311
Abstract.-Populations ofAtlantic hagfish, Myxine glutinosa (L.), are A population profile for Atlantic found throughout the GulfofMaine in hagfish, Myxine glutinosa in the soft-bottom substrates atdepths greater fl.), than 50 m. This report presents data Gulf of Maine. Part I: Morphometries on the sizes. weights, morphometric characters, and reproductive states for and reproductive state specimens collected at a study site ap proximately 50 km offshore in the Gulf of Maine. Limited comparisons with Frederic Martini'" data from specimens collected else where suggest that this data setis rep John B. Heiser'" '" resentative of hagfish populations Michael P. Lesser'" '" '" within the inner Gulf of Maine. The small number of eggs produced (less Shoals Marine Laboratory. G-14 Stimson Hall than 30 per female), the large number Cornell University, Ithaca. New York J4853 ofanimals withoutmacroscopically vis 'Present address: 5071 Hana Hwy. Haiku. Hawaii 96708 ible gonadal tissue (25% ofthe popula E-mail address:[email protected] tion), and the small number of males «6% ofthe population). gravid females "Present address: Section of Ecology and Systematics (<1%1. and postovulatory females «5%) Cornell University. Ithaca, New York 14853 suggest that hagfish have limited re '''Present address: University of New Hampshire productive potential. This raises serious Department of Zoology and Center for Marine Biology questions about the long-term viability Durham. New Hampshire 03824 ofthe New England eelskin fishery.
The hagfishes, or Myxinoidea, are unitedunderthe family Myxinidae: worldwide in distribution, with 59 the Eptatretinae, typified by the species recognized at presentCFern genus Eptatretus (30-35 species), holm1). Hagfishes are noteworthy and the Myxininae, typified by the from an evolutionary standpoint genus Myxine (19 species) but also because they represent the oldest including the genera Nemamyxine, extant clade among the craniates. Neomyxine, and Notomyxine (Nel A betterunderstandingoftheirana son, 1994). The characteristics of tomical and physiological charac the Myxine appear to be more de ters may thus reveal information rived than those of the Eptatretus. about an early stage in vertebrate For example, hagfishes ofthe genus evolution. Although eel-like in Eptatretus have multiple efferent general body form, hagfish lack gill openings on each side of the jaws, paired fins, vertebrae, bone, pharynx, vestigial eyes beneath a and a variety ofother gnathostome pale skin patch, and traces of a characteristics. cephalic lateral line complex. In All known species ofhagfish live contrast, hagfishes of the genus inclose association withthebottom, Myxine have a single commoneffer resting on the substrate or occupy ent duct opening on each side ofthe ing burrows within soft sediments pharynx, even smaller eyes covered (Gustafson, 1935;AdamandStrahan, by undifferentiated integument, 1963, a and b; Foss, 1963; Fern and no traces of ~my lateral line holm, 1974; Neira, 1982; Martin components. In general, the genus and Heiser, 1989; Cailliet et al., Eptatretus has a more widespread 1992; Barss, 1993). They are gener distribution than the genus Myxine, ally described as predators on inver whose center ofdiversity appears to tebrates and as opportunistic scav be the New World, where 14 of 19 engers on both invertebrate and
Manuscript accepted 12 November 1996. vertebrate remains. There are two 1 Fernholm, B. 1996. Box 50007, S-104 05, Fishery Bulletin 95:311-320 (1997). major groups of living hagfishes Stockholm, Sweden. Personal commun. 312 Fishery Bulletin 95(2}, J997 species have been identified (Wisner and McMillan, ern Atlantic, and to give western Atlantic popula 1995). tions, including those ofthe GulfofMaine, separate Only one myxinid, Myxine glutinosa L., is found status as Myxine limosa. on both sides of the Atlantic Ocean, and this is the only hagfish reported within the GulfofMaine. There are several reasons why Myxine glutinosa is an im Materials and methods portant species for the GulfofMaine: The primary study site was adjacent to a small rock 1 The substantial numbers present and their ongo ledge known locally as "the Nipper" (near 42°57'N, ing energetic requirements suggest that they play 700 17'W). This site is within the Bigelow Bight, ap a significant role inthe benthic ecosystem through proximately 