The Ecology and Behaviour of Ascidian Larvae
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FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1989 Taylor & Francis Group. This is an electronic published version of an article which may be cited as: Svane, I., & Young, C. M. (1989). The ecology and behaviour of ascidian larvae. Oceanography and Marine Biology: an Annual Review 27, 45-90. Oceanogr. Mar. BioI. Annu. Rev., 1989,27,45-90 Margaret Barnes, Ed. AberdeenUniversity Press • .. THE ECOLOGY AND BEHAVIOUR OF ~ ASCIDIAN LARVAE* I IB SVANE Kristineberg Marine Biological Station, Kristineberg 2130, S-450 34 Fiskebiickstil, Sweden and CRAIG M. YOUNGt Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, Florida 34946, USA ABSTRACT Recent studies of ascidian larval biology reveal a diversity of struc ture and behaviour not previously recognised. The introduction of direct methods for observing ascidian larvae in situ has provided important insights on larval behaviour, mortality, and dispersal not possible with the microscopic larvae Of most other marine invertebrates. In the context of these recent advances, this review considers the ecology of pelagic phases (egg, embryo, and larva) of the ascidian life cycle and relates aspects of reproduction and larval biology to the recruitment, abundance, and distribution of adult populations. INTRODUCTION The ascidian larva functions in site selection and dispersal while transporting adult rudiments between generations (Berrill, 1955, 1957; Millar, 1971; Cloney, 1987). Interest in the ecology of ascidian larvae has recently been stimulated by the introduction of new ideas and methods, most notably in situ observations of living larvae. The resulting advances justify a recon sideration of ascidian larval ecology. From an ecological standpoint, all pelagic phases of the ascidian life cycle (which may include eggs, embryos and larvae) influence adult populations. Thus, our definition oflarval ecology is broad; it includes reproductive processes leading to the production of gametes and larvae, as well as post-settlement consequences of larval pro . '!I' cesses. The literature on larval evolution as it relates to ascidian and chordate phylogeny is large, and will not be considered in the present paper. Reviews on ascidian biology dealing with aspects of reproduction and larval ecology have been published by Millar (1971), Berrill (1975), and Cloney (1987), and * Harbor Branch Contribution No. 678. t Order of authorship is alphabetical. 46 IB SVANE AND CRAIG M. YOUNG detailed reviews on ascidian metamorphosis have been presented by Cloney (1978, 1982). More recently, ascidian metamorphosis and larval locomotion have been treated as parts ofgeneral comprehensive reviews by Burke (1983) and Chia, Buckland-Nicks & Young (1984), respectively. It is our goal to bring together a scattered literature that comprises ascidian larval ecology. While emphasising ecological aspects of larval release, development, disper sal, behaviour, and settlement in relation to the distribution and abundance of adult populations, we also deal with reproductive, morphological, and developmental problems that help to elucidate aspects of ascidian larval ecology. REPRODUCTION, FERTILISATION, AND LARVAL ANATOMY MODES OF REPRODUCTION Ascidians may be either oviparous (typical of most solitary ascidians), ovo viviparous (typical ofmost compound ascidians), or viviparous (Fig I). True viviparity in which nutrients are exchanged between parent and embryo across a placenta-like structure is known to occur in only a single species, Hypsistozoafasmeriana (Brewin, 1959). Much ofthe earlier literature, includ ing the classic works ofBerrill (e.g. 1929, 1935, 1950) uses the term in reference to ovoviviparous species that retain embryos to hatching, but without appar ent transfer ofnutrients after ovulation. In oviparous forms, fertilisation and all subsequent developmental stages occur externally. Ascidian embryology and developmental biology have been the subjects of numerous important studies which have been reviewed by Cloney (1987) and Berrill (1975), and provided the theme for a recent symposium (Lambert, 1982). Conklin's (1905) study is still the classic description of cell lineage, although there has been a late resurgence ofcell lineage studies using modern fluorescent markers and immunological techniques (Whittaker, 1987). The most common developmental pattern (urodele development) terminates in the production of a swimming tadpole larva. Many mo1gulids and a few species in the family Styelidae (Pelonia corrugata and Polycarpa tinctor) undergo direct development, bypassing the larval stage completely (reviewed by Berrill, 1931; Millar, 1971; Young et aI., 1988). In ascidians, such direct development