How do temperature and global warming affect the sex of reptiles?

In most animals the sex of an individual is determined at the moment of fertilization; when the egg and the sperm fuse together it is fixed if that animal will be male or female. Yet in many reptilian groups sex determination is established later during incubation, and the determinant external factor is the incubation temperature of the eggs. In reptiles, this means that the environment plays a crucial role in determining the sex ratio emerging from an egg clutch, and that these animals are very susceptible to alterations in temperature caused, for example, by climate change.

SEXUAL DETERMINATION: GSD VS TSD

In the majority of animal species, sexual differentiation (the development of ovaries or testes) is determined genetically (GSD). In these cases, the sex of an individual is determined by a specific chromosome, gene or allele which will cause the differentiation to one sex or the other. In vertebrates there exists two main types of GSD, the XX/XY system in mammals (in which XX is a female and XY is a male) and the ZW/ZZ system in birds and some fishes (ZW corresponds to a female and ZZ to a male).

Examples of different types of genetic sexual determination systems found in vertebrates and invertebrates, by CFCF.

In the case of reptiles, there is a great variety of sexual determination mechanisms. Some present GSD models; many snakes follow the ZW/ZZ system and some lizards the XX/XY. Still, in many groups the sex of the offspring is determined mainly by the egg incubation temperature (TSD), and therefore the environment plays an important role in the proportion of males and females found in a population.

The eastern bearded dragon (Pogona barbata) is an example of a reptile with GSD, but which is also affected by incubation temperature. Photo by Trent Townsend.

Nevertheless, the genetic and temperature sexual determination are not mutually exclusive. Reptiles with TSD have a genetic base for the ovarian and testicular differentiation which is regulated by temperature. Similarly, it’s been observed that in reptiles with DSG, such as the eastern bearded dragon (Pogona barbata), high temperatures during incubation causes genetically male individuals (ZZ chromosomes) to develop functionally as females. This proves that in reptiles, there is no strict division between GSD and TSD.

TEMPERATURE AND SEX

The incubation period during which the sex of an individual is determined is called thermosensitive period and usually corresponds to the second third of the incubation period, during which temperature must be maintained constant. This critical incubation period usually lasts between 7 and 15 days, depending on the species. After this period the sex of an individual usually cannot be reversed (all or nothing mechanism).

Komodo dragon baby (Varanus komodoensis) hatching. Photo by Frank Peters.

Temperature during the critical incubation period affects the functioning of the aromatase, a hormone which converts androgens (masculinizing hormones) to estrogens (feminizing hormones). At male-producing temperatures, the activity of the aromatase is inhibited, while at female-producing temperatures the activity of the aromatase is maintained.

Graphics of the aromatase’s activity related to gonadal hormones on European pond turtle’s embryos (Emys orbicularis) at 25oC (males) and at 30oC (females), during the critical incubation period, from Pieau et al. 1999.

The TSD is found in all reptile groups except snakes (which have the ZW/ZZ system). In lizards and turtles we can find both genetic-based and temperature-based sexual determination, while in tuataras and crocodilians sex is determined exclusively by temperature. Currently, different patterns of temperature sex determination are known.

PATTERN I

This pattern is the simplest one, in which higher incubation temperatures produce one sex and lower incubation temperatures produce the other sex. Intermediate temperatures usually produce individuals of both sexes and very rarely, intersex individuals. This pattern can be further divided in:

• Pattern Ia TSD, in which eggs incubated at warmer temperatures produce high female percentages and eggs incubated at cooler temperatures produce high male percentages. This pattern is found in many species of turtles.

Photo of a European pond turtle (Emys orbicularis), species that follows the pattern Ia TSD; at 25oC or less during incubation only males are born, while at 30oC or more only females are born. Photo by Francesco Canu.

• Pattern Ib TSD, in which the contrary occurs; high temperatures produce males and low temperatures produce females. We find this pattern in some lizards with TSD and in the tuataras.

The tuatara (Sphenodon punctatus) is one of the reptiles that follows the pattern Ib TSD; the pivotal temperature is between 21-22oC, above which males will be born and below which females will be born.

PATTERN II

This pattern is a bit more complex than the previous one. In this one, embryos incubated at extreme temperatures (very high or very low) will differentiate to one sex, while the ones incubated at intermediate temperatures will differentiate to the other sex.

Photo of different aged American alligators (Alligator mississippiensis). These reptiles follow the pattern II TSD; at about 34oC males are born, and at higher and lower temperatures, females are born.

This pattern appears in crocodilians, some turtles and in many lizards. Recent phylogenetic studies indicate that this is the ancestral TSD model in reptiles. Some people even argue that all the TSD cases belong to the pattern II, but that in nature temperatures never reach both extremes, although this is yet to be proved.

