Distribution and size of a stalked barnacle (Octolasmis mulleri) on the blue crab, Callinectes sapidus

BULLETIN OF MARINE SCIENCE, 68(2): 181–190, 2001

181

DISTRIBUTION AND SIZE OF A STALKED BARNACLE(OCTOLASMIS MUELLERI) ON THE BLUE CRAB,

CALLINECTES SAPIDUS

Harold K. Voris and William B. Jeffries

ABSTRACTThe objective of this research was to redescribe the spatial distribution of Octolasmis

muelleri on Callinectes sapidus in order to explore the relationship between the spatialdistribution and the size of O. muelleri on C. sapidus. Size distributions of O. muelleri

were also investigated in order to elucidate the mechanism of colonization by the cypridlarvae. The distribution of 1832 O. muelleri over the inside and outside surfaces andproximal, medial and distal regions of gills 1 to 8 of 17 C. sapidus was non-random andin agreement with previous studies. A weak relationship was found between the size of O.

muelleri and their spatial arrangement on the gills of C. sapidus. The modest differencesin the size of O. muelleri on different gills and in different gill regions could be a functionof different growth rates in different gill regions or colonization patterns that would placeearly arrivals in selected regions and thus give them a head start and a longer period ofgrowth. An extended period of cyprid settling that occupies from 25 to 100% of theintermolt period of the adult instars of C. sapidus was suggested by the size distributionpatterns of O. muelleri.

In temperate, subtropical, and tropical coastal waters of the world pedunculate bar-nacles of the genus Octolasmis are frequently found on decapod crustaceans. On the eastcoast of the U.S., for example, Octolasmis muelleri (Coker, 1902) lives on the gills andthe lining of the branchial chambers of the blue crab, Callinectes sapidus (Rathbun, 1896),among others. Coker (1902) reported a higher infestation rate of O. muelleri among fe-male than male blue crabs and a greater average number of individuals in the gill cham-bers of the females than in males. De Turk (1940) reported very similar infestation ratesin blue crabs and the average number of octolasmid barnacles per host was also somewhathigher in females than in males. In addition to counts, Humes (1941) provided details ofthe O. muelleri attachment sites on the gills and the chamber walls of C. sapidus. Walker(1974) observed O. muelleri on the gills of 25 C. sapidus, noted 83% were on the efferent(inner or hypobranchial) side, and described their attachment sites in relation to gill plate-let projections (spines and knobs) and the efferent and afferent branchial blood vessels.More recently, Jeffries and Voris (1983) described the distribution of O. muelleri attach-ment sites on 17 C. sapidus by: gill chamber (left, right), gill number (1–8), gill surface(outside vs inside), and gill region (proximal, medial, and distal). In addition, the capitu-lar length (mm) of each barnacle was measured.

The purpose of this report is three fold. First, we briefly refine our description of thespatial distribution of O. muelleri on the series of 17 C. sapidus which are the basis of thisreport and were the subject of an earlier publication (Jeffries and Voris, 1983). Second, wedescribe for the first time the relationship between the spatial distribution and the averagesize of O. muelleri on C. sapidus. And third we present typical size distributions of O.

muelleri from individual blue crabs and interpret these distributions in terms of two mecha-nisms of colonization by the cyprid larvae, pulsed settlement and trickle settlement.

182 BULLETIN OF MARINE SCIENCE, VOL. 68, NO. 2, 2001

MATERIALS AND METHODS

The sample of 17 blue crabs (C. sapidus), including two males and 15 females used in this studywere collected from the Newport River estuary in Carteret County immediately north of Beaufort,North Carolina (Jeffries and Voris, 1983). The crabs were examined for O. muelleri cyprids, juve-niles, and adults. The exact site of barnacle attachment (left or right gill chamber, gill number,inside [hypobranchial] or outside [hyperbranchial] gill surface, proximal, medial, or distal gill re-gion, and the length of the capitulum (mm) of each barnacle were recorded using methods em-ployed by Jeffries and Voris (1983). A dissecting microscope was used to determine the reproduc-tive status of the barnacles.

