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Egg deposition and development of eggs and larvae of Bigmouth Sculpin (Hemitripterus bolini).

ABSTRACT--The Bigmouth Sculpin, Hemitripterus bolini, is a cottoid fish in the family Hemitripteridae found throughout the Bering Sea and Gulf of Alaska to British Columbia, Canada, and northern California. Hemitripterids have internal gametic association with external fertilization as their mode of reproduction. With this strategy, spermatozoa are stored in the micropyle of eggs within the ovary after gamete transfer to the female and eggs are not fertilized until immersed in seawater. Female H. bolini deposit their eggs into at least 4 species of sponges. We collected eggs from Barrel Sponge (Halichondria lambei), Clay-Pipe Sponge (Aphrocallistes vastus), Boot Sponge (Acanthascus dawsoni), and Tree Sponge (Mycale loveni) in the Gulf of Alaska and Bering Sea. In contrast to its congeners, there has been little research on H. bolini particularly any focusing on aspects of early life history stages. In this study, we describe the development of H. bolini eggs and larvae from newly-hatched stages to juveniles, and include general observations of osteology. The descriptions of larvae and juveniles are based on examination of 32 specimens, 5 of which were differentially cleared and stained to examine osteological development. Larvae hatch at a large size (13 to 14 mm SL) in an advanced stage of development. Postflexion occurs at approximately 20 mm SL, and transformation to the juvenile stage begins at about 31 mm SL. Larvae are heavily pigmented through late flexion, when pigmentation becomes reduced. Postflexion larvae and juveniles are also heavily pigmented. Ossification of most skeletal elements does not occur until postflexion. The description will help distinguish H. bolini from other hemitripterids and sympatric larvae of the family Agonidae that are similar in appearance but generally smaller and more slender-bodied at all developmental stages. The behavior of egg deposition in sponges, in conjunction with the use of sponges by other fishes such as juvenile rockfish and invertebrates such as Golden King Crabs (Lithodes aequispina) as refuge habitat, suggests that sponge grounds may provide essential fish habitat for H. bolini and other species.

Key words: Alaska, Bigmouth Sculpin, development, eggs, egg deposition, essential fish habitat, Hemitripterus bolini, larvae, sponges

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The Bigmouth Sculpin, Hemitripterus bolini (Meyers 1934), is a cottoid fish in the order Scorpaeniformes, family Hemitripteridae. This family is composed of 3 extant genera and 8 species (Nelson 2006), and is characterized by the unique condition of minute spines covering the body (Yabe 1985). Adult Hemitripterus bolini are distinguished by having a large flattened head with a big mouth and protruding lower jaw (Fig. 1). The species is also notable for its elevated orbits, many blunt knob-like spines, and dorsal spines greatly exserted from the fin membrane (Hart 1973; Mecklenburg and others 2002). Hemitripterus bolini is found in the Bering Sea, Aleutian Islands, and Gulf of Alaska (Mecklenburg and others 2002), coastal waters of northern British Columbia, Canada (Hart 1973), and in northern California (based on a single record; Lea and Quirollo 1986) at depths of 25 to 925 m, but is most commonly encountered at 100 to 300 m (Mecklenburg and others 2002). There are no records of this species off the coasts of Oregon and Washington. This species reaches a maximum standard length of 86 cm (JW Orr, National Marine Fisheries Service (NMFS), Alaska Fisheries Science Center (AFSC), Seattle, WA, pers. comm.), and is reported to be a voracious predator of several fish species (R Lauth, NMFS, AFSC, Seattle, WA, pers. comm.).

Some species in the families Agonidae, Cottidae, and Hemitripteridae reproduce by internal gametic association with external fertilization. This mode of reproduction was first described in the cottid Alcichthys alcicornis (Elkhorn Sculpin), and is characterized by the association of eggs and spermatozoa in the ovary (Munehara and others 1989). While gametes remain in the ovary, entry of spermatozoa into the egg is chemically blocked in the micropylar canal, preventing fertilization (Munehara and others 1997). Entry of spermatozoa into the egg and subsequent fertilization occurs after the eggs are deposited in seawater, where concentrations of [Ca.sup.+] ions are greater than in the ovarian fluid. This gradient of [Ca.sup.+] ion concentration promotes membrane fusion of the male and female pronuclei (Munehara and others 1989). Munehara and others (1991) also observed this reproductive strategy in the hemitripterid Blepsias cirrhosus (Silverspotted Sculpin) and determined that no development occurred while eggs of a post-copulatory female B. cirrhosus were kept in ovarian fluid, but fertilization and development occurred once the eggs were immersed in seawater. Females of B. cirrhosus have also been shown to deposit their eggs near the oscular cavity of the sponge Mycale adhaerens, which is thought to provide protection from predation (Munehara and others 1991). Using histological methods, Munehara (1997) determined that the agonid Podothecus sachi also exhibits this mode of reproduction.

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Internal gametic association has also been reported in Hemitripterus villosus (Shaggy Sea Raven). Females secrete a jelly-like fluid at the tip of an extendable genital duct. Males then release sperm that adheres to the jelly-like material and is retracted into the ovary with the genital duct (Munehara 1996). Eggs do not begin development in ovarian fluid but do so when immersed in seawater (Munehara 1996). In addition, H. villosus deposits its eggs among tubes in polychaete colonies and multiple individuals may deposit eggs within a single polychaete colony (Munehara 1992).

