A critical review of ontogenetic development in Terebellidae (Polychaeta

A Z O Journal Name

4

Manuscript No.

Acta Zoologica (Stockholm)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

3

4

B

Dispatch: 12.8.09

Journal: AZO CE: Anusha

Author Received:

No. of pages: 12 PE: Priya

doi: 10.1111/j.1463-6395.2009.00434.x

REVIEW

A critical review of ontogenetic development in Terebellidae (Polychaeta) Andre´ R. S. Garraffoni and Paulo C. Lana

Abstract Centro de Estudos do Mar, Universidade Federal do Parana´, Av. Beira Mar s ⁄ n, CP 50002, Pontal do Parana´, PR 83255-000, Brazil Keywords: morphology, Terebellida, Terebellomorpha, cephalic region, uncini Accepted for publication: 22 July 2009

Garraffoni, A.R.S. and Lana, P.C. 2009. A critical review of ontogenetic development in Terebellidae (Polychaeta). — Acta Zoologica (Stockholm) xx: 00–00 This study reviews the ontogenetic variability of the head, the first segments and the uncini in Terebellidae, based on primary literature and development series of four terebellid species. We test hypotheses on character homologies and indicate informative characters for future phylogenetic analyses. The prostomium, identified as the region above the prototroch band of the larva, in addition to being the region of origin of the buccal tentacles, contains a series of nerves originating from the cerebrum. The peristomium, which contains the mouth, is innervated by the stomogastric nerve and consists of upper and lower lips and an internal pharynx. The loss of the first notochaetae and neurochaetae in the course of development is a recurrent pattern in terebellids. The claviform chaetae disappear with age and growth, and can be used to define the larval stage. Chaetogenesis shows that the long shaft-shaped manubrium and posterior process develop from different regions. The uncini terminology ‘double rows’ was reinterpreted and renamed ‘inverted rows’, which better reflects the inversion of chaetal positions during ontogenetic development. Andre´ R. S. Garraffoni, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Departamento de Cieˆncias Biolo´gicas, Campus II, Rodovia BR-367, Diamantina, MG 39.100-000, Brazil. E-mail: [email protected]

Introduction Ontogenetic development can be understood as a continuous process, by which an organism undergoes gradual alterations, from the fertilization of the egg and embryogenesis to the adult or reproductive age (Qian 1999). In general, this is very evident in marine animals, which present successive metamorphoses (Strathmann 1993). In spite of the apparent ease of observation of morphological variability, there are still wide gaps in the knowledge of the ontogeny of many polychaete groups. One example is the family Terebellidae, with more than 550 valid species grouped in 72 different genera, which occurs worldwide from shallow waters to deep oceans (Hutchings 2000; Rouse 2001; Garraffoni et al. 2006; Garraffoni and Lana 2008), and whose reproductive biology and ontogeny remain little studied. Most ontogenetic studies of Terebellidae have concentrated mainly on structural transformations of a few characters in a few species. More inclusive attempts to find common patterns of variation in different species are scarce (Wilson 1928;

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

Heimler 1981; Bhaud and Gre´mare 1988; Blake 1991). The studies of McHugh (1993) and Bhaud (2000) on the life cycle and the biology of larvae and juveniles of several species of Terebellidae are exceptions. The lack of consistent information about the ontogenetic development makes it difficult to even understand basic questions, such as the segmental homologies of the prostomium and peristomium, and leads to a confused terminology. Day (1967) mentioned that ‘since the prostomium is not distinct in adult Terebellids there has been considerable doubt as to the segmental homologies of anterior structures’. In turn, Rouse (2001) stated that ‘The nature of the head in Terebellidae, especially with reference to the peristomium, has yet to be fully resolved’. More recently, Zhadan and Tzetlin (2002) suggested that the prostomium in Terebellidae and Trichobranchidae is reduced and fused with the peristomium, but that it is very difficult to define the limit between these structures in the adults. The present study reviews the development of the prostomium, the peristomium and related structures, as well as the

1

1 Review of ontogenetic development

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

•

Garraffoni and Lana

loss of the first notochaetae and neurochaetae in particular reference to ontogenetic development of Terebellidae. Additional contributions are made in the investigation of chaetogenesis, and segmental arrangement of uncini. The study utilizes and reinterprets information from the pertinent literature, in addition to original data generated from observations of the development of larvae and juveniles of four species of Terebellidae: Lanice conchilega, Loimia sp., Nicolea venustula, and N. uspiana. The studied material was collected at different locations and periods. Samples of Lanice conchilega were taken with plankton nets in the North Sea (Wilhelmshaven, Germany, 53º30¢N–08º08¢E, from 06 ⁄ 20 ⁄ 2004 to 06 ⁄ 30 ⁄ 2003) and in the German Bight (Helgoland, Germany, 54º10¢N–75º04¢E, from 08 ⁄ 11 ⁄ 2004 to 08 ⁄ 14 ⁄ ⁄ 2004. Loimia sp. was sampled with plankton nets in Paranagua´ Bay (Parana´, Brazil, 25º34¢S–48º20¢W) and Sa˜o Sebastia˜o Channel (Sa˜o Paulo, Brazil, 23º47¢S–45º22¢W). Nicolea venustula was sampled by SCUBA diving (8 m depth) at the German Bight (Helgoland, Germany, 54º10¢N–75º04¢E) and N. uspiana from rocky shores in Mel Island (Parana´, Brazil, 25º33¢S–48º18¢W) and rocky shore of Porchat Island, on Itarare´ Beach (Sa˜o Vicente, Brazil, 23º57¢S–46º23¢W). The larvae were sorted and examined alive under stereo and light microscopes. Samples were fixed in 7% seawater formalin and preserved in 70% ethanol. For SEM observations, specimens were dehydrated via graded ethanol series, critical point dried using CO2, coated wit Au-Pd and examined in a CamScan CS 24 SEM. The fixed specimens were dehydrated in ascending ethanol concentrations and after 1 h in a 1 : 1 mixture of ethanol and HistoResin (Zeis), infiltrated with full strength resin overnight and then embedded. Sections were cut on a microtome (3 lm) and stained with toluidine blue. Current Contradictions in the Delineation of the Prostomium, Peristomium and Associated Structures Beginning with Goodrich (1897), different authors have proposed quite distinct interpretations of the origin and definition of the peristomium, prostomium and associated structures. These discordances were surely caused by the limitation of the analyses to the morphology of adult worms. Thus, the upper lip, which is flap-shaped and possesses muscle fibers that allow a variety of movements, has been considered either as prostomial (Dales 1955; Hilbig 2000; Orrhage 2001) or peristomial (Sutton 1957; Holthe 1986; Fauchald and Rouse 1997). In the former case, the peristomium is considered as composed only by the lower lip. In the latter case, both the upper and lower lips would be peristomial. A third hypothesis was suggested by Rouse (2001), that the upper lip is composed of parts derived both from the prostomium and peristomium. In an attempt to establish a single, consistent proposal regarding the origins of the prostomium, peristomium and associated structures in terebellids, we present a new interpretation based on larval and adult observations. The hypothesis

