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According to Edmonds (1998), delayed death “occurs when the [human] victim appears to recover from the [nearly drowning] incident, but then proceeds to die.” My brief search of the Internet produced the following additional descriptions of effects of aspiration of seawater by humans (see also Lunetta & Modell 2005): (1) http://medical-dictionary.thefreedictionary.com/drowning - “Sea water aspiration results in fluid-filled but perfused alveoli, accompanied by a V/Q abnormality due to pulmonary edema; the shifts of fluids and electrolytes in salt water drowning result in hemoconcentration, CHF [congestive heart failure], and hypernatremia. ”

(2) <http://armymedical.tpub.com/MD0587/MD05870088.htm> - “The effect on the casualty is different when the incident occurs in salt water. Salt water entering the lungs has a higher solute concentration than the plasma in the bloodstream. This causes fluid to be drawn out of the bloodstream into the lungs, causing a massive pulmonary edema (congestion of the lungs). The concentration of salt in the sea water has drawn the normal body water into the lungs. If enough fluid has been drawn out of the patient's bloodstream, the person may go into shock and drown in his own interstitial fluid (fluid bathing the cells). ”

( 3 ) <http://emedicine.medscape.com/article/772753-overview> - “Additional classification may include the type of water in which the submersion occurred, such as freshwater and saltwater, or natural bodies of water versus man made. Although initial treatment of submersion victims is not affected by the type of water, serum electrolyte derangements may be related to the salinity of the water (particularly if large amounts of water are ingested), while long-term infectious complications are primarily related to whether the victim was submersed in a natural or a man-made body of water. ”

The sea turtle pulmonary system consists of glottis, trachea, a bronchus to each lung, and left and right lungs (Wyneken 2001, 2006). When a sea turtle surfaces and dives under normal circumstances, its glottis opens at surfacing to allow air passage into the lungs and it is closed during normal breath-hold diving; also, the anterior tissue lining the nares is erectile in adult sea turtles, and has the ability to seal the nostrils when the turtles are submerged (Wyneken 2001, 2006).

Physiological effects of normal, quiescent, breath-hold dives by sea turtles are mild to moderate compared to those associated with vigorous breath-hold swimming, or with struggling accompanying forced submergence (Stabenau et al. 1991; Moon & Stabenau 1996; Lutcavage & Lutz 1997; Lutcavage et al. 1997; Lutz 1997; Hoopes et al. 2000; Moon & Foerster 2001; Harms et al. 2003; Stabenau & Vietti 2003; Wyneken et al. 2006; Snoddy et al. 2009; Work & Balazs 2010). Voluntary dives appear aerobic, with little if any increase in blood lactate and only minor changes in acid- base balance; however, during such dives, a sea turtle incurs an oxygen debt, which must be repaid through resumed breathing when it surfaces (Lutcavage & Lutz 1997). During voluntary dives, sea turtles typically do not exceed their aerobic diving limit (Southwood et al. 1999; Hochscheid et al. 2007). However, during vigorous breath-hold swimming, or struggling accompanying forced submergence, oxygen stores are consumed rapidly, anaerobic glycolysis occurs, and acid-base balance is disturbed, sometimes to lethal levels (Lutcavage & Lutz 1997).

Apparent recovery of comatose or debilitated sea turtles collected and resuscitated following forced submergence can require many hours (Balazs 1986; Harms et al. 2003; Snoddy et al. 2009). If seawater aspiration by sea turtles is a common occurrence during forced submergence, 24 hr of post-submergence treatment may not be sufficient to assure their survival following release (<http://www.nefsc.noaa.gov/nefsc/publications/crd/crd1110>). For example, of nine Kemp’s ridleys (Lepidochelys kempii) found stranded alive in 1994, only two survived and were released; five died within 72 hr of being retrieved for rehabilitation, and two survived more than 72 hr before dying (Cannon 1998). Of the two that survived more than 72 hr before dying, necropsies revealed that “... both had abnormal development of the lungs”, and that “[d]efects causing inefficient gas exchange were likely contributors to the demise of these two animals” (Cannon 1998).

It is difficult to confirm drowning as the cause of death due to forced submergence based on necropsies of dead-stranded sea turtles (Wolke & George 1981). NMFS (2012) provided the following description: “Suspicion of drowning (i.e., involuntary or forced submergence) in a stranded sea turtle, such as that for PTT102741, is not based on any one finding alone (e.g., sediment in the lungs), but relies on exclusion (to the extent possible) of other potential causes of death/debilitation. It is not unusual to identify drowning as a potential cause of death for any air-breathing animal that lives in an aquatic environment. Furthermore, there is nothing diagnostic about a forced submergence scenario that would necessarily distinguish it from other causes of drowning. A conclusion of forced submergence is generally based on other findings, specifically the lack of any significant trauma, disease or indicators of poor general health; evidence of a sudden event (e.g., food in the mouth or esophagus); and/or absence of harmful algal bloom and other toxins. ” Interestingly, various commentaries on preliminary results of Brian Stacy’s necropsies of sea turtles found stranded in the northern Gulf of Mexico during 2011 mentioned evidence of drowning, including aspiration of sediment-rich water. That sediment-rich water most likely was seawater.

