Shark Nursery Areas: Concepts, Definition, Characterization and Assumptions
Shark Nursery Areas: Concepts, Definition, Characterization and Assumptions
Shark Nursery Areas: Concepts, Definition, Characterization and Assumptions
REVIEW
ABSTRACT: The concept of elasmobranch species using nursery areas was introduced in the early
1900s and has been an accepted aspect of shark biology and behavior for several decades. Despite
several descriptions of how shark species use nursery areas and what types of regions nurseries may
be found in, no explicit definition of what constitutes a shark nursery area has been presented. Here
we evaluate the assumptions of the current shark nursery paradigm in light of available data. Based
on examination of these assumptions and available methods of quantifying and accurately describing
shark nursery areas, a new more quantitative definition of shark nursery areas is proposed. This def-
inition requires 3 criteria to be met for an area to be identified as a nursery: (1) sharks are more com-
monly encountered in the area than other areas; (2) sharks have a tendency to remain or return for
extended periods; and (3) the area or habitat is repeatedly used across years. These criteria make the
definition of shark nursery areas more compatible with those for other aquatic species. The improved
definition of this concept will provide more valuable information for fisheries managers and shark
biologists.
weak definition of the shark nursery area concept To promote some consistency with which the term
means that such identification and prioritization is dif- shark nursery area is used, and so help improve the
ficult, if not impossible. identification and protection of EFH, we review the
The lack of methods to define and identify nursery history of the concept and propose a clear definition
areas is not restricted to sharks. Beck et al. (2001) iden- of the term that is consistent with theoretical consider-
tified the problem more generally in aquatic organisms ations while allowing practical application. In addi-
and also provided a framework by which nursery areas tion, consideration is given to: (1) what data may
could be assessed. These authors pointed out that estu- appropriately be used to identify a shark nursery
arine and marine ecosystems are often referred to as area; (2) the validity of some assumptions that are
nurseries although the nursery–role concept has rarely made concerning shark nursery areas; and (3) future
been stated clearly or tested. They defined a nursery as directions for nursery area research that will improve
a region where juvenile fish occur at higher densities, the concept.
avoid predation more successfully, grow at a faster rate
than in other habitats and so provide a greater relative
contribution to adult recruitment, than other areas. HISTORY OF THE CONCEPT
Such a definition means that not all areas where juve-
niles occur can be considered nursery areas, only those The concept of shark nurseries arose in several early
that make a proportionally greater contribution to the studies that summarized observations on the general
adult stock than the average. organization of shark populations. Although these con-
In the years since the publication of Beck et al. (2001) cepts have been carried forward, they were all based
the approach advocated has been embraced by teleost on observations not designed for examining shark
and invertebrate researchers and has been applied in a nursery function. Originally, Meek (1916) reported that
variety of studies (e.g. Heck et al. 2003, Stoner 2003, shallow coastal waters were important nursery areas
Kraus & Secor 2005, Bethea et al. 2006). However, based on observations of pupping of 2 carcharhiniform
within the shark literature, the definition by Beck et al. sharks (Galeorhinus sp. and Mustelus sp.). Olsen
(2001) has gone almost unnoticed and the use of the (1954) reported nursery areas of the school shark Gale-
term ‘shark nursery area’ by a wide array of scientists, orhinus galeus in southern Australia, but like Meek
resource managers, and conservationists appears to be (1916) did not consider them in any detail. Springer
inconsistent and lacks proper scientific analysis and (1938, 1960, 1967) made comments regarding coastal
justification. In some cases regions are labeled shark shark species based on his observations along the east
nurseries simply because of the presence of a few juve- coast of the United States over several decades. He
nile sharks. Designation based on such limited data framed his comments in the context of a generalized
threatens to undermine the importance of protecting shark species and did not intend them to describe any
EFH by potentially identifying all coastal waters as species in particular:
shark nurseries.