25 km west of Jeffrey's Ledge and 50 out the Gulfof Maine (Lesser et al., in pressl. km east of the New Hampshire coast. The Bigelow 2 This species has both direct and indirect effects Bight and Jeffrey's Ledge are both important on commercial fisheries in the Gulf of Maine. In groundfishing areas. Hagfish in the study area in areas of abundance their opportunistic feeding habit a superficial zone offine, organic sediment cov habits can reduce the value of the catches made ering a layer ofgrainy clay that overlies a thick layer by longline or fixed gillnet fisheries. Hagfish have of silty clay. Individual hagfish are usually found in been known to feed on restrained or moribund cod, shallow, sinusoidal, temporary burrows, with nose herring, haddock, hake, mackerel, spiny dogfish, and barbels exposed to passing currents. The bot and mackerel sharks caught in fisheries gear tom temperature year-round is 4-6°C, and the sa (Gustafson. 1934; Bigelow and Schroeder, 1953; linity is 32 ppt or higher at all times. The superficial Strahan, 1963). Equally important, feeding stud biotic community includes representatives from sev ies by Shelton (1978) suggest that hagfish preda eral families of tube worms, Cerianthid anemones, tion could have a significant impact on Pandalus tunicates, sponges, and shrimp (Pandalus borealis l. borealis populations within the GulfofMaine. Comparable habitats that could support hagfish 3 Myxine glutinosa populations are now targeted by populations cover 60-70% ofthe floor of the Gulfof American and Canadian fishermen in the Gulfof Maine (National Ocean Service3 ). Maine to meet the South Korean demand for Hagfish were collected with baited traps set on the "eelskin" used to manufacture expensive leather bottom in depths of 130-150 m. The traps consisted goods. In 1990, the sale of eelskin leather goods, of garbage cans with holes punched in the side and all produced from hagfish skin, brought South with an internal screen that funneled hagfish toward Korea revenues ofapproximately US$100 million the enclosed bait. The baited traps were left on the (Gorbman et al., 1990). The value ofeelskin prod bottom fm' periods of30 minutes to 1 hour and then ucts imported into the U.S. alone in 1992 was retrieved. The animals were then placed in seawa US$70 million (Melvin and Osborn2 l. So large is ter chilled to approximately 4°C for transport to the this market that Korean processors, unable to Shoals Marine Laboratory on Appledore Island, supply the demand from overexploited eastern Maine. After being held in refrigerated aquaria for a Asian fisheries, have begun sampling and purchas period ofhours to days, animals were sacrificed and ing hagfish from several other regions, including measurements were taken. The aquarium complex North and South America I.Gorbman et al., 1990l. was monitored daily, and animals dying in captivity During 1993 and 1994, Gulf of Maine fishermen were measured immediately, prior to disposal. Mor harvested roughly 1600 metric tons (3.6 million phometric data were collected from fresh specimens pounds) of hagfish, and there were unknown ef from the primary site between June 1989 and Au fects on the ecologyofthe region (Kuenstner, 19961. gust 1992. Methods ofmeasuring and counting followed those Part 1 of this report presents morphological data of Fernholm and Hubbs (1981) and McMillan and and a population profile generated in a study of a Wisner (984). All measurements were recorded in hagfish population in the Gulf of Maine. Part 2 of millimeters. For descriptive purposes, after total this report, published separately, will relate these length (TLl was recorded, the body axis was divided and other data to the proposal made by Wisner and into 3 regions (snout-pcd, trztnk, and tail regions; McMillan (1995) to reserveM. glutinosa for the east- n=1431 or 4 regions (prebranchial. branchial, trunk,
2 Melvin. E. F., and S. A. Osborn. 1992. Development of the 3 National Ocean Service. Coast and Geodetic Survey. west coast fishery for Pacific hagfish. Seattle, WA. Nat!. Mar. 1995. GulfofMaine and George's Bank, Chart No. 13009. Na Fish. Serv.. NOAA. Final Rep. NA90AA-H-SK142. tional Ocean Service, Silver Springs, MD. Martini et al.: Population profile of Gulf of Maine Myxine glutinosa 313
Table 1 Morphological measurements for the sample population ofAtantic hagfish. Myxine glutinosa.
