what is the normal body temperature of birds

The thermal physiology of most birds and mammals is characterised by considerable spatial and temporal variation in body temperature. Body temperature is, therefore, a key parameter in physiological, behavioural and ecological research. Temperature measurements on freely moving or free-ranging animals in the wild are challenging but can be undertaken using a range of techniques. Internal temperature may be sampled using thermometry, surgically implanted loggers or transmitters, gastrointestinal or non-surgically placed devices. Less invasive approaches measure peripheral temperature with subcutaneous passive integrated transponder tags or skin surface-mounted radio transmitters and data loggers, or use infrared thermography to record surface temperature. Choice of technique is determined by focal research question and region of interest that reflects appropriate physiological or behavioural causal mechanisms of temperature change, as well as welfare and logistical considerations. Particularly required are further studies that provide opportunities of continuously sampling from multiple sites from within the body. This will increase our understanding of thermoregulation and temperature variation in different parts of the body and how these temperatures may change in response to physiological, behavioural and environmental parameters. Technological advances that continue to reduce the size and remote sensing capability of temperature recorders will greatly benefit field research.

The thermal physiology of vertebrates can be broadly classified by their stability in body temperature and source of body heat [1]. Ectotherms are most commonly poikilothermic where body temperature tracks environmental temperature, allowing thermal tolerances across a wide range of temperatures [2, 3]. Endothermy is the maintenance of a high and relatively constant homeothermic body temperature through high metabolic heat production that appears to have evolved separately in avian and mammalian lineages [4]. Core temperature in birds ranges between 34 and 44 °C, scaling with body size in some groups. Mammalian core temperature varies between 30 °C in the monotremes and as high as 40 °C in other groups [5]. However, many species of both mammals and birds are regionally or temporally heterothermic, with variable endothermic heat production and a body temperature that is not regulated within a narrow range [1, 6].

Common to all these groups, body temperature is a key physiological parameter that provides important insights into the study of thermoregulation, physiology and behaviour or responses to environmental change [7, 8]. However, while the ectotherm to endotherm continuum is useful for broadly describing the mean physiological state of an organism, this may mask our understanding of the dynamic nature of thermoregulation. The complex control of body temperature in endotherms occurs through autonomic regulation of blood flow in combination with a number of processes including shivering and non-shivering thermogenesis, panting or sweating and by a range of thermoregulatory behaviours [1, 9]. It is a common misassumption that there exists a standard reference core or deep body temperature for each species and each individual [10]. The temperature of any anatomical region is a product of metabolic heat production and blood flow within that region, including the rate of heat lost from physical processes [10]. Confusingly rectal or cloacal temperature is often used synonymously with the terms core or deep body temperature and not surprisingly considerable research effort has been invested in cross-validation of techniques to measure these respective temperatures [11–14]. Therefore, for any study involving body temperature measurement it is important to understand the spatial variation and differential regulation in temperature within the body and how the temperature of different body regions may change with time and environmental context. Here, the term core temperature is used throughout to describe the homeostatic temperature within the centre of the body.

Accordingly, the first step in deciding which technique to use when sampling temperature from an animal is to determine which body region is suited to answer the research question and on what timescale measurements are required. Precision and response time of the sensor should be chosen to reflect the rate of change of temperature at that site. However, choice of measurement sites may be constrained by the extent to which invasive methods are appropriate for the study species.

This review is aimed at researchers wishing to undertake body temperature measurements on freely moving or free-ranging birds and mammals. In particular, the merits of a range of techniques that are suited to studies of animals in the wild are considered (Table 1). This is intended to help researchers choose the most appropriate technologies and complements previous reviews that have focused either on single techniques [15–17] or have examined body temperature measurement in particular taxonomic groups [10, 18, 19]. The current review compares techniques that measure core and peripheral temperature and discusses calibration, analytical approaches and future instrument design.

