Does polymorphism predict physiological connectedness? A test using two encrusting bryozoans.
Coloniality has many potential benefits: in aggregations of unitary organisms, these include the ability to share resources and the partitioning of predation risk among colony members (e.g., Wilson, 1971). These advantages are retained in modular plants and invertebrates in which colonial units are physically cohesive. In addition, modular colonies may benefit metabolically from being able to attain large increases in size and volume while the component units (modules, polyps, zooids, etc.) remain small (Hughes and Hughes, 1986; Hughes, 2005; but see Vollmer and Edmunds, 2000). Although individual units within colonies often have the capacity to independently feed and reproduce, communication and cooperation between lower-level entities is essential for effective colonywide functioning in areas such as growth, reproduction, response to threats, or recovery from damage (Mackie, 1986; Stuefer et al., 2004). In eusocial insects, for example, well-integrated colonies may be identified through patterns of food sharing and olfactory, visual, or tactile communication between colony members (e.g., Wilson, 1971; Anderson and McShea, 2001). In taxa where members are physically connected, however, indirect morphological measures are often used (e.g., Dewel, 2000; McShea and Venit, 2002; Hageman, 2003). Higher-level colonial integration can be identified in colonies that have sheetlike (as opposed to runnerlike) growth forms (e.g., Harper, 1985; Pitelka and Ashmun, 1985; Schmid, 1986; Blackstone, 1998), and by cnidarian colonies with branching forms (e.g., Sanchez and Lasker, 2003) or perforate walls between polyps (Soong and Lang, 1992). Similarly, shorter distances between functional modules can be indicative of higher levels of physiological integration in cnidarian and bryozoan colonies (e.g., Hageman, 2003; Sanchez et al., 2007). Increases in the numbers of functional units within a colony, usually resulting in increased colony size, also necessitate more complex coordination between units, particularly to respond to outside threats or internal damage to the colony (Dewel, 2000; Hughes, 2005) and, in colonies that form a single sheet of modules, to enable growth at the lengthening colony perimeter. A larger colony with more numerous size-similar modules should therefore be more integrated than a smaller colony.
Colonial integration is also associated with the physical and functional specialization of colony members, as partitioning tasks within colonies requires higher levels of functional coordination and communication (e.g., Wilson, 1971; Dewel, 2000; Anderson and McShea, 2001; McShea and Venit, 2002). In modular invertebrates, the level of polymorphism may range from the production of defensive spines or reproductive structures on otherwise monomorphic zooids, to the complete partitioning of feeding, reproductive, and defensive tasks in highly polymorphic colonies such as siphonophores and some bryozoans (Reed, 1991; Harvell, 1994). The development and maintenance of polymorphs within a colony will often require the delivery of resources from other colony areas, and a complex, highly polymorphic colony should thus be more integrated than a colony with low complexity and monomorphic modules (e.g., Jackson, 1985). This level of integration is ultimately reliant on the fundamental organization and functioning of the nervous and circulatory systems, as more numerous connections will increase the abilities of modules within a colony to share resources and function in a coordinated manner (e.g., McShea and Venit, 2002; Stuefer et al., 2004). However, potential relationships between the numbers of physiological connections, polymorphism, and colonial integration, as well as the importance of intracolonial systems of resource transfer in determining these relationships, have yet to be fully examined in modular invertebrate taxa.
In colonial cnidarians and ascidians, common coelomic cavities or gastrovascular circulatory systems enable the transfer of resources between colony regions (Carle and Ruppert, 1983; Gladfelter, 1983; Mackie, 1986; Gateno et al., 1998; Cartwright, 2003). In contrast, the zooids of bryozoans are compartmentalized and the intracolony transfer of nutrients is more complex. In cheilostome taxa, hollow branching strands of epithelial tissue (funiculi) run from the gut and are distributed throughout the zooid. Funicular tissue is associated with minute communication pores in the zooid walls, providing the only means by which adjacent zooids may be physiologically connected (Carle and Ruppert, 1983; Mukai et al, 1997). Several studies have investigated the morphology and histology of communication pores and the pore plates on which they are arranged (Banta, 1969; Lutaud, 1969; Bobin, 1971, 1977; Silen, 1977; Chaney, 1983), but none have examined the potential for these connections to imply colonial integration within colonies.