‘In this hypothetical population, the young are
Strict application of the definition of a nursery area
born in the spring or early summer on specific
from Beck et al. (2001), however, is difficult. For exam-
nursery grounds that are in somewhat shallower
ple, Kraus & Secor (2005) attempted to apply the
waters than adults of the population usually fre-
revised nursery-role concept to white perch Morone
quent... The young in the hypothetical population
americana using otolith microchemistry. Although
remain in the vicinity of the nursery grounds while
they noted the value of the points made by Beck et al.
feeding and growing to sexual maturity but may
(2001), they also concluded that empirical testing of the
move from the area if forced to do so by seasonal
nursery-role concept can be difficult and clouded by
temperature changes.’ (Springer 1967, p. 153)
inter-annual variability in populations. This observa-
tion demonstrated that a strict definition of the nurs- Most researchers who study coastal shark species
ery-role concept can be difficult to apply. Beck et al. agree with the observations made by Springer (1967),
(2001) recognized this problem, noting that some habi- although no definition of what constitutes a nursery
tats are likely to serve as nursery areas even though area was laid out in his description. He did, however,
there is no definitive test to delineate their contribution consider the evolutionary significance when he ob-
to the adult population. Such a discrepancy between served that: ‘The availability of nursery areas, not only
the definition and the ability to practically apply it to suitable to each species but also comparatively free of
specific areas means that nursery areas would poten- predation by larger sharks, is very important in inter-
tially be identified only in rare situations, and so their species competition’ (Springer 1967, p. 159).
protection through EFH or other conservation regimes Bass (1978) built on Springer’s description based on
would be limited. prior observations of sharks in southern Africa (Bass et
Heupel et al.: Shark nursery areas 289
al. 1973, 1975) by suggesting that juvenile sharks may inter-specific and intra-specific predation. Castro
have 2 types of nursery areas: (1993) also described the organization of shark nurs-
eries in some detail from observations made in Bulls
‘An interesting feature of the distribution of nurs-
Bay, South Carolina. This described how seasonal
ery areas along the east coast of southern Africa is
migrations, mediated mostly by changes in water
that secondary nursery areas of tropical species
temperature, may result in a species having geograph-
often extend further into subtropical regions than
ically separate summer and winter nurseries. This con-
do the primary nursery areas. By primary nursery
cept appears to overlap with Bass’s description of pri-
areas is meant those where the young sharks are
mary and secondary nursery areas when he described
actually born and spend the first part of their lives.
how secondary nursery areas were often in more tem-
Secondary areas are those inhabited by the
perate regions.
slightly older but not yet adolescent or mature
sharks.’ (Bass 1978, p. 579)
Although somewhat ambiguous, the delineation of FIELD STUDIES
primary and secondary nurseries by Bass (1978)
reflects a more realistic view of most shark populations Concurrent with (and subsequent to) publications
than provided by Springer’s (1967) generalized de- that dealt with the shark nursery area concept, there
scription. Bass’s (1978) primary nursery areas are in have been numerous studies that have examined shark
essence the area where females give birth or lay eggs, nursery areas. These can be divided into 2 categories.
while the secondary areas are those in which juveniles Firstly, there are those that that have aimed to identify
spend the ensuing years as they grow towards matu- and map nursery areas. These studies have mostly
rity. taken a survey approach to determine the presence of
In a review of the early life history characteristics of juvenile sharks in specific regions, often in response to
northwest Atlantic Ocean carcharhinoid and lamnoid informational needs for the development of manage-
sharks, Branstetter (1990) commented on the utility of ment plans (e.g. Snelson & Williams 1981, Castro 1993,
nursery areas for juvenile shark growth and survival. Simpfendorfer & Milward 1993, Thorpe et al. 2004,
He suggested that food is unlikely to be a limiting Parsons & Hoffmayer 2005, Saïdi et al. 2005, Blackburn
resource for juvenile sharks since nurseries are typi- et al. in press, Gurshin in press, Neer et al. in press,
cally found in areas of high productivity that would Merson & Pratt in press, Parsons & Hoffmayer in press).
provide ample food for these opportunistic feeders. The second type of study has aimed to better under-
Instead, he suggested that predation risk is a much stand the function of nursery areas by investigating the
greater concern for young sharks within coastal waters ecology of juvenile sharks and the habitats in which
and identified 2 further types of nursery area: they occur. These detailed ecological studies have
often been undertaken over extended periods in loca-
‘The nursery grounds can be categorized by their
tions identified as potential nursery areas for specific
degree of exposure to potential predators. Some are
species. For example, sandbar sharks Carcharhinus
‘protected,’ because they are in areas infrequently
plumbeus in the Chesapeake Bay–Delaware Bay
inhabited by adult sharks, while others are very ‘un-
region (e.g. Medved & Marshall 1983, Wetherbee &
protected,’ because they are located in habitats oc-
Rechisky 2000, Merson & Pratt 2001, Rechisky &
cupied by adults.’ (Branstetter 1990, p. 18)
Wetherbee 2003, Grubbs & Musick in press, Grubbs et
Branstetter (1990) recognized that the degree of pro- al. in press), lemon sharks Negaprion brevirostris at
tection afforded by nursery areas can be variable, and Bimini, Bahamas (e.g. Gruber et al. 1988, Morrissey &
also that as such they represent a component of the life Gruber 1993a,b, Gruber et al. 2001, Sundström et al.
