V. Nekton Assemblages (Crustacea, Squid, Sharks, and Bony Fishes)
In describing the nektonic (strong swimmer) assemblages, we will follow an arbitrary division of the water column into three depth zones: the epipelagic, mesopelagic and bathypelagic. These zones are not actually delineated; rather, the definitions refer more to the continuum of environmental features that typify each. Because these habitats are relatively remote and hard to sample, we will concentrate on what is known and suggest the many areas which are poorly known and need considerable ecological study.
A. Epipelagic Zone
This region, characterized as the upper 200 m of the water column, is penetrated by sunlight and subject to seasonal variation in temperature and salinity. However, the oceanographic features previously covered make it much more structured than previously thought which has in turn influenced the assemblages of fishes that occur here (Mais 1972; Cailliet et al. 1979; CalCOFI Rep. 24 1983; CalCOFI Rep. 33 1992; and Leet et al. 1992). Sampling the fauna in this large area is difficult and researchers usually resort to straightfoward techniques such as hook and line, very large trawls, acoustics, and more recently, drift gill nets.
Data sheets of typical organisms collected in midwater trawls are available from MLML and other nearby institutions that study this habitat, and they document the numerous phyla represented in the epipelagic region. They include the cephalopods, the most common of which is the market squid (Loligo opalescens: Figure 3), which is discussed in Mais (1972), Cailliet et al. (1979) and Cailliet & Vaughn (1983). Many other species of cephalopods occur here both inshore and offshore (see Anderson 1977, Nybakken 1996). Two large relatively common squid are Onychoteuthis borealijaponicus and Moroteuthis robustus.
The chondrichthyans are represented by the blue shark (Prionace glauca: Figure 6), common thresher shark (Alopias vulpinus), mako shark (Isurus oxyrhinchus), basking shark (Cetorhinus maximus), spiny dogfish(Squalus acanthias) and ratfish (Hydrolagus colliei)(Hanan et al. 1993; Cailliet and Bedford 1983). Occasionally, the bigeye thresher shark (Alopias superciliosus), salmon shark (Lamna ditropis), and soupfin shark (Galeorhinus galeus) are taken in pelagic fishing gear (Cailliet et al. 1993). The white shark (Carcharodon carcharias) is seen around two locations, the Farallon Islands and Año Nuevo Island, but only occasionally observed in the open water habitat.
The epipelagic bony fishes are very diverse (Mais 1972, Cailliet et al. 1979, Hanan et al. 1992). From a cursory examination of catch records in the MLML museum files, these include anadromous fishes such as the king (or Chinook) salmon (Oncorhynchus tswatchyta), as well as pelagic fishes like anchovies (Engraulis mordax), sardines (Sardinops sagax), and Pacific saury (Cololabis saira) (Parrish et al. 1971-73; Anderson et al. 1979, Lasker 1985, Parrish et al. 1985, Parrish et al. 1986, Watanabe et al. 1988, Barnes et al. 1992, Wolf 1992).
Another group of pelagic fishes are the tunas (Laurs and Lynn 1977, MacCall 1983, Parrish et al. 1989, Coan and Jackson 1992, Bartoo and Uozumi 1993), including the most common ones, the albacore (Thunnus alalunga) and Pacific bonito (Sarda chiliensis). Other relatively large pelagic fishes are the jacks and jack mackerels (family Carangidae: Parrish 1971-1973, MacCall et al. 1985, MacCall and Stauffer 1983), commonly including the Pacific mackerel (Scomber japonicus) and jack mackerel (Trachurus symmetricus). The largest in this group are the billfishes, which generally only includes the swordfish (Xiphias gladius), although occasionally a striped marlin (Tetrapturus audax) will appear this far north (Hill and Haight 1992).
The pelagic drift gill net and midwater trawling fisheries have indicated the abundance of other miscellaneous pelagic fishes, including the hake or Pacific whiting (Merluccius productus: Figure 5), Pacific butterfish (Peprilus simillimus), yellowtail (Seriola lalandi), the North Pacific frostfish (Benthodesmus elongatus pacificus), opah (Lampris guttatus), louvar (Luvarus imperialis), ocean sunfish (Mola mola: Figure 7), and medusafish (Icichthys lockingtoni). Rarer pelagic species like the prowfish (Zaprora silenus: Cailliet and Anderson 1975), oilfish (Ruvettus pretiosus), oxeye oreo (Allocyttus folletti), lancetfish (Alepisaurus ferox), and black scabbardfish (Aphanopus carbo) sometimes appear in these catches (Anderson et al. 1979).
