Age and growth of the knobbed whelk Busycon carica (Gmelin 1791) in South Carolina subtidal waters.

ABSTRACT Knobbed whelk, Busycon carica (Gmelin, 1791), age and growth were estimated using tagged and recaptured individuals (n = 396) from areas off South Carolina coastal islands. Recaptured whelks were at large an average of 298 d (4-2,640 d). Growth, an increase in shell length (SL), was evident in 24% of the recaptured whelks, whereas 29% of recaptured individuals were the same size as when released and 47% were smaller than the released size. Mean growth rate was <0.001 mm SL/d and 0.022 mm SL/d if decreases in SL were assumed to be zero. Smaller whelks ([less than or equal to] 90 mm SL) at large for over one year grew seven times faster than larger whelks. The yon Bertalanffy growth model: [SL.sub.t] = 159.5(1 - [e.sup.-0.0765(t+0.4162)]), was developed from the mark--recapture whelks exhibiting growth. Based on a South Carolina minimum legal size of 102 mm SL, whelks recruit into the fishery at 13 y of age. The longevity, large size at maturity and slow growth suggest the potential for over harvest of knobbed whelk. Future whelk management plans may wish to consider whether economically viable commercial harvest can be sustainable.

KEY WORDS: whelk, growth, age, management, tagging, mark-recapture, Busycon carica

INTRODUCTION

The knobbed whelk, Busycon carica (Gmelin 1791), occurs along the western Atlantic coast from the south shore of Cape Cod, MA, to Cape Canaveral, FL (Abbott 1974). Busycon carica and fellow member of the family Melongendiae, the channel whelk, Busycotypus canaliculatus (Linnaeus 1758) are commercially harvested throughout their ranges. A whelk fishery started in South Carolina in 1978 when two commercial shrimp fishermen began harvesting knobbed and channel whelks offshore of barrier islands. Using gear similar to that used for commercial shrimp harvesting, the fishery evolved into the largest subtidal fishery in the United States. Whelk harvest in South Carolina peaked in 1982 after an extremely poor 1981 shrimp season (Anderson et al. 1985); however, annual landings have since decreased and even ceased in some years because of low product prices and high harvest costs. Vessels expended more time traveling to fishing areas, less time fishing and experiencing lower catch per unit effort after 1982 (Anderson et al. 1985). In Georgia, the whelk fishery, which started in 1980 mirrored the South Carolina fishery; peak production in the mid to late 1980s was then followed by a decline, and currently operates at historically low production levels (Georgia Department of Natural Resources, unpub, data).

In South Carolina, in an effort to maintain the whelk resource under increased exploitation, a research program was initiated in the early 1980s. South Carolina initially established a 127-ram shell length (SL) minimum size that was subsequently reduced to 102 mm SL at the request of commercial fishermen. Because age and growth information, one of the more important life history parameters considered in establishing harvest regulations was lacking, size limits were based on size frequency information and an assumed size of first reproduction.

Magalhaes (1948) provided the first data for knobbed whelk growth. Her returns from a small sample of tagged whelks indicated growth was irregular and some individuals exhibited no growth after a year or two in a North Carolina estuary. Growth rate estimate, an increase in SL, calculated from data in Magalhaes (1948, Table 15) was 0.028 mm SL/d; however, the ages of the tagged whelks were not reported. Kraeuter et al. (1989) used mark-recaptured whelks, growth lines on the operculum and laboratory-reared individuals to estimate the growth rate and age of knobbed whelks in an intertidal sand flat in Virginia. These investigators also observed zero and irregular growth, and some whelks exhibited an incremental loss in SL (i.e., negative growth). Average growth rate estimate, including the negative growth values as zero, for a wide range of whelk sizes was 0.015 mm SL/d. Using growth values including negative growth for tagged-recaptured knobbed whelks, Power et al. (2002) estimated that whelk growth averaged 0.020-mm SL/d in the intertidal waters of Wassaw Sound, GA. Similar growth information is not available for subtidal populations of knobbed whelks or whelk populations in South Carolina.

The present study reports the results of a mark-recapture study to determine the age and growth of knobbed whelks in subtidal waters along coastal South Carolina. Effort was directed at determining the age and growth of subtidal knobbed whelks because the fishery targeted populations off barrier islands and the knobbed whelk was the predominant species, averaging about 90% of the total catch (Anderson et al. 1985).