We present surveys of lateral pores and pore plates across colony regions in two common unilaminar encrusting bryozoans. Zooids within colonies of these species have four lateral walls abutting adjacent zooids, a basal wall cementing the colony to the substrate, and a frontal wall that forms the surface of the colony. Growth is by the budding of new zooids at the colony margin (Jackson and Coates, 1986; Lidgard and Jackson, 1989; McKinney and Jackson, 1989), and zooid arrangement is staggered so that each is connected to six others, with connections along one lateral wall serving to receive and transmit resources from adjacent zooids (Fig. 1). Pore plates along lateral walls (termed septulae or septal chambers by other authors) form as double-layered calcium carbonate hemispheres and contain a number of pores. These pores are plugged with cell complexes that aid in the transport of material through the cells of the funiculus (Bobin, 1977; Mukai et al., 1997). Significantly, material can be transmitted only one way through the pore via these cells, and the morphology of the plates reflects the probable function of the connection. The nucleated lobes of the special cells are positioned on the distal side of the pore chamber (Bobin, 1977) and enlarge with maturity, with the development of a surrounding ring of calcium carbonate (the annulus). The pore chamber becomes convex on the side of the donor zooid (the outgoing, or abannular, side) and concave on the side of the receiving zooid (the incoming, or annular, side) (Banta, 1969; Bobin, 1977; Mukai et al., 1997). Direct confirmation of the function of the funicular system is scarce, although Bobin (1971) showed movement of lipids through the special cells in a ctenostome species, and movement of radiolabeled carbon products was primarily toward the growing edge in young Membranipora membranacea colonies (Miles et al., 1995; Best and Thorpe, 2002). The system thus remains the most likely means of carbon transport between zooids in bryozoans (Mackie, 1986).
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To clarify the directional functions of the funicular connections and to assess their potential role in enabling nutrient transfer within colonies, we surveyed the numbers of pore plates and pores of differing morphology within zooids across colony regions. We did this in two species that commonly occur in southern Australian waters: the cosmopolitan Watersipora subtorquata (d'Orbigny, 1852), and the endemic Mucropetraliella ellerii (MacGillivray, 1869). W. subtorquata (F. Watersiporidae) is a monomorphic species, and zooids have minimal calcification. Zooids within M. ellerii (F. Petraliellidae) colonies have fully calcified frontal walls with a small avicularian complex (a modified autozooid) present below the operculum (Stach, 1936; Cook and Bock, 2002; Tillbrook and Cook, 2005). Lecithotrophic larvae are brooded in ovicells external to the maternal zooid, and most colonies used in this analysis contained these reproductive polymorphs. In this analysis, we considered only the connections on lateral walls of functional zooids (autozooids) as indicators of integration, and not those that may be present within modified zooids such as ovicells and avicularia, as feeding autozooids appear to be the main source of nutritious resources within the colony, and polymorphs were not present in W. subtorquata. In addition, we considered ovicells rather than avicularia as measures of within-colony polymorphism in M. ellerii, as the high energetic demands of ovicells necessitate the transfer of resources, whereas the functions of avicularia, although suggested by morphology, have not been rigorously examined (Carter et al., 2010). We predicted that, if the morphological features of pore plates reflect their function, as implied by previous histological and microscopic evidence, there should be no convex "outgoing" pore plates at the extreme colony edges in either species. We expected the polymorphic M. ellerii colonies to be more highly integrated, and thus have higher numbers of connections per zooid, than those of the monomorphic W. subtorquata; we also predicted that connection numbers per zooid would increase with colony size in both species.
