Guidelines for the instrumentation of wild birds and mammals

Animal Behaviour 78 (2009) 1477–1483

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Commentaries

Guidelines for the instrumentation of wild birds and mammals Ruth M. Casper* Wildlife Advisory Panel, University of Tasmania Animal Ethics Committee

a r t i c l e i n f o Article history: Received 29 July 2009 Initial acceptance 28 August 2009 Final acceptance 14 September 2009 Available online 16 October 2009 MS. number 09-00507R Keywords: animal behaviour animal welfare biologging ethics telemetry

Attaching electronic devices to wild animals to acquire behavioural data is becoming increasingly more widespread. Birds and mammals are the most common taxa instrumented, with devices usually designed to store or transmit information relating to movement patterns. The electronic devices most often used are radiotransmitters, platform transmitter terminals, geolocation positioning system loggers and depth loggers. These are generally attached to animals externally using glues, collars or harnesses, or are implanted internally. It is recognized that negative effects associated with instrumentation cannot be completely avoided. This is because handling alone is likely to cause some stress to wild animals and also because some energetic cost is associated with carrying an extra load (Murray & Fuller 2000; Kenward 2001; Wilson & McMahon 2006). However, only a small proportion of publications include information on the impact of instrumentation on animals and the range of species used in these studies is limited, as are the parameters used to evaluate effects (Calvo & Furness 1992; Murray & Fuller 2000; Kenward 2001; Withey et al. 2001; Hawkins 2004). In particular, there is a lack of evidence with which to justify the broad application of hard and fast rules for instrumentation across avian or mammalian species which span widely different sizes and lifestyles. Furthermore, the reasons underlying adverse impacts of instrumentation are multifactorial and are related not only to the mass, size and shape of the device, but also, * Correspondence: R. Casper, Wildlife Advisory Panel, University of Tasmania Animal Ethics Committee, Private Bag 1, Hobart, Tasmania 7001, Australia. E-mail address: [email protected]

for example, to the sensitivity of the animal to disturbance, the capture method, the handling time, the attachment method, food availability and the length of deployment. Consequently, attaching devices to animals may result in combinations of immediate, delayed, short-term, long-term, direct and indirect effects. As such, the magnitude of the effects of instrumentation of animals is case-, species- and physiological status-specific (Gaunt et al. 1997; Murray & Fuller 2000; Kenward 2001; Withey et al. 2001; Hawkins 2004). Researchers and animal ethics committees alike aim to minimize the negative effects of instrumentation. This not only considers the welfare of the animals, but also provides confidence that the data collected from instrumented animals are representative of the behaviour of the sampled population. However, a practical framework with which to achieve this is currently lacking and guidelines for instrumentation are often based on limited rules which do not account for the complexity and specificity of each situation. In particular, there appears in the literature a ‘5% (or 3%) rule’ which refers to a commonly accepted standard that the mass of an instrument should not exceed 5% (or 3%) of the body mass of an animal, and that any ratio less than 5% (or 3%) is acceptable (Gaunt et al. 1997; Wilson et al. 2002; Phillips et al. 2003; Gannon & Sikes 2007). The ‘5% rule’ is essentially arbitrary (Caccamise & Hedin 1985; Aldridge & Brigham 1988; Gessaman & Nagy 1988), while the ‘3% rule’ appears to have been extrapolated from a review of albatross and petrel studies correlating device loads with foraging trip durations and nest desertions (Phillips et al. 2003). It is clear that this approach is too simplistic. Differences in energy budgets between, and within, species preclude a single rule