history of a species. We shall return to both of these 2001, Clermont-Edrén & Gruber 2005), scalloped ham-
concepts later. merhead sharks Sphyrna lewini in Kaneohe Bay,
In 1993, field surveys on sharks in US and Australian Hawaii (e.g. Clarke 1971, Holland et al. 1993, Bush &
bays reported that multiple species use the same loca- Holland 2002, Lowe 2002, Bush 2003, Duncan & Hol-
tion as potential nursery areas. Castro (1993) reported land 2006), sympatric coastal sharks (several taxa) in
9 species of shark utilizing Bull’s Bay on the US east northwest Florida (e.g. Carlson & Brusher 1999, Carl-
coast as a nursery area, and Simpfendorfer & Milward son 2002, Bethea et al. 2004, Bethea et al. 2006), and
(1993) reported 8 species utilizing Cleveland Bay on blacktip sharks Carcharhinus limbatus in central west
Queensland’s east coast. Simpfendorfer & Milward Florida (e.g. Heupel & Hueter 2001, 2002, Hueter &
(1993) referred to these locations as ‘communal nurs- Tyminski 2002, Heupel et al. 2004, Heupel & Sim-
eries’ and suggested that these shared nursery areas pfendorfer 2005, Heupel in press). In other instances
may have increased evolutionary benefits by reducing isolated ecological studies have occurred (e.g.
290 Mar Ecol Prog Ser 337: 287–297, 2007
Williams & Schaap 1993, Stevens & West 1997). These there is a paucity of data on exactly what constitutes a
ecological studies have provided data to further refine shark nursery and as a result a fairly broad or liberal
the concept of shark nursery areas. interpretation has been given to the largely observa-
Despite all of this research, there has been relatively tional work (i.e. Springer 1967, Bass 1978, Branstetter
little change in the shark nursery area paradigm since 1990, Castro 1993). Many of these studies have failed
it was first elucidated. As a result there is still a limited to provide compelling evidence that such areas pro-
view of what a shark nursery area actually consists of, vide a nurturing function for the juvenile sharks that
or how one can be defined. Few studies have specifi- ultimately contribute to the adult population. For
cally tested hypotheses on the quality of a proposed example, Simpfendorfer & Milward (1993) concluded
nursery habitat or areas. Most authors still suggest that Cleveland Bay on the Queensland coast was a
these regions must benefit the young by providing nursery area for at least 8 species based purely on the
ample food resources and protection from predation occurrence of neonate or juvenile specimens in sur-
based on the early conceptual work of Springer (1967), veys. They provided limited information to support the
Bass (1978), Branstetter (1990) and others. However, concept that this area provided any advantages to the
questions still arise about this current paradigm of populations. Many other current and previous
shark nursery areas: research efforts that have identified and mapped nurs-
• Can this paradigm be used as a definition for a shark ery areas have similarly defined nursery regions based
nursery area (i.e. a region providing abundant food on the presence of juvenile individuals and little else,
and reduced risk of predation as compared to other e.g. Castro 1993, Thorpe et al. 2004, Blackburn et al. in
regions) and can it be used to delineate habitats or press, Merson & Pratt in press. As such, vast tracts of
regions of critical importance during early life coastal bays and estuaries have now been identified as
stage(s)? nursery areas based simply on the fact that juvenile
• Does this paradigm equip current and future sharks were observed there. The risk with this
researchers with a clear enough definition to use the approach is that with such broad areas being defined
term appropriately and consistently in scientific as nurseries, the ability to conserve habitat —
research (i.e. for hypothesis testing) and in presenta- especially the most valuable habitats — is diluted (Beck
tions and publications? et al. 2001). This has lead to growing concern that pro-
• Finally, given what has been published in the 40 tecting areas for juvenile sharks is unrealistic since
years since the Springer (1967) description of a hypo- they cover such a large amount of ocean.
thetical population, is there a need for a change in One factor that makes the delineation of shark nurs-
the shark nursery area paradigm, and can we do any ery areas difficult is the mobility of many sharks, even
better at defining this term than those who have while young. The precocious nature of newborn sharks
done so before us? means that they are normally mobile, have relatively
large home ranges (e.g. Holland et al. 1993, Morrissey
& Gruber 1993a, Wetherbee & Rechisky 2000, Merson
WHAT CONSTITUTES A SHARK NURSERY AREA? & Pratt 2001, Heupel et al. 2004) and typically occur in
a range of habitats (e.g. Castro 1993, Holland et al.
