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Sub-adult and adult loggerhead, green, and hawksbill turtles (approximately 20 turtles) rescued from Okinawan waters have been kept in the Ocean Expo Park, Okinawa Prefecture, Japan since 1994. Captive breeding has occurred since 1995 for loggerheads, since 1999 for greens, and since 2012 for hawksbills. In August 2006, 70 loggerhead hatchlings from this program were maintained in an outdoor holding tank (570 mm in diameter and 250 mm in depth) that consisted of an open-water system with seawater drained from the holding tanks of adult and sub-adult sea turtles. Water temperature was measured daily for a year and ranged between 20 °C and 30 °C, simulating the sea surface temperature around Okinawa Island. Hatchlings were fed a mixture of fish and squid in quantities equivalent to 5% of their body weight, at 24-h intervals.

Twenty-five of the 70 turtles (one to four months old) died between September-December 2006 (Fig. 1A). Pathological examination of these dead turtles was performed immediately after death. The livers were fixed in 10% neutral-buffered formalin, dehydrated in an alcohol series, cleared in xylene, and embedded in paraffin. Cross-sections were stained with hematoxylin and eosin and were observed by light microscopy.

In an autopsy immediately after the death of the turtles, all livers showed denaturation and ischemia (yellowing and softening), and gallbladders were markedly enlarged (Fig. 1B). As shown in Fig. 2A and B, egg and adult parasitic blood flukes were found intravascularly in 23 (92%) and 6 (24%) of the 25 turtles, respectively. Additionally, the inflammatory cells, particularly those around parasite eggs, were infiltrated in 22 (88%) of the 25 turtles (Fig. 2C).

Figure 1. Photographs of liver lesion in the loggerhead turtle hatchling. (A) Dead hatchling, (B) Ventral view of the viscera.

Figure 2. Histopathological analysis of the livers of infected loggerhead turtle hatchlings. (A) Parasite eggs in the hepatic vein, (B) Parasite adults and eggs in the hepatic vein, (C) Inflammatory response around the parasite eggs. Solid line and dotted line indicate the parasite egg and adult, respectively.

Morphology of the eggs detected from microscopic lesions in turtle livers was considerably similar to that of eggs of cardiovascular blood flukes (Digenera: Spirorchidae) described previously, in particular resembling eggs of Hapalotrema, Monticellius, and Learedius species (Wolke et al. 1982; Dailey et al. 1993; Jacobson 2007; Greiner 2013). In this type of eggs, the miracidium was present in the central oval portion of the egg (Wolke et al. 1982). Furthermore, the eggs of Spirorchidae released into the blood are transported to the organs, which induce an inflammatory response (Jacobson 2007). A similar tendency was observed in the present study; blood flukes were found intravascularly in the liver, and the inflammatory cells were infiltrated in most of the dead turtle livers. Although our histological approach has a limitation in the identification of species, the hatchlings were suspected to be infected with cardiovascular blood flukes belonging to Spirorchidae. To the best of our knowledge, the present study is the first report on blood fluke infection in sea turtle hatchlings.

Spirorchidae is commonly detected in wild sea turtles. Stacy et al. (2010) detected Neospirorchis sp. and Hapalotrema sp. in 96.3% and 77.8% of the sub-adult and adult loggerhead turtles, respectively, examined in Florida. Such high infection rates have been reported in green and hawksbill turtles on the Great Barrier Reef, Australia (Glazebrook et al. 1989), green turtles in Hawaii (Santoro et al. 2007), and hawksbill turtles in the Yaeyama Islands, Japan (Kamezaki et al. 2002). Hence, cardiovascular blood flukes may be indigenous in many wild sea turtles, indicating that the captive and rescued sub-adult and adult turtles in the present study may also host the parasite. Interestingly, the hatchlings were kept in the seawater drained from the holding tanks of adult and sub-adult sea turtles. As a result, the hatchlings may have been infected through the seawater drained from the holding tanks of captive adult and sub-adult sea turtles. Other loggerhead hatchlings in this center are kept in an open-water system of natural seawater (not the same seawater as sub-adult and adults) and no mortality due to parasitic infection has been observed in these hatchlings, supporting the idea that hatchlings may have been infected by cardiovascular blood flukes passed from the sub-adult and adult turtles.

Taken together, the results of the present study indicate that loggerhead turtle hatchlings are infected by blood flukes causing serious mortality. Based on these findings, we believe that blood fluke infection could be a serious mortality factor in loggerhead turtle hatchlings in natural waters.

Acknowledgments. We express our deep gratitude to the staff responsible for the captive sea turtles at the Okinawa Churashima Foundation for their assistance with the rearing of the loggerhead hatchlings. We also thank Dr. Y. Kagawa of North Lab for her advice on histopathological examination.

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