TY - JOUR
AU - Hamasoto,, Harumi
AB - Abstract We analyzed the nutritional condition and morphological characteristics of wintering Long-billed Murrelets (Brachyramphus perdix) in Japan. These birds were well nourished with an average body mass of 293 g, composed of a mean total body fat of 40.7 g (14%). The fat deposit was equivalent to an average energy reserve of 2.5 days at the estimated energy consumption of 615 kJ day−1 or 2.1 kJ g−1 day−1. Muscle mass consisted mainly of water (73%) and fat-free dry matter (26%), with small amounts of fat. Uropygial glands consisted of 33% fat and 17% fat-free dry matter, with 48% water. Long-billed Murrelets were characterized by large pectoral (26% of fat-free body mass) and small leg muscles (2% of fat-free body mass). We believe that these muscular traits, which contrast with those of alcids breeding at coastal colonies, reflect specific adaptations to inland nesting and long-distance foraging. Condición Nutricional y Características Musculares durante el Período de Invernada de Brachyramphus perdix en Japón Resumen. Analizamos la condición nutricional y características morfológicas durante el período de invernada de Brachyramphus perdix en Japón. Estas aves se encontraron bien alimentadas con una masa corporal promedio de 293 g, compuesta por una media de grasa corporal total de 40.7 g (14%). El depósito de grasa fue equivalente a una reserva energética promedio de 2.5 dias a una tasa de consumo energético estimada en 615 kJ día−1 o 2.1 kJ g−1 día−1. La masa muscular estuvo representada principalmente por agua (73%) y materia seca libre de grasa (26%), con pequeñas cantidades de grasa. Las glándulas uropigiales presentaron 33% de grasa y 17% de materia seca libre de grasa, con un 48% de agua. B. perdix se caracteriza por tener músculos pectorales grandes (26% de la masa corporal libre de grasa) y pequeños músculos en las piernas (2% de la masa corporal libre de grasa). Creemos que estos rasgos musculares, que contrastan con los de aves de la Familia Alcidae que nidifican en colonias en la costa, reflejan adaptaciones específicas para nidificar tierra adentro y forrajear a larga distancia. The wintering ecology of seabirds remains little known due to the difficulties of collecting data even for birds inhabiting coastal waters. The Long-billed Murrelet (Brachyramphus perdix) is a small alcid endemic to the northwestern coasts of the North Pacific, with a world population of only tens of thousands (Konyukhov and Kitaysky 1995). It is an exceptionally difficult species to study in summer because it breeds solitarily in old-growth forests on remote mountainous habitats around the Okhotsk Sea (similar to the closely related Marbled Murrelet [B. marmoratus] of the northwestern coasts of North America). It winters in the coastal waters around central and western Japan (Ornithological Society of Japan 1974), but its wintering ecology remains entirely obscure. Wintering alcids at higher latitudes may metabolize more energy in winter than in summer in order to maintain body heat, and therefore may carry more energy reserves than summer birds (Gaston et al. 1983, 1993, Emslie et al. 1990). Recent studies on field metabolic rates for several species of alcids reveal that during the breeding season alcids metabolize large quantities of energy on a daily basis, varying from relatively low values for large species like Common Murres (Uria aalge; Cairns et al. 1990) and Black Guillemots (Cepphus grille; Mehlum et al. 1993) to high values for smaller species like Least Auklets (Aethia pusilla; Roby and Ricklefs 1986) or Dovekies (Alle alle; Gabrielsen et al. 1991). Because of the high energy expenditure, even large species such as Common Murres are estimated to carry energy reserves for an average of only 1.5 days during the breeding season (Gabrielsen 1994); small species probably carry shorter-lasting energy reserves while breeding. However, little is known of the nutritional ecology of wintering alcids, and nothing is known for Long-billed Murrelets. Recent analyses of nutritional condition of dead, oiled alcids reveal small energy stores and rapid mortality associated with lethal or sublethal oiling that increased energy consumption of birds with oil-soaked plumage (Oka and Okuyama 2000). To help bridge this gap of information on nutritional ecology for wintering alcids, we present the first report on the nutritional status and muscular characteristics of wintering Long-billed Murrelets, through analysis of body