The 17 blue crabs hosted 2067 O. muelleri including attached and unattached cyprid larvae. Thisstudy considered the 1832 juvenile and adult O. muelleri that were attached to the gills of the crabs.The 1832 barnacles ranged from 1.43 to 5.575 mm in capitular length (Jeffries and Voris, 1983).

The numbers, density, and size of barnacles and their location on the gills of the crabs wereconsidered from several perspectives. In one approach we pooled the data from barnacles from all17 crabs and considered the number and mean capitular length (MCL) of barnacles located in theleft and right gill chambers, on gills 1 to 8, on the inside and outside gill surfaces, and on theproximal, medial, and distal gill regions of all crabs.Table 1 provides the distribution of the num-bers of O. muelleri over the eight gills on the inside and outside gill surfaces of the 17 crabs.Thevast majority of the O. muelleri were located on the inside surfaces and the MCLs of these bar-nacles are given in Table 2. For these tables data from the left and right chambers of all crabs werepooled.

Because the analysis of these data required a large number of comparisons two approaches werewarranted. Where a limited number of comparisons were involved we provided the probabilitiesbased on the Least Significance Difference (LSD) test. These tests are equivalent to individual t-tests and offer no protection from error resulting from multiple post hoc comparisons. For multiplecomparisons of MCLs between regions we used the Tukey Honest Significant Difference Test forunequal sample sizes (Tukey ≠ N HSD Test, see Spjotvoll and Stoline, 1973).

Because the different gills and gill regions had very different surface areas we measured thesurface area of each gill and each gill region to determine barnacle densities. Areas for the insidesurface of gills 1 to 8 and the proximal, medial and distal regions of each gill were determined fromten repeated measurements of one set of gills using a digitizer. Densities were determined for eachregion using the measured areas.

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183VORIS AND JEFFRIES: PEDUNCULATE BARNACLE SIZE AND LOCATION ON BLUE CRABS

RESULTS

NUMBERS AND DENSITY OVER GILLS.—The distribution of 1832 O. muelleri over the in-side and outside surfaces and proximal, medial and distal regions of gills 1 to 8 of 17 bluecrabs, C. sapidus is given in Table 1. For this table the left and right chambers of crabswere pooled. The observed distribution was non-random. For example, there were 13.3times more barnacles on the inside surfaces of the gills than the outside surfaces. Thenumbers of barnacles over the inside surfaces of gills 1 to 8 varied greatly and rangedfrom six (0.4%) O. muelleri on gill 1 to 431 (25.3%) on gill 6. On the inside surfaces thenumbers of barnacles decreased from the proximal region (50%) to the medial region(43%) to the distal region (7%).

The eight pairs of gills varied in length and surface area. The gill lengths and gill areasare presented in Table 3 as percentages along with the percentage distribution of bar-nacles on the inside surface. The distributions of the number and the density of barnaclesover the inside surfaces of gills 1 to 8 are given in Figure 1. Although the distributions ofnumbers and densities of barnacles were correlated (r = 0.926, P < 0.001) there werenotable differences. Gill 3 had relatively small numbers of barnacles but because gill 3

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had a relatively small surface area (9.23%, Table 3) it bore a relatively high density ofbarnacles (Fig. 1). In addition, the difference in densities between gill 4 and 7 were lessthan the difference in numbers between these same gills. Comparisons of the numbersand densities of barnacles over the proximal, medial and distal regions of the inside of thegills also showed significant correlations (P < 0.01).

Figure 1. The distribution of the numbers and the densities of Octolasmis muelleri over the inside(hypobranchial) surfaces of gills 1 to 8 on 17 Callinectes sapidus.

Figure 2. The number of Octolasmis muelleri observed on the inside (hypobranchial) surfaces ofgills 1 to 8 of 17 Callinectes sapidus compared to the number expected if the barnacles weredistributed evenly according to the inside surface area of each gill.