TEMPERATURE DETERMINED SEX: PROS AND CONS

Even today the evolutionary advantages of the sex determination by temperature are not fully understood. The case of the reptiles is pretty curious because birds, mammals and amphibians determine their sex genetically in most cases, while in reptiles there is a bit of everything.

Currently, there are studies which are being conducted to see if certain temperatures improve the health of males and if other temperatures the health of females. In one of these studies, it was observed that snapping turtles incubated at intermediate temperatures (which produced both males and females) were more active than the ones incubated at temperatures producing only one sex, making them more vulnerable to be attacked by sight-based predators. Currently, there isn’t enough evidence that indicates to what extent these discoveries could be applied. It is possible that reptiles with TSD are able to manipulate the sex of its offspring, altering the proportion of sexual hormones based on the temperature of their nesting site.

Common snapping turtle (Chelydra serpentina) an American fresh-water chelonian, laying its eggs. Photo by Moondigger.

The disadvantages of the TSD are much easier to predict.  Any change in the environmental temperature of the nesting areas may affect negatively the populations of a determined species. If a previously shadowy forest is cut down or buildings are constructed in a previously sunny place, the microclimates of the egg clutches of any reptile nesting there will be changed.

Global change, or climate change, represents an additional threat to reptilians with TSD. The rise of the average temperature on the planet and the temperature fluctuation from one year to another, affect the number of males and females that are born in some species of reptiles. This phenomenon has been observed, for example, in painted turtles (Chrysemys picta), in which it has been predicted that a rise of 4^oC in their habitat’s temperature could cause the extinction of the species, because only females would be born.

Baby of a painted turtle (Chrysemys picta), species in which incubation temperatures between 23-27oC produce males, and temperatures above and below it produce females (pattern II). Foto de Cava Zachary.

REFERENCES

During the elaboration of this entry the following sources have been used:

• Cover photo: Animalspot.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://www.scientificamerican.com/article/experts-temperature-sex-determination-reptiles/
• http://www.ncbi.nlm.nih.gov/books/NBK9989/
• http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2603247/
• https://embryo.asu.edu/pages/temperature-dependent-sex-determination-reptiles
• http://onlinelibrary.wiley.com/doi/10.1002/jez.465/abstract
• http://link.springer.com/article/10.1007/s000180050342#page-2
• http://www.nbcnews.com/science/weird-science/hotter-temperatures-trigger-sex-change-australian-lizards-n385241
• http://www.herpconbio.org/Volume_5/Issue_2/Nelson_etal_2010.pdf

How can we save marine turtles from longline fishing?

This week, in this article we discuss how can we save marine turtles from longline fishing, since many species of marine turtles are endangered due to accidental captures. 

INTRODUCTION

Loggerhead sea turtle (Caretta caretta) and leatherback sea turtle (Dermochelys coriacea) are the marine turtles most captured with superficial longline fishing (Gilman et al. 2006), but are also captured the other species (Polovina et al. 2003).  Despite accidental captures of this species are strange, the worldwide whole has an important effect (Lewison et al. 2004). Here, we are focusing in the measure to reduce these accidental captures in the loggerhead sea turtle for the huge available bibliography.

Loggerhead sea turtle (Caretta caretta) (Picture from DeviantArt).

THE LONGLINE FISHING

Longline fishing is a type of fishing that consists on a main line from which puts up hooks with bait. It’s one of the most ancient fishing systems that are known. The main line can measure between some hundreds of meters to 50-60 km, with a distance between hooks from 1 meter to 50 m. Despite of being considered the most selection fishing, because depending on the bait and the hook size it is possible to catch one type of fish or another, it is not free from accidental captures, among which we can find sea birds and marine turtles.

Longline fishing, despite of being very selection, captures marine turtles (Picture from Sea Turtle Conservancy).

HOW CAN WE SAVE MARINE TURTLES FROM LONGLINE FISHING?

Reduction of the fishing time

If fishers reduced the time in which the longline is in the water, it would be reduced the accidental captures of loggerhead sea turtle, but this doesn’t happen with leatherback sea turtle (Watson et al. 2005). The problem is that is not economically possible for the reduction in the goal species captures.

