Indian Journal of Geo-Marine Sciences Volume 44(1), January 2015 pp. 56-62

Sucker naucrates Linnaeus 1758 of west coast of India S.K. Naik1, Asheesh Shivam2 & A.B.Kar1*

1 Fishery Survey of India, Visakhapatanam-530 001, India

2Fishery Survey of India, Murmugao-403 803, India

[E-mail:[email protected]]

Received 7 January 2014; revised 12 September 2014

Result of the studies made on live sharksucker (commonly known as sucker fish) Echeneis naucrates Linnaeus 1758 collected from November 2003 to October 2005 from the Central west coast of India is discussed in this study. Study indicated the dominance of male with a sex ratio (M:F) of 1:0.4. Length–weight relationship for male and female sucker fish was 3. 3829 3. 6255 W=0.0006536 L (r=0.98) and W=0.0002620 L (r=0.93) respectively. Regression equations between them differed significantly (F= 35.83). There were seven stages of maturity and twelve stages of ova observed in the . Ova observed were between 5-8 and 169-172 micrometer division (0.1 - 0.16 mm and 1.85-1.89 mm respectively). Size at first maturity was 51cm. Fish appears to be a batch spawner. About 38% of the were found with empty stomachs. Gut content analysis showed that the food items are mainly cephalopods and juvenile fishes especially lizard fishes, goat fishes, threadfin breams and anchovies. Females were found to be poor feeders.

[Key words: Sucker fish, sex ratio, Length-Weight relationship, maturity, ova diameter study, food and feeding]