composition. Methods We obtained four carcasses of Long-billed Murrelets that drowned accidentally in fixed shore nets set at depths of 3.5–4.0 m in Lake Shinji (35°30′N, 132°56′E), Shimane Prefecture, Japan. Lake Shinji is 79 km2 in area and 6.4 m in maximum depth, and is one of the largest brackish lagoons in Honshu. The winter climate is usually wet and occasionally windy, but air temperature averages 3.8°C and 4.2°C in January and February, respectively (Kira 1995), and the lake never freezes. The four birds were collected on 22 December 1995 (two birds in the same net on the same day), 28 December 1996, and 10 January 1997. There are no observations or specimens for this species for Lake Shinji at any time of the year, but the specimens we studied suggest that the lake may be a favored wintering habitat (Oka 1999) that is shared with a large diving duck community (Oka et al. 1999). The carcasses were frozen until examination. From dissection we ascertained that all four birds were male; one was a juvenile, and the other three were adults (i.e., more than 1.5 years old), based on plumage characteristics (Oka 1999). After measuring weight and body length and examining the plumage, we plucked and dissected the carcasses. The contents of the digestive tract were removed and their mass subtracted from fresh body weight. Wet, dry, and lipid weights were obtained for the whole body, the left pectoral muscles, the liver, uropygial gland, and the marrow of four bones: tibia, femur, humerus, and ulna. These measures are considered effective indexes of the nutritional status of seabirds (Oka and Maruyama 1985, Oka and Okuyama 2000). The pectoral muscle and liver were homogenized using dissection scissors, separately. After removing feathers, head, wing and leg bones, digestive tract, uropygial gland, left pectoral muscle, and liver, the remainder of the carcass was refrozen and then homogenized using a meat grinder. Small samples (about 5 g wet weight) were dried to constant weights in a forced-air oven at about 50°C for 8 hr to determine water content. Lipid was extracted through a FATEX apparatus (Mitamura Riken Co., Tokyo) for 5 hr, using an ethanol-benzene (1:1) solution. Two wing bones and two leg bones were cracked and their marrows were removed by tweezers as completely as possible, before being weighed and dried using the above procedure. Marrow lipid was measured as the difference of values with and without the dry matter. The body lipid reported in this study gives the total extracted from the minced carcasses and removed organs. To evaluate the nutritional condition of murrelets, we converted measured fat reserves to energy reserves. The caloric value of fat was assumed to be 9.3 kcal g−1 (Dargolts 1973) and 1 kcal is equivalent to 4.184 kJ. The daily existence metabolism (DEM) at subzero temperatures (°C) in winter was calculated using the allometric formula reported in Kendeigh et al. (1977): DEM (kJ g−1 day−1) = 17.719W0.5316, where W is bird body weight in grams. DEM is the sum of basal metabolism, costs of thermoregulation, digestion, and limited locomotor activity excluding aerial and underwater flights. As time budgets have never been reported for murrelets, we assumed that 4 of the 10 diurnal hours available at the lake during midwinter were spent on aerial and underwater foraging flights. To estimate the costs of foraging, we calculated the energy requirement of costly flapping flight (ERF) using the allometric formula reported in Furness and Cooper (1982): ERF (kJ g−1 hr−1) = 1.4W0.67, where W is bird body weight in grams. This value was added to DEM to produce an estimate of total daily energy expenditure. Means are presented ± SD. We compared body mass of our murrelet specimens to murrelets collected in Okhotsk, Russia (Konyukhov and Kitaysky 1995), using an unpaired two-tailed t-test with α = 0.05. Results Body, Muscle and Internal Organ Masses All four murrelets had empty stomachs, even though they were killed in the course of diving activity. Mean body weight was 293.3 ± 23.2 g (range 263.8–319.5 g; Table 1). This was similar to two mean weights of murrelets from the Okhotsk (295.8 g, range 258–357 g, Shibaev 1990, sex and sample size not reported; and 287.0 ± 41.7 g, range 258.0–358.0 g, n = 5, Konyukhov and Kitaysky 1995; t7 = 0.27, P = 0.79). Our four murrelets were somewhat lighter than three other adult specimens (possibly with some digestive tract contents) in the bird collection at the Yamashina Institute for Ornithology: