Effects of habitat on settlement growth and postsettlement surviva

antic cod Gadus morhua

M Tupper and RC Boutilier

Abstract Settlement and growth of age 0+ cod were monitored using snorkel and self-contained underwater breathing apparatus (SCUBA) in four distinct habitat types (sand seagrass cobble and rock reef) in St Margarets Bay Nova Scotia Newly settled cod were marked with acrylic dye allowing repeated visual length estimates of individual fish Settlement of cod did not differ between habitat types but postsettlement survival and subsequent juvenile densities were higher in-more structurally complex habitats These differences appear to be due to increased shelter availability and decreased predator efficiency in structurally complex habitats Growth rate was highest in seagrass beds while the efficiency sf cod predators was lowest and cod survival was highest om rocky reefs and cobble bottoms Thus trade-offs occur between energy gain and predation risk In St Margarets Bay the population structure of Atlantic cod may be less influenced by patterns of larval supply than by postsettlement processes such as habitat-specific growth and mortality

RdsnmC Nous avons surveil16 la colonisation et la croissance de morues d8ge 0+ en plong6e autonome et avec masque et tube dans quatre types diffdrents dhabitats (sable herbier galets rCcifs rocheux) dans la baie St Margarets en Nouvelle-ficosse kes morues nouvellement instalH6es dtaient marqukes avec une peinture acrylique ce qui a permis de mesurer visuellement de f a ~ o n rCpCt6e la longueur des psisssns pris individuellement Le mode de colonisation ne diffkrait pas dun habitat B Iautre mais la survie aprks installation et la densit6 des juvdniles par la suite Ctaient plus 6levCes dans les habitats structurellement plus complexes Ces diffdrences semblent dues h une plus grande disponibilitk des abris et B une efficacitd plus faible des prkdateurs dam les habitats structurellement complexes Le taux de croissance Ctait au plus haut dans les herbiers tandis que 19efficacirC des prkdateurs de Ia rnorue Ctait au plus bas et la survie des poissons au plus haut sur les rkcifs rocheux et Hes fonds de galets IH sq6tablit donc des compromis entre le gain dCnergie et le risque de prCdation Dans la baie St Margarets la structure de la population de morane franche sernble Ctre moins tributaire du rCgirne dapport de larves que des processus post-colonisation comme la croissance et la mortalirk specifiques B un habitat [Tsaduit par la Rcdaction]

lntroduetion

Variability in the survival of early life-history stages of fish is proposed to be a major factor limiting the size of adult populations While studies s f recruitment variability have largely focused on survival of planktonic larvae (Doherty 1982 1983 Victor 1983 1986 Doherty and Fowler 1994 Williams et al B994) recent evidence has pointed to early juvenile survivorship as an important con- tributor to recruitment variation (Hunt von Herbing and

Received March 25 1994 Accepted March 24 1995 312316

M fippecl Department of Biology Dalhousie University Halifax NS B3H 411 Canada RG Boutilier Department of Zoology University of Cambridge Downing Street Cambridge UK CB2 3EJ

Author to whom correspondence should be sent at the following address Bellairs Research Institute of McGill University Holetown St James Barbados

Hunte 199 1 Jones 199 1 Malloy and Targett 199 1 de Lafsntaine et al 1992 Tupper and Hunte 1994 Tupger and Boutilier 1995) However little is known about the processes regulating settlement and survival s f age Q + (first-year juvenile) fish in northern marine ecosystems

Spatial variation in demersal fish recruitment is often perceived as habitat selection particularly when recruitment to a specific habitat is dispropoflisnately high relative to the abundance of that habitat (Carr 1991) While some fish species may actively select specific microhabitats at settle- ment (Sale et al 1984) recruitment variation m s n g habitats may result from a number of factors (i) arnong-habitat variation in the availability of presettlernent larvae (ii) dif- ferential availability of shelter from predation ie habitat complexity (Shulman 1985 Behrents 1987 Hixsn and Beets 1989 C a n 19941 or (iii) agonistic interactions with conspecifics or competitors (Sweatman 1985 1988) Pre- dation efficiency of piscivorcsus predators has been shown to decrease with increasing habitat complexity (Mattila 1992) Thus habitats characterized by high substrate complexity

Can J Fish Aquat Ssi 52 1834-1841 (1895) Printed in Canada Imprim6 au Canada

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Tupper and B~blPilier

should favour postsettlement survival through decreased predation pressure

The high mortality rates typically associated with psst- settlement juveniles are thought to be primarily due to predation (Houde 1987) Many piscivorous fishes select smaller size-classes (Juanes 1994) In addition overwinter survival of young-of-the-year fish in northern climates is generally higher in larger individuals (Walsh 1987 Henderson et al 1988) Thus rapid growth sf newly settled fish may confer a selective advantage both physiologically and in terms of reduced predation risk In general we should expect higher survival rates in those habitats provid- ing the greatest potential for growth However conflicts in habitat selection may occur if those habitats providing maximum growth are not also those that provide the max- imum amount of shelter from predation (Sogard 1992) In such cases high predation risk may force newly settled fish into habitats that do not optimize growth or alterna- tively insufficient food abundance may force newly settled fish into a habitat where the risk of predation is significantly higher

Studies of these effects of habitat on the demography of juvenile fishes have focused mainly on reef-associated species (eg Sale et al 1984 Carr 1991 Connell and Jones 1991 Levin 199 1 1993) Indeed much of what is known about the recruitment dynamics of demersal marine fishes stems from studies of coral reef fishes In this paper we applied a sampling approach typical of reef fish studies to the juvenile demographics of the Atlantic cod (Gadus morhua) a key commercial species in the temperate North Atlantic region We compared settlement growth and post- settlement survival of individually tagged age 0 + Atlantic cod in four distinct habitat types In addition we measured the density and capture success of predators on juvenile cod in each habitat The goal of the study was to answer the following questions ( i ) Do settlement growth and survival of age 0+ cod vary among habitat types (It) Do predator densities and capture success rates influence survival of age O+ cod in each habitat (iii) Is the among-habitat pat- tern of settlement preserved in the juvenile population or modified by mortality and (or) emigration

Methods

Study locations The study was conducted at three locations along the shore of St Margarets Bay Nova Scotia The nearshore bottom of St Margarets Bay can be divided into four broad habitat types rocky reef (characterized by bedrock strewn with large granitic boulders) cobble bottom seagrass (Zostera marina) beds and sand bottom Macroalgae were scarce at these sites owing to herbivorous grazing by the sea urchin Strongg~locentrotkes drobachieresks Rocky reefs were typically covered by crustose algae and (or) a short turf of filamentous algae neither of which would provide suitable shelter for juvenile cod

At each location four 15-m transect lines were laid in each of the four habitat types (is 16 transectsllocation) AH1 transects were within 180 m of shore at a depth of 15-2 m (mean low tide) The substrate mgosity (a measure of habitat complexity see Chandler et al 1985) of each

transect site was estimated by fitting a fine-link brass chain to the bottom contours along the transect Iine The total distance covered by the chain was then divided by 15 m (the horizontal distance covered by the transect line) pro- ducing an index of substrate rugosity It is important to note that substrate rugosity is simply a measure of the actual surface area of bottom structure available to an organism and does not account for other possible shelter sites such as that provided by seagrasses However even in dense seagrass beds newly settled cod in this study were not closely associated with vegetation but sought refuge within the interstices of rocks shells and other hard bottom (M Tupper personal observations)

Census techniques Visual censuses of juvenile cod abundance were conducted at roughly 10-day intervals from May B to July 1 1992 by snorkelling slowly along the transect lines and counting all cod within 1 rn on either side of the transect line (30 m2 planar surface area) Settlement was measured as the mean number of newly settled cod on the four transect lines at each transect site Newly settled cod were recognizable as being 4 0 mm in total length and having a barred pig- mentation pattern and a silvery underbelly This pattern slowly fades until the adult pigmentation is assumed at 1-2 weeks postsettlement (M Tupper personal observa- tions) Newly settled cod were anaesthetized in situ using a 10 solution of Quinaldine in seawater The total length of each animal was measured to the nearest millimetre with a 100-mrn plastic ruler and the animal was then marked with injections of acrylic paint using a specific pattern of dots to identify individuals This allowed marked individuals to be recognized as prior residents in subsequent censuses and allowed growth mortality and emigration to be quantified at each site The length of each fish was estimated visually at each census using a clear plastic ruler fastened to the end of a 60 cm length of wooden dowel The procedure was facilitated by the behaviour of young- of-the-yea cod which tend to flatten themselves against the substrate and remain immobile when approached This technique was accurate to k39 rnm for cod under 180 rnm in totaH length (Tupper and Boutilier 1995) Individual growth rates of tagged fish were calculated as the increase in total length divided by the number of days since the previous study in July divided by the total number of set- tlers tagged on that transect Individual growth rates of tagged fish were calculated as the increase in total length divided by the number of days since the previous measure- ment Continuous water temperature records were not avail- able for the specific study sites but were available from an aquaculture site at the head of St Margarets Bay approx- imately 2 km from the study sites Water temperatures on each transect were recorded immediately following a census with a mercury thermometer

Predation Observations of predation by other fishes on juvenile cod were made in situ at roughly 10-day intervals from mid-May to early July 1992 at each transect site The observer floated motionless above the site while recording the species and number of predators the number of attempted strikes

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1836

Fig 1 Temporal variation in settlement of age 8-4- cod to different habitat types (rocky reef cobble bottom seagrass beds and sandy bottom) at three sites in St Margarets Bay Nova Scotia Error bars represent k1 standard deviation

BACK COVE

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MILL COVE

-5 L I I I i I I 1 April May June July

Month I - postsettlemerat period - (

(lunges at a juvenile cod) and the number of successful strikes (capture and ingestion of a juvenile cod) over a I-h

eriod An index of capture success was then calculated by dividing the number of successful strikes by the total number of strikes for each of the four habitat types Mean capture success in each habitat was calculated as the average capture success over the six observation periods Predation was initially observed at dawn in the afternoon at dusk and at night However the time of observation appeared to have no effect on the number or species of predators on the transects and observations were therefore continued during the afternoon only

Data analysis Settlement rates population densities and mean growth rates were compared among sites and habitats using two- way analysis of variance (ANOVA) (Sokal md RoMf 1981) Sites and habitats were considered fixed treatment effects while censuses were considered random effects and a repeated measure All numeric data were log (x + 1) trans- formed prior to analysis to ensure hsmoscedasticity

artletts test for homogeneity of variance (Wilkinson 1990)) Predator densities and capture success rates were

Can J Fish Aquat Sci Vol 52 1995

also compared among locations and habitats using two- way analysis of variance To determine where significant differences among locations or habitats occurred post hoc analyses were conducted using Tukey9s honestly significant difference test (HSD) (Wilkinssn 19966) Linear regression analyses were used to determine the effects of substrate rugssity on settlement postsettlement survival predator success and growth rate

Variation in environmental variables Water temperature throughout the study ranged from 4degC in early May to 9OC in early July On any sampling day throughout the study there was less than I O C difference in temperature between locations and between transect sites at a location The general uniformity of temperature across the lower reaches of St Margarets likely due to regular tidal flushing It was there that differences in growth between habitats or locations were not attributable to spatial variations in temperature

Mean substrate mgosity (measured for each habitat type as the average of all transects in that habitat type) differed between the four habitat types (ANOVA F - 9-85 p lt

I) The mean values (138 for sand 204 for grass 337 for cobble and 376 for reef) differed in all pairwise comparisons (Tukeys HSD p lt 085 for all comparisons) We are therefore confident that the four habitat types chosen represent real differences in terms of the amount of shelter available to newly settled cod

itat variation in settlement and population density

Comparisons between transects revealed no differences in the timing or strength of settlement among sites or habitats No juvenile cod were observed on any s f the transect sites upon initiation of the monitoring program in early April Juvenile cod settl mostly in one pulse during the 2nd and 3rd weeks of ay (Fig 1) The timing of settlement was generally si r across locations and across habitat types within a location ie at scales of several kihnetres or several metres No significant differences ( p gt 005) in settlement were found between habitat types or between sites (Table I) although a significant location-by-habitat interaction was detected (Table I) The settlement of juve- nile cod and the substrate rugosity of the transect sites were not correlated (r2 = 02 p gt 005)

The population density of age O f cod rose rapidly at all transect sites following the pulse of settlement in mid- May then began to decrease in late May or early June (Fig 2) The decline in population de attributed to postsettlement mortality rather than behavioural studies of age 0+ cod in revealed them to be strongly site attached fo 2-3 months of demersal life (Tupper and In addition marked individuals were not found in monthly monitoring of the areas sumownding the transect sites The decline in density was much greater in sand and seagrass habitats than in the structurally more complex cobble and reef habitats (Fig 2) At all three locations population densities of age g+ sod on sand bottom reached 0 by late

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June Substrate rugosity accounted for 75 of the variance in postsettlement survival ( p lt 00001 Fig 3) In summary despite a uniform pattern of settlement among habitats and locations survival varied significantly between habitats and was positvely correlated with the complexity of the habitat These results suggest that demersal young-of-the- y e a cod in St Margarets ay are limited by the availability of shelter sites and that suitable nursery habitats for age 04- cod should provide an abundance of refugia The fact that population density in a given habitat did not differ between locations presumably reflects a combination of the spatially uniform pattern of cod settlement in St Margarets Bay with a similarity between locations in the postsettlement processes controlling among-habitat variations in population density

Predation om juvenile cod Thee species of Cottidae (Hernitripterus amep-icanus Myoxo- cephalus sctodecemspincasus and Myoxocephalus atmeus) were observed preying on age 0 + cod in St Margarets Bay Because these three species have very similar behav- iours they were pooled as cottid predators Predator den- sities did not vary among habitat types but did vary among locations (two-way NOVA Table 1) A total of 96 predator- prey interactions (attempted captures) were observed dur- ing the course of the study The number of attempted cap- tures did not vary significantly between habitat types or locations (Table I) Ca ture success varied among habi- tats but not among sites (two-way ANOVA Table I) Predators were most successfuH on open sand bottoms and least successful in reef and cobble habitats Capture success on a given transect was not related to predator density (r2 = 009 p gt 03) but was inversely related to substrate rugosity (2 = 074 p lt 0001 Fig 4) Because the among- habitat pattern of capture success is inversely related to the survival of age 0 + cod it appears that predation is a rna~or factor influencing variation among habitats in recruit- ment of young-of-the-year cod

Among-habitat variation in growth There was no difference in mean size at settlement between habitat types or locations (ANOVA F = 143 p gt 005) Significant differences in mean growth rate were observed among habitat types but not among locations (Table I) There was no significant location-by-habitat interaction ( F = 035 p gt 09) At all three locations the growth rate of juvenile cod was highest in seagrass habitats (range 059-067 mm-day-) and lowest on sand bottoms (range 002-006 rnmday-I) Growth rates did not significantly dif- fer between reef (range 838-045 mrnsday-) and cobble (range 035-041 rnmday-) habitats at any of the three locations (Table I)

Discussion

Settlement of youm In this study juven onstrate any pref- erence for habitat type at settlement (Table 1) In contrast to patterns of settlement survival of Quvenile cod varied greatly between habitat types (Table 1) The processes reg- ulating among-habitat variation in juvenile cod density

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Can J Fish Aquat Sci Vol 52 1995

Fig 2 Temporal variation in population density (no of individuals per 15-m transect) of age 0+ cod in four habitat types (rocky reef cobble bottom seagrass beds and sandy bottom) at each of three sites in St Margarets Bay Nova Scotia Error bars represent ampI standard deviation

BACK COVE -I-

I I I I I I

Aprii May J u n e July

Month

( - post settlement period - (

must therefore occur postsettlement with differential sur- vival rather than differential settlement leading to the observed patterns of density In contrast Sale et al (1984) clearly demonstrated that several species of coral reef fish settle preferentially to specific micrshabitats and suggested that spatial variation in microhabitat structure may result in spatial variation in settlement and subsequent recruitment

The relative importance of settlement and postsettlement processes in determining fish-habitat associations is unknown for most species (Jones 1991) Habitat type may influence postsettlement processes to either reinforce or alter spatial patterns established at settlement For example the darnselfish Pomacentrus amboineresks settles preferen- tially in deeper lagoonal waters where its subsequent growth rate and survival are higher than in shallow water

Ion (Jones 1986) In contrast the blennoid fish f i r s f e r j g a ~ r i u m settles uniformly among habitat types differing in structural complexity but exhibits extreme differences in subsequent survival and density which are much higher in more complex habitats (Connell and Jones 1991) This pattern is identical to that exhibited by juvenile cod in this

Fig 3 Effect of substrate rugosity of a transect on postsettlement survival of age 0+ cod Survival is calculated as the percentage of all fish settling onto a given transect that survived until the end of the experiment

0 Reef O Cobble B Grass r Sand

10 15 20 25 30 35 40 45

Substrate Rugosity

study As with E varium among-habitat variation in the sur- vival of juvenile cod radically altered patterns of settlement

The existence of a positive correlation between survival of juvenile fish and habitat complexity is considered evi- dence for space limitation ie intraspecific competition for limited shelter sites (eg Shkalman 1985) In this study the efficiency s f cottid predators decreased with increasing habitat complexity and similar results were observed for predation on amphipods by yellow perch Pema flavescens and mffe Gyrmocephalus cernuus (Mattila 1992) Gotcietas and Brown (1993) found that young-sf-the-year cod kept in aquaria selected more complex substrates in the presence of a predator Thus the relationship between habitat corn- plexity and survival need not be explained solely by corn- petition for living space but can also be attributed to dif- ferential predation among habitat types Thus a very high predator density in more complex habitats could still lead to higher predation mortality in those habitats However in St Margarets Bay predator density did not vary signifi- cantly between habitats As a result survival remained positively correlated with habitat complexity (Fig 3)

Mattila ( 1992) suggests that predation efficiency is not automatically reduced by a high level of habitat complexity per se the prey must be able to utilize that complexity as an effective shelter In this study seagrass beds could con- ceivably provide the greatest complexity of the four habitats if the vertical area of each blade of grass were measured However young-of-the-year cod did not utilize seagrass blades as shelter they preferred rocks empty scallop shells and other debris found within the seagrass beds Considering

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the rapid postsettlement growth rates of young-of-the-year cod it seems probable that they essentially outgrow seagrass blades as a suitable refuge soon after settlement Connell and Jones (1991) hypothesized that the lack of habitat- specific settlement in E varkwn may be due to settlement- sized fish finding adequate shelter in a wide range of habi- tats while habitat-specific mortality may arise when settled fish outgrow suitable shelter in habitats of lower com- plexity This hypothesis fits our findings for young-of-the- year cod equally well If cod at their smallest sizes can find shelter in all habitats more or less equally differences in set- tlement strength between habitats would not be expected Patterns of distribution in juvenile cod populations would then be determined by habitat-specific predation pressure Lough et al (1989) offered a similar hypothesis to explain the demography of young-of-the-year cod and haddock on Georges Bank They observed that pelagic juvenile gadids were widespread over the bank in June but that in July demersal juveniles were found mainly on pebble-gravel beds and were poorly represented on other less complex sedimentary substrates They also suggested that in addition to providing more shelter sites than the other substrates the pebble-gravel deposits most closely matched the mottled colouring of demersal juvenile cod making the small fish very difficult to see and therefore reducing their predation risk From these results Lough et al (1989) concluded that the availability of a complex habitat with reduced pre- dation pressure may be critical to the recruitment success of cod and haddock on Georges Bank

uence of habitat structure on The growth rates of young-of-the-ye

han previously published values for fish of this 01 and Lough (1988) reported growth rates of

071 mrnday- for cod of 31 mm standard length to 109 mm-day- for cod of 67 mm standard length In the present study mean growth rate over all habitats was approximately 04 mm-day- However Bolz and Lough studied populations on Georges Bank during the summer and fall months these fish were growing at higher tem- peratures than the spring cohort of young-of-the-year cod from St Margarets Bay

Connell and Jones (1991) suggested that habitat corn- plexity may influence the growth and survival of juvenile fish through increased prey density and prey diversity The growth rate of young-of-the-year cod in this study differed between habitats but was not related to substrate mgosity per se However as discussed in the previous section the shelter provided by vegetation was mot accounted for in this measure of complexity For small prey items seagrass beds undoubtedly offer the greatest habitat complexity For example Sogard (1992) reported that the presence of seagrass beds increased copepod densities by 49 and amphipod densities by 64 Thus if habitat complexity is measured with regard to prey size rather than predator size then prey densities and predator growth rates should increase in more complex habitats

In this study young-of-the-year cod experienced elevated growth rates in seagrass beds (presumably because of the higher prey densities within this habitat) but experienced significantly reduced predation risk in rocky reef and cobble