is known as anural development (Fig 2). As in many other kinds ofanimals, larval size is correlated with the degree of parental protection. Compound ascidians releasing fully developed larvae generally produce relatively few large larvae, whereas the eggs released by oviparous solitary ascidians are relatively more numerous and result in the production of much smaller, less differentiated tadpoles. In many invertebrates, there appears to be a correlation between adult size and brooding (Menge, 1975; Strathmann & Strathmann, 1982); within a given taxon, species with smaller individuals are more likely to brood than those with larger individuals. If we define an individual as a single zooid, not a colony, the relationship also seems to hold in ascidians. Accordingly, most colonial ascidians, having small zooids, brood relatively large complex larvae which develop from large eggs. Among solitary ascidians, brooders tend to THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN LARVAE 47 _---j~~SMALL. -SIMPLE /'C",NG "DPOll ~ EMBRYOGENESIS SETTLEMENT I SOLITARY \ f EXTERNAL OVIPAROUS FERTILIZATION \ URODELE ""AMO"'""'" ~A~m ) ~ . JUVENILE ~ADULT~ LARGE. _-----,~., SHORT COMPLEX - ~t'LANKTONIC TADPOLE PERIOD ~ / SEffiEMENT lARVAl. RELEASE ~ METAMORPHOSIS / COLONIAL \ IN1ERNAL OVOVIVIPAROUS ~= EM""\N"" URODELE \ 0JOlOOID ~ INTHiNAL SEASONAL t REGRESSION ~ FERTIUZA~ (Of ZOOIOS ) BU>.ST~D'NG ~ ADULT ~ ____ COLON~ Fig I.-Generalised life cycles of typical solitary ascidians (top) and com .. pound ascidians (bottom). The diagrams incorporate characteristics ofmany species; not all aspects (e.g., fusion of colonies) are present in the life cycle of any given species. • have small bodies and produce relatively large eggs and larvae, whereas oviparous species often have relatively larger bodies and produce small eggs. Exceptions to this pattern are found in Boltenia echinata (Berrill, 1948b; Svane, 1983) and Corella inflata (Child, 1927; Lambert, Lambert & Abbott, 1981), both of which brood small eggs and produce small, simple tadpole larvae. At least one solitary ascidian, Polycarpa pomaria, is observed in the 48 IB SVANE AND CRAIG M. YOUNG SECRETION --------. AD~SlVE ATTACHMENT ~GENESIS ( SOLITARY \ EXTERNAl OVIPAROUS HATCHING FERTlllZAlION \ ANURAL ) ~A~AOOH~~ Fig 2.~Generalised life cycle of a molgulid ascidian with anural develop ment. laboratory to brood facultatively. It is normally oviparous and produces small eggs, but developing larvae have not been found in the atrial cavity in nature (Berrill, 1950). One explanation for the relationship between brooding and zooid size is that cost of reproduction prohibits formation of numerous eggs in small individuals (Vance, 1973; Chia, 1974; Menge, 1976; Heath, 1977; Strathmann & Strathmann, 1982). This explanation, however, begs the question of why very large colonies of genetically identical zooids invest their resources for sexual reproduction in few large tadpoles rather than numerous small ones. Strathmann, Strathmann & Emson (1984) have suggested that self-fer tilisation can lead to brooding in echinoderms. The same argument could be applied to ascidians if we knew the extent of self-fertilisation. Botryllus schlosseri, which brood their embryos in the atrial cavity, can be either semelparous or iteroparous (R. Grosberg, pers. comm.). When fully developed larvae are removed surgically from the atrial cavities of a semel parous colony, the brood is replaced, suggesting that reproduction is not constrained by energy limitations. When a brood is replaced with inert glass beads, the colony dies shortly thereafter, just as in a typical semelparous colony (R. Grosberg, pers. comm.). Based on these findings, Grosberg has suggested that large broods prevent water flow through the atrium, killing the parent colony before a second brood is formed. FERTILISATION Sperm morphology and the physiology of ascidian fertilisation have been reviewed by Lambert (1982). Ascidian sperm are among the simplest in the THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN LARVAE 49 animal kingdom in that they lack a midpiece. The excentric mitochondrion lies next to the nucleus in the head region. Paradoxically, this simple sperm must penetrate a complex egg covering consisting of two layers of somatic cells and a chorion. Ascidian eggs have an effective block to polyspermy that appears to involve the egg membrane rather than the accessory cells or chorion (Lambert & Lambert, 1981). Moreover, many species demonstrate complete or partial blocks to self-fertilisation (Morgan, 1938, 1942). Sto lidobranchs tend to have a better block to self-fertility than phlebobranchs (Cloney, 1987). Many ascidiids and corellids are completely self-fertile. Sev eral species in the genus Ascidia demonstrate