Materials and Methods
Colony collection and measurements
Watersipora subtorquata colonies were collected from acrylic settlement plates deployed at Breakwater pier, Williamstown, Victoria (37[degrees]51'53.60"S, 144[degrees]54'58.40"E). Settling colonies were monitored every 2-3 days, with nearby competitors carefully cleared from the plates, using forceps and a fine paintbrush, to ensure uninterrupted colony growth. Seven immature W. subtorquata colonies were used in the analysis (colony areas 5.00-62.50 [mm.sup.2], mean 29.29 [mm.sup.2]), and sampled zooids ranged 0.6-0.8 mm in length and 0.3-0.5 mm in width. As it proved very difficult to obtain Mucropetraliella ellerii colonies from settlement onto artificial substrata, experimental colonies were instead collected from St. Leonard's pier in southern Victoria (38[degrees]10'13.00"S, 144[degrees]43'15.00"E), and carefully removed from their ascidian (Pyura stolonifera) substrate using fine forceps. Eight M. ellerii colonies were used in the analysis, and most colonies were reproductively active (colony areas: 43.75 [mm.sup.2], 1 embryo; 56.25 [mm.sup.2], 16 embryos; 68.75 [mm.sup.2], 28 embryos; 87.50 [mm.sup.2], 12 embryos; 93.75 [mm.sup.2], 0 embryos; 106.25 [mm.sup.2], 55 embryos; 112.50 [mm.sup.2], 46 embryos; 212.50 [mm.sup.2], 63 embryos). Zooid sizes in sampled colonies ranged 0.60-0.90 mm in length and 0.25-0.45 mm in width. Owing to the nature of the collection, the damage histories and ages of the colonies were unknown.
Scanning electron microscopy
The patterns of pores and pore plates within lateral zooid walls were examined using scanning electron microscopy (SEM). Colonies were prepared for SEM by first immersing colony fragments in a 5% sodium hypochlorite solution until all living tissue was dissolved. For some colonies, this process took under 1 h, whereas other colonies, especially those with larvae present within ovicells, required repeated applications of the solution. After this process, the remaining calcium carbonate skeleton was rinsed with distilled fresh water and dried. Colonies were then dissected to reveal the area of interest, cleaned of loose material, fixed to SEM stubs, and sputter-coated in gold using a Polaron E5000 sputter-coating unit before being viewed under a Phillips 505 scanning electron microscope. Images were captured using Spectrum PC software, ver. 3 (Dindima Imaging, Victoria, Australia). Examples of images generated from the SEM process are shown for W. subtorquata (Fig. 2) and M. ellerii (Fig. 3).
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Survey design and statistical analysis
On each colony, frontal zooid walls were removed to reveal the lateral internal walls in a sequence from the colony center to the perimeter; this transect was staggered to include zooids at each position relative to the edge (example shown in Fig. 4). In some cases, the dissection process resulted in damage to parts of a colony or the accumulation of fine particles of calcium carbonate that occluded the structures of pores or plates. These and any other areas where visualization of pores was ambiguous, such as where tissue dissolution was incomplete, were excluded from SEM analysis. The position relative to the colony edge and, where possible, the ancestrula was noted for each zooid suitable for analysis, but in M. ellerii, the fragmentation of some colonies upon collection meant that the position of the ancestrula could not be determined. Within each zooid, the number and type of pore plates and pores were noted along one lateral wall. In W. subtorquata, 43 zooids at positions up to 4 zooid rows from the edge were suitable for analysis over the five colonies (numbers of zooids analyzed at each position: 4 rows (n = 2); 3 rows (n = 7); 2 rows (n = 9); 1 row (n = 19); 0 rows (n = 6)). A total of 57 zooids were suitable for analysis at distances up to five zooid rows from the edge in the eight M. ellerii colonies (numbers of zooids analyzed at each position: 5 rows (n = 3); 4 rows (n = 6); 3 rows (n = 10); 2 rows (n = 20); 1 row (n = 14); 0 rows (n = 4)). In both species, patterns of plate and pore numbers per zooid wall at each position were analyzed with two-factor analysis of covariance, with pore direction and distance from edge as fixed factors, colony size ([mm.sup.2]) included as a covariate, and the number of embryos included as an additional covariate for M. ellerii. Total numbers of connections (pore plates and pores) per lateral zooid wall were compared between species, using one-way analysis of variance, and the relationships between connection numbers and colony size for each species were analyzed using linear regression. Further, linear regression analysis was used to assess the relationships between embryo numbers and overall connection numbers in M. ellerii. All analyses were done using Systat ver. 12 (Point Richmond, CA).