Character Mean SD Range %TU SD Range n
Total length (mm) 509 104 195-724 100 202 Snout-pcd2 135 27 54--200 27.0 1.6 24--37 143 Prebranchial 82 20 34--130 17.0 1.9 67 Branchial 46 14 16-75 9.3 2.1 5-21 67 Trunk 311 72 107-459 61.4 3.8 42-83 143 Tail 64 14 25-106 12.6 1.1 9-17 143 Width 14 7 4--35 2.7 1.1 2-6 91 Depth (trunk) 22 7 8--35 4.2 0.7 2-7 87 Depth (cloaca) 19 5 6-28 3.7 0.5 2-5 198 Depth (tail) 20 5 8-30 4.0 0.5 2-5 97 Weight (g) 136 67 8-290 80 Total cusps 35 2 28-40 97 Multicusps outer 2 0.3 1-3 97 inner 2 0.1 1-2 97 Unicusps outer 7 0.7 5-9 97 inner 7 0.7 6-9 97 Total slime pores (left side) 114 7 91-128 %TL3 SD Range 94 Snout-pcd 33 4 20-45 29 3.0 21-40 94 Trunk 67 4 51-77 59 2.9 51-69 94 Tail 13 2 8--19 11 1.3 9-15 94
1 %TL = Percentage of total length. 2 pcd = pharyngocutaneous duct. 3 % TP = Percentage oftotal slime pore counts.
and tail regions; n=67). The snout-pcd measurement pcd count, which corresponds to the prebranchial extends from the tip of the snout to the anterior count of Wisner and McMillan (1995). This distinc margin of the pharyngocutaneous duct (pcd), the tion was made to maintain consistency with the trunk continues to the anterior margin ofthe cloaca, length data, where prebranchial and branchial and the caudal region extends from that point to the lengths together constitute the snout-pcd length. tip of the tail. The sum of these measurements is Reproductive state was determined by visual inspec equal to the total length. tion, ratherthan histological analysis. Ifpresent, ova For one series ofanimals, prebranchial and bran were measured and the maximum length recorded. chial measurements were taken within the snout pcd length. The prebranchial region extends from the tip ofthe snout caudally to the rostral margin ofthe Results first gill pouch, the branchial region extends from that point to the anterior margin of the pharyn Table 1 summarizes pertinent morphometric data for gocutaneous duct. this population ofMyxine glutinosa. Hagfish species Width is the maximum width of the trunk; depth in general show remarkable variation in number of (trunk) is the body height, exclusive of fin fold, at gill pouches. Table 2 presents data on the total num that site. Cloacal depth, measured at mid-cloaca, ber of gill pouches in our sample population. The excludes the dorsal fin fold, whereas tail depth spans range of gill pouch data (range:10-14, n=941 is the entire tail, including dorsal and ventral fin folds. greater than that reported for M. glutinosa in the Cusp counts (unicusps and multicusps on outer and eastern Atlantic by Fernholm and Hubbs (1981) inner rows) were recorded for the left side; then the (range: 11-13, n=8). right side was counted to obtain the total cusp count. Despite the size ofthe landings (over 1,400 metric When slime pores were counted, the first two axial tons in 1994 [Kuenstner, 1996]), there are relatively regions were combined and recorded as the snout- few available data concerning the lengths and 314 Fishery Bulletin 95(2), 1997
Note the preponderance of adult specimens and Table 2 the absence ofjuveniles smaller than 195 mm (7.6 Number ofgill pouches in Myxine glutinosa (n=94,. in.) atthis collection site. No smallerindividuals have been seen with ROV's or manned submersibles in No. ofgill pouches (total) this area, either on the soft bottom or over the asso 10 11 12 13 14 ciated rocky ledges (Martini and Heiser, 1989: 1991). Data on 1,172 animals from other locations in the Incidence (%) 1.1 1.1 74.5 7.4 15.9 Gulf of Maine (details below) indicate animals as small as 170 mm TL. However, the size of M. glutinosa. at hatching has been estimated to