ALTHOUGH GARDENS PROVIDE MANY DIFFERENT opportunities for birds, such as access to high-energy foods at the times of the year when natural food supplies are low and energetic demands high, there are a number of risks that birds using gardens may face. These include predation by both wild and domestic animals, disease, and encounters with windows, netting and other objects that may bring about injury or even death. We have already looked at the opportunities associated with the volume of supplementary food provided by householders keen to help visiting wild birds, and at the nesting opportunities to be found in gardens, so this chapter examines a small number of other opportunities before the focus shifts to some of the risks.
THE BRIGHT LIGHTS – ARTIFICIAL LIGHT AND GARDEN BIRDS
Artificial light is one of the most significant anthropogenic changes associated with the built environment (Hölker et al., 2010). Street, security and ornamental lighting now illuminate our towns and cities, penetrating the darkness of night and potentially altering the behaviour of birds and other urban wildlife. Light is a key behavioural cue for many species and artificial lighting has been shown to alter the timing of various activities, including those associated with breeding-season song, reproductive physiology and foraging behaviour (Ockendon et al., 2009a; Dominoni et al., 2013; Gaston et al., 2013; Nordt & Klenke, 2013).
We saw in previous chapters how there is increasing evidence that birds living within urbanised landscapes have a longer breeding season, brought about by the earlier onset of reproduction. This has been linked to the provision of supplementary food (Chapter 2), to a warmer microclimate, to greater levels of social stimulation and to increasing levels of light pollution. Evidence for the latter comes from work on London’s Starling population (Rowan, 1938) and from experimental studies of Blackbirds (Dominoni et al., 2013). Observations have also revealed that Robins and Blackbirds frequently sing or even forage at night in those parts of UK towns and cities lit by street lighting (Hollom, 1966; Mitchell, 1967; Fuller et al., 2007b), though the avoidance of daytime traffic noise may, as we have already seen, contribute to this.
Dominoni’s work, carried out in Germany, involved the use of light loggers attached to free-living Blackbirds, the information collected revealing the levels of light that individuals encountered in the wild. Free-living forest birds were exposed, on average, to 0.00006 lux of light at night, with little variation witnessed between individuals. In contrast, free-living city birds were exposed to significantly higher levels of light, averaging 0.2 lux. The amount of light that the city birds encountered at night was highly variable, ranging from 0.07 to 2.2 lux. Dominoni and his colleagues used the measurements collected to examine the influence of these differing levels of light on captive Blackbirds, some caught in the city and some in the forest. Birds exposed to light at night developed their reproductive system up to one month earlier than birds kept under dark nights; they also moulted earlier. Perhaps most interesting of all was the finding that city birds responded to the presence of artificial light at night differently to birds that had been captured in the forest, suggesting that the process of urbanisation might alter the physiological phenotypes of birds.
The timing of reproduction in birds is thought to be controlled through the process of natural selection, with optimal timing likely to deliver fitness benefits. Birds living within the temperate zone have been shown to use photoperiod – the period of time each day during which an organism receives illumination – to predict the optimal timing of reproduction. In species such as Blackbird, it is the increase in day length in early spring that initiates a series of neurological and physiological changes that lead to the development of the reproductive organs (Dawson et al., 2001). If the photoperiod is altered through the presence of artificial light, this can lead to the types of changes being seen in populations exposed to artificial light.
Light pollution has also been shown to alter the activity levels of garden birds, both in the breeding season and at other times of the year. Davide Dominoni’s work on Blackbirds has, for example, revealed that the onset of daily activity is significantly earlier in urban populations than it is in rural ones – though the end of daily activity does not appear to vary between the two (Dominoni et al., 2014). Much of the work on this topic has concentrated on the timing of the dawn chorus, an obvious component of the breeding season whose timing has already been explored in relation to a range of different factors, including the level of background noise (Fuller et al., 2007a), female fertility (Mace, 1987), food availability (Saggese et al., 2011) and foraging success (Kacelnik & Krebs, 1983). The timing of dawn song has been linked to male quality in Eastern Kingbirds Tyrannus tyrannus and to the level of extra-pair paternity in male Blue Tits (Murphy et al., 2008; Kempenaers et al., 2010), so any change in its timing that results from the presence of artificial lighting may have profound consequences for breeding birds (see Chapter 3).
FIG 69. Having a large eye relative to its body size may be one reason why the Robin is able to be active early at garden feeding stations during the winter months. (John Harding)
Less work has been done on the influence of light pollution on the activity of garden birds during the winter months. This is something that we were able to examine through the BTO’s Shortest Day Survey (Ockendon et al., 2009a; 2009b), a citizen science survey which asked participants to record the time (relative to daybreak) at which birds first visited garden feeding stations during one particular December morning. At northern latitudes, the long winter nights, with their associated low temperatures, may place additional stresses on small garden birds. Energy reserves, expended maintaining body temperature overnight, need to be replenished come dawn and this may prompt small birds to visit garden feeding stations as soon as it is light enough to do so. If this dawn activity is limited by light intensity, then small birds living in areas illuminated by street lighting may be active earlier than those living in areas without such illumination. The data collected from 5,800 participants through the Shortest Day Survey revealed a clear relationship between the average time at which garden bird species were first seen at garden feeding stations and their eye size. Species with larger eyes relative to their body size were active earlier (see Table 8), with Blackbird and Robin leading the way (Ockendon et al., 2009a).
TABLE 8. Mean arrival time (defined as the time between first light and a species being seen at garden feeding stations) and mean eye diameter for 24 common bird species recorded in the BTO’s Shortest Day Survey (Ockendon et al., 2009a).
Although the degree of illumination at each site was not recorded during this study – all observations were made on the same winter morning – individual garden sites were categorised as being either urban or rural in nature, allowing us to explore an assumption that urban sites received more illumination than rural ones. Based on this assumption, it was hypothesised that, within a species, average arrival times would be earlier in urban gardens than rural ones. Surprisingly, the opposite pattern to that expected was found for nine of the ten species included in this aspect of the study; only Collared Dove matched the hypothesised pattern. This suggests that while the time at which garden birds begin to forage on winter mornings may be limited by their visual capabilities at low light levels, factors other than the degree of illumination must also play a role in shaping activity (Ockendon et al., 2009b). As we shall see below, one such factor is heat pollution and the ‘urban heat island effect’. An experimental approach to examining the effects of artificial lighting on foraging times in winter has been adopted by colleagues working at the Max Planck Institute in Germany, where Arnaud Da Silva, David Diez-Méndez and Bart Kempenaers used video cameras to study feeder use by six forest songbirds under different levels of artificial lighting (Da Silva et al., 2017). The researchers found that while two early foraging species – Blue Tit and Great Tit – started foraging earlier during experimentally lighted mornings, Blackbird, Jay, Nuthatch and Willow/Marsh Tit Poecile palustris did not.
HOT IN THE CITY – TEMPERATURE AND GARDEN BIRDS
Ambient temperature can be of particular importance to garden birds during the winter months, when many individuals require additional energy in order to keep warm. Small garden birds, such as Blue Tits, only lay down small amounts of body fat, perhaps only enough to get them through a single night. This means that they have to spend a significant part of the day searching for food, something that may be less of an issue for individuals using garden feeding stations than it is for those living within the wider countryside – the latter may spend 85 per cent of the available daylight hours looking for food. While small birds may alter their roosting behaviour to minimise the impacts of low temperatures – perhaps by roosting communally in a nest box – most will lose weight overnight. Research has shown, for example, that Blue Tits and Great Tits are some 5 per cent lighter at dawn than when going to roost the previous evening (Lehikoinen, 1987).
FIG 70. House Sparrow plumage weight increases by as much as 70 per cent following the autumn moult, providing additional insulation during the cold winter months. (John Harding)
The insulation provided by a bird’s feathers can also help to reduce heat loss, with the downy under-feathers the most important. Increasing the quantity of downy feathers during the winter may help. In the House Sparrow, plumage weight increases by 70 per cent following the autumn moult, helping to increase insulation. The plumage can also be fluffed up to increase the number of air pockets, something that again reduces heat loss. Other birds may roost communally, perhaps even occupying roosting pouches – a recent addition to the garden bird care product range – or nest boxes (see Chapter 5).
The temperatures encountered within urban environments may be several degrees higher than those of the surrounding countryside (Landsberg, 1981), a result of ‘waste’ heat escaping from offices, housing and factories. The magnitude of this effect is related to the size of the urban area, and in our largest cities the temperature may be as much as 5–8°C higher than that of the surrounding countryside. It is worth noting, however, that local temperatures within a large urban area can also vary considerable with location; vegetation cover has an important role in local daytime temperatures, and pavements and other human structures an important role in night-time temperatures (Buyantuyev & Wu, 2010). Higher temperatures overnight may mean that small birds can roost for longer, having used up fewer reserves maintaining their body temperature and with less urgency to feed come dawn. The effects of urban heat may interact with those of light pollution, the timing of dawn activity being pushed back by temperature but pulled forward because of light pollution. Ideally, these two processes would be investigated using an experimental approach, but in the absence of such work we can use the results of the BTO’s Shortest Day Survey to get an idea of how their effects might influence the activity of small birds.