A ‘nursery’ is defined as ‘something that fosters, 1993, Morrissey & Gruber 1993a, Grubbs & Musick
develops or promotes’ and ‘a place where animals are 2002, McCandless et al. 2002). This is not to say that
cared for’ (Babcock 1993). Such a definition undoubt- they do not have relatively high levels of site fidelity,
edly formed the basis for the development of the nurs- just that they are less likely to be constrained to indi-
ery area concept for sharks (e.g. Springer 1967, Bass vidual habitat types in the way many teleost and inver-
1978, Branstetter 1990). However, early work on this tebrate species are (Beck et al. 2001). This limits our
subject was based on observations from researchers ability to describe a specific habitat as being typical of
who had spent many years working with sharks and shark nursery areas. In addition, sharks can move out
who summarized their observations into a simple con- of one potential nursery area to new regions which
cept that could be applied broadly. This has provided a may, or may not, act as nurseries.
detailed background to the problem, but this back-
ground has been poorly supported by empirical studies
designed to test the benefits of specific areas to shark ASSUMPTIONS
populations.
Scientists and resource managers have concluded In the 40 years since the publication of Springer
that nursery areas must benefit the population as a (1967) on the social organization of shark populations,
whole and have expended considerable resources and several aspects of the shark nursery area concept have
effort in mapping and identifying them. However, become accepted as fact, even though they have
Heupel et al.: Shark nursery areas 291
rarely, if ever, been thoroughly tested. These assump- tribute to recruitment into the adult population. How-
tions have resulted from the vague nature of the cur- ever, several species of small coastal sharks with small
rent definition of shark nursery areas and from the lag sizes at birth appear not to have nursery areas. For
between the development of theory and the collection example, blacknose sharks Carcharhinus acronotus
of data to test it. Here we examine a number of these give birth in a wide variety of coastal habitats, from
assumptions and the evidence for or against them in an shallow coastal bays (Carlson 2002) to open beaches
attempt to help further the development of the shark where large predators are known to be present (C. A.
nursery area concept. Simpfendorfer unpubl. data). Based on the small size of
blacknose shark pups (ca. 29 cm TL) it would seem log-
ical for these newborn sharks to occupy some form of
1. All sharks have nursery areas protected habitat as a means of avoiding predation.
Similarly, Atlantic sharpnose sharks Rhizoprionodon
The vague definition in the literature, where the terraenovae which are among the smallest of coastal
occurrence of juveniles is the only criterion for identi- species are born offshore, recruit to coastal bays in
fying a nursery, has meant that all shark species would spring (Carlson 2002, Parsons & Hoffmayer 2005) and
be considered to have a nursery or nurseries. Such a then appear to move throughout adjacent coastal habi-
definition, however, is increasingly out of step with the tats during summer (J. K. Carlson & M. R. Heupel
nursery concepts for other groups of aquatic organ- unpubl. data). Movements among adjacent bays would
isms, where definitions such as that of Beck et al. theoretically expose these sharks to higher predation
(2001) have been adopted. With stricter definitions than would be afforded if individuals remained within
there will be fewer areas identified as shark nurseries, confined, shallow regions. These small coastal sharks
and some species may have no nursery areas at all. are species that have relatively productive life history
This concept is consistent with the observations of strategies (i.e. rapid growth, early maturity, annual
Springer (1967) who noted that some species do not reproduction etc.) and high rates of population growth
have defined nursery areas, e.g. tiger shark Galleo- (see Cortés 2002 for a review) when compared to other
cerdo cuvier. There is also variation in the occurrence shark species. Given a life history that is relatively tol-
of potential nursery areas between stocks of the same erant of juvenile mortality, the benefits of nursery
species. For example, sandbar shark nursery areas areas for these species may be limited.
have been documented in bays along the east coast of For species that have small size at birth and slow
the United States (Grubbs & Musick in press, Grubbs juvenile growth rates the opposite is probably true (i.e.
