Erythropoietin concentration in developing harbor seals (Phoca vitulina)
Introduction
Erythropoietin (Epo) is a glycoprotein hormone that stimulates red blood cell (RBC) production in response to changes in oxygen tension, oxygen storage capacity, and oxygen affinity of the blood (Jelkmann, 1992, Moritz et al., 1997). Prior to parturition, Epo is produced in the fetal liver. After birth, Epo is produced primarily in the kidneys (Jelkmann, 1992, Palis and Segel, 1998), with smaller amounts produced in the adult liver (Moritz et al., 1997), testes (Tan et al., 1992), and brain (Digicaylioglu et al., 1995, Masuda et al., 1994). As part of a negative feedback control mechanism, Epo production increases in response to hypoxia (low oxygen) and decreases in response to hyperoxia (high oxygen) (Krantz, 1991, Porter and Goldberg, 1994). Erythropoietin is highly specific with no known effect other than to enhance the production of red blood cells, or erythropoiesis (Jelkmann, 1992), particularly during anemic conditions.
Anemia, a condition of reduced hemoglobin concentration [Hb], hematocrit (Hct), and/or RBC count, has been associated with postnatal development in a variety of terrestrial mammals, such as mice, rabbits, rats, piglets, calves, and humans (Halvorsen and Bechensteen, 2002, Heikinheimo and Siimes, 1992, Sanengen et al., 1987, Sjaastad et al., 1996). Typically, this period of reduced blood oxygen stores in developing mammals is known as early anemia. Early anemia results from the rapid expansion of plasma volume and decreased RBC and/or [Hb] per unit blood volume (Feldman et al., 2000). This ‘physiological anemia of infancy’ typically occurs throughout the nursing period (Halvorsen and Bechensteen, 2002) and is not pathological in nature. The decreased oxygen storage capacity during the nursing period induces tissue hypoxia due to the reduced availability of oxygen for tissue use (Jelkmann, 1992). In response, Epo concentrations are elevated and stimulate red blood cell production to increase the oxygen carrying capacity of blood. Early anemia, therefore, can be detected by measuring blood parameters of rapidly developing young mammals.
With a relatively short postnatal developmental period (∼28 days), young harbor seals (Phoca vitulina) enter the water soon after birth and follow their mothers throughout lactation (Bigg, 1969, Boulva and McLaren, 1979, Bowen et al., 1999, Knudtson, 1977). Harbor seal pups must quickly develop the physiological mechanisms necessary for diving and ultimately independent foraging. This includes rapid development of blood oxygen stores (Clark, 2004, Jørgensen et al., 2001), and the ability to reduce metabolic rate, regulate diving heart rate, and control peripheral vasoconstriction (Greaves et al., 2004, Greaves et al., 2005, Kooyman, 1989, Lapierre et al., 2004). Since diving mammals are limited in their breathhold ability by the amount of oxygen available prior to a dive (Butler and Jones, 1997, Kooyman, 1989), and since harbor seals store more than 60% of their total tissue stores in blood (Clark, 2004), the development of blood oxygen stores is crucial to maximize breathhold ability. However, there have been no studies on the factors that stimulate or regulate the increase in blood oxygen stores in any phocid. Therefore, this study investigates Epo concentration changes in harbor seals from birth to weaning, to assess whether postnatal changes in Epo are coupled with simultaneous changes in [Hb], Hct, RBC counts, and blood oxygen stores. From this work, we will determine if the mechanism that regulates neonatal blood development in diving and terrestrial mammals are similar.
Section snippets
Animal capture, handling, and sample collection
Harbor seal pups and adult females were captured during May–July of 2000, 2001, and 2002 near two haul-out sites, “Bic Island” (48°24′N, 68°51′W) and “Métis” (48°41′N, 68°01′W), along the south shore of the St. Lawrence River estuary in Quebec, Canada (Fig. 1). Seals were captured using a 5 m inflatable boat and a modified dip net (Dubé et al., 2003), and once captured basic morphometric measurements (e.g., sex, mass ± 0.5 kg) were taken. After weighing, pups were outfitted with uniquely numbered
Results
Over the 3 years of this study, 114 pups and 20 adults were sampled. Of these, 78 pups and 20 adult females were sampled only once, while 36 pups were sampled two or more times. There were significant age-related changes in plasma Epo concentration in the cross-sectional group (one-way ANOVA, F4,93 = 3.398, P = 0.012, Fig. 2). Comparisons between age categories revealed that newborns had low plasma Epo concentration that increased in early nursing (6.64 ± 0.83 to 9.53 ± 0.86 mU/ml, Fig. 2) and remained
Discussion
This study provides the first measurements of plasma Epo concentration in developing harbor seals. As in terrestrial mammals, neonatal harbor seals had Epo concentrations that were higher than those of adults (Moritz et al., 1997, Sanengen et al., 1987) and Epo remained elevated throughout the lactation period. The rapid early increase in Epo concentration occurred within 4 days of birth when oxygen carrying capacity decreased due to the significant reduction in [Hb], Hct, and RBC counts. These
Acknowledgments
Many thanks to the 2000–2002 field crews for their hard work and enthusiasm, most-notably: P. Carter, D. Dion, Y. Dubé, J.-F. Gosselin, D. Greaves, J. Greig, J. Lapierre, S. Turgeon, and G. Yunker. Thank you to L. Measures and S. Atkinson for access to laboratory space and equipment and to K. Mashburn for assistance with the radioimmunoassay. A special thank you to L. Clark and J. Richmond for assistance with manuscript preparation and laboratory analysis. Funding for this work was provided by
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