Reproductive Philopatry in Bull Sharks, by Rachel Wadsworth

The Bull Shark, Carcharhinus leucas, is an apex predator reaching lengths over 11 feet, and can be found prowling in shallow tropical and subtropical waters around the world (Tillett 2012). Adults have been tracked migrating long distances stretching over 2000 km, and are targeted by commercial and recreational fisheries throughout their range (Karl 2011, Lea 2015). Due to the large scale migration patterns observed of Carcharhinus leucas, it has been assumed there is no population genetic structure. However, further research challenges this assumption after discovering characteristics of female habitat use indicates philopatry. With declining population concerns observed by the fisheries, further understanding of how reproductive philopatry shapes the Bull Shark population structure is crucial in the development and implementation of an effective management plan (Karl 2011)

Reproductive philopatry is when an organism returns to a specific nursery to mate or give birth (Tillett 2012). Although marine, Bull Sharks are capable of move up streams into brackish and freshwater habitats. This behavior is observed during the reproductive cycle where females return to an estuarine nursery for parturition. This nursery is then utilized by juveniles for 4 years before migrating to ocean habitats (Tillett 2012). Studies have determined the nursery chosen by a female is not random, indicating reproductive philopatry. Males are rarely found in freshwater estuaries suggesting male-mediated dispersal due to mating events occur elsewhere, and only females showing reproductive philopatry (Tillett 2012). 

Female Bull Shark.  Source National Geographic

Research was conducted in Northern Australia to test reproductive philopatry in Carcharhinus leucas by determining if population structure exists between close nurseries and if the structure is shaped by sex-specific movements or geographic distance (Tillett 2012). The population structure and sex-specific movement patterns was analyzed by comparing the relatedness of juveniles within and between each nursery and genetic difference between msDNA and mtDNA. Microsatellite (ms) DNA was used to differentiate male genetics while mtDNA was used to identify female genetics. The study determined population structure among juveniles from different nurseries exists in mtDNA, but not in msDNA in closely located nurseries (Tillett 2012). Because the population genetic structure is absent in msDNA but present in mtDNA, the habitat and migration of males is different in females. Due to the lack of correlation between genetic and geographic distances, females straying to nearby rivers does not occur frequently enough for an increase in genetic similarities (Tillett 2012).

With an increasing human population, Bull Sharks are faced with increasing fishing pressures from commercial and recreational fisheries globally. Bull Sharks of all age classes are targeted, and very little records the catch data are kept (Karl 2011). Because of insufficient records, the current population trend is unknown. However, fisheries have reported noticing long term declines in Carcharhinus leucas populations. With little regulations and current management plans, it is believed this fishery is overharvested (Karl 2011).

Not only are Bull Sharks faced with increasing fishing pressure, but they are also faced with degrading habitats as a result of an increasing human activity and development along coasts. Anthropogenic activity near coasts alters crucial habitats both directly through modification and indirectly from pollution (Heupel 2010). The loss of estuaries is most concerning since these habitats are critical to the reproductive and juvenile stages of Bull Sharks. With new studies revealing female reproductive philopatry, the degradation of these estuaries is extremely alarming because the estuary chosen by a female is not random, shaping the population structure of bull sharks (Tillett 2012).

The degree of reproductive philopatry and sex based gene flow has a direct effect on population subdivisions and genetic structure (Karl 2011). New research studying genetic structure supports previous evidence of female reproductive philopatry and determined strong subdivisions with in the population over long and short distances (Karl 2011). The false assumption of the abundance and genetic connectivity for Carcharhinus leucas because these species are vastly distributed must be removed from conservation management strategies. Understanding population subdivisions and migration patterns as a result of sex biased reproductive philopatry is extremely important in the construction of conservation management strategies (Karl 2011). Failure to implement proper management strategies with the updated knowledge will cause overexploitation and local extirpation that will ultimately lead to global extinction (Karl 2011). The conservation of Carcharhinus leucas will require a global effort with management plans implemented at local, regional, and international levels.