Hemitripterus bolini deposits eggs in at least 4 species of sponges, which provide protection from predators and also aerate eggs with water circulating throughout the cavity. This use of sponges for egg deposition behavior, as well as their use as refuge habitat by other fishes and invertebrates, including juvenile rockfish (Sebastes spp.; Freese and Wing 2003) and juvenile Golden King Crabs (Lithodes aequispina), has created interest in conserving sponge grounds as essential fish habitat (EFH; Hogg and others 2010; Stone and others 2011).

Much is known about the development of the early life stages of the 2 other Hemitripterus species: H. villosus and H. americanus (Sea Raven). Kyushin (1968) described the embryonic and early larval development of H. villosus, and Okiyama and Sando (1976) provided a more detailed description of larvae and juveniles. Markevich (2000) reported observations from SCUBA dives of spawning and egg deposition habits of H. villosus in Peter the Great Bay, Russia. He also described spawning locations, egg deposition substrate, and fecundity, and reported that spawning occurred synchronously. Warfel and Merriman (1944) found adhesive egg clusters of H. americanus attached to the sponge Chalina sp. in southern New England and described eggs and early larvae, and Fuiman (1976) described early larvae of H. americanus.

In contrast to its congeners, little research has been conducted on H. bolini and its larval development has not been described. Our objectives in this study were to report occurrences of eggs of H. bolini in sponges, describe the development of eggs and larvae from newly-hatched stages to juveniles, and include general observations of osteology. The results of this study will assist in the identification of larvae and juveniles of H. bolini in the field and laboratory, and will allow a greater understanding of the biology of this species, particularly its interactions with sponges and the benthic community.

METHODS

Field Collections

Twenty-four egg masses of H. bolini, including 2 containing newly-hatched larvae, were found in sponges collected during bottom trawl surveys conducted from 1980 to 2008 by the Resource Assessment and Conservation Engineering (RACE) Division of the AFSC; 21 of those were retained for further study (Table 1). Sponges and egg masses were preserved in 10% seawater-buffered formalin at sea. One sponge containing an egg mass was frozen and partially thawed before being preserved. Of the 21 sponges collected that held egg masses, 13 sponges appeared unfragmented, completely surrounding egg masses, which we assumed were entire clutches. All eggs in these masses were counted and staged (Tables 2 and 3). A minimum of 50 eggs from each mass was then randomly selected and measured to the nearest 0.01 mm (Table 2). Although the chorion of eggs was clear enough to see many of the structures of the embryo, it was removed to facilitate examination. Eggs with visible embryos were all late stage. This stage was expanded into 3 substages for descriptions of development: early-late, middle-late, and late-late stage. In early-late-stage eggs, the tail is clearly separated from the yolk and the embryo length is 1/2 to 3/4 the diameter of the egg. In middle-late-stage eggs, the embryo is curled 3/4 around the top of the yolk and begins developing eye and body pigment. In late-late-stage eggs, the embryo is curled 7/8 around the top of the yolk, the eyes are fully pigmented, and more pigment is present on the body (Table 3). In addition, eggs from the ovaries of 3 ripe adult female H. bolini (65 to 67 cm TL) were counted for comparison with egg counts found in sponges.

Thirty-three larval and juvenile H. bolini (13.0 to 63.5 mm SL) were also examined. These specimens were collected using 60-cm bongo nets, 1-[m.sup.2] Multiple Opening and Closing Nets with Environmental Sensing Systems (MOCNESS), 3-[m.sup.2] Methot nets, and survey or commercial bottom trawls. They were initially preserved in 5% buffered formalin solution and later transferred to 70% ethanol.

Distribution and catch per unit effort (CPUE) of adult and juvenile H. bolini in Alaska waters were determined from bottom trawl surveys conducted by the AFSC, RACE Division, in the Aleutian Islands (2006), eastern Bering Sea slope (2008) and shelf (2009), and Gulf of Alaska (2009). CPUE is calculated as the species catch weight (kg) divided by the area trawled in hectares (distance trawled x measured net width). General distribution of adult H. bolini in the region was determined from catch records for RACE Division bottom trawl surveys conducted from 1980 to 2008.

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Laboratory Analysis

Morphological measurements of 32 larvae and juveniles were made using an image analysis system consisting of a computer and video camera attached to a dissecting stereomicroscope. Measurements were taken on the left side of the specimen whenever possible. Standard length (SL) is used throughout unless otherwise noted. Body depth, pre-dorsal length, snout to anus length, head length (HL), eye diameter, and pectoral-fin length (Moser 1996; Busby 1998) were measured and reported as percent SL or HL.

Five specimens of H. bolini were differentially cleared and stained using Alcian Blue and Alizarin Red-S to describe osteological development (Potthoff 1984). The flexion stage, defined by Kendall and others (1984), was expanded to include 3 sub-stages: early, mid-, and late flexion (De Forest and Busby 2006). Early flexion includes the interval from hatching until the formation of the 4th hypural and epurals, at which point the specimen is considered midflexion. Late flexion begins when the 5th hypural forms and ends when the notochord and posterior hypural margins are vertically oriented.

