmineralised, organisms or plants; certainly a small proportion of the T.retusa specimens collected from off the west coast of Scotland were attached to sponges, hydroids, etc. Yet such a mode of life can scarcely explain the widespread occurrence of fossil pedunculate brachiopods in rocks formed from fine-grained sediment and lacking readily-apparent substrate. The recent population described below provides an important insight into a possible mode of life for such enigmatic populations. The majority of these specimens are attached to narrow tapering scaphopod shells (Dentalium sp.) by an intricate network of pedicle rootlets (Plate 16, A-C; 17,C). Pedicle rootlets are a common feature in many species of Terebratulina, but are particularily well-developed in these specimens of

T.septentrionalis (Plate 16,E). The scaphopod shells are rather unsuitable substrate, being narrow and of small surface 247

area, and presumably the encircling network of rootlets (which, distally, bore into the scaphopod shell) ensures a firmer attachment than would be possible with a less-branched pedicle. Internal tissues are preserved in some of the scaphopods, indicating that they were alive when collected, and certainly many of the brachiopods were attached to the tapering anterior region of the scaphopod which, in life, would have protruded above the sediment (Plate 16,B). The palaeoecological significance of this collection, however, stems primarily from the discovery of specimens which clearly were alive when collected, and which had been free- lying on the sea-floor (Plate 16,D). Some small fragments (primarily of scaphopod shell) are enmeshed within the pedicle rootlets of some of these specimens (Plate 17,B), suggesting that they became free-lying because of the disintigration of their substrate. However the rootlets networks of other specimens are devoid of any such fragments (Plate 16,D; 17,E), and it is clear that these specimens relied solely on their pedicle networks, and the sediment trapped by them, for anchorage. Laboratory experiments with the closely related species T.retusa have shown that free-lying specimens will survive provided the anterior commissure is unobstructed. There- fore it is reasonable to assume that these free-lying specimens of T.septentrionalis were lying, either on their dorsal or ventral valves, in a slightly posterior-downwards orientation, and perhaps partially buried. Such an interpretation is confirmed by encrusting sponges on some specimens, which delineate their position relative to the sediment-water inter- face (Plate 17,B). The ability to rotate around their point 248 of attachment, a frequently-observed movement in attached specimens of T.retusa, will obviously be curtailed in such an orientation, but this ability is probably of minimal importance in this offshore, low-energy, habitat where the fine- grained sediment accumulates slowly. Certainly the environmental and biological disturbances which induce rotational movements in attached brachiopods are likely to be less frequent than in high-energy intertidal or shallow subtidal habitats with high sedimentation rates. There is some indication that this free-lying mode of life is 'self-perpetuating' as, due to the limited availability of hard substrate, the larvae of T.septentrionalis settle on the pedicle rootlets of free-lying adults (Plate 17,D,E). Subsequently the rootlet network which provided a substrate for the larva will be strengthened by the interdig- itation of the developing rootlets of the newly-settled specimen; these new rootlets will compensate for the decaying rootlets of dead specimens , and the continually refurbished pedicle network will 'survive' long after the original specimens have disappeared. A remarkable feature of this population is that the pedicle morphology of individual specimens varies considerably (Plate 17,A0E) depending on the nature, or absence, of substrate. It is tempting to regard such extreme variation in 'attachment' strategy as an example of 'evolution in action'. A further reduction in the available hard substrate would result in the predominance of the free-lying mode of life. Subsequently, over many generations, evolutionary processes will favour specimens with posteriorly-thickened shells 24.9

(which settle in an ideal feeding orientation when free-lying without recourse to an anchoring mechanism); the atrophied, non-functional, pedicle observed in one of the free-lying specimens of T.septentrionalis is, perhaps, an indication of the early stages of such a development. The posteriorly- weighed shells and atrophied (?) pedicles of Recent species of Gryphus and Neothyris could be interpreted as a more advanced stage of a similar evolutionary trend. Clearly the extent of morphological adaptation depends on the prevailing environmental conditions; the Recent free-lying and posteriorly- weighted species Magadina cumingi (Davidson) has adapted to a high energy environment by developing a retractable pedicle (significantly with short distal rootlets) which allows disturbed specimens to re-orientate within their gravel substrate (Richardson and Watson, 1975). Similarly the inferred free- lying, quasi-infaunal, mode of life of thick-shelled adult productaceans is facilitated by supportive spines (Brunton,

1965). There is good evidence, therefore, that this evolutionary scenario, from attached to free-lying and perhaps vice versa, has occurred in many brachiopod stocks and at various stages throughout the geological history of the phylum. 250

APPENDIX III

COMMENTS ON THE FUNCTION OF CAECA

During investigation of the shell structure of Recent brachiopods, using electron microscopy techniques, some microscopic circular borings, on average 3 microns in diameter, were observed on the external surface of the New Zealand species Terebratella sanguinea (Leach). These micro-borings are thought to have been the work of microscopic algae which derive their energy from carbon dioxide produced by the dissolution of calcium carbonate during their boring activity.. The significant feature of these micro-borings is that, whilst being so concentrated in some regions of the shell as to have completely destroyed the external surface of the primary layer (Plate 14,F; 15,B,C), they are absent from adjacent areas of shell which are permeated by the minute extensions of the caeca. Caeca are microscopic outgrowths of mantle which are housed in cylindrical tubes within the shell material (the endopunctae - Plate 14,A), and are connected to the outermost periostracum by a number of minute canals (collectively known as the brush) which impart a 'porous' texture to the thin layer of primary shell material (the canopy) which overlies the distal portion of each caecum

(plate 15,A). The fact that the endopunctal canopies survive intact in even the most densely bored regions of the shell (Plate 14,F; 15,B,C) suggests that the boring activity of the algae was greatly inhibited by compounds contained within the canals 251 of the caecal brush. Mucopolysaccharide has been identified within these canals by Owen and Williams (1969), who were the first to suggest that this compound may inhibit boring; the disposition of these micro-borings provides strong empirical confirmation for such a function. However there seems little doubt that the caeca are multi-purpose, and it has already been suggested that they function as nutrient storage centres (Owen and Williams, 1969; Subsection I.5.2.2.). With this consideration in mind the author compared the fecundity of two similarly-sized species from the Lyttelton Harbour rockpool, nr. Christchurch, New Zealand, both of which produce ova of comparable size. A single mature specimen of the endopunctate Terebratella inconspicua (Sowerby) contains, on average 18,000 - 20,000 ova, almost double the number contained within specimens of the impunctate (= lacking endopunctae) Notosaria nigricans (Sowerby). It is tempting, if somewhat premature, to interpret the reduced fecundity of the impunctate species in terms of an inability to store nutrients to the same extent as the endopunctate species. The specimens were examined during the southern spring (November) and the gametes observed had therefore developed during the winter months when external food sources are reduced; the fact that the endopunctate T.inconspicua could withdraw nutrients stored within its caeca during the previous summer may explain the greater fertility of this species. Impunctate brachiopod stocks would, therefore, be at a significant disadvantage in habitats subjected to seasonal fluctuations in nutrient supply, which would have far reaching implications for the interpretation of the 252 geographic range and evolutionary history of impunctate brachiopods. However a precise correlation between caecal content and gametogenesis has yet to be demonstrated.

APPENDIX IV

'BRITISH BRACHIOPODS'

A synopsis prepared in conjunction with C.H.C.BRUNTON

SEE INSIDE BACK COVER 253

ANSELL, A.D. and PARULEKAR,A.H., 1978. On the rate of growth of Nuculana minuta (Mailer) (Bivalvia, Nuculanidae). J. moll. Stud., Vol. 44, 71 - 82.

ATKINS,D, 1959. The growth stages of the lophophore of the brachiopods Platidia davidsoni (Eudes-Deslongchamps) and P.anomioides (Phillippi), with notes on the feeding mechanism. J. mar. biol. Ass., U.K. Vol 21, 103 - 132.

BIERNAT, G. and WILLIAMS,A. 1970. Ultrastructure of the protegulum of some acrotretide brachiopods. Palaeontology, Vol. 13, (3), 491 - 502.

=NO ENO , 1971. Shell structure of the siphonotretacean Brachiopoda. Palaeontology, Vol. 14, (3), 423 - 430.

BRUNTON, C.H.C., 1965. The pedicle sheath of young product- acean brachiopods. Palaeontology, Vol. 7, (4), 703-4.

, 1969. Electron Microscope studies of growth margins of Articulate brachiopods. Z.Zellforsch., Vol. 100, 189 - 200.

,1975. Some lines of Brachiopod research in the last decade. Palāont. Zeit., Vol. 49, (4), 512 - 529.

,COCKS,L.R.M., and DANCE,S.P., 1967. Brachiopods 254

in the Linnaean Collection. Proc. Linn. Soc. Lond., Vol. , (2), 161 - 183.

BRUNTON, C.H.C., and CURRY, G.B., in press. British Brachiopods. Synopsis of the British Fauna, Linnean Soc. and Academic Press, London. 65 pp.

CHUANG,S.H., 1959(a). The structure and function of the Alimentary canal in Lingula unguis (L.), Brachiopoda. Proc. zool. Soc. Lond., Vol. 12g, (2), 283 - 311.

MD =ID 1959(b). The Breeding Season of the Brachiopod Lingula unguis (L.). Biol. Bull., Vol. 117, (2), 202 - 207.

MN Mr , 1961. Growth of the post-larval shell in Lingula unguis (L.). Proc. zool. Soc. Lond., Vol. 12z, 299 - 310.

COMELY, C.A., 1978. Modiolus modiolus (L.) from the Scottish West Coast. I, Biology. Ophelia, Vol. 17, (2), 167 - 193.

CRAIG,G.Y. and HALLAM,A., 1963. Size-frequency and growth- ring analysis of Mytilus edulis and Cardium edule, and their Palaeoecological significance. Palaeontology, Vol. 6, (4), 731 - 750.

and OERTEL,G., 1966. Deterministic models of 255

living and fossil animals. Q. Jl. geol. Soc. Lond., Vol. 122, (3), 315 - 355.

CRISP,D.J., 1976. Settlement responses in marine organisms. in Adaptations to Environment (Ed. R.C.NEWELL). Butterworths; London, Boston.

,and MEADOWS,P.S., 1962. The chemical basis of gregariousness in cirripedes. Proc. Roy_. Soc. Lond., ser. B, Vol. 116., 500 - 520.

AMD MN , 1963. Adsorbed layers: the stimulus to settlement in barnacles. Proc. Rost. Soc. Lond., ser. B, Vol. , 364 - 387.

DALL,W.H., 1920. Annotated List of the Recent Brachiopoda in the U.S. National Museum, with Descriptions of 33 new forms. Proc. U.S. National Museum, Vol. 57, 261 - 377.

DAVIDSON,T., 1886 - 1888. A monograph of Recent Brachiopoda. Trans.Linn. Soc., ser. 2, Vol. 4, pts. I - III.

DOHERTY,P.J., 1976. Aspects of the feeding Ecology of the brachiopod Terebratella inconspicua (Sowerby). MSc. thesis, Auckland Univ., New Zealand.

, 1979. A Demographic Study of a Subtidal Pop- ulation of the New Zealand Articulate Brachiopod Terebratella inconspicua. Marine Biology, Vol. 52., 256

(4), 331 - 342.

FOSTER,M.W., 1974. Recent Antarctic and sub-antarctic Brachiopods. Antarctic Research Series, Vol. 21, American Geophysical Union, 189Pp.

GURR,P.R. and PENN,J.S.W., 1971. On the feeding activity of Terebratulina retusa Linn and its possible significance. Zool. J. Linn. Soc., Vol. 50, (4), 449-454.

HANCOCK,A., 1859. On the organisation of the Brachiopoda. Phil. Trans., 148, 791 - 869.

JOUBIN,L., 1886. Recherches sur l'anatomie des Brachiopodes Inrticu1es, Arch. Zool. Exp.. Gen., ser. 2, Vol. 4, 161 - 303.

KING,J.M. and SPOTTE,S., 1974. Marine Aquariums in the Research Laboratory. Aquarium Systems, Ohio.

KIRSTENSEN,J.,1959. The coastal waters of the Netherlands - as an environment of mollusca life. Basteria, Vol. 23, 18 - 55.

LaBARBERA,M., 1977. Brachiopod orientation to water movement. I; Theory, Laboratory behaviour, and field orientations. Paleobiology, Vol. 3, (3), 270 - 287.

LUTZ,R.A. and RHOADS,D.C., 1977. Anaerobiosis and a theory 257

of growth-line formation. Science, Vol. 122, 1222 - 27.

McCAMMON,H.M., 1972. Establishing and maintaining Articul- ate Brachiopods in Aquaria. J. geol. Educ., May 1972.

, and REYNOLDS,W.A., 1972. Implications of the brachiopod lophophore as an organ of nutrient assimilation. Abs. Geol. Soc. Amer., Vol. 4, (7), p. 587.

MACKAY,S., and HEWITTR.A., 1978. Ultrastructural studies on the brachiopod pedicle. 1,ethaia, Vol. 11, 331 - 339.

MACKINNON, D.I., 1974. The shell structure of Spiriferide Brachiopoda. Bull. Br. Mus. (Nat. Hist.), Vol. 25, no. 3, 187 - 261.

, and WILLIAMS,A., 1974. Shell structure of Terebratulid brachiopods. Palaeontology, Vol. 17, (1), 179 - 202.

MARGALEF,R., 1977. Ecosystem Diversity Differences: Polar and Tropics. in Polar Oceans (Ed. Dunbar), publ. Arctic Institute of N.America, Calgary.

MOORE,H.B., 1958. Marine Ecology. John Wiley and Sons, New York.

MORSE,E.S., 1871. On the early stages of Terebratulina septentrionalis. Mem. Boston Soc. Nat. Hist.,II(I).,

258

29 - 39.