be ap weights of the harvested hagfish. This may in part proximately 50 mm (Fernholm, 1969), and there has reflect the effort required to immobilize and weigh longbeen a general consensus that hagfishes, includ individual hagfish. To address this problem we re ingMyxine, do nothave a larval stage (Putnam, 1874: viewed the morphometric data for a relatively quick Dean, 1900; Worthington, 1905: Walvig, 1963I. The and reliable method ofestimating sizes and weights absence of animals of 50-170 mm TL from traps at in the field. The easiest and most accurate method widespread locations and in visual surveys of bait found involved measuring the depth of the body at stations suggests that newly hatched M. glutinosa. the cloaca, excluding the dorsal fin fold. The fin fold may target different feeding resources from those was excluded to make the measurement easier to targeted by older animals. Juveniles may, for ex perform at sea with unanesthetized animals. (A cali ample, feed solely on invertebrates within the sub per measurement of cloacal depth can be taken strate. quickly, with minimal stress to the animal.) No data are available concerning the reproductive Figure 1 presents the relationship between total cycle and behavior of M. glutinosa.. The sampled length and weight for a sample population of n=83. population contained a mixture of sexually imma Figure 2A is a length histogram for the entire sample ture and sexually mature individuals (Fig. 4>. The population (n=306) which comprised 202 animals following patterns can be recognized: whose lengths were measured directly (see Table 1) and 104 lengths calculated on the basis of cloacal 1 Individuals shorter than 400 mm TL are sexually depth using the formula shown in Figure 2B. immature. These animals either lack macroscopi Figure 3A is a weight histogram for the entire cally visible gonads altogether or have granular sample popul~tion which comprised 80 direct mea tissue in the gonadal mesentery that cannot be surements (see Table 1), 122 weights calculated on identified as either testicular or ovarian in nature. the basis oftotal length (see Fig. 1), and 104 weights 2 Approximately 59% of the population is classified calculated on the basis ofcloacal depth with the for as females on the basis ofegg development. Testicu mula shown in Figure 3B. lar tissue is usually rudimentary in these animals.
300
250 y = 13.699 - 0.222)( + 0.001 x' 200 § 1: Cl 150 s:'ill 100
50
0 100 200 300 400 500 600 700 800 Total length (mm)
Figure I Total length (mm) versus body weight (gl in a sample population of Atlantic hagfish, Myxine glutinosa In=801. Martini et al.: Population profile of Gulf of Maine Myxine glutinosa 315
3 Males represent a very small percentage of the slime pores is fixed for each individual and that ad population Uess than 6%). ditional slime pores are not added as growth occurs. 4 Roughly 25% ofthe adult population does not have However, with growth, the prebranchial region forms macroscopically identifiable gonadal tissue; the a significantly smaller percentage ofthe total length. presence of large numbers of sterile individuals The feeding apparatus, consisting of the tooth cusp has also been reported for populations in the east plates and the dental muscle complex (Dawson, ern North Atlantic (Schreiner, 1955; Jespersen, 1960), is therefore relatively large in smaller indi 1975). viduals. No data are available concerning the life 5 The overlap in sizes between males and females span or growth rates for this species. suggests neither protandry nor protogyny. To determine whether or not our data were repre sentative ofthe Gulf ofMaine as a whole, we began Regression analyses were performed on morpho by comparing the morphological data from our study logical data sets to detect significant trends. No re site with data from eight specimens collected at lationships were found between total slime pores, Stellwagen Bank in Massachusetts Bay (42°20'N, snout-pcd slime pores, or tail slime pores versus to 700 17'W), roughly 36 km from our primary studysite. tal length. This finding indicates that the number of The size range (460-600 mm TL; average: 523 mm