RESULTS

Egg Deposition--Use of Sponges

Based on our collections, adult female H. bolini in the Gulf of Alaska, Aleutian Islands, and Bering Sea deposit their eggs at depths of 108 to 522 m into 4 species of sponges: Barrel Sponge (Halichondria lambei: Fig. 2a), Clay-Pipe Sponge (Aphrocallistes vastus: Fig. 2b), Sharp Lipped Boot or Chimney Sponge (referred to as Boot Sponge throughout; Acanthascus dawsoni: Fig. 2c), and Tree Sponge (Mycale loveni: Fig. 2d; Table 1 and Fig. 3). Egg counts in each sponge ranged from 68 to 3019 (Table 2). Highest egg counts were found in Tree and Boot Sponges. Eggs were usually found in 1 adhesive mass in the Barrel, Clay-Pipe, and Boot Sponges, while Tree Sponges contained both single eggs and egg masses. Sponges were not saved for identification in 3 samples: 1 sample consisted of eggs only, a 2nd was only larvae, and the 3rd consisted of both eggs and larvae (Table 1, Fig. 3). Ovarian egg counts of 3 ripe females (65 to 67 cm TL) ranged from 2465 to 7152.

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Egg Morphology and Development

Mean diameter of H. bolini eggs 4.73 [+ or -] 0.33 mm, with a wide range (3.81 to 5.40 mm; Table 2). Eggs demersal, usually deposited in adhesive mass, adhering to each other but not to the inner surface of sponges. Egg mostly spherical, surfaces contacting other eggs often somewhat flattened. Egg masses remain intact after preservation, easily broken apart. Chorion thick, smooth, translucent.

Earliest stage of eggs with asymmetrical blastodisc (Table 3), though the asymmetry may be an artifact of preservation. Oil present as mass of >50 small oil droplets 0.08 to 0.12 mm diameter. Oil mass appearing frothy and opaque, resembling cellular material rather than the typical clear yellow or orange color of oil in pelagic eggs.

Embryo is formed in the next developmental stage collected, length about 1/2 to 3/4 egg diameter. Tip of tail straight, lifted from yolk surface. Lens of eye visible. With development, tail lengthening, curving away from longitudinal axis of embryo. Gut terminating about 75% SL, myomeres 39.

With further development, head broadening, becoming wider than rest of body. Eye pigment visible; gut terminating about 60% SL. Dorsal finfold present, extending anteriorly to nape. With continued growth, eye pigment increasing. Melanophores uniformly scattered on nape and laterally on body. Pigment heavier on either side of dorsal midline, extending from midbody to about 70% SL; no pigment on body posterior to end of dorsal midline pigment. Posterior 25% of gut lifted away from yolk; this area the most heavily pigmented part of body. Pigment visible on yolk next to body posterior to pectoral-fin buds, extending to area of gut still attached to yolk. As tail lengthens, position of embryo moving to top half of yolk. Tail curving anteriorly toward head, tip about 3/4 around yolk. Dorsal finfold extending anterior to hindbrain.

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When eyes become fully pigmented, tip of tail extending 3/4 to 7/8 around yolk. Oil mass within yolk below head, typically on right side of embryo. Dorsal finfold extending anteriorly to midbrain; anal finfold extending from anus to caudal area. Light pigment present on snout, midbrain, opercular area, and hindbrain. Internal pigment present on posterior margin of hindbrain, forming posteriorly pointing v-shape (Fig. 4a). Entire body pigmented to 80% SL; heavier concentration of melanophores present on either side of dorsal midline, extending from anus to 70% SL. Posterior 25% of gut more heavily pigmented than rest of body. Yolk pigment near gut persisting, covering gut as embryo develops.

Close to hatch, most of body heavily pigmented. Melanophores on mediolateral body fine and closely spaced, those near dorsal and ventral margins larger (Fig. 4b). Nares, gular region, ventral surface of gut, caudal region, and most of finfolds unpigmented (Fig. 4c). Pigment present on anal finfold close to ventral margin of body at about 75% SL. Eyes large, diameter equal to about 1/3 egg diameter. Maxillary and dentary teeth present toward posterior edges of jaws. Embryo curling 1 1/2 times around inside of egg. Gut large, no yolk visible. Embryo in late preflexion stage with nine caudal rays formed in ventral caudal finfold.

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Most eggs were collected during June and July when AFSC groundfish surveys are conducted (Table 1). The progression of developmental stages of eggs during years when multiple egg masses were collected (1996, 1997, and 2004) indicates that egg deposition occurs in spring (that is, eggs at the earliest stages were collected June to mid-July). The collection of an egg mass in February that contained near-hatching eggs and newly-hatched larvae suggests an incubation duration of at least 10 mo.

