Biological reference points for American lobster(Homarus americanus) populations: limits toexploitation and the precautionary approach1
Michael J. Fogarty and Louise Gendron
Abstract: Large-scale changes in American lobster (Homarus americanus) landings and abundance have been docu-mented in both Canada and the United States over the last several decades. The spatial coherence of these changessuggests the importance of common environmental and fishery-related factors operating over broad areas in the westernNorth Atlantic. Changes in both biotic and abiotic factors have been hypothesized to underlie the recent increases inlobster production. Area expansion of lobsters to previously unoccupied or low-density areas appears to be an impor-tant element of the population increase. Here, we review biological reference points applied to American lobster popu-lations in the United States and Canada. Egg production per recruit models have been used to specify limit referencepoints (F10% in the United States) or target reference points (increasing egg production per recruit to twice its 1995level in Canada). Surplus production and yield-per-recruit models have also been employed to provide qualitative man-agement guidelines. We describe sources of uncertainty in the development of biological reference points for Americanlobster based on dynamic pool models in relation to the precautionary approach. Finally we consider auxiliary indica-tors and reference points with potential application to lobster stocks.
Résumé : On a observé durant les dernières décennies, tant au Canada qu’aux États-Unis, des changements à grandeéchelle dans les débarquements et l’abondance du homard d’Amérique (Homarus americanus). La concordance de ceschangements dans différentes régions laisse croire que des facteurs communs reliés à l’environnement ou à la pêcheagissent sur de grandes surfaces de l’ouest de l’Atlantique Nord. On a émis l’hypothèse que des changements dans lesfacteurs abiotiques et biotiques expliquent les accroissements récents de la production de homards. L’extension d’airedes homards dans des régions antérieurement peu ou pas occupées semble être un élément important de l’accroissementde la population. Nous examinons les points de référence biologiques utilisés pour les populations du homardd’Amérique aux États-Unis et au Canada. Des modèles de production d’oeufs par recrue ont servi à déterminer despoints de référence limites (F10% aux États-Unis) et des points de référence cibles (accroissement de la productiond’oeufs par recrue au double de sa valeur en 1995, au Canada). Les modèles de production excédentaire et de rende-ment par recrue ont aussi été utilisés pour fournir des règles qualitatives de gestion. Nous décrivons les sourcesd’incertitude dans le développement de points de référence pour le homard d’Amérique basés sur des modèles analyti-ques en relation avec le principe de précaution. Nous examinons finalement des indicateurs et des points de référenceauxiliaires qui pourraient s’appliquer potentiellement aux stocks de homards.
[Traduit par la Rédaction] Fogarty and Gendron 1403
Introduction
The American lobster (Homarus americanus) has sup-ported important commercial fisheries on the eastern sea-board of North America since the early nineteenth century.
The lobster resource is consistently ranked among the mostvaluable fishery commodities in Canada and the UnitedStates. Reported lobster landings are currently at or near his-torically high levels in both countries (Fig. 1). Annual ex-ploitation rates are high, with current estimates often
Received 22 April 2003. Accepted 1 April 2004. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on26 October 2004.J17504
M.J. Fogarty.2 National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Woods Hole, MA 02543,USA.L. Gendron. Department of Fisheries and Oceans, Maurice Lamontagne Institute, Mont-Joli, QC G5H 3Z4, Canada.
1Derived from the Workshop on Reference Points for Invertebrate Fisheries held in Halifax, N.S., on 2–5 December 2002.2Corresponding author (e-mail: [email protected]).
exceeding 80% (Fisheries Resource Conservation Council(FRCC) 1995; Fogarty 1995; Atlantic States Marine Fish-eries Commission (ASMFC) 2000b). The apparently highresilience of American lobster stocks to exploitation (seeFogarty (1995) for stock status) has been linked to the exis-tence of spatial refugia and larval source–sink dynamics(Anthony and Caddy 1980; Fogarty 1998), the nature of thestock–recruitment relationship, and lobster life history char-acteristics (Caddy 1986; Fogarty and Idoine 1986; Ennis andFogarty 1997). Dramatic increases in lobster landings, mostnotably during the 1980s and 1990s, appear to be related tochanges in fishery characteristics and shifts in environmentaland ecological conditions affecting production levels (Fogarty1995; ASMFC 2000a, 2000b). Recent sharp declines inlandings in the southern New England region and reducedlandings in some Lobster Fishing Areas in Canada highlightthe need to understand the factors resulting in shifting lob-ster production domains.
The American lobster has traditionally been managedthrough input controls, including limitation of fishing effortor fishing activity and controls on the size and reproductivecondition of lobsters taken (Miller 1995; Annala andSullivan 1997). The rationale for these management mea-sures has been based principally on yield-per-recruit (YPR)considerations, attempts to conserve the breeding popula-tion, and marketing factors. Output controls such as quotas
have not been used as management tools to date, except inone fishing area off southern Nova Scotia. In Canada, regu-lation of fishing effort includes controls on the number andtype of traps, the number of licenses holders, and the dura-tion of the fishing season. In the majority of the areas, nonew licenses have been granted since the beginning of the1970s (Miller 1995). Despite these tight controls, nominalfishing effort is nevertheless considered too high (FRCC1995). Moreover, effort regulations did not prevent impor-tant increases in the effective fishing effort over the last twoor three decades (e.g., Gendron and Archambault 1997). Inthe United States, the lobster fishery has traditionally beenan open-access fishery and trap limitations and some formsof access restriction have only recently been implemented.