2

Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

proposed here takes into account the obvious fact that all polychaetes pass part of their lives as larvae, whether planktonic (as planktotrophic or lecithotrophic) or benthic (with the entire development within the capsule), and part as adults (Giangrande et al. 1994; Bhaud et al. 1995). This reinterpretation utilizes the definitions proposed by Schroeder and Hermans (1975), the analyses of Heimler (1981), the anatomy of the central nervous system of Pista cristata studied by Orrhage (2001), and the comparative studies of the buccal apparatus by Dales (1955) and Zhadan and Tzetlin (2002), as well as primary data generated by us. In addition, the ciliary band of the prototroch present in the larvae of terebellids was also utilized to aid in delimiting the prostomal and peristomal regions in the initial stages of development. This ciliary band is very common in other families of Polychaeta, and is a very conservative and easily recognized structure (Anderson 1959, 1966; Rouse 1999, 2000a,b,c). The correct understanding of the origin of the buccal tentacles and the peristomial structures is of primary importance for the formulation of the hypothesis of robust homologies that facilitates the clarification of phylogenetic relationships within and in groups close to the Terebellidae (Bhaud 1988a). Position of the ‘brain’ and buccal tentacles In polychaetes the head is composed of the prostomium and peristomium, and the region between the prostomium ⁄ peristomium and the pygidium is considered segmented or metamerically organized due to the fact that each segment is a repetition of homologous body structures derived by teloblas2 tic growth (Rouse and Fauchald 1995; Rouse and Fauchald 1997). Furthermore, this metamerization is reflected in the rope–ladder neural system. This system is composed by paired segmental ganglia connected intersegmentally by connectives and intrasegmentally by commissures (Orrhage and Mu¨ller 2005; Mu¨ller 2006). The brain is located at the beginning of the circum-esophageal connection, distant from the connection of the latter nerve with the transverse ventral commissure where the pairs of ganglia are located (Orrhage and Mu¨ller 2005; Mu¨ller 2006). The typical terebellid brain (Fig. 1) is positioned in the posterior region of the prostomium, a small intumescence or dorsal crest dorsally fused with the upper lip, also called distal part, which bears the eyespots and cerebrum (Wilson 1928; Day 1967; Fauchald and Rouse 1997). For us, the brain and its respective innervations and connections for the buccal tentacles and the dorsal ridge are definitely not positioned on the first segment. This point of view is shared by Orrhage (2001, p. 64, fig. 6) who observed that the nerves of the dorsal ridge of the terebellids are rooted in the brain, whereas the four anteriormost paired nerves derive from the ventral cord. In the four species analyzed in this study (Figs 1 and 2) and in the many examples in the literature (Wilson 1928; p. 141, fig. 7; Thorson 1946, p. 130; fig. 74A,B,C,D,E; Eckelbarger 3 1974, p. 108, fig. 5D,E,F,G,H,I; Heimler 1983, p. 417, figs 2

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

1 Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

Fig. 1—Histological section of a juvenile of Nicolea uspiana showing the anterior region. pa, prostomium anterior surface; b, brain; bo, buccal organ; br, branchiae; bt, buccal tentacles; ll, lower lip; pa, prostomium anterior surface; pp, prostomium posterior surface; ul, upper lip; vnc, ventral nerve cord; 1s, segment 1; 2s, segment 2; 3s, segment 3; 4s, segment 4; 5s, segment 5; vnc, ventral nerve cord. Scale: 400 lm.

and 3; Bhaud and Gre´mare 1988, p. 349; figs 1,2,3 and 4; Blake 1991, p. 454; fig. 4A,B), the prostomial origin of the tentacles is evident (Fig. 3); there is no possibility that they are located on the dividing line between the prostomium and peristomium (Fauchald and Rouse 1997), or are situated externally to the upper lip (Rousset et al. 2003), or are peristomial (Hutchings and Glasby 1988) or change their position during the ontogenesis. Our interpretation of the prostomial origin of the tentacles is mainly based on the definition of prostomimum ⁄ peristomium provided by Anderson (1959, 1966) and Schroeder and Hermans (1975). For them the distinct ciliated band in the immediately preoral region of a larva corresponds to a prototroch. Thus, the peristomium is the region containing the mouth, originating in front of the anteriormost segment and including the prototroch (and the metatroch, when present). The prostomium is the anteriormost region to the prototroch. In the early development stages of different terebellid species (Fig. 3: Eupolymnia nebulosa, A–C; Ramex californiensis, D–F; and Lanice conchilega G–I) a slightly anterior prolongation denotes the anlage of the prostomium (Fig. 3A,D,G). With growth, the embryos begin to elongate both anteriorly and posteriorly, the cilia apparatus becomes reduced and the prostomium elongation continues until rudimentary tentacles appears (Fig. 3B,C,E,F,H). Furthermore, in the detailed illustrations by Orrhage (2001, p. 66, fig. 7) and Orrhage and Mu¨ller (2005, p. 81, fig. 2) the nerves of buccal and stomogastric tentacles of Pectinariidae and Ampharetidae are clearly connected to each other and to the common trait which runs to the cerebrum. In Terebellidae the nerves of the buccal tentacles are rooted directly in the brain and not connected with the stomogastric nerve, which runs to the common trait, and its anterior and

