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Gouldian finch metabolic data for Buttemer et al. 2021 jeb242577

Citation

Buttemer, William (2021), Gouldian finch metabolic data for Buttemer et al. 2021 jeb242577, Dryad, Dataset, https://doi.org/10.5061/dryad.51c59zw8r

Abstract

Evidence from a number of species suggests behaviours associated with social rank are positively correlated with metabolic rate. These studies, however, are based on metabolic measurements of isolated individuals, thereby ignoring potential effects of social interactions on metabolic rates. Here, we characterised three pertinent metabolic indices in the two predominant genetic colour morphs of the Gouldian finch (Erythrura gouldiae): diurnal resting metabolic rate (RMR), nocturnal basal metabolic rate (BMR), and exercise-induced maximal metabolic rate (MMR). Research reveals red-headed morphs consistently dominate the less aggressive black-headed morphs and the two morphs to differ in other behavioural and physiological traits. We measured daytime RMR of intermorph naïve birds (first-year virgin males maintained in total isolation from opposite colour morphs) and their metabolic responses to viewing a socially unfamiliar bird of each colour. Subsequently, each bird was placed in a home cage with an opposite colour morph (intermorph exposed) and the series of measurements repeated. Daytime RMR was indistinguishable between the two morphs, whether intermorph naïve or intermorph exposed. However, both red- and black-headed birds showed a greater short-term increase in metabolic rate when viewing an unfamiliar red-headed bird than when seeing a black-headed bird, but only when intermorph naïve. Measurements of BMR and exercise-induced MMR did not differ between the two morphs, and consequently aerobic scope was indistinguishable between them. We propose that the suite of behavioural differences between these two sympatric morphs are functionally complementary and represent evolutionary stable strategies permitting establishment of dominance status in the absence of metabolic costs.

Methods

Animals and experimental design

We used 24 black-headed and 24 red-headed captive-reared wild-type male Gouldian finches. Birds had been raised by parents of the same colour and, upon fledging, were housed alone in complete social isolation (Pryke et al. 2007). While in seclusion and prior to experiments, juveniles transitioned from the drab grey/olivaceous immature plumage common to both morphs to the brightly coloured adult plumage of their male parent. Two cohorts of first-year virgin males were studied (one in 2007 and one in 2009); both involved 12 intermorph naïve birds of each colour morph. Upon arrival at the University of Wollongong, visual isolation of the two colour morphs was maintained by partitions between cages. Birds of the same colour morph were placed 2 per cage (34 cm × 45 cm × 45 cm; Hoei Cage Co., Japan). Cages were fitted with multiple perches and one dispenser each for commercial finch seed (Golden Cob, Mars Birdcare Australia), mineralised grit, and water, all available ad libitum. Individuals of both cohorts remained with their initial cage partners for two weeks before metabolic measurements commenced.

Experiment 1: Metabolic response to viewing a socially unfamiliar bird of each colour morph

Phase 1: All birds intermorph naive

This involved two sets of metabolic measurements that took place on consecutive days (Tests 1 and 2), with Test 1 involving a pair of birds of the same or opposite colour morphs; for Test 2 each bird was exposed to a morph of the opposite colour of that viewed in Test 1. Experimental pairs were randomly selected from all birds other than either bird’s cage partner. The sequence in which each bird viewed the same or opposite colour morph was varied among birds to balance morph colour combinations for Tests 1 and 2.

Phase 2: All birds intermorph exposed

Upon completion of Phase 1, birds were transferred to cages containing an individual of the opposite colour morph for five days. Subsequently, two sets of metabolic measurements (Tests 3 and 4) were made on consecutive days (we define these individuals as ‘intermorph exposed’). As in Phase 1, the sequence in which each bird viewed the same or opposite colour morph to itself on consecutive days was varied among all birds to balance morph colour combinations for Tests 3 and 4.

Experiment 2: Relation between colour morphology and aerobic scope in intermorph exposed birds.

Birds from the 2009 cohort were placed as mixed morph groups in outdoor flight cages (2.5 m × 3 m × 4 m, 12 birds per cage) following completion of Experiment 1. Cages had multiple feeding sites, extensive perching locations, and shelter from weather. After at least 4 days in aviaries, individuals were collected about mid-morning through midday to measure exercise-induced maximal metabolic rates (MMR). Upon completing MMR measurements, birds were placed in individual holding cages with free access to food and water. The following day, food was removed three hours before initiation of nocturnal measurements of basal metabolic rate (BMR). 

