Biology of Macrourid Fishes. Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California 92037
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1 AM. ZOOLOGIST, 11: (1971). Biology of Macrourid Fishes CHARLES F. PHLEGER Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California SYNOPSIS. Macrourid fishes are one of the most diverse and numerous groups of deep bottom fishes in the world. The great majority are benthopelagic, with a few bathypelagic members. Benthopelagic species are usually endemic, and most common on continental slopes, whereas bathypelagic species are more cosmopolitan in distribution. The center of distribution for Macrourids is in the Indo-Pacific region. Little is known of their life history; eggs are thought to ascend after fertilization and develop in the midwatcr below 200 m. Although few gut content analyses of adults have been performed, fin structure and photographs indicate that they feed mostly on bottom invertebrates. The purpose of this paper is to give a brief discussion of general biology of Macrourid fishes. This will include systematics, distribution, and life history. Although pertinent papers have been cited when necessary, this is not meant to be a comprehensive review. I have placed much reliance upon the work of Marshall (especially 1965). This paper is primarily directed towards supplying general information about the major experimental animal used on the 1970 expedition of the R/V Alpha Helix to the Galapagos Islands. This animal, Coryphaenoid.es sp., was collected from 2000 m depth using free vehicle methods (Phleger and Soutar, 1971). It has not been identified to species at this time. No discussion of Galapagos Macrourids is included here, as our collection methods only yielded one species of Coryphaenoides. The reader is referred to Garman (1899) for a discussion of different Macrourid species collected near the Galapagos Islands., SYSTEMATIC^ Macrourid fishes belong to the order Gadiformes and the suborder Macrouroidei (Greenwood et al., 1966). According to Marshall (1965), the family Macrouridae is divided into four subfam- 1 thank T. MaLsui, R. Rosenblatt, and M. Barnett for critically reading the manuscript and for advice. 419 ilics: the Macrourinae, Bathygadinae, Macrouroidinae, and Trachyrhynchinae. Okamura (1970) has provided a more recent classification. Structural features that characterize the family include a long abdomen and tail tapering to a point, a large head with large eyes, two dorsal fins (the first short and the second long and manyrayed), and a long anal fin which meets the second dorsal at the tip of the tail, almost excluding the caudal fin (Barnett, 1968) (Fig. 1). Pelvic fins are located at a thoracic position, and the short-based pectoral fins are located close to the midline of the body. Jaws, located beneath the snout, usually have a mental barbel. The Macrourinae is the largest subfamily of Macrourid fishes and includes 17 genera (including Coryphaenoides) and over 250 species (Marshall, 1965). Most are benthopelagic and probably feed on bottom organisms. Anal fin rays in this group are longer than second dorsal fin rays. The protrusible mouth with large teeth is subterminal to a well developed snout. A fold of skin restricts the first gill slit, and the gill rakers are small and tubercular. In most males, the well developed swimbladder has attached drumming muscles. A number of species have ventral light organs. The Bathygadinae comprise the second largest subfamily (two genera, many species). They are benthopelagic and proba-
2 420 CHARLES F. PHLEGER N, ' W), from the R/V Thomas Washington, 7 August It was provided by John D. Isaacs, Marine Life Research Group, Scripps Institution of Oceanography. bly feed mostly on zooplankton. The anal fin rays in this group are shorter than the second dorsal fin rays. The large terminal mouth has a slightly protrusible jaw with many rows of small teeth. The first gill slit is unrestricted and the gill rakers are long and numerous. The swimbladder is well developed. The Trachyrhynchinae is also a benthopelagic subfamily with only one genus, probably feeding on zooplankton above the bottom. The dorsal rays are longer than the anal rays; the small jaws are inferior to the pronounced snout, and the first gill arch has many small gill rakers. The Macrouroidinae include two genera and are probably bathypelagic (Marshall, 1964; Marshall and Taning, 1966). The greatly enlarged or inflated head is due primarily to a highly developed cephalic lateral line system. The eyes, trunk, and tail are small and the swimbladder is re- gressed. The abarbate, highly protrusible jaws are located much inferior to the snout. DISTRIBUTION Macrourid fishes are probably the most numerous group of deep-sea benthic