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Morphology of cyprid attachment organs compared across disparate barnacle taxa: Does it relate to habitat?

Abstract. This study used morphometric analyses to compare the structure of the third antennular segment, also called the attachment organ, in cyprid larvae from cirripede species representing a diverse set of taxonomic groups. The aim was to investigate the degree of morphological variation in view of the diversity of habitats, settlement substrata, and modes of life found in the Cirripedia. In all cyprids the third segment features a flat surface (the attachment disc) covered with small cuticular villi thought to function in adhesion. The parameters analyzed were the angle of this disc relative to the long axis of the antennule, its shape (outline), the density of cuticular villi, and the type of cuticular structure encircling the disc. The 10 species studied came from most major groups of cirripedes, and comprised shallow-water forms inhabiting hard bottoms (Capitulum mitella, Pollicipes pollicipes, Semihalanus balanoides, Austrominius modestus, Megabalanus rosa), sublittoral forms (Verruca stroemia, Scalpellum scalpellum), epibiotic forms settling on live, soft tissues (Balanus spongicola, Savignium crenatum), and a parasite (Peltogaster paguri). Significant structural variation was found among the species, but due to limited taxon sampling it was unclear whether the differences relate to ecological factors or phylogenetic affiliation. The disc perimeter is guarded by either a series of long and thin cuticular fringes overreaching the rim of the disc (= a velum) or a few low, but very broad cuticular flaps (= a skirt). The presence of a velum (in all rocky-shore species) or a skirt (all other species) around the attachment disc was the only parameter that was clearly correlated with habitat. The shape of the third antennular segment varied from a symmetrical bell shape with a distally facing attachment disc having a circular disc outline, to segments that were elongated in side view, with a very tilted ventral disc surface having an elliptical disc outline. The bell shape may be most common in forms from rocky shores, but in our test of morphometric parameters only Scalpellum scalpellum (sublittoral), Savignium crenatum (epibiotic in corals), and Peltogaster paguri (parasitic) had shapes that differed significantly from the other species. The density of villi on the attachment disc varied significantly, but also showed no clear-cut correlation with substratum or habitat. Attachment organ structure is clearly the most variable feature in cirripede cyprids. To evaluate the degree to which attachment organ structure is correlated with habitat, settlement substratum, and mode of life, future studies should employ a more refined statistical analysis on an enlarged dataset, with much increased taxon sampling and a more multifaceted definition of ecological variables.

Introduction

Cirripedes are primary models in the study of invertebrate larval settlement in general, in part due to their role in the fouling of man-made objects in the sea (Aldred and Clare, 2008, 2009). All cirripedes are permanently sessile as adults, and are found in a variety of habitats from the upper intertidal to the deep sea, with the larvae settling on very diverse substrata, ranging from hard surfaces, such as rocks and crustacean cuticles, to the soft, live tissues of corals and marine sponges. Added to this variation, cirripedes can be suspension feeders, epibiotic organisms on a wide variety of organisms (e.g., crustaceans, marine sponges, corals, turtles, whales), and highly advanced parasites such as the Rhizocephala that infest Crustacea (Anderson, 1994; Hoeg and M0ller, 2006). While adult cirripedes differ extensively in structure, life style, and habitat, settlement is always accomplished by the highly specialized cyprid larva, which seems to have a remarkably constant morphology across the entire taxon (Glenner, 1998; Hoeg et al., 2004). This raises the question: how can this type of larva accomplish settlement in such diverse habitats and on widely different substrata? Analysis by scanning electron microscopy (SEM) indicates that cyprids do deviate in the detailed structure of their antennules, and these are precisely the organs used during settlement for surface exploration, attachment site selection, and adhesion (Glenner et al., 1989; Moyse et al., 1995; Kolbasov and Hoeg, 2007; Chen et al., 2013; Chan et al., 2014). Therefore, the aim of our study was to investigate the extent of this structural variation by including species from across the taxon and representing different habitats, settlement substrata, and modes of life.

