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Epibiont Preservational and Observational Bias in Fossil Marine Decapods

Posted on: Thursday, 9 September 2004, 06:00 CDT

ABSTRACT-

Epibionts on both living and fossil decapod crustaceans may serve as valuable proxies for paleoecological factors such as behavior and environment. Prevalence of epibionts, as observed primarily on the carapaces of fossil brachyurous decapod crustaceans, appears to be less than observed on living crabs, based upon observations in the literature, and from the study of a limited preserved biological and fossil collection. Among these factors, the three most important are that many extant epibionts do not possess skeletal structures and, therefore, are unlikely to be preserved; the epicuticle upon which epibionts attach to living brachyurans is lightly calcified and tends to be lost readily as a result of taphonomic processes; and the most common mode of preservation of fossil brachyurans is in concretions which tend to break open and leave a layer of cuticle on the counterpart, thus obscuring the potential surface of attachment of epibionts. Other factors such as the life habits of the crab, whether burrowing, burying, or remaining above the substrate; lifestyle, whether benthic or pelagic; and duration of the intermolt phase of the organism also play important roles in potential prevalence of epibionts. Careful preparation of part and counterpart remains of brachyurans as well as reference to the occurrence of epibionts in systematic studies will enhance knowledge of the host and epibiont.

INTRODUCTION

EPIBIONTS HAVE been utilized in eeological studies of both Recent and fossil organisms. The exterior and parts of the interior (i.e., gill chambers) of the host organism provide a habitat for epibionts. The nature of this habitat is controlled by the activities of the host; therefore, activities of the host affect the nature and distribution of epibionts, which can then be used to make inferences about the ecology of the host organism as well as of the epibionts. The nature of extinct organisms precludes direct behavioral observations; thus, studying epibiont distribution and prevalence is useful in reconstructing the paleoecology of the host (Brandt, 1996). As with extant organisms, preserved epibionts can be used as proxies to help understand the paleoecology of their fossilized hosts (Alexander and Brett, 1990). However, epibionts on fossil marine decapod crustaceans are less common than would be predicted from examination of living decapod populations. If epibionts are to be used as eeological proxies, taphonomic and observational effects must be understood so that the artifacts they create can be discriminated from useful paleoecologic information. The purpose of this paper is to examine the reasons for the disparity in numbers of epibionts observed on extant arthropod faunas as compared with the lower prevalence of epibionts found in fossil populations of one major group of decapods, the crabs. The term "prevalence" as used here refers to the percentage of hosts fouled in a population (Margolis et al., 1982). We propose several possible taphonomic and observational biases that result in the lower epibiont prevalence observed in fossil decapods.

Many of the epibiont preservational biasing processes discussed here are unique to arthropods. The structure of the arthropod cuticle and system of molting during growth of arthropods require that preservation of epibionts be addressed separately for this group. The nature of the taphonomic and preservational factors discussed here precludes application of strictly biologic concepts and procedures to the fossil record. Works on epibionts of extant decapods combined with the consideration of preservational biases discussed in this study will be crucial to studies of epibionts on fossil arthropods and their use as paleoecological proxies.

BACKGROUND ON FOULING ORGANISMS

Terminology.-The terminology surrounding epibionts has been extensively reviewed and discussed (Margolis et al., 1982; Overstreet, 1983; Ross, 1983; Wahl, 1989; Taylor and Wilson, 2002). This study exclusively concentrates on organisms that attach to the skeletal surface of the decapod cuticle; thus, relationships such as that of epibionts fouling mollusk shells inhabited by hermit crabs are excluded. The more general term epibiont, "organisms growing attached to a living surface" (Wahl, 1989, p. 175), is used even though the majority of epibionts considered are animals and could be considered epizoans. Discussion of the symbiotic or parasitic nature of the epibionts is beyond the scope of this paper.

Extant decapods as substrates.-Almost any surface exposed to seawater will become fouled (Wahl, 1989), and lack of available substrate is often the limiting factor for fouling organisms (Connell and Keough, 1985). Decapod crustaceans often populate soft sediments and provide some of the only hard substrates suitable for epibiont attachment (Abello el al., 1990; GiIi et al., 1993; Abello and Corbera, 1996). Thus, decapod cuticle is an attractive substrate for epibionts. Some species of crabs are gregarious, increasing settlement opportunity and, therefore, their attractiveness as an epibiont niche (Abello et al., 1990). A four-stage model of the fouling process was proposed by Wahl (1989), which included: biochemical conditioning, bacterial coloni/ation, colonization by unicellular eukaryotes, and colonization by multicellular eukaryotes. Although unicellular organisms can scar the cuticle surface (Nagasawa, 1987), this study will only consider the last stage of colonization, multicellular eukaryotes. The other stages involve organisms with extremely low preservation potential or ones that exist at scales too small for recognition with the methods used. Jakobsen and Feldmann (2004) suggest novel preparation methods that may make possible increasingly small scales of observation to resolve these other mostly unrecognized interactions in fossil material.