Fig 4 The effect of substrate rugosity on capture success of cottid predators on age 0+ cod Capture success is calculated as the number of successful captures divided by the number of attempted captures

0 Reef O Cobble v Grass

Substrate Rugosity

habitats It remains unclear which strategy is the more advantageous for young-of-the-yea cod Several researchers (Werner and Hall 1988 Connell and Jones 1991 Sogard 1992) have suggested the possibility of trade-offs in habitat utilization by fish Present ecological theory tells us that fish should select for the habitat that maximizes energy gain (growth) while minimizing the risk of mortality Cod in St Margarets Bay appear to lose their site fidelity by their first winter at which point they disperse from shallow nearshore habitats presumably joining the older juvenile population in deeper warmer water (Tup 1995) The greatest numbers of fish undergoing this migra- tion will be from complex hard-bottom habitats (reef and cobble) while the largest individuals will be from sea- grass habitats Overwinter survival of several temperate fishes has been demonstrated to be size dependent with the largest individuals surviving best (Henderson et a 1988) Thus one can foresee a scenario in which one habitat supplies 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 Further research is needed to establish the relative importance of these dif- fering strategies to the population dynamics of Atlantic cod

Conclusions Over the past decade studies of demersal marine fish recruitment have generally concluded that recruitment vari- ation results mainly from stochastic I m a l survival (DoheHty 1982 1983 Victor 1983 1986 Houde 1987 Miller et al 1988 Beyer 1989 Pepin and Myers 1991 Milicich et al 1992 Boherty and Fowler 1994) Recently a more plu- ralistic view has been suggested in which both pre- and post-settlement events a e considered important in regulating adult population size (Forrester 1990 Jones 1990 Jones 1991 Hunt von Herbing and Hunte 199 1 Tupper and

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Hunte 1994 Tupper and Boutilier 1995) The relative ortance or pre- and post-settlement events in deter- ing recruitment strength will vary with location time

and habitat (Jones 1996 Cswraell and Jones 199 1) While almost all research in this field has been conducted on coral reef fishes similar me s seem to apply to y o u n g - o f - t e e Atlantic cod tudy spatid patterns of settlement of cod were completely altered by habitat- specific postsettlement mortality In addition growth rates of young-of-the-year cod were influenced by habitat type which may in turn influence overwinter survivaI However in yews or locations in which larval survival and settlement were very low the importance of these gostsettlement processes would likely decrease and the abundance of young-of-the-year cod would be regulated mainly by larval input Longer term studies are needed to assess the impsr- tance of pre- and post-settlement events over several y e a s (Forrester 1990 Jones 1990)

1 Hunt von Herbing and R Conrad provided assistance in the field This study is a contribution s f the Ocean Pro- duction Enhancement Network MT was funded by a Natural Sciences and Engineering Research Council

C ) postgraduate scholarship mQ a Ddhousie graduate scholarship Funding for this study was provided by an operating grant f rom the NSERC Production Enhancement Network to

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Sogard S 1992 Variability in growth rates of juvenile fishes in different estuarine habitats Mar E d Prog Ser 85 35-53

W and FJ Rohlf 1981 Biometry 2nd ed Freeman San Francisco Calif

Sweatman H 1985 The influence of adults of some coral reef fishes on larval recruitment Ecol Monsgr 55 469-485

Sweatrnan H 1988 Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues J Exp Mar B i d Ecol 124 163-174

Tupper M and WG Boutilier 1995 Size and priority at settle- ment determine growth and competitive success of juvenile Atlantic cod Mar Ecol Prog Ser 118 295-308

Tupper M and W Hunte 11994 Recruitment of coral reef fishes to artificial and natural reefs in Barbados WI Mar Ecol Prog Ser 108 225-235

Victor BC 1983 Recruitment and population dynamics of a coral reef fish Science (Washington DC) 219 4 3 9-420

Victor BC 1986 Larval settlement and juvenile mortality in a recmitment-limited coral reef fish population Ecol Monogr 56 145-160

Walsk WJ 1987 Patterns of recruitment and spawning in Hawaiian reef fishes Environ BioB Fishes 4 257-276

Werner EE and D3 Hall 1988 Ontogenetic habitat shifts in bluegill the foraging rate - predation risk trade-off Ecsl- ogy 69 1352-1 366

Wilkinson W 1990 SYSTAT the system for statistics Systat Inc Evansasn 111

Williams DMcB S English and MJ Milicich 1994 Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement Bull Mar Sci 54 314-33 B

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should favour postsettlement survival through decreased predation pressure

The high mortality rates typically associated with psst- settlement juveniles are thought to be primarily due to predation (Houde 1987) Many piscivorous fishes select smaller size-classes (Juanes 1994) In addition overwinter survival of young-of-the-year fish in northern climates is generally higher in larger individuals (Walsh 1987 Henderson et al 1988) Thus rapid growth sf newly settled fish may confer a selective advantage both physiologically and in terms of reduced predation risk In general we should expect higher survival rates in those habitats provid- ing the greatest potential for growth However conflicts in habitat selection may occur if those habitats providing maximum growth are not also those that provide the max- imum amount of shelter from predation (Sogard 1992) In such cases high predation risk may force newly settled fish into habitats that do not optimize growth or alterna- tively insufficient food abundance may force newly settled fish into a habitat where the risk of predation is significantly higher

Studies of these effects of habitat on the demography of juvenile fishes have focused mainly on reef-associated species (eg Sale et al 1984 Carr 1991 Connell and Jones 1991 Levin 199 1 1993) Indeed much of what is known about the recruitment dynamics of demersal marine fishes stems from studies of coral reef fishes In this paper we applied a sampling approach typical of reef fish studies to the juvenile demographics of the Atlantic cod (Gadus morhua) a key commercial species in the temperate North Atlantic region We compared settlement growth and post- settlement survival of individually tagged age 0 + Atlantic cod in four distinct habitat types In addition we measured the density and capture success of predators on juvenile cod in each habitat The goal of the study was to answer the following questions ( i ) Do settlement growth and survival of age 0+ cod vary among habitat types (It) Do predator densities and capture success rates influence survival of age O+ cod in each habitat (iii) Is the among-habitat pat- tern of settlement preserved in the juvenile population or modified by mortality and (or) emigration

Methods

Study locations The study was conducted at three locations along the shore of St Margarets Bay Nova Scotia The nearshore bottom of St Margarets Bay can be divided into four broad habitat types rocky reef (characterized by bedrock strewn with large granitic boulders) cobble bottom seagrass (Zostera marina) beds and sand bottom Macroalgae were scarce at these sites owing to herbivorous grazing by the sea urchin Strongg~locentrotkes drobachieresks Rocky reefs were typically covered by crustose algae and (or) a short turf of filamentous algae neither of which would provide suitable shelter for juvenile cod

At each location four 15-m transect lines were laid in each of the four habitat types (is 16 transectsllocation) AH1 transects were within 180 m of shore at a depth of 15-2 m (mean low tide) The substrate mgosity (a measure of habitat complexity see Chandler et al 1985) of each

transect site was estimated by fitting a fine-link brass chain to the bottom contours along the transect Iine The total distance covered by the chain was then divided by 15 m (the horizontal distance covered by the transect line) pro- ducing an index of substrate rugosity It is important to note that substrate rugosity is simply a measure of the actual surface area of bottom structure available to an organism and does not account for other possible shelter sites such as that provided by seagrasses However even in dense seagrass beds newly settled cod in this study were not closely associated with vegetation but sought refuge within the interstices of rocks shells and other hard bottom (M Tupper personal observations)

Census techniques Visual censuses of juvenile cod abundance were conducted at roughly 10-day intervals from May B to July 1 1992 by snorkelling slowly along the transect lines and counting all cod within 1 rn on either side of the transect line (30 m2 planar surface area) Settlement was measured as the mean number of newly settled cod on the four transect lines at each transect site Newly settled cod were recognizable as being 4 0 mm in total length and having a barred pig- mentation pattern and a silvery underbelly This pattern slowly fades until the adult pigmentation is assumed at 1-2 weeks postsettlement (M Tupper personal observa- tions) Newly settled cod were anaesthetized in situ using a 10 solution of Quinaldine in seawater The total length of each animal was measured to the nearest millimetre with a 100-mrn plastic ruler and the animal was then marked with injections of acrylic paint using a specific pattern of dots to identify individuals This allowed marked individuals to be recognized as prior residents in subsequent censuses and allowed growth mortality and emigration to be quantified at each site The length of each fish was estimated visually at each census using a clear plastic ruler fastened to the end of a 60 cm length of wooden dowel The procedure was facilitated by the behaviour of young- of-the-yea cod which tend to flatten themselves against the substrate and remain immobile when approached This technique was accurate to k39 rnm for cod under 180 rnm in totaH length (Tupper and Boutilier 1995) Individual growth rates of tagged fish were calculated as the increase in total length divided by the number of days since the previous study in July divided by the total number of set- tlers tagged on that transect Individual growth rates of tagged fish were calculated as the increase in total length divided by the number of days since the previous measure- ment Continuous water temperature records were not avail- able for the specific study sites but were available from an aquaculture site at the head of St Margarets Bay approx- imately 2 km from the study sites Water temperatures on each transect were recorded immediately following a census with a mercury thermometer

Predation Observations of predation by other fishes on juvenile cod were made in situ at roughly 10-day intervals from mid-May to early July 1992 at each transect site The observer floated motionless above the site while recording the species and number of predators the number of attempted strikes

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1836

Fig 1 Temporal variation in settlement of age 8-4- cod to different habitat types (rocky reef cobble bottom seagrass beds and sandy bottom) at three sites in St Margarets Bay Nova Scotia Error bars represent k1 standard deviation

BACK COVE

-

MILL COVE

-5 L I I I i I I 1 April May June July

Month I - postsettlemerat period - (

(lunges at a juvenile cod) and the number of successful strikes (capture and ingestion of a juvenile cod) over a I-h

eriod An index of capture success was then calculated by dividing the number of successful strikes by the total number of strikes for each of the four habitat types Mean capture success in each habitat was calculated as the average capture success over the six observation periods Predation was initially observed at dawn in the afternoon at dusk and at night However the time of observation appeared to have no effect on the number or species of predators on the transects and observations were therefore continued during the afternoon only

Data analysis Settlement rates population densities and mean growth rates were compared among sites and habitats using two- way analysis of variance (ANOVA) (Sokal md RoMf 1981) Sites and habitats were considered fixed treatment effects while censuses were considered random effects and a repeated measure All numeric data were log (x + 1) trans- formed prior to analysis to ensure hsmoscedasticity

artletts test for homogeneity of variance (Wilkinson 1990)) Predator densities and capture success rates were

Can J Fish Aquat Sci Vol 52 1995

also compared among locations and habitats using two- way analysis of variance To determine where significant differences among locations or habitats occurred post hoc analyses were conducted using Tukey9s honestly significant difference test (HSD) (Wilkinssn 19966) Linear regression analyses were used to determine the effects of substrate rugssity on settlement postsettlement survival predator success and growth rate

Variation in environmental variables Water temperature throughout the study ranged from 4degC in early May to 9OC in early July On any sampling day throughout the study there was less than I O C difference in temperature between locations and between transect sites at a location The general uniformity of temperature across the lower reaches of St Margarets likely due to regular tidal flushing It was there that differences in growth between habitats or locations were not attributable to spatial variations in temperature

Mean substrate mgosity (measured for each habitat type as the average of all transects in that habitat type) differed between the four habitat types (ANOVA F - 9-85 p lt

I) The mean values (138 for sand 204 for grass 337 for cobble and 376 for reef) differed in all pairwise comparisons (Tukeys HSD p lt 085 for all comparisons) We are therefore confident that the four habitat types chosen represent real differences in terms of the amount of shelter available to newly settled cod

itat variation in settlement and population density

Comparisons between transects revealed no differences in the timing or strength of settlement among sites or habitats No juvenile cod were observed on any s f the transect sites upon initiation of the monitoring program in early April Juvenile cod settl mostly in one pulse during the 2nd and 3rd weeks of ay (Fig 1) The timing of settlement was generally si r across locations and across habitat types within a location ie at scales of several kihnetres or several metres No significant differences ( p gt 005) in settlement were found between habitat types or between sites (Table I) although a significant location-by-habitat interaction was detected (Table I) The settlement of juve- nile cod and the substrate rugosity of the transect sites were not correlated (r2 = 02 p gt 005)

The population density of age O f cod rose rapidly at all transect sites following the pulse of settlement in mid- May then began to decrease in late May or early June (Fig 2) The decline in population de attributed to postsettlement mortality rather than behavioural studies of age 0+ cod in revealed them to be strongly site attached fo 2-3 months of demersal life (Tupper and In addition marked individuals were not found in monthly monitoring of the areas sumownding the transect sites The decline in density was much greater in sand and seagrass habitats than in the structurally more complex cobble and reef habitats (Fig 2) At all three locations population densities of age g+ sod on sand bottom reached 0 by late

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June Substrate rugosity accounted for 75 of the variance in postsettlement survival ( p lt 00001 Fig 3) In summary despite a uniform pattern of settlement among habitats and locations survival varied significantly between habitats and was positvely correlated with the complexity of the habitat These results suggest that demersal young-of-the- y e a cod in St Margarets ay are limited by the availability of shelter sites and that suitable nursery habitats for age 04- cod should provide an abundance of refugia The fact that population density in a given habitat did not differ between locations presumably reflects a combination of the spatially uniform pattern of cod settlement in St Margarets Bay with a similarity between locations in the postsettlement processes controlling among-habitat variations in population density

Predation om juvenile cod Thee species of Cottidae (Hernitripterus amep-icanus Myoxo- cephalus sctodecemspincasus and Myoxocephalus atmeus) were observed preying on age 0 + cod in St Margarets Bay Because these three species have very similar behav- iours they were pooled as cottid predators Predator den- sities did not vary among habitat types but did vary among locations (two-way NOVA Table 1) A total of 96 predator- prey interactions (attempted captures) were observed dur- ing the course of the study The number of attempted cap- tures did not vary significantly between habitat types or locations (Table I) Ca ture success varied among habi- tats but not among sites (two-way ANOVA Table I) Predators were most successfuH on open sand bottoms and least successful in reef and cobble habitats Capture success on a given transect was not related to predator density (r2 = 009 p gt 03) but was inversely related to substrate rugosity (2 = 074 p lt 0001 Fig 4) Because the among- habitat pattern of capture success is inversely related to the survival of age 0 + cod it appears that predation is a rna~or factor influencing variation among habitats in recruit- ment of young-of-the-year cod

Among-habitat variation in growth There was no difference in mean size at settlement between habitat types or locations (ANOVA F = 143 p gt 005) Significant differences in mean growth rate were observed among habitat types but not among locations (Table I) There was no significant location-by-habitat interaction ( F = 035 p gt 09) At all three locations the growth rate of juvenile cod was highest in seagrass habitats (range 059-067 mm-day-) and lowest on sand bottoms (range 002-006 rnmday-I) Growth rates did not significantly dif- fer between reef (range 838-045 mrnsday-) and cobble (range 035-041 rnmday-) habitats at any of the three locations (Table I)

Discussion

Settlement of youm In this study juven onstrate any pref- erence for habitat type at settlement (Table 1) In contrast to patterns of settlement survival of Quvenile cod varied greatly between habitat types (Table 1) The processes reg- ulating among-habitat variation in juvenile cod density

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Can J Fish Aquat Sci Vol 52 1995

Fig 2 Temporal variation in population density (no of individuals per 15-m transect) of age 0+ cod in four habitat types (rocky reef cobble bottom seagrass beds and sandy bottom) at each of three sites in St Margarets Bay Nova Scotia Error bars represent ampI standard deviation

BACK COVE -I-

I I I I I I

Aprii May J u n e July

Month

( - post settlement period - (

must therefore occur postsettlement with differential sur- vival rather than differential settlement leading to the observed patterns of density In contrast Sale et al (1984) clearly demonstrated that several species of coral reef fish settle preferentially to specific micrshabitats and suggested that spatial variation in microhabitat structure may result in spatial variation in settlement and subsequent recruitment

The relative importance of settlement and postsettlement processes in determining fish-habitat associations is unknown for most species (Jones 1991) Habitat type may influence postsettlement processes to either reinforce or alter spatial patterns established at settlement For example the darnselfish Pomacentrus amboineresks settles preferen- tially in deeper lagoonal waters where its subsequent growth rate and survival are higher than in shallow water

Ion (Jones 1986) In contrast the blennoid fish f i r s f e r j g a ~ r i u m settles uniformly among habitat types differing in structural complexity but exhibits extreme differences in subsequent survival and density which are much higher in more complex habitats (Connell and Jones 1991) This pattern is identical to that exhibited by juvenile cod in this

Fig 3 Effect of substrate rugosity of a transect on postsettlement survival of age 0+ cod Survival is calculated as the percentage of all fish settling onto a given transect that survived until the end of the experiment

0 Reef O Cobble B Grass r Sand

10 15 20 25 30 35 40 45

Substrate Rugosity

study As with E varium among-habitat variation in the sur- vival of juvenile cod radically altered patterns of settlement

The existence of a positive correlation between survival of juvenile fish and habitat complexity is considered evi- dence for space limitation ie intraspecific competition for limited shelter sites (eg Shkalman 1985) In this study the efficiency s f cottid predators decreased with increasing habitat complexity and similar results were observed for predation on amphipods by yellow perch Pema flavescens and mffe Gyrmocephalus cernuus (Mattila 1992) Gotcietas and Brown (1993) found that young-sf-the-year cod kept in aquaria selected more complex substrates in the presence of a predator Thus the relationship between habitat corn- plexity and survival need not be explained solely by corn- petition for living space but can also be attributed to dif- ferential predation among habitat types Thus a very high predator density in more complex habitats could still lead to higher predation mortality in those habitats However in St Margarets Bay predator density did not vary signifi- cantly between habitats As a result survival remained positively correlated with habitat complexity (Fig 3)

Mattila ( 1992) suggests that predation efficiency is not automatically reduced by a high level of habitat complexity per se the prey must be able to utilize that complexity as an effective shelter In this study seagrass beds could con- ceivably provide the greatest complexity of the four habitats if the vertical area of each blade of grass were measured However young-of-the-year cod did not utilize seagrass blades as shelter they preferred rocks empty scallop shells and other debris found within the seagrass beds Considering

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the rapid postsettlement growth rates of young-of-the-year cod it seems probable that they essentially outgrow seagrass blades as a suitable refuge soon after settlement Connell and Jones (1991) hypothesized that the lack of habitat- specific settlement in E varkwn may be due to settlement- sized fish finding adequate shelter in a wide range of habi- tats while habitat-specific mortality may arise when settled fish outgrow suitable shelter in habitats of lower com- plexity This hypothesis fits our findings for young-of-the- year cod equally well If cod at their smallest sizes can find shelter in all habitats more or less equally differences in set- tlement strength between habitats would not be expected Patterns of distribution in juvenile cod populations would then be determined by habitat-specific predation pressure Lough et al (1989) offered a similar hypothesis to explain the demography of young-of-the-year cod and haddock on Georges Bank They observed that pelagic juvenile gadids were widespread over the bank in June but that in July demersal juveniles were found mainly on pebble-gravel beds and were poorly represented on other less complex sedimentary substrates They also suggested that in addition to providing more shelter sites than the other substrates the pebble-gravel deposits most closely matched the mottled colouring of demersal juvenile cod making the small fish very difficult to see and therefore reducing their predation risk From these results Lough et al (1989) concluded that the availability of a complex habitat with reduced pre- dation pressure may be critical to the recruitment success of cod and haddock on Georges Bank

uence of habitat structure on The growth rates of young-of-the-ye

han previously published values for fish of this 01 and Lough (1988) reported growth rates of

071 mrnday- for cod of 31 mm standard length to 109 mm-day- for cod of 67 mm standard length In the present study mean growth rate over all habitats was approximately 04 mm-day- However Bolz and Lough studied populations on Georges Bank during the summer and fall months these fish were growing at higher tem- peratures than the spring cohort of young-of-the-year cod from St Margarets Bay

Connell and Jones (1991) suggested that habitat corn- plexity may influence the growth and survival of juvenile fish through increased prey density and prey diversity The growth rate of young-of-the-year cod in this study differed between habitats but was not related to substrate mgosity per se However as discussed in the previous section the shelter provided by vegetation was mot accounted for in this measure of complexity For small prey items seagrass beds undoubtedly offer the greatest habitat complexity For example Sogard (1992) reported that the presence of seagrass beds increased copepod densities by 49 and amphipod densities by 64 Thus if habitat complexity is measured with regard to prey size rather than predator size then prey densities and predator growth rates should increase in more complex habitats

In this study young-of-the-year cod experienced elevated growth rates in seagrass beds (presumably because of the higher prey densities within this habitat) but experienced significantly reduced predation risk in rocky reef and cobble