MORSE,E.S., 1873. Embryology of Terebratulina. Mem. Boston Soc. Nat. Hist., II, 249 - 264.

aMM , 1902. Observations on living Brachiopoda. Mem. Boston Soc. Nat. Hist., V, 313 - 386.

NEALL,V.E., 1970. Notes on the ecology and paleoecology of Neothyris, an endemic New Zealand brachiopod. N. Z. J1. mar. freshw. Res., Vol. 4, 117 - 125.

NOBLE,J.P.A., LOGAN,A., and WEBB,G.R., 1976. The Recent Terebratulina Community in the rocky subtidal zone of the Bay of Fundy, Canada. Lethaia, Vol. 1, 1 - 17.

OLSON, E.C., 1957. Size-frequency distribution in samples of extinct organisms. J. Geol., Vol. 65, (3), 309 - 333.

OWEN,G., and WILLIAMS,A., 1969. The caecum of articulate Brachiopoda. Proc. R_ oy. Soc. Lond., ser. B, Vol. 172, 187 - 201.

PAINE,R.T., 1963. Ecology of the Brachiopod Glottidia pyramidata. Ecol. Monog. Vol. 33, (3), 255 - 280.

MI/ Mal , 1969. Growth and size-distribution of the Brachiopod Terebratalia transversa, Sowerby. Pacif. Sci., Vol. XXIII, (3),337 - 343. 259

PERCIVAL,E.,1944. A contribution to the Life-History of the Brachiopod Terebratella inconspicua, Sowerby. Trans. Roy. Soc. N. Z., Vol. 24, (1), 1 - 23.

PROSSER,C.L., 1973. Comparative Animal physiology, 3rd Ed., W.B.Saunders & Co., Philadelphia.

RAUP,D.M., and STANLEY,S.M., 1978. Principles of Paleontology. 2nd Ed. Freeman & Co., San Francisco.

RICHARDSON,J.R. and WATSON,J.E., 1975. Form and function in a Recent free living brachiopod Magadina cumingi. Paleobiology, Vol. 1, (4), 379 - 387.

RICKWOOD,A.E., 1968. A contribution to the Life-History and Biology of the Brachiopod Pumilus antiquatus, Atkins. Trans. Rol. Soc. N.Z., (Zool), Vol. 10, no 18, 163 - 182.

, 1977. Age, growth and shape of the intertidal brachiopod Waltonia inconspicua, Sowerby, from New Zealand. Amer. Zool., Vol. 17, (1).

ROWELL,A.J., 1960. Some early stages in the development of the brachiopod Crania anomala (Muller). Ann. Mag. nat. Hist., ser. B, Vol. III, P. 35.

RUDWICK,M.J.S., 1961. The Anchorage of Articulate Brachiopods on soft substrate. Palaeontology, Vol. 4, (3), 475 - 476. 260

RUDWICK,M.J.S., 1962. Notes on the ecology of brachiopods in New Zealand. Trans. La. Soc. N.Z., Vol. 1, no. 25 327 - 335.

ow ale , 1970, Living and fossil Brachiopods. Hutchinson & Co., London. 199 pp.

SAVAGE,N.M., 1972. Some observations on the behaviour of the Recent brachiopod Megerlina pisum under laboratory conditions. Lethaia, Vol.,, 61 - 67.

SIMPSON,G.G., ROE,A., & LEWONTIN,R.C., 1960. Quantitative Zoology. Revised Ed. Harcourt, Brace & Co., New York.

SMITH,A.G., BRIDEN,J.C., & DREWRY,G.E., 1973. Phanerozoic World Maps. in Organisms and continents through time, Spec. Paper in Palaeo.no 12, Pal. Ass., London.

SOMERO,G.N., & HOCHACHKA,P.W., 1976. Biochemical adaptations to temperature. in Adaptations to Environment, (Ed. R.C.NEWELL), Butterworths, London. 539 pp.

STEELE-PETROVIC,H.M., 1976. Brachiopod food and feeding processes. Palaeontology, Vol. 19, (3), p. 419.

THAYER,C.W., 1975. Size-frequency and population structure of brachiopods. Palaeogeogr. Palaeoclimat, Palaeoecol., Vol. 12, 139 - 148. 261

THAYER,C.W., 1977. Recruitment, growth, and mortality of a living articulate brachiopod, with implications for the interpretation of survivorship curves. Paleobiology, Vol. 3, (1), 98 - 109.

THOMSON,J.A., 1927. Brachiopod morphology and genera. N.Z. Board of Sci. and Art, Manual no. 7, Wellington. 338 pp.

WALKER,K.R., & PARKER,W.C., 1976. Population structure of a pioneer and a later stage species in an Ordovician ecological succession. Paleobiology, Vol 2, (3), 191 - 201.

WEBB,G.R., LOGAN,A., & NOBLE,J.P.A., 1976. Occurrence and significance of brooded larvae in a Recent brachiopod, Bay of Fundy, Canada. J. Paleont., Vol. 50, (5), p. 869.

WESENBURG-LUND,E., 1940. Brachiopods in the zoology of east Greenland. Meddr. Gronland, Vol. 121, (5), p. 12.

WILLIAMS,A. 1956. The calcareous shell of the Brachiopoda and its importance to their classification. Biol. Rev., Vol. 31, 243 - 287.

=II GNP 1966. Growth and structure of the shell of Living Articulate Brachiopods. Nature, Vol 211, no. 5054, 1146 - 1148. 262

WILLIAMS,A., 1968(a). Evolution of the shell structure of articulate brachiopods. Spec. Papers in Palaeo., no 2, 55 pp. Pal. Ass., London.

I■111 .06 ,1968(b). A history of skeletal secretion among articulate brachiopods. Lethaia, Vol. 1, (3). 268 - 287.

MO an ,1968(c). Significance of the structure of the brachiopod periostracum. Nature, Vol. 218, no. 5141, 551 - 554.

,1968(d). Shell structure of the billingsellacean brachiopods. Palaeontology, Vol. 11, (3), 486 - 490.

▪ MID ,1970. Origin of laminar shelled articulate brachiopods. Lethaia, Vol. 3, 329 - 342.

MID aM , 1971(a). Comments on the growth of the shell of articulate brachiopods. in Paleozoic Perspectives: a Paleontological tribute to G. Arthur Cooper, (Ed. Dutro). Smithsonian Contributions to Paleobiology, no 3, 47 - 67.

,1971(b). Scanning Electron Microscopy of the calcareous skeleton of fossil and living brachiopods. in Scanning Electron Microscopy: Systematic and Evolutionary Applications (Ed. Heywood). Academic Press, for the Systematics Association. pp. 3? - 66.

NM .11 ,1973. The secretion and structural evolution 263

of the shell of the thecideidine brachiopods. Phil. Trans. Roy. Soc. Lond.,ser. B, Vol. 264, no. 865, 439 - 478.

,1977. Differentiation and growth of the brachiopod mantle. Amer. Zool.,Vol. 17, (1), 107- 120.

,& al., 1965. Treatise on Invertebrate Paleontology, (Ed. Moore); (H), pts. 1 - 2, Univ. of Kansas Press.

,& MACKAY,S., 1978. Secretion and ultrastructure of the periostracum of some terebratulide brachiopods. ?roc. Boy. Soc. Lond., ser.B, Vol. 202, 191 - 209.

,& WRIGHT,A.D., 1970. Shell structure of the craniacea and other calcareous inarticulate Brachiopoda. Spec. Paper in Palaeo, no 7, Pal. Ass., London. 51 pp.

YATSU,N., 1902. On the habits of the Japanese Lingula. Annot. zool. Japan, Vol. 4, 61 - 67.

ZEZINA,O.N., 1976. Ecology and distribution of Recent brachiopods, (in Russian). Academy of Sciences of the USSR, Nauka, Moscow. EXPLANATION OF PLATE 1.

Morphological features of the calcareous exoskeleton of Terebratulina retusa (Linnaeus); Recent; Firth of Lorne, Scotland.

A. Scanning electron micrograph of the internal surface of the dorsal valve of a juvenile specimen, (ZB 3847). x 37.5.

C. Enlarged view of the anterior margin of the same specimen showing radial alignment of the endopunctae corresponding to the position of the external ribs. On the external surface of the shell the endopunctae are evenly distributed. x 75.

B. Lateral view of adult specimen showing pustules on ventral umbo, (ZB 3718). x 8.

D. Ventral view of rigidly interlocking spicules which support the lophophore in an adult specimen (the lophophoral tissues have been dissolved). x 8.

E,F. Ventral view of the brachidium of an adult specimen

(ZB. 3719). E x 6.5; F x 3.5. A B

c D

E f EXPLANATION OF PLATE 2.

A. Living specimens of T.retusa attached to a mussel, photographed in feeding position in an aquarium. x 6.

B. View of the clam-dredge used to collect samples from the Firth of Lorne mussel beds; the dredge is 1.2 metres in width.

C. Enlarged view of the clam-dredge showing the outer chain bodywork (75mm in diameter), and the inner nylon meshwork (15mm x 15mm).

D,E. The clam-dredge being hoisted on to the deck of R/V 'Calanus' after a successful trawl in the Firth of Lorne. fil►' ' ~'±:~•

!g/ f w it l«Dāiō.'f 'Iji71t~ r

,74 N 44,4. EXPLANATION OF PLATE 3.

A - F. Views of the bulk sample collected by the clam- dredge from the Firth of Lorne mussel beds in January 1979. The largest brachiopods visible are 20 mm in length. 3

A B

c EXPLANATION OF PLATE 4.

Soft part morphology of T.retusa; Recent; Firth of Lorne, Scotland.

A. Scanning electron micrograph showing oblique view of a seta and its follicle enclosed within mantle epithelium at the lateral margin of a juvenile specimen; the primary and secondary shell layers have been exposed along the margins of the shell by the shrinkage of the overlying epithelium, (ZB 3859). x 150.

B. Scanning electron micrograph showing the pedicle and its associated rootlets in an adult specimen, (ZB 3862). x 37.5.

C. Scanning electron micrograph of the lobes of the digestive diverticula, (ZB 3860). x 150.

D,E. Scanning electron micrographs of a well-developed female gonad; the central yolk-sac of the ova have collapsed during the drying process, (ZB 3851). D x 75; E x 150.

F. View of undeveloped female gonad showing the genital canals and a few unspawned mature ova. The spicules in the outer epithelium are visible. x 62.5. D

1dr_

■Aullr:vedift411114,!°14,

E F

4 EXPLANATION OF PLATE 5.

Terebratulina retusa (Linnaeus); Recent; Firth of Lorne, Scotland.

A. Scanning electron micrograph showing mucus strands and particulate matter trapped by them within the mantle cavity of a juvenile specimen, (ZB 3826). x 750.

B. Large pseudofaecal pellet enmeshed within mucus strands within the mantle cavity of the same specimen. x 375.

C. Group of faecal/pseudofaecal pellets at the lateral margin of the same specimen, prior to ejection from the shell. x 150.

D. Disarticulated dorsal valves of living juvenile specimens; the lophophoral filaments in the upper specimens are opening into feeding position. x 25.

E. Enlarged view of one of the specimens in D; the shell is transparent, and the caeca are visible. x 64.

F. View of a disarticulated dorsal valve of a juvenile specimen (approx. 5mm in length) showing the plectolophe in feeding position. x 12.

.4jit sit

;i-A:AILAteir., inIti-, ;...... ,,ukt- \ 40.140.::. 01, - 44111, 111 * Otlf coN s ,ts 4.4

:-:'; ‘i 4ft ' \ A=4:41'4, fi ' 5 r I, 4 4.'104 416!.:!■:%.,' ' < EXPLANATION OF PLATE 6.

A - C. View of disarticulated dorsal valves of living specimens of T.retusa showing various stages of the development of the lophophore.

A. Adult plectolophe. x 6.

B. Juvenile trocholophe; the filaments are curled up. x 55.

C. Juvenile schizolophe with filaments in feeding position. x 35.

D - F. Scanning electron micrographs of a polished and etched longitudinal section through the shell of Gryphus vitreus (Born); Recent; Bay of Naples, showing primary, (at top), secondary, and tertiary shell layers. Prominent microscopic growth-lines, associated with the formation of an external macroscopic growth-line, are discernible in the primary layer (e.g. F). Anterior is to the left, and external shell surface at the top, (ZB 3808). all x 375.

A 3 .- 4.-AP.-... 1.111111110.1.1111 ''''%•11 .L...4;° 42411.‘ 4 10.41. ,...4.14, ■••.„.,..-"No. ,..t...... m. _,...••■,,,,,r.. .,.. .••• ...... IM.elo, '...... q..M., _..,'.....* ....MN..

.M1•.....10.7...4k...... =...±. :Ifta: ...„...... or .0 ., ...... 1.••■.''"...'....._ '.. i0...... ,M1...

. ..,, ....,...... ,..■. ...i• ,:;,...... , 0,...."•■••• .....ZW,....,=.e.,...... OrT•e/•- 0...._ ..■ A :,,...... 1.. .., • . G • •. . .. . , . . .. • .•• ..--. '''''''''' .....-.• ,,,,ir. „1..,-..-_...... /.■••-• I ,n,...... ••• /... 1.- "...... =•■ ■■• /..=.•,..r.- ..:;•,... ..r••••■•.- ...i ,...... '' e it.■ .../.•••■■■•,..,...••,'''..••■••••'-.,- . ...••• • ..../ 11

• k •,.

eft00 •

- • 2: !:• '

• - ••••• a 3

- 40.• I. F.

9 EXPLANATION OF PLATE 7.

A - F. Scanning electron micrographs of a polished and etched longitudinal section through the shell of Gryphus vitreus (Born); Recent; Bay of Naples; showing microscopic growth-lines in the primary and secondary shell layers. In all cases the anterior is to the left, and the external surface is at the top. (ZB 3808)

A. Primary layer growth-lines. x 1500.

B. Growth-lines in primary and secondary layer. x 1500.

C. Growth-lines in secondary fibre. x 3750.

D. Primary layer growth-lines. x 1500.

E. Prominent growth-lines within the primary layer. x 1500.

F. Enlargement of portion of E showing continuation of prominent microscopic growth-lines from primary shell to secondary fibre. x 3750. A 3

a 3

.ses

, 0,,,,p.„-., - • ..., ,....,„...,.,..„ i

..,‘ , .~'c •'. i , J EXPLANATION OF PLATE 8.

