Orthides, Brachiopoda) and Its Endoskeletobionts and Predators from the Middle Devonian Dundee Formation of Ohio, United States

PALAIOS, 2010, v. 25, p. 196–208 Research Article DOI: 10.2110/palo.2009.p09-119r

ECOLOGICAL INTERACTIONS BETWEEN RHIPIDOMELLA (ORTHIDES, BRACHIOPODA) AND ITS ENDOSKELETOBIONTS AND PREDATORS FROM THE MIDDLE DEVONIAN DUNDEE FORMATION OF OHIO, UNITED STATES

RITUPARNA BOSE,1* CHRIS SCHNEIDER,2 P. DAVID POLLY,3 and MARGARET M. YACOBUCCI 4 1Department of Geological Sciences, Indiana University, 1001 East 10th Street, Bloomington, Indiana 47405, USA; 2Department of Geology, Energy Resources Conservation Board, Alberta Geological Survey, 402, Twin Atria Building, Edmonton, Alberta T6B 2X3, Canada; 3Department of Geological Sciences, Indiana University, 1001 East 10th Street, Bloomington, Indiana 47405, USA; 4Department of Geology, Bowling Green State University, 190 Overman Hall, Bowling Green, Ohio 43403, USA e-mail: [email protected]

ABSTRACT dead shells. Although such boring organisms as clionid sponges are well known from modern shells, fossil examples are encountered less Only the small (2.0 6 0.1 cm) orthide brachiopod Rhipidomella in the frequently or, as Lescinsky (1996) has stated for encrusting organisms Middle Devonian Dundee Formation exposed at Whitehouse Quarry, in general, are overlooked. Taylor and Wilson (2002) used the term Ohio, preserves evidence of interactions with endoskeletobionts and endoskeletobiont for organisms boring into and infesting the surfaces predators (39.6 ,n5 48), as opposed to the slightly larger atrypides, % of organic media (5substrates) whether living or dead; the commonly spiriferides, and stropheodonts (n 5 245). All traces of predation and used terms encruster, encrusting organism, and epizoan generally refer boring by other organisms are lacking on such larger brachiopods as to episkeletobionts. Although highly useful for descriptive precision, strophomenides and spiriferides, which are more often encrusted in Taylor and Wilson’s (2002) terminology for categories of encrusting Devonian localities of North America—the Silica Shale of Ohio, organisms has not yet gained acceptance in the modern epibiosis Hamilton Group of New York, and Cedar Valley Limestone of Iowa. literature. We use their terminology herein. Punctate shells of Rhipidomella preserve interactions with endoskeleto- Episkeletobionts are useful as autecological or postmortem environ- bionts and predators, phenomena less common for punctate brachiopods. mental indicators for their hosts—whether the host was living at the All traces on Rhipidomella were preserved as endoskeletobionts; if time of encrustation (Rodriguez and Gutschick, 1975; Pitrat and calcified encrusters were present, they likely were lost postmortem. Rogers, 1978; Kesling et al., 1980; Watkins, 1981; Anderson and Several Rhipidomella individuals bear partially repaired grooves from Megivern, 1982; Brezinski, 1984; Spjeldnaes, 1984; Alvarez and Taylor, parasitic interactions with sinuous, boring organisms, attributed to 1987; Harland and Pickerill, 1987; Morris and Felton, 1993; Peters, ctenostome bryozoans. These parasites bored into the shell along the 1995; Lescinsky, 1995; Sandy, 1996; Sumrall, 2000; Morris and Felton, commissure, likely benefiting from the inhalant and exhalant currents 2003; Schneider, 2003, 2009a; Zhan and Vinn, 2007; Rodrigues et al., produced by the brachiopod, and in some cases, expanded away from the 2008) or was dead (Thayer, 1974; Rodriguez and Gutschick, 1975; commissure following the host’s death. The straight, U-shaped borings in Watkins, 1981; Anderson and Megivern, 1982; Brezinski, 1984; Gibson, one Rhipidomella specimen with boreholes are similar in morphology to 1992). Episkeletobionts have been studied with regard to the Caulostrepsis traces that occurred with their tubes opening along the orientation of brachiopod valves (Rudwick, 1962; Hurst, 1974; Pitrat margins of a modern brachiopod. Other endoskeletobiont traces likely and Rogers, 1978; Kesling et al., 1980; Spjeldnaes, 1984), to the formed on the postmortem shells of Rhipidomella. Predation repair scars preferred orientation in marine currents (Kesling et al., 1980), to the are present on two specimens, indicating the presence of predators and the potential as camouflaging agents for hosts (Schneider, 2003, 2009a), to survival of some Rhipidomella individuals from durophagy. No specimens the attracting or antifouling nature of ornamentation (Richards and contain evidence of drilling predators. Shabica, 1969; Richards, 1972; Carrera, 2000; Schneider, 2003, 2009a; Schneider and Leighton, 2007), and in regard to the purpose of the INTRODUCTION valve punctae (Thayer, 1974; Curry, 1983; Bordeaux and Brett, 1990). In addition, the presence of encrusting organisms in marine paleocom- The Middle Devonian Dundee Formation, located in the Michigan munities signifies a level of trophic and three-dimensional (3D) Basin of North America, has long been recognized as a highly complexity in the benthos, particularly in environments where fossiliferous unit. The sedimentology and stratigraphy of the Dundee inorganic hard media are lacking. Encrusting organisms respond to Formation has been well studied (Bassett, 1935; Sparling, 1988), but and, in turn, create a level of 3D complexity in an ecosystem through paleoecological studies are lacking for major portions of the unit. In secondary tiering on other organisms (Walker and Alberstadt, 1975; general, fossils are well preserved, including encrusting and predation Bottjer and Ausich, 1986, Peters and Bork, 1998; Schneider, 2003, traces that are direct evidence of paleoecological interactions. The 2009a). Encrusting organisms in a community increase its biodiversity nonpredatory boring traces on brachiopod shells from the Dundee and may additionally feed back into community biodiversity and Formation are described here for the first time, providing a rare biomass by attracting other encrusters. Fossil episkeletobionts have example of paleoecological interactions in a carbonate environment. even been suggested to be good indicators of primary productivity Episkeletobionts—organisms that adhere to the surface of a shell, levels in paleoecosystems (Lescinsky and Vermeij, 1995). Often, also known as encrusting organisms (Taylor and Wilson, 2002)—are brachiopods are the host of preference for studying encrustation in well known from the paleoecological literature. Less understood are the Paleozoic fossil record, usually because of the abundance of attached and encrusting organisms that bore into shell material, usually specimens and, in the case of many siliciclastic units, ease of removal considered to have parasitized live hosts and often found colonizing from the matrix. Indeed, because of the abundance of data collected about brachiopods and their encrusters, episkeletobiont ecological * Corresponding author. relationships are fairly well understood for the Paleozoic record.

Copyright g 2010, SEPM (Society for Sedimentary Geology) 0883-1351/10/0025-0196/$3.00 PALAIOS ENDOSKELETOBIONTS ON RHIPIDOMELLA 197

FIGURE 1—Study area. A) Regional geologic structures of Ohio and adjacent states. Black star symbol marks the location of Whitehouse Quarry. Inset illustration of the United States map indicates Ohio shaded in black. B) Stratigraphic section of Whitehouse Quarry. Numbers mark the units. Samples collected from units 10, 11, and 12 (adapted from Wright, 2006).

