Occurrence of Pedunculate Barnacles of the Symbiotic Genus Octolasmis (Cirripedia: Crustacea) in Two Species of Edible Crabs

Shazia Rasheed1,* and Javed Mustaquim2

1Lasbela University of Agriculture, Water and Marine Sciences, Uthal, Balochistan

2Centre of Excellence in Marine Biology, University of Karachi, Karachi

ABSTRACT

In the present study, 5356 octolasmids hosted by two Portunus crabs, Potunus pelagicus and p. sanguinolentus, they belong to five species; namely Octolasmis angulata (Aurivillius, 1894), O. cor (Aurivillius, 1894), O. lowei (Darwin, 1851), O. tridens (Aurivillius, 1894) and O. warwickii Gray, 1825. The rate of infestation was found markedly low in P. pelagicus (2.9 %) and P. sanguinolentus (10.8 %) during present investigation. Octolasmids prevalence was significantly higher in female P. pelagicus (81.2%) than that of male (18.8%) while in case of P. sanguinolentus the prevalence was significantly higher in male (60.5%) rather than female (39.5%).

Article Information

Received 8 April 2016

Revised 11 August 2016

Accepted 27 November 2016

Available online 22 September 2017

Authors’ Contribution

JM conceived and designed the study. JM supervised the study. SR executed the experimental work, analyzed the data and wrote the article.

Key words

Pedunculate, Octolasmis, Cirripeds, infestation, Portunus.

DOI: http://dx.doi.org/10.17582/journal.pjz/2017.49.5.1879.1888

* Corresponding author: [email protected]

0030-9923/2017/0005-1879 $ 9.00/0

INTRODUCTION

Barnacles of the genus Octolasmis Gray, 1825 are commonly called pedunculate barnacles or stalked barnacles. They belong to subclass Cirripedia of class Crustacea. Pedunculate barnacles of the genus Octolasmis are frequently found in shallow waters attached to the exoskeleton of the decapod Crustacea, including crabs. When the octolasmids inhabit branchial chambers of the crabs, they occupy space on the gills surface normally available for gaseous exchange and can severely impair host respiration (Hudson and Lester, 1994). They have bilaterally compressed body which is divided into two parts: peduncle or stalk and capitulum (Fig. 1). The base of peduncle is cemented to the substratum, which may be the exoskeleton or gills of the host, mostly decapod Crustacea. The top of the peduncle is attached with capitulum which in encased in a carapace composed of two leathery mantle folds or valves. This fleshy structure is strengthened by three to seven calcareous plates. These plates include a median dorsal carina, and on each side one to two scuta and a tergum. The scuta are posterior to the tergum, and near to peduncle. The six pairs of thoracic limbs (cirri) project from a gap between the edges of the carapace.

The genus Octolasmis was first described by Gray in 1825. Darwin (1851) introduced few additional species followed by Aurivillius (1892) and (1894) who described six new species. According to Jefferies et al. (1995) more than thirty species of Octolasmis have been described.

Octolasmids are highly modified crustaceans and distributed worldwide in tropical and temperate seas (Jeffries et al., 1995). Their habitats differ from those of acorn barnacles and common goose-neck barnacles. The epizoic relationship between octolasmids and the commercially important crabs, such as Callinectes sapidus, Scylla serrata and Portunus pelagicus, has received much attention by several authors from Australia, USA, UK and Thailand (Walker, 1974, 2001; Jefferies et al., 1982, 1985, 1989a, b, 1991, 1992, 1995; Jefferies and Voris, 1983, 1996, 2004; Gannon, 1990; Shield, 1992; Gannon and Wheatly, 1992; Voris et al., 1994, 2000; Voris and Jefferies, 1997, 2001; Key et al., 1997; Mantelatto et al., 2003; Shield and Overstreet, 2003; Gaddes and Sumpton, 2004). From Tamil Nadu, India Kumaravel et al. (2009) have reported distribution of Octolasmis spp. on the gills of some edible crabs including Portunus pelagicus and P. sanguinolentus.