As we have just seen, analysis of the data collected through the Shortest Day Survey revealed that urban populations of nine of the ten species studied were active significantly later than populations located in rural areas. This was counter to the pattern expected if light pollution – which should be greater within urbanised landscapes than rural ones – was the sole driving factor. Instead, it seems to suggest that, while light levels may influence the timing of dawn activity, urban heat pollution plays a more significant role in shaping dawn activity during the winter months (Ockendon et al., 2009a). In an attempt to explore these patterns in more detail, by seeking to quantify the degree of artificial light present at or close to sites, the survey was repeated in January 2014 (Clewley et al., 2015). Additional information on local weather conditions, including temperature, was extracted from the MIDAS Land and Marine Surface Stations Dataset (UK Meteorological Office). Arrival times of the 10 species most commonly recorded during the study were found to be associated with a combination of the density of artificial lights, rainfall, temperature and urban land cover. However, the study failed to find any evidence that birds advanced the onset of foraging in those gardens with more artificial lights nearby. Clearly, there is more work to be done in this area.
THE RISKS OF URBAN LIFE
In addition to the balance of opportunity and risk associated with light and heat pollution, which may alter the longer-term fitness of individual birds, there are other components of the garden environment that may have more obvious and more immediate consequences. These may be revealed by the presence of dead birds, found within the garden. One of the challenges in understanding the levels of predation and disease-related mortality associated with gardens and garden feeding stations is that many dead birds go undetected, especially where scavengers – both avian and mammalian – are present and remove carcasses. It can also prove challenging to determine the ultimate cause of mortality; for example, a bird that is found dead on a patio may have died from colliding with a nearby window or succumbed to disease picked up at a nearby bird table; equally, a bird suffering from the disease trichomonosis and reluctant to move away from a garden feeding station may be more readily taken by a visiting Sparrowhawk. Projects like Garden Wildlife Health, organised by the Institute of Zoology in partnership with the BTO, RSPB and Froglife, can provide some useful information in such cases, with post-mortem examinations revealing both the cause of death and the presence of other contributing factors.
FIG 71. Sparrowhawk predation is just one of the risks faced by garden birds. (Jill Pakenham)
Understanding which factors are the most important drivers of the mortality witnessed within the garden environment is currently hampered by a lack of appropriate data. This issue was first examined in a systematic manner as part of the Garden Bird Health initiative and, latterly, through Garden Wildlife Health (Lawson et al., 2018). These two projects utilised a network of citizen scientists to collect systematic information on mortality incidents in a garden setting, information that could then be used alongside the opportunistic reporting from worried members of the public that has been the more traditional source for information, particularly that relating to disease.
DISEASE AND GARDEN BIRDS
Wherever individual birds congregate there is an increased risk of disease transmission. Because garden feeding stations typically provide a concentration of feeding opportunities within a relatively small area, they may potentially have a role to play in disease transmission (Lawson et al., 2015a; 2018). Additionally, since gardens are a place where people are able to observe birds at close quarters, garden feeding stations may also provide an opportunity to identify the presence of emerging diseases and to assess their impact on populations of wild birds (Friend et al., 2001). Being able to tap into established networks of citizen scientists (see Chapter 6), and to partner these with professional staff working within the fields of animal health, wildlife management and ecology, has facilitated the establishment of disease surveillance schemes, such as the Garden Bird Health initiative and Garden Wildlife Health (www.gardenwildlifehealth.org).
Many existing disease surveillance schemes rely on the opportunistic reporting of wildlife disease by members of the public, and such opportunistic reporting typically secures the greatest potential network of reporters, increasing the chances of identifying unusual, emerging or novel incidents. However, the lack of standardisation makes it difficult to secure important information on the spatial and temporal distribution of incidents, not least because opportunistic reporting is often triggered in response to media appeals, and these may hit one region or audience but miss another. An alternative approach is to secure the participation of citizen scientists in a structured, standardised process – much like the standardised approach used by the weekly BTO Garden BirdWatch survey. This approach also has the benefit that it is often possible to collect baseline information on species abundance (e.g. the host bird species) and on disease occurrence alongside that being collected on disease itself. This approach, sometimes incorporating an additional opportunistic component, has made important contributions to disease surveillance in relation to emerging infectious diseases, such as trichomonosis (Robinson et al., 2010) and mycoplasmal conjunctivitis (Hochachka & Dhondt, 2000). Information on the diseases of garden birds may also be collected through other citizen science networks, such as the network of bird ringers operating within the UK; the availability of such highly skilled volunteers opens up the possibility for background swabbing and surveillance for emerging infectious diseases, and indeed for other types of non-infectious disease.
THE NUMBERS OF BIRDS AND DISEASE INCIDENCE
Work in North America, involving a questionnaire approach to members of the Wisconsin Society for Ornithology, revealed that reported levels of mortality were higher at sites with a large number of individuals using the feeders, and with a larger number of different species present (Brittingham & Temple, 1986; 1988b). Of course, it may simply be that as the number of individuals visiting a feeding station increases, so do the chances of encountering a sick, dying or dead bird. Brittingham and Temple’s work also suggested that observed mortality levels were lower at urban sites than rural ones, and that mortality occurred most frequently at feeding stations where platform feeders were in use. It is likely that platform feeders, which allow birds to stand in food, increase the probability of disease transmission. Hurvell et al. (1974) found that incidence of salmonellosis declined when feeders were cleaned and disinfected regularly, and where the feeder designs used prevented faecal contamination of the food being presented. Regardless of the type of feeder used, it is inevitable that some contaminated food will end up on the ground below the feeders, where ground-feeding species like Chaffinch and Dunnock may be placed at risk. There is also evidence that faecal contamination of nearby vegetation may act as a pathway for disease transmission (Petrak, 1982).
Another approach to exploring the question of disease transmission at garden feeding stations is to examine the feeders and to swab and test for disease agents. Prescott et al. (2000) did this in response to an outbreak of salmonellosis at feeding stations in southern Ontario that occurred over the winter of 1997–98. Prescott and his colleagues scored each of 124 feeding stations for its state of hygiene and swabbed for Salmonella. In the event no Salmonella were isolated from faeces recovered from the feeders. While the research failed to identify any significant differences in the degree of contamination of different types of bird feeder, it did identify that feeder hygiene scores were significantly lower where responsibility for keeping them clean was shared equally between two different people.
FIG 72. Poor feeder hygiene may increase the risk of disease transmission between infected birds. (Jill Pakenham)
SALMONELLOSIS
Salmonella, or more strictly speaking salmonellosis, outbreaks have been documented in wild birds from at least the middle of the twentieth century, with a suggestion that the prevalence of incidents has risen over the past 40 years because of the increasing trend for providing supplementary food at garden feeding stations (Wilson & MacDonald, 1967; Kirkwood et al., 1995; Tizard, 2004). The disease is caused by a bacterium, Salmonella enterica subspecies enterica serotype Typhimurium, which is seen in a number of different forms, known as phage types; definitive phage type DT 40, DT 56 (variant) and DT 160 account for most of the isolates recovered from infected garden birds here in the UK. Prevalence of the disease tends to be greater in those species of garden bird that are granivorous and which forage together in flocks. Although salmonellosis has been recorded in Blackbird, Dunnock and even Green Woodpecker (MacDonald & Cornelius, 1969), such cases are rare.
Examination of a national dataset, largely comprised of reports contributed by the general public, has enabled the seasonal and longer-term patterns of salmonellosis outbreaks to be determined by a team of researchers (Lawson et al., 2010). Some 698 garden birds were examined post-mortem from 1993 to 2003, inclusive. Salmonellosis was confirmed as the primary cause of death in a quarter of the birds examined, from 7 of the 45 different species represented. During the period of the Lawson study, salmonellosis was the most common infectious disease cause of death in garden bird species; this has since changed following the emergence of finch trichomonosis, and the number of salmonellosis outbreaks has reduced significantly since 2008.
Greenfinch and House Sparrow were the two species most commonly diagnosed with the disease by Becki Lawson and her colleagues. The 157 Salmonella isolates cultured through the study revealed the presence of 10 different phage types, with DT 40 and 56 the most common; most of the others were only found in a single individual or came from a single outbreak site. Incidents showed a pronounced seasonal pattern, with a peak in occurrence during the winter months – i.e. between December and February. Over the course of the study period, the prevalence of particular phage types changed; DT 160 was only found during the initial five years of the study, while DT 56 – which had been found sporadically up until 2000 – suddenly increased considerably in its occurrence (Lawson et al., 2010) but then dropped away again. Looking back over a longer period of time, you do get a sense that phage types may come and go; for example, the phage type U 218 seems to have been prevalent within many of the outbreaks reported during the 1967–68 winter (Cornelius, 1969) but not since.
