An important first step towards avoiding or reducing effects of deploying tracking devices on waterfowl is to know what can go wrong. We found that 17% of all original tracking studies (40% of studies reporting potential effects) reported major, long-lasting negative effects of their tracking method. Here, we review the effects of different transmitter attachment techniques on waterfowl, including effects on survival, behaviour, migration and reproduction.
Harness attachment methods can have strong negative effects on survival. In one of the first studies using a harness as attachment method, all swans equipped with PTTs died before or during migration, which was attributed mostly to the weight of the 170 g devices . Over the years, it has become clear that apart from the burden of carrying a heavy device, harness backpacks themselves are probably the main cause of deleterious effects on the birds carrying them. The main problematic features of harness backpacks are that they are relatively large external structures causing abrasion and drag, disrupt waterproof plumage and that the harness may be too loose or too tight, partly depending on the bird’s body stores, which can vary greatly over the year especially in migrants [30, 43, 61, 62]. Effects on survival are most often detected by low return rates of tagged birds to breeding or staging sites compared to ring-marked individuals. The lowest return rate was reported in a study on female Barrow’s Goldeneyes Bucephala islandica, with none of 16 tagged birds being recaptured in nest boxes during successive breeding seasons, relative to a background return rate of 66% . Almost as poor was the 4% return rate of 62 Brent Geese Branta bernicla fitted with backpack transmitters to their Alaskan breeding site, compared to 57–83% return rates of colour-ringed individuals . In a study in Saskatchewan, Canada, Mallards with harness transmitters had a return rate of 22.6% to their breeding grounds compared to 55% in individuals with an implanted transmitter . Given the high site fidelity of these species, mortality is the most likely cause of these low return rates, although emigration cannot be fully ruled out. In contrast, other studies did not find any effects of harness attachments on survival. Survival rates over the course of the breeding season did not differ between Blue-winged Teals Anas discors with a harness backpack (61% survival over 90-day period) and individuals with an implanted transmitter (73% survival over 90-day period), and although both groups could have suffered from reduced survival, the observed cases of mortality in this study seemed unrelated to the transmitter . Winter survival of Northern Pintails did not differ between tagged and control individuals . Cappelle et al.  reported loss of signal for nine out of 47 harness-attached satellite transmitters within 3 days after deployment for Garganey Anas querquedula (1 out of 18), Fulvous Duck Dendrocygna bicolour (2 out of 3) and Comb Duck Sarkidiornis melanotos (4 out of 20). Signal loss may result from transmitter failure, and bird mortality was only confirmed in four of these cases. The authors speculated that this was related to stress induced by handling and capture. Other studies did not observe increased mortality shortly after release (e.g. . Linking long-term effects of transmitters to bird mortality is often difficult in the field.
Besides occasionally reported to increase mortality, harnesses have been found to affect behaviour of tagged birds. Disturbed behaviour shortly after tag deployment is reported regularly, involving increased maintenance behaviour and reduced foraging [6, 30, 32, 62, 65, 70]. In some studies, these effects diminished over time (, E.K. pers. obs.), while they persisted in others [30, 62]. In several cases, avoidance of water was observed, most likely due to loss of waterproofing capacity of the plumage caused by the harness, which may limit the access to food, reduce body condition and prompt (sometimes fatal) illness or starvation ([62, 30, 43, E.K. pers. obs.). On the longer term, feather and skin abrasion may occur, especially on the bird’s back (underneath the transmitter) or at the pectoral muscle where the harness goes under the wing (, E.K. and T.L. pers. obs.). These abrasions could potentially lead to infection of the skin or altered behaviour due to thermoregulation problems. It should be noted that most physical effects can only be observed when birds are recaptured or when transmitter effects are tested in captivity. However, as most captivity studies (e.g. [14, 57]) are relatively short term (1–2 months) and captive birds are often incapable of prolonged flight, it remains difficult to fully assess the negative effects of transmitters.
