Intertidal Bioerosion by the Chiton <I>Acanthopleura Granulata</I

Home , Acanthopleura granulata, Bioerosion

BULLETIN OF MARINE SCIENCE, 47(3): 680-695, 1990

INTERTIDAL BIOEROSION BY THE CHITON ACANTHOPLEURA GRANULATA; SAN SALVADOR, BAHAMAS

Kenneth A. Rasmussen and Eben W Frankenberg

ABSTRACT Rates of daily fecal pellet production and intertidal bioerosion by the chiton, Acanthop/eura granu/ata Gmelin, 1791 were measured along the shore of Pigeon Creek, an interior marine tidal creek on San Salvador Island. Chitons grazed upon pitted, biokarstic Pleistocene limestones which form outcrops within the intertidal zone. The low-energy, tide-dominated char- acter of the waterway fosters excellent preservation of delicate chiton fecal pellets, and allowed a more accurate, in situ measurement of bioerosion by directly counting their daily accu- mulation.

Chitons were abundant (5.5 chitons· m-2), with adults and juveniles present in a 2.8: I ratio along the exposed rocky shoreline. An average daily production rate of67.2 pellets' chiton-I was calculated from 43 individuals monitored for 4 days. Pellet counts were highly variable among days and among individuals. Organically bound, 3-4 mm long fecal pellets were 94.3% CaCO) by weight, and composed of a variety of constituent grain types and textures. Individual pellets from adults and juveniles contained about 2.1 and 0.7 mg CaCO), respectively. Assuming that the mass of carbonate deposited as fecal pellets is equal to that eroded from the coast, an annual carbonate erosion rate of 41.5 g·yr-'·chiton-' results. Combined with the 1.82 g·cm-) average density of the pelletal grainstone/packstone which they graze, a volumetric erosion rate of 22.8 cm)'yr-"chiton-' results. Using local population density, an overall bioplanation rate of 0.12 mm ·yr-I exists across the rocky intertidal zone due to the activities of A. granu/ata alone. Intertidal exposure hardens otherwise easily disaggregated chiton pellets, and may enhance their geologic preservation potential. If recognized in the fossil record, preserved chiton pellets may indicate proximity to low-energy, tide-dominated rocky shores, along which this process is most common.

Chitons (Mollusca, Polyplacophora) are common grazers of intertidal epilithic and endolithic algae along rocky carbonate coastlines throughout the world (Neu- mann, 1968; Glynn, 1970; 1973; Schneider and Torunski, 1983). Using a magnetite-enriched radula (Lowenstam, 1962), they rasp limestone surfaces during their nightly grazing activities, and in doing so erode their substrate. Despite a wealth ofinformation on bioerosion in a variety of settings (Otter, 1937; Ginsburg, 1953; Neumann, 1968; Warme, 1975; Hutchings, 1986 for reviews), the role of chitons in the process of coastal limestone bioerosion remains uncertain. The ongoing nature of epilithic grazing suggests that chitons may contribute substan- tially to long-term coastal retreat, perhaps approaching the importance of endo lith- ic biotas such as sponges or bivalves (Neumann, 1966; Riitzler, 1975; Warme, 1975), which presumably bore more episodically for shelter. Chitons may have modified marine hard substrata to some degree since their first appearance in the Late Cambrian (Smith, 1960). Earliest trace fossil evidence for bioerosion by chi tons or gastropods exists in distinctive grazing scars (Rad- ulichnus) etched upon Upper Jurassic bivalves (Voigt, 1977). The erosive potential of modem chitons in combination with other intertidal biotas has gained wide- spread recognition, though the actual amount of material which they alone remove from rocky shorelines remains poorly quantified (Trudgill, 1983; Donn and Board- man, 1988). This is primarily because chitons often live along high-energy coasts, where it is difficult to monitor grazing and defecation activities in situ. Moreover, high-energy shorelines are often eroded by wave-borne projectiles through mechanical "bombardment" (McLean, 1964). Such factors can severely influence

680 RASMUSSEN AND FRANKENBERG: INTERTIDAL BIOEROSION BY A. GRANULATA 681 intertidal community structure, as well as complicate the calculation ofa particular organism's contribution to substrate loss (Shanks and Wright, 1986). Typical rates of carbonate shoreline retreat (planation) range from 0.1-4.0 mm· yel (Hodgkin, 1964, and Trudgill, 1983, in Australia; Schneider and Torunski, 1983, in the northern Adriatic; Taylor and Way, 1976, and Trudgill, 1976, on Aldabra Atoll; Donn and Boardman, 1988, in the Bahamas). As discussed by Neumann (1968) and Spencer (1985), worldwide rates for overall coastal planation I appear to cluster around 1 mm·yr- • With reference to the chiton component, l Taylor and Way (1976) maintained that 3.4% (0.017 mm ·ye ) of the coastal planation at Aldabra Atoll is due to grazing by the small (-3.6 cm long) species Acanthopleura brevispinosa. Indirect data of Trudgill (1983) suggest that populations of the larger species A. gemmata (5.7-6.9 cm long) account for up to 34% l (0.7 mm ·ye ) of the extensive planation measured at One Tree Island, Australia. Donn and Boardman (1988) measured 2.2 mm ·yr-I overall planation at the l windward coast of Andros Island, of which they estimated 9.6% (0.21 mm·ye ) was due to the common Caribbean chiton A. granulata. Their estimate was based on the unpublished laboratory grazing experiments of McLean (1964) in Barbados, who estimated that a mid-sized (-4.0 cm long) A. granulata individual can erode limestone at a rate of 21.9 g·yr-I. Glynn (1973) has cited his own unpublished data from Puerto Rico, which indicated a comparable bioplanation rate for A. granulata populations of 0.18 mm·yr-I. He did not, however, state the method by which this value was determined. All the estimates of chiton bioplanation cited above are highly dependent upon local rock density and chiton population density (both of which vary greatly), and commonly suffer from the need to extrapolate laboratory results to the field. For these reasons, the most valuable unit quantifying chiton bioerosion may be mass of CaC03 eroded per individual per unit time, measured from a large population under natural field conditions. Table 1 summarizes the results of past. attempts to determine a per capita bioerosion rate for chitons. The only direct field measurements listed are those of Taylor and Way (1976) for A. brevispinosa. They calculated an erosion rate of I only 3.3 g·yr- .chiton-I on the basis of three individuals monitored for 3 days. The remaining studies relied upon few chitons, removed from their natural habitat, and permitted to graze on small pieces of substrate in aquaria. Laboratory measurements of bioerosion, limited to A. granulata alone, range from 17.9-54.0 I g' yr- .chiton-I. Given the paucity of rigorous field measurement of this important process, and the three-fold range of laboratory estimates for a single species, we undertook an in situ study of substrate removal, fecal pellet production, and sediment contribution by the common intertidal chiton A. granulata on San Salvador Island, Bahamas.

