lated to the attempt to conserve stock structure, as indicated by molecular ... Here, we explore the hypothesis that MPAs can protect a stock against ... Undoubtedly violated in many cases, but we argue that this problem does not ..... exchange migrants with nearby areas where fishing takes place (Fig. ...... Hedrick, P. w: 1983.
MJU.ImN OF NAaJNE SCIEI'«:I. 64(3): 8S)-873. ~
CAN MARINE PROrEcrED AREASRESIOREAND CONSERVE STOCKATTRIBUTESOF REEFFISHES? Joel C. Trexler and Joseph Travis ABSTRACT Oneof the proposedbenefitsof marineprotectedareas(MPAs)is to conservegenetic diversity for life-history traits and to restoresomesemblanceof the life history that was expressedbefore intenseexploitation.Strong size-selectivemortality from fishing has promotedan earlier ageand smallersizeat maturity in many speciesanda concomitant reductionin subsequent adultbodysizes.Theseattributesarelesseconomicallydesirable thanthoseof fish from lessheavilyexploitedstocks.Weattemptedto determinewhether the establishmentof marine protectedareas,and the resulting relaxation of the directional selectionproducedby fishing mortality,wouldpromotea substantialrestorationof later agesat maturity. Our quantitativegeneticmodels,calibratedwith historical data from Gulf of Mexico popu\ationtof red snapper,Lutjanuscampechanus, indicatedthat adequatevariation shouldremainfor life-history traits like ageat maturity to respondto new fitness profiles. Marine specieswith planktonic 1arvac,including most economically important fIShes,havehigh gene-flowratesthat will precludegeneticdifferentiation betweenthe no-takeMPAs and the rest of the population.Any changesin the life history that are promotedby the n()-takeareamay thereforeramify through the entire population.The establishmentof no-takeMPAswill promotesubstantialincreasesin the ageat maturity ifrecruitmcnt into themis not limited by density-dependent mortality. If it is, the benefit of n()-takeareasfor increasingthe ageat maturity will be decreased. The no-take MPAs must serve as the major sourceof recruits for nearby fishing areasto producethe proposedbenefits.The creationof MPAs will not replacethe benefits of limiting ageor sizebiasesin harvestingby traditional fisheriesmanagement. The global decline in quantity and quality of fishing stocks has created a need for new methods of stock management (Botsford et al., 1997). Marine protected areas (MPAs) and fishing no-take zones are proving to be valuable tools for management of marine fiShery resources (Roberts, 1997; Allison et al., 1998; Lauck et al:, 1998). The proposed virtues of MPAs include protection of spawning stock, elevation of recruitment rates, maintenance of the age and size structures of stocks, and preservation of a balance in the frequencies of predatory and prey species (Ballantine, 1991; Bohnsack, 1992; Gubbay, 1995; Shackell and Willison, 1995; Bohnsack and Ault, 1996). One possible benefit of no-take reserves that has received little attention is the protection of genetic resources for life-history patterns within stocks (Plan Development Team, 1990). This benefit is related to the attempt to conserve stock structure, as indicated by molecular genetic markers (Avise, 1998), but is distinct in referring to the genetic basis of the attributes of individual fiSh that make them economically desirable and sustain higher population numbers (Stokes et al., 1993). The most important life-history characters for fishery stocks include the size and age at which individuals mature, the distribution of reproductive effort during life, and agespecific survivorship. Changes in these traits can change the size and age structure of a stock, altering its population dynamics and economic value. For example, a decreasein age at maturity appearsto entail maturation at smaller sizes and an overall decreasein the adult body-size distribution (Trippel, 1995). Although earlier maturation can be associas3
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ated with more rapid population growth, the exponential nature of the size-fecundity relationship in many species will combine with the smaller body sizes to reduce substantially the maximum possible yields and the economic value of the fishery (Law and Grey, 1989). Size-structured mortality, a common result of fishing, can greatly alter the age and size distribution of the spawning population and, potentially, the genetic composition of subsequent generations (Nelson and Soule, 1987; Bergh and Getz, 1989; Smith et al., 1991; McAllister and Peterman, 1992; Law and Rowell, 1993; Rijnsdorp, 1993). There are two reasons to believe that important fisheries have been altered genetically by size-selective removal of individuals from the spawning pool. First, fisheries are commonly age and siz;ebiased, removing the largest and oldest individuals preferentially (see, e.g., Ricker, 1981) and causing marked declines in the average size and age in many heavily fished stocks (pauly, 1979; Policansky and Magnuson, 1998). Second,the estimated age at sexual maturity is declining in many heavily fished stocks (Trippel, 1995). This change is consistent with predictions from life-history theory about the effects of age-specific mortality (Roff, 1992). Although some of these changesmay be attributable to phenotypic plasticity (Remick, 1993) or other environmental changes,the repetition of the patterns across dozens of species in many locations and the consistency of those patterns with the predictions of life-history theory implicate an evolutionary effect. Here, we explore the hypothesis that MPAs can protect a stock against further undesirable evolutionary changes and promote a partial restoration of the pre-exploitation life history, particularly restoring later agesat maturity. We baseour exploration on the premise that directional selection by fisheries has been promoting earlier age and smaller size at maturity and that this selection pressure will be reversed within the MPAs (cf. Horppila and Peltonen, 1994). We evaluate this hypothesis by attempting to answer three questions. First, is there likely to be enough genetic variation remaining for the age at maturity to respond to selection? Second, will stocks within an MPA be connected strongly enough with those outside of it to overcome the divergent selection pressures in each habitat type such that the age at maturity can increase in the entire fishery? Third, which features of the selection process are most important in promoting an overall increase in the age at maturity? Our approach is to use standard models of quantitative genetics, calibrated with data from red snapper (Lutjanus campechanus) populations in the Gulf of Mexico (Goodyear, 1994), to find likely answers to each question. We will focus on age at maturity because there is ample evidence for an evolutionary effect of fishing pressure and because it is so influential on adult size-structure and consequent economic value of the fishery. Our simulations assumethat size and age are tightly linked throughout the fish's life cycle so that selection on size is also selection on age. This expedient assumption is Undoubtedly violated in many cases, but we argue that this problem does not limit the generality of our results. DOES ENOUGHGENETICV ARIAnON REMAIN? ESTIMATINGORIGINALHERITABILITY.