There is also evidence that harnesses increase the cost of migration. The shape and size of external backpacks (including the presence of an external antenna) can greatly affect the drag during flight. An increased drag, rather than the mass of the device, may reduce the migration distance and the reserves of the birds upon arrival, as shown by computer simulations by Pennycuick et al. . This is supported by Bowlin et al.  who show that backpack attached geolocators on stuffed Common Swifts Apus apus increased drag and thus their flight ranges. Similarly, Hupp et al.  found that Northern Pintails equipped with 12–20 g satellite transmitters [1–3% of the bird’s body weight (BBW)] in East Asia build up a delay of 7.7 days per 1000 km during their migration compared to birds that were only ringed. Higher energetic costs during flight are given as a likely explanation. In a recent study on Barnacle Geese Branta leucopsis, timing of migration of individuals equipped with GPS-loggers (35 g, 2% BBW) was slightly delayed in the first stretch of northward migration when compared to individuals that carried lightweight (1 g) geolocators on their colour rings (Lameris et al. unpublished data). Blouin et al.  speculate that the tag or harness may have contributed to the fact that none of the six satellite-tagged Greater Snow Geese Chen caerulescens in their study completed migration successfully (tag weight: 100–140 g, 4–5% BBW). However, migration is not always affected, given the lack of any difference in timing of arrival at spring staging sites in Greenland White-fronted Geese equipped with dummy satellite transmitters (38–54 g, 1.5–2.0% BBW; ) and timing of arrival and departure at a fall staging site in radio-tagged Brent Geese B. b. nigricans (radio transmitters of 26–25 g, 1.5–2.0% BBW; ) compared to ringed-only individuals. It is likely that effects on energy expenditure or flight capacity are especially manifesting during the most energy-demanding migratory flights, as suggested also by the loss of three satellite-tagged Garganeys during the last stretch of their migratory flight across the Sahara (12 g satellite transmitters, 3% BBW; ). During other activities, the negative effects on energy expenditure are probably less, as shown by a study of captive Brent Geese, where energy expenditure during activities other than flight was not affected by carrying a 35 g transmitter (2% BBW; ).
If backpacks have a negative effect on migration and the condition of birds upon arrival on their breeding grounds, this may have carry-over effects on the breeding success, additional to potential direct effects of devices on breeding effort. Backpack attachments have been found to affect clutch size and timing and propensity of breeding. Pennycuick et al.  point out that lower energy height (a measure of energy reserves) in Barnacle Geese after spring migration may directly affect reproductive investment such as clutch size. Even though timing of migration in Brent Geese was not affected in a study by Ward and Flint , return rates from the wintering grounds to Alaska were dramatically low (1 out of 62) and the one female that had returned with a transmitter did not breed, in contrast to 90% breeding initiation in colour-ringed females. Pietz et al.  suggest that the significantly later onset of breeding and smaller clutches in radio-tagged Mallards compared to ringed individuals may have been related to the energetic consequences of a shifted time budget, with less feeding and more preening and maintenance behaviour due to the radio-tag. Accordingly, Rotella et al.  report that Mallards with harness transmitters nested 2 weeks later than birds with sutured-and-glued or implanted transmitters, although both groups could have been affected by the transmitter attachment. Barnacle Geese with GPS-loggers bred some days later than a control group carrying lightweight geolocators (Lamsiers et al. unpublished data). Blue-winged Teals captured and equipped with a backpack shortly before the breeding season failed to produce a nest twice as often as conspecifics with implanted devices . Similarly, two Barrow’s Goldeneyes equipped with a transmitter shortly before the onset of incubation abandoned the nest . In contrast, the Blue-winged Teals as well as most of the Barrow’s Goldeneyes captured and tagged during incubation did continue breeding [29, 70]. Mallards tagged during late incubation did not have lower brood or duckling survival than mallards with implanted transmitters . Finally, reproduction could be impaired by negative effects of harness-attached transmitters on pair bond, as suggested by a high proportion of unpaired tagged female Brent Geese (, Lameris et al. unpublished data).
