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The Biological and Ecological Drivers of Shell Growth in Bivalves

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The Biological and Ecological Drivers of Shell Growth in Bivalves UNIVERSITY OF SPLIT, UNIVERSITY DEPARTMENT OF MARINE STUDIES UNIVERSITY OF DUBROVNIK INSTITUTE OF OCEANOGRAPHY AND FISHERIES, SPLIT Postgraduate study of Applied Marine Sciences Ariadna Purroy Albet THE BIOLOGICAL AND ECOLOGICAL DRIVERS OF SHELL GROWTH IN BIVALVES Doctoral thesis Split, March 2017 This doctoral thesis was performed at the Institute of Oceanography and Fisheries, in the Laboratory of Fisheries Science and Management of Pelagic and Demersal Resources under the guidance of Prof. Melita Peharda Uljević Ph.D., in the framework of the inter-university postgraduate studies of Applied Marine Sciences at the University of Split and University of Dubrovnik. This research has been carried out in the framework of the ARAMACC Project “Annually Resolved Archives of Marine Climate Change” (FP7-PEOPLE-2013-ITN) under an ESR Marie Curie Fellowship. I “It is a curious situation that the sea, from which life first arose, should now be threatened by the activities of one form of that life. But the sea, though changed in a sinister way, will continue to exist; the threat is rather to life itself.” Rachel Carson II TABLE OF CONTENTS BASIC DOCUMENTATION CARD VII TEMELJNA DOKUMENTACIJSKA KARTICA VIII 1. GENERAL INTRODUCTION 1 1.1. Rationale and objectives …………………………………………………………………………………. 2 2. LITERATURE REVIEW 4 2.1. Species of study ……..………………………………………………………………………………………. 4 2.1.1. Callista chione 4 2.1.2. Glycymeris bimaculata 4 2.1.3. Glycymeris pilosa 4 2.2. Feeding ecology ……………………………………………………………………………………………… 5 2.2.1. Stable isotope analysis 6 2.2.1.1. Stable isotope analysis in food sources 7 2.2.1.2. Stable isotope analysis in consumers 7 2.2.2. Fatty acid analysis 8 2.2.2.1. Fatty acid in food sources 9 2.2.2.2. Fatty acid in consumers 11 2.3. Reproduction …………………………………………………………………………………………………. 12 2.3.1. Reproduction in Callista chione 13 2.3.2. Reproduction in Glycymeris sp. 15 2.4. Shell growth ……………………………………………………………………………………………………. 16 2.4.1. Shell growth in Callista chione 19 2.4.2. Shell growth in Glycymeris sp. 20 3. MATERIAL & METHODS 23 3.1. Study area ………………………………………………………………………………………………………. 23 3.2. Environmental variables …………………………………………………………………………………. 24 3.2.1. Temperature, salinity and precipitation 24 3.2.2. Characterization of water column and sediment 24 3.3. Feeding ecology ……………………………………………………………………………………………… 25 3.3.1. Isotopic analysis 25 III 3.3.2. Fatty acid analysis 26 3.4. Reproduction ………………………………………………………………………………………………….. 27 3.4.1. Qualitative: Histological analysis of gonad tissue 27 3.4.2. Quantitative: Gonadosomatic Index 29 3.5. Growth …………………………………………………………………………………………………………… 30 3.5.1. Micromilling on the shell surface of Callista chione 30 3.5.2. Micromilling in the cross-sectioned valve of Glycymeris bimaculata 32 3.6. Statistical analysis ………………………………………………………………………………………… 34 3.6.1. Environmental variables 34 3.6.2. Feeding ecology 34 3.6.2.1. Environmental variables 34 3.6.2.2. Stable isotopes 35 3.6.2.3. Fatty acids 35 3.6.3. Reproduction 35 3.6.4. Growth 36 4. RESULTS 37 4.1. Environmental variability ……………………………………………………………………………….. 37 4.2. Feeding ecology ……………………………………………………………………………………………… 38 4.2.1. Trophic ecology of Callista chione and Glycymeris bimaculata from two populations: Pag and Cetina 38 4.2.1.1. Food sources: Environmental variables as food quality indicators 38 4.2.1.2. Consumers: Glycymeris bimaculata and Callista chione 43 4.2.2. Trophic ecology of Glycymeris pilosa from two populations: Pag and Pašman 50 4.2.2.1. Food sources: Environmental variables as food quality indicators 50 4.2.2.2. Consumer: Glycymeris pilosa 54 4.3. Reproduction ………………………………………………………………………………………………….. 56 4.3.1. Reproductive cycle of Callista chione at two study sites 56 4.3.1.1. Histological analysis 56 4.3.1.2. Gonadosomatic index 60 4.3.1.3. Reproductive investment, output and fecundity 63 4.3.1.4. Comparative analysis of methods 64 IV 4.3.2. Reproductive cycle of Glycymeris bimaculata at two study sites 65 4.3.2.1. Histological analysis 65 4.3.2.2. Gonadosomatic index at Pag 70 4.3.2.3. Reproductive investment, output and fecundity 71 4.3.2.4. Comparative analysis of methods 72 4.3.3. Reproductive cycle of Glycymeris pilosa from Pašman 73 4.3.3.1. Histological analysis 73 4.4. Growth …………………………………………………………………………………………………………… 76 4.4.1. Micromilling on the shell surface of Callista chione 77 4.4.1.1. Correlating growth with environmental and biological variables 82 4.4.2. Micromilling in the cross-sectioned valve of Glycymeris bimaculata 85 5. DISCUSSION 91 5.1. Feeding …………………………………………………………………………………………………………… 91 5.1.1. Characterization of food sources 91 5.1.1.1. Identifying the origin