This is the first study to document the occurrence, severity, and progression of GE in marine turtles captured by commercial bottom trawl gear and to provide estimates of on-board and post-release mortality of turtles released without treatment. This study is also the first report of GE in marine turtles outside the Mediterranean Sea, indicating a high likelihood that DCS is a global concern among all fisheries that capture turtles in a manner that results in underwater entrapment or forced submergence. Furthermore, GE was diagnosed in an olive ridley sea turtle for the first time. To date, four species of marine turtles, including loggerhead, green, leatherback, and olive ridley have been diagnosed with GE13, (Garcia-Párraga & Crespo-Picazo pers. com.).
All turtles assessed by ultrasonography and/or post-mortem examination developed various degrees of GE. GE developed immediately and was detectable in all cases at the time of initial assessment, as soon as 15 minutes post-surfacing. We did not expect such a high frequency of occurrence based on previous studies in Spain, which found GE in only 43–55% of turtles captured by trawl at depths of 25–75 meters13,20. Notably, turtles examined during these earlier studies were evaluated up to 8–10 hours post-capture. It is possible that those with mild GE were able to eliminate and resolve the gas bubbles prior to examination. Our understanding of the progression and resolution of GE under natural conditions, as well as the various factors that may influence this condition and its clinical outcome, remains limited and worthy of further study20.
The severity of GE quickly worsened over the 2-hour monitoring period, with most animals reaching a 3/3 severity score, particularly those caught during the warmer months. This progression was less evident in animals caught during the winter, although seasonal differences were not statistically significant (p = 0.08) and there was no association between season and turtle mortality rates. Sasso and Epperly9 reported a higher mortality rate of turtles captured by trawling in colder months, thus we were interested as to whether such a seasonal affect could be associated with risk of GE. We did not find evidence of this, but our sample size was small. Various factors, such as prior dives, activity level, or previous fishery interactions may influence gas bubble formation in marine turtles and confound interpretation of results, especially when sample sizes are limited, as is often the case due to many logistical challenges associated with fisheries-based studies23.
The post-release mortality rate for turtles examined in our study was 20% based on the satellite telemetry results for 15 bycaught turtles, 11 of which survived at least 30 days. This rate is most relevant to those turtles that are active and alert upon release, and did not include animals that were weak, but responsive and subsequently died on-board, which may have been immediately released if not for our study. Additional mortality beyond 30 days from long-term effects of GE needs to be considered, but was not assessed in this study. There are in fact other potential health risks associated with development of GE that may cause a long-term mortality18,24. Although further studies of GE and long-term mortality are warranted, accurate determination of post-release mortality is logistically challenging, especially over 90 days after release, due to the numerous factors that can influence risk of death6.
Our mortality rate is in contrast to findings by Maxwell et al.12, who reported that 3 comatose bycaught turtles revived on-board vessels survived at least 30 days after release. In their study, however, trawl depth was shallower and of shorter duration compared to our study (i.e., 12 and 17 meters, and 1,5 to 3,5 hours, respectively) and presence of GE was not assessed. Most unresponsive turtles encountered during our study died and were found to have both GE and evidence of water aspiration. In our experience, GE and DCS entail a worse prognosis if they occur concurrently with water aspiration13,25.
All turtles but two (captured during the cold season) developed moderate to severe GE as measured by ultrasonography. While this degree of GE in turtles admitted to rehabilitation centres tends to be fatal when untreated13, nearly 80% of released turtles in our study survived at least for 30 days post release. One possible explanation for the lower mortality in our study is that turtles may have been in the early gas-off phase with intravascular gas forming micro-bubbles throughout the body, leading to an overestimated GE scoring by ultrasound. However, in animals admitted to rehabilitation centres several hours after the decompression event, the gas-off phase is most probably over. Most circulating gas emboli may have already been eliminated through the lung via respiration, and the residual gas tends to be retained in organs and tissues, forming larger nitrogen bubbles after coalescence. This results in a much lower degree of GE at that point, even when originally and based only on ultrasonography it would have been scored as more severe. Moderate and severe GE cases seen at rehabilitation centres are those cases that accumulate so much gas from the onset of cardiorespiratory failure that clearance is hindered during the first 8–12 hours after surfacing.
Another hypothesis is that, once released, active turtles may be able to dive back to depths necessary to recompress, resulting in reduction of bubble size and allowing partial reperfusion and re-dissolution of nitrogen bubbles formed after surfacing. Repeated diving and ascent phases coupled with minimal time at the surface may allow turtles to successfully manage elimination of non-dissolved nitrogen bubbles over several days. This could minimize the risk of accumulating large amounts of bubbles in circulation, which would otherwise impede normal tissue or organ perfusion. In this study, the diving profile of released animals could not be assessed, but records of the transmitters show that all animals dived between 9 to 138 meters at least once every day. To confirm this hypothesis, it would be useful to evaluate the diving profile of decompressed turtles during the first days after release and compare their behaviour with healthy turtles. Based on maximum registered diving depths recorded by sPAT tags of the study animals, we believe that deeper dives did not occur immediately after the decompression event.