Brachiopod hosts are useful for investigating influences on such number of unsuccessful predation attempts, rather than the intensity of episkeletobiont preferences as media texture (Schneider and Webb, durophagous predation pressure (Alexander, 1981; Kowalewski et al., 2004; Rodland et al., 2004; Schneider and Leighton, 2007), size of host 1997; Alexander and Dietl, 2000; Leighton, 2003). Conversely, the lack (Ager, 1961; Kesling et al., 1980), antifouling strategies (Schneider and of repair scars does not indicate lack of predation pressure; rather, Leighton, 2007), and host switching during taxon loss across mass successful durophagous predation destroys the shell, leaving no record extinctions (Schneider and Webb, 2004). Although other taxa have been of predation (Vermeij, 1982). Hoffmeister et al. (2003) reported a utilized for similar investigations, brachiopods remain one of, if not the sample of the small-sized brachiopod Cardiarina cordata collected from most, well-understood hosts for Paleozoic episkeletobionts. a late Pennsylvanian limestone unit in Grapevine Canyon, New Endoskeletobionts have rarely been studied in Devonian brachiopods Mexico, that were frequently drilled (drilling intensity 5 32.7%)by of carbonate environments in North America. Brachiopods from the predators or parasites of unknown origin. They suggest that relatively Middle Pennsylvanian Naco Formation, central Arizona, display a wide high frequencies of drilling may be found on smaller bodied Paleozoic diversity of endoskeletobionts that colonized their hosts both during life animals relatively similar to the observed drilling frequency in the Late and after death (Sumrall, 1992; Lescinsky, 1997; Dyer and Elliott, 2003; Mesozoic and Cenozoic, perhaps indicating the presence of a distinct Irmis and Elliott, 2006). These endoskeletobiont traces on brachiopod small-bodied predator guild. hosts included ramifying networks of borings (Dyer and Elliott, 2003). Although the benefits of studying epi- and endoskeletobionts and The endoskeletobiont Chaetosalpinx sp. (class Polychaeta; order predation traces for understanding paleoecological interactions are Serpulimorpha) has been reported to have occurred within the skeletons great, such studies are rare for Devonian carbonate regimes, and of the tabulate coral Yavorskia sp. (Favositida, Cleistoporidae) from the lacking entirely for the Dundee Formation. In this paper, we present latest Famennian (‘‘Strunian’’) in the Etroeungt area (Northern France), the results of an intensive survey for synecological interactions within and their interaction with the host coral has been described as the Dundee Formation brachiopod fauna. commensalism (Tapanila, 2004). In the case of Chaetosalpinx, parasitism seems to be more probable (Zapalski 2004; Zapalski et al., 2008). GEOLOGICAL SETTING Tapanila (2005) described diversity in boring that occurs in various skeletal marine invertebrates, including tabulate and rugose corals, The study area within the Dundee Formation is located at White- calcareous sponges, bryozoans, brachiopods, and crinoids. house, Lucas County, Ohio, on the northwestern flank of the Findlay Predatory interactions are those in which the predator benefits by Arch, which was a topographic high separating and isolating the consuming all or part of the prey organism. The interaction is always Michigan Basin from the Appalachian Basin (Fig. 1A). Specimens for detrimental for the prey organism, even if it survives, because any this study were collected from the Whitehouse Quarry, which is east of damage incurred by the predator must be repaired. Such predation Whitehouse, Ohio, and was actively worked by the Whitehouse Stone traces as durophagous repair scars indicate not only the presence of a Company in the early twentieth century. The Dundee Formation, predator and the interaction of said predator with its prey organism, which is Eifelian in age (397.5 6 2.7 Ma to 391.8 6 2.7 Ma) (Gradstein but also trophic complexity in fossil ecosystems. Such data are, et al., 2004), is a predominantly carbonate unit deposited along the therefore, useful for understanding the paleoecology of an ancient southeastern margin of the Michigan Basin (Fig. 1A). The name system. Repair scars, however, represent failed attempts of the predator Dundee Limestone was first used for the rocks exposed in the to successfully kill and consume its prey; instead, the prey organism has abandoned Pulver Quarry in Dundee, Monroe County, Michigan survived and repaired its shell. This evidence, therefore, records the (Ehlers et al., 1951). 198 BOSE ET AL. PALAIOS

recorded in order to interpret aspects of the depositional environment of this unit relevant to the study. For consistency, the ventral valves of all brachiopod specimens collected were investigated for evidence of activity by episkeletobionts, endoskeletobionts, and predators. Each brachiopod was identified to genus level. Brachiopod specimens were examined under a stereomi- croscope using 403 magnification. Under 403 magnification, only Rhipidomella shells showed some evidence of biotic interaction (Figs. 3– 4). The ventral valves of all Rhipidomella were further examined under 1003 magnification. Those with evidence of borings were photo- graphed using a high-resolution digital camera attached to the microscope. Branching grooves, scars, and borehole traces on the external surface of Rhipidomella were observed under the scanning electron microscope (SEM) to determine possible qualitative differences in type and intensity of boring. Fourteen Rhipidomella specimens of comparable FIGURE 2—Trace fossils. A) T-shaped branching network of burrows in the Dundee Formation identified as Thalassinoides. B) Criss-cross pattern of the trace fossils in size (2.0–2.1 cm) were selected for SEM analysis. These specimens were the same bed of the Dundee Formation in units 10–12. Scale bar 4 cm. first dried in an oven at 80 uC for 12 hours; no additional coating was used. Under 30–2003 magnification, the trace types were determined, The paleoenvironment of the Dundee Formation was a shallow, measured, and photographed. Borehole traces (0.1–0.3 mm in tropical, high-energy shelf with intervals of decreased energy and diameter), and sinuous traces formed by an unknown network of occasional storm events. Most of the Dundee Formation was deposited borings (0.04–0.2 mm in diameter) were recorded. The specimens are below normal wave base but above storm wave base; there is evidence deposited at the Indiana University Paleontology Collections for that the Middle Devonian sea in this region was shallow, but may have further investigations. extended occasionally below storm wave base (Hansen, 1999). Where possible, endoskeletobiont traces were identified to the most The Dundee Formation in the Whitehouse Quarry studied herein precise taxonomic identification of the trace-makers. The shape, size, contains a rich faunal assemblage of brachiopods, corals, bryozoans, and position of these traces were noted. Diameters of boreholes and mollusks, rare crinoids, and rare tentaculitids originally described by dimensions of branching grooves were determined using digital Stauffer (1909), Bassett (1935), and Ehlers et al. (1951). photographs and image analysis software. The presence of new shell Beds sampled for this study included the fossiliferous units 10, 11, material partially filling in grooves and scars was considered as and part of unit 12 from Whitehouse Quarry. The lower unit 10 is a evidence of shell repair and its absence as evidence for the lack of shell packstone, 0.19 m thick, grading upward into the wackestone of unit repair. 11, about 0.07 m thick, transitioning into the nodular-bedded unit 12 grainstone, 0.06 m thick (Fig. 1B). These units were chosen for study Quantifying Epizoan Occurrences because of their high fossil abundance and diversity. These three fossiliferous units also contained the ichnofossil Following the methods previously established by Kesling et al. Thalassinoides (Fig. 2). These burrows either formed in softgrounds (1980), each valve of the 17 best-preserved Rhipidomella hosts was within the Cruziana ichnofacies, or in firmgrounds of the Glossifungites divided into six regions (Fig. 5). Area ratios were used to standardize ichnofacies (Ekdale et al., 1984). Syndepositional hardgrounds are each region of the shell to the others following this equation (Fig. 5): lacking in these units, and the intensity of burrowing suggests that the A ~ R seafloor remained unconsolidated during biotic activity. Presence of R , ð1Þ AT abundant intraclasts in the sampled units are the remnants of prior firmgrounds or of buried, early lithified sediments that were exhumed, where R is the area ratio, AR is the area of each region, and AT is the broken, and redistributed as clasts during high-energy events, total area. suggesting intermittent storm activity during sediment deposition. The frequency of endoskeletobiont activity in each region was Background sedimentation rates are considered herein to be slow: low recorded by counting individual colonies as one occurrence and then enough for soft-sediment burrowing networks to be maintained, but summing for all Rhipidomella hosts. For comparison with the actual not slow enough for hardground cementation. Thus, trace-fossil frequency of endobiosis, expected endobiosis for each region was associations indicate a shallow marine environment and slow sediment calculated by: deposition below fair weather wave base. The presence of intraclasts E~NRi, ð2Þ suggests deposition above storm wave base, with tempestite grains reworked into sediment by burrowing organisms. The sediments likely in which the expected number of endoskeletobiont traces (E) is were deposited in a well-oxygenated environment based on the calculated by multiplying the total number of endoskeletobiont traces moderate size (0.5–1.0 cm in diameter) of the burrows. (N) for all Rhipidomella specimens by the area ratio (R) for a given region on the Rhipidomella shell (i). Chi-square tests were performed for the total observed and expected endoskeletobionts of the six regions to MATERIALS AND METHODS test for endoskeletobiont preference for location on the Rhipidomella Sampling valve. Boring traces—straight and branching—posed a problem for these A total of 245 brachiopod specimens were collected in 72 limestone calculations because these specimens often crossed borders into slabs from fossiliferous units of the Dundee Formation. Brachiopod adjacent regions. For these specimens, frequency of colonization of shells were collected throughout the thickness of each sampled bed, an endoskeletobiont in an observed region, which also extended into although most were recovered from the packstone of unit 10 and the another region, was divided by the total number of regions it inhabited. lower part of the unit 12 grainstone. In addition, the taphonomic, For example, branching grooves that were observed in all the three sedimentological, and ichnological character of the formation was also anterior regions were counted as 1/3 for each region. PALAIOS ENDOSKELETOBIONTS ON RHIPIDOMELLA 199

