Prepared by: EFH Technical Team
(Excerpted from the 1999 Habitat Annual Review Report)
--------------------------------------------------------------------------------
Habitat Areas of Particular Concern (HAPC)
According to the language of the NMFS guidelines [Federal Register 62 (244): 6653 1-66559], EFH that is judged to be particularly important to the long-term productivity of populations of one or more managed species, or to be particularly vulnerable to degradation, should be identified as a "habitat area of particular concern" (HAPC) to help provide additional focus for conservation efforts. There are four basic criteria suggested by NMFS for identifying areas or habitat types for consideration as an HA.PC:
(1) the importance of the ecological function provided by the habitat;
(2) the extent to which the habitat is sensitive to human-induced environmental degradation;
(3) whether, and to what extent, development activities are, or will be, stressing the habitat type; and,
(4) the rarity of the habitat type.
Habitats that are particularly vulnerable to specific fishing equipment types should be identified for possible designation as habitat areas of particular concern.
The intent of the HAPC designation is to identify those areas that are known to be important to species in need of additional levels of protection from adverse impacts (fishing or non-fishing). Designation of an HAPC is intended to determine what areas within EFH should receive more of the Council's and NMFS' attention when providing comments on federal and state actions, and in establishing higher standards to protect and/or restore such habitat.
In the omnibus EFH amendment, the Council made two HAPC designations. One, for juvenile Atlantic cod, designated a small portion of northeastern Georges Bank within the boundaries of Closed Area II, based on the identification of gravel habitat with an increasing biomass of emergent epifauna. Current scientific studies identify this type of habitat as important for recently settled juvenile cod, providing shelter from predation and possibly an increased food supply. The second HAPC includes eleven rivers in Maine that support the only remaining U.S. populations of naturally spawning Atlantic salmon that have river-specific characteristics.
The Council's EFH Strategic Plan states that with each Habitat Annual Review Report, the Habitat Conunittee will consider any additional information for the designation of additional HAPC's, as appropriate, where the quantity or quality of a particular habitat type or area is directly linked to an ecological bottleneck for one or more species. The designation of HAPC's will extend, as appropriate, to areas or habitat types that are EFH for a vulnerable life stage of a significant number of Council-managed species or group of Council-managed specks (i.e., fiatfish, Gadidae, etc.).
Juvenile Atlantic Cod and Inshore Gulf of Maine
Presently, the Georges Bank cod stock is assessed as well below the maximum sustained yield biomass threshold (B~~); however, the spawning stock biomass has been increasing in recent years under a broad suite of management regulations pursuant to the conservation goals of the FMP (NEFMC's MSMC 1998). Unfortunately, recent recruitment has been poor, and 1994-97 year classes have been among lowest on record (NEFSC 1997).
---------------------------------------------------------------------------------
Inshore GOM HAPC page 2
The situation for Atlantic cod in the Gulf of Maine is now much more problematic. Despite implementation of management measures in 1994 to reduce fishing mortality, commercial catch and landings have continued to decline. Spawning stock biomass is at a record low level, the frilly recruited fishing mortality rate remains high, and recruitment and survival of pre-recruit fish are at record lows -- all indications that the stock is collapsing (NEFSC 1997). Both the NEFSC trawl survey, covering the entire Gulf of Maine, and the Massachusetts Division of Marine Fisheries trawl survey, operating in Massachusetts territorial waters, have found that recent year classes are the poorest in the survey time series (NEFMC's MSMC 1998). Moreover, NEFSC survey catches for the period 1979-1983, compared to 1994-1998, illustrate a contraction in distribution of age-3 and older cod to the historic center of abundance off Cape Ann, Massachusetts. A further decline in biomass in 1999 has been projected even with a drastic reduction in fishing mortality.
If the Gulf of Maine cod stock is to be rebuilt to ~ the Habitat Committee may want to consider recommending an HAPC to provide more protection for critical habitat. Available data and a review of recent scientific literature suggests that consideration be given to designating a juvenile Atlantic cod HAPC for the perimeter of the Gulf of Maine from mean low water (MLW) to a depth of 9 m below MLW (30'). The benthic community within this very narrow coastal zone has been found to be critical for Atlantic cod during a short period following metamorphosis from the larval stage and prior to settlement to demersal habitat. It serves as a source of cod replenishment for seaward fishing areas because juveniles move into deeper offshore water as they mature. Other valuable groundflsh (e.g., winter flounder and white hake) as well as American lobster would also be afforded the same protection.
Recent Research
During the late 1980's, Atlantic cod inhabiting the waters off southern Labrador and eastern Newfoundland (viz, northern cod stock) underwent a dramatic decline in biomass, with the result that the famous Grand Bank fishery collapsed in 1992. This lead to a fishing moratorium as well as an economic and ecological disaster (Hutchings 1996; Myers, et al. 1996). It also triggered unprecedented research at federal fisheries laboratories and universities in eastern Canada under the auspices of the Government of Canada's Northern Cod Science Program and the governni~nt I industry-funded Ocean Production Enhancement Network program. In total, there were 58 study initiatives and projects covering a broad suite of research costing about $48 million from 1990-95 (Campbell 1997).
The following description of research results from Canada and other countries deals with life history and behavioral ecology of newly settled juvenile cod, particularly post-settlement events relating to habitat that may ultimately affect recruitment strength. Studies have focused on laboratory observation experiments as well as field capture efforts utilizing active sampling equipment, SCUBA and submersible vehicles for in situ observations, and seabed classification techniques for acoustically classifying juvenile habitat. Nearly three dozen scieutific papers relating to this subject have been published in recent years. The information is directly applicable to coastal nursery areas in the Gulf of Maine, the inference being that knowledge gained from such studies should be used for more risk-adverse habitat management.
------------------------------------------------------------------------------
Inshore GOM HAPC page 3
Juvenile Cod Community & Interactions - Research Results
Pelagic Juvenile Settlement Post-larval pelagic juveniles are transported by prevailing currents to shallow waters off eastern Newfoundland beginning in May and may continue arriving in periodic pulses as late as December (Methven and Bajdik 1994; Grant and Brown 1998). Their length upon settlement is 25-45 mm (Pinsent and Methven 1997). In southwest Nova Scotia, pelagic juveniles arrive inshore slightly larger (~40-50 mm) in May (Tupper and Boutilier 1995a and 19951,), whereas influxes of larvae begin earlier in Massachusetts waters two to three months after hatching (Bigelow and Schroeder 1953). On Georges Bank, cod settle out in July at 40-60 mm, and those reaching rough and cobble bottom may experience reduced predation risk. This particular habitat may be an important demographic bottleneck to benthic recruitment on Georges Bank (Loughetal. 1989).
Pelagic juveniles exhibit no preference for habitat types at settlement, and they occupy rock reef, cobble, eelgrass (Zostera marina) beds, and sand bottom (Tupper and Boutilier 199 Sb). Tupper and Boutilier (1995b) assumed that settling also occurred on macroalgae habitat, as noted by Keats et al. (1987) off eastern Newfoundland, however, algal stands were scarce in the St. Margaret's Bay, Nova Scotia, study area due to subtidal grazing by sea urchins (Strongylocentrotus drobachiensis). Sea urchins commonly leave a partially denuded or "barren" zone along nearshore sections of the maritime provinces and Gulf of Maine.
Age-O Movements and Diel Feeding Shallow water depths (<5 m) and a strong attraction to features on most substratums, except sand, afford settled juveniles an environment conducive to growth and survival (Tupper and Boutilier 1995a; Grant and Brown 1998b). The shallowness appears to ecologically segregate the 0-group cod from older age-groups at least during daylight (Tupper and Boutilier 1995a; Fraser et al. 1996; Gotceitas et al. 1997; Grant and Brown 1998a and 1998b). Age-0 cod maintain a strict diurnal foraging cycle, school (or shoal) feeding on zooplankton in a tide-related pattern during the day, and remain near protective bottom habitat which they readily seek when threatened (Gotceitas and Brown 1993; Gotceitas et al. 1995; Grant and Brown 1998a). The mottled coloring of young juveniles effectively conceals them in a pebble-gravel environmeifl (Lough et al. 1989; Gregory and Anderson 1997). In contrast, pelagic juveniles on Georges Bank maintain a nocturnal feeding pattern (Perry and Neilson 1988). Age-0 cod cease feeding in surface waters and disperse to the substratum at night (Grant and Brown 1998b) where they are less active to reduce interactions with potential predators (Grant and Brown 1998a). The diel change in vertical distribution and activity of 0-group cod coincides with a nocturnal shoreward movement and foraging by older (age-1-3) conspecifics (Bosgstad Ct al. 1994; Gotceitas et al. 1997; Grant and Brown 1998a). Intercohort cannibalism is common. The occurrence of age-O cod in very shallow water (<1.2 m) at night (Methven and Bajkik 1994) has also been interpreted as possibly an evasive response to predation risk (Grant and Brown 1998a).