Although barnacle numbers and densities were correlated and showed a similar pat-tern, O. muelleri was not simply distributed according to the amount of gill surface area.Figure 2 illustrates the relationship between the numbers of O. muelleri on gills 1 to 8 andthe expected numbers based on the available surface area on the inside surface of each ofthe gills. Gills 1, 2 and 8 were observed to host many fewer O. muelleri than would beexpected on the basis of area alone and gills 5 and 6 hosted more than expected. Overallthe deviations between the observed numbers and the expected numbers were signifi-cantly different (Chi-square = 132.4, P < 0.001).

RELATIONSHIP BETWEEN SIZE AND LOCATION.—The mean capitular lengths (MCL) of theO. muelleri located on the proximal, medial and distal regions of the inside surfaces ofgills 1 to 8 of 17 C. sapidus are presented in Table 2. Sample sizes on the outside surfaceswere small (Table 1) and thus only the MCLs for the combined regions are provided forthe outside surfaces. Gill 1 hosted only six barnacles on the inside surface but they weresignificantly smaller on average than the 173 O. muelleri on gill 3 (Fig. 3, LSD test, P <0.05). In addition, the MCLs of barnacles on gills 3 and 4 were significantly larger thanthe MCLs of barnacles on gills 5 through 8 (Fig. 3, LSD test, P < 0.05). However, none ofthese comparisons showed significant differences using the more conservative Tukey ≠ NHSD test (P > 0.05).

Likewise, between gill comparisons of barnacle MCLs on the outside gill surfacesshowed some significant differences using the LSD test but none were significant usingthe Tukey ≠ N HSD test. The small sample sizes on the outside gill surfaces made thesecomparisons less robust.

A one-way ANOVA of the MCLs of O. muelleri located on the proximal, medial anddistal regions of the inside surfaces resulted in a significant F value (F = 4.354, df = 2, P= 0.013). The MCLs of O. muelleri on the proximal and medial gill regions were signifi-

Figure 3. Box and whisker plot of the mean capitular lengths (MCL), one standard error and onestandard deviation are given for Octolasmis muelleri located on the inside (hypobranchial) surfaceof gills 1 to 8 of 17 Callinectes sapidus. The number of barnacles on each gill is given below eachbox and whisker.


cantly larger than the MCL of those on the distal portion (Fig. 4, proximal, mean = 1.13,n = 846, s = 0.805, medial, mean = 1.19, n = 739, s= 0.915, distal, mean = 0.95, n = 119,s = 0.748; LSD test , P < 0.05). However, neither of these two comparisons were signifi-cant using the more conservative Tukey ≠ N HSD test (P > 0.05). It should be noted thatthe O. muelleri on the distal region were both fewer in number and smaller in MCL thanthose on the proximal and medial regions (Fig. 4).

Figure 4. The mean capitular lengths (MCL), one standard error and one standard deviation aregiven for the Octolasmis muelleri located on the proximal, medial and distal regions on the inside(hypobranchial) gill surfaces of 17 Callinectes sapidus. The number of barnacles in each region isgiven below each box and whisker.

Figure 5. The mean capitular lengths (MCL) of Octolasmis muelleri and the densities of O. muelleriover the inside (hypobranchial) surfaces of gills 1 to 8 on 17 Callinectes sapidus are compared.


RELATIONSHIP BETWEEN SIZE AND DENSITY.—The MCLs of the O. muelleri on the insidesurface of gills 1 through 8 did not show a significant correlation (r = 0.697, P > 0.05)with the density of barnacles on the gills (Fig. 5). Gills 3 and 4 had the largest barnaclesbut ranked 3rd and 5th in density. Likewise the MCLs on the inside surface of gills 1through 8 did not show a significant correlation (r = 0.478, P > 0.05) with the numbers ofbarnacles on the gills. However, where numbers were low and densities were less than 5barnacles per unit area on gills 1 and 2 the barnacles had the smallest MCLs.