A survey of literature shows that only four papers have been published so far on stalked barnacles from Pakistan. First paper was published by Hashmi and Zaidi (1965) who reported stalked barnacle infestation on the gills of Scylla sp. (then identified as S. serrata - see Keenan et al. (1998) for revision of the genus) from Karachi waters. Hashmi and Zaidi (1965) identified stalked barnacles as Lepas sp. instead of Octolasmis cor (Moazzam and Rizvi, 1978; Mushtaq and Mustaquim, 2009, p.58). Two more papers were published by Moazzam and Rizvi (1978) and (1982) on the systematic of the pedunculate barnacles from the Pakistan coast. They described a total of twelve species: seven species of the genus Octolasmis, two species of Lepas and one species each of Conchoderma, Poecilasma and Trilasmis. Fourth paper has been published recently by Mushtaq and Mustaquim (2009) on the occurrence and distribution of Octolasmis on the gills of mud crab Scylla cf. tranquebarica (Fabricius, 1798) from Karachi. The occurrence and distribution of octolasmids on Portunus pelagicus and P. sanguinolentus have never been studied in detail from Pakistan.

MATERIALS AND METHODS

For the study of octolasmid infestation on the crabs, a total of 2725 specimens of the two species of Portunus, collected during January 2004 to December 2005, were examined. Crabs for the present study were collected from the commercial landing at Korangi Fish harbour (24o 48/ 50// N; 67o 13/ 45// E), Karachi. The dorsal and ventral surfaces of all crabs were examined for octolasmids with number of each species recorded. The carapace of each crab was removed and the branchial chambers and gills were visually inspected for the presence of octolasmids. Settlement was also recorded on the different part of the body like (hypobranchial gill rake, epibranchial gill rake, and scaphognathite) and the inner wall of the branchial chambers. Octolasmis species were identified on the basis of morphological features such as overall shape, capitular shape and capitular plate morphology as described by Daniel (1956), Newman (1960a), (1967), (1987), Moazzam and Rizvi (1978) and (1982) and Jefferies et al. (2005). Length and width of the peduncle and capitulum were taken under stereomicroscope with the help of an ocular micrometer. Student’s t-test and Chi-square were calculated by Zar (1996).

Table I.- Minimum and maximum size of the five species of Octolasmis found/attached on Portunus pelagicus and P. sanguinolentus.

Species	n	Peduncle		Capitulum		Total length
Species	n	Length (mm)	Width (mm)	Width (mm)	Length (mm)	(mm)
O. angulata	106	1.1 - 6.9	0.4 - 1.5	1.0 - 3.6	0.5 - 2.6	2.1 - 10.5
O. cor	23	1.3 - 6.5	0.5 - 1.7	1.2 - 3.4	0.8 - 2.5	2.5 - 9.0
O. lowei	4599	0.5 - 7.2	0.1 - 1.5	0.5 - 4.2	0.2 - 3.1	1.0 - 11.4
O. tridens	625	1.5 - 8.0	0.5 - 2.7	1.4 - 5.2	0.4 - 3.7	2.9 - 13.2
O. warwickii	3	3.5 - 8.1	1.5 - 3.0	3.5 - 6.0	2.0 - 5.0	7.0 - 14.1

RESULTS

Of 2725 specimens of the two species of Portunus examined for the presence or absence of octolasmids, only 162 crabs (5.94%) were found infested. The number of octolasmids hosted by these crabs was 5356 and they belong to five species; namely Octolasmis angulata (Aurivillius, 1894), O. cor (Aurivillius, 1894), O. lowei (Darwin, 1851), O. tridens (Aurivillius, 1894) and O. warwickii Gray, 1825 (Fig. 2). The minimum and maximum sizes of the peduncle and capitulum of these octolasmids are given in Table I.