a 300-g male (specimen 14319–51) and a 319-g female (specimen 14319–52), both collected in Tokyo Bay on 25 January 1953; and a 325-g female (specimen 82–0217) collected in Abashiri Bay, Hokkaido, on 25 August 1982. Table 1. Body and organ masses and tissue composition of four male Long-billed Murrelets wintering in Lake Shinji, Japan. FFDM = fat-free dry matter Open in new tab Table 1. Body and organ masses and tissue composition of four male Long-billed Murrelets wintering in Lake Shinji, Japan. FFDM = fat-free dry matter Open in new tab The murrelets had large pectoral muscles and small leg muscles (Table 1). Right and left pectoral and leg muscle masses constituted 23% and 2%, respectively, of total body mass. The small leg muscle mass of the murrelets corresponds to their distinctively short leg bones (tarsus 17.9 ± 0.6 mm, femur 26.1 ± 0.2 mm, tibia 41.7 ± 0.6 mm). The mean ratios of fat-free muscles to fat-free body mass were 26 ± 1% for pectoral muscles and 2.4 ± 0.1% for leg muscles. On average the liver weighed 15.9 g (5% of body mass), the heart weighed 5.6 g (2% of body mass), and the uropygial gland weighed 0.6 g (0.2% of body mass). Fat Reserves The murrelets were in good nutritional condition, storing a relatively large total fat reserve (40.7 ± 16.4 g; range 29.8–65.1 g), which was equivalent to a mean 14 ± 5% of total body fat (range 10–20%, Table 1). Large muscles and organs contained little fat (mean 3% by weight in muscle and 3% in liver, Table 1). Whole pectoral and leg muscles contained 2.4 g fat, or 6% of the whole body fat. The liver contained 0.5 g fat, or 1% of whole body fat. Fat was also concentrated in some small organs: mean 33% in uropygial gland, 54% in humerus marrow, and 53% in the ulna marrow. Leg bone marrow contained a much smaller proportion of fat (mean 8% in tibia and 4% in femur), but may have been incompletely extracted from the dried matter. The uropygial gland and marrow of four bones contained 0.2 g fat respectively, each equivalent to 0.5% of whole body fat. Marrow lipid was oil rather than solid fat. Although we did not measure the fat contained in other organs, fat deposits in these were considered to be small. The remaining 37.4 g of fat, equivalent to 92% of the whole fat deposit, was mainly stored subcutaneously and in the abdominal region. The pectoral muscle and liver contained similar proportions of water (mean 73% in pectoral muscle and 71% in liver) and lipid-free matter (mostly protein; mean 26% in pectoral muscle and 28% in liver). The uropygial gland and leg bone marrow also contained similar, though smaller, proportions of water (mean 48% in uropygial gland, 45% in tibia, and 47% in femur marrow). Wing bone marrow contained less water than leg bone marrow (mean 24% in humerus and ulna marrow, each); these proportions were similar to wing bone lipid-free matter (mean 21% and 22% in humerus and ulna marrow, respectively). Using the DEM equation, murrelets were calculated to have a mean daily basal energy consumption of 362.9 ± 15.4 kJ day−1 (range 343.2–380.0 kJ day−1) or 1.24 ± 0.05 kJ g−1 day−1 (range 1.19–1.30 kJ g−1 day−1). Using the ERF equation, birds were calculated to have a mean energy demand of 63.0 ± 3.4 kJ hr−1 (range 58.7–66.7 kJ hr−1) or 0.21 ± 0.01 kJ g−1 hr−1 (range 0.21–0.22 kJ g−1 hr−1). In total they consumed 614.7 ± 28.8 kJ day−1 (range 577.9–646.8 kJ day−1) or 2.10 ± 0.07 kJ g−1 day−1 (range 2.02–2.19 kJ g−1 day−1). Thus, without any foraging activity, fat reserves would be consumed in a mean of 4.3 ± 1.5 days (range 3.2–6.7 days), assuming the murrelets were dependent solely on fat reserves, as the energy generated from glycogen and protein is small (Klasing 1998). With four hours of foraging activity per day, fat reserves would last a mean of 2.5 ± 0.9 days (range 1.9–3.9 days). Discussion Because the weights of Long-billed Murrelets wintering in Lake Shinji were similar to those of specimens collected from the Okhotsk Sea, their main habitat, they likely represent the normal nutritional condition for this species. Dry weights and water content of the marrow represent good indices of the physical condition of birds, except for egg-laying females (Oka and Maruyama 1985). The low water contents of the murrelets' marrow indicate they were in good nutritional condition. They carried on average 14% body fat, which could last them 4.3 days at a minimum existence metabolism or 2.5 days allowing for four daily hours of foraging activity. The latter estimate of the duration