FIGURE 3—Trace types on Rhipidomella shells (Endoskeletobiont type A). Inset illustrations indicate view of endoskeletobiont traces relative to the entire valve. A) (IU#19011) Y-shaped branching grooves (BG) close to the hinge in the posteromedial region (103). Black arrow points to BG perpendicular to the direction of rib direction.B) (IU#19012-1) Deep BG close to the hinge of the shell in the posteromedial region (163). Black arrow points to BG perpendicular to the direction of rib direction.C) (IU#19012-2) BG along the commissure of the shell covering the antero–left lateral, anteromedial, and antero–right lateral regions (203). Dashed square indicates the healing region of the bifurcating grooves. D) (IU#19012-2) Higher magnification of the dashed square region in C showing the bifurcating BG (613). E) (IU#19012-2) Healing of the bifurcating grooves along the anterior margin magnified in SEM image (803). F) (IU#19012-3) Deep wide BG in a partially recrystallized shell, covering the entire posterior and anterior regions of the shell except the antero–right lateral margin (83). Dashed square points to the BG perpendicular to the direction of rib direction. G) (IU#19012-3) SEM image magnifies the direction of the BG perpendicular to the rib in the postero–left lateral region (403). H) (IU#19014) Deep, wide, BGs close to the hinge along the posteromedial region (163). Dashed square represents some grooves perpendicular to rib direction similar to Figure 3D. I) (IU#19012-3) SEM figure magnifies the cross- cutting ribs in the posteromedial region (383). J) (IU#19015) Distinct BG along the anteromedial region of the shell bifurcating toward the commissure. White arrow shows the point where the branching groove ends, probably indicating signs of healing (83). K) (IU#19015) Very deep, BG well captured in SEM (2023). L) (IU#19016) Clear BGs all over the shell surface, branching out from the hinge toward the shell margin and along the lateral sides (83). SEM figure magnifies the grooves in M) (IU#19014) posteromedial and postero–right lateral region (403), N) (IU#19014) anteromedial (503) and O) (IU#19012-3) antero–right lateral region (803). Note: Scale bar 5 mm in views A–C, F, H–J, L; scale bar 0.5 mm in views D–E, G, I, K, M–O.

RESULTS rhynchonellide shells were recrystallized and lacked surface detail, whereas others were abraded. Many stropheodontides occurred as Frequency of Traces single valves, evident from preserved cardinal processes. Atrypides could not be identified to genus because of the similarity between Out of 245 brachiopod specimens counted from the samples, 163 genera and poor preservation of key identifying details. Most were identified as Strophodonta,48asRhipidomella, 17 as unidentified Rhipidomella shells were well preserved, containing all external features. rhynchonellids, 9 as Atrypa, and 8 as Mucrospirifer (Table 1). Of all of A few Rhipidomella shells were recrystallized, and others show evidence the brachiopod taxa encountered, only Rhipidomella bore endoskele- of a little abrasion and fragmentation, including exposure of punctae. tobiont traces and predation scars. Nineteen specimens out of 48 Microscopic examination of nonrecrystallized Rhipidomella specimens Rhipidomella, that is, 39.6 percent of the shells, bear evidence of reveals endoskeletobiont traces on hosts in contrast to other endoskeletobionts on their examined ventral valves (Table 2). SEM brachiopod taxa; even the large nonrecrystallized stropheodontids bore analysis on fourteen specimens closely examined the depth and no evidence of endobiosis. direction of sinuous traces and gave evidence for how these cross cut the Rhipidomella ribs (Figs. 3C–D, F–G). Some shells had branching Types and Nature of Traces on Rhipidomella Shells grooves that could be produced by borers: branching endoskeletobiont type A (Figs. 3A–O). Some shells bore scars with disrupted growth lines Endoskeletobiont Type A (Branching Grooves).—(13 specimens). (Figs. 4A–E) and one had numerous, shallow, large boreholes with Endoskeletobiont traces of curved, deep or shallow, narrow or wide, elongated straight grooves: straight endoskeletobiont type B (Figs. 4F– bifurcating grooves range from 0.01 to 0.20 mm in diameter on the G). external surface of the ventral valve. Traces of Y-shaped, wide, branching grooves (0.03 mm deep, 0.08 mm in diameter) were observed Preservation of Shells near the hinge on some Rhipidomella hosts (Figs. 3A–B). On one specimen, wide, branching groove traces were parallel to the shell Specimens of Strophodonta, Mucrospirifer, atrypides, and unidenti- margin and showed signs of active repair by the brachiopod (Figs. 3C– fied rhynchonellides were moderately well preserved, meaning largely E), whereas on other specimens these traces covered much of the shell uncrushed and unbroken with little or no abrasion and minimal surface, originating at the hinge and branching outward toward the postdepositional distortion. Some Strophodonta, Mucrospirifer, and commissure (Figs. 3F–G, L–O). Another specimen also exhibited deep, 200 BOSE ET AL. PALAIOS

