As we are approaching the peak of the mating season in the Mediterranean we will review here an interesting aspect of sea turtle breeding, which is multiple paternity.
It is well known that multiple paternity (or polyandry) that is, the fact that females will mate with more than one male during the mating season, occurs with high frequency among sea turtle populations globally. The females will store sperm from different males and then use it to fertilise the several clutches of eggs which will lay later on, in the nesting season. The result is that hatchlings coming from the same nest will have of course the same mother but can have different fathers! A 2003-2004 study by Zbinden et al., the authors using genetic techniques, estimated that 93% of all the nests that are laid on Zakynthos island, Greece, have contributions from more than one male, with some of them from at least five! This means that the vast majority of the female loggerheads of Zakynthos will mate with more than one male. In fact, a recent careful global review of this phenomenon by Lee et al. showed that this percentage in Zakynthos, was among the highest (if not the highest) in the world! In fact this percentage is very similar to two of the largest sea turtle rookeries in the world: Tortuguero in Costa Rica, with around 60000 green turtles nesting annually) and the impressive arribada in Ostional beach, also Costa Rica, with 125000 olive ridley turtles nesting there. In these both sites multiple paternity was estimated to occur in 92% of the clutches.
But why would the females do that? And why is that phenomenon so common in Zakynthos? One possibility would be to ensure maximum reproductive output. As the fellow blogger Jacques-Olivier Laloë put it (in a previously written very similar blog post) “…having more than one mate can decrease the chance of having one “bad” (for example infertile) mate while increasing the chance of having at least one “good” (for example exceptionally fit) mate“. However, this was not confirmed in the study by Zbinden et al., as the hatching success of clutches was not significantly affected by the number of males that had contributed to them. Thus, the simplest explanation is that multiple paternity occurs as a result of increased chance of encounters between females and males. It is expected that the larger the population then the larger this chance is, something that explains this 92% in Tortuguero and Ostional. However, this by itself does not explain satisfactorily the 93% of Zakynthos, a site where the number of females is of the order of 400. What Lee et al. showed, was that, what also plays a significant role is the movement of females during the breeding season which can result in some cases in high density aggregations. Hence, when the population size was correctly scaled with the size of the area where the females disperse during the breeding season, it turned out that it could very well predict the multiple paternity percentage! In Zakynthos, it is well known that females aggregate in the shallows of Laganas Bay during breeding season, see the studies by Schofield et. al, here and here, resulting in dense aggregations in which encounters with males can become very frequent. It is characteristic that in the second study, the authors managed with the help of drones to detect up to 242 females in an area of length of couple of kilometers and width around 400 metres, and up to 89 incidents of mating in a single day.
It is thought however that females are in control of mating, i.e., they can use a variety of strategies to avoid males who want to mate with them (even though in some cases, males manage to violently mount females, see for instance this impressive video). These actions to avoid mating though, are energy consuming and it is sometimes preferable for the female to accept the male. As the authors of Lee et. al put it: “…female sea turtles simply “give in” to unwanted mating attempts”. If they resist, more males will come soon, resulting in more avoidance behaviour that will result in higher energetic cost. Thus it is better for them to accept the male and obtain peace of mind for a few hours.
Sea turtle mating dynamics are not as well studied as other areas of sea turtle biology due to logistic constraints. However, we see that the advance of new technologies, e.g. genetics and drones, has been able to provide exciting insights.
This is a blog post I wanted to write for some time now but the more I was thinking about it, the more difficult it seemed. This has to do with the term “non” in the title which means that it is difficult, if not impossible, to derive a universal guide/set of rules, about how people should behave or what to expect during in-water turtle observation. As we will stress many times in the following, each turtle is unique and should be treated separately. Guidelines of the type “one should stay at most X minutes with a turtle, keeping a minimum distance of Y metres” are difficult to be applied to all turtles. For instance, X minutes and Y metres might already be too long and too close for some individuals, or irrelevant for some others. Nevertheless, 8 years of underwater observations and almost 1000 sea turtle encounters allow me to say a few things, that have more to do with what should someone expect when she/he swims with turtles.
Let me stress that what follows has to do only with the loggerhead sea turtles encountered inside Laganas Bay, in the island of Zakynthos, Greece. Already in such a restricted geographical area, there is a great variability in the behaviour among individuals, that I would never dare to say that these (non)-guidelines apply to other areas in the world where also other sea turtle species can be observed underwater.
So this post has following the general purposes:
To give an idea on what kind of sea turtle behaviours can somebody observe, something that will help on
keeping a low degree of disturbance to the animal, and
having a greater and more thorough experience from the observer’s part.
To serve as a personal reference for me, when people are asking about this matter.
Is it ok to swim with turtles?
Let us start with this basic question, even though with so many encounters in my pocket I am not the most objective person to answer this. In principle, philosophically speaking, I think there is nothing wrong with two different species meeting randomly. One should keep in mind, that during their lives, sea turtles have probably met with far more dangerous animals than a creature who can barely keep its breath for more than a minute and is a very slow swimmer. In fact, turtle-turtle encounters many times have far more impact than turtle-human encounters, and sometimes, one can see specific individuals be more cautious when another turtle approaches rather than a human.