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

Garraffoni and Lana

•

Review of ontogenetic development

posterior nerves, to finally root in the brain. Thus, the innervation of the buccal tentacles of Terebellidae is rather distinct from that of the Ampharetidae and Pectinariidae. Unfortunately, there is no information on the innervations of alvinellid tentacles in the literature. In fact, Zhadan and Tzetlin (2002) correctly pointed out that the buccal tentacles of the terebellids are not connected with the ciliated pharynx. This evidence stands against the hypothesis presented by Holthe (1986), Orrhage (2001) and Orrhage and Mu¨ller (2005), who considered that the buccal tentacles are homologous in these four families, and also considered them a part of the alimentary canal. In addition, there are no neuro-anatomical indications of the presence of palps or antennae in Terebellidae, Ampharetidae and Pectinariidade (Orrhage 2001; Orrhage and Mu¨ller 2005), contrary to the interpretation of Rouse and Fauchald (1997). Thus, we reinterpret the multiple, grooved buccal tentacles as non-homologous to the palps from other polychaetes. Two distinct hypotheses about their origins have to be taken into account in the case of Ampharetidae, Pectinariidae and Terebellidae. Their origin is clearly prostomial in Terebellidae, including Trichobranchinae, and peristomial in Ampharetidae, Pectinariidae and Alvinellidae (Garraffoni and Lana 2008). So, it seems unequivocal that the multiple grooved buccal tentacles condition evolved twice in the evolutionary history of Terebellida. Blake (1991) stated that the growth patterns of the buccal tentacles are similar in all Terebellidae. A middle buccal tentacle appears at the beginning of larval development, and later, more tentacles are added to the left and right of this middle tentacle. The new tentacles always appear as small intumescences located on the sides of the middle tentacle. We agree with Blake’s interpretation, since this pattern was observed by us in Loimia sp. and Nicolea uspiana and by Bhaud and Gre´mare (1988) in Eupolymnia nebulosa. Peristomial lips The peristomial lips have received little attention in most systematic studies. We agree with Sutton (1957) and Zhadan and Tzetlin (2002) and reject Dales’s (1955) interpretation with respect to the composition of the peristomial region of terebellids. The peristomium consists of upper and lower lips and a buccal organ (also called the ventral bulb or ventral pharynx); the only visible adult peristomial structure is the area immediately surrounding the mouth or upper lip (Fauchald and Rouse 1997). The dorsal surface of the upper lip, a hood-like structure (Figs 1, 2 and 3), is covered by a non-ciliated epithelium. Its ventral surface is ciliated (Sutton 1957). Dales (1955) made a detailed study of the internal anatomy of the lower lip, dividing it into two regions with five areas in total, as a function of the muscle insertions (Figs 4A,C and 5A,C): outer lip (2 areas) and inner lip (3 areas). The outer lip is formed by the areas termed ‘a’ and ‘b’, and the inner lip by the areas termed ‘c’, ‘d’ and ‘e’ (in some species, area ‘e’ is not present). Dales (1955) probably used the definition of

3

1 Review of ontogenetic development

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

•

Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

Garraffoni and Lana

and Tzetlin (2002) did not differentiate these, considering them as two distinct parts of the same structure, respectively, the upper lip and the free expansion of the upper lip (Fig. 6A,C,E). In addition, the first segment was also represented in the scheme (Fig. 6B,D,F), the better to differentiate this structure from the other prostomial and peristomial structures in the anterior region. First segments

Fig. 2—Anterior region of a juvenile of Nicolea uspiana, in lateral view

(modified from Garraffoni and Amaral 2009). br, branchiae; bt, buccal tentacles; p, prostomium; ul, upper lip; 1s, segment 1; 2s, segment 2; 3s, segment 3; 4s, segment 4; 5s, segment 5. Scale: 150 lm.

Goodrich (1897) and interpreted the first segment as being part of the outer region of the lower lip, always designating it as region ‘a’. However, the peristomium is herein treated as a pre-segmentary structure, and as such it must be distinguished from the first segment (see discussion above). Therefore, the five areas proposed by Dales (1955) need to be repositioned, as they are not restricted to the lower lip (Figs 4B,D and 5B,D). In most cases, the lower lip, composed of areas ‘a’ and ‘b’, will be covered by the first segment located ventrally in the species of Terebellidae. In this way, the upper and lower lips are considered distinct and independent of the first segment, also called the buccal segment or peristomial segment in different studies (Fauvel 1927; Dales 1955; Hutchings and Glasby 1988). Some examples of the new hypotheses of homologies are the reinterpretations of area ‘a’ in Polycirrus aurantiacus or areas ‘a’ and ‘e’ in Amphitrite johnstoni (Fig. 4A,B,C,D), as well as areas ‘a’, ‘b’, ‘c’, ‘d’ and ‘e’ in Lanice conchilega and areas ‘a’ and ‘e’ in Terebellides stroemii (Fig. 5A,B,C,D). In accord with the present reinterpretation, each muscle group with its respective folds is considered to be homologous in each of the four species analyzed by Dales (1955). Besides the reinterpretation of the study of Dales (1955), it is possible also to reevaluate the hypotheses proposed by Zhadan and Tzetlin (2002) for the anterior region (Fig. 6), with which we disagree concerning the positions of the upper lip and the prostomium. Zhadan