A,B. Scanning electron micrograph of sporadically developed microscopic growth-lines in a polished and etched longitudinal section through the primary layer of Gryphus vitreus (Born); Recent; Bay of Naples. The shell anterior is to the left, and the exterior to the top. (ZB 3808), A,B x 3750.

C - F. Scanning electron micrographs of poorly defined microscopic growth-lines in a polished and etched longitudinal section through the primary layer of Magellania venosa (Solander); Recent; Falkland Islands. A resin infilled endopuncta is visible at the top right- hand corner of C. (ZB 3820). C,E,F, x 1600; D x 800. 8

A - ./.°1- ,...... ■•••■1 70000.111r- "PCIOri.°°°°°P.-

-.1 ♦ acr ..

r .S . •.+.her ~:1:v

- + .

d.Ar •

' a • a

1,4 1 ,rr:ef, r,

a EXPLANATION OF PLATE 9.

A - D. Scanning electron micrographs of microscopic growth- lines in a polished and etched longitudinal section through the primary layer of a juvenile specimen of Magellania venosa (Solander); Recent; Falkland Islands. The low inclination of the growth plane may reflect an adaptation for rapid growth. The anterior of the shell is to the left and the external surface at the top. (ZB 3820). A,C x 750; B,D x 1500.

E. Scanning electron micrograph of the internal shell surface of a juvenile specimen of Terebratella inconspicua (Sowerby); Recent; New Zealand, showing the mosaic of secondary shell fibres. Faint growth-lines can be seen in some fibres. (ZB 3779). x 1500.

F. Scanning electron micrograph of the internal shell surface of a juvenile specimen of Terebratulina retusa (Linnaeus); Recent; Firth of Lorne; Scotland, showing bifurcation of secondary layer fibres. The normal pattern of alternating rows of fibres had been distorted by the superposition of a fibre directly above another, and the bifurcation allows re- arrangement of the fibres into an orthodox stacking pattern. (ZB 3850). x 1500. o. _ Lt_

U A w EXPLANATION OF PLATE 10.

A,B. Scanning electron micrographs showing transverse fractured sections through the thin-shelled abyssal species Macandrevia africana, Cooper; Recent; from 4,200 metres off S.W.Africa; showing the radial, inwardly narrowing, rods of dense calcite within the primary layer. These rods are thought to be an adaptation for life in abyssal habitats. The external shell surface is at the bottom in A, and at the top in B. (ZB 3836). A x 750; B x 1500.

C. Scanning electron micrograph showing dorso-lateral view of the protegular plate in a juvenile specimen of Eucalathis tuberata (Jeffreys). (ZB 3850). x 150.

D. Enlargement of C showing junction between primary layer (bottom left) and the pitted protegular plate (top right). x 1500

E. Scanning electron micrograph showing dorso- lateral view of the pedicle aperture of a juvenile specimen of T.retusa; Recent; Firth of Lorne , Scotland; showing umbonal erosion and prominent postero-lateral pustules on both valves. (ZB 3840). x 100.

F. Ventro-lateral view of attached specimen of Macandrevia africana, Cooper; Recent; S.W.Africa; showing umbonal erosion resulting from rotational movements around the pedicle. (ZB 3866). x 8. ■• P4' 1 1.'710 • 4 - 4 I '

-n EXPLANATION OF PLATE 11.

A - F. Scanning electron micrograph of a longitudinal fractured section through the shell of Gryphus vitreus (Born); Recent; Bay of Naples; showing primary, secondary and tertiary shell layers (A), and prominent transverse growth-lines in the tertiary layer prisms (e.g. C). The anterior of the shell is to the right, and the external surface at the top. Recognition of growth-related banding in both secondary and tertiary layer calcite is, on occasions, complicated by the presence of cleavage planes. (zB 3793). A - F x 750. r d r ► j ...00•009.611 ?I"loolgerror t

• e,4

-, ~. . ~qt. r.

•

• 111 EXPLANATION OF PLATE 12.

Montage of scanning electron micrographs of an embedded, polished, and etched longitudinal section through the anterior of a juvenile specimen of Magellania venosa (Solander); Recent; Falkland Islands. Sporadically developed microscopic growth-lines are discernible in the primary layer; the resin-infilled endopunctae occur at regular intervals. (ZB 3820) x 500.

The section is continued in Plate 13. 12 EXPLANATION OF PLATE 13.

Continuation of Plate 12, showing longitudinal section through a juvenile specimen of Magellania venosa (Solander). (ZB 3820). x 500. 13 EXPLANATION OF PLATE 14.

A. Scanning electron micrograph showing a resin-infilled endopuncta and brush in a polished and etched longitudinal section through a juvenile specimen of Magellania venosa (Solander), (ZB 3820). x 375.

B - G. Scanning electron micrographs of the micro-borings on the external surface of Terebratella sanguinea (Leach); Recent; Marlborough Sound, New Zealand. (ZB 3823).

B. Oblique view of the bored area; the micro-borings- are barely discernible in this view, the circular holes are endopunctae exposed by the removal of the overlying canopy of primary shell material. x 37.5.

C. Lateral view of a fractured surface through the primary layer showing reorientation of a micro-boring when it impinges on the porous canopy of an endopuncta (on right). x 2000.

D - F. Vertical view of the external shell surface showing micro-borings. In F the outer surface of the primary layer has been destroyed by the micro-borings, whilst the porous canopy of an endopuncta remains intact. all x 1000.

G. Lateral view of a fractured longitudinal section showing bored area along the ridge of a macroscopic growth-line. It is impossible to determine if the growth-line formed in response to the disruption caused by the algal boring. x 150. it

•

• EXPLANATION OF PLATE 15.

Scanning electron micrographs of the external surface of Terebratella sanguinea (Leach); Recent; Marlborough Sound, New Zealand; showing algal micro-borings, (ZB 3823).

A. Vertical view showing bored primary layer (left) and non-bored, porous, endopunctal canopy (right). x 2000.

B. Vertical view of non-bored endopunctal canopy surrounded by densely bored primary layer. x 1000.

C. Oblique view showing porous, non-bored, endopunctal canopy (top left) and adjacent densely bored primary layer. x 2000. ∎ 1 th EXPLANATION OF PLATE 16.

Terebratulina septentrionalis (Couthouy); Recent; off Nova Scotia. (see Appendix II). USNM 551142.

The majority of the specimens illustrated are attached to fragmentary or complete (B) scaphopod shells by a dense encircling network of pedicle rootlets. The specimens illustrated in D had been free-lying, anchored posteriorly by a sediment-impregnated meshwork of pedicle rootlets. In E the detached pedicle of an adult specimen is visible (on the left) showing the tremendous development of pedicle rootlets. A, B, D, x 12; E,F, x 2; C x 3.

I am indebted to Dr. G.A.Cooper, Dept. of Paleobiology, National Museum of Natural History, Washington, DC., for the photographs in Plates 16 and 17. A

C D

16 EXPLANATION OF PLATE 17.

A - E. Terebratulina septentrionalis (Couthouy); Recent; off Nova Scotia. (see Appendix II). USNM 551142.

A. Adult specimen attached to a molluscan fragment by a non-branched pedicle. x 5.

B. Two free-lying adult specimens ; a few fragments_. of scaphopod shell are enmeshed within their entangled rootlet networks. Encrusting sponges indicate that the left-hand specimen was lying on the sea-floor with its dorsal valve completely exposed, whilst the right-hand specimen was , partially buried. x 12.

C. Two adult specimens attached to the anterior of a complete scaphopod shell. x 1.

D. Free-lying adult specimen with two juveniles attached posteriorly. x 3.

E. Enlarged view of specimen illustrated in D showing juvenile attached to the pedicle rootlets. x 6.

F. A specimen of T.septentrionalis from a different locality (Gulf of Maine) showing pebbles enmeshed within pedicle rootlets; a further demonstration of the increased anchorage resulting from this mode of attachment in regions where substrate is of small surface area. USNM 551143. x 2. m 0 'BRITISH BRACHIOPODS' A Synopsis, prepared in conjunction with C.H.C.Brunton, published by the Linnean Society and Academic Press, and submitted as Appendix IV of SHELL GROWTH AND ECOLOGY OF RECENT BRACHIOPODS FROM SCOTLAND AND NEW ZEALAND

GORDON BARRETT CURRY, B.A.(MOD.); (T.C.D.).

A thesis submitted for the degree of Doctor of Philosophy of the Univ- ersity of London and for the Diploma of Membership of Imperial College.

Department of Geology, Royal School of Mines, Imperial College, London, SW7.

• UN CO RRCc-Tell) RGe 'PRODF5 A Synopsis of the British Brachiopods

C. HOWARD C. BRUNTON

AND 9 SEP ii GORDON B. CURRY

Pl'I'f',t,d 04 :°s± Department of Palaeontology, British Museum (Natural History), fin f London SW7, England

CONTENTS

Introduction I General structure 2 Internal anatomy 4 Biology 5 General 11 Shell morphology 11 Feeding 12 Ecology 13 The distributions of brachiopod species around the British Isles 14 Collecting and preservation 17 Classification 19 Key to British species 22 Systematic descriptions 26 Glossary 59 Acknowledgments • 61 Literature list 62 Index to species 63

Introduction

. Brachiopods are grouped together as a single phylum, usually assigned by invertebrate zoological textbooks to a group of minor coelomate phyla, and they are quite distinct from the bivalve Mollusca, which they resemble only super- ficially. The main differences are explained on p. 19. The term "Brachiopodes" was first used by the French palaeontologist Cuvier in 1805 and the following year Duntcril formalized the name "Brachiopoda" for an order of the Mollusca. The name is derived from the Greek words for "arm" and "foot" and was given in the mistaken belief that the obvious coiled "arms" (what we now call the lophophore) could be extended from the shell and used in locomotion as "feet". Although this notion was soon shown to be erroneous the name survives enshrined in zoological literature and the term "brachial" is used for structures associated with the lophophore. Not only is the name Brachiopoda misleading as a description of the animals but it can be confused with the group of crustaceans called branchiopods. · . 2 BKnlSII BRACIIIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY

Brachiopods are entirely marine sessile benthic invertebrates having different Food grooves dorslIl .lIld ventral valves. They are found in waters from below antarctic ice 10 tropic." reefs, and from intertidal situlltions to depths of llbout 6000 rn. ~'lost commonly they occur below low-wmer mark, from between about 200 III 10 5110 m del)th. For this reason, and because .the shells break ellsily oncc Ihe Dashed line animal h'ls died, brachiopmls arc seldom found on sea shores. re presenting ----position of shell Bnu.:hil)Plld'i arc divitled iJlto Iwu classes according to the lack or presclll:e uf &Ifliculating ~tructures hetween Ihe two valves of thc shell- the Inarticulalll ami the Articulata. Today hrachiopoJs arc less divcrse than in past'ages when Iheir ~hl!ll~ were commonly prcservcJ in marinc scJimcnts. For this rea~on fo:--:--il hrachiopmls arc commonly 1ll00C familiar to people than are Recent species. 'I he numher of distinct species fuund today in the waters around the Brili:--h hies, illld de~crihcd in this SY"O/l,\';\', is twenty-onc, out of a descrihed prc~elll day wurld total uf about 300 :--pecics. , Ufilchinpods arc usually ident il iell from their shells alone, partly because I hey ----'...... --Brachlal cavity arc stuJied llIorc by palaeonlOlogists than by zoologists, but also because inlernal shell morphology reI/eels Ihe form of many of the principal inlelllal -l~I-__-f- __S plcular lophophor· organs. connecting tissue

Lophophore--~~--~~~-~~

General Structure Dorsal gonad Ventral Brachiopods are sessile creat ures, attached to the substrate usually by a fle!'!hy stalk - the pellicle. They '1fe enclosed in a shell with dorsal and ventral vilhes, each of which is bisected by a mellian plane of symmetry, and wh.ieh diHer:-- in shapc frum the olher. The valves arc hinged at the .posterior cnd, near Ihe pedide, and '1I1leriorly they gape open whil~ the animal ,feeds. Thus to~,. icnlille a hrachiopod, thc larger vain:, Imm which the pedicle emerges, IS JllaL:~d Blind I ntestlne ---";~!4L-_ ~~~y--~ velllrally, and Ihe pedicle is pmilioJled posteriurly (Fig. 9). Thc cUIlIPOSilioll allll ~-oL....;;.,.~--Body cavity Ventral adJusto~r_---:~~... ~ I1IUrphol0!tY of valves vary wilh :--pccie:--. (The terms dorsal and venlral ale t1~ed muscle 'IJI:tlomically allll may not rel/ecl Ihe oricntation of the animal in life.)