FIG 73. House Sparrow is one of the species for which incidents of salmonellosis have been most commonly reported. (Jill Pakenham)
The Lawson study also suggests regional variation in the level of incidence, with incidents generally absent from across central England and East Anglia, even though House Sparrow and Greenfinch carcasses are regularly submitted for post-mortem analysis from these regions. Although the sample sizes are relatively small, there is evidence of regional variation in the prevalence of phage types within Scotland. Tom Pennycott and colleagues have found phage type DT 40 to predominate in the north of Scotland, while the DT 56 variant is more common in the south of the country (Pennycott et al., 2010). How much this pattern might relate to the species affected – Greenfinch predominates in the north of Scotland, House Sparrow predominates in the south – is unclear.
There is a suggestion that birds in poor condition are more susceptible to the infection, with infected individuals often of low body weight. However, low body weight might instead be a consequence of becoming infected – the birds unable to feed. This needs further investigation, as does the North American finding that more strongly ornamented Common Redpolls Carduelis flammea were more likely to die in the outbreak studied (van Oort & Dawson, 2005). Ornamentation in this species, expressed through the strength of carotenoid pigments, is a signal of male quality – the more brightly marked individuals being of highest status. This being the case, their lower survival during a salmonellosis episode might well be linked to the priority access they are likely to have to food sources during difficult times. Such access might put them at greater risk of ingesting the bacterium.
Regional variation in the distribution of salmonellosis cases has been found within the United States, the authors of this work suggesting that increased human population density and reduced area of wild habitat might be linked to increased incidence. If birds do not have access to natural habitat, but instead forage at garden feeding stations, then there may well be an increased potential for disease transmission, as individuals congregate together to feed under crowded conditions (Hall & Saito, 2008).
One interesting question is the extent to which Salmonella is present in populations of healthy individuals, not least because there appear to be significant differences between samples obtained from healthy birds and those obtained from dead or dying birds. Tizard et al. (1979) isolated the Typhimurium serotype from 15 per cent of the healthy House Sparrows they sampled in Ontario, Canada, but Wobeser & Finlayson (1969) isolated the same serotype from 90 per cent of the dead and dying House Sparrows they sampled from the same area. Although studies of healthy populations have almost all taken place away from garden feeding stations, it does appear that the incidence of Salmonella in healthy populations is low, particularly where these populations exist away from sites of human activity. Here in the UK, Wilson & MacDonald reported on Salmonella infections over a 20-year period, from 1939 to 1959, isolating serotype Typhimurium from just 9 birds of 1,573 sampled. Between 1960 and 1966, the same investigators found an increased incidence, identifying 19 isolates, including 10 from House Sparrow and 4 from Greenfinch (Wilson & MacDonald, 1967; MacDonald, 1965). More recently, the work of Tom Pennycott and colleagues has highlighted the prevalence rates that may be encountered at garden feeding stations, where members of the public are alerted to the problem by the large numbers of birds found sick or dead (Pennycott et al., 1998; 2002). Individual birds infected with salmonellosis collapse and die quickly, often within a few hours; those that survive for more than 24 hours appear lethargic and are reluctant to move away when approached.
One of the reasons for government interest in the diseases of garden birds is that in some cases wild birds may act as a reservoir for diseases that impact human, companion animal or livestock health. Salmonellosis is one such disease. As we have just seen, in garden birds the disease is predominantly caused by Salmonella enterica subspecies enterica serotype Typhimurium phage types 40, 56(v) and 160. While these phage types are considered to be highly host-adapted, with a high degree of genetic similarity among isolates and suggesting that there is only a low risk of transmission to humans or livestock (Hughes et al., 2008), recent research has revealed that wild birds are the primary source of these phage types in some cases of human infection (Lawson et al., 2014). Since most documented outbreaks in wild birds occur at or around garden feeding stations, there is a clear risk to people of coming into contact with sick birds or their faeces. A New Zealand study into an outbreak of S. Typhimurium DT 160 infection in humans revealed that, in addition to consumption of fast food and contact with people with gastrointestinal disease, contact with dead wild birds was a significant risk factor for infection (Thornley et al., 2003).
That there is the potential for Salmonella to be passed on through contaminated faeces is underlined by the finding of the bacterium in 48 per cent of bird faeces collected from a bird table, 42 per cent of those collected from under a hanging bird feeder and from 33 per cent of those found under a House Sparrow roost, all at a garden site in Scotland (Pennycott et al., 2002). It appears that infected birds may shed the Salmonella through their faeces over many days; an outbreak of salmonellosis in Australian sheep was traced to crows and magpies, which were found to have been shedding the bacterium for up to 27 days (Watts & Wall, 1952). James Kirkwood and colleagues have suggested that the winter outbreaks of salmonellosis previously witnessed in the UK were a direct result of the high densities of seed-eating birds seen at garden feeding stations (Kirkwood, 1998), although this is difficult to prove. It does, however, seem likely that the high densities of birds seen at feeding stations might lead to an increased risk of disease transmission.
One of the pathways that may be of particular concern in relation to gardens, bird tables and transmission to humans is the one that sees transmission through gulls. The large increase in gull numbers, and the increasing size of urban breeding populations of certain species, has its origins in the availability of anthropogenic food. Gulls make use of food scraps near fast-food outlets and around landfills, sources which place them at particular risk of ingesting Salmonella bacteria. These may then be shed through their faeces at garden feeding stations, where Black-headed Gull tends to be the most commonly encountered gull species. Although the presence of Salmonella has been determined in a not insignificant portion of the UK gull populations (Williams et al., 1976; Butterfield et al., 1983), most infected individuals show few obvious signs of the infection (MacDonald & Brown, 1983). In fact, it appears that salmonellosis is primarily only a problem in young gulls.
Salmonella bacteria are found within the intestine and so may be spread to other individuals either through contaminated faeces or through predation, where the intestine is eaten by the predator. One Spanish study found that 4 per cent of sampled free-living birds of prey tested positive for Salmonella (Reche et al., 2003), with the range of different serotypes indicating that the infections had been acquired from a number of different sources. Cats are thought to become infected with the wild bird strains of Salmonella enterica through the small birds they predate and there is some evidence that this is the case (Taylor & Philbey, 2010). Salmonellosis in cats has long been called ‘songbird fever’, which is suggestive of the link to the predation of infected wild birds. However, salmonellosis in cats is associated with a wider range of serovars than just S. Typhimurium – though it is the most frequent – and with a range of different phage types, not just those associated with wild birds. Phage types DT 40 and DT 56 variant have certainly been isolated from domestic cats showing evidence of illness (Philbey et al., 2008) but the consumption of raw meat is considered to be perhaps the most important source of the disease in domestic pets. Cats that have become infected display vomiting, anorexia and haemorrhagic enteritis, which usually lasts from two to seven days and follows on from an incubation period of two to five days. Full recovery may take up to three weeks, with a small proportion of individuals – those with impaired immunity – dying as a result of the infection.
FIG 74. Salmonellosis in cats has long been referred to as ‘songbird fever’, underlining the clear pathway from prey to predator. (Jill Pakenham)
TRICHOMONOSIS AND FINCHES
The impact that an emerging infectious disease can have on garden birds is perhaps best illustrated by the outbreak of finch trichomonosis first reported from the United Kingdom in 2005. Trichomonosis, which was already known as a disease of pigeons, doves and some raptor species, is caused by infection with the protozoal parasite Trichomonas gallinae. The parasite typically infects the upper region of the alimentary tract, where it causes lesions of necrotic ingluvitis or pharyngitis; these often result in death, perhaps through secondary infection, starvation or because of an elevated predation risk. Infected birds are unable to swallow food, become lethargic and fluffed up in their appearance, and are often reluctant to fly away from garden feeding stations. The parasite may be transmitted between individuals through shared food – for example, when adults feed their chicks or during courtship feeding – or water. The Trichomonas gallinae parasite cannot survive for long periods outside of the host body because it is vulnerable to desiccation but it has been found to survive for up to two days in moist birdseed (McBurney et al., 2017). An infected bird, unable to swallow, may regurgitate contaminated food items that in turn are then taken by another individual, spreading the disease throughout the population. More widely, trichomonosis has been a significant cause of nestling mortality in the Madagascan Pink Pigeon Nesoenas mayeri and it has also been suggested as contributing to the extinction of the North American Passenger Pigeon Ectopistes migratorius. The disease is known by bird keepers as ‘canker’ (in pigeons and doves) and as ‘frounce’ in birds of prey; you sometimes see academics refer to it as trichomoniasis rather than trichomonosis.