et al. in press), while off Western Australia the young they may be more likely to have nursery areas), since
occur offshore and appear to not have a distinct nurs- the population would be more susceptible to higher
ery area (McAuley et al. in press). McElroy et al. (2006) juvenile mortality. One example of a shark with this
also found no use of bays as potential nurseries in type of life history strategy is the school shark Gale-
Hawaiian waters. orhinus galeus. Olsen (1954) identified a number of
With fewer areas identified as nurseries, we antici- areas for this species in eastern Tasmania and Victoria,
pate that the terms pupping, birthing or hatching areas Australia, where high densities of newborn animals
will be more commonly used in the literature to indi- were regularly observed. The life history of school
cate areas where the young are born or hatched. sharks includes a small size at birth (33 to 35 cm, Com-
Unlike the present situation where all pupping areas pagno 1984), slow growth (von Bertalanffy K = 0.124)
are considered nursery areas, a stricter definition and late maturity (ca. 8 yr, Moulton et al. 1992). Based
would mean that some pupping areas may be nurs- on these life history characteristics this species may
eries, but not all. directly benefit from the use of nursery areas.
Rather than assume that all sharks have nursery Trade-offs between life history components would
areas, we suggest that they are one component of a also suggest a species that has protected nursery areas
shark’s life history. Branstetter (1990) introduced this may be predicted to have fewer young and have longer
concept and suggested that there was a relatively com- periods between reproductive events since the young
plex trade-off relationship between this and other life should have higher survival rates. Support for this
history components. In addition to nursery areas, size- hypothesis comes from the blacktip shark Carcharhi-
at-birth, rate of growth, time to maturity, litter size and nus limbatus, which has some well defined nursery
frequency of breeding are probably important factors areas (Heupel & Hueter 2002, Hueter & Tyminski 2002,
in life history strategy trade-offs with nursery areas. Keeney et al. 2003, Heupel et al. 2004, Heupel &
It is often assumed that sharks with a small size-at- Simpfendorfer 2005). This species has relatively small
birth would benefit from protected nursery areas as it litters (4 to 6 pups) and females produce litters every 2
would increase their chance of survival and so con- yr after reaching maturity (Castro 1996).
292 Mar Ecol Prog Ser 337: 287–297, 2007
The above examples demonstrate that nursery areas to the low calorific value of their main prey types and
are potentially traded-off with other components of the intense competition for food with congeners immedi-
life history strategy of sharks. It follows that only those ately after birth. Bush & Holland (2002) hypothesized
species for which nursery areas provide some increase that this food limitation may be unique to this location
in production are likely to benefit from using them. At because of the limited productivity of the island
the very least, there will be different levels of nursery ecosystem. However, more recently, similar situations
area use. However, we suggest that further research is have been reported for young-of-the-year bonnethead
needed to help with the identification of habitats as (Carlson et al. 2004) and Atlantic sharpnose sharks
nurseries: this would involve improved definition of (Hoffmayer et al. 2006) in the northern Gulf of Mex-
attributes of habitat that enable increases in produc- ico. While Atlantic sharpnose sharks may not have
tion. Given that reduced predation risk is unlikely to nursery areas, and it is doubtful for bonnethead
be a factor in the increase in production for unpro- sharks, these studies clearly demonstrate that new-
tected nurseries, other factors such as those that born sharks may be more food limited than previously
increase rates of growth (e.g. abundant food, optimal contended by nursery area studies.
temperatures) and reduce time spent at vulnerable Sympatric species of sharks are often found simulta-
smaller sizes may be more important. In some cases it neously occupying a proposed nursery (i.e. the com-
may be found that areas considered to be ‘unprotected munal nursery of Simpfendorfer & Milward 1993). One
nurseries’ do not increase production and so are not disadvantage of several species utilizing the same
nurseries at all. nursery area is the increased chance of competition.
