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Keywords:

  • Conservation;
  • fisheries management;
  • juveniles;
  • neonates;
  • nursery areas;
  • sharks

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. How important are young sharks for population persistence?
  5. Possible consequences of nursery-centric management
  6. Implications for shark management
  7. Conclusion
  8. References

Concern over declining shark populations has led to an intense interest in their conservation and management. Due to the difficulties involved in managing adult sharks, focus has been placed on young juvenile and neonate age classes that inhabit discrete inshore nursery areas. However, past confusion over what qualifies as a nursery habitat has led to the identification of vast coastal areas as nurseries, making conservation unfeasible. With the establishment of more discerning criteria for nursery area identification such concerns have been somewhat alleviated, but while effort has been put into defining, identifying, mapping, and in some cases protecting nursery areas, little attention has been paid to the practical value of nurseries for the recovery of exploited shark populations. Often neonate and young juveniles are considered the most critical age classes in terms of population stability/recovery, but evidence is mounting that suggests life stages outside the nursery may be more important in this regard. While nursery area protection should remain a component in shark management strategies it will be critical to link early life stage conservation with management strategies that encompass older individuals residing outside nurseries if effective management is to be achieved.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. How important are young sharks for population persistence?
  5. Possible consequences of nursery-centric management
  6. Implications for shark management
  7. Conclusion
  8. References

The life history traits of many shark species, including large body size, slow growth, late maturity, and low fecundity, make them particularly vulnerable to overfishing and other anthropogenic threats (Musick et al. 2000; Frisk et al. 2005). Indeed, many shark populations have declined with respect to their pre-exploited biomass (Baum & Myers 2004; Shepherd & Myers 2005; Cortés et al. 2007), raising concern for their conservation and requiring the development of management planning.

The difficulty of managing adult sharks with expansive ranges, along with the tendency of some fisheries to apply teleost-based management to sharks, has at times steered strategies toward the protection of younger age classes, particularly neonates and young juveniles. The application of such management strategies, which emphasize increasing recruit survival to boost populations, raised interest in so-called “essential fish habitat” (NOAA 1996). For sharks, essential fish habitat has mostly centered on the identification of discrete inshore nursery areas used by early life stages in the belief that these stages were vital for population stability and recovery (Bonfil 1997). Such belief stemmed from the teleost type of management model, of which the protection of young individuals within nursery habitats is a standard principle. As a result of the NOAA 1996 mandate, which required the identification of essential fish habitat in all fisheries management plans in the United States, shark nursery area research increased (McCandless et al. 2007).

Greater focus on identifying shark nurseries as essential fish habitat generated a push for nurseries to be designated marine protected areas (MPAs) (Bonfil 1999). The ideal MPA design provides protection for all life stages of the species of concern (Bonfil 1999), which is impractical for the majority of shark species because they are wide ranging. Instead, MPAs could be used to protect some sharks during certain life stages, such as younger age classes within nursery areas (Bonfil 1999; Roberts 2000; Heupel & Simpfendorfer 2005). While this option has been examined theoretically for a number of nursery areas (Heupel & Simpfendorfer 2005; Garla et al. 2006b), implementation of MPAs in such areas has been limited (Bonfil 1999; Heupel & Simpfendorfer 2005).

MPA designation for shark nursery areas has lagged due partly to confusion over which habitats constitute true “nurseries.” As Heupel et al. (2007) point out, for several decades there was a lack of standardized criteria to differentiate between nursery and nonnursery habitat, resulting in the identification of large coastal stretches as nurseries, often based solely on the presence of neonates, juveniles, or both (Castro 1993; Simpfendorfer & Milward 1993; Hammerschlag & Fallows 2005; Blackburn et al. 2007). The subsequent addition of nursery area subcategories such as primary, secondary (Bass 1978), and communal (Simpfendorfer & Milward 1993) further complicated the debate regarding what constitutes a nursery. The large geographic area and number of these purported shark nurseries would render protective measures (i.e., MPAs) extraordinarily expansive, costly, and complicated (Heupel et al. 2007). A more refined definition for shark nurseries was necessary to avoid labeling vast areas as nurseries and diluting the ability to protect the most valuable areas (Beck et al. 2001). In response, Heupel et al. (2007) recently outlined three basic criteria designed to standardize the classification of shark nursery areas and identify those of greatest importance: (1) that sharks are more commonly encountered in the area than in other areas, (2) that sharks have a tendency to remain or return for extended periods, and (3) that the area or habitat is used repeatedly across years.