An index case of finch trichomonosis was first documented in the UK in April 2005, emerging from a Chaffinch submitted for post-mortem examination from a garden site in Ayrshire, Scotland (Pennycott et al., 2005a; Lawson et al., 2012a). The following year, summer 2006, saw a dramatic increase in the numbers of mortality incidents involving Greenfinches, Chaffinches and a number of other garden bird species. The Garden Bird Health initiative – a national monitoring scheme being coordinated by the Institute of Zoology, BTO, RSPB and others – reported 1,054 incidents between 1 April and 30 September 2006, involving a combined total of some 6,300 dead Greenfinches and Chaffinches. Confirmation that Trichomonas gallinae was the disease agent came from scanning electron microscopy and DNA sequencing, which later confirmed that a single clonal strain was involved (Lawson et al., 2011a).
FIG 75. The outbreak of trichomonosis in UK Greenfinches was tracked through BTO Garden BirdWatch data and the Garden Bird Health initiative. (Jill Pakenham)
Fortunately, the disease monitoring work was running alongside the already existing BTO Garden BirdWatch survey, which enabled researchers, myself included, to explore the impact of this emerging disease on finch populations. Using data from both BTO Garden BirdWatch and the BTO/JNCC/RSPB Breeding Bird Survey, we were able to show that the disease outbreak had resulted in a significant decline of around 35 per cent of the UK’s breeding Greenfinch population and around 20 per cent of the breeding Chaffinch population (Robinson et al., 2010). This work used information on disease occurrence submitted by members of the public (classed as ‘opportunistic’ records) and those participating in the weekly BTO Garden BirdWatch (classed as ‘systematic’ records). These records also enabled us to identify regions where the disease outbreak was most pronounced, and to chart the movement of the outbreak between these regions over different years. The initial outbreak was largely focussed on the West Midlands, southwest England and Wales during 2006, shifting first to East Anglia and the southeast of England and then Scotland in subsequent years (SAC Veterinary Services, 2008; Lawson et al., 2011a). During this initial outbreak period, there was strong seasonality to the pattern of incidents, with most reported between 1 April and 30 September – and with a peak in late summer – a pattern quite distinct from that seen in salmonellosis.
The impact of the disease outbreak on Greenfinch populations is revealed from the weekly BTO Garden BirdWatch results. When plotted as a reporting rate – a simple measure showing the proportion of garden sites recording the species during a given week – the sudden loss of Greenfinches is evident from September 2006, the impacts carrying over into 2007 (see Figure 76a). When the same dataset is viewed through the numbers of individual Greenfinches seen at garden feeding stations, the longer-term consequences of the outbreak are revealed (see Figure 76b).
FIG 76. BTO Garden BirdWatch reporting rate data show the impact of trichomonosis on garden Greenfinch populations, something that is evident in both (a) the weekly reporting rate, and (b) the number of individuals visiting gardens. Data provided by the British Trust of Ornithology with permission.
TABLE 9. Change in the breeding populations of Greenfinch, Chaffinch and Dunnock between 2006 and 2007, as revealed by the BTO/JNCC/RSPB Breeding Bird Survey, according to disease region. Disease regions were characterised by the number of cases of trichomonosis reported per thousand households and defined as ‘high’, ‘intermediate’ and ‘low’ incidence (after Robinson et al., 2010).
BTO/JNCC/RSPB Breeding Bird Survey data were then used to look at the impact at a wider population level, the survey being the main mechanism for monitoring change in breeding populations for our most common and widespread breeding species. Data from regions with ‘high’, ‘intermediate’ and ‘low’ disease incidence were analysed separately for both Greenfinch and Chaffinch, the two species seemingly most heavily hit by the outbreak, with Dunnock also included in the statistical models as a control. Dunnock was not a species in which significant mortality was being reported, so if it had shown a similar pattern of population change to Greenfinch and/or Chaffinch, then this would have suggested that something else, other than the disease, was behind the changes observed. As hypothesised, Greenfinch and Chaffinch populations showed the most significant declines in the areas of high disease incidence, while Dunnock did not show any evidence of decline (see Table 9). The spatial and temporal changes in populations matched the pattern of disease outbreak and, coupled with the DNA work, strongly pointed to trichomonosis as the agent that had brought about the dramatic and rapid decline in finch populations.
The spread of trichomonosis within the UK was then followed by emergence of the disease elsewhere in Europe, with cases confirmed from multiple sites within southern Fennoscandia during the summer of 2008. Examination of the genetics of the disease agent revealed no variation between the British and Fennoscandian strains of the parasite, suggesting a direct link between the two outbreaks. Examination of ring-recovery data from the British and Irish ringing scheme suggests that a migratory Chaffinch may have been responsible for carrying the disease from its British wintering grounds to breeding sites in Fennoscandia. If we are correct in our assumption, then this would be the first case of a protozoal emerging infectious disease being transmitted by a migrating bird (Lawson et al., 2011a). Both Greenfinch and Chaffinch are widespread across Europe and both undertake medium-distance migratory movements. Trichomonosis was first noted in Finland in 2008 and resulted in a significant (47 per cent) decline in breeding numbers from 2006 to 2010 (Lehikoinen et al., 2013).
The presence of trichomonosis in Sparrowhawks submitted through the Garden Bird Health initiative and the scheme that has since replaced it – Garden Wildlife Health – suggests that these predators may have been exposed to the disease when predating infected finches. The disease has also been diagnosed in a small number of other garden bird species, including House Sparrow, Bullfinch, Siskin, Goldfinch, Yellowhammer and Great Tit (Lawson et al., 2011a). Interestingly, in addition to what we have witnessed here in Europe, trichomonosis has since emerged in several passerine species within North America, with cases documented from 2007 onwards. These cases have largely involved American Goldfinch Carduelis tristis and Purple Finch Carpodacus purpureus (Forzán et al., 2010).
Quite why trichomonosis brought about this novel disease outbreak in UK finches is uncertain, but comparison of the genetics of the parasite – recovered from infected finches and Sparrowhawks – with material held in a sequencing library suggests a spill-over event from a pigeon or dove (Chi et al., 2013). The most likely candidate is Woodpigeon, a species that as we shall see later has been increasing in numbers at garden feeding stations across much of the UK. Trichomonas gallinae appears to be present in a sizeable component of the Woodpigeon population, something suggested by work on wintering Woodpigeons in Spain, where a third of sampled birds shot by hunters were found to be positive for presence of the disease (Villanúa et al., 2006). Prevalence was higher in birds from the south of Spain than the north, and higher in adults than in juveniles, but there was no significant difference between males and females. Parasitised birds exhibited lower body mass and had smaller fat reserves, indicating that they were in poorer condition than non-parasitised individuals.
FIG 77. A scanning electron microscope image of the disease agent Trichomonas gallinae, found to be behind the UK finch trichomonosis outbreak. (Robinson et al. 2010)
There is also the question of why the Greenfinch appears to be so susceptible to the disease when other, equally common, garden bird species seem so much more resilient. The granivorous habits of Greenfinches, coupled with their gregarious nature, may result in high levels of contact between individuals and facilitate disease transmission, but this cannot be the only reason. Perhaps there is something about their morphology or physiology that may make them more susceptible. Jon Barrett, working at the School of Biological Sciences at the University of East Anglia, has done some initial work on this. His findings suggest that the way in which Greenfinches utilise hanging bird feeders may make them particularly susceptible to increased risk of disease transmission, with a suite of behaviours likely to result in transmission of the parasite between individuals (Barrett unpublished). It does, however, seem likely that controlled experiments using captive birds would be needed to take this area of work forward, and that is something that would be unpalatable to many of us working on garden birds and disease.
AVIAN POX AND GARDEN BIRDS
Avian pox is a well-known disease of both wild and captive birds, caused by viruses belonging to the genus Avipoxvirus and known from some 280 species of 70 different bird families worldwide (Thomas et al., 2007). Within the UK, avian pox is considered endemic and has been reported from a number of garden bird species, including Woodpigeon, Jackdaw, Carrion Crow, Starling, House Sparrow, Dunnock, Blackbird and, more recently, Great Tit, Blue Tit and Coal Tit (Lawson et al., 2012b). The virus causes discrete wart-like lesions on the featherless parts of the body, typically on the legs and feet or around the eyes. These lesions are described clinically as ‘dry’ pox, recognising the distinction from the ‘wet’ pox diphtheritic lesions that may form in the respiratory or alimentary systems. Wet pox lesions are rarely reported, presumably because they are significantly less obvious than the external dry lesions. Dry pox lesions are usually pink, red, yellow or grey in colour.
Most avian pox lesions are small and only rarely do they seem to impede the individual affected; in fact, most birds recover – the duration of the infection being from a few days to several months. More recently, since 2006, we have seen Great Tits and Blue Tits with larger lesions, many of which impede vision to such an extent that they are likely to lead to higher levels of mortality. Another unusual feature of these lesions is the number of individuals affected at any given site; while reports of avian pox in birds other than tits usually refer to just a single individual, those linked to tits usually involve several. The reports suggest that Great Tit is the species of tit most likely to be affected – representing, for example, 90 per cent of the incidents reported by Lawson et al. (2012b). From those individuals submitted for post-mortem examination, including the index case from Sussex in September 2006, it has been possible to diagnose avian pox virus as the cause of the infection. The reports also indicate spatial clustering in the cases and a pattern of spread away from the south coast of England, from where the disease was first reported, to areas located further north and west within the UK (Lawson et al., 2012b). As with the work on trichomonosis already mentioned, BTO Garden BirdWatch data have proved invaluable in helping to reveal the pattern of disease spread (Figure 79).