Introduction attempt has been made to understand the biology The members of the family Echeneidae which are of the commonly occurring sucker fish along the commonly known as sucker fishes form ecologically central west coast of India. important community in the coastal and oceanic Materials and Methods waters. Distributed in the warm waters, they are known For this study a total 126 specimens to be found in all the oceans. Out of the eight species collected from the sampling stations covered by recorded worldwide, seven species are known to occur MFV Matsya Vishwa( Stern Trawler,OAL:36.5m, in western Indian Ocean (Fischer and Bianchi1). Four GRT:327.18 T, BHP: 825) and M. F. V species have been reported in the Indian Ocean region. Sagarika(Stern Trawler, OAL:28.8m, GRT:186T, In Indian waters three species of suckerfish viz, BHP:650) of Fishery Survey of India, during their Echeneis naucrates (Live Sharksucker), routine survey cruises from Dec 2003 to remora ( sucker) and Remora brachyptera November 2005 were used. The samples were (Spearfish Remora) have been recorded. However, the collected from the area 110 N to 180 between 35m species E. naucrates is commonly caught. They and 200 m depth using two types of demersal associate themselves with host species like , trawl nets viz 27.5 m fish trawl and 30m shrimp perches, sting rays, turtles, dolphins, , dugongs, trawl. manatees and even ships for their transportation as well Frozen samples were brought to the as feeding. They do so as they lack the essential swim laboratory to record the total length, weight, sex, bladder to maneuver comfortably. The sucking stages of maturity and gut content after thawing. apparatus of the sucker fish is located at the top of the For length-weight analysis TL (tip of snout to tip head which is its modified spiny dorsal fin. It consists of upper caudal lobe in centimeter) was taken and of numerous pairs of crests capable of producing weight to the nearest gram was taken. Sex ratio strong vacuum helping it to attach to its hosts. But (M: F) was calculated. Length weight relationship species of genus Echeneis are often found free W=aLb was calculated as per Le Cren11. swimming and found in inshore and off shore waters. Regression lines of both males and females were Association of the species with sharks, Cetaceans tested for significant difference by ANOVA (whales and dolphins), pelagic and reef fish and (Snedecor and Cochran12 ) and significance of Sirenians (Dugongs and Manatees) is well established variation in the estimate of b from 3 was tested (O’Toole2, Fertl and Landry3, Williams & Bunkley using 't ' test where, t= [(b~3)/SEb.]. Maturity Williams4, Mignucei- Giannoni et al5 and Williams stage was examined and classified as per ICES E.H Jr. et al6). Feeding behavior of the species has classification. Ovaries were preserved in 5 % been studied by various researchers (Smith7, formalin for the study of ova-diameter. Each Strasburg8, Burn9 and Marsh et al10).It is one of the ovary was weighed to the nearest 0.01mg. Mass NAIK et al.: SUCKER FISH ECHENEIS NAUCRATES LINNAEUS 1758 57 least studied fish in Indian waters and biological of ova was weighed. From this, 3 sub samples information on this particular species occurring in the from each lobe (anterior, middle and posterior) Indian coast is not documented well. In this study an were taken and Gilson’s fluid was added to it and the number of ova was counted and the diameter But in case of female, it was not significantly was measured with the help of an ocular micrometer different from 3 (t=3.3272; df=35). ANOVA attached to a binocular microscope. Ova diameter results obtained for the species are given in table measurements were further analyzed by plotting the 2. Regression lines for male and females were ova diameter with the frequency and observing the significantly different (F= 35.8287).Hence a occurrence of the modes to find out different stages of combined length weight equations could not be ova of the species. Gonado-somatic index was proposed for the species. estimated by the following formula. The results of the detail examination of the ovaries of E. naucrates is given below -In order to Gonado-Somatic Index (GSI) = study the maturity and ascertain the spawning Weight of gonad X100 season 36 females were examined. Maturity Weight of fish stages were recognized both by gross observation Gut content analysis was carried out following Index as well as by the ova diameter measurements. The of Relative Importance (IRI), Pinkas et al13. description is given below: Results Immature I Ovary translucent, orange Stage A red in colour, occupy less Sucker fish, was dominated by a single species E. than 30% of body cavity. naucrates and is distributed in the area Lat 11°N to Eggs microscopic. Not 18°N where as only few samples of E. remora were visible without aid. recorded in the area between Lat. 140N and 150 N. Frequencies with one mode They occurred free swimming in deep as well in shore (5-8 M.D, 0.05-0.08mm), shallow water depth ranging from 30 – 85 M. Among maximum ovum diameter is the recorded species 90 were males ranging from 28 – 25-28 M.D( 0.27-0.30mm). 70 cm in length and weighing 44 - 1050 gm and 36 This stage was common all were females ranging from the 33-62 cm in length and year round. weighing 93-866 gm. Maturing II Ovary translucent, A total of 126 specimens consisting of 90 males Stage B somewhat reddish brown in measuring 28-70cm and 36 females measuring 33-62 colour and occupies 40% cm were taken for sex ratio analysis. Sex ratio portion of the body cavity. indicated the dominance of male in all the size groups. Eggs are not visible to The male to female ratio was found to be 1:0.4.The naked eye, very small in males completely outnumbered the females in all the size. Frequencies with one size groups except 51-60cm where the female mode (9-12 M.D, 0.09- population came close to the male (1:0.7) (Table 1). 0.13mm), maximum ovum diameter is 57-60 M.D Table.1. Sex ratio(M:F) of E naucrates in the west coast of India (0.62-0.66mm). Length range(cm) Male Female Ratio Maturing III Ovary light red in colour, Stage C,D occupies 40% of the 21-30 01 -- -- visceral cavity. Eggs 31-40 04 01 1:0.25 visible. Frequencies with three to five modes, 41-50 18 04 1:0.22 maximum ovum diameter is 51-60 40 28 1:0.70 97-100 M.D (1.06- 61-70 27 03 1:0.11 1.10mm). TOTAL 90 36 1:0.4 Mature IV Ovary large, orange to Stage E, reddish yellow coloration, The data for the length weight study was analyzed F,G reaches upto 70% of the separately for both the sexes and the equations body cavity, lumen filled obtained are as follows. with eggs, eggs large, Males : Log W= -3.1847+3.3878 Log L (r = 0.98) opaque, clearly visible. Female: Log W= -3.5817 +3.6255 Log L(r= 0.93) Frequencies with seven The slope for male was significantly different from modes, maximum ovum 3(t=1.4496; df=89). diameter is 137-140 M.D