Some crabs actively seek anemones and sponges as epibionts that may be used for camouflage, and in some cases, as an emergency meal (Carlisle, 1952; Cutrcss et al., 1969; Abello et al., 1990). These biotic relationships do not affect skeletal components and therefore have low preservation potential and are not considered further.

Crabs, like all organisms, can be encrusted before or after death. In the study of fossil populations, the timing of encrustation is important, although both encrustation during life or after death provides ecological and taphonomic data (Brandt, 1996). If epibionts appear on the exterior surface of the carapace we can conclude that they may have infested the animal during its life. If the epibionts are positioned to take advantage of currents generated by the animal or to seek protection, then the argument is further strengthened (see Taylor and Wilson, 2003 for other criteria). If they were found on the underside of the cuticle, they must have been emplaced on a molt or corpse with the viscera removed (Jakobsen and Feldmann, 2004).

TABLE 1-Table of all known fossil occurrences of epibionts on decapods, "located on claw.

Epibionts as ecological proxies.-Paleontologists are accustomed to using indirect methods to reconstruct paleoecological information; it is interesting that the usefulness of epibionts in studying the ecology of extant decapods is such that biologists also use them to study living populations. A biological understanding of these host-epibiont associations is obviously important for the paleontologist who wishes to use them as modern analogs in paleoecological studies.

Neontologists studying decapods utilize epibionts to study indirectly the ecology of the host organisms (Abello et al., 1990; Shields, 1992; GiIi et al, 1993; Abello and Corbera, 1996; Key et al., 1996a, 1997; Fernandez-Leborans et al., 1997; Gordon and Wear, 1999). Epibionts have been used to test for the presence of terminal molts (Abello et al, 1990), burrowing frequency (Abello et al., 1990), changes in burrowing behavior with ontogeny (Barnes and Bagenal, 1951), size of organisms at sexual maturity (Abello et al., 1990), intermolt duration (Barnes and Bagenal, 1951; GiIi et al, 1993), and age of host (Botton and Ropes, 1988).

Record of fossil epibionts.-Epibionts preserved on fossil decapods are not often observed. A nonsystematic search in museum collections for evidence of fouling has been conducted by one of us (RMF) over the past two decades and has yielded almost nothing. There are several possible explanations for this scarcity. However, there are many organisms with durable exoskeletons known to encrust decapods that should be anticipated as epibionts. These include some Foraminiferida, Hydrozoa and Scleractinia, Bryozoa, Brachiopoda, Pelecypoda, Polychaeta, and Cirripedia. Table 1 lists all published occurrences of epibionts on the cuticle of fossil decapods known to us. Notably absent are the Foraminiferida and the Scleractinia. The former may be explained by the relatively small size. The latter may simply be uncommon (although see Jakobsen and Feldmann, 2004); scleractinians are rarely reported as epibionts on extant organisms.

TABLE 2-Table of fouling prevalence of extant arthropods gathered from the literature. The specific literature was selected because it provided details o\f epibiont prevalence and contained a broad range of taxa.*true crab, #marine isopod, [dagger]lobster, horseshoe crab. Total prevalence is based on the total number of hosts and the total number of fouled hosts.

MATERIALS AND METHODS

To ascertain the prevalence of epibionts on extant arthropods, the neontological literature was surveyed. Studies of fouled arthropods include horseshoe crabs, isopods, stomatopods, lobsters, and true crabs. Paucity of studies utilizing only true crabs, and the functional similarities of these other marine arthropods in terms of structure of the cuticle and large fused segments, make the inclusion of the noncrab arthropods in this data set desirable. Although most of the data used to develop our taphonomic model is based on crabs, other arthropods share similar cuticle and preservation styles with true crabs and therefore are included when possible. The tabulated fouling data for neontological occurrences includes only metazoan epibionts that appeared on the external surface of the cuticle (Table 2). Epibionts, although common in the branchial chambers of crabs (Jeffries et al., I989a, 1992), were excluded from these figures because they would be unlikely candidates for the fossil record.

Epibiont prevalence in extant material was also measured from the preserved biological collection housed in the Kent State University Geology Department. All complete or nearly complete decapods in the collection were studied, regardless of taxon or locality. All preserved specimens in the collection were visually examined for epibionts and all occurrences recorded. Three hundred and fifty- four extant decapods across 16 superfamilies were observed. Decapods that exhibited algae as the only visible epibiont were included with the unfouled specimens because the algae have little chance of being preserved in the fossil record. All other macro-epibionts were included.