Pedicle ----~~~-

3mm A

FIG. 1. A, generalized lateral view (based on 1'erebrUltI/ifla Telusa (Linnaeus», wilh shell removed, showing the main features of internal analomy. B, section through lophophore with filaments truncated (after Williams, 1965). 4 HRH !NH BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 5

Internal Anatomy The internal space between the Iwo valves is divided into a posterior body cavity and anterior brachial cavity (Fig. 1) by the thin epithelial body wall. "I he Adductor brachial cavity is much the largest and contains a pair of coiled filamentous Gonad Diductor Muscles Adjustor structures called the lophophore. This serves as a respiratory and food gathering organ having free contact with the surrounding sea when the shell is open. 'I he Mantle body cavity, containing muscles, alimentary canal, digestive diverticular, Une canals reproductive system, etc. is restricted to the postero-median part of the shell and Iron here (laps of mantle epithelium extend forwards lining both valves internally. This mantle tissue secretes the shell material and contains coelomic cavities within which strands of reproductive tissue develop during the breeding -Setce season. The internal soft part anatomy is known in detail for comparatively few species. however, it seems that the anatomy is relatively stable throughout the phylum, the main difference being that the alimentary canal is open-ended, hat ing an anus, in the lnarticulata, whilst in the Articulata it is blind-ended. The general structure of the lophophore is a long tube with a pair of ridges along its length, between which is a food groove. 'I he outer side bears long, closely spaced rows of filaments with frontal and lateral ciliated surfaces. The food groove is continuous around the lophophore and leads postero-medianly to the wuuth, (Linnaeus). Ventral view, with shell removed, showing situated on the transverse section of the lophophore, by the body wall. Inside the Fla. 2. Terebratulina reiusa underlying tissues. lophophore, canals connect to the coelomic or body cavity posteriorly. In some species the lophophore is suppot ted by branching spicules of calcium carbonate, as \tell as by the turgidity of the coelontic fluid and, in addition, the Inner socket ridge Terebratulida have a skeletal brachial loop built within part of the Iophuphote. Cardinal process The hotly wall, separating the brachial aard body cavities, is situated between the Socket crura and lies close to the anlerlor edges of the muscles. In the body wall ate Median septum Crus paired excretory pores connecting to conical excretory glands, the metane- Adductor phridia, suspended in the body cavity on either side of the intestine. scar .1 he alimentary canal is simple and similar in all articulate species investigated. The trnnotlt, at the mid posterior point of the lophophore, leads to a skill oesophagus, which curves towards the dorsal valve, and a roughly U-shaped expanded stomach. Around this are large digestive diverticula. In the Art iculata, a shout blind intestine extends ventrally, normally finishing near the base of the didnetor muscles. The In articulata have tin anus which, in the case of lingotitis, is at the end of a long twisted intestine, and in conical discinaceans and craniaceaits terminates a shorter U-shaped gut. • Little is known of the reproductive system of brachiopods; whilst most species appear to he dioecious, some are hermaphroditic. The reproductive glands develop from coelomic epithelium in the body cavity and, as they enlarge, they commonly extend anteriorly into the mantle canals. In sexually mature individuals the ovaries normally show as light brown to orange-red masses adherent to the insides of the valves; the testes are less obvious and lightly coloured. Ova and sperm are discharged through the metanephridia. 4 mm

FIG. 3. Internal features of the dorsal valve of a generalized brachiopod. •

6 HRIIISH BRACHIOPODS r The nervous and circulatory systems are poorly known and can only be seen Delthyrium by careful dissection. Circulation is open and the blood free from cells, but contractile "hearts" lie medianly, usually on the stomach. The nervous system consists of enteric ganglia, situated around the oesophagus, from which nerves Dental serve the muscles, lophophore, mantles and alimentary tract. No special sensory plates organs have been proven, other than the marginal setae (Fig. 2), which appear to sense movement in the sill rnWilling water. Some species from shallow Ovaler seem to he light sensitive, but no receptors have been isolated. Deltidial plates Shell Morphology A 10mm •I he two brachiopod classes, the Inarticulata and the Articulata, differ quite markedly, but are distinguished principally on the hinge apparatus of the valves; the Articulata having a pair of teeth in the ventral valve, fitting paired sockets in • Tooth the dorsal valve (Fig. 3, 4); the Inarticulata rely upon internal muscles to hold 2mm B the valves together and to move them apart, so for this reason their musculature differs from that of the Articulate. As a whole the Inarticulata are a varied group but the two British species resemble one another in being more or less circular in outline and with irregularly conical dorsal valves, quite unlike the articulate species (Figs 11, 12). The articulate species of British waters mostly have biconvex shells, Inn some have somewhat flattened dorsal valves pressed closely against the hard sub- I mm strate. All species have a pedicle attachment, and the pedicle aperture, situated C in the dclth3riuur, may he restricted in size by variably developed deltidial plates (Figs 4, 5). The external surfaces of the valves are marked by growth lines, Fla. 4. Fallax dallinijormis Atkins. A, showing locations of B and C. B, postero-lateral developed during pauses in the secretion of shell, and by various fortes of radial view of adult ventral umbo showing joined deltidial plates. C, dorsal view of ventral umbo ornamentation. Radial ribs form prominent ridges on the valves and extend showing unjoined (=disjunct) deltidial plates in a young specimen. (After Atkins, 1960.) anteriorly from the umbos (sing. umbo)' (Fig. 5). In addition there may be line Ventral umbo radial striations, or tubercles, commonly associated with ribs. The Iwo mineralized valves are the most obvious features of brachiopods, and are important in the recognition of species. All articulate valves are trade of Pedicle aperture calcium carbonate, whereas inarticulates may be calcareous or have shells made Radial of thin layers of chitinophosphatic material. Calcareous valves tend to he Tubercules striations light-coloured and brittle, whilst chitinophosphatic valves are normally dark coloured and somewhat leathery. Microscopy reveals that the calcareous shell of brachiopods is layered. The outer surface is covered by a thin brown cuticle, the periostracum, which may become abraded from parts of the shell dining life; below this is a uniformly thin layer of calcite, the primary layer, in the tin ut of minute needles perpendicular to the external surface. Inside this the secondary layer is of variable thickness and may form structures on the inside of the valves. The secondary layer thins peripherally and in articulates is typically composed of long fibres, 10 to 20irm wide, dipping more or less anteriorly towards the inner surface. When exposed on the internal surface of valves these fibres forme an Rib overlapping pattern, called the internal shell mosaic (Fig. 6C), which is characteristic for major groups of brachiopods. Inarticulate calcareous valves have Growth line latnellusc secondary layers. Some articulates have a tertiary layer, on tie inner 5mm sutlaccs, in which the calcite is in the form of prisms perpendicular to the inside of the valve. FIC. 5. Generalized ribbed articulate brachiopod. 8 UKIIISII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 9 In addition to the above structures, three conditions of brachiopod shell are recognized which characterize broad groups of taxa. These shell types are impunctate, endopunctate (Fig. 6C) and pseudopunctate. An impunctate shell lacks either endopunctae or pseudopunctae and is characteristic of all living rl►ynchonellids.'I he endopunctate condition is of regularly spaced narrow canals penetrating from the inside of the valve almost to the outside of the primary layer. In life these canals, the endopunctae (Fig. 6C), accommodate Cvaginalions of the mantle epithelium, called caeca, whose purpose remains to he lully understood. Recent work indicates that the caeca probably store food materials, and they may help inhibit boring into the shell by other organisms. All the Hinge plate "1'erebratulida are endopunctate. The pseudopunctate condition is known Iru►n fossil brachiopods and is recognized by inwardly facing conical flexures in the microstructural layering of the shell, which commonly form small tuhereules on the insides of the valves. These shell conditions can usually be recognised with the aid of a good hand-lens. Internal skeletal structures, visible on dead articulate valves front which the soft tissues have been removed, are important in the recognition of species. In the middle of dorsal valves, close to their posterior margins, there are scars of muscle attachment manifesting themselves as a ridged and grooved, elevated or depressed region, known as the cardinal process (Fig. 3); in its most clearly developed form it is a prominent bilobed knob-like structure. The cardinal A process is flanked by the sockets, into which fit the pair of teeth. The sockets are 10 mm variable in form but usually are hounded medianly by prominent socket ridges, which may be supported from the floor of the valve by hinge or crural plates. Socket The morphology and disposition of these plates are important taxonomically. From the anterior ends of the socket ridges, skeletal structures project Crus lot wards which, in life, help support the lophophore. In rhynchonellid Median 20µm C brachiopods these- projections are called crura (sing. crus) while in Iiving septum terchratulids the crura grow forwards and develop into complicated loops which support much of the length of the coiled lophoplmre. In some taxa this brachial Brachial loop (Fig. 6A, II) is connected not only posteriorly to the crura but also medianly loop onto a median septum running down the middle of the valve from near the cardinal process. The morphology of the loop commonly alters considerably during growth of the animal but its form, and that of the crura, play important roles in taxonomy. B l.ess obvious, but still commonly visible on the insides of valves, are the scars of muscle attachment. The articulate species Iiave three sets of paired major Fin. 6. Dalfina septigera (Love n). Internal views of the dorsal valve showing the brachial muscles. 'I he adductor muscles (Figs I, 2) are used to close the valves sud attach loop. A, ventral view. B, oblique lateral view. C, enlarged detail of internal surface to the dorsal valve postern-medianly, divided, where present, by the median showing shell mosaic and endopunctae. (A, B after Atkins 1960.) septum. '[heir ventral attachment sears are more or less opposite and ceutt ally placed.') he tliductor muscles open the shell and are fixed dorsally to the cardinal process, posteriorly of the hinge axis which passes through the teeth. 'I Itese muscles divide ventrally and attach to the ventral valve on either side of the adductor muscles, but commonly extend further forwards. Thirdly, theee ale

10 • BRI'IISII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 11 several pairs of muscles attached to the proximal end of the pedicle, situated Biology • within the ventral umbo. These muscles allow the brachiopod to swivel around the pedicle, so changing its position relative to the substrate; they are called General pedicle adjustor muscles (Fig. 1) and may leave scars in the dorsal valve near the socket ridges. In ventral valves their scars are usually closely associated with the There are about 300 described living species of brachiopods distributed over the diduclor muscle scars. world, compared to several tens of thousands of known fossil species. On the insides of bolls valves, extending towards the margins, shallow Brachiopods have one of the longest observable evolutionary histories, having branching grooves may be distinguished which mark the positions of mantle existed for at least 550 million years. Their remains are important constituents canals in the mantle tissues. These coelomic canals, connecting posteriorly to the of many fossil faunas. For this reason most brachiopod studies have been carried hotly cavity, carry nutrients to the mantle tissues and contain part of the ,out by palaeontologists. The best general book on Living and Fossil generative strands from which ova and spermatozoa develop. Brachiopods is by M. J. S. Rudwick (19701) and some aspects of brachiopod "1 he insides of ventral valves have fewer structures than dorsal valves. In ecology have been reviewed by Brunton (1975). The most complete work, addition to muscle scars and traces of mantle canals there is a pair of teeth including the descriptions of about 1600 fossil and recent genera, is the situated antero-laterally of the delthyrial opening. The shape and detailed brachiopod volume (Williams, 1965) of the series entitled Treatise on Inverte- dispositions of teeth are variable and in some taxa they are supported by dental brate Paleontology.. plates (Fig. 4). The pedicle opening may be within the delthyrium, restricted The life histories of few brachiopods have been described in detail, but Atkins apically or marginally by deltidial plates, or the delthyrium may be almost (1959-1961) has studied several species from the Western Approaches of the completely covered by Shelly plates so that the pedicle extrudes from a small English Channel. Most species described in this Synopsis live for between five hole almost at the tip of the ventral umbo. During life the pedicle opening may and ten years and probably become sexually mature in their second or third become enlarged by abrasion against the hard surface of attachment. year. Ova and sperm mature in different specimens and are released to the sea at various times of the year, controlled perhaps, in temperate regions, by sea temperature fluctuations. Fertilization takes place outside the body cavity but fertilized eggs may be found in the brachial cavity. In some species, especially the warm water thecideaceans, a brooding mechanism exists to hold the developing larvae within the lophophore. Cleavage of the fertilized egg leads to gastrulation after which the external surface commonly becomes ciliated. Differentiation of the posterior lobe leads to the development of the pedicle and mantle rudiments. The free-swimming larva develops for several days providing the only normal means of dispersal for the species. At about the time of settlement to the substrate, the mantles of articulate species reverse their positions from enclosing the pedicle to extending anteriorly around the body. This brings the ciliated surface of the mantle to the inner side, freeing the new outer surface for the secretion of shell material. The larvae of inarticulates do not reverse their mantle and the pedicle develops at a later stage. The first formed shell, the protegulum, is only about 0.3 mm long, and appears to be similarly shaped in most articulates. Some internal organs are recognizable at this stage and the lophophore, with only a few filaments, is a simple ring extending forward from the mouth. It is not until the shells have grown to more distinctive shapes or developed characteristic ornamentation that species recognition becomes possible. Once the outside surface of the shell has been secreted it remains unmodified by the brachiopod itself and so provides a record of the specimen's life history. The external growth lines develop when shell growth is interrupted by the retraction of the marginal mantle epithelium. This retraction is caused by disturbances such as seasonal availability of food, spawning activity, or storms, or by the predation of other organisms. Predation or damage to the shell is recorded by localized areas of distortion of the valve. 12 B121'1 1511 BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 13