The IUCN has listed Carcharhinus leucas as near threated as a result of heavy fishing pressures and the degradation of key estuaries (Lea 2015). The assumption of the abundance and genetic connectivity for Carcharhinus leucas due to the vast distribution is outdated with increasing evidence supporting female reproductive philopatry shaping population genetic structure (Tillett 2012). The importance of estuaries and sex based gene flow is a critical in the development of effective conservation management strategies (Karl 2011). The Bull Shark is an important apex predator, and conservation of this species is necessary for the health of marine ecosystems (Chapman 2015). Further research must be conducted on the Bull Shark to implement the most effective management strategy and ensure a prosperous future for this crucial species.

References


Demian D. Chapman, Kevin A. Feldheim, Yannis P. Papastamatiou, and Robert E. Hueter. (2015), There and Back Again: A Review of Residency and Return Migrations in Sharks, with Implications for Population Structure and Management. Annu. Rev. Mar. Sci. 2015. 7:547–70. doi:10.1146/annurev-marine-010814-015730


Feldheim, K. A., Gruber, S. H., DiBattista, J. D., Babcock, E. A., Kessel, S. T., Hendry, A. P., Pikitch, E. K., Ashley, M. V. and Chapman, D. D. (2014), Two decades of genetic profiling yields first evidence of natal philopatry and long-term fidelity to parturition sites in sharks. Mol Ecol, 23: 110–117. doi:10.1111/mec.12583


Heupel, M. R., Yeiser, B. G., Collins, A. B., Ortega, L. & Simpfendorfer, C. A. (2010). Longterm presence and movement patterns of juvenile bull sharks, Carcharhinus leucas, in an estuarine river system. Marine and Freshwater Research 61, 1–10.


Hueter, R. E., Heupel, M. R., Heist, E. J. & Keeney, D. B. (2005). Evidence of philopatry in sharks and implications for the management of shark fisheries. Journal of Northwest Atlantic Fisheries Science 35, 239–247.


Karl, S.A., Castro, A.L.F., Lopez, J.A. et al. Conserv Genet (2011), Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA,  Conservation Genetics 12: 371-382. doi:10.1007/s10592-010-0145-1


Lea, J. S. E., Humphries, N. E., Clarke, C. R. and Sims, D. W. (2015), To Madagascar and back: long-distance, return migration across open ocean by a pregnant female bull shark Carcharhinus leucas. J Fish Biol, 87: 1313–1321. doi:10.1111/jfb.12805


Tillett, B. J., Meekan, M. G., Field, I. C., Thorburn, D. C. and Ovenden, J. R. (2012), Evidence for reproductive philopatry in the bull shark Carcharhinus leucas. Journal of Fish Biology, 80: 2140–2158. doi:10.1111/j.1095-8649.2012.03228.x

Reproductive Philopatry in the Bull Shark, by Andrew Penney

The bull shark (Carcharhinus leucas), known for its aggressive nature and adaptation that allows it to live in brackish and freshwater environments in addition to the normal marine environment, is a requiem shark found worldwide in shallow coastal waters and rivers. Philopatry is defined as a behavior where an animal remains in or returns to a specific location and reproductive philopatry specifically refers to when adults return to a specific location to either mate or give birth (Tillett et al., 2012). Reproductive philopatry is significant because it can have a large effect on species management and conservation. If a local population of animal that practices reproductive philopatry experiences decline, the possibility of it recovering in that specific area is reduced and needs to be managed as a unique population separate from other populations of the same species (Tillett et al., 2012). Strategies such as shark nursery areas, spatial management of shark fisheries, and stocking areas with local and genetically similar populations would be better for philopatric animals (Hueter et al., 2005). Although bull sharks and sharks in general are not traditionally seen as philopatric animals, there is genetic and statistical evidence that shows bull sharks exhibit reproductive philopatry and this can have implications on the management and conservation of the species.

