Nocturnal torpor by superb fairy-wrens: a key mechanism for reducing winter daily energy expenditure

Abstract

Many passerine birds are small and require a high mass-specific rate of resting energy expenditure, especially in the cold. The energetics of thermoregulation is, therefore, an important aspect of their ecology, yet few studies have quantified thermoregulatory patterns in wild passerines. We used miniature telemetry to record the skin temperature ( T skin ) of free-living superb fairy-wrens ( Malurus cyaneus , 8.6 g; n = 6 birds over N = 7–22 days) and determine the importance of controlled reductions in body temperature during resting to their winter energy budgets. Fairy-wrens routinely exhibited large daily fluctuations in T skin between maxima of 41.9 ± 0.6°C and minima of 30.4 ± 0.7°C, with overall individual minima of 27.4 ± 1.1°C (maximum daily range: 14.7 ± 0.9°C). These results provide strong evidence of nocturnal torpor in this small passerine, which we calculated to provide a 42% reduction in resting metabolic rate at a T a of 5°C compared to active-phase T skin . A capacity for energy-saving torpor has important consequences for understanding the behaviour and life-history ecology of superb fairy-wrens. Moreover, our novel field data suggest that torpor could be more widespread and important than previously thought within passerines, the most diverse order of birds.

Heterothermy in a Small Passerine: Eastern Yellow Robins Use Nocturnal Torpor in Winter

“…The magnitude of nocturnal T s drop during torpor increased with decreasing mean and minimum T a . This relationship was previously found in other passerine species (Reinertsen and Haftorn, 1983;Nord et al, 2009Nord et al, , 2011Romano et al, 2019) and supports the assumption that the controlled reduction of T s aims to conserving energy during energetically expensive periods, (Reinertsen and Haftorn, 1984)]. Captive noisy miners Manorina melanocephala reduced metabolic rate by ∼40% when they were measured under T a s of 0-15 • C, with a T b drop of only 4 • C (Geiser, 2019).…”

“…To deal with these energetic costs, many endothermic species use torpor, a controlled reduction in metabolism and typically T b (Namekata and Geiser, 2009;Ruf and Geiser, 2015). Torpor is used as a strategy to overcome energetically challenging periods such as cold (Maddocks and Geiser, 2007;Romano et al, 2019;Wolf et al, 2020), reduced food/water or foraging opportunities (Nicol and Andersen, 1996;Nord et al, 2009;Smit et al, 2011) or even hot conditions (Reher and Dausmann, 2021), and its use varies considerably among avian taxa (Geiser, 2021). Some evidence of intra-specific variation in torpor patterns along latitudinal or elevation gradients (Geiser and Ferguson, 2001;Dunbar and Brigham, 2010;Zervanos et al, 2010;Stawski and Geiser, 2011) suggests that T a may play a major role in torpor expression in passerines, but only little information on geographical variation is available for birds (Chaplin, 1976;Sharbaugh, 2001).…”

“…To date, only two passerine species studied in the wild have been shown to express torpor. The T b of noisy miners (Manorina melanocephala) fell by 7 • C on average, to a minimum of 33 • C during winter in eastern Australia, where night time temperatures frequently drop to near 0 • C (Geiser, 2019), and fairy wrens (Malurus cyaneus) dropped their skin temperature (T s ) by over 14.5 • C, with minimum T s of 27.4 • C recorded at average minimum T a of about 3 • C (Romano et al, 2019). Other passerines species which were studied in the wild remained euthermic, even during challenging conditions [e.g., red-headed finch Amadina erythrocephala (Mckechnie and Lovegrove, 2003), five species of tropical montane passerines (Burnett et al, 2019), willow tit Parus montanus (Reinertsen and Haftorn, 1984), bronze mannikins Spermestes cucullatus (Lovegrove and Smith, 2003), great tits Parus major (Nilsson et al, 2020), blue tits Cyanistes caeruleus (Nord et al, 2009)].…”

Seasonal Expression of Avian and Mammalian Daily Torpor and Hibernation: Not a Simple Summer-Winter Affair†

“…Captive passerine sunbirds (Nectarina famosa) from South Africa enter nocturnal torpor in summer when exposed to low T a (Downs and Brown, 2002) suggesting that torpor may also be used at other times of the year. Free-ranging noisy miner (Manorina melanocephala) expressed frequent, shallow nocturnal torpor from autumn to early spring (Geiser, 2019) and fairy wrens (Malurus cyaneus) in winter, other seasons were not examined (Romano et al, 2019).…”

Response to ‘No evidence for hibernation in rockwrens’

“…Although less serious than problems of methodology and inference, most of the thermal energetics citations are out of date and recent thermal biology studies on free-ranging passerines are missed. For example, Romano et al (2019) reported that Australian fairy-wrens (Malurus cyaneus) reduce skin temperature by approximately 14°C from 41 to 27°C, followed by endogenous rewarming. The one recent study on babblers (Pomatostomus superciliosus) that is cited is misreported.…”