In order to better answer that question pragmatically, one should examine two things: (i) what is the impact, if there is any, to specific individuals, and (ii) if there is any impact, is the population endangered enough, such that this impact will affect significantly their numbers somehow. For the second point, recently IUCN classified the Mediterranean loggerheads as least concern, which is the lowest category possible. Even though terms like under extinction, or rare species are no longer representative for characterising the species, the term conservation-dependent was suggested as more appropriate, and hence the existence of any potential impact between turtles and humans should be still investigated (first point above). I will argue that in Zakynthos, for the majority of the individuals if there is any impact this is minimal. We note that we are not referring here to the boat-based turtle spotting industry that exists in Zakynthos (for that see this study) but we are restricting ourselves to underwater observations, e.g., snorkelling.
What kind of turtles can somebody see in Zakynthos?
Zakynthos is one the main reproductive sites for the Mediterranean loggerhead sea turtles. However apart from the regular reproductive migratory population, Zakynthos hosts a number of resident individuals that live and forage on the island all year around. In particular we have the following categories:
Actively reproducing migratory males. Seen any time between February and June, see here, here and here, as well as references therein.
Actively reproducing migratory females. Seen any time between March and beginning of September, see same references as above as well as here.
Actively reproducing non-migratory (residents) males. Seen all year around (see here as well as personal observations).
Immature turtles (juveniles) of unknown sex, residents and (?) migratory. Seen all year around (personal observations).
Interestingly a small number of juvenile green sea turtles have also been spotted over the years (see here for example). But if one sees one, he/she should consider him/herself extremely lucky for these few seconds before it disappears instantly in full speed! Notably, no resident actively reproducing females have been observed so far on the island.
As far as behaviour is concern and response to human presence there are differences not only between the 4 above categories but also within them. Let us briefly describe first what sea turtles do normally.
During the mating season (March-June), actively reproducing males, migratory and residents, are looking constantly for females to mate, swimming most of the time. The typically get involved in interactions, aggressive or not, with other males and females.
Resident males, after the end of the mating season, will typically start foraging.
Actively reproducing migratory females,during mating season they can be seen mating/interacting with males, basking/resting in warm waters, actively swimming towards warm patches of water, as well as interacting with other females aggressively or not, presumably competing for optimal resting places. After mating season and as the water temperature rises, they become more lethargic and they spend a great amount of time resting on the seabed, generally avoiding aggressive interactions with other individuals. Some females also invest on cleaning behaviour, see for instance our latest paper. Most of the females will leave the island by the middle of August.
Juvenile turtles spend most of their time foraging. We know very few about their movements but some of them do exhibit long term residency (personal observations).
A relevant fact that we are going to refer to later on, is that, for nesting females, water temperature seems to be crucial for their levels of activity: turtles are more active during mating season/beginning of nesting season and their activity is decreased after end of June when water temperature has increased considerably. This has been confirmed with the use of accelerometers but it is also very easily noticeable by direct observations. The following paragraph from the above linked paper puts it nicely:
“Activity levels were not constant throughout the season, being impacted by both ambient water temperature and female reproductive status. In cold water at the beginning of the nesting season, high levels of activity suggested that females behaviourally thermoregulated by seeking out warm water patches along the shoreline. Interactions with male turtles (courtship and/or avoidance) may also explain this high level of activity. As sea temperatures warmed up and the amount of energy devoted to reproduction probably increased, the turtles spent more time resting during long sequential flat-bottomed dives, and reduced any unnecessary locomotory activity.” [Source: Fossette, Schofield, Lilley, Gleiss, Hays: Acceleration data reveal the energy management of a marine ectotherm during reproduction, Functional Ecology 2012]
We should also note here that actively reproducing female turtles seem to possess a natural stress-reduction mechanism during their reproductive period that helps towards a maximal reproductive output. This seems to help mitigating the effects that stressing factors might have in the reproduction process, like interaction with other turtles, shark attacks (in Australia), or in our case interaction with other species. Tim Jessop has worked a lot in that area, see some relevant papers of his, here and here (also in Biology of Sea Turtles volume 1, Section 188.8.131.52)
Summarising, here are a few resources regarding in-water loggerhead behaviour (by direct observations) in Zakynthos (some links are the same as above):
After summarising the general in-water behaviour of Zakynthos loggerheads, we will now focus on their behaviour upon meeting with humans underwater.
How do turtles react to the presence of humans underwater?
We are now coming to core of this article. This is a subject that so far has not been studied systematically and in depth (even though this relevant study about Hawksbill turtles in Honduras exists), so what follows is mostly a result of personal observations. Again, I cannot stress enough the variability that characterises this issue.
Category 1: Great degree of disturbance, typically characterised by immediate abandonment of the site in high swimming speeds.
Category 2: Moderate disturbance, characterised by abandonment of activities (e.g., foraging, resting), accelerating when being approached, performing sharp turning movements.
Category 3: Slight disturbance. Here no significant signs of disturbance are shown, but the behaviour cannot be yet classified in the next category. The turtle does calm but avoiding movements when the person approaches too close.
Category 4: No disturbance. The turtle shows no disturbance signs, almost indifference to the human presence. Examples include, foraging or resting, with these activities not being interrupted even when the person approaches really close (in the scale of centimetres!).
For a more detail description see this video, that accompanied the symposium presentation. We will analyse a bit more in depth the two extreme categories, 1 & 4:
Video showing turtles that exhibit great degree of disturbance (Category 1):
You notice in the video above that the second turtle was actually surprised and got scared away. When someone encounters a foraging turtle, it is generally a good idea not to approach it from behind, but to let the turtle see him/her first. This is one of the few rules we can say here: Turtles do not like surprises! Turtles as small as the third one in the video seem to swim away immediately. Some green turtles that have been sighted in the bay, and have similar size, have also shown analogous behaviour.