Results of clinical evaluations were similar to those previously described with DCS in loggerheads25,26. Compared to blood data from clinically normal marine turtles27,28, blood analyses indicated physiological and hemodynamic derangements with reduced glomerular filtration rate attributable to forced submergence, physical exertion, and GE. The degree of lactic acidosis was extreme and up to 3 times higher than reported for loggerhead turtles caught by trawl at shallower depths using shorter tows of 30 minutes29. We also found evidence of reduced renal function that was more pronounced in turtles that died as suggested by significantly higher potassium and phosphorus concentrations. GE is known for its main accumulation around the kidney region with time13. Furthermore, PCV was significantly lower in turtles that died, suggesting potential impaired blood flow, shunting, or shock, given the context of lactic acidosis. Tissue enzyme activities (e.g., creatine kinase, aspartate aminotransferase, lactate dehydrogenase, and alanine aminotransferase) upon arrival on deck were similar to stranded loggerhead sea turtles reported in Deem et al.27, and slightly above normal ranges for foraging turtles, suggesting effects from trawling and/or developing GE.
Although blood data from turtles at time of release was not available, the observed clinical and ultrasonographical presence and worsening of GE while on-board would presumptively result in continuous development of tissue damage while on board. This, in addition to comparatively higher glucose, demonstrates the presence of anaerobic metabolism resulting from hypoventilation and reduced tissue perfusion from forced submergence, in addition to stress. Shorter trawl periods would likely be conducive to reduce these detrimental pathophysiological effects.
The neurological examination yielded highly variable and inconsistent responses and was not considered clinically useful in the evaluation of GE or its severity. In 5 animals, the response was considered “hyper-responsive”, with the animal immediately trying to bite or abruptly removing limbs when touched. Such responses are consistent with previously reported findings in marine turtles with GE in Spain25,26 and are believed to be indicative of severe pain caused by nitrogen bubbles accumulating in different tissues.
Our observations highlight some significant challenges in caring for bycaught turtles in a manner that maximizes their survival post-release. We documented multiple well-known effects of underwater capture, including severe physiological derangements and risk of seawater aspiration. These conditions benefit from opportunity for recovery following capture and expelling water from the airways, as incorporated into common handling practices and recommendations for “resuscitation” of bycaught marine turtles30. On the other hand, we also documented a high frequency of GE in conjunction with clinical indications of DCS and resulting mortality, conditions that may be exacerbated when decompressed turtles remain at the surface without treatment. These findings demonstrate that the effects of underwater capture on marine turtles are complex and have clinically significant implications that are not easily addressed under fishing conditions. For all these reasons, the authors emphasize the importance of integrating the use of TEDs into all trawling fisheries with a high capture-rate of marine turtles as a legal requirement, since TEDs are the only way to significantly reduce incidental captures. However, we acknowledge the fact that it may take years before TEDs become a legal requirement in different parts of the world. Until TED implementation into fishing regulations will come into effect, the following summarizes our recommendations for trawlers not carrying TEDs, reflecting our current understanding and assessment:
Until further research is completed under different trawl conditions, assume that GE occurs in all turtles captured by trawls lasting more than 3 hours and greater than 17 m of depth regardless of ambient temperature. It should be emphasized that the presence of GE is not always associated with clinically overt manifestation of DCS;
Active turtles captured under the above conditions may benefit from being released as soon as possible to give them the highest chance of recovery. Keeping bycaught turtles on-board allows for continuation of gas bubble formation, presumptively worsening its pathophysiological effects. At this time it is not possible to determine how long a turtle can remain on-board safely;
If a turtle is unresponsive or weak and in need of time to recuperate, it is imperative to place it in a cool/shaded area for recovery. Warm temperatures may increase the rate of GE, likely worsening its effects;
The only situation in which it is advisable to retain a turtle on-board for a few hours, regardless of its clinical condition (active vs. unresponsive), is for transport to a qualified rehabilitation centre with means of adequate treatment, such as hyperbaric chamber or alternative specific GE/DCS treatment options. Treatment increases the probability of survival to almost 100%26. Otherwise, based on current knowledge, we strongly recommend releasing turtles back to the sea as soon as they are active and alert, and when conditions are safe to do so.
Gas embolism associated with trawl fisheries was first diagnosed in marine turtles in 201413 and there is still very little known about its incidence in turtles captured by different types of fisheries around the world, its progression over the first hours post-capture, and its resulting acute and delayed effects and mortality. Further research is imperative to ascertain how fisheries operational parameters and environmental conditions affect the onset and severity of GE in marine turtles, and to develop further recommendations to reduce DCS-related mortality. Another essential field of research is the behaviour and outcome of released turtles in order to improve recommendations for immediate handling of incidentally captured turtles in trawl and other net fisheries.
Source: Ecology - nature.com