During settlement, the cyprid uses the antennules to walk over the substratum in search of an attachment site, until it finally and irreversibly cements itself and commences metamorphosis (Fig. 1A). The antennule consists of four segments, but during settlement only the distal two directly engage the substratum (Lagersson and Hoeg, 2002). The third segment, the attachment organ, is short and carries a flat area called the attachment disc (Nott, 1969). This disc is carpeted with small cuticular villi and contains the glands used both in semi-permanent adhesion during surface exploration and final and irreversible cementation (Walker et al., 1987; Hoeg et al., 2004; Bielecki et al., 2009). The small, fourth segment carries many setae believed to be primarily responsible for distinguishing the site for attachment (Clare and Nott, 1994;Maruzzo et al., 2011).

We used SEM images of cyprids from 10 species to study 4 questions: 1) Which type of structure surrounds the attachment disc? According to Moyse et al., (1995), it can be either a velum or a skirt. A velum consists of long and thin cuticular filaments, attached on the side of the segment and draping down to overreach the edge of the disc surface (Fig. 1B, D). A skirt consists of short, broad flanges attached at the disc perimeter (Fig. 1C, D). 2) Is there variation in the angle of the attachment disc relative to the antennular long axis? The third segment can be either nearly symmetrically bell-shaped with a disc angle close to 90[degrees] (Fig. 1B), or it can be more or less shoe-shaped (elongated) when seen in side view and with an acute disc angle (Fig. 1C). 3) What is the shape of the attachment disc? The outline of the disc, seen face on, can be nearly circular, elliptical, or have a pronounced elongated shape (Fig. 1B, C). 4) Is there variation in the density of cuticular villi on the disc? These minute structures are implicated in the adhesive properties of the cyprid, but they have only been studied in a quantitative fashion in a single species (Phang et al., 2010; Aldred et al., 2013). Where possible, the SEM images were subjected to a biometrical analysis.

The 10 species selected for the present study included forms from the rocky intertidal, sublittoral forms, obligatory epibiotic forms (on marine sponges and corals), and a parasitic barnacle. Systematically, they cover the acorn barnacles (Thoracica Balanomorpha), the asymmetric barnacles (Verrucomorpha), the paraphyletic assemblage of stalked barnacles (Thoracica Pedunculata), and the parasitic Rhizocephala.

Materials and Methods

The investigated species, their habitat, and systematic affiliation are listed in Table 1. Species from rocky shores comprise the balanomorphans Semibalanus balanoides, Austrominius modestus, and Megabalanus rosa, but also Capitulum mitella and Pollicipes pollicipes, two of the very few pedunculated species from this habitat. From sublittoral habitats, we studied the asymmetrical barnacle Verruca stroemia (Verrucomorpha) and the pedunculated species Scalpellum scalpellum. Both are habitually epibiotic, but not linked to any particular host species, and can also attach to physical objects. Obligatory epibiotic species were the sponge barnacle Balanus spongicola and the coral barnacle Savignium crenatum, both from the Balanomorpha. Finally, we included the parasitic barnacle Peltogaster paguri (Rhizocephala), which infests hermit crabs.

Larval culture and preparation

The cyprids were cultured and prepared for scanning electron microscopy (SEM), as described in Jensen et al. (1994) and Moyse et al. (1995). Additionally, we studied cyprids of Capitulum mitella from Japan, which were raised and prepared following Kado and Kim (1996). SEM observation was conducted using JEOL microscopes (models JSM-6380LA, JEOL JSM-840, and JEOL JSM-6335; JEOL, Ltd., Tokyo, Japan) with digital image capture systems. Each of these instruments had stages that allowed 360[degrees] stub rotation and tilting up to 90[degrees].

Morphometric measurements

For all species we investigated the antennular structure in multiple cyprids (Table 2). Where possible, we scored the attachment disc angle, disc shape, villus density, and presence of a skirt or velum for both antennules on each larva, but specimen mounting limitations precluded the recording of all parameters from all antennules. To obtain photos for measurements, we tilted and rotated the specimens so that the third segment of the appropriate antennule was seen in near perfect lateral or medial view (for the disc angle) or directly face on with the attachment disc (for outline and villus density). In some cases, optimum viewing angles were impossible to achieve.