With some improvement in the identification, mapping, and in some cases protection, of nursery areas, little attention has been given to the practical value of nurseries to the recovery of harvested shark populations. We examine the importance of shark nurseries in the wider context of shark population recovery and management by discussing the relative importance of neonates and young juveniles (i.e., those stages that occur in nursery areas) to population recovery, and by reviewing the possible repercussions of focusing conservation efforts on nursery-using early life stages while adult populations remain comparatively undermanaged. While it is recognized that not all shark species use nursery areas in early life (Heupel et al. 2007) this review will focus on those species that do.

How important are young sharks for population persistence?

  1. Top of page
  2. Abstract
  3. Introduction
  4. How important are young sharks for population persistence?
  5. Possible consequences of nursery-centric management
  6. Implications for shark management
  7. Conclusion
  8. References

Demographic models can illustrate how various factors affect the intrinsic rate of population increase in long-lived, slow-growing marine species (Musick 1999a). Elasticity/sensitivity analyses within these models estimate how a population's intrinsic rate of increase is affected by various mortality rates at selected life stages. For example, Gallucci et al. (2006) used an age-structured Leslie matrix model for Rhizoprionodon taylori and Squalus acanthias and found that the survival of juveniles nearing maturity was proportionately more important to population maintenance than the survival of any other age class. Studies on other species such as Dipturus batis (Brander 1981) obtained similar results. Additionally, three separate studies published in a single volume (Musick 1999b) came to similar conclusions for four different shark species (Cortés 1999; Heppell et al. 1999; Simpfendorfer 1999). Each of the previous studies found that neonate (age 0–1) survival had relatively little influence on the overall population growth rate. Brewster-Geisz & Miller (2000) went so far as to model the “perfect nursery ground closure” where mortality for neonate Carcharhinus plumbeus was set at zero. Although the model's results showed that with “perfect” nursery area protection, fishing pressure on the rest of the population could increase slightly while remaining sustainable, in reality the complete protection of early life stages to the point of zero mortality is clearly impossible. For most shark species, only neonates and young juveniles typically occupy nursery areas whereas larger juveniles nearing maturity tend to move away from nurseries, so Brewster-Geisz & Miller (2000) concluded that nursery closures or size limits that protect only neonates and young juveniles are unlikely to promote population recovery; effective management must involve protection for older age classes along with nursery-using life stages.

In regard to the above demographic models, a brief discussion of stage-based and age-based modeling is prudent since both are drawn upon here as evidence. There has been debate regarding the appropriateness of using stage-based demographic models for sharks. Originally, stage-based models were considered to allow demographic modeling of data-deficient species (Cortés 1999; Miller et al. 2003). This, coupled with the hypothesis that small errors in parameter estimates for life-history tables could be magnified for long-lived species (Brewster-Geisz & Miller 2000; Miller et al. 2003) led some authors to see stage-based models as a way around these limitations (Cortés 1999; Brewster-Geisz & Miller 2000). Problems arise when stage-based models define a limited number of stages, (three or less), or do not include fixed-stage durations that can lead to inaccurate elasticity calculations and questionable estimates of population recovery times (Mollet & Cailliet 2003). Of the demographic models mentioned above, only two are stage based (Cortés 1999; Brewster-Geisz & Miller 2000). Both include fixed-stage durations and define more than three stages, thus avoiding the two major pitfalls identified in stage-based demographic models of shark populations. Conclusions derived from these stage-based models, while potentially not exactly the same as those from age-based models, are generally in agreement. There is still debate over the appropriateness of stage-based demographic modeling of sharks; however, that is beyond the scope of this review.

For nursery-using sharks, the above demographic studies illustrate the potential limitations of management based on nursery conservation. For example, Simpfendorfer (1999) found that for Carcharhinus obscurus the most important age class in terms of maintaining a positive intrinsic rate of population increase was that of large juveniles nearing maturity. Estimates place the age at maturity for C. obscurus around 17–22 years for females (220–250 cm), and 20–23 years for males (230–243 cm) (Simpfendorfer et al. 2002). This places older juveniles of the species far outside the age and size range of individuals normally recorded within nurseries. Indeed, Castro (1993) found the typical size range of C. obscurus within a nursery was between 101 and 104 cm. This demonstrates that the age classes identified as essential for maintaining a positive intrinsic rate of population increase (i.e., older juveniles) in the aforementioned demographic models are not the same age classes inside nursery areas (i.e., neonates and younger juveniles), which has considerable ramifications for shark management priorities. Unfortunately, continued emphasis on the importance of protecting nurseries tends to overshadow the evidence that, for many species, such an approach would not benefit the most important age classes in terms of population stability and recovery.