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Intraspecific connection patterns
In Watersipora subtorquata zooids, the numbers of pore plates and pores varied significantly according to both their directional morphology and their position within the colony. The interaction between these factors was also significant (Table 1), with no outgoing plates and pores at the extreme colony edge (Fig. 5a, b). Post hoc pairwise comparisons (Tukey's HSD) confirmed that there were significant differences between numbers of outgoing plates and pores in zooids at the growing edge (position 0) and those at -3, -2, and -1 zooid rows behind the edge. At four zooid rows behind the growing edge, however, the numbers of outgoing connections appeared lower than at other positions behind the edge (Fig. 5a, b). There were no significant differences between the numbers of incoming versus outgoing pores or plates at any of the colony positions, with the exception of those at position 0.
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Table 1 Two-factor analysis of covariance comparing the numbers of pore plates (a) and pores (b) of both incoming and outgoing directions, across varying distances from the colony edge in Watersipora subtorquata colonies; colony size ([mm.sup.2]) was included as a covariate Source of variation df Mean squares F-ratio P a) Pore plates Direction 1 12.897 35.074 <0.001 Distance from edge 4 2.877 7.825 <0.001 Direction x distance 4 5.438 14.788 <0.001 Size 1 0.395 1.074 0.303 Residual 75 0.368 b) Pores Direction 1 301.811 14.860 <0.001 Distance from edge 4 97.340 4.793 0.002 Direction x distance 4 163.590 8.054 <0.001 Size 1 125.649 6.186 0.015 Residual 75 20.311
In Mucropetraliella ellerii, there were 2-3 plates per zooid wall at each position within the colony, but outgoing plate numbers decreased at the colony edge (Fig. 6a). The number of incoming pores showed a high amount of variation, with between 2 and 13 pores present on zooid walls across the colony; outgoing pores ranged from 0 to 15 per zooid wall across colony regions, with lower numbers, ranging from 0 to 2 per zooid wall, at the edge (Fig. 6b). There were significant differences in the numbers of pores and plates according to both their position within the colony and their direction, and a significant interaction between pore direction and distance (Table 2). Again, the drop in outgoing plates and pores within developing zooids at the edge of the colony appeared to be driving these significant results, and post hoc pairwise comparisons (Tukey's HSD) showed a significant difference in the numbers of outgoing plates and pores between zooids at the edge (position 0) and those at all other positions measured. There were no significant differences between the numbers of incoming versus outgoing pores or plates at any of the colony positions, with the exception of those at position 0.