To determine the epibiont prevalence of fossil crabs, the fossil collection at the Kent State University Geology Department was surveyed. Only crabs with more than 95 percent of the dorsal carapace exposed were selected. Two hundred and seventy-eight crabs across seven superfamilies were selected from the catalogued fossil collection. A stereoscopic microscope (25) was used to examine all specimens for epibionts. Crabs were selected without regard to geologic age, taxon, and locality by systematically proceeding through the collection counting all the crabs that met the criterion. This systematic approach ensured that the samples were from diverse ages and taxa. Thus, this was a nonselective sample of fossil decapods, not a sample of one fossil assemblage, although the number of species in each taxon in the collection varied. The fossil crabs were prepared at different times and by different people. The effect this may have had on the epibiont prevalence is unknown.

FOULING PREVALENCE: PAST AND PRESENT

Extant arthropod fouling.-Review of the neontological literature showed an average epibiont prevalence of 38 percent (Table 2) as reported from studies of six crab, two horseshoe crab, one lobster, and one marine isopod population(s).

Specimens from the preserved biological collection included members of the true crabs (infraorder Brachyura), clawed lobsters (infraorder Astacidea), false lobsters and false crabs (infraorder Anomura), Spanish lobsters (infraorder Palinura), mantis shrimp (order Stomatopoda), and various shrimp. Of these, 10.2 percent of the total number examined exhibited epibionts. In half of the decapod superfamilies studied (Galatheoidea, Cancroidea, Hippoidea, Coenobitoidea, Paguroidea, Nephropidea, Alpheoidea, and Penaeoidea), no epibionts were found. Although we did not have a large enough sample to determine trends in epibiont prevalence among decapod families, it appears that the prevalence was significantly higher in the Majoidea (spider crabs), similar to Becker's (1996) findings. Spider crabs neither burrow nor bury themselves and thus are consistently exposed to fouling.

Fossil decapod fouling.-Of the 278 fossil crabs studied, only one individual was found to possess an incrusting serpulid worm on the protogastric region of the dorsal carapace and another serpulid on a walking leg (Fig. 1). This one encrusted crab out of 278 crabs makes the fouling prevalence on carapaces of the fossil crabs we surveyed 0.4 percent. Sixty-one percent of the crabs observed in this study were preserved within concretions with both a part and counterpart available for study. The vast majority of these were concretions split along an internal lamination of the cuticle, and therefore the outer surface of the cuticle (epicuticle) was not exposed for examination. Legs and ventral surfaces were rarely exposed for study. This means that the 0.4 percent fouling frequency is only the observed value and the actual rate is likely to be higher. The other crabs, some preserved in concretions and missing the counterpart, and others not preserved in concretions, most likely did not possess a preserved epicuticle that would have been the substrate of epibiont attachment, further reducing the reported prevalence.

In the data we have collected on extant epibionls, prevalence ranges from 10 to 38 percent. Epibionts are not evenly distributed across taxa or populations, as will be discussed later. The patchy epibiont distribution in combination with the small and diverse sample size explain the high variance in the extant decapod fouling rates. In addition, the fouling rates collected from the biologic literature were from studies that focused on epibionts and therefore some are undoubtedly enriched in heavily encrusted populations.

The observed epibiont prevalence of 0.4 percent as observed in the fossil crab collection at Kent State University (KSU), combined with the few reports of fossil crabs with epibionts and our personal observations compared with the prevalence of epibionts on extant populations, clearly show the fossil record is anomalously poor in observed epibionts. Quantification of the disparity will have to wait until large populations on similar fossil and extant taxa can be examined.

DECAPOD TAPHONOMY

Before the specific mechanisms of epibiont loss are discussed, the larger bias against arthropod preservation must be considered. Mikulic (1990) noted that the arthropod fossil record is especially patchy and systematically controlled. This taphonomic filter to which all fossils are subject immediately complicates comparisons of extant and fossil populations. Most arthropods do not possess calcified cuticle; only the crustaceans, trilobites, and millipedes have cuticle containing calcite (Mikulic, 1990; Plotnick, 1990). Possession of uncalcified cuticle greatly reduces the chances of arthropod preservation (Plotnick, 1986). The decapod crustaceans include the shrimp, lobsters, and crabs; of these, the lobsters and crabs have the thickest and most heavily calcified cuticle, whereas the shrimps tend to have thinner and more poorly calcified cuticle (Bishop, 1986). The fossorial (burying or burrowing) shrimp have higher chances of preservation than the pelagic shrimp (Bishop, 1986).

Decapod corpses or molts have an even lower chance of survival due to effects of mechanical breakdown (Schfer, 1972; Lincoln and Parsons-Hubbard, 2000) and scavenging (Tshudy et al., 1989). Molts or corpses that spend time on the sea floor typically tend to be decomposed or scavenged (Tshudy et al., 1989; Lincoln and Parsons- Hubbard, 2000). Experience of working with decapod fossils and published experimental taphonomic studies on arthropods leads us to conclude that many, if not most, decapod fossils are the result of rapid burial. Feldmann et al. (1999) described such a rapid burial event from the Cretaceous of Colombia that we believe to be typical of decapod preservation. However, Jakobsen and Feldmann (2004) provide a striking exception; the population they studied from the Paleocene of Denmark has extensive fouling of the underside of the cuticle and therefore must consist of molts or corpses in which the viscera have decayed (Jakobsen and Feldmann, 2004). In general, decapods are not subject to the time-averaging to which other more durable organisms are subject.