Here, we review applications to date of biological refer-ence points (BRPs) for American lobster populations in theUnited States and Canada and provide a perspective onAmerican lobster management in the context of an apparentregime shift (sensu Steele 1998) in lobster production. Weexamine the underlying conceptual foundations of the BRPsapplied to lobster, explore important sources of uncertaintyin the determination of limit BRPs, and describe cases whererisk analysis has been used to cope with uncertainty. We dis-cuss the implementation of a precautionary approach (PA)and address specification of alternative BRPs currently un-der consideration in American lobster stocks. Finally, we ex-plore the applicability of alternative management tools formeeting conservation objectives.
Lobster BRPs
Early development of BRPs for American lobster popula-tions was based on application of surplus production and dy-namic pool models. These reference points, however, havebeen principally used as qualitative guides for lobster man-agement rather than negotiated targets or limits used to trig-ger a specified sequence of management actions.
Examination of yield–effort relationships have providedthe basis for general recommendations concerning the desir-ability of reductions in overall levels of fishing effort in lob-ster fisheries in the United States (e.g., Halgren 1980; Fogartyand Murawski 1986; Jensen 1986). Surplus production mod-els have been applied as a basis for management for otherlobster taxa including rock lobster (Jasus edwardsii) (Sailaet al. 1979; Booth and Breen 1994) and western rock lobster(Panulirus cygnus) (Hall and Brown 1994). Fogarty (1995)demonstrated a shift in the yield–effort relationship for theMaine fishery during the last several decades. Although cau-tion is necessary in interpreting the available catch and effortseries, the change suggests the possibility that an altered andnonstationary production domain now exists in this fishery.The change may be the result of alteration in ecological orenvironmental conditions, changes in fishery characteristics,or both (Fogarty 1995). The implications for shifts in pro-duction characteristics for BRPs are addressed more fullybelow.
YPR considerations have played a central role in the de-velopment of lobster management advice in both Canadaand the United States including recommendations for reduc-tions in fishing mortality rates and changes in minimum le-gal size limits (e.g., Ennis 1980; Fogarty 1980; Campbell
Fig. 1. Trends in landings (thousand metric tons) of Americanlobster in (a) the United States and (b) Canada and (c) the win-ter North Atlantic Oscillation (NAO) index. The NAO index issmoothed using a low-pass filter.
1985). American lobster assessments consistently indicatehigh levels of fishing mortality on inshore populations andthat increases in YPR and (or) economic efficiency wouldresult under reductions in exploitation rates and increases inminimum size limits (e.g., Ennis 1980; Fogarty 1980; Camp-bell 1985). Again, in all cases, however, these analyses havebeen used as qualitative guides to regulatory action ratherthan as hard targets despite clear indications of growth over-fishing based on YPR considerations.
In the last decade, egg production per recruit (EPR) refer-ence points have formally been adopted in both the UnitedStates (New England Fishery Management Council(NEFMC) 1995; ASMFC 2000a, 2000b) and Canada (FRCC1995). In the United States, a reduction in EPR to 10% ofthe unexploited state has been implemented as a manage-ment limit (NEFMC 1995; ASMFC 2000a, 2000b). In Can-ada, a goal of doubling EPR relative to 1995 levels has beenadopted as a management target (FRCC 1995). The possibil-ity of implementing a 5% limit EPR reference point in Can-ada is currently under consideration. In both countries, EPRis currently calculated using extensions to the Fogarty andIdoine (1988) model (Gendron and Gagnon 2001; J. Idoine,National Oceanic and Atmospheric Administration, Fisheries,166 Water Street, Woods Hole, MA 02543, USA, personalcommunication; D. Pezzack, Department of Fisheries andOceans, Bedford Institute of Oceanography, P.O. Box 1006,Halifax, NS B2Y 4A2, Canada, personal communication).
The definition of a limit reference point based on EPRconsiderations is linked to the rate of recruitment at low lev-els of population egg production. Given information on theslope of the recruitment curve at the origin and an analysisof EPR for a specified fishery selection pattern, an estimateof the limiting level of fishing mortality for the stock can bedefined. The EPR limit reference point applied to the Ameri-can lobster was implemented without definitive informationon the slope of the recruitment curve at the origin. In theUnited States, the choice of the F10% level was based onmetaanalyses of the slope of the recruitment curve at the ori-gin for a number of marine species (e.g., Mace and Sissen-wine 1993) with further qualitative consideration of lobsterlife history features. Fogarty and Idoine (1986) and Ennisand Fogarty (1997) provided indications that the slope of thelobster recruitment curve at the origin is relatively steep(Fig. 2), consistent with the apparently high resilience to ex-ploitation exhibited by this species.
The application of limit reference points for lobster stockshas been controversial because of the perceived mismatchbetween the apparent health of the resource as indicated byhigh landings and recommendations to take remedial actionindicated by low levels of estimated EPR. In part, the con-troversy is also due to the misapprehension that the EPRmodels “predict” a stock collapse. The overall controversymust be viewed in the context of an apparent shift in lobsterproduction rates over the last several decades. Non-stationarity in production dynamics of exploited aquatic re-sources on decadal and multidecadal time scales can beexpected (Walters 1987) and may require adjustment in ref-erence points and (or) management strategies. Preferably,BRPs should be sufficiently robust to accommodate a rangeof environmental and ecological conditions. Strategies forcoping with low-frequency shifts in the environment and
production were evaluated by Walters and Parma (1996) andMacCall (2001). The uncertainty related to identifying andpredicting these shifts in productivity is a major issue in lob-ster risk assessment and management.