Fig 4 The effect of substrate rugosity on capture success of cottid predators on age 0+ cod Capture success is calculated as the number of successful captures divided by the number of attempted captures

0 Reef O Cobble v Grass

Substrate Rugosity

habitats It remains unclear which strategy is the more advantageous for young-of-the-yea cod Several researchers (Werner and Hall 1988 Connell and Jones 1991 Sogard 1992) have suggested the possibility of trade-offs in habitat utilization by fish Present ecological theory tells us that fish should select for the habitat that maximizes energy gain (growth) while minimizing the risk of mortality Cod in St Margarets Bay appear to lose their site fidelity by their first winter at which point they disperse from shallow nearshore habitats presumably joining the older juvenile population in deeper warmer water (Tup 1995) The greatest numbers of fish undergoing this migra- tion will be from complex hard-bottom habitats (reef and cobble) while the largest individuals will be from sea- grass habitats Overwinter survival of several temperate fishes has been demonstrated to be size dependent with the largest individuals surviving best (Henderson et a 1988) Thus one can foresee a scenario in which one habitat supplies 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 Further research is needed to establish the relative importance of these dif- fering strategies to the population dynamics of Atlantic cod

Conclusions Over the past decade studies of demersal marine fish recruitment have generally concluded that recruitment vari- ation results mainly from stochastic I m a l survival (DoheHty 1982 1983 Victor 1983 1986 Houde 1987 Miller et al 1988 Beyer 1989 Pepin and Myers 1991 Milicich et al 1992 Boherty and Fowler 1994) Recently a more plu- ralistic view has been suggested in which both pre- and post-settlement events a e considered important in regulating adult population size (Forrester 1990 Jones 1990 Jones 1991 Hunt von Herbing and Hunte 199 1 Tupper and

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Can J Fish Aejuat Sci Vol 52 199

Hunte 1994 Tupper and Boutilier 1995) The relative ortance or pre- and post-settlement events in deter- ing recruitment strength will vary with location time

and habitat (Jones 1996 Cswraell and Jones 199 1) While almost all research in this field has been conducted on coral reef fishes similar me s seem to apply to y o u n g - o f - t e e Atlantic cod tudy spatid patterns of settlement of cod were completely altered by habitat- specific postsettlement mortality In addition growth rates of young-of-the-year cod were influenced by habitat type which may in turn influence overwinter survivaI However in yews or locations in which larval survival and settlement were very low the importance of these gostsettlement processes would likely decrease and the abundance of young-of-the-year cod would be regulated mainly by larval input Longer term studies are needed to assess the impsr- tance of pre- and post-settlement events over several y e a s (Forrester 1990 Jones 1990)

1 Hunt von Herbing and R Conrad provided assistance in the field This study is a contribution s f the Ocean Pro- duction Enhancement Network MT was funded by a Natural Sciences and Engineering Research Council

C ) postgraduate scholarship mQ a Ddhousie graduate scholarship Funding for this study was provided by an operating grant f rom the NSERC Production Enhancement Network to

ehrents K 1987 The influence of shelter availability on recruitment and early juvenile survivorship of Lythryhbnkcs d d i Gilbert (Pisces Gobiidae) J Exp Mar Biol Ecol

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Bolz GR and RG Eough 1988 Growth through the first six months of Atlantic cod (Gadus morhm) and haddock (Melanogrammus aeglefinus) based on daily otolith incre- ments Fish Bull $6 223-235

Car MH 1991 Habitat selection and recruitment of an assem- blage of temperate zone reef fishes J Exp Mar Biol Ecol 146 113-137

C m MH 1994 Effects of macroalgal dynamics on recruitment of a temperate reef fish Ecology 75 1320-1333

Chandler CR RR Sanders Jr and AM Landry Jr 1985 Effects of three substrate variables on two artificial reef fish communities Bull Mar Sci 37 129-142

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de Lafontaine Ye T Lambert GR LiHHy WD McKone and RJ Miller (Editors) 1992 Juvenile stages the missing link in fisheries research Can Rch Rep Fish Aquat Sci No 1890

Boherty PJ 1982 Coral reef fishes recruitment-limited assem- blageswaz Proceedings of the Fourth International Coral Reef Symposium Manila The Phillipines VoH 2 pp 465-470

Doherty P-J 1983 Tropical territorial damselfishes is density limited by aggression or recruitment Ecology 64 176-190

Doherty PJ and AJ Fowler 8994 An empirical test of recruitment limitation in a coral reef fish Science (Washington DC) 263 935-939

Fsrrester GE 1990 Factors influencing the juvenile demog- raphy of a coral reef fish population Ecology 71 1666-1681

Gotceitas V and A Brown 1993 Substrate selection by juvenile Atlantic cod (Gadus mor8zua) effects of predation risk Oecologia 93 3 1-37

Henderson PA RHA Holmes and RN Size-selective overwintering mortality in the sand smelt Atkerina boyeri Risso and its role in population regulation J Fish Biol 33 221-233

Hixon MA and JP Beets 1989 Shelter characteristics and Caribbean fish assemblages experiments with artificial reefs Bull Mar Sci 44 666-680

Houde E 1987 Fish early life dynamics and recruitment variability Am Fish Soc Symp Ser 2 17-29

Hunt von Herbing I and W Hunte 1991 Spawning and recruitment of the bluehead wrasse Thakassoma Ea~ascdatum in Barbados WI Mar Ecol Prog Ser 72 49-58

Jones GPe 1986 Food availability affects growth in a coral reef fish Oecologia 70 136-139

Jones GP 1990 The importance of recruitment to the dynamics of a coral reef fish population Ecology 71 1691-1 698

Jones GP 1991 Postrecruitment processes in the ecology of coral reef fish populations a multifactoria2 perspective In The Ecology of fishes on coral reefs Edited by PF Sale Academic Press San Diego Calif pp 294-328

Juanes E 1994 What determines prey size selectivity in pis- civorous fishes Paz Theory and application in fish feeding ecology Edited by DJ Stouder KL Fresh and RJ Feller Belle W Baruch Library in Marine Sciences No 18 University of South Carolina Press Columbia SC

Levin PS 1991 Effects of microhabitat on recruitment vari- ation in a Gulf of Maine reef fish Mar Ecol Prog Ser 75 183-189

Levin PS 1993 Habitat structure conspecific presence and spatial variation in the recruitment of a temperate reef fish Oecologia 94 176-1 85

Lsugh RG PC Valentine DC Potter Pa Auditore GZ Bolz J Neilson and RI Berry 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 1-1 2

Malloy KD and TE Targett 1991 Feeding growth and survival of juvenile summer flounder Parakichthys dentatus experimental analysis of the effects of temperature and salin- ity Mar Ecol Prog Ser 72 213-223

Mattila J 1992 The effect of habitat complexity on predation efficiency of perch Perm fluvinbikis L and suffe Gyrnmo- cephcalus cernuus (L) f Exp Mar Biol Ecol 157 55-67

Milicich MJ MG Meekan and PJ Boherty 1992 Larval supply a good predictor of recruitment of 3 species of reef fish (Pomacentridae) Mar Ecol Psog Ser 86 153- 166

Miller IT LB Crowder JA Rice and EA Marshall 1988 Larval size and recruitment mechanisms in fishes toward a conceptual framework Can J Fish Aquat Sci 45 1657-1670

Pepin P- and RA Myers 1991 Significance of egg and larval size to recruitment variability of temperate marine fish Can Fish Aquat Sci 48 503-5 18

Sale PF WA Douglas and PJ Doherty 1984 Choice of microhabitats by coral reef fishes at settlement Coral Reefs 3 91-99

Shulman M 1985 Recruitment of coral reef fishes effects of distribution of predators and shelter Ecology 66 lOX9-1O66

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Sogard S 1992 Variability in growth rates of juvenile fishes in different estuarine habitats Mar E d Prog Ser 85 35-53

W and FJ Rohlf 1981 Biometry 2nd ed Freeman San Francisco Calif

Sweatman H 1985 The influence of adults of some coral reef fishes on larval recruitment Ecol Monsgr 55 469-485

Sweatrnan H 1988 Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues J Exp Mar B i d Ecol 124 163-174

Tupper M and WG Boutilier 1995 Size and priority at settle- ment determine growth and competitive success of juvenile Atlantic cod Mar Ecol Prog Ser 118 295-308

Tupper M and W Hunte 11994 Recruitment of coral reef fishes to artificial and natural reefs in Barbados WI Mar Ecol Prog Ser 108 225-235

Victor BC 1983 Recruitment and population dynamics of a coral reef fish Science (Washington DC) 219 4 3 9-420

Victor BC 1986 Larval settlement and juvenile mortality in a recmitment-limited coral reef fish population Ecol Monogr 56 145-160

Walsk WJ 1987 Patterns of recruitment and spawning in Hawaiian reef fishes Environ BioB Fishes 4 257-276

Werner EE and D3 Hall 1988 Ontogenetic habitat shifts in bluegill the foraging rate - predation risk trade-off Ecsl- ogy 69 1352-1 366

Wilkinson W 1990 SYSTAT the system for statistics Systat Inc Evansasn 111

Williams DMcB S English and MJ Milicich 1994 Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement Bull Mar Sci 54 314-33 B

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1836

Fig 1 Temporal variation in settlement of age 8-4- cod to different habitat types (rocky reef cobble bottom seagrass beds and sandy bottom) at three sites in St Margarets Bay Nova Scotia Error bars represent k1 standard deviation

BACK COVE

-

MILL COVE

-5 L I I I i I I 1 April May June July

Month I - postsettlemerat period - (

(lunges at a juvenile cod) and the number of successful strikes (capture and ingestion of a juvenile cod) over a I-h

eriod An index of capture success was then calculated by dividing the number of successful strikes by the total number of strikes for each of the four habitat types Mean capture success in each habitat was calculated as the average capture success over the six observation periods Predation was initially observed at dawn in the afternoon at dusk and at night However the time of observation appeared to have no effect on the number or species of predators on the transects and observations were therefore continued during the afternoon only

Data analysis Settlement rates population densities and mean growth rates were compared among sites and habitats using two- way analysis of variance (ANOVA) (Sokal md RoMf 1981) Sites and habitats were considered fixed treatment effects while censuses were considered random effects and a repeated measure All numeric data were log (x + 1) trans- formed prior to analysis to ensure hsmoscedasticity

artletts test for homogeneity of variance (Wilkinson 1990)) Predator densities and capture success rates were

Can J Fish Aquat Sci Vol 52 1995

also compared among locations and habitats using two- way analysis of variance To determine where significant differences among locations or habitats occurred post hoc analyses were conducted using Tukey9s honestly significant difference test (HSD) (Wilkinssn 19966) Linear regression analyses were used to determine the effects of substrate rugssity on settlement postsettlement survival predator success and growth rate

Variation in environmental variables Water temperature throughout the study ranged from 4degC in early May to 9OC in early July On any sampling day throughout the study there was less than I O C difference in temperature between locations and between transect sites at a location The general uniformity of temperature across the lower reaches of St Margarets likely due to regular tidal flushing It was there that differences in growth between habitats or locations were not attributable to spatial variations in temperature

Mean substrate mgosity (measured for each habitat type as the average of all transects in that habitat type) differed between the four habitat types (ANOVA F - 9-85 p lt

I) The mean values (138 for sand 204 for grass 337 for cobble and 376 for reef) differed in all pairwise comparisons (Tukeys HSD p lt 085 for all comparisons) We are therefore confident that the four habitat types chosen represent real differences in terms of the amount of shelter available to newly settled cod

itat variation in settlement and population density

Comparisons between transects revealed no differences in the timing or strength of settlement among sites or habitats No juvenile cod were observed on any s f the transect sites upon initiation of the monitoring program in early April Juvenile cod settl mostly in one pulse during the 2nd and 3rd weeks of ay (Fig 1) The timing of settlement was generally si r across locations and across habitat types within a location ie at scales of several kihnetres or several metres No significant differences ( p gt 005) in settlement were found between habitat types or between sites (Table I) although a significant location-by-habitat interaction was detected (Table I) The settlement of juve- nile cod and the substrate rugosity of the transect sites were not correlated (r2 = 02 p gt 005)

The population density of age O f cod rose rapidly at all transect sites following the pulse of settlement in mid- May then began to decrease in late May or early June (Fig 2) The decline in population de attributed to postsettlement mortality rather than behavioural studies of age 0+ cod in revealed them to be strongly site attached fo 2-3 months of demersal life (Tupper and In addition marked individuals were not found in monthly monitoring of the areas sumownding the transect sites The decline in density was much greater in sand and seagrass habitats than in the structurally more complex cobble and reef habitats (Fig 2) At all three locations population densities of age g+ sod on sand bottom reached 0 by late

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June Substrate rugosity accounted for 75 of the variance in postsettlement survival ( p lt 00001 Fig 3) In summary despite a uniform pattern of settlement among habitats and locations survival varied significantly between habitats and was positvely correlated with the complexity of the habitat These results suggest that demersal young-of-the- y e a cod in St Margarets ay are limited by the availability of shelter sites and that suitable nursery habitats for age 04- cod should provide an abundance of refugia The fact that population density in a given habitat did not differ between locations presumably reflects a combination of the spatially uniform pattern of cod settlement in St Margarets Bay with a similarity between locations in the postsettlement processes controlling among-habitat variations in population density

Predation om juvenile cod Thee species of Cottidae (Hernitripterus amep-icanus Myoxo- cephalus sctodecemspincasus and Myoxocephalus atmeus) were observed preying on age 0 + cod in St Margarets Bay Because these three species have very similar behav- iours they were pooled as cottid predators Predator den- sities did not vary among habitat types but did vary among locations (two-way NOVA Table 1) A total of 96 predator- prey interactions (attempted captures) were observed dur- ing the course of the study The number of attempted cap- tures did not vary significantly between habitat types or locations (Table I) Ca ture success varied among habi- tats but not among sites (two-way ANOVA Table I) Predators were most successfuH on open sand bottoms and least successful in reef and cobble habitats Capture success on a given transect was not related to predator density (r2 = 009 p gt 03) but was inversely related to substrate rugosity (2 = 074 p lt 0001 Fig 4) Because the among- habitat pattern of capture success is inversely related to the survival of age 0 + cod it appears that predation is a rna~or factor influencing variation among habitats in recruit- ment of young-of-the-year cod

Among-habitat variation in growth There was no difference in mean size at settlement between habitat types or locations (ANOVA F = 143 p gt 005) Significant differences in mean growth rate were observed among habitat types but not among locations (Table I) There was no significant location-by-habitat interaction ( F = 035 p gt 09) At all three locations the growth rate of juvenile cod was highest in seagrass habitats (range 059-067 mm-day-) and lowest on sand bottoms (range 002-006 rnmday-I) Growth rates did not significantly dif- fer between reef (range 838-045 mrnsday-) and cobble (range 035-041 rnmday-) habitats at any of the three locations (Table I)

Discussion

Settlement of youm In this study juven onstrate any pref- erence for habitat type at settlement (Table 1) In contrast to patterns of settlement survival of Quvenile cod varied greatly between habitat types (Table 1) The processes reg- ulating among-habitat variation in juvenile cod density

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Can J Fish Aquat Sci Vol 52 1995

Fig 2 Temporal variation in population density (no of individuals per 15-m transect) of age 0+ cod in four habitat types (rocky reef cobble bottom seagrass beds and sandy bottom) at each of three sites in St Margarets Bay Nova Scotia Error bars represent ampI standard deviation

BACK COVE -I-

I I I I I I

Aprii May J u n e July

Month

( - post settlement period - (

must therefore occur postsettlement with differential sur- vival rather than differential settlement leading to the observed patterns of density In contrast Sale et al (1984) clearly demonstrated that several species of coral reef fish settle preferentially to specific micrshabitats and suggested that spatial variation in microhabitat structure may result in spatial variation in settlement and subsequent recruitment

The relative importance of settlement and postsettlement processes in determining fish-habitat associations is unknown for most species (Jones 1991) Habitat type may influence postsettlement processes to either reinforce or alter spatial patterns established at settlement For example the darnselfish Pomacentrus amboineresks settles preferen- tially in deeper lagoonal waters where its subsequent growth rate and survival are higher than in shallow water

Ion (Jones 1986) In contrast the blennoid fish f i r s f e r j g a ~ r i u m settles uniformly among habitat types differing in structural complexity but exhibits extreme differences in subsequent survival and density which are much higher in more complex habitats (Connell and Jones 1991) This pattern is identical to that exhibited by juvenile cod in this

Fig 3 Effect of substrate rugosity of a transect on postsettlement survival of age 0+ cod Survival is calculated as the percentage of all fish settling onto a given transect that survived until the end of the experiment

0 Reef O Cobble B Grass r Sand

10 15 20 25 30 35 40 45

Substrate Rugosity

study As with E varium among-habitat variation in the sur- vival of juvenile cod radically altered patterns of settlement

The existence of a positive correlation between survival of juvenile fish and habitat complexity is considered evi- dence for space limitation ie intraspecific competition for limited shelter sites (eg Shkalman 1985) In this study the efficiency s f cottid predators decreased with increasing habitat complexity and similar results were observed for predation on amphipods by yellow perch Pema flavescens and mffe Gyrmocephalus cernuus (Mattila 1992) Gotcietas and Brown (1993) found that young-sf-the-year cod kept in aquaria selected more complex substrates in the presence of a predator Thus the relationship between habitat corn- plexity and survival need not be explained solely by corn- petition for living space but can also be attributed to dif- ferential predation among habitat types Thus a very high predator density in more complex habitats could still lead to higher predation mortality in those habitats However in St Margarets Bay predator density did not vary signifi- cantly between habitats As a result survival remained positively correlated with habitat complexity (Fig 3)

Mattila ( 1992) suggests that predation efficiency is not automatically reduced by a high level of habitat complexity per se the prey must be able to utilize that complexity as an effective shelter In this study seagrass beds could con- ceivably provide the greatest complexity of the four habitats if the vertical area of each blade of grass were measured However young-of-the-year cod did not utilize seagrass blades as shelter they preferred rocks empty scallop shells and other debris found within the seagrass beds Considering

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the rapid postsettlement growth rates of young-of-the-year cod it seems probable that they essentially outgrow seagrass blades as a suitable refuge soon after settlement Connell and Jones (1991) hypothesized that the lack of habitat- specific settlement in E varkwn may be due to settlement- sized fish finding adequate shelter in a wide range of habi- tats while habitat-specific mortality may arise when settled fish outgrow suitable shelter in habitats of lower com- plexity This hypothesis fits our findings for young-of-the- year cod equally well If cod at their smallest sizes can find shelter in all habitats more or less equally differences in set- tlement strength between habitats would not be expected Patterns of distribution in juvenile cod populations would then be determined by habitat-specific predation pressure Lough et al (1989) offered a similar hypothesis to explain the demography of young-of-the-year cod and haddock on Georges Bank They observed that pelagic juvenile gadids were widespread over the bank in June but that in July demersal juveniles were found mainly on pebble-gravel beds and were poorly represented on other less complex sedimentary substrates They also suggested that in addition to providing more shelter sites than the other substrates the pebble-gravel deposits most closely matched the mottled colouring of demersal juvenile cod making the small fish very difficult to see and therefore reducing their predation risk From these results Lough et al (1989) concluded that the availability of a complex habitat with reduced pre- dation pressure may be critical to the recruitment success of cod and haddock on Georges Bank

uence of habitat structure on The growth rates of young-of-the-ye

han previously published values for fish of this 01 and Lough (1988) reported growth rates of

071 mrnday- for cod of 31 mm standard length to 109 mm-day- for cod of 67 mm standard length In the present study mean growth rate over all habitats was approximately 04 mm-day- However Bolz and Lough studied populations on Georges Bank during the summer and fall months these fish were growing at higher tem- peratures than the spring cohort of young-of-the-year cod from St Margarets Bay

Connell and Jones (1991) suggested that habitat corn- plexity may influence the growth and survival of juvenile fish through increased prey density and prey diversity The growth rate of young-of-the-year cod in this study differed between habitats but was not related to substrate mgosity per se However as discussed in the previous section the shelter provided by vegetation was mot accounted for in this measure of complexity For small prey items seagrass beds undoubtedly offer the greatest habitat complexity For example Sogard (1992) reported that the presence of seagrass beds increased copepod densities by 49 and amphipod densities by 64 Thus if habitat complexity is measured with regard to prey size rather than predator size then prey densities and predator growth rates should increase in more complex habitats

In this study young-of-the-year cod experienced elevated growth rates in seagrass beds (presumably because of the higher prey densities within this habitat) but experienced significantly reduced predation risk in rocky reef and cobble