Mikulic (1990) and Bishop (1986) summarized our current knowledge of decapod taphonomy. Bishop (1986) grouped the processes that result in our final knowledge of fossil decapods as follows: 1) biologic effects including habitat and ecology; 2) taphonomic effects; and 3) effects of collection and publication. The intrinsic effects of biology and the extrinsic effects of taphonomy, collection, preparation, and observation provide a useful framework for discussion of epibiont preservational biases. It must be remembered that isolating these steps for organizational purposes is useful; but these processes are interconnected and the distinction is somewhat artificial.

FIGURE 1-Panopeus prosakrolophos Schweitzer, 2000 (Eocene). 1, Counterpart; 2, part; 3, 4, basal attachment surfaces of serpulid worms attached to counterpart of hepatic region (3) and pereiopod (4).

EPIBlONT PRESERVATIONAL BIAS-INTRINSIC FACTORS

Patchiness of epiblont distribution.-Epibiont prevalence on decapods can be variable among populations of sympatric species and patchy among populations of the same species separated by relatively short geographic or temporal distances (Barnes and Bagenal, 1951; Williams and Moyse, 1988; Abello and Corbera, 1996; Becker and Wahl, 1996). Many decapod populations seem to be little fouled (Ross, 1983). In a study of 47 species of malacostracan arthropods, Becker (1996) found that most of the taxa were not heavily fouled. These reports contrast with studies of heavily fouled populations observed elsewhere (Williams and Moyse, 1988; Jeffries et al, 1989b; Key et al., 1996b). The variance seen in these epibiont prevalences is high, even among interspecifi\c and intraspecific populations and must be considered when populations of fossil or extant crabs are compared. Factors leading to patchy epibiont distribution among populations, including habitat and behavior of both the epibiont and host, are summarized in Table 3.

Decapod hosts may engage in antifouling activities, a behavior that may explain why some species have lower occurrences of epibionts than that recorded on artificial substrates (Mori and Zunino, 1987; Becker, 1996; Becker and Wahl, 1996; Key et al., 1996b). Becker and Wahl (1996), in a series of experiments to test for antifouling mechanisms in crabs, concluded that behavior such as burrowing played the largest role in antifouling. Antifouling strategies such as grooming are partly adaptations to keeping the cuticle free of fouling organisms. Experimental studies have shown than when grooming appendages are removed, a marked increase in fouling results (Bauer, 1989). In general, most arthropods are able to keep their sensory organs free of epibionts by grooming them; body grooming, however, is less universal (Bauer, 1981). Decapod body plans are correlated to locomotion, and these body plans also seem to be correlated with the amount of body grooming. The natant decapods (shrimp) engage in the most extensive grooming. The macruran and brachyuran decapods, which are not as dependent on swimming, and therefore are less concerned with body drag, do not engage in general body grooming, with few exceptions (Bauer, 1981).

TABLE 3-Factors leading to the patchy prevalence of epibionts among decapod populations, "populations of the same species separated by short distances, "related to behavior and molting frequency.

In light of this patchiness, even excluding any taphonomic or observational bias, it is clear that not all fossil decapod populations would be expected to show signs of epibionts. If decapod populations are not time-averaged and are rapidly buried communities, epibiont patchiness should be the rule in decapods more often than in other groups with more durable skeletons.

Ontogeny of fossil organisms.-Juvenile crustaceans have low fouling rates due to frequent molting during this stage of rapid growth (Barnes and Bagenal, 1951; Abello et al., 1990; Jeffries et al., 1992; Maldonado and Uriz, 1992) and behaviors that change during ontogeny such as a decrease in time spent in cryptic habitats (Barnes and Bagenal, 1951). The lower prevalence rates associated with juveniles are more strongly related to shorter intermolt duration than to the smaller surface area of juveniles (Abello et al., 1990). Barnes and Bagenal (1951) reasoned that lobsters under 11 cm had lower numbers of epibionts because they tended to bury themselves completely, unlike the adults.

If a fossil population is enriched with juveniles (molts or corpses), either for taphonomic reasons or because younger crabs live in different environments than their adult counterparts, the population would be expected to have lower epibiont prevalences. This biasing factor is unique to organisms that molt or shed their skin during growth.

