22. Dec, 2016

Becoming a shark: the hardships and mysteries of shark reproduction

Species living in the sea  differ in many respects from those on land.  Fishes  not only developed  special respiratory organs to  extract oxygen from water, but also different ways of reproduction than mammals. Sharks even have three different reproductive modes: viviparity, oviparity and ovoviparity. Viviparity  is seen as a more advanced level of reproduction than ovi- and ovoviparity. It probably evolved in a more recent  stage of  evolution in  certain species for which which  the benefits of increasing offspring survival exceeded the costs of reduced  mobility and the greater metabolic demands of carrying offspring throughout development.Viviparous sharks give  birth to living pups connected to a placenta just like in mammals. The hammerhead, bull, lemon and oceanic sharks for example are viparous.The opposite of viviparous is oviparous which are sharks  that lay eggs, like reptiles.  An example is the Jackson shark that lays eggs that have the shape of a corkscrew. In cat sharks  the leathery transparent eggs have the shape of a small purse. The third way of reproduction  is ovoviviparity  or aplacental viviparity. Ovoviparity is  found in many  big sharks, like the tiger, sand tiger and great white  shark. Here embryos develop inside eggs that are retained within the mother's body until they are ready to hatch. It is  similar to viviparous but differs in that there is no placental connection and the unborn young are nourished by egg yolk (see picture left). The young may eat non fertilised  eggs or even  other embryos in the uterus if the yolk sac is depleted. The pups of  the sand tiger shark have the reputation  to eat most of the  embryos of its siblings, leaving  only very few pups in a litter survive until birth.

New techniques have been developed in the last decades that allow to map migratory routes of sharks with more precision, and to identify their genetic identity. But the reproductive biology of elasmobranches is a highly complex process that is still not fully understood  by marine biologists. One reason being that  the nature of their habitats makes it very difficult to observe mating in the field.

Shark mating   In the eyes of the human observer  shark mating does not look like an affectionate and loving sexual event at all. During copulation, the male shark  will bite down on the female’s flank or fins to stabilize himself enough and then wrap his body around the female to  successfully insert one of his claspers for insemination.  Although the  shark is not an universally  beloved animal like the dolphin, its hard not to feel sorry for the  female shark when we observe the mating proces. But we must keep in mind that mating in animals serves only one purpose, which is reproduction. So copulation will only take place when the female is in estrus (with Pan, that is chimpanzees and bonobos as rare exceptions). Moreover, the mating behavior of the 'ferocious' male shark is not so different from that of the 'loveable' male dolphin, that also has a reputation of herding and sexual coercion to seduce a female.

More mates, more dads. Female sharks often copulate with different sharks (called polyandry). This may lead to multiple paternity (MP), implying  that one  litter of sharks contains baby sharks that are sired  by different fathers. MP has recently been established by marine biologists  taking DNA samples from adult females and their litters. It is the same technique  for DNA profiling  that has been  used in humans for kinship  analysis, paternity testing  and in forensic biology. There is however a  substantial variation between species, with  some species being predominantly polyandrous with a litter dominated by a several fathers, and other species genetically monandrous with litters dominated by single father. Also within  a species -such as leopard sharks living in the same territory-  some  litters are dominated  by one dad, while  others are shared by two or even more dads.  Mating with multiple partners and MP are more likely  to occur in situations  when males outnumber the females. Males may then  often unite in groups herding or mobbing to subdue the female. Which may further increase the level of stress of the female shark. Still, female sharks  are known to migrate each year over great distances to breeding sites where males congregate in greater numbers.

Costs and end benefits of polyandry. The evolutionary role of polyandry  is still  a matter of debate among  marine biologists. What benefits could there be for a female shark in enduring sexual intercourse with multiple partners,  with the risk of more physical injuries?  A direct positive benefit has been hard to establish so far.  But three explanations   seem to be accepted  most widely, in the following order.

