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Comparative Seabird Diving Physiology: First Measures of Haematological Parameters and Oxygen Stores in Three New Zealand Procellariiformes

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Comparative Seabird Diving Physiology: First Measures of Haematological Parameters and Oxygen Stores in Three New Zealand Procellariiformes Vol. 523: 187–198, 2015 MARINE ECOLOGY PROGRESS SERIES Published March 16 doi: 10.3354/meps11195 Mar Ecol Prog Ser Comparative seabird diving physiology: first measures of haematological parameters and oxygen stores in three New Zealand Procellariiformes B. J. Dunphy1,*, G. A. Taylor2, T. J. Landers3, R. L . Sagar1, B. L. Chilvers2, L. Ranjard4, M. J. Rayner1,5 1School of Biological Sciences, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand 2Department of Conservation, PO Box 10420, Wellington 6143, New Zealand 3Auckland Council, Research, Investigations and Monitoring Unit, Level 4, 1 The Strand, Takapuna Auckland 0622, New Zealand 4The Bioinformatics Institute, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand 5Auckland Museum, Private Bag 92018, Victoria Street West, Auckland 1142, New Zealand ABSTRACT: Within breath-hold diving endotherms, procellariiform seabirds present an intriguing anomaly as they regularly dive to depths not predicted by allometric models. How this is achieved is not known as even basic measures of physiological diving capacity have not been undertaken in this group. To remedy this we combined time depth recorder (TDR) measurements of dive behaviour with haematology and oxygen store estimates for 3 procellariiform species (common diving petrels Pelecanoides urinatrix urinatrix; grey-faced petrels Pterodroma macro ptera gouldi; and sooty shearwaters Puffinus griseus) during their incubation phase. Among species, we found distinct differences in dive depth (average and maximal), dive duration and dives h−1, with sooty shearwaters diving deeper and for longer than grey-faced petrels and common diving petrels. Conversely, common diving petrels dove much more frequently, albeit to shallow depths, whereas grey-faced petrels rarely dived whatsoever. Such differences in dive behaviour were reflected in haematological parameters, with sooty shearwaters having higher red blood cell counts and haematocrit (Hct) values compared to common diving and grey-faced petrels; whereas common diving petrels had significantly lower Hct but possessed higher haemoglobin concentrations per cell and greater respiratory oxygen stores than both sooty shearwaters and grey-faced petrels. Such results provide the first insights into the physiological traits underpinning procellariiform dive behaviour, and confirm the trend for deep-diving seabirds to have proportionally lower blood and respiratory oxygen stores than shallow divers. KEY WORDS: Petrel · Shearwater · Physiology · Time depth recorder · TDR · Allometry Resale or republication not permitted without written consent of the publisher INTRODUCTION of diving endotherms are being realised via the use of time depth recorders (TDRs) which log multiple Breath-hold diving in endotherms is a complex recordings over extended periods (Wilson & Vanden- interplay between competing ecological, behavioural abeele 2012). From this, precise estimates of dive and physiological exigencies (Halsey et al. 2006a). duration and average/maximal dive depth can be Understanding the contribution of each of these ascertained, and, by matching this information to demands relies upon accurate characterisation of physiological data, a mechanistic insight into the dive behaviour, most notably dive depth (average physiological dive capacities of a species is afforded. and maximal) and duration (Halsey et al. 2007). Physiologically, there is a general trend for larger High-resolution insights into underwater behaviour endothermic species to attain greater depths (Schreer *Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 188 Mar Ecol Prog Ser 523: 187–198, 2015 & Kovacs 1997). This is because oxygen usage and MATERIALS AND METHODS oxygen stores in the blood, muscle myoglobin and respiratory system scale with mass; thus larger ani- Study location and specimens mals use less oxygen and have more oxygen reserves to draw upon when underwater (Halsey et al. 2006b). The procellariiform species used in this study were However, one group of animals that deviate from from breeding colonies within the Auckland region this relationship are procellariiform seabirds, which of New Zealand (Fig. 1). Characterisation of diving can regularly attain depths greater than their mass behaviour and haematological samples of common would predict (Halsey & Butler 2006). The exact diving petrel were taken from a colony located on physiological mechanisms underpinning this result Burgess Island (35° 54’ 10’’ S, 175° 07’ 05’’ E) Moko- are unknown as no information exists on procellari- hinau Island group; whereas