FIGURE 4—Trace types on Rhipidomella shells (Endoskeletobiont type B 5 straight grooves, type C 5 boreholes, and type D 5 scars). A) (IU#19017) Two deep scars, one in the posteromedial region close to the hinge, the other on the antero–right lateral region marked in dashed square; punctae exposed near margin (83). Black circle outlines the scar showing evidence of repair. Inset illustrates the scar of the antero–right lateral region in SEM (1013). B) (IU#19018) Two parallel deep scars (in dashed square) along the margin of the antero–left lateral region (12.53) similar to the scars on Paraspirifer collected from Silica (Sparks et al., 1980, pl. 9, fig. 4). White arrows indicate the evidence for shell repair. C) (IU#19018) SEM illustrates the scars at 703 magnification. D) (IU#19018) Deep scar on the right lateral margin (within white dashed square marked as a black line), compressing one side of the shell surface with respect to the other side (12.53). E) (IU#19018) Magnified cleft is illustrated in SEM (533). F) (IU#19019) Central straight elongated grooves branching out from the hinge with shallow larger boreholes along the postero–left lateral, postero- and anteromedial regions of the shell (83). One center borehole marked by a white line. G) (IU#19019) SEM illustrates the cylindrical (longer than width) shallow boreholes along the postero–left lateral region (713). H) (IU#19020) Numerous branching and V-shaped grooves on the shell surface and a large scar along the commissure (83). Note: Scale bar 5 mm in views A, B, D, F, H; scale bar 0.5 mm in views C, E, G. wide, branching groove traces only near the brachiopod hinge toward the hinge of some Rhipidomella shells, crosscutting the ribs, and (Figs. 3H–I). One partially recrystallized specimen had a deep, wide, had no evidence of shell repair. slightly branching groove located centrally that shows signs of shell Endoskeletobiont Type B (Straight Grooves).—(1 specimen). Elon- repair along its margins (Figs. 3J–K). Traces of deep, but much gated straight grooves ranging from 0.9 to 1.2 mm in diameter were narrower (0.01 mm), dendritic grooves extended from the commissure observed in one Rhipidomella valve in the central portion of the shell, extending toward the hinge (Fig. 4F). Endoskeletobiont Type C.—(1 specimen). Circular borehole traces, ranging from 0.16 to 0.28 mm in diameter on the external valve surface, were found positioned between the ribs of Rhipidomella specimens. One host contained ten large circular holes, 0.16–0.28 mm in diameter, that were located centrally, with grooves terminating in, or extending from, holes. This aggregation of boreholes covered over half of the surface area of the valve (Figs. 4F–G). Durophagous Repair Scars.—(4 specimens). Crushing scars indicate damage caused to the brachiopod while alive by either abiotic (mechanical breakage) or biotic factors (a predator or parasite) that must be repaired, affecting the growth of the shell and leading to irregular, deformed growth lines. Two deep tapered scars were observed in one specimen; one located in the central region and the other in the lower right lateral region (Fig. 4A). In this specimen, there is a clear edge to the scar that is not parallel to the growth lines, and the associated ribs are discontinuous and deflected, indicating a repair scar. Another Rhipidomella specimen bore two deep parallel and geometric tapered scars along the lower left lateral margin (Figs. 4B–C). The same host specimen contains a deeply cleaved scar, almost parallel to the shell

TABLE 1—Taxa and abundance of sampled brachiopods.

Brachiopod genus Number of shells Percentage (%)

Strophodonta 163 66.53 Rhipidomella 48 19.59 FIGURE 5—Rhipidomella valve divided into six regions for endoskeletobiont Unidentified rhynchonellids 17 6.93 frequency study; PLL 5 postero–left lateral, PM 5 posteromedial, PRL 5 Atrypa 9 3.67 postero–right lateral, ALL 5 antero–left lateral, AM 5 anteromedial, and ARL 5 Mucrospirifer 8 3.26 antero–right lateral. Numbers represent the area ratios of each grid across the Total 245 100.00 Rhipidomella host valve. Scale bar 1 mm. PALAIOS ENDOSKELETOBIONTS ON RHIPIDOMELLA 201

TABLE 2—Morphology and abundance of biological traces on Rhipidomella shells. Note that only 4 specimens show live-live interactions for endoskeletobiont type A and 2 specimens for durophagous scars. Overall 19 out of 48 potential Rhipidomella hosts (39.6%) show these endoskeletobiont and predation traces.

Types of biological traces Number of shells Percent of traces (%) Percent of shells (%)

Branching grooves (Endoskeletobiont type A) 13 (4 live interactions) 68.42 27.08 Straight grooves (Endoskeletobiont type B) 1 5.26 2.08 Large boreholes (Endoskeletobiont type C) 1 5.26 2.08 Durophagous scars 4 (2 live interactions) 21.05 8.33 No traces 29 60.40 Total shells with traces 19 100.00 Total shells 48 100.00 costae along the lower right lateral margin, with one side of the shell rate (chi-square; p 5 0.008). Conversely, the opposite region, postero– margin compressed (Figs. 4D–E). Another specimen bears a central left lateral, was bored at a frequency higher than expected (chi-square, p deep scar, containing punctures, near the commissure of one specimen. 5 0.017). The remaining regions do not show any significant difference A large scar near the commissure of another specimen appears abraded, between expected and observed endoskeletobiont frequency (Table 4, with the shell material fragmenting in the scar area (Fig. 4H). Fig. 7). Overlapping occurrences of endoskeletobiont type B and type C— two types of endoskeletobiont borings, or predation plus environmental DISCUSSION impedence—could result in complex traces on the shell. One specimen shows evidence of continuous, shallow, large, perpendicular holes, Despite the highly diverse brachiopod community in the Dundee ranging in size from 0.1 to 1.0 mm in diameter along with centrally Formation and higher relative abundance of stropheodontides as located elongated straight grooves extending toward the hinge compared to other brachiopod taxa, only the smallest brachiopod (Fig. 4F). Another specimen had a crushing scar, ,6 mm wide, with genus Rhipidomella (diameter roughly 2.0 6 0.1 cm) of the orthide several V-shaped branching grooves along the valve surface (Fig. 4H). group retains some evidence of endoskeletobionts and furthermore, only when viewed at very high magnification. Concavo-convex stropheodontides generally are thought to be oriented with their Location of Traces concave valve upright during life (e.g., Rudwick, 1970; Richards, 1972; The frequency of biotic interactions varies among the six regions on however, see Lescinsky, 1995 for an alternate hypothesis). All of the the ventral valves of the Rhipidomella hosts (Fig. 6). The posteromedial stropheodontids were oriented with their ventral valves up, suggesting region contains the most frequent occurrence of endoskeletobiont type overturning. The somewhat larger stropheodontids (3.0–4.0 cm) from A (branching grooves) traces, although the postero–left lateral and the locality bore no evidence of any biologic activity. Of all of the anteromedial areas also have a high abundance of these traces. brachiopod taxa encountered, only Rhipidomella bore endoskeletobiont Durophagous scars are most frequent in the antero–left lateral region. traces and predation scars. Due to the uniform size of all Rhipidomella The postero–left lateral and anteromedial regions have the highest valves investigated (2.0 6 0.1 cm), however, it was not possible to frequency of boreholes—endoskeletobiont type C—in the single bored discern a relationship between valve size and degree of shell damage specimen. within the genus. Combining all endoskeletobiont data, the observed frequency of endobiosis across all regions of the Rhipidomella shell is significantly Is There Any Taphonomic Influence on Brachiopods? different than expected if the endoskeletobionts randomly bored any While convincing evidence for endoskeletobiont activity has been portion of the shell (chi-square; p , 0.01) (Table 3, Fig. 7). Specifically, documented for Dundee Formation Rhipidomella specimens, no the postero–right lateral region was bored at a lower rate than expected evidence for episkeletobiont activity has been found. Two possible explanations for this discrepancy exist. Episkeletobionts were either not preserved or were nonexistent on the Rhipidomella specimens in this study. Given that the sedimentology of these beds suggests a high- energy environment and likely storm events, it is possible that calcified episkeletobionts were present, but lost through taphonomic processes.

TABLE 3—Sum of the observed and expected number of endoskeletobiont and predation trace occurrences for three types of endoskeletobionts (type A 5 branching grooves, type B 5 straight grooves, and type C 5 boreholes) and durophagous scars across six shell regions. The six grids are as follows: PLL 5 postero–left lateral region; PM 5 posteromedial region; PRL 5 postero–right lateral region; ALL 5 antero–left lateral region; AM 5 anteromedial region; ARL 5 antero–right lateral region.