Rectal or cloacal temperature is commonly measured using thermometry. This fast, affordable, and minimally invasive method relies on inserting a thin temperature-sensitive probe into the rectum via the anus or cloaca [20–22]. It is commonly undertaken using thermocouples or thermistors either custom adapted for use or using standard medical or veterinary thermometers. Oesophageal temperature may also be taken in this way [23]. Thermometry has wide applicability in ecology, and has been used for example to record functional thermoregulation in relation to climatic variables, immune function, natural occurrence of pathogen infection and when studying the ontogeny of thermoregulation [20, 24–27]. While highly accurate and repeatable [20], thermometry generally only provides a cross-sectional temperature sample, because subjects must be captured and handled during sampling. The stress of capture and indeed the temperature measurement itself can bring about stress-induced hyperthermia (SIH) mediated by the sympathetic adrenal and the hypothalamic–pituitary–adrenal (HPA) axes, as well as through increased metabolic heat production associated with the escape response [28, 29]. Therefore, the time from capture to measurement should be as rapid as possible, particularly for small animals. For example, measurement of rectal temperature in mice typically results in an increase of 0.5–1.5 °C in 10–15 min [23] and is associated with peripheral cooling at the surface through vasoconstriction [30]. Thermometry is, therefore, inappropriate for studying functional body temperature responses or longitudinal patterns in body temperature regulation in free-ranging or free-moving animals. This problem can be partly remedied by physically attaching one or several thermocouples by leads to different body regions to allow for continuous body temperature recordings (Nord and Folkow, unpublished data) or by connecting temperature sensors to an externally mounted radio transmitter [31]. However, physical attachment is a viable option only for inactive, or relatively inactive animals or when contained in a confined space (such as a metabolic chamber or a roosting cavity) where thermocouple wiring can be adjusted to confinement size and animal movement is relatively small. Stress from having the thermocouple attached may also bias the temperature reading (Esa Hohtola, pers. comm., see also [32]). Regardless of such shortcomings, thermometry remains an inexpensive, fast, and attractive method for body temperature recording, especially when cross-sectional data are desirable and subjects can be caught and measured with relative ease. With larger animals, measurements of blood and muscle temperature may be made by percutaneous insertion of a thermistor via a catheter and temperature logged with a surface-mounted recorder [33–35]. This allows for continuous monitoring of body temperature while animals are exhibiting natural behaviours but requires recapture of the animal for removal of instrument.

One indirect thermometry method of estimating rectal temperature is to measure the temperature of newly defecated faeces [36]. This technique has recently been applied to body temperature measurement by careful calibration of the rate of temperature change following defecation [37]. However, it is likely to have limited applicability by the fact that it only provides single time point measurement and will be strongly influenced by changes in environmental conditions.

Intra-peritoneal (and sometimes also intra-abdominal) implants are commonly used when continuous long-term body temperature profiles are desirable, such as when studying the functional characteristics of thermoregulation. Implantable temperature-sensitive devices have been used for this purpose in a wide range of species (see references in [17]), and have provided considerable insights into the thermal biology of a large number of free-ranging animals. The devices basically come in two forms; data loggers and radio transmitters. Common to all implants is the need for surgery, which requires anaesthesia. Sedation itself is often unproblematic, but mortality may occur despite proper dosage [38] so care must be taken to monitor vital signs and provide post-surgical recovery. Although surgical implantation is logistically demanding, it has been successfully used on wild animals by either transporting animals to temporary surgical facility [39] or directly undertaking surgery in the field [40]. Implantation of devices may actually be preferable to externally attached loggers in long-term studies [41].

Most data loggers integrate a thermistor, a real-time clock, and an internal memory for storing temperature, time and date at a user-defined interval. Temperature sensors may be held within the body of the logger but where more rapid response rates are required these can be mounted on external leads or on the surface of the instrument [42]. Data loggers are invaluable when recording long-term body temperature profiles and are often combined with heart rate loggers [43–45]. Logger weight considerations can constrain use of many commercially available data loggers on small species. For example, Thermocron iButtons (Dallas Semiconductor, Sunnyvale, CA, USA), which are amongst the smallest available data loggers, weigh approximately 3 g in their standard format. However, iButtons can be remodelled for a 50 % weight reduction [17] and water proofing [19], which allows for measurements on considerably smaller subjects (?30 g).

Implanted data loggers are, therefore, particularly suited to long-term deployments. Examples of these include studies on thermoregulation [42, 43], circadian rhythms [39, 46–48], hibernation and torpor [40, 49, 50], temperature change during diving and foraging [43, 51, 52], incubation [53], egg laying in monotremes [54] and comparison between wild and captive species [47, 55]. One disadvantage with data loggers is that animals must normally be recaptured for data retrieval, which can be difficult or even impossible for some species. Technological solutions have been developed to remedy this, for example using UHF transmission of temperature data to a telemetry collar that can then transmit data by VHF [56] or implanted archive tags on pinnipeds that float to the sea surface and transmit data by satellite when the animal dies [57].

Animals implanted with radio temperature transmitters do not require recapture as data are transmitted continuously, and in general the small size does not impose weight constraints. However, the applicability of radio transmitters can be constrained by battery life and signal strength is sometimes compromised in structurally complex habitats. In addition, transmitters do not have internal storage capacity, which requires manual recording of signal pulse rate or the purchase of automated recording equipment [58]. Care must, therefore, be taken when tracking animals to ensure that disturbance does not disrupt natural behaviours. Automated recording systems provide a solution to this problem, allowing recording of multiple individuals where good signal transmission is possible but will obviously be constrained by range size and habitat complexity for some species. Regardless of such potential shortcomings, radio transmitters continue to provide an effective option for remote recording of body temperature in free-ranging animals over relatively long time periods [50, 59–62].