The diversity of the pelagic fish fauna is relatively low, especially considering the volume of water habitat available. Their major adaptations include constant swimming (e.g., fusiform shape, both red and white muscles, heat retention mechanisms), well-developed vision and perhaps mechanoreception, countershading, fast growth, broadcast spawning, relatively large seasonal migrations often following thermal fronts, carnivorous feeding habits, schooling, and association with floating objects like kelp and flotsam or jetsam.
The major advances in knowledge of these fishes have come from large scale fishing activities, plus the use of correlative satellite oceanography to determine fish associations with specific water characteristics. Recently, tagging and tracking techniques, coupled with advanced differential Global Positioning Systems (GPSs), have produced some interesting results. The use of genetic tools has just begun to help unravel details of their population structure (Hedgecock et al. 1989). Because of their size, speed and ability to move great distances, there are many gaps in information about these fishes. Based upon information mostly gleaned from fisheries (see Hanan et al. 1992), it is known that most of these species are worldwide. Despite the tight correlation with water temperatures found by Laurs and Lynn (1977) and reviewed by Leet et al. (1992) and others for tunas like albacore, there are presently no fixed geographic ranges known for the species.
Movement patterns are poorly known for most epipelagic fishes, except for important commercial fishes like albacore (Leet et al. 1992) and some of the conspicuous summer visitors, like blue sharks, Prionace glauca (Carey and Scharold 1990) and swordfish, Xiphias gladius (Carey and Robison 1981). One must remember that these fishes range throughout an enormous habitat and therefore are hard to track. Undoubtedly, there is considerable trophic interaction among these larger epipelagic fishes and their meso- and bathypelagic counterparts during diel vertical migration. Also, there are known north-south movements that occur during normal seasonal thermal events and northern range extensions, especially during ENSO years.
Seasonal changes do occur in the pelagic fish fauna of the Bay. As mentioned above for the blue shark, summer in the greater Monterey Bay area brings an increase in many fishes which normally occupy more southern waters, such as the common thresher (Alopias vulpinus) and bonito or mako (Isurus oxyrinchus) sharks, ocean sunfish (Mola mola), and opahs (Lampris guttatus).
There is also year-to-year variation in the fish fauna, most likely due to oceanographic and/or climatic conditions, including of course, ENSO years. Other, long-term changes also occur. Certainly, one example of this would be the sardines, whose populations continue to increase following their crash in 1940s. Another would be the appearance of cold, saline water from the south via the Davidson Current, which also can bring southern fauna to the Monterey Bay area.
There are vertical links between the epipelagic fauna and the fauna of deeper waters. The most obvious is the deep scattering layer, a loose assemblage of krill, sergestid shrimp and mesopelagic fishes (e.g., lanternfishes or Myctophidae) that moves up at night and down during the day. The trophic interactions of the organisms comprising this layer and those organisms which feed upon them transport food from the surface to deeper water (Isaacs and Schwartzlose 1965, Pereyra et al. 1969, Isaacs et al. 1974, Youngbluth 1976). Other interactions involve the simple sinking of detrital materials, such as midwater fish fecal matter, which are a source of food for deeper organisms (Robison and Bailey 1981).
The main human impacts on the epipelagic zone include shipping and fishing. Many large cargo vessels and tankers venture upon this habitat annually and a large number of chartered vessels take passengers out to view the local fauna, including birds, mammals and epipelagic fishes. Certainly, commercial and recreational fishing can have an influence, as exhibited by the large fleet of salmon trollers and larger vessels that set pelagic drift gill nets to capture swordfish and other, non-targeted fishes, such as sharks. Undoubtedly these activities have some sort of interaction with the epipelagic fauna (Squire 1992, Leet et al. 1992).
B. MESOPELAGIC AND BATHYPELAGIC ZONE
These zones will be considered together. Collectivley they occur immediately below the epipelagic zone, discussed above, and down to several thousand meters. This zone is characterized by low light levels, decreasing temperature, slower currents, lower food availability, and increasing salinity and pressure. This relatively voluminous water mass has been described as harsh and resource limited.