Influence of Habitat Structure and Predation on Age-O Demography Tupper and Boutilier (1995b) found that the spatial pattern of settlement was altered by post-settlement mortality in St. Margaret's Bay, Nova Scotia. Age-0 survival was positively correlated with an index of rugosity, a measure of actual bottom surface or complexity. Capture success by fish predators (in this case, three species of Cottidae during a diurnal field study) was
--------------------------------------------------------------------------
Inshore GOM HAPC page 4
inversely related to the index of rugosity. As a result, higher densities of age-C cod were found in cobble and rock reef habitats than in eelgrass. However, the rugosity index could not account for the complexity of surface area that eelgrass offered. Higher survival in sites of cobble and rock reef was attributed to increased shelter that the more structurally complex habitats afforded coupled with decreased predator efficiency (Keats et al. 1987; Lough et al. 1989; Tupper and Boutilier 1995b; Gotceitas et al. 1997; Grant and Brown 1998a and 1998b).
Tupper and Boutilier's (1995b) and Grant and Brown's (1998a) in situ studies confirmed earlier and subsequent laboratory experiments on substrate preference and predator efficiency. Clearly, the presence of conspecifics may influence the distribution and food intake of age-C cod in the wild. Both age-C and 1 cod preferred finer grained substrate in absence of a predator, but when in the presence of an age-3 conspecific, young-of-the-year and age-i either avoided the predator or selected the coarser substrate (cobble vs. gravel) where they hid in interstitial spaces (Gotceitas and Brown 1993; Gotceitas et al. 1995; Fraser et al. 1996). Age-C avoided the yearling conspecific resulting in a significant increase in use of gravel and cobble confirming the level of habitat segregation noted in the wild (Fraser et al. 1996). Also, age-O cod avoided kelp (Lam maria) except when exposed to an actively foraging predator and cobble was unavailable. In this situation, kelp significantly reduced predation risk (Gotceitas et al. 1995). Both field and laboratory studies indicate that the association with coarse substrates, when coupled with behavior patterns that reduce predation risk, give young cod competitive advantage in avoiding detection or capture.
Eelgrass Habitat and Abiotic Factors The presence of eelgrass beds or meadows appears to be a very important factor influencing the distribution of age-0 cod throughout the Canadian maritime provinces (Tupper and Boutilier 1995a; Gotceitas et al. 1997; Grant and Brown 1998a, 1998b). Grant and Brown (1998b) noted that cod were more highly concentrated in eelgrass beds with >65% submersed canopy coverage. Gotceitas et al. (1997) captured age-0 cod almost exclusively in eelgrass beds of Trinity Bay, Newfoundland, where their usage by 0-group cod was consistent spatially and temporally. The eelgrass sites most sheltered to natural physical disturbance produced the highest catches; lower catches occurred at the shallowest and least saline sites (10.4-19.5 ppt). Salinities were usually high (>25 ppt) at most Newfoundland study sites (Methven and Bajkik 1994). Age-C tolerate much lower salinities as was observed in coastal waters of Wales and England where catches occurred from 20-3 1 ppt (Riley and Parnell 1984).
Post-settlement cod may respond to environmental gradients in addition to substrate structure and salinity. For example, high water clarity may be important for feeding (Home and Campana 1989). Strong tidal currents may be beneficial for concentrating food in seagrass beds (Tupper and Boutilier 1995b; Grant and Brown 1998a). Water temperatures coinciding with age-C collections in St. Margaret's Bay, Nova Scotia, ranged between 4-90C from May to July (Tupper and Boutilier 1995b) while July to September temperatures in age-C habitat of Trinity Bay, Newfoundland, were 12-160C with a year-round range of 1.7-17.00C (Methven and Bajdik 1994). Water temperature might displace 0-group and yearlings to slightly deeper waters south of Newfoundland, however (Methven and Schneider 1998).
---------------------------------------------------------
Inshore GOM HAPC page 5
Among-Habitat Variation in Age-O Growth
Growth of settled age-0 cod appears to be temperature dependent (Tupper and Boutilier 1995 a). Growth was most rapid in eelgrass beds, which may positively effect overwinter survival of demersal 0-group juveniles. Growth was slowest on sand bottoms; differences in growth between young inhabiting reef and cobble bottoms were not significant (Tupper and Boutil jet 1995b). The growth advantage conferred by seagrass is related to the variety of microhabitats therein that support a diverse community of invertebrates (Orth et al 1984; Heck and Crowder 1991; Heck et al. 1995; Grant and Brown 1998a). Planktonic organisms may be passively concentrated by water currents and effectively retained within the eelgrass canopy. Also, invertebrates and fish may actively seek its confines even crossing predation-risky sand to reach isolated patches (Sogard 1992).
Small planktonic crustaceans, but mostly copepods, are preyed upon by young cod (Keats and Steele 1992; Grant and Brown 1998a). When mouth gape size is large enough, at a length of 6 to 10 cm, cod transition to predominately benthic prey (Keats et al. 1987; Lomond et al. 1998) which they then consume at dusk and dawn (Grant and Brown 1998 a).
Among-Habitat Variation in Age-O Survival
Eelgrass provides age-0 cod protection from predators (Tupper and Boutilier 1995; Gotceitas et al. 1997; Grant and Brown 1998b). In a laboratory experiment, eelgrass significantly increased the time required for an age-3 cod to capture 0-group cod and decreased the number captured. With a predator present, young cod either bid in cobble or in eelgrass when stem density was
>720 stems/m2. Time to capture was highest and total prey taken was lowest in combinations with cobble or vegetation of 1,000 stemlm2 (Gotceitas et al. 1997). Results demonstrated that high plant density andlor biomass, whether eelgrass or macrophytic algae (Isaksson et al. 1994), means reduced predation risk just as does use of certain substrates. Moreover, there may be a trade-off between nutritional gain and enhanced predation risk for age-0 cod utilizing eelgrass habitat (Tupper and Boutilier 1995).
Mark-recapture experiments indicate age-0 cod remain very localized, not moving more than several hundred meters in both eelgrass and no-eelgrass habitats (Grant and Brown 1998b). Those that settled earliest and were largest at settlement grew faster and defended a larger territory than later! smaller settlers (Tupper and Boutilier 1995 a), thus a competitive advantage in growth and survival may exist for the earliest pulse of post-larval juveniles over those settling later when temperatures and day length are reduced (Tupper and Boutilier 1995b).
Abundance in the seagrass sites of St. Margaret's Bay, Nova Scotia, was noted to decline after early June. This was attributed to predation rather than emigration because young were strongly site-attached and defended territory as they grew. Marked individuals were not found in areas surrounding the study site (Tupper and Boutilier 199 Sb). As the summer season advanced, a greater decline in abundance occurred in eelgrass beds and on sand than in structurally more complex reef and cobble habitat. Observing in situ young-of-the-year seeking shelter in rock crevices, empty scallop shells, and other debris within dense grass beds, Tupper and Boutilier (1995b) believed that cod out-grew eelgrass blades as suitable refuge.
----------------------------------------------------------------
Inshore GOM HAPC page 6
Unable to compete for nonexistent shelter on sand habitat, age-0 cod school for protection (Tupper and Boutilier 1995a); however, the population density in these areas reached zero by late June (Tupper and Boutilier I 995b). Predation by three Cottids - sea raven (Hemitripterus americanus), grubby (Myoxocephalus aeneus) , and longhorn sculpin (Myoxocephalus octodecemspinosus) - was most successful on sand and least successful on cobble and rock reef. Age-O cod schooling over sand bottoms have low site fidelity which is disadvantageous to survival (Grant and Brown 1998a).