Endoskeletobiont and predation activity Regions Observed Expected

Postero–left lateral PLL 27.5 24.735 Posteromedial PM 32.5 24.225 FIGURE 6—Total standardized frequency of endoskeletobiont activity across each Postero–right lateral PRL 13 24.735 region for 17 Rhipidomella hosts. (Note: Standardized frequency 5 Frequency of Antero-left lateral ALL 21.5 13.26 colonized endoskeletobionts on host Rhipidomella) The six grids are as follows: PLL Anteromedial AM 25 26.775 5 postero–left lateral region; PM 5 posteromedial region; PRL 5 postero–right Antero–right lateral ARL 8 13.26 lateral region; ALL 5 antero–left lateral region; AM 5 anteromedial region; and SUM 127.5 126.99 ARL 5 antero–right lateral region. 202 BOSE ET AL. PALAIOS

TABLE 4—Results of chi-square test of observed versus expected endoskeletobiont and predation trace occurrences. A p-value , 0.05 indicates either more or less biological activity in that shell region than expected, as indicated.

p values Observed is — than expected

PLL vs. sum of other areas 0.549 PM vs. sum of other areas 0.219 PRL vs. sum of other areas 0.008 LESS ALL vs. sum of other areas 0.017 MORE AM vs. sum of other areas 0.17 ARL vs. sum of other areas 0.123

on large and small brachiopods, this sort of taphonomic study is beyond the scope of this paper. FIGURE 7—Observed versus expected endoskeletobiont activity across the six Unit 11 was a wackestone, representing a lower energy environment regions of Rhipidomella hosts. Observed values are the actual frequency of than the bounding lower and upper beds. Likely, brachiopod specimens encrustation for each region of the shell; expected values are calculated as described underwent fewer episodes of transport than in preceding or subsequent in the text. PLL 5 postero–left lateral region; PM 5 posteromedial region; PRL 5 environments. Fossils in unit 11, therefore, were likely autochthonous postero–right lateral region; ALL 5 antero–left lateral region; AM 5 anteromedial rather than transported into the locality. Brachiopods in the higher region; and ARL 5 antero–right lateral region. energy environments of units 10 and 12, however, were very similar in diversity to those preserved in the wackestone of unit 11. These Packstones and grainstones, common in the Dundee Formation of the diversity similarities between the sampled lithological facies suggest that Whitehouse Quarry, represent high-energy environments; in this study, the brachiopods of units 10 and 12 underwent only local transport or units 10 and 12—from which the majority of specimens came—were a reworking, and that the brachiopod biofacies were essentially the same packstone and a nodular-bedded, intraclast-bearing grainstone, respec- from unit 10 through unit 12. tively. Fragmented and abraded shells suggest that some of the horizons Exposure history can control the surface area available for coloniza- from which the fossils were collected were storm beds; burrows mixing tion and the temporal window in which encrustation may occur, so this the fossils occurred after storm events. These data would further factor should be taken into account (Best and Kidwell, 2000; Rodland et support the loss of encrusting organisms to abrasion, but other reasons al., 2004). Higher levels of damage observed on some subsets of need to be evaluated for reporting episkeletobiont loss, e.g., shells in Rhipidomella valves could be a consequence of greater exposure time and motion in the seafloor, prior to drawing this conclusion. such postmortem degradation events as storm transport, reworking, or Local shifting of shells on the seafloor can affect encrustation. postburial diagenesis. Particular types or higher intensities of endoske- Encrustation rates were very low on modern mollusk shells derived letobiont activity on some highly abraded Rhipidomella valves could be a from the carbonate reef and lagoon systems in the northeastern consequence of relatively higher postmortem residence time of these Caribbean and transported into nearby, high-energy beach environ- shells on the seafloor as compared to the other brachiopod taxa. ments, likely because of shells being in constant motion (Parsons- All brachiopod taxa occurred in all three units. The presence of Hubbard, 2005). In addition to constant motion, which results in bioturbation in the sediments, however, increases the likelihood that the abrasion, a shell that does not rest cannot attract episkeletobionts; a entire brachiopod assemblage is time averaged to some extent and that moving seafloor is difficult to encrust (Parsons-Hubbard, 2005). high-resolution facies changes are lost. We cannot rule out the possibility McKinney (1996) demonstrated the rapidity with which epizoans were that Rhipidomella specimens that appear to be contemporaneous with removed from shells during experimental abrasion; natural abrasion other brachiopods mixed from other time-horizons or bioturbated, and during storm events and in other high-energy environments would hence lost, microfacies, because of the small size of Rhipidomella produce similar results. Furthermore, one of us (Schneider) noted that, compared to other taxa and the high degree of bioturbation. among Terebratalia and Laqueus brachiopods dredged from Puget Of all brachiopod taxa sampled, only Rhipidomella specimens bear Sound, Washington, only live specimens bore episkeletobionts; all dead signs of endoskeletobionts and durophagous predation scars regardless specimens from both rocky and muddy environments were devoid of of preservation. The lack of observed episkeletobionts and endoskele- skeletal and soft-bodied encrusters. Rodland et al. (2006), however, tobionts in all the host brachiopods from the Dundee Formation could have shown that taphonomic processes need not erase all evidence of be due to abrasion, but this is unlikely. Endoskeletobionts leave deep biotic interaction through time, a fact evident from the rich traces within the shell material that would readily be preserved despite endoskeletobiont activity preserved on Rhipidomella in our study. abrasion of the shell surface, particularly on hosts with ribs or other All the brachiopods from this study appear to have undergone type external ornament capable of providing shelter. Furthermore, dur- III shell alteration (Emig, 1990), where the large anterior part of the ophagous predation scars, which would be preserved even in valves is frequently mechanically fragmented into small pieces. recrystallized or abraded shells, are absent on larger host brachiopods. Dissolution of calcium carbonate or cryptocrystallization, according Whether the larger brachiopods and Rhipidomella existed contempo- to local environmental conditions, likely were other processes that raneously or were redistributed and mixed from time averaging is affected shell layers (Emig, 1990). These processes could readily erode unknown; therefore, either (1) Rhipidomella was encrusted in commu- any trace of episkeletobionts; however, endoskeletobionts and preda- nities containing only the one brachiopod taxon and then later time- tion traces are preserved on Rhipidomella and, therefore, should have averaged with other communities containing large brachiopods, or (2) been preserved, if present, on larger taxa affected by the same endoskeletobionts selectively colonized only Rhipidomella shells in taphonomic processes resulting in similar shell-surface alteration. In multitaxa brachiopod communities. other words, traces of endoskeletobionts and durophagous predation scars should be found on the larger brachiopod taxa as well as Identification of Tracemakers Rhipidomella if such traces were originally present, as all brachiopod taxa were equally affected by shell breakage and fine-scale cryptocrys- Many of the endoskeletobiont traces can be attributed to uncalcified, tallization. Although we cannot rule out differential taphonomic effects boring bryozoans. Traces of deep, wide branching grooves on PALAIOS ENDOSKELETOBIONTS ON RHIPIDOMELLA 203