In conclusion, although the weight of modern tracking devices is no longer the limiting factor for reducing negative effects of tracking devices, especially for larger birds, the device and the harness itself may still induce changes in survival and behaviour. These effects depend strongly on the device shape, the moment of attachment and probably also harness design, which can all be optimized to fit the study system. When aiming for long-term tracking of birds, devices need to be solar-charged, requiring external attachment. Unless the lifetime of tiny batteries will be greatly enhanced, which would enable less-invasive alternative attachment like attachment to leg rings, harnesses remain the only available attachment method for many species.
White et al.  argue, based on a meta-analysis, that detrimental effects of implanted devices on birds are less severe than for external devices. This is supported by several studies in waterfowl. Direct comparison between implants with internal antenna and (anchored) backpacks in wild female Mallards revealed that individuals with implants experienced significantly less negative impacts on survival and reproduction . Dzus and Clark  compared the return rates of Mallards with harness-style backpacks and implants with internal antenna to their breeding areas and found a twice as high return rate for birds with an implant. However, in both studies the effect of implants is unclear since no untagged control group was included in the experimental design. A study with captive Blue-winged Teal, in which individuals with backpack, implant and no transmitter were compared, showed that birds with implants lost weight in the first week after surgery compared to both other groups, but had recovered by the second week. Blue-winged Teals with implants with internal antenna did not alter their behaviour, unlike birds with harness transmitters . In the field, Blue-winged Teals with implanted transmitters with internal antenna had slightly, but not significantly, higher survival over the course of a breeding season than birds with harness transmitters and were more likely to initiate a nesting attempt .
An important impact of using implanted tags may be direct physical effects or mortality due to surgery. Korschgen et al.  describe the histological reaction of Mallards to implanted transmitters with external antennas and conclude that the mild to moderate air sac alterations they found did not cause any behavioural or physiological effects. Post-surgery survival of Spectacled Eiders Somateria fischeri equipped with implants with external antennas was found to be impacted by pH and haematocrit values of the blood prior to surgery. Birds with low pH, or extremely low or high haematocrit had lower survival rates during the critical first five days after surgery . Obtaining these values prior to surgery may help reduce the mortality rate. A paper describing the surgical procedure for implantation of transmitters in Canvasbacks Aythya valisineria reports no abnormal behaviour or increased mortality after implanting devices with internal antennas . Hupp et al.  reported no post-surgery mortality in Lesser Canada Geese Branta canadensis parvipes tagged with radio transmitters with external antennas. Survival during their first year was similar to that of control individuals, although survival and return rates 2–4 years after tag deployment were slightly lower, potentially suggesting a subtle chronic tag effect. The feeding, maintenance and active behaviour of these tagged individuals were similar to that of unmarked individuals, and there was no sign that implantation affected the frequency of agonistic interactions . The implantation of satellite transmitters with external antennas in Common Eiders Somateria mollissima during incubation led to the abandonment of 11 out of 12 nests in a Canadian study, but 30% of the tagged birds were observed nesting in the following years. Furthermore, the tagged birds spent more time preening than colour-ringed birds and suffered a 20% decrease in survival during the first year after surgery compared to the control group . Limping was observed in some individuals, something which was also found by 1 out of the 6 Common Eiders in the study of Latty et al. .
The lack of a harness and large external structures other than percutaneous antennas makes implanted transmitters the preferred tracking devices for diving ducks, such as eider species Somateria spec. and Harlequin Ducks Histrionicus histrionicus. Negative effects seem limited, but the difficulty with these seaduck species is that monitoring them post-surgery is often impossible. Brodeur et al.  were faced with signal loss of most satellite transmitters with internal antennas implanted in Harlequin Ducks in the months after deployment, but argue that resightings of several individuals up to 4 years later, combined with normal body temperature measurements before signal loss, indicated that this problem was caused by transmitter failure rather than bird mortality. Only one case of mortality was confirmed in this study and occurred within a few days after implantation, likely as a direct effect of surgery. An analysis of Harlequin Duck survival in Alaska revealed that recapture rates did not differ between birds with and without implants with external antennas, and only an average loss of body mass of 15 g was detected in the 2 weeks following the surgery . Implanted transmitters can cause a change in diving behaviour as was shown in Common Eiders . The descents and ascents of foraging dives were slower, and total dive durations were longer after implantation of transmitters with an external antenna than before. This may have been caused by muscle damage from the surgery, or by a biomechanical change affecting buoyancy or imbalance in these birds. The prolonged active phase of the dives may result in overall higher energy expenditure in tagged eiders, or force them to use different (e.g. shallower) habitats than untagged birds . Latty et al.  also showed that implanted transmitters with external antennas affected bird health and physiology by a change in biomarkers up to 3.5 months after surgery. Although we did not find clear negative effects of implanted devices with external antennas compared with internal antennas, and no studies comparing the two, Hupp et al.  suggest that chronic low-grade infections from bacteria entering the body along the external antenna could potentially reduce long-term survival.