The need to better define shark nursery areas and to However, Bethea et al. (2004) found that moderate
apply testable criteria will require the shark research overlap in diet resources was offset by low overlap in
community to provide greater proof when reporting habitat use by 4 species of sharks in Apalachicola Bay,
nursery areas. Not all species will have nursery areas, Florida. If diet resources are limiting in this bay, then
and not all areas where juvenile sharks occur will be sharks may distribute themselves on different spatial
nursery areas. This will help focus conservation and and temporal scales to reduce competition pressure.
management efforts for nursery areas on those that Further evidence indicates that in some habitats juve-
provide the greatest value to the populations. This will niles do not distribute themselves in relation to food
also allow better definition of birthing and hatching abundance. Juvenile blacktip shark movement pat-
areas, providing additional information for manage- terns and habitat use were more consistent with preda-
ment of these areas as needed. tor avoidance than with prey distribution (Heupel &
Hueter 2002, Heupel & Simpfendorfer 2005). Thus
although some putative nursery areas are highly pro-
2. Nursery areas provide ample resources for ductive, it seems likely that some shark species are
juvenile sharks selecting these habitats based more on predator avoid-
ance trading-off against food consumption. This obser-
Conventional shark nursery area theory assumes vation is consistent with the theoretical considerations
that nursery areas provide the most advantageous of Heithaus (in press) that individuals may select habi-
habitat for the growth and survival of young sharks by tats based on trade-offs between food availability and
being in productive areas and having an abundant predation risk.
supply of food. While this concept is intuitively sensi- The preponderance of food in nursery areas that has
ble, field studies are drawing this assumption into for decades been a central tenet of the shark nursery
question. Lowe (2002) reported low energetic con- concept therefore appears to be in question. While
dition of neonate scalloped hammerhead sharks some nurseries may have ample food resources, food
Sphyrna lewini in Kaneohe Bay, Hawaii. Using res- limitation does occur in others. Further research to
pirometry, tracking and a bioenergetic model he cal- investigate if food limitation occurs in the nursery
culated that in the first summer after birth many indi- areas of other species is required to determine how
viduals did not consume enough food to maintain a wide-spread this phenomenon is. Research to investi-
constant growth rate. As a result, he hypothesized gate the causes of food limitation may also reveal new
that a substantial proportion of these animals die from insights into the functioning of nursery areas and the
starvation. Bush (2003) also demonstrated that food advantages they provide. These studies should also
consumption rates in Kaneohe Bay were below those consider historical aspects of the habitat where possi-
estimated by Lowe (2002) to meet energetic demands. ble. Many coastal habitats have been altered, har-
Duncan & Holland (2006) demonstrated that weight vested or degraded. Human use of these regions may
and condition factor declined in S. lewini during their have changed their dynamics. If sharks are philopatric
first summer. Lowe (2002) attributed this phenomenon to these regions (e.g. Hueter et al. 2005) they may con-
Heupel et al.: Shark nursery areas 293
tinue to use a region that was historically a good nurs- crete from adult habitat for one species, proposed
ery, but at present does not provide the benefits it once nurseries are commonly located in areas frequented by
held. large individuals of other species. For example, Pine
Island Sound, Charlotte Harbor, and Apalachicola Bay,
Florida could be documented as potential blacktip
3. Nursery areas reduce predation risk and therefore shark nursery areas (Carlson 2002, Hueter & Tyminski
have low mortality rates 2002). These areas are known to have high densities of
newborn blacktip sharks (measured as a standardized
The assumption that shark nursery areas provide catch-per-unit effort) over many years, compared to
protection from predation should lead to the prediction lower densities in adjacent habitats. Although these
that natural mortality rates of juveniles within these areas are relatively shallow estuaries (< 4.0 m deep)
habitats are low compared to rates in non-nursery they are large systems and are inhabited by juvenile
areas. Data concerning survival rates of young sharks, and adult bull, great hammerhead, and lemon sharks
however, are very limited and are often based on life (J. Carlson unpubl. data, M.R. Heupel unpubl. data).