Metabolic Measurements

Experiment 1

We measured resting metabolic rate (RMR) during the day using an open-circuit respirometry system that allowed us to continuously monitor two metabolic chambers simultaneously. For a given metabolic series (Tests 1 through 4), birds were removed from holding cages, had body mass (Mb) measured on a digital scale (±0.01g; Model OHAUS AV413C), and then placed individually in 1.5l chambers fashioned from sealable polycarbonate plastic food containers. Chambers were optically transparent, rectangular, and fitted with a perch at 1/3 height, as well as inlet and outlet tubes for airflow. The chamber containing the first bird was positioned in the constant-temperature cabinet and then screened with an opaque partition before positioning the second bird’s chamber within 2 cm of one another. The perches were oriented perpendicularly to the partition, resulting in mutual viewing irrespective of perching location. Overhead fluorescent lighting within the temperature-controlled cabinet illuminated the birds evenly and a webcam was used to monitor behaviour.

Cabinet temperature was regulated at 30°C, which is within the thermoneutral zone for Gouldian finches (Burton and Weathers, 2003). Mass-flow controllers (Mykrolis, model FC-2902V-T) provided a constant air supply of 500 ml min–1 STP of dry air into each metabolic chamber. The outflows of each chamber and sequential sampling of inlet air were subsampled (approximately 100 ml min–1). Subsampled air was passed through Drierite and soda lime to remove water and CO2, respectively, en route to a two-channel O2 analyser (Oxilla II; Sable Systems International; Henderson, NV, USA). We used LabHelper software (warthog.ucr.edu) to control the multiplexer outputs and read chamber O2-concentration at 1-sec intervals. We used LabAnalyst (warthog.ucr.edu) to correct oxygen readings for drift between consecutive baselines and to calculate O2 consumption rates ( O2, ml min-1) according to Eqn. 2 of Hill (1972).

Oxygen consumption was recorded continuously after closure of the cabinet door. Video monitoring showed that birds usually settled within a few minutes, and their metabolic rates declined steadily, reaching a plateau about 30 to 60 min after door closure. About 10 min after both birds exhibited a stable RMR, the partition was lifted so birds could see one another, and  O2 was recorded for a further 60 minutes. Resting MR (RMR) was identified as the lowest 3-min running mean  O2 recorded over the entire measurement period. This duration was selected as birds tended to be restive under full illumination and periods of sustained rest levels of metabolic rate rarely exceeded 5 min. Peak MR (MRpeak) was designated as the highest 3-min running mean  O2 recorded after the partition was lifted. These measurements were used to evaluate the maximum factorial increase in MR associated with birds viewing one another, which we calculated as MRpeak/RMR. The average  O2 over the entire 60-min period that birds viewed one another was designated as MRmean.

Experiment 2

Procedures used for measuring basal (BMR) and exercise-induced maximal metabolic rates (MMR) are described in detail elsewhere (Buttemer et al. 2019). In brief, for MMR tests, birds were collected from the flight cages and placed individually in a hop-flutter wheel which was rotated to elicit maximal oxygen consumption during exercise. Rotation speed was dynamically adjusted to each bird’s pattern of movement to achieve maximal activity until they exhibited exhaustion. Data were adjusted with ‘instantaneous’ conversion procedures to account for gas mixing characteristics of the wheel and accurately resolve short-term changes in  O2 (Chappell et al. 1999; Buttemer et al. 2019). The peak 30-sec instantaneous rate of  O2 during exercise was designated as MMR. Following MMR tests, birds were placed in holding cages (2 birds per cage) with free access to food and water. BMR tests were performed on these birds the following evening, with food removed from their holding cages three hours prior to measurements. Birds were placed in 2-l metal metabolic chambers for overnight measurements of  O2 under thermoneutral conditions (30°C) in total darkness. BMR was calculated as the minimum 5-min running average  O2 over the entire night; BMR obtained using this averaging interval was significantly repeatable in another study of similar-sized passerine birds (Careau et al. 2014a).

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Funding

Australian Research Council, Award: LP0667562