There is no reason to try and give guidelines for this kind of behaviour. A turtle in full speed will disappear out of someone’s sight in seconds and it is pointless to try to follow it. Note that this behaviour can be pretty much exhibited by all type of turtles, male, females, juveniles while performing any kind of activities. There seem to be some exceptions. A mating pair is too bulky for the female to swim away in full speed (not too much experiences with mating pairs though). Foraging turtles will also rarely swim away like that, especially those that forage for molluscs in the sand. Actually the foraging turtle in the video was just surprised and on subsequent, more careful approaches, exhibited more like a category 3 behaviour. Thus it can also happen, but not so often, that a turtle exhibits different types of behaviours during the same encounter. Nesting female turtles can exhibit this behaviour at any time, but it is less likely to do so, as the water temperature rises as we discussed above. In fact, seen a turtle in July-August exhibiting this kind of behaviour, with no apparent signs that she is a nesting female (e.g. external tags placed by Archelon), should put you into thoughts that she might not be reproductively active at that moment, or that it is a juvenile. Males during mating season are also possible to react like that, but they can also have a more passive reaction, sometimes even being aggressive (personal communication with Gail Schofield).
Summarising, Category 1 turtles might likely be:
Females during mating/beginning of mating season when water temperature is low
Males during mating season
Very small turtles
Possibly turtles that have never or rarely seen a human before (difficult to verify)
As we have stressed many times, no strict rules apply anywhere here and in principle any type of turtle might exhibit this behaviour.
Video showing turtles that exhibit no disturbance (Category 4):
I never cease to be surprised by turtles that exhibit this category’s behaviours. Sometimes, it is remarkable how close you can approach an individual and it still acts like you are invisible! Again behaviours of this category can be observed in all types of turtles. However, even though the sample size is small, it occurs particularly often to foraging turtles (males, juveniles), especially those who are foraging for molluscs in the sand.
As we also mentioned previously, the behaviour of nesting females after the middle of the nesting season can be also quite often classified as Category 4, especially when they are resting on the sea floor. Even when they have their eyes wide open (as we saw at the beginning of the first video), someone can approach really close with no reaction. Sometimes, turtles (females or not) will even rest in the presence of humans (swimming first and then resting), an act, which I consider a combination between non-significance disturbance and urge to rest in order to minimise energy that will eventually go into reproduction. The stress-reduction mechanism we discussed earlier might also play a role on that.
More rarely, some turtles will exhibit Category 4 behaviour, even when they are just swimming. In that case, even when you go directly in front of them, they will just stop for a while, look at you and swim slowly overpassing you. A very representative example is Hercules, a male loggerhead, one of the most “relaxed” turtles around.
Having discussed more in depth Categories 1 & 2, we must note that on average, during the nesting season, nesting females are more likely to exhibit a Category 2 or 3 behaviour, probably trying to achieve an optimal balance between saving energy and avoiding any interactions with other individuals (humans or conspecifics). In the aforementioned study presented in Turkey, I classified all the encounters that I had during 2014 (n=64):
Category 1 (great degree of disturbance): 24% of all encounters (n=15)
Category 2 (moderate disturbance): 42% of all encounters (n=27)
Category 3 (slight disturbance): 20% of all encounters (n=13)
Category 4 (no disturbance): 14% of all encounters (n=9)
The fact that when considering only nesting females, 72% of them classified as Category 2, confirms what was mentioned in the previous paragraph. Interestingly, in most cases same individuals exhibited behaviour of the same category over different encounters. In fact, if in the list above, we consider individuals instead of encounters, the percentages will not change too much (but that should be seen as a coincidence at it depends how many times a specific individual was encountered). However, this fact brings us to the next point.
The “personality” factor
By this we mean the consistent exhibition of the same type of behaviour of a specific individual, not only within the same season but over different years as well. We will dare to call that personality of the turtle even though zoologists and biologists are very cautious to use this term. This observation is particularly notable in the long term resident turtles for some of which I have underwater behavioural data for up to 7 years now. For example, some turtles are consistently foraging in almost every single encounter over different years, exhibiting similar responses upon approach (from indifference till high disturbance signs). Others, seem to be more reluctant to the human presence over the years (which supports the thought that new recruits are more easily scared) and others despite being long term residents exhibit behaviour which is more like 1 or 2. There are also a few examples of nesting females seen year after year (mostly after 2 or 3) that still exhibit similar behaviours and responses. So someone should always remember the following non-scientific statement (but nevertheless true):
Independently of time of the year, water temperature, type of turtle and reproductive status, every individual has its own distinct personality which, in addition to the factors above, also drives its behaviour and response to human presence.
To put that into context, it has been very useful for me to know the personalities of a number of turtles in Laganas Bay and adjust my own movements to achieve optimal observation and photo opportunities on one hand, and minimum disturbance, on the other. For instance, when somebody is observing Lucretia above, when she is focusing on foraging, she can be approached at a very closed distance, but when she stops chewing and lifts her head up, she can be very easily annoyed. At that point, I try and keep my distance.
Observation times vs different exhibited behaviours
In the study presented in Turkey, I also made the following graph that shows the time I spent in every turtle encounter also in relation to the 4 behaviour categories:
It is easily seen that the behavioural response of the turtle clearly affected my observation times. This results from the strategy approach as close and for as long as the turtle permits. In particular the average observation times where 1.5 minutes, 8.8 minutes, 16.7 minutes and 30.4 minutes for turtles that belonged to Categories 1, 2, 3 and 4 respectively. Notice the outlier of Category 2, with 41 minutes observation time. That was the well-known Bertha, followed from a certain distance.