history correlations (e.g. Cortés 2002, Simpfendorfer et The continuous presence (inferred from acoustic and
al. 2005a). In addition, if a species is known to use satellite monitoring data) of larger sharks known to
nursery areas as a means to reduce mortality it is often prey on elasmobranchs suggests that newborn black-
difficult to determine what the mortality rate, would be tip sharks are exposed to predation within these poten-
outside the nursery because of their mobility, which tial nurseries. Whether juvenile blacktip sharks
may make apportioning mortality to a specific site or employ strategies to avoid predators within the nurs-
habitat complex. Despite this, some data on the mortal- ery is currently poorly understood. Based on ecological
ity rate of sharks in proposed nursery areas are avail- theory Heithaus (in press) suggested that juvenile
able. Analysis of acoustic monitoring data of juvenile sharks should aggregate to avoid predators if foraging
blacktip sharks within Terra Ceia Bay, Florida, times were short. Aggregation behavior was reported
revealed natural mortality rates of 32 to 70% in the first for naïve populations of neonate blacktip sharks over 3
15 wk of summer (Heupel & Simpfendorfer 2002). Sim- consecutive years within a nursery area (Heupel &
ilarly, Manire & Gruber (1993) estimated 44 to 61% Simpfendorfer 2005) suggesting that this is a natural
and Gruber et al. (2001) reported 35 to 62% of neonate behavior for some species of sharks and therefore that
lemon sharks Negaprion brevirostris born at Bimini, predation affects movement patterns and habitat use
Bahamas, died in their first year. These mortality rates within a nursery area. If predation risk was only a
suggest that nursery areas may not always provide suf- minor concern for these individuals it seems unlikely
ficient resources or protection from predation. The that their behavior patterns would focus on predator
importance of predation as opposed to food limitation, avoidance.
which may result in starvation (see above), cannot eas- More research is required to fully understand the
ily be determined and awaits further research. How- role that predation plays in nursery areas. As previ-
ever, a multi-year study of the lemon shark nurseries in ously discussed, some species may trade low food
Bimini has revealed no evidence for starvation and so availability and hence high starvation risk, for lower
mortality in these areas is likely to be the result of pre- predation rates. Studies that manipulate predator lev-
dation (S. Gruber pers. comm.). els within nursery areas would especially increase our
Mortality rates of some young sharks, however, understanding of how juvenile sharks modify their
appear to be considerably lower than those estimated behavior to avoid predators, and how natural mortality
for blacktip and lemon sharks. For example, only 4 of is partitioned among starvation, predation and other
55 individual young-of-the-year bull sharks Carcharhi- sources.
nus leucas suffered mortality over a 3 yr period (M.R.
Heupel unpubl. data). This low level of mortality may
be the result of bull sharks utilizing rivers where salin- 4. Primary nursery areas overlap with secondary
ity is below those that are tolerated by other shark spe- nursery areas
cies and potential predators (Simpfendorfer et al.
2005b). Thus there appears to be at least some areas The concept of primary and secondary nursery areas
that produce very low rates of mortality, possibly due is a difficult one to define. The original description by
to low rates of predation. Bass (1978) is not detailed enough to provide clarity.
An extension of this assumption is that adult sharks Careful examination of Bass (1978) reveals that his
(i.e. predators) are not present or are present in only original description implied 2 geographically discrete
relatively small numbers within nursery areas. regions (note that ‘Natal’ is referring to the South
Although nursery areas are often geographically dis- African province):
294 Mar Ecol Prog Ser 337: 287–297, 2007
‘An example of this phenomenon is shown by Car- primary and secondary nursery as observed by Bass
charhinus plumbeus. Immature C. plumbeus of 90 (1978). We suggest that regions containing newborn
to 160 cm are fairly common in Natal waters, but and juvenile sharks be limited in description and sim-
newborn specimens (60 to 65 cm in length) are ply referred to as nursery areas providing they meet
completely absent.’ (Bass 1978, p. 579) the criteria proposed herein. The distinction between
primary and secondary nurseries awaits a more suit-
Bass (1978) also stated that newborn sharks move able scientifically acceptable definition.
from the primary nursery to the secondary nursery, and
reported evidence from at least 5 other species along
the African coast. Therefore descriptions of overlapping PROPOSED DEFINITION
primary and secondary nursery areas appear to contra-
dict the original definition. Secondary nursery areas are It is our contention that the occurrence of juvenile
currently interpreted as regions where older (non-new- sharks in an area is insufficient evidence to proclaim it
born) sharks occur regardless of whether newborns are a nursery. Such a liberal definition does not demon-
present or not (see McCandless et al. 2002). Therefore, strate the value of a habitat or region to a population,
current usage of this term allows direct geographic and would probably result in most coastal areas being
overlap of primary and secondary nursery areas. identified as shark nurseries. If we assume that Beck et
Although this seems like a minor distinction, Bass al.’s (2001) assertion is correct, then juveniles pro-
(1978) stated that individuals of different size classes duced in nursery area habitat should have increased
were not sharing habitat and must have moved from production relative to those from other non-nursery
one region to another. The limited definition provided habitats, since these individuals will be more likely to
by Bass (1978) leaves it to the reader to interpret the end up in the reproductive population. Such an
definition of these regions. If an individual is born in a assumption should result in 2 phenomena. First, natal
nursery area (therefore primary nursery), migrates homing and philopatry would more than likely occur
away for the winter and returns to the natal nursery as and so these habitats would be used year after year.
