Biotic Interactions among Recent and among Fossil ... - Springer Link

Chapter 9

Biotic Interactions among Recent and among Fossil Crinoids DAVID L. MEYER and WILLIAM I. AUSICH

1. 2.

3.

4.

5.

6. 7.

8.

Introduction . . . . . . . . . . . . . . . . . . . . . . . Predation . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Sources of Predation on Living Crinoids .. 2.2. Possible Antipredator Adaptations of Living Crinoids 2.3. Predation on Ancient Crinoids . . . . . . . . . . . . . . 2.4. Possible Antipredator Morphology in Ancient Crinoids 2.5. Regeneration and Nonlethal Predation . Competition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Possible Mechanisms of Competition . . . . . . . . . . . 3.2. Niche Differentiation among Living and among Ancient Crinoids Associations of Living Crinoids with Other Organisms 4.1. Polychaetes 4.2. Molluscs .. 4.3. Crustaceans 4.4. Fishes ... Associations of Ancient Crinoids with Other Organisms 5.1. Nature of Associations .. 5.2. Commensalism . . . . . . . 5.3. Stereomic Malformations . 5.4. Crinoids as Epizoans 5.5. Parasitism . . . . . . . . . . Other Interactions . . . . . . . . . Habitat Modification by Crinoids 7.1. Contribution to Sediment 7.2. Effects on Substrata .. 7.3. Consequences for Community Succession Role of Biotic Interactions in Crinoid Evolution

415 415 416 418 418

References . . . .

420

378 378 378 380 381 383 385 385 387 388 392 395 396 396 397 398 398 399 406 411 412 414

DAVID L. MEYER • Department of Geology, University of Cincinnati, Cincinnati, Ohio 45221. WILLIAM I. AUSICH • Department of Geological Sciences, Wright State University. Dayton, Ohio 45435. 377

M. J. S. Tevesz et al. (eds.), Biotic Interactions in Recent and Fossil Benthic Communities © Springer Science+Business Media New York 1983

378

1.

Chapter 9

Introduction

Most previous reports on the biotic interactions of crinoids have treated either the living or the fossil forms exclusively. Major treatments of the biotic interactions of living crinoids are those of Clark (1921), Hyman (1955), Fell (1966), and Breimer (1978). Interactions of extinct crinoids have been summarized by N. G. Lane (1978). In the present review, we have compiled evidence for biotic interactions of both living and fossil crinoids in order to elucidate the role of biotic interactions in crinoid evolution. In Sections 2 through 6, we consider direct interactions of crinoids with other organisms and other crinoids. In Section 7, Habitat Modification, we consider ways by which crinoids modify their environment which will affect other organisms. The evolutionary history of biotic interactions of crinoids provides evidence that predation and competition have played significant roles in crinoid evolution.

2. 2.1.

Predation Sources of Predation on Living Crinoids

Until very recently, living crinoids have been assumed to be free from major predators. In 1915, H. L. Clark observed that comatulids in the Torres Strait of Australia were avoided by fishes when allowed to fall to the bottom, while other edible objects were readily attacked. Clark suggested that crinoids were recognized as inedible by fishes, possibly because of some secretion of the crinoids. Very little work was done with living crinoids in their natural habitat for almost 50 years following Clark's pioneering observations, and the notion the Recent crinoids are without predators became widely accepted (A. H. Clark, 1921, p. 687; Mortensen, 1927, p. 14; Fell, 1966, p. 53; Breimer, 1978, p. 325). The report by Brun (1972, p. 230) of Antedon bifida in the stomach contents of the sea star Luidia ciliaris (Philippi) is unique in view of Fell's (1966, p. 53) statement that sea stars apparently do not consume crinoids, although many other echinoderms are frequent prey. Observations of crinoids in the natural habitat (Magnus, 1963; Rutman and Fishelson, 1969; Meyer, 1972, 1973a,b; Macurda, 1973, 1975; Fishelson, 1974; Macurda and Meyer, 1974; Meyer and Macurda, 1980) have not revealed major predation on crinoids, but a great deal of new information derived from these and other studies indicates that crinoids are not immune to predation. Furthermore, it has become clear that predation may play a major role in Recent crinoid ecology and likely did so far back into the group's evolutionary past. Arthropods and fish are the most likely predators of Recent crinoids.

Biotic Interactions among Recent and among Fossil Crinoids

379

Vasserot (1965, p. 371) observed that the lobster Panulirus vulgaris (Latreille) attacked and devoured the comatulid Antedon De Freminville in an aquarium experiment, although no attacks were observed in nature. Several instances of fish predation on crinoids indicate that crinoids are by no means immune to fish attacks. Crinoid remains have been reported from the gut contents of a grouper (Lethrinus sp.) and a filefish (Aiutera sp.) (Meyer and Macurda, 1977). Seven specimens of the Australian snapper, Chrysophrys auratus (Bloch and Schneider), caught during the afternoon at the southern end of the Great Barrier Reef all had two to four fresh crinoids in their stomachs (W. Nash, personal communication, 1982). Nash mentioned that these fish often have crinoids in their guts according to local fisherman. Two species of Lethrinus (L. chrysostomus and L. nebulosus) from the Townsville region of the Great Barrier Reef contained small amounts of crinoids (Walker, 1975). Diving studies by Meyer and Macurda have revealed very few cases of direct attacks of fish on crinoids, and most cases involved artificial exposure of the crinoid from its semicryptic attachment site. In one instance, possible rejection of a crinoid by a fish was observed. Nevertheless, numerous comatulids in the Great Barrier Reef region have been observed with sublethal damage to the arms and calyx that may be the result of fish attack (Meyer and Macurda, unpublished observations). Magnus (1963, p. 364) observed that fishes like the sergeant major (Abudefduf saxatilis (L.)] and the butterfly fishes (Chaetodon) interfered with a Red Sea comatulid by sucking up strings of mucus adhering to the arms and pinnules, sometimes tugging on the arms and causing them to undergo self-induced breakage. This occurred just before these nocturnal crinoids coiled the arms of the filtration fan at daybreak when the fish were becoming active. During the day, the same crinoids were coiled up and completely exposed in the presence of many fishes, but were unmolested. At night, actively feeding crinoids were undisturbed by marauding moray eels. The immunity of Red Sea crinoids was further implied by Fishelson (1974, p. 191), who suggested that the epizoic community of crinoids benefitted because the host crinoids are "very rarely attacked or eaten by other animals." He also noted, however, that the clingfish (Lepadichthys lineatus Briggs) associated with a comatulid feeds on the host's pinnules as well as on commensal worms and copepods. Earlier, Potts (1915, p. 79), reporting on the commensals of Torres Strait crinoids, commented: "It is hardly to be supposed that even a rapacious fish would take a mouthful of these hard and unsatisfying arms for the sake of the shrimp which lies amongst them. In no case at least which we saw were the arms of crinoids mutilated." Observations of deep-water crinoids also suggest possible sources of predation. In a recent photographic survey (Conan et al., 1981) of the

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stalked crinoid Diplocrinus wyvillethomsoni at 1246 m in the Bay of Biscay, a fish (family Oreosomatidae) was shown apparently feeding on the arms and pinnules of the stalked crinoid, which had several arms broken. Crinoids (presumably comatulids) comprised about 5% by weight of stomach contents of the spiny eel Notacanthus bonapartei from 200 to 800 m on the Mediterranean slope (Macpherson, 1981). Arrow crabs (? Stenorhynchus sp.) were observed on the crowns of isocrinids at 180-300 m off Jamaica by Meyer and Macurda (unpublished observations). The activities of the crabs are uncertain, but predation is a possibility. 2.2.