fishes with respect to number of species and number of individuals. Their center of distribution is in the Indo-Pacific region, where over half the known species are found. The great majority of species are benthopelagic, which means they live a short distance above the bottom, usually within a few hundred meters. Despite this great abundance, Macrourids are not found in the Red Sea, the Arctic Ocean (Barnett, 1968), or the Sea of Japan (Hubbs, 1930). Shallow sill depths are probably an important factor in excluding these fishes (200 m sill depth for the Red FIG. 1. Coryphaenoides acrolepis, a Macrourid fish, swarming around a bait can at a depth of 2000 m. Hagfish, an echinoderm, and a decapod crustacean may also be seen in the picture. This photograph was taken off Baja California (30 53'
3 BIOLOGY OF MACROURID FISHES 421 Sea, and 180 m for the Sea of Japan). The non-cosmopolitan nature of the different groups of Macrourids has long been recognized. Examples of endemism are given by Gilbert and Hubbs (1920) for the Sulu Sea, and Townsend and Nichols (1925) for the continental slope off California and Baja California. Bathypelagic forms are more cosmopolitan in nature. For example, Odontomacrurus murrayi has been collected in the South China Sea, Indian Ocean, and Atlantic Ocean, and Cynomacrurus piriei may be circumpolar in the Southern Ocean (Marshall, 1964). Macrouroides inflaticeps is known from the south Atlantic, Indian Ocean, and Philippine region (Marshall and Taning, 1966). The endemism of the benthopelagic forms correlates with a lack of dispersal of larvae and eggs, and with proximity of most species to continental slopes. It is well known that these fish are mostly associated with continental slopes rather than regions of the sea distant from land. A regular decrease in biomass of benthic invertebrates with distance from land has been recorded (Zenkevich and Birstein, 1956). Bottom feeding Macrourids depend on invertebrates for food. Higher slope biomass is related to nutrient material brought by river runoff from land and resultant greater productivity of coastal waters. Benthic animals are most abundant offshore from large rivers (Isaacs, 1969). LIFE HISTORY Despite the importance of Macrourid fishes in the deep-sea biosphere, which covers over half the earth's surface, there is an impressive lack of data with regard to their life history. This is primarily due to the difficulty of collecting eggs and larval stages of these fish. Giinther first recognized this problem on the Challenger expedition. Although numerous adults were collected, no young specimens were obtained (Giinther, 1963). Since this time, work on life history has been clouded by frequent misidentification of material (Mead et al, 1964). Johnsen (1927) described ten bathypelagic Macrourid larvae collected in the north Atlantic. However, he stressed difficulties in identification of the larvae, because the characters used to identify the adults (such as configuration of the head and spinous armament of the scales) are not well developed in the larval stages. Marshall (1965) suggested a possible life history. Swimbladder drumming muscles in males may attract females. A light organ below the skin along the abdomen midline helps to keep some individuals together. Eggs are fertilized as they are shed near the bottom. They slowly float upwards as they develop. Larvae hatch at 200 m or deeper. The young then float downwards and end up on the bottom as adults. The possibility of a 200 m depth limit for eggs explains lack of Macrourids in partially enclosed basins such as the Sea of Japan (Hubbs, 1930). This tentative life history plan is currently being tested off California (Matsui, unpublished). Mead et al. (1964) presented a similar life history, but suggested that eggs normally develop bathypelagically or near the bottom with occasional displacement upwards to develop into expatriate bathypelagic prejuveniles (as described by Hubbs, 1958). Very little is known about age in Macrourids. Kulikova (1959) determined age from scales in four species of Coryphaenoides collected from the north Pacific. She found a growth decline after the first few years, and that an age of six years could be attained. Despite lack of much seasonal change in the deep sea, Macrourids have specific spawning seasons. Coryphaenoides acrolepis spawns between late February and early May off the coast of California (T. Matsui, personal communication). A similar breeding season has been noted in the Lesser Antilles region off the Caribbean for Hymenocephalus spp., whereas C. rupestris seems to be a summer and autumn breeder in the Norwegian Sea (Marshall, 1965). The major difficulty in studying food of Macrourid fishes is that expansion of