4

The terebellids show a consistent pattern of loss of the first notochaetae (sometime the second as well) and neurochaetae in the course of ontogenetic development. The claviform notopodial chaetae typical of the larval stage are present only in the first development stages, and are later replaced by capillary chaetae. This replacement can be used to delimit the transition from larvae to juveniles (Bhaud 1988a,b; Bhaud and Gre´mare 1988). Concomitantly with the loss of the notochaetae, the neurochaetae on the first segments are also lost (Fig. 7). Thus, it is possible to observe three distinct patterns of loss of the notochaetae and neurochaetae during development: 1 – Loimia medusa, Loimia sp., Nicolea zostericola, N. uspiana, Lanice conchilega, Eupolymnia crescentis: loss of the notochaetae and neurochaetae on two anterior segments: the first notochaetae are present on the second segment in the larva and on the fourth segment in the adult, and the first neurochaetae are present on the third segment in the larva and the fifth segment in the adult (Wilson 1928; Eckelbarger 1974; McHugh 1993; Garraffoni and Amaral 2009; present data); 2 – Ramex californiensis: loss of the notochaetae on two anterior segments and loss of the neurochaetae on one anterior segment: the first notopodium is present on the second segment in the larva and the fourth segment in the adult, and the first neuropodium is present on the fourth segment in the larva and the fifth segment in the adult (Blake 1991); 3 – Eupolymnia nebulosa: loss of the notochaetae on one anterior segment and loss of the neurochaetae on one anterior segment: the first notopodium is present on the third segment in the larva and the fourth segment in the adult, and the first neuropodium is present on the fourth segment in the larva and the fifth segment in the adult (Bhaud and Gre´mare 1988). Bhaud (1988a) suggested that the loss of claviform chaetae may be restricted only to the subfamily Terebellinae. However, although all the species that the early development is know belongs to the subfamily Terebellinae, a similar situation is observed in species of the ampharetids, such as subfamily Ampharetinae (Alkmaria romijni – Cazaux 1982; Amphictei floridus – Zottoli 1974) and subfamily Melinninae (Melinna palmata – Grehan et al. 1991). Thus, the loss of some of the notopodia located on the first segments during development due to the reduction of the claviform chaetae may constitute a possible evolutionary novelty present in the ancestral line of the Terebellomorpha (sensu Rouse 2001), and not only in some species of Terebellidae. The understanding of the patterns of loss of the notochaetae and neurochaetae is of primary importance for the

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

LOW RESOLUTION FIG

1 Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

Garraffoni and Lana

A

B

C

D

E

F

G

H

I

•

Review of ontogenetic development

7 Fig. 3—Early development of trochophore and larva in Eupolymnia nebulosa (A–C; modified from Bhaud and Gre´mare 1988), embryo and

trochophore in Ramex californiensis (D–F; modified from Blake 1991), and trochophore, larva and juvenile in Lanice conchilega (G–I; simplified and modified from Heimler 1983) b, brain; bo, buccal organ; bt, buccal tentacles; es, eyespot; ll, lower lip; mo, mouth; ne, neurotroch; p, prostomium; pe, peristomium; pro, prototroch; vnc, ventral nerve cord; 1s, segment 1; 2s, segment 2. Scales A. 90 lm; B. 135 lm; C. 230 lm; D–F. 100 lm.

taxonomy of the group, to the extent that these characters are used to differentiate genera. Thus, juveniles and adults of the same species, if collected separately, may be identified as different species, just because they do not possess the first notopodia and the first neuropodia on the same segments. Presence of Aulophore Larva in the Terebellidae There are terebellid species with indirect development, with short-lived lecithotropic or long-lived planktonic larvae, and species with direct development, which incubate the eggs in gelatinous masses inside or outside the tube (Bhaud 1988a,b).

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

Although planktonic development is widely spread in polychaetes (Wilson 1991; Giangrande 1997), only Lanice and Loimia have an aulophore larva among terebellids (Marcano and Bhaud 1995). To Garraffoni and Lana (2008) this pattern is a synapomorphy shared by Lanice and Loimia, contrary to the interpretation that this larva is common to all the terebellids (Strathmann 1993). Bhaud (1986) and Marcano and Bhaud (1995) recognized two dispersal stages for the aulophore larvae. In the first stage, the larvae remain for a short period of time in the water column after the fertilization, soon returning to the sediment. On returning to the sediment, the larvae produce a tube formed

5

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

LOW RESOLUTION FIG

1 Review of ontogenetic development

•

Garraffoni and Lana

A

B

C

D

Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

8 Fig. 4—Comparison of the lip structure in

two terebellids. —A, C. show Dales (1955) interpretations. —B, D. show the interpretation proposed herein. —A–B. Polycirrus aurantiacus. —C–D. Amphitrite johnstoni (modified from Dales 1955). a-e: distinct areas from the lower lip; 1s: segment 1. Scale 1 mm.

by a mucus secretion plus sediment particles. Later, the larva with the mucus tube returns to the water column and continues its development. Nevertheless, we are not sure whether this first larval stage actually exists, because we were not able to observe Loimia and Lanice without the mucus tube, even in four- or five-segmented individuals. However, we also assume that widespread species can present different development modes in different regions of the world, and that we could have studied species that do not have the first larval stage as recognized by Bhaud (1986) and Marcano and Bhaud (1995). Definitions and Characterization of the Uncini Long-shafted manubrium and posterior process in uncini Uncini in species of Trichobranchinae and in some species of Terebellinae have typically a long-shafted manubrium (Fig. 8C) and a posterior process (Fig. 8B). There is not a literature consensus on the real meaning of these two structures.

6

Holthe (1986) recognized and named manubrioavicular and opisthavicular uncini on the basis of the relative development of the manubrium and the posterior process (Holthe 1986, p. 33, fig. 7A,L). Manubrioavicular uncini have a long, more or less straight manubrium crowned with a toothed or smooth capitium behind the rostrum, whereas opisthavicular uncini have a manubrial plate with a more or less developed posterior shaft, with a toothed capitium behind the rostrum. This clear separation between different parts of the uncini was not emphasized by later authors. Hutchings and Glasby (1988) reported that specimens of the genus Lanicides have long-shafted uncini (Hutchings and Glasby 1988, p. 23; fig. 8G), specimens of genus Pista have some thoracic segments with long-handled uncini (Hutchings and Glasby 1988: 38; table 1), and specimens of the genus Longicarpus have anterior thoracic uncini with well-chitinised shafts (Hutchings and Glasby 1988, p. 32). All these uncini could 4 be referred to the opisthaviscular shape. Hutchings (2000 p. 230, 5 fig. 3E) and Garraffoni and Lana (2003, p. 361, fig. 4)

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

LOW RESOLUTION FIG

1 Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

Garraffoni and Lana

A

B

C

D

•

Review of ontogenetic development

9 Fig. 5—Comparison of the lip structure in

two terebellids. —A, C. show Dales (1955) interpretations. —B, D. show the interpretation proposed herein. —A–B. Lanice conchilega. —C–D. Terebellides stroemii (modified from Dales 1955). a–e: distinct areas from the lower lip; 1s: segment 1. Scale 1 mm.