Change of the hook

Changes in the hooks are the most effective. Wider hooks reduce turtle’s captures and the proportion of the animals that swallows the hook without compromising the commercial viability the swordfish in the North Atlantic (Gilman et al. 2006), but these doesn’t happen in other fisheries. The shape determines the place where the hook gets hooked: while circular hooks gets hooked in the mandible or in the mouth, J hooks gets hooked internally. The change to a circular hook reduces the captures and the mortality after the freeing (post-release death) in the loggerhead sea turtle because they usually are captured with they bite the bait and this get hooked more externally and it is easier to free them (Gilman et al. 2006; Bolten & Bjorndal 2005; Watson et al. 2003). The change in the shape is effective in certain fisheries and areas, like for example in the swordfish (maintaining the captures (Piovano et al. 2009)) an the blue shark in Azores (Bolten & Bjorndal 2005). For this reason, circular hooks don’t reduce the captures of goal species and suppose a low-cost investment, but complicate their removal and they usually are more breakable than J hooks (Gilman et al. 2006). In conclusion, the use of circular hooks in the swordfish fishery in the Mediterranean and the Northwest Atlantic can suppose an easy and cheap technique to reduce marine turtle captures (Piovano et al. 2009; Watson et al. 2005; Gilman et al. 2006, 2007). The direct mortality produced for the hooks is reduced, so the 80% of the freed turtles are alive, but the post-release death depends on the position of the hook (Camiñas & Valeiras, 2001).

Hook types. (A) Circular hook and (B) J hook(Picture from Cicmar).

Change of the bait 

Bait is another important factor. When the bait is fish, the captures of loggerhead turtles are reduced compared to the use of squid, and the captures of swordfish become bigger (Watson et al. 2005). The reason is that they feed on fish doing small bites and this prevent from being swallowed, while squid is more resistant and they swallow the bait completely (Watson et al. 2003, 2004). In the Mediterranean and Northwest Atlantic, using mackerel maintains the swordfish’s captures and reduces the captures of loggerhead sea turtles (Alessandro & Antonello 2010; Watson et al. 2005; Gilman et al. 2006, 2007), but reduces the captures of the Atlantic bluefin tuna (Rueda et al. 2006; Rueda & Sagaraminaga 2008). Using baits with different colours don’t seem to be a good measure because don’t prevent from capturing them (Swimmer et al. 2005; Watson et al. 2002).

Change of the depth of fishing and the distance to the coast 

Loggerhead sea turtles usually dive over the 40 m deep, maximum until 100 m (Polovina et al. 2003). For this reason, if the longline was placed under the depth of more abundance, the captures would be reduced (Rueda & Sagarminaga 2008). The problem is that the goal species captures would be reduced too depending on the fishery (Gilman et al. 2006) and, moreover, if they got hooked, they wouldn’t be able to breath in the surface and they would die. According to fishers, the hooks closer to the buoys capture more turtles because they are in swallower depths (Watson et al. 2002). So, these secondary lines should be longer. The turtle captures also depend on the distance to the coast (Báez et al. 2007), and the longline should be place further than 35 nautical miles and the captures of swordfish captures don’t be affected (Alessandro & Antonello 2010).

Elimination of light sticks 

Light sticks should be banned because increase their capture (Alessandro & Antonello 2010).

Change of the fishing areas 

Marine turtles gather in areas, so one capture increases a lot the probability of capturing more. For this reason, a good measure should be the communication between ships and the shift in the areas (100 km away) during a period of time (for example, one week) (Gilman et al. 2007). This would be very effective, but suppose an extra gas expense and the reduction of the time that fishers are fishing due to the journeys. Another measure could be the permanent or seasonal closure of areas, but this is economically infeasible.

Sea temperature monitoring

The capture rate of loggerhead sea turtles increases when the temperature is over 22ºC, while the capture of swordfish increases under 20ºC. For this reason, it should be better to fish in waters under 20ºC (Watson et al. 2005). However, in this case the fishing pressure on the swordfish should be controlled.

Fisher observers 

A good manage tool is the presence of observers on board a ship, like in the longline swordfish fleet in Hawaii (Gilman et al. 2007). Fisher observers record the number of fishing devices, the fishing days, the fishing position and the number of captured turtles (Álvarez de Quevedo et al. 2010).

A good manage tool is the presence of observers on board a ship (Picture from Journal of Applied Ecology).

HOW DO TURTLES HAVE TO BE FREED?

Turtles have to be freed using the right device to remove the hook and, in the case that it is not possible, the line has to be cut as closer to the hook as possible because this reduces the mortality because the line can affect the intestines (Casale et al. 2007).

To free the turtles, the line has to be cut as closer to the hook as possible (Picture from Greenpeace).

CONCLUSION

The effectiveness and the commercial viability of the strategies to avoid the capture of loggerhead turtles depend on the fishery, the size of the animal, the goal species and other differences between fleets (Gilman et al. 2006, 2007). The combination of circular hooks and fish like a bait is very effective in reducing the captures of turtles without affecting the goal species. This changes, together with tools to remove the hooks and the lines, reduce the accidental captures and the post-release deaths.