Attachment disc angle

The third antennular segment, also called the attachment organ, is connected to the cylindrical second segment by a very flexible joint. It can therefore have a variety of stances in both live and preserved larvae (Lagersson and Hoeg, 2002). To avoid any bias, we measured an angle relating only to the shape of the third segment. We defined this angle as the ventrally subtended angle between the mid-axis of the segment and the plane representing the attachment surface, as seen in perfect lateral or medial views (Fig. 1B, C, E, G). The mid-axis was traced from the midpoint between the proximal dorsal and ventral corners of the segment through the midline of the disc surface. The angle was measured from SEM photos with an accuracy of [+ or -]1 degree.

Disc outline

The attachment disc could vary from near circular to a narrow elliptical shape. To quantify the shape, we calculated the ratio between the transverse and median diameters. For elliptically shaped discs, the transverse diameter was the widest span of the disc perpendicular to the mid-axis (Figs. 1B, C; Fig. 4).

Villus density

The cuticular villi are simple, hair-shaped projections (not setae) on the thin disc cuticle. From face-on photos of the attachment disc taken at high magnification, we counted villus density in as many one-square-micrometer (1 [micro][m.sup.2]) areas as possible for each antennule studied. Counting was done by enumerating the tips of villi visible in the test area. Aside from density, the villi also vary in both length and thickness between the species, but these parameters can only be recorded in side views, and this is rarely possible unless velar filaments or skirt flaps are accidentally folded or torn away from the segment. The specimens used for villus counts were, for observational reasons, not always the same as those used for the other morphometrics.

[FIGURE 1 OMITTED]

Velum and skirt

We recorded the presence of any cuticular structures encircling (guarding) the perimeter of the attachment disc and classified them, where possible, as either a velum or a skirt. We also documented variations within each of these types of structures, although such variation in the cuticular structures was not quantified.

Statistics

The dataset on disc shape (ratio of long to short axis) and disc angle did not pass the equal variance test, and thus the variation in these two parameters was analyzed using a non-parametric Kruskal-Wallis test, followed by Dunn's pairwise comparisons (Sigma Stat ver. 3.5; Systat Software, Inc., San Jose, CA). The villus density among species fulfilled the assumption of homogeneity of variance, and this parameter was analyzed using one-way ANOVA. We had too few pictures of Pollicipes pollicipes to include it in any of the statistical analyses. In the analysis of disc shape, Savignium crenatum was not included, since only two specimens could be viewed at the appropriate orientation. Villus density was not scored for this species, because the infolded rims of the skirt impeded observation of the narrow attachment disc itself.

[FIGURE 2 OMITTED]

Results

Representative scanning electron microscopy (SEM) of the third antennular segments are illustrated in Figures 1E-L and 2A-0. These show lateral views to document the disc angle and velum or skirt and face-on views of the attachment disc to document shape and villus density. The structure of the velum and skirt is further detailed in Figure 3. The morphometric data are summarized in Figure 4 and Table 2.

[FIGURE 3 OMITTED]

Attachment disc perimeter

A velum was found around the disc in all cyprid specimens of Pollicipes pollicipes studied (n = 1), Capitulum mitella (n = 5), Semibalanus balanoides (n = 8), Megabalanus rosa (n = 11), and Austrominius modestus (n = 11). A skirt was found in all cyprid specimens of Balanus spongicola (n = 11), Verruca stroemia (n = 7), Scalpellum scalpellum (n = 5), Savignium crenatum (n = 5), and Peltogaster paguri (n = 5). There was no case in which classification as either a velum or a skirt was questionable. The velar filaments were always much longer than they were broad, and were always attached some distance from the disc surface, draping down the side of the segment to hang over the attachment disc (Fig. 3A, B). The low flaps of a skirt were always attached at the perimeter of the attachment disc (Figs. 3C, D). The width of the velar filaments did vary from very narrow (e.g., P. pollicipes and C. mitella) to relatively broad (e.g., M. rosa) (Fig. 3A, B). The velar filaments could also be numerous (e.g., C. mitella), originating from a broad base that soon divided into very thin, fringing straps (Fig. 3A). Furthermore, a velum always forms a closed fence around the entire disc, whereas the low and broad flaps of a skirt can be either continuous, as in B. spongicola (Fig. 3C) and S. crenatum, or missing along some stretches, as in S. scalpellum (Fig. 3D). In P. paguri the skirt was one continuous and very low, cuticular flap, extending all along the distal and lateral parts of the disc perimeter. Both the filaments of a velum and the flaps of a skirt consist of a very thin and flexible cuticle.