Incidental capture of sea turtles in towed trawls or dredges represents a special case of forced submergence. When sea turtles are caught in shrimp trawls, which are towed at rates of 0.5-1.5 m s-1 (<http://www.fao.org/fishery/fishtech/1021/en>), they initially face the current and are pressed against the netting above them (e.g., Ogren et al. 1977; <http://www.nmfs.noaa.gov/pr/species/turtles/loggerhead_video.htm>). Any sea turtle caught incidentally in a shrimp trawl obviously failed to out-swim or out-maneuver the trawl. Therefore, the question arises whether sea turtles caught in towed trawls aspirate seawater due to exposure to currents and turbulence within the trawls. A somewhat comparable human model might be the seawater aspiration syndrome in divers, including those affected by a fast-towed underwater search, faulty (leaking) SCUBA equipment, exertion, swimming against currents, exhaustion, panic, etc. that can lead to seawater aspiration as part of the sequence leading to their death (Edmonds 1998; Lunetta & Modell 2005). Van Beeck et al. (2005) proposed a new definition of drowning in humans, noting large variations related to types of activity and water to which they are exposed (including oceans).

If delayed mortality due to seawater aspiration occurs in sea turtles, it might help explain continued strandings of sea turtles concomitant with shrimp trawling in the southeastern U.S., despite regulations requiring turtle excluder devices (TEDs) in shrimp trawls (Stabenau et al. 1991; Caillouet et al. 1996; Shaver 1998; McDaniel et al. 2000; Epperly 2003; Lewison et al. 2003; Sasso & Epperly 2006; NMFS 2012). Obviously, prolonged forced submergence and associated mortality in sea turtles could result from various violations of TED regulations described by NMFS (<http://www.nmfs.noaa.gov/pr/pdfs/species/deis_seaturtle_shrimp_fisheries_interactions.pdf>): “NMFS has recently noticed compliance issues with TED requirements in the shrimp fisheries. During numerous evaluations conducted in both the Gulf of Mexico and Atlantic Ocean over the past two years, NMFS gear experts have noted a variety of compliance issues ranging from lack of TED use, TEDs sewn shut, TEDs installed improperly, and TEDs being manufactured that do not comply with regulatory requirements. ” When sea turtles aspirate seawater into their lungs during forced submergence and cold-stunning, delayed mortality might occur even though the turtles are resuscitated (Balazs 1986; Norton 2005; Wyneken et al. 2006; NMFS SEFSC 2008; Canion & Rogers 2010a, 2010 b), provided medical treatment, and released alive (<http://www.nero.noaa.gov/prot_res/stranding/SeaTurtleHandlingResuscitationv1.pdf>). Evidence of or speculation about seawater inhalation into the lungs of sea turtles and its consequences can be found in Ryder et al. (2006), Wyneken et al. (2006), Innis et al. (2009), Snoddy & Williard (2010), Work & Balazs (2010), Upite (2011), and Stockman et al. (in press). The following description of delayed effects of seawater aspiration by sea turtles was given by Wyneken et al. (2006): “Saltwater drowning is a serious condition. Even if the patient is resuscitated, the residual seawater in the lungs induces a secondary drowning as body water follows the osmotic gradient, leaving the pulmonary tissue and entering the lungs. Treatment is difficult, and the prognosis is grave. Antibiotics, fluids, positional drainage (inclined with head down), suction, and oxygen supplementation may be necessary. ”

Sea turtles that are comatose, lethargic, or active after known exposure to forced submergence and cold-stunning, but otherwise appear healthy, are the best candidates for further research on potential effects of seawater aspiration on delayed mortality. However, for research purposes, they should be tracked after release (e.g., Snoddy & Williard 2010), or retained in captivity under conditions amenable to resuscitation, medical treatment, extended observation, and rehabilitation, over periods long enough for full evaluation of their recovery (Upite 2011). If they die while receiving medical treatment, more information would be available on the cause(s) of death. In any case, the working hypotheses concerning delayed mortality associated with seawater aspiration by sea turtles subjected to forced submergence or exposed to hypothermia seem worthy of further attention and research.

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