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Table 2 Two-factor analysis of covariance comparing the numbers of pore plates (a) and pores (b) of both incoming and outgoing directions, across varying distances from the colony edge in Mucropetraliella ellerii colonies;colony size ([mm.sup.2]) and embryos per colony were included as covariates Source of variation df Mean squares F-ratio P a) Pore plates Direction 1 5.302 14.517 <0.001 Distance from edge 5 1.750 4.791 0.001 Direction x distance 5 3.770 10.323 <0.001 Size 1 6.925 18.960 <0.001 Embryos 1 1.689 4.625 0.034 Residual 100 0.365 b) Pores Direction 1 8.373 1.869 0.175 Distance from edge 5 20.913 4.669 0.001 Direction x distance 5 39.140 8.738 <0.001 Size 1 6.534 1.459 0.230 Embryos 1 2.184 0.488 0.487 Residual 100 4.479
The numbers of pore plates per zooid were similar in colonies of the polymorphic M. ellerii and the monomorphic W. subtorquata ([F.sub.1,98] = 0.206; P = 0.651: Fig. 7), but the numbers of pores were significantly different, with W. subtorquata having higher numbers of pores per zooid (26.86 [+ or -] 8.23 s.d.) than M. ellerii (16.18 [+ or -] 3.63 s.d.) ([F.sub.1,98] = 76.529; P < 0.001; Fig. 7). The numbers of pores, but not pore plates, differed significantly with colony size in W. subtorquata (pore plates = 0.013 x (colony size) + 4.556, [F.sub.1,41] = 2.687, P = 0.109, [r.sup.2] = 0.062; pores = 0.069 x (colony size) + 11.634, [F.sub.1,84] = 5.288, P = 0.024, [r.sup.2] = 0.059), with larger colonies generally having more pores per zooid than smaller colonies (Fig. 8a). In M. ellerii (Fig. 8b), there were significant increases in the numbers of both pore plates and pores per zooid with increasing colony size (pore plates = 0.008 X (colony size) + 4.057, [F.sub.1,55] = 15.061, P < 0.001, [r.sup.2] = 0.097; pores = 0.019 X (colony size) + 14.085, [F.sub.1,55] = 5.895, P = 0.018, [r.sup.2] = 0.215). The numbers of embryos per colony had a significant effect on the overall numbers of connections per zooid, with colonies that had higher numbers of embryos also having more numerous pores, but not pore plates (pore plates = 0.010 x (embryos) + 4.653, [F.sub.1,55] = 3.197, P = 0.079, [r.sup.2] = 0.055; pores = 0.043 X (embryos) + 14.820, [F.sub.1,55] - 4.924, P = 0.031, [r.sup.2] = 0.082).
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There were differences in the morphology of the pore plates across species, with those in Mucropetraliella ellerii colonies having more heavily calcified annular rims and more pronounced curvature than those in Watersipora subtorquata colonies. Such differences could be a result of the maturity of the component zooids, as M. ellerii colonies were larger, and most likely older, than W. subtorquata colonies. Banta (1969) examined communication pores and plates in 10 species of cheilostome bryozoans, concluding that the general morphology of the connections was similar, and that most differences were seen in the number of pores and relative calcification of the pore chambers. In this study, colonies of both species exhibited comparable patterns in incoming and outgoing plate connections, with around 3-6 plates per lateral wall, evenly divided between the two types. The exception was the reduction in outgoing pore plates at the extreme colony margin, which was consistent in colonies of both species. In all zooids examined at the growing edge in W. subtorquata, and in one of these edge zooids in M. ellerii, the zooid walls were complete but no new, developing buds had formed subsequent to the edge. Nutrient transport was therefore not required beyond this edge, rendering an outgoing porous connection redundant. The morphology of pore plates is thus consistent with histological evidence given by other workers (e.g., Banta, 1969; Bobin, 1977), and may be used to indicate the direction of resource transfer across colony regions.