-In order to assess the likelihood that a species will be able to respond genetically to relaxation of directional selection, we must estimate the present heritability of age at maturity. To do so, however, we must first estimate its value before mass exploitation and then estimate the amount of genetic variation lost through the process of evolving the lower ages at maturity. The data available for red snapper are
TREXLER
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the estimated average age at maturity and its variance in unfished and fished stocks. To estimate the original heritability, we asswne that the differences in these values represent the cwnulative changesthat have occurred in the fished stocks through the selective pressure generated by size- and age-selective harvesting. We begin with the breeder's equation of quantitative genetics, which describes the standardized responseto selection as a function of the heritability and the standardized selection differential (Falconer and Mackay, 1996). This equation is
where R is the change in the average value of the trait across a single generation; 0' is the standard deviation (SO) of the trait before selection acts; S is the selection differential, the difference in the averagetrait value between the selected and the original, unselected cohort; and h2 is the heritability of the trait, the ratio of the additive genetic to phenotypic variance. To apply this equation, we must make indirect estimates of the response as well as the differential. We will estimate the cumulative responseby the difference between the average ages at maturity in fished and unfished populations. For red snapper, at most six generations have passed (estimated generation time = 14 yrs, Goodyear, 1994) since the onset of heavy exploitation at the beginning of this century. To estimate the cumulative differential, we begin by assuming that fishing exerts complete truncation selection against individuals who are above the average age at maturity. For a symmetric distribution, this assumption means that fishing selectively removes the upper 50%, leaving the lower 50% to contribute to the next generation. For a distribution skewed to the right (as are many distributions of age at maturity), the fraction removed would actually be less, but we will use the assumption of 500/0.This level corresponds to a standardized selection intensity (S/O') of about 0.80 (Falconer and Mackay, 1996:190, fig. 11.3). The basic equation is therefore converted to
R/a=O.80h2 To express the cumulative response, we rewrite R as XI-XU' the difference between the average trait value in the original population (xU>and that in the first generation after
selection(xJ andrewrite the basicequationas
(xl-xo)/a=O.80h2 or XI
=0.80 1.0 Spottedseatrout 75,(XX) Greateramberjack 57,(xx) Black drum »10 17,(XX) Red grouper »10 10,(XX) Black seabass 5,(XX) North AmericanPacific Coastal Woolly sculpin 5.7-7.5 Island kelpfish 8.7-19.4 Bluebandedgoby 30.0-42.9 Blacksmith chromis 12.0-87.4 Opaleyechub 24.9-62.3 California sheephead 14.4-23.5 Halfmoon chub 26.1
Reference Avise, 1992 Komfie1dand Bogdanowicz,1m Avise, 1992 Gold et al., 1993, 1994a,b Gold et al., 1994b Gold et al., 1993 Gold et al., 1993 Gold et al., 1993, 1994b Gold and Richardson.1994 Avise. 1992 Waples. 1987* Waples. 1987* Waples, 1987* Waples. 1987* Waples. 1987* Waples,1987* Waples. 1987
*Ranges are derived from multiple estimates reported.
ence in optima; we will estimate the fraction of the difference in optima that can be
obtained«M.- ~)/( O.- OJ)by usingestimates ofk andm fromtheliterature. THEDATAANDCALCULAlloNs.-We can estimate migration rates from estimates of the number of effective migrants per generation (N.m, where m is the level of gene flow and N. is the genetic effective population size) obtained from analysis of neutral or nearly neutral molecular markers in fishery species.The results of these studies universally indicate very open population structure (that is, very high gene flow) for estuary-dependent, reef-associated,and pelagic fish species(Table 1; Ward et al., 1994; Gold and Richardson, 1998). The published estimates ofN.m for economically important marine fish species all exceed 5, and most exceed 10. These estimates of high gene flow are consistent with the life hiStory of most marine fish, which includes a drifting larval phase sometimes lasting several weeks (Allison et al., 1998). The exception to these estimates, Acanthochromis polyacanthus, is a reef species that is unusual in lacking a larval phase (Planes and Doherty, 1997). An emerging knowledge of drift distances in the pelagic larval life stage of reef species suggests that many individuals (perhaps 100/0or more of recruits) disperse and settle significant distances from the location of their birth (Fig. 2; Jones et al., 1999; Swearer et al., 1999; Warner et al., this issue). The balance of local and long-distance recruitment (i.e., recruitment not from adjacent reefs or islands) depends on poorly known factors including vertical migration, stratified current flows, and MPA location (Cowen et al., 2000). An argument for low gene-flow rates might be made from observations of regional stock collapses and failure of immigrants to recolonize an area. Normal gene flow and recolonization may, however, be quite different entities ecologically and can produce different genetic patterns (Wade and McCauley, 1988; Ewens, 1989; McCauley, 1992). Moreover, the spatial and temporal scales at which recolonization failed to replenish a
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