STUDY AREA

Pigeon Creek is a shallow, low-energy, interior tidal creek located on the subtropical Bahamian island of San Salvador. Our study was situated on the southern shore of the south branch of that waterway, approximately I krn from its mouth at Snow Bay. Daily tidal exchange at the site (range = 0.4 m) is sufficient to maintain normal, subtropical marine salinity, biota, and calcareous sediment (Mitchell, 1986). A. granulata are common along outcroppings of Pleistocene pelletal grainstone/ packstone which form the modem rocky intertidal shoreline (Fig. 1). No other chiton species was detected in the study area. Areas inhabited by chitons are interrupted by dense stands of red mangrove (Rhizophora mangle), which line substantial portions of Pigeon Creek. Limestone outcrops in the study area are either vertical, in the form of intertidal notches and nips, or subhorizontal, in the form of narrow sloping terraces (Fig. IA). Muddy calcareous sand onlaps the rock in the low-intertidal zone. The shoreline is comprised mostly of coherent limestone outcroppings, with scattered areas of broken, discontinuous rock and rubble. During the day, many chitons nestle 682 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.3, 1990

Table I. Summary of previous bioerosion rate estimates made for common intertidal chitons inhabiting rocky carbonate coastlines. Only one of the reported rates (d) was measured in situ; others may be influenced by metabolic stress, indirect calculation methods, and/or grazing range limitations

Erosion rate (g·yr-!. Reference/species Locale/substrate Method chiton-')

McLean (l964)/A. granulata Barbados/beachrock Lab (pellet wt.) 17.9" 21.9b Glynn (1973; unpubl.)/ Puerto Rico/coral rubble Lab (pellet wt.) 54.0c A. granulata Taylor and Way (1976)/ Aldabra Atoll/calcarenite Field (pellet wt.) 3.3d A. brevispinosa (gut cont.) 8.4c Hoskin et al. (1986)/A. granulata Little Bahama Bank/eolianite Lab (pellet wt.) 26.JC • Lab Test A (N = 9 chi tons, t = 24 h), defecation following unrestricted grazing of, and removal from host rock. b Lab Test C (N = I chiton, t = 24 h), defec.1lion during restricted-range grazing of host rock. o Lab results of Glynn (1973, p. 285) corrected for 94.3% Caco, content. Defecation during restricted-range grazing of host rock (N - 10-12 chitons, t - 7-10 days; Glynn, pcrs. comm.). • Pellet weights (N = 3 chitons, t = 3 days), defecation during unrestricted grazing of host rock in field. e Indirect approximation using gut mass content (N = 108 chitons) and mean % gut~contentvoided/day (N = 3, t = 3 days) following unrestricted grazing of host rock in field. r Pellet weights (N = 12 chi tons, t = 2l days), defecation during restricted-range grazing of host rock in lab.

within small depressions termed "homing pits" (Mook, 1983), which are most common on high- intertidal rock surfaces (Fig. IB). Many individuals cling beneath protected ledges, or to the inner sides of grazing "trackways." These areas form smoothed gutters on the otherwise pitted and irregular coastal biokarst. As a result, a light-tan colored band of grazed limestone 0.3-0.9 m wide appears in the intertidal zone. Encrusting coralline algae are uncommon in the band occupied by chitons. The subsurface "green line" of endolithic blue-green algae, which is observed so ubiquitously within coastal carbonate substrates worldwide, appears to be the primary food source of the chitons. Whereas wave- dominated coastal settings transport or destroy chiton pellets upon defecation, those deposited along this low-energy shoreline often remain in place and intact. Irregular bedrock topography, characterized by homing pits, trackways, and smaller-scale phytokarstic cusps ("pit and pinnacle" structure), provides ubiquitous catchments into which fecal pellets are deposited and remain relatively undisturbed. This fortuitous condition allows confident calculation of chiton bioerosion rates by directly counting daily fecal pellet production.