Reference points and environmentalvariability
The trend in increasing lobster landings in both the UnitedStates and Canada through the 1980s and 1990s can be at-tributed, in part, to a number of fishery-related factors in-cluding overall increases in fishing effort, expansion of thefishing grounds to include offshore and deeper water sitesthat may have served as de facto refuge areas, changes ingear and overall technological efficiency, increases in theminimum legal size in some areas, increased compliancewith regulations such as minimum legal size limits and pro-tection of ovigerous females, and more complete reportingof landings (for a detailed review, see Fogarty 1995). In theCanadian fishery, where effort is controlled, increase inlandings is partly attributed to improvements in fishing effi-ciency brought by technological changes (e.g., Gendron andArchambault 1997).
The change in landings is also related to an apparent in-crease in abundance. The geographical scale of the recentincrease suggests common underlying environmental or eco-logical factors operating over broad regions. Changes in phys-ical environmental factors and in predation levels have beenproposed as potential mechanisms underlying the increase inrecruitment and abundance (for a review, see Fogarty 1995).An expansion of the population(s) into habitats with low
Fig. 2. Relationship between population egg production and re-cruitment to the adult population in Arnold’s Cove, Newfoundland.Recruitment has been estimated using a protracted recruitment pat-tern (Sheehy 2001) in which recruitment occurs over the ages 8–11 (triangles). The proportion recruiting at age represents a modi-fication of the schedule considered by Sheehy (2001) with p8 =0.15, p9 = 0.45, p10 = 0.25, and p11 = 0.15. The modification con-solidates the partial recruitment pattern of Sheehy (2001) bygrouping recruitment for ages 7 and 8 and ages 11 and 12 intosingle age groups. The smooth curve is the recruitment functiondetermined by Ennis and Fogarty (1997). The circles are the origi-nal recruitment indices used by Ennis and Fogarty 1997).
shelter availability and structural complexity has also beensuggested. Anecdotal information from fishers indicates thepresence of lobsters on grounds where traditionally no lob-sters were found (e.g., Archambault 1997). In the UnitedStates, the clearest evidence for population increases is de-rived from bottom trawl surveys (ASMFC 2000a), whichsample most effectively on soft-substrate habitats that werepreviously characterized by low density.
A shift in biotic and (or) abiotic conditions affecting sur-vival rates during the early life history stages has direct con-sequences for the specification of limit and target referencepoints. For example, a change in the density-independentmortality rates during the early life stages will principallyaffect the rate of recruitment at low egg production levels,thereby influencing the limiting level of fishing mortality(FT) at which the risk of a population collapse is high. Therelationship between egg production (E) and recruitment(R) can be expressed as
Rt = αf(Et–r)
where α is the rate of recruitment at low egg production lev-els, r is the delay between spawning and recruitment, andf(Et–r) is a compensatory function. For the American lobster,empirical evidence (Fogarty and Idoine 1986; Ennis andFogarty 1997) (see Fig. 2) and theoretical considerations(Caddy 1986) suggest an overall asymptotic relationship be-tween egg production and recruitment. One possible com-pensatory function for this relationship is
f EEE k
t rt r
t r
[ ]/
−−
−=
+1
where k is the population egg production level above whichdensity-dependent factors dominate (see Shepherd 1982).The estimate of FT is given by the fishing mortality rate fora given age- or size-selective pattern of fishing that results ina level of EPR equal to α−1. Accordingly, any factor thatresults in sustained shifts in α through changes in density-independent mortality rates will directly affect the appropri-ate choice of FT (Fig. 3a). An increase in α will result notonly in an increase in the overall recruitment level but alsoin an increase in the resilience of the population to exploita-tion. In contrast, factors affecting the density-dependentcomponent will principally result in changes in the asymp-totic recruitment level (Fig. 3b). If habitat suitability and (or)availability has increased or habitat types occupied havechanged, overall increases in recruitment and abundancecould occur even if bottlenecks (Wahle and Steneck 1991)were previously important in hard-substrate environments.
Reductions in fish predators through overharvesting havebeen suggested as one potential mechanism underlying anincrease in lobster recruitment. Reduction in predatory fishpopulations has been linked to higher abundance levels ofother crustacean populations in the Northwest Atlantic (e.g.,Witman and Sebens 1992; Worm and Myers 2003). A poten-tial role of declining Atlantic cod (Gadus morhua) predationon lobster populations has also been posited (Jackson et al.2001), although Hanson and Lanteigne (2000) concludedthat changes in predation rates by cod on lobster in the Gulfof St. Lawrence could not account for changes in landings in
this region. The potential role of other predators has notbeen fully explored.
Changes in large-scale climatic conditions in the NorthAtlantic have also been identified. For example, the winterNorth Atlantic Oscillation (NAO) index exhibited a gener-ally increasing trend from the early 1970s to the mid-1990s(see Fig. 1). Changes in the NAO potentially affect windfields, temperature patterns, and precipitation over the NorthAtlantic. In turn, these factors can potentially affect larvaltransport, individual growth, and ecosystem productivity.Drinkwater et al. (1996) examined temperature-related ef-fects on lobster landings and concluded that the recent in-creases in landings cannot be attributed to increasing watertemperatures alone. Information on NAO effects on larvaltransport and ecosystem productivity is not currently avail-able. It is likely that the increase in lobster abundance re-flects the interplay of a number of fishery-related, abiotic,and biotic factors. One or more of these factors may be dom-inant during different time periods. With respect to defininglobster BRPs, the key issue remains to determine whetherenvironmental changes have affected density-dependent ordensity-independent factors (or both).