FIG 78. An emerging form of avian pox has been reported in British tit populations, its spread charted through Garden Wildlife Health. (Hazel Rothwell)
These reports of avian pox virus in UK tit species are not the first of their kind within Europe; Great Tits were first reported with avian pox lesions in the early 1970s in Norway, with others reported from Sweden in 2003 and the Canary Islands in 2006 – the latter incident involving an African Blue Tit Cyanistes teneriffae. There has been a marked increase in the numbers of reports of avian pox in Great Tits in several central European countries, including Austria, Hungary, Germany and the Czech Republic. Molecular examinations of the DNA extracted from the skin lesions of two dozen UK Great Tits has revealed that the avian pox virus present here is identical to that documented elsewhere in Europe. Coupled with the south coast origins of the UK outbreak, this points to the arrival of the virus from continental Europe. Since ring recoveries underline the sedentary nature of UK tit populations, leaving little opportunity for interchange between UK and continental tit populations, the question arises as to how this particular avian pox virus reached our shores.
FIG 79. The spread of Paridae pox was mapped and modelled using data from citizen science schemes, demonstrating its origins on England’s southern coast.
It is known that the avian pox virus can be transmitted between individual birds through direct contact, through contaminated surfaces or via an intermediary insect vector – such as a mosquito. In this case, it seems likely that the virus arrived here via an insect vector, pushed across the English Channel within a plume of warm air, much like the way that Blue-tongue disease reached our shores. The seasonality of avian pox in UK tits is similar to that seen in finch trichomonosis, with a peak in records in August and September. The warmer months of summer might facilitate higher levels of disease transmission, since more mosquitoes are likely to be on the wing at this time, though it might also be linked to the entry into the tit population of a cohort of young, immunologically naïve first-year birds.
Although it is still too early to say what the impact of the emergence of this strain of avian pox within the UK might mean for our tit populations, thanks to the long-term monitoring work taking place at Wytham Woods in Oxfordshire, it has been possible to examine the impact on an established tit population (Lachish et al., 2012a). Shelly Lachish and her colleagues were able to show that the pox virus reduced the reproductive output of infected individuals by reducing the ability of adult birds to feed their chicks. Furthermore, the researchers found evidence of transmission from parent birds to their young, leading to significant mortality of those chicks that became infected. Survival rates of individuals with avian pox virus were lower and this meant that the virus had the potential to reduce population growth rates, though not to the extent where a decline in overall population size would then follow. Its presence might, however, reduce the resilience of the population to other external factors that could reduce population size. The work at Wytham Woods also revealed that the avian pox virus became established at the site within two years, reaching a relatively high peak prevalence of 10 per cent of the 8,000 or so individuals caught and monitored by the research team (Lachish et al., 2012b).
LEG ABNORMALITIES IN FINCHES
It is not unusual to see Chaffinches with legs that appear white, rough and thickened, sometimes to the extent that the entire foot is covered in a growth. These lesions have two main causes, the visible symptoms of both being similar in appearance. The first is Chaffinch papillomavirus, which can cause the skin disease papillomatosis, sometimes referred to as ‘tassel foot’ (Atkinson et al., 2008; Gavier-Widén et al., 2012; Prosperi et al., 2016). As the name suggests, the resulting lesions are tassel-like or spiky, developing mostly around the foot and toes but sometimes spreading further up the leg. The second, producing crusty, scab-like lesions, is brought about by a sarcoptid mite belonging to the genus Cnemidocoptes. Several species are known to affect birds, with C. mutans known from poultry, C. pilae known from pet Budgerigars Melopsittacus undulatus, and C. jamaicensis and C. intermedius known from garden songbirds. Mite infestation or cnemidocoptosis, which is sometimes referred to as ‘mange’ or ‘scaly foot’, often results in grey-coloured growths on the toes, feet and legs, very occasionally also appearing on the face.
FIG 80. The leg lesions seen on Chaffinches have two main sources, one a virus and the other a mite. (John Harding/ Becki Lawson)
The skin abnormalities resulting from both sources are thought to develop slowly over a period of time, from several weeks to several months; in the case of papillomatosis these may disappear with spontaneous recovery (Pennycott, 2003). Disease progression in cnemidocoptosis is not well understood and more research is needed to better understand its impacts on garden birds. In both cases, the extent of the lesions can be highly variable, from small discrete lesions through to much larger growths that can result in lameness or put the individual at risk of secondary infection. It is not unusual, for example, to see a Chaffinch that has lost digits or even an entire foot. Both conditions have been documented in the UK since at least the 1960s, with Chaffinch the species most commonly affected. Brambling and Bullfinch have also been reported displaying similar leg lesions, though the incidence of these is much less common than that seen in Chaffinch.
Within the UK, the two conditions appear to be endemic and long-established, with only a small proportion of individuals within any Chaffinch flock likely to be affected – a similar pattern has been noted elsewhere in Europe (Literák et al., 2003). MacDonald & Gush (1975) found a prevalence rate of 14 per cent in their Chaffinch population in Devon. However, epidemic disease has been reported elsewhere: for example, in American Robin in the mid-1990s, where a high proportion of the population was observed to have the lesions (Pence et al., 1999). Diagnosis of the two conditions requires laboratory tests since there is a significant overlap in their appearance and it is entirely possible that some individual birds may be suffering from a mixed infection, with both present.
OTHER DISEASES OF GARDEN BIRDS
Bacteria
Chlamydiosis
Chlamydiosis will be familiar as a disease of mammals – including humans – and birds that is caused by infection with bacteria in the genus Chlamydia. The specific strain known to infect garden birds is Chlamydia psittaci – a different species to that which causes venereal disease in people. It is often recognised as a disease of pet parrots, budgerigars and cockatiels, but is also seen as a disease of pigeons and doves (Thomas et al., 2007). The disease is sometimes referred to as ‘psittacosis’ or alternatively ‘ornithosis’. The first reported case of the disease in wild passerines in the UK came from a garden in the southwest of England, where it was confirmed in individual Robins, Dunnocks and tits (Simpson & Bevan 1989). Subsequently, it has been reported from finches, tits and Robins in a Scottish garden (2008) and from other sites in England during 2009 (one incident) and 2011 (five incidents) (Colville et al., 2012). A review of archived tissues by Beckmann et al. (2012) revealed additional cases and suggested that chlamydiosis may be more common in British garden birds than previously suspected; the disease has also been recorded in a number of other bird species – including Barn Owl Tyto alba, Moorhen Gallinula chloropus and Herring Gull Larus argentatus (Sharples & Baines, 2009).
FIG 81. The first reported case of chlamydiosis in a wild bird in the UK came from a garden in southwest England. (John Harding)
Birds infected with Chlamydia show the usual signs of ill health, being fluffed up and lethargic in appearance. On post-mortem examination infected individuals may show enlargement of the spleen and liver, together with infection of the respiratory tract. The bacteria are likely to be passed from one bird to another through direct contact, ingestion of infected secretions (e.g. faeces) or inhalation of contaminated dust – the bacterium can persist in the environment for many months. The strains of Chlamydia psittaci that affect wild birds do have the potential to cause disease in humans, where the resulting respiratory disease may be displayed through symptoms that can include those associated with a common cold; sometimes the disease may result in flu-like symptoms or more severe chest problems. There have been very occasional reports of disease in dogs and cats associated with Chlamydia psittaci infection, though in many of these cases the source is thought to have been a pet parrot rather than a wild bird.
Escherichia albertii
E. coli serotype O86 – now known as Escherichia albertii – is a bacterium belonging to the Enterobacteriacae which has been recognised in several species of garden bird, both here in the UK and elsewhere in the world. The bacterium may cause inflammation of the stomach and intestines, resulting in diarrhoea and, in some cases, accumulation of food in the crop and oesophagus. While some individuals may show no signs of ill health, others may appear lethargic with fluffed-up plumage. The disease caused by E. albertii infection, which is often referred to as colibacillosis, may result in death and there are occasional reports of epidemic mortality in small birds. Records of the disease from the UK have tended to refer to granivorous species like Chaffinch, Siskin and Greenfinch (Pennycott et al., 1998; 2002; 2005b), with most of these coming from Scotland; it is unclear as to whether this is a genuine geographical pattern or an artefact of sampling effort. The sporadic outbreaks noted in Scotland since the 1990s have tended to occur during the spring months, with reports peaking between April and July.