Portunus pelagicus

Out of 2725 crabs examined, 1668 were P. pelagicus (789 male, 879 female including 74 berried female). The size of the male and female crabs ranged from 23-140 mm short carapace width (82.15±3.62 mm) and 26-148 mm short carapace width (83.77±3.07 mm), respectively. Number of infested P. pelagicus was found to be 48 (2.9% of the total P. pelagicus examined) (Fig. 3A). The short carapace width of infested crabs varied from 70-140 mm (70-120 mm for non-berried female, 84-107 mm for berried female and 77-140 mm for male). Total number of octolasmids hosted by these 48 P. pelagicus was 188 (Table II).

Table II.- Number of octolasmids hosted by Portunus pelagicus (n = 48).

Species	Number	Percent
O. angulata	2	1.1
O. cor	11	5.8
O. lowei	174	92.6
O. tridens	1	0.5
O. warwickii	0	0
Total	188

Frequency of infestation

Forty four crabs out of 48 were infested by O. lowei only, while one crab each was infested by O. angulata, O. tridens and O. cor. Only one crab having 120 mm short carapace width hosted two species: O. cor (4 individuals) and O. lowei (1 individual). In other words O. lowei was found in 45 (44+1) crabs, O. cor in 2 crabs and O. angulata and O. tridens in one crab each. Octolasmis warwickii was not found in P. pelagicus during present investigation.

Octolasmids prevalence in male and female P. pelagicus was found significantly different as determined by chi-square test (x2 = 18.75; α = 0.05). Out of 48 infested crabs, only 9 were males (18.8%) and remaining 39 were females (81.2%) including 10 berried (25.6% of the total infested females) (Fig. 3B).

Intensity of infestation

The most heavily infested crab was a berried female having 94 mm short carapace width. This female crab harboured 21 O. lowei in the gill chambers (17 in the left gill chamber and 4 in the right). The next most heavily infested crab was a male, having 125 mm short carapace width, which harboured 14 O. lowei (7 in each gill chamber).

The mean intensity of infestation was found to be 3.92±4.44 S.D (range 1-21). The mean intensity of infestation was not found significantly different between male (mean 4.11±4.10 S.D) and female (3.87±4.57) as determined by student’s t-test (t = 0.207; α = 0.05). The intensity of infestation was also found insignificantly different between berried (4.4±6.3) and non-berried females (3.69±3.9) (t = 0.501; α = 0.05).

Relationship between the number of octolasmids found in the gill chambers and size of the crab is shown in Figure 3C. Although the rate of infestation was found to increase with the increase in size of the host crab, the two variables are poorly correlated (R2 = 0.0802). The regression equation was found to be y = 0.0748 x- 3.0175, where y is the number of octolasmids and x is the short carapace width of the crab.

Seasonal abundance of infested crab

Infested P. pelagicus was registered in all months except in January, February, April, May, November, December 2004, July, September and December 2005. The highest number of infested crab was recorded in March 2005 (32%) followed by April 2005 (11%) and March 2004 (10.6%) as shown in Figure 3D.

Table III.- Size frequency distribution of infested Portunus pelagicus in different size groups.

Size- group (SCW ) mm	Number of crabs			No. of Octolasmid	No. of male crabs			No. of Octolasmid	No. of female crabs			No. of Octola smid
Size- group (SCW ) mm	Exa.	Inf.	%	No. of Octolasmid	Exa.	Inf.	%	No. of Octolasmid	Exa.	Inf.	%	No. of Octola smid
23-38	27	0	0	0	12	0	0	0	15	0	0	0
39-54	112	0	0	0	60	0	0	0	52	0	0	0
55-70	320	0	0	0	160	0	0	0	160	0	0	0
71-86	580	25	4.31	72	245	4	1.63	10	335	21	6.27	62
87-102	443	11	2.48	44	227	1	0.44	2	216	10	4.63	42
103-118	131	5	3.82	35	64	0	0	0	67	6	8.95	35
119-134	42	5	11.9	32	19	3	15	20	23	2	8.69	12
135-151	13	1	7.69	5	2	1	50	5	11	0	0	0
	1668	48	2.82	188	789	9	1.14	37	879	39	4.44	151

Exa., examined; Inf., infested; SCW, short carapace width.