The effects of environmental variability on recruitmentdynamics represent an important source of uncertainty in thespecification of the form of the relationship between eggproduction and recruitment and the slope of the recruitmentcurve at the origin. This has practical implications in estab-lishing limit reference points for American lobster; the cur-rent EPR-based limits may seem too conservative in periodsof high productivity but may not be conservative enough un-der adverse conditions.
Ennis and Fogarty (1997) noted that the available popula-tion time series for Arnold’s Cove is drawn from a period ofhigh landings (and high population size relative to the previ-ous two or three decades) and may reflect unusually favor-
Fig. 3. Effect of changing (a) the rate of increase in recruitmentat low egg production levels and (b) the egg production level atwhich density-dependent processes dominate for a Shepherdstock–recruitment model.
able conditions for recruitment. If density-independentmortality rates were lower during the period of observation,the slope of the recruitment curve would be higher than un-der less favorable environmental conditions and would im-ply a higher resilience to exploitation. Ennis and Fogarty(1997) noted that indication of a steeply ascending limb ofthe egg production – recruitment relationship is not a justifi-cation for allowing high levels of fishing mortality. Althoughthe form of the relationship between egg production and re-cruitment for Arnold’s Cove is not an artefact as suggestedby Sheehy (2001) (see Fig. 2), several important sources ofuncertainty remain. Ennis and Fogarty (1997) noted that it isnot known if this stock can be considered a closed popula-tion. Larval or juvenile input from exogenous sources wouldaffect inferences on the form of the egg production – recruit-ment relationship. In particular, inferences concerning therate of recruitment at low egg production levels would be af-fected. These sources of uncertainty must be strongly con-sidered in any attempt to use the extant information on theegg production – recruitment relationship directly to set limitreference points.
Uncertainties in EPR and risk assessment
Two main sources of uncertainty must be examined in thedetermination of limit reference points: the estimation ofEPR for a virgin population and the variability in parametersused in the assessment of EPR. In the United States, thelimit EPR reference point is expressed as a percentage of theEPR when F = 0. Lobsters have an extensive history of ex-ploitation in coastal waters and virgin stock conditions arenot known. Furthermore, information is not currently avail-able on whether density dependence exists in growth, matu-ration, and natural mortality of recruited lobsters.Accordingly, concern has been expressed about standardiz-ing EPR to unexploited conditions. In recognition of theseconcerns, a goal of doubling EPR relative to recent (1995)levels was adopted in Canada in preference to a limit refer-ence point expressed as a percentage of the estimated maxi-mum egg production level under the assumption of nodensity dependence. The strategy underlying the F10% levelin the United States with its implicit assumption of no den-sity dependence in growth and reproduction is appropriatelyviewed as an application of a risk-averse reference point,since it will yield more conservative results than correspond-ing analyses incorporating density-dependent processes.However, uncertainties in growth rates, reproductive pat-terns, and factors such as egg and larval viability of progenyproduced by larger, older lobsters become increasingly im-portant when results are expressed in reference to the unex-ploited case.
The model-based EPR reference point relies on a numberof parameters subject to uncertainty. Calculation of EPRproduction integrates every component of the annual cycleof the recruited lobster (natural and fishing mortality, moltincrement and molt frequency, size at sexual maturity, fecun-dity and reproductive cycle). All of these parameters aresubject to considerable process and measurement uncer-tainty. Quantitative expression of uncertainties and its trans-lation into probabilistic statements of reaching a given targetor falling below a limit are the basis of explicit risk evalua-
tion. Although risk analysis has been broadly applied to fishstocks, application to American lobster populations has onlyrecently been attempted. Gendron and Gagnon (2001) pro-vided an evaluation of management risk (the probability ofnot achieving a management target (doubling of EPR)) fol-lowing the implementation of a number of different manage-ment actions. Management actions examined include measuressuch as increasing the minimum legal size from its initialvalue of 76 mm carapace length. Uncertainty functions wereattributed to the parameters of the EPR model, and propaga-tion of uncertainty to the final estimates of EPR productionwas done using Monte Carlo simulations. EPR values werethen expressed relative to the estimated values of EPR be-fore the implementation of new management measures. Theratio between the two values, referred to as the incrementfactor, was used to determine which management scenarioscan, at least in theory, achieve the objective of doublingEPR (an increment factor of 2). Cumulative frequency distri-bution of the EPR increment factor values obtained from100 iterations were computed and used for assessing themanagement risk, i.e., the probability of not reaching an in-crement factor of 2, corresponding to the management targetof doubling EPR. An example is provided for the MagdalenIslands fishery (Quebec) for different minimum legal sizes(Fig. 4). From the analysis, a management plan including anincrease in minimum carapace length from 76 to 83 mm,1 mm each year from 1997 to 2003, was agreed upon andimplemented to reach the target of doubling EPR. Probabil-ity curves proved useful to illustrate to stakeholders theuncertainty in the evaluation of EPR production and themanagement risk associated with a given management ac-tion. To date, however, there has been no real discussion onwhat could be considered an acceptable level of manage-ment risk. In this example, the management measure of in-creasing carapace length was set not to go beyond a 50%risk of not reaching the target.