Young-of-the-year appear to lose site fidelity and disperse into deeper water during the December-January period (Tupper and Boutilier 1995a; Gregory and Anderson 1997) adopting winter behavior of reduced activity and food consumption (Brown et al. 1989). Still, some marked demersal juveniles remained localized in the shallowest (<1.2 m) sampling site in Trinity Bay, Newfoundland, throughout the winter even when ice was present (Grant and Brown 1998b). Age-0 and older juveniles are more adapted than adult cod to survive icy subzero water due to elevated plasma antifreeze levels in their blood (Goddard et al. 1992).
Age-1 and Older Juvenile Habitat and Movements
Age-1 juveniles are found during day and night in shallow inshore waters, including locations with moderate to high wave exposure (Keats 1990). Older juveniles are generally distributed farther away from shore than 0-group and 1-group cod and at depths >25 m. Age-1 associate to a greater degree with rocky substrate and fleshy macroalgae or bottom dominated by sea urchins and coralline algae (Keats et al. 1987; Keats 1990; Gotceitas et al. 1997). The association with a macroalgal canopy seems to be more one of refuge from predators than feeding purposes (Keats et al. 1987; Gotceitas et al. 1995; Gotceitas et al. 1997). They congregate in small groups near boulders and in large crevices. In Newfoundland bays, age-1 cod have been collected within a slightly narrower temperature range, 1-160C, than demersal 0-group fish (-1.7-i70C) (Methven and Bajdik 1994).
At dusk during sunmier and autumn seasons, age-i and older juveniles move shoreward into warmer water feeding areas where the young-of-the-year cod are concentrated. The attracting stimulus appears to be the periodic influxes of early settled cod (Keats 1990; Clark and Green 1990; Methven and Bajkik 1994). Age-1 cod have usually been found feeding until dawn primarily on mysids and ganimarid ampbipods; however, when they become about three times larger than settled age-0 juveniles, they begin cannibalizing the demersal 0-group cod (Grant and Brown i998a). By late fall, the earliest age-0 settlers may be large enough to begin intracohort cannibalism on the late settlers, as has been noted in waters of Iceland (Bogstad et al. 1994). When abundance of older juveniles is high, mortality may increase on young-of-the-year because of competition and predation from conspecifics (Grant and Brown 1998a).
Age-1 cod have also been observed feeding on plankton after moving inshore in spring (Keats Ct al. 1987) as well as resting near bottom in shallow water at night (Keats and Steele 1992). In the latter situation, age-i were not feeding and analysis of stomach contents indicated daytime foraging on planktonic crustaceans leading the authors to speculate that post-transitional feeding on benthic invertebrates might be patchy in space and time. Where, when, and to some extent what yearlings eat is likely related to trade-offs between predation risk and food availability.
--------------------------------------------------------
Inshore GOM HAPC page 7
Juvenile cod may utilize the intertidal zone for feeding purposes although there is no mention of this in recent studies. Earlier, an underwater television camera mounted on a herding fence recorded 423 "young" Atlantic cod (no size given), and Atlantic tomcod (Microgadus tomcod), which were sometimes indistinguishable from cod, as well as six, 3 0-40 cm (age-3 to 4) cod moving up and down a beach, either with or against tidal current, during daytime between June and October in Passamaquoddy Bay, New Brunswick (Tyler 1971). Of eight fish species observed undertaking these movements, the cod! tomcod combination ranked third, behind only winter flounder (Pseudopleuronectes amercianus) and Atlantic herring (Clupea harengus) in their use of the intertidal zone.
Diel Dfferences in Abundance
Keats (1990) found one- and two-year-olds 16 times more abundant at night than during the day while making SCUBA transects at a depth of 5-9 m MLW. Methven and Bajdik (1994) were able to seine age-i cod throughout the year but only at night in a cove of Trinity Bay, Newfoundland, whereas age-i were caught both day and night by Grant and Brown (1998a) in a different cove of the same embayment. An explanation for the difference in catch of yearling cod between the two studies may be related to sampling techniques. The first study employed a 9 m seine pulled from a maximum depth of 1.2 m (no bridle). The second utilized a 30 m seine deployed by small boat 50 m from shore and pulled by towropes thereby encircling age-i cod inhabiting a slightly greater depth range.
Researchers studying young cod recognized that gear avoidance occurred during daylight, but avoidance was secondary to diel activity in explaining abundance differences between day and night catches for both age-0 and the older juveniles (Methven and Bajdik 1994; Gibson et al. 1996; Methven and Schneider 1998; Grant and Brown 1998b). Abundance of age-i peaked in the shore zone from August-November and again in April-June period, but was much reduced in winter (temperature <00C) indicating withdrawal to deeper habitat. The offshore movement by young cod was also reported in Passamaquoddy Bay, Bay of Fundy (MacDonald et al. 1984).
Juvenile Winter Habitat and Activity
Juveniles inhabit progressively deeper water and associate with coarser substratum as they grow and mature, especially in winter (Keats et al. 1987). Age-1-4 cod were observed at 18 to 1 50dm from submersible vehicles during April (-1 0C at 25-7 Sm), Placenta Bay, Newfoundland (Gregory and Anderson 1997; Gregory et al. 1997). They found that 80% of two-to four-yearolds were associated with rock, boulders, and high bathymetric relief (cliffs) and often maintained fidelity to such features including crevices in rocks. They exhibited significant increases in swimming speed with increasing distance from structure. Yearling cod showed no such connection, 59% of those observed were primarily over gravel and low relief with the fish appearing to rely on cryptic patterns to remain undetected. Macroalgae was neither avoided or preferred by either group. Age-1 and ages 2-4 co-occurred laterally and vertically throughout the study area most abundantly at depths of 60-120 m. Juveniles did not appear to undertake a diet movement shoalward during the winter! early spring season. However, onshore movements may be initiated during March and April after ice break-up and coincident with nearshore water temperature of~2-30C. The same temperature prompts offshore movements in late autumn (Metbven and Bajkik 1994).
----------------------------------------------------------
Inshore GOM HAPC page 8
Sonic tagged age-3 cod (28-33 cm) rested almost exclusively in rocky areas at night during winter (Clark and Green 1990). Between June and September, however, individuals were active nocturnally and wide ranging (>3 km]day), moving daily between deep (30 m) cold water, where they were inactive in rocky areas, to shallow (<15 m) sandy substratum where they were active at night in relatively small feeding areas (~540-2,580 in2). When the water column became isothermal in September, age-3 cod remained in the shallow water during dayligtit leading researchers to speculate that the switch from nocturnal to diurnal feeding might be an antipredator strategy, i.e., to avoid being cannibalized at night when adult cod are seasonally active in relatively shallow water. Other common predators of juvenile cod off Newfoundland are pollock (Pollachius virens) and shortfinned squid (Jllex illecebrosus).
Spatial Depth Gradient of Juveniles
For three years following stock collapse, Methven and Schneider (1998) undertook extensive sampling of the Newfoundland coastal zone to a depth of 55 m and by a variety of gears. Finding consistent spatial and diel changes in catch across gears, they interpreted results as characteristic of cod distribution. Catch rate of age-0 cod was inversely related to depth each year, highest at night, and higher at 4-7 m, the center of 0-group distribution during autumn. There was a sharp decrease in catch rate at 20 m (Schneider et al. 1997). Demersal age-0 cod were found almost exclusively alongshore within the northeastern coastal bays of Newfoundland; yearlings extended further offshore and older juveniles were widely distributed on the continental shelf confirming an ontogenetic pattern of movement to deeper water with increasing size. Age-dependent distribution was also obvious from trawl station catches on survey transects extending from the coast to hundreds of kilometers offshore (Dailey and Anderson 1997). When the stock was more robust, demersal age-0 cod were distributed more widely onto the shelf.