reported that trichobranchins have avicular uncini with long shafts, which could be referred to of Holthe’s manubrioavicular shape. To detect whether or not there is a homology between the long-shafted manubrium and the posterior process, we reinterpreted their development based on studies of Nicolea zostericola and Capitella capitata (Bartolomaeus 1998; Hausen 2005). On observing the chaetogenesis of the neurochaetae in the two species, it is possible to note two different growth zones. The first zone is represented by a group of longitudinal microvilli all along the base of the chaeta, and the second by a zone of microvilli restricted to the posterior part of the chaeta. The development of the microvilli from the former growth zone gives rise to the manubrium (Fig. 8A). The manubrium in Polycirrinae, Thelepodinae and Terebellinae (as in the case of Nicolea zostericola) is short (Fig. 8A), but elongated in trichobranchins, forming a kind of shaft (Fig. 8C). It is tempting to speculate that the hypotheses of development of the first growth zone in tricobranchins follows a process very similar to that observed in Capitella capitata (Fig. 8D), since this last species also has a long manubrium in the form of a shaft and

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

is phylogenetically close Terebellidae (Bartolomaeus 1998; Almeida et al. 2003; but see Rouse and Fauchald 1997). The posterior process of uncini in Pista, Longicarpus, Eupistella and Pseudopista is formed by the development of a second microvilli zone restricted to the base of the manubrium (opposite to the main tooth) on the posterior part of the chaeta (Fig. 8B). In this manner, the evidence obtained from analysis of the development of the chaetae complements the information generated by the morphometric studies in respect to the lack of homology between the long shaft manubrium present in Trichobranchinae, and the posterior process present in some species of Terebellinae (Garraffoni and Camargo 2006, 2007). Bartolomaeus (1998) and Bartolomaeus et al. (2005, p. 351, fig. 4) carried out phylogenetic analyses of groups of polychaetes with hooks. They stated that the uncini with a short manubrium (or a reduction in the length of the manubrium) is an apomorphy shared by the different taxa that compose the clade Uncinifera (Terebellida, Sabellida and Pogonophora). Thus, the reappearance of the long-shafted manubrium in Trichobranchinae is a clear case of reversion,

7

•

Garraffoni and Lana

A

B

C

D

E

F

Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

10 Fig. 6—Present interpretation of the anterior

LOW RESOLUTION FIG

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

LOW RESOLUTION FIG

1 Review of ontogenetic development

region in three terebellids (A–B Terebellinae, Thelepodinae, C–D Artacama, E–F Polycirrinae). —A, C, E. show Zhadan and Tzetlin (2002) interpretation. —B, D, F. show the interpretation proposed in the present study. (modified from Zhadan and Tzetlin 2002). b, brain; ll, lower lip; oe, oesophagus; p, prostomium; ul, upper lip; vpho, ventral pharyngeal organ; 1S, segment 1.

11 Fig. 7—Modifications in the first 8 segments

during the ontogenetic development from larva to adult, based on observations derived from our data and from Bhaud (1988a,b), Bhaud and Gre´mare (1988), Wilson (1928), Blake (1991), McHugh (1993), Heimler (1981), Eckelbarger (1974). A, adult; L, larva; P, prostomium. Numbers represent the segments.

since this same character was already present at the base of the clade Uncinifera, e.g. in Spionida, Arenicolidae and Maldanidae. This reversion observed in the formation of the long shaft manubrium is an additional strong argument to reinforce the idea of its apomorphic condition, thus supporting the hypothesis of the monophyly of the Trichobranchinae (Garraffoni and Lana 2004, 2008). However, we feel that a

8

more extensive study regarding the terebellids chaetogenesis are required. Uncini in inverted rows The presence of uncini in double rows was hypothesized as a possible synapomorphy of the Terebellinae (McHugh 1995;

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

LOW RESOLUTION FIG

1 Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

Garraffoni and Lana

•

Review of ontogenetic development

A

B

C

D 12 Fig. 8—Hypothesis about the possible origin of the anterior process in Terebellinae and the long shaft uncini in Trichobranchinae. —A. Chaetog-

enis in Nicola zostericola, Terebellinae (modified from Hausen 2005), —B. Uncini with posterior process in Lanicides lacuna, Terebellinae (modified from Hutchings and Glasby 1988), —C. Uncini with long shaft manubrium in Terebellides sepultura, Trichobranchinae (modified from Garraffoni and Lana 2003), —D. Chaetogenesis of Capitela capitata, Capitellidae (modified from Bartolomaeus 1998). cb: chaetoblastum, m: manubrium, pp: posterior process. Scales unknown.

Rousset et al. 2003) or even of the Terebellidae (Glasby et al. 2004). However, all these studies were based on observations made in adults and did not consider the first ontogenetic stages. McHugh (1995) codified this antagonistic uncini arrangement as ‘‘double row of uncini’’ (front to front or back to back) on the body segments. However, this uncini arrangement is only evident in juveniles or adults, as there is only one row of chaetae in the first larval stages (Wilson 1928; Eckelbarger 1974; Bhaud and Gre´mare 1988; Bhaud 1988a; Blake 1991; Garraffoni and Amaral 2009; present data). Bhaud and Gre´mare (1988) pointed out that specimens of Eupolymina nebulosa have only one row of uncini until the larva is about 45 days old. This change in the uncinal pattern with age and growth also occurs in all Terebellinae species (Bhaud 1988a; Blake 1991; Garraffoni and Amaral 2009; Present data). Thus, the evolutionary novelty present in terebellin species is not the presence

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

of a double row of uncini in the adult, but the inversion of some chaetae originally arranged in a single row, originating from the chaetoblasts located in the upper part of the segment (Bhaud 1988a; Bhaud and Gre´mare 1988; Hausen 2005). This inversion occurs gradually, beginning with older segments located in the anterior region (Fig. 9A,B,C), and extending to more posterior regions with newer segments (Wilson 1928; Bhaud 1988a; Bhaud and Gre´mare 1988). Therefore, it is more appropriate to use the term ‘‘uncini in inverted rows’’ as opposed to the older term ‘‘double row of uncini.’’ The new term has the great advantage of taking into consideration occurrences in all the life stages of an individual, not only the final pattern observed in the adults. The change in the uncini arrangement during development may produce two very different morphological patterns in the adult. In the first pattern, the inversion effectively forms two rows of uncini positioned front-to-front or back-to-back (e.g.

