Natal homing: the animals that always find their way back home

By Rachel Chan 

Natal homing is a process whereby animals return to their birthplace to reproduce, despite dispersing long distances away in their adult lives (Lohmann, Putman & Catherine, 2008). The long journey can prove to be beneficial, as their natal region provides a suitable and safe breeding ground. This is common in marine animals such as sea turtles, salmon, and bluefin tuna. The ability to navigate across expansive oceans to their birthplace is a fascinating feat, and several hypotheses have been put forward (and proven) to partially explain this. 

Many species of Pacific salmon spawn in streams or lakes and migrate to the ocean after a few years for better foraging opportunities. Once mature, they return to their natal site to spawn, often exactly to their river of origin, travelling hundreds or thousands of kilometres to do so (Dittman & Quinn, 1996). While their ocean navigation is less understood, more research has been done to investigate their final stage of migration through freshwaters. This stage involves olfactory imprinting, where salmon can distinguish between waters of different streams using their sense of smell. The hypothesis was first introduced in the 1950s on the basis that streams differ in chemical makeup and are stable over time, so that salmon can learn this as juveniles and recognise these cues later in life (Hasler & Wisby, 1951). Using artificial odorants, experimental evidence has been provided in favour of olfactory cues in salmon migration (Cooper et al., 1976). A few decades later, it was found that odours were learned by Coho salmon (Oncorhynchus kisutch) at a specific period in their life cycle called the parr-smolt transformation (Dittman, Quinn & Nevitt, 1996). This transformation involves physiological and behavioural changes which are largely attributed to increased plasma levels of the hormone thyroxine. Indeed, it is also a general finding that salmon reared at one site but released from a different site prior to the transformation will return to the release site and not the rearing one (Jensen & Duncan, 1971).  

While olfactory imprinting has largely been proven experimentally, these studies usually involve hatchery-reared salmon and artificial odorants. In hatcheries, salmon are reared in stable conditions while conditions in the wild are constantly changing (Dittman & Quinn, 1996). Furthermore, the chemical makeup of streams is more complex, whereas the studies have used a single artificial odorant (Dittman & Quinn, 1996). There is much life history variation amongst different salmon species, indicating that there is much plasticity involved in the spatial and temporal aspects of this mechanism (Fleming, 1996). Ultimately, the mechanism of olfactory imprinting may be much more complex in wild salmon. A large uncertainty as well is their ocean navigation prior to reaching freshwater. Olfactory cues cannot extend as far as hundreds of kilometres into the open sea (Lohmann & Lohmann, 2019), prompting questions about the mechanism of their earlier phase of navigation. 

One of the most well-known examples of natal homing is sea turtles. Green turtles (Chelonia mydas) are an example of this: some populations nest on Ascension Island, and the hatchlings travel to forage near the Brazilian coast, a casual 2000 kilometres away (Endres et al., 2016).  Upon maturity, they return to Ascension Island to breed and nest. Amongst sea turtle species there is also variation in their precision of navigation and distances of migration. Some turtles will nest in their natal region rather than a specific beach – this behaviour may be beneficial as nesting areas can be destroyed by flooding or erosion (Dittman & Quinn, 1996). Their navigation is thought to be attributed to their ability to detect elements of the Earth’s magnetic field. They are also thought to use airborne and waterborne odorants as cues, but again this does not extend past the general vicinity of their natal area (Endres et al., 2016). 

Enter the geomagnetic imprinting hypothesis, which proposes a multi-modal navigation mechanism for natal homing in sea turtles and salmon. It hypothesises that sea turtles and salmon imprint on the unique magnetic signatures of their birthplace and use this to direct their ocean migration (Lohmann, Putman & Catherine, 2008). However, this hypothesis only aims to explain navigation to the general vicinity of their birthplace, and postulates that local cues are used to locate a more precise area. The unique magnetic signatures of coastlines refer to elements of the Earth’s magnetic field like inclination angle and field intensity, which vary predictably across the globe. Coastlines have different inclination angles and field intensities, which salmon and sea turtles could imprint on to (Lohmann, Putman & Catherine, 2008). The simplest version of this hypothesis is that only one element of the magnetic field is imprinted upon and used to locate a coastline. Of course, more complex strategies are possible, such as having both inclination angle and intensity as redundant markers. 

This hypothesis is plausible given sea turtles’ known ability to detect elements of the magnetic field. For example, it has been found that hatchling loggerhead turtles can detect magnetic inclination angles and field intensity (Lohmann & Lohmann, 1996). While it has not been proven to occur, it is a possibility that sea turtles use geomagnetic imprinting as a mechanism for natal homing. A complication is that some sea turtles’ nest on islands instead of coastlines, which requires more than just the geomagnetic field as islands are much smaller targets (Endres et al., 2016). This then indicates that magnetic navigation alone is not responsible for navigation. For salmon, the proposal that geomagnetic imprinting is used for ocean migration is in keeping with the use of olfactory cues as local cues once they reach freshwater. Furthermore, juvenile Chinook salmon (Oncorhynchus tshawytscha) have been shown to respond to magnetic fields, also using a combination of inclination angle and magnetic intensity (Putman et al., 2014). However, there is still much research to be done on their ability to detect magnetic parameters. 

