Functional controls on monticule height and spacing in Permian stenolaemate bryozoans Open Access

Bryozoans (also known as colonial moss animals) filter plankton from ocean water for their food. They struggle with refiltering the same water repeatedly. They have evolved bumps on their colony surfaces to solve this problem. We think the height and spacing of these bumps should be inversely proportional to how curved the colony surface is. We test this idea using 285 million year old fossil bryozoans from Greenland and Australia. We show that the bumps are larger and closer on less-curved colonies as we predicted.

One of the challenges for filter feeding animals is how to maximize feeding by minimizing refiltering previously filtered water (Hentschel and Shimeta, 2008). This is less of a problem for motile filter feeders (e.g., whale sharks or flamingos; Colman, 1997; Anderson, 2017) than for sessile ones. Bryozoans are sessile filter feeders whose ciliated tentacles of their lophophore create a feeding current that draws plankton toward their mouth (Pratt, 2004, fig. 2; Winston and Migotto, 2021, fig. 6.4). This creates two problems for bryozoans. First, the filtered water accumulates between the canopy of tentacles and the colony surface causing a pressure buildup that stifles feeding (Shunatova and Ostrovsky, 2002, figs. 4, 5). Second, previously filtered water gets refiltered in eddies (Grünbaum, 1995, fig. 6a; Pratt, 2004, fig. 7A(i)). Bryozoans overcome this problem by creating colony-wide feeding currents that keep the incurrent unfiltered water separate from the excurrent of previously filtered water, thus reducing refiltering of water and improving feeding efficiency (Banta et al., 1974; Cook, 1977; Winston, 1978, 1979; Taylor, 1979; Lidgard, 1981; Dick, 1987; Eckman and Okamura, 1998; Pratt, 2004; von Dassow, 2005a). The same phenomenon has also evolved in sponges (Bidder, 1923) and colonial ascidians (Vogel, 1994).

Empirical data and mathematical modeling of water flow in encrusting bryozoan colonies have shown that currents created by individual zooids may interact deleteriously (Bishop and Bahr, 1973; Thorpe and Ryland, 1987; Grünbaum, 1995). This suggests colony-wide feeding currents are beneficial to the colony at least in low current velocities where flow remains laminar (Grünbaum, 1997; Eckman and Okamura, 1998). The filtered water typically flows between the canopy of tentacles and the colony surface toward macular chimneys through which the previously filtered water is ejected away from the colony surface (McKinney, 1986a, fig. 4A; Taylor, 1999, fig. 41.3; Okamura and Partridge, 2009, fig. 3). Macular chimneys typically form on flat or more often elevated parts of a colony called monticules (Banta et al., 1974, fig. 1; Winston, 2010, fig. 2).

The bigger and flatter the colony surface, the greater the problem with refiltering water due to the greater incurrent volume (McKinney, 1986a, b). McKinney (1986b) showed that in cylindrical colonies, macular chimneys form only in branches >2 mm diameter. That is because the surfaces of smaller-diameter cylinders are curved enough that the previously filtered water can escape between the lophophores. Larger-diameter cylinders have less surface curvature (Fig. 1). That is why the surface of our large spherical planet seems flat when standing on it. Branches on the largest bryozoan colonies are not cylindrical but frondose (Cuffey and Fine, 2006). Frondose branches are typically more elliptical in cross section, for example, Heterotrypa frondosa (d'Orbigny, 1850). Curvature varies across a frondose branch unlike a cylindrical branch.

As a result, curvature across an elliptical branch decreases with increasing eccentricity (Fig. 3).

The goal of this study is to see how branch surface curvature affects monticule height and spacing using two Permian stenolaemate bryozoans, both with blade-like monticulate branches with varying cross-sectional shape and size. Our hypothesis is that the curvature of the colony surface is inversely proportional to both the height and spatial density of monticules.