Fig 4 The effect of substrate rugosity on capture success of cottid predators on age 0+ cod Capture success is calculated as the number of successful captures divided by the number of attempted captures

0 Reef O Cobble v Grass

Substrate Rugosity

habitats It remains unclear which strategy is the more advantageous for young-of-the-yea cod Several researchers (Werner and Hall 1988 Connell and Jones 1991 Sogard 1992) have suggested the possibility of trade-offs in habitat utilization by fish Present ecological theory tells us that fish should select for the habitat that maximizes energy gain (growth) while minimizing the risk of mortality Cod in St Margarets Bay appear to lose their site fidelity by their first winter at which point they disperse from shallow nearshore habitats presumably joining the older juvenile population in deeper warmer water (Tup 1995) The greatest numbers of fish undergoing this migra- tion will be from complex hard-bottom habitats (reef and cobble) while the largest individuals will be from sea- grass habitats Overwinter survival of several temperate fishes has been demonstrated to be size dependent with the largest individuals surviving best (Henderson et a 1988) Thus one can foresee a scenario in which one habitat supplies 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 Further research is needed to establish the relative importance of these dif- fering strategies to the population dynamics of Atlantic cod

Conclusions Over the past decade studies of demersal marine fish recruitment have generally concluded that recruitment vari- ation results mainly from stochastic I m a l survival (DoheHty 1982 1983 Victor 1983 1986 Houde 1987 Miller et al 1988 Beyer 1989 Pepin and Myers 1991 Milicich et al 1992 Boherty and Fowler 1994) Recently a more plu- ralistic view has been suggested in which both pre- and post-settlement events a e considered important in regulating adult population size (Forrester 1990 Jones 1990 Jones 1991 Hunt von Herbing and Hunte 199 1 Tupper and

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Can J Fish Aejuat Sci Vol 52 199

Hunte 1994 Tupper and Boutilier 1995) The relative ortance or pre- and post-settlement events in deter- ing recruitment strength will vary with location time

and habitat (Jones 1996 Cswraell and Jones 199 1) While almost all research in this field has been conducted on coral reef fishes similar me s seem to apply to y o u n g - o f - t e e Atlantic cod tudy spatid patterns of settlement of cod were completely altered by habitat- specific postsettlement mortality In addition growth rates of young-of-the-year cod were influenced by habitat type which may in turn influence overwinter survivaI However in yews or locations in which larval survival and settlement were very low the importance of these gostsettlement processes would likely decrease and the abundance of young-of-the-year cod would be regulated mainly by larval input Longer term studies are needed to assess the impsr- tance of pre- and post-settlement events over several y e a s (Forrester 1990 Jones 1990)

1 Hunt von Herbing and R Conrad provided assistance in the field This study is a contribution s f the Ocean Pro- duction Enhancement Network MT was funded by a Natural Sciences and Engineering Research Council

C ) postgraduate scholarship mQ a Ddhousie graduate scholarship Funding for this study was provided by an operating grant f rom the NSERC Production Enhancement Network to

ehrents K 1987 The influence of shelter availability on recruitment and early juvenile survivorship of Lythryhbnkcs d d i Gilbert (Pisces Gobiidae) J Exp Mar Biol Ecol

ecruitment stability and survival sample size- specific theory with examples from the early life dynamics of marine fish Dana Rep 7 45-147

Bolz GR and RG Eough 1988 Growth through the first six months of Atlantic cod (Gadus morhm) and haddock (Melanogrammus aeglefinus) based on daily otolith incre- ments Fish Bull $6 223-235

Car MH 1991 Habitat selection and recruitment of an assem- blage of temperate zone reef fishes J Exp Mar Biol Ecol 146 113-137

C m MH 1994 Effects of macroalgal dynamics on recruitment of a temperate reef fish Ecology 75 1320-1333

Chandler CR RR Sanders Jr and AM Landry Jr 1985 Effects of three substrate variables on two artificial reef fish communities Bull Mar Sci 37 129-142

Connel1 SD and GP Jones 1991 The influence of habitat complexity on postrecruitment processes in a temperate reef fish population J Exp Mar Bid Ecol 151 271-294

de Lafontaine Ye T Lambert GR LiHHy WD McKone and RJ Miller (Editors) 1992 Juvenile stages the missing link in fisheries research Can Rch Rep Fish Aquat Sci No 1890

Boherty PJ 1982 Coral reef fishes recruitment-limited assem- blageswaz Proceedings of the Fourth International Coral Reef Symposium Manila The Phillipines VoH 2 pp 465-470

Doherty P-J 1983 Tropical territorial damselfishes is density limited by aggression or recruitment Ecology 64 176-190

Doherty PJ and AJ Fowler 8994 An empirical test of recruitment limitation in a coral reef fish Science (Washington DC) 263 935-939

Fsrrester GE 1990 Factors influencing the juvenile demog- raphy of a coral reef fish population Ecology 71 1666-1681

Gotceitas V and A Brown 1993 Substrate selection by juvenile Atlantic cod (Gadus mor8zua) effects of predation risk Oecologia 93 3 1-37

Henderson PA RHA Holmes and RN Size-selective overwintering mortality in the sand smelt Atkerina boyeri Risso and its role in population regulation J Fish Biol 33 221-233

Hixon MA and JP Beets 1989 Shelter characteristics and Caribbean fish assemblages experiments with artificial reefs Bull Mar Sci 44 666-680

Houde E 1987 Fish early life dynamics and recruitment variability Am Fish Soc Symp Ser 2 17-29

Hunt von Herbing I and W Hunte 1991 Spawning and recruitment of the bluehead wrasse Thakassoma Ea~ascdatum in Barbados WI Mar Ecol Prog Ser 72 49-58

Jones GPe 1986 Food availability affects growth in a coral reef fish Oecologia 70 136-139

Jones GP 1990 The importance of recruitment to the dynamics of a coral reef fish population Ecology 71 1691-1 698

Jones GP 1991 Postrecruitment processes in the ecology of coral reef fish populations a multifactoria2 perspective In The Ecology of fishes on coral reefs Edited by PF Sale Academic Press San Diego Calif pp 294-328

Juanes E 1994 What determines prey size selectivity in pis- civorous fishes Paz Theory and application in fish feeding ecology Edited by DJ Stouder KL Fresh and RJ Feller Belle W Baruch Library in Marine Sciences No 18 University of South Carolina Press Columbia SC

Levin PS 1991 Effects of microhabitat on recruitment vari- ation in a Gulf of Maine reef fish Mar Ecol Prog Ser 75 183-189

Levin PS 1993 Habitat structure conspecific presence and spatial variation in the recruitment of a temperate reef fish Oecologia 94 176-1 85

Lsugh RG PC Valentine DC Potter Pa Auditore GZ Bolz J Neilson and RI Berry 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 1-1 2

Malloy KD and TE Targett 1991 Feeding growth and survival of juvenile summer flounder Parakichthys dentatus experimental analysis of the effects of temperature and salin- ity Mar Ecol Prog Ser 72 213-223

Mattila J 1992 The effect of habitat complexity on predation efficiency of perch Perm fluvinbikis L and suffe Gyrnmo- cephcalus cernuus (L) f Exp Mar Biol Ecol 157 55-67

Milicich MJ MG Meekan and PJ Boherty 1992 Larval supply a good predictor of recruitment of 3 species of reef fish (Pomacentridae) Mar Ecol Psog Ser 86 153- 166

Miller IT LB Crowder JA Rice and EA Marshall 1988 Larval size and recruitment mechanisms in fishes toward a conceptual framework Can J Fish Aquat Sci 45 1657-1670

Pepin P- and RA Myers 1991 Significance of egg and larval size to recruitment variability of temperate marine fish Can Fish Aquat Sci 48 503-5 18

Sale PF WA Douglas and PJ Doherty 1984 Choice of microhabitats by coral reef fishes at settlement Coral Reefs 3 91-99

Shulman M 1985 Recruitment of coral reef fishes effects of distribution of predators and shelter Ecology 66 lOX9-1O66

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Sogard S 1992 Variability in growth rates of juvenile fishes in different estuarine habitats Mar E d Prog Ser 85 35-53

W and FJ Rohlf 1981 Biometry 2nd ed Freeman San Francisco Calif

Sweatman H 1985 The influence of adults of some coral reef fishes on larval recruitment Ecol Monsgr 55 469-485

Sweatrnan H 1988 Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues J Exp Mar B i d Ecol 124 163-174

Tupper M and WG Boutilier 1995 Size and priority at settle- ment determine growth and competitive success of juvenile Atlantic cod Mar Ecol Prog Ser 118 295-308

Tupper M and W Hunte 11994 Recruitment of coral reef fishes to artificial and natural reefs in Barbados WI Mar Ecol Prog Ser 108 225-235

Victor BC 1983 Recruitment and population dynamics of a coral reef fish Science (Washington DC) 219 4 3 9-420

Victor BC 1986 Larval settlement and juvenile mortality in a recmitment-limited coral reef fish population Ecol Monogr 56 145-160

Walsk WJ 1987 Patterns of recruitment and spawning in Hawaiian reef fishes Environ BioB Fishes 4 257-276

Werner EE and D3 Hall 1988 Ontogenetic habitat shifts in bluegill the foraging rate - predation risk trade-off Ecsl- ogy 69 1352-1 366

Wilkinson W 1990 SYSTAT the system for statistics Systat Inc Evansasn 111

Williams DMcB S English and MJ Milicich 1994 Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement Bull Mar Sci 54 314-33 B

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This article has been cited by

1 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek Aysun Gumus 2012 One century of eel growth changesand implications Ecology of Freshwater Fish 213 325-336 [CrossRef]

2 Mary R Ryan Shaun S Killen Robert S Gregory Paul VR Snelgrove 2012 Predators and distance between habitatpatches modify gap crossing behaviour of juvenile Atlantic cod (Gadus morhua L 1758) Journal of Experimental MarineBiology and Ecology 422-423 81-87 [CrossRef]

3 David K A Barnes Kathleen E ConlanThe Dynamic Mosaic 255-290 [CrossRef]

4 Felicity Huntingford Susan Coyle William HunterAvoiding Predators 220-247 [CrossRef]

5 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek 2012 One century of eel growth changes and implications One century of eel growth Ecology Of Freshwater Fish no [CrossRef]

6 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 9107 1403-1412 [CrossRef]

7 Gisle K Sverdrup Justin J Meager Anders Fernouml Jon E Skjaeraasen Petra Rodewald Anne G V Salvanes Torbjoumlrn Jaumlrvi2011 Territorial and agonistic interactions between farmed and wild cod (Gadus morhua) Aquaculture Research 42101539-1548 [CrossRef]

8 Christopher N Rooper Mark E Wilkins Craig S Rose Catherine Coon 2011 Modeling the impacts of bottom trawling andthe subsequent recovery rates of sponges and corals in the Aleutian Islands Alaska Continental Shelf Research [CrossRef]

9 MD Renkawitz RS Gregory DC Schneider 2011 Habitat dependant growth of three species of bottom settling fish ina coastal fjord Journal of Experimental Marine Biology and Ecology [CrossRef]

10 D K Demain A Gallego A Jaworski I G Priede E G Jones 2011 Diet and feeding niches of juvenile Gadus morhuaMelanogrammus aeglefinus and Merlangius merlangus during the settlement transition in the northern North Sea Journalof Fish Biology 791 89-111 [CrossRef]

11 John CaddyHow Artificial Reefs Could Reduce the Impacts of Bottlenecks in Reef Fish Productivity within Natural FractalHabitats 20114347 45-64 [CrossRef]

12 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 917 1403 [CrossRef]

13 Sandra Ramos Pedro Reacute Adriano A Bordalo 2010 Recruitment of flatfish species to an estuarine nursery habitat (Limaestuary NW Iberian Peninsula) Journal of Sea Research 644 473-486 [CrossRef]

14 MA Warren RS Gregory BJ Laurel PVR Snelgrove 2010 Increasing density of juvenile Atlantic (Gadus morhua)and Greenland cod (G ogac) in association with spatial expansion and recovery of eelgrass (Zostera marina) in a coastalnursery habitat Journal of Experimental Marine Biology and Ecology 3941-2 154-160 [CrossRef]

15 R GREGORY LOUGH 2010 Juvenile cod ( Gadus morhua ) mortality and the importance of bottom sediment type torecruitment on Georges Bank Fisheries Oceanography 192 159-181 [CrossRef]

16 Esben Moland Olsen Stephanie M Carlson Jakob Gjoslashsaeter Nils Chr Stenseth 2009 Nine decades of decreasingphenotypic variability in Atlantic cod Ecology Letters 127 622-631 [CrossRef]

17 R J David Wells J O Harper J R Rooker A M Landry T M Dellapenna 2009 Fish assemblage structure on a drownedbarrier island in the northwestern Gulf of Mexico Hydrobiologia 6251 207-221 [CrossRef]

18 Jonathan S F Lee Barry A Berejikian 2009 Structural complexity in relation to the habitat preferences territoriality andhatchery rearing of juvenile China rockfish (Sebastes nebulosus) Environmental Biology of Fishes 844 411-419 [CrossRef]

19 Ann Marie Gorman Robert S Gregory David C Schneider 2009 Eelgrass patch size and proximity to the patch edgeaffect predation risk of recently settled age 0 cod (Gadus) Journal of Experimental Marine Biology and Ecology 3711 1-9[CrossRef]

20 W R Hunter M D J Sayer 2009 The comparative effects of habitat complexity on faunal assemblages of northerntemperate artificial and natural reefs ICES Journal of Marine Science 664 691-698 [CrossRef]

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June Substrate rugosity accounted for 75 of the variance in postsettlement survival ( p lt 00001 Fig 3) In summary despite a uniform pattern of settlement among habitats and locations survival varied significantly between habitats and was positvely correlated with the complexity of the habitat These results suggest that demersal young-of-the- y e a cod in St Margarets ay are limited by the availability of shelter sites and that suitable nursery habitats for age 04- cod should provide an abundance of refugia The fact that population density in a given habitat did not differ between locations presumably reflects a combination of the spatially uniform pattern of cod settlement in St Margarets Bay with a similarity between locations in the postsettlement processes controlling among-habitat variations in population density

Predation om juvenile cod Thee species of Cottidae (Hernitripterus amep-icanus Myoxo- cephalus sctodecemspincasus and Myoxocephalus atmeus) were observed preying on age 0 + cod in St Margarets Bay Because these three species have very similar behav- iours they were pooled as cottid predators Predator den- sities did not vary among habitat types but did vary among locations (two-way NOVA Table 1) A total of 96 predator- prey interactions (attempted captures) were observed dur- ing the course of the study The number of attempted cap- tures did not vary significantly between habitat types or locations (Table I) Ca ture success varied among habi- tats but not among sites (two-way ANOVA Table I) Predators were most successfuH on open sand bottoms and least successful in reef and cobble habitats Capture success on a given transect was not related to predator density (r2 = 009 p gt 03) but was inversely related to substrate rugosity (2 = 074 p lt 0001 Fig 4) Because the among- habitat pattern of capture success is inversely related to the survival of age 0 + cod it appears that predation is a rna~or factor influencing variation among habitats in recruit- ment of young-of-the-year cod

Among-habitat variation in growth There was no difference in mean size at settlement between habitat types or locations (ANOVA F = 143 p gt 005) Significant differences in mean growth rate were observed among habitat types but not among locations (Table I) There was no significant location-by-habitat interaction ( F = 035 p gt 09) At all three locations the growth rate of juvenile cod was highest in seagrass habitats (range 059-067 mm-day-) and lowest on sand bottoms (range 002-006 rnmday-I) Growth rates did not significantly dif- fer between reef (range 838-045 mrnsday-) and cobble (range 035-041 rnmday-) habitats at any of the three locations (Table I)

Discussion

Settlement of youm In this study juven onstrate any pref- erence for habitat type at settlement (Table 1) In contrast to patterns of settlement survival of Quvenile cod varied greatly between habitat types (Table 1) The processes reg- ulating among-habitat variation in juvenile cod density

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Can J Fish Aquat Sci Vol 52 1995

Fig 2 Temporal variation in population density (no of individuals per 15-m transect) of age 0+ cod in four habitat types (rocky reef cobble bottom seagrass beds and sandy bottom) at each of three sites in St Margarets Bay Nova Scotia Error bars represent ampI standard deviation

BACK COVE -I-

I I I I I I

Aprii May J u n e July

Month

( - post settlement period - (

must therefore occur postsettlement with differential sur- vival rather than differential settlement leading to the observed patterns of density In contrast Sale et al (1984) clearly demonstrated that several species of coral reef fish settle preferentially to specific micrshabitats and suggested that spatial variation in microhabitat structure may result in spatial variation in settlement and subsequent recruitment

The relative importance of settlement and postsettlement processes in determining fish-habitat associations is unknown for most species (Jones 1991) Habitat type may influence postsettlement processes to either reinforce or alter spatial patterns established at settlement For example the darnselfish Pomacentrus amboineresks settles preferen- tially in deeper lagoonal waters where its subsequent growth rate and survival are higher than in shallow water

Ion (Jones 1986) In contrast the blennoid fish f i r s f e r j g a ~ r i u m settles uniformly among habitat types differing in structural complexity but exhibits extreme differences in subsequent survival and density which are much higher in more complex habitats (Connell and Jones 1991) This pattern is identical to that exhibited by juvenile cod in this

Fig 3 Effect of substrate rugosity of a transect on postsettlement survival of age 0+ cod Survival is calculated as the percentage of all fish settling onto a given transect that survived until the end of the experiment

0 Reef O Cobble B Grass r Sand

10 15 20 25 30 35 40 45

Substrate Rugosity

study As with E varium among-habitat variation in the sur- vival of juvenile cod radically altered patterns of settlement

The existence of a positive correlation between survival of juvenile fish and habitat complexity is considered evi- dence for space limitation ie intraspecific competition for limited shelter sites (eg Shkalman 1985) In this study the efficiency s f cottid predators decreased with increasing habitat complexity and similar results were observed for predation on amphipods by yellow perch Pema flavescens and mffe Gyrmocephalus cernuus (Mattila 1992) Gotcietas and Brown (1993) found that young-sf-the-year cod kept in aquaria selected more complex substrates in the presence of a predator Thus the relationship between habitat corn- plexity and survival need not be explained solely by corn- petition for living space but can also be attributed to dif- ferential predation among habitat types Thus a very high predator density in more complex habitats could still lead to higher predation mortality in those habitats However in St Margarets Bay predator density did not vary signifi- cantly between habitats As a result survival remained positively correlated with habitat complexity (Fig 3)

Mattila ( 1992) suggests that predation efficiency is not automatically reduced by a high level of habitat complexity per se the prey must be able to utilize that complexity as an effective shelter In this study seagrass beds could con- ceivably provide the greatest complexity of the four habitats if the vertical area of each blade of grass were measured However young-of-the-year cod did not utilize seagrass blades as shelter they preferred rocks empty scallop shells and other debris found within the seagrass beds Considering

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the rapid postsettlement growth rates of young-of-the-year cod it seems probable that they essentially outgrow seagrass blades as a suitable refuge soon after settlement Connell and Jones (1991) hypothesized that the lack of habitat- specific settlement in E varkwn may be due to settlement- sized fish finding adequate shelter in a wide range of habi- tats while habitat-specific mortality may arise when settled fish outgrow suitable shelter in habitats of lower com- plexity This hypothesis fits our findings for young-of-the- year cod equally well If cod at their smallest sizes can find shelter in all habitats more or less equally differences in set- tlement strength between habitats would not be expected Patterns of distribution in juvenile cod populations would then be determined by habitat-specific predation pressure Lough et al (1989) offered a similar hypothesis to explain the demography of young-of-the-year cod and haddock on Georges Bank They observed that pelagic juvenile gadids were widespread over the bank in June but that in July demersal juveniles were found mainly on pebble-gravel beds and were poorly represented on other less complex sedimentary substrates They also suggested that in addition to providing more shelter sites than the other substrates the pebble-gravel deposits most closely matched the mottled colouring of demersal juvenile cod making the small fish very difficult to see and therefore reducing their predation risk From these results Lough et al (1989) concluded that the availability of a complex habitat with reduced pre- dation pressure may be critical to the recruitment success of cod and haddock on Georges Bank

uence of habitat structure on The growth rates of young-of-the-ye

han previously published values for fish of this 01 and Lough (1988) reported growth rates of

071 mrnday- for cod of 31 mm standard length to 109 mm-day- for cod of 67 mm standard length In the present study mean growth rate over all habitats was approximately 04 mm-day- However Bolz and Lough studied populations on Georges Bank during the summer and fall months these fish were growing at higher tem- peratures than the spring cohort of young-of-the-year cod from St Margarets Bay