Chen and Wilson (2002) provided an evaluation of the bi-ological risk of overfishing by comparing the current level ofexploitation (Fcur) with the level of fishing mortality that re-duces EPR production to 10% of its maximum, i.e., that pro-duced in the absence of a fishery (F10%), corresponding tothe limit reference point currently used for the Americanlobster in the United States. Methodology to quantify uncer-tainty in the assessment of F10% was similar to the one de-scribed above where uncertainty functions were attributed tothe parameters of the EPR model. Propagation of uncertaintywas evaluated using the Monte Carlo method. Chen and Wil-son (2002) employed assumed levels of variability in the in-put parameters of the EPR model. Five levels of uncertaintywere used in the simulations. Uncertainty in Fcur was basedon bootstrapped estimates from a DeLury analysis (ASMFC2000b). Probability distribution functions of estimated val-ues of Fcur and F10% were superimposed and the risk that thecurrent fishing exceeds the limit reference point of F10% wasdetermined by the degree of overlap of the two probabilitydistribution function curves following a stochastic decision-making framework developed by Helser et al. (2001). Theauthors concluded that the uncertainties do not permit a de-finitive conclusion that the lobster resource is overfished inthe Gulf of Maine. Chen and Wilson (2002) noted that workis still needed to accurately determine stock status in relation
to the EPR limit reference point and, more specifically, ap-proaches to reducing uncertainty in the estimates of currentfishing mortality. Sensitivity analysis could complementthese types of studies to determine the relative importance ofthe different parameters in the uncertainty in the overall EPRestimates. Chen and Wilson (2002) presented a decision-making framework; however, standard guidance on the utili-zation of confidence and risk levels remains to be specified toderive solid interpretations on the status of the stock.
Uncertainties still remain concerning the female life cycle.A recent study by Comeau and Savoie (2002) in the south-ern Gulf of St. Lawrence indicated that a significant numberof females could spawn in successive years, molt and spawnin the same year, or skip molting or spawning for a year, de-pending on their size and reproductive status (first-timespawners or multiple spawners). Such features are differentfrom the generally accepted 2-year cycle with molting and
spawning in alternate years as described by Aiken andWaddy (1982) for females smaller than 120 mm carapacelength and still need to be quantified in many areas and in-cluded in the EPR simulation models.
Harvest control rules and the PA
In the United States, a determination that the EPR limitreference point is being exceeded is intended to trigger theestablishment of mandated reductions in fishing mortality orother actions to reduce overfishing. In practice, managementactions have been deferred in the face of debate concerningthe status of the resource. At present, a unidimensional con-trol rule based on fishing mortality reference points is em-ployed in lobster management, where Fcurr is compared withF10%. Fishing mortality is currently estimated based on aDeLury analysis as noted above (ASMFC 2000b).
In the application of a PA to fisheries management, a for-mal adoption of harvest control rules has been recommended(Food and Agriculture Organization 1996). The PA has nowbeen broadly adopted within international and national man-agement arenas where decisions in fisheries managementmust be made in situations of high scientific uncertainty. Inthe United States, principles of the PA in fisheries manage-ment are included in the National Standards Guidelines (par-ticularly the Guidelines for National Standard 1) under theMagnuson–Stevens Fisheries Conservation and ManagementAct (National Oceanic and Atmospheric Administration1996). In Canada, implementation of the PA is in accordwith the framework developed by the Canadian Privy Coun-cil Office (Department of Fisheries and Oceans 2002). Sofar, the PA has not been formally implemented for Americanlobster. In the PA context, limits are conceived as referencelevels that should have a low probability of being exceededand are designed to prevent stock declines through recruit-ment overfishing, while targets are used for the determina-tion of harvest control rules that are risk-averse and have alow probability of causing serious harm.
In instances where the limit fishing mortality referencepoint is exceeded, overfishing is said to occur; when thestock declines below the limit biomass reference point, thestock is overfished. Shifts in ecological and environmentalconditions that persist over multiyear periods can, however,result in circumstances where enhanced recruitment occurs,despite systemic overfishing. In these cases, the stock maynot be considered overfished even though overfishing is oc-curring (see Restrepo et al. 1998). A fuller representation oflobster resource status by including measures of biomass,abundance, and other biological characteristics of lobsterpopulations (see alternative BRPs) would permit a distinc-tion between overfishing and the overfished state under pre-vailing environmental conditions.
An example of a two-dimensional control rule using abun-dance information derived from fishery-independent andfishery-dependent sources (ASMFC 2000b) and the EPR ref-erence point is provided for lobster in the Gulf of Maine(Fig. 5). Abundance and fishing mortality estimates wereavailable for the period 1982–1997 (ASMFC 2000b). For il-lustrative purposes, we have mapped this empirical informa-tion against the F10% limit and a hypothetical limit set at themedian of the observed abundance time series (Fig. 5). Un-
Fig. 4. Cumulative frequency distribution of the 100 EPR incre-ment factor values obtained from Monte Carlo simulations. Theincrement factor corresponds to the ratio of EPR calculated for agiven management measure to EPR calculated before its imple-mentation. In this example, different increases in minimum legalsize to (a) 78- to 81-mm carapace length and (b) 82- to 84-mmcarapace length from an initial value of 76-mm carapace lengthare examined for the Quebec Magdalen Islands fishery. The per-centage of EPR increment factor values <2 illustrates the man-agement risk, i.e., the probability of not reaching themanagement target of doubling EPR under the management sce-nario tested.
der this set of possible control rules, overfishing would beconsidered to occur but the stock would not be classified asoverfished in the more recent part of the time series. Such anapproach would permit a better representation of stock statusand would reflect more fully the apparent increase in recruit-ment and productivity over this time period. This approachcould possibly be used as a basis for the implementation of aPA to lobster management and the determination of relevantcontrol rules. In practice, the choice of limiting fishing mor-tality rates and biomass levels would ideally be developed inconsultation with user groups and used to define a preagreedand accepted sequence of management actions if the stock isdetermined to be overfished.