BO 70 A -- 60 c 50 - 5 40 U '-- 30 - 20
10 o ~ h o 100 200 300 400 500 600 700 BOO 900 1000
TOlallenglh (mm)
BOO
700 B 0 E y = 43.922 + 31.BB5x - 0.342x' E- 600 ~ l: 500 .!!! 0 "iij (5 400 I- 300
200
100 5 7.5 10 12.5 15 17.5 20 22.5 25 27.5 30
Cloacal depth (mm)
Figure 2 Total length (TLJ(mmJ in the sample population ofAtlantic hagfish. IA) A frequency histogram for total length In=306). This graph in cludes direct measurements (n=202J and lengths calculated from the equation in part (H) In=104). For these data: Mean = 511 mm. SD = 93 mm. range = 195-724 mm. (B) The relationship between cloacal depth and total length (n=831. r 2=O.835, P=O.OOOl. 316 Fishery Bulletin 95/2), 1997
60
50 A
40 E '"0 0 30
20
10
0 0 50 100 150 200 250 300 350 400 Weight (g)
300
00 250 B Y =15.893 - 3.686x + 0.446.Y' § 200 1: Cl "iii 150 ~ 0
100
50
0 5 10 12.5 15 17.5 20 22.5 25 27.5 30
Cloacal depth (mm)
Figure 3 Body weight (g) in the sample population ofAtlantic hagfish. (A) A fre quency histogram for body weight (n=306). This graph includes direct measurements (n=80I, weights calculated from the equation in Figure 1 (n=22), and weights calculated from the equation in part (Bl (n=041. (B) The relationship between cloacal depth and body weight (n=53l. r2 =0.864, P=O.OOOI
TL) was comparable to that found at the Nipper agreement between the data sets (Fig. 2A vs. Fig. 5) (range: 195-724 mm TL; average: 509 mm TL). Al suggests that the sampling reported here is repre though the small size ofthe Stellwagen sample con sentative ofhagfish populations throughout the Gulf strains the power ofstatistical comparison, the only ofMaine. statistically significant differences found between these groups were that the maximum depth and width (in percent of body length) of animals from Discussion Stellwagen Bank were greater than those from the original study site. This may reflect differences in The gonads in hagfishes develop within a mesenterial the substrate and food availability between the two fold located to the right ofthe dorsal mesentery that locations, or itmay be an artifact ofthe small sample supports the gut. The anterior 2/3 ofthe gonad may size. develop into ovarian tissue, and the posterior 1/3 may We next compared our length distribution data develop into testicular tissue. Details of sexual dif with catch statistics collected between 19 May and ferentiation are known for only a few species, nota 28 July 1994 by the New England Fisheries Devel bly the Pacific hagfish, Eptatretus stouti. Gorbman opment Association (Kuenstner, 1996I. The close (1990) reported that E. stouti are protogynolls her- Martini et al.: Population profile of Gulf of Maine Myxine glutinosa 317 maphrodites: sexually immature animals are found at some stage of female differ- 8 entiation, and mature animals are usually 0 000 0 6 differentiated as either males or females. o OCJlll)O 0 0 Mature females are longer than 200 mm 4 0 00(1)00 TL and males are longer than 280 mm TL. 000 000 0 The largest animals are usually females. 2