This study is based on colonies of two species of Permian stenolaemate bryozoans. Evactinostella crucialis (Hudleston, 1883) is a cystoporate stenolaemate bryozoan (Yancey et al., 2019). This species forms erect four-vaned colonies (Håkansson et al., 2016). The bifoliate vertical vanes are very elliptical in cross section, up to 1 cm thick, less than 10 cm wide, with heights reaching more than 25 cm (Crockford, 1957). For this study, 17 colonies of E. crucialis were selected from Cisuralian strata in the East Gondwana Rift Zone in Western Australia. Of these, four specimens were selected from the Jimba Jimba Member of the Callytharra Formation exposed northwest of Jimba Jimba Station at 25.0239°S, 115.0717°E, and 13 colonies were selected from the Callytharra Formation exposed in the Lyndon River gully at 23.8600°S, 114.4792°E (Fig. 4). Both sections are in the Merlingleigh Subbasin at the southern end of the onshore Southern Carnarvon Basin, Western Australia (Haig et al., 2014) (Fig. 5). Specimen numbers and collection information are available in Table 1. Stratigraphically following the International Chronostratigraphic Chart v2023/09, these colonies lived during the Artinskian Age of the Cisuralian Epoch of the Permian Period (Haig et al., 2014; Henderson et al., 2020). Paleogeographically, they were deposited toward the southernmost marine strata in the East Gondwana Rift Zone at ~50°S paleolatitude (van Hinsbergen et al., 2015; Haig et al., 2017).

Tabulipora sp. is a trepostomate stenolaemate bryozoan (Taylor, 2020; Bock, 2023). Our specimens were originally assigned to Amphiporella (Madsen and Håkansson, 1989; Madsen, 1994). But since Boardman and Buttler's forthcoming Treatise on Invertebrate Paleontology (Part G, Bryozoa, Revised, Volume 2) subsumes Amphiporella into Tabulipora in keeping with Astrova's (1978) classification, we here refer to them as Tabulipora sp. Our species forms erect frondose colonies. The bifoliate, platy fronds are up to 1 cm thick, reaching over 20 cm wide (Madsen and Håkansson, 1989; Madsen, 1994). For this study, 15 colonies of Tabulipora sp. were selected from the series of samples collected from the Kim Fjelde Formation, Mallemuk Mountain Group, Wandel Sea Basin in North Greenland (Fig. 6) (Stemmerik and Håkansson, 1991; Watt, 2019). One colony came from the Midnatfjeld section in eastern Peary Land at 82.7592°N, 22.1356°W, and 14 colonies came from the Kap Jungersen section in Amdrup Land 80.6283°N, 15.7489°W (Madsen, 1994) (Fig. 7). Specimen numbers and collection information are available in Table 2. Stratigraphically, these colonies lived during the Artinskian to Kungurian Ages of the Cisuralian Epoch of the Permian Period (Stemmerik et al., 1996, 2000; Henderson et al., 2020). Paleogeographically, they were deposited in the Wandel Sea Basin (Håkansson and Pedersen, 2015) at ~40°N paleolatitude (van Hinsbergen et al., 2015; Blakey, 2021, fig. 8).

All specimens used in this study are deposited in the Western Australia Museum (WAM), Perth, Australia. Each specimen's WAM repository number is indicated in Table 1 or 2.

We measured branch width, branch thickness, and monticule height with digital calipers to the nearest 0.01 mm (Fig. 8). As discussed previously in Equation (3), curvature K was calculated as: /K/  = where a is the length of the semi-major axis (i.e., one-half branch width) and b is the length of the semi-minor axis (i.e., one-half branch thickness). Therefore, curvature in mm^–1 as calculated in Equation (2) was /K/  = ⁠. Monticule spatial density in number per mm² was calculated as the number of monticules per branch side/area of branch side. On some more weathered branches, monticules were not well enough preserved to be counted on both sides of the branch.

Using the structure-from-motion (SfM) method (Fonstad et al., 2013), we built digital elevation models (DEMs) of two branch surfaces. This is the first time SfM-DEM technology has been used in bryozoology. SfM applies the principles of stereoscopic photogrammetry to a series of two-dimensional digital images to reconstruct a three-dimensional DEM of the surface of an object (Westoby et al., 2012). For creating the DEMs, we chose one side of one branch from one colony from each species that had the largest surface area (i.e., the most monticules): WAM 2024.325C for Tabulipora sp. and WAM 2024.317A for E. crucialis. The DEMs were built in Agisoft's Metashape Pro version 1.64 with 0.1 mm resolution on the x and y coordinate axes and 0.01 mm resolution on the z (vertical) axis. Topographic profiles through the colony surface were made with QGIS version 3.30 from monticule crest to monticule crest.

The surfaces of the Evactinostella crucialis colonies (N = 17, curvature [mm^–1] range: 0.0021–0.0441, mean = 0.0118, standard deviation = 0.0104) are more curved than those of Tabulipora sp. (N = 15, curvature [mm^–1] range: 0.0012–0.0122, mean = 0.0063, standard deviation = 0.0032) (Tables 3, 4, respectively). On average, the more elliptical Evactinostella branches are significantly more (i.e., twice as) curved than those of the flatter Tabulipora branches (t-test two-sample assuming unequal variance: t-stat = 2.005, p = 0.059).