Much of the early knowledge of meso- and bathypelagic organisms came from early surveys, such as the 3 1/2 year voyage of H.M.S. Challenger begun in 1873, and covering 68,890 miles (Marshall 1954). In U.S. waters, the Coast Survey Streamer Blake initiated deep-sea explorations in 1877, while the first major survey of the west coast was that of the U.S.S.Albatross, headed by Alexander Agassiz from 1882-1924.
Earliest samples of deepsea organisms were obtained from the stomach contents of large predators that washed up on beaches. Later, surveys used trawls, which in early years were open nets, but were eventually deployed with a technology that allowed the mouth and codend to be closed at discrete depths, allowing sampling which produced a better description of depth distributions of the deepwater fauna. Using such trawling gear has many biases, including those caused by patchiness, escape, extrusion, and speed.
More recently, remotely operated and manned submersibles (ROVs like MBARI's "Ventana" and "Tiburon" operated from the research vessels Point Lobos and Western Flyer, respectively), have allowed more direct exploration of midwater regions (Robison 1994, 1995). Also, manned submersibles like "Alvin," "WASP," "Deep Rover," "MIR" (see Mysteries of the Deep, Time, 14 August, 1995), and the "Delta" have been actively exploring parts of the Monterey Submarine Canyon and environs (Yoklavich et al. 1993, 1995 ). While there is disagreement about the utility of manned versus unmanned submersibles (see Science 1993, 259:1534-1536) the combined approach has been successful in determining that the invertebrate fauna is dominated by eight phyla: Ctenophora, Cnidaria (Coelenterata, including the Siphonophora), Nemertea, Annelida, Chaetognatha, Arthropoda (mainly Crustacea), Mollusca, and Chordata.
The Siphonophora are undoubtedly very common but underestimated in trawl samples due to their fragile nature. Some can simply be called "pointed siphonophores," but progress is being made, especially at MBARI, identifying and naming other siphonophores like Praya dubia, Nanomia (bijuga?), and Apolemia spp. These undoubtedly play important trophic (predatory) roles in the midwater zone off the sanctuary, a subject presently being investigated by Bruce Robison and Kim Reisenbichler at MBARI.
The only common mesopelagic nemertean is Nectonemertes sp., an orange pelagic form regularly taken in midwater trawls (Pam Roe, personal communication). Sometimes the annelid genera Tomopterus, Alciopina, Poebius and Vanadus are caught in trawls or observed from ROVs. Other polychaetes are described in Nybakken (1996). The feeding ecology of one of these, (Poebius) was described by Uttal and Buck (1996). Thuesen and Childress (1993) studied the metabolic rates of the pelagic worms (Nectonemertes and Poeobius) and found that the polychaetes had higher metabolic rates than bathypelagic shrimps, copepods and fishes, perhaps the highest among deep-sea organisms.
The Crustacea comprise the dominant invertebrate group in the mesopelagic, including at least three species of Euphausiacea (Euphausia pacifica, Nematoscelis difficilis, and Thysanoessa spinifera). The Decapoda are also well represented, including at least the following six species: Sergestes similis, Pasiphaea pacifica, P. emarginata, and P. chacei, Parapasiphaea sulcatifrons, and Gennadas propinquus. Also represented are several species of galatheid crabs, the adults of which are benthic, but whose larvae appear in the water column. Also included in this group are the Ostracoda, including Conchoecia spp. and Gigantocypris. These animals are interesting in that they often exhibit parental care.
The large Copepoda include the black Gaussia princeps and numerous types and sizes of red copepods. The Mysidacea are represented in the deeper depths by Gnathophausia ingens, Boreomysis spp., and Eucopia spp. The Amphipoda are probably the most speciose crustacean group, numbering at least a dozen species, including the genera Hyperia, Paraphronima, Vibilia, Paracallisoma, Phronima, Scina, Orchomenella, Primno, Cystisoma, Streetsia, Cyphocaris, and many species in the family Gammaridea. The genus Phronima exhibits parental care by housing its offspring in a discarded gelatinous house.
A study by Childress and Nygaard (1974) indicated that deep-dwelling crustaceans tended to have different chemical composition and buoyancy mechanisms than shallower dwelling forms. This is undoubtedly one of many adaptations to the harsh midwater habitat.