Larval Morphology and Development

Larval H. bolini hatching at approximately 13 to 14 mm in early flexion stage. Yolk sac present with yolk nearly exhausted (Fig. 5a). Mid-flexion stage beginning at approximately 15 mm (Fig. 5b); late flexion, at 16.5 mm (not illustrated). Cirri around head developing mid-to late flexion. Postflexion beginning at approximately 19 mm (Fig. 5c); transformation to the juvenile stage beginning at around 31 mm and complete by 40 mm (Fig. 5d). Anteriormost dorsal-fin spines raised and exserted from fin membrane during flexion through transformation stages; all exserted in transformation and early juvenile stages. Small dermal prickles (spinules) present on gut and most of lateral body formed by 20 mm with the exception of the caudal peduncle (Fig. 5c). Caudal peduncle covered with prickles by 40 mm (Fig. 5d).

Larvae deep-bodied throughout development. Relative body depth and head length increasing from flexion to postflexion stage, decreasing in juveniles (Table 4). Larger benthic juvenile specimens with wider, more dorsally-compressed head than postflexion larvae and pelagic juveniles. Eye diameter decreasing from preflexion to juvenile stage. Relative predorsal and snout-to-anus lengths increasing from flexion to postflexion stage, decreasing in juveniles. Pectoral-fin length increases from preflexion to juvenile stage. Juveniles examined 31.1 to 63.5 mm; similar in appearance to adults, but with notably fewer cirri on and around head (Fig. 5e).

Larval Pigmentation

Early flexion larvae heavily pigmented with small, closely-spaced melanophores covering head and body to about 80% SL (Fig. 5a). Cluster of melanophores present on operculum with more on hyoid region. Snout, anterior ventral surfaces from lower jaw to anus, pectoral-fin base, finfolds, and caudal peduncle unpigmented.

In midflexion larvae, snout and mandible pigment present. Opercular pigment heavier than in early flexion larvae; area between orbits unpigmented. First dorsal fin heavily pigmented anteriorly with large, oval-shaped patch present near middle of fin extending slightly onto dorsal body margin; pigmentation on dorsal fin increasing as development progresses. Second dorsal fin initially unpigmented, pigment present at base in more developed larvae; anal-fin base lightly pigmented with a small patch and scattered individual melanophores near base. Melanophores present on pectoral-fin base (Fig. 5b).

Opercular region in postflexion larvae less pigmented than in flexion larvae; melanophores smaller, widely spaced. Mandible darkly pigmented; mouth pigmented internally, with several large melanophores. Snout pigment present in some specimens. First dorsal fin heavily pigmented with bare patch at medial base of spines. Two or more patches of melanophores present on base of second dorsal fin. Distal margin of pectoral fin with large, irregularly-shaped patch of pigment covering approximately 1/3 of surface area (Fig. 5c). Within patch, 2 ovoid unpigmented areas of unequal size present: dorsal area small, ventral area large. Pigment on body of larger larvae more diffuse; separated into irregularly-shaped bands with more uniform pigmentation covering gut.

Snout and pelvic fins pigmented, body generally dark with widely-spaced patches during transformation and early juvenile stages. Lateral and ventral surfaces of gut mostly unpigmented, covered with tiny prickles (Fig. 5d). First dorsal fin heavily pigmented with darker patches on anterior, median, and posterior regions of membrane. Pigment on 2nd dorsal fin consisting of 3 somewhat faint, irregularly-shaped patches of decreasing size from anterior to posterior. Pectoral fins with wide band of pigment on distal margin; rows of melanophores radiating along the rays inward toward relatively unpigmented pectoral-fin base; fin membranes pigmented proximally with 2 faint vertical bands. Large patch of pigment present on caudal peduncle with band extending posteriorly to cover hypural area. Dark pigment patches present on dorsal and ventral margins of caudal fin at insertion of posteriormost procurrent rays, with dorsal patch being larger.

Pigmentation generally lighter on head and opercular region of larger juveniles (>60 to 70 mm), with large blotches absent and smaller melanophores present on the head. Pectoral fins fan-shaped, covered almost entirely with pigment. Four aggregations comprising alternating bands of pigmentation, 3 dorsal and 1 mediolateral, present along postanal body (Fig. 5e). Row of irregularly-spaced spots along lateral line. Bands on body more diffuse, less prominent than during transformation. Second dorsal fin covered almost entirely with pigment. Anal fin with band of pigment along distal margin. Caudal peduncle heavily pigmented. Caudal fin mostly unpigmented. Pigmentation of juveniles closely resembling adults.

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Osteology

Ossification beginning during postflexion stage; all bones in head and hyoid region ossified. Pectoral-fin rays beginning to develop by 13.6 mm; complete but unossified by 15.5 mm; ossified by about 20 mm. Unossified precursors of dorsal- and anal-fin elements apparent during midflexion; pterygiophores, fin rays, and spines ossified by postflexion. Five branchiostegal rays ossified by 19.7 mm; all 6 branchiostegal rays ossified in juveniles (Table 5). Teeth in embryos and early flexion larvae becoming prominent and increasing in size during midflexion but not ossified. Vertebrae beginning to differentiate in late flexion larvae by about 18 mm but not ossified until postflexion at about 19.5 mm. Counts of vertebral centra consistent with adult counts by postflexion stage (Table 5). By 37 mm, early juveniles with adult complement of ossified meristic features.