REFERENCES

• Alessandro L,  Antonello S (2010) An overview of loggerhead sea turtle (Caretta caretta) bycatch and technical mitigation measures in Mediterranean Sea. Rev. Fish Biol. Fisheries 20: 141-161
• Álvarez de Quevedo I, Cardona L, De Haro A, Pubill E, Aguilar A (2010) Sources of bycatch of loggerhead sea turtles in the western Mediterranean other than drifting longlines. ICES Journal of Marine Science, 67: 000-000
• Báez JC, Real R, García-Soto C, De la Serna JM, Macías D, Camiñas JA (2007) Loggerhead sea turtle bycatch depends on distance to the coast, independent of fishing effort: implications for conservation and fisheries management. Mar Ecol Prog Ser 338:249–256
• Bolten A, Bjorndal K (2005) Experiment to evaluate gear modification on rates of sea turtle bycatch in the swordfish longline fishery in the Azores – Phase 4. Final Project Report submitted to the National Marine Fisheries Service. Archie Carr Center for Sea Turtle Research, University of Florida, Gainesville, Florida, USA.
• Camiñas JA, Valeiras J (2001) Marine turtles, mammals and sea birds captured incidentally by the Spanish surface longline fisheries in the Mediterranean Sea. Rapp Comm Int Mer Medit 36:248
• Casale P, Freggi D, Rocco M (2007) Mortality induced by drifting longline hooks and branchlines in loggerhead sea turtles, estimated through observation in captivity. Aquatic Conserv: Mar Freshw Ecosyst doi: 10.1002/acq. 894
• Gilman E, Kobayashi D, Swenarton T, Brothers N, Dalzell P, Kinan-Kelly I (2007) Reducing sea turtle interactions in the Hawaii-based longline swordfish fishery. Biol Cons 139:19–28
• Gilman E, Zollet E, Beverly S, Nakano H, Davis K, Shiode D, Dalzell P, Kinan I (2006) Reducing sea turtle bycatch in pelagic longline fisheries. Fish Fish 7:2–23
• Lewison RL, Freeman SA, Crowder LB (2004) Quantifying the effects of fisheries on threatened species: the impact of pelagic longlines on loggerhead and leatherback sea turtles. Ecol Lett 7(3):221–231
• Piovano S, Swimmer Y, Giacoma C (2009) Are circle hooks effective in reducing incidental captures of loggerhead sea turtles in a Mediterranean longline fishery? Aquatic conservation: marine and freshwater ecosystems. Published online in Wiley InterScience
• Polovina JJ, Howell EA, Parker DM, Balazs GH (2003) Dive depth distribution of loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea) turtles in the central North Pacific: Might deep longline sets catch fewer turtles? Fish Bull (Wash DC) 101:189–193
• Rueda L, Sagarminaga R (2008) Reducing bycatch of loggerhead sea turtles in the southwest Mediterranean via collaborative research with fishermen. Poster presented to the 28th international sea turtle symposium Loreto, Baja California Sur, Mexico, 19–26 January 2008
• Rueda L, Sagarminaga RJ, Báez JC, Camiñas JA, Eckert SA, Boggs C (2006) Testing mackerel bait as a possible bycatch mitigation measure for the Spanish Mediterranean swordfish longlining fleet. In: Frick M, Panagopoulou A, Rees A, Williams K (eds) Book of abstracts of the 26th annual symposium on sea turtle biology and conservation. Island of Crete, Greece, 3–8 April 2006
• Swimmer Y, Arauz R, Higgins B, McNaughton L, McCracken M, Ballestero J, Brill R (2005) Food color and marine turtle feeding behaviour: Can blue bait reduce turtle bycatch in commercial fisheries? Mar Ecol Prog Ser 295: 273–278
• Watson J, Foster D, Epperly S, Shah A (2002) Experiments in the Western Atlantic Northeast Distant Waters to Evaluate Sea Turtle Mitigation Measures in the Pelagic Longline Fishery. Report on Experiments Conducted in 2001. US National Marine Fisheries Service, Pascagoula, MS, USA
• Watson JW, Epperly SP, Shah AK, Foster DG (2005) Fishing methods to reduce sea turtle mortality associated with pelagic longlines. Can J Fish Aquat Sci 62:965–981
• Watson JW, Foster DG, Epperly S, Shah A (2004) Experiments in the western Atlantic Northeast Distant Waters to evaluate sea turtle mitigation measures in the pelagic longline fishery. Report on experiments conducted in 2001, pp 135
• Watson JW, Hataway BD, Bergmann CE (2003) Effect of hook size on ingestion of hooks by loggerhead sea turtles. Report of NOAA National Maritime Fisheries Service, Pascagoula, MS, USA

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