MATERIALS AND METHODS

Shallow (<20-m depth) areas off coastal barrier islands along South Carolina from Beaufort to Georgetown represented the study area. Knobbed whelks (n = 9,317) were collected by commercial fisherman or from a research vessel from July 20, 1982 to October 23, 1984. Individuals were measured for shell length (SL, maximum distance from the spire to the end of the siphonal canal) to the nearest millimeter with a measuring board. Shells of individuals were scrubbed with a wire brush to remove epifauna and allowed to dry before tags were applied with an epoxy adhesive. Two tag sizes were used: a 19-mm Peterson disc was used with the larger ([greater than or equal to]70 mm SL) whelks and an elliptical-shaped tag (16 x 6 mm) for the smaller (<70 mm SL) whelks (Floy Tag, Seattle, Washington, USA). The reverse surface of the tags was abraided with an emery cloth to improve tag retention. Tagged whelks were held overnight so that the epoxy could cure, then returned to the general location of their capture.

A reward program was instituted to encourage returns of tagged whelks. The date of recovery and SL were used to calculate growth for the number of days individual whelks were in the field. Chipped and damaged shells are common in knobbed whelks and other busyconine whelks that use their shell in feeding (Magalhaes 1948, Carriker 1951, Kraeuter et al. 1989), so negative growth (increment losses) are frequently observed in repetitive shell measurements of individuals. Because of these observations and to meet the assumptions to calculate the yon Bertalanffy growth model, those returned whelks that failed to exhibit positive growth were deleted from the age and growth calculations.

Non-linear regression was used to estimate the asymptotic shell length (SL [infinity]) and growth (k) parameters of the von Bertalanffy growth function from mark-recapture length data using a method described by Fabens (1965). Growth parameters were estimated by minimizing the sum of squares of errors between the observed SL at recapture and the predicted SL at recapture. The von Bertalanffy growth function was then used to estimate age at SL of the tagged whelks and to develop the age frequency distribution of the sample.

RESULTS

Recapture date and SL were available for 396 of the 438 returned whelks. Most of the whelks (74%) were returned by commercial fishermen during the whelk trawling operations in release areas offshore. Seven percent of the whelks were recaptured within a week and another 8% were recaptured within one month.

Returned whelks were in the field an average ([+ or -]SD) of 298 [+ or -] 390.6 d. Whelks exhibiting growth (n = 94) were at large an average of 542 [+ or -] 553.6 d, with one individual at large for 2624 d. Returned whelks the same size or smaller than when released were at large less time, 222 [+ or -] 289.0 d (mean [+ or -] SD). Growth was not detected in 95% of the whelks recaptured in less than one month.

Almost half (47 %) of the returned whelks exhibited negative growth. Negative growth was observed in individuals of all sizes and release times. For example, the smallest recaptured tagged individual (34 mm SL) exhibited negative growth after being in the field for only four days and the largest (223 mm SL) recaptured whelk was 2 mm shorter after 305 d. Mean growth rate of the 396 returned whelks, including those with negative growth, was <0.001 [+ or -] 0.045 mm SL/d (mean [+ or -] SD); however, when those whelks exhibiting negative growth were assumed to be zero, growth was 0.022 [+ or -] 0.011 mm SL/d.

The largest growth increment, 46 mm SL, was recorded for an 87 mm SL whelk recaptured after 2590 d and the fastest growth rate (0.042 mm SL/d) for a 74 mm SL individual in the field for 377 d. Growth rate for these individuals and other small ([less than or equal to] 90 mm SL) tagged whelks returned one year after release exceeded that of the larger (>90 mm SL) whelks returned after a year. Small whelks grew, if negative rates were zero, 0.014 [+ or -] 0.013 mm SL/d in comparison with only 0.002 [+ or -] 0.006 mm SL/d for the larger recaptured whelks. Growth (change in SL) was also detected in a lower percentage of these >90 mm SL individuals than were observed with [less than or equal to] 90 mm SL whelks.

The size and age frequency distribution of the returned whelks including those individuals exhibiting no or negative growth is presented in Figure 1. The modal sizes and ages were 110-120 mm SL and 15-20 y. Several individuals were larger than the 150 mm SL and older than 30 y of age. The von Bertalanffy growth parameters were: [SL.sub.[infinity]] = 159.5 mm, k = 0.0765, and [t.sub.o] = q).4163 mm (Fig. 2).