The shark fishery for Galeorhinus galeus in southern Australia is an example of a management strategy with a heavy nursery component. The commercial shark fishery in southern Australia that began in the 1920s focused primarily on G. galeus and to a lesser extent on Mustelus antarcticus. Concerns over the collapse of the fishery date back to the 1950s (Olsen 1959), and in the 1960s, numerous bays around Tasmania that had been identified as important nursery habitats for G. galeus and M. antarcticus were protected. Despite these efforts, by the late 1980s G. galeus populations had been severely depleted (see Punt et al. 2000 for a detailed discussion of declining catch rates of G. galeus). In response, an interim management plan was introduced that further restricted access to these nurseries in an attempt to reduce the incidental mortalities considered to hinder the population's recovery capacity (Williams & Schaap 1992). During the 1990s, an investigation into the G. galeus nursery areas around Tasmania revealed that juvenile numbers within the nurseries had plummeted since Olsen's (1959) original observations. Whereas Olsen could handline up to 80 juveniles a day in the period 1948–1952, in 1992 no school sharks were caught in 23 hours of fishing in the same location and using the same technique (Stevens & West 1997). Concurrently, the standardized catch rate for G. galeus declined by over 50% from 1983 to 1997 (Punt et al. 2000). Thus, despite nursery-focused protective measures that had been in place for around 30 years, G. galeus populations had declined to the point of fishery collapse because fishing of adults had continued unsustainably over the same period. Nursery area management in the absence of effective protection for mature individuals led to declining numbers of pups until managed areas contained so few pups that their classification as nurseries was unwarranted.

Following the decline of G. galeus populations, the Southern Shark Fishery switched focus to the less profitable, but evidently more sustainable M. antarcticus. Prince (1992) attributed the apparent sustainability of the M. antarcticus fishery to the fact that only certain sized sharks were vulnerable to the fishery. He characterized this as a “gauntlet fishery,” in which only a subset of the population is exposed to fishing pressure. Subsequent demographic models helped refine this explanation by revealing that fishing effort focused on particular age classes, specifically the youngest age classes, could yield sustainable fisheries for certain shark species. In his demographic model of C. obscurus in a western Australian fishery, Simpfendorfer (1999) found that up to 64.6% of the youngest age class could be removed without decreasing the intrinsic rate of populations increase, as long as fishing did not occur on any other age class. This contrasted with a maximum of 4.3% sustainable removal when fishing effort is spread across all age classes. If considered on a simple biomass extracted basis the taking of a small proportion of larger animals may be preferable, the use of yield per recruit analysis would provide improved information in this situation. However, for the C. obscurus fishery the smallest individuals achieve a significantly greater price and so maximizes economic yield. This indicates the complexity of gauntlet fisheries since many factors including biology of the species and economics of the fishery will impact the effectiveness of such a strategy.

Prince (2005) came to a similar conclusion regarding the removal of young individuals for why the fishery for G. galeus collapsed but the fishery for M. antarcticus succeeded in southern Australia. Galeorhinus galeus were fished throughout the year and across all age classes, leading to rapid declines wherever they where fished intensively. Conversely, a combination of gear selectivity and age-specific swimming patterns, which increased the probability of mesh entanglement for younger individuals (Stevens & West 1997), led to the fishery for M. antarcticus selectively targeting mostly the younger age classes. Subsequently, the term “gauntlet fishery” was modified to define fisheries that focus effort on younger age classes while leaving adult populations relatively unfished (Prince 2005).

The usefulness of gauntlet-style fisheries for sharks relates to the shape of their stock–recruitment curve (the relationship between the number of recruits and the number of mature breeders). Whereas teleost stock–recruitment curves typically have high curvature that translates to high recruitment even at low population sizes, shark stock–recruitment curves typically have limited curvature, meaning recruitment is strongly related to the size of the breeding population. Thus, for sharks any removal of the breeding population has a proportionally greater and longer-lasting effect on population size than a similar removal would have on a teleost population. Gauntlet fisheries therefore attempt to restrict fishing to younger age classes in recognition of the importance of maintaining sufficient breeding population sizes. The two most reliable methods for achieving this are to use highly size-selective gear, such as gillnets, or to confine fishing to areas where only the young age classes are typically found, which in many cases would be nurseries (Simpfendorfer 1999).