Possible Antipredator Adaptations of Living Crinoids

The apparent low predation pressure on Recent crinoids, comatulids in particular, may be a consequence of unique biochemical, morphologic, and behavioral traits. The frequently repeated suggestion that crinoids may be distasteful, or even toxic to predators (H. L. Clark, 1915, p. 114; A. H. Clark, 1921, p. 687; Fell, 1966, p. 53; Breimer, 1978, p. 325), has been substantiated in recent reports by Rideout et al. (1979) and Bakus (1981). Rideout and coworkers reported feeding tests that indicated avoidance by fishes of food that contained polyketide sulfates at concentrations found in Australian comatulid crinoids. Bakus reported a comatulid from Lizard Island, Great Barrier Reef, that was toxic to fish. If toxicity or distastefulness is widespread among comatulids, it may explain why many species live in an exposed and conspicuous position (e.g., Meyer, 1973a; Meyer and Macurda, 1980) with little or no predation by fish. Among many morphologic adaptations of comatulid crinoids (Meyer and Macurda, 1977), the development of enlarged, rigid, and spike-like proximal pinnules is very likely a protective modification. These specialized pinnules form a palisade over the vulnerable oral disk of the crinoid (Meyer and Macurda, 1977, Fig. 4). These structures occur in comatulids that typically occupy exposed feeding perches, although they are not present in members of the Comasteridae that also live in exposed positions. Swimming and crawling capabilities of comatulids may be advantageous in predator avoidance (Meyer and Macurda, 1977, p. 77), either as an escape mechanism or by enabling retreat to a daytime cryptic position for nocturnal crinoids. Nocturnal emergence for feeding is common among comatulids of tropical coral reefs (Magnus, 1963; Rutman and Fishelson, 1969; Meyer, 1973a,b; Fishelson, 1974; Meyer and Macurda, 1980). Although alternative explanations cannot be precluded, avoidance of visual predators may be an advantage of this behavior. Most nocturnal comatulids are completely hidden by day, but Magnus (1963, p. 367) reported that Heterometra savignyi remains in an exposed position while coiled up


381

during the day. Experiments by Meyer designed to expose day-cryptic comatulids to potential predation during the day have not resulted in any attacks. Fishelson (1974, p. 185) indicated that comatulids active only at night at shallow depths (3-6m) were active day and night at greater depths (below 6-10 m) on the same reefs in the Red Sea. He believed that sensitivity to light intensity controls the activity pattern. While this may be the proximate cause, it would be interesting to know how fish activity changes along the same depth profile.

2.3.

Predation on Ancient Crinoids

The crinoid fossil record confirms the impression gained from Recent crinoids by revealing several cases of possible predation on crinoids. The apparent scarcity of crinoid calyxes in relation to the great volume of columnal material in Carboniferous crinoidal deposits led Laudon (1957, pp. 962-967) to suggest that "carnivores, perhaps shell-feeding sharks, were eating the crinoids, leaving the columns .... " The common occurrence of teeth of shell-crushing sharks in association with crinoidal sediments was cited in support of this hypothesis. Certain living sharks of the family Heterodontidae, such as the Port Jackson Shark [Heterodontus portusjacksoni (Meyer)] are known to feed on echinoids and sea stars (N. G. Lane, 1978, p. 347). Lane (1971, p. 1442) noted that an alternative explanation for the apparent discrepancy between preserved calyxes and columnals may be that disarticulated calyx plates are so small and rare compared to columnals that they can be easily overlooked by most collectors. The role of predators as agents of taphonomic destruction of crinoids remains conjectural, but other evidence clearly points to fishes as predators of crinoids during the Paleozoic. Crinoid arm fragments have been found in the stomach contents of the Permian bradyodont shark Janassa (Malzahn, 1968, p. 83). In another case, crinoid columnals were found in a shark coprolite mass from the Pennsylvanian Logan Quarry Shale of Illinois (Zangerl and Richardson, 1963, p. 142). Zangerl and Richardson noted that crinoids would seem to have been an extremely poor food source, and that it is not possible to determine whether the shark devoured a living crinoid or merely ingested the columnals from the substratum. Arthropods may also have been predators of crinoids in the past. In the Lower Devonian Hunsnlck Shale of Germany, a pycnogonid, Palaeoisopus broili, has been found intertwined with a crinoid, Imitatocrinus gracilior F. Roemer (Bergstrom et al., 1980, pp. 32-33). Orientation of the head of the pycnogonid toward the calyx of the crinoid, together with the large eyes, cheliphores, and presumed swimming ability of the pycno-

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gonid, suggested to Bergstrom and co-workers that the pycnogonid was predatory on crinoids. An earlier life reconstruction of the pycnogonidcrinoid association by Dubinin (1957, cited in Bergstrom et al., 1980) also favored this interpretation. On the basis of his observation of the attack on comatulid crinoids by lobsters in the aquarium, Vasserot (1965, pp. 381-382) discussed the possibility that predation pressure on stalked crinoids coinciding with the diversification of lobsters in the Mesozoic might account for the decline of stalked crinoids in shallow waters. Vasserot noted that the reduction of the crinoidallimestone facies in the Cretaceous Table I.

Possible Protective Morphologic Features of Crinoids 0

Feature Mouth and proximal ambulacra subtegminal; tegmen sometimes rigidly plated Tegmina! clefts for arms Spines on aboral cup and tegmen on aboral cup on tegmen also "wing plates" spinose, expanded summit of anal sac on arms Arm and pinnule modifications

Column modifications

Taxa

Occurrence

References

Camerata, Inadunata

Ord.-Trias.

Ubaghs, (1953)

Eucalyptocrinites Timorechinus Proapsidocrinus

Sil. Perm. Perm.

T497; Ubaghs (1953) T753; Ubaghs (1953)

Calliocrinus Arthroacantha Gennaeocrinus goldringae Dorycrinus Pterotocrinus

Sil.-Dev. Dev. Dev.

T497; Ubaghs (1953) T474; Ubaghs (1953) T446; Kesling (1965)

Miss. Miss.