Generalising a bit let us have a look at observation times for the last 8 years (2010-2017) without however classifying the encounters in different categories (that requires quite a bit of time and it is beyond the purposes of the current post)
A few words are in order for the graph above. First of all I was personally surprised that around 50% of my encounters lasted approximately one minute or less. These encounters certainly include turtles of Category 1 but also individuals I had little interest to stay with, for one reason or the other. Interestingly 81% of the encounters lasted 10 minutes and less. Certainly, when you are in the water it seems longer than that! Moreover, the majority of turtles that were observed more than a hour, were foraging turtles, with the longest observations 90 minutes, 83 minutes and 70 minutes being turtles foraging on molluscs (90 & 70 was the turtle named Eva, shown in the photograph above). It is clear that long observations for these type of turtles has minimal if not no effect at all. However, in order to have a more complete view and try and answer the initial question about the impact on the population, the following questions need to be answered:
Do other snorkelers follow a similar strategy regarding observation times?
How often and for how long, are specific individuals observed by humans in a given season, especially for nesting females?
Does underwater observation have an effect on the reproductive output of nesting females and in what extent?
For the first question, my feeling is that most snorkelers, in general would stay less than me with a turtle, but this is something that should be investigated.
For the second question, given that the majority of the bay is a snorkeler-free zone (a typical human will only stay in the shallows and tourists aggregate in specific spots), also together with the fact that nesting females move around a lot, I would say that the accumulative time they spent with a human is relatively low. However, this is also something that should be investigated in detail. The fact that females are actively swimming towards warm patches of water, is also relevant for their encounter with humans. In May and early June, the females tend to aggregate in the very swallow parts of the Bay (knee depth) where the water becomes warmer especially in the afternoon (personal communication with Gail Schofield). In these situations, they are more likely to be approached by people.
We should mention that low probability of an encounter with human, is probably not true for some residents that forage in a highly touristic area (Agios Sostis), but there, I would consider the real anthropogenic stressor to be the intense and largely uncontrolled presence of boats, turtle spotting or private hired ones, some of them exceeding by far the 6 knot speed limit, that by law exists in Laganas Bay. In fact, two of the residents seem to have recently suffered minor injuries caused by boat propellers. Illegal fishing and feeding also cause problems in that area. It is generally a good idea for snorkelers not to approach a group of such boats for everyone’s safety. So here’s another general advice: avoid the crowds.
Something that I have a few data on, is whether observation by a large group of people, lead the behavioural response to a lower category (e.g. from Category 3 when the turtle is observed by one snorkeler, to Category 2 when observed by a group). My initial feeling is that this is the case but it needs to be looked at more carefully.
For the third question, again we have no clues, however given the stress-reduction mechanisms it is more likely that a few minutes of daily underwater observation have no effect at all, rather than having one. Of course observation should be regarded here as a mild one, it goes without saying that for instance, grabbing/feeding turtles should be avoided.
We provided an overview of different sea turtle behaviours and responses to the presence of humans and how these are influenced by a variety of factors, such as sex, water temperature, reproductive status, performed activities at the time of the encounter etc. We stressed many times the variability that characterises these behaviours both within and among turtles of the same status (personality factor). We argued that given our current knowledge, there is little or no risk to the population linked to (mild) underwater encounters by humans.
So, get in the water, act sensibly and with respect, and live the magical experience of being underwater with a sea turtle.
Many thanks to Gail Schofield for having useful discussions and providing constructive comments on this post.
This is a short report on the annual 37th international sea turtle symposium (ISTS) that took place in Las Vegas, USA, 15-20 April 2017. I am writing this on the way back home, while waiting in Las Vegas, Los Angeles and Reykjavik airports.
Every year the ISTS provides an excellent opportunity for all sorts of people to meet up and discuss ongoing issues with regards to local and global aspects of sea turtle research and conservation. I will try here to convey my impressions and pinpoint specific subjects that I found very interesting.
Every year the symposium has a different theme and this year’s theme was climate change. Climate change is a hot topic in sea turtle research (both literally and metaphorically) for many reasons. Temperature has many effects on the different life stages of sea turtles and it is of utmost importance to see how they will react on the global temperature rise (as well as interesting from an academic point of view).
One main issue here is that all species of sea turtles exhibit what is called temperature dependent sex determination. Roughly, (and this roughly is a subject of current research) higher egg incubation temperatures produce female hatchlings and lower produce male ones. However, as James Spotila noted in his speech – also addressed in this paper here and here – the problem with high temperatures is not so much the feminisation of the populations rather than the increased hatchling mortality in the nests. In other worlds, as Spotila said:
“High temperatures: loads of dead female hatchlings”
Marc Girondot, an expert on the mechanisms under which sea turtle sex is determined gave a very interesting talk with title “Thermal reaction norm for sexualisation: the missing link between nest temperature and ratio”. He stressed that under variable incubation temperatures it is not true that the sex is determined in the middle third of the incubation duration (as at least I thought) but the issue is rather more complicated. Moreover, he stated that incubation duration is not indicative of sex ratios. That is, even though someone would think that high incubation durations (which could be resulted by lower temperatures) should produce more males, this is not necessarily true. Moreover, he said that when examining sex ratios in a specific population, one should not rely on important values e.g. pivotal temperatures (temperature that produces 50% males and 50% females) that have been derived in other populations but each population should be examined separately. In any case the subject is more complicated than what one might initially think (at least I am lacking the technical knowledge to fully understand it). Remember though that the more we are learning about a subject the more we realise that we have yet to learn!
