Immunocytochemical studies on the naupliar nervous system of Balanus improvisus (Crustacea, Cirripedia, Thecostraca)
Introduction
Recent studies using immunocytochemistry against nerve fibres and neurotransmitters in Crustacea proved to be an important source for phylogenetically relevant data (for review see Harzsch, 2006).
Until now, analyses on the anatomy and the development of arthropod nervous systems have been dominated by studies on insects, especially Drosophila melanogaster, but the data based on neurogenesis of Crustacea is steadily increasing (Whitington, 2004). There is a number of immunocytochemical investigations on the nervous system of adult Crustacea including cirripedes (Gallus et al., 1997, Webster, 1998, Callaway and Stuart, 1999), several malacostracans (e.g. Beltz and Kravitz, 1983, Sandeman et al., 1988, Breidbach et al., 1990, Thompson et al., 1994, Harrison et al., 1995, Schmidt and Ache, 1997, Utting et al., 2000, Harzsch and Waloszek, 2000, Moreau et al., 2002, Helluy and Thomas, 2003), and branchiopods (Zhang et al., 1997, Harzsch and Waloszek, 2000, Kirsch and Richter, 2007). In contrast to this, the few immunocytochemical studies on the development of the crustacean nervous system are heavily biased towards Decapoda and other malacostracans (e.g. Beltz et al., 1990, Sandeman and Sandeman, 1990, Beltz et al., 1992, Whitington et al., 1993, Helluy et al., 1993, Cournil et al., 1995, Harzsch and Dawirs, 1995, Harzsch and Dawirs, 1996, Schneider et al., 1996, Scholz et al., 1995, Harzsch et al., 1998, Harzsch et al., 1999, Mittmann and Scholtz, 2003, Vilpoux et al., 2006). So far the nervous systems of nauplius larvae has not been studied using immunocytochemical techniques, with the notable exception of Harzsch (2001) and Harzsch and Glötzner (2002) who examined some aspects in the larvae of Artemia salina and Triops cancriformis. This is astonishing, considering the major role the nauplius plays for our understanding of crustacean and arthropod relationships (e.g. Walossek, 1993, Dahms, 2000, Scholtz, 2000).
While the position of the Cirripedia as a member of the monophylum Thecostraca is widely accepted (Pérez-Losada et al., 2004), the placement of the Thecostraca within Crustacea is highly uncertain (see Walossek, 1993, Richter, 2002, Regier et al., 2005, Mallatt and Giribet, 2006). Many authors include the Thecostraca within a taxon Maxillopoda, but the monophyly of this group is doubtful (see Martin and Davis, 2001, Richter, 2002, Regier et al., 2005, Mallatt and Giribet, 2006).
Cirripedes have a life cycle comprising pelagic nauplii, retaining features known from the stem line Crustacea from the Cambrian (Walossek et al., 1996). The naupliar phase is followed by the cypris larva, which is highly specialized compared to the preceding instars and again by a metamorphic moult develops into the sessile adult (Høeg and Møller, 2006). Early cirripede embryology has featured prominently in discussions about arthropod relationships in general (Anderson, 1973, Nielsen, 2001, Scholtz, 2002). In addition to older accounts (Münter and Buchholz, 1869, Groom, 1894, Chun, 1896), Walley (1969) outlined the development of the nervous system in Semibalanus balanoides, while Kauri (1962) analysed the function and structure of the nauplius eye and frontal filaments of Semibalanus balanoides, Balanus improvisus and Balanus crenatus, and Walker (1974) studied the naupliar frontal filaments of Semibalanus balanoides, Chirona hameri, and Elminius modestus in great detail. Harrison and Sandeman (1999) described the nervous system of the cyprid of Balanus amphitrite by applying semithin and ultrathin sections. Hallberg and Elofsson (1983) investigated the compound eyes of cyprid larvae. The adult nervous system of Semibalanus cariosus was studied by Gwilliam and Cole (1979). Webster (1998) investigated the distribution and structure of peptidergic neurons in Balanus balanus, Balanus perforatus and Chirona hameri and observed neurons immunoreactive for pigment-dispersing hormone (PDH) and crustacean cardioactive peptide (CCAP). The distribution of histamine and serotonin in adults of Semibalanus cariosus and Balanus nubilus was investigated by Callaway and Stuart (1999).
Opposed to this, the microanatomical details of the central and peripheral nervous system in cirripede nauplii remain poorly studied (see Anderson, 1994), and immunocytochemical investigations are totally lacking, both for cirripede nauplii and for nauplii of the Maxillopoda in general. This is unfortunate, both because the nervous and sensory systems of the cirripede larva play a key role in determining the choice of the settlement site (Harrison and Sandeman, 1999, Lagersson and Høeg, 2002) and because larval neuroanatomy in general provides important phylogenetic information. We therefore initiated a study on the development of the nervous system in nauplii of the cirripede B. improvisus using immunofluorescence staining and confocal laser scanning microscopy (CLSM). For comparison we applied the same methods to nauplius larvae of the anostracan Artemia franciscana. We discuss our results with respect to the reduction of brain structures in adult barnacles and nervous system development of other crustaceans. Some potentially phylogenetic signals are evaluated.
Section snippets
Balanus improvisus
B. improvisus comprises six nauplius stages followed by the terminal cypris larva, which presents the ground pattern of cirripede larval development (Anderson, 1994). In the Baltic Sea this hermaphrodite spawns continuously from June until September, with distinct peaks in late July and late August/beginning of September (Blom and Nyholm, 1961). The development from 1st nauplius to the cypris larva in estuarine and brackish waters covers one week at 14 °C.
Adult barnacles were collected at the
Balanus improvisus
Cirripede nauplii differ from other crustacean nauplii by possessing a pair of frontolateral horns (see Høeg et al., 2004) and a pair of frontal filaments. The general morphology of nauplii of B. improvisus as exemplified by the 2nd naupliar stage is shown in Fig. 1. The characteristics of the perioesophageal nervous system are established by the second nauplius stage and do not change much during the first four naupliar stages. In later stages the changes concern mainly the formation of the
General neuroanatomy
The present study reveals a gross neuroanatomy in the nauplius larvae of Balanus improvisus that is consistent with what has been described for other crustacean embryos and larvae (e.g. Harzsch and Glötzner, 2002, Mittmann and Scholtz, 2003, Scholtz and Edgecombe, 2006). There is a circumoral nerve ring which we interpret as forming a classical tripartite brain. The protocerebrum contains a central part, comprising a median serotonergic neuropil structure which might be the anlage of a central
Acknowledgements
We are very grateful to Kent Berntsson (TMBL, Gothenburg) for access to barnacle research facilities and for skillfully keeping this system operating on a daily basis. The authors thank Michael Hansen, Alexander Schulz (Royal Veterinary and Agricultural University, Copenhagen) and Aase Frandsen (Danish University of Pharmaceutical Sciences, Copenhagen) for providing access and help with the CLSM. We are also indebted to Cornelis Grimmelikhuijzen (University of Copenhagen) for providing the
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