Tholocrinus Eirmocrinus Melocrinites michiganensis Eretmocrinus Barrandeocrinus Calceocrinidae Eugeniacrinites Comatulida

Miss. Penn. Dev.

T472; Ubaghs (1953) T478; Welch (1978), Ubaghs (1953) T750; Ubaghs (1953) T725 Kesling (1964)

Miss. Sil. Ord.-Perm. Jur.-Cret. Jur.-Rec.

Myelodactylus Carnptocrinus Arnrnonicrinus Dolatocrinus

Sil.-Dev. Miss. Dev. Dev.

T155; Ubaghs (1953) T157; Ubaghs (1953) T114 TB34; Ubaghs (1953) Ubaghs (1953]. Meyer and Macurda (1977) T78; Springer (1926a). Ubaghs (1953) T499

"T references are to illustrations in Moore and Teichert (1978); others to original sources where illustrated or mentioned in connection with protective function. This is not a comprehensive list of taxa having possible protective features; only representative taxa are listed.


383

as compared to the Jurassic is in agreement with the appearance of lobsters in the Late Jurassic followed by their diversification in the Cretaceous. Cephalopods may also be predators on crinoids, but the only direct evidence comes from the Jurassic Solnhofen Limestone. Janicke (1970) reported that the Solnhofen trace fossil Lumbricaria Munster consists mainly of remains of the planktonic crinoid Saccocoma Agassiz. He interpreted Lumbricaria as a coprolite produced by teuthoid cephalopods. Whether cephalopods in the Paleozoic and Mesozoic preyed on benthic crinoids is conjectural.

2.4.

Possible Antipredator Morphology in Ancient Crinoids

The repeated development of certain morphologic features among ancient crinoids strongly suggests antipredator, defensive adaptations. Many of these supposed adaptations were listed and illustrated by Ubaghs (1953, p. 725, Figs. 114-119). Table I and Fig. 1 summarize some of these features along with representative examples. Possible defensive adaptations include those that completely hide the calyx or arms. In Myelodactylus Hall, Camptocrinus Wachsmuth and Springer, and Ammonicrinus Springer, the delicate calyx could be completely or partly enclosed within a coiled stem equipped with closely spaced cirri (Figs. 1j, k). This adaptation arose independently in three subclasses. Modifications enabling the arms to be secured within tegminal clefts evolved at least twice in two subclasses (Figs. 1a, b). In a third subclass, Eugeniacrinites Miller developed enlarged primibrachials between which the arms could be withdrawn into recesses (Fig. 1c). Other arm modifications that may be reasonably interpreted as protective evolved in different crinoid taxa (Table I). The most common recurring antipredator morphology was the development of spines. Spines on the aboral cup, tegmen, arms, and distal anal sac first developed in Silurian crinoids and were present throughout the Paleozoic in the inadunates and carnerates, but not in the flexible crinoids (Figs. 1d-g). Lewis and Strimple (1979) interpreted a spinose, mushroom-shaped anal sac as a convergent protective adaptation in many Carboniferous inadunate crinoid genera. Spinosity reappeared in the comatulids through stiffening and enlargement of the proximal pinnules to form a "palisade" protecting the unplated tegmen (Fig. 1i; Meyer and Macurda, 1977). In addition to shielding of vulnerable regions, radiating spines could also serve to make the crinoid appear larger, possibly deterring predators limited to smaller size ranges of prey.

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a

e

f

..........

h

g

j

.........

k


2.5.

385

Regeneration and Nonlethal Predation

Recent and fossil crinoids exhibiting regenerating parts may be indicative of nonlethal predation, although some of these occurrences are open to other interpretations. Regenerating arms are frequently seen in living comatulids and have also been reported among fossil forms (Springer, 1926a, pp. 402-403; Lane and Webster, 1966, pp. 13-14). Springer discussed a specimen of the Mississippian flexible crinoid Taxocrinus colletti in which the entire crown above the infrabasals was regenerated. Living comatulids have been observed with the visceral mass in various stages of regeneration (Smith et al., 1981). Evidence of damaged andregenerating oral pinnules surrounding the regenerating viscera in some of these comatulids clearly points to attack by predators as a cause. Regenerating arms could also follow autotomy caused by some disturbance other than predation. Uniform breakage and regeneration of spines on a Pennsylvanian inadunate crinoid suggested to Burke (1973, p. 161) possible nipping by fishes. Fossil remains of a potential fish culprit occurred in the same formation with the crinoid.

3.

Competition

In evaluating the role of competition in crinoid biology and paleobiology, it is important to consider two distinct aspects of competition. First, competition can sometimes be observed directly in nature as an ongoing process [for example, the "aggressive" interactions among reef corals (Lang, 1973)]. Second, competition can be inferred to have occurred Figure 1. Possible protective features in crinoids. (a-c) Tegmina! clefts for arms. (a) Eucalyptocrinites rosaceus Goldfuss, Devonian (after Schultze, from Ubaghs, 1953). (b) Timorechinus mirabilis Wanner. Permian (from Wanner, 1916). (c) Eugeniacrinites cariophilites (von Schlotheim), Upper Jurassic (from Rasmussen, 1969); note clefts for arms formed by expansion of primibrachials. (d-g] Development of spines and other projections. (d) Gennaeocrinus goldringae Ehlers, Devonian (from Kesling, 1965; used with permission of R. V. Kesling]. (e) Calliocrinus murchisonianus Angelin, Silurian (from Angelin, 1878). (f) Tholocrinus wetherbyi (Wachsmuth and Springer]. Mississippian (from Moore and Teichert, 1978). (g) Pterotocrinus bifurcatus Wetherby, Mississippian (after Springer, from Ubaghs, 1953). (h) Halysiocrinus nodosus (Hall). Mississippian (from Moore and Teichert, 1978); note asymmetric aboral cup that permits crown to be closely enfolded along column. (i) Cenometra bella (Hartlaub], Recent, Palau Islands; oral side of comatulid showing palisade over oral disk formed by spike-like second pinnules, which are about 7 mm long. (j,k] Concealment of crown by coiled, cirriferous column. (j) Myelodactylus ammon is (Bather]. Upper Silurian (after Springer, from Moore and Teichert, 1978). (k) Camptocrinus multicirrus Springer, Mississippian (after Wachsmuth and Springer, from Moore and Teichert, 1978). All scales 1 em.

Feeding period

Elevation above substratum; type of substratum

Differential feeding efficiency (?)