Connell and Jones (1991) suggested that habitat corn- plexity may influence the growth and survival of juvenile fish through increased prey density and prey diversity The growth rate of young-of-the-year cod in this study differed between habitats but was not related to substrate mgosity per se However as discussed in the previous section the shelter provided by vegetation was mot accounted for in this measure of complexity For small prey items seagrass beds undoubtedly offer the greatest habitat complexity For example Sogard (1992) reported that the presence of seagrass beds increased copepod densities by 49 and amphipod densities by 64 Thus if habitat complexity is measured with regard to prey size rather than predator size then prey densities and predator growth rates should increase in more complex habitats

In this study young-of-the-year cod experienced elevated growth rates in seagrass beds (presumably because of the higher prey densities within this habitat) but experienced significantly reduced predation risk in rocky reef and cobble

Fig 4 The effect of substrate rugosity on capture success of cottid predators on age 0+ cod Capture success is calculated as the number of successful captures divided by the number of attempted captures

0 Reef O Cobble v Grass

Substrate Rugosity

habitats It remains unclear which strategy is the more advantageous for young-of-the-yea cod Several researchers (Werner and Hall 1988 Connell and Jones 1991 Sogard 1992) have suggested the possibility of trade-offs in habitat utilization by fish Present ecological theory tells us that fish should select for the habitat that maximizes energy gain (growth) while minimizing the risk of mortality Cod in St Margarets Bay appear to lose their site fidelity by their first winter at which point they disperse from shallow nearshore habitats presumably joining the older juvenile population in deeper warmer water (Tup 1995) The greatest numbers of fish undergoing this migra- tion will be from complex hard-bottom habitats (reef and cobble) while the largest individuals will be from sea- grass habitats Overwinter survival of several temperate fishes has been demonstrated to be size dependent with the largest individuals surviving best (Henderson et a 1988) Thus one can foresee a scenario in which one habitat supplies 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 Further research is needed to establish the relative importance of these dif- fering strategies to the population dynamics of Atlantic cod

Conclusions Over the past decade studies of demersal marine fish recruitment have generally concluded that recruitment vari- ation results mainly from stochastic I m a l survival (DoheHty 1982 1983 Victor 1983 1986 Houde 1987 Miller et al 1988 Beyer 1989 Pepin and Myers 1991 Milicich et al 1992 Boherty and Fowler 1994) Recently a more plu- ralistic view has been suggested in which both pre- and post-settlement events a e considered important in regulating adult population size (Forrester 1990 Jones 1990 Jones 1991 Hunt von Herbing and Hunte 199 1 Tupper and

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Hunte 1994 Tupper and Boutilier 1995) The relative ortance or pre- and post-settlement events in deter- ing recruitment strength will vary with location time

and habitat (Jones 1996 Cswraell and Jones 199 1) While almost all research in this field has been conducted on coral reef fishes similar me s seem to apply to y o u n g - o f - t e e Atlantic cod tudy spatid patterns of settlement of cod were completely altered by habitat- specific postsettlement mortality In addition growth rates of young-of-the-year cod were influenced by habitat type which may in turn influence overwinter survivaI However in yews or locations in which larval survival and settlement were very low the importance of these gostsettlement processes would likely decrease and the abundance of young-of-the-year cod would be regulated mainly by larval input Longer term studies are needed to assess the impsr- tance of pre- and post-settlement events over several y e a s (Forrester 1990 Jones 1990)

1 Hunt von Herbing and R Conrad provided assistance in the field This study is a contribution s f the Ocean Pro- duction Enhancement Network MT was funded by a Natural Sciences and Engineering Research Council

C ) postgraduate scholarship mQ a Ddhousie graduate scholarship Funding for this study was provided by an operating grant f rom the NSERC Production Enhancement Network to

ehrents K 1987 The influence of shelter availability on recruitment and early juvenile survivorship of Lythryhbnkcs d d i Gilbert (Pisces Gobiidae) J Exp Mar Biol Ecol

ecruitment stability and survival sample size- specific theory with examples from the early life dynamics of marine fish Dana Rep 7 45-147

Bolz GR and RG Eough 1988 Growth through the first six months of Atlantic cod (Gadus morhm) and haddock (Melanogrammus aeglefinus) based on daily otolith incre- ments Fish Bull $6 223-235

Car MH 1991 Habitat selection and recruitment of an assem- blage of temperate zone reef fishes J Exp Mar Biol Ecol 146 113-137

C m MH 1994 Effects of macroalgal dynamics on recruitment of a temperate reef fish Ecology 75 1320-1333

Chandler CR RR Sanders Jr and AM Landry Jr 1985 Effects of three substrate variables on two artificial reef fish communities Bull Mar Sci 37 129-142

Connel1 SD and GP Jones 1991 The influence of habitat complexity on postrecruitment processes in a temperate reef fish population J Exp Mar Bid Ecol 151 271-294

de Lafontaine Ye T Lambert GR LiHHy WD McKone and RJ Miller (Editors) 1992 Juvenile stages the missing link in fisheries research Can Rch Rep Fish Aquat Sci No 1890

Boherty PJ 1982 Coral reef fishes recruitment-limited assem- blageswaz Proceedings of the Fourth International Coral Reef Symposium Manila The Phillipines VoH 2 pp 465-470

Doherty P-J 1983 Tropical territorial damselfishes is density limited by aggression or recruitment Ecology 64 176-190

Doherty PJ and AJ Fowler 8994 An empirical test of recruitment limitation in a coral reef fish Science (Washington DC) 263 935-939

Fsrrester GE 1990 Factors influencing the juvenile demog- raphy of a coral reef fish population Ecology 71 1666-1681

Gotceitas V and A Brown 1993 Substrate selection by juvenile Atlantic cod (Gadus mor8zua) effects of predation risk Oecologia 93 3 1-37

Henderson PA RHA Holmes and RN Size-selective overwintering mortality in the sand smelt Atkerina boyeri Risso and its role in population regulation J Fish Biol 33 221-233

Hixon MA and JP Beets 1989 Shelter characteristics and Caribbean fish assemblages experiments with artificial reefs Bull Mar Sci 44 666-680

Houde E 1987 Fish early life dynamics and recruitment variability Am Fish Soc Symp Ser 2 17-29

Hunt von Herbing I and W Hunte 1991 Spawning and recruitment of the bluehead wrasse Thakassoma Ea~ascdatum in Barbados WI Mar Ecol Prog Ser 72 49-58

Jones GPe 1986 Food availability affects growth in a coral reef fish Oecologia 70 136-139

Jones GP 1990 The importance of recruitment to the dynamics of a coral reef fish population Ecology 71 1691-1 698

Jones GP 1991 Postrecruitment processes in the ecology of coral reef fish populations a multifactoria2 perspective In The Ecology of fishes on coral reefs Edited by PF Sale Academic Press San Diego Calif pp 294-328

Juanes E 1994 What determines prey size selectivity in pis- civorous fishes Paz Theory and application in fish feeding ecology Edited by DJ Stouder KL Fresh and RJ Feller Belle W Baruch Library in Marine Sciences No 18 University of South Carolina Press Columbia SC

Levin PS 1991 Effects of microhabitat on recruitment vari- ation in a Gulf of Maine reef fish Mar Ecol Prog Ser 75 183-189

Levin PS 1993 Habitat structure conspecific presence and spatial variation in the recruitment of a temperate reef fish Oecologia 94 176-1 85

Lsugh RG PC Valentine DC Potter Pa Auditore GZ Bolz J Neilson and RI Berry 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 1-1 2

Malloy KD and TE Targett 1991 Feeding growth and survival of juvenile summer flounder Parakichthys dentatus experimental analysis of the effects of temperature and salin- ity Mar Ecol Prog Ser 72 213-223

Mattila J 1992 The effect of habitat complexity on predation efficiency of perch Perm fluvinbikis L and suffe Gyrnmo- cephcalus cernuus (L) f Exp Mar Biol Ecol 157 55-67

Milicich MJ MG Meekan and PJ Boherty 1992 Larval supply a good predictor of recruitment of 3 species of reef fish (Pomacentridae) Mar Ecol Psog Ser 86 153- 166

Miller IT LB Crowder JA Rice and EA Marshall 1988 Larval size and recruitment mechanisms in fishes toward a conceptual framework Can J Fish Aquat Sci 45 1657-1670

Pepin P- and RA Myers 1991 Significance of egg and larval size to recruitment variability of temperate marine fish Can Fish Aquat Sci 48 503-5 18

Sale PF WA Douglas and PJ Doherty 1984 Choice of microhabitats by coral reef fishes at settlement Coral Reefs 3 91-99

Shulman M 1985 Recruitment of coral reef fishes effects of distribution of predators and shelter Ecology 66 lOX9-1O66

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Sogard S 1992 Variability in growth rates of juvenile fishes in different estuarine habitats Mar E d Prog Ser 85 35-53

W and FJ Rohlf 1981 Biometry 2nd ed Freeman San Francisco Calif

Sweatman H 1985 The influence of adults of some coral reef fishes on larval recruitment Ecol Monsgr 55 469-485

Sweatrnan H 1988 Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues J Exp Mar B i d Ecol 124 163-174

Tupper M and WG Boutilier 1995 Size and priority at settle- ment determine growth and competitive success of juvenile Atlantic cod Mar Ecol Prog Ser 118 295-308

Tupper M and W Hunte 11994 Recruitment of coral reef fishes to artificial and natural reefs in Barbados WI Mar Ecol Prog Ser 108 225-235

Victor BC 1983 Recruitment and population dynamics of a coral reef fish Science (Washington DC) 219 4 3 9-420

Victor BC 1986 Larval settlement and juvenile mortality in a recmitment-limited coral reef fish population Ecol Monogr 56 145-160

Walsk WJ 1987 Patterns of recruitment and spawning in Hawaiian reef fishes Environ BioB Fishes 4 257-276

Werner EE and D3 Hall 1988 Ontogenetic habitat shifts in bluegill the foraging rate - predation risk trade-off Ecsl- ogy 69 1352-1 366

Wilkinson W 1990 SYSTAT the system for statistics Systat Inc Evansasn 111

Williams DMcB S English and MJ Milicich 1994 Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement Bull Mar Sci 54 314-33 B

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This article has been cited by

1 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek Aysun Gumus 2012 One century of eel growth changesand implications Ecology of Freshwater Fish 213 325-336 [CrossRef]

2 Mary R Ryan Shaun S Killen Robert S Gregory Paul VR Snelgrove 2012 Predators and distance between habitatpatches modify gap crossing behaviour of juvenile Atlantic cod (Gadus morhua L 1758) Journal of Experimental MarineBiology and Ecology 422-423 81-87 [CrossRef]

3 David K A Barnes Kathleen E ConlanThe Dynamic Mosaic 255-290 [CrossRef]

4 Felicity Huntingford Susan Coyle William HunterAvoiding Predators 220-247 [CrossRef]

5 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek 2012 One century of eel growth changes and implications One century of eel growth Ecology Of Freshwater Fish no [CrossRef]

6 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 9107 1403-1412 [CrossRef]

7 Gisle K Sverdrup Justin J Meager Anders Fernouml Jon E Skjaeraasen Petra Rodewald Anne G V Salvanes Torbjoumlrn Jaumlrvi2011 Territorial and agonistic interactions between farmed and wild cod (Gadus morhua) Aquaculture Research 42101539-1548 [CrossRef]

8 Christopher N Rooper Mark E Wilkins Craig S Rose Catherine Coon 2011 Modeling the impacts of bottom trawling andthe subsequent recovery rates of sponges and corals in the Aleutian Islands Alaska Continental Shelf Research [CrossRef]

9 MD Renkawitz RS Gregory DC Schneider 2011 Habitat dependant growth of three species of bottom settling fish ina coastal fjord Journal of Experimental Marine Biology and Ecology [CrossRef]

10 D K Demain A Gallego A Jaworski I G Priede E G Jones 2011 Diet and feeding niches of juvenile Gadus morhuaMelanogrammus aeglefinus and Merlangius merlangus during the settlement transition in the northern North Sea Journalof Fish Biology 791 89-111 [CrossRef]

11 John CaddyHow Artificial Reefs Could Reduce the Impacts of Bottlenecks in Reef Fish Productivity within Natural FractalHabitats 20114347 45-64 [CrossRef]

12 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 917 1403 [CrossRef]

13 Sandra Ramos Pedro Reacute Adriano A Bordalo 2010 Recruitment of flatfish species to an estuarine nursery habitat (Limaestuary NW Iberian Peninsula) Journal of Sea Research 644 473-486 [CrossRef]

14 MA Warren RS Gregory BJ Laurel PVR Snelgrove 2010 Increasing density of juvenile Atlantic (Gadus morhua)and Greenland cod (G ogac) in association with spatial expansion and recovery of eelgrass (Zostera marina) in a coastalnursery habitat Journal of Experimental Marine Biology and Ecology 3941-2 154-160 [CrossRef]

15 R GREGORY LOUGH 2010 Juvenile cod ( Gadus morhua ) mortality and the importance of bottom sediment type torecruitment on Georges Bank Fisheries Oceanography 192 159-181 [CrossRef]

16 Esben Moland Olsen Stephanie M Carlson Jakob Gjoslashsaeter Nils Chr Stenseth 2009 Nine decades of decreasingphenotypic variability in Atlantic cod Ecology Letters 127 622-631 [CrossRef]

17 R J David Wells J O Harper J R Rooker A M Landry T M Dellapenna 2009 Fish assemblage structure on a drownedbarrier island in the northwestern Gulf of Mexico Hydrobiologia 6251 207-221 [CrossRef]

18 Jonathan S F Lee Barry A Berejikian 2009 Structural complexity in relation to the habitat preferences territoriality andhatchery rearing of juvenile China rockfish (Sebastes nebulosus) Environmental Biology of Fishes 844 411-419 [CrossRef]

19 Ann Marie Gorman Robert S Gregory David C Schneider 2009 Eelgrass patch size and proximity to the patch edgeaffect predation risk of recently settled age 0 cod (Gadus) Journal of Experimental Marine Biology and Ecology 3711 1-9[CrossRef]

20 W R Hunter M D J Sayer 2009 The comparative effects of habitat complexity on faunal assemblages of northerntemperate artificial and natural reefs ICES Journal of Marine Science 664 691-698 [CrossRef]

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Can J Fish Aquat Sci Vol 52 1995

Fig 2 Temporal variation in population density (no of individuals per 15-m transect) of age 0+ cod in four habitat types (rocky reef cobble bottom seagrass beds and sandy bottom) at each of three sites in St Margarets Bay Nova Scotia Error bars represent ampI standard deviation

BACK COVE -I-

I I I I I I

Aprii May J u n e July

Month

( - post settlement period - (

must therefore occur postsettlement with differential sur- vival rather than differential settlement leading to the observed patterns of density In contrast Sale et al (1984) clearly demonstrated that several species of coral reef fish settle preferentially to specific micrshabitats and suggested that spatial variation in microhabitat structure may result in spatial variation in settlement and subsequent recruitment

The relative importance of settlement and postsettlement processes in determining fish-habitat associations is unknown for most species (Jones 1991) Habitat type may influence postsettlement processes to either reinforce or alter spatial patterns established at settlement For example the darnselfish Pomacentrus amboineresks settles preferen- tially in deeper lagoonal waters where its subsequent growth rate and survival are higher than in shallow water

Ion (Jones 1986) In contrast the blennoid fish f i r s f e r j g a ~ r i u m settles uniformly among habitat types differing in structural complexity but exhibits extreme differences in subsequent survival and density which are much higher in more complex habitats (Connell and Jones 1991) This pattern is identical to that exhibited by juvenile cod in this

Fig 3 Effect of substrate rugosity of a transect on postsettlement survival of age 0+ cod Survival is calculated as the percentage of all fish settling onto a given transect that survived until the end of the experiment

0 Reef O Cobble B Grass r Sand

10 15 20 25 30 35 40 45

Substrate Rugosity

study As with E varium among-habitat variation in the sur- vival of juvenile cod radically altered patterns of settlement

The existence of a positive correlation between survival of juvenile fish and habitat complexity is considered evi- dence for space limitation ie intraspecific competition for limited shelter sites (eg Shkalman 1985) In this study the efficiency s f cottid predators decreased with increasing habitat complexity and similar results were observed for predation on amphipods by yellow perch Pema flavescens and mffe Gyrmocephalus cernuus (Mattila 1992) Gotcietas and Brown (1993) found that young-sf-the-year cod kept in aquaria selected more complex substrates in the presence of a predator Thus the relationship between habitat corn- plexity and survival need not be explained solely by corn- petition for living space but can also be attributed to dif- ferential predation among habitat types Thus a very high predator density in more complex habitats could still lead to higher predation mortality in those habitats However in St Margarets Bay predator density did not vary signifi- cantly between habitats As a result survival remained positively correlated with habitat complexity (Fig 3)

Mattila ( 1992) suggests that predation efficiency is not automatically reduced by a high level of habitat complexity per se the prey must be able to utilize that complexity as an effective shelter In this study seagrass beds could con- ceivably provide the greatest complexity of the four habitats if the vertical area of each blade of grass were measured However young-of-the-year cod did not utilize seagrass blades as shelter they preferred rocks empty scallop shells and other debris found within the seagrass beds Considering

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the rapid postsettlement growth rates of young-of-the-year cod it seems probable that they essentially outgrow seagrass blades as a suitable refuge soon after settlement Connell and Jones (1991) hypothesized that the lack of habitat- specific settlement in E varkwn may be due to settlement- sized fish finding adequate shelter in a wide range of habi- tats while habitat-specific mortality may arise when settled fish outgrow suitable shelter in habitats of lower com- plexity This hypothesis fits our findings for young-of-the- year cod equally well If cod at their smallest sizes can find shelter in all habitats more or less equally differences in set- tlement strength between habitats would not be expected Patterns of distribution in juvenile cod populations would then be determined by habitat-specific predation pressure Lough et al (1989) offered a similar hypothesis to explain the demography of young-of-the-year cod and haddock on Georges Bank They observed that pelagic juvenile gadids were widespread over the bank in June but that in July demersal juveniles were found mainly on pebble-gravel beds and were poorly represented on other less complex sedimentary substrates They also suggested that in addition to providing more shelter sites than the other substrates the pebble-gravel deposits most closely matched the mottled colouring of demersal juvenile cod making the small fish very difficult to see and therefore reducing their predation risk From these results Lough et al (1989) concluded that the availability of a complex habitat with reduced pre- dation pressure may be critical to the recruitment success of cod and haddock on Georges Bank

uence of habitat structure on The growth rates of young-of-the-ye

han previously published values for fish of this 01 and Lough (1988) reported growth rates of

071 mrnday- for cod of 31 mm standard length to 109 mm-day- for cod of 67 mm standard length In the present study mean growth rate over all habitats was approximately 04 mm-day- However Bolz and Lough studied populations on Georges Bank during the summer and fall months these fish were growing at higher tem- peratures than the spring cohort of young-of-the-year cod from St Margarets Bay

Connell and Jones (1991) suggested that habitat corn- plexity may influence the growth and survival of juvenile fish through increased prey density and prey diversity The growth rate of young-of-the-year cod in this study differed between habitats but was not related to substrate mgosity per se However as discussed in the previous section the shelter provided by vegetation was mot accounted for in this measure of complexity For small prey items seagrass beds undoubtedly offer the greatest habitat complexity For example Sogard (1992) reported that the presence of seagrass beds increased copepod densities by 49 and amphipod densities by 64 Thus if habitat complexity is measured with regard to prey size rather than predator size then prey densities and predator growth rates should increase in more complex habitats

In this study young-of-the-year cod experienced elevated growth rates in seagrass beds (presumably because of the higher prey densities within this habitat) but experienced significantly reduced predation risk in rocky reef and cobble

Fig 4 The effect of substrate rugosity on capture success of cottid predators on age 0+ cod Capture success is calculated as the number of successful captures divided by the number of attempted captures

0 Reef O Cobble v Grass

Substrate Rugosity

habitats It remains unclear which strategy is the more advantageous for young-of-the-yea cod Several researchers (Werner and Hall 1988 Connell and Jones 1991 Sogard 1992) have suggested the possibility of trade-offs in habitat utilization by fish Present ecological theory tells us that fish should select for the habitat that maximizes energy gain (growth) while minimizing the risk of mortality Cod in St Margarets Bay appear to lose their site fidelity by their first winter at which point they disperse from shallow nearshore habitats presumably joining the older juvenile population in deeper warmer water (Tup 1995) The greatest numbers of fish undergoing this migra- tion will be from complex hard-bottom habitats (reef and cobble) while the largest individuals will be from sea- grass habitats Overwinter survival of several temperate fishes has been demonstrated to be size dependent with the largest individuals surviving best (Henderson et a 1988) Thus one can foresee a scenario in which one habitat supplies 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 Further research is needed to establish the relative importance of these dif- fering strategies to the population dynamics of Atlantic cod