METHODS

Field methods consisted of censusing all chi tons present along a random section of exposed rocky coast, selecting and marking individuals or groups of individuals whose pellet production could be counted accurately (i.e., in isolated "catchment groups"), and monitoring their daily production. An accessible 99-m stretch of shoreline was divided into eight contiguous transects according to distinctive

Figure I. (A) Typical coastal structure found along the Pigeon Creek shoreline. Intertidal grazing of endolithic and epilithic algae by chitons creates a lighter band of rack 0.3-0.9 m wide, depending on outcrop slope. A. granulata individual is visible near right foot. (B) Close-up of an individual adult chiton defecating copious fecal pellets within its daytime homesite, or "homing pit." Individual pellets are about 3-4 mm long. RASMUSSEN AND FRANKENBERG: INTERTIDAL BIOEROSION BY A. GRANULATA 683

breaks in geomorphology, or the presence of other natural boundaries (e.g., mangroves). Using a tape- measure, each transect was measured for planar, or one-dimensional lineal length (LL), omitting small, cm-scale heterogeneity in the craggy rock surface. A more detailed, or two-dimensional irregular length (IL) was similarly measured, but in that case the contours of such structures were followed closely, and thereby include small-scale geomorphic details of the coast. Due to the craggy, convoluted nature of the shoreline, IL is most representative of true transect length, and was used in the calculation of surface area and chiton population density. Width of the grazed surface was calculated by making four to five measurements within each of the eight transects, and weighting the average of these in proportion to transect length. Outcrop profile was designated as vertical (;?: 60°) or subhorizontal (<60°), measuring slope with respect to the water line. Chiton population density and size distribution were determined using three replicate censuses. Individuals were designated as adults (> 3 cm) or juveniles (~3 cm), based loosely on the growth rate data of Glynn (1970). Forty-three chitons were monitored for daily fecal pellet production during each of four calm- weather days from 14-18 December 1987. This sample population was broken into 15 distinct and separate catchment groups of one to seven individuals each, chosen specifically from areas where postdepositional pellet loss was minimal. Sites characterized by deep homing pits on topographically irregular sub horizontal surfaces were optimal for this purpose. Fecal pellet production rates were determined by removing all pellets from each catchment site, and counting how many accumulated during a 24-h period. Whole pellets were counted beginning at 0900 each day. After each count, pellets were collected, or destroyed by gently brushing them with a paintbrush. Each site was then thoroughly flushed with seawater to remove disaggregated fecal material. Chiton behavior was observed each day, and during one night in order to study nocturnal feeding habits and movement. Average mass per pellet was determined by calculating the average dry mass of pellets from both adult and juvenile chitons, and weighting these according to the size-frequency distribution of individuals in the overall, natural population. CaCO, content per pellet was determined by acid digestion (10% HCI) of bulk dry pellets, followed by distilled water rinse of insoluble residues (to remove salts) during vacuum filtration (0.4 Ilm Nuclepore® filter). A standard mass of CaCO, per pellet was then calculated by multiplying overall average mass per pellet by % CaCO,. All mass, volume, and surface planation values therefore refer to CaCO, removal. Annual mass of CaCO, eroded per chiton was calculated by multiplying the standard CaCO, mass per pellet by the estimated average number of pellets excreted per chiton per year. Average density of the coastal limestone was determined from five rock chips sampled randomly from the outer I cm of grazed, intertidal substrate. This value was used to calculate rate of volumetric erosion (cm"yr-I) and overall coastal planation (mm·yr-I). Petrographic thin sections of whole chiton pellets were made after drying and vacuum impregnation with epoxy resin. Textural and constituent analyses of fecal pellets disaggregated in 20% Clorox ill> solution were made by wet-sieving the bulk material through 33, 63, 88, 125, 177, and 250 Ilm screens with buffered distilled water (Neumann, 1965). The scanning electron microscope (SEM) was used to examine constituents within these individual size fractions. We consider our calculated rate of daily bioerosion by A. granulata to be more accurate as a result of direct, in situ measurement techniques. Extrapolation to annual bioerosion levels may result in a slight underestimation, however, in light of the following biological factors: (I) chitons were monitored during winter, when metabolic activities (including grazing and substrate abrasion) are perhaps subtly subdued (Segal et al., 1953; Schneider and Torunski, 1983), and (2) measurements were made in a low-energy intertidal zone, where rock surfaces may be relatively rich in algal biomass, requiring less grazing effort (Newell et al., 1971; Mook, 1983), and presumably fostering less substrate abrasion.

RESULTS

Transect dimensions, substrate structure and irregularity, and chiton distribution and abundance for each of eight transects are shown in Table 2. Average width of the grazed, intertidal substrate was 0.46 m. Population density varied 2 from 0-15 chitons·m- , averaging 5.47 chitons·m-' overall. The ratio of adult to juvenile chitons was 2.8: 1. Continuous outcrops with a solid-vertical or solid- subhorizontal aspect (transects I, II, VII, and VIII) maintained significantly greater population densities (P = 0.007, t-test) than those which were discontinuous, broken, and/or composed largely of rock rubble (transects III, IV, V, and VI). Coastal irregularity index calculated by (lULL) ranged from 1.2 for the smoothest transects, through 2.5 for those with the most small-scale heterogeneity. Average irregularity index was 1.7, suggesting the generally craggy, convoluted nature of 684 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.3. 1990

Table 2. Areal dimensions, substrate structure, shoreline irregularity, and chiton population data for the eight studied transects. Total area censused equals 49 m2• Solid, coherent substrata invariably maintained greater chiton densities, regardless of subhorizontal or vertical aspect. Relative irregularity exerted no obvious control over population density

Irregu- Chiton population Dimensions larity index Density Transect# IL x W(m) Area (m') Substrate structure (lULL) Adult: Juv. (c·m-')