The only coastal region of eastern Canada where the seasonal pattern of distribution for young cod appears to be different is the coastal portion of southern Gulf of St. Lawrence where water temperatures might be too warm during summer months (Hanson 1996). Fine scale distribution studies with trawls found that cod did not occupy water 2-12 m deep along shores of Pnnce Edward Island during summer. They were mostly absent from shallow waters (<20 m deep) in the Miramichi estuary and the contiguous Shediac Valley coastal shelf during any time of yeat. Yearlings and 2-year-olds, but not age-0 cod, were almost exclusively found in 15-35 m depths of the Gulf from June to early October before joining older age-groups in an extensive migration to deep (>100 m) offshore water for winter.
The spatial depth gradient of juvenile cod from all other areas of eastern Canada seems consistent with published information from the Northeast Atlantic. The depth of highest age-0 cod abundance using a beam trawl off the British Isles was 6 m (Riley and Parnell 1984). Greatest density of age-i cod sampled with gill nets off Greenland was <20 m (Hansen and Lehmann 1986; Hovgard and Nygaard 1990). Acoustic surveys off the Norwegian coast showed most juveniles at depths <35 m and highest densities of demersal 0-group cod very close to rocky shores where the research vessel could not survey (Olsen and Soldal 1989).
Density-dependent Habitat Use and Mortality
Contraction or expansion of geographic range with decreasing or increasing population size has
--------------------------------------------------------------------------------
Inshore GOM HAPC page 9
been observed in a number of cod stocks including the Labrador-East Newfoundland complex and southern Gulf of St. Lawrence stock. In the latter region, the area occupied by age groups 3-8+ cod increased as abundance increased (Swain and Wade 1993). In comparison to the older cod, age-3 were more spatially restricted at low population size, their range expanded more slowly as abundance increased, and changes in relative density among parts of the Gulf were smaller between years of low- and high-abundance. Younger juveniles were thought to experience less severe competitive pressures for food or wider variation in habitat quality than the older age-groups.
A behavioral theory applied to explain the pattern of geographic distribution is density-dependent habitat use. This hypothesis was applied to young cod in coastal habitats (Olsen and Soldal 1989) where catches of post-settlement juveniles showed a high degree of small-scale spatial consistency regardless of cohort size. In years of high year-class abundance, density increases to an upper limit in the most suitable habitat and as the fitness of individuals occupying the prime sites declines due to intraspecific competition, diffusion to and use of suboptimal habitat expands.
Accordingly, at low population size, individuals occupy habitat with high basic foraging and protective suitability.
The theory was tested for the Labrador-East Newfoundland stock complex for which contraction has been confirmed for adult cod at low stock size (Taggart et al. 1994; Atkinson et al. 1997). Catches of age-groups 0-2 were analyzed from 1959-64 and 1992-94 at a series of fixed sampling sites extending over 1,500 miles of Newfoundland coastline (Schneider et al. 1997). In years of low cohort size, contraction did not occur in coastal habitats, i.e., density of juvenile cod was independent of area within the occupied <20 m depth range. They noted that sampling sites with high densities in some years had low densities in years of high abundance, an observation inconsistent with spillover theory in good years.
In support of density-dependent theory, high post-settlement densities of age-0 cod were found in eelgrass beds of Trinity Bay, Newfoundland, during 1994 and 1995, years of good and bad year-classes, respectively; however, a significant increase in abundance in less suitable no-eelgrass habitat was noted in 1994 when settlement strength was high (Grant and Brown 1998a). The high 1994 densities in less-utilized no-eelgrass habitat during a year of high abundance would be consistent with the hypothesis of density-dependent habitat use or selection. The researchers acknowledged that their observations were on a small temporal and spatial scale. Re-analysis of the fixed sampling site juvenile catch data from Newfoundland showed a stronger recruitment signal from a small number of sites visited frequently than the entire set of sites (Lngs et al. 1997). The 1994 year class was ranked significantly stronger than the three previous year-classes following stock collapse in a broad-scale study (Anderson and Dalley 1997). On the other hand, there was no evidence of fewer settled 0-group juveniles anywhere along the coast in 1995 relative to the 1992-94 year-classes (Smedbol et al. 1998).
For a number of cod stocks, variability in year class strength is usually determined in the larval
stage and attenuated by density-dependent juvenile mortality (Myers and Cadigan 1993a).
Biological processes that may result in density-dependent mortality would include:
(1) competition for food with mortality resulting from increased predation or starvation;
(2) intercohort cannibalism; (3) predators switching to abundant year-classes; and (4) a
------------------------------------------------
Inshore GOM HAPC page 10
circumscribed area of prime juvenile habitat with those settling surviving while others do not, resulting in a upper limit to the number of survivors regardless of egg/larval production. This mechanism could involve food limitation and/or increased predation risk outside a prime nursery area. It presumes mechanisms maintaining a relatively constant density such as territorial behavior or some other form of density-dependent habitat utilization.
Notwithstanding the study by Schneider et al. (1997), many of the research results discovered and re-confirmed by scientists undertaking the studies summarized herein, describe or infer habitat mediated density-dependent mortality rates. These mechanisms systematically affect cod survival rates from the post-settlement pelagic stage well into the demersal juvenile stage. Annual variation in survival rates on these life stages may be more important in affecting year class size than survival in pre-settlement stages (Sissenwine 1984). This suggests that the nearshore bottom habitat may become a potential bottleneck to year-class size particularly in areas where the availability of the most suitable habitat might be low.
Summary of Research
In shallow (< 5 m) coastal areas of eastern Canada, pelagic juvenile cod settle onto various subtidal habitats in several periodic pulses beginning in May. Space use is highly localized and primarily focused on the need to acquire food and avoid predators. Relative to fulfilling both needs, activity periods, substrate choices, and interactions with members of same species and others are critical. Diurnal feeding in intercohort schools aids location of patchily distributed plankton and provides protection against predators. Site fidelity and nightly concealment in all habitats, except sand, minimizes interactions with cannibalistic age-i cod that move shoalward at dusk to feed. The spatial pattern of age-0 cod distribution is altered by post-settlement mortality such that abundance among bottom habitats matches substratum complexity: cobble/gravel _rock reef> eelgrass _ macroalgae> sand. Of bottom habitats studied, eelgrass confers a significant advantage in growth to age-0 cod. Significantly reduced predation risk also occurs if eelgrass stems are above a threshold density and/or they are associated with cobble bottom. Eelgrass meadows are highly utilized as nursery habitat both spatially and temporally through at least mid-summer. The transition to a demersal existence occurs at a length of 6-10 cm and is marked by a switch to benthic prey foraged at dawn and dusk.
The distribution of age-0 cod in autumn is centered at depths of 4-7 m MLW with a sharp drop off at 20 m. In late autumn! early winter, age-0 lose site fidelity and disperse to deeper water where they congregate primarily over gravel and low relief cover.
Older juveniles inhabit progressively deeper water and associate with coarser, hard-bottom features as they grow. Seasonal inshore movements are usually associated with nocturnal feeding. the availability of better information about the actual distribution and spatial extent of seagrasses and hard bottom habitats.
Inshore Gulf of Maine Activities
This proposed HAPC would be located entirely within the waters of the states of Maine, New Hampshire and Massachusetts. The only jurisdiction the Council has over activities occurring in this proposed HAPC is for the fishing activities of federal permit holders who also fish in near-shore state waters. Most activities that would occur within the proposed HAPC fall under the management jurisdiction of state agencies.
There are a range of alternatives the Council could consider to minimize the potential adverse impacts of fishing gear and practices within the proposed HAPC. One option would be to impose no additional restrictions on the fishing activities of federal permit holders within this area. At the other end of the range of options, the Council could consider restricting all fishing activity by federal permit holders within this proposed HAPC. The Council could also consider restricting only such fishing activities of federal permit holders that employ bottom-tending mobile fishing gear.
To have a meaningful effect on the activities that may adversely impact the proposed HAPC, it may be necessary for state fishery agencies to restrict the use of certain fishing gears and practices. The Council can make specific recommendations to state fishery agencies and encourage them to protect EFH and HAPCs. Many seemingly benign activities -- ranging from hand raking of bay scallops, which are almost always found in eelgrass beds, to subtidal aquaculture operations -- may require more scrutiny than they have been given to date and the Council could recommend that state fishery agencies consider these activities in light of the importance of this habitat.