The valves grow by peripheral shell accretion and thicken by the addition of sponges, bryozoans or barnacles may use the shell substance for habitation shell material over their inner surfaces. At the same time the lophophore grows, before or after the death of the brachiopod. Older brachiopods are commonly passing through more or less complex stages of development, some of which encrusted by sponges, solitary corals, bryozoans, foraminifera, etc. but these resemble the adult stages found in other species. Inside the tcrebratudid usually do no harm and might aid the brachiopod by adding camouflage lophophore the brachial loop develops, also altering shape as it grows. For these Various predators and parasites have been found in brachiopods; in rare reasons it is important to recognize whether a specimen is juvenile or adult instances polychaete worms are probably responsible for eating away some ' before identifying the species. lophophore filaments, but no general survey of host; parasite or predator Most brachiopods remain attached to the substrate throughout life. There is relationships has been published. some evidence that a few species, living outside British waters, may alter their positions, if their pedicle is "rooted" in coarse sediment, by withdrawing the Ecology pedicle front the sediment and re-rooting close by. Lingulids move up and down their burrows in silty sand, according to the state of the tide, but these are the Our knowledge of brachiopod ecology is increasing through various studies only burrowing brachiopods. being carried out around the world. Apart from the burrowing lingulids, all brachiopods require a firm substrate upon which the larvae can settle and attach. Feeding Attachment is by the pedicle or, more rarely, by cementation of part or all of the ventral valve. Some living brachiopods, when adult, probably rely upon their When the animal is feeding the two valves gape open anteriorly so that the pedicles merely as anchors or tethers, rather than as a support for the shell and brachial cavity becomes a partially enclosed area of the sea. Within this cavity lie passively on the sea floor. The distal end of the pedicle can be divided into the lophophore, the organ concerned with food gathering and providing the short "rootlets" requiring hard surfaces of attachment, such as pebbles, sedi- main respiratory surface, creates a water current by the beating of cilia on the ment grains, skeletal material, or living shells. The development of these lophophore filaments, and this carries food particles to the filaments. 'Hie rootlets is variable within a species and depends on the substrate available to the structure of the lophophore and arrangement of the filaments is such as 10 individual. Although not represented in British waters, there are small species produce defined inhalent and exhalent areas in the brachial cavity. The lateral having long hair-like pedicle "roots" capable of gripping fine sediment and cilia on the filaments pass water from the food-groove side of the lophophore to penetrating the calcareous shells of Foraminifera. Brachiopods do not occur in the exhalent chamber. Frontal cilia pass food particles down the filaments into areas of soft fine sediment with a high rate of sedimentation, since such the food groove where, in a mucus strand, they are carried to the mouth and conditions would tend to clog their lophophores. However, they can survive ingested. Undigestible particles are also ingested but periodically this waste is strong water currents and thrive in the tidal races between the islands off the gathered into pscudofaecal pellets which are expelled front the mouth and west coast of Scotland. flushed from the brachial cavity in the exhalent stream. The food of brachiopods Apart from a suitable substrate, perhaps the most important criterion for remains in some question. It had been thought that they fed on organic pa titles, brachiopod distribution is the availability of food. The concentration of food and but in recent years there has been the suggestion, based on experimentation dissolved nutrient is linked with sea-floor topography, temperature of the water (McCammmou, 1969), that food as dissolved nutrients can be absorbed by the and its depth. The wide geographical distribution and bathymetric range of brachial tissues. The opinion of Zezina (1976), that brachiopods probably feed brachiopods suggests a wide tolerance to, or variation in, their food materials. both by ingestion of particles and directly front dissolved nutrients, is probably. Zezina's (1976) review of brachiopod distributions indicates that the greatest corner►. species diversity occurs at depths along Continental Shelves and Slopes, Brachiopods appear to have no habitual enemies, but their valves may be between 150 m and 500 m deep. The bathymetric range of known living damaged or bored by several predators and there is some evidence of the specimens over the world is front the intertidal zone to about 6000 m. At abyssal animals being killed by carnivorous invertebrates or fish. Other than for the depths probably both the availability of nutrients and of calcium carbonate, and digestive tract and small posterior muscles there is little solid matter in a the ability to secrete this into shell substance, limits brachiopod distributions. brachiopod on which to feed and, perhaps for this reason, they are not often Some sea-floor studies and collections in the last fifteen years have demons- sought after by carnivores. trated that brachiopods are very abundant, and in some localities they are the The most obvious and commonly seen form of damage to brachiopods are dominant constituents of the sea-bed fauna. Figures for densities vary consider- circular holes penetrating the valve, produced by boring carnivorous gastropods. ably and, at times, are distorted by concentrations of specimens attached to large These attacks are not always fatal, as can be seen by those specimens in which rocks, but densities up to about 400 specimens per m2 have been recorded. the hole has been covered internally by a-blister of newly formed shell. Boring 14 BRPlfBIl BRACHIOPODS 1 1 I 1 I I I I 12° 10° 8° .. 4° . , 2°W 0° ' 2°E Brachiopods will not normally tolerate salinities which deviate more than a few per cent from that of normal sea-water. Only lingulids, in their intertidal burrows, can tolerate exposure in the brackish conditions resulting from nearby rivers or rain falling at times of low tides. I lowever, even here protection against reduced salinity around the tissues may be provided by keeping the valves tightly closed within the burrow. Light itself `seems insignificant in controlling brachiopod distributions. • Laboratory experiments suggest that some shallow-water species may be ** sensitive to light fluctuations, while other deeper-water species, at depths —56°N greater than that normally penetrated by light, remain insensitive. Similar experiments show that some species react to disturbances, such as the addition of unusual substances to the water or sudden water movements, by snapping their valves shut. Water temperature, linked probably with food supply, has broad controlling influences, but some species are tolerant of wide fluctuations locally or geographically (some species off Japan tolerate an annual range of about I S°C), — 54° and brachiopods are found from polar waters of —2°C to the tropics at about 30°C. Temperature probably has important seasonal controlling influences on spawning which, in some species, occurs only within narrow limits of water temperature in spring and autumn. It is probably because of the general tolerance to temperature variations that many species are widely distributed. The species in this Synopsis mostly have tk —52° geographical ranges extending beyond British waters, for around these islands are inked faunal provinces of Mediterranean, North Atlantic and circumpolar aspects. ° V ° Celtic Sea The Distributions of Brachiopod Species around the British Isles V — 50° a ° The distributions are.plotted from published records and from the collections of brachiopods in the British Museum (National I history), London (Figs 7, 8). Western The patterns, to some extent, rellect areas of study of the marine faunas. "I b us Approaches the high diversity of species in the Western Approaches and Bay of Biscay may result from collections made by the Marine Biological Association's laboraluty at Plymouth. Ilowever, it is noteworthy that brachiopods appear to be absent from the Celtic Sea and southern legion of the North Sea. — 48° Key Crania ° cryp/Dporo *. 'fl V onoma/o gnomon ° ° • Pelapodiscus * P/oddio ol/onllcus onomioides Boy of TirobrQlulinD Ponomioides ° 'slow • ear onnu/ola Biscay Torebrotoltho P/a/idio septentriono/lS ° dovidsoni • Fol/os Mega/hiris da//iniformis ° d./runcalo /I sponirhynch/o cnrneo

Flo. 7. Brachiopod distribution map. C. HOWARD, C. BRUNTON AND G. B. CURRY 1 12° 10° 8° •.6° 4° 2°W 0° 1 ■ °.o o, Collecting and Preservation

In this section we consider only those species included in this Synopsis although the methods described are commonly applicable to species fount • elsewhere. Since none of the species is found intertidally, collecting is not easy, an depends upon diving or bottom trawl methods. This is not the place to describ diving methods, other than to say that nobody should attempt to dive withou —56°N full equipment, training, and trained companions. Most brachiopods have been collected by trawling, usually by research vessel from various marine research laboratories. Whilst dredging may be the mo> North •• successful, it is certainly not the ideal collection method, as specimens are liahl Sea to become damaged, and brachiopods attached to large rocks are unlikely to b sampled. However, under favourable conditions, trawling can be extreme)

— 54° productive, such as off the west coast of Scotland where, using a "clam-dredge' the yield from a single trawl can be several thousands of brachiopods. Once collected, brachiopods can be transported alive for long distances, ove a period of several days, provided certain basic conditions are fulfilled: befor transportation as much as possible of the associated fauna and substrate must b removed, but the exterior of the brachiopods should not be scraped, as th damages the periostracum. Where brachiopods are attached to the shells c — 52° other hard-shelled invertebrates, such as molluscs, a pair of strong pliers can b used to break up the host shell, leaving the brachiopods attached only to a sma fragment. It is preferable to leave the pedicle undamaged, but when collectin specimens attached to large rocks they will have to be cut as close as possible t the rock, using a sharp scalpel. (When introduced into aquaria such brachiopoe can he kept alive by placing them, posterior-down, in suitably sized perforation — 50° in a plastic sheet; see McCammon, 1972 for details.) Once cleaned, the specimens should he placed in a small plastic bag, eithc with a small supply of fresh sea-water, or wrapped in cotton wool or sea-wee. Western soaked in sea-water. The plastic bag should be sealed so as to enclose as muc Approaches air as possible and placed in a vacuum-flask for trnsportation. The addition 41. ice to the flask (hut not to the bags) will ensure that the desirable lo• temperature is maintained. Brachiopods transported in this way have survive — 48° France journeys of up to five days duration. 1(•y ,0 The ideal situation for keeping brachiopods alive is in a tank with a constat llemifAiris Arpyroiheco inflow of fresh sea-water (carrying food), balanced by an outflow removir psilloceo a Cisfal/u!O • waste materials from the tank. In practice this is possible only in marir Oal/ina ArpyrorA.co s ep"pero cuneofo 0 laboratories. However, brachiopods have lived successfully in sea-water mac MoCandierrd • GIypAus up from commercially available synthetic salts, to which has been adde cramum re reus G/oc ,orculo £uco/o/Ais nutrients, such as beef-heart minced in a blender with sea-water and the sp,lyderpensis AI Iuberal° Bay o f Biscay filtered (see McCammon, 1972). In addition, vitamins are needed to keep tl• Megerfio Gwynio brachiopods healthy, and suitable commercial preparations are available. A Iruncola * copsu/o Meperho echino/o r. airlift system, as • described by King and Spotte (1974), will ensure watt

Fu:. 8. Brachiopod distribution map. 18 uB11i511 BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 19 circulation within the tank, while a light-proof covering inhibits algal growth on Classification its walls. It is important that the temperature is maintained at a low and constant value; 10°C will suit most British species. Brachiopods are prone to fungal Brachiopods and some bivalve molluscs look somewhat similar externally but infections which, if untreated, will eventually cause death. Suitable fungicides ' the two groups can be separated by the following characteristics (see Figs 9, 10). are available commercially, and should be added at the recommended concentrations. Methods of setting up a salt-water aquarium have been described by BRACHIOPODA BIVALVIA King and Spotte (1974); whilst the specific requirements for brachiopods have been described by McCanuuun (1972). A. Articulata It the soft tissues of specimens are to be studied it is necessary to fix them in a Valves dorsal and ventral, the Valves right and left, normally suitable solution, e.g. 10% formalin, before placing in a preservative, e.g. latter normally larger and with externally like one another alcohol, 5' b formalin, formal saline, or Phenoxetol. Alternatively specimens can a pedicle aperture. and lacking umbonal aperture. he allowed to dry, and kept in covered containers. If the shell alone is required, free of soft tissue, the specimen can be cleaned by placing in a solution of sodium Plane of symmetry median, Plane of symmetry separates hypochlorite (domestic bleach or Milton's solution) for about half an hour. Care bisecting the two valves from two valves laterally. is necessary as bleach is caustic. Specimens should not be left in these solutions front to back. for longer periods as their shells will soften. Then carefully wash in clean Attached to substrate by single Attached to substrate by numerous running water, if necessary brushing with a fine paint brush to remove traces of short stalk (pedicle). Rarely threads, cemented or free moving. tissue. Great care must be taken to avoid breaking the brachial loops in cemented by ventral valve. terebratuiids. It is very important to record full information about the specimens: locality, Internally with coiled lophophore. No lophophore, but, with gills. depth, water temperature, associated fauna, method of collection, date of May have locomotory muscular collection, etc. and assistance with identifications can be obtained !rum the foot. senior author at the British Museum (Natural History), London. Mantle margins sometimes fused. Single pair of strong articulating Hinge teeth very variable, valves teeth. Internal skeletal hinged with an elastic ligament. structures posteriorly, including Usually no skeletal internal lophophore support. structures.

B. Inarticulata The pedicle of lingulids protrudes from between the posterior umbos— no valve aperture—and is much reduced in conical discinaceans and craniaceans.

Brachiopods are grouped in a phylum of their own, evolutionarily distinct from the class Bivalvia in the phylum Mollusca. Emig in Synopsis No. 13, British and other Phoronids (1979) includes the Brachiopoda along with the Bryozoa and Phoronida in a phylum Lophophorata. We agree that there are similarities between these groups, but nevertheless prefer to retain three separate phyla. The following classification is as in Williams (1965). •

20 BRIt ISII .IIRACIIIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 2 Phylum BRACHIOPODA Class INARTICULATA Order ACROTRETIDA Suborder CRANIIDINA Superfamily CRANIACEA Family CRANIIDAE Crania anonrala (Muller) Suborder ACROTRETIDINA Superfamily DISCINACEA Family DISCINIDAE Pelagodiscus whatnots (King) Class ARTICULATA Order RIIYNCHONELLIDA Superfamily RHYNCIIONELLACEA Family CRYPTOPORIDAE Cryptopora gnomon Jeffreys ventral Family HEMITI-IYRIDIDAE Ile,nii/tiris p.sittacea (Gmelin) Family FRIELEIIDAE Ifispanirhynchia cornea (Davidson) Order TEREBRATUL1DA Suborder TEREBRATULIDINA Superfamily TEREBRATULACEA Family TEREBRATULIDAE • Gryphus vitreus (Born) Family CANCELLO'I'1I?RIDIDAE 7erebratrtlina retusa (Linnaeus) Terebratulina septentrionalis (Couthouy) Et:cab:this trrberata (Jeffreys) Suborder '1 EREBRA'I ELL.IDINA Superfamily 'lT RE13RA"I'ELLACEA Family MEGATIIYRIDIDAE Megathiris detruncata (Gmelin) Argyrotheca cistellula (Searles-Wood) Argyrothecu cuneata (Risso) FIGS 9, 10. Diagrams of a generalized articulate brachiopod (above) and a bivalve mollusc (below) showing their orientation and symmetry. Gwynia capsula (Jeffreys) Family PLA'I'IDIIAE Platidia anonrioides (Scacchi and Philippi) Platidia anomioides var annulata Atkins Platidia davidsoni (Deslongchamp) Family KRAUSSINIDAE Megerlia trurncata (Linnaeus) Megerlia ec/rinwa (Fischer and Oehlert) Family DALLINIDAE Dallina septigera (Lovén) Pallas dallinijbrnris Atkins Glaciarcula spitzbergensis (Davidson) Macandrevia cranium (Muller) 22 BRITISH BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 2 Key to the British Species 4. Small (less than 5 mm long) thin shells with high dorsal median septun