I 8.0 X 0.32 2.56 Solid-vertical 1.3 25:13 14.8 II 14.8 x 0.45 6.66 Solid-subhoriz. 1.5 40:4 6.6 III 12.8 x 0.45 5.76 Broken/rubble-vertical 2.5 12:2 2.4 IV 6.0 x 0.30 1.80 Broken/rubble-vertical 1.2 0:0 0.0 V 4.1 x 0.85 3.49 Broken/rubble-subhoriz. 1.6 3:0 0.9 VI 15.0 x 0.55 8.25 Broken/rubble-subhoriz. 2.3 10:3 1.6 VII 23.0 x 0.50 11.5 Solid-subhoriz. 1.4 61:25 7.5 VIII 15.0 x 0.60 9.00 Solid-subhoriz. 1.6 47:23 7.8 Averages 1.7 2.8:1 5.5 IL = irregular length; W = width; LL = lineal length; c = chiton. the shoreline. Irregular transects did not consistently maintain greater or lesser population densities than those with less convolution. Individual body size characteristics (L x W) and daily fecal pellet production rates for the sample population (N = 43) are shown in Table 3. Average body size was 4.8 x 2.9 cm. Body length distribution is illustrated in Figure 2. Body lengths ranged from 1.0-8.8 cm, and 63% of the chitons formed a modal group 4-6 cm long. Seventy-nine percent of the measured chitons were categorized as adults, and 21% as juveniles. This distribution nearly matches that of the overall population (N = 268), which contained about 74% adults and 26% juveniles. Average fecal pellet production for the sample population equaled 67.2 pellets' I day-I ·chiton- • The elongate, sausage-shaped fecal pellets were 2.7-4.0 mm long, and 0.6-1.0 mm in cross section. Average individual pellet weights for adult and juvenile chitons were 2.2 mg and 0.7 mg, respectively. Chitons typically did not defecate pellets until they had nearly returned to their high-intertidal homing areas each morning. Following defecation, pellets were subaerially exposed for several hours between successive high tides. During this desiccation period they hardened considerably, and became more resistant to disintegration upon sub- sequent submersion. Whereas most production values in Table 3 represent total pellets in each catchment group divided by more than one contributing member, chi tons C, L, 0, and W each occupied their own, exclusive catchment group each day. These individuals were used to estimate daily and average pellet production by single, specified chitons, and thus their respective standard deviations reflect true variations in daily output. Daily production by these chitons was highly variable, both among days and among individuals (Fig. 3). These data underscore the need for production measurements made of many chi tons monitored over several days. A typical fecal pellet from the overall population, consisting of 73.9% adults and 26.1 % juvenile~, has a weighted average mass of 1.79 mg, of which 94.3%, or 1.69 mg is CaC03• An average A. granulata individual excreting 67.2 pellets· day-I is thus capable of removing limestone at a rate of 41.5 g'yr-l (67.2 pellets' day-I x 1.69 mg CaC03'pelleC' x 365.25 days·yr-I). Our calculated lithologic density of 1.82 g'cm-3 suggests a volumetric loss of22.8 cm3·ycl·chiton-l• Local population density of 5.47 chitons·m-21eads to an overall bioerosion rate of 227 g·m-2·yr-1 across the exposed shoreline, or a surface bioplanation rate of 0.12 mm ·yr-I due to the grazing activities of A. granulata. RASMUSSEN AND FRANKENBERG: INTERTIDAL BIOEROSION BY A. GRANULATA 685

40 CHITON SIZE

n=43 mean=4.8±1.7(SD)

~ c:~ 20 w a..

o C\I C") <0 co VI C\I II) <0 co LENGTH (em) Figure 2. Length distribution of sample chiton population, as measured from the outer girdle. In- dividuals ::S 3 em in length were designated as juveniles (21%), those> 3 em long as adults (79%). Size/ age distribution of this sample population parallels that of the total population (N = 268).

Chitons were nocturnally active, and generally grazed between 2000 and 0400. Individual forays extended to a maximum radius of - 25 cm, as chi tons slowly described circuitous paths about their homing pits. Each individual did not graze every night. Glynn (1970) similarly observed chitons resting at night, and ex- pressing no radular activity over a 24-h period. Daily pellet output was also occasionally rhythmic (e.g., chiton W, Fig. 3), reflecting periods of active foraging and enhanced pellet production, punctuated by periods of rest, with little or no foraging and defecation. The homing behavior often displayed by chitons (Glynn, 1970; Chelazzi et al., 1983; Mook, 1983) was imperfect here, as many individuals did not return to the same pit each morning, and many did not appear to occupy a well-defined depression at all. Among those that did return to a specific homing pit, reorientation was very common. During the 6 days spent at the study site, a single detached adult was found dead, high in the supratidal zone. The nocturnal timing of its death, its displace- ment high above the normal intertidal position of the living chitons, and the torn- apart condition of its carcass all suggest predation by a shore bird during the early-morning grazing period. Despite the effective clamping mechanism by which chitons can tenaciously adhere to rock surfaces while at rest (Glynn, 1968), such 686 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.3, 1990

DAILY PELLET PRODUCTION

200 200 CHITON C: 74 ±i8 CHITON L: 34 ±22

150 150

100 100

50 50 I- Z :J 0 8 14 15 16 17 18 15 16 17 18 tD....J ....J W 200 200 a... CHITON 0: 19 ±17 CHITON W: 85 ±86

150 150

100 100

50 50 •

0 14 15 16 17 18 15 16 17 18

DATE Figure 3. Daily fecal pellet production of 4 chitons (C, L, 0, and W) which were monitored indi- vidually throughout the study Cfable 3). Daily pellet production values are highly variable for each chiton, as standard deviations range from 24-101% of individual means. Production by chiton W appeared to follow a distinct on/off rhythm. Average production among chitons also varied markedly from 19-85 pellets/day. Values equal mean ± SD.