Distribution of Larvae

Larvae and pelagic juveniles of H. bolini are very uncommon; only 21 individuals were collected during AFSC ichthyoplankton surveys since 1978 and, until 8 May 2010, none had been caught since 25 May 1999 (Fig. 6, Table 6). All collections have been of single individuals, mostly near Kodiak Island in the Shelikof sea valley. Two individuals were collected in the Bering Sea between the Aleutian and Pribilof Islands and most recently from Unimak Pass in the Aleutian Islands. We recently became aware of 3 larvae and pelagic juveniles from Southeast Alaska: 1 larva, 18.0 mm SL, from Taku Inlet, and 2 pelagic juveniles, lengths unknown, from Icy Strait. We have been unable to confirm the identifications of these specimens.

Distribution of Adults and Benthic Juveniles

Adult H. bolini are distributed throughout the eastern Bering Sea, Aleutian Islands, and Gulf of Alaska (Fig. 7a). Bottom trawl surveys in these areas captured specimens at bottom depths of 43 to 638 m. Most, however, were caught on the outer continental shelf (100 to 200 m) and upper slope regions (>200 m). Adults and benthic juveniles were never captured in large numbers compared to other species, averaging 2.54 kg and 0.58 fish/ha from tows in which they were captured (Fig. 7b). The spatial and depth distribution of adult H. bolini closely follow that of sponges containing egg masses, both frequently occurring near the outer continental shelf (Fig. 3).

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DISCUSSION

We found eggs of H. bolini in 4 species of sponges that share characteristics such as having large oscula (openings) or being cone-shaped, and we hypothesize that these features make them particularly suitable for egg deposition. Barrel Sponges are barrel-shaped, as the common name suggests, and have a large opening and soft consistency (Fig. 2a). Very little is known about this species, but it apparently attaches to cobbles (Stone and others 2011). Clay-Pipe Sponges are hollow, thin-walled, hard, and brittle with a cone-shaped oscula (Fig. 2b). They are large sponges, up to 2 m high and 3 m wide, and are common throughout Alaska on cobble and pebble bottoms at depths to 756 m (Stone and others 2011). The usual coloration of the Clay-Pipe Sponge in life varies from white to light yellow and orange (Fig. 8) (Stone and others 2011), and the gray coloration of the individual shown in Figure 2b suggests that it was dead (a skeleton). It is possible that the sponge was suffocated by being overly filled with eggs (H. Reiswig, Biology Department, University of Victoria, BC, Canada, pers. comm.). Boot Sponges (Fig. 2c) are soft, curved, and tube- or barrel-shaped, with a height to 1 m and diameter to 30 cm. They are found attached to bedrock, cobbles, and pebbles on flat, inclined, or vertical surfaces at depths of 10 to 437 m (Stone and others 2011). Tree Sponges have a soft and fibrous, vase- or cone-shaped body supported with branching polyspicular tracts and a rigid stalked base (Fig. 2d). Cones may reach 1 m or more in height and width and are attached to bedrock, boulders, and cobbles at depths of 143 to 289 m (Stone and others 2011).

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The large variation in egg mass size within the sponges (68 to 3019 eggs) may be a result of the size of the oscula of the individual sponge, as most of the egg-bearing sponges collected were completely full. Because the ripe ovaries of 3 adult female H. bolini examined contained considerably more hydrated eggs (2400 to 7100) than the egg-bearing sponges, it appears that females may deposit eggs in a sponge cavity until it is full, then move on to another sponge, repeating the process until the ovaries are spent (Fig. 8). While it is unclear whether maturation occurs synchronously or in batches (T. Tenbrink, NMFS, AFSC, Seattle, WA, pers. comm.), it is apparent that egg deposition occurs in batches. Examination of the limited amount of egg development information we collected suggests a relatively long incubation period. Early developmental stages with visible cell cleavage were not found, but blastodisc and late-stage eggs were collected in June (Table 3). This suggests that the eggs had likely been fertilized for some time, perhaps a month or even more. Eggs with middle-late stage embryos were found in late July and early August and another mass that was beginning to hatch was collected in late February. Deposition likely occurs over a protracted period in early spring (March and April), with hatching occurring the following February for an incubation period of at least 10 and perhaps 11 mo. However, this incubation period may be an overestimate, as there were no opportunities to collect eggs in the fall months, and it is unclear when the hatching period might begin or end.

This description of H. bolini can be used to distinguish larvae from sympatric species of the closely related family Agonidae, which may be the sister group of the Hemitripteridae (Yabe 1985). Although generally more slender-bodied, many agonid larvae share the dark pigmentation, large eye, and prickly body of Hemitripterus species (Busby 1998). Larvae of Hypsagonus mozinoi (Kelp Poacher) and H. quadricornis (Fourhorn Poacher) closely resemble H. bolini but have slightly more slender bodies (Figs. 9a and 9b). Larvae of these agonids also lack caudal-fin pigment, similar to H. bolini. However, H. bolini is considerably larger during the flexion stage (Mean length =15.2 [+ or -] 1.5 mm) than both H. mozinoi (6.2 [+ or -] 1.8 mm) and H. quadricornis (7.2 [+ or -] 0.9 mm). Co-occurring agonids of the genus Bathyagonus are notably more slender and smaller than H. bolini during all stages of development. In addition, larvae of Bathyagonus species differ in that the dorsal and anal finfolds are densely pigmented (Busby 1998).