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for device loading (Murray & Fuller 2000; Kenward 2001). For example, transmitter weights based on a fixed percentage of body weight affect flight characteristics of large birds more than those of small birds because they have proportionally less surplus power (Caccamise & Hedin 1985). Alternatively, small birds may work with much narrower safety margins (the difference between the working mass and mass at nest desertion) than larger species (Chaurand & Weimerskirch 1994; Weimerskirch et al. 2000), and may therefore be less able to tolerate device loads. Furthermore, it is likely that an animal can carry a particular load with more ease when attached close to its centre of gravity than when placed towards an extremity (Kreighbaum & Barthels 1996). This may not always be possible, for example in mammalian species where a collar is the best method of attaching a device. In these cases, application of the ‘5% (or 3%) rule’ may be misleading. In this paper, I suggest a more comprehensive framework of guidelines for minimizing the effects of instrumentation. This method broadly categorizes the main components of experimental design that should be considered as potential sources of adverse outcomes. These are researchers, study animals, equipment (instruments plus attachments), expected effects of equipment, procedures (capture, handling and attachment methods), and expected effects of procedures. The need for pilot studies and control and/or monitoring components to experimental designs should also be considered. Below, guidelines for instrumentation are presented under each of these categories, with an emphasis on avian and mammalian examples. Examining aspects of instrumentation in this way will allow more complete assessments and consequently more informed decisions to be made. While there is some overlap between categories, this framework provides a systematic method with which to highlight aspects of concern that are relevant in any particular case. These features can then be scrutinized to determine whether the identified potential risks can or need to be reduced, while still achieving the scientific aims of the study. Researchers and animal ethics committees can then decide if this resulting design is acceptable in terms of animal welfare. That issue, however, is beyond the scope of this paper (Plous & Herzog 2001). Researchers Competent instrumentation of animals requires the appropriate selection, capture, restraint and release of animals, as well as attachment of devices. Each of these techniques may vary depending on the species being instrumented. The research team must possess the necessary skills to carry out each of the proposed procedures in a manner that will minimize negative effects on the nominated species. In many cases, each procedure should be carried out by a person who is skilled at that procedure on the nominated species, or is under the direct supervision of someone who is (Murray & Fuller 2000; Rismiller & McKelvey 2000; Kenward 2001; Gannon & Sikes 2007). If this is not possible, or not deemed necessary, then the reasons for this should be justified. Similarly, to optimize experimental design and reduce the risk of adverse outcomes, it is important that researchers are familiar with the relevant literature already available, for example pertaining to the study species, methods, parameters and behaviours that they are studying (CCAC 2003b; Beausoleil et al. 2004). Study Animals The effects of devices on animals may vary depending on their lifestyle. For example, attention to aerodynamics is important for flying and gliding animals, such as albatrosses and bats (Aldridge & Brigham 1988; Obrecht et al. 1988), while attention to

hydrodynamics is important for swimming and diving animals, such as penguins and pinnipeds (Bannasch et al. 1994; Culik et al. 1994; Beausoleil et al. 2004). In some species, external equipment may increase drag in both air and water. This may occur, for instance, in alcids with very high wing loadings (high body mass to wing area ratio) which fly long distances and also forage underwater (Ackerman et al. 2004; Paredes et al. 2005). The effect of externally mounted devices on animals that inhabit or move through confined spaces should also be considered. For example, enlarging the profile of an animal that burrows or moves through dense vegetation or narrow openings, such as winter sea-ice holes, may impede its normal movement, cause it to expend extra energy or become entrapped. The use of instruments such as radiotransmitters on juvenile mammals may require particular attention because juveniles of many mammalian species grow rapidly and tend to disperse. Rapid growth increases the risk of attachments such as collars and harnesses becoming too tight, while dispersal reduces the chances of recapturing these individuals to check on or remove equipment (Soderquist & Serena 2000; Kenward 2001; Vashon et al. 2003). The species and classes of species used should be appropriate to the study questions being investigated. For example, broad ecological questions may be best addressed using a species and class for which basic life history traits are already known and the proposed procedures are already well established. Alternatively, questions may specifically address important knowledge gaps in a particular species or species class. It may be valid to study a particular species primarily because it is threatened or endangered. However, if the population is sensitive to disturbance, it may be more appropriate to use a similar but more common species, particularly where the proposed procedures are not well established (Sykes et al. 1990). Equipment: Instruments Plus Attachments While it is recommended that the smallest possible devices and attachments are used (Withey et al. 2001), attention to other aspects of equipment will also reduce potential adverse impacts. Equipment should be balanced and positioned so as to minimize effects on the animal’s lifestyle. Equipment should not wound the animal, impair insulation, place pressure on internal organs, restrict normal movement or interfere with postures such as curling up to sleep, behaviours such as grooming and preening, or physiological processes such as moulting (Smith et al. 1998; Murray & Fuller 2000; CCAC 2003b; Godfrey et al. 2003; Hawkins 2004; Beausoleil et al. 2004). Streamlining equipment is especially important for aquatic and flying animals and those that inhabit or move through confined spaces. This can be achieved by considering the effects of equipment shape, orientation and placement on the profile and energetics of the animal (Obrecht et al. 1988; Bannasch et al. 1994; Culik et al. 1994; Watson & Granger 1998; Bethge et al. 2003; Beausoleil et al. 2004; Hawkins 2004; Estes-Zumpf & Rachlow 2007). Ideally, equipment attached to aquatic animals should be neutrally buoyant because positively or negatively buoyant equipment may modify normal diving behaviour (Webb et al. 1998; Elliott et al. 2007). The colour of equipment may also influence the behaviour of animals, their social status and their vulnerability to predation (Kessler 1964; Wilson et al. 1990; Diefenbach et al. 2003; Hawkins 2004). Electronic devices may emit acoustic frequencies or light spectra to which animals are potentially sensitive. For example, some mammalian species use acoustic signals for communication and foraging and may modify their behaviour in response to anthropogenic emissions (Kalcounis-Reuppell et al. 2006; Schaub et al. 2008; Willis et al. 2009). Similarly, instruments producing a light