Rhipidomella resemble the traces made by ctenostome bryozoans on late anterolateral region (Fig. 4A). Another Rhipidomella specimen with Eifelian crinoid columnals collected from Devonian strata in the Skaly two parallel scars on the lower left anterolateral margin (Fig. 4B) shows Beds in the Holy Cross Mountains, Poland (Gluchowski, 2005). The evidence of a crushing attempt by a predator, as suggested by distortion branching traces on Rhipidomella in this study resemble the grooves of in the ribbing and intense, and likely rapid, repair in the area of the scar an Ordovician through recent trace made by a ctenostome bryozoan (L. Leighton, personal communication, 2008). SEM imaging at a higher with a similar diameter, 0.15–0.40 mm. Moreover, ctenostome magnification (703) shows the depth and intensity of the scarred region bryozoan zooids form a characteristic network of delicate, uniserial, (Figs. 4C–E), and Fig. 4B shows repair of the scar in the next lower branching lines and are uncalcified forms boring into calcareous media successive layer as compared to the deep scar in the upper layer. (McKinney and Jackson, 1989; Wood and Marsh, 1996), traits seen in Other specimens contain anterior and lateral scars that resemble the morphology of the branching grooves on Rhipidomella from the those attributed to shell-crushing sharks in Chesterian brachiopods Dundee Formation. Botquelen and Mayoral (2005) have reported from the Confusion Range of west-central Utah, with scars positioned irregular, narrow, sinuous branching bioerosion traces made by tunnels anteriorly or laterally (Figs. 4A–B; Alexander, 1981). Nautiloids also of ctenostomate bryozoans on Lower Devonian internal molds of were efficient predators, equipped with crushing beaks and were major brachiopods from the Rade De Brest, Armorican Massif, France. These predators from the Ordovician through the Devonian (Alexander, are oriented parallel to the host medium and range from 10 to 100 mm 1986). One orthoconic nautiloid specimen was noted from the sampled (0.01–0.1 mm) in diameter. Both the diameter and shape of the traces units, which may have contributed to local predator activity. Other found in the Dundee Formation brachiopods vary within this range, such durophages as placoderm and chondrichthyan fishes and with only a few traces wider than the range for boring ctenostomate phyllocarid and eumalacostracan arthropods, however, were also active bryozoans from France. The branching endoskeletobiont type A traces predators during the deposition of the Dundee Formation carbonates on the Dundee Formation Rhipidomella likely were the product of (Signor and Brett, 1984; Leighton, 1999). The Rhipidomella predation ctenostome bryozoans. scars could have been produced by any one of these shell-crushing Boreholes in shelly benthos are often made by parasites or by predators. Although the scars on Rhipidomella described above appear predators of live hosts, or organisms boring into dead shells. to be characteristic of predator activity and subsequent damage repair, Nonsinuous, perpendicular borings in Paleozoic brachiopods have repair of abiotic breakage during the life of the brachiopod cannot be been attributed to many organisms. The morphologies of these multiple ruled out (Sarycheva, 1949; Alexander, 1981). boreholes in Rhipidomella lacked the tapering at the margins with Scars in brachiopod shells can be produced by phenomena other than concentric or aconcentric openings caused by stratigraphically younger predators; mechanical damage and impedance by objects (e.g., other predatory gastropods studied by Arua and Hoque (1989). organisms) also can deflect brachiopod growth (Ferguson, 1962; Most nonpredatory borers excavate multiple holes (e.g., sponges, Alexander, 1981). Other shell disruptions and scars have been Tapanila, 2006; polychaetes, Kern, 1979; worms, Cameron, 1969; Smith interpreted as being the result of parasites (e.g., Cornulites, Hoare et al., 1985). Multiple borings on the single Rhipidomella specimen and Steller, 1967), but the extent and morphology of injuries present on (Fig. 4F) could be attributed to Paleozoic worms, which ranged from brachiopods of this study suggest that these scars were the result of 0.05 to 1 mm in diameter, because other evidence for worms exists in durophagous predators, not parasites. One specimen that bears a the form of worm tubes (Coleolus sp.) from the fossiliferous units of the predation scar also has a cleft-like indentation along the commissure, a Dundee Formation (Wright, 2006). Borings attributed to worms are feature of growth deflection that might not be attributed to a predator roughly cylindrical, generally longer than their width, and usually (Figs. 4D–E). Cleft-like damage was common in such Late Ordovician oblique to the host’s surface (Cameron, 1969; Smith et al., 1985), very brachiopods as Rafinesquina from the Cincinnatian Series of the tri- similar in morphology to those found on the Rhipidomella of this study state area of Indiana-Kentucky-Ohio (Alexander, 1986, fig. 5.1, p. 276). from the Dundee Formation (Figs. 4F–G). Thus, the endoskeletobiont This Rhipidomella specimen may have experienced impedance to type B traces (straight grooves) are identified as worm borings. growth along the margin at the area of deflection, although whether On the same specimen with the multiple borings, the straight U- the impedance was another organism or an abiotic object cannot be shaped borings are similar in morphology to Caulostrepsis traces discerned. attributed to the polychaete Polydora (Rodland et al., 2006; Rodrigues et al., 2008). The U-shaped boring in this specimen, therefore, were Are the Endoskeletobiont and Durophagous Predation likely caused by a polychaete worm. Traces Random? The identification of the organism that caused the large boreholes in the Dundee Formation Rhipidomella is uncertain, except that a Trace occurrence varies among the six regions sampled on the ventral predator likely did not cause the holes, as they do not meet the criteria valves of the Rhipidomella hosts (Fig. 6). Durophagous predation scars for predatory drilling (Carriker and Yochelson, 1968). Borings are most frequent in the antero–left lateral region, suggesting a produced by drilling predators are recognizable in that they have a preferred attack scheme by an unknown predator, an example of a distinct morphology (e.g., type A or type B holes of Ausich and frequently failed attack direction, or a repeated mishandling orientation Gurrola, 1979), they often are singular, circular, complete drills by the predator. perpendicular to the shell (Carriker and Yochelson, 1968), and they Ctenostome bryozoans most heavily bored the posteromedial region typically occur in such optimal areas as the region of the shell of the valve with branching grooves, although the postero–left lateral protecting the muscle field versus the area that covers the mantle cavity and anteromedial also have a high frequency of these traces (Leighton, 2001; Kelley and Hansen, 2003). Furthermore, given that the (endoskeletobiont type A; Fig. 6). The postero–left lateral and borings show no sign of repair or growth response to parasitism, these anteromedial regions have the highest frequency of straight grooves borings likely caused, or occurred after, the death of the brachiopod, and boreholes (endoskeletobiont type B and type C) in the single bored such that the host was unable to initiate repairs. specimen. These location preferences of the endoskeletobionts could Predation scars resulted from damage by an attacking durophagous imply a preference for settling and growing near their hosts’ predator while the Rhipidomella brachiopods were alive; if the posterolateral inhalant currents. Posteromedial, postero–left lateral, brachiopod survived, it repaired the damage by adding new shell and anteromedial regions that show higher frequency of endoskeleto- material, resulting in a characteristic pattern of deflected growth lines biont traces, suggest that bryozoans were utilizing both the hosts’ (Leighton, 2001) (Figs. 4A–C). One specimen bears two nonlethal inhalant and exhalant currents (Figs. 3C, E, G–H, M). Thus, these predation scars, one located medially and the other on the right endoskeletobiont traces are not random and likely the result of a live 204 BOSE ET AL. PALAIOS endoskeletobiont-host Rhipidomella interaction. This nonrandom predation. Predatory relationships, always detrimental to the prey, distribution of borings on Rhipidomella host could possibly be a real, are recognized by distinctive repair scars (failed predatory attempts) biological signal with the antero–left lateral region having greater and drillholes (successful predatory attempts). Episkeletobiotic and exposure to colonization by endoskeletobionts, possibly due to the life endoskeletobiotic relationships can be mutualistic, commensal, or orientation of their hosts relative to water current direction, similar to parasitic (see review in Taylor and Wilson, 2003). the distribution of episkeletobionts on Paraspirifer brachiopods from Endoskeletobiont Type A (Branching Grooves).