predation events may be more frequent during the mobile, less adherent, and therefore more vulnerable grazing period. Chips of Pleistocene rock sampled from shoreline outcrops were composed of moderately indurated pelletal grainstone/packstone. Subaerial diagenetic features such as caliche glaebules surrounded by tangential needle fiber cements were common (Esteban and Klappa, 1983). The average density of the rock (1.82 ± 0.15 g·cm-3) attests to its porous, incompletely cemented, and often extensively bored nature (by endolithic algae, sponges, polychaetes, etc.). Surface texture was microscopically irregular, as individual allochems were weathered-out in positive relief, and formed prominent projections from the pitted bedrock (Fig. 4A). En- dolithic penetration by blue-green algal filaments was ubiquitous, and readily visible within freshly broken cross sections of the rock surface (Fig. 4B). Textural analyses of disaggregated fecal pellets from Pigeon Creek indicate that the rasping activity of chitons can remove particles of widely different grain size from heterogeneous, weakly cemented limestone surfaces (Fig. 5). Fecal pellets contained constituent grains spanning size-classes from < 33 /-tm through > 250 /-tm. Half the bulk pellet mass was comprised of mud-sized material «63 /-tm), with most (36%) concentrated in the <33 /-tm fraction. The <33 /-tm fraction RASMUSSEN AND FRANKENBERG: INTERTIDAL BIOEROSION BY A. GRANULATA 687

Table 3. Body size (L x W) and daily fecal pellet production of 43 test chitons comprising 15 separate catchment groups (indicated by horizontal lines). Standard deviations (SO) of daily averages are shown only for catchments comprised of single, specified individuals monitored for 4 days. 67.2 pellets' day-I'chiton-I translates to a daily limestone erosion rate of 0.11 g·day-I.chiton-t, or an annual rate of 41.5 g·yr-I •chiton-I. NO = no data

Fecal pellet production

Chiton 10 Body size (em) Dec. 14 Dec. IS Dec. 16 Dec. 18 Avg. ± SO AB I 6.4 x 4.0 0 132 65 66 AB2 6.0 X 3.8 0 132 65 66 AB 3 7.2 X 4.0 NO 132 65 69 AB4 3.6 X 2.4 NO 132 65 66 AB 5 5.0 X 3.0 NO 132 65 66

C 5.8 X 3.8 65 64 61 105 74 ± 18

E 5.2 X 3.2 132 70 106 78 F 2.6 X 6.2 132 70 106 78 G 5.0 X 3.2 132 70 106 78 H 5.6 X 3.8 132 70 106 78 I 8.0 X 4.2 132 70 106 78 I' 4.8 X 3.0 132 70 106 78

J 3.0 X 2.0 70 59 84 87 K 4.6 X 2.8 70 59 84 87

L 5.6 X 3.4 70 18 31 15 34 ± 22

M 4.8 X 3.2 22 13 99 I N 5.0 X 3.4 22 13 99 I N' 6.0 X 3.6 22 13 99 I 0 4.0 X 2.4 4 0 32 38 19 ± 17 p 8.8 X 4.0 80 5 19 25 Q 2.6 X 1.8 80 70 130 74 R 7.0 X 3.8 60 33 80 19 S 4.2 X 2.4 60 33 80 19 T 2.7 X 1.3 60 33 80 19 U 4.6 X 2.7 60 33 80 19 V 5.4 X 3.6 60 33 80 19 V' 5.4 X 2.8 ND 40 26 21 W 5.2 X 2.3 186 0 153 0 85 ± 86 RKI 5.8 X 3.6 NO 34 64 89 RK2 5.2 X 2.8 NO 34 64 89 RK3 5.8 X 3.5 NO 34 64 89 RK4 2.8 X 2.1 NO 34 64 89 RK5 5.8 X 3.0 NO 34 64 89

X 5.0 X 3.4 62 173 69 13 X' 2.4 X 1.2 62 173 69 13 y 4.8 X 3.0 62 173 69 13 Y' 1.6 X 1.1 62 173 69 13 Z 5.2 X 3.3 62 173 69 13 Z' 1.0 X 0.6 62 173 69 13 AA 4.4 X 2.6 62 173 69 NO

BB 5.1 X 3.0 73 67 48 60 CC 6.0 X 3.0 73 67 48 60 00 1.1 X 1.0 73 67 48 60 Overall avg. 4.8 x 2.9 67.2 688 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.3, 1990

Figure 4. (A) SEM of microscopically pitted and bored limestone surface sampled from the grazed intertidal zone. An irregular microtopography of weakly bound, coherent allochems is presented to the enlarged radular cusp illustrated in Figure 4F. (B) SEM cross section of the surface shown in Figure 4A. The outer rock surface is infested with algal filaments which easily penetrate between individual grains. Algae provide a food source for the chitons, and also weaken the outer rock surface. (C) Thin section of two whole fecal pellets showing their variable internal structure and texture. Pleistocene allochems plucked from the weathered limestone surface (Fig. 4A, B) occur as discrete dark elements in a fine, organically-bound matrix. Large and small constituents are packaged randomly throughout the externally smooth, sausage-shaped pellets (epoxy imbedded, PPL). (D) SEM of microbored composite Iithociast (left) and an individual pelletal allochem (right) isolated from the> 250 ILm fraction of wet-sieved fecal material. (E) SEM of the 33-62 ILm fraction of disaggregated fecal pellets which is composed predominantly of microbored detritus. This material and finer grains « 33 ILm) form half of the fecal pellet mass (Fig. 5). (F) SEM of the enlarged, magnetite-enriched cusp of an A. granu/ata radula (Thiele, 1893). This chisel-shaped tooth was found during wet-sieving of chiton feces, and apparently broke off and was swallowed during grazing. RASMUSSEN AND FRANKENBERG: INTERTIDAL BIOEROSION BY A. GRANULATA 689