Negative effects of transmitters placed under the skin are not often reported, which could be due to the low number of studies in our analysis that used this method. There is some evidence that subcutaneously anchored devices affect survival and reproduction of birds. In ducklings of Mallard and Gadwall Anas strepera, survival was lower for individuals equipped with subcutaneously anchored radio transmitters compared to an untagged control group [2, 47, 66]. The authors note entanglement as possible cause for lower survival, which was also reported for Harlequin Ducks . Bakken et al.  found raised surface temperatures around transmitters attached with subcutaneous anchors in Mallard ducklings, but did not find differences in energetic costs for thermoregulation between marked and unmarked ducklings. The reduction in short-term survival rates of female Mallards of up to 23% in Paquette et al. , which was only significant in one out of five study sites, indicated that tags attached with subcutaneous anchors may sometimes affect adult birds. Other studies using subcutaneous implants found no effect on short-term survival of Lesser Scaups Aythya affinis , Surf Scoters Melanitta perspicillata and White-winged Scoters Melanitta deglandi  or on annual survival of Wood Ducks Aix sponsa . Subcutaneous attachments have been found to negatively affect reproduction in some cases. Paquette et al.  found female Mallards with subcutaneously anchored backpacks to spend less time on egg laying and incubation and to initiate fewer nests. Enstipp et al.  found strongly altered behaviour in Long-tailed Ducks Clangula hyemalis with subcutaneous attachments, with increased preening behaviour and less time spent on the water, and two out of five individuals developed a bacterial infection at the site of attachment. Radio transmitters attached with prong and suture had no effect on reproduction in Wood Ducks .
Neck collars with tracking devices are often used in large, long-necked species, such as swans and geese. For these species, a neck collar can be more suitable than a backpack, as it diminishes the area over which abrasion and drag occurs, and lacks a harness which can be wrongly adjusted to the bird’s shape and disrupts the plumage. However, as the weight of the tag is not positioned at the centre of gravity, this may become problematic for the bird when tags are relatively heavy . In general, we found that neck collars used in studies are lighter (in mass relative to the bird’s body mass) than harness-attached or implanted tags (backpack vs. neck collar: t
185, 33 = 8.26, p < 0.001; implant vs neck collar: t
105,33 = 8.34, p < 0.001). Although several studies combined the use of neck collars and backpack attachments [6, 63, 78], a proper comparison of effects is lacking. Blouin et al.  report that none of the Greater Snow Geese equipped with backpack transmitters reached the breeding grounds in 1993 and 1994 (due to signal loss, natural mortality or being shot), while four out of 11 birds equipped with neck collar transmitters did reach the breeding grounds in 1995. However, these transmitters were also lighter than the backpacks and direct comparison of attachment methods could not be made.
Neck collars with tracking devices can alter bird behaviour in similar ways as harness-attached backpacks, but this seems to be a short-term effect. In a captivity experiment, Kölzsch et al.  reported no difference in behaviour between Canada Geese equipped with neck collar transmitters or backpack transmitters, but both groups tended to spend more time preening and less time feeding. Increased preening behaviour was also observed in a study on captive Bewick’s Swans C. columbianus bewickii with neck collar transmitters, but this effect had disappeared after 6 weeks . Short-term effects on behaviour were also observed in the field. Snow Geese equipped with neck collar radio transmitters spent 2–3 times less time foraging than the control group in the season in which they were tagged, but this difference had disappeared in the following season . Black Swans Cygnus atratus equipped with conventional neck collars were not affected in their behaviour compared to the control group .