Size frequency distribution of infested crab

Table III shows size frequency distribution of infested P. pelagicus. The three smallest size groups (23 mm to 70 mm) had no infested crab at all, although a total of 459 crabs belonging to these size-groups were carefully examined for the presence of octolasmids. The highest percentage of infested crabs was found in size-group 119-134 mm, where 11.9% crabs harboured octolasmids. The next highest percentage of infested crabs was found in size group 135-151 mm followed by size group 71-86 mm. Crabs belonging to size-group 87-102 mm had the least percentage of infested crab (2.48%).

Portunus sanguinolentus

The number of P. sanguinolentus examined was 1057 (635 male, 442 female including 128 berried female). The size of the male and female crabs ranged from 24-122 mm short carapace width (80.3±7.4mm) and 28-130 mm short carapace width (76.9±6.42 mm), respectively. Number of infested P. sanguinolentus (Fig. 4A) was 114 (10.8% of the total P. sanguinolentus examined). Out of which 69 (60.53%) were male and 45 (39.47%) were female including 10 berried female. The short carapace width of infested crabs varied from 67-130 mm (67-117 mm for berried female, 68-122 mm for male and 70-130 mm for non- berried female). Total number of octolasmids hosted by these 114 P. sanguinolentus was 5168 (Table IV).

Table IV.- Number of octolasmids hosted by Portunus sanguinolentus.

Species of Octolasmis	Number	Percent
O. angulata	104	2.01
O. cor	12	0.23
O. lowei	4425	85.62
O. tridens	624	12.07
O. warwickii	3	0.06
Total	5168

Frequency of infestation

Table V shows number of P. sanguinolentus infested by different species of Octolasmis. Forty four crabs out of 48 were infested by O. lowei only, while one crab each was infested by O. angulata, O. tridens and O. cor. Only one crab having 120 mm short carapace width hosted two species: O. cor (4 individuals) and O. lowei (1 individual). In other words O. lowei was found in 45 (44+1) crabs, O. cor in 2 crabs and O. angulata and O. tridens in one crab each. Octolasmis warwickii was not found in P. pelagicus during present investigation.

Octolasmids prevalence in male and female P. pelagicus was found significantly different as determined by chi-square test (x2 = 18.75; α = 0.05). Out of 48 infested crabs, only 9 were males (18.8%) and remaining 39 were females (81.2%) including 10 berried (25.6% of the total infested females) (Fig. 4B).

Table V.- Number of Portunus sanguinolentus infested by different species of Octolasmis.

No. of crabs	Infested by Octolasmis species (No. of octolasmids)
78	O. lowei (751)
24	O. lowei (2567) + O. tridens (280)
3	O. lowei (89) + O. cor (11)
2	O. lowei (750) + O. tridens (155) + O. warwickii (2)
1	O. angulata (6)
1	O. cor (1)
1	O. tridens (1)
1	O. lowei (15) + O. angulata (1)
1	O. angulata (94) + O. tridens (6)
1	O. lowei (154) + O. tridens (165) + O. angulata (1)
1	O. lowei (99) + O. tridens (17) + O. angulata (2) + O. warwickii (1)
114	O. lowei (4425) + O. tridens (624) + O. angulata (104) + O. cor (12) + O. warwickii (3) = (5168)