But what about turtles that are already live on very hot areas? Nicolas Pilcher, gave a talk about the hawksbills in the Arabian gulf, where air temperatures can reach 50 degrees during the summer. He noted the existence of, maybe unexpected, high proportions of males to females in the population there. He explained that this is due to the fact the hawksbills there nest quite early in the summer season. That is, turtles there have adapted to the warm conditions. In fact colonisation of northern (southern for the south hemisphere) beaches is an adaptation which could help mitigate the effect of climate change. Maybe this has started already: this year there was a loggerhead nest in the south part of France, near Saint-Tropez, the northmost point that has been recorded for the species ever. Sandra Hochscheid also presented some nest time series from Italy that suggests that a colonisation might be happening there as well. Pilcher finally noted in his talk that
“Sea turtles have survived large scale climatic changes over millennia. The question is how fast they are able to do that…”
which is the main message that one should keep in mind here.
There were many presentations regarding the use of drones in sea turtle research and in fact one entire workshop was dedicated to that technology which has been recently introduced to the sea turtle community. Among their main applications are: sea turtle abundance estimates in the sea, behavioural studies, estimates of operational sex ratios during mating season as well as sex ratios in foraging grounds, beach monitoring and constructions of 3D beach maps. The insights that they provide are numerous and no doubt they can be of great use. My feeling is that even though their use might not be groundbreaking (at least not yet), things might change soon, especially if their flight time, currently very restricted, becomes much longer. Regarding, general use of video footage, its usefulness was also highlighted in a talk by Alexandra Gulick, student of Karen Bjorndal, who studied green turtle foraging behaviour using static cameras in the sea floor.
The use of drones and static cameras had also a main role in my presentation about the cleaning stations of Zakynthos island, Greece. The talk was titled “Detection and use of seasonally ephemeral fish-cleaning stations by breeding sea turtles using drones and undewater cameras” and it was a joint work with Gail Schofield, Rebecca Haughey and Kostas Katselidis. It was accompanied by a video presented in the symposium’s video night, which entertained the crowd quite a bit! I am going to come back soon with a blog post exclusively dedicated to that subject.
Genetics play now a main role in sea turtle research substituting or accompanying the traditional flipper tagging methods. Researchers are able to assign to every nest the genetic profile of the mother – the corresponding SWOT article. A very nice example is the research that it is being done with hawksbills in Jumby Bay on Long Island, Antigua in the West Indies. This was presented in a form of a poster by Kathryn Levasseur. Through genetic studies, people in that project were able to verify the presence of mother-daughter as well as sibling pairs in the same nesting beach. In combination with saturation tagging they were also able to determine in a very good accuracy the sexual maturation age for this specific population (around 15 years). In fact the same result was also confirmed by another study presented by Jamie Clark et al. using skeletochronology (google that word) another very powerful technique which is able to estimate the age of a turtle using growth layers/rings in their bones.
A very nice message was given by Selina Heppell in a talk titled “Great, we saved them! Now what?”. She stressed that conservation successes should be addressed and celebrated and in many cases we should “switch from an emergency conservation mode to a larger horizon, more holistic picture”. In fact this rhetoric is strongly supported by many scientists. Brendan Goldley gave a similar message in the final part of his plenary talk in the previous ISTS in Lima, Peru, 2015. I will also come back to that in a future blog.
Finally, the usual ISTS festivities were adapted to match the spirit of Las vegas…
…and it was also announced that the next symposium will take place next year in Kobe, Japan:
Many thanks to all people who worked towards the organisation of this very successful symposium! I am also grateful to the International Sea Turtle Society for providing a travel grant which allowed me to take part in it!
Conservationists and biologists have been always uncomfortable – if not categorically against – with the idea of humans feeding animals in the wild. Sometimes the reasons are obvious especially when human safety is compromised: you really don’t want to start feeding a polar bear, a lion or a great white shark. Beyond safety issues there can be other concerns of course, like the health of the animal itself (when it is fed food that is not used to) as well as changes in its habits and its behaviour. Of course, it all depends on the scale that this feeding take place. In this post we will focus on feeding wild sea turtles and in particular as this takes place around a very specific area in the greek island of Zakynthos, an area that I have been closely observing for the last years. Before we start, we should stress that feeding sea turtles is not illegal in Greece.
Agios Sostis is located on the west part of Laganas bay, Zakynthos, within the limits of the National Marine Park of Zakynthos. We are going to focus on 3 specific areas around Agios Sostis: A small port that local fishermen regularly use, a patch near the shore that a few of the all year-round resident loggerhead sea turtles naturally forage, and the marine area between these spots. This marine area is characterised by turtle spotting boat activities, especially during August and September. This is due to the fact that the area has relatively high density of resident loggerheads, who, in contrast to the actively reproductive females, do not migrate to any distant foraging grounds. See here for photos of some of the resident turtles of the area.
The little port is used daily from local fishermen, who after returning from the night’s fishing, they are typically cleaning off their nets, discarding any unwanted bycatch. A male loggerhead, named Sotiris, who has been possibly around for more than 15 years now, started to take advantage of this discard. Thus, an interesting relationship started between him and the local fishermen who sometimes just throw fish, crabs squid etc in the water or other times feed him directly in the mouth. It is clear that the scale of this feeding is very small. As far as this specific turtle itself is concerned, Sotiris has also been observed foraging naturally in several occasions.