Within the Hemitripteridae, Nautichthys oculofasciatus (Sailfin Sculpin) differs from H. bolini in having enlarged pectoral fins and being smaller at similar developmental stages (Fig. 9c). Blepsias bilobus (Crested Sculpin) and B. cirrhosus (Silver-spotted Sculpin) are smaller than H. bolini at similar stages of development and have fewer pectoral-fin rays (15 to 17 and 11 to 14 versus 20 to 23, respectively). Blepsias cirrhosus also has chin pigment that is absent in H. bolini (Fig. 9d). In addition, species of Blepsias have a more developed 2nd dorsal fin and anal fin during postflexion, whereas H. bolini have a more developed 1st dorsal fin (Matarese and others 1989).

Differences in morphology and pigmentation among H. bolini, H. americanus, and H. villosus larvae are not sufficient to allow identification of each species without clearing and staining to reveal meristic elements. However, H. bolini is generally larger than H. americanus and smaller than H. villosus at similar developmental stages. In addition, H. bolini has a nearly exhausted yolk sac at hatching, whereas H. americanus and H. villosus have a relatively large yolk sac (Kyushin 1968; Fuiman 1976). In addition, the geographic ranges of the 3 species of Hemitripterus do not overlap, each species occurring in different oceanic regions (H. americanus, western Atlantic; H. villosus, western North Pacific, Japan, and western Bering Sea; H. bolini, eastern North Pacific and eastern Bering Sea). Records of H. villosus from the Gulf of Alaska and western Aleutian Islands are now thought to be H. bolini (see Mecklenburg and others 2002).

Our observation that ossification does not occur until postflexion, when the larvae are well developed, suggests that the description of osteological development presented here is suspect. Preservation in formalin of improper pH may have decalcified bones. Obtaining additional larvae and early juveniles would permit more clearing and staining, thus allowing further osteological examination.

An important management implication resulting from this study is that conservation of sponge grounds may become crucial for the preservation of H. bolini populations due to the apparent reliance of this species on sponges for egg deposition and subsequent early larval development. Our finding that 4 different sponge species are used as such by H. bolini, and that eggs have not been found anywhere else than in sponges, further establishes the importance of sponge grounds as essential fish habitat and provides additional justification to support conservation measures.

ACKNOWLEDGMENTS

The authors would like to thank A Matarese (AFSC) for encouragement, advice, and help in the laboratory. Illustrations were prepared by B Vinter (AFSC retired, larvae and juveniles) and A Maust (AFSC, eggs). W Austin (BC, Canada), R Stone (AFSC, Juneau, AK), K Palenscar (California Academy of Sciences), and H Reiswig (Biology Department, University of Victoria and Natural History Section, Royal British Columbia Museum, Canada) assisted with sponge identifications. We also thank T Pietsch, R Arnold, K Maslenikov, and D Roje for advice, assistance, and use of the University of Washington Fish Collection. A Matarese, D Stevenson, R Stone, and T Tenbrink (AFSC) reviewed earlier drafts of this manuscript and provided helpful comments. R Cartwright (formerly AFSC) provided technical support and assistance in the laboratory. W Carlson and L De Forest (AFSC) assisted with graphics. The findings and conclusions in this paper are those of the authors and do not necessarily represent the views of the National Marine Fisheries Service. This research is contribution EcoFOCI-0764 to NOAA's Fisheries-Oceanography Coordinated Investigations.

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Submitted 18 April 2011, accepted 18 August 2011. Corresponding Editor: James W Orr.

MORGAN S BUSBY, DEBORAH M BLOOD, ADAM J FLEISCHER, AND DANIEL G NICHOL

Resource Assessment and Conservation Engineering Division, Alaska Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 7600 Sand Point Way NE, Seattle, WA 98115-6349
TABLE 1. Collection date, locality, and depth of 24 sponges
containing egg masses of Bigmouth Sculpin, Hentitripterus bolini.
Numbered masses were counted, measured, and staged; those without
numbers were incomplete because of damage during collection. All
are collections of single sponges with the exception of 3 Barrel
Sponges collected in one tow on 26 July 1997. UW = University of
Washington Fish Collection; AI = Aleutian Islands; BS = Bering
Sea; GOA = Gulf of Alaska.

Egg    Catalog                           Lat          Long      Depth
mass   Number      Date               [degrees]N   [degrees]W    (m)

1      UW 136167   26 July 1997         58.74        175.03      146
2      UW 136168   5 August 1997        53.00        172.33      176
3      UW 136169   27 July 1996         55.93        134.87      180
4      UW 136170   5 July 1996          56.02        168.25      152
5      UW 136171   28 July 1997         51.90        178.35      145
6      UW 136172   27 June 1997         52.09        172.43      166
7      UW 136173   27 February 1982     53.08        169.92      144
8      UW 136174   6 June 2004          53.13        168.93      140
9      UW 136175   16 July 2002         52.23        175.24      152
10     UW 136176   19 June 2004         52.23        173.43      108
11     UW 136177   23 July 2004         57.80        174.19      329
12     UW 136178   12 June 2005         56.12        157.76      166
13     UW 136179   1 July 2008          59.37        177.61      259
                   31 July 1997         52.05        177.40      132
                   4 June 2000          52.06        172.55      145
                   22 May 2001          53.11        166.97      288
                   26 May 2003          52.67        169.07      117
                   16 July 2003         59.16        149.59      182
                   14 June 2004         52.28        170.60      242
                   30 July 2004         54.94        167.64      522
                   14 June 2005         56.68        156.67      175
                   ?                    57.29        154.96       ?