(1.50-1.54mm). 58 INDIAN J. MAR. SCI., VOL. 44, NO.1 JANUARY 2015

Fishes up to 61cm come under this. The stages Ripe V Ovary massive, yellowish in I,J and K indicates partial spent ovaries. In stage Stage H colour, occupies almost entire I two major modes wire there in the beginning body cavity. Eggs clearly visible and subsequently due to spawning activities there and blood vessels clearly seen on are no modes however there were few minor the gonads. Eggs are ready to be modes to the last. Above 125 M.D (1.37mm) released. Frequencies with seven there were no ova. In stage J however due to major modes, maximum ovum spawning activities only two major modes were diameter is 169-172 M.D(1.85- noticed and they were in the last. Above 136 1.89mm). M.D (1.49mm) there were no ova. In the stage K Partial VI Ovary pale, reddish, covers 60% spawning was more and very few minor modes spent of the body cavity. Opaque eggs, were noticed with no ova beyond 112 Stage I, yellowish. Ovary hollow inside. M.D(1.23mm). The occurrence of the three J.K Gonad reduced and flaccid. Blood stages of ova were more during different times of vessels clearly seen. Eggs partly the year. The stage L represents the completely released. Frequencies with two spent ovary. It indicates the spawning activity is major modes, maximum ovum intense and all groups of matured ova are diameter is 133-136 M.D(1.46- released except one mode in the beginning. This 1.49mm). is clear that this group of ova will be there during Fully VII Ovary reduced, in a shrunken the resting stage of ovary and is carried over to Spent stage and occupies half of the the succeeding season for the spawning activity. Stage L body cavity. Reddish in colour. All these indicates that the spawning of the Most of the ova released a few are species is a continuous process. there to be released. Frequencies For this study the percentage of maturing and with two major modes, maximum mature ovaries was taken into consideration. ovum diameter is 65-68 M.D When the % was plotted against the total length a (0.71-0.74mm). Resembles stage sigmoid curve was obtained (fig.2). This curve B( II). shows that 50% of fish are mature at 51 cm, 80% The ova diameter frequency in various months has at 56cm and almost all fishes over 58cm. Hence shown that the fish is a batch spawner and has the fish attains first maturity in the size 51cm prolonged breeding season. The stages of maturity (50% mature ovaries). From the figure 3 it could varies in a different months, even in a particular month be seen that all individuals less than 40cm were almost all stages of maturity were noticed. Hence the immature (stage I). Fish maturing at 41-50cm ovaries were grouped according to the largest mode in length and 50% maturity was attained at 51- the diameter frequency curve. The results indicated 12 60cm. Maturing stages as well as mature stages of maturity (fig. 1(A to L). specimens were encountered in this length group. Stage A (I) is the immature ovary and has only one However fully matured, partial spent and fully group of ova. Fishes upto 41 cm were in this stage. This spent ovaries were encountered in the length particular stage was encountered throughout the year. range 61-70cm. Stage B shows the shifting of the mode to the next The Gonado Somatic Index (GSI) varied diameter group from the immature stock. Fishes of size from 0.19 (stage I) to 1.64(stage VII) in the case 45cm comes under this stage. Stage C (III) shows three of male. However in the case of female it was distinct modes and the shifting of modes from the 0.51(stage I) to 7.59(stage IV), 8.65(stage V) and previous stage. In stage D there appears another two 1.65(stage VII), which clearly indicates that minor modes in the higher ova diameter group. Fishes stage IV and V are the mature and ripe stages up to the size 46cm comes under this stage. Stages E, F and spawning activity starts in the stage VI and it and G are mature ovaries where the gradual withdrawal is intensive in stage VII(fig. 4). of different groups of ova from the reserve stock was Among the stomachs of 126 specimens noticed. Fishes up to the size 56cm comes under this. examined, 15.1 % were gorged, 27.8 % were The stages F and G shows the advance of the modes of full, 7.9 % three fourth, 10.3% half full, 0.8% maturing ova. The stages H represents the fully one fourth and 38.1% were empty. matured/ripe ovary with seven major modes and all groups of ova. Further emergence of maturing group of ova was not encountered after this stage and spawning NAIK et al.: SUCKER FISH ECHENEIS NAUCRATES LINNAEUS 1758 59 started after this.

Table.2.Comparison of regression lines (ANOVA) of E.naucrates (male & female)

Source of Df (n-1) SSQ SSQ SSQ B Df SSQ MSSQ Variation X Y XY Within

Male 89 0.508 5.863 1.719 3.382 88 0.047 0.0005

Female 35 0.092 1.224 0.334 3.625 34 0.011 0.0003

Deviation from individual regression 122 0.059 0.0004 (MSSR)

Pooled data 124 0.600 7.087 2.053 3.420 123 0.063 0.0005 (MSSP)

Difference between slops 1 0.004 0.0045 (MSSE)

Individual regression(MSSE/MSSR) 9.488

Total Data 125 0.600 7.086 2.056 3.424 124 0.045 0.0003

Between adjusted mean 1 0.018 0.018 MSSA

Individual interception or elevation(MSSA/MSSP): 35.828

100 M 10 90 8.65 a 9 7.59 t 80 8 u 70 G 7 r 5.29 60 S 6 i 50 5

( I t 4 40 1.65

%)

( y 4041 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 3 1.93 2.13 2.02 1.66 1.64 %) 2 1.24 0.51 0.49 0.78 Total Length(cm) 1 0.19 0 Stage I StageII Stage Stage Stage Stage Stage Fig.2.Size at first maturity of E.naucrates in the West coast of India. III IV V VI VII

Stages of Gonads

Male Female

Fig.4.Gonado Somatic Index(GSI) of E. naucrates in the West coast of India

Fig.3. Relative proportion of gonad stages and maturity(%) of E. naucrates(female)