Travelling hundreds of kilometres is no easy task, so why has natal homing evolved? This boils down to the very specific environments that are required for nesting and breeding, many of which are difficult for animals to assess. For example, sea turtles require a specific type of sand that allows nest construction, in addition to having a beach that has appropriate incubation temperatures and is relatively free of egg predators (Lohmann, Putman & Catherine, 2008). A natal coastline provides the assurance of these suitable conditions, while a nearby beach may not. For salmon, their spawning areas must be of a suitable temperature and depth, again, not something that can be assessed by swimming past the mouth of an unfamiliar river (Lohmann, Putman & Catherine, 2008).

Natal homing also influences population structure. If animals only breed at their natal region, there may be reduced gene flow between populations with different natal homes. For instance, isolated salmon populations that home in a specific river have evolved specialised adaptations to improve survival there (Hendry et al., 2000). Therefore, salmon that return to their natal homes may have more of an advantage than strays. However, straying from natal regions can also occur, and if successful, new habitats can be colonised. In salmon, it has been suggested that homing and straying exist in a dynamic equilibrium (Quinn, 1984). Where regions are suitable for spawning and are stable through time, precise homing may be selected for. However, if spawning sites vary in quality each year, natural selection may favour females that produce some offspring that home and some offspring that stray. 

Ultimately, there are multiple components that could explain natal homing, many of which are still enigmatic. Regardless, the arduous journey of returning to one’s birthplace is a truly fascinating process, and the mechanisms that underlie it are a testament to the powerful workings of evolution.

References:

Cooper, J. C., Scholz, A. T., Horrall, R. M., Hasler, A. D. & Madison, D. M. (1976) Experimental confirmation of the olfactory hypothesis with homing, artificially imprinted coho salmon (Oncorhynchus kisutch). Journal of the Fisheries Board of Canada. 33(4), 703-710. Available from: doi: 10.1139/f76-087

Dittman, A. & Quinn, T. (1996) Homing in Pacific salmon: mechanisms and ecological basis. Journal of Experimental Biology. 199, 83-91. Available from: https://jeb.biologists.org/content/199/1/83 [Accessed 26th February 2021] 

Dittman, A. H., Quinn, T. P. & Nevitt, G. A. (1996) Timing of imprinting to natural and artificial odors by coho salmon (Oncorhynchus kisutch). Canadian Journal of Fisheries and Aquatic Sciences. 53(2), 434-442. Available from: doi:10.1139/f95-185. 

Endres, C. S., Putman, N. F., Ernst, D. A., Kurth, J. A., Lohmann, C. M. F. & Lohmann, K. J. (2016) Multi-Modal Homing in Sea Turtles: Modeling Dual Use of Geomagnetic and Chemical Cues in Island-Finding. Frontiers in Behavioral Neuroscience. 10(19). Available from: doi:10.3389/fnbeh.2016.00019. 

Fleming, I. A. (1996) Reproductive strategies of Atlantic salmon: ecology and evolution. Reviews in Fish Biology and Fisheries. 6(4), 379-416. Available from: doi:10.1007/BF00164323. 

Hendry, A. P., Wenburg, J. K., Bentzen, P., Volk, E. C. & Quinn, T. P. (2000) Rapid Evolution of Reproductive Isolation in the Wild: Evidence from Introduced Salmon. Science. (5491), 516-518. Available from: doi:10.1126/science.290.5491.516. 

Jensen, A. L. & Duncan, R. N. (1971) Homing of transplanted coho salmon. The Progressive Fish-Culturist. 33(4), 216-218. Available from doi:10.1577/1548-8640(1971)33[216:HOTCS]2.0.CO;2. 

Lohmann, K. J. & Lohmann, C. M. F. (2019) There and back again: natal homing by magnetic navigation in sea turtles and salmon. Journal of Experimental Biology. 222. Available from: doi:10.1242/jeb.184077. 

Lohmann, K. J. & Lohmann, C. M. F. (1996) Detection of magnetic field intensity by sea turtles. Nature. 380(6569), 59-61. Available from: doi:10.1038/380059a0. 

Lohmann, K. J., Putman, N. F. & Catherine, M. F. L. (2008) Geomagnetic Imprinting: A Unifying Hypothesis of Long-Distance Natal Homing in Salmon and Sea Turtles. Proceedings of the National Academy of Sciences. 105(49), 19096-19101. Available from: doi:10.1073/pnas.0801859105. 

Putman, N. F., Scanlan, M. M., Billman, E. J., O’Neil, J. P., Couture, R. B., Quinn, T. P., Lohmann, K. J. & Noakes, D. L. G. (2014) An Inherited Magnetic Map Guides Ocean Navigation in Juvenile Pacific Salmon. Current Biology. 24(4), 446-450. Available from: doi:10.1016/j.cub.2014.01.017. 

Quinn, T. P. (1984) Homing and straying in Pacific salmon. In: Anonymous Mechanisms of migration in fishes. [e-book], Springer. pp. 357-362. 

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