Cryptopora gnomon (p. 25 This key allows the identification of well-preserved adult brachiopods from the seas around the British Isles. As far as possible identification can be made without the use of a hand-lens or binocular microscope. However, several Medium sized (20-30 mm long) globose black shells with delicate externa species are small (less than 5 nun in length) and their morphology can only be ribs Hemidriris psittacea (p. 2t • seen adequately using a microscope. Being the first published key for Iiving brachiopods, this is likely to require Medium sized, globose light-coloured shells with only fine external radia emendation and the authors welcome comments. The following points should be born in mind. striations Hispanirhynchia cornea (p. 2 (1) The characteristics of juvenile specimens may be very different from the adult characteristics used in this key. 5. Shells lacking a dorsal median septum and with short brachial loop (2) A short brachial loop reaches less than half the length of the dorsal valve. (3) It is important to see inside the brachiopod shell, many of which do not Shells with a dorsal median septum and long brachial loop open easily or widely. Larger wet specimens can be opened by pinching postero-laterally and slipping a match between the valves anteriorly. Complete disarticulation is commonly impossible without breaking the 6. External ribbing absent, medium sized (30-40 mm long) teeth or sockets. The opening of small dry specimens is a delicate operation. The insertion of a finely pointed scalpel anteriorly may help. Gryphus vitreus (p. 2t, (17)Brachiopod brachial loops are fragile structures, easily becoming broken. Since brachial loop morphology is important taxonomically, specinens with Valves with external ribbing, commonly less than 20 mm long broken loops must be studied carefully for evidence of previous points of attachment between loops, crura and septa. 7. Small (less than 5 mm long), subcircular outline, crural processes n (5) With specimens retaining desiccated tissue, it is important to distinguish this from skeletal structures. meeting ventro-medianly Eucalathis tuberata (p. 3 . (6) The recognition of endopunctation normally requires magnification in excess of about 10x. holding the specimen up against the light often helps. Q Up to about 20 mm long, ovate outline, crural processes unit ventrally forming a complete brachial ring

1. Shells with upper valve conical (Figs 11, 12) 2 8. Number of ribs on dorsal valve in 5 mm width at 10 mm from umbo rang Shells with two free valves, pedicle attachment and paired teeth 3 from 11 to 14 (mean value 12) Terebratulina retusa (p. 2~

2. Thin chitinophosphatic shell (dark coloured and leathery), ventral valve Number of ribs on dorsal valve in 5 mm width at 10 mm from umbo rang

with pedicle notch Pelagodiscus adanticus (p. 24) from 16 to 21 (mean value 18) Terebratulina septentrionalis (p. 31

Thin calcareous shell (light coloured and brittle), ventral valve cemented to 9. Small (less than 5mm long) variably shaped shells with broad simple substrate Crania anoanala (p. 23) lophophore support attached at least once anteriorly in the dorsal valve,

no dental plates 10 3. Shell material impunctate, no internal brachial loops 4 Small (less than 10 mm long), variable shells, the 'adults with minute or long Shell material endopunctate (Fig. 6C), having brachial loops 5 complex brachial loops 14

24 BRIIIxII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 25

Medium sized (greater than Ill mm long) variably shaped shells 17 17. Valves commonly ribbed, having wide straight posterior margins 18 10. Shell strongly ribbed, loop attached at three or five points around dorsal Smooth, elongate and globose shells with a narrow hinge- valve Megathiris detrnncuta (p. 33) line 19 Shell smooth with minute loop tir ribbed with loop attached .anteriorly to median septum 11

II. Minute (less than 2 mm long) ovate globose shells

Gwynia capsula (p. 36) 18. About 15 mm long, with persistent external ribs....Megerlia truncata (p. 39)

Small, straight hinged, well ribbed or smooth shells 12 About 10mm long, with tuberculate exterior, especially the ventral valve

Megerlia echinara (p. 40) 12. Shells having ring shaped loop attached antero-medianly 14

Shells smooth, having long loop or minute simple lophophore ..13 19. Subtriangular globose shells with sulcate anterior commissure 20

Ovate, non-sulcate shells with disjunct deltidial plates 13. Small rounded shells with minute brachial loops 15 Macandrevia cranium (p. 44)

Usually medium sized, variably shaped shells with long complex loops..l6 20. Shells reaching 35 mm in length; no dental plates and loop unattached to

14. Smooth shells up to 3mm long .Argyrotheca cistellulu (p. 34) median septum (Fig. 6B) Dallina septigera (p. 41)

Strongly ribbed shells .Argyrotheca cuneata (p. 35) Shells reaching 25 mm in length; with dental plates (Fig. 4) and loop attached to median septum Fallcrx dallinifornlis (p. 42) 15. Valve exterior tuberculate and loop incomplete..Platidia davidsoni (p. 38)

Valve exterior smooth and loop complete

Platidia wnOatiOiHeS (l). 33)

16. Elongate shells (up to 10 mm long), with prominent pointed ventral umbo Glaciarcula spitzbergensi.s (p. 43)

Adults more than 10 mm long 17 26 BRI'IISI,I BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 27 Systematic Descriptions

Class 1NARTICULATA Shells with calcareous or chitinophosphatic valves, never articulated by teeth and sockets, and the lophophore never supported by shelly material. The alimentary canal terminates with an open anus and muscles alone articulate the ` shell.

Crania anomala (Muller) (Fig. 11A, B)

Patella anomala Muller, 1776 Orbicula norvegica Lamarck, 1801 Crania anonuda is usually oval in vertical view, reaching about 15 nun in width, but will reflect the irregularities of the substrate to which its ventral valve is attached. The dorsal valve of the shell is conical in lateral view, with the apex situated slightly posteriorly (Fig. 11B). Its surface is usually smooth or finely striate, and concentric growth-lines are present. C. anomala is very variable in colour, the periostracunt being dark brown or reddish, while the underlying shell is light grey. It has neither a functional pedicle nor a pedicle opening. The shell is endopunctate. A C. anomala is found abundantly off the west coast of Scotland, attached to boulders and the hard skeletons of other invertebrates. It has also been recorded 5mm from around the Shetlands, Ilcbrides, oil the north-west and south of Ireland, the south coast of England and in the English Channel. It is noticeably absent in the Irish Sea and off the east coast of England. Elsewhere it has been found olf the Canary Islands, the Faeroes, Nolway, Iceland and Spitzbergen. C. auQanQuli is most commonly found in shallow water (15-165 m) although it has been collected, infrequently, from depths of 183 to 914 tu; and there is one rceoud front 1484 m.

FIG. 11. Crania anomala (Muller). Dorsal valve: A, plan view; B, lateral view.

•

28 BRIIISII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 29

Pelagodiscus ailanticus (King)

a (Fig. 12A, B)

Discina Manteca King, 1868 Discinisca etIlanNlca Davidson, 1888 I'rlasi'otliscu.s atlunticus (King) is a cemented inarticulate. brachiopod, circular • in outline and conical in profile. Morphologically it is similar to Crania ununtula hut much smaller; its maximum diameter being approx. 6mm. The valves of the shell are dark to light brown in colour, and have concentric growth-lines. The shell is chitinophosphatic and endopunclate. Mantle setae are very long, and help distinguish P. atlunticus from juvenile Crania anontala. P. atlunticus occurs off north-west and west Ireland, the former being the type area of the species. Elsewhere it has been recorded from all oceans and appeals to be one of the most cosmopolitan of Recent brachiopods. It is always found in deep water (366-5482 m) attached to hard substrates, such as rock or other shells.

3 mm

Fla. 12. Pelagodiscus adanticus (King). Dorsal valve: A, plan view; B, lateral view.

30 8R1't aStt BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 31

Class ARTICULATA Shells with only calcareous valves, articulated by a pair of teeth and sockets. All living species have variably developed skeletal lophophore supports. 'I he alimentary 'canal ends blindly, having no anus.

Crypropora gnomon Jeffreys (Fig. 13A-C) Crypropora gnomon Jeffreys, 1 869 Aireria gnomon Davidson, 1887 Neutre►ia gnomon Fischer and Oehlert, 1891 Crypropora gnomon Jeffreys reaches a maximum length of approx. 6 mm. The shell outline is suhoval, with pointed ventral umbo and slight anterior sulcation. The external surfaces are smooth. The shell is impunctate and transparent. The pedicle is long and thread-like. Internally it is characterized by a large blade-like dorsal median septum; the lophophore is supported by thin, curved crura. C. gnomon occurs off north-west, western and southern Ireland. Elsewhere it has been collected in the Atlantic, where it extends as far south as Florida and Cuba. It has been found attached to rocks and other pieces of debris at ilel+ths ui A B 183 to -1023 in. 2mm

FIG 13. Crypropora gnomon Jeffreys. Exterior views: A, dorsal; B, ventral; C, lateral.

32 BRITISH BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 33

Reatitbiris psirtacea (Gmelin) (fig. 14A—D) Anomia.psittacea Gmelin, 1790 latynchonella psirtacea Davidson, 1887 Rentit/tiri.r psirtacea (Gmelin) reaches a maximum length of approx. 26 nun; the length and width of the shell of adults are approximately equal, and the outline is subtriangular. Valve exteriors are finely ribbed and have concentric growth-lines. The colour varies from dark bluish-black to a variety of shades of grey and brown. The pedicle foramen is elongate and the sharp prominent ventral umbo is recurved. Sulcation of the anterior commissure occurs only in specimens more than about 16 mm long. The shell is impunctate. 'I he lophupkore is supported by short flattened crura. 11. psinaceu occurs in the North Sea, around the Shetlands, Orkneys, and Hebrides and off north-west Ireland. Elsewhere it has been collected in the Arctic Ocean, off Spitzhergen, Greenland, the west and east coasts of Canada and the USA and off Japan. IL psirtacea, therefore, has a cold-water circumpolar distribution, and its relatively rare occurrences in British waters represent its southern-most extension into the Atlantic. It has been collected at depths from 15 to 10% m. 10 mm

Flo. 14. Hemithiris psirtacea (Gmelin). Exterior views: A, dorsal; B, ventral; C, lateral; D, anterior (with ventral valve uppermost). 34 BRI11511 BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 35

fIlsporirhy:u•biu cornea (Davidson) (Fig. 15A-D) • RhynchoHella cornea Davidson, 1887 Ilispunirhyncl:ia cornea (Davidson) reaches a maximum length of approx. 25 mm and a maximum width of approx. 20mm. Theshell outline is sublriangu- lar and the lateral profile is slightly globose. External surfaces are finely striated and have concentric growth-lines. The ventral umbo is slightly recurved. 'I he shell is impunctate. The lophophore is supported by short, thin crura. Il. cornea has only been found in the English Channel and off south-west Ireland, at depths from 105 to 2388 m.

A B

I0 mm

Fm. 15. llispanirhynchia cornea (Davidson). Exterior views: A, dorsal; B, ventral; C, lateral; 1), anterior (with ventral valve uppermost).

36 BRIT ISII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 37

Grypluts vitreus (Born)

(Fig. 16A-C) Anomia vitrea Born, 1778 Liothyris vitrea Davidson, 1886 Terebratula (Liothyrina) vitrea Fischer and Oehlert, 1891 • Gryphus vitreus (Born) reaches approx. 40 mm in length and approx. 35 mm in width. The outline of the shell is oval and external surfaces are smooth, marked only by concentric growth-lines. It is white to light grey in colour. The ventral mho is small and the deltidial plates unite medianly forming a circular pedicle foramen. The brachial loop is short. Posteriorly the shell substance is much thickened, causing the shell to tip posteriorly when placed on a flat surface. The shell is endopunctate. Spicules are present in the body tissues and the filaments of the lophophore. G. vitreus has been collected in the Western Approaches. Elsewhere it has been found in the Bay of Biscay, the Mediterranean and off the coast of North Africa. It occurs at depths from 73 to 2663m.

.5mm

Flo. 16. Gryphus vitreus (Born). Exterior views: A, dorsal; B, lateral; C, ventral.

38 BRIl1511 HRACIIIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 39

Genus TEREBRATULINA d'Orbigny, 1847 Type species: Terebratulina retusa (Linnaeus), 1758 Ovate, biconvex shells with a straight to slightly folded anterior commissure. Both valves are 'entirely ribbed and the deltidial plates are disjunct. Internally with converging crura supporting a short ring-like brachial loop; there are no dental plates ur median septa and the internal epithelia are supported by spicules.