Conclusions Over the past decade studies of demersal marine fish recruitment have generally concluded that recruitment vari- ation results mainly from stochastic I m a l survival (DoheHty 1982 1983 Victor 1983 1986 Houde 1987 Miller et al 1988 Beyer 1989 Pepin and Myers 1991 Milicich et al 1992 Boherty and Fowler 1994) Recently a more plu- ralistic view has been suggested in which both pre- and post-settlement events a e considered important in regulating adult population size (Forrester 1990 Jones 1990 Jones 1991 Hunt von Herbing and Hunte 199 1 Tupper and

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Can J Fish Aejuat Sci Vol 52 199

Hunte 1994 Tupper and Boutilier 1995) The relative ortance or pre- and post-settlement events in deter- ing recruitment strength will vary with location time

and habitat (Jones 1996 Cswraell and Jones 199 1) While almost all research in this field has been conducted on coral reef fishes similar me s seem to apply to y o u n g - o f - t e e Atlantic cod tudy spatid patterns of settlement of cod were completely altered by habitat- specific postsettlement mortality In addition growth rates of young-of-the-year cod were influenced by habitat type which may in turn influence overwinter survivaI However in yews or locations in which larval survival and settlement were very low the importance of these gostsettlement processes would likely decrease and the abundance of young-of-the-year cod would be regulated mainly by larval input Longer term studies are needed to assess the impsr- tance of pre- and post-settlement events over several y e a s (Forrester 1990 Jones 1990)

1 Hunt von Herbing and R Conrad provided assistance in the field This study is a contribution s f the Ocean Pro- duction Enhancement Network MT was funded by a Natural Sciences and Engineering Research Council

C ) postgraduate scholarship mQ a Ddhousie graduate scholarship Funding for this study was provided by an operating grant f rom the NSERC Production Enhancement Network to

ehrents K 1987 The influence of shelter availability on recruitment and early juvenile survivorship of Lythryhbnkcs d d i Gilbert (Pisces Gobiidae) J Exp Mar Biol Ecol

ecruitment stability and survival sample size- specific theory with examples from the early life dynamics of marine fish Dana Rep 7 45-147

Bolz GR and RG Eough 1988 Growth through the first six months of Atlantic cod (Gadus morhm) and haddock (Melanogrammus aeglefinus) based on daily otolith incre- ments Fish Bull $6 223-235

Car MH 1991 Habitat selection and recruitment of an assem- blage of temperate zone reef fishes J Exp Mar Biol Ecol 146 113-137

C m MH 1994 Effects of macroalgal dynamics on recruitment of a temperate reef fish Ecology 75 1320-1333

Chandler CR RR Sanders Jr and AM Landry Jr 1985 Effects of three substrate variables on two artificial reef fish communities Bull Mar Sci 37 129-142

Connel1 SD and GP Jones 1991 The influence of habitat complexity on postrecruitment processes in a temperate reef fish population J Exp Mar Bid Ecol 151 271-294

de Lafontaine Ye T Lambert GR LiHHy WD McKone and RJ Miller (Editors) 1992 Juvenile stages the missing link in fisheries research Can Rch Rep Fish Aquat Sci No 1890

Boherty PJ 1982 Coral reef fishes recruitment-limited assem- blageswaz Proceedings of the Fourth International Coral Reef Symposium Manila The Phillipines VoH 2 pp 465-470

Doherty P-J 1983 Tropical territorial damselfishes is density limited by aggression or recruitment Ecology 64 176-190

Doherty PJ and AJ Fowler 8994 An empirical test of recruitment limitation in a coral reef fish Science (Washington DC) 263 935-939

Fsrrester GE 1990 Factors influencing the juvenile demog- raphy of a coral reef fish population Ecology 71 1666-1681

Gotceitas V and A Brown 1993 Substrate selection by juvenile Atlantic cod (Gadus mor8zua) effects of predation risk Oecologia 93 3 1-37

Henderson PA RHA Holmes and RN Size-selective overwintering mortality in the sand smelt Atkerina boyeri Risso and its role in population regulation J Fish Biol 33 221-233

Hixon MA and JP Beets 1989 Shelter characteristics and Caribbean fish assemblages experiments with artificial reefs Bull Mar Sci 44 666-680

Houde E 1987 Fish early life dynamics and recruitment variability Am Fish Soc Symp Ser 2 17-29

Hunt von Herbing I and W Hunte 1991 Spawning and recruitment of the bluehead wrasse Thakassoma Ea~ascdatum in Barbados WI Mar Ecol Prog Ser 72 49-58

Jones GPe 1986 Food availability affects growth in a coral reef fish Oecologia 70 136-139

Jones GP 1990 The importance of recruitment to the dynamics of a coral reef fish population Ecology 71 1691-1 698

Jones GP 1991 Postrecruitment processes in the ecology of coral reef fish populations a multifactoria2 perspective In The Ecology of fishes on coral reefs Edited by PF Sale Academic Press San Diego Calif pp 294-328

Juanes E 1994 What determines prey size selectivity in pis- civorous fishes Paz Theory and application in fish feeding ecology Edited by DJ Stouder KL Fresh and RJ Feller Belle W Baruch Library in Marine Sciences No 18 University of South Carolina Press Columbia SC

Levin PS 1991 Effects of microhabitat on recruitment vari- ation in a Gulf of Maine reef fish Mar Ecol Prog Ser 75 183-189

Levin PS 1993 Habitat structure conspecific presence and spatial variation in the recruitment of a temperate reef fish Oecologia 94 176-1 85

Lsugh RG PC Valentine DC Potter Pa Auditore GZ Bolz J Neilson and RI Berry 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 1-1 2

Malloy KD and TE Targett 1991 Feeding growth and survival of juvenile summer flounder Parakichthys dentatus experimental analysis of the effects of temperature and salin- ity Mar Ecol Prog Ser 72 213-223

Mattila J 1992 The effect of habitat complexity on predation efficiency of perch Perm fluvinbikis L and suffe Gyrnmo- cephcalus cernuus (L) f Exp Mar Biol Ecol 157 55-67

Milicich MJ MG Meekan and PJ Boherty 1992 Larval supply a good predictor of recruitment of 3 species of reef fish (Pomacentridae) Mar Ecol Psog Ser 86 153- 166

Miller IT LB Crowder JA Rice and EA Marshall 1988 Larval size and recruitment mechanisms in fishes toward a conceptual framework Can J Fish Aquat Sci 45 1657-1670

Pepin P- and RA Myers 1991 Significance of egg and larval size to recruitment variability of temperate marine fish Can Fish Aquat Sci 48 503-5 18

Sale PF WA Douglas and PJ Doherty 1984 Choice of microhabitats by coral reef fishes at settlement Coral Reefs 3 91-99

Shulman M 1985 Recruitment of coral reef fishes effects of distribution of predators and shelter Ecology 66 lOX9-1O66

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Sogard S 1992 Variability in growth rates of juvenile fishes in different estuarine habitats Mar E d Prog Ser 85 35-53

W and FJ Rohlf 1981 Biometry 2nd ed Freeman San Francisco Calif

Sweatman H 1985 The influence of adults of some coral reef fishes on larval recruitment Ecol Monsgr 55 469-485

Sweatrnan H 1988 Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues J Exp Mar B i d Ecol 124 163-174

Tupper M and WG Boutilier 1995 Size and priority at settle- ment determine growth and competitive success of juvenile Atlantic cod Mar Ecol Prog Ser 118 295-308

Tupper M and W Hunte 11994 Recruitment of coral reef fishes to artificial and natural reefs in Barbados WI Mar Ecol Prog Ser 108 225-235

Victor BC 1983 Recruitment and population dynamics of a coral reef fish Science (Washington DC) 219 4 3 9-420

Victor BC 1986 Larval settlement and juvenile mortality in a recmitment-limited coral reef fish population Ecol Monogr 56 145-160

Walsk WJ 1987 Patterns of recruitment and spawning in Hawaiian reef fishes Environ BioB Fishes 4 257-276

Werner EE and D3 Hall 1988 Ontogenetic habitat shifts in bluegill the foraging rate - predation risk trade-off Ecsl- ogy 69 1352-1 366

Wilkinson W 1990 SYSTAT the system for statistics Systat Inc Evansasn 111

Williams DMcB S English and MJ Milicich 1994 Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement Bull Mar Sci 54 314-33 B

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Tupper and Boutilier

the rapid postsettlement growth rates of young-of-the-year cod it seems probable that they essentially outgrow seagrass blades as a suitable refuge soon after settlement Connell and Jones (1991) hypothesized that the lack of habitat- specific settlement in E varkwn may be due to settlement- sized fish finding adequate shelter in a wide range of habi- tats while habitat-specific mortality may arise when settled fish outgrow suitable shelter in habitats of lower com- plexity This hypothesis fits our findings for young-of-the- year cod equally well If cod at their smallest sizes can find shelter in all habitats more or less equally differences in set- tlement strength between habitats would not be expected Patterns of distribution in juvenile cod populations would then be determined by habitat-specific predation pressure Lough et al (1989) offered a similar hypothesis to explain the demography of young-of-the-year cod and haddock on Georges Bank They observed that pelagic juvenile gadids were widespread over the bank in June but that in July demersal juveniles were found mainly on pebble-gravel beds and were poorly represented on other less complex sedimentary substrates They also suggested that in addition to providing more shelter sites than the other substrates the pebble-gravel deposits most closely matched the mottled colouring of demersal juvenile cod making the small fish very difficult to see and therefore reducing their predation risk From these results Lough et al (1989) concluded that the availability of a complex habitat with reduced pre- dation pressure may be critical to the recruitment success of cod and haddock on Georges Bank

uence of habitat structure on The growth rates of young-of-the-ye

han previously published values for fish of this 01 and Lough (1988) reported growth rates of

071 mrnday- for cod of 31 mm standard length to 109 mm-day- for cod of 67 mm standard length In the present study mean growth rate over all habitats was approximately 04 mm-day- However Bolz and Lough studied populations on Georges Bank during the summer and fall months these fish were growing at higher tem- peratures than the spring cohort of young-of-the-year cod from St Margarets Bay

Connell and Jones (1991) suggested that habitat corn- plexity may influence the growth and survival of juvenile fish through increased prey density and prey diversity The growth rate of young-of-the-year cod in this study differed between habitats but was not related to substrate mgosity per se However as discussed in the previous section the shelter provided by vegetation was mot accounted for in this measure of complexity For small prey items seagrass beds undoubtedly offer the greatest habitat complexity For example Sogard (1992) reported that the presence of seagrass beds increased copepod densities by 49 and amphipod densities by 64 Thus if habitat complexity is measured with regard to prey size rather than predator size then prey densities and predator growth rates should increase in more complex habitats

In this study young-of-the-year cod experienced elevated growth rates in seagrass beds (presumably because of the higher prey densities within this habitat) but experienced significantly reduced predation risk in rocky reef and cobble

Fig 4 The effect of substrate rugosity on capture success of cottid predators on age 0+ cod Capture success is calculated as the number of successful captures divided by the number of attempted captures

0 Reef O Cobble v Grass

Substrate Rugosity

habitats It remains unclear which strategy is the more advantageous for young-of-the-yea cod Several researchers (Werner and Hall 1988 Connell and Jones 1991 Sogard 1992) have suggested the possibility of trade-offs in habitat utilization by fish Present ecological theory tells us that fish should select for the habitat that maximizes energy gain (growth) while minimizing the risk of mortality Cod in St Margarets Bay appear to lose their site fidelity by their first winter at which point they disperse from shallow nearshore habitats presumably joining the older juvenile population in deeper warmer water (Tup 1995) The greatest numbers of fish undergoing this migra- tion will be from complex hard-bottom habitats (reef and cobble) while the largest individuals will be from sea- grass habitats Overwinter survival of several temperate fishes has been demonstrated to be size dependent with the largest individuals surviving best (Henderson et a 1988) Thus one can foresee a scenario in which one habitat supplies 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 Further research is needed to establish the relative importance of these dif- fering strategies to the population dynamics of Atlantic cod

Conclusions Over the past decade studies of demersal marine fish recruitment have generally concluded that recruitment vari- ation results mainly from stochastic I m a l survival (DoheHty 1982 1983 Victor 1983 1986 Houde 1987 Miller et al 1988 Beyer 1989 Pepin and Myers 1991 Milicich et al 1992 Boherty and Fowler 1994) Recently a more plu- ralistic view has been suggested in which both pre- and post-settlement events a e considered important in regulating adult population size (Forrester 1990 Jones 1990 Jones 1991 Hunt von Herbing and Hunte 199 1 Tupper and

Can

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oade

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Can J Fish Aejuat Sci Vol 52 199

Hunte 1994 Tupper and Boutilier 1995) The relative ortance or pre- and post-settlement events in deter- ing recruitment strength will vary with location time

and habitat (Jones 1996 Cswraell and Jones 199 1) While almost all research in this field has been conducted on coral reef fishes similar me s seem to apply to y o u n g - o f - t e e Atlantic cod tudy spatid patterns of settlement of cod were completely altered by habitat- specific postsettlement mortality In addition growth rates of young-of-the-year cod were influenced by habitat type which may in turn influence overwinter survivaI However in yews or locations in which larval survival and settlement were very low the importance of these gostsettlement processes would likely decrease and the abundance of young-of-the-year cod would be regulated mainly by larval input Longer term studies are needed to assess the impsr- tance of pre- and post-settlement events over several y e a s (Forrester 1990 Jones 1990)

1 Hunt von Herbing and R Conrad provided assistance in the field This study is a contribution s f the Ocean Pro- duction Enhancement Network MT was funded by a Natural Sciences and Engineering Research Council

C ) postgraduate scholarship mQ a Ddhousie graduate scholarship Funding for this study was provided by an operating grant f rom the NSERC Production Enhancement Network to

ehrents K 1987 The influence of shelter availability on recruitment and early juvenile survivorship of Lythryhbnkcs d d i Gilbert (Pisces Gobiidae) J Exp Mar Biol Ecol

ecruitment stability and survival sample size- specific theory with examples from the early life dynamics of marine fish Dana Rep 7 45-147

Bolz GR and RG Eough 1988 Growth through the first six months of Atlantic cod (Gadus morhm) and haddock (Melanogrammus aeglefinus) based on daily otolith incre- ments Fish Bull $6 223-235

Car MH 1991 Habitat selection and recruitment of an assem- blage of temperate zone reef fishes J Exp Mar Biol Ecol 146 113-137

C m MH 1994 Effects of macroalgal dynamics on recruitment of a temperate reef fish Ecology 75 1320-1333

Chandler CR RR Sanders Jr and AM Landry Jr 1985 Effects of three substrate variables on two artificial reef fish communities Bull Mar Sci 37 129-142

Connel1 SD and GP Jones 1991 The influence of habitat complexity on postrecruitment processes in a temperate reef fish population J Exp Mar Bid Ecol 151 271-294

de Lafontaine Ye T Lambert GR LiHHy WD McKone and RJ Miller (Editors) 1992 Juvenile stages the missing link in fisheries research Can Rch Rep Fish Aquat Sci No 1890

Boherty PJ 1982 Coral reef fishes recruitment-limited assem- blageswaz Proceedings of the Fourth International Coral Reef Symposium Manila The Phillipines VoH 2 pp 465-470

Doherty P-J 1983 Tropical territorial damselfishes is density limited by aggression or recruitment Ecology 64 176-190

Doherty PJ and AJ Fowler 8994 An empirical test of recruitment limitation in a coral reef fish Science (Washington DC) 263 935-939

Fsrrester GE 1990 Factors influencing the juvenile demog- raphy of a coral reef fish population Ecology 71 1666-1681

Gotceitas V and A Brown 1993 Substrate selection by juvenile Atlantic cod (Gadus mor8zua) effects of predation risk Oecologia 93 3 1-37

Henderson PA RHA Holmes and RN Size-selective overwintering mortality in the sand smelt Atkerina boyeri Risso and its role in population regulation J Fish Biol 33 221-233

Hixon MA and JP Beets 1989 Shelter characteristics and Caribbean fish assemblages experiments with artificial reefs Bull Mar Sci 44 666-680

Houde E 1987 Fish early life dynamics and recruitment variability Am Fish Soc Symp Ser 2 17-29

Hunt von Herbing I and W Hunte 1991 Spawning and recruitment of the bluehead wrasse Thakassoma Ea~ascdatum in Barbados WI Mar Ecol Prog Ser 72 49-58

Jones GPe 1986 Food availability affects growth in a coral reef fish Oecologia 70 136-139

Jones GP 1990 The importance of recruitment to the dynamics of a coral reef fish population Ecology 71 1691-1 698

Jones GP 1991 Postrecruitment processes in the ecology of coral reef fish populations a multifactoria2 perspective In The Ecology of fishes on coral reefs Edited by PF Sale Academic Press San Diego Calif pp 294-328

Juanes E 1994 What determines prey size selectivity in pis- civorous fishes Paz Theory and application in fish feeding ecology Edited by DJ Stouder KL Fresh and RJ Feller Belle W Baruch Library in Marine Sciences No 18 University of South Carolina Press Columbia SC

Levin PS 1991 Effects of microhabitat on recruitment vari- ation in a Gulf of Maine reef fish Mar Ecol Prog Ser 75 183-189

Levin PS 1993 Habitat structure conspecific presence and spatial variation in the recruitment of a temperate reef fish Oecologia 94 176-1 85

Lsugh RG PC Valentine DC Potter Pa Auditore GZ Bolz J Neilson and RI Berry 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 1-1 2

Malloy KD and TE Targett 1991 Feeding growth and survival of juvenile summer flounder Parakichthys dentatus experimental analysis of the effects of temperature and salin- ity Mar Ecol Prog Ser 72 213-223

Mattila J 1992 The effect of habitat complexity on predation efficiency of perch Perm fluvinbikis L and suffe Gyrnmo- cephcalus cernuus (L) f Exp Mar Biol Ecol 157 55-67

Milicich MJ MG Meekan and PJ Boherty 1992 Larval supply a good predictor of recruitment of 3 species of reef fish (Pomacentridae) Mar Ecol Psog Ser 86 153- 166

Miller IT LB Crowder JA Rice and EA Marshall 1988 Larval size and recruitment mechanisms in fishes toward a conceptual framework Can J Fish Aquat Sci 45 1657-1670

Pepin P- and RA Myers 1991 Significance of egg and larval size to recruitment variability of temperate marine fish Can Fish Aquat Sci 48 503-5 18

Sale PF WA Douglas and PJ Doherty 1984 Choice of microhabitats by coral reef fishes at settlement Coral Reefs 3 91-99

Shulman M 1985 Recruitment of coral reef fishes effects of distribution of predators and shelter Ecology 66 lOX9-1O66

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Sogard S 1992 Variability in growth rates of juvenile fishes in different estuarine habitats Mar E d Prog Ser 85 35-53

W and FJ Rohlf 1981 Biometry 2nd ed Freeman San Francisco Calif

Sweatman H 1985 The influence of adults of some coral reef fishes on larval recruitment Ecol Monsgr 55 469-485

Sweatrnan H 1988 Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues J Exp Mar B i d Ecol 124 163-174

Tupper M and WG Boutilier 1995 Size and priority at settle- ment determine growth and competitive success of juvenile Atlantic cod Mar Ecol Prog Ser 118 295-308

Tupper M and W Hunte 11994 Recruitment of coral reef fishes to artificial and natural reefs in Barbados WI Mar Ecol Prog Ser 108 225-235

Victor BC 1983 Recruitment and population dynamics of a coral reef fish Science (Washington DC) 219 4 3 9-420

Victor BC 1986 Larval settlement and juvenile mortality in a recmitment-limited coral reef fish population Ecol Monogr 56 145-160

Walsk WJ 1987 Patterns of recruitment and spawning in Hawaiian reef fishes Environ BioB Fishes 4 257-276

Werner EE and D3 Hall 1988 Ontogenetic habitat shifts in bluegill the foraging rate - predation risk trade-off Ecsl- ogy 69 1352-1 366

Wilkinson W 1990 SYSTAT the system for statistics Systat Inc Evansasn 111

Williams DMcB S English and MJ Milicich 1994 Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement Bull Mar Sci 54 314-33 B

Can

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This article has been cited by

1 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek Aysun Gumus 2012 One century of eel growth changesand implications Ecology of Freshwater Fish 213 325-336 [CrossRef]

2 Mary R Ryan Shaun S Killen Robert S Gregory Paul VR Snelgrove 2012 Predators and distance between habitatpatches modify gap crossing behaviour of juvenile Atlantic cod (Gadus morhua L 1758) Journal of Experimental MarineBiology and Ecology 422-423 81-87 [CrossRef]