1. Females engage in polyandry to avoid the physical costs such as harassment and injuries  associated with avoidance rather than acceptance, which is also called  convenience polyandry. The only benefit for the female shark then  would be  to keep the physical damage of mating within limits.  Stronger and bigger females might cope better with mating stress  than weaker species, thus diminishing the physical costs for themselves and enhancing the chance of fertilization of  a succesful offspring.

2. Females mate promiscuously because there is little opportunity to evaluate a male’s fitness prior to procreation. Mating with several males will therefore increase the likelihood of at least one of the males contributing to an increased offspring survival rate. And it might contribute to greate genetic diversity.

3. Females that take multiple partners create an environment that promote sperm competition, which ultimately might lead either increased fertilization success or perhaps better genes of their offspring. Fertilization may  happen right after the shark mates in which case the order of copulation determines when eggs are fertilized.  But many elasmobranches have developed the  ability to store the males sperm in specialized glands for long periods (a year or more) before using the sperm to fertilize their ova. Storing sperm also decreases the need for mating repeatedly to fertilize all ova during the breeding season. And it may facilitate post-copulatory influences on paternity by allowing either sperm competition, i.e. the competition among the ejaculates of different males,  and possibly also  the differential storage and utilization of sperm of different mates.  

Taken together, it seems that  multiple paternity  depends  a variety of factors such as the reproductive mode differences between sharks species, the occurrence of sperm storage in some shark species as well as the rate of male encounter, which in turn is influenced by factors such as population density, aggregative behaviour and site fidelity.

What about the puppies?  After fertilization the pregnant female sharks  will often move  to more protected  in-shore locations such as bays or mangrove forests, that are  suitable as nursery zones to deliver their pups. They then leave the pups, which already have the instinct and capacity to hunt smaller species in their habitat.  In the nurseries  the  vulnerable shark pups bide their time until they are big enough to venture out of their shelter. They  also  provide a shelter for  juvenile sharks ranging from several months to five years in age with a place to feed and grow.  Baby and juvenile sharks thus  lack parental care, and will not mix with adult sharks at the risk of being eaten by the bigger sharks, which may even  include  their own mothers.  A team of researchers recently  tagged nine baby  great white sharks right off the coast of Long Island, which gave rise to the suspicion  that there's a nursery of this powerful species just outside of New York City!  Even not so far from the Trump building.

Growing up Little sharks grow rapidly. This is especially true for the juvenile tiger shark that shows a growth rate of around 1 meter per year and  reaches maturity at a relatively young age. The average female tiger shark reaches maturity by age 5 and males by age 4. With an average length at birth of 1 meter, the adult tiger sharks  maximum size is typically between 380 & 450 cm, with a few individuals reaching 550 cm.Their rapid growth may be a strategy for reducing juvenile predation risk. Other shark species in the family of Carcharhinidae seem to  follow the same (albeit slower) growth pattern. 

Links and sources

http://www.nbcnews.com/science/one-female-sharks-litter-may-have-many-dads-study-finds-6c10848675

http://www.foxnews.com/science/2016/10/06/research-group-confirms-great-white-shark-nursery-off-new-yorks-long-island.html

  •  Byrne, R. J. & Avise, J. C. (2012). Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Marine Biology 159, 749–756.
  • Marino, I. A. M., Riginella, E., Gristina, M., Rasotto, M. B., Zane, L. & Mazzoldi, C. (2015). Multiple paternity and hybridization in two smooth-hound sharks. Scientific Reports 5, 1–11.
  • Daly-Engel, T. S., Grubbs, R. D., Feldheim, K. A., Bowen, B. W. & Toonen, R. J. (2010). Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversityin the shortspine spurdog Squalus mitsukurii. Marine Ecology Progress Series 403, 255–267.
  • Nosal, A. P., Lewallen, E. A., and Burton, R. S. (2013). Multiple paternity in leopard shark (Triakis semifasciata) litters sampled from a predominantl female aggregation in La Jolla, California, USA. Journal ofExperimental Marine Biology and Ecology 446, 110–114
  • Carl G. Meyer et al. (2014). Growth and Maximum Size of Tiger Sharks (Galeocerdo cuvier) in Hawaii. PLOS 1/January 2014. Volume 9. Issue 1