Terebruudina retusa (Linnaeus) (Fig. 17A-C) Anomia retusa Linnaeus, 1758 Anomia curputserpenlis Linnaeus, 1767 Terebrcnulina carputserpentis Davidson, 1886 On present evidence Terebrurulinet retusa (Linnaeus) is the most common brachiopod in British waters. The shell achieves a maximum length of approx. 30 n t, although large collections from the west coast of Scotland indicate that in this area the maximum length is 23 mm. The shape is roughly oval, and the anterior commissure is slightly sulcate. Externally the valves have numerous, rather coarse, radial ribs (approx. 12 in a 5 nun width on the dorsal valve, 1() mm from the umbo—ace under Terebratalinu xepreorrionalis). These ribs become nodose forming smooth rounded Iuhercules, at the postero-lateral margins of both valves, although they are best developed on the flanks of the ventral umbo. A variable number of concentric growth-lines are present. The colour varies from white to yellowish-grey. Additional colouration is often present during the breeding season, as the colour of ripe gonads (females are yellow or orange, males cream) often shows through to the external surface. The deltkial plates are small and disjunct. r. retusa is cndopunctate, with a tendency for the endopunetae to be arranged radially on the interior of the valves—in positions corresponding to the external ribs. Spicules are present in the body tissue being densely packed in the lophophore and in the tissue covering the mantle canals. T. retusa has been collected widely around the British Isles, although it has never been found off the east coast of England or in the southern Irish Sea. Elsewhere it has been found in the northern North Atlantic from Scandinavia to the east coast of Greenland, and as far south as the Mediterranean. it ()cents at depths from 15 to 1478 m. On the west coast of Scotland it has a rather patchy distribution, preferring deeper water (811-200 m) where it can be obtained in FIG. 17. Terebratulina retusa (Linnaeus). Exterior views: A, dorsal; B, lateral; C, ventral considerable numbers (thousands per dredge haul). It is commonly found attached to the horse-mussel Modiolus ucocIioIus (Linnaeus), as well as on blocks of clinker and boulders; it has also been found attached to sponges, hydroids, and assorted pieces of debris. 40 BRI'I1511 BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 4

Terebratulina septentrionalis (Cout houy) (Fig. 18C) Terebratula sepren►rionalis G. B. Sowerhy, 1846

T erebrundl►ta septentrionalis (Couthouy) is very similar to Terebratulina retusa :(Linnaeus) in size, shape, and colour. The surface ornamentation of the shell is also similar but the ribs on T seprentrionalis are finer and more numerous, and the pustules, typical of T. relusu, are absent. As T. septentrionalis and T. retusa have often been confused the exact distribution of the two species is unclear. However, around the British Isles T. sepreu:rionu►lis seems to be confined to deep water areas off north-west Ireland and west Scotland. This is in contrast with its distribution on the east coast of Canada and the USA, where it commonly occurs in shallow water. It has been recorded from the northern and eastern North Atlantic at depths from 0 to 1238 in. Differentiation of the two species of 7erebrandina is possible by studying the ribs and postero-lateral pustules. The table below shows the numbers of ribs in a width of 5 m On the dorsal valve, at a distance of 10 min from the vent' al umbo (it being easier to measure from the ventral umbo):

number of ribs average

• 7. retusa 11-14 12 7'. septentrionalis 16-21 18

• The biological distinction of these species has not been fully verified, and the differences in ribbing may prove to result from variations in ecological conditions. •

B 05mm C 0 5mm

Flo. 18. Comparison between T. retusa and T. septentrionalis. A, showing location of B and C. B. exterior view of coarse ribbing in T. retusa. C, exterior view of finer ribbing in T. septentrionalis.

42 HKtrlSI( BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 4: Ettcaladais tuberuta (Jeffreys) Megathiris detruncata (Gmelin)

A B 3 mm 2mm

Flo. 19. F:ucalathis sabering (Jeffreys). !islet or views: A, dorsal; B, ventral; C, lateral.

7erebru(rtht iuberatu Jeffreys, 1878 FIG. 20. Megathiris detruncata. (Gmelin) Exterior views: A, dorsal; B, lateral; C. ventral. Terebrutulina ntberato Davidson, 188( Eucula his tuberata (Jeffreys) is a small brachiopod—its maximum length Anomia detruncata Gmelin, 1790 being approx. 5 mm. The shell outline is triangular with a rounded anterior; it is Argiope decollate Davidson, 1887 greyish-white in colour. The ventral Limbo is pointed, and the deltidial plates do Megathyris decollate Fischer and Oehlert, 1891 not join mediaely; the pedicle foramen is oval in shape. The external surlaces Megathiris detruncata (Gmelin), a small brachiopod, reaches a maximum have numerous ribs, which are commonly tuberculate, especially on the ventral length of approx. 5 mm. The outline of the shell is transversely oval, with a wide, valve. 1 he shell is endopunctate. E. tuheruta has a short loop. straight, hinge-line. Specimens are often wider than long. The external surfaces E. ttrhertta occurs in the Western Approaches; elsewhere it has been recorded have a few broad ribs. The shell has small deltidial plates, a large pedicle from the flay of Biscay, around the Azores, and in the south-west Mediterra- foramen, and is endopunctate. M. detruncata has a lobed brachial loop, attached nean. It has only been found in deep water (539-2736 m). at three or five points on the internal surface of the dorsal valve. M. detruncata is known from the Western Approaches and around Guernsey. Elsewhere it has been collected from the Mediterranean; it occurs at depths from 37 to 896 m.

44 BRli ISII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 45 Genus ARGYROTHECA Dall, 1900 Type species: Argyrotheca cuneuta (Risso), 1826 Small transversely ovate shells with a wide hinge-line and gently biconvex profile. The pedicle aperture is large, with small disjunct deltidial plates. The valves of the shell are broadly ribbed or smooth. Internally the crura are widely separated and sl ort. The long brachial loop almost reaches the margins of the dorsal valve and is attached to the median septum anteriorly.

Argyrotheca cistellula (Searles-Wood) (Fig. 21A—C) A B Ierebrutula cistellula Searles-Wood, 1841 . Aleguthyris cistelluTh Forbes and Hanley, 1850 I mm Cistella cistellula Davidson, 1887 Argyrotheca cistellula (Searles-Wood) reaches a maximum length of approx. 3 mm. In outline the shell is sub-rectangular, and may be slightly bilobed anteriorly. It has a wide straight hinge-line. The external surfaces are smooth save for faint concentric growth-lines. It is white, yellow, or grey in colour. The deltidial plates do not join mediclly, and the pedicle foramen is large. The shell is endopunctate. A. cistellula has a simple bilobed, long loop, attached to the valve attic ro- media lily. A. cistellula is the more common of the two species of this genus in Iln illsh waters and occurs off north-east Scotland, the I lebrides, Donegal, Anti int, Dublin Bay, Exmouth, Guernsey and Normandy. Elsewhere it has been found off Norway and around Sardinia and Sicily. It occurs at depths from 37 W 82111. Flo. 21. Argyrotheca cistellula (Searles-Wood). Exterior views: A, dorsal; B, lateral; It lives attached to hard substrates, and one report mentions 200 specimens C, ventral. attached to a stone.

Argyrotheca cuneata (Risso) 22A, 13) 7•erebrauda cuneuta Risso, 1826 Cisiellu cuneuta Davidson, 1887 The shells of Argyrotheca cuneuta (Risso) and Argyrotheca cistelhda (Searles-Wood) are similar in size and shape, but A. cuneuta can be distinguished by having broad ribs on the external surface of each valve. It is white or grey in colour, often with a distinctive red colouration between the ribs. A B I mm t A. euneant occurs in the Western Approaches of the English Channel and elsewhere has been found in the Mediterranean, the Aegian, and around the Canaries. It occurs at depths from 51 to 366m. FIG. 22. Argyrotheca cuneuta (Risso). Exterior views: A, dorsal; B, lateral.

46 BR11ISII BRACHIOPODS ' C. HOWARD, C. BRUNTON AND G. B. CURRY 47

Gwynia capsula (Jeffreys) (Fig. 23A-C) Terehrarula capsula Jeffreys, 1859 Gwynia capsula (Jeffreys) is an extremely •small brachiopod, reaching a maximum length of approx. 1.5 mm. The outline of the shell is ovate and ' globose. The external surfaces are smooth save for faint concentric growth-lines. It is white or yellowish in colour. 1 he deltidial plates are small and do not join medianly; the pedicle foramen is relatively large. The shell is endopunctate. G. capsula has been collected oil the north coast of Ireland (Portrush), in Belfast Lough and Dublin Bay, off the coasts of north Wales, Dorset, Guernsey, Jersey, north France and in the Western Approaches. It has been found in shallow water (15-46 m) attached to rocks, where it is difficult to spot because of its extremely small size. 0.5mm • There has been considerable speculation about this tiny brachiopod—the fact that it often occurs alongside Argyroslwca cis-renal(' (Searles-Wood) has led to the suggestion that it is a permanently immature form of that species. I fowever, this has never been proved convincingly, and G. capsula remains one of the most unusual and interesting of the Recent brachiopods described here.

Fin. 23. Gwynia capsula (Jeffreys). Exterior views: A, dorsal; B, lateral; C, ventral.

} I

BRIIISII 48 BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 49 Genus PLATIDIA Costa, 1852

Type species: i'lenidia anomioides (Scacchi & Philippi), 1844 Small subcircular shells with a wide hinge-line and a large pedicle aperture extending into bath valves. The shell is thin and semitransparent with smooth or finely tuberculate exteriors. Internally the crura and brachial loop are minute.

1'luridiu anomioides (Scacchi and Philippi)

24A-C) A B 3 mm Orthis anomioides Scacchi and Philippi, 1844 Mlorrisia anomioides Davidson, 1852 . Platydiu anomiokles Davidson, 1 887 The shell of 1'lutidia anomioides (Scacchi and Philippi) reaches a maximum length of approx. 5 mm, and an approx. maximum width of 6 mm. In outline it is circular to transversely oval. The dorsal valve is almost flat, and the external surfaces are smooth except for concentric growth-lines. It is yellow or while in colour. The pedicle foramen is large and extends into the dorsal valve; narrow deltidial plates are present. The shell is endopunctate. Spicules are common in the body tissues. P. anomioides has a short loop. P. emumiuides occurs off the Hebrides, to the west of Ireland, and in the Western Approaches and the Bay of Biscay. Elsewhere it has been found in the Mediterranean, and off Florida, Cuba, and the West Indies. It occurs at depths Fio. 24. Platidia anomioides (Scacchi & Philippi). Exterior views: A, dorsal; B, ventral; from 82 to 741 in. In the Western Approaches it has been found attached to the C, lateral. dead regions of the coral Lopheliu profiJeru (Linnaeus).

Plaiidia diuoatiohles var. utnudata Atkins, 1959 Platidia tantalum Atkins was a recently described species based on only a few specimens. In size, shape and colour it was said to be similar to P. anomioides, from which it was distinguished by having extremely long mantle setae, and internally, by having a complete brachial ring attached to a median septum. Atkins found her specimens in the Western Approaches of the English Channel from 1298 to 17741n, attached to the dead regions of the coral Anisupsaimho rostrate (I'ourtales). Until larger samples, showing Complete growth series, are available for study, we do not feel confident in retaining P. annuluru as a separate species and therefore treat it as a variety of P. anomioides.

50 IIRIUISH BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 51

Platidia davidsoni (Deslongchamp) (Fig. 25A-C) Morrisia tluvidsoni Deslongchamp, 1885 The shell of Platidia duvidsoni (Deslongchamp) is similar to, although larger than,'that of Plutidiu unontiuides (Scacchi and Philippi), reaching a maximum size of approx.'8 mm. The presence of numerous small pustules on the exte►nal surfaces of the ventral valves of P. davidsoni distinguish it from P. unu niuidcs. P. duvid. oui has been found in the Bay of Biscay and the Mediterranean, at imm depths from 82 to 402 m. A B

Fin. 25. Platidia davidsoni (Deslongchamp). Exterior views: A, dorsal; B. ventral; C, lateral. o

52 IiKt'I ISII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 53

Genus MEGERLIA King 1850 Type species: Megerlia mascara (Linnaeus), 1767 Transversely oval to suhyuadrate in outline, with a wide hinge line and a pedicle itperture restricted by disjunct deltidial plates. The valve exteriors are finely ribbed to tuberculate. Internally there is a wide cardinal process and a long loop attached to a posterior median septum.

Aegerlia Iruncata (Linnaeus) (Fig. 26A-C) Anomia Iruncata Linnaeus, 1767 M171tfeldtia mascara Fischer and Ochlert, 1891 The shell of Megerlia Inutcata (Linnaeus) reaches a maximum length of approx. 20 mm—adults are wider than long. The outline is transversely oval, and 5mm the dorsal valve is relatively flat. The colour varies from white to yellow, and may be tinged red due to internal tissue colouration. The pedicle foramen is large and circular, extending slightly into the dorsal valve. The deltidial plates are narrow and do not join medianly. The external surfaces of the valves have numerous fine radial ribs, and concentric growth-lines. The shell is endupunc- tate. Spicules are common in the body tissue. M. truncata has a long loop remaining attached to the median septum. il. truneuht has been found in the Bay of Biscay, and in the Western Approaches where it has been found growing on the coral Dendrol'h►•lliu eamigerr Lamarck, and here its life-position is perpendicular to the substrate. Elsewhere it has been recorded from the Mediterranean, the Acgian, and around Teneriffe. it has been found at depths from 82 to 192 in.

FIG. 26. Megerlia truncata (Linnaeus). Exterior views: A, dorsal; B, lateral; C, ventral

. • . .

54 BRI'IIStt BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 55

Megerliu echintua (Fischer and Oehlert) Dallina septigera (Lovén)

2mm

A 10 mm • B FIG. 27. ittegerlia echinata (Fischer and Oehlert). Exterior views: A, dorsal; B, lateral.

Muhlfeldlia echinata Fischer and Oehlert, 1891 Pantellariu echinata DaII, 19211 Megerliu echinura (Fischer and Oehlert) is similar to Megerlia truneala (Linnaeus) in size, shape and colour, but can easily be distinguished by its external spinose pustules, especially on the ventral valve. In life-position the dorsal valve lies against the substrate, and reflects its irregularities. M. echinata occurs in Western Approaches. Elsewhere it has been recorded front off West Africa, the Cape of Good Hope, Australia and in the Caribbean. It has been found at depths from 585 to 1426 m. 0

Fla. 28. Dallina septigera (Lovett). Exterior views: A, dorsal; B, ventral; C, lateral; D, anterior (with ventral valve uppermost).

Terebratula septigera Lovén, 1846 Waldheimia septigera Davidson, 1886 Magellania septigera Fischer and Oehlert, 1891 The shell of Dallina septigera (Lovén) reaches a maximum length of approx. 37 mm. The outline is triangular; it is widest anteriorly and may be wider than long. A broad anterior sulcation is present. The external surfaces of the valves are smooth except for concentric growth-lines. It is white or yellowish in colour: The pedicle foramen is circular, and deltidial plates unite medianly. The shell is endopunctate. D. septigera has a long loop with a wide, hooded, transverse band. D. septigera occurs in the North Sea, off the Shetlands, northern Scotland, and north-west and south-west Ireland. Elsewhere it has been collected off Norway, west Portugal and around the Canary Islands. It has been found at depths from 219 to 1037 m. 56 HRH IS11 BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 57

Fu Ilwi dol(iniforuvk Atkins, 1960 Glaciarculu spitzbergensis (Davidson) (rig. 4A-C, p. 7)

This brachiopod is homeomorphic with Dulling septigera (Lovén), and has only recently been recognized as a separate genus. The distinguishing features are that F drtllinifonnis has dental plates, well developed spiculation in the body tissue and a loop connected to the median septum. l: dalliniformis has been found in the Western Approaches at depths hum 219 to 1037 m. The distribution of this brachiopod is likely to be wider than presently known, as specimens collected before 1960 may have been identified as Minim, septigera (Lovell).