4 422 CHARLES F. PHLEGER swimbladder gases during ascent from the deep sea floor causes expulsion of the gut and its contents. Many individuals appear at the surface with the inner stomach everted from the mouth. Nevertheless, individuals from trawls are occasionally brought up with stomachs in a normal state. Podrazhanskaya (1967) analyzed gut contents of Coryphaenoides rupestris individuals from Iceland, collected in the summer. Shrimps (Pasiphaea) and their young stages comprised 74.4% of the food, with Euphausiidae (8.8%) and Tliemislo sp. (3.8%) consumed in smaller amounts. To do a thorough food study of many individuals, however, it will be necessary to invent a closing bag or trap that will retain the gut contents for study when they are expelled by swimbladder gas expansion. Marshall (1965) suggested that tail fin patterns relate to feeding habits. The longer anal rays in the Macrourinae tend to propel the tail upward while the fish swims by undulations of its tail. This points the snout downwards and enables the jaws situated beneath the snout to grasp food off the bottom. Moving picture photographs (by the Marine Life Research Group, Scripps Institution of Oceanography) show rattails swimming with a typical head down inclination. Some rattails (such as Coelorliynchns asteroides) have a pronounced snout (2/5 as long as the head) equipped with a sharp rostral spine armed with spinules (Okamura, 1963). Food requirements of Macrourids correlate with their abundance and distribution. Dredge hauls of these fishes usually depend on the abundance and variety of invertebrate life (Townsend and Nichols, 1925). It is generally recognized that continental slope regions represent population centers for deep-sea fishes. This reflects proximity to coastal waters with their high productivity and nutrient supply. Isaacs (1969) has suggested that large organic falls, such as dead whales, large dead sharks or fish, and ship's garbage may be an important food source. Baited camera evidence indicates presence of large populations of these fishes on the sea floor readv to investigate any new food supply (Fig. 1). Curtis (1971) has recently discussed the role of such a food source in the deep sea. REFERENCES Barnett, M. A Macrouridae: Biology and distribution. Scripps Institution of Oceanography (Unpublished manuscript). Curtis, T. C The role of large organic falls in the nutrition of the deep sea megafauna. MS thesis. Scripps Institution of Oceanography, Univ. California, San Diego. Garman, S The fishes. Albatross Expedition Reports 26: Gilbert, C. H., and C. L. Hubbs The Macrourid fishes of the Philippine Islands and the East Indies, U.S. Nat. Mus. Bull : Greenwood, P. H., D. E. Rosen, S. H. Weitzman, and G. S. Myers Phyletic Studies of Teleostean Fishes, with a Provisional Classification of living Forms. Bull. Amer. Mus. Natur. Hist. 131: Giinther, A Report on the shore fishes, deep-sea fishes, pelagic fishes, collected by the H. M. S. Challenger. Reprint by J. Cramer. Weinheim. Hafner Publishing Co., New York. Hubbs, C. L The hydrographic and faunal independance of certain isolated deep water seas in Eastern Asia. Proc. Int. Pac. Sci. Cong. 4th. 3:1-6. Hubbs, C. L Dikellorhynchtis and Kanazaxvaicthys: Nominal fish genera interpreted as based on prejuveniles of Malacanthus and Antennarius respectively. Copeia (4): Isaacs, J. D The nature of oceanic life. Sci. Amer. 221 (3): Johnsen, S On some bathypelagic stages of Macrourid fishes. N)t. Mag. f. Naturv. 65: Kulikova, E. B Growth and age of deep water fishes (In Russian). Tr. Inst. Okeanol. Akad. Nauk. SSSR : Transl. by Amer. Inst. Biol. Sci Marshall, N. B Bathypelagic Macrourid fishes. Copeia (1): Marshall, N. B Systematic and biological studies of the Macrourid fishes (Anacanthini- Teleostii). Deep-Sea Res. 12: Marshall, N. B., and A. V. Taning The bathypelagic Macrourid fish, Macrouroidcs inflaticeps. Smith and Radcliffe. Dana Report. Carlsberg Found. No. 69:1-6. Mead, G. W., E. Bertelsen, and D. M. Cohen Reproduction among deep-sea fishes. Deep-Sea Res. 11: Okamura, O Two new and one rare Macrourid fishes of the genera, Coelorhynchus and Jjonurus, found in the Japanese waters. Kyoto Univ. Misaki Mar. Biol. Inst. Bull. 4: Okamura, O Fauna Japonica, Macrourina (Pisces). Academic Press of japan, Tokyo. Phleger, C. F., and A. Soutar Free vehicles and deep-sea biolog\. Amer. Zool. 11: Podrazhanskava, S. G Feeding of Macrurus rupeitris in the Iceland area. Ann. Biol. 24:
5 BIOLOGY OF MACROURID FISHES 423 Touiisencl, C. H., and J. T. Nichols Deep Sea Zenkevich, I,. A., and J. A. Birstein Studies fishes of the "Albatross" Lower California of the deep water fauna and related problems. Expedition. Bull. Amer. Mus. Xatur. Hist. 52:1-20. Deep-Sea Res. 4:54-64.
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