9

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

LOW RESOLUTION FIG

1 Review of ontogenetic development

•

Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

Garraffoni and Lana

A

of feeding apparatus and anatomy of the central nervous system. This study provides new data and has led to new conclusions to shed light on a number of issues, that have been considerable dubious for a long time. A critical review of the hypotheses and the use of many morphological and embryological data have led us to consider that several traditional views about the homology of the structures may be not correct, while some questions remain unresolved.

B

Acknowledgements

C

This research was supported by a grant provided to the first author by the Brazilian funding agencies CAPES – Coordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superior-, FAPESP – Fundac¸a˜o de Amparo a Pesquisa do Estado de Sa˜o Paulo – (05-59809-7), and the DAAD from Germany. We are much indebted to Cinthya Santos, Walter Boeger, Gabriel Mello, Cecı´lia Amaral, Joa˜o Nogueira, Anete Lourenc¸o and an anonymous referee for advice and comments to different versions of this manuscript. Pedro Martı´nez provided working facilities to the first author at the Senckenberg Institute (Wilhelmshaven, Germany) and Klaus Anger at the Biologische Anstalt Helgoland (Helgoland, Germany) where part of the material used in the present study was examined. Janet Reid edited the manuscript in English.

13 Fig. 9—Change in the uncinal pattern showing the inverted rows in

the juvenile. —A. Nicolea zostericola. —B. N. uspiana. —C. Loimia sp. Vertical arrows represent the direction of the main fang of the uncini and numbers correspond to the segments.

Nogueira et al. 2003, p. 765; fig. 2L,M). In the second pattern, the inversion of the uncini does not form a second row strictly speaking, but only alternately inverts the position of the uncini (which appear to be arranged in a single row), always arranged front-to-front (e.g. London˜o-Mesa 2003, p. 749, fig. 1F). The general shape of the uncini changes in species of Loimia during development (Wilson 1928; Hutchings and Glasby 1988). The few larval uncini have an avicular shape (a hook with four or five rows of innumerable small secondary teeth over a single principal tooth), as in all the other genera of the family (Holthe 1986; Hutchings 2000; Garraffoni and Lana 2008). However, in the transition from juveniles to adults, the uncini assume the pectinate shape (a single vertical row with three to five secondary teeth on the tooth), totally different from the avicular shape. This modification of the shape of the hook is one of the synapomorphies that support the monophyly of the genus Loimia (Garraffoni and Lana 2008). In conclusion, the complex questions raised by the composition of the head region in terebellids, especially the homologies of the appendages and first segments, the loss of the noto- and neurochaetae and the uncini morphology have been readdressed by the present work with a review of the literature concerning studies about larval ontogeny, morphology

10

References Almeida, W. O., Christoffersen, M. L., Amorim, D. S., Garraffoni, A. R. S. and Silva, G. S. 2003. Polychaeta, Annelida, and Articulata are not monophyletic: articulating the Metameria (Metazoa, Coelomata). – Revista Brasileira de Zoologia 20: 23–57. Anderson, D. T. 1959. The embryology of the polychaete Scoloplos armiger. – Quarterly Journal of Microscopical Science 100: 89–166. Anderson, D. T. 1966. The comparative embryology of the Polychaeta. – Acta Zoologica 47: 1–42. Bartolomaeus, T. 1998. Chaetogenesis in polychaetous Annelida – Significance for annelid systematic and the position of the Pogonophora. – Zoomorphology 100: 348–368. Bartolomaeus, T., Purschke, G. and Hausen, H. 2005. Polychaeta phylogeny based on morphological data – a comparison of current attempts. – Hydrobiologia 535 ⁄ 536: 341–356. Bhaud, M. 1986. Preliminary data on the meroplanktonic larvae of Polychaeta in the Noumea lagoon, south-western New Caledonia. – Journal of Coastal Research 2: 297–309. Bhaud, M. 1988a. Change in setal pattern during early development of Eupolymnia nebolusa (Polychaeta: Terebellidae) grown in simulated natural conditions. – Journal of Marine Biological Association of United Kingdom 68: 677–687. Bhaud, M. 1988b. The two planktonic larval periods of Lanice conchilega (Pallas, 1766) Annelida Polychaeta, a peculiar example of the irreversibility of evolution. – Ophelia 29: 141–152. Bhaud, M. 2000. Some examples of the contribution of planktonic larval stages to the biology and ecology of Polychaeta. – Bulletin of Marine Science 67: 345–358. Bhaud, M. and Gre´mare, A. 1988. Larval development of the terebellid polychaete Eupolymnia nebulosa (Montagu) in the Mediterranean Sea. – Zoologica Scripta 17: 347–356.