Suttonella ornithocola
This recently discovered bacterium appears to occur most commonly in the Blue Tit (Kirkwood et al., 2006), though it has also been seen in related Paridae species, such as Coal Tit and Great Tit, and in the Long-tailed Tit (Aegithalidae). It has yet to be diagnosed in other garden bird species. Suttonella ornithocola has been found to cause a pneumonia-like condition in affected individuals, resulting in breathing difficulties and general signs of ill health (Lawson et al., 2011b). The most likely route of disease transmission, given that the bacterium causes a lung infection, is via aerosol or air-borne pathways (Foster et al., 2005). Although the bacterium was first isolated in 1996, when 11 mortality incidents involving a range of tit species were reported from sites across England and Wales, it was not identified as a novel bacterium until 2005. The recent discovery of Suttonella ornithocola means that relatively little is known about it, but national surveillance through the Garden Bird Health initiative and, more recently, Garden Wildlife Health, has identified a small number of more recent incidents. This, coupled with the wide regional spread of the incidents, suggests that the infection is endemic within the British tit population.
Yersiniosis
The diagnoses of this bacterial disease, caused by the bacteria Yersinia pseudotuberculosis, requires culture of the disease agent from the sites of infection within the carcass. The presence of multiple pale areas within the spleen and liver are suggestive of its presence but are not conclusive. Available evidence suggests that the disease is sporadic in terms of its appearance but that it can cause mortality incidents of a localised nature. Infections have been identified in several species of tit and finch, together with Dunnock, Blackbird and Song Thrush (Kapperud & Rosef, 1983; Brittingham et al., 1988b).
Mycoplasma gallisepticum
Although not directly relevant to garden bird populations within the UK, it is worth briefly mentioning mycoplasmal conjunctivitis, the disease caused by the poultry pathogen Mycoplasma gallisepticum, which is a bacterium. This was first diagnosed in North American House Finches in 1994 and it then spread rapidly throughout the eastern United States and Canada. The disease was particularly debilitating and caused very high levels of mortality within the House Finch populations affected. The disease outbreak is of interest because of its parallels with the outbreak of finch trichomonosis here in the UK; both resulted in high levels of mortality, both spread rapidly and both were studied by researchers who used networks of citizen scientists to collect information on the outbreak.
The mycoplasmal conjunctivitis outbreak reached epidemic proportions within three years of emergence, the scale and spread of which was then tracked by a network of citizen science observers coordinated by scientists at the Cornell Laboratory of Ornithology. These efforts were then brought in alongside finer-scale, intensive field studies, which together enabled the researchers to examine the effects of the disease on host behaviour and vice-versa (Dhondt et al., 2005). In the late 1990s, the proportion of infected birds dying fell significantly and asymptomatic infection became more common within the population, though with continuing fluctuations in disease occurrence and annual outbreaks. We might, perhaps, be able to look to the patterns evident within the dynamics of House Finch/mycoplasmal conjunctivitis system – which appears to be density dependent – and learn lessons that might aid our interpretation of how the Greenfinch/trichomonosis system might play out (Hochachka & Dhondt, 2000). One other interesting aspect of the work on this disease relates to the risk factors associated with it; in addition to seasonal risk factors – an increased risk associated with the cooler non-breeding period from September through to March – there was an increased risk associated with the provision of food in hanging, tube-style feeders, suggesting that transmission rates might be higher where these were used (Hartup et al., 1998). The role of food provision in disease transmission is something that we explored in Chapter 2.
A number of other bacteria have been reported from garden birds, which is unsurprising given the broad intestinal bacterial flora that one would expect to see. Those that tend to be mentioned are the ones that pose a potential threat to human, companion animal or lifestock health. These include various species of Pseudomonas, Staphylococcus and Streptococcis, all of which are of human and livestock health interest (Brittingham et al., 1988b). Detecting the presence of these bacteria in live birds involves catching the birds to collect cloacal swabs, something that could be deployed within the UK at a wide spatial scale through the national ringing scheme, if needed. Bird ringers are highly trained and licensed to catch wild birds, making them an ideal group to involve in the collection of samples through swabbing.
Viruses
One of the groups of viruses that is giving particular cause for concern is the flaviviruses, which includes both West Nile virus and Usutu virus. These viruses show the ability to evolve rapidly when presented with the opportunity to occupy a new ecological niche, something that can lead to large-scale disease outbreaks (Vazquez et al., 2011). The mosquito-borne Usutu virus neatly illustrates the threat that such viruses might pose. First isolated from mosquitoes in South Africa in 1959, it was not at that time associated with disease in humans or animals. However, when it emerged in Austria in 2001, it resulted in epidemic mortality in Blackbirds (Chvala et al., 2007) and subsequent work has suggested an earlier arrival in Italy in 1996. The northward expansion of the virus has continued, reaching Germany in 2011 and resulting in large-scale mortality of wild birds in the Netherlands in 2016 – this time with at least 1,800 Blackbirds dying across eight provinces (Rijks et al., 2016). Screening of wild birds here in the UK has yet to document the arrival of Usutu virus but given the scale of Blackbird and other bird movements between the UK and continental Europe, it is highly likely to reach us soon. Certainly, the species of mosquito involved in transmission elsewhere within Europe is present in the UK (Horton et al., 2012).
UK researchers have also been screening for West Nile virus (Phipps et al., 2008), a disease which has had a significant impact on the population trajectories of a number of North American bird species, including the American Crow, which declined by 45 per cent in the six years after West Nile virus arrived (LaDeau et al., 2007). Should the virus reach the UK, then we might expect to see similar patterns of decline in garden corvids, like Jackdaw, Rook and Carrion Crow, plus possibly other species including thrushes and Blackbirds. This is another mosquito-borne virus, seemingly expanding its range in response to a changing climate.
Parasites
We have already seen the impact that a parasite – in the form of Trichomonas gallinae – can have on a wild bird population but this impact is small when compared with the impacts of another group of parasites, the Plasmodium species, which cause malaria. Transmitted by insect vectors, notably mosquitoes, malaria is widely recognised as a threat to human, animal and bird populations. The infection rate in bird species has been studied over many decades, avian malaria being a key model for researchers, and this information has recently been used to examine the extent to which a changing climate might alter malaria prevalence at a global scale (Garamszegi, 2011). The results of this work demonstrate that birds are at an increasing risk of malaria infection as a direct consequence of the changing climate, with the effects being felt most strongly within Europe and Africa. In addition to the impacts of a warming climate on the insect vectors, warming temperatures may also benefit the malaria pathogens more directly – the pathogen incubation period is blocked completely when temperatures drop below 15°C.
Of course, parasites are just as likely to be encountered on birds living away from gardens and the built environment. Some may show particular habitat associations, perhaps being more prevalent at sites close to water, but relatively little work has been done comparing the infestation patterns of parasites between urban (garden) and rural sites. Reporting on differences in the prevalence of tick infection across 11 paired urban and rural Blackbird populations from across Europe and North Acfrica, Evans et al. (2009b) found large and consistent reductions in both tick prevalence and intensity within urban areas. Grégoire et al. (2002) also found a difference between the infestation patterns of Ixodes ricinus ticks on Blackbirds living in urban and rural locations; infestation was much higher in rural populations (74 per cent) than urban ones (<2 per cent). The researchers attributed this to possible differences in tick survival between the two habitats or to differences in the availability of other hosts. Blackbird densities were higher in the urban habitat, suggesting that the density of this particular host was not related to the presence of the ticks. However, densities of final hosts – such as Hedgehog Erinaceus europeaus, Red Fox Vulpes vulpes and Roe Deer Capreolus capreolus – are likely to be significantly lower in gardens than they are in the wider countryside.
Tick infestation rates are important, not just because of the potential harm to host birds, but also because they may carry the bacterium Borrelia burgdorferi, the causal agent of Lyme disease. A study of 1,229 birds of 22 species, caught in a rural residential area in Scotland, found 29 per cent of the individuals examined were carrying larval ticks and 5 per cent were carrying nymphs (James et al., 2011). Although the larval ticks were more difficult to remove to test for the bacterium, 8 per cent of the 24 sampled tested positive for Borrelia burgdorferi. At 20.6 per cent, prevalence of the bacterium was higher in the larger sample of 107 nymphs tested. Looking at what these results mean for the birds themselves, this suggests infection rates range from zero (Coal Tit) to 77 per cent (Blackbird), with ground-feeding bird species tending to show higher rates of infestation with infected ticks than those that feed arboreally in trees and shrubs.
FIG 82. Urban Blackbirds carry lower numbers of ticks than their wider countryside counterparts. (John Harding)
Along with ticks, the other obvious external parasites of many garden bird species are fleas, which may be encountered when people come to clean out nest boxes at the end of the breeding season. The flea species found in nest boxes and natural cavity sites overwinter as pupae within cocoons, their emergence in spring triggered by rising temperatures and by the vibrations caused by visiting birds. After emergence, the fleas mate and the females then go in search of a meal of blood, necessary for the maturation of their eggs. Feeding throughout her life, a female flea will lay 2 to 5 eggs per day, resulting in infestations that can reach up to 800 fleas per nest box – though more typically averaging just 80.