Attachment disc angle and shape

Variation in both disc angle and shape was significantly different among the species available for testing (Kruskal-Wallis test, P < 0.05, Table 2), but there was also much variation within species. For the nine species examined for disc angle, S. scalpellum, S. crenatum, and P. paguri had a significantly smaller angle when compared to the other species (Kruskal-Wallis test, Table 2). Among the eight species examined for disc shape (excluding S. crenatum and P. pollicipes), the ratio of the two axes was significantly smaller in S. scalpellum and P. paguri (Table 2). Although S. crenatum was excluded from this test, the specimens observed had extremely elongated discs, the most elongated of all species studied. A similarly elongated disc is found in cyprids from other coral barnacles (Brickner and Hoeg, 2010; Liu et al., 2016).

Villus density

Significant differences in villus density on the attachment disc were found among the species. Capitulum mitella and M. rosa had the highest density, while the lowest densities were found in S. scalpellum and P. paguri. All the remaining species had intermediate levels of villus density (one-way ANOVA, Table 2).

[FIGURE 4 OMITTED]

Discussion

Our morphometric analysis of antennular structure found significant differences between species in all tested parameters (attachment disc angle, disc shape, villus density on the disc, and type of structure encircling the disc), but only the structure encircling the disc correlated directly with habitat. In all species that inhabit rocky shores (Capitulum mitella, Pollicipes pollicipes, Semibalanus balanoides, Megabalanus rosa, Austrominius modestus), the attachment disc was surrounded by a velum consisting of long, elongated fringes of thin cuticle. In all the remaining species, irrespective of their habitat or systematic affiliation, the disc was surrounded by a skirt consisting of low, but broad cuticular flaps (Figs. 1-3). The remaining parameters measured did not show any clear correlation to habitat. A high disc angle (close to 90[degrees]) was found in some individual cyprids from all barnacles inhabiting rocky shores (C. mitella, P. pollicipes, S. balanoides, M. rosa, and A. modestus), but in our test these species did not form a group that differed significantly from those occupying other habitats. Only S. scalpellum, the epibiotic S. crenatum, and the parasitic P. paguri formed a group that had a significantly lower disc angle than all the remaining species studied (Table 1). Near circular discs were found in some cyprid specimens from C. mitella, P. pollicipes, S. balanoides, and A. modestus (all rocky shore species), but in our test only S. scalpellum and P. paguri were significantly different in having very elongated outlines of the attachment discs. Nevertheless, the scanning electron microscopy (SEM) pictures (Figs. 1, 2) suggest that species from rocky shores do have a disc angle close to 90[degrees] and a near circular disc, while species from other habitats have shoe-shaped third segments with lower disc angles and more elongated outlines. The illustrated cyprids (Figs. 1, 2) were all photographed at optimal orientations, but this was never possible for all the specimens used in the statistical analysis (Fig. 4, Table 2). Furthermore, the fourth segment and its multiple setae could obscure points on the third segment that were needed for accurate measurements. An analysis with more cyprid specimens, in which only optimal photographs are used, may therefore yield a different result. The density of villi was similarly difficult to estimate, due to frequent bulges in the cuticle of the attachment disc. These several factors explain some of the intraspecific variation (Fig. 4).

