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Changes in Plasma Levels of Adrenaline, Noradrenaline, Glucose, Lactate and CO2 in the Green Turtle, Chelonia Mydas, During Peak Period of Nesting

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Changes in Plasma Levels of Adrenaline, Noradrenaline, Glucose, Lactate and CO2 in the Green Turtle, Chelonia Mydas, During Peak Period of Nesting Available online at www.sciencedirect.com General and Comparative Endocrinology 155 (2008) 581–588 www.elsevier.com/locate/ygcen Changes in plasma levels of adrenaline, noradrenaline, glucose, lactate and CO2 in the green turtle, Chelonia mydas, during peak period of nesting A.Y.A. AlKindi *, A.A. Al-Habsi, I.Y. Mahmoud Department of Biology, College of Science, Sultan Qaboos University, 123, Al-Khod, Muscat, Oman Received 12 March 2007; revised 14 September 2007; accepted 15 September 2007 Available online 21 September 2007 Abstract Plasma concentrations of stress hormones [adrenaline (ADR), noradrenaline (NR)], lactate, glucose and CO2 were monitored during peak nesting period (May–October) at different phases of nesting in the green turtle, Chelonia mydas. These include, emergence from sea, excavating body and nest chambers, oviposition, covering and camouflaging the nest and then returning to sea. Turtles that completed all phases of nesting including oviposition before returning to sea were considered ‘‘successful’’ turtles, while those that completed all phases but failed to lay their eggs were ‘‘unsuccessful’’. Blood samples were taken from the cervical sinus within 5 min of capture to avoid stress due to handling. The turtles were usually sampled for blood between 20:00 and 1:00 h of nesting time to ensure uniformity in the sam- pling. Plasma ADR and NR values were highly significant (P < 0.001) in successful turtles over emergence, excavating and unsuccessful turtles. Plasma glucose levels remained stable throughout the nesting phases while lactate levels were significantly higher in successful turtles over the other phases (P < 0.05) which signifies anaerobic metabolism during nesting. Plasma CO2 values were negatively corre- lated with ADR and NR (r = À0.258, P = 0.03; r = À0.304, P = 0.010), respectively. Hematocrit was significantly higher in successful phase (P < 0.05) compared to other phases, and this may signify a higher degree of stress in successful turtles. Body temperature were significantly lower (P < 0.005) in the excavating phase compared to the other three phases. Overall, body temperatures were lower than sand temperatures around the nest, which may indicate a behavioral thermoregulation used by the turtles during nesting. This informa- tion will be of value to the ongoing conservation program at Ras Al-Hadd Reserve in the Sultanate of Oman. Ó 2008 Published by Elsevier Inc. Keywords: Catecholamine; Nesting; Sea turtles 1. Introduction moisture, sand obstacles or disturbance. This is the case in green turtles where, nesting can be a long stressful ordeal Female sea turtles go through exhaustive and difficult and sometimes lasts for several hours, depending on the physical activities during nesting phases that include number of nest abandonments during excavation (AlKindi emerging from the sea and crawling to a selected nest site, et al., 2003). excavating the nest, ovipositing, burying the eggs, and It is well documented that in reptiles, exhaustive exercise crawling back to sea (AlKindi et al., 2003; Hendrickson, triggers the release of catecholamines (adrenaline ADR, 1982; Bustard, 1973; Bustard and Greenham, 1969). Before noradrenaline NR) into the bloodstream to accelerate ven- choosing a favorable nesting site to lay their eggs, sea tur- tilation, heart rate, glycogen utilization, and oxygen uptake tles frequently investigate and then abandon several sites (AlKindi et al., 2003; Gleeson et al., 1993). Moreover, sea because of unfavorable conditions, such as lack of sand turtles, like some lung-breathing reptiles, ventilate intermit- tently (Comeau and Hicks, 1994; Shelton and Burggren, * Corresponding author. Fax: +968 24413415. 1976; Wasser and Jackson, 1991). Thus, after a burst of E-mail address: [email protected] (A.Y.A. AlKindi). strenuous exercise (about 30–60 s) during the nesting 0016-6480/$ - see front matter Ó 2008 Published by Elsevier Inc. doi:10.1016/j.ygcen.2007.09.012 582 A.Y.A. AlKindi et al. / General and Comparative Endocrinology 155 (2008) 581–588 process, the turtle stops its exercise so it can acquire O2 and get rid of CO2 (for about 30–40 s) (AlKindi et al., 2003). Sea turtles require only a few breaths lasting less than 2– 3 s to empty and refill their lungs with fresh O2 (Lutcavage and Lutz, 1997). Catecholamines are known to play an important role in augmenting hepatic glucose metabolism during acute stress (Hargrove et al., 1988). Catecholamines trigger an increase in glucose turnover due to an increase in hepatic glycogen- olysis and gluconeogenesis. Gleeson and Kolok (1990) demonstrated in vitro that, in the red and white muscles of the lizard Dipsosaurus dorsalis, lactate metabolism was influenced by adrenaline, in both the presence and the absence of glucose. They concluded that