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Ecophysiology of Marine Invertebrate Planktonic Larvae: Species and Community Level Approach

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Ecophysiology of Marine Invertebrate Planktonic Larvae: Species and Community Level Approach PhD thesis Ecophysiology of marine invertebrate planktonic larvae: species and community level approach Ecosiologia de larves planctòniques d’invertebrats marins: aproximació a nivell d’espècies i comunitat Rodrigo Almeda García Barcelona - January 2011 Institut de Ciències del Mar (CSIC) Universitat de Barcelona Ecophysiology of marine invertebrate planktonic larvae: species and community level approach Ecofisiología de larvas planctónicas de invertebrados marinos: aproximación a nivel de especies y comunidad Ecofisiologia de larves planctòniques d'invertebrats marins: aproximació a nivell d'espècies i comunitat Rodrigo Almeda García Memòria presentada per Rodrigo Almeda García per optar al grau de Doctor per la Universitat de Barcelona. Tesi realitzada al Institut de Ciències del Mar e inscrita al Departament dEcologia, Facultat de Biologia, Universitat de Barcelona. Programa de doctorat de Ciències del Mar (Bienni 2003 ‐2005). Vist i plau Vist i plau Vist i plau del codirector del codirector de la tutora Rodrigo Almeda Dr. Miquel Alcaraz Dr. Albert Calbet Dra. Montserrat Vidal Doctorando Professor dinvestigació Investigador científic Professora titular ICM ‐CSIC ICM ‐CSIC ICM ‐CSIC UB Barcelona Gener 2011 A mi abuela Paula ... A la meva àvia Paula ... To my grandmother Paula ... Cover : Copepod larva (“nauplius”). Digital image of Wim van Egmond. Contents Contents 1 General introduction & thesis outline 5 Hypotheses & objectives 33 Results Chapter 1 Seasonal abundance and vertical distribution of zooplankton in NW Mediterranean 39 coastal waters: importance of small planktonic metazoans ( article I ) Chapter 2 Trophic role and carbon budget of metazoan microplankton in northwest Mediterranean 75 coastal waters ( article II ) Chapter 3 Feeding rates and abundance of marine invertebrate planktonic larvae under harmful algal 95 bloom conditions o Vancouver Island ( article III ) Chapter 4 Ecophysiology of early developmental stages of the cyclopoid copepod Oithona davisae 4.1. Eects of temperature and food concentration on survival, development and growth rates of naupliar stages of Oithona davisae (Copepoda, Cyclopoida) ( article IV ) 115 4.2. Feeding rates and gross growth eciencies of larval developmental stages of Oithona 133 davisae (Copepoda, Cyclopoida) ( article V ) 4.3. Metabolic rates and carbon budget of early developmental stages of the marine cyclopoid copepod Oithona davisae ( article VI ) 149 Chapter 5 Ecophysiology of planktonic larvae of the spionid polychaete Polydora ciliata 5.1. Swimming behavior and prey retention of the polychaete larvae Polydora ciliata 167 (Johnston) ( article VII ) 5.2. Feeding and growth kinetics of the planktotrophic larvae of the spionid 181 polychaete Polydora ciliata (Johnston) ( article VIII ) 5.3. Larval growth in the dominant polychaete Polydora ciliata is food-limited in a 193 eutrophic Danish estuary (Iseord) ( article IX ) General discussion 209 Main conclusions 221 Resum/ Resumen (Catalan & Spanish summaries) 225 Reference list 281 Report of the directors 297 Acknowledgements/ Agraïments/ Agradecimientos 305 Annex- Image gallery 309 1 General introduction & thesis outline “I am quite tired having worked all day at the produce of my net. e number of animals that the net collects is very great & fully explains the manner so many animals of a large size live so far from land. Many of these creatures so low in the scale of nature are most exquisite in their forms & rich in colours. It creates a feeling of wonder that so much beauty should be apparently created for such little purpose.” Johannes Müller’s trip diary, 11 th January 1845 Introduction & thesis outline General introduction Most marine invertebrates have a complex life history involving stages of planktonic larval development between the egg and the adult form (Thorson 1950; Strathmann 1987, 1993). These larvae may differ from adults in size, form, habitat, mode of nutrition, and/or ability to disperse (Barnes et al. 1988; Young 2002). The environmental conditions experienced during larval development can have profound effects on the subsequent performance of individuals and cohorts (Pechenik et al. 1998, 2002). Survival and growth of marine invertebrate larval stages can influence species recruitment success and population connectivity, distribution and abundance (Roughgarden et al. 1988; Eckert 2003). However, in spite of the obvious importance of larvae in the life cycles of most marine animals, the ecophysiology of larvae of many ecologically relevant invertebrates remains poorly understood in comparison to our knowledge of the adult phases. Additionally, as important components of