Food particle size

Food particle size

2. Feeding site

3. Feeding posture

4. Ambulacral groove width

5. Tube foot spacing and length

Separation effected

1. Temporal activity pattern

Niche dimension

Living crinoids

Meyer (1973a,b). Meyer and Macurda (1980) Rutman and Fishelson (1969). LaTouche and West (1980) Meyer (1979)

Meyer (1973a,b), Meyer and Macurda (1980) Meyer (1973a,b). Meyer and Macurda (1980)

References

3. Ambulacral groove width

2. Filtration fan density

1. Stalk length

Niche dimension

Food particle size; differential feeding efficiency Food particle size

Elevation above substratum

Separation effected

Fossil crinoids

Table II. Major Known Dimensions of Crinoid Niche Differentiation

Ausich (1980)

Lane (1963, 1973). Haugh (1979). Ausich (1980) Ausich (1980). Meyer and Lane (1976)

References

w

n

0

(/)

CD

Cl

c 0

c. (/) CD

Iii ID

c

(/)

0

"5

(/)

0

.! ~ 0

I

I

I I

I

Iii !

~

(/)

c

"' 0

£

e "' 0

eg.

.Q

E

·t:! ..c: 0

Cl)

:s

..5

~ gj

~:; CIO.:C:

Figure 4. Temporal distribution of organisms epizoic on crinoids. Question mark in circle indicates that for a given period it cannot be verified that the crinoid host was alive. Larger question mark indicates that the occurrence is queried.

396

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or endozoic life with crinoids. Clark (1921, pp. 651-675) provided an extensive review of the occurrence of myzostomids as known at that time. Myzostomids possess an eversible proboscis that is used in sucking up material being transported in the host's ambulacral grooves (Gislen, 1924, Fig. 333; Fishelson, 1974, p. 189). Other myzostomids live freely within the host's gut or occur within cysts or swellings within the host's tissues, sometimes causing malformations of the skeletal ossicles (Fig. 4). Individual myzostomid species are not necessarily restricted to a single host species, nor does a host crinoid necessarily support only a single myzostomid species (Clark, 1921; Fishelson, 1974). Numbers of individual myzostomids on a single host individual vary from none to as many as 93 (Clark, 1921; Fishelson, 1974). Myzostomids are associated with both comatulids and stalked crinoids occurring in a wide range of environments including tropical and polar waters (Clark, 1921). The aphroditid polychaete Scelisetosus longicirrus Schmarda occurs widely on most of the comatulids studied by Fishelson (1974, p. 189) in the Red Sea. This worm is epizoic and feeds on copepods, myzostomids, and mucous secretions of the host.

4.2.

Molluscs

According to a review by Lutzen (1972), the majority of gastropods parasitic on crinoids belong to the family Eulimidae, although some genera are of uncertain affinities. Twenty-four instances of gastropod parasitism on both comatulid and stalked crinoids are listed by Lutzen. While some parasitic gastropods insert a proboscis into the tissue of the host, Goodingia varicosa (Schepman and Nierstrasz), redescribed by Lutzen (1972), utilizes a sucker disc that is applied to the surface of the host. Digestion of tissue beneath the disc leaves an impression in the surface of the brachial ossicle; and a series of these impressions on the host indicated repeated attacks by the parasite. Fishelson (1974, p. 189) illustrated two species of melanellid gastropods parasitic on Red Sea comatulids.

4.3.

Crustaceans

Table III indicates that many crustaceans are associated with crinoids: herein lie some of the most interesting and yet largely unexplored relationships. In a review of caridean shrimps associated with coral reef organisms, Bruce (1976) emphasized that the nature of shrimp-host associations is very poorly understood. Bruce listed six genera of shrimps


397

associated with Indo-West Pacific crinoids. Clark (1921, p. 614) included most of the crustacean associates of crinoids under "semi parasitic" forms, which were thought to remove food material from the crinoid's ambulacra. However, Fishelson's (1974) observations on the associates of Red Sea comatulids suggest that some of these shrimps and crabs do not actually feed on the host or its food. Instead, the shrimp Periclimenes tenuis Bruce feeds on copepods associated with the host as well as on mucous secretions of the crinoid. The crab Gala thea elegans Adam and White appeared to feed on mucous secretions of the host and on detrital material carried along by the current. For other shrimp and crab species inhabiting crinoids, there is little or no information as to modes of life or association. Detailed descriptions of crustacean associates of comatulids from single localities were provided by Potts (1915, for Torres Strait) and Fishelson (1974, for the Red Sea). A particularly interesting association described by Potts is that of the snapping shrimp, Synalpheus spp., with comatulids. These usually occur as a male and female pair on a host and exhibit coloration matching the host, which is highly variable. Nothing seems to be known as to the life habits of these shrimps. Commensal shrimps also occur on tropical Western Atlantic comatulids, apparently belonging only to the genus Periclimenes. Two species, each showing close correspondence of color patterns to that of the host, were described by Chace (1969). Isopods and amphipods also associate with crinoids (Table III; Clark, 1921, pp. 632-635). Earlier reports summarized by Clark indicated the occurrence of isopods within the anal tube of crinoids. Potts (1915, p. 90) reported that Cirolana lineata Potts is often seen diving into the gut of the host, where it apparently spends a large part of its time. Meyer (unpublished observation) also recorded the occurrence of an isopod within the gut or anal tube of two species of comatulids at Lizard Island on the Great Barrier Reef. Copepods occur in abundance on comatulids, with 350-500 individuals comprising several species found on a single host crinoid (Fishelson, 1974, p. 187). Laboratory observations by Fishelson indicated that these copepods are preyed upon by other crustaceans, polychaetes, and the clingfish also associated with the crinoids. Another copepod reported by Fishelson is a crinoid endoparasite. Fishelson (1974, p. 188) suggested that the epizoic copepods form the lowest level of a food chain existing on the Red Sea comatulids. 4.4.

Fishes

The association of clingfishes (Gobiesocidae) with Indo-Pacific crinoids has become known only recently (Fishelson, 1966, 1974; Allen and Starck, 1973). These small fishes attach to the arms of the host by means

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of an adhesive disc located beneath the head of the fish (Fishelson, 1966); they also attach to the oral or aboral body surface (N.D. Holland, personal communication). Although clingfishes occur with other organisms, two species definitely associated with comatulid crinoids have been described (Fishelson, 1966; Allen and Starck, 1973). The remarkable abilities of Lepadichthys lineatus Briggs to change color either to match the coloration of the crinoid host or to reflect different behavioral responses have been described by Fishelson (1966, pp. 42-44). On the basis of laboratory observations, Fishelson (1966, 1974) indicated that clingfishes feed on the pinnules of the host, and on associated worms and copepods. He suggested that clingfishes perform a "cleaning" function by removing other epizoans. Allen and Starck (1973, p. 96) suggested that clingfishes capture planktonic food from the water sweeping by the crinoid host, which perches on prominent, current-swept sites. A further intriguing observation by Fishelson (1966, 1974) is that comatulids in the Red Sea inhabited by galatheid crabs do not host clingfishes, possibly because the two compete for the region of the host between the arm bases and cirri as a favored attachment site. Other associates (crabs, shrimp) coexist on a single host. Associates of living crinoids clearly present a wide variety of challenging research problems. In addition to the question of the precise nature of crinoid-associate interactions, there are interesting biogeographic problems pertaining to these associations. For instance, why are myzostomids as a group found on crinoids worldwide, while many other associates are strictly tropical? Also, what accounts for the greater diversity of crinoid associates (as well as crinoids) in the Indo-West Pacific as compared to the tropical Western Atlantic? Careful documentation of species diversity and abundance on known crinoid hosts in different regions will be necessary in order to approach these problems.