Ingestion of radio-telemetry pills or miniaturised data loggers allows a relatively non-invasive method of measuring internal temperature. These devices record temperature during passage through the gastrointestinal tract and have been used widely on relatively large species and in humans [10, 63, 64]. Recording duration is determined by gut passage rate, which may vary from hours to weeks but in large ruminants devices have been retained for up to 4 years (retention time was actually improved by increasing the size of the device) [56]. The extent to which gastrointestinal temperature reflects core temperature is dependent on food ingestion and subsequent digestion (and fermentation in the case of ruminants). The temperature recorded may be filtered to account for these processes and thereby provide informative longer term recording of core temperature [56]. Radio-telemetry pills have the advantage that temperature can be recorded externally and do not require recovery of the pill. Systems that provide a combination of radio-telemetry and data logger output have been custom built for this purpose [56, 64]. By far the greatest application of gastrointestinal sensors in wild species has been to detect feeding events in marine endotherms, to which these devices are especially appropriate as the stomach temperature of these animals drops temporarily during the ingestion of cooler ectothermic prey [65–67]. The location of the temperature sensor in the stomach will affect the likelihood that ingested prey comes into contact with the sensor [65, 68]. Thermistor pills can either be gently pushed through the oesophagus via a flexible silicone intubation tube under anaesthesia or fed to the studied animal inside a refrigerated prey during captive experiments. Recorded temperature measurements are stored in the device and retrieved through stomach flushing at the end of experimentation, e.g. after about 10 days for captive seabirds [69]. Measured stomach temperatures of free-ranging species are transmitted to an external logger placed on the back of the animals that is subsequently retrieved. More recently signals from temperature sensors are monitored by satellite transmitters and data are directly relayed through the Argos Data Collection and Location System [70]. Stomach temperature sensors have also been used in conjunction with other temperature loggers to examine physiological processes such as hypothermia [71] and the heat increment of feeding [72]. More recently, stomach temperature sensors have been identified as a promising method to study the suckling behaviour and the transition to nutritional independence of pinnipeds [73, 74].

Take a Dip Image:

Cool water helps birds regulate their body temperatures.

Did you know? Birds, like mammals, are warm-blooded. This implies that they generate heat from their own bodies rather than depending on their environment. Indeed, certain untamed avian species in your backyard, such as blue jays and robins, produce so much heat internally that their typical body temperatures can reach 109 degrees Fahrenheit, or 42 degrees Celsius!

Fortunately, birds have some reliable ways to avoid overheating. A quick soak is one of the best ways for birds to stay cool. Their feathers’ moisture allows heat to leave their bodies quickly. When the heat gets too intense, backyard birds can find refuge in fountains, birdbaths, and other water features.

How Do Birds Handle the Heat?

Imagine it’s hot, and you’re trying to stay cool. Imagine trying to beat the heat without access to air conditioning, an ice-cold pitcher of lemonade, or even the capacity to perspire.

Welcome to the life of a bird.

It seems impossible to humans, but for birds, it’s part of the job. From scorching deserts to freezing oceans, birds have developed incredible methods for regulating their body temperatures. Some species modify their behavior when extreme weather hits. Others take advantage of unique natural adaptations. (After all, plenty of avian species can trace their evolutionary history to eras when global temperature averages were much higher. So maybe all that dinosaur blood coursing through their veins is helping?)

Check out some of the incredible ways birds combat the heat:

Wading birds, like scarlet ibises, use their long, thin legs as a means of staying cool.

Wading birds, such as flamingos and ibises, have long, thin, featherless legs that make it easy to release heat from their bodies. When the blood circulates up and down their legs, heat dissipates through their skin. This natural method of thermoregulation gets a boost when the birds’ feet are submerged in cool water. (It even works in reverse! Watch how flamingos at the Smithsonian’s National Zoo use hot water to stay warm in winter.)

Non-surgical methods for measurement of internal temperature

When it may not be feasible to surgically implant temperature sensors, some innovative techniques have been employed to measure internal body temperatures. Aural temperature [77], vaginal [76], and rectal [75] data loggers are a few examples of these. These methods are particularly helpful for large species where subjects can be recaptured, and they may be appropriate for relatively short time periods (days to weeks).

Peripheral blood circulation and body insulation regulate temperature at the periphery, which can be subcutaneous or at the skin’s surface. Environmental elements like wind speed and ambient temperature also have an impact. Changes in skin surface temperature may be closely correlated with internal temperature for small animals (whose bodies are usually too small to maintain a regulated core-to-shell temperature gradient) [18, 58, 78, 79]. However, as body size increases, peripheral temperature is typically not a reliable indicator of core temperature [80, 81]. These elements are crucial to take into account when determining whether peripheral temperature measurement is appropriate for a particular project or research question.

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