PELLET CONSTITUENT TEXTURE

~0 l- 20 I CJ W ~

0 . C') C\I r-.. v co en 0 C') <0 co C\l •...... ,. It) V I , .,.... .,.... C\I C\I C') C') •, , I 1\ C') co eX) II) r-.. eX) C\I r-..

GRAIN SIZE (J.Lm)

Figure 5. Constituent grain size of bulk chiton pellets. Mud-sized grains «63 !tm) were comprised of irregularly shaped microbored debris and smaller, bladed particles. Components> 125 !tm are typically whole or fractured bits of microbored allochems eroded from the Pleistocene rock surface. contains the 3-1 0 ~m particles which dominated A. granulata pellets from Andros Island (Donn and Boardman, 1988), as well as most of the silt which comprised 60-70% of A. gemmata pellets from Australia (McLean, 1974). Thin sections of individual pellets (Fig. 4C) confirm the textural variability of their internal constituents, and further illustrate pellet structure in cross section. Conspicuous Pleistocene allochems (e.g., pellets, caliche glaebules, and composite grains) ranging in size from 100-400 ~m are held in an organically-bound, fine matrix (10-45 ~m) of microbored debris (Fig. 4E). When the enlarged, chisel- shaped cusp of A. granulata (Fig. 4F) meets coherent allochems held weakly at the rock surface (Fig. 4A, B), these grains are often plucked-out and incorporated into the chiton's fecal pellet in toto. Discrete allochems of primary and diagenetic origin are directly conveyed intact from the Pleistocene limestone to the modem tidal creek environment, with no apparent change in their original form. Even delicate tangential needle cements formed around sand grains during subaerial diagenesis are passed through the chiton's gut unscathed, arguing against digestive losses of CaC03• Repetitive structural patterns of clear diagnostic value were not 690 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.3, 1990 observed in pellet cross sections, unlike in those of other sedimentologically important faunas such as callianassid shrimp (Favreina). Perhaps the very absence of consistent internal structure and grain size is most characteristic of fecal pellets from chitons grazing non-homogeneous, incompletely cemented limestone.

DISCUSSION When comparing bioerosion rates between particular organisms, the most meaningful and useful measurement is the mass of material which a "standard" individual is capable of removing from its substrate, and contributing to the local sedimentary environment per unit time. Published values of coastal bioerosion by intertidal chitons are rare, and those which do exist were not determined rigorously from large, natural populations (Table 1). Our in situ measurements of mass removal by A. granulata from the shores of Pigeon Creek suggest that laboratory estimates provide a poor indication of the bioerosive potential of chitons. Possible reasons for this are manifold, and as McLean (1964) proposed, may to a large extent reflect the perturbation of chiton metabolism by transferral to, and maintainance in, unnatural and perhaps stressful laboratory conditions. Behavioral studies of A. granulata have shown that chiton grazing and radular activity (and hence, bioerosion) are regulated more by day/night regime than by tidal cycle (Glynn, 1970; Boyle, 1977; Mook, 1983). It was further observed that individual chitons commonly range 12-36 cm from their homesites in search of sufficient algal food. The restriction of normal grazing range to small laboratory substrates may promote a compensatory increase in grazing effort (Mook, 1983), resulting in turn, in rapid, unnatural denudation of surficial algal coatings (Mc- Lean, 1964). Conversely, decreased effort may result when food abundance rises, as was shown for similarly grazing winkles (Newell et al., 1971). Importantly, natural day/night rhythms, and appropriate, unrestricted grazing areas were not maintained during the laboratory experiments of McLean (1964), Glynn (1973; unpubl.), nor Hoskin et al. (1986). The common design of each of these experiments could spuriously enhance, or conversely inhibit the calculated rate ofbioerosion via the following alternative pathways. First, compensatory increases in grazing effort and radular scraping, caused by restriction to small laboratory substrates, may account for the particularly high rate of bioerosion (54.0 g.yr-l. chiton-I) calculated by Glynn (1973; unpubl.). He monitored A. granulata on hand samples in aquaria for -7-10 days, without artificial stimulation of algal regrowth (P. Glynn, pers. comm., 1989). A considerably lower erosion rate of 26.1 g'yr-I .chiton-1 was calculated by Hoskin et al. (1986), who may have sup- pressed the need for increased grazing by stimulating algae with fluorescent lamps. In the second, alternative scenario, bioerosion can be inhibited by an increase in surficial rock hardness and density. McLean (1964) observed that natural limestone surfaces are usually kept "soft and loose" by algal endoliths, but that the loose outer surface and its algal coating were effectively lost within only a few days of restricted-range grazing by chitons. In that case, an anomalously hard outer surface results, which inhibits abrasion by the chiton's radula, and thereby suppresses the rate at which substrate is removed overall. This latter effect, plus the poor health of chitons transferred to the laboratory, caused McLean (1964) to base his rate calculations upon experiments limited to only 24 h duration. Given daily variability observed in the pellet output of isolated individuals (Fig. 3), bioerosion rates based on such brief periods cannot be extrapolated to population effects over the long-term. RASMUSSEN AND FRANKENBERG: INTERTIDAL BIOEROSION BY A. GRANUUTA 691