COLONIZATION AND SIZE DISTRIBUTION PATTERNS.—The size distribution of barnacles withinthe gill chambers of individual crabs was a result of the pattern of colonization by thebarnacle cyprid larvae. Figure 6 presents the size distributions of the O. muelleri associ-ated with the gills of six of the 17 blue crabs studied. Each of these size distributions wasbroad and included juveniles (0.143 to 1.430 mm) as well as large sexually mature adults(>3.575 mm). The size distributions of O. muelleri on 15 of 17 of the blue crabs examinedin this study exhibited similar broad size distributions.

DISCUSSION AND CONCLUSIONS

Our findings on the non-random nature of the spatial distribution of O. muelleri are inagreement with previous studies on O. muelleri (Jeffries and Voris, 1983; Walker, 1974)and other species of Octolasmis on other host species (Arudpragasam, 1967; Bullock,1964; Voris et al., 1994). Our findings on the weak relationship between the size of O.

muelleri and their spatial arrangement on the gills of C. sapidus are in contrast to whatwas observed for O. angulata (Aurivillius, 1894) and O. cor (Aurivillius, 1892) on themangrove crab, Scylla serrata (Forskål, 1755) (Voris et al., 2000). The modest differencesobserved in the size of O. muelleri on different gills and in different gill regions could bea function of different growth rates in different gill regions or colonization patterns that

Figure 6. The size distributions of Octolasmis muelleri are plotted for the populations on sixCallinectes sapidus.


would place early arrivals in select regions where they would have a head start and alonger period for growth.

The breadth of the size range of barnacles on a particular crab can thus serve as a proxyfor the duration of the colonization process. Previous studies suggest that barnacle growthrates are highest among juveniles and lowest among large sexually mature adults (Jeffrieset al.,1985; Jeffries and Voris, 1998). For purposes of discussion we have used two differ-ent growth rates in our analysis. For a high rate estimate we have used the growth rateestimated for O. cor (0.336 mm per day, Jeffries et al., 1985) under natural conditions ofunfiltered sea water and 28 to 31oC). For a more conservative estimate of growth rate wehave used the growth rate estimated for O. muelleri (0.0383 mm d−1, Jeffries and Voris,1998) determined in the laboratory at temperatures between 25 and 27oC. Figure 7 pre-sents the size distribution of O. muelleri on C. sapidus number 41. The implied ages ofthe barnacles based on the fast growth rate are provided accross the top of the graph. If weapply the slower growth rate (0.0383 mm d−1) the age scale extends from 1 to 124 d. Bothinterpretations support an extended period of cyprid settling that occupies from 25 to100% of the intermolt period of the adult instars under consideration here.

The asymmetrical distributions illustrated by the six crabs in Figure 6 are likely a prod-uct of a sporadic low level of infestation occasionally punctuated by one or more periodsof higher rates of settlement. This trickle mode of settlement with intermittent pulses ofgreater numbers of attachments contrasts to the sharp post-ecdysis pulsed mode demon-strated for O. angulata and O. cor on the mangrove crab, S. serrata (see Jeffries et al.,1989). In the latter case newly molted mangrove crabs are colonized by Octolasmis cypridlarvae in a highly pulsed manner. The cyprids aggregate on premolt crabs (but do not

Figure 7. The size distribution of Octolasmis muelleri from one Callinectes sapidus (#41). Anestimate of the approximate age of the barnacles is provided along the upper X axis. The age axisshown is based on growth rates measured for O. cor in tropical waters. If the slower growth ratemeasured for O. muelleri under laboratory conditions is applied the age scale extends from 1 to124 d.


attach) and at the time of host ecdysis the cyprids move from the old exuviae to theintegument of the newly molted crab (Jeffries et al., 1989). Figure 8 illustrates the typicalsize distributions that result from the pulsed mode of colonization in S. serrata.