As a conservationist, I always found it very hard to come up with arguments against that type of feeding. For me, it has always symbolised an alternative relationship, between turtles and fishermen, a relationship very often devastating for the animal as the interaction with the fishing industry has always been considered the number one anthropogenic threat for the sea turtles worldwide. One should never forget that many people, including fishermen, view marine life in a completely different way, than others who, for example, have grown up with David Attenborough documentaries. As we will also stress in a future blog post, understanding people’s relationship with animals is crucial for conservation. Not all people make the discrimination between not wild and wild animals (the ones that “shouldn’t be fed”). One does not have to look too far in order to see that other people can categorise animals differently: useful for humans, dangerous for humans, animals that do harm with one way or another, animals that are indifferent to humans.
Even though, it could have always been the case, the first time it came to my attention that more turtles are entering the port, seeking for food, was in 2011. In this video (3:42-7:44), another resident-to-be male loggerhead turtle, Agisilaos, makes one of his first appearances in the port. It is interesting how the french narrator of this particular documentary, also describes the story with great amounts of romanticism. Until today, Sotiris and Agisilaos are the two turtles that regularly occupy the port, with other resident turtles appearing from time to time. When two turtles meet at the port, a fight between them starts. Typically, one turtle is the attacker, the other being the offender, and the fight typically consists of head to tail circling and several attempted bites (we should note that the loggerheads have pretty good defensive skills against these bites).
These type of fights however do not occur only in the port but also in a nearby foraging ground. Only a few meters away from the part, there exists a patch of relatively small size where most turtles are observed foraging on a sponge from the phylum Porifera. Regular fighting is observed among turtles that have never been observed to be involved in a human feeding incident. In fact, one can identify specific individuals that occupy the patch more often than others and also being the most aggressive.
It is safe now to conclude, that loggerheads can exhibit some territorial behaviour, defending their foraging grounds, by attacking other turtles that are trying to be there as well. Moreover there are indications that the more spatially restricted the foraging place is, the more aggressive these interactions become. Even though, it is not easy to quantify, the interactions inside the port seem to be more aggressive and last longer than the ones in the natural foraging ground, where the food is more available and spread out. In fact in this one of a kind video, shot by Giannis Xenos, one can see a long term resident male loggerhead looking for molluscs, in a very wide sandbank area, while being followed closely by another resident. No aggressive interaction occurs between the two turtles whatsoever, possibly having to do with the fact that the food in this case is scarce and spread out. However, one should also not underestimate the personality factor, it is true that different turtles react differently in similar situations.
More research is required to see if this feeding can indeed result to increased antagonistic interactions and how this affects the welfare of the turtles, see also this interesting preliminary study from the nearby island of Kefalonia. Again, it all depends on the scale of the feeding. It seems to be the case that in Kefalonia this is more intensive and tourists are even encouraged to buy fish from the fishermen in order to feed the turtles themselves. Here the issue loses its romantic flavour and becomes more complicated.
Turtles being fed by or for tourists
Apart from Kefalonia, Zakynthos recently experienced a similar issue. Last summer, it became somehow a trend, to feed with tomatoes a specific turtle, right near the port and the foraging ground. This feeding was coming from both turtle spotting and private boats. Interestingly only one turtle seemed to be involved, Achilles, a young male loggerhead also a long term resident.
Having been observing Achilles for the last 5 years, I could say that his habits were a bit different this year. He was slightly more aggressive, mostly swimming around the area, and not spending as much time naturally foraging on sponges as the year before (he did not quit doing this however). It could be the case that this had something to do with this feeding in which he was continuously involved. The National Marine Park of Zakynthos and Archelon released a joint public statement about this issue (greek version, english version, article in a Zakynthian newspaper in greek).
Encouraging tourists to feed sea turtles is problematic. On one hand the scale of this activity increases a lot, more turtles can be involved also for a larger amount of time and as we have explained this can potentially have a negative impact on their welfare. On the other hand, it gives the wrong messages to the visitors of the island, about how to treat wildlife. I can understand that the word “wrong” here can be debated by people who see wildlife in a different way. However I would encourage the Zakynthians involved in sea turtle spotting to think what they would like to see in their island:
Sea turtle tours that look like visits to the zoo or a farm.
Sea turtle tours that promote nature in its pure and untouched form.
Even though, I don’t want to tell people what to do, I hope they go for the second option and encourage others to do the same.
We began as two sport divers with an interest in underwater photography. We weren’t marine biologists and had no background in conservation. We knew nothing about the Hawaiian green turtle, or honu as the Hawaiians call them.
Peter Bennett and Ursula Keuper-Bennett start their book with these phrases. Originally from Canada, Peter and Ursula had their first underwater experience with a sea turtle in 1998, on the reefs of Honokowai, in the Hawaiian island of Maui. They named her Clothahump. The Bennets kept returning back to Maui every year up until today (at least I hope-their last video in their youtube channel is from 2013). All these years, they have spent countless hours observing and documenting the local Hawaiian green sea turtle population in a dedicated and consistent way, that probably very few – if any – people had done before them. They summarised their accumulated knowledge in their book, The book of Honu: Enjoying and learning about Hawai’i’s sea turtles, published by the University of Hawai’i’ Press in 2008.