zooplankton communities, the trophic role of planktonic larvae in marine food webs should not be neglected. Brief introduction to the history of invertebrate larval biology The first crustacean larvae were probably observed by Van Leeuwenhoek in 1699, who appreciated the important morphological diffe rences between the newly hatched forms and the adult stages of the copepod Cyclops (Gurney 1942). However, these larval forms were not initially recognized as such and were classified as the crustacean genus Nauplius by O.F. Müller (1776). Martinus Slabber (1778) was likely the first to correctly identify and illustrate several larvae of benthic invertebrates, but his observations were largely ignored (Fig.1). John Vaughan Thompson (1828, 1830) discovered that small planktonic organisms could be collected in fine mesh nets and he presented the first evidence of metamorphosis in larvae of crabs and barnacles from laboratory observations. After the discoveries of Thompson, the descriptions of larval anatomy and metamorphosis increased in the following decades (e.g. Milne-Edwards 1834-1840; 1842; Sars 1844; Nordman 1846). Many organisms that were previously described as genera (e.g. Nauplius -Müller 1776; Zoea-Bosc 1802; Megalopa -Leach 1815) or minuscule adults (e.g. veliger larvae) were then recognized as marine invertebrate larval stages (MacDonald 1858 ). Johannes Müller (1846, 1850), apparently unaware of Thompson’s findings, improved and 5 Introduction & thesis outline developed the use of net-tows for plankton sampling and discovered and illustrated a wide number of planktonic larval forms from the North Sea. In the following decades, compound microscopes and marine laboratory facilities improved rapidly, which facilitated the study of larval development of representatives of most marine phyla (e.g. Kowalevsky 1867, 1883; Agassiz 1877; Prouho 1892). The discovery of larval forms played a pivotal role in the studies of general evolution and phylogeny. For example, Darwin (1851) employed evidence from larval forms to fully accept that barnacles were crustaceans, and Ernst Haeckel’s biogenetic law (Haeckel 1866) was based largely on larval anatomy. In the early years of the 20 th century, notable contributions included detailed studies of larval morphogenesis and metamorphosis of a large number of species from temperate habitats (e.g. Grandori 1912; Mortensen 1921; Gurney 1930) and, descriptions of larval behavior (e.g. habitat selection by meroplanktonic larvae, Mortensen 1921; Wilson 1932,1948). The Danish marine biologist, Gunnar Thorson (1946, 1950, 1964) provided a detailed description of larval forms and distributions and a comprehensive categorization of larval developmental patterns. Thorson was the first to compile the previous studies on larval biology and put them into an environmental context; he is considered the pioneer of current discipline of larval ecology (Young 2002). Figure 1. Illustrationsll off planktonic l k llarvae bby Martinus Slabber (from Slabber 1778). Research on larval ecology, biochemistry and physiology has expanded rapidly in recent decades ( see reviews in McEdward 1995; Anger 2001; Hadfield & Paul 2001). Despite increased contributions to the knowledge of larval biology many areas in this field remain poorly understood. 6 Introduction & thesis outline The definition of 'larva'. Classification and diversity of marine invertebrate larvae Animal development that includes larval stages is termed ‘indirect development’; this is in contrast to ‘direct development’ where the embryo develops directly into a juvenile, which is typically a miniature, sexually immature version of the adult. Biologists have used the term 'larva' in a number of different ways and there is no generally accepted definition at this time (Strathmann 1987; McEdward & Jaines 1993; Young 2002). The definition that is used depends on whether the research focus is on morphology, evolutionary history, developmental progression, or ecological aspects (McEdward & Jaines 1993; Young et al. 2002). In this thesis, we have used the concept of larva described by Hickman (1999): 'the larva is a structural state or series of states that occurs between the onset of the divergent morphogenesis following embryonic development and the onset of metamorphosis to the adult body plan'. Marine invertebrate’s larvae show an impressive diversity of body forms (Fig. 2) and many larval body plans have been given specific names (Table 1). The external morphology and developmental sequences of larvae are not only relevant for the description of the ontogeny of individual species, but may reflect also evolutionary relationships between taxa (Haeckell 1866; Jägersten 1972; Bininda-Emonds et al. 2002). Marine larvae have been classified by site of development, nutritional mode, dispersal potential, and morphogenesis (Thorson 1950; Mieikovsky 1971; Levin & Bridges
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