Velum and skirt

The function of the structures encircling the attachment disc (skirt or velum) is not understood, but it is striking that a velum is found only in the rocky shore species, and with no obvious correlation to systematic affiliation (see also Moyse et al., 1995; Glenner and Hoeg, 1995; and Rao and Lin, 2014). All other species here investigated have a skirt, irrespective of habitat or taxonomy (see also Glenner et al., 1989; Kolbasov and Hoeg, 2007; Yorisue et al., 2016). The thin flaps of a velum are very flexible and may extend laterally to cover a much larger surface area than the disc itself, which could be a factor when picking up stimuli during surface exploration. It would be valuable to use high-resolution video, as in Maruzzo et al. (2011) and Aldred et al. (2013), to investigate the dynamics of both vela and skirts during settlement in species from different habitats.

Disc shape and settlement

Variation in the angle of the attachment disc (Figs. 2, 3) may affect the stance of the cyprid and the flexibility of motion, both during surface exploration and at the ensuing metamorphosis. Like other species from rocky shores, cyprids of Amphibalanus (Balanus) amphitrite possess a bell-shaped third segment (Glenner and Hoeg, 1995), and they perform a wide repertoire of movements during surface exploration, including bending or reorienting the body in almost any direction while being attached by one antennule only (Lagersson and Hoeg, 2002). This flexibility allows them to change direction with only "one step," and it also insures that the body can easily respond by bending if impacted by strong and unpredictable waves. Thus, a bell-shaped third segment may allow more complex surface exploration behavior and better protection against accidental tearing loose in a high-energy environment compared to a possibly more restricted envelop of motion in cyprids with an elongated segment. Yet our preliminary observations on coral barnacle cyprids do not indicate that they have restricted antennular mobility. Direct observations of surface exploration behavior in a range of species are needed to support this theory. Variations in disc angle could also be related to differences in metamorphosis that follows the cementation. During this phase some species go through radical changes in orientation relative to the substratum surface, while being attached only by the third antennular segments (Hoeg et al., 2012; Maruzzo et al., 2012). These critical body movements may again depend on morphological parameters such as the attachment disc angle.

Density of villi

We observed clear differences in the density of villi on the attachment disc, but there was no clear relation to habitat. The presence of villi in all species, irrespective of habitat or substratum, testifies to their general importance in settlement, but the function of these minute surface structures is by no means well understood (Walker, 1995; Aldred and Clare, 2008, 2009; Phang et al., 2010; Aldred et al., 2013). If villus density is correlated with the adhesive strength of the attachment disc, we would expect species from high-energy habitats (such as the upper intertidal zone) to have the highest density of villi. In our study this is certainly true for Capitulum mitella, which settles in rocky shores swept by very strong waves, but Semibalanus balanoides had a significantly lower value, although it occupies a very similar habitat (Fig. 4, Table 1). Simple counts of density may not be the only parameter to measure. The length and thickness of the villi also vary between species, but these parameters are very difficult to measure accurately.

Conclusions

The morphology of the third segment in cirripede cyprids varies markedly in shape and structural features, but the explanation for this remains unclear. Some features may be correlated with either habitat or substratum type or both, but this is such a multifaceted grouping of variables that our limited taxon sampling does not allow proper separation of phylogenetic affiliation from ecological factors influencing morphological evolution. Future comparative analyses of cyprid antennular structure should therefore use a more refined statistical analysis on an enlarged dataset, with increased taxon sampling and a more critical definition of habitat and substratum types. Since a detailed phylogeny is now available for all cirripedes, such an approach could yield important insights, as was recently the case for an analysis of the evolution of cirripede sexual systems (Lin et al., 2015).

Acknowledgments

JTH thanks the King Saud University, Saudi Arabia, for arranging a visit that enabled the completion of this study. JTH was also funded by the Carlsberg Foundation. HAY and JTH provide their sincere thanks to Prof. Emeritus J. Moyse, University of Swansea, and Dr. Alireza Sari, University of Tehran, for many inspiring discussions on cyprid biology. BKKC acknowledges the Senior Investigator Award (Academica Sinica), which supported this work.