Although depths <9 m are rarely fished with large bottom-tending mobile fishing gear, small boat commercial fishermen use dredges to fish for sea scallops and sea urchins. Such gear might be more properly restricted to waters deeper than 9 meters. When nearshore fisheries commenced for these species, they were reported to be initially undertaken by SCUBA divers but now dredging is the most popular method. Hand gathering may be a more appropnate method for harvesting relatively sessile resources in sensitive shallow habitats. The Council could recommend that state fishery agencies consider options to close this shallow coastal zone to some or all bottom-tending mobile fishing gear.
Other traditional fisheries undertaken close to the littoral zone, such as dragging for blue mussels (Mytilus edulus), raking Irish moss (Chondrus crispus), or hand digging quahogs (Mercenaricz mercenaria) may not be a problem based on the substratum occupied. It is possible that these types of activities may be benign to critical habitat for age-O cod.
The Council could consider recommending that state fishery agencies review the potential impacts of these types of activties and, if necessary, consider options to minimize their impacts on the proposal HAPC. Even if no specific measures arc proposed, the HAPC designation would create a higher level of review for non-fishing related activities during the NMFS EFH consultation process.
Age-1 cod, while co-existing in all but the shallowest depths with young-of-the-year, are many times more abundant in the shore zone at night than during the day apparently attracted thereby the presence of periodic influxes of post-larval pelagic juvenile cod. Competitive advantage accrues to the largest and earliest settling juveniles especially those finding coarse substratum with vegetative cover. Those less favored must disperse from feeding patches more often thereby accepting a lower rate of food intake in order to avoid detection and capture. As Tupper and Boutilier (1995b) hypothesized: "one habitat might supply the population with a greater number of smaller recruits, each with a somewhat lesser chance of survival, while another habitat supplies fewer, larger recruits, each with a relatively high chance of survival".
-------------------------------------------------------
Inshore GOM HAPC page 11
The trade-offs between habitat use and frequency of feeding in the face of predation risk are processes consistent with density-dependent habitat use and mortality. Although empirical evidence of density-dependent usage off Newfoundland is contradictory, stock size/recruitment may not yet be large enough following the northern cod stock collapse to induce significant density-dependent effects on a large spatial scale. Nevertheless, behavioral research details ways age-O juveniles respond to spatial heterogeneity, the consequences for fitness through utilization of resources, and the intraspecific competitive effects which emphasizes the importance of habitat availability and quality in determining recruitment success.
Gulf of Maine Coastal Marine Environment and Juvenile Cod Distribution
Coastal Environment
The margin of the Gulf of Maine is similar to the Canadian coastal zone of higher latitudes with the exception that the latter generally has more imposing headlands and bathymetric relief, narrower beaches, and a more steeply sloping shore zone. The coastline of the northern Gulf between Passamaquoddy Bay and Cape Elizabeth, Maine, is also rugged, wave-exposed, and rock-framed. Within hundreds of indented bays and coves are thousands of islands and ledges. The subtidal seafloor is largely hard-bottom (ledge and boulder), often giving way to cobble/gravel, and sediment within <9 m depth. Submerged bedrock outcroppings and rocks provide bathymetric relief and substantial vegetative algal habitats.
From Cape Elizabeth to Cape Cod, the coast is characterized by long sandy beaches, unconsolidated cliffs and bluffs, and occasional rocky headlands, most prominently Cape Ann and Marblehead. With the exception of the headland littoral zone, the nearshore seafloor is generally wave-rippled coarse sand broken occasionally by restricted patches of cobble. Numerous barrier beaches protect estuaries and occasionally extensive salt marshes lying behind them. Along the southern part of the coast, in particular, but near entrances of protected inlets or river deltas, sand may be vegetated with eelgrass meadows. Sublittoral hard bottom relief including sand ripples, troughs, empty shells, worm tubes, motile or sessile invertebrate taxa (e.g., mussels, starfish, urchins, anemones, hydrozoans, bryozoans, ascidians, and sponges) and marine vegetation provides valuable interspersion of cover types for age-O juvenile nurser habitat similar to the nearshore regions of the Canadian maritime provinces. However, unhikç some areas north of the international border, the coastal zone is the only known source of recruits to the Gulf of Maine cod stock.
Juvenile Cod Distribution
For the Gulf of Maine cod stock, the distribution pattern of eggs, larvae, and juveniles has been demarcated along the coast from eastern Maine to Cape Cod; hence, the western perimeter of the Gulf has been designated EFH for these life stages (NEFMC 1998). The EFH designation for juveniles (<35 cm) was based on presence/absence as identified by several sources: NMFS and MDMF inshore bottom trawl surveys (1963-97 and 1978-97, respectively), NMFS MARMAP ichthyoplankton survey (1977-87), and NOAA's Estuarine Living Marine Resources (ELMR) program encompassing abundance records for 13 major bays and harbors and four river systems. Results from additional, less systematic or more spatially restricted coastal sampling efforts (the basis for ELMR classifications with some exceptions) are now being compiled and should reveal more complete information on cod distribution. A pertinent example is the notation that juvenile Atlantic cod were seined only at night from eelgrass meadows of Nauset Harbor, Cape Cod. (Heck etal. 1989).
--------------------------------------------------------------------
Inshore GOM HAPC page 12
The mapped EFH designations mirror the long held knowledge that inshore waters are principal habitat for juvenile cod. The distribution ofjuvenile cod observed in the latter half of 19th century and early part of this century was summarized by Bigelow and Schroeder (1953). They described young-of-the-year cod living in very shoal water to the littoral zone, and small, presumably one-year-olds, along the coast within two fathoms (~4 m) in summer.
From the contemporary NMFS trawl survey catch in the Southern New England-Georges Bank region, water temperature was determined to be a factor in explaining interseasonal spatial and depth distribution of age-1-4 cod. However, water temperatures were insufficient to explain distributional differences among age classes (Wigley and Serchuk 1992). From a slightly earlier time series of research vessel catches in the Gulf of Maine, as well as collections on Georges Bank and Southern New England, Wigley and Gabriel (1991) noted juvenile (<37 cm) cod inhabiting a mean depth of 62 m in the spring and 75 m in the autumn with seasonal occurrence at minimum depths of about 9 m in both seasons. Within the Gulf of Maine, juvenile concentrations occurred between Jeffrey's Ledge and Cape Cod in spring and were more restricted to Massachusetts Bay in fall. Lower densities of juveniles also occurred all along the 100 m isobath off New Hampshire! Maine coast during both seasons. However, the NMFS survey completes relatively few stations nearshore in the northern part of the Gulf due to the rough bottom habitats that are untrawlable with traditional survey gear.
.The most southern inshore portion of the Gulf of Maine is more accessible to research vessels and has been covered by the MDMF survey. The occurrence of juvenile cod (<35 cm) matched all temperatures (<130C) and depths sampled in spring (5-80 in), but during fall surveys, young cod tended to occur at deeper (15-50 m) and cooler (<170C) sampling stations. The juvenile cod catch per tow was highest along the north shore of Massachusetts Bay and Cape Ann! Ipswich Bay in spring (500-1,765 fish/tow) and fall (500-2,925 fish/tow), as well as the tip of Cape Cod in spring (200-500 fish/tow), and throughout Cape Cod Bay in fall (500-2,925 fish/tow) (NEFMC 1998). Age-groups 0 and 1 cod predominate in the fall survey with the highest densities of 0-group cod usually occurring at alongshore stations, catches invariably associated with bycatch of live bottom material [e.g., sulphur sponge (Cliona), kelp, spaghetti grass (Codium), and eelgrass (A. Howe, pers. comm.)].