The presence of fleas in an occupied nest box may reduce the growth, body mass and condition of nestling birds (Dufva & Allander, 1996), something that is usually compensated for by increased provisioning on the part of the parent birds. Tripet et al. (2002), working on Blue Tits, found that a high density of fleas reduced nestling weight during the early nestling stage but that these costs were fully compensated for by an increase in female feeding effort. Interestingly, the male Blue Tits did not increase their frequency of food provisioning to nestlings in heavily infested nests. The increased feeding effort put in by the female Blue Tits has consequences for their future reproduction (Richner & Tripet, 1999). In some years, however, where favoured invertebrate prey are scarce, the parents may be unable to provide sufficient food to counter the impacts of the fleas, resulting in chicks fledging in poor condition (Richner et al., 1993). There may also be an effect within a season, with second broods suffering more from higher levels of flea infestation as flea numbers increase throughout the summer.
Birds are not defenceless when it comes to those parasites that live on the outside of the body. The oily secretions of the uropygial gland, which are used to insulate and waterproof feathers during preening, have been found to also retard the growth of bacteria and fungi that may damage the plumage (Jacob & Zisweiler, 1982; Shawkey et al., 2003). Individuals may also modify their behaviour in response to the presence of ectoparasites: for example, by selecting nest and roost sites that hold fewer parasites (Christe et al., 1994; Merilä & Allander, 1995), by removing old nesting material from a newly secured nest site (Mazgajski et al., 2004) or by increasing their levels of grooming behaviour (Cotgreave & Clayton, 1995). Various bird species, including Starling, have also been recorded adding sprigs of green vegetation to their nests (Clark, 1990); one of the leading hypotheses explaining this behaviour is that birds preferentially select plant species that contain volatile chemicals with insecticidal properties and add these to the nest material in order to reduce the numbers of parasites. Work by Clark (1991) revealed that mite populations were significantly higher in Starling nests from which any greenery present was experimentally removed. A neat experiment looking at Yarrow Achillea millefolium, one of the plants sometimes added to Starling nests and known to be rich in volatile compounds, investigated this further (Shutler & Campbell, 2007). The experiment was carried out using nesting Tree Swallows Tachycineta bicolor, a species that doesn’t add material to its nest – and thereby removing several potentially confounding effects linked to other hypotheses concerning the role of green material. Addition of the Yarrow was associated with a significant reduction in the numbers of nest ectoparasites.
PLUMAGE ABNORMALITIES
It is not unusual to see a garden bird showing some form of plumage abnormality; while many of these are simply the bird going through the normal process of feather replacement, there are occasions where disease, a parasite or some other factor is involved (Keymer & Blackmore, 1964; Blackmore & Keymer, 1969). Robins and Blackbirds are the two species in which, within the UK, plumage abnormalities are most often recorded. The degree of feather loss or damage may extend from just a few feathers – for example, around the beak or eye – through to the loss of feathers from the entire head and part of the neck (Soper & Hosking, 1961). A number of the cases examined to date – for which it was possible to carry out post-mortem examination – have revealed the presence of fungi. In one instance, the fungal hyphae were shown to have infiltrated the superficial layers of skin and the feather follicles, suggesting that the fungus was responsible for the observed feather loss (Keymer & Blackmore, 1964).
Feathers may also be damaged by the activities of ectoparasites, most notably chewing lice (Mallophaga, and part of the Phthiraptera), the damage sometimes sufficient to be seen with the naked eye on birds visiting garden feeding stations. Many different types of chewing lice are to be found on birds, and an individual bird is likely to be parasitised by a number of different species of louse. At least six different louse species, belonging to five different genera, may be found on a Rook. Some feed on both feathers and blood, the latter often obtained from developing feathers; others live within the feather quill and feed on the pith. Each species of louse tends to show adaption to living within the feathers of its host, sometimes even to particular feather tracts; for example, species found on the head and neck are typically more rounded in appearance than those species which live within the wing feathers, the latter being elongated and flattened dorso-ventrally. Such is the strength of the evolutionary relationship between louse and host that knowledge of louse taxonomy has sometimes been used to assess the taxonomic placement of its avian host.
FIG 83. Plumage abnormalities may be seen in many garden bird species and may involve loss or damage to feathers or changes in plumage colouration, as in this House Sparrow. (John Harding)
PSITTACINE BEAK AND FEATHER DISEASE
Psittacine Beak and Feather Disease (PBFD) is caused by the Beak and Feather Disease virus, which is one of the Circoviridae viruses. It has been known from both captive and free-living parrots since at least the 1970s, with cases recorded from nearly 80 parrot species worldwide (Fogell et al., 2016). The only UK species likely to be affected by PBFD is the Ring-necked Parakeet, an introduced species, and this was confirmed in 2012 when an infected individual, showing the characteristic feather loss across the head and body, was reported from London (Sa et al., 2014). A small number of cases of Ring-necked Parakeets with plumage abnormalities have been reported through Garden Wildlife Health since then, with PBFD suspected as the causal agent. Further research is needed to establish whether BFDV is well established in the UK parakeet population – but with only infrequent disease – or is still emerging. Although there does not appear to be any risk to other UK bird species, it is worth noting that cases have recently been confirmed in a Rainbow Bee-eater Merops ornatus and a Powerful Owl Ninox strenua in Australia, where the disease is thought to have originated (Sarker et al., 2015; 2016).
BEAK ABNORMALITIES
The avian beak is a key tool, its size and shape linked to the bird’s feeding preferences, and so it is unusual to encounter an individual whose bill is substantially different from others of its kind. Such individuals can look very different and may show a degree of abnormality that reduces their chances of feeding successfully (Pomeroy, 1962). There are a number of recognised deformities that may occasionally be seen in those birds visiting garden feeding stations. These are usually described by the resulting appearance of the deformity, rather than the underlying cause.
Bill deformities arise in part because a bird’s bill grows throughout its life, but the reason why this sometimes goes awry is often unclear. A number of possible reasons have, however, been put forward (Galligan & Kleindofer, 2009). Included within these is exposure to an environmental contaminant, such as an industrial pollutant, insecticide or herbicide. While such compounds have been implicated in the occurrence of bill deformities, strong evidence is lacking. Physical trauma, such as collision with a window, has also been suggested (Pomeroy, 1962; Olsen, 2003), but again clear evidence to substantiate this suggestion is lacking. Another possible cause is a nutritional deficiency (Tangredi, 2007) – particularly where related to calcium metabolism; nutritional deficiency could also include the absence of some textural component in the diet, since it is known, for example, that without access to bones, captive birds of prey may suffer from overgrowing mandibles – the bill tip is presumably shaped through abrasion when picking at a bone.
In excess of three dozen bird species have been recorded with beak deformities through the BTO’s ‘Big Garden Beak Watch’ survey – an opportunistic reporting scheme collecting information on bill deformities in garden birds. Blackbird and Blue Tit are the most commonly reported species showing deformities, but others include Coal Tit, Goldfinch and Long-tailed Tit.
Types of deformity
Crossed mandibles are an infrequent abnormality – I have seen just three examples in two decades of catching and ringing wild birds – and result in the upper mandible becoming down-curved, while the lower mandible becomes up-curved, the two crossing each other. This gives the bird the appearance of a Common Crossbill Loxia curvirostra, where the crossed mandibles are an adaptation enabling the Common Crossbill to extract and feed on conifer seeds. Related to this abnormality is one where just one of the mandibles grows beyond the point at which it would normally meet the other mandible, resulting in an extended and curving shape. In many cases where just a single mandible curves well beyond its usual shape, there is evidence of damage to the tip of the other mandible (Pomeroy, 1962). Overgrowth of the upper mandible appears to be more common than overgrowth of the lower mandible. In a few cases, one or both of the mandibles may curve in the opposite direction, such that, for example, the upper mandible grows up and over the head. Pomeroy (1962) reports a Starling whose upper mandible was curved back so strongly over its shoulder that in flight it appeared as if it was carrying a stick.
FIG 84. Bill deformities are unusual but do get reported from time to time, often by garden birdwatchers or bird ringers, both of whom get to see birds at close quarters. (Mark Grantham)
Elongation of both mandibles is probably less common than the curving of one or other mandible. This is nearly always associated with a slight down-curving of the whole beak and usually involves the elongation of both mandibles equally. Starling appears to be the species in which this abnormality is most commonly reported. These elongated bills may be prone to damage, the end section breaking off. Not all of the abnormalities may occur along the usual angle of the bill. In some cases, there may be lateral curvature with one or other mandible growing to the right or to left.