In other lobster taxa, multidimensional control rules havebeen employed. In the spiny lobster (Panulirus argus) fish-ery in Florida, an F5% control rule is employed in concertwith a recruitment indicator; the stock is considered over-fished if the F5% limit is exceeded and recruitment declinesfor 3 consecutive years (Rosenberg et al. 1996). Starr et al.(1997) employed a decision rule approach based on trajecto-ries of catch-per-unit-effort for the New Zealand rock lobster.Similar approaches can be employed using alternative mea-sures of abundance or stock condition for American lobster.
Ideally, biological reference limits should be robustenough and remain conservative under different productionregimes. However, in practice, when changes in productioncharacteristics occur and persist over extended time frames,it may be necessary to adjust BRPs and control rules. Har-vest control rules for a hypothetical situation in which boththe slope of the recruitment curve at the origin and the egg
production level at which density dependence dominates areincreased under favorable environmental conditions relativeto unfavorable states of nature are depicted in Fig. 6. If thefactors leading to enhanced recruitment are not fully under-stood and cannot be predicted, however, a substantial sourceof uncertainty (and controversy) is introduced into the man-agement process. The risk to the resource is high if referencepoints are set to reflect favorable environmental conditionsand the environment subsequently shifts to a lower produc-tivity domain.
Alternative BRPs
In addition to the BRP mentioned above, additional or al-ternative measures based on demographic characteristics andother features of lobster populations could also be specified.A blend of model-based reference points such as EPR andempirical measures of stock condition can provide an effec-tive approach to the evaluation of stock status (see Caddy2003). The former can provide an important basis for pro-active management, while the latter are firmly grounded incurrent resource status and can be readily communicated tostakeholders.
Alternative reference points are presently being consid-ered in Canada in support of the conservation objectives ex-pressed by the FRCC (1995). Aside from increasing eggproduction, another objective stated by FRCC is to enhancethe size structure of lobster populations. Presently, most lob-ster fisheries are dependent on newly recruited animals andpopulations are characterized by highly truncated size fre-quency distributions (e.g., Gendron and Savard 2003). Evenif the target of doubling EPR has theoretically been reachedin some Canadian fishing areas by an increase in minimumlegal size, the size structures of the exploited populationsstill remain sharply compressed (Gendron and Savard 2003).Moreover, increasing minimum legal size without any reduc-tion of fishing effort or other controls on fishing mortalitymay have undesirable effects. Increasing minimum legal sizewill increase the number of reproductive females. However,since berried females are protected from the fishery, thegreater protection afforded to females compared with malescan potentially result in an asymmetry in exploitation ratesbetween males and females. As a result, the sex ratio can beaffected and the number of large males could be further re-duced if other protections are not implemented. Decreasingabundance of larger males could lead to sperm limitation.This phenomenon has been observed previously in rock lob-ster and spiny lobster (MacDiarmid and Butler 1999) wherefemales were observed to produce smaller clutches whenmated with smaller males. Research is now under way on theAmerican lobster’s copulatory system to determine whetherthis species also shows a potential for sperm limitation. In alaboratory mating experiment, Gosselin et al. (2003) showedthat similarly sized females accumulated more ejaculate whenmated with large males compared with small males. More-over, examination of the receptacle load of females in thewild from a heavily exploited population suggests that theywere mating mainly with small males. The question ofwhether ejaculate may actually be limiting to females in thefield is still unanswered, but these first observations warrantfurther research (Gosselin et al. 2003).
Fig. 5. Two-dimensional control rule utilizing empirical informa-tion on abundance and the F10% EPR reference point. Empiricalestimates for the period 1982–1997 (ASMFC 2000b) are illus-trated (circles) in the control rule phase space. A hypotheticalapplication of an abundance reference point set at the medianabundance level and using the existing fishing mortality refer-ence point is illustrated for the control rule (lower line); the up-per line illustrates a hypothetical control rule in which themedian of both the abundance series and the fishing mortalityrate for the period 1982–1997 is used. Lowest acceptable bio-mass set to lowest observed in series. Control rules based on ex-tant time series must be carefully evaluated for changes inproduction levels; those depicted are for illustration only.
Increases in minimum legal size reduce fishing pressureon immature lobsters and thus increase the contribution ofeggs by first-time spawners. Recent studies on maternal ef-fect on egg size and quality and larval growth by Ouellet etal. (2003) have shown that in the Gulf of St. Lawrence(Magdalen Islands), larvae (stage I) from first-time spawnerswere significantly smaller than larvae from larger females(assumed to be multiparous). Additional observations sug-gest also that larger larvae grow more efficiently. Althoughsubstantial heterogeneity within size groups was observed, itis suggested that all of these characteristics may indicatebetter survival potential of larvae produced by multiparousspawners. The current absence of control of fishing mortal-ity on larger animals will not favor the increase of the contri-bution of multiple spawners to egg production in this area.
In addition to the EPR reference point, Powles (2001)suggested a reference point based on a ratio of multiparousto primiparous spawners to ensure that a given minimumpercentage of egg production is produced by multiplespawners. Similarly, a reference point based on sex ratiocould also be developed to prevent any problem of spermlimitation.
In the United States, the overfishing definition adopted bythe NEFMC (1995) did in fact include additional measuresin addition to the EPR reference point. The full definition isas follows:
The American lobster is considered recruitment over-fished when, throughout its range, the fishing mortalityrate (F), given the regulations in place at the time underthe suite of regional management measures, results in a
reduction in estimated egg production per recruit of 10%or less of a non-fished population.