60 INDIAN J. MAR. SCI., VOL. 44, NO.1 JANUARY 2015

50.0 L,1(Stage-VII)

0.0 50 K,9(Stage-VI)

0 20 J,7(Stage-VI)

0 20 I,6(Stage-VI)

0 10.0 H,4(Stage-V)

0.0 10 G,1(Stage-IV)

0 20 F,1(Stage-IV)

0 20 E,1(Stage-IV)

0 50 D,2(Stage-III) Frequency of Ova(%)

0 50 C,1(Stage- III)

0 50.0 B,1(Stage-II)

0.0 80 A,2(Stage-I) 60 40 20 0

Ova Diameter in Micro Meter Divisions

Fig.1. Ova-diameter frquency polygons of various maturing stages showing the position and progression of modes during maturation of E.naucrates

NAIK et al.: SUCKER FISH ECHENEIS NAUCRATES LINNAEUS 1758 61

Among males 29.5% of the stomachs were empty out in Indian coasts. However the anatomical and in the case of female 71.6% were empty. In males structure, the way of association with host species the average volume of food per fish was 7.2 ml. and and its feeding pattern made the species unique to female 6.9 ml. Index of Relative Importance (IRI) be studied. Out of the four species recorded in the et al13 (Pinkas ,) was used to ascertain the dietary Indian Ocean only three are recorded and composition by taking into consideration the documented in Indian waters. Present study was percentage, number, volume and frequency of specifically undertaken to throw some light on a occurrence of the prey. In the species E. naucrates, least studied fish having some interesting features. Loligo duvauceli composed the bulk of the diet (45% vol, 66.5% IRI) and formed the most important and This is recorded almost everywhere around the abundant prey. Second most important and abundant world and mostly in tropical waters. It is not very prey was lizard fish (Saurida tumbil) which clear whether the species is an active feeder or contributed 17.7% by volume, 26.3% by number and takes the rejected food of the host or the host fecal with an IRI of 21.5%. Other two dominant items were matters. Williams Jr. et al6 reported fecal matters Upeneus spp. with an IRI of 6.8% and Saurida in the gut of the shark sucker in the Australian and undosquamis with an IRI of 3.9%. Rest of the items South African waters and established the accounted for < 1% of the diet and all together they Echeneid and Sirenians association. Presence of contributed 1.3% IRI (table 3). fin fishes, shell fishes and mollusks in the gut of

the species and also the percentage of

Table.3. Index of Relative Importance of E.naucrates in the West digestion(quality of gut)clearly indicates that this coast of India species is just like other fin fishes and must be collecting its own food. But it is a well Species/groups %No %Vol IRI established fact that the species lacks a swim bladder and rely on others (host species) for Loligo duvauceli 49.7 45.0 66.522 locomotion hence it can not be an active feeder. Saurida tumbil 26.2 17.7 21.482 Considering this it can be said that the species Upeneus spp 7.0 14.7 6.790 gets its food from some other sources and the Saurida undosquamis 5.0 10.7 3.987 following can be said about the possible ways of getting the food. By analyzing the gut contents it Stolephorus commersoni 3.4 1.3 0.092 is clearly seen that there is no trace of fecal

Nemipterus japonicus 2.3 3.0 0.511 matters of the Sirenians (Dugongs and Manatees).

N. mesoprion 1.6 1.8 0.200 Hence the possibility of association with Sirenians and depending on them for food as reported Leiognathus spp. 1.1 0.2 0.053 earlier (Williams Jr. et al 6) is completely ruled Lutjanus spp. 0.9 0.6 0.059 out. Crab 0.9 0.2 0.068 Next thing to ponder is the association of the species with a piscivorous host for the Decapterus russelli 0.7 2.0 0.105 rejected/leftover food of host species for its own Semi digested fish 0.5 2.0 0.096 consumption. This appears to be correct as the gut Epinephelus diacanthus 0.2 0.1 0.006 comprised of mostly bony fishes and cephalopods. It could be with sharks or with Cetaceans like Aluterus spp. 0.2 0.1 0.007 dolphins, which is not confirmed. The feeding

Cynoglossus spp. 0.2 0.2 0.005 behavior of shark suggests that the host species Other cephalopods 0.1 0.4 0.017 could be shark. In depth biological analysis