This book is a treasure. Really. They provide highly detailed information about the underwater life and habits of the Honus like no other before, scientist or not. Not any modern and fancy sea turtle behaviour study technique like GPS fine scale tracking, accelerometers, remotely operated vehicles, cameras attached to sea turtles, or even, the so popular these days, use of drones, can provide such a great insight into the daily routine of sea turtles that resulted from their dedication and enthusiasm for more than 2 decades. (the linked studies and videos however provide very useful insights of different nature and they are highly recommended!). It is not surprising that
We attended the 13th annual sea turtle symposium in Georgia. Once the turtle specialists heard that we’d been observing turtles underwater for years, they began asking us questions: How did we tell them apart, whether they got along together, if they had favorite spots, just what is it that they did all day long-the same sort of queries that everyone had.
The Bennetts give many answers (or at least insights) to questions of the above type in their book.
“Upon approach from humans, young turtles are caught up in a delicate dance between curiosity and caution”.
“Juvenile turtles seem to enjoy play. A dance of round-and-round where one would try to nip the tail of the other”.
“Male-male mounting turns out to be so common. Perhaps it is a dominance behaviour”.
“Some honu occupy exactly the same spot year after year. Some have 2 or 3 favorite places, while others are content to stay in the same small area”.
“They scratch the tops and bottoms of their shells, their throats, their heads”.
“We’ve concluded that the honu create their own cleaning stations”.
“They mostly do the same things we do at home: eat and sleep”.
“They don’t seem to have a pecking order. We have never seen one honu consistently dominating another. Even size is not a reliable predictor of which turtle will prevail in a confrontation. At times, we’ve seen the smaller honu chase off the larger”. I can personally confirm this last one.
The book is full of descriptions of the above style. Notice the absence of dry scientific language. In fact positive, turtle-huggy emotions are overflowing:
There is no better experience – no happier time – for us than resting with old friends on the ocean bottom.
But that should not discourage people, even highly qualified marine biologists, to read this book and take its content into serious account. Of course sea turtle behaviour of the above kind is hard to quantify and it is open to many explanations – even I disagree with a couple of their interpretations. But if I was writing a book about my own underwater sea turtle encounters, I hardly imagine I would use a much different tone.
One of the first questions that people ask after hearing about our turtle experience, is “How do you tell them apart?”
The Bennetts were among the first people (if not the first) who consistently used photo id techniques to distinguish individuals: their facial scales (scutes) are practically unique, like a human fingerprint. Until the end of 2004, they had logged more than 750 unique individuals. They gave names to turtles that were repeatedly observing and naturally they became attached to them. It is really enjoyable, to read their narrations about the lives of known turtles, how they first met, how they were reacting in their presence as well as with other turtles, and about their transition from being young juveniles to mature adults. This emotional attachment however sometimes came with a cost.
Seeing an afflicted turtle will probably disturb you. It certainly upsets us.
Fibropapillomatosis (FP) was firstly recorded in Florida, in 1938 and in Hawaii in 1958. It is a disease that gives the turtles nasty external and internal tumours that can be more than 10cm large in diameter. The tumours grow steadily, sometimes, blinding the turtle, while the tumours on the skin, neck and plastron, make swimming difficult. The cause and how FP spreads still remains a great mystery. Some healthy turtles have remained healthy even if they live close to infected ones. A herpesvirus seem to play a role in the disease, as well as poor quality of water, even though infected turtles have been found in clean waters. The Marine Turtle Specialist group consider FP as one of the key unsolved mysteries of sea turtle biology.
The Bennetts were unfortunate to see many of their friends dying from the disease, including Clothahump itself.
We saw her only once in 1993. The white spots had mushroomed into tumors. We both cried underwater. That day, we vowed to tell Clothahump’s story and somehow help the ocean community on her reef.
And so they did. Their long term observations of affected turtles led to a better understanding on how the disease appears, progresses and disappears. They discovered that the tumours start from the eyes, and in general one can tell the severity of an affected turtle, by assessing the eye tumours. They also discovered that it affected primary young turtles, and that most adult turtles recover within 3 or 4 years. They collaborated with George Balazs, an expert on Hawaiian sea turtles, and they published a series of scientific papers and reports, like this one and this one (page 37) (also available here). The Bennetts comforted their readers:
Our records and other studies show that FP isn’t nearly as deadly as was first feared. FP related deaths are not affecting the chances for survival of the whole population. It certainly kills some, but others live and grow to reproduce and replenish the population. There’s comfort in knowing that.
Nevertheless, for these two people that see turtles as individuals and not as part of a population, many sea turtle deaths were like losing a friend.
In a population level things are looking great till today indeed.
Peter and Ursula have contributed a lot in our knowledge of sea turtle biology with their observations. But they have inspired us even more with their passion…
The story of loggerhead sea turtle nesting area of Kyparissia bay is an interesting one. Several issues have been risen during the last years, both in a political and a conservation level. In this post, we will focus on the latter. Situated in the western part of Peloponnese, Greece, the whole bay has total length of 44 km with the majority of loggerhead nests (around 85%) concentrated in the south 9.5 km. The average nest number in this core area used to be, up a decade ago, around 550-600 nests (a bit more in the whole bay), see this paper. It was considered to be the second largest reproductive site for the species in the Mediterranean, after Laganas bay, Zakynthos, where typically double the amount of nests were laid each year. However, unlike Zakynthos, the Kyparissia nests were suffering from mammal predation (e.g. dogs, foxes) as well as severe flooding due to large waves. Hence intensive conservation efforts began in the early 90’s by Archelon, the Sea Turtle Protection Society of Greece, with the objective to reduce these effects. Metal grids were placed on top of nests to reduce predation and nests laid close to the sea were being relocated into a safer place. It goes without saying that this requires a tremendous effort every year, by dedicated young volunteers. The result: hatchling production was steadily increasing every year. Hence, 15 years after (around 2007) Kyparissia’s nests started increasing as well. Up to then, its nest numbers, as well as the ones of Zakynthos was pretty much stable. Given the fact that the minimum sexual maturation age for loggerheads is 14-15 years (check here the source), this increase, as expected, is naturally attributed to the increased hatchling production since the beginning of the 90’s. In fact Kyparissia’s nesting data itself could lead to a nice scientific paper regarding sexual maturation age and other general parameters of the demographics of the Mediterranean loggerheads.