Contrary to predictions, pore numbers per zooid were generally higher in the monomorphic W. subtorquata than in the polymorphic M. ellerii, and this effect was consistent across colony regions. The growth form of a colony and the resultant astogenetic and ontogenetic relationships between modules influence the way resources need to be distributed within that colony, and in sheetlike colonies, energy to fuel the development of new modules is provided through source-sink movement of metabolites across colony regions. For example, Oren et al.(1997) demonstrated movement of carbon products toward regenerating areas in a scleractinian coral, and corallivore snails fed preferentially on growing colony margins that were higher in nutritious value (Oren et al., 1998). Further, compensatory growth and induced reproduction after the removal of the growing edge in the bryozoan Membranipora membranacea suggested a likely source-sink mechanism of within-colony resource transfer (Harvell and Helling, 1993). High numbers of porous connections in W. subtorquata could therefore indicate high rates of resource transfer between zooids, and in the immature colonies used in the present study these resources may be primarily directed toward further colony growth at the edge. This supports work by Hart and Keough (2009), who showed that re-growth of fragments containing young modules from the original colony edge was greater than that of older fragments, suggesting a high level of investment in growth at the edge; zooids up to a few rows behind the edge also appeared to be primarily responsible for this growth. In the mature M. ellerii colonies, the numbers of both incoming and outgoing pores per zooid wall were relatively even at all sampled positions across the colony, and were consistently lower than pore numbers in W. subtorquata. Klemke (1993) showed no differences in growth rates of M. ellerii fragments originating from the young colony edge and the older colony center, suggesting that, in this species, resources might not be strongly directed toward growth, and low numbers of pores in zooids near the edge could be indicative of these patterns in the sampled colonies.
In M. ellerii, maternal ovicells are the main type of functional polymorph requiring the intracolonial transfer of resources, and assessing connection numbers in colonies with different numbers of ovicells could provide an intra-specific estimate of colonial integration. Overall numbers of pores per zooid increased with this intraspecific measure of polymorphism, suggesting that these colonies might have a higher capacity for nutrient transfer. However, this relationship was very weak, with limited explanatory power, and appeared to be of less importance than the relationship between connection numbers and colony size. Maternal zooids with reproductive ovicells attached also possess a feeding lophophore, and the resource requirements of the developing embryo might instead be met through increased feeding intensity by the lophophore within the maternal zooid. This would in turn make the formation of additional, "incoming" connections to the reproductive zooid less important, which could account for the lack of any discernible changes in funicular morphology across colony regions.
Colony size significantly influenced the numbers of lateral pores per zooid in both W. subtorquata and M. ellerii. Increases in the number of modules in a colony might necessitate the development of more intracolonial connections to improve the efficiency of resource transfer throughout the colony, and therefore indicate increased levels of colonial integration. However, in the absence of disturbance, size is a valid indicator of colony age in modular organisms (e.g., Jackson, 1985; Jackson and Coates, 1986; Hughes and Connell, 1987; Hughes, 2005), and more inter-zooid connections in larger, older colonies could therefore result from the development of more connections over time in mature colonies. In addition, if communication pores are able to be created or closed off depending on the nutritious needs of individual zooids, the number of connections between zooids might not show any predictable variation with colony age or size. Further examination of the patterns of connections across colonies of known ages will provide more detailed estimates of the role of the mechanisms of resource transfer across colonies, and the energetic requirements of component zooids.
To our knowledge, this study represents the first investigation of the nutrient transfer capacities of bryozoan colonies by analyzing the morphological features of the funicular system. The absence of outgoing pores at the extreme edges of colonies suggests that plate morphology is a true indicator of function; and within each species, the variation in pore numbers, coupled with the relative consistency in plate numbers, suggests that this system might be flexible, possibly in response to changes in both the external environment and the internal conditions of a colony. Environmental conditions appear likely to cause changes to the size and shape of zooids (O'Dea and Okamura, 1999; O'Dea, 2003; Atkinson et al., 2006; O'Dea et al., 2007), and changes in colony growth patterns and calcification rates as a response to external pressures such as competition, damage, and overgrowth are common in cheilostome species (Lidgard and Jackson, 1989; Harvell and Helling, 1993; Bone and Keough, 2005, 2010). Because these changes in growth rates and size need to be supported by the movement of metabolites and carbon compounds toward the growing areas, we might expect the calcification of the internal structures of the funicular system to be under plastic regulatory mechanisms. Shapiro (1992) noted the formation of new types of connections, indicative of fusion, in colonies that were genetically compatible and growing in close proximity. Similar plasticity across the funicular system as a whole would enable more efficient use of resources within a colony, but further work, involving confocal microscopy or fluorescent tracers, is required to elucidate the potential for flexibility under differing internal conditions.