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HAMAD AL-YAHYA (1, [dagger]), HSI-NIEN CHEN (2, [dagger]), BENNY K. K. CHAN (3, (*), RYUSUKE KADO (4), AND JENS T. HOEG (5)

(1) King Saud University, College of Science, Zoology Department, Riyadh, Saudi Arabia; (2) Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, Taiwan; (3) Biodiversity Research Center, Academia Sinica, Taipei, Taiwan; (4) Kitasato University, School of Marine Biosciences, Minami-ku, Sagamihara, Kanagawa, Japan; and (5) University of Copenhagen, Department of Biology, Marine Biology Section, Copenhagen, Denmark

Received 15 September 2015; accepted 9 August 2016.

(*) To whom correspondence should be sent. E-mail: chankk@gate.sinica.edu.tw

([dagger]) These authors contributed equally to the paper.
Table 1
Species investigated in this study along with their habitat type and
taxonomic affiliation

Species                 Habitat

Scalpellum scalpellum   Medium depth, mostly epibiotic
Capitulum mitella       Intertidal rocky shore
Pollicipes pollicipes   Intertidal rocky shore
Semibalanus balanoides  Intertidal rocky shore
Megabalanus rosa        Sublittoral rocky shore
Austrominius modestus   Intertidal rocky shore
Balanus spongicola      Epibiotic on Porifera
Savignium crenatum      Epibiotic on stony corals
Verruca stroemia        Medium depth, mostly epibiotic, also on rocks
Peltogaster paguri      Parasitic on hermit crabs

       Species          Systematic position (*)

Scalpellum scalpellum   Thoracica Pedunculata
Capitulum mitella       Thoracica Pedunculata
Pollicipes pollicipes   Thoracica Pedunculata
Semibalanus balanoides  Thoracica Balanomorpha
Megabalanus rosa        Thoracica Balanomorpha
Austrominius modestus   Thoracica Balanomorpha
Balanus spongicola      Thoracica Balanomorpha
Savignium crenatum      Thoracica Balanomorpha
Verruca stroemia        Verrucomorpha
Peltogaster paguri      Rhizocephala

(*) Current taxonomy of the Cirripedia Thoracica does not reflect
relationships well. For a recent phylogeny, see Perez-Losada et al.,
2008, 2014.

Table 2
Comparison of three structural features (see Figs. 1-3) in the
attachment organs of nine species of cirripede cyprids representing a
wide range of substrata and habitats: 1) shape of the attachment disc
(ratio of short to long axis), 2) angle to the substratum, and 3)
density of cuticular villi on the disc surface

Factor                       Kruskal-Wallis test/ANOVA

Ratio of short to long axis  H = 45.27, P < 0.05, df = 7

Disc angle                   H = 56.62, P < 0.05, df = 8

Villus density               F = 9.52, P > 0.05, df = 7

Factor                       Pairwise test and specimen counts

Ratio of short to long axis  S. balanoides (8/4) = M. rosa (10/5) = A.
                             modestus (11/7) = B. spongicola
                             (11/7) = V. stroemia (7/6) = C. mitella
                             (3/3) > S. scalpellum (5/3) >
                             P. paguri (5/3)
Disc angle                   S. balanoides (6/4) = M. rosa (11/6) = A.
                             modestus (6/10) = B. spongicola
                             (5/10) = V. stroemia (7/9) = C. mitella
                             (5/6) > S. scalpellum (3/4) >
                             S. crenatum (4/5) = P. paguri (4/4)
Villus density               C. mitella = M. rosa > B. spongicola = V.
                             stroemia = S. balanoides >
                             A. modestus = S. scalpellum = P. paguri

Numerals in parentheses indicate the number of antennules/cyprids
studied for the feature. The results are shown graphically in Figure 4.
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Author:Al-Yahya, Hamad; Chen, Hsi-Nien; Chan, Benny K.K.; Kado, Ryusuke; Hoeg, Jens T.
Publication:The Biological Bulletin
Date:Oct 1, 2016
Words:5058
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