ACKNOWLEDGMENTS

We thank the staff of the Duke University Marine Laboratory for their assistance and we areespecially appreciative of the encouragement of the past Director, J. D. Costlow. Support for thiswork was provided by the Field Museum of Natural History, the Dickinson College Faculty Re-search Fund, and two anonymous donors. We are grateful to the numerous Dickinson College stu-dents who participated in the early phases of this project. We also thank, K. Heck, Director ofResearch, and the support staff at the Dauphin Island Sea Lab where a part of this work was com-pleted.

LITERATURE CITED

Arudpragasam, K. D. 1967. Distribution and variation of the cirripede Octolasmis cor (Aurivillius1893) in relation to the respiratory current of its host Scylla serrata. Ceylon J. Sci. 7(1&2):105–115.

Bullock, J. A. 1964. Variation in the commensal cirriped, Octolasmis cor (Aur.), in relation to itsposition in the branchial chamber of Scylla serrata Forskål. Federation Mus. J. 9: 84–94.

Coker, R. E. 1902. Notes on a species of barnacle (Dichelaspis) parasitic on the gills of ediblecrabs. Bull. U. S. Fish Comm. 21: 401–411.

DeTurk, W. E. 1940. The parasites and commensals of some crabs of Beaufort, North Carolina.Ph.D. Thesis, Duke Univ. 99 p.

Humes, A. G. 1941. Notes on Octolasmis mülleri (Coker), a barnacle commensal on crabs. Trans.Amer. Micros. Soc. 60: 101–103.

Figure 8. The size distributions of Octolasmis cor populations on six mangrove crabs, Scylla serrata.


Jeffries, W. B. and H. K. Voris. 1983. The distribution, size, and reproduction of the pedunculatebarnacle, Octolasmis mülleri (Coker, 1902), on the blue crab, Callinectes sapidus (Rathbun,1896). Fieldiana Zool. N.S. 16: 1–10.

____________ and __________. 1998. Relative growth rates of the capitulum and its plates inOctolasmis mülleri (Cirripedia: Thoracica: Poecilasmatidae). J. Crust. Biol. 18(4): 695–699.

____________, ___________ and C. M. Yang. 1985. Growth of Octolasmis cor (Aurivillius, 1892)on the gills of Scylla serrata (Forskål, 1755). Biol. Bull. 169: 291–296.

____________, ___________ and __________. 1989. A new mechanism of host colonization:pedunculate barnacles of the genus Octolasmis on the mangrove crab Scylla serrata. Ophelia31(1): 51–58.

Spjotvoll, E. and M. R. Stoline. 1973. An extension of the T-method of multiple comparison toinclude the cases with unequal sample sizes. J. Amer. Stat. Assoc. 68: 976–978.

Voris, H. K., W. B. Jeffries and S. Poovachiranon. 1994. Patterns of distributions of two barnacleson the mangrove crab Scylla serrata. Biol. Bull. 187(3): 346–354.

__________, ___________ and _______________. 2000. Size and location relationships of stalkedbarnacles of the genus Octolasmis on the mangrove crab, Scylla serrata. J. Crust. Biol. 20(3):483–494.

Walker, G. 1974. The occurrence, distribution and attachment of the pedunculate barnacle Octolasmis

mülleri (Coker) on the gills of crabs, particularly the blue crab, Callinectes sapidus Rathbun.Biol. Bull. 147: 678–689.

DATE SUBMITTED: October 13, 1999. DATE ACCEPTED: September 28, 2000.

ADDRESSES: (H.K.V.) Department of Zoology, Field Museum of Natural History, 1400 S. Lake Shore

Drive, Chicago, Illinois 60605-2496. (W.B.J.) Department of Biology, Dickinson College, Carlisle,

Pennsylvania 17013. CORRESPONDING AUTHOR: (H.K.V.) E-mail: <[email protected]>.

Distribution and size of a stalked barnacle (Octolasmis mulleri) on the blue crab, Callinectes sapidus

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