Senescence, either accompanied by a terminal molt or just an increase in intermolt duration, will increase fouling rates (Shields, 1992). Gordon and Wear (1999), in a study of 241 Ovallpes catharus (White, 1843), found that the fouled crabs were often old, with signs of cuticle damage and missing limbs. Increased intermolt period also allows increased growth time for epibionts. Longer growth times will result in larger epibionts, and these larger epibionts will increase the likelihood of recognition during study of fossil decapods.

Epibiont distribution on the host.-Epibionts on living decapods are not limited to the dorsal carapace (Barnes and Bagenal, 1951; Abello et al., 1990; GiIi et al., 1993; Key et al., 1996a, 1996b, 1997, 1999a; Fernandez-Leborans et al., 1997; Gordon and Wear, 1999). However, the fossil record is enriched in the dorsal carapaces of decapods (Jakobsen and Feldmann, 2004) and, therefore, a nonrandom prevalence and distribution of epibionts will be observed in fossils. This enrichment of the fossil record in dorsal carapaces may be controlled taphonomically and by collection bias. Fragmented cuticle and small bits of appendages are not always collected. Many of the epibionts on extant arthropods in the surveyed literature, even if calcified, were not present, or were present in reduced numbers, on the dorsal carapace. The combination of nonrandom epibiont distribution and significant enrichment of dorsal carapaces in the observed decapod fossil record are major factors explaining the lower epibiont preservation in fossil populations.

Host pathologies.-Any condition that increases the length of the intermolt period will increase epibiont prevalence and percent epibiont cover by affording epibionts more time to foul the surface. A range of pathologies may increase intermolt duration or stop molting altogether. An example of such pathology is an infestation by rhizocephalan barnacles. Crabs that suffer parasitic castration from rhizocephalan barnacles show fcminization of males (broadening of the abdomen) and a reduction in molting frequency in both sexes when infected (O'Brien and Skinner, 1990; H0eg and Ltzen, 1995). Thus, this parasitic condition causes a marked increase in fouling rates in extant crab populations (Weng, 1987; Shields, 1992; Abello and Corbera, 1996; Gordon and Wear, 1999) but may leave no direct evidence of the former presence of the barnacles on the crab. This parasitic condition is common among crab populations (Schfer, 1972, p. 138) and has also been recognized in fossil crab populations (FeIdmann, 1998). The prevalence of these rhizocephalan barnacles infecting crabs can be as high as 70 percent in a given population (Takahashi and Matsuura, 1994); Thomson (1951) found that barnacle prevalence ranged from 5 to 30 percent in crab populations in Moreton Bay, Australia. The evidence of this parasitic condition in the fossil record suffers from its own set of strong taphonomic and observational biases, mainly that a sufficient number of ventral surfaces needs to be exposed, which is uncommon in the fossil record (Feldmann, 1998).

Increased prevalence of epibionts may never be correlated with confidence to a pathologic condition in the host, but host pathology must be considered when observing fossil populations, especially because the presence of pathologic specimens may be more common than thought.

Epibiont ecology through time.-Decapods range as far back in the stratigraphie record as the Late Devonian (Schrm et al., 1978) and crabs possibly to the Mississippian (Schrm and Mapes, 1984). By the Mississippian, most taxa with epibiotic guilds had evolved. Encrusted trilobites occur as early as the Late Ordovician (Brandt, 1996). Lower epibiont prevalence in fossil decapods due to lack of encrusters seems unlikely.

Coevolution of epibiont associations cannot be ignored. Some epibionts are host specific (Cutress et al., 1969; GiIi et al., 1993; Abello and Corbcra, 1996; Key et al., 1999a). Subtle changes in host selection could affect encrustation rates as paleocommunities evolved or changed due to introduction of invading species or events that altered the ecosystem structure in both the short and long term. An example of the close association of epibionts with their host species is shown in a ctenostome bryozoan that has a reproductive cycle synchronized with the molting of a shrimp (Eggleston, 1971).

FIGURE 2-1, Weakly calcified bryozoan peeling off lobster claw (Recent); 2, balanomorph barnacles on Recent portunid crab, note basal plate of barnacle, indicated with arrow.

Bryozoans, common decapod encrusters, have shown a trend toward an increase in encrusting species on hard substrates through time (McKinney and Jackson, 1991, p. 92); it is not clear how this trend would have affected decapod epibiont prevalences. If an increase in bryozoan species diversity is accompanied by an increase in niche diversity, then the prevalence of bryozoan epibionts on crabs may indeed increase following this trend if unrealized niches associated with crabs existed and could be exploited. At this time, the combination of the taphonomic biases reducing epibiont prevalence described here and the low resolution and spotty preservation of decapod faunas (Bishop, 1986; Mikulic, 1990) make this hypothesis difficult to test.