of fat reserves is 0.5 day shorter than the 3 days estimated for wintering Thick-billed Murres in peak condition (Gaston et al. 1983) and a full day longer than the 1.5 days estimated for breeding Common Murres (Gabrielsen 1994). The average existence requirement for Long-billed Murrelets is higher than the basal metabolic value found for Common Murres (0.4 kJ g−1 day−1; Cairns et al. 1990). The average daily energy consumption for the wintering murrelets is similar to the field metabolic values for large alcids such as Common Murres (1.9–2.1 kJ g−1 day−1; Cairns et al. 1990, Gabrielsen 1994), and is much smaller than those for several midsize to small alcids during the chick-rearing period: 2.3 kJ g−1 day−1 for Black Guillemots (380 g; Mehlum et al. 1993), 4.2 kJ g−1 day−1 for Dovekies (164 g; Gabrielsen et al. 1991), and 4.3 kJ g−1 day−1 for Least Auklets (83 g; Roby and Ricklefs 1986). Diving activity is probably highly expensive energetically as has been reported for diving ducks (Lovvorn 1994, de Leeuw 1996). Our value for daily energetic expenditure is probably underestimated because we did not calculate energy consumption for costly underwater foraging flight separately from aerial foraging flight. Thus in effect, wintering Long-billed Murrelets may carry energy stores sufficient for no more than a day or two. Under this nutritional condition, in case of oil spillage in winter, oiled murrelets would die very quickly due to enormous drain of thermal energy that must be counteracted with increased metabolism. Because body weight changes with the amount of fat reserve, the fat-free weight rather than the total weight becomes a better index of mass variation between species. Fat-free pectoral muscles (26% of fat-free body mass) of Long-billed Murrelets are larger than those of Rhinoceros Auklets (20%, calculated from Oka and Okuyama 2000) and those of Ancient Murrelets (17%, Oka and Hamasoto unpubl. data). Conversely, fat-free leg muscles (2% of fat-free body mass) of Long-billed Murrelets are smaller than those of Rhinoceros Auklets (Cerorhinca monocerata; 6%, calculated from Oka and Okuyama 2000) and those of Ancient Murrelets (4%, Oka and Hamasoto unpubl. data). These muscular features correspond to bone lengths: long wing bone and short leg bone proportions in Long-billed Murrelets, and short wing bone and long leg bone proportions in Rhinoceros Auklets and Ancient Murrelets (Oka unpubl. data). The latter two species breed mainly in burrows on small islands. In contrast, Long-billed Murrelets have the remarkable habit of flying to nests in trees, often far inland (up to tens of km from the sea, Nechaev 1995, Konyukhov and Kitaysky 1995). The closely related Marbled Murrelet also breeds far inland (up to 100 km) in trees or on the ground in alpine areas (Nelson 1997). In the fjords of southeastern Alaska, radio-marked Marbled Murrelets flew up to 250 km round trip from nests to foraging areas at sea, but most of this distance was over water (Whitworth et al. 2000). Marbled Murrelets fly at high speeds (mean 77 km hr−1, maximum 104 km hr−1; Hamer et al. 1995). The large pectoral muscles of the similar Long-billed Murrelet facilitate long flights to inland breeding locations and, in winter, may facilitate southern dispersal movements, searches for winter prey, and wing-propelled underwater foraging. Small leg muscle mass most likely reflects the reduced ambulatory ability of inland- or tree-nesting Long-billed Murrelets compared to ground-nesting alcids, but may also influence underwater foraging. Skeletal features such as short leg and long wing bones may have evolved in response to their selection of inland breeding sites, as shown in Marbled Murrelets (Storer 1945). We are grateful to M. Yamamuro and J. Hiratsuka for providing net-drowned murrelets in Lake Shinji. We are much obliged to H. R. Carter and J. F. Piatt for valuable comments on the manuscript and to G. W. Gabrielsen for his sending us his literature on seabird energetics. Literature Cited Cairns , D. K. , W. A. Montevecchi , V. L. Birt-Friesen , and S. A. Machko . 1990 . 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TI - Nutritional Condition and Muscular Features of Wintering Long-Billed Murrelets in Japan
JF - Condor: Ornithological Applications
DO - 10.1093/condor/103.4.874
DA - 2001-11-01
UR - https://www.deepdyve.com/lp/oxford-university-press/nutritional-condition-and-muscular-features-of-wintering-long-billed-vMmScnMzgO
SP - 874
VL - 103
IS - 4
DP - DeepDyve
ER -