—Branching grooves the Silica Shale (Kesling et al., 1980). As there was no discernable observed in Rhipidomella shells cut across ribs in repetitive patterns, difference in frequency of endosymbiosis on the anterior or posterior suggesting that an organism actively bored through the rib (Figs. 3A– regions of the shell, it is assumed that settling larvae did not prefer one O). One specimen bore a deep, straight groove produced by a region over the other, preferring only the left side of the shell surface. ctenostome bryozoan, branching near and deflecting toward the commissure (Fig. 3F). Shell repair is evident in some of these borings, Is Endoskeletobiont Activity Pre- or Postmortem? supporting a relationship between a live endoskeletobiont and a live host, at least during a portion of the endoskeletobiont’s lifespan. It is In most cases, direct evidence of live episkeletobiont–host relation- possible that some of the ctenostome colonies creating these branching ships is rare. In the present study, a live host–live endoskeletobiont grooves may have benefitted from host-generated currents by settling relationship can be inferred from evidence of shell repair in a few near commissures as larvae (Figs. 3E, J–K) or by concentrating in Rhipidomella specimens and the location of these endoskeletobionts postero–left lateral and anteromedial regions (Figs. 3C, E, G). Other with respect to host inhalant currents (Figs. 3A–J). Four Rhipidomella studies have shown that borers located close to the brachiopod’s specimens show probable evidence of healing of endoskeletobiont (type commissure are known to have taken advantage of the increased water A) traces along the anterior commissure (Figs. 3A–J). flow created by the host’s inhalant current system to maximize feeding In several instances (Figs. 3K, M–O), it is difficult to determine efficiency (Pickerill 1976; Daley, 2008). whether endoskeletobiosis occurred on a live or dead Rhipidomella host. The relationship between these boring ctenostome bryozoans and One host specimen bore a series of branching grooves radiating from the their Rhipidomella hosts is considered to be parasitic. Feeding from the hinge toward the commissure (Fig. 3L). These traces covered the entire exhalant current of the host would cause no detriment to the external valve surface with no evidence of utilization of host inhalant or brachiopod, and consequences of utilizing the host’s inhalant current exhalant current, and no evidence of shell repair. Given the nature of are undetermined. Boring into and, therefore, destroying shell material these traces when compared to those considered parasitic, it is possible was harmful to the living host. Given that some of the host that this ctenostome bryozoan colony encrusted a dead brachiopod, but Rhipidomella brachiopods exhibit repair attempts to these borings, it whether the host was originally alive or dead at the time of settlement of is evident that these borings were not tolerated by the brachiopod. the metamorphosing larva cannot be determined precisely. Endoskeletobiont Type B (Straight Grooves).—One Rhipidomella Another Rhipidomella specimen bore numerous branching grooves specimen bears wide, straight grooves that end in large boreholes, originating from the commissure and progressing toward the hinge. In originating within the central region and progressing hingeward this case, the larva clearly settled near the commissure, but the colony (Fig. 4F). Close to the hinge, the groove bifurcates, becoming a boring expanded hingeward, rather than following the commissure for best within the shell that continues until it truncates at the hinge. Unlike advantage of brachiopod-generated currents. Additional groovelike other groovelike borings, an enigmatic wormlike organism likely borings along the central region of the same host indicate additional created these types of borings, perhaps similar to those attributed to bryozoan activity in these areas, away from the commissure and Devonian polychaete worms (Cameron, 1969). This interpretation is beneficial feeding currents (Fig. 3F). In another specimen, the cteno- further supported by a recent study by Rodrigues et al. (2008) who have stome borings extend from the commissure and lateral margins and shown that live polychaetes resided inside Caulostrepsis borings in live converge toward the hinge (Fig. 3G). By not following the commissure brachiopods. The straight U-shaped borings present on the same and instead deflecting away from the commissure, this mature bryozoan specimen of Rhipidomella are similar in morphology to these colony did not obviously utilize host inhalant and exhalant currents. Caulostrepsis traces attributed to the polychaete Polydora (Rodrigues In the Devonian episkeletobiont fossil record, auloporids and et al., 2008). Endoskeletobiosis may have occurred during the life of the cornulitids frequently display preferential growth along or toward the Rhipidomella, based on the location of the traces. It is more likely, commissure, particularly on alate spiriferides and large atrypides, in order however, that the brachiopod was dead at the time of boring, suggested to take advantage of feeding and respiration currents actively generated by the extent of the boring within the shell and lack of repair to the by the host’s lophophore (e.g., Ager, 1961; Hoare and Steller, 1967). Such damaged valve. other Devonian episkeletobiotic organisms as bryozoans, hederellids, and Endoskeletobiont Type C (Large Boreholes).—Boring is accom- spirorbids do not consistently exhibit preference for the commissural area plished by secretion of acids or mechanical rasping (Taylor and Wilson, or host-generated inhalant and exhalant currents. In the current study, 2003). In some groups (e.g., clionid sponges, ctenostome bryozoans), lack of preference for commissure-oriented or commissure-parallel the borer remains stationary within this hole, such that the external growth of the entire colony, therefore, does not indicate either live or shape of the organism is maintained in the shape of the hole and, as dead status of the host, but rather implies a nondependence of the mature such, is treated as a body fossil (Pohowsky, 1978). ctenostome colony on any actively host-generated feeding and respiration In the single specimen with multiple, nonpredatory bore holes, the currents. Thus, live or dead status of some Rhipidomella hosts, anteromedial and postero–left lateral regions were most frequently particularly those with no evidence of repair of ctenostome borings, bored (Fig. 6). Since there was only one specimen with bore holes, it is cannot be readily discerned. There is some suggestion, however, of impossible to determine if there was stereotypy for boring position. It is preferential settlement of ctenostome larvae near the commissure and also difficult to conclude any potential cause for these regions being potential expansion of the colony away from the commissure after the bored. The unrepaired nature of the holes indicates boring either of a host’s death, but instances are too few for broad extrapolation. live host, just before its death, or on a dead host, suggesting a postmortem domicile or feeding trace (Fig. 4F). Endoskeletobiont and Predatory Interactions with Rhipidomella Durophagous Predation Scars.—Repair scars and drill holes are common in Devonian brachiopods, such as frequently drilled brachio- In the fossil record, relationships between fossil organisms can pods from the Ludlowville and Moscow Formations of New York, sometimes be recognized, especially in the case of epibiosis and including several specimens that showed signs of repair (Smith et al., PALAIOS ENDOSKELETOBIONTS ON RHIPIDOMELLA 205