3 David K A Barnes Kathleen E ConlanThe Dynamic Mosaic 255-290 [CrossRef]

4 Felicity Huntingford Susan Coyle William HunterAvoiding Predators 220-247 [CrossRef]

5 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek 2012 One century of eel growth changes and implications One century of eel growth Ecology Of Freshwater Fish no [CrossRef]

6 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 9107 1403-1412 [CrossRef]

7 Gisle K Sverdrup Justin J Meager Anders Fernouml Jon E Skjaeraasen Petra Rodewald Anne G V Salvanes Torbjoumlrn Jaumlrvi2011 Territorial and agonistic interactions between farmed and wild cod (Gadus morhua) Aquaculture Research 42101539-1548 [CrossRef]

8 Christopher N Rooper Mark E Wilkins Craig S Rose Catherine Coon 2011 Modeling the impacts of bottom trawling andthe subsequent recovery rates of sponges and corals in the Aleutian Islands Alaska Continental Shelf Research [CrossRef]

9 MD Renkawitz RS Gregory DC Schneider 2011 Habitat dependant growth of three species of bottom settling fish ina coastal fjord Journal of Experimental Marine Biology and Ecology [CrossRef]

10 D K Demain A Gallego A Jaworski I G Priede E G Jones 2011 Diet and feeding niches of juvenile Gadus morhuaMelanogrammus aeglefinus and Merlangius merlangus during the settlement transition in the northern North Sea Journalof Fish Biology 791 89-111 [CrossRef]

11 John CaddyHow Artificial Reefs Could Reduce the Impacts of Bottlenecks in Reef Fish Productivity within Natural FractalHabitats 20114347 45-64 [CrossRef]

12 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 917 1403 [CrossRef]

13 Sandra Ramos Pedro Reacute Adriano A Bordalo 2010 Recruitment of flatfish species to an estuarine nursery habitat (Limaestuary NW Iberian Peninsula) Journal of Sea Research 644 473-486 [CrossRef]

14 MA Warren RS Gregory BJ Laurel PVR Snelgrove 2010 Increasing density of juvenile Atlantic (Gadus morhua)and Greenland cod (G ogac) in association with spatial expansion and recovery of eelgrass (Zostera marina) in a coastalnursery habitat Journal of Experimental Marine Biology and Ecology 3941-2 154-160 [CrossRef]

15 R GREGORY LOUGH 2010 Juvenile cod ( Gadus morhua ) mortality and the importance of bottom sediment type torecruitment on Georges Bank Fisheries Oceanography 192 159-181 [CrossRef]

16 Esben Moland Olsen Stephanie M Carlson Jakob Gjoslashsaeter Nils Chr Stenseth 2009 Nine decades of decreasingphenotypic variability in Atlantic cod Ecology Letters 127 622-631 [CrossRef]

17 R J David Wells J O Harper J R Rooker A M Landry T M Dellapenna 2009 Fish assemblage structure on a drownedbarrier island in the northwestern Gulf of Mexico Hydrobiologia 6251 207-221 [CrossRef]

18 Jonathan S F Lee Barry A Berejikian 2009 Structural complexity in relation to the habitat preferences territoriality andhatchery rearing of juvenile China rockfish (Sebastes nebulosus) Environmental Biology of Fishes 844 411-419 [CrossRef]

19 Ann Marie Gorman Robert S Gregory David C Schneider 2009 Eelgrass patch size and proximity to the patch edgeaffect predation risk of recently settled age 0 cod (Gadus) Journal of Experimental Marine Biology and Ecology 3711 1-9[CrossRef]

20 W R Hunter M D J Sayer 2009 The comparative effects of habitat complexity on faunal assemblages of northerntemperate artificial and natural reefs ICES Journal of Marine Science 664 691-698 [CrossRef]

Can

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Can J Fish Aejuat Sci Vol 52 199

Hunte 1994 Tupper and Boutilier 1995) The relative ortance or pre- and post-settlement events in deter- ing recruitment strength will vary with location time

and habitat (Jones 1996 Cswraell and Jones 199 1) While almost all research in this field has been conducted on coral reef fishes similar me s seem to apply to y o u n g - o f - t e e Atlantic cod tudy spatid patterns of settlement of cod were completely altered by habitat- specific postsettlement mortality In addition growth rates of young-of-the-year cod were influenced by habitat type which may in turn influence overwinter survivaI However in yews or locations in which larval survival and settlement were very low the importance of these gostsettlement processes would likely decrease and the abundance of young-of-the-year cod would be regulated mainly by larval input Longer term studies are needed to assess the impsr- tance of pre- and post-settlement events over several y e a s (Forrester 1990 Jones 1990)

1 Hunt von Herbing and R Conrad provided assistance in the field This study is a contribution s f the Ocean Pro- duction Enhancement Network MT was funded by a Natural Sciences and Engineering Research Council

C ) postgraduate scholarship mQ a Ddhousie graduate scholarship Funding for this study was provided by an operating grant f rom the NSERC Production Enhancement Network to

ehrents K 1987 The influence of shelter availability on recruitment and early juvenile survivorship of Lythryhbnkcs d d i Gilbert (Pisces Gobiidae) J Exp Mar Biol Ecol

ecruitment stability and survival sample size- specific theory with examples from the early life dynamics of marine fish Dana Rep 7 45-147

Bolz GR and RG Eough 1988 Growth through the first six months of Atlantic cod (Gadus morhm) and haddock (Melanogrammus aeglefinus) based on daily otolith incre- ments Fish Bull $6 223-235

Car MH 1991 Habitat selection and recruitment of an assem- blage of temperate zone reef fishes J Exp Mar Biol Ecol 146 113-137

C m MH 1994 Effects of macroalgal dynamics on recruitment of a temperate reef fish Ecology 75 1320-1333

Chandler CR RR Sanders Jr and AM Landry Jr 1985 Effects of three substrate variables on two artificial reef fish communities Bull Mar Sci 37 129-142

Connel1 SD and GP Jones 1991 The influence of habitat complexity on postrecruitment processes in a temperate reef fish population J Exp Mar Bid Ecol 151 271-294

de Lafontaine Ye T Lambert GR LiHHy WD McKone and RJ Miller (Editors) 1992 Juvenile stages the missing link in fisheries research Can Rch Rep Fish Aquat Sci No 1890

Boherty PJ 1982 Coral reef fishes recruitment-limited assem- blageswaz Proceedings of the Fourth International Coral Reef Symposium Manila The Phillipines VoH 2 pp 465-470

Doherty P-J 1983 Tropical territorial damselfishes is density limited by aggression or recruitment Ecology 64 176-190

Doherty PJ and AJ Fowler 8994 An empirical test of recruitment limitation in a coral reef fish Science (Washington DC) 263 935-939

Fsrrester GE 1990 Factors influencing the juvenile demog- raphy of a coral reef fish population Ecology 71 1666-1681

Gotceitas V and A Brown 1993 Substrate selection by juvenile Atlantic cod (Gadus mor8zua) effects of predation risk Oecologia 93 3 1-37

Henderson PA RHA Holmes and RN Size-selective overwintering mortality in the sand smelt Atkerina boyeri Risso and its role in population regulation J Fish Biol 33 221-233

Hixon MA and JP Beets 1989 Shelter characteristics and Caribbean fish assemblages experiments with artificial reefs Bull Mar Sci 44 666-680

Houde E 1987 Fish early life dynamics and recruitment variability Am Fish Soc Symp Ser 2 17-29

Hunt von Herbing I and W Hunte 1991 Spawning and recruitment of the bluehead wrasse Thakassoma Ea~ascdatum in Barbados WI Mar Ecol Prog Ser 72 49-58

Jones GPe 1986 Food availability affects growth in a coral reef fish Oecologia 70 136-139

Jones GP 1990 The importance of recruitment to the dynamics of a coral reef fish population Ecology 71 1691-1 698

Jones GP 1991 Postrecruitment processes in the ecology of coral reef fish populations a multifactoria2 perspective In The Ecology of fishes on coral reefs Edited by PF Sale Academic Press San Diego Calif pp 294-328

Juanes E 1994 What determines prey size selectivity in pis- civorous fishes Paz Theory and application in fish feeding ecology Edited by DJ Stouder KL Fresh and RJ Feller Belle W Baruch Library in Marine Sciences No 18 University of South Carolina Press Columbia SC

Levin PS 1991 Effects of microhabitat on recruitment vari- ation in a Gulf of Maine reef fish Mar Ecol Prog Ser 75 183-189

Levin PS 1993 Habitat structure conspecific presence and spatial variation in the recruitment of a temperate reef fish Oecologia 94 176-1 85

Lsugh RG PC Valentine DC Potter Pa Auditore GZ Bolz J Neilson and RI Berry 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 1-1 2

Malloy KD and TE Targett 1991 Feeding growth and survival of juvenile summer flounder Parakichthys dentatus experimental analysis of the effects of temperature and salin- ity Mar Ecol Prog Ser 72 213-223

Mattila J 1992 The effect of habitat complexity on predation efficiency of perch Perm fluvinbikis L and suffe Gyrnmo- cephcalus cernuus (L) f Exp Mar Biol Ecol 157 55-67

Milicich MJ MG Meekan and PJ Boherty 1992 Larval supply a good predictor of recruitment of 3 species of reef fish (Pomacentridae) Mar Ecol Psog Ser 86 153- 166

Miller IT LB Crowder JA Rice and EA Marshall 1988 Larval size and recruitment mechanisms in fishes toward a conceptual framework Can J Fish Aquat Sci 45 1657-1670

Pepin P- and RA Myers 1991 Significance of egg and larval size to recruitment variability of temperate marine fish Can Fish Aquat Sci 48 503-5 18

Sale PF WA Douglas and PJ Doherty 1984 Choice of microhabitats by coral reef fishes at settlement Coral Reefs 3 91-99

Shulman M 1985 Recruitment of coral reef fishes effects of distribution of predators and shelter Ecology 66 lOX9-1O66

Can

J F

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Aqu

at S

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al u

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nly

Sogard S 1992 Variability in growth rates of juvenile fishes in different estuarine habitats Mar E d Prog Ser 85 35-53

W and FJ Rohlf 1981 Biometry 2nd ed Freeman San Francisco Calif

Sweatman H 1985 The influence of adults of some coral reef fishes on larval recruitment Ecol Monsgr 55 469-485

Sweatrnan H 1988 Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues J Exp Mar B i d Ecol 124 163-174

Tupper M and WG Boutilier 1995 Size and priority at settle- ment determine growth and competitive success of juvenile Atlantic cod Mar Ecol Prog Ser 118 295-308

Tupper M and W Hunte 11994 Recruitment of coral reef fishes to artificial and natural reefs in Barbados WI Mar Ecol Prog Ser 108 225-235

Victor BC 1983 Recruitment and population dynamics of a coral reef fish Science (Washington DC) 219 4 3 9-420

Victor BC 1986 Larval settlement and juvenile mortality in a recmitment-limited coral reef fish population Ecol Monogr 56 145-160

Walsk WJ 1987 Patterns of recruitment and spawning in Hawaiian reef fishes Environ BioB Fishes 4 257-276

Werner EE and D3 Hall 1988 Ontogenetic habitat shifts in bluegill the foraging rate - predation risk trade-off Ecsl- ogy 69 1352-1 366

Wilkinson W 1990 SYSTAT the system for statistics Systat Inc Evansasn 111

Williams DMcB S English and MJ Milicich 1994 Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement Bull Mar Sci 54 314-33 B

Can

J F

ish

Aqu

at S

ci D

ownl

oade

d fr

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ww

nrc

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This article has been cited by

1 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek Aysun Gumus 2012 One century of eel growth changesand implications Ecology of Freshwater Fish 213 325-336 [CrossRef]

2 Mary R Ryan Shaun S Killen Robert S Gregory Paul VR Snelgrove 2012 Predators and distance between habitatpatches modify gap crossing behaviour of juvenile Atlantic cod (Gadus morhua L 1758) Journal of Experimental MarineBiology and Ecology 422-423 81-87 [CrossRef]

3 David K A Barnes Kathleen E ConlanThe Dynamic Mosaic 255-290 [CrossRef]

4 Felicity Huntingford Susan Coyle William HunterAvoiding Predators 220-247 [CrossRef]

5 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek 2012 One century of eel growth changes and implications One century of eel growth Ecology Of Freshwater Fish no [CrossRef]

6 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 9107 1403-1412 [CrossRef]

7 Gisle K Sverdrup Justin J Meager Anders Fernouml Jon E Skjaeraasen Petra Rodewald Anne G V Salvanes Torbjoumlrn Jaumlrvi2011 Territorial and agonistic interactions between farmed and wild cod (Gadus morhua) Aquaculture Research 42101539-1548 [CrossRef]

8 Christopher N Rooper Mark E Wilkins Craig S Rose Catherine Coon 2011 Modeling the impacts of bottom trawling andthe subsequent recovery rates of sponges and corals in the Aleutian Islands Alaska Continental Shelf Research [CrossRef]

9 MD Renkawitz RS Gregory DC Schneider 2011 Habitat dependant growth of three species of bottom settling fish ina coastal fjord Journal of Experimental Marine Biology and Ecology [CrossRef]

10 D K Demain A Gallego A Jaworski I G Priede E G Jones 2011 Diet and feeding niches of juvenile Gadus morhuaMelanogrammus aeglefinus and Merlangius merlangus during the settlement transition in the northern North Sea Journalof Fish Biology 791 89-111 [CrossRef]

11 John CaddyHow Artificial Reefs Could Reduce the Impacts of Bottlenecks in Reef Fish Productivity within Natural FractalHabitats 20114347 45-64 [CrossRef]

12 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 917 1403 [CrossRef]

13 Sandra Ramos Pedro Reacute Adriano A Bordalo 2010 Recruitment of flatfish species to an estuarine nursery habitat (Limaestuary NW Iberian Peninsula) Journal of Sea Research 644 473-486 [CrossRef]

14 MA Warren RS Gregory BJ Laurel PVR Snelgrove 2010 Increasing density of juvenile Atlantic (Gadus morhua)and Greenland cod (G ogac) in association with spatial expansion and recovery of eelgrass (Zostera marina) in a coastalnursery habitat Journal of Experimental Marine Biology and Ecology 3941-2 154-160 [CrossRef]

15 R GREGORY LOUGH 2010 Juvenile cod ( Gadus morhua ) mortality and the importance of bottom sediment type torecruitment on Georges Bank Fisheries Oceanography 192 159-181 [CrossRef]

16 Esben Moland Olsen Stephanie M Carlson Jakob Gjoslashsaeter Nils Chr Stenseth 2009 Nine decades of decreasingphenotypic variability in Atlantic cod Ecology Letters 127 622-631 [CrossRef]

17 R J David Wells J O Harper J R Rooker A M Landry T M Dellapenna 2009 Fish assemblage structure on a drownedbarrier island in the northwestern Gulf of Mexico Hydrobiologia 6251 207-221 [CrossRef]

18 Jonathan S F Lee Barry A Berejikian 2009 Structural complexity in relation to the habitat preferences territoriality andhatchery rearing of juvenile China rockfish (Sebastes nebulosus) Environmental Biology of Fishes 844 411-419 [CrossRef]

19 Ann Marie Gorman Robert S Gregory David C Schneider 2009 Eelgrass patch size and proximity to the patch edgeaffect predation risk of recently settled age 0 cod (Gadus) Journal of Experimental Marine Biology and Ecology 3711 1-9[CrossRef]

20 W R Hunter M D J Sayer 2009 The comparative effects of habitat complexity on faunal assemblages of northerntemperate artificial and natural reefs ICES Journal of Marine Science 664 691-698 [CrossRef]

Can

J F

ish

Aqu

at S

ci D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y D

epos

itory

Ser

vice

s Pr

ogra

m o

n 07

11

12Fo

r pe

rson

al u

se o

nly

Sogard S 1992 Variability in growth rates of juvenile fishes in different estuarine habitats Mar E d Prog Ser 85 35-53

W and FJ Rohlf 1981 Biometry 2nd ed Freeman San Francisco Calif

Sweatman H 1985 The influence of adults of some coral reef fishes on larval recruitment Ecol Monsgr 55 469-485

Sweatrnan H 1988 Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues J Exp Mar B i d Ecol 124 163-174

Tupper M and WG Boutilier 1995 Size and priority at settle- ment determine growth and competitive success of juvenile Atlantic cod Mar Ecol Prog Ser 118 295-308

Tupper M and W Hunte 11994 Recruitment of coral reef fishes to artificial and natural reefs in Barbados WI Mar Ecol Prog Ser 108 225-235

Victor BC 1983 Recruitment and population dynamics of a coral reef fish Science (Washington DC) 219 4 3 9-420

Victor BC 1986 Larval settlement and juvenile mortality in a recmitment-limited coral reef fish population Ecol Monogr 56 145-160

Walsk WJ 1987 Patterns of recruitment and spawning in Hawaiian reef fishes Environ BioB Fishes 4 257-276

Werner EE and D3 Hall 1988 Ontogenetic habitat shifts in bluegill the foraging rate - predation risk trade-off Ecsl- ogy 69 1352-1 366

Wilkinson W 1990 SYSTAT the system for statistics Systat Inc Evansasn 111

Williams DMcB S English and MJ Milicich 1994 Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement Bull Mar Sci 54 314-33 B

Can

J F

ish

Aqu

at S

ci D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y D

epos

itory

Ser

vice

s Pr

ogra

m o

n 07

11

12Fo

r pe

rson

al u

se o

nly

This article has been cited by

1 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek Aysun Gumus 2012 One century of eel growth changesand implications Ecology of Freshwater Fish 213 325-336 [CrossRef]

2 Mary R Ryan Shaun S Killen Robert S Gregory Paul VR Snelgrove 2012 Predators and distance between habitatpatches modify gap crossing behaviour of juvenile Atlantic cod (Gadus morhua L 1758) Journal of Experimental MarineBiology and Ecology 422-423 81-87 [CrossRef]

3 David K A Barnes Kathleen E ConlanThe Dynamic Mosaic 255-290 [CrossRef]

4 Felicity Huntingford Susan Coyle William HunterAvoiding Predators 220-247 [CrossRef]

5 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek 2012 One century of eel growth changes and implications One century of eel growth Ecology Of Freshwater Fish no [CrossRef]

6 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 9107 1403-1412 [CrossRef]

7 Gisle K Sverdrup Justin J Meager Anders Fernouml Jon E Skjaeraasen Petra Rodewald Anne G V Salvanes Torbjoumlrn Jaumlrvi2011 Territorial and agonistic interactions between farmed and wild cod (Gadus morhua) Aquaculture Research 42101539-1548 [CrossRef]

8 Christopher N Rooper Mark E Wilkins Craig S Rose Catherine Coon 2011 Modeling the impacts of bottom trawling andthe subsequent recovery rates of sponges and corals in the Aleutian Islands Alaska Continental Shelf Research [CrossRef]

9 MD Renkawitz RS Gregory DC Schneider 2011 Habitat dependant growth of three species of bottom settling fish ina coastal fjord Journal of Experimental Marine Biology and Ecology [CrossRef]

10 D K Demain A Gallego A Jaworski I G Priede E G Jones 2011 Diet and feeding niches of juvenile Gadus morhuaMelanogrammus aeglefinus and Merlangius merlangus during the settlement transition in the northern North Sea Journalof Fish Biology 791 89-111 [CrossRef]

11 John CaddyHow Artificial Reefs Could Reduce the Impacts of Bottlenecks in Reef Fish Productivity within Natural FractalHabitats 20114347 45-64 [CrossRef]

12 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 917 1403 [CrossRef]

13 Sandra Ramos Pedro Reacute Adriano A Bordalo 2010 Recruitment of flatfish species to an estuarine nursery habitat (Limaestuary NW Iberian Peninsula) Journal of Sea Research 644 473-486 [CrossRef]

14 MA Warren RS Gregory BJ Laurel PVR Snelgrove 2010 Increasing density of juvenile Atlantic (Gadus morhua)and Greenland cod (G ogac) in association with spatial expansion and recovery of eelgrass (Zostera marina) in a coastalnursery habitat Journal of Experimental Marine Biology and Ecology 3941-2 154-160 [CrossRef]

15 R GREGORY LOUGH 2010 Juvenile cod ( Gadus morhua ) mortality and the importance of bottom sediment type torecruitment on Georges Bank Fisheries Oceanography 192 159-181 [CrossRef]

16 Esben Moland Olsen Stephanie M Carlson Jakob Gjoslashsaeter Nils Chr Stenseth 2009 Nine decades of decreasingphenotypic variability in Atlantic cod Ecology Letters 127 622-631 [CrossRef]

17 R J David Wells J O Harper J R Rooker A M Landry T M Dellapenna 2009 Fish assemblage structure on a drownedbarrier island in the northwestern Gulf of Mexico Hydrobiologia 6251 207-221 [CrossRef]