Multiple studies report negative effects of neck collars on reproduction. Snow Geese equipped with neck collar transmitters showed a high rate of divorce from their original mate . In subsequent breeding seasons, they delayed nest initiation and had smaller clutch sizes [5, 19]. Also Canada Geese with neck collar transmitters experienced a lower nesting propensity and nested later than the control group . Delayed laying can be the result of delayed or slowed down migration caused by drag of neck collars during flight , but such an effect has not yet been proven.
Shorter-necked species seem affected more by neck collars, although this has not specifically been studied. Older studies using neck collars with radio transmitters on various duck species (Wood Duck, Canvasback, Redhead Aythya americana) showed adverse effects on behaviour, survival and reproduction [31, 54, 79]. As can be expected for shorter-necked species, ducks with neck collars can get their lower mandible stuck in the collar, which leads to retarded behaviour and sometimes mortality [54, 79]. Not only ducks experience problems with neck collars, but negative effects have also been found for shorter-necked geese. The relatively short-necked Emperor Geese Chen canagica experienced lower survival, lower breeding propensity and laid one average one egg less when carrying a neck collar compared to a control group with leg rings . Ross’s Geese Chen rossii wearing neck collars were more vulnerable to being shot by hunters than birds marked with tarsal bands . Feeding behaviour during winter was not affected in Brent Geese carrying narrow neck collars with radio transmitters , but negative effects of conventional neck collars have been found on courtship behaviour  and nesting success in this species .
A specific concern with the use of neck collars is that ice has been reported to accumulate on plastic collars under freezing temperatures (e.g. ). Formation of ice has in rare cases been shown to be fatal for birds (e.g. ), although other studies showed no effect on goose behaviour [27, 53]. There are no reports of ice accumulation on other types of tracking devices.
Other attachment methods
The effects of other tag attachment methods, like gluing a device onto feathers or rings, have not often been tested in comparative studies. Enstipp et al.  compared tesa-sutured devices with subcutaneously anchored devices in Long-tailed Ducks and found that while birds with tesa-sutured devices recovered more rapidly from alterations of behaviour, tracking devices were lost after 26 days on average. Effects of other attachment methods were reported in original tracking studies. Survival and (re)nesting of Wood Ducks carrying a radio transmitter on a bib, a piece of fabric hanging from the neck on the chest, were lower than expected based on earlier studies, which may be related to the transmitter attachment . We are unaware of other experiences with waterfowl carrying bibs. More conventional are devices mounted to the tail feathers. Guillemain et al.  glued and bound 3.5 g radio transmitters to the central rectrices of five dabbling ducks species. One of 21 individuals was found dead three days after logger deployment, but this was likely unrelated to tag attachment. Similarly, radio transmitters were glued and bound to the tail feathers of Mallard, Eurasian Teal and Northern Pintail in France by Legagneux et al. , but no details are provided about whether or not this affected the birds. Seven out of 20 tail-mounted transmitters of 17 g in Barnacle Geese were lost prematurely in a study by Phillips et al. , but no transmitter effects on the birds were reported. Reynolds  cut a small patch of feathers on the lower back of Laysan Teal Anas laysanensis to glue radio transmitters directly onto the skin and adhered them to uncut feathers with strips of tape. Also in this study, transmitter loss by detachment was frequent and the author did not report the presence or absence of effects on the birds. Miniature geolocators (light loggers) were attached to plastic leg rings of Barnacle Geese in a study by Eichhorn et al. , and no effects on nesting or survival were reported. A peculiar tag attachment method was tested in canvasbacks. After particularly bad experiences with harness backpacks,  tested the attachment of radio transmitters on canvasback nasal saddles. Pilot studies on a limited number of canvasbacks in the laboratory and in the field were reported as promising and after a 6-h adjustment period the birds behaved normally. However, we are not aware of follow-up studies by the author or any more recent study using this attachment method.