DISCUSSION

Irregular growth including negative growth has been observed in other mark-recapture studies with Busycon carica (Magalhaes 1948, Kraeuter et al. 1989, Power et al. 2002). The percentage of the returned whelks with negative growth (47%) observed in this study is high, but similar to the 42% reported for marked whelks released and recaptured on sand flats in Virginia (Kraeuter et al. 1989). Some of the small deceases in SL between release and recapture of tagged whelks may be because of measurement error. Other whelks exhibiting negative growth may have experienced shell breakage during feeding or harvest. Knobbed whelks use the margin of their own shell to hammer the shell of bivalve prey and in turn often chip the body whorl resulting in a decrease in shell size (Magalhaes 1948, Carriker 1951). Shell damage occurs in trawl harvest (74% of the tagged whelks in this study were returned from commercial fishermen) when the catch was dropped on the ship's deck and the catch was hand sorted and bagged. Shell erosion, which has been observed in the apex of heavy-shelled turbid gastropods (Yamaguchi 1977), could also result in negative growth. The cause of negative growth in this and other growth studies was not determined; however, the use of a zero increment in SL for those recovered whelks with negative growth results in liberal growth rate estimates.

The calculated arithmetic growth rate for mark-recaptured whelks varied among populations; the estimated rate for a 365-d year in this study (8.0 mm SL/yr) was higher than the estimated rate for recaptured-tagged whelks in Virginia (5.5 mm SL/yr; Kraeuter et al. 1989), lower than in North Carolina (10.2 mm SL/yr; Magalhaes 1948) and comparable whelks in Georgia (7.3 mm SL/yr; Power et al. 2002). Some of the variation in growth rate estimates may be because of the statistical treatment of negative growth data. Individuals with negative growth were represented with a zero SL increment in this study and Kraeuter et al. (1989), whereas Power et al. (2002) growth estimate included negative growth in the analysis. The data from Magalhaes (Table 15; 1948) used to calculate growth rate did not include whelks with negative growth, although she mentioned that some recovered whelks were "smaller than when they were first measured," so this growth estimate would be lower if these data were included. The size of the whelks tagged influences the growth rate estimate, because growth rate is faster in the smaller young individuals. In this study, for example, growth rate was seven times faster in individuals [less than or equal to] 90 mm SL than in recaptured whelks >90 mm SL. The fact that the tagged whelks recovered by Kraeuter et al. (1989) were all >130 mm SL could be one reason their rate estimate was lower than the current study. Because whelk growth is irregular (Magalhaes 1948, Kraeuter et al. 1989, Power et al. 2002), the time period and length of release also becomes important in growth rate calculations. Walker et al. (2004a) observed that tagged whelks released in winter remain buried and do not move to oyster reefs to feed until water temperatures warm. Kraeuter et al. (1989) also found growth of laboratory-reared whelks was reduced in ambient seawater tables in winter. Consequently, growth rate estimates for tagged whelks released before and recaptured after winter would be lower than the rate estimates for individuals released and recaptured over summer. Basing growth estimates on changes in SL observed over long time periods (e.g., 1 year) reduces some of the problems associated with episodic growth and detection of longitudinal differences in growth should be easier.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

The von Bertalanffy growth parameter [SL.sub.[infinity]] was 151 mm for a mixed-sex sample of returned tagged whelks. Walker et al. (2004b) using sectioned operculums estimated 105-mm [SL.sub.[infinity]] for males and 231-mm [SL.sub.[infinity]] for female knobbed whelks collected in Georgia. Our lack of information on sex makes a comparison difficult, but it is worth noting that our parameter estimate is bracketed by Walker et al. (2004b) estimates.

South Carolina commercial fishermen are required to use size-selective gear (>115-mm stretched mesh nets) in the subtidal whelk fishery. Fishermen hand cull catches to the minimum legal size without regard to sex or species at sea. Statewide dockside samples revealed that knobbed whelks exceeded 130-mm SL in 1982-1983 catches, but the number of whelks per bushel and daily catches was decreasing (Anderson et al. 1985). These observations indicate that the exploitation rate was exceeding the knobbed whelks potential to recruit to the fishery. The fishery essentially collapsed thereafter; only a few licenses were requested and very few of these individuals prosecuted the fishery. Based on data from Anderson et al. (1985) an increased minimum legal size, 115-mm SL, went into in effect in 2005 in South Carolina. The average age of a minimum legal knobbed whelk increased from 13.4 y to 16.8 y according to the age and growth model determined in this study.