A B

5mm

Fla. 29. Glaciarcula spirzbergensis (Davidson). Exterior views: A, dorsal; B, lateral; C, ventral; D, anterior (with ventral valve uppermost).

Terebratella spitzbergensis Davidson, 1852 7erebratalia spitzbergensis Dall, 1920 Diestothyris spitzbergensis Thomson, 1927 The shell of Gluciurculu spitzbergensis (Davidson) reaches a maximum length of approx. 10 mm. The outline is circular or oval, and the external surfaces are smooth except for fine concentric growth-lines. It is yellowish-white in colour. The pedicle foramen is elongate, and the deltidial plates do not join medianly. The ventral umbo is slightly incurved. The shell is endopunctate. G. spitzbergen- sic has a long loop attached to a median septum. In British waters G. spitzbergensis has been found around the Shetlands and the Scilly Isles, at depths from 73 to 701 m. Elsewhere it has a circum-Arctic distribution, having been found off Iceland, the Faeroes, Norway, Spitzbergen, arctic Canada and Japan. 58 BRI IISII BRACHIOPODS C. HOWARD, C. BRUNTQN AND G. B. CURRY 59

Macandrevia cranium (Miller)

Glossary

ADDUCTOR MUSCLES: The paired muscles which, on contraction, close the shell. Each is commonly divided dorsally into anterior and posterior elements (Fig. 1). BODY CAVITY: The posterior coelomic region between the two valves, enclosed by epithelium, containing the body organs; digestive system, muscles, metanephridia, etc. (Fig. 1). BRACHIAL (or mantle) CAVITY: The anterior space between the valves, • lined by mantle and body-wall epithelium, containing the lophophore (Fig. 1). BRACHIAL LOOP: Delicate shelly loop-like support for the lophophore extending anteriorly from the crura. There may be a supporting median 2mm septum (Fig. 6A, B). CAECA (sing. CAECUM): Outgrowths of the outer mantle epithelium contained in the endopunctae of the shell substance. CARDINAL PROCESS: Postero-median area of attachment of the diductor muscles in the dorsal valve, commonly a bilobed boss of shell (Fig. 3). COMMISSURE: The line of junction between the edges of the two valves. CRURA (sing. CRUS): Shelly processes extending forwards from the socket region of the dorsal valve, giving support posteriorly to the lophophore. The distal ends may be prolonged into a brachial loop supporting much of the lophophore (Fig. 3). CRURAL PLATES: Shelly plates extending medianly from the crura, sometimes fusing to the floor of the dorsal valve. DE1.TI IYRIUM: Median triangular aperture in the margin of the ventral valve, wholly or partially used as the pedicle aperture (Fig. 4). DELTIDIAL PLATES: Pair of shelly plates, growing medianly from the • delthyrial margins, constricting the pedicle aperture (Fig. 4). DENTAL PLATES: Shelly walls supporting the teeth from the floor of the Fin. 30. Macandrevia cranium (Muller). Exterior views: A, dorsal; B, lateral; C, ventral. ventral valve (Fig. 4). DIDUCI'OR MUSCLES: The paired muscles which, on contraction, open the 7erebrazula cranium Muller, 1776 shell by pulling on the cardinal process, situated on the opposite side of the Waldheimia (Macandrevia) cranium Davidson, 1886 hinge axis from the ventral areas of attachment (Fig. 1). Magellanic (Macandrevia) cranium Fischer and Oehlert, 1891 DIGESTIVE DIVERTICULA: Large secretory organ, assisting in the diges- The shell of Macandrevia cranium (Muller) reaches a. maximum length of tion of food, more or less surrounding the stomach and with ducts opening.to approx. 3(1 mm. The outline is oval, some of the largest specimens having a the stomach (Fig. 1). truncated anterior. The pedicle foramen is small, and the small deltidial plates ENDOPUNCTATE: The shell condition in which minute canals do not join medianly. The external surfaces are smooth, save for concentric (ENDOPUNCTAE, sing. ENDOPUNCTA) extend from the inner valve growth-lines. It is white, yellowish, or grey in colour. The shell is endopunctale. surface almost to the exterior. In life these endopunctae accommodate M. cranium has a long loop, dental plates, but no median septum. prolongations of outer mantle epithelium (CAECA) (Fig. 6C). Al. cranium has been found around the Shetlands, the Orkneys, the I lebrides, ENTERIC GANGLIA: The principal nerve centre of the brachiopod body, off north Scotland, in the Western Approaches, and off north-west and consisting of a ring of nerves with swollen regions (GANGLIA, sing. south-west Ireland. Elsewhere it has been collected off Greenland, Hance, GANGLION) surrounding the oesophagus. Nerves lead from this to various Spain and in the Mediterranean. It occurs at depths from 9 to I2(12 in. parts of the body (Fig. 1). c-w

60 HRH 1SII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 61

FOOD GROOVE: The canal along the inner side of the lophophore along PUSTULE: Small nodose protuberance forming part of the external ornamen- which food is transported to the postero-medianly positioned mouth (Fig. 111). tation of the shell. When larger they are called tubercules. "I IEART": Small, thin-walled contractile organs situated close to the stomach, RIBS: A form of external ornamentation in which the shell surface is radially thought to assist in the circulation of coelomic fluid. ridged. Very fine radial ridges are called striations (Fig. 5). HINGE AXIS: The line joining the points of articulation, the teeth, about which SHELL MOSAIC (see MOSAIC). the salves rotate when opening and closing (Fig. 9). SOCKETS: A pair of cavities, near the posterior margin of the dorsal valve, into IIINGE PLATES: A general term, including crural plates, for skeletal mine- which the teeth fit (Fig. 3). lures connected with the sockets and crura in the dorsal valve. SPICULES: Variably shaped calcareous plates within, and helping to support, 1M PI. INC-TAT E: Shell lacking either endopunctae or pseudopunctac. the mantle and lophophore epithelia in some species. INTESTINE: That part of the digestive system beyond the stomach ending at SOCKET RIDGES: Ridges of shell, extending antero-laterally from the the anus, in inarticulates, and blindly in the articulates (Fig. 1). cardinal process, bordering the inner side of the tooth sockets on.the dorsal LO1'I IO1'I IC)RE: Filamentous, commonly coiled, feeding organ symmetrically valve (Fig. 3). disposed about the mount and occupying the brachial cavity. Within it are TEETH (Hinge teeth): The two principal articulatory processes, situated on the coelomic cavities and, at the base of the filaments, the food groove leads to ventral valve at the anterio-lateral margins of the delthyrium (Fig. 4B, C). the postero-medianly positioned mouth (Fig. I). TUBERCLES: Large nodose protuberances on the shell surfaces (see LOOP or BRACHIAL LOOT': Delicate shelly loop-like support for the PUSTULES) (Fig. 5). lophophore extending anteriorly from the crura (Fig. 6A, B). UMBO:-Median, special posterior region of either valve (Fig. 5). MANTLE: Folds of ectodermal epithelium, extending forwards from the body VALVE: One of the two skeletal coverings of the brachiopod, together wall, which line the brachial cavity and secrete shell tissue (Fig. 1). constituting the shell. These are entirely calcareous in articulates and calcare- MANTLE CANALS: Canals in the mantle epithelium radiating from the body ous or chitinophosphatic in the inarticulates. cavity (Fig. 2). MEDIAN SEPTUM: A vertically disposed shell plate of variable height or length in the median plane of either valve, normally present in the body cavity Acknowledgements only (Fig. 613). ME-PANIgIRID1A: The principal excretory organs. Normally a single pair We particularly thank the Head of the Department of Palaeontology, British (but rhynchunelloids have two pairs) situated in the body and connected by Museum, for granting us access to the brachiopod collections and literature in short duets to openings in the body wall leading into the brachial cavity. 'IThey his care..In addition we acknowledge the assistance of the staff at the Scottish serve also as the openings through which eggs and sperm are ejected (fig. I ). Marine Biological Association's Laboratory, Dunstaffnage, particularly Drs A. MOSAIC: The pattern on the imtetmal surfaces of valves formed by the nen gins Ansel) and J. Gage; also Drs A. D. Rice and J. Wilson of the Institute of Of microscopic shell units in the secondary layer (Fig. 6C). Oceanographic Sciences, Wormley for access to their collections. The junior PEDICLE: Cuticle-covered stalk, commonly protruding from the ventral valve, author gratefully acknowledges a Department of Education (Northern Ireland) attaching the animal to the sea floor, and controlled by muscles (Fig. I). Postgraduate Research Studentship. PEDICLE APERTURE: The aperture, normally confined to the ventral valve, through which the pedicle extends. This aperture is within the delthyrium, but may be restricted in size by the growth of deltidial plates (Fig. 5). P1iDICI.I: ADJUSTOR MUSCLES: The muscles, commonly at least lour, attached to the base of the pedicle which control the movement of the shell around its attached pedicle. In some species these muscles assist in shell articulation (Fig. I). . PERIOS'IRACUM: The thin organic layer on the exterior of the shell. PROTEC;ULUM: The first-formed valves secreted by the juvenile brachiopod and commonly distinguished from later shell by the absence of ornamentation. I'SEUDOI'UNC"TATE: The shell condition of having PSEUDO- PUNCIAE (sing. PSEUDOI'UN1'A), which are conical flexures in the lamellose shell of many fossil brachiopods forming rod-like structures superfi- cially resembling cndopunctae.

62 RRIIISII BRACHIOPODS C. HOWARD, C. BRUNTON AND G. B. CURRY 6.

Literature List

AIKINS, D. 1959. The early growth stages and adult structure of the Iophophote of Macundrevia cranium (Muller), (Brachiopoda, Dallinidae). J. mar. biol. Ass. UK. 38, 335-350. •. AIKINS, D. 1959. The growth stages of the lophophore of the brachiopods !'haiditt daridson/ (Eudes Deslongchamp) and P. anontioides (Philippi), with notes on the feeding mechanism. J. mar. hiel. Ass. UK. 38, 103-132. AIKINS, D. 1960. A new species of Brachiopoda from the western approaches, and the growth stages of the lophophore. J. mar. biol. Ass. UK. 39, 71-89. AIKINS, D.1960. A note on [)a ling septigera (Lovén), (Brachiopoda, Dallinidae). J. mar. biol. Ass. UK. 39, 91-99. A'1 AINS, D. 1960. The ciliary feeding mechanism of the Megathyridae (Braehiopoda), and the growth stages of the lophophore. J. mar. biol. Ass. UK. 39, 459-479. A'ININS, D. 1961. The growth stages and adult structure of the lophophore of the brachiopods Met erlia truactuu (L.) and M. echinata (Fischer and Oehlert). J. mar. Lief. Ass. (1K. 41, 95-111. AtkINS, D. and RtowrcK, M. J. S. 1962. The lophophore and ciliary feeding mechanisms of the brachiopod Crania (no„adu (Muller). J. mar. biol. Ass. UK. 42, 469-4(01. Bto stoN, C. II. C. 1975. Some lines of Brachiopod research in the last decade. Paltton:. Zeit. 49(4), 512-529. Cut.sNt:, S. I I. 1960. An anatomical, histological, and histochemical study of the gut of the brachiopod Crania anontalu. Q. J! microsc. Sci. 101, 9-18. Ceti sn Es, 1. 1918. The Fauna oldie Clyde Sea Area. Glasgow University Press. Glasgow, 21111 pp. DAI I , W. II. 1920. Annotated list of the Recent Brachiopoda in the collection of the tIS National Museum, with descriptions of 33 new forms. Proc. USNM. 57, 261-377. 1)AsutsuN,'I. 1886-1888. A Monograph of Recent Brachiopoda. Trans. Linn. Sec. Sel. 2, 4, pts. I-III. • Eu`uo, C. C. 1979. British and (l/her l'horonids. Synopsis of the British Fauna No. 13, I.innc:nt Society, Estuarine and Brackish Water Sciences Association and Academic I',ess, istndhn. KIM., J. M. and Stupe, S. 1974. Marine Aquariums in the Research Laboratory. Aquarium Systems, Ohio. MASSt.s, A. I.. 1916. Mollusca and Brachiopoda of the Irish Atlantic slope. J. Conch., Lund. 15(2). Msssts, A. L. 1925. The brachiopods off the Coast of Ireland. Proc. R. Jr. Acad., Lublin 37(11), 37-4o. Mt('AStsu,N, I I. M. 1969. The loud of articulate brachiopods. J. Paleont. 43, 970-'185. Mt CAnrNON, II. M. 1972. Establishing and maintaining Articulate Brachiopods in :upu:u ia. J. geol. Elie. May 1972. 1211wt.1 I , A. 1. 1900. Shute early stages in the development of the brachiopod ( )retia anumula (NI tiller). Atm. Mug. nut. hist. (13), 3, 35-52. Runwu s, M. J. S. 1970. Living 11•issil Brachiopods. I lutchinson, !minion. 'I'novtsoN, J. A. 1927. Brachiopod Morphology and Genera. N.Z. Board of Sci. and Art Manual 7, 338 pp. Wu.t tAsts, A. et al. 1965. Treatise on Invertebrate Paleontology. (I I.), Brachiopoda. University of Kansas Press, Kansas. Ili/INA, D. N. 1976. Ecology and distribution of Recent Brachiopods (in Russi.m). Academy of Sciences of the USSR, Nauka, Moscow.