5. 5.1.

Associations of Ancient Crinoids with Other Organisms Nature of Associations

Many kinds of fossil organisms are commonly preserved encrusting crinoid pluricolumnals (more than one articulated crinoid columnal). Two questions, often unanswerable, must be addressed in order to evaluate such associations: (1) was the attached organism an epizoan living on a live crinoid or was the pluricolumnal a sedimentary grain at the time of attachment; (2) if an epizoan, what type of relationship existed between the epizoan and its host?


399

Crinoids commonly displayed a pathologic response to the presence of an attached organism by secreting stereomic overgrowths on or around the attached organism. The crinoid host was certainly alive in cases where stereomic overgrowths are present. The crinoid can also be assumed to have been a living host if attached organisms are present around the entire column circumference, although this inference is more tenuous. The nature of the relationship is more difficult to assess when there are neither skeletal overgrowths nor attachment around the column circumference. In most cases, a definitive interpretation is not possible. The following are all plausible relationships: (1) the attached organism cemented itself to a crinoid pluricolumnal that was a sedimentary grain; (2) the attached epizoan produced no pathologic response to the living host; or (3) an epizoan attached to a mature portion of a living column where no subsequent overgrowths were produced. We have included, but questioned, reported occurrences where attached organisms display neither stereomic overgrowths nor attachment around the column circumference. Determining the precise biotic interaction of an epizoan with a crinoid can be very difficult. At what point can it be inferred that an epizoan was detrimental enough to its host that the epizoan should be considered a parasite rather than a commensal? Does a pathologic stereomic overgrowth response or a boring habit necessarily signify that the epizoan is a parasite? These and other questions are difficult or impossible to answer in many fossil situations. The attachment of an epizoan to a living crinoid column or stalk does not a priori suggest a parasitic habit, because a clear advantage can be inferred for an epizoan elevated above the bottom. First, the ability of an epizoan larva to attach to a crinoid stalk would provide an advantage over other larvae competing for a hard substratum at the sediment-water interface. Second, in a tiered epifaunal suspension-feeding community (Lane, 1963; Ausieh, 1980), a brachiopod [or other epizoan) that could attach higher in the structure of the community would not be competing directly for food with other similar organisms attached to the substratum. Because an advantage can be inferred for organisms that are attached to a crinoid column and because an epizoan on a stalk should not hinder a crinoid's activities, we will assume that epizoans are commensals unless other evidence suggests that they are parasitic. 5.2.

Commensalism

Organisms that were commensal on fossil crinoids can be subdivided into two major groups: (1) organisms that were epizoan on other substrata in addition to crinoids [facultative commensals); (2) organisms that are especially adapted to life as crinoid commensals [obligate commensals).

400 5.2.1.

Chapter 9

Facultative Commensals

Commensals that normally lived as epizoans are varied, and it is commonly difficult to determine whether they occurred on a live host. Bryozoans, Cornulites Schlotheim, encrusting foraminiferans, Spirorbis Daudin, oysters, calcareous sponges, serpulid worms, and barnacles are all found epizoic on crinoids as well as on other hosts. Bryozoans are preserved on crinoid columns from the Silurian to the Mississippian and in the Jurassic (Fig. 4). In a Silurian example (Strimple, 1963), commensal bryozoans produced grooves on crinoid pluricolumnals; and in Mississippian strata, Etheridge (1880) figured commensal bryozoans with partial stereomic overgrowths. Cornulites (conoidal shell fossil of unknown biological affinities) is also reported on crinoids and is considered a suspension-feeding commensal. Franzen (1974) illustrated a Cornulites that induced stereomic overgrowths. Cornulites is also reported attached to Devonian crinoid columns (Rodriguez and Gutschick, 1975). Foraminiferans encrusted on crinoid pluricolumnals from the Silurian through the Mississippian but never elicited skeletal hypertrophy. Franzen (1974) illustrated Silurian foraminiferans encrusting on the inner walls of boreholes (or pits) in crinoidal tissue and suggested that the foraminiferans were responsible for the borings. We agree with Brett (1978a) that insufficient evidence is present to confirm a boring habit for these Silurian foraminiferans. Instead, the foraminiferans discussed by Franzen (1974) were probably commensals that coincidently attached to or selectively chose the vacated pits for a domicile. Spirorbis is reported attached to crinoids only during the Mississippian by Hudson et al. (1966) and Ausich (1979). It is not known whether the crinoid host was alive. If the Spirorbis-crinoid association is commensal and Spirorbis sought out crinoid columns for a suspension-feeding perch, this relationship may have existed at times other than the Mississippian. Several groups developed an epizoic habit with stalked crinoids in Jurassic epifaunal communities. It was during the Jurassic when stalked crinoids were reestablished into epifaunal suspension-feeding communities (Ausich and Bottjer, 1980). Oysters, calcareous sponges, serpulid worms, and barnacles are associated with Jurassic crinoids. The oysters, calcareous sponges, and serpulid worms (Hess, 1975) are attached around a sufficient portion of the column circumference so that they can be inferred to have been attached to a living crinoid. At least one acrothoracian barnacle boring that infested crinoids has been given a generic assignment, Simonizapfes Codez.


5.2.2.

401

Obligate Commensals

Certain gastropods, brachiopods, starfish, corals, and several gallforming organisms were adapted only to a commensal existence on crinoids. The association between certain Paleozoic crinoids and the platyceratid gastropods is perhaps the best known and most thoroughly documented biotic interaction among Paleozoic crinoids. The family Platyceratidae were trochinid archaeogastropods that ranged from Ordovician to Permian (Fig. 5). Austin and Austin (1843-1849) first noted the persistent association of platyceratids on crinoid tegmens, and they reasoned that the gastropods were preying upon the crinoids. Meek and Worthen (1873) were among the first to observe that platyceratids affixed themselves permanently over the anal opening on the crinoid tegmen. Meek and Worthen further suggested that the platyceratids were sedentary organisms that obtained their nutrition by ingesting crinoid excrement. This view was advanced by other paleontologists, such as Thomas (1924) who stated: The crinoid is already well known to paleontologists from the fact that it habitually harbored a large parasitic limpet. ... Its purpose obviously was to feed upon such refuse matter as the crinoid eliminated from its alimentary canal. ... show that they were unquestionably the unhappy hosts of a weighty and persistent parasite. [pp. 450-451]