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source, such as a camera flash, may cause alterations to normal behavioural patterns (Heaslip & Hooker 2008). In summary, the size, weight and configuration of an instrument and attachments should be appropriate to the species, class, behaviour and habitat of the animals in question (Mellor et al. 2004). Expected Effects of Equipment Components of equipment attached to animals may be harmful. Glues used to attach packages should be applied moderately, taking care to minimize the horizontal and vertical profiles of the glue. Excessive amounts of glue may burn an animal’s skin as well as add unnecessary weight and drag. Some dyes or glues may be toxic if inhaled or damage eyes. Researchers should be familiar with the potential hazards of materials used and how to avoid these. Instruments and attachments may cause skin wounds and feather damage in birds (Sykes et al. 1990; Foster et al. 1992; Wilson et al. 1997). They may also disrupt waterproofing and increase heat loss at the attachment site (Godfrey et al. 2003; Ackerman et al. 2004). In mammals, some collar materials may stretch and create a risk of snagging on vegetation or entrapping a leg or jaw (Robertson & Harris 1996; Cypher 1997; O’Neill et al. 2008). Conversely, some collar materials may be too rigid and cause wounds (van der Ree et al. 2001; Vashon et al. 2003; Belcher & Darrant 2004; Krausman et al. 2004; Wilson et al. 2007). In addition, instruments and attachments may be chewed by offspring or adult conspecifics which may also use equipment to grab onto during mating (Soderquist 1993; Robertson & Harris 1996; de Mendonca 1999; Rismiller & McKelvey 2000; van der Ree et al. 2001). These behaviours could cause injury to the instrumented animal and its offspring or conspecifics. Changes in body size should be predicted because this can increase the risk of equipment causing injury (Gannon & Sikes 2007). For example, rapidly growing juvenile mammals may be strangled by collars as they mature (Kenward 2001). This could also occur if underweight individuals are collared and subsequently gain weight. Conversely, collar fit may become slack during a drought. The circumference of adult necks of some species, such as ungulates and dasyurids, may increase and decrease markedly before and during the breeding season resulting in collars becoming too tight or too loose (Gedir 2001). If collars or harnesses are likely to become ill-fitting, plans based on realistic estimates of recapture rates should be made to check and adjust these frequently enough to prevent injury. Animals should not be fitted with collars or harnesses if the probability of recapture is too low to ensure this (Vashon et al. 2003). In addition, it is highly desirable to avoid situations where the welfare of animals is compromised as a result of being encumbered with equipment indefinitely. Where this is likely and recapture of animals for removal of equipment is uncertain, the use of safe nonpermanent attachment mechanisms should be used. For example, where the study period is short, attaching devices temporarily with glue may be satisfactory in terms of data collection together with the knowledge that the instrument will fall off the animal if it is not recaptured (Estes-Zumpf & Rachlow 2007). Various types of temporary collars and harnesses have been designed, typically relying on links that degrade over time and/or break if stretched. Potential problems do exist with these kinds of attachments if release of equipment does not occur reliably within the required time frame, or if release fails or is incomplete leaving equipment dangling off the animal (Jackson et al. 1985; Vashon et al. 2003). Programmable drop-off collars and harnesses are also available commercially, although at present their suitability for some species is limited by aspects of design, such as size, shape and materials used. Successful design of nonpermanent collars and