There is, however, an inherent danger in applying gauntlet fisheries to nursery areas due to the numerous ways existing nurseries are defined. Under the original definition of shark nurseries, Springer (1967) assumed that all nurseries were of equal recruitment value to the population. More recently, Beck (2001) redefined nursery area concepts for fish, establishing the idea of differential value to a population; that is, certain areas may be more valuable to population recruitment than others, and that only those with above-average contributions to the breeding population should be considered nursery areas. Beck's process for establishing the relative value of individual areas was complex, requiring extensive research over prolonged periods. Heupel et al. (2007) simplified this process for sharks when they revised the definition of shark nurseries to areas with high juvenile abundances across years (high in comparison to surrounding areas), relating this high abundance to high recruitment value for adult populations, therefore allowing a straightforward assessment of its importance. If gauntlet fisheries are established within nurseries that provide a uniquely high proportion of recruitment to the target population, this could put the population in danger of decline. Thus, before a gauntlet fishery is implemented, the recruitment value of target nurseries as well as the relative importance of other valuable nurseries for the species must be determined. It is also paramount to understand what rate of exploitation is sustainable; while younger age classes may be able to support proportionally more fishing pressure than older age classes, the concentrated nature of a nursery must be recognized. Without proper management a gauntlet fishery may still quickly overharvest young sharks and lead to a population decline.

The young age classes of some shark species are candidates for sustainable gauntlet fisheries because they can withstand proportionally higher rates of exploitation relative to older age classes. For other species, conserving neonates and young juveniles that reside in nursery areas will still play an important part in population stability, especially for nursery-using species that mature quickly. To date, only the fishery for M. antarcticus in southern Australia and the fishery for C. obscurus in western Australia exist as scientifically established examples of sustainable gauntlet fisheries, and seemingly little effort has focused on identifying other species for which such fisheries would be plausible. Instead, management continues to focus on the identification and protection of nursery areas as a strategy for stabilizing declining shark populations, despite strong evidence that such broad strategies overlook the importance of species-specific life history traits.

Possible consequences of nursery-centric management

  1. Top of page
  2. Abstract
  3. Introduction
  4. How important are young sharks for population persistence?
  5. Possible consequences of nursery-centric management
  6. Implications for shark management
  7. Conclusion
  8. References

It is not surprising that the different life history strategies among sharks make some species much more susceptible to over-exploitation than others. The same is true for conservation; protective measures that enhance the recovery of one shark species may be ineffective for other species, or even detrimental. Worryingly, nursery protection is a strategy often intended to promote the recovery of large-bodied, long-lived, and late-maturing shark species, but could prove more beneficial to those species that are comparatively smaller-bodied, shorter-lived, and earlier-maturing. Consider Negaprion brevirostris for which elasticities of large juveniles approaching maturity are higher than all other age classes (Frisk et al. 2005). Age validation studies indicate an average age at maturity of around 12 years (Brown & Gruber 1988). Extensive nursery area work on N. brevirostris conducted at Bimini, Bahamas indicates maximum residency periods in nurseries of around four years for juvenile N. brevirostris (Dibattista et al. 2007). As with C. obscurus, these findings suggest that protection of nursery areas alone would overlook the older juvenile age class that occurs outside of the identified nursery areas and instead protect the proportionately less important (in regard to population stability/recovery) neonate and young juvenile stages.

It should be noted that the Frisk et al. (2005) stage-based model for N. brevirostris included stage durations but only defined three stages. While Hoenig & Gruber (1990) produced an age-based model for N. brevirostris its lack of elasticity or sensitivity calculations precludes its usefulness in this case. However, the findings of Frisk et al. (2005) are in agreement with age-based models for biologically similar species, and while its limited number of stages reduces confidence, its use here remains appropriate in terms of its management implication.

The inconsistent suitability of nursery area protection is made apparent when N. brevirostris is compared to a smaller, more rapidly maturing shark species such as Mustelus canis. Whereas the older juveniles of N. brevirostris typically reside outside nursery areas for around 7–8 years before reaching maturity, M. canis attain maturity 6–18 months after leaving the nursery (Compagno et al. 2005). Species like C. obscurus or N. brevirostris would thus spend more time outside protected nurseries before reaching maturity than would species like M. canis. This disproportionately exposes the postnursery life stages of later-maturing species to greater risk of mortality before they can reproduce.

High mortality rates for these older juveniles, coupled with the continued exploitation of adults, inevitably leads to a reduction in the number of pups found within nursery areas. Again, this effect would be more pronounced for those species that are slower-growing, longer-lived, and attain maturity at a later age, while for species like M. canis the probability of surviving to maturity and successfully breeding at least once is comparatively greater.