18 Jonathan S F Lee Barry A Berejikian 2009 Structural complexity in relation to the habitat preferences territoriality andhatchery rearing of juvenile China rockfish (Sebastes nebulosus) Environmental Biology of Fishes 844 411-419 [CrossRef]

19 Ann Marie Gorman Robert S Gregory David C Schneider 2009 Eelgrass patch size and proximity to the patch edgeaffect predation risk of recently settled age 0 cod (Gadus) Journal of Experimental Marine Biology and Ecology 3711 1-9[CrossRef]

20 W R Hunter M D J Sayer 2009 The comparative effects of habitat complexity on faunal assemblages of northerntemperate artificial and natural reefs ICES Journal of Marine Science 664 691-698 [CrossRef]

Can

J F

ish

Aqu

at S

ci D

ownl

oade

d fr

om w

ww

nrc

rese

arch

pres

sco

m b

y D

epos

itory

Ser

vice

s Pr

ogra

m o

n 07

11

12Fo

r pe

rson

al u

se o

nly

This article has been cited by

1 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek Aysun Gumus 2012 One century of eel growth changesand implications Ecology of Freshwater Fish 213 325-336 [CrossRef]

2 Mary R Ryan Shaun S Killen Robert S Gregory Paul VR Snelgrove 2012 Predators and distance between habitatpatches modify gap crossing behaviour of juvenile Atlantic cod (Gadus morhua L 1758) Journal of Experimental MarineBiology and Ecology 422-423 81-87 [CrossRef]

3 David K A Barnes Kathleen E ConlanThe Dynamic Mosaic 255-290 [CrossRef]

4 Felicity Huntingford Susan Coyle William HunterAvoiding Predators 220-247 [CrossRef]

5 Franccediloise Daverat Laurent Beaulaton Russell Poole Patrick Lambert Haringkan Wickstroumlm Jan Andersson MiranAprahamian Besma Hizem Pierre Elie Sukran Yalccediln-Oumlzdilek 2012 One century of eel growth changes and implications One century of eel growth Ecology Of Freshwater Fish no [CrossRef]

6 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 9107 1403-1412 [CrossRef]

7 Gisle K Sverdrup Justin J Meager Anders Fernouml Jon E Skjaeraasen Petra Rodewald Anne G V Salvanes Torbjoumlrn Jaumlrvi2011 Territorial and agonistic interactions between farmed and wild cod (Gadus morhua) Aquaculture Research 42101539-1548 [CrossRef]

8 Christopher N Rooper Mark E Wilkins Craig S Rose Catherine Coon 2011 Modeling the impacts of bottom trawling andthe subsequent recovery rates of sponges and corals in the Aleutian Islands Alaska Continental Shelf Research [CrossRef]

9 MD Renkawitz RS Gregory DC Schneider 2011 Habitat dependant growth of three species of bottom settling fish ina coastal fjord Journal of Experimental Marine Biology and Ecology [CrossRef]

10 D K Demain A Gallego A Jaworski I G Priede E G Jones 2011 Diet and feeding niches of juvenile Gadus morhuaMelanogrammus aeglefinus and Merlangius merlangus during the settlement transition in the northern North Sea Journalof Fish Biology 791 89-111 [CrossRef]

11 John CaddyHow Artificial Reefs Could Reduce the Impacts of Bottlenecks in Reef Fish Productivity within Natural FractalHabitats 20114347 45-64 [CrossRef]

12 Colin Trigg Dan Harries Alastair Lyndon Colin G Moore 2011 Community composition and diversity of two Limariahians (Mollusca Limacea) beds on the west coast of Scotland Journal of the Marine Biological Association of the UnitedKingdom 917 1403 [CrossRef]

13 Sandra Ramos Pedro Reacute Adriano A Bordalo 2010 Recruitment of flatfish species to an estuarine nursery habitat (Limaestuary NW Iberian Peninsula) Journal of Sea Research 644 473-486 [CrossRef]

14 MA Warren RS Gregory BJ Laurel PVR Snelgrove 2010 Increasing density of juvenile Atlantic (Gadus morhua)and Greenland cod (G ogac) in association with spatial expansion and recovery of eelgrass (Zostera marina) in a coastalnursery habitat Journal of Experimental Marine Biology and Ecology 3941-2 154-160 [CrossRef]

15 R GREGORY LOUGH 2010 Juvenile cod ( Gadus morhua ) mortality and the importance of bottom sediment type torecruitment on Georges Bank Fisheries Oceanography 192 159-181 [CrossRef]

16 Esben Moland Olsen Stephanie M Carlson Jakob Gjoslashsaeter Nils Chr Stenseth 2009 Nine decades of decreasingphenotypic variability in Atlantic cod Ecology Letters 127 622-631 [CrossRef]

17 R J David Wells J O Harper J R Rooker A M Landry T M Dellapenna 2009 Fish assemblage structure on a drownedbarrier island in the northwestern Gulf of Mexico Hydrobiologia 6251 207-221 [CrossRef]

18 Jonathan S F Lee Barry A Berejikian 2009 Structural complexity in relation to the habitat preferences territoriality andhatchery rearing of juvenile China rockfish (Sebastes nebulosus) Environmental Biology of Fishes 844 411-419 [CrossRef]

19 Ann Marie Gorman Robert S Gregory David C Schneider 2009 Eelgrass patch size and proximity to the patch edgeaffect predation risk of recently settled age 0 cod (Gadus) Journal of Experimental Marine Biology and Ecology 3711 1-9[CrossRef]

20 W R Hunter M D J Sayer 2009 The comparative effects of habitat complexity on faunal assemblages of northerntemperate artificial and natural reefs ICES Journal of Marine Science 664 691-698 [CrossRef]

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21 Alysa J Remsburg Monica G Turner 2009 Aquatic and terrestrial drivers of dragonfly (Odonata) assemblages within andamong north-temperate lakes Journal of the North American Benthological Society 281 44-56 [CrossRef]

22 JS Barber DM Chosid RP Glenn KA Whitmore 2009 A systematic model for artificial reef site selection New ZealandJournal of Marine and Freshwater Research 431 283-297 [CrossRef]

23 M Shaw R Diekmann J van der Kooij S Milligan P Bromley D Righton 2008 Assessment of the diets of cod Gadusmorhua and whiting Merlangius merlangus juveniles in a frontal region close to the Norwegian Trench co-existence orcompetition Journal of Fish Biology 737 1612-1634 [CrossRef]

24 C T T Edwards R A Rademeyer D S Butterworth E E Plaganyi 2008 Investigating the consequences of MarineProtected Areas for the South African deep-water hake (Merluccius paradoxus) resource ICES Journal of Marine Science661 72-81 [CrossRef]

25 BG Clynick CW McKindsey P Archambault 2008 Distribution and productivity of fish and macroinvertebrates inmussel aquaculture sites in the Magdalen islands (Queacutebec Canada) Aquaculture 2831-4 203 [CrossRef]

26 B LAUREL A STONER C RYER T HURST A ABOOKIRE 2007 Comparative habitat associations in juvenile Pacificcod and other gadids using seines baited cameras and laboratory techniques Journal of Experimental Marine Biology andEcology 3511-2 42-55 [CrossRef]

27 M HORINOUCHI 2007 Review of the effects of within-patch scale structural complexity on seagrass fishes Journal ofExperimental Marine Biology and Ecology 3501-2 111-129 [CrossRef]

28 Axel Temming Jens Floeter Siegfried Ehrich 2007 Predation Hot Spots Large Scale Impact of Local AggregationsEcosystems 106 865-876 [CrossRef]

29 Fiona M Gibb Iain M Gibb Peter J Wright 2007 Isolation of Atlantic cod (Gadus morhua) nursery areas Marine Biology1513 1185-1194 [CrossRef]

30 F Juanes 2007 Role of habitat in mediating mortality during the post-settlement transition phase of temperate marine fishesJournal of Fish Biology 703 661-677 [CrossRef]

31 J STAL L PIHL H WENNHAGE 2007 Food utilisation by coastal fish assemblages in rocky and soft bottoms on theSwedish west coast Inference for identification of essential fish habitats Estuarine Coastal and Shelf Science 713-4593-607 [CrossRef]

32 D KA Barnes K E Conlan 2007 Disturbance colonization and development of Antarctic benthic communitiesPhilosophical Transactions of the Royal Society B Biological Sciences 3621477 11-38 [CrossRef]

33 P M Ross S F Thrush J C Montgomery J W Walker D M Parsons 2007 Habitat complexity and predation riskdetermine juvenile snapper ( Pagrus auratus ) and goatfish ( Upeneichthys lineatus ) behaviour and distribution Marine andFreshwater Research 5812 1144 [CrossRef]

34 Alisa A Abookire Janet T Duffy-Anderson Christina M Jump 2006 Habitat associations and diet of young-of-the-yearPacific cod (Gadus macrocephalus) near Kodiak Alaska Marine Biology 1504 713-726 [CrossRef]

35 M SULLIVAN R COWEN K ABLE M FAHAY 2006 Applying the basin model Assessing habitat suitability of young-of-the-year demersal fishes on the New York Bight continental shelf Continental Shelf Research 2614 1551-1570 [CrossRef]

36 M LAZZARI B STONE 2006 Use of submerged aquatic vegetation as habitat by young-of-the-year epibenthic fishes inshallow Maine nearshore waters Estuarine Coastal and Shelf Science 693-4 591-606 [CrossRef]

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38 Elizabeth T Methratta Jason S Link 2006 Associations between Surficial Sediments and Groundfish Distributions in theGulf of MainendashGeorges Bank Region North American Journal of Fisheries Management 262 473-489 [CrossRef]

39 Marc Mangel Phillip Levin Anand Patil 2006 Using Life History And Persistence Criteria To Prioritize Habitats ForManagement And Conservation Ecological Applications 162 797-806 [CrossRef]

40 K Lekve K Enersen S E Enersen J Gjosaeter N Chr Stenseth 2006 Interannual variability in abundance and length ofyoung coastal cod in the subtidal zone Journal of Fish Biology 683 734-746 [CrossRef]

41 B LAUREL J BROWN 2006 Influence of cruising and ambush predators on 3-dimensional habitat use in age 0 juvenileAtlantic cod Gadus morhua Journal of Experimental Marine Biology and Ecology 3291 34-46 [CrossRef]

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42 K ABLE M FAHAY D WITTING R MCBRIDE S HAGAN 2006 Fish settlement in the ocean vs estuary Comparisonof pelagic larval and settled juvenile composition and abundance from southern New Jersey USA Estuarine Coastal andShelf Science 661-2 280-290 [CrossRef]

43 Anne Gro Vea Salvanes Victoria A Braithwaite 2005 Exposure to variable spatial information in the early rearingenvironment generates asymmetries in social interactions in cod (Gadus morhua) Behavioral Ecology and Sociobiology592 250-257 [CrossRef]

44 M D J Sayer S H Magill T J Pitcher L Morissette C Ainsworth 2005 Simulation-based investigations of fisherychanges as affected by the scale and design of artificial habitats Journal of Fish Biology 67 218-243 [CrossRef]

45 P LEVIN G STUNZ 2005 Habitat triage for exploited fishes Can we identify essential ldquoEssential Fish Habitatrdquo EstuarineCoastal and Shelf Science 641 70-78 [CrossRef]

46 V A Braithwaite A GV Salvanes 2005 Environmental variability in the early rearing environment generates behaviourallyflexible cod implications for rehabilitating wild populations Proceedings of the Royal Society B Biological Sciences2721568 1107-1113 [CrossRef]

47 ROSAMONDE R COOK PETER J AUSTER 2005 Use of Simulated Annealing for Identifying Essential Fish Habitat ina Multispecies Context Conservation Biology 193 876-886 [CrossRef]

48 PDN Srinivasu IL Gayatri 2005 Influence of prey reserve capacity on predatorndashprey dynamics Ecological Modelling1812-3 191-202 [CrossRef]

49 Kelly Denit Su Sponaugle 2004 Growth Variation Settlement and Spawning of Gray Snapper across a Latitudinal GradientTransactions of the American Fisheries Society 1336 1339-1355 [CrossRef]

50 ROBERT E BLYTH MICHEL J KAISER GARETH EDWARDS-JONES PAUL J B HART 2004 Implications of azoned fishery management system for marine benthic communities Journal of Applied Ecology 415 951-961 [CrossRef]

51 D Cote S Moulton P C B Frampton D A Scruton R S McKinley 2004 Habitat use and early winter movements byjuvenile Atlantic cod in a coastal area of Newfoundland Journal of Fish Biology 643 665-679 [CrossRef]

52 JF Caddy DJ Agnew 2004 An overview of recent global experience with recovery plans for depleted marine resourcesand suggested guidelines for recovery planning Reviews in Fish Biology and Fisheries 141 43-112 [CrossRef]

53 Christopher N Rooper Donald R Gunderson David A Armstrong 2004 Application of the concentration hypothesis toEnglish sole in nursery estuaries and potential contribution to coastal fisheries Estuaries 271 102-111 [CrossRef]

54 Kelly Denit Su Sponaugle 2004 Growth Variation Settlement and Spawning of Gray Snapper across a Latitudinal GradientTransactions of the American Fisheries Society 1336 1339 [CrossRef]

55 H Hinz M J Kaiser M Bergmann S I Rogers M J Armstrong 2003 Ecological relevance of temporal stability inregional fish catches Journal of Fish Biology 635 1219-1234 [CrossRef]

56 Christopher N Rooper Donald R Gunderson David A Armstrong 2003 Patterns in use of estuarine habitat by juvenileEnglish sole (Pleuronectes vetulus) in four Eastern North Pacific estuaries Estuaries 264 1142-1154 [CrossRef]

57 A Stoner 2003 Biological structures and bottom type influence habitat choices made by Alaska flatfishes Journal ofExperimental Marine Biology and Ecology 2921 43-59 [CrossRef]

58 M Lazzari 2003 Nursery use of shallow habitats by epibenthic fishes in Maine nearshore waters Estuarine Coastal andShelf Science 561 73-84 [CrossRef]

59 CALLUM M ROBERTS HELEN SARGANT 2002 FISHERY BENEFITS OF FULLY PROTECTED MARINERESERVES WHY HABITAT AND BEHAVIOR ARE IMPORTANT Natural Resource Modeling 154 487-507[CrossRef]

60 Phillip S Levin James A Coyer Rachel Petrik Thomas P Good 2002 COMMUNITY-WIDE EFFECTS OFNONINDIGENOUS SPECIES ON TEMPERATE ROCKY REEFS Ecology 8311 3182-3193 [CrossRef]

61 Simon F Thrush Paul K Dayton 2002 DISTURBANCE TO MARINE BENTHIC HABITATS BY TRAWLING ANDDREDGING Implications for Marine Biodiversity Annual Review of Ecology and Systematics 331 449-473 [CrossRef]

62 Linda A Deegan 2002 Lessons learned The effects of nutrient enrichment on the support of nekton by seagrass and saltmarsh ecosystems Estuaries 254 727-742 [CrossRef]

63 Michel J Kaiser Jeremy S Collie Stephen J Hall Simon Jennings Ian R Poiner 2002 Modification of marine habitats bytrawling activities prognosis and solutions Fish and Fisheries 32 114-136 [CrossRef]

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64 Kyrre Lekve Geir Ottersen Nils Chr Stenseth Jakob Gjoslashsaeligter 2002 LENGTH DYNAMICS IN JUVENILE COASTALSKAGERRAK COD EFFECTS OF BIOTIC AND ABIOTIC PROCESSES Ecology 836 1676-1688 [CrossRef]

65 Jeffrey S Shima 2001 RECRUITMENT OF A CORAL REEF FISH ROLES OF SETTLEMENT HABITAT ANDPOSTSETTLEMENT LOSSES Ecology 828 2190-2199 [CrossRef]

66 J Linehan 2001 Predation risk of age-0 cod (Gadus) relative to depth and substrate in coastal waters Journal of ExperimentalMarine Biology and Ecology 2631 25-44 [CrossRef]

67 James B Lindholm Peter J Auster Matthias Ruth Les Kaufman 2001 Modeling the Effects of Fishing and Implicationsfor the Design of Marine Protected Areas Juvenile Fish Responses to Variations in Seafloor Habitat Conservation Biology152 424-437 [CrossRef]

68 Romain Julliard Nils Chr Stenseth Jakob GjoslashsAEligter Kyrre Lekve Jean-Marc Fromentin Didrik S Danielssen 2001NATURAL MORTALITY AND FISHING MORTALITY IN A COASTAL COD POPULATION A RELEASEndashRECAPTURE EXPERIMENT Ecological Applications 112 540-558 [CrossRef]

69 Jean-Marc Fromentin Ransom A Myers Ottar N Bjoslashrnstad Nils Chr Stenseth Jakob Gjoslashsaeligter Hartvig Christie2001 EFFECTS OF DENSITY-DEPENDENT AND STOCHASTIC PROCESSES ON THE REGULATION OF CODPOPULATIONS Ecology 822 567-579 [CrossRef]

70 Robert A McConnaughey and Keith R Smith 2000 Associations between flatfish abundance and surficial sediments in theeastern Bering Sea Canadian Journal of Fisheries and Aquatic Sciences 5712 2410-2419 [Abstract] [PDF] [PDF Plus]

71 Joseph T DeAlteris Laura G Skrobe Kathleen M Castro 2000 EFFECTS OF MOBILE BOTTOM FISHING GEAR ONBIODIVERSITY AND HABITAT IN OFFSHORE NEW ENGLAND WATERS Northeastern Naturalist 74 379-394[CrossRef]

72 Richard A Wahle 2000 FISHERIES IN A SEA OF CHANGE ECOLOGY AND OCEANOGRAPHY OF NEWENGLANDS FISHING GROUNDS Northeastern Naturalist 74 317-328 [CrossRef]

73 Peter J Auster Nancy L Shackell 2000 MARINE PROTECTED AREAS FOR THE TEMPERATE AND BOREALNORTHWEST ATLANTIC THE POTENTIAL FOR SUSTAINABLE FISHERIES AND CONSERVATION OFBIODIVERSITY Northeastern Naturalist 74 419-434 [CrossRef]

74 David C Schneider Tammo Bult Robert S Gregory David A Methven Danny W Ings and Vytenis Gotceitas 1999Mortality movement and body size critical scales for Atlantic cod (Gadus morhua) in the Northwest Atlantic CanadianJournal of Fisheries and Aquatic Sciences 56S1 180-187 [Abstract] [PDF] [PDF Plus]

75 S J Turner S F Thrush J E Hewitt V J Cummings G Funnell 1999 Fishing impacts and the degradation or loss ofhabitat structure Fisheries Management and Ecology 65 401-420 [CrossRef]

76 Patricia A Chambers Robert E DeWreede Elizabeth A Irlandi and Herbert Vandermeulen 1999 Management issues inaquatic macrophyte ecology a Canadian perspective Canadian Journal of Botany 774 471-487 [Abstract] [PDF] [PDFPlus]

77 GALLEGO HEATH BASFORD MACKENZIE 1999 Variability in growth rates of larval haddock in the northern NorthSea Fisheries Oceanography 82 77-92 [CrossRef]

78 Les Watling Elliott A Norse 1998 Disturbance of the Seabed by Mobile Fishing Gear A Comparison to Forest ClearcuttingConservation Biology 126 1180-1197 [CrossRef]

79 MJ Kaiser PJ Armstrong PJ Dare RP Flatt 1998 Benthic Communities Associated With a Heavily Fished ScallopGround in the English Channel Journal of the Marine Biological Association of the United Kingdom 7804 1045 [CrossRef]

80 Michael J Fogarty Steven A Murawski 1998 LARGE-SCALE DISTURBANCE AND THE STRUCTURE OF MARINESYSTEMS FISHERY IMPACTS ON GEORGES BANK Ecological Applications 8sp1 S6-S22 [CrossRef]

81 M Sano 1997 Temporal variation in density dependence recruitment and postrecruitment demography of a temperate zonesand goby Journal of Experimental Marine Biology and Ecology 2141-2 67-84 [CrossRef]

82 E L Dalley and J T Anderson 1997 Age-dependent distribution of demersal juvenile Atlantic cod (Gadus morhua) in inshoreoffshore northeast Newfoundland Canadian Journal of Fisheries and Aquatic Sciences 54S1 168-176 [Citation] [PDF][PDF Plus]

83 Peter J Auster Richard J Malatesta Richard W Langton Les Watting Page C Valentine Carol Lee S Donaldson ElizabethW Langton Andrew N Shepard War G Babb 1996 The impacts of mobile fishing gear on seafloor habitats in the gulf of

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Maine (Northwest Atlantic) Implications for conservation of fish populations Reviews in Fisheries Science 42 185-202[CrossRef]

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