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harnesses is specific to each situation and requires careful monitoring until proven functional and safe for the species in question (Strathearn et al. 1984; Jackson et al. 1985; Soderquist 1993; Smith et al. 1998; Diefenbach et al. 2003; Vashon et al. 2003). Innovation and collaboration between researchers and people with appropriate technical expertise are encouraged to overcome the current difficulties with nonpermanent attachment mechanisms. The development of safe and effective ways to attach instruments temporarily to animals is an under-explored opportunity to contribute positively to animal welfare. The severity of adverse effects of instrumentation is likely to increase the longer an animal is encumbered (Gaunt et al. 1997; Wilson & McMahon 2006). These effects may manifest in the equipped animals themselves, their mates and/or their offspring. Common consequences to an instrumented bird are increased trip durations and decreased nest attendances and chick provisioning (Wanless et al. 1989; Saether et al. 1993; Sohle et al. 2000). Energetic costs may also be added to the mates of instrumented birds which compensate for their partner’s handicap by increasing provisioning of chicks (Paredes et al. 2005). In long-lived species, birds may reduce their parental effort and transfer costs associated with instrumentation to their offspring to avoid diminishing their own prospects for survival and future reproduction (Saether et al. 1993; Mauck & Grubb 1995). It is likely that this also occurs in longlived mammalian species. In mammals, carrying devices can prevent adequate grooming and increase damage from external parasites, reduce foraging and hunting efficiency, increase foraging trip and nursing visit durations, skew the sex ratio of offspring, cause weight loss and reduce survival (Aldridge & Brigham 1988; Walker & Boveng 1995; Cypher 1997; de Mendonca 1999; Moorehouse & MacDonald 2005). Procedures: Capture, Handling and Attachment Methods The methods used to select, capture, handle and release animals, and to attach equipment to them, all provide opportunities to reduce the potential negative effects of instrumentation. For example, birds that display strong fidelity to their mate or offspring may be less likely to abandon their breeding effort as a result of instrumentation. Animals must be handled gently and procedures completed quietly and efficiently. Stress levels in animals are often reduced by keeping their eyes covered. Distress should be minimized in target animals as well as other animals in the vicinity. Where possible, capture and other procedures should be carried out away from other animals (Holmes et al. 2005; de Villiers et al. 2006). This is particularly relevant where target individuals belong to a group such as a colony or herd. Animals should not be held captive for longer than necessary (Bali & Delaney 1997; Serena et al. 1998; Rismiller & McKelvey 2000; Suedkamp Wells et al. 2003; Mellor et al. 2004; Newman et al. 2005; O’Neill et al. 2008). Release procedures should maximize the likelihood that animals that were tending offspring will return to these duties. The method of capture should be appropriate to the species and situation. For example, a combination of wire cage traps and a drive fence is effective for small forest-dwelling macropods, cage traps are suitable for brushtail possums, Trichosurus vulpecula, quolls, Dasyurus maculatus, and antechinus, Antechinus minimus maritimus, hand captures are appropriate for echidnas, Tachyglossus aculeatus, while the best trapping method for platypuses, Ornithorhynchus anatinus, may depend on the type of waterway targeted (Vernes 1993; Rismiller & McKelvey 2000; Isaac 2005; Glen & Dickman 2006; Koch et al. 2006; Sale & Arnould 2009). Adverse impacts on habitat, such as destruction of dens or burrows, should be avoided. Traps must be checked as required to prevent distress or injury to captured animals. For example, nets set for platypuses