EXTRINSIC FACTORS

Soft-bodied epibiont loss.-The most obvious and possibly the most important factor resulting in epibiont loss on fossils is the decomposition of epibionts without mineralized skeletons. Soft tissues are subject to rapid degradation and are only preserved in unusual circumstances (Briggs, 2003). Soft-bodied epibionts that encrust decapods include algae (Overstreet, 1979), annelids (Overstreet, 1979), ciliates (Fernandez-Leborans et al., 1997), hydrozoans (Vader et al, 1981), uncalcified or weakly calcified bryozoans (Fig. 2.1), and sponges (Maldonado and Uriz, 1992). Under most conditions, there is little hope for these uncalcified epibionts to be preserved (Brandt, 1996). The skeletal epibionts that frequently foul decapods are some calcareous hydrozoans, bryozoans, annelids, and barnacles.

Not all bryozoans are calcified; the degree of calcification and mineralogy also varies. Bryozoans of the class Stenolaemata and Cheilostomata are calcified, whereas the order Ctenostomata in the class Gymnolaemata are not calcified, although some produce borings (McKinney and Jackson, 1991; Taylor et al., 1999). The calcite/ aragonite and Ca/Mg ratios of bryozoan skeletal elements vary within and between taxa (Smith et al., 1998). Encrusting bryozoans are more likely to contain aragonitic or exhibit a mixed skeletal mineralogy (Poluzzi and Sartori, 1975; Smith et al., 1998). Ctenostomes, which are common epibionts of decapods, are not calcified and, unless they produce boringsor have undergone bioimmuration, have a very low fossilization potential. Aragonitic skeletons that are common among the encrusting bryozoans further lower the fossilization potential of this phylum, because lightly calcified or aragonitic cheilostome bryozoans are subject to recrystallization and taphonomic loss (Taylor et al., 1999).

Serpulid worms are another common epibiont recorded on decapods. Serpulid worms or worms with agglutinated tests have a high chance of preservation, and they are one of the commonly recognized fossil epibionts observed on crabs (Table 1).

Barnacles are well-known and common fouling organisms. Balanomorph barnacles with their heavily calcified skeletons have a high likelihood of preservation. The calcified basal disk cemented to the host has a high potential of remaining attached to the host cuticle even if the plates are lost (Fig, 2.2). Pedunculate barnacles, with fleshy stalks, suffer from reduced preservational potential. Even if individual calcified plates may be preserved, the preservation of the plates in close association with their fossilized host is unlikely as these plates disarticulate after death (Schfer, 1972, p. 122). We have not serially sectioned crabs to look for pedunculate barnacles contained within the branchial chambers of fossil crabs; such preparation techniques may allow recognition of the fossil association of these barnacles with their hosts.

FIGURE 3-SEM photomicrograph of Cancer antennarlus Stimpson, 1856 (Recent, dried). A, exocuticle; B, epicuticle; C, bryozoan peeling off.

FIGURE 4-I, Part (right) and 2, counterpart of Orbitoplax tuckerae Schweitzer, 2000 (Eocene). Note the exocuticle coating the counterpart. 3, Thin sections of part (bottom) and counterpart (top) of O. tuckerae showing separation of exocuticle from endocuticle when concretion split. 4, Thin section of O. tuckerae (part) showing cuticle emerging from the concretion. Note the loss of exocuticle where counterpart has been removed.

Other taphonomic effects.-Interaction of the sediment may either smother or abrade the epibionts. Fernandez-Leborans et al. (1997) reasoned that this interaction removed ciliate epibionts from their crab hosts. Siliciclastic silt and sand are especially effective scouring agents (Smith and Nelson, 2003). Taylor et al. (1999) suggested this as a mode of encrusting bryozoan removal. If corpses or molts are transported in siliciclastic environments, which are typical habitats of many decapods, a loss of bryozoans and other epibionts may be anticipated. If the assumption that most decapod remains are the result of rapid burial events, and decapod remains are easily disintegrated, then long distance or duration of transportation events most likely will result in complete loss of the cuticle rather than adding significantly to the biasing of fouling prevalence by producing 'cleaned' or fragmented carapaces.

Predation, resulting in removal of epibionts from the cuticle, is also likely to contribute to epizoan loss. Bowers (1968), in a study of pedunculate barnacles on lobster maxillipeds, found that the molts often lacked the barnacles and concluded that fish and other predators had removed the epibionts from the molts.

Epicuticle loss.-In healthy cuticle on a living decapod, the epicuticle is the outermost surface to which epibionts must attach. The integrity of this layer affects the degree to which epizoans can firmly attach and remain attached to the cuticle surface. Although the epicuticle may be degraded during the life of the host (Key et al., 1996b), that is an intrinsic factor leading to epibiont patchiness, not a result of taphonomy.