Status of Eelgrass
The presence of eelgrass beds may be an equally important factor influencing distribution and abundance of post-settled cod juveniles in the Gulf of Maine as documented in the Canadian maritime provinces and certain countries bordering the Northeast Atlantic. However, eelgrass has been in general decline in U.S. coastal regions for over half a century. There are multiple stressors and disturbances contributing to loss of eelgrass acreage (Short et al. 1987, Muehlstein and Porter 1991; Nixon 1995). Wasting disease caused by the pathogenic marine slime mold, Labyrinthua sp. Nov. is responsible for epidemic losses a half century ago and has re-occurred in some areas. In many estuaries and coastal areas, sediment loading (turbidity) from the watershed and increased anthropogenic nitrogen loading (eutrophication) via groundwater has stimulated algal competitors that shade and stress plants and significantly reduce stem density and depth of the plants. Fishing gear that cuts shoots has also been implicated.
--------------------------------------------------------------------------
Inshore GOM HAPC page 13
Because eelgrass is sensitive to variations in water quality from watershed-level impacts, it is considered an indicator of ecosystem state (Dennison et al. 1993). Whereas once large eelgrass meadows colonized much of the shallow water of Boston Harbor, they are now restricted to a few, small patches (Colarusso et al. in press). Airborne remote sensing, field observations, and GIS technology are being used to find and map eelgrass meadows in nearshore habitats of the Gulf of Maine.
In comparison to other estuarine nursery habitats measured, species richness, macroinvertebrate biomass, and primary production is significantly higher in eelgrass. Its loss and subsequent changes in food web structure (McClelland and Valiela 1998) has not only resulted in foregone predator (benthic fish, lobster, and large shellfish) biomass (Heck et al. 1995), but also lost habitat complexity and diminished sediment stability. It is thought that some recolonization of former eelgrass meadows will occur slowly if nitrogen loading is reduced (Duarte 1995). Protecting eelgrass habitat should be an high priority with respect to conservation of coastal nurseries for Atlantic cod (Gotceitas et al. 1997).
Utilization of Proposed HAPC by American Lobster and other Multispecies Groundfish The American lobster (Homarus americanus) is New England's largest single-species fishery and its most valuable. The life stage distribution relative to nearshore habitats of coastal lobster populations has been well documented. Densities tend to be at least two orders of magnitude higher on hard bottoms than on sediment habitat. Lobster larvae settle in shallow subtidal or low intertidal cobble! gravel! pebble substrates, and like post-settlement cod, are very susceptible to predation. These hard-bottom patches support high densities of one and two-year-olds (<40 mm CL) because of the protection afforded by the interstitial spaces (Wahle and Steneck 1992). No studies have detected early benthic stages (<10 mm CL) on featureless sediment (Wahle 1993). As lobsters outgrow the early benthic phase, they become increasingly mobile on nearshore sediment habitat. The research trawl catch of sublegal (3 0-82 mm CL) lobster alongshore at depths _9 m may reach 4,000 lobsters (13 bu) in tow times of less than 20 minutes in MDMF bottom trawl surveys (A. Howe, pers. comm.).
Among other multispecies groundfish, it is well known and corroborated by scientific information that winter flounder spend their first two years of life in very shallow coastal w~.ter co-occurring with young cod throughout the northern part of their range. While they are commonly reported occupying unvegetated substrates in Canada and New England, eelgrass meadows also serve as nurseries for winter flounder as well as white hake, Urophycis tenuis (Heck et al. 1989).
Conclusion
Although Atlantic cod adults are depleted in the Gulf of Maine, some recruitment will continue to occur because density-dependent effects will increase juvenile survival rates at low abundance (Myers and Cadigan 1 993b). Unfortunately, recruitment at low spawner abundance happens at greatly reduced levels for cod (Myers and Barrowman 1996). Recognizing critical habitat (e.g., nearshore cobble patches and eelgrass beds), and protecting it from anthropogenic impacts by risk-adverse management measures should improve juvenile survivorship.
----------------------------------------------------------------
Inshore GOM HAPC page 14
Inshore Gulf of Maine HAPC
Based on the information presented on juvenile Atlantic cod and the inshore areas of the Gulf of Maine, the EFH Technical Team suggests that the areas identified in this report and on Figure 1 meet the criteria for designation as an HAPC. A coastal L-IAPC designation would be justified on the criteria of ecological function and sensitivity to induced environmental degradation. An IIAPC designation for the nearshore Gulf of Maine could assist in the enhancement of Atlantic cod, American lobster, and other groundfish species, such as winter flounder and white hake. Potential measures to protect this proposed HAPC are discussed below.
The most practical approach for delineating an HAPC for settled age-0 cod is to circumscribe the reported center of distribution for this life stage throughout the range of the stock. The information available suggests that the HAPC should be from the low tide line to a depth of 9 m (30') MLW from eastern Maine to Cape Cod, Massachusetts, conforming to the center of distribution (4-7 in). This narrow depth range describes critical habitat from settlement (<5m) through the first autumn of life and overlaps seasonal babitat of age-i juvenile cod. It also bounds the critical nursery zone for early benthic stages of American lobster as well as important juvenile habitat for some other groundfish. Consideration of a more encompassing HAPC to the depth range occupied by most age-0 cod would involve extending the isobath to at least the 20 m (66') and might be unjustiflably exclusionary to mobile gear fisheries conducted on sandy seafloor seaward of hard bottom habitat and generally >10 m, should these gears be restricted with the proposed HAPC.
The HAPC proposal should be somewhat flexible to allow modification as results from additional research and fine-scale resource mapping become available. For example, drawing a mean low water boundary of HAPC is problematic given knowledge that eelgrass beds may extend well inside embayments and river deltas, so drawing a shoreline boundary crossing from headland to headland versus across arbitrary points farther up estuary or river is initially convenient. Fine-scale mapping of most important habitat components might resolve the above dilemma and afford more localized protection to the most sensitive habitat components. It also could result in more permitted activities within the proposed HAPC zone.
Future information could also prompt consideration of extending the HAPC into contiguous waters east of Cape Cod and south of Nantucket and Martha's Vineyard into Buzzards Bay. For assessment purposes, cod inhabiting this area are considered part of the Georges Bank stock. Settled age-0 cod are taken nearshore in May by the Massachusetts DMF trawl survey (NEFMC 1998). There is no information on whether or not these fish survive the summer. They do not re-occur at larger size on later inshore surveys but that does not mean that the southern shore zone does not serve an important role relative to recruitment for the Georges Bank stock.
With consideration of the above caveats, the EFH Technical Team suggests that the Habitat Committee consider designating an HAPC for subtidal age-0 Atlantic cod, within the existing juvenile Atlantic cod EFH designation, from MLW to 9 in (30') below MLW extending from the international border with Canada southwestward along the entire western perimeter of the Gulf of Maine to Race Point, Provincetown, Massachusetts, including subtidal bottom to 9 m below MLW around all coastal islands. This designation could be refined at a later date, depending on
-------------------------------------------------------
Inshore GOM HAPC page 15
the availability of better information about the actual distribution and spatial extent of seagrasses and hard bottom habitats.
Inshore Gulf of Maine Activities
This proposed HAPC would be located entirely within the waters of the states of Maine, New Hampshire and Massachusetts. The only jurisdiction the Council has over activities occurring in this proposed HAPC is for the fishing activities of federal permit holders who also fish in near-shore state waters. Most activities that would occur within the proposed HAPC fall under the management jurisdiction of state agencies.
There are a range of alternatives the Council could consider to minimize the potential adverse impacts of fishing gear and practices within the proposed HAPC. One option would be to impose no additional restrictions on the fishing activities of federal permit holders within this area. At the other end of the range of options, the Council could consider restricting all fishing activity by federal permit holders within this proposed HAPC. The Council could also consider restricting only such fishing activities of federal permit holders that employ bottom-tending mobile fishing gear.
To have a meaningful effect on the activities that may adversely impact the proposed HAPC, it may be necessary for state fishery agencies to restrict the use of certain fishing gears and practices. The Council can make specific recommendations to state fishery agencies and encourage them to protect EFH and HAPCs. Many seemingly benign activities -- ranging from hand raking of bay scallops, which are almost always found in eelgrass beds, to subtidal aquaculture operations -- may require more scrutiny than they have been given to date and the Council could recommend that state fishery agencies consider these activities in light of the importance of this habitat.