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and bats should be monitored continuously so that trapped animals can be removed immediately (CCAC 2003a; Koch et al. 2006; Churchill 2008). Traps set overnight should be covered, or checked and cleared prior to dawn, to prevent undue stress to nocturnal animals such as bettongs (Bettongia spp.). For species prone to capture stress, it may be necessary to use trap transmitters to alert researchers as soon as the trap is activated (O’Neill et al. 2008). Traps need to be insulated externally and/or internally where necessary and located in appropriate positions to prevent thermal stress to captured animals. Trapped animals must be protected from pests and predators. Traps and equipment should be cleaned as needed to prevent transfer of parasites and disease between animals (Glen & Dickman 2006; Gannon & Sikes 2007; Lachish et al. 2007; Sale & Arnould 2009). Sedation or anaesthesia is required when implanting devices, is usually necessary for instrumentation of large mammalian species such as pinnipeds, and may be useful in species difficult to trap, such as ringtail possums, Pseudocheirus peregrinus, or those prone to capture stress such as macropods. Procedures involving sedation, anaesthesia and surgery require detailed planning and particular care and expertise (Kenward 2001; Hawkins 2004; Gannon & Sikes 2007; Wilson et al. 2007; Horning et al. 2008; Lindenmayer et al. 2008; O’Neill et al. 2008), but may be unacceptable in some species despite these precautions (Meyers et al. 1998). The methods of attachment used should be appropriate for the situation. For example, harnesses may have deleterious effects on mallards, Anas platyrhynchos, and yellowthroats, Geothlypis trichas (Sykes et al. 1990; Rotella et al. 1993), but may be suitable for use on goshawks, Accipiter gentilis (Reynolds et al. 2004). Attachments such as harnesses, straps and collars need to be fitted expertly to animals and proper fit should be confirmed with the animal in multiple natural positions (Bali & Delaney 1997; Kenward 2001; Kortner et al. 2004; Glen & Dickman 2006). It is highly desirable that equipment is removed from animals once data collection is complete. This may be achieved by recapturing the animals, or may occur during a natural moult or through some self-release mechanism. If equipment is to be removed manually, it is important that recapture rates are predicted so that the numbers of live animals still instrumented can be estimated at any time. Recapture rate predictions should account for natural mortality over the duration of the study, as well as other likely causes of mortality, for example motor vehicles, poisons, bullets or predation (Isaac 2005). The likelihood of failing to recapture instrumented live animals should also be included in recapture rate estimations, for example because of dispersal from the study area, instrument failure or difficult terrain. The range of capture rates should be realistic and be consistent with the degree of certainty of these estimates. For example, the uncertainty of estimates based on few data should be reflected by a wide recapture rate ranges. Where equipment is to be removed by some other means, the speed at which it will be shed should be considered. Partially attached equipment may pose additional risks to animals, for example by impeding their movement, increasing the risk of entanglement and injury, or increasing their vulnerability to predation (Gaunt et al. 1997; Withey et al. 2001). If equipment is not removed, researchers should anticipate the physiological and behavioural consequences of their study animals being encumbered indefinitely. Expected Effects of Procedures The sensitivity of animals to disturbance may vary considerably depending on their reproductive or physiological status. For example, storm petrels (Hydrobatidae), larger Puffinus shearwaters and giant petrels (Macronectes spp.) may be more likely to abandon