And this increase continues till today. Last summer (2016), the 9.5 core sector had around 2650 nests, a truly unprecedented number. Projections elevate this number to more than 3000 nests for the whole bay. To compare with, the most nests that Zakynthos ever had was a bit more than 2000, in 1995. We should note here that 2016 was an exceptional year for the whole Mediterranean with record breaking nest numbers in many areas.
It is also worth noting that unless our assumptions on demographic parameters are wrong, this current increase has not hit yet its exponential phase. This is because the turtles that nest for the first time (neophytes) still belong to the first generation of hatchlings that were born after the conservation measures. So very very roughly, until now, the gain in neophytes every year, should directly correlate to the number of hatchlings that were “saved” 15 years due to conservation measures. That should theoretically result in a linear increase these days, i.e., a fixed amount of “saved” neophytes is added every year. It could be the case that 15 years after the first increase of the nest numbers (i.e., around 2022), the second generation of hatchlings will be mature enough to start laying eggs as well.
Will the nest numbers explode then? If yes, is that necessarily something good? Is it always true that the more nests, the better? With how many nests will we be happy? And at which point, conservation stops and intervention begins?
We envision marine turtles fulfilling their ecological roles on a healthy Planet where all Peoples value and celebrate their continued survival.
While this statement does not give a straight answer, to how many sea turtles we would like to have out there, it implies that a healthy population is desirable, meaning that its dynamics are driven by natural powers only while the anthropogenic impact is absent. In order to find out these ideal population numbers we would have to use a time machine and go many years back in time. How many years back though? Scientists and conservationists often suffer from the baseline syndrome: The tendency to regard healthy population levels as the ones that one sees at the beginning of her/his career, see for instance here and here. Regarding Kyparissia bay, nobody can know what the correct baseline is (i.e., the population number in equilibrium where no anthropogenic effects have acted). Let us note that given the fact that Kyparissia’s beaches are pretty much pristine, the main anthropogenic effect is that of the fishing industry. In fact, it is estimated that (source), over 44000 sea turtles die every year because of the fishing industry. (Note: however, all these do not belong to the Mediterranean population, as the majority of sea turtles in the west part of the Mediterranean basin come from the Atlantic populations. Thus, always with regards to conservative estimations, the number of deaths of local Mediterranean turtles should be less). It could be the case that the average nest number in the 80’s, around 600 nests per year, was an equilibrium point driven by a combination of natural dynamics and interactions with fishing industry. Of course with such long lived species, as sea turtles are, we cannot even be certain if this number was actually an equilibrium or not.
In any case, current conservation measures in Kyparissia address only nest predation and inundation, which are both natural processes (though even that is still debatable; are predator numbers what they should be? where they always predating nests? does climate change increase inundations?). Moreover, it could be the case that even these measures do not come without a cost. In fact, given that low nest incubation temperatures produce male hatchlings, nest inundations could be a natural mechanism to boost male turtle production in, what seems to be, a female biased population, see here (page 67). Also, sea turtles lay their nest away from the surf, something that has resulted as a natural selection process. One could argue that by relocating a doomed nest, that would result in survival of hatchlings that will keep doing the same wrong choice of nest site. However in this interesting study for an Australian loggerhead population, it was shown that
…doomed-egg relocation does not substantially distort the gene pool in the eastern Australian loggerhead stock and should not be abandoned as a strategy for the conservation of marine turtle populations.
Still further research is required on this topic. Taking all the above into account, my opinion is:
The current conservation measures in Kyparissia are only justified if they are considered as counter-measures to sea turtle mortality in the sea. If the anthropogenic sea turtle mortality was zero then they shouldn’t exist in the first place.
Of course the above statement, implies that we are trying to solve a problem (anthropogenic mortality), not by dealing with the problem directly but sort of by patching it up. Of course, this is not big news in sea turtle conservation. Mortality at sea due to fishing industry is extremely difficult to control and hence reduce. Thus, it looks like that start of conservation measures in the beginning of the 90’s was well justified indeed.
But what about in the future? Should we always celebrate after another record breaking year? Nest numbers are starting to blow up, making the protection of every single nest, an almost impossible task. Unless any density effects come into play, introducing some negative dynamics, this increase is likely to continue (?). We have seen cases where nesting beaches host a huge number of nesting females, like the case of Raine island in Australia (see this impressive video), the largest green sea turtle rookery in the world with tens of thousands females every year. In fact, Raine island is an example where, turtles are just too many. So many in fact, that they destroy each other’s nests, resulting in an extremely low nesting and hatching success (just Google “Raine island reproductive failure”).
Yet, the young conservationist in Kyparissia has a decision to make: protect or not the nest she/he just found? Depending on if none, half or all the nests are decided to be protected, the long term equilibrium nest number that corresponds to each decision will be different (and currently unknown). None decision seems right or wrong at the moment, but we should definitely dream of a time where sea turtle population dynamics are only driven by natural processes.
This post is dedicated to those, who have walked thousands kilometres, poured hundreds kilos of sweat and spent countless sleepless nights at the beaches of Kyparissia.