The development of the status of the stock report and theevaluation of fishery induced effects will consider infor-mation based on one or more indices but not limited to:a) Larval abundance index in surface waters; b) larvalsettlement index (the relative success of each new yearclass in reaching the benthos); c) pre-recruit indices byyear class; d) landings; e) size composition of the land-ings; f) spawning stock biomass; g) numbers of egg-bearing females; h) effort levels and catch-per-unit-effortand i) possible development of relationships of biologicalparameters to water temperature or other environmentalparameters.
The measures identified in the second section of theNEFMC overfishing definition have also been considered inCanada (Caddy 2001; Department of Fisheries and Oceans2001). Such measures have not been fully used in assessingthe status of the resource, in part because clear limit or tar-get reference points based on these elements have not beendefined (Restrepo et al. 1998). However, the potential to en-hance the biological bases on which management decisionsare made argues strongly for further development of theseideas.
Caddy (2003) argued strongly for a data-based approachas an alternative or in addition to model-based approaches tothe determination of BRPs (also see Hilborn 2002). Caddysuggested that greater reliance should be placed in simpleand direct observations of population characteristics that aremeaningful in terms of population productivity and relatedto empirical knowledge of limiting conditions or safe-stocksituations. For example, Tremblay and Lanteigne (2003)suggested that simple measures of population status such assize at capture relative to size at sexual maturity could con-stitute simple BRPs that could be emphasized in scientificadvice to managers and industry. The traffic light approachcould be adopted for the inclusion of such BRPs into scien-tific advice (Halliday 2000; Caddy 2002).
Management tools
Measures taken in recent years to comply with the EPRtarget (Canada) or threshold (United States) have mainlybeen oriented towards increases in escapement (increase inminimum size, implementation of a maximum legal size, aclosed-window size, and female v-notching). Althoughstrongly advocated by lobster assessment scientists, directcontrols on fishing effort (reduction of the number of li-censes and number of traps and reduction of the duration ofthe fishing season) have encountered some resistance, re-flecting social and cultural norms. In Canada, resistance to areduction of license holders and a limitation of the durationof the fishing season reflects concerns such as maintainingemployment in small communities. Concerns over employ-ment opportunities also exist in the US.
Because of the overcapacity of the lobster fishing fleet,fishing effort reductions would have to be drastic to haveany significant effect on fishing mortality. Moreover, thebenefits of fishing effort reduction on fishing mortality maybe variable. The relationship between fishing effort and fish-ing mortality is governed by catchability, which is rarely
Fig. 6. Two-dimensional control rule based on fishing mortalityand biomass (above an acceptable limit) under two sets of envi-ronmental conditions. The shaded area represents the regionwhere differences in reference points exist under favorable envi-ronmental conditions and under less favorable environmentalconditions affecting both the slope of the recruitment curve atthe origin and the level of egg production beyond which densitydependence dominates. Broken lines represent possible referencelevels for fishing mortality and biomass under the two sets ofenvironmental conditions.
constant and is known to vary seasonally with life cycle andtemperature (for a review, see Miller 1990). Variablecatchability will, for instance, generate uncertainty in theoutcome of modifications in fishing seasons. This issue hasbeen recently addressed by Gendron and Brêthes (2002) forthe Magdalen Islands (Quebec) lobster fishery who showedthat reducing the length of the fishing season by closing thefishery earlier was less effective in reducing fishing mortal-ity than delaying the opening of the fishing season becauseof higher catchability at the beginning of the season. An-other issue relates to fishers’ behavior who tend to continu-ously improve their fishing efficiency, particularly whenfishing effort reductions are imposed, thus potentially can-celling some of the benefits of reducing the number of traps.
Implementation of controls on fishing effort will have abetter chance of success in achieving reductions in fishingmortality if the patterns of fishing effort allocation with re-spect to resource concentration and movements are well un-derstood. This type of knowledge can eventually help assessthe effectiveness of spatial management measures such asclosing areas during certain periods of the fishing season. Inmany areas, patterns of fishing effort allocation have signifi-cantly evolved in the last decades in response to technologi-cal advances. Fishers are more mobile, cover greater distances,and are more effective at locating lobster. In the MagdalenIslands (Quebec), lobsters are mostly found on offshoregrounds at the start of the fishing season (spring) and movecloser to shore as the season progresses. Most fishers haveadapted their fishing strategy to take into account this move-ment through a so-called pursuit strategy: fishers will moveoffshore at the beginning of the fishing season to target lob-sters in their wintering grounds and then move their traps in-shore to follow concentrations (Gendron et al. 2000). Thishas resulted in higher fishing mortality, since in the past, notall lobsters would reach the interception site before the endof the fishing season. Gendron and Brêthes (2002) integratedpast and current fishing strategies as well as seasonal lobstermovement in a two-box spatial model that was used to simu-late different tactics of reduction of fishing effort on theoverall fishing mortality within a 9-week fishing season. Theexercise provided interesting insights into how temporal clo-sures of certain areas could be used as a management tool toreach a given target for fishing mortality. For example, byclosing the offshore area at the beginning of the season (first3 weeks) and then allowing only a small part of the fleet tofish in the offshore area resulted in an 8%–9% reduction inthe exploitation rate.
Year-round closures of particular areas for lobster manage-ment have not yet been widely implemented. The establish-ment of fishery closed areas in Bonavista Bay, Newfoundland,has been the most intensively studied case (Rowe 2001,2002). Two small reserves encompassing a total of 2.1 km2
were established in 1997; increases in male population den-sity and mean size were observed at both sites (Rowe 2002).An increase in female size and the proportion of ovigerousfemales was observed at one of the sites. Restricted move-ments of lobsters resulted in considerable protection af-forded to individuals within the closed areas (Rowe 2001).These results suggest that the broader application of year-round fishery closures could be beneficial as a tool in lobstermanagement, particularly where direct controls on fishing
effort are difficult to implement. Sizes of reserves would,however, need to be adjusted in relation to local lobstermovement patterns. Lobsters can potentially disperse overlarger areas than those observed in the Newfoundland closedareas (see Lawton and Lavalli 1995).