Egg    Catalog
mass   Number      Date               Region   Species of sponge

1      UW 136167   26 July 1997       BS       Barrel Sponge (n = 3)
2      UW 136168   5 August 1997      Al       Clay-Pipe Sponge
3      UW 136169   27 July 1996       GOA      Clay-Pipe Sponge
4      UW 136170   5 July 1996        BS       Barrel Sponge
5      UW 136171   28 July 1997       Al       Tree Sponge
6      UW 136172   27 June 1997       Al       Unknown sponge with eggs
7      UW 136173   27 February 1982   Al       Unknown sponge with eggs
                                                 and larvae
8      UW 136174   6 June 2004        Al       Tree Sponge
9      UW 136175   16 July 2002       Al       Boot Sponge
10     UW 136176   19 June 2004       Al       Clay-Pipe Sponge
11     UW 136177   23 July 2004       BS       Boot Sponge
12     UW 136178   12 June 2005       GOA      Clay-Pipe Sponge
13     UW 136179   1 July 2008        BS       Clay-Pipe Sponge
                   31 July 1997       Al       Tree Sponge
                   4 June 2000        Al       Clay-Pipe Sponge
                   22 May 2001        GOA      Clay-Pipe Sponge
                   26 May 2003        Al       Tree Sponge
                   16 July 2003       GOA      Clay-Pipe Sponge
                   14 June 2004       Al       Tree Sponge
                   30 July 2004       BS       Clay-Pipe Sponge
                   14 June 2005       GOA      Clay-Pipe Sponge
                   ?                  GOA      Unknown sponge with
                                                 larvae

TABLE 2. Species of sponges and summary of egg data from egg masses
of Bigmouth Sculpin, Hemitriptems bolini, including number of eggs
per sponge, number with diameter measured, mean egg diameter
[+ or - ] standard deviation (SD), and range. Values on last line
are mean number of eggs per sponge [+ or -] standard deviation (SD),
total number of egg diameter measurements, mean egg diameter [+ or -]
standard deviation (SD) for all eggs measured, and range of all
diameter measurements.
                                    Number         Number
Egg mass   Species of sponge       of eggs        measured

1          Barrel Sponge             228             60
2          Clay-Pipe Sponge          436             50
3          Clay-Pipe Sponge           76             55
4          Barrel Sponge             512             54
5          Tree Sponge              1262             51
6          Unknown sponge             68             56
7          Unknown sponge             73             61
8(a)       Tree Sponge              1565             60
9          Boot Sponge              1161             60
10         Clay-Pipe Sponge          263             50
11         Boot Sponge              3019             50
12         Clay-Pipe Sponge          631             50
13         Clay-Pipe Sponge          194             50
                               730 [+ or -] 847     707

                 Mean egg         Range of egg
Egg mass   diameter [+ or -] SD     diameter

1           4.78 [+ or -] 0.05     4.48-4.88
2           4.29 [+ or -] 0.08     4.05-4.40
3           4.77 [+ or -] 0.06     4.67-4.89
4           4.68 [+ or -] 0.06     4.57-4.81
5           4.83 [+ or -] 0.06     4.71-4.94
6           4.54 [+ or -] 0.08     4.27-4.75
7           3.99 [+ or -] 0.08     3.81-4.17
8a          4.82 [+ or -] 0.23     4.57-5.31
9           4.93 [+ or -] 0.12     4.74-5.30
10          4.72 [+ or -] 0.14     4.40-4.98
11          5.21 [+ or -] 0.08     5.06-5.40
12          5.14 [+ or -] 0.09     4.90-5.31
13          5.02 [+ or -] 0.16     4.57-5.35
            4.73 [+ or -] 0.33     3.81-5.40

(a) Frozen

TABLE 3. Date of collection and stage of development of eggs of
Bigmouth Sculpin, Hemitripterus bolini, from  different masses.

Egg development                  Date of collection   Egg mass number

Blastodisc                       12 June, 2005              12
Embryo 1/2-1/4 diameter of egg   6 June, 2004                8
Embryo 1/2-3/4 diameter of egg   19 June, 2004              10
Embryo 1/2-3/4 diameter of egg   16 July, 2002               9
Embryo curled 3/4 way around     27 June, 1997               6
  top of yolk
Embryo curled 3/4 way around     1 July, 2008               13
  top of yolk
Embryo curled 3/4 way around     27 July, 1996               3
  top of yolk
Embryo developing eye pigment,   5 July, 1996                4
  light body pigment
Embryo eyes darker, light        26 July, 1997               1
  body pigment
Embryo curled 7/8 way around
  top of yolk, eyes fully
  pigmented, more body pigment   23 July, 2004              11
Embryo curled 7/8 way around
  top of yolk, eyes fully
  pigmented, more body pigment   28 July, 1997               5
Embryo curled 7/8 way around
  top of yolk, eyes fully
  pigmented, more body pigment   5 August, 1997              2
Eggs beginning to hatch          27 February, 1982           7

TABLE 4. Body proportions of larval and juvenile Bigmouth Sculpin,
Hemitripterus bolini. Proportions are expressed as percentage of
standard length (SL) or head length (HL): mean [+ or -] standard
deviation (SD), range in parentheses.