breeding efforts following disturbance during incubation (Warham 1990). Cassin’s auklets, Ptychoramphus aleuticus, are highly likely to desert their nests when instrumented during incubation, but this risk is minimized when devices are attached posthatching (Ackerman et al. 2004). Furthermore, activities associated with instrumentation may impact both target and nontarget animals. For example, capturing an incubating bird may cause disturbance to other birds in the nesting colony, leave unattended eggs vulnerable to cooling or predation, and/or provoke the captured bird to desert its nest. Targeting populations or individuals that are vulnerable to energetic challenge or stress should be avoided (Cypher 1997). For example, disturbing hibernating bats and maternal bat colonies may be detrimental to their survival (CCAC 2003a). Similarly, nursing mothers should not be trapped when they are separated from young that are unable to thermoregulate (Belcher & Darrant 2004). Individuals in poor condition or with signs of disease or wounds should not be instrumented unless data from these animals are central to the aims of the study. Consideration should also be given to the effects of repeated disturbance to the same animals. Frequent disturbances to birds may increase sensitization to human presence and result in reduced nest attendances and chick survival (Ellenberg et al. 2009; Holm & Laursen 2009; Wheeler et al. 2009). Persistent low levels of stress may accumulate to render animals more vulnerable to the effects of natural stressors (Murray & Fuller 2000; Mellor et al. 2004; O’Neill et al. 2008). Individuals of some species, such as Tasmanian devils, Sarcophilus harrisii, spotted-tailed quolls and antechinus, tend to be trapped repeatedly over several days and can lose weight. This can be avoided by, for example, limiting the number of consecutive trapping days, increasing the amount of bait in the traps and/or providing the trapped animals with extra food. Obviously the latter two methods are not useful where animals fail to eat the food provided. For animals with high metabolic rates, such as small mammals, it is particularly important that the bait supplied is sufficient to replace the food and moisture that they would have consumed if they had not been trapped (Glen & Dickman 2006; Sale & Arnould 2009). In these cases, if the risk of thermal stress is high, trapping can be fatal and should be avoided. The risks of capture stress, abandonment of offspring, loss of territory and predation should be minimized. It is important that operators have the ability to detect signs of stress in the captured species and make timely decisions to alleviate these where necessary. This may entail simply releasing the animal or may require intervention such as cooling or warming (Bali & Delaney 1997; Baker & Johanos 2002; O’Neill et al. 2008). Animals that have entered torpor should be rewarmed to regain full mobility prior to release (Churchill 2008). Capture myopathy has been reported in a variety of animals but some species, including macropods, ungulates, ursids and some birds, are especially susceptible. Capture myopathy is harmful to animals, difficult to treat and may be fatal through direct physiological effects or as a consequence of predation (Mason 1998; Rogers et al. 2004; Abbott et al. 2005; DelGiudice et al. 2005; Cattet et al. 2008; Webb et al. 2008). Care should be taken to prevent this condition occurring, particularly in vulnerable species, where the use of sedatives may be necessary. Risk factors are believed to include the capture method, the length of the capture period, the number of animals captured together, the number of times an individual is captured, age, gender, selenium deficiency, human contact, noise level, heat stress and exhaustion (Vernes 1993; Beringer et al. 1996; Coulson 1996; Lentle et al. 1997; Mason 1998; Rogers et al. 2004; Abbott et al. 2005; Cattet et al. 2008; Webb et al. 2008). The welfare of the offspring of captured animals must be attended to and care taken to reunite them with their parents (Vashon et al. 2003). For example, eggs and brooded chicks should

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be protected from thermal stress, conspecifics and predators until safely attended by a parent. Some marsupial species, such as bettongs, are liable to relax their pouches and drop their young when stressed. In these cases, replacing the young and closing the pouch with masking tape is effective, but requires expertise. For some species such as arboreal possums, placing the mother and young in a Hessian bag hung in a suitable tree, thereby allowing them to reunite and leave in their own time, is an effective technique. Generally, animals should be released at the site where they were captured as soon as they have recovered from instrumentation procedures (Bali & Delaney 1997; Rismiller & McKelvey 2000; Estes-Zumpf & Rachlow 2007; Nicol & Andersen 2007; Lindenmayer et al. 2008; O’Neill et al. 2008). However, there are exceptions. For example, platypuses likely to be recaught in nets should be held until removal of nets at the completion of a trapping session. Nocturnal animals may be vulnerable to predation if released during daylight hours or if the capture site provides little refuge. In these cases, animals should be released somewhere nearby that is safe, or may even need to be held and released the following night (Churchill 2008). It is important that field programmes have enough resources to care properly for all animals disturbed by any procedures. These resources should include the capacity to respond to reasonably anticipated problems (Bali & Delaney 1997; Gannon & Sikes 2007). For example, extra effort is likely to be needed to locate and recapture instrumented animals that den, have large home ranges or where the terrain is hilly and densely vegetated (Jiang et al. 2008). It is particularly important that contingency plans are in place where recapture rates are uncertain. Where traps are used, capture of non-target species may occur (van der Ree et al. 2001; Koch et al. 2006). Where by-catch numbers are high or these species are prone to capture stress, modification to aspects of the trapping protocol, such as trap checking times and frequency, trap design, trap locations or bait type, can alleviate these problems. Ideally traps should be deactivated at times when target species are unlikely to be caught. For example, traps set to catch nocturnal animals should be closed during the day. If this is not possible, then traps should be positioned to prevent thermal stress to any diurnal by-catch and checked just prior to dark to release these animals. In summary, researchers should anticipate likely problems and plan in advance to avoid adverse consequences of their activities. Pilot Studies If any equipment or procedure is new, or untried on the proposed study species, there may be a case for carrying out a pilot study or captive trial first to assess the suitability of the equipment or procedure for the nominated species. This is because the effects of instrumentation may be taxon, equipment and technique specific (Robertson & Harris 1996; Murray & Fuller 2000; Withey et al. 2001; CCAC 2003b; Mellor et al. 2004). In birds, harnesses that go around the wings are unsuitable for many species (Gaunt et al. 1997), alcids may react negatively to both external and implanted devices (Burger & Shaffer 2008), while attaching loads to very small birds requires particular care (Sykes et al. 1990). Collar materials and shape may need to be customized for some mammalian species to prevent injuries (Krausman et al. 2004). In addition, some species including otters, Lutra lutra, and many macropods, are particularly sensitive to stress (O’Neill et al. 2008). In such cases, it may be useful initially to trial and perfect new procedures on captive individuals before application to their wild counterparts. In some situations, a preliminary field trip may be appropriate to establish the best technique, such as trapping method, at a new site (Koch et al. 2006).