1975. Ovulation and eggs of the hagfish. Eptatretus IMyxinidae, Eptatretus) from the Pacific Ocean. Proc. burgeri. Acta ZooI. (Stockh.J 56:199-204. Calif. Acad. Sci. 43:249-267. Fernholm, B., and C. L. Hubbs. Nansen,F. 1981. Western Atlantic hagfishes of the genus Eptatretus 1887. A protandric hermaphrodite (Myxine glutinosa. L..l IMyxinidae) with description of two new species. Fish. amongst the Vertebrates. Bergen Mus. Aarsber. 7:1-34. Bull. 79:69--83. Neira, F. J. C. Foss, G. 1982. Behavioral aspects ofPolistotrema decatrema. Bre 1963. Myxine in its natural habitat. In A. Broda) and R. nesia 19-20, 181-182. Fange leds.), The biology ofMyxine, p. 42-46. Universi Nelson, J. S. tetsforlaget, Oslo. 1994. Fishes of the world, 3rd ed. John Wiley and Sons, Gorbman,A. New York. NY. 688 p. 1990. Sex differentiation in the hagfish, Eptatretus stouti. Patzner, R. A. Gen. Compar. EndocrinoI. 77:309-323. 1977. Cyclical changes in the testis ofthe hagfish Eptatretus Gorbman, A., H. Kobayashi, Y. Honma, and M. Matsuyama. burgeri ICyclostomata). Acta ZooI. IStockh.) 58:223-226. 1990. The Hagfishery ofJapan. Fisheries 15:12-18. Patzner, R. A., and H. Adam. Gustafson, G. (1981). Changes in the weight of the liver and the rela 1935. On the biology of Myxine glutinosa L. Ark. ZooI. tionship to reproduction in the hagfish Myxine glutinosa 28:1-8. (Cyclostomata). J. Mar. BioI. Assoc. U. K. 61:461-464. Hall·Arber, M. Putnam, F. W. 1996. Workshop probes hagfish processing potential in US: 1874. Notes on the genus M.vxine. Proc. Boston Soc. Nat. fishery discards worry fishennen. Commercial Fisheries Hist. 16:127-135. News:18B-19B. Stonington, ME. Schreiner, A., and K. A. Schreiner. Holmgren, N. 1904. tIber die Entwicklung der mannlichen Geschlechts 1946. On two embryos of Myxine glutinosa. Acta ZooI. zellen von Myxine glutinosa IL.l Vermehrungsperiode. XXVII IStockh.J:I-90. Reifungsperiode, und Reifungsteilungen. Arch. BioI. Jespersen, A. 21:183-355. 1975. Fine structure of spermiogenesis in eastern Pacific Schreiner, K. E. species of hagfish (Myxinidae). Acta ZooI. IStockh.) 1955. Studies on the gonad ofM.vxine glutinosa L. Univ. 56:189-198. Bergen. Bergen. Johnson, E. W. Shelton, R. G. J. 1994. Aspects of the biology of Pacific IEptatretus stouti) 1978. On the feeding of the hagfish Myxine glutinosa in and Black IEptatretus deani) hagfishes from Monterey Bay. the North Sea. J. Mar. BioI. Assoc. U. K. 58:81-86. California. M.S. thesis, School ofNatural Sciences, Cali fornia State Univ., Fresno. CA. 130 p. Strahan, R. Kuenstner, S. E. 1963. The behavior ofMyxinoids. Acta Zoologica 44:1-30. 1996. Harvesting the value-added potential of Atlantic Tsuneki, K., M. Ouji, and H. Saito. hagfish. New England Fisheries Development Assoc., 1983. Seasonal migratiof'. and gonadal changes in the hag Boston, MA, 46 p. fish. Eptatretus burgeri. Jpn. J. Ichthyol. 29:429-440. Lesser, M., F. H. Martini, and J. B. Heiser. Walvig, F. In press. Ecology of hagfish, Myxine glutinosa, L., in the 1963. Gonads and the fonnation ofsexual cells. In A. Brodal Gulfof Maine. I: Metabolic rates and energetics. J. Exp. and R. Fange leds.l, The biology of M.vxine, p. 530 Mar. BioI. EcoI. 580. Universitatsforlaget, Oslo. Martini, F., and J. B. Heiser. Wisner, R. L., and C. B. McMillan. 1991. A population profile for a community of hagfish, 1995. Review of the new world hagfishes of the genus Myxine glutinosa. Am. Zool. 31:35A. Myxine IAgnatha, MyxinidaeJ with descriptions ofnine new 1989. Field observations on the Atlantic hagfish. Myxine species. Fish. Bull. 93:530-550. glutinosa, in the Gulfof Maine. Am. ZooI. 29:38A. Worthington, J. McMillan, C. B., and R. L. Wisner. 1905. Contribution to our knowledge of the Myxinoids. 1984. Three new species of seven-gilled hagfishes Am. Nat. 39:625-663.