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

1 Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

Bhaud, M., Jae-Hoon, C., Ducheˆne, J. C., Martin, D. and Nozais, C. 1995. Larval biology and benthic recruitment: New ideas on the role of egg-masses and modeling life-cycle regulation. – Scientia Marina 59: 103–107. Blake, J. A. 1991. Larval development of Polychaeta from the Northern California coast V. Ramex californiensis Hartman (Polychaeta: Terebellidae). – Bulletin of Marine Science 48: 448–460. Cazaux, C. 1982. De´ve`lopement larvaire de l’Ampharetidae lagunaire Alkmaria romijini Horst 1919. – Cahiers de Biologie Marine 23: 143– 157. Dales, R. P. 1955. Feeding and digestion in terebellid polychaetes. – Journal of Marine Biological Association of United Kingdom 24: 55–79. Day, J. H. 1967. A monograph on the Polychaeta of Southern Africa. Part. 2 Sedentaria. British Museum of Natural History, Trustees of the British Museum (Natural History), London. Desbruye`res, D. and Laubier, L. 1991. Systematics, phylogeny, ecology and distribution of the Alvinellidae (Polychaeta) from deep-sea 6 hydrothermal vents. – Ophelia supplement 5: 31–45. Eckelbarger, K. J. 1974. Population biology and larval development of the terebellid polychaete Nicolea zostericola. – Marine Biology 27: 101–113. Fauchald, K. and Rouse, G. W. 1997. Polychaete systematics: Past and present. – Zoologica Scripta 26: 71–138. Fauvel, P. 1927. Faune de France vol. 16. Polyche`tes se´dentaires. Addenda aux Errantes, Archianne´lides, Myzostomaires. Librairie de la Faculte´ des Sciences Paul Lechevalier, Paris. Garraffoni, A. R. S. and Amaral, A. C. Z. 2009. Postlarval development of Nicolea uspiana (Polychaeta: Terebellidae). – Revista Brasileira de Zoologia 26: 61–66. Garraffoni, A. R. S. and Camargo, M. G. 2006. First application of morphometrics in a study of the variation in uncinial shape present within the Terebellidae (Polychaeta). – Zoological Studies 45: 75–80. Garraffoni, A. R. S. and Camargo, M. G. 2007. A new application of morphometrics in a study of the variation in uncinal shape present within the Terebellidae (Polychaeta): a reevaluation from digital images. – Cahiers de Biologie Marine 48: 229–240. Garraffoni, A. R. S. and Lana, P. C. 2004. Cladistic analysis of the subfamily Trichobranchinae (Polychaeta, Terebellidae). – Journal of Marine Biological Association of United Kingdom 84: 973–982. Garraffoni, A. R. S. and Lana, P. C. 2008. Phylogenetic relationships within Terebellidae (Polychaeta: Terebelomorpha) based on morphological characters. – Invertebrate Systematics 22: 605– 626. Garraffoni, A. R. S., Nihei, S. S. and Lana, P. C. 2006. Distribution patterns of Terebellidae (Annelida: Polychaeta): an application of Parsimony Analysis of Endemicity (PAE). – Scientia Marina 70S3269–276. Giangrande, A. 1997. Polychaete reproductive patterns, life cycles and life histories: an overview. – Oceanography and Marine Biology Annual Review 35: 323–386. Giangrande, A., Geraci, S. and Belmonte, G. 1994. Life-cycle and life-history diversity in marine invertebrates and the implication in community dynamics. – Oceanography and Marine Biology Annual Review 32: 305–333. Glasby, C. J., Hutchings, P. A. and Hall, K. 2004. Assessment of monophily and taxon affinities within the polychaete clade Terebelliformia (Terebellidae). – Journal of Marine Biological Association of United Kingdom 84: 961–971. Goodrich, E. S. 1897. On the relation of the arthropod head to the annelid prostomium. – Quarterly Journal of Microscopy Science 40: 439–457.

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

Garraffoni and Lana

•

Review of ontogenetic development

Grehan, A., Retie`re, C. and Keegan, B. 1991. Larval development in the ampharetid Mellina palmata Grube (Polychaeta). – Ophelia 5: 321–332. Hausen, H. 2005. Chaetae and chaetogenesis in polychaetes (Annelida). – Hydrobiologia 535 ⁄ 536: 37–52. Heimler, W. 1981. Untersuchungen zur Larvalentwicklung von Lanice conchilega (Pallas) 1766 (Polychaeta, Terebellomorpha). Teil II: Bau und Ultrastruktur der Trochophora-Larve. – Zoologische Jahrbu¨cher (Anatomie und Ontogenie der Tiere) 106: 236–277. Hilbig, B. 2000. Family Terebellidae. In Blake, J. A., Hilbig, B. and Scott, P. V. (Eds): Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel, pp. 231–293. Santa Barbara Museum of Natural History, Santa Barbara. Holthe, T. 1986. Evoluton, systematics, and distribution of the Polychaeta Terebellomorpha, with a catalogue of the taxa and bibliography. – Gunneria 55: 1–236. Hutchings, P. 2000. Family Terebellidae. In Beesley, P. L., Ross, G. L. B. and Glasby, C. J. (Eds): Polychaeta and Allies: The Southern Synthesis. Fauna of Australia. Vol. 4a Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula, pp. 232–235. CSIRO, Melbourne. Hutchings, P. A. and Glasby, C. J. 1988. The Amphitritinae (Polychaeta: Terebellidae) from Australia. – Records of Australian Museum 40: 1–60. London˜o-Mesa, M. H. 2003. Revision of Spinosphaera and establishment of the genus Hutchingsiella (Polychaeta: Terebellidae: Terebellinae). – Journal of Marine Association of United Kingdom 83: 747– 759. Marcano, G. and Bhaud, M. 1995. New observations on the terebellid (Polychaeta) aulophore larvae on the French coast. – Ophelia 43: 229–244. McHugh, D. 1993. A comparative study of reproduction and development in the polychaete family Terebellidae. – Biological Bulletin 185: 153–167. McHugh, D. 1995. Phylogenetic analysis of the Amphitritinae (Polychaeta: Terebellidae). – Zoological Journal of Linnean Society 11: 405–429. Mu¨ller, M. C. M. 2006. Polychaete nervous systems: Ground pattern and variations – CLS microscopy and the importance of novel characteristics in phylogenetic analysis. – Integrative and Comparative Biology 46: 125–133. Nogueira, J. M. M., Hutchings, P. A. and Amaral, A. C. Z. 2003. Articulatia, a new genus of Terebellinae (Polychaeta: Terebellidae) living in Brazilian corals. – Journal of Marine Association of United Kingdom 83: 761–770. Orrhage, L. 2001. On the anatomy of the central nervous system and the morphological value of the anterior end appendages of Ampharetidae, Pectinariidae and Terebellidae. – Acta Zoologica 82: 57–71. Orrhage, L. and Mu¨ller, M. C. M. 2005. Morphology of the nervous system of Polychaeta (Annelida). – Hydrobiologia 535 ⁄ 536: 79–111. Qian, P. Y. 1999. Larval settlement of polychaetes. – Hydrobiologia 402: 230–253. Rouse, G. W. 1999. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. – Biological Journal Linnean Society 66: 411–464. Rouse, G. W. 2000a. Bias? What bias? The evolution of downstream larval-feeding in animals. – Zoologica Scripta 29: 213–236. Rouse, G. W. 2000b. Polychaeta have evolved feeding larvae numerous times. – Bulletin of Marine Science 67: 391–409. Rouse, G. W. 2000c. The epitome of hand waving? Larval feeding and hypotheses of metazoan phylogeny. – Evolutionary Development 2: 222–233. Rouse, G. W. 2001. Family Terebellidae. In Rouse, G. W. and Pleijel, F. (Eds): Polychaetes, pp. 246–250. Oxford, London.