Although depths <9 m are rarely fished with large bottom-tending mobile fishing gear, small boat commercial fishermen use dredges to fish for sea scallops and sea urchins. Such gear might be more properly restricted to waters deeper than 9 meters. When nearshore fisheries commenced for these species, they were reported to be initially undertaken by SCUBA divers but now dredging is the most popular method. Hand gathering may be a more appropnate method for harvesting relatively sessile resources in sensitive shallow habitats. The Council could recommend that state fishery agencies consider options to close this shallow coastal zone to some or all bottom-tending mobile fishing gear.
Other traditional fisheries undertaken close to the littoral zone, such as dragging for blue mussels (Mytilus edulus), raking Irish moss (Chondrus crispus), or hand digging quahogs (Mercenaria mercenaria) may not be a problem based on the substratum occupied. It is possible that these types of activities may be benign to critical habitat for age-O cod.
The Council could consider recommending that state fishery agencies review the potential impacts of these types of activties and, if necessary, consider options to minimize their impacts on the proposal HAPC. Even if no specific measures arc proposed, the HAPC designation would create a higher level of review for non-fishing related activities during the NMFS EFH consultation process.
---------------------------------------------------------
Inshore GOM HAPC page 16
New England Fishery Management Council
Essential Fish Habitat
Proposed Inshore Gulf of Maine Juvenile Atlantic Cod Habitat Area of Particular Concern
IMAGE
This map displays the area proposed for Habitat Area of Particular Concern (HAPC) designation. Within the existing boundaries of EFH for juvenile Atlantic cod, the HAPC proposal could include all areas of the perimeter of the Gulf of Maine, from the mean low water (MLW) mark out to the 10 meter isobath. A text description of the HAPC designation could specify the particular habitat types that are either included or excluded from the designation.
---------------------------------------------------------
Inshore GOM HAPC page 17
Literature Cited
Anderson, J.T. and E.L. Dailey. 1997. Spawning and year-class strength of northern cod (Gadus morhua) as measured by pelagic juvenile cod surveys, 1991-1994. Can. J. Fish. Aquat. Sd. 54(Suppl. 1): 158-167.
Atkinson, D.B., Rose, G.A., Murphy, E.F., and C.A. Bishop. 1997. Distribution changes and abundance of northern cod (Gadus morhua), 1981-1993. Can. J. Fish. Aquat. Sci. 54(Suppl. 1):132-138.
Brown, J.A., Pepin, P., Methven, D.A. and D.C. Somerton. 1989. The feeding, growth and behavior of juvenile cod, Gadus morhua L., in cold environments. J. Fish. Biol. 35:373-380.
Bigelow, H.B. and W.C. Schroeder. 1953. Fishes of the Gulf of Maine. U.S. Fish Wildl. Serv., Fish. Bull. 53:1-577.
Bogstad, B., Lilly, G.R., Mehl, S., Palsson, O.K., and G. Stefansson. 1994. Cannibalism and year-class strength in Atlantic cod (Gadus morhua) in Arcto-boreal ecosystem (Barents Sea, Iceland, and eastern Newfoundland. ICES Mar. Sci. Symp. 198:576-594.
Campbell, J.S. 1997. Introduction to the Northwest Atlantic cod symposium. Can. J. Fish. Aquat. Sci. 54(Suppl. 1):1
Clark, D.S. and J.M. Green. 1990. Activity and movement patterns ofjuvenile Atlantic cod, Gadus morhua, in Conception Bay, Newfoundland as determined by sonic telemetry. Can. J. Zool. 68:1434-1442.
Dailey, E.L. and J.T. Anderson. 1997. Age-dependent distribution of demersal juvenile Atlantic cod (Gadus morhua) in inshore! offshore northeast Newfoundland. Can. J. Fish. Aquat. Sci. 54(Suppl. 1): 168-176.
Dennison, W.C., Orth, R.J., Moore, R.A., Stevenson, J.C., Carter, V., Kollar, S., Bergstrom, P.W., and R.A. Batiuk. 1993. Assessing water quality with submersed aquatic vegetation. Bioscience 43:86- 94.
Duarte, C.M. 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41:87- 112.
Fraser, S., Gotceitas, V. and l.A. Brown. 1996. Interactions between age-classes of Atlantic cod and their ~istribution among bottom substrates. Can. J. Fish. Aquat. Sci. 53:305-314.
Gibson, R.N., Robb, L., Barrows, M.T., and A.D. Ansell. 1996. Tidal, diel and longer term changes in the distribution of fishes on a Scottish sandy beach. Mar. Eco!. Prog Ser. 130:1-17.
Goddard, S.V., Kao, M.H., and G.L. Fletcher. 1992. Antifreeze production, freeze resistance, and overwintering ofjuvenile northern Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sd. 49:516- 522.
Gotceitas, V. and l.A. Brown. 1993. Substrate selection by juvenile Atlantic cod (Gadus morhua): effects of predation risk. Oecologia 93:31-37.
Gotceitas, V., Fraser, S. and l.A. Brown. 1995. Substrate selection by juvenile Atlantic cod in the presence of an actively foraging and non-foraging predator. Mar. Biol. 123:421-430.
Gotceitas, V., Fraser, S. and l.A. Brown. 1997. Use of eelgrass (Zostera marina) by juvenile Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 54:1306-1319.
Grant, S.M. and l.A. Brown. 1998a. Diel foraging cycles and interactions among juvenile Atlantic cod (Gadus morhua) at a nearshore site in Newfoundland. Can. J. Fish. Aquat. Sci. 55:1307-1316.
----------------------------------------------------
Inshore GOM HAPC page 18
Grant, S.M. and J.A. Brown. 1 998b. Nearshore settlement and localized populations of age-0 Atlantic cod (Gadus morhua) in shallow coastal waters of Newfoundland. Can. J. Fish. Aquat. Sci. 55:13 17-1327.
Gregory, R.S. and J.T. Anderson. 1997. Substrate selection and use of protective cover by juvenile Atlantic cod Gadus morhua in inshore waters of Newfoundland. Mar. Ecol. Prog. Ser. 146:9-20.
Gregory, R.S., Anderson, J.T. and E.L. Dailey. 1997. Distribution of juvenile Atlantic cod (Gadus morhua) relative to available habitat in Placentia Bay, Newfoundland. NAFO Sci. Coun. Studies 29:3-12.
Hansen, H.H., and K.M. Lehmann. 1986. Distribution of young cod in coastal regions of west Greenland, 1985. NAFO 5CR. Doc. 86/42 Ser. No. NI 158.
Hanson, J.M. 1996. Seasonal distribution of juvenile Atlantic cod in the southern Gulf of St. Lawrence. J. Fish. Biol. 49:1 138-1152.
Heck, K.L.,Jr., Able, K.W., Fahey, M.P. and C.T. Roman. 1989. Fishes and decapod crustaceans of Cape Cod eelgrass meadows: species composition, seasonal abundance patterns and comparisons with unvegetated substrates. Estuaries 12:59-65.
Heck, K.L. and L.B. Crowder. 1991. Habitat structure and predator-prey interactions in vegetated aquatic systems. In Habitat structure: the physical arrangement of objects in space. Edited by S.S. Bell, E.D. McCoy, and H.R. Mushinsky. Chapman and Hall, New York. pp. 282-299.
Heck, K.L., Jr., Able, K.W., Roman, C.T. and M.P. Fahey. 1995. Composition, abundance, biomass, and production of rnacrofauna in a New England estuary: comparison among eelgrass meadows and other nursery habitats. Estuaries 1 8(2):379-3 89.
Home, J.K. and S.E. Campana. 1989. Environmental factors influencing the distribution of juvenile groundfish in nearshore habitats of southwest Nova Scotia. Can. J. Fish. Aquat. Sci. 46:1277-1286.
Hovgard, H.H. and K.H. Nygaard. 1990. Young cod distribution and abundance in west Greenland inshore areas, 1989. NAFO 5CR. Doe. 90/30 Ser. No. Nl747.
Hutchings, J.A. 1996. Spatial and temporal variation in the density of northern cod and a review of hypotheses for the stock's collapse. Can. J. Fish. Aquat. Sci. 53:943-962.
Ings, D.W., Schneider, D.C., and D.A. Methven. 1997. Detection of a recruitment signal in juvenile Atlantic cod (Gadus morhua) in coastal nursery areas. Can. J. Fish. Aquat. Sci. 54(Suppl. 1):25-29.