Field and laboratory data of Taylor and Way (1976) indicated thatA. brevispino- I sa erode only 3.3-8.4 g·yr- • The lower value of this range was based on direct pellet counts made from only 3 in situ individuals monitored over a 3-day period. Their upper value was based upon gut-content measurements of 108 individuals, and required estimates of percentage voided per day for average-sized chitons. As such, these data are subject to large errors associated with limited sample size for pellet counts, and indirect approximations of the percentage of total gut- contents voided per day for various individuals. Chiton population densities and the lithologic densities ofthe limestones which they graze are important factors in the calculation of both areal bioerosion rate 2 1 l (g·m- ·yr- ), and of overall coastal bioplanation rate (mm·yc ). Biological and lithological factors are notoriously variable and site-specific, rendering between- site comparisons of areal bioerosion and bioplanation rates of questionable sig- nificance. For example, correcting for about 94% CaC03 in pellets, Glynn (1973) estimated about 432 g'm-2'yr-1 eroded by A. granulata in Puerto Rico, and a l bioplanation rate of 0.18 mm·yc • Donn and Boardman (1988) estimated 286 g'm-2'yr-1 eroded by A. granulata from the Andros Island coast, and 0.21 mm· yel bioplanation. Our data from Pigeon Creek indicate 227 g·m-2.yr-l eroded, I and a bioplanation rate of 0.12 mm ·yr- • Importantly, this two-fold range in areal bioerosion and bioplanation rates (227-432 g·m-2·ycl, and 0.12-0.21 mm'yr-I, respectively) largely results from combining a population density range of 5.5-13 chitons'm-2 with a lithologic density range of 1.35-2.40 g·cm-3• Figure 6 illus- trates the considerable breadth of bioplanation rate which can result from a constant per capita rate ofbioerosion, and variations made in population density I and/or rock density values. Using our bioerosion rate of 41.5 g·yr-I·chiton- , any bioplanation rate previously cited for A. granulata can be easily achieved by reasonable combinations of population density and/or substrate density values. Bioplanation rates are therefore best used to describe the geomorphic impact of a given population of grazers on a localized substrate type, and not to compare the bioerosive efficacy of different organisms in any general sense. Chiton population density differs even between individual transects within a single study area. This appears to be a function of shoreline structure, since chitons were significantly more abundant on solid and continuous bedrock surfaces than on those which were broken and discontinuous, or consisted of rubble (Table 2). Solid, continuous substrates form broad intertidal surfaces, and provide an appropriate setting for the development of the smoothed trackways in which chitons often graze. Broken and/or rubble-strewn zones are more discontinuous, and necessitate numerous crossings between separate grazing surfaces. This maneuver requires lifting the mantle up and away from the rock during grazing, when latero- pedal muscles are already more relaxed for locomotion (Boyle, 1977). Inter- substrate crossings which break the chiton's firm grip presumably make grazing individuals more vulnerable to predation by shore birds or crabs. Thus chitons inhabiting solid/continuous substrate types may benefit from decreased vulner- ability during grazing, especially in quiet coastal habitats which allow unimpeded and prolonged bird and crab predation. Generalized comparisons between the bioerosive potential of sedentary endoliths such as Chona (domichnial borers), and vagile epiliths such as A. granulata (pascichnial grazers; sensu Seilacher, 1953) are problematical. This is due in part to differences inherent in the body form of modular sponges and solitary molluscs, and in part to differences in the mechanism and function of substrate removal in each case. In addition to substantial differences in sponge or chiton population densities between sites, the erosion rate of specific individuals within any given 692 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.3, 1990

0.45 CHITON BIOPLANATION RATES A. granulata @41.5 g/yr/chiton 0.35 ill I-« a:: z 0'2- >, 1---. « 0.25 z E « E -l n... 0as 0.15

0.05 4 6 8 10 12 14 POPULATION DENSITY (chitons/sq. meter) Figure 6. Relationship between chiton population density and estimated bioplanation rate for various values of coastal limestone density (RD). Ranges for organism abundance and lithologic density span those found in the published literature for chitons inhabiting limestone coasts. Annual bioerosion rate used is our value of 41.5 g·yr-l.chiton-l for A. granulata. A broad range in bioplanation rate results from reasonable variations in local organism abundance and rock density.