Bowsher published an important summary paper in 1955 in which he detailed the life habits and evolutionary history of the platyceratid gastropods. Bowsher (1955) agreed with some previous authors that platyceratids were sessile and fed on crinoid excrement. He applied the term coprophagous to the association. We concur with Bowsher (1955) and others and consider the platyceratids as coprophagous commensals on crinoids. A major problem in platyceratid taxonomy is that the conch aperture is quite variable. This variability results from the molding of each gastropod to the irregularities of the tegmina! morphology of the host crinoid. Little or no subsequent deformation of the tegmen resulted from this attachment (Bowsher, 1955). The deviations in conch aperture of earlier growth stages are reflected as growth lines and demonstrate that the gastropods lived most if not all of their postlarvallife affixed to a crinoid tegmen. The Platyceratidae contain six genera that range from the Upper Ordovician to the Permian (Fig. 5). The temporal occurrences of Platyceras Conrad, Naticonema Perner, and Cyclonema Hall on the crinoids belonging to the three Paleozoic subclasses are given in Fig. 5. Other platyceratid genera include Strophostylus Hall, Ptychospirina PernRr, and ?Himantonia Perner.

402

Chapter 9

Occurences of Platyceratids

Ranges of Platyceratidae genera

-t--------- ~.,\l_..{i.1_- ~~ ~- :~~!? .·.·· _.p , Penn.

1-

-+----- - - - - --1-

(.)

'2

Dev.

v....... Y............Y

.......

...._V ' - -

Cambrian

Figure 5. Temporal distribution of platyceratid genera and their association with the Paleozoic crinoid subclasses. Modified and updated from Bowsher {1955) . C, Cyclonema ; N, Naticonema; P. Platyceras.

The association of platyceratids with camerate crinoids appears to have been the most common. The solid camerate tegmen probably provided a better surface for a firm attachment. During the range of platyceratids, only the Pennsylvanian lacks examples of platyceratids attached to carnerates (Fig. 5). Although not as significant in terms of numbers of preserved instances , platyceratids and inadunate crinoids display a consistent association throughout most of the Paleozoic. Few occurrences of platyceratids attached to flexible crinoids (Springer, 1920, Plate 52 , Fig. 11b; Clarke, 1921, Fig. 60) have been reported. As outlined by Bowsher (1955) and N. G. Lane (1978), the platyceratid-crinoid association developed through the Paleozoic. The Ordovician platyceratids Cyclonema and Naticonema are not consistently preserved over the anal opening. Instead they are preserved in different positions on the tegmen. Thus, early platyceratids were probably mobile and wandered over the tegmen. By at least the Devonian, individuals of the genus Platyceras are preserved invariably over the anal opening, and members of this genus were undoubtedly permanently affixed to the crinoid tegmen throughout their postlarval life (Fig. 6D). Although different platyceratid species were capable of adapting to


403

several hosts, a high degree of host specificity was prevalent by at least the Mississippian. Table IV summarizes the distribution of two species of Platyceras at Crawfordsville, Indiana. In this Mississippian example reported by Lane (1973), Platyceras (Orthonychia) acutirostre was preserved attached only to Platycrinites hemisphericus. Although P. (Platyceras) equilateralis had a greater adaptability than its sympatric congener, the former clearly preferred Gilbertsocrinus tuberosus and perhaps Springericrinus magniventrus. The platyceratids continued the coprophagous habit on both inadunate and camerate crinoids until at least the Middle Permian. During the Middle Permian or certainly by the end of the Paleozoic, the platyceratids became extinct during the biotic crisis that nearly drove their "unhappy hosts" to extinction, as well. As at the present, ophiuroids are found associated with crinoids. The fossil ophiuroid Onychaster Meek and Worthen is preserved rarely either intertwined within crinoid arms, wrapped around a crinoid tegmen or cup, or positioned adjacent to a crinoid. In fossil examples, this association has been interpreted to represent a coprophagous behavior (Clarke, 1921) and predatory behavior (Howell, 1975) by the ophiuroid. Because certain living ophiuroids are commensals on stalked crinoids (Macurda and Meyer, 1974, Fig. 1a), using them as a perch for suspensionfeeding, this interpretation (Spencer and Wright, 1966) seems more plausible for Onychaster. The phrynophiurid ophiuroids evolved in the Devonian. The phrynophiurids, which include Onychaster, are suspension-feeders and possess arm morphology such that they could climb and cling to narrow objects by coiling the arms (Spencer and Wright, 1966). The development of this climbing and coiling ability coincides with the oldest reported occurrence of ophiuroids preserved in close association with crinoids [Devonian (Schmidt, 1942)]. Other preserved examples are known throughout the Mississippian (Wachsmuth and Springer, 1897; Lane, 1973) and in the Jurassic (Austin and Austin, 1843-1849). Ophiuroids are preserved wrapped around or intertwined with camerate and inadunate crinoids in the Paleozoic and with articulate crinoids later. At individual localities, Onychaster displayed host specificity. Wachsmuth and Springer (1897, p. 566) reported the following associations at Mississippian localities in Indiana: Indian Creek, Onychaster is found only on Actinocrinus multiramosus Wachsmuth and Springer; Canton, Onychaster is preserved on A. multiramosus and on almost all specimens of Scytalocrinus robustus (Hall). This high degree of host specificity during the Mississippian further indicates that the ophiuroid-crinoid association is not a preservational fluke, but that it represents a true biotic relationship.

404

Chapter 9

405


Table IV.

Host Specificity of the Two Platyceras Species That Occur at Crawfordsville, Indiana (Mississippian)a

Crinoid host Platycrinites hemisphericus (Meek and Worthen) Gilbertsocrinus tuberosus (Lyon and Casseday) Cyathocrinus multibrachiatus (Lyon and Casseday) Springericrinus magniventrus (Meek and Worthen) Cydocrinus concinnus (Meek and Worthen) Agaricocrinites a

No. of Platyceras (Orthonychia) acutirostre (Hall)

No. of Platyceras (Platyceras) equilateralis (Hall)

No. of crinoids examined

85 {25%)

4 (1%)

343

0

40 (23%)

212

0

1 (0.4%)

255

0

3 (50%)

6

0

1 (4%)

23

0

1

?

From Lane (1973].