Isaksson, I., Pihl, L. and J. vanMontfrans. 1994. Eutrophication-related changes in macrovegetatiofl and foraging of young cod (Gadus morhua L.): a mesocosm experiment. J. Exp. Mar. Biol. Ecol. 177:203-217.
Keats, D.W. 1990. A nocturnal inshore movement of juvenile cod Gadus morhua L. in eastern Newfoundland. J. Exp. Mar. Biol. Ecol. 139:167-173.
Keats, D.W., Steele, D.H., and G.R. South. 1987. The role of fleshy macroalgae in the ecology of juvenile cod (Gadus morhua L.) in inshore waters off eastern Newfoundland. Can. J. Zool. 65:49-53.
Keats, D.W. and D.H. Steele. 1992. Diurnal feeding of juvenile cod (Gadus morhua) which migrate into shallow water at night in Eastern Newfoundland. J. Northw. Atl. Fish. Sd. 13:7-14.
Lomond, T.M., Schneider, D.C., and D.A. Methven. 1998. The transition from pelagic to benthic prey of 0-1 group Atlantic cod. Fish. Bull. 96:908-911.
Lough, R.G., Valentine, P.C., Potter, D.C., Auditore, P.J., Bolz, G.R., Neilson, J.D., and R.P. Perry. 1989. Ecology and distribution of juvenile cod and haddock in relation to sediment type and bottom currents on eastern Georges Bank. Mar. Ecol. Prog. Ser. 56:1-12.
-----------------------------------------------
Inshore GOM HAPC page 19
MacDonald, J.S., Dadswell, M.J., Appy, R.J., Melvin, G.D., and D.A. Methven. 1984. Fishes, fish assemblages, and their seasonal movements in the lower Bay of Fundy and Passamaquoddy Bay, Canada. Fish. Bull. 82(1): 121-140.
McClelland, J.W. and I. Valiela. 1998. Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries. Mar. Ecol. Prog. Ser. 168:259-271.
Methven, D.A., and C. Bajdik. 1994. Temporal variation in size and abundance of juvenile Atlantic cod (Gadus morhua) at an inshore site off eastern Newfoundland. Can. J. Fish. Aquat. Sci. 51:78-90.
Methven, D.A. and D.C. Schneider. 1998. Gear-independent patterns of variation in catch of juvenile Atlantic cod (Gadus morhua) in coastal habitats. Can. J. Fish. Aquat. Sci. 55:1430-1442.
Muehlstein, L.K. and D. Porter. 1991. Labyrinthula zosterae sp. Nov. the causative agent of wasting disease of eelgrass, Zostera marina. Mycologia 83(2): 180-191.
Myers, R.A. and N.J. Barrowman. 1996. Is fish recruitment related to spawner abundance? Fish. Bull. 94:707-724.
Myers, R.A. and N.C. Cadigan. 1993a. Density-dependent juvenile mortality in marine demersal fish. Can. J. Fish. Aquat. Sd. 50:1576-1590.
Myers, R.A. and N.C. Cadigan. 1993b. Is juvenile natural mortality in marine demersal fish variable? Can. J. Fish. Aquat. Sci. 50:1591-1598.
Myers, R.A., Hutchings, l.A. and N.J. Barrowman. 1996. Hypotheses for the decline of cod in the North Atlantic. Mar. Ecol. Prog. Ser. 13 8:293-308.
NEFMC. 1998. Omnibus essential fish habitat amendment to fishery management plans. Saugus, MA.
NEFMC's Multispecies Monitoring Committee. 1998. Report of the New England Fishery Management Council's Multispecies Monitoring Committee. Dee, 1998.
NEFSC [Northeast Fisheries Science Center]. 1997. Report of the 27th Northeast Regional Stock Assessment Workshop (27th SAW) Consensus summary of Assessments.
Nixon, S.W. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41:199-219.
Olsen, S. and A.V. Soldal. 1989. Observations on inshore distribution and behaviour of 0-group northeast Arctic cod. Rapp. P.-v. Reun. Cons. mt. Explor. Mer., 191:296-302.
Orth, R.J., Heck, K.L., and 1. vanMontfrans. 1984. Faunal communities in seagrass beds: a review cff the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7:339- 350.
Perry, R.I. and J.D. Neilson. 1988. Vertical distributions and trophic interactions of age-0 Atlantic cod and haddock in mixed and stratified waters of Georges Bank. Mar. Ecol. Prog. Ser. 49:199-214.
Pinsent, D.L. and D.A. Methven. 1997. Protracted spawning of Atlantic cod (Gadus morhua) in Newfoundland waters: evidence from otolith microstructure. Can. J. Fish. Aquat. Sc 54(Suppl. 1): 19-24.
Riley, J.D. and W.G. Pumell. 1984. The distribution of young cod. In The propagation of cod, Gadus morhua L. Edited by E. Dahl, S.S. Danielssen, E. Moksness, and P. Solemdal. Flod. Rapp. 1:563-580. (ISSN 0333-2594).
Schneider, D.C., Methven, D.A., and E.L. DaIley. 1997. Geographic contractions in juvenile fish: a test with northern cod (Gadus morhua) at low abundances. Can. J. Fish. Aquat. Sci. 54(Suppl. 1): 187-199.
------------------------------------------------------------
Inshore GOM HAPC page 20
Short, F.T., Muehlstein, L.K. and D. Porter. 1987. Eelgrass wasting disease: cause and recurrence of a marine epidemic. Biol. Bull. 173:557-562.
Sissenwine, M.P. 1984. Why do fish populations vary? In Exploitation of marine communities. Edited by R.M. May. Springer-Verlag, Berlin. pp. 59-94.
Smedbol, R.K., Schneider, D.C., Wroblewski, J.S. and D.A. Methven. 1998. Outcome of an inshore spawning event by northern Atlantic cod (Gadus morhua) at a low stock level. Can. J. Fish. Aquat. Sci. 55:2283-2291.
Sogard, S.M. 1989. Colonization of artificial seagrass by fishes and decapod crustaceans: importance of proximity to natural eelgrass. J. Exp. Mar. Biol. Ecol. 133:15-38.
Swain, D.P. and E.J. Wade. 1993. Density-dependent geographic distribution of Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence. Can. J. Fish. Aquat. Sci. 50:725-733.
Taggart, C.T., Anderson, J., Bishop, C., Colbourne, E., Hutchings, J., Lilly, G., Morgan, J., Murphy, E., Myers, R., Rose, 1., and P. Shelton. 1994. Overview of cod stocks, biology, and environment in the Northwest Atlantic region of Newfoundland with emphasis on northern cod. ICES Mar. Sci. Symp. 198:140-157.
Tupper, M. and R.G. Boutilier. 1995a. Size and priority at settlement determine growth and competitive success of newly settled Atlantic cod. Mar. Ecol. Prog. Ser. 118:295-300.
Tupper, M. and R.G. Boutilier. 1 995b. Effects of habitat on settlement, growth, and postsettlemeflt survival of Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 52:1834-1841.
Tyler, A.V. 1971. Surges of winter flounder, Pseudopleuronectes americanus, into the intertidal zone. J. Fish. Res. Bd. Canada 28(1 1): 1727-1731.
Wahle, R.A. 1993. Recruitment to American lobster populations along an estuarine gradient. Estuaries 1 6(4):73 1-73 8.
Wahle, R.A. and R.S. Steneck. 1992. Habitat restrictions in early benthic life: experiments in substratum selection and in situ predation with the American lobster. J. Exp. Mar. Biol. and Ecol. 157:91-114.
Wigley, S.E. and W.L. Gabriel. 1991. Distribution of sexually immature components of 10 Northwest Atlantic groundfish species based on Northeast Fish. Center bottom trawl surveys, 1968-86. NOAA Tech. Memo. NMFS-F/N7EC-80: 17p.
Wigley, S.E. and F.M. Serchuk. 1992. Spatial and temporal distribution of juvenile Atlantic cod Gadus morhua in the Georges Bank-Southern New England region. Fish. Bull. 90:599-606.
---------------------------------------------------------------------
END