sooty shearwaters were iform dive physiology. Moreover, some species of from a colony on Kauwahaia Island, Bethells beach Procellariiformes undertake annual trans-equatorial (36° 53’ 13’’ S, 174° 26’ 12’’ E). For grey-faced petrels, migrations (e.g. sooty shearwater Puffinus griseus) dive be haviour was characterised for adults located thus placing them in an adaptive valley between on Ihumoana Island (located 400 m south of Kauwa- being a migratory flight or dive specialist (Shaffer et haia Island, Bethells Beach) and haematological sam- al. 2006, Elliott et al. 2013). Strategies used to sup- ples were taken from adults on Burgess Island. All port this dual mobility cannot be understood in birds used were adults in the incubation phase of the the absence of basic physiological metrics of dive breeding cycle. Species weights, TDR deployment capacity. duration and the number of replicates for quantifying We undertook a comparative study of dive behav- dive behaviour and physiological parameters in this iour and physiology in 3 procellariiform species that study are summarised in Table 1. Morphological dif- breed in New Zealand waters. The species studied ferences exist among these species, with the common were common diving petrels Pelecanoides urinatrix diving petrel noted for its shorter wing (reminiscent urinatrix, grey-faced petrels Pterodroma macroptera of the Alcidae) compared to the longer wings of grey- gouldi and sooty shearwaters Puffinus griseus, which exhibit large differ- ences in mass (147, 503 and 848 g, respectively). Moreover, whilst these species are known to have differences in maximal dive depth (Taylor 2008), temporal measures of average dive depth, dive duration and dive fre- quency are yet to be determined. We attempted to match dive behaviour measurments to measures of oxygen stores (blood and respiratory) and haematology to allow a mechanistic understanding of dive capacity in these species. Finally, for many bird species oxygen carrying capacity changes intraspecifically as a result of ontogeny or migration (Minias et al. 2013), thus we concentrated on birds during their incubation phase in order to standardise comparisons among spe- cies. Our specific questions were: Do differences in dive behaviour (average depth and duration) exist among 3 species of Procellariiformes? If so, is this information reflected in key phy - siological parameters of dive capacity Fig. 1. Location of Burgess Island, Ihumoana Island and Kauwahaia Island (oxygen stores and haematology)? study sites in northern New Zealand Dunphy et al.: Procellariiform dive behaviour and physiology 189 Table 1. Weight (mean ± SE), time depth recorder (TDR) deployment data and number of replicates taken for characterising dive behaviour and haematology/ oxygen stores in incubating adult common diving petrels Pelecanoides urinatrix urinatrix, grey-faced petrels Pterodroma macroptera gouldii and sooty shearwaters Puffinus griseus Species Weight (g) TDR deployments (n) TDR deployment duration (d) Haematology (n) Common diving petrel 146.9 ± 4.9 15 1–2 21 Grey faced petrel 502.9 ± 16.9 10 30–90 22 Sooty shearwater 847.50 ± 37.6 10 30–60 10 faced petrels and sooty shearwaters (Warham 1977). Haematology and oxygen stores Additionally, dietary differences exist between com- mon diving petrels (crustaceans), grey-faced petrels We employed conventional clinical haematology (fish, cephalopods and crustaceans) and sooty shear- techniques as laid out in Lewis et al. (2006). Blood waters (euphasiids, cephalopods and fish) (Warham samples were obtained from the tarsal vein of incu- 1990). bating birds using a 27 gauge needle and 1 ml Due to natural offsets in breeding phases among syringe. Blood samples (approx. 100 to 250 µl) were species, haematological analyses were undertaken in collected within 4 min of handling the bird and were September 2013 for common diving and grey-faced placed in lithium heparin-lined tubes to prevent coag- petrels, whereas sooty shearwaters were sampled in ulation of the blood. Following this, blood samples December of that year. were immediately analysed for haematocrit (Hct) and red blood cell count (RBCC) with a portion frozen at –20°C for later analysis of haemoglobin concentra- Diving behaviour tion ([Hb]) as in accordance with the methods of Elliott et al. (2010). Hct was analysed in triplicate using mi- Measures of dive behaviour were obtained using crohaematocrit capillary tubes which were spun for LAT1400 (11 × 35 mm, 4.8 g) and LAT1500 (8 × 3 min. Cell counts were made using an improved 32 mm, 3.2 g) TDRs (Lotek Wireless). Tags deployed Neubauer haemocytometer for 6 subsamples of red on common diving petrels were applied with water- blood cells diluted in isotonic saline. Haemoglobin proof tape to small clusters of central back feathers. content of thawed samples was measured spectropho- The tape was further sealed with superglue
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