1985). In another example, several taxa of brachiopods from the Silica 2. Conversely, it is possible that predators of large brachiopods were Formation, which overlies the Dundee Formation, also were the prey of more capable than the smaller predators of Rhipidomella, providing the crushing and drilling predators (Alexander, 1986; Leighton, 2003). It is Rhipidomella more opportunities to survive a predatory attempt. interesting to note, however, that modern rhynchonelliform brachio- 3. In the case of epibiosis, punctate Rhipidomella is likely the pods are rarely attacked by predators due to their unpalatability while preferred host over other brachiopods. drilling rates for coexisting bivalves in the same locality are significantly 4. Burrowing by Thalassinoides-producing organisms likely pro- higher (Thayer and Allmon, 1990; D.L. Rodland, personal communi- duced a time-averaged record of the community and obscured cation, 2009). microfacies favoring Rhipidomella over other brachiopods, thus, biasing Biconvex brachiopods were more likely to explode when crushed the sample toward a seemingly preferred Rhipidomella host and more than to suffer breakage that could easily be repaired; the fossil record frequent predation attempt survivor. for predatory scars on brachiopods is, thus, generally higher in concavo-convex brachiopods than most biconvex brachiopods, includ- One other factor should be noted in the encrusting and predatory ing orthides (Alexander, 1986). In addition to potential explosion of the interactions with Rhipidomella, and that is the potential epibiotic nature shell, apparent predation frequency on orthide brachiopods may have of Rhipidomella itself. It was a small, pedunculate brachiopod, and an been further reduced from actual, higher predation pressure. Predation obligate attacher to other media. Therefore, Rhipidomella specimens frequencies on such orthides as those of Schizophoria of the Silica may be episkeletobionts themselves, secondarily tiering themselves Formation may appear lower because predators may have had easier higher into the water column on larger brachiopod shells themselves or access through an open delthyrium in the orthide, thereby bypassing the attached to intraclasts. Modern, heavily encrusted Terebratalia and protective shell and dispensing with the need for energetically and Laqueus brachiopods in mixed muddy and rocky and shelly environ- temporally costly drilling (Leighton, 2002). In a study of brachiopods ments of benthic Puget Sound frequently are attached to rocks and from the Upper Pennsylvanian Magdalena Group, a limestone unit shells, and bear an epibiont community distinct from their rocky or exposed in Grapevine Canyon, New Mexico, Hoffmeister et al. (2003) shelly media (C. Schneider, personal observation, 2009). (5) Rhipido- demonstrated that the small brachiopod Cardiarina cordata was mella, therefore, may be preferentially encrusted by ctenostome selectively drilled over larger Olygothyrina alleni and Coledium bowsheri bryozoans taking advantage of secondarily tiered individuals, and by predators or parasites of unknown origin (C. cordata drilling may attempt to avoid small biting predators through secondary tiering. intensity 5 32.7%). Similarly, Ahmed and Leighton (2009) found that, in the Upper Devonian Lime Creek Formation of Iowa, the small The Effects of Shell Texture and Punctae brachiopods Devonoproductus and Douvellina were frequently prey for crushing predators. The Middle Pennsylvanian Vanport Shale of Ohio In a study of modern brachiopods, encrustation frequency was also displays evidence of predatory damage, including apertural recorded to be higher for taxa with pronounced radial ribs as compared breakage and boreholes, on small (,15 mm) components of the fauna, to finer ribbed taxa; the lowest frequencies were attained by the including the brachiopod Composita, the nautiloid Pseudorthoceras smooth-shelled Bouchardia and the spinule-bearing Platidia (Rodland knoxense, and the microgastropod Microdoma conicum (Koy and et al., 2004). Endoskeletobiosis of various types of brachiopod shell Yacobucci, 2001; Yacobucci, personal observation, 2008) These ornament is poorly understood; however, this study reveals a unique occurrences support the idea that the smaller Rhipidomella hosts could preference of endoskeletobionts within the Dundee Formation bra- be preferentially selected in lieu of larger brachiopods by Paleozoic chiopods. Studies of Devonian encrusting organisms across entire predators, and bolster the assertion of Hoffmeister et al. (2003) that a brachiopod assemblages indicates the preference of most encrusting distinct small-bodied predator guild may have been an important organisms for ribbed hosts and the avoidance of smooth hosts (Hurst, component of Paleozoic ecosystems. 1974; Thayer, 1974; Anderson and Megivern, 1982; Schneider and Rhipidomella, although punctate, certainly was the focus of at least a Webb, 2004; Zhan and Vinn, 2007; Schneider, 2009b). The more few predation attempts, as revealed in several repaired attacks. On one coarsely ribbed, costate brachiopods Mucrospirifer and rhynchonellids specimen, the evidence of a repaired durophagous predation attempt in do not show any evidence of endoskeletobiosis. Additionally, the two the central region and subsequent shell repair by the secretion of finely ribbed taxa, Strophodonta and the atrypides, also were lacking in younger skeletal material suggests that the brachiopod shell was alive obvious shell borings. Only the small, radially and finely ribbed, during the time of damage (Fig. 4A). This scar shows a period of punctate Rhipidomella retained evidence of interactions with fouling cessation of growth, followed by shell production and resulting in organisms. deformation of growth lines. On the same specimen, a second scar on Brachiopod punctae have been suggested to be antifouling and the right lateral region obscures and distorts growth lines (Fig. 4A). antipredatory defenses. Caeca within the punctae apparently produce Another specimen bears two deep, parallel, and tapered scars located chemical deterrents that deter borers (Clarkson, 1986). Spicules near the lower left lateral margin (Fig. 4B). This specimen also shows supporting the caecae may also have an antipredatory function (Peck, repair along the anterior-most commissure through a minor distortion 1993). Punctate brachiopods are less frequently encrusted than those of ribs. Furthermore, these scars are oriented in a manner that strongly that were impunctate (Curry, 1983; Thayer, 1986). The impunctate suggests a biting attempt, similar to other scars noted on brachiopods in spiriferide Meristella bore higher rates of encrustation compared to the the Middle Devonian Silica Formation (Sparks et al., 1980, pl. 9, fig. 4). punctate terebratulides (except the orthide Tropidoleptus) collected In the current study, Rhipidomella brachiopods in the Dundee from the Kashong Shale of the Middle Devonian Hamilton Group of Formation certainly were the target of Devonian durophagous New York State (Bordeaux and Brett, 1990). Modern punctate predators, but not drilling predators, and were bored by endoskeleto- brachiopods, however, can be encrusted heavily by episkeletobionts bionts. There is no evidence of endoskeletobiosis or predation of other during life (C. Schneider, personal observation, 2008). Orthide brachiopods in fossiliferous units 10 through 12 of the Dundee brachiopods can be punctate or impunctate, depending on the taxon Formation, but Rhipidomella was obviously both attacked and fouled. (Rowell and Grant, 1987). We suggest four potential hypotheses for these phenomena: Rhipidomella was a punctate brachiopod that experienced predation. It is certain that punctae did not entirely deter predators from attacking 1. In these paleoecosystems, crushing predators could likely only Rhipidomella in Dundee Formation environments. Given that these take small prey and, thus, larger brachiopods were within a large size durophagous scars represent failed predation attempts, however, it is refuge, too large for predators to attack. difficult to determine whether predation frequency on Rhipidomella was 206 BOSE ET AL. PALAIOS higher or lower than that of other brachiopods. Predators may have secondary tiering or cryptic behavior by attached Rhipidomella on successfully attacked impunctate brachiopods, or may have been encrusting organisms. Predation differences between larger brachio- deterred from finishing a predation attempt on Rhipidomella because pods and Rhipidomella may have resulted from (1) smaller predators of antipredatory function by the punctae or caecae. being excluded from the large size refugia of other brachiopods, (2) Impunctate brachiopod taxa from the Dundee Formation lack more successful destructive predation on larger brachiopods, (3) the evidence of endoskeletobionts. Although Rhipidomella was punctate, effects of cryptic behavior or secondary tiering on predation attempts, the brachiopod was a medium for boring organisms. Evidence provided or (4) punctae causing predation deterrence. above suggests the association between live hosts and endoskeleto- Paleoecological interactions are more frequently documented from bionts, at least in some individual brachiopods. Thus, the Rhipidomella Paleozoic siliciclastic units than from carbonate units. The present specimens herein are a rare example of preferential Paleozoic study of the Dundee Formation documents a relatively rare incidence endobiosis of a punctate host. of endobiosis from a carbonate sedimentological regime, which significantly contributes to our understanding of endoskeletobiont Paleoecological Interactions in Paleozoic Carbonate Regimes occurrences in Paleozoic limestones. We anticipate future work to compare epi- and endobiosis in brachiopods from various settings in While there has been evidence of immense biotic activity in carbonate order to pursue the question of why such interactions appear to be sedimentary regimes, studies undertaken in shaly units far outnumber more common in siliciclastic versus carbonate environments. those in limestones. Limestones likely are less studied for encrusting organisms because of the difficulty of removing host specimens from ACKNOWLEDGMENTS the matrix with the encrusters intact. Preparing limestone samples is much more time consuming than the collection of brachiopods from We express our appreciation to the Village of Whitehouse, as well as shales popularly studied, such as those of the Silica Formation of the Toledo Metroparks, for granting access to the Whitehouse Quarry. Michigan and Ohio and the Lime Creek Group of Iowa. The present We thank Dr. Don C. Steinker and Dr. Richard Hoare for their study, although affected by taphonomic alteration of the brachiopods, support and suggestions. A special thanks to Dr. Lindsey Leighton for suggests that Paleozoic carbonate regimes have untapped potential to his helpful comments on scarred specimens and literature recommen- contribute to our understanding of paleoecological interactions. dations. Thanks to Christopher Wright for providing stratigraphic information about the Dundee Formation, and his assistance in CONCLUSIONS fieldwork. RB thanks Juergen Schieber, Stephaney Puchalski and Monalisa Mishra for help with SEM and Claudia Johnson for help with The detailed study of brachiopods from units 10 through 12 of the housing these field collections in the Indiana University Paleontology Middle Devonian Dundee Formation in the Whitehouse Quarry reveals repository. Finally, a special thanks to D. L. Rodland, the two that larger (3.0–4.0 cm) brachiopod genera that were typically encrusted anonymous reviewers, and Editor Stephen T. Hasiotis for their careful or preyed upon elsewhere bore no episkeletobionts, endoskeletobionts, reviews. Last but not least, we express our deep gratitude to Sheila J. or predation traces, but valves of the somewhat smaller (2.0 6 0.1 cm), Roberts, James E. Evans, and other faculty and staff members of punctate brachiopod genus Rhipidomella bore traces left by endoske- BGSU for the opportunity to carry out this research. letobionts and predators. 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