11

1 Review of ontogenetic development

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

•

Garraffoni and Lana

Rouse, G. W. and Fauchald, K. 1997. Cladistics and polychaetes. – Zoologica Scripta 26: 269–301. Rousset, V., Rouse, G. W., Feral, J. P., Desbruye`res, D. and Pleijel, F. 2003. Molecular and morphological evidence of Alvinellidae relationships (Terebelliformia, Polychaeta, Annelida). – Zoologica Scripta 32: 185–197. Schroeder, P. C. and Hermans, C. O. 1975. Annellida: Polychaeta. In Giese, A. C. and Pearse, J. R. (Eds): Reproduction of Marine Invertebrate, pp 1–123. Academic Press, Nova York. Strathmann, R. R. 1993. Hypotheses on the origins of marine larvae. – Annual Review in Ecology and Systematic 24: 89–117. Sutton, M. F. 1957. The feeding mechanism, functional morphology and histology of the alimentary canal of Terebella lapidaria L. (Polychaeta). – Proceedings of Zoological Society of London 29: 487– 523.

12

Acta Zoologica (Stockholm) xx: 00–00 (August 2009)

Thorson, G. 1946. Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the Sound (Oresund). – Meddelelser fra Kommissionen forDanmarks Fiskeri- Og Havundersøgelser, Serie: Plankton 4: 1–523. Wilson, D. P. 1928. Post-larval development of Loimia medusa Sav. – Journal of Marine Biological Association of United Kingdom 15: 129– 149. Wilson, W. H. 1991. Sexual reproductive modes in polychaetes: classification and diversity. – Bulletin of Marine Science 48: 500–516. Zhadan, A. E. and Tzetlin, B. 2002. Comparative morphology of the feeding apparatus in the Terebellida (Annelida: Polychaeta). – Cahiers de Biologie Marine 43: 149–164. Zottoli, R. A. 1974. Reproduction and larval development of the ampharetid polychaete Amphicteis floridus. – Transactions of the American Microscopical Society 93: 78–89.

 2009 The Authors Journal compilation  2009 The Royal Swedish Academy of Sciences

Author Query Form Journal:

AZO

Article:

434

Dear Author, During the copy-editing of your paper, the following queries arose. Please respond to these by marking up your proofs with the necessary changes/additions. Please write your answers on the query sheet if there is insufficient space on the page proofs. Please write clearly and follow the conventions shown on the attached corrections sheet. If returning the proof by fax do not write too close to the paper’s edge. Please remember that illegible mark-ups may delay publication. Many thanks for your assistance.

Query reference

Query

Q1

AUTHOR: A running head short title was not supplied; please check if this one is suitable and, if not, please supply a short title of up to 40 characters that can be used instead.

Q2

AUTHOR: Rouse and Fauchald 1995 has not been included in the Reference List, please supply full publication details.

Q3

AUTHOR: Heimler 1983 has not been included in the Reference List, please supply full publication details.

Q4

AUTHOR: Hutchings and Peart (2000) has been changed to Hutchings (2000) so that this citation matches the Reference List. Please confirm that this is correct.

Q5

AUTHOR: Garraffoni and Lana (2003 has not been included in the Reference List, please supply full publication details.

Q6

AUTHOR: Desbruye`res and Laubier (1991) has not been cited in the text. Please indicate where it should be cited; or delete from the Reference List.

Q7

AUTHOR: Figure 3 has been saved at a low resolution of 433 dpi. Please resupply at 600 dpi. Check required artwork specifications at http://www.blackwellpublishing.com/authors/digill.asp

Q8

AUTHOR: Figure 4 has been saved at a low resolution of 303 dpi. Please resupply at 600 dpi. Check required artwork specifications at http://www.blackwellpublishing.com/authors/digill.asp

Q9

AUTHOR: Figure 5 has been saved at a low resolution of 289 dpi. Please resupply at 600 dpi. Check required artwork specifications at http://www.blackwellpublishing.com/authors/digill.asp

Q10

AUTHOR: Figure 6 has been saved at a low resolution of 229 dpi. Please resupply at 600 dpi. Check required artwork specifications at http://www.blackwellpublishing.com/authors/digill.asp

Q11

AUTHOR: Figure 7 has been saved at a low resolution of 214 dpi. Please resupply at 600 dpi. Check required artwork specifications at http://www.blackwellpublishing.com/authors/digill.asp

Remarks

Q12

AUTHOR: Figure 8 has been saved at a low resolution of 77 dpi. Please resupply at 600 dpi. Check required artwork specifications at http:// www.blackwellpublishing.com/authors/digill.asp

Q13

AUTHOR: Figure 9 has been saved at a low resolution of 137 dpi. Please resupply at 600 dpi. Check required artwork specifications at http://www.blackwellpublishing.com/authors/digill.asp

MARKED PROOF Please correct and return this set Please use the proof correction marks shown below for all alterations and corrections. If you wish to return your proof by fax you should ensure that all amendments are written clearly in dark ink and are made well within the page margins. Instruction to printer Leave unchanged Insert in text the matter indicated in the margin Delete

Textual mark under matter to remain

New matter followed by or through single character, rule or underline or through all characters to be deleted

Substitute character or substitute part of one or more word(s) Change to italics Change to capitals Change to small capitals Change to bold type Change to bold italic Change to lower case Change italic to upright type

under matter to be changed under matter to be changed under matter to be changed under matter to be changed under matter to be changed Encircle matter to be changed (As above)

Change bold to non-bold type

(As above)

Insert ‘superior’ character

Marginal mark

through letter or through characters

through character or where required

or new character or new characters

or under character e.g.

Insert ‘inferior’ character

(As above)

Insert full stop Insert comma

(As above)

Insert single quotation marks

(As above)

Insert double quotation marks

(As above)

over character e.g.

(As above) or

or

(As above)

Transpose Close up Insert or substitute space between characters or words Reduce space between characters or words

linking

and/or

or

or

Insert hyphen Start new paragraph No new paragraph

or

characters

through character or where required

between characters or words affected

and/or