Brachiopods attached to crinoids either as a juvenile attachment or as a permanent domicile. Only strophomenid brachiopods are attached to crinoids, and this relationship was present from the Devonian to the Permian (with no reported Pennsylvanian occurrences) (Fig. 6C). Chonopectus Hall and Clarke (Muir-Wood and Cooper, 1960) and Mississippian productids (Waters, 1977) are brachiopods reported to have attached to crinoid columns and other erect cylindrical objects as juveniles. Two or more anchor spines centrally positioned along the hinge line cemented juveniles to columns. At a time when the juvenile was sufficiently large to survive on the substratum, the spine attachment would break, allowing the brachiopod to fall to the seafloor. In addition, other strophomenids took advantage of a high attachment position throughout their life (Etheridge, 1880; Grant, 1963; Ramovs, 1964). Mcintosh (1980) has recently reviewed the commensal relationships displayed between crinoids and two tabulate corals [Antholites specious Figure 6. Examples of crinoid epizoans. (A) Reconstruction of the tabulate corals Cladochonus (below) and Emmonsia (above) attached to a crinoid column (redrawn from Hudson et al., 1966, Fig. 5). (B) Gall of Myzostoma tenuispinum Graff on the arm of a recent crinoid (from von Graff, 1884, Plate 13, Fig. 11; Welch, 1976, Text-Fig. 1). (C) Reconstruction of the brachiopod Linoproductus angustus King at various ontogenetic stages attached to a crinoid column (from Grant, 1963, Text-Fig. 1; used with permission of the Society of Economic Paleontologists and Mineralogists). (D) Reconstruction of Platyceras attached to the crinoid Platycrinites (from Bowsher, 1956, Fig. 4a; used with permission of the American Museum of Natural History).

406

Chapter 9

Davis and Cladochonus antiquo (Whiteaves)]. In the Devonian examples studied by Mcintosh, these corals are only found attached to columns on which they are commonly positioned around the entire circumference. Stereomic overgrowths by the crinoid host were common. Favositids, clearly on a living host, have been reported from the Silurian and Mississippian by Halleck (1973) and Etheridge (1880), respectively. Cladochonus is known also from Mississippian rocks where it is a common commensal. Lane (1973) demonstrated that Mississippian Cladochonus from Crawfordsville, Indiana, attached to a living crinoid host (Fig. 6A).

5.3.

Stereomic Malformations

In 1793, Ure recognized anomalously shaped crinoid pluricolumnals in the Carboniferous of England and identified them as scar tissue from broken cirri. Malformed crinoid pluricolumnals have continued to draw the attention of paleontologists ever since. Despite their recognition, the origin of the various malformations has remained problematic. Although some malformations are clearly a pathologic response to the presence of an encrusting epizoan, other malformations include pits and boreholes with or without associated galls or enlargements of affected stereom. Arms, calyx plates, and the column of crinoids were all subject to attack. Whereas acrothoracian barnacles, ctenostome bryozoans, and clionid sponges produce diagnostic boreholes, the pits or boreholes on crinoids are usually circular to elliptical and undiagnostic. The classification used here is based on number, size, and shape of pits and the presence and symmetry of associated stereomic enlargements. This scheme is presented in Table V and is largely derived from three important papers recently published on malformations of Paleozoic crinoids (Franzen, 1974; Welch, 1976; Brett, 1978a). Each category may represent the activity of more than one organism; however, no further subdivisions are warranted at this time. Establishment of the relationship between the crinoid and the epizoic or boring organism is as difficult as postulating the taxonomic affinity of the attacker. Most pits are judged to represent the activity of commensal organisms or parasites rather than predators, because pits do not penetrate calyx plates and only rarely penetrate to the lumen of the column (Table V). The term pits rather than boreholes is preferred for many infestations (Brett, 1978a), because few infestations are interpreted to represent boreholes produced by a boring organism. Predaceous gastropods are commonly cited as a boring organism that attacked crinoids. Franzen (1974) believed that foraminiferans bored into

Descriptio n

Asymmetr ical spherical to ellipsoida l Parasitic Myzostom e annelid gall on crinoid arms and aboral infestation s cups with usually a single noncircula r opening to the exterior. U-shaped boring with paired Parasitic Schizopro biscina openings on lower part of arms. Yakovlev Borehole apertures may occur at sutures, and infestation induced an asymmetri cal swelling. Commensa l (some Asymmetr ical spherical to ellipsoidal Phosphan nulus gall on crinoid pluricolum nals questionab ly Muller, Nogami, and with a single circular opening parasitic) Lenz leading into a cavity inside gall. In well-prese rved specimens a phosphati c cylinder is present in gall. Symmetric al barrel-sha ped Commensa l (?) Infestation A: enlargeme nt of pluricolum nals Annular boring within with one large oval opening to column exterior. Opening is connected to an annular-sh aped boring around the lumen.

Infestation

-

Barrel-sha ped inflations type B

Type 4

Type 5

Type 2

Type 2

[Continue d)

Welch (1976), Warn (1974)

Welch (1976), Clark (1921)

Classificat ion of Classificat ion of Other pertinent references Franzen (1974) Brett (1978a)

Classifica tion of Pitted, Bored, and Malforme d Crinoid Ossicles

Associatio n with host

Table V.

ttl

'-l

Q

~

"'

5:

s·0

n ....

"' :;

0

"'1

00

::s

"'i30

::s"'p,.

CD

a

n

~

00

0

s"'::s

5' ::s

"'~

Cii ....

5'

r;·

[

Commensal

Commensal (?)

Parasitic

Commensal

Infestation C: Multiple circular to ellipsoidal pits

Infestation 0: Galls on holdfast cirri

Tarrichnium Wanner

Association with host

Infestation B: Single large pit

Infestation

(Continued)

Multiple (rarely singular) circular to elliptical (rare) pits on pluricolumnals, aboral cup, and arms with or without asymmetrical stereomic enlargements. Ellipsoidal to spherical galls that form a more or less symmetrical enlargement on cirri. Usually a single elliptical opening from the exterior to a gall that penetrates to the lumen. Sinuous interconnecting furrows entrenched along numerous pluricolumnals.

Asymmetrically positioned large spherical gall on pluricolumnals with a single large deep pit.

Description

Table V.

Type 7

Excessive growth around large depressions involving several columnals Types 1 & 2

Wachsmuth and Springer (1897, Plate 1, Fig. 2). Ausich (1979) Hantzschel (1975)

Classification of Classification of Other pertinent Brett (1978a) Franzen (1974) references