Female knobbed whelks occurred significantly more frequently than males in South Carolina commercial catches (Anderson 1985, Anderson et al. 1985). Female whelks were also significantly larger than males in these catches (Anderson 1985, Anderson et al. 1985). Sex ratios and the larger size classes favoring females were reported for knobbed whelk populations from Virginia to Georgia (Magalhaes 1948, Anderson 1985, Walker 1988, Castagna & Kraeuter 1994, Power et al. 2002, Walker et al. 2004b). Gear restrictions target the larger faster growing individuals; consequently, females in the population are more subject to harvest. What effect the disproportionate harvest of females has on the long-term health of the whelk fishery is not known, but because of their slow growth the fishery is less resilient to exploitation. The earlier 102-mm SL legal harvest size posed another management issue because female knobbed whelks mature at 100-mm SL (Walker et al. 2004b). These biological characteristics, the relatively low annual reproductive potential (Castagna & Kraeuter 1994), and limited movement (Walker et al. 2004a) make the knobbed whelk a difficult species to manage at sustainable levels. Anderson et al. (1985) suggested that the maximum sustainable yield (MSY) of offshore whelk aggregations should be determined so the fishery can be managed accordingly. Closed seasons and areas have been suggested as viable options for maintaining a sustainable whelk fishery (Anderson et al. 1985, Walker et al. 2004b). The longevity, large size at maturity, and slow growth suggest the potential for over harvest of the knobbed whelk resource. Future whelk management plans may wish to consider whether economically viable commercial harvest can be sustainable.

ACKNOWLEDGMENTS

The authors thank those individuals, especially the commercial fishermen, that returned tagged whelks. Preliminary funding for the project was provided by South Carolina Sea Grant Consortium and National Marine Fishery Service. Cooperators of the United States Geological Survey South Carolina Cooperative Fish and Wildlife Research Unit include the United States Fish and Wildlife Service, the South Carolina Department of Natural Resources, Clemson University and the Wildlife Management Institute. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the United States government.

LITERATURE CITED

Abbott, R. T. 1974. American seashells, 2nd ed. New York: Van Nostrand Reinhold Co. 663 pp.

Anderson, B. A. 1985. Stock assessment on the whelk resource along the South Atlantic bight. Masters thesis, Clemson University, Clemson, SC. 21 pp.

Anderson, W. D., A. G. Eversole, B. A. Anderson & K. B. Van Sant. 1985. A biological evaluation of the knobbed whelk fishery in South Carolina. National Marine Fishery Service Completion Report (No. 2-392-R). 72 pp.

Carriker, M. R. 1951. Observations on the penetrations of tightly closing bivalves by Busycon and other predators. Ecology 32:78-83.

Castagna, M. & J. N. Kraeuter. 1994. Age, growth rate, sexual dimorphism, and fecundity of knobbed whelk Busyeon carica (Gmelin, 1791) in a western mid-Atlantic lagoon system, Virginia. J. Shellfish Res. 13:581-585.

Fabens, A. J. 1965. Properties and fitting of the von Bertalanffy growth curve. Growth 29:265-289.

Kraeuter, J. N., M. A. Castagna & R. Bisker. 1989. Growth rate estimates for Busycon carica (Gmelin, 1791) in Virginia. J. Shellfish Res. 8:219-225.

Magalhaes, H. 1948. An ecological study of snails of the genus Busycon at Beaufort, North Carolina. Ecol. Monogr. 18:379-409.

Power, A. J., M. Sweeney-Reeves, T. C. Recicar, D. M. Thompson & R. L. Walker. 2002. Population biology of intertidal whelks in Wassaw Sound, Georgia. Poster, National Shellfish Association Meeting. Mystic, CT.

Walker, R. L. 1988. Observations on intertidal whelk (Busycon and Busycotypus) populations in Wassaw Sound, Georgia. J. Shellfish Res. 7:473-478.

Walker, R. L., J. H. Smith & A. J. Power. 2004a. Movement and behavioral patterns of whelks on intertidal flats in Wassaw Sound, Georgia. Marine Extension Bulletin 29: 18 pp.

Walker, R. L., A. J. Power, M. Sweeney-Reeves, E. Covington, C. Sellers & M. Mitchell. 2004b. Life history of the knobbed whelk, Busycon carica, in Georgia. Poster, World Aquaculture Meeting. Honolulu, HI.

Yamaguchi, M. 1977. Shell growth and mortality rates in the coral reef gastropod Cerithium nodulosum in Pago Bay, Guam, Mariana Islands. Mar. Biol. 44:249-263.

ARNOLD G. EVERSOLE, (1) * WILLIAM D. ANDERSON (2) AND J. JEFFERY ISELY (3)

(1) Department of Forestry and Natural Resources, Clemson University, Clemson, South Carolina 29634; (2) Marine Resources Division, South Carolina Department of Natural Resources, Charleston, South Carolina 29422; (3) United States Geological Survey, South Carolina Cooperative Fish and Wildlife Research Unit, Clemson University, Clemson, South Carolina 29634

* Corresponding author. E-mail: [e-mail]