catecholamine Fig. 1. Annual nesting activity of green turtles (C. mydas) at Ras Al-Hadd release associated with exercise in lizards, and in reptiles Reserve, Oman. in general, facilitates muscle glycogen resynthesis and lac- 2.2. Temperature measurements tate removal. Other studies have also confirmed that skele- tal muscles in lizards are capable of resynthesizing muscle As a representative measure of body temperature, core body tempera- glycogen in situ shortly after strenuous exercise (Gleeson, ture (Jessop et al., 2000; Mrosovsky, 1980) was recorded for each turtle sam- 1991; Gleeson and Dalessio, 1989, 1990). pled for blood using a battery-operated digital thermometer with ‘k’ type These stress hormones are believed to adapt the body to thermocouple (model 2103, Jenway Co., UK). The probe was inserted into stressors that present an immediate threat to homeostasis the body (around 15–18 cm) until there was no change in the temperature reading. Each body temperature reading was conducted immediately after (Lance, 1994). Sea turtles, like other reptiles, must main- blood sampling. Sand and air temperatures were taken using the same digital tain a steady physiological state in response to a changing thermometer but with a probe specialized for sand and air. The sand temper- environment. An understanding of the stress response is ature was taken parallel to the nest chamber while the turtle was ovipositing essential to evaluate the physiological mechanisms that her eggs at the depth of 30 cm below the surface. Air temperature was taken maintain homeostasis in turtles and reptiles in general. two feet above the sand surface directly above the nest chamber. Endocrine products of the hypothalamo–pituitary–adrenal 2.3. Phases of nesting and blood collection axis have been used extensively as indicators of physiolog- ical stress in vertebrates (Axelrod and Reisine, 1984; 2.3.1. Criteria for classifying phases of nesting Greenberg and Wingfield, 1987; Greenberg, 1990; Wing- Emergence (EM), emerging from sea after the turtle is 10–15 m ashore. field and Sapolsky, 2003). Excavation (EX), excavating body and/or nest chambers after the tur- Changes in hematological parameters have also been tle chooses a specific nesting site. Unsuccessful (UN), excavating body and/or nest chambers but fails to widely used to assess stress in a variety of reptiles and verte- lay eggs, usually because of nest collapse. After one or several trials, the brates in general (Aguirre et al., 1995; Sørensen and Webber, turtle returns to sea. 1995) particularly in relation to environmental stressors Successful (SU), excavating body chamber, nest chamber, laying eggs, (Aguirre et al., 1995; Hajduk et al., 1992; Swimmer, 2000). covering and camouflaging nest and then returns to sea. A population of green turtles at Ras Al-Hadd has a unique reproductive pattern because of year-round nesting. 2.3.2. Blood collection Blood samples were collected from normal healthy nesting green tur- From May to October, nesting density is high (peak per- tles without any physical defects or injuries such as missing or damage iod), whereas from November to April, density is low to the flippers broken shell, or any injuries to the other body parts. All tur- (non-peak period; Fig. 1). The nesting behavior of the tles examined were free of fibropapilloma. green turtles in Ras Al-Hadd is described extensively dur- The turtle’s flippers were held by four people and the fifth person held ing peak and non-peak periods (AlKindi et al., 2003). the head into a depression made in the sand so the blood could flow easily into the neck region. Immediately after that, the blood was drawn by a The physiological data obtained from this study will be sixth person. of significant value in the overall understanding of the nest- The blood sample was collected immediately after each turtle had com- ing physiology of the green turtles at Ras Al-Hadd Reserve pleted a particular nesting phase. In the emergence and excavation phases, in the sultanate of Oman. a turtle would not continue its nesting activities after the blood was taken and it immediately returns to sea. This behavior was also noticed by AlK- indi et al. (2003). 2. Materials and methods In unsuccessful turtles, the blood sample was not taken until the turtle abandoned its nesting activities and has already headed toward the sea. 2.1. Study sites In successful turtles, the blood sample was taken when the turtle had completed all its nesting activities and was in the process of leaving its Ras Al-Hadd Reserve is located on the Gulf of Oman and the Arabian nesting site for the sea. Thus each turtle in this study was sampled only Sea (between 22°320N and 59°450E and 22°140N and 59°480E). The coast- once at any given night for each specific nesting phase. line is characterized by moderate to high-energy wave action, and is Moreover, all the turtles used in this study had either been tagged pre- mostly sheltered by rocky hills (Salm and Salm, 1991). Approximately viously or were tagged after the blood sampling. The tagging operation at twenty beaches with different lengths (50 m–5.3 km) make up the Reserve.
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