Bull sharks spend most of their time in warm, shallow waters along the coast and in rivers and feed on a variety of fish, birds, sea turtles, and mammals. Ecologically, they help keep the populations of their wide variety of prey items in check. Bull sharks are not known to migrate long distances consistently (Encyclopedia of Life). They usually breed during the summer months and young are born roughly 10 to 11 months after mating occurs (Encyclopedia of Life). Bull sharks are viviparous which means they give birth to live young and can have liters of up to 13 pups. Sexual maturity in bull sharks is estimated to occur at the age of 8 to 10 years old (Encyclopedia of Life).

One study that was conducted and supported the existence of reproductive philopatry in bull sharks used mitochondrial and microsatellite DNA comparisons in juvenile bull sharks. The study was conducted across 13 river systems in northern Australia and targeted the NADH dehydrogenase subunit 4 gene in mitochondrial DNA and three microsatellite loci in nuclear DNA (Tillett et al., 2012). The study found that there were population structures in the mitochondrial DNA but not at the same scale in the microsatellite DNA (Tillett et al., 2012). This supported the hypothesis that the population structure is caused by at least the females’ movements and supported the existence of reproductive philopatry in bull sharks. The lack of population structure in the microsatellite DNA and absence of sexually mature males in the nurseries suggest that the male bull shark’s movements are different (Tillett et al., 2012). Using the comparisons, they were also able to rule out the possibility that geographic barriers were the cause of the genetic structures in the populations of bull sharks because they did not find any clusters of haplotypes that were closely related enough in geographically similar locations to be caused by geographic barriers.

Bull Shark   Source Wikimedia Commons

Another study that was conducted looked at the change in populations and average length of various shark species (one of them being the bull shark) off the coast of Florida. The study looked at the effects of recreational fishing that took place in the 1970s and how overfishing caused the population and size decline of shark species in the area. The study showed that sizes and populations of sharks (one of them being the bull shark) declined heavily one at a time in coastal sites where recreational shark fishing was introduced, not at the same time across all the fishing sites (Hueter, 1991). This supports the hypothesis of reproductive philopatry in bull sharks because the population and size declines occurred one at time and was limited to the coastal area where the fishing took place. If bull sharks did not practice reproductive philopatry, then the population and size decline would have been seen at the same time in areas that were close to each other.

In conclusion, there is genetic and statistical evidence that shows reproductive philopatry in bull sharks. The study done in northern Australia used genetic evidence to support this hypothesis by comparing mitochondrial and microsatellite DNA in juvenile bull sharks across 13 river systems. Although the microsatellite DNA did not show any population structure, the mitochondrial DNA did which supported reproductive philopatry in at least the female bull sharks. This study was also able to rule out the possibility of geographic barriers causing the genetic structures in populations of bull sharks due to the lack of clusters of haplotypes in geographically similar locations that were closely related enough. The population and size study done in the coastal regions of Florida where commercial shark fishing occurred supported reproductive philopatry by showing that the declining size and populations occurred one at a time and separately as recreational shark fishing appeared in those coastal areas. Although these studies support the hypothesis of reproductive philopatry in bull sharks, more studies in different aspects could be done to make the hypothesis more concrete. For example, a study that uses tagging or another form of tracking method to study the actual movements of a bull shark would help make reproductive philopatry in bull sharks a more concrete hypothesis. However, a study like this could possibly take a long time if researchers decide to study a shark from when it is a juvenile to mature adult because it takes 8 to 10 ten years for a bull shark to reach sexual maturity.

References

Encyclopedia of Life. Available from http://www.eol.org. Accessed 01 Apr 2017.

Hueter, R.E. 1991. Survey of the Florida recreational shark fishery utilizing shark tournament and selected longline data. Mote Mar. Lab. Tech. Rpt., 232A: 1–94.

Hueter, R. E., M. R. Heupel, E. J. Heist, and D. B. Keeney. 2005. Evidence of Philopatry in Sharks and Implications for the Management of Shark Fisheries. J. Northw. Atl. Fish. Sci.  35: 239-247.

Tillett, B. J., Meekan, M. G., Field, I. C., Thorburn, D. C. and Ovenden, J. R. 2012. Evidence for reproductive philopatry in the bull shark Carcharhinus leucas. Journal of Fish Biology  80: 2140–2158.