a 1 or 2 yr old individual, does that mean this is also a Although there is limited data regarding these phe-
secondary nursery? If so, is it useful to have 2 classifi- nomena in sharks there is increasing evidence that it
cations for the same region? What if, as in the case of occurs (Hueter et al. 2005). For example, Keeney et al.
some tropical species, sharks remain within the pri- (2003) provided genetic evidence that Carcharhinus
mary nursery for a period of several years? Is the limbatus is philopatric, at least to broad coastal bays.
region then both a primary and secondary nursery if Second, there would be a tendency for individuals to
individuals never left the primary nursery? The com- have a high level of site fidelity to these areas because
plex and variable nature of shark life history strategies these areas have the ability to increase production.
makes it difficult to apply the term secondary nursery Thus it is possible to define a nursery on the basis of a
to these populations in a uniform manner. species’ abundance, residency and inter-annual use.
On the opposite side of this issue is the fact that indi- We suggest that a shark nursery area could be
viduals of some species leave the primary nursery for defined based on 3 primary criteria for newborn
the winter and may then utilize a different area in the or young-of-the-year (i.e. individuals <1 yr old):
following summer that may be >100 km away from the (1) sharks are more commonly encountered in the area
primary nursery. Is the new region a secondary nurs- than in other areas, i.e. density in the area is greater
ery? If this area is labeled as a secondary nursery then than the mean density over all areas, (2) sharks have a
highly dispersed sharks will result in large tracts of tendency to remain or return for extended periods
coastline being labeled as nursery. This labeling (weeks or months), i.e. site fidelity is greater than the
dilutes the effectiveness of defining a nursery and mean site fidelity for all areas, (3) the area or habitat is
clouds the issue for management purposes. It is critical repeatedly used across years, whereas others are not.
that a common definition be determined for these This proposed definition does not discount the im-
regions and that terminology is standardized. If this portance of other factors identified previously by
fails to happen, the applicability of these data for con- research, such as food abundance or refuge from
servation and management is severely diminished. predators. Instead it provides researchers and resource
Based on the ambiguity of the original definition put managers a definition that can be tested in a straight-
forth by Bass (1978) and observations of tropical spe- forward manner using data collected in the field.
cies remaining within nurseries for periods of several These proposed criteria remove much of the ambigu-
years (Castro 1993, Heupel unpubl. data), it seems ity that exists in many published shark nursery studies.
inappropriate to attempt to apply qualifiers to those The necessity of encountering a relatively large number
regions. Therefore we propose elimination of the terms of individuals that remain within the area and use it over
Heupel et al.: Shark nursery areas 295
multiple years increases the amount of information that area paradigm may trouble some researchers and
is required to demonstrate an area is a nursery and resource managers. However, if science is to keep
would discount some that are currently considered nurs- pace with the needs of resource management and our
ery areas. For example, if a group of sharks are captured growing understanding of nursery areas, this shift is
together off a beach en route to their winter grounds, this essential. We hope that this paper will lead to a period
area would not be considered a nursery since there is no of transition, during which the merits of criteria for
residency (i.e. site fidelity) in the area. However, given identifying shark nurseries are debated and sound sci-
the criteria used in many past and current studies, the ence to support them is undertaken. Such a transition
area would be considered a nursery area. This is not to should allow the emergence of a new paradigm on the
discount the potential importance of this habitat as a mi- concept of shark nursery, forming the basis for
gratory corridor, but we argue that there is no evidence improved management of these areas and for further
that the area is providing a nursery function. research and monitoring.
The more rigorous nursery area definition set forth
by Beck et al. (2001) has proven difficult to implement;
Acknowledgements. We thank J. Bass and S. Gruber for in-
we believe our definition can be more easily used to
formation pertaining to this manuscript and P. Sheridan for
define and test whether a region qualifies as a shark valuable comments on an earlier draft.
nursery. Currently available techniques can be used to
determine if an area meets the criteria. Scientific sur-
veys can be designed to quantify the number of sharks LITERATURE CITED
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Editorial responsibility: Howard Browman (Associate Editor- Submitted: May 22, 2006; Accepted: September 28, 2006
in-Chief), Storebø, Norway Proofs received from author(s): April 22, 2007