Fogarty (1998) examined the potential importance of dis-persal processes in a simple discrete space – discrete timemodel to explore implications for the stability and resilienceof lobster populations. The model represented two areaswith differential patterns of fishing mortality within each. Itwas shown that even relatively small rates of exchange po-tentially confer substantial resilience to exploitation if asource area experiences lower exploitation rates. Althoughnot configured to explicitly represent a marine protectedarea, these results are directly relevant to the case wherefishing mortality in one area is set to zero as in a no-takemarine reserve and suggest that the potential benefits of pro-tection of some segment of the population could be signifi-cant. The key consideration would rest in identifyingimportant source areas for protection, possibly defined byhabitat or other characteristics, while fishing would continuein areas receiving larval subsidies from the closed areas.Specification of the size of the areas required for protectionwould require further study.
Discussion
A dominant feature of the management environment forAmerican lobster is the uncertainty resulting from an incom-plete understanding of the factors affecting recent trends inrecruitment and productivity. Threshold or limit EPR refer-ence points that appear to be conservative under prevailingenvironmental conditions have generated considerable con-troversy. Although dramatic declines in lobster abundancehave recently occurred in the southern portion of the rangeand these declines have been linked to the combined effectsof overfishing, disease, and environmental conditions, thecontroversy has persisted. It is not currently possible to pre-dict how long the period of enhanced recruitment will last inother areas or whether we will enter a period of lower pro-ductivity in these areas. Wahle et al. (2004) documented anoverall decline in settlement at two locations in New Eng-land during the mid- to late 1990s.
Under these conditions, it would appear prudent to retaina limit reference point for lobster. Indeed, two successivepeer reviews of the overfishing definition for American lob-ster in the United States have advised retention of the EPRreference point as a precautionary measure in the face of un-certainty over whether favorable recruitment will continue(National Marine Fisheries Service 1995; ASMFC 2000a).The adoption of a conservative reference point in the contextof unpredictable environmental conditions is consistent witha PA to management of this valuable resource. Indeed, it canbe reasonably asked whether it will be sufficiently conserva-tive if adverse environmental conditions are encountered inthe future. With respect to setting reference points, it is criti-cal to understand whether the population increase was due todensity-independent factors affecting survival and growth ordensity-dependent factors related to overall carrying capacityand habitat expansion.
A full understanding of the dynamics of lobster popula-tions is complicated by the “shifting baseline syndrome”.Large-scale changes in the nearshore abundance of largelobsters and the overall demographic structure of the popula-tions have occurred over more than a century of intensiveexploitation (see Fogarty 1995). The sharp truncation in thesize composition in inshore components of the populationrelative to historical demographic characteristics and theconsistently high estimates of fishing mortality for lobsterpopulations underlie the concerns for the vulnerability of theresource (Fogarty 1995). These changes affect factors suchas the survival probabilities of larval lobsters in relation tosize and larval delivery patterns in relation to preferred set-tlement sites. Further ecological changes in system structureunder exploitation may have affected factors such as preda-tion risk, with implications for habitat utilization patterns.
Clear evidence of growth overfishing in virtually all in-shore American lobster fisheries suggests the utility of re-ducing the fishing mortality rates. High fishing mortalityrates and resulting reduction in size composition hold impor-tant consequences for the lifetime reproductive output offemale lobsters. Although the longevity of the Americanlobster is not known precisely, it is thought to be in excessof 30 years in the absence of exploitation. Presumably, thelong life span and large number of potential reproductiveevents throughout the life cycle are adaptations to variableenvironmental conditions on decadal time scales. Excessiveexploitation interferes with this important reproductive strat-egy (for a general discussion, see Fogarty 1993). Longhurst(2002) has noted that among fish species, taxa with longerlife spans are characterized by higher levels of recruitmentvariability and that iteroparity is an important evolutionarymechanism for coping with environmental uncertainty. Inhighly exploited lobster populations, we have imposed a con-dition approaching functional semelparity. These consider-ations suggest that BRPs that directly measure factors suchas individual female size, male size and numbers, and thenumber of reproductive opportunities afforded each female,etc., could be important adjuncts to EPR reference points.
It should be noted that BRPs that specify either limitingor target fishing mortality rates would not preclude takingadvantage of favorable environmental conditions such asthose that apparently prevailed during the 1980s and 1990s.Nor would they necessarily result in foregone yield. Under afixed exploitation rate strategy, the yield would increase withincreasing recruitment. Reductions in fishing mortality rateswould further result in YPR benefits. Application of a con-stant fishing mortality reference point is generally robust toenvironmental change (Walters and Parma 1996), althoughthere are circumstances where a further adjustment would berequired if the rate of recruitment at low population levelsdeclined under unfavorable environmental conditions.
The uncertainty surrounding the factors underlying the ap-parent increase in production and yield over the last severaldecades argues for a PA to lobster management. Should en-vironmental conditions shift to an unfavorable regime, levelsof exploitation that are now sustainable may then result instock decline. The inclusion of additional indicators of stockstatus as BRPs can provide a multidimensional approach forassessing these changes and providing more robust manage-ment advice in the face of environmental variability.
Acknowledgements
We are grateful for the comments on and criticisms of thispaper by Josef Idoine, Wendy Gabriel, Paul Breen, and ananonymous referee. Dedicated to the memory of James C.Thomas.
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