~

(D

"'

co

'0

OJ

n

::r

~

0


409

Silurian columns from Gotland, Sweden, and Girty (1915) attributed boreholes to sponges. However, none of these agents appears to represent the borer. As discussed by Brett (1978a), no compelling evidence from the Silurian material suggests that foraminiferans bored. Also, there may have been no Paleozoic boring gastropods (Carriker and Yochelson, 1968), although several authors disagree with this view (Rohr, 1976; Ausich and Gurrola, 1979; and others). Even if predaceous gastropods were present in Paleozoic communities, what possible benefit could be derived for a predator by boring part way into a crinoid column? Although mesodermal tissue does exist within the stereomic skeleton of crinoids, this tissue would presumably be of little nutritional value. In general, boreholes of a predator are systematically positioned on their prey and most commonly penetrate the entire thickness of shell material (Carriker and Yochelson, 1968; Ausich and Gurrola, 1979). For the reasons stated above, it does not seem reasonable to assign boreholes on crinoids to the work of predatory gastropods. If not gastropods, what organisms made the boreholes? Although the taxonomic affinity is unknown, the organism that produced multiple pits (infestation C) on crinoid stems and cups has commonly been considered a suspension-feeding commensal that used the epizoic habit as a means to position itself above the sediment-water interface for feeding. As such, the pits represent shallow domichnial traces (dwelling trace fossil), which helped the commensal to obtain a secure attachment. An alternative interpretation may be that infestation C represents a domichnial trace of a parasitic gastropod. Lutzen (1972) has studied the occurrence of Goodingia, a prosobranch gastropod on crinoids. It is parasitic, forms pits on the outer stereom surface, and occurs as multiple pits. More work needs to be completed on Goodingia and its allies. The pits (infestation C) occur singly or most commonly as multiple boreholes and are present on columns, dorsal cups, and rarely on arms. Individual pits are circular or slightly elliptical (rare) in outline, paraboloid in shape, and generally shallow. Individual pits do not interconnect on multiple infestations. The stereomic swelling resulting from this boring activity is most commonly a localized enlargement that produced an asymmetrical swelling with respect to the longitudinal axis of the column. Multiple pits with or without swelling were probably produced by the same commensal group. As discussed by Brett (1978a), on complete individuals with multiple infestations, the pits on the column are accompanied commonly by stereomic swellings, whereas the pits on the aboral cup are not. Franzen (1974, Fig. 6) illustrated a specimen displaying the same phenomenon, and a perusal of crinoid literature bears out this generality. For examples, see the following: Silurian, Franzen (1974); Devonian, Schmidt (1942); Pennsylvanian, Girty (1915) and Moore and

410

Chapter 9

Plummer (1940); Permian. Wanner (1916) and Fabian and Strimple (1974a). Examples of multiple pits with or without associated stereomic swellings are known from every Paleozoic period (Fig. 4) from the Silurian to the end of the era. One type of crinoid column infestation contains associated phosphatic material (Etheridge. 1880; Warn, 1974; Welch. 1976). These are circular to ellipsoidal stereomic swellings that are typically asymmetrical swellings with a central cavity. They have a single circular opening to the exterior and were generally considered to have been myzostomid infestations (Warn, 1974). In 1976, Welch demonstrated that a phosphatic cylinder penetrated from the circular opening into the column. Adaxially the cylinder flares to a funnel shape within the column (Welch, 1976, Plates 1, 2). Welch suggested that phosphatic cylinders were attachment bases of the hyolithelminthid Phosphannulus. The temporal range of the Phosphannulus association is from the Ordovician to the Permian and perhaps in the Jurassic. The occurrences of the Silurian and Jurassic examples are questioned, because no phosphatic cylinder was associated with the gall, even though the gall morphology is most similar to this infestation type. The Jurassic assignment is also doubted, as it would extend the range of the hyolithelminthids, which are thought to be Paleozoic organisms. The adaxially expanded terminus of the phosphatic cylinder of Phosphannulus is most commonly in the adaxial position of the gall chamber and may or may not penetrate to the lumen. Welch (1976) reasoned that the Phosphannulus holdfast became attached to the exterior of the holdfast during a juvenile stage of column development. The column would have secreted stereom over the cylindrical holdfast to produce a gall. Because some holdfasts do penetrate the column lumen, interpretation of the Phosphannulus life habits is questioned. Welch (1976, p. 224) suggested two alternative life styles: where the lumen was tapped. Phosphannulus individuals were facultative parasites; and where the lumen was not penetrated, the Phosphannulus animal was a suspension-feeding epizoan. The primary life habit of Phosphannulus was probably that of a commensal suspension-feeder. Penetration of the Iuman by the holdfast may simply be a fortuitous phenomenon. If some Phosphannulus were parasitic, this probably represents a derived habit of some phosphannulids developed throughout their long association with stalked crinoids (Welch, 1976). Infestations A and B each had peculiar morphologies and most certainly represent the activity of suspension-feeding commensals (for the same arguments as presented for the multiple borings). Both of these borings were reported by Franzen (1974). Infestation A is an annular borehole that encircled the lumen. A single large elliptical opening connected both ends of this borehole to the ex-


411

terior. Numerous columnals are affected by this infestation, and a segment of the column is swollen into a barrel shape symmetrical about the longitudinal axis of the column. Franzen (1974) attributed this boring to the work of a parasite, yet she stated that the annular boring did not penetrate the lumen. A commensal suspension-feeding habit is more plausible for this borer. Infestation B is a single large pit on a large spherical enlargement (Franzen, 1974, Fig. 8). The spherical enlargement is a knot on the side of a stem and therefore is asymmetrical with respect to the longitudinal axis of the column. Infestation B is known only from the Devonian. 5.4.

Crinoids as Epizoans

In addition to serving as host for numerous commensals, crinoids themselves were commensal on many organisms. The problems in interpretation of crinoid epizoans parallel those of the epizoans on crinoids, as outlined above. Was the host alive and what exact relationship existed? In all cases, crinoids have been interpreted to be commensal epizoans, and we concur with this interpretation. The chronology of known associations is given in Fig. 7. Although undoubtedly an incomplete listing, stromatoporoids, tabulate and rugose corals, bryozoans, brachiopods, bivalves, and cephalopods are reported to have served as hosts for crinoid holdfasts in the Early and Middle Paleozoic (Faber, 1929; Halleck, 1973; Franzen, 1977; Strimple, 1977). Brachiopods are also reported as hosts in Jurassic communities (Hess, 1975). Not included in Fig. 7 is the association between crinoids and logs. During both the Devonian (Mcintosh, 1978) and the Jurassic (Seilacher et al., 1968), crinoids are reported to have attached to floating logs and assumed a pseudoplanktonic existence. Although this does not represent a biotic interaction, this particular encrusting habit results in an unusual life habit among crinoids. In Holocene communities, comatulid crinoids are commensal epizoans on numerous organisms including sponges, corals, and octocorals (Meyer, 1973a; Meyer and Macurda, 1980). The geological extent of these recent associations is unknown. Last among crinoid interactions are crinoids that are epizoic upon other crinoids, both between the same and different species. In certain Holocene comatulids, juveniles of the pentacrinoid stage are epizoic on conspecific adults. Juveniles either extend from brood pouches (Hyman, 1955) or are attached to cirri (Springer, 1920). This is perhaps an early developmental manifestation of gregarious behavior and provides the juvenile with a secure attachment site. Adult comatulids attached to the columns of living stalked crinoids were observed by Macurda and Meyer

----

412

(j)

0 ·e0 (.)o~ :c ai.r::.c. c.