Epicuticle may also degrade after death. Experimental taphonomic studies have shown that the epicuticle does, in fact, degrade and begins to slough off with prolonged exposure to seawater after the death of the host (Lincoln and Parsons-Hubbard, 2000). Friability of the epicuticle will lead to epibiont loss, as the attachment point of the epibiont has been separated from the cuticle. The friable nature of the cuticle (Fig. 3) may act much like the self-abating paint used on boats to prevent the accumulation of fouling organisms on ship hulls. Lincoln and Parsons-Hubbard (2000), in addition to showing epicuticle loss, reported on experimentally deployed decapods and showed that with exposure, the carapace is fragmented over time and often only the thick cuticle of the claws is preserved intact. The fragmentation of exposed decapod cuticle may obliterate any detail of the epibionts because fragmentary remains are much less likely to be recognized, collected, or studied in sufficient detail.

FIGURE 5-Counterpart of a concretion bearing a nearly complete specimen of Trichopeltarion greggi Dell, 1969, with outer cuticular layers adhering to the counterpart. Note the barnacle observable where cuticle has broken away (arrow and inset).

Postpreservational biases.-Decapod crustaceans are often preserved in concretions which serve to protect the fossil remains. Most concretions do not split at the rock/cuticle interface but rather split along internal laminations in the cuticle (Fig. 4). The exposure of internal laminations on both the part and counterpart automatically precludes the recognition of any epibionts that existed. This seemingly simple observational problem may have the greatest significance for the underrepresentation of fossil epibionts on their decapod hosts. Not all concretions split in this manner, however; careful observation and recognition of just which surface is exposed may allow observation of epibionts (Fig. 5). Tshudy and Feldmann (1988) made such observations on the counterpart of concretions containing macruran decapods in which the exocuticle did not exfoliate, and they recognized serpulid worms and oysters that had encrusted the host. Careful preparation techniques that remove the exocuticle from the counterpart and subsequent casting of the resulting mold are promising preparation methods that will aid in the observation of fossil epibionts (Jakobsen and Feldmann, 2004).

FIGURE 6-Chela fragment of Scylla serrata (Forskl, 1775) (Pleistocene) Guam, two views.

Layers in fossil decapod cuticle are often planes of weakness and may separate upon weathering. Decapods that are not preserved in concretions and that either had prolonged exposure before burial or were subjected to weathering on the outcrop after exposure may result in the loss of cuticle layers and subsequently any attached epibionts. Loss of surrounding matrix during weathering, or collection, will also remove any epibionts that were not firmly attached to the cuticle surface.

Fossil crab populations commonly occur in coastal plain deposits that are subject to erosion from present-day coastal processes (Schweitzer and Feldmann, 1999; Schweitzer et al., 2002). A locality in Argentina yielded such a deposit, in which the Miocene crabs were exhumed in the modern intertidal zone, and were locally fouled with Recent barnacles. Coastal exposures like this also result in erosion of decapod material before collection (Fig. 6), and are likely to result in loss of fossil epibionts as well as the fouling of the fossil material by living organisms.

OBSERVATIONAL BIAS

In addition to the taphonomic biases that result in reduction of epibiont prevalence, observational biases may also prevent discovery or recognition of preserved epibionts. The size of the epibiont can affect the observational potential of an epibiont. Epibionts are often small and, therefore, even if they are exposed on the specimen, they may go unnoticed. They also may be observed but never recorded because the material is being described for a taxonomic work in which presence of epibionts seems irrelevant. In addition, observations of epibionts, even when recorded in the literature, may go unnoticed due to the very specilic nature of taxonomic works on the host.

FIGURE 7-Conceptual diagram showing the stages leading up to recognition of epibionts on fossil material.

The recognition that when concretions split, the cuticle is often separated along internal laminations, will enhance the search for epibionts. Time need not be wasted searching internal surfaces of the cuticle where no epibiont could have settled. Techniques described by Jakobsen and Feldmann (2004) will aid in the observation of epibionts that are preserved but located between the matrix and the cuticle. The surrounding matrix of the fossil, which creates a natural mold, should also be thoroughly examined. With conscious effort and careful observation, it is likely that more epibionts can be recognized in association with arthropod material. Once observed, the data should be published; epibiont data is an important source of information on the ecology of extinct decapods as well as the epibionts themselves.

DISCUSSION

Although the data used in this study was biased toward crabs, many of the biasing factors on epibiont prevalence should be applicable to other arthropod groups. The basic architecture of decapod cuticle appears to have been very stable over time, and the cuticle structure of extant marine decapods certainly shares the same general structure with fossil decapods of an outermost epicuticle, exocuticle, and endocuticle. It is therefore assumed that cuticle of these decapods will be subject to similar taphonomic pathways. Other arthropods, including horseshoe crabs, lack a calcified cuticle (Robison, 1987). Further work on the preservation of these other groups is needed.

Many of the discussed biases should hold true for extinct taxa, such as trilobites. The utility of epibionts as ecological proxies for trilobite ecology was shown by Brandt (1996). She used epibiont data to make inferences of both behavior and of the size of the animal at its terminal moll in an Ordovician lrilohite. Epibionts have been found to have a low prevalence on trilobites (Mikulic, 1990; Brandt, 1996)\. The preservation of trilobiles is different from decapods, most notably the seeming lack of concretions. The biologic component of taphonomic loss, such as scavenging, may also have been significantly different in the Paleozoic.