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Monitoring and Controls Assessing the impacts of instrumentation on animals through monitoring and/or controls provides an important contribution towards continually improving animal welfare and experimental design. Monitoring for problems from equipment may be necessary in some situations, for example when a design is untried on the proposed species, or if changes in body condition are expected (Bali & Delaney 1997; Kenward 2001; Kortner et al. 2004; Glen & Dickman 2006). Where indicated, equipment design may need to be modified. For example, changing collar materials may be necessary to prevent injuries (Belcher & Darrant 2004; Wilson et al. 2007). The design of controlled experiments should consider that any impact of instrumentation may manifest in a number of ways. For example, adverse effects are often related to the life history traits of the species and current food availability, and may only be apparent under certain conditions, such as when provisioning offspring or diving (Walker & Boveng 1995; Webb et al. 1998; Heaslip & Hooker 2008). In birds, effects may be evident in the instrumented bird itself, for example reduced body mass or increased foraging trip durations (Sohle et al. 2000); its unencumbered mate, for example increased provisioning of offspring (Paredes et al. 2005); its offspring, for example reduced chick growth rate or peak mass (Saether et al. 1993; Mauck & Grubb 1995; Weimerskirch et al. 2000); or in its future breeding status, for example failure to return to breed in the following season (Ackerman et al. 2004). Furthermore, negative impacts are not always overt and may sometimes only be detected biochemically. It is therefore important that the parameters used to compare controls and instrumented animals are appropriate to the species and situation being studied (Murray & Fuller 2000; Kenward 2001; Withey et al. 2001). Conclusions It is clear that the potential causes of negative effects of attaching electronic devices to animals are multiple and complex. In addition, the primary sources of these outcomes vary both between and within species and are therefore best assessed on a case by case basis. It is currently not possible to calculate the overall impact of instrumentation for any particular situation because not all of the likely significant component causes have been measured. This type of quantitative approach has been suggested (Wilson & McMahon 2006) and, while commendable, such a system is unsupported by the required data and is therefore is not readily usable at present. This emphasizes the importance of incorporating control and/or monitoring components into experimental designs wherever possible, and publishing those results. The guidelines for instrumentation of animals presented in this paper are categorized according to the main components of experimental design that can cause adverse outcomes. This framework allows, and encourages, consideration of multiple potential influences. Furthermore, it considers the effects of instrumentation on nontarget animals, such as offspring, mates, conspecifics and nontarget species. This approach allows the potential effects of instrumentation to be assessed in a more comprehensive manner than through the use of simplistic rules which do not account for the complexity and specificity of each situation. This paper resulted from work commissioned by the Wildlife Advisory Panel (WAP), an ad hoc subcommittee of the University of Tasmania Animal Ethics Committee. Many thanks are due to the WAP for numerous discussions on these guidelines: Mark Hindell, Hamish McCallum, Nick Mooney, Dianne Nicol, Stewart Nicol, David Pemberton and Barrie Wells. I am grateful to the following researchers for generously sharing their field expertise with me:

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