site may change during the lifetime ofthe organism. For example, the prodigious rate of initial substrate excavation by C. lampa as measured by Neumann (1966) (23.7 kg·m-2·yr-1) greatly exceeds that for long-term C. lampa habitation made 2 I by Riitzler (1975) (7 kg·m- ·yr- ). Variations in long-term organism abundance and lifetime erosive rate can lead to many, widely different estimates ofbioerosion even at a specific locale. In an attempt to make the most realistic comparison between long-term clionid and chiton bioerosion at a single site, we can use the abundance data for Cliona and A. granulata available in Donn and Boardman (1988) for Andros Island (i.e., 13 chitons·m-2; 38% clionid coverage). Using the long-term rate determined by Riitzler (1975), intertidal bioerosion by Cliona at 2 1 the Andros Island site may equal 2.7 kg·m-2·yr-1 (0.38 x 7.0 kg·m- .yr- ). In comparison, using our rate of bioerosion measured from a reasonable adult: juvenile population distribution of chitons, the rate ofbioerosion by A. granulata 2 I 1 at Andros equals 0.55 kg·m-2·yr-I (13 chitons'm- x 0.042 kg·yr- ·chiton- ). Thus the overall, long-term erosive effectof Cliona may exceed that ofA. granulata by a factor of 5 x at least at this specific locale. Different organism abundance and life-history characteristics (e.g., turnover rate) of another coastal community might easily render a different relationship. In their study of coastal bioerosion and sediment production in the northern Adriatic, Schneider and Torunski (1983) observed a consistent, unimodal grain size (20-63 ILm) in the feces of grazing intertidal gastropods. They maintained that this derived from the narrow size distribution of "biogenic fractures" created RASMUSSEN AND FRANKENBERG: INTERTIDAL BIOEROSION BY A. GRANULATA 693 in the limestone surface by modem algal endoliths. In contrast to their result, the chitons which rasp heterogeneous, weakly cemented limestones along Pigeon Creek remove a wide variety of larger, coherent grains ranging from 100 JLm through 400 JLm. Such heterogeneity in original carbonate components and diagenetic grade is common in Quaternary limestones throughout the Bahamas. It is perhaps most characteristic of Pleistocene carbonates incompletely cemented by ongoing subaerial processes (Esteban and Klappa, 1983; James and Choquette, 1984). Perhaps in settings where more mature, well-indurated limestones outcrop, recent mi- croendolithic processes such as those described by Schneider and Torunski (1983) restrict fecal constituent grain sizes to <63 JLm. Along Pigeon Creek, however, lithologic weaknesses inherited from incomplete cementation appear to promote surficial plucking oflarger grains. McLean (1974) similarly demonstrated sand-sized grains in the feces of A. gemmata grazing beachrock at Heron Island, Australia. An analogous plucking process was reported for the grazing echinoid Echinometra lucunter at Black Rock, Bahamas (Hoskin and Read, 1985), which removes large surficial grains from weathered Pleistocene eolianites exposed there. The absence of a small, consistent size class for the sedimentary by-products of chiton bioerosion, as found, for example, in the case of clionid sponge "chips" (Neumann, 1966; Riitzler, 1975; Riitzler and Rieger, 1973), is a combined function of inherited substrate properties (e.g., inconsistent texture or diagenesis), and the less precise, mechanical rasping method of the relatively large radular cusp (Fig. 4).

SUMMARY AND CONCLUSIONS The pitted, biokarstic morphology and subdued energy regime of the Pigeon Creek shoreline results in excellent preservation of delicate chiton fecal pellets. This fortuitous setting allowed accurate, in situ measurement of coastal bioerosion by the common Caribbean chiton A. granulata through direct counts of its daily fecal pellet production. Our measurements, made from a large, natural population, suggest that previous laboratory experiments have typically underestimated the bioerosive potential of intertidal chitons. Shoreline habitats composed of coherent, solid limestone surfaces maintained significantly more individuals than those which were discontinuous, broken, or composed of rock rubble. This may be because chitons can cling more tenaciously to broad, continuous surfaces even while grazing, and are thus better protected from predatory birds and crabs during that most vulnerable activity. Chiton density was not noticeably higher in areas of craggy, convoluted shoreline, despite apparently more numerous microhabitats there. Individual chitons defecated 67.2 pellets' day-l on average. Pellet production was highly variable among days and among individuals. Average fecal pellet mass was 1.79 mg, of which 94.3%, or 1.69 mg was composed of CaC03• These data suggest that a typical A. granulata individual is capable of eroding limestone at a rate of 41.5 g.yr-l. This in situ value is higher than any previously determined under laboratory conditions, except for that of Glynn (1973; unpubl.). Using population density and substrate density values from Pigeon Creek, shoreline 1 bioplanation rate was calculated as 0.12 mm' yr- • All extrapolated bioplanation rates are highly site-specific, however, as they are heavily influenced by variable lithological (texture, diagenesis, density) and biological (algal biomass, chiton abundance) factors. Radular activity of chitons can remove a wide variety of grain types and sizes from heterogeneous, weakly cemented limestones. Pleistocene-age materials < 10 694 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.3, 1990

J.Lm through 400 J.Lm in size are removed from the coast, and recycled to the modern sedimentary environment of Pigeon Creek at an estimated rate of227 g' m-2·yr-1• Although chiton pellets deposited in higher-energy, wave-dominated settings would presumably disaggregate upon defecation, shoreline habitats such as those found here afford a relatively undisturbed, post-depositional period of desiccation and hardening prior to the next high tide. This leads to enhanced preservation of chiton pellets here, and presumably would in an analogous ancient habitat as well. The peculiar taphonomic environment necessary for pellet preservation, as exemplified by Pigeon Creek, suggests that fossilized chiton pellets may be indicative of proximity to low energy, tide-dominated rocky shores.

ACKNOWLEDGMENTS

The authors wish to thank E. Duffy, D. Frankenberg, D. and M. Littler, and 1. Macintyre for their review of early versions of this manuscript. D. Dean and B. Boykins are thanked for their help with the photographic plates. Our research was supported in part by a Smithsonian Post- Doctoral Fellowship to K. Rasmussen, a NSF grant to A. C. Neumann and K. Rasmussen, and a grant from the Shell foundation to E. Frankenberg.

LITERATURE CITED

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DATEACCEPTED:January 30, 1990.

ADDRESSES:(K.A.R.) Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, and Curriculum in Marine Sciences, University of North Carolina at Chapel Hill, CB #3300, Chapel Hill, North Carolina 27599-3300; (E. W.F.) Department of Geo- physics, Stanford University, Stanford, California 94305.