The Chaetognatha, according to Karen Light, Monterey Bay Aquarium, includes at least 15 species in three families, with the following 7 documented from midwater trawls in the Bay: Caecosagitta macrocephala, Flaccisagitta hexaptera, Parasagitta euneritica, Pseudosagitta lyra, Pseudosagitta maxima, and Solidosagitta zetesios.
The nektonic Mollusca include at least 23 species in 14 families (Nybakken 1996). The most common cephalopods in the water column are Loligo opalescens, Histioteuthis heteropsis, Gonatus spp., and Chiroteuthis calyx (Okutani and McGowan 1969). Perhaps the most interesting is the archaic, football-sized vampire squid,Vampyroteuthis infernalis. Some of the mesopelagic molluscs, such as young octopods, are bioluminescent (Robison and Young 1981, Thuesen 1993).
The meso- and bathypelagic fishes are quite diverse, ranging from two species of catshark (Parmaturus xaniurus and Apristurus brunneus) through various higher bony fish families such as the Myctophidae (at least 12 species, dominated by Stenobrachius leucopsarus), Gonostomatidae (3 species, including Cyclothone signata and Cyclothone acclinidens), Sternoptychidae or Photichthyidae (at least 6 species of Argyropelecus, Sternoptyx, and Danophos), Searsidae (Holtbyrnia spp. and Sagamichthys abei), Alepocephalidae (Talismania bifurcata and Alepocephalus tenebrosus), Argentinidae (Argentina sialis), Bathylagidae (five species, with Leuroglossus stilbius dominating), Opisthoproctidae (Macropinna microstoma and Dolichopteryx longipes), Idiacanthidae (Idiacanthus antrostomus), Melanostomiatidae (Bathophilus flemingi and Tactostoma macropus), Malacosteidae (Aristostomias scintillans), Chauliodontidae (Chauliodus macouni), Liparidae (Nectoliparis pelagicus and Lipariscus nanus), Zoarcidae (Lycodapus mandibularis and Melanostigma pammelas), Melamphaeidae, Anoplogasteridae (Anoplogaster cornuta), Oneirodidae (Oneirodes acanthias, Trachipteridae (Trachipterus altivelis) and larval hake, flatfishes (Bothidae, Pleuronectidae) and rockfishes (Scorpaenidae).
These fishes have adaptations which include silvery or transparent to black and red coloration, large eyes well-equipped with rods, rhodopsin pigment and having a tubular structure, and bioluminescence (Robison 1995). The photophores of myctophids, sergestids and cephalopods emit blue light which can adjust to downwelling light. Bioluminescence has multiple functions, including: schooling, species recognition, counter-shading, reproduction, predator deterence, prey lures, and simply as light source (Marshall 1954, 1979).
These deepsea fishes are generally neutrally buoyant, either through swimbladders or their flabby, buoyant tissue. They also exhibit metabolic economy by maintaining reduced skeletons and muscle and while storing more fat (Marshall 1979). They are generally lethargic, have thin tails, and are mostly made of water. Their growth rates are high, but their bodies are economized (Childress and Nygaard 1973, 1974; Childress et al. 1980).
Feeding adaptions among meso- and bathypelagic fish include bioluminescent lures, large mouths, large and flexible teeth, dispensable stomachs. Many fishes send their eggs and larvae to the surface, or they exhibit parental care. Many deep-water fishes appear be semelparous; that is, they reproduce once, relatively late in life (Childress et al. 1980).
One of the most important and unique features of Monterey Bay is that deep midwater habitats are very close to shore. This increases the ability of scientists from many institutions to sample, observe and study the organisms in this habitat and to provide information on the links of these assemblages to organisms and processes in nearshore habitats. Of special interest is the head of the Monterey submarine canyon because of the potential interaction of vertically migrating zooplankton and nekton with the bottom fauna (Isaacs and Schwartzlose 1965, Pereyra et al. 1969, Cailliet and Ebeling 1990).
There is very little fishing activity in meso- or bathypelagic habitats, and therefore human impact through fishing in this zone is minimal. However, major fisheries for the hake or Pacific whiting, Merluccius productus, may could affect trophic interactions in this zone.
Section IV. Zooplankton