Intensity of infestation

The most heavily infested crab was a female (non- berried) having 80 mm short carapace width. This female crab harboured 537 octolasmids (473 O. lowei + 64 O. tridens) in the gill chambers. The right gill chamber had 301 octolasmids (246 O. lowei + 55 O. tridens) while the left gill chamber had 236 octolasmids (227 O. lowei + 9 O. tridens). The only specimen of O. warwickii found in male crab was attached to fifth swimming leg (Fig. 5A, B). The second most heavily infested crab was a male of 120 mm short carapace width and was found infested with 471 octolasmids (436 O. lowei + 34 O. tridens + 1 O. warwickii). The right gill chamber of this particular crab harboured 175 octolasmids (155 O. lowei + 20 O. tridens) whereas the left gill chamber had 295 octolasmids (281 O. lowei + 14 O. tridens). O. warwickii found in this crab was attached on the carapace (Fig. 5C).

The mean intensity of infestation was found to be 34±74.16 (range 1-537). The mean intensity of infestation was not found significantly different between male (29.68±68.74) and female (40.52±81.73) as determined by student’s t-test (t = 0.692: α = 0.05). The intensity of infestation was also found insignificantly different between berried (37.5±59.25) and non-berried female (40.62±86.88) (t = 0.0935: α = 0.05).

Table VI.- Size frequency distribution of infested Portunus sanguinolentus in different size-groups.

Size-group (SCW ) mm	Number of crabs			No. of Octolasmid	No. of male crabs			No. of Octolas mid	No. of female crabs			No. of Octola smid
Size-group (SCW ) mm	Exa.	Inf.	%	No. of Octolasmid	Exa.	Inf.	%	No. of Octolas mid	Exa.	Inf.	%	No. of Octola smid
23-38	7	0	0	0	4	0	0	0	3	0	0	0
39-54	8	0	0	0	5	0	0	0	3	0	0	0
55-70	81	7	8.64	16	22	1	4.54	2	59	6	10.2	14
71-86	479	46	9.6	809	280	29	10.36	123	199	17	8.54	686
87-102	394	29	7.36	1167	267	18	6.74	464	127	11	8.66	703
103-118	76	24	31.58	1890	50	15	30	863	26	9	34.6	1027
119-134	12	8	66.66	1286	7	6	85.71	1160	5	2	40	126
	1057	114	10.78	5168	635	69	10.86	2612	422	45	10.7	2556

Exa., examined; Inf., infested; SCW, short carapace width.

Relationship between the number of octolasmids found in the gill chambers and size of the crab is shown in Figure 4C. The regression analysis revealed that the two variables are not strongly correlated (R2 = 0.1372), although the rate of infestation was found to increase with the increase in size of the host crab. The regression equation was found to be y= 1.9492x -139.51, where y is the number of octolasmids and x is the short carapace width of the crab.

Seasonal abundance of infested crab

Infested P. sanguinolentus was registered in all months except in January, February, April, May, November, December 2004, July, September and December 2005. The highest number of infested crab was recorded in March 2005 (32%) followed by April 2005 (11%) and March 2004 (10.6%) as shown in Figure 4D.

Size frequency distribution of infested crabs

Table VI shows size frequency distribution of infested P. sanguinolentus. The two smallest size groups (23mm to 54 mm) had no infested crab, although a total of 15 crabs belonging to these size groups were carefully examined for the presence of octolasmids. The highest infestation was found in size group 119-134 mm, where 66.66% crabs harboured octolasmids. The next highest infestation (31.58%) was found in size-group 103-118 mm. These two size groups (that is 103-118 and 119-134 mm) contained 98.24 % of the total octolasmids. Crabs belonging to size group 87-102 mm had least percentage (7.36%) of infested crabs (n = 394).