of organic matter through stable isotope analysis 91 5.1.1.2. Biogenic parameters as indicators of particulate matter quality 93 5.1.1.3. Identifying the composition of OM through fatty acid analysis 94 5.1.2. Spatial and temporal variation in bivalve diet: Callista chione and Glycymeris bimaculata study 97 5.1.3. Contribution of food sources to bivalve diet and feeding niche: Callista chione and Glycymeris bimaculata study 99 5.1.4. Spatial and temporal variation in bivalve diet: Glycymeris pilosa study 102 5.2. Reproduction ………………………………………………………………………………………………… 103 5.2.1. Reproductive cycle and temperature 103 5.2.2. Body mass index 107 5.2.3. Reproductive investment, output and fecundity 108 5.2.4. Future scenario/ implications 109 5.3. Growth …………………………………………………………………………………………………………. 110 5.3.1. Use of δ18O and δ13C as proxies 110 5.3.2. Growth patterns: timing and rate of shell growth 111 5.3.2.1. Growth patterns in Callista chione 111 V 5.3.2.2. Growth patterns in Glycymeris bimaculata 113 5.3.3. Environmental and physiological controls of shell microincrement growth 114 5.3.4. Potential for paleoclimate reconstructions 118 5.3.5. Future research 119 6. CONCLUSION 121 7. LITERATURE 123 8. ANNEX 161 9. PROŠIRENI SAŽETAK 183 10. BIOGRAPHY 197 ACKNOWLEDGEMENTS 199 ABSTRACT IN CATALAN VI BASIC DOCUMENTATION CARD University of Split and University of Dubrovnik Ph.D. thesis Ph.D. in Applied Marine Sciences THE BIOLOGICAL AND ECOLOGICAL DRIVERS OF SHELL GROWTH IN BIVALVES Ariadna Purroy Albet Thesis was performed at the Institute of Oceanography and Fisheries, Split Abstract Bivalve mollusks incorporate life-history traits in their shells during growth making them valuable archives of environmental, biological and evolutionary information. This thesis provides insights into the biological and environmental drivers of shell growth in Callista chione, Glycymeris bimaculata and Glycymeris pilosa. The study was performed in the middle-eastern Adriatic Sea (Pag Bay, Cetina river mouth and Pašman Channel) from May 2014 until October 2015. A characterization of the feeding ecology of these species within their habitat analyzed several biochemical parameters including stable isotope and fatty acid composition. The reproductive behavior was studied applying two complementary approaches, histology and gonadosomatic index. Lastly, stable isotope analyses of carbonate samples were linked to high-resolution temperature records to describe shell microgrowth patterns. Spring and summer were identified as the periods with the best food quality in the particulate matter. Food resource partitioning was observed between C. chione and G. bimaculata at each site and the nitrogen isotopic composition of bivalve tissues was influenced by the presence of diazotroph biomass which differentiated among sites. Inter-site variations in the spawning timing and duration of C. chione were likely associated with temperature whereas in Glycymeris sp. spawning was not directly connected. Such small-scale biological responses are essential to address climate oscillation influences. Shell accretion took place between May and December pointing (i) temperature as an important determinant of shell growth (ii) food availability setting the limits for the growth season and (iii) the onset of gametogenesis close to the growth line formation, evidencing higher energy requirements for reproduction. These results contribute to knowledge on bivalve ecology in the Adriatic Sea and outlined the importance of coupling sclerochronology to ecological studies for a better understanding of species life-history traits. (202 pages, 52 figures, 18 tables, 414 references, original in English) Thesis deposited in National and University Library in Zagreb, Split University Library, and Library of Institute of Oceanography and Fisheries in Split Keywords: bivalves, feeding ecology, fatty acids, stable isotopes, histology, gonadosomatic index, shell growth, sclerochemistry, sclerochronology, Adriatic Sea Supervisor: Prof Melita Peharda Uljević Ph.D. / Senior Research Scientist Reviewers: 1. Prof Nedo Vrgoč Ph.D. / Full professor 2. Ivana Bočina Ph.D. / Associate professor 3. Ivan Župan Ph.D. / Assistant professor Thesis accepted: March 3rd 2017 VII TEMELJNA DOKUMENTACIJSKA KARTICA Sveučilište u Splitu i Sveučilište u Dubrovniku Doktorska disertacija BIOLOŠKI I EKOLOŠKI ČIMBENICI KOJI UTJEČU NA RAST LJUŠTURA ŠKOLJKAŠA Ariadna Purroy Albet Rad je izrađen u Institutu za oceanografiju i ribarstvo u Splitu Sažetak Školjkaši u svoje ljušture ugrađuju osobine životnog ciklusa, što ih čini vrijednim arhivima okolišnih, bioloških i evolucijskih podataka. Ovaj rad pruža uvid u biološke i ekološke čimbenike koji utječu na rast vrsta Callista chione, Glycymeris bimaculata i Glycymeris pilosa. Istraživanje je provedeno u istočnom dijelu srednjeg Jadrana (Paška uvala, ušće rijeke
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