100.0 100.0 100.0 indicated that the species is just like other bony fishes. Discussion The sex ratio indicated the dominance of male Studies on the Sucker fish in Indian coast is limited to in the population and the dominance was more in only reporting of occurrence. There is no clear study the higher length class (51-60cm and 61-70cm). on the association of the species with the host species. Length weight study indicated a positive As it is not taken commercially hence aimed fishery allometry however the t test indicated that the does not exist for the species and due to lack of the slope for male was significantly different from 3 availability of specimens the biological studies for this species has not been carried 62 INDIAN J. MAR. SCI., VOL. 44, NO.1 JANUARY 2015 and also the ANOVA study indicated that the 5. Mignucci-Giannoni, A. A., Beck, C. A., Montoya- regression coefficient for the both the sexes Ospina, R. A. and Williams Jr., E. H. Parasites and commensals of the West Indian manatee from Puerto significantly differ and hence a single equation Rico. Journal of the Helminthological Society of combining both the sexes could not be derived. Fish Washington., 66(1999) 67-69. attains maturity at 51 cm. Reproductive studies such as ovary maturity and microscopic study i.e ova diameter 6. Williams Jr., E.H., Mignucci- Giannoni,A.A., Bunkleywilliams,L., Bonde,R.K., Selfsullivan,C., study has indicated that there are seven stages of Preen,A. and Cockcroft, V.G. Echeneid-sirenian maturity observed and there are 12 different stages of associations, with information on sharksucker diet, ova encountered in the seven different maturity stages. Journal of Fish Biology.,(2003)1-6. The species has prolonged breeding season and is a batch spawner. GSI indicated that stage IV and V are 7. Smith, J. L. B., The Sea Fishes of Southern Africa. Capetown, South Africa: Central News Agency.,(1950) mature and ripe stages and spawning activity starts in 550 p. the stage VI and it is more in stage VII. The feeding pattern indicated that the species is 8. Strasburg, D. W., Notes on the diet and correlating associated with a piscivorous host. Preference for food structures of some central Pacific echeneid fishes. in the species is also ruled out as the fish does not Copeia.,( 1959) 244-248. search for its food instead it takes food that are lost or rejected by the host. Gut intensity indicated that the 9. Burn, D. M., The digestive strategy and efficiency of the West Indian manatee, Trichechus manatus. Comparative females were poor feeder (75% empty stomach). Biochemistry and Physiology., 85A (1986) 139-142. Dietary composition indicated the dominance of (L. duvauceli) with an IRI of 66.5% followed by 10. Marsh, H., Beck, C. A. and Vargo, T. A., comparison of Lizard fish (S. tumbil) with an IRI of 21.5%. Other the capabilities of dugongs and West Indian manatees to items leaving Upeneus spp. and S. undosqamis masticate sea grasses. Marine Mammal Science., 15(1999) 250-255. contributed very little to the composition. Conclusion 11. Le Cren E D. The length-weight relationship and seasonal cycle in gonad weight and condition in the One of the least studied fish in the Indian waters is perch (Percafluviatilis).I. Anion. Ecol., 20(1951)21-219. the shark suckerfish. Present study has revealed some biological aspects of the fish. It is clearly understood 12. Snedecor,G.W and Cochran, W.G. Statistical Methods. that in the west coast of India the host species of the Lowa State University Press.,(1967). sucker fish are not the Sirenians (Dugongs and Manatees) and it could be either shark or dolphin or 13. Pinkas, L., Olipahnt,M.S. and Iverson,I.L.K. Food whales. Next important aspect is that the sucker fish habits of albacore, bluefin tuna, and bonito in Californian waters. Calif. Dep.Fish Game, Fish. associate with the host probably for three main causes Bull.,(1971) 152: 1-105. i.e locomotion, protection (to save from predators) and food. Acknowledgement Authors are grateful to the Director General, Fishery Survey of India, Mumbai for suggesting the topic and encouragement. References 1. Fisher, W. and G. Bianchi., (eds), FAO Species identification sheets for fishery purpose- Western Indian Ocean( fishing area 51), Vol.V(1984) FAO, Rome. 2. O’Toole, B., Phylogeny of the species of the superfamily Echeneoidea (Perciformes: Carangoidei: Echeneidae, Rachycentridae, and Coryphaenidae), with an interpretation of echeneid hitchhiking behaviour. Canadian Journal of Zoology., 80(2002) 596-623. 3. Fertl, D. and Landry, A. M., Sharksucker (Echeneis naucrates) on a bottlenose dolphin (Tursiops truncatus), and a review of other cetacean-remora associations. Marine Mammal Science., 15(1999) 859-863. 4. Williams Jr., E. H. and Bunkley-Williams, L., Parasites of Offshore, Big Game Sport Fishes of Puerto Rico and the Western North Atlantic Mayagüez, Puerto Rico: Puerto Rico Department of Natural and Environmental Resources and Department of Biology(1996) University of Puerto Rico, 384p.