The main epibiont prevalence biasing mechanisms have been discussed and are summarized in diagrammatic form in Figure 7. These taphonomic and observational biases ultimately result in lower epibiont prevalences realized in fossil material. Fouling rates of extant arthropods are certainly higher than those recorded in the fossil record, 37 percent (Table 2) versus 0.4 percent (this paper). From data gathered on epibiont prevalence from extant populations, an expected prevalence can be calculated for that population after fossilization. This estimate is done by calculating prevalence based solely upon lhe calcified epibionts on the dorsal carapace. When these estimates were made for the prevalences of extant epibionts recorded in Table 2, the numbers were not markedly different from lhe epibionl prevalence recorded in lhe fossil material. Great uncertainly exists at this lime in all the epibionl prevalence numbers and specific conclusions cannot be made from them, but the data suggest thai soft-bodied epibiont loss, and lack of ability to observe epibionts on the dorsal carapace because of loss or lack of recognition of the cpicuticle, are lhe Iwo largesl negalive epibiont- biasing mechanisms.

The low prevalence of epibionts found on fossil decapods is not surprising given the number of taphonomic and observational controls, most of which are destructive to epibionts. With the model of epibionl preservalional biases presented here, along with preparation techniques unique Io fossil arthropods, il is hoped that the meaningful use of epibionts as ecological proxies can increase.

CONCLUSIONS

Epibiont prevalence is lower in fossil decapod populations than would be predicted from the study of extant decapod populations.

Epibiont prevalence in extant decapod populations is patchy and often low to nonexistent; even before the addition of a taphonomic bias, many crab populations would not be expected to have epibionts, let alone to have them preserved. This patchiness may be preserved in fossil decapods due to the small amount of time-averaging in fossil decapods caused by their lack of a more durable skeleton.

Fossil assemblages enriched in juveniles will exhibit a reduced prevalence of epibionts due to their more frequent molting and in some cases different behaviors than adult populations.

Loss of noncalcified epizoans is the single factor that most dramatically reduces epibiont prevalence rates recorded in fossil decapods.

The anomalously high number of dorsal carapaces preserved and recognized in fossil decapods, coupled with the observation that many epibionts occur on the ventral surface or the appendages on extant decapods, biases the fossil epibiont record, as most fossil epibionts that were not on the dorsal carapace were probably lost.

Pathology of the host, such as infestation by rhizocephalan barnacles, resulting in the loss of the ability to molt, or any other increase in intermolt duration, significantly increases fouling rates.

With exposure after death, the epicuticle, which is the epibiont attachment surface, has been shown to degrade. This negative biasing factor is tempered by the further observation that exposed cuticle is often fragmented, which results in a lower collection potential.

Concretions, by far, are the most common preservation medium of fossil decapods. When opened, concretions often break along internal laminations in the cuticle, masking the living surface to which the epibionts would have attached. The cuticle laminations lining the counterpart obscure epibionts and reduce the resultant epibiont prevalence in the fossil record.

Host specificity of epibionts is subject to ecosystem perturbations and may be expected to alter epibiont prevalence during short-term events or as a result of long-term trends.

Rocks containing fossil crabs are often subject to coastal erosion processes that result in loss of material, erosion of fossil epibionts, and emplacement of extant fouling organisms.

Reports of epibionts on extant taxa should include factors that will help predict the preservation potential of the epizoan population. Factors such as location on the host, and degree of both host and epibiont calcification will aid in predicting how the epibiont/host prevalence in a living population will be expressed following fossilization. Thus, the modem analog can be fine-tuned.

ACKNOWLEDGMENTS

The authors with to thank C. Schweitzer, of KSU, for her careful and helpful review of this manuscript. P. Scott-Smith graciously provided the specimen from Guam. N. Wells provided useful discussions along the way. M. Hubbard made helpful comments on an early version of the manuscript. Constructive reviews by M. Key Jr., Dickinson College, P. Taylor, the Natural History Museum, London, and J. M. Erickson, St. Lawrence University, substantially improved the work. A part of this work was supported by an NSF grant OPP9909184 to R. Feldmann and K. Bice.

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ACCEPTED 29 DECEMBER 2003

DAVID A. WAUGH,1 RODNEY M. FELDMANN,1 ROBERT S. CRAWFORD,1 STEN LENNAFiT JAKOBSEN,2 AND KYLE B. THOMAS1

'Kent State University, Department of Geology, Kent, Ohio 44242, USA, lt;dwaugh@kent.edu> and 2Geological Museum, University of Copenhagen 0ster Voldgade 5-7, DK-1350 Copenhagen K, Denmark,

Copyright Paleontological Society Sep 2004

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