The caliper-based heights of the monticules on the Evactinostella crucialis colonies (N = 17, height [mm] range: 0.35–0.60, mean = 0.50, standard deviation = 0.08) are shorter than those on the Tabulipora sp. colonies (N = 10, height [mm] range: 0.40–1.85, mean = 1.10, standard deviation = 0.53) (Tables 3, 4, respectively). On average, monticules on the more elliptical Evactinostella branches are significantly shorter (i.e., half as high) than those of the flatter Tabulipora branches (t-test two-sample assuming unequal variance: t-stat = –3.364, p = 0.008).

The DEM-based monticule heights yielded similar results. The monticules on Evactinostella crucialis (N = 40, height [mm] range: 0.10–2.68, mean = 0.78, standard deviation = 0.47) are shorter than those on Tabulipora sp. (N = 31, height [mm] range: 0.89–2.40, mean = 1.48, standard deviation = 0.39). On average, monticules on the more elliptical Evactinostella branches are significantly shorter (i.e., half as high) than those of the flatter Tabulipora branches (t-test two-sample assuming unequal variance: t-stat = 6.761, p < 0.001) (Fig. 9).

Only among the Evactinostella colonies was branch surface curvature inversely proportional to monticule height as we expected (Fig. 10). The same was not true for the flatter Tabulipora sp. branches.

The monticules on the Evactinostella crucialis colonies (N = 16 colonies, spatial density [number/mm²] range: 0.010–0.020, mean = 0.014, standard deviation = 0.003) are less densely spaced than those of Tabulipora sp. (N = 10, spatial density [number/mm²] range: 0.016–0.025, mean = 0.018, standard deviation = 0.003) (Tables 3, 4, respectively). On average, the monticules on the more elliptical Evactinostella branches are significantly (i.e., 22%) less densely spaced as those of the flatter Tabulipora branches (t-test two-sample assuming unequal variance: t-stat = –3.746, p = 0.001).

Only among the Evactinostella colonies was branch surface curvature inversely proportional to monticule spatial density as we expected (Fig. 11). The same was not true for the flatter Tabulipora sp. branches.

This study presumes that the monticules are sites of excurrent colony-wide feeding currents as previous authors have done (e.g., Yancey et al., 2019). Four independent pieces of evidence support this.

One: the monticules lack incurrent-generating feeding autozooids (Fig. 12). When an area of a colony surface is devoid of functioning autozooids with enough surrounding surface area of incurrent-generating autozooids, the devoid area by default becomes an excurrent chimney (Banta et al., 1974, fig. 1; McKinney, 1986a, fig. 4A; von Dassow, 2005a, fig. 1A). This study also assumes the monticules are the only sites of excurrent colony-wide feeding currents, and therefore, there are no non-skeletal chimneys interfering with our skeletal chimney interpretations. It is known that extant cheilostomes (e.g., Membranipora) can create excurrent chimneys simply by temporarily leaning their lophophores away from each other or retracting their polypides (Winston, 1978; Cook and Chimonides, 1980; Lidgard, 1981; Taylor, 1999; Shunatova and Ostrovsky, 2002). Fortunately, as shown by Shunatova and Ostrovsky (2002, table 1), such non-skeletal excurrent chimneys are not known from any stenolaemate bryozoans such as those in this study.

Two: the monticules have a stellate shape (Fig. 12) like other excurrent structures with centripetal flow. Many excurrent maculae are star-shaped (Anstey, 1987), for example, those in the cystoporate Constellaria (Boardman, 1983, fig. 59.1) and the trepostomes Heterotrypa (Anstey and Perry, 1973, pl. 17) and Tabulipora (Key et al., 2002, fig. 1). Key et al. (2011) used stream channel network analysis to show that stellate maculae in Tabulipora are excurrent chimneys. As first noticed by Anstey and Pachut (1976) and Anstey et al. (1976), stellate maculae are analogous to inorganic centripetal flow structures such as star dunes (e.g., Folk, 1971, fig. 5B; Nielson and Kocurek, 1987, fig. 2A) and araneiform CO₂ geysers on Mars (Portyankina et al., 2020, fig. 1). They are even more similar to centripetal flow structures in other organisms such as astrorhizae in living sclerosponges (e.g., Hartman and Goreau, 1970, fig. 5; Boyajian and LaBarbera, 1987, fig. 1) and fossil stromatoporoids (e.g., LaBarbera and Boyajian, 1991, fig. 1). The conical mamelons with radial bands in the Eocene demosponge Pickettispongia tabelliformis (Chapman and Crespin, 1934) from Australia illustrated by Pisera et al. (2023, fig. 5C) is a stunning example of evolutionary convergence with the monticules in this study.