In the present study, the level of connectedness between functional autozooids did not increase with polymorphism in two species of extant Bryozoa, challenging the legitimacy of assumed positive relationships between levels of within-colony specialization and physiological integration. Lower numbers of connections could be a sign of a less well-integrated colony, but it may also be that using the numbers of functional polymorphs within and between species, or the numbers of connections between autozooids, is not sufficient to infer integration at the species level. Quantification of connections between all modules in the colony (including ovicells and other polymorphs such as avicularia) could therefore provide more detailed estimates of colonial integration. High levels of specialization within a colony must be supported by coordinated intra-colonial movement of metabolites, but this could equally be necessary following changes to a colony's form and life history. Further understanding of functional integration across colonies in these taxa might be achieved only through detailed analysis of the resource requirements and nutrient movement at the level of individual zooids and colony regions. We also need to consider more complicated relationships within colonies, including interactions between module age and position within the colony, and how these may vary with changes to colony form. A thorough investigation of colonial integration first requires, therefore, an understanding of the ways colonies are structured, the relative resource requirements across colonies, and the capacity for resource acquisition and translocation--information that cannot be garnered from morphological analysis alone. In addition, although pore size was not considered in this study, preliminary inspection of the SEM images suggested that pores in M. ellerii were substantially larger than those in W. subtorquata colonies. Few, large pores could enable transport of more material, but more numerous small pores might enable finer control of this transport. Thus, if the capacity for nutrient movement is dependent on the total volume of funicular tissue, pore size needs to be considered in tandem with pore numbers in the development of future models of colonial integration in bryozoans.
Given the apparent resemblance of the bryozoan funicular system to the blood vascular system (e.g., Ruppert and Carle, 1983), we might consider the level of integration in these organisms as being relative to the complexity of the branching exponents of the network of nutrient delivery, and therefore informative to important discussions on metabolic scaling (e.g., West et al., 1997, 1999). However, it seems unlikely that the funicular system could be analyzed in the same way as other systems with branching epithelial networks, for several reasons: (1) funicular branching is not three-dimensional; (2) the system does not exhibit hierarchical branching with size-similar final vessels; (3) movement of metabolites is not a passive delivery system based on fluid transport dynamics, but rather an active system operating between individual zooids; and (4) it is unclear whether the system network is optimized according to space or energetic needs (Cates and Gittleman, 1997). It is therefore complex, dynamic, and unique, and may not be easily explained by any mathematical predictors currently in use (e.g., Murray's law; LaBarbera, 1990). Further investigation into the mechanisms controlling inter-zooid resource delivery in these taxa will continue to illuminate the dynamics of the bryozoan funicular system, and will be of fundamental importance to discussions on the evolution and maintenance of coloniality as a life-history strategy.
Funding for this work was provided through an Australian Research Council grant to M. J. Keough, and E. K. Bone was supported throughout by an Australian Postgraduate Award. We thank Joan Clark for use of and initial assistance with the scanning electron microscopy facilities in the Department of Zoology, The University of Melbourne, and E. K. B. is grateful to Matt Symonds and David Reid for comments that improved the manuscript.
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ELISA K. BONE *, [dagger] AND MICHAEL J. KEOUGH
Department of Zoology, The University of Melbourne, Victoria 3010, Australia
Received 1 August 2010; accepted 26 October 2010.
* To whom correspondence should be addressed: E-mail: email@example.com
[dagger] Current address: 14A Genevieve Way. RD9 Hamilton 3289, New Zealand.
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|Author:||Bone, Elisa K.; Keough, Michael J.|
|Publication:||The Biological Bulletin|
|Date:||Dec 1, 2010|
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