These findings about the limited value of nursery-focused conservation-strategies are not limited to sharks, but have been identified in other long-lived marine species as well. For example, Caretta caretta (loggerhead turtle) is a large-bodied, slow-growing, late maturity species for which demographic models have identified the importance of older juveniles in maintaining a positive intrinsic rate of population increase. Heppell et al. (1996b) concluded that the loss of only a few hundred subadult and adult females each year could lead to extinction of the eastern Australian C. caretta in less than a century. Investigations into headstarting (the captive rearing of hatchlings from eggs collected in the wild) for marine turtles have revealed that attempts to boost the number of young turtles artificially have little to no effect on the population (Heppell et al. 1996a). Similar to Brewster-Geisz & Miller (2000) for C. plumbeus, Crowder et al. (1994) modeled the effects of 100% first year survival for C. caretta. Their model predicted that even at this extraordinary survival rate, the model population continued to decline. Later models for various marine turtle species (Chaloupka 2002; Mazaris et al. 2006) have come to similar conclusions in regard to the importance of subadult and adult individuals for population persistence.

Implications for shark management

  1. Top of page
  2. Abstract
  3. Introduction
  4. How important are young sharks for population persistence?
  5. Possible consequences of nursery-centric management
  6. Implications for shark management
  7. Conclusion
  8. References

Nursery areas are not stand-alone systems; the effects of depleted adult populations have direct effects on them due to the strong link between breeding population size and recruitment. Management strategies must include plans for the protection of both young age classes in nursery areas and older members of the population beyond nurseries. Similar to C. caretta, while the subadult and adult populations are the most important age classes in terms of maintaining a positive intrinsic rate of population increase there is still a strong positive relationship between first year survival and population persistence. Additionally, it is not hard to imagine that the functional elimination of coastal nursery areas though habitat destruction could push populations to a tipping point where suitable nursery areas become a limiting factor. Therefore, management must attempt to apply appropriate conservation measures to both year one individuals and older juveniles. For shark populations especially, managers must recognize the varied importance of these age classes and understand that while each is important for population persistence, management strategies must reflect the proportionally greater importance of older juveniles. More time- and resource-intensive, species-specific management should be a goal for shark conservation, at least for those species whose populations are depleted to the point where their intrinsic rate of population increase is in danger of becoming negative. This approach is important not simply because conservation efforts can disparately affect various species as previously discussed, but also because grouping species can mask local disappearances and declines. We must confront the idea that nursery area protection alone is typically not enough to ensure the stability of exploited, or recovery of depleted, shark populations. Instead, shark management must acknowledge both the diverse array of shark life history strategies, and the relative importance of different habitats to the various life stages of each species.

Implementing MPAs for species that show some site fidelity, such as reef-inhabiting sharks, may be a useful approach in certain cases (Bonfil 1999; Garla et al. 2006a, 2006b). However, for species thought to be fished at unsustainable rates, MPAs must be coupled with reductions in fishing capacity to avoid simply displacing effort to other sites (Fogarty & Murawski 1998). For species that lack site fidelity altogether or in all but the earliest age classes, maximum size limits may be beneficial as a way of protecting actively breeding individuals or those near breeding age, (i.e., maximum size limits that are less than the size at maturity), if this suits their particular life histories (Simpfendorfer 1999; Prince 2005). These are just some of the management options available to protect individuals approaching maturity. Again, management decisions must be made on a species-by-species basis and strategies will vary depending on a species' life history and level of conservation concern.

Nurseries designated for protection should be refined in accordance with more substantial criteria (Heupel et al. 2007) allowing managers to prioritize nurseries that contain higher neonate and young juvenile populations, have longer residency periods and are repeatedly used across years.

Conclusion

  1. Top of page
  2. Abstract
  3. Introduction
  4. How important are young sharks for population persistence?
  5. Possible consequences of nursery-centric management
  6. Implications for shark management
  7. Conclusion
  8. References

This review examined the importance of nursery areas to the management and recovery of shark populations. There is increasing information available demonstrating that well-protected and well-managed nursery areas are likely to provide little overall benefit to populations in the absence of management for other age classes. Demographic models and fisheries experience indicate that management focused on older juveniles (those that live outside nursery areas) and mature individuals may be most beneficial. Management plans must recognize the relative importance of various age classes to reverse the declining trends observed in some shark populations. While protecting nursery areas may not be able to conserve shark populations on their own, they remain an important component of broader shark management strategies.

Editor : Corey Bradshaw

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  2. Abstract
  3. Introduction
  4. How important are young sharks for population persistence?
  5. Possible consequences of nursery-centric management
  6. Implications for shark management
  7. Conclusion
  8. References
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