Three: the autozooecial skeletal apertures are radially arranged around the centers of the monticules with the apertures facing away from the monticules (Fig. 12.1). Lunaria typically develop on the side of the aperture closest to the maculum (Anstey, 1981, 1987; Patzkowsky, 1987; Taylor, 1999). This is most evident in the cystoporate Evactinostella crucialis colonies that have lunaria on the sides of autozooecial apertures nearest the centers of the monticules (Crockford, 1957; Utgaard, 1983). This makes the autozooecial apertures meet the colony surface very obliquely (Crockford, 1957) (Fig. 12.1). In extant colonies, this arrangement is associated with excurrent colony-wide feeding currents centered on maculae (Banta et al., 1974, fig. 1; Grünbaum, 1997, fig. 2a; von Dassow, 2005a, fig. 1B, 2005b, fig. 1B; Winston, 2010, fig. 2).

Four: the maculae are elevated (i.e., monticulate) (Figs. 8.3, 9). Most studies have attributed monticules to sites of excurrent flow (Banta et al., 1974, fig. 1; Taylor, 1999, fig. 41.3; Shunatova and Ostrovsky, 2002, fig. 7b; Winston, 2010, fig. 2; Taylor, 2020, fig. 4.22). However, not all monticules are centers of excurrent flow (Shunatova and Ostrovsky, 2002, fig. 7a).

Among the Evactinostella colonies, branch surface curvature was significantly inversely proportional to monticule height as we expected (Fig. 10). The same was true for the flatter Tabulipora sp. branches, but it was not significantly so (linear regression, y = –22.644x + 1.2571, R² = 0.0176, p = 0.715). We attribute this difference between Evactinostella and Tabulipora to less branch surface curvature in the latter. Flatter colonies (e.g., Tabulipora) will have a greater need to expel filtered water so should need higher monticules producing higher excurrent velocities. This is similar to star dunes where height is proportional to wind speed (Zhang et al., 2016).

Among the Evactinostella colonies, branch surface curvature was inversely proportional to monticule spatial density as we expected (Fig. 11). The same was not true for the flatter Tabulipora sp. branches. We attribute this difference between Evactinostella and Tabulipora to less branch surface curvature in the latter. The magnitude of curvature in Evactinostella is more than twice as much as in Tabulipora, and the range is four times greater.

Alternatively, the weaker inverse correlation between branch surface curvature and monticule height and density in Tabulipora compared with Evactinostella may be a function of the former retaining a more constant branch cross-sectional shape through astogeny compared with Evactinostella, whose curvature changes more with colony age. This may not be the case as monticules have previously been correlated with bryozoan branch curvature. McKinney (1986b) measured 914 bryozoans with cylindrical branches and showed that macular chimneys form only in branches >2 mm diameter. Key et al. (2002) measured macular size in ramose Tabulipora colonies. They showed that as branch diameter increases (i.e., substrate curvature decreases), macular size increases. Wyse Jackson et al. (2014) measured monticule size in trepostomes encrusting conical nautiloids. They showed that as cone diameter increases (i.e., substrate curvature decreases), monticule size increases. Therefore, we conclude that the smaller and more curved the surface of a stenolaemate colony, the less the colony needs robust colony-wide feeding currents created by closely spaced tall monticules. Larger and flatter plate-like colonies need more robust colony-wide feeding currents created by closely spaced tall monticules.

We thank L. Madsen (University of Copenhagen), L. Stemmerik (Geological Survey of Denmark and Greenland), and C. Heinberg (Roskilde University) for help collecting the Greenland samples, and A. Ernst (University of Hamburg) for helping collect the Australian samples. We thank P. Sak (Dickinson College) for help with quantifying surface curvature. We thank P. Taylor (Natural History Museum, London) for discussion on the potential for excurrent chimneys being formed non-skeletally by lophophores leaning away from the macular centers. We thank A. Ernst and an anonymous reviewer for their positive reviews.

The authors declare none.