Category            Flexion          Postflexion          Juvenile

Sample size            25                 2                  5

Standard        15.2 [+ or -]      20.4 [+ or -]      42.4 [+ or -]
length (SL)     1.5 (13.0-17.9)    0.9 (19.8-21.0)    12.4 (31.1-63.5)

Body depth/SL   26.2 [+ or -]      37.7 [+ or -]      31.7 [+ or -]
                0.04 (20.3-32.9)   0.01 (36.8-38.6)   0.03 (28.6-35.7)

Predorsal       25.9 [+ or -]      32.9 [+ or -]      28.8 [+ or -]
length/SL       0.04 (20.1-33.3)   0 * (32.5-33.3)    0.03 (24.8-32.0)

Snout to anus   62.7 [+ or -]      71.8 [+ or -]      59.5 [+ or -]
length/SL       0.05 (56.4-70.5)   0 * (71.8-71.9)    0.06 (53.7-68.2)

Head length/    31.4 [+ or -]      43.2 [+ or -]      40.0 [+ or -]
SL              0.05 (24.1-41.0)   0 * (43.2-43.3)    0.04 (35.4-46.5)

Eye diameter/   47.7 [+ or -]      37.2 [+ or -]      30.1 [+ or -]
HL              0.06 (34.4-56.1)   0.04 (34.6-39.7)   0.03 (26.9-34.5)

Pectoral-fin    13.6 [+ or -]      28.4 [+ or -]      30.9 [+ or -]
length/SL       0.05 (6.9-21.3)    0 * (28.1-28.7)    0.03 (28.0-35.7)

* SD<0.01

TABLE 5. Meristics of cleared and stained larval and juvenile Bigmouth
Sculpin, Hemitripterus bolini. Counts are of ossified structures only.
Specimens above dashed line (--) are in flexion stage.

Standard                  Spines, Rays
length
(mm)        Dorsal-fin    Anal-fin    Pectoral-    Branchiostegal
             elements     elements     fin rays         rays

13.6
15.5
17.8
19.7           XIV,11        13           21             5
37.1         XIII, 12        14           21             6

Standard    Neural spines
length
(mm)                                        Haemal
            abdominal    caudal    total    Spines

13.6
15.5
17.8
19.7            16         21        37       20
37.1            18         22        40       21

Standard                Centra
length
(mm)                                       Caudal-fin
            abdominal   caudal    total       rays

13.6
15.5
17.8
19.7           16         21        37     7, 6+6, 5
37.1           18         22        40     7, 6+6, 6

Table 6. Collection date, locality, depth, and length of 21 larvae and
pelagic juveniles of Bigmouth Sculpin, Hemitripterus bolini,
collected in plankton tows. GOA = Gulf of Alaska; BS = Bering Sea.

Date                 Lat        Long      Region   Depth     Length
                  [degrees]   [degrees]             (m)       (mm)
                      N           W

30 March, 1978      58.30      151.04      GOA      110        7.1
31 March, 1978      59.05      151.93      GOA      184       13.1
6 March, 1979       57.69      150.35      GOA       97       12.2
1 April, 1981       57.70      155.25      GOA      220       14.0
18 March, 1985      57.19      155.45      GOA      222       14.1
6 April, 1987       57.65      155.08      GOA      250       16.0
24 April, 1988      57.78      155.04      GOA        1       18.2
1 May 88            57.69      155.17      GOA      139       23.0
12 April, 1989      57.90      154.88      GOA      142       15.0
14 April, 1989      56.88      155.76      GOA      290       13.6
30 April, 1989      57.03      156.36      GOA      208       17.0
21 April, 1991      56.86      156.14      GOA      178       15.0
5 April, 1993       57.96      154.48      GOA      246       16.0
10 April, 1993      57.12      155.33      GOA      244       16.0
24 April, 1993      54.88      168.33      BS        21       17.0
8 May 1993          56.16      156.53      GOA      101       19.0
13 May 1993         56.62      156.33      GOA      101       21.3
1 June, 1993        57.16      155.67      GOA      107       32.5
18 April, 1997      55.43      168.07      BS       212       16.0
25 May 1999         55.55      158.79      GOA      101       15.9
8 May 2010          54.42      165.15      BS       151       16.0
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Author:Busby, Morgan S.; Blood, Deborah M.; Fleischer, Adam J.; Nichol, Daniel G.
Publication:Northwestern Naturalist: A Journal of Vertebrate Biology
Article Type:Report
Geographic Code:1USA
Date:Mar 22, 2012
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