DISCUSSION

The rate of infestation was found markedly low in P. pelagicus (2.9%) and P. sanguinolentus (10.8%) during present investigation than the rates reported by Gaddes and Sumpton (2004) for P. pelagicus (92%) from Australia and Jefferies et al. (1982) for P. pelagicus (89%) and P. sanguinolentus (57%) from the seas adjacent to Singapore. On the other hand the rate of infestation found in the present study is close to rates reported by Kumaravel et al. (2009) for P. pelagicus (11.1%) and P. sanguinolentus (14.1%) from India. It is well documented in the literature that the infection by rhizocephalan parasite inhabits moulting in crabs which makes infected crab an ideal host for epizoic barnacles (Phillips and Cannon, 1978). Gaddes and Sumpton (2004) reported 92% infestation rate as mentioned above, found 12.3% P. pelagicus infested with rhizocephalan parasites Sacculina granifera Boschma, 1973 and reported that only the female P. pelagicus infected by S. granifera exhibited higher barnacle abundances. They attributed this higher infestation rate to the different habitat preferences of females (Sumpton et al., 1989) rather than rhizocephalan parasitization. However, Walker (2001) from Australia reported that the branchial chambers of rhizocephalan parasitized crab Charybdis callianasa had the greatest number of barnacle O. angulata. During present study not a single crab (out of 1668 P. pelagicus and 1057 P. sanguinolentus) was found parasitized by rhizocephalan. Parasitisation of P. pelagicus by rhizocephalan has never been reported from Pakistan so far. Recently Moazzam and Moazzam (2004) reported Hetrosaccus ruginosus Boshma, 1931 – a rhizocephalan parasite – from two specimens of P. sanguinolentus obtained from Karachi Fish Harbour (commercial landing) in November 1998. Some other species of anomuran crabs like Petrolisthes boscii Audouin 1826, and P. rufescens Heller, 1861 and brachyuran crabs such as Leptodius exartus (H.M. Edward, 1834) occurring in the coastal waters of Pakistan were found infested with rhizocephalan parasites (Ahmed and Mustaquim, 1974; Siddiqui and Ahmed, 1994). These parasitized crabs were not studied for epizoic infestation, so the effect of the parasite on epizoic cannot be gauged from these studies.

Octolasmids prevalence in male and female crabs was found significantly different in this study which contrasts the finding of Gaddes and Sumpton (2004) for P. pelagicus from Australia, who reported insignificant difference in the prevalence of octolasmids between male and female. In the present study it was found that octolasmids prevalence was significantly higher in female P. pelagicus (81.2%) than that of male (18.8%) while in case of P. sanguinolentus the prevalence was significantly higher in male (60.5%) rather than female (39.5%). This finding of present study – as far as P. pelagicus is concerned – supports the observation of Shields (1992) from Australia who found significantly more Octolasmis spp. in female P. pelagicus. Shield (1992) stated several factors that may help to explain the differences in the prevalence of epizoites between the sexes. These factors include slower growth rate (that is longer intermoults period) in female crabs and possible differences in the feeding and migratory habits between the sexes that may result in different prevalence of epizoites.

Size of the crab was found positively correlated with the number of octolasmids in the present study, although the relationship was not found strongly correlated. Similar observations have been reported earlier by Jefferies et al. (1992) for Scylla serrata from Thailand, Santos and Bueno (2002) for Callinectes danae from Brazil, Mantelatto et al. (2003) for ten species of brachyuran crabs from Brazil, Yan et al. (2004) for Charybdis feriatus from China, Kumaravel et al. (2009) for five species of crabs including P. pelagicus and P. sanguinolentus from India and Mushtaq and Mustaquim (2009) for Scylla cf. tranquebarica from Pakistan.

CONCLUSION

In the coastal waters of Karachi, Portunus pelagicus and P. sanguinolentus are not as heavily infested by octolasmids as reported from elsewhere. P. sanguniolentus is more prone to the infestation than P. pelagicus. Absence of rhizocephalian parasites in the two crabs species are noteworthy.

ACKNOWLEDGMENTS

Thanks are due to Pakistan Science Foundation for providing the financial support for this study. The present study was carried out within the Research Project No. PSF/Res/S - KU/ Bio (342).

Statement of conflict of interest

No conflict of interest.

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