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University of Southampton Research Repository Eprints Soton University of Southampton Research Repository ePrints Soton Copyright © and Moral Rights for this thesis are retained by the author and/or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder/s. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given e.g. AUTHOR (year of submission) "Full thesis title", University of Southampton, name of the University School or Department, PhD Thesis, pagination http://eprints.soton.ac.uk UNIVERSITY OF SOUTHAMPTON FACULTY OF ENGINEERING, SCIENCE AND MATHEMATICS School of Ocean and Earth Science Latitudinal gradients in marine invertebrate shell morphology: production costs and predation pressure By Sue-Ann Watson B.Sc. (Hons) M.Sc. Thesis for the degree of Doctor of Philosophy June 2009 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF SCIENCE SCHOOL OF OCEAN AND EARTH SCIENCE Doctor of Philosophy LATITUDINAL GRADIENTS IN MARINE INVERTEBRATE SHELL MORPHOLOGY: PRODUCTION COSTS AND PREDATION PRESSURE by Sue-Ann Watson Calcareous marine invertebrates are found in all the world’s oceans and extend across latitudes from equatorial to polar seas. Latitudinal gradients in shell morphology may be controlled by the additional cost of producing a shell or the lack of durophagous predators at high latitudes. Representatives from four megabenthic calcareous groups: bivalve and gastropod molluscs, brachiopods, and echinoid echinoderms; were studied across latitudes in both hemispheres. Shell morphology and elemental content, metabolic rate, growth, shell cost and predation pressure were analysed. Total inorganic content, a proxy for skeletal calcium carbonate, decreased with latitude in all four groups. Shell thickness decreased with latitude in buccinid gastropods and echinoids. No difference was found in shell thickness for brachiopods of the genus Liothyrella. Within the infaunal bivalve genus Laternula, the polar representative had the thickest shell. Shell Ca and minor elements, such as Mg, Sr and Na, were analysed using scanning electron microscope energy dispersive spectroscopy and wavelength dispersive spectroscopy (SEM EDS/WDS). For the taxa studied, Sr:Ca increased with latitude in bivalves and brachiopods, but decreased with latitude in gastropods. Mg:Ca decreased with latitude in molluscs, but there was no trend in brachiopods. Na:Ca increased with latitude in molluscs and brachiopods. The control of substitution of these elements may differ among taxa with latitude. Metabolic rate generally decreased with latitude as a function of temperature in all four taxa. Analysis of Q10 values provided no evidence of metabolic cold adaptation. Growth curves determined from shell increments showed polar gastropods and brachiopods were slow growing, but the polar bivalve Laternula elliptica had rapid absolute growth compared to tropical and temperate congeners. Growth curves were used in conjunction with metabolic data to estimate the cost of shell production as a percentage of the total energy budget for each species. This proportional cost of shell production was 3-4% in polar molluscs compared to 1.5-2% for temperate molluscs and 0.5-1% for tropical molluscs. Predation pressure, inferred by repaired shell damage and defence architecture decreased with increasing latitude in buccinid gastropods and brachiopods. Although defence morphology decreased with increasing latitude in Laternula bivalves, the polar species had more repairs than non-polar congeners. Since these clams are infaunal, shell repair frequency is argued to be a function of their abiotic environment, rather than controlled by predation. For all taxa, relationships of shell repairs with shell thickness suggest an evolutionary control on shell morphology, particularly shell thickness, for the protection of the occupant whether from biotic factors such as predation or abiotic factors such as ice scour. The evolutionary cost of shell failure is high and the ecological need for the shell as protection thus seems to provide a greater control over shell thickness and defence morphology than the energetic cost of producing a shell. However, despite the moderately low cost of shell production in tropical and temperate species, many calcareous forms are vulnerable to climate change, particularly ocean acidification. The additional energetic cost of producing a shell in acidified seawater may be too much to tolerate for larvae of the commercially important edible oyster Saccostrea glomerata, which exhibited a marked reduction in survival of 43-72%, reduced growth and retarded development under upper and lower seawater pH predictions for the year 2100. For polar calcareous marine invertebrates, their 1.33-8 times greater proportional shell cost and their adaptation to a low predation environment mean that these polar species are particularly at risk from ocean acidification and climate warming. List of contents Chapter 1: Introduction ...................................................................................................... 2 1.1 Rationale ...................................................................................................................... 2 1.2 Calcium carbonate shells and skeletons....................................................................... 2 1.3 Shell formation.............................................................................................................3 1.4 Patterns in shell morphology with latitude................................................................... 6 1.5 Competing hypotheses: shell cost versus shell function.............................................. 8 1.6 Aims and hypotheses ................................................................................................. 11 1.7 Structure of the thesis................................................................................................. 12 Chapter 2: Sample sites and study species....................................................................... 14 2.1 Introduction................................................................................................................ 14 2.2 Sample sites................................................................................................................ 14 2.3 Study species.............................................................................................................. 16 2.4 Collection of animals ................................................................................................. 20 2.5 Sample site-specific animal collection information................................................... 21 2.6 Data and statistical analyses....................................................................................... 32 2.7 Summary .................................................................................................................... 33 Chapter 3: Latitudinal trends in shell morphology ........................................................ 35 3.1 Introduction................................................................................................................ 35 3.1.1 Aims and hypothesis ........................................................................................... 36 3.2 Methods...................................................................................................................... 37 3.2.1 Sample collection................................................................................................ 37 3.2.2 Morphological data collection............................................................................. 37 3.2.3 Shell thickness measurements............................................................................. 39 3.2.4 Correcting for size differences among species.................................................... 43 3.2.5 Statistical analysis............................................................................................... 44 3.3 Results........................................................................................................................ 45 3.3.1 Whole animal morphology (shell and soft tissues)............................................. 45 3.3.2 Shell morphology................................................................................................ 57 3.4 Discussion .................................................................................................................. 82 Chapter 4: Shell chemistry - elemental content of calcium carbonate shells and skeletons .............................................................................................................................. 89 4.1 Introduction................................................................................................................ 89 4.1.1 Aims and hypotheses .......................................................................................... 92 iii 4.2 Methods...................................................................................................................... 93 4.2.1 Preparation of sample material...........................................................................
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