It appears that in most instances the bony parts of the beak remain unaffected, the abnormalities occurring in the middle layer (the dermotheca) and the outer keratinous sheath (rhamphotheca). One of the most interesting developments in this area of research is the work that has been done recently in North America, where researchers have documented a significant cluster of cases in Alaska, the bulk of which are from just two species: Black-capped Chickadee and Northwestern Crow Corvus caurinus. Chickadees are the North American relatives of the tits, with the Black-capped Chickadee being similar in size and appearance to our Coal Tit. The discovery of this cluster in the 1990s, which could have signalled a wider problem within the region, prompted the establishment of a comprehensive research programme. The North American researchers coined the term ‘avian keratin disorder’ to describe what they were seeing. Alongside the beak abnormalities, they also noted abnormalities in the plumage, legs, feet and claws of some individuals (Handel et al., 2010).
The Alaskan outbreak appears to have started in the early 1990s, increasing exponentially until about 2000, and then levelling off. With several thousand reports of chickadee beak deformities from the affected area – compared with just a few dozen from elsewhere in North America, this was a significant event. Examination of chickadees and crows by trained bird ringers (termed bird banders in the United States) suggests that the deformities do not begin to appear until individuals are at least six months old. The use of bird ringing also means that it has been possible to establish that individuals can suddenly develop a beak deformity after several years of seemingly normal fortunes. The levels of beak deformities being seen echo two previous instances in North America, both of which were associated with exposure to contaminants – selenium in California and organochlorine compounds in the Great Lakes. Having said this, the virtual absence of beak deformities among young birds in the Alaskan study area would seem to suggest a different proximal cause. Indications from the opportunistic work taking place here in the UK might suggest a recent increase in bill deformities in Blue Tits, making the Alaskan work all the more relevant.
The presence of a bill deformity can make it difficult for a bird to feed, or indeed to preen. Birds with damaged beaks may be attracted to garden feeding stations because of the easier foraging conditions. At least some individuals can compensate for their deformity, perhaps by feeding with their head tilted to one side. Difficulties in preening may lead to increased numbers of parasites, making the individual less efficient at flying or leading to a general deterioration in their health.
HYGIENE AND REDUCING THE RISK OF DISEASE TRANSMISSION
As we have seen earlier in this chapter, many of the common diseases of garden birds outlined above may be spread through food contaminated with the saliva or faeces of infected individuals. It follows that the risk of a disease being transmitted between individuals will increase where large numbers of birds gather together to feed at the same sites, day after day. In order to reduce the risk of disease transmission, you should use several feeding sites, so that the numbers of individuals at any one site are reduced. Rotating the sites, effectively splitting periods of use with rest periods, should also help to reduce levels of disease transmission, as should the regular cleaning of feeders and bird tables with an appropriate product. Such products include a weak solution of domestic bleach (5 per cent sodium hypochlorite) or professional veterinary products such as Ark-klens or Tamodine-E.
Feeder design may also influence disease risk, with the flat surfaces of bird tables and hanging feeder trays potentially posing a greater risk – through faecal contamination – than a hanging feeder alone. Feeder design can also determine how easy a feeder is to take apart and clean; if it is difficult or impossible to take apart, then the cleaning is unlikely to be thorough, leaving an increased risk of future infection (Feliciano et al., 2018). Some of the feeders now on the market have been designed with cleaning in mind, coming apart easily. Bird baths may also be a site for disease transmission and so should be cleaned and refilled regularly.
Albeit small, the risk to human health means that you should not use the brushes, cloths, buckets or other equipment used for cleaning bird feeders for any other purpose. They should be used and kept outside and you should wear rubber gloves when handling the feeders, washing your hands and forearms thoroughly afterwards. Feeding equipment should be rinsed after cleaning and then left to air-dry before being refilled. A similar approach should be adopted for birdbaths.
FIG 85. Garden feeding stations may increase opportunities for diseases to spread between individuals. Keeping feeders and bird tables clean should be a regular part of providing food for garden birds like these Tree Sparrows. (John Harding)
MYCOTOXINS AND GARDEN BIRDS
Detectable levels of aflatoxin – a type of mycotoxin – have been found in garden bird species, such as Greenfinch and House Sparrow, within the UK (Lawson et al., 2006). These toxins are produced as secondary metabolites by several different species of fungus, some of which may be found in grain and other food crops (e.g. peanuts and maize) destined to enter the human, domestic animal or wild bird food chain. Aflatoxins are produced by Aspergillus flavus and Aspergillus nomius, and as a group include aflatoxin B1 and aflatoxin B2. Aflatoxin B1 has been described as the most prevalent naturally occurring, acutely toxic and carcinogenic member of this group (Smith & Ross, 1991). While aflatoxins tend to be seen most often in peanuts and maize, they can also be found at high levels in wheat, barley and oats if the cereals are of low quality. Production of aflatoxins is influenced by storage and handling conditions, and by the local environmental conditions, such that it is greatest in the warm environments seen in many tropical areas. Interestingly, Thompson & Henke (2000) showed experimentally that the production of aflatoxin on maize could occur under the cool-dry conditions (a temperature of 14–18°C and a relative humidity of 35–40 per cent) typically witnessed within the UK. Testing for aflatoxins in foodstuffs is largely geared to the human and domestic animal food chain, with maximum permitted levels stipulated under core legislation and regulations. The maximum permitted level for aflatoxin B1 in the UK is set at 20 ppb (parts per billion), so in theory the wild bird care products on sale in the UK should not contain levels above this.
The toxic effects of aflatoxins vary depending upon the toxin involved (for example, aflatoxin G2 shows just 10 per cent of the toxicity of aflatoxin B1) but are also determined by the size of the dose ingested and the species and health of the animal or bird involved (Gourama & Bullerman, 1995). The relative susceptibilities of different garden bird species to these toxins have yet to be determined, but experience for other species suggests that it can be difficult to predict whether or not a species will be particularly susceptible. The toxic effects are felt in the liver, with affected birds typically displaying the clinical signs associated with liver disease. They can also impact on the ability of the blood to clot (Pier, 1992) and lead to immunosuppression, weight loss and general ill health.
The significance of the aflatoxin residues found in House Sparrows and Greenfinches by Lawson et al. (2006) is unclear. Although no evidence of the liver disease consistent with aflatoxicosis was observed by Becki Lawson and her colleagues, most of the birds found to have the residues also showed signs of infectious disease (namely salmonellosis), something not seen in a similar sample of birds for which the cause of death had been determined as ‘predation’ or ‘other trauma’. This might suggest that aflatoxin poisoning could weaken an individual’s immune response but this is something that will require further investigation.
Another area where more work is needed is the presence of aflatoxins in the wild bird food chain. A small amount of work has already been done in this area, both here in the UK and elsewhere. Scudamore et al. (1997), for example, tested 15 samples of wild bird food purchased in the UK, of which one sample (some peanuts) was found to contain some 370 ppb of aflatoxin B1. Killick et al. (unpublished) carried out a pilot study to test both branded and non-branded wild bird feed mixes for aflatoxins. This work tested the mixes when opened and, additionally, during exposure to UK climatic conditions. Aflatoxin concentrations of 24 ppb (aflatoxin B1) and 5 ppb (aflatoxin B2) were found in a sample of non-branded peanuts when opened. Higher levels, 341 ppb (aflatoxin B1) and 49 ppb (aflatoxin B2), were found in a sample of non-branded peanuts exposed to UK climatic conditions for two months. As part of our review of garden bird disease, we screened food residues from a sample of bird feeders and found detectable levels of aflatoxin in all seven samples (Lawson et al., 2018). Two of these greatly exceeded the maximum permitted limits set for such residues in peanuts destined for livestock feed – which includes wild bird food – and it therefore seems likely that garden birds may be exposed to these toxins at levels associated with the kinds of toxic effects noted in captive birds. A larger piece of work, looking across a wider range of the wild bird feeds on the market and covering some of the other climatic conditions experienced in the UK, would be timely.
A study of wild birdseed purchased in the US state of Texas revealed aflatoxins in 17 per cent of the 142 samples tested, with levels ranging from non-detectable up to 2,780 ppb (Henke et al., 2001). Aflatoxin poisoning has been linked to mass mortality incidents in wild birds in North America, including Mallards in Texas in the late 1970s (Robinson et al., 1982) and geese in Louisiana during the 1998–99 winter (Cornish & Nettles, 1999), the latter incident involving in excess of 10,000 individuals. Given the potential risks to wild birds associated with the mycotoxins this is an area where more research is urgently needed, once again underlining the need to better understand both the opportunities and potential risks associated with feeding wild birds.
WINDOW STRIKES
Collision with windows and other structures can cause significant mortality in some urban areas (Klem, 1990b; Ogden, 2002) but its impact on wider populations has yet to be determined. Daniel Klem, largely working in Illinois, estimates that the annual mortality resulting from window collisions in the United States is between 97.6 and 975.6 million individuals annually (Klem, 1990b) – we lack a corresponding figure for the UK. These are staggering figures and underline the urgent need to secure more information on both the scale of the problem and on opportunities to mitigate its impact. If correct, it is likely that collision with window panes is the second most important human-related cause of mortality in birds (after hunting).
The information that birds extract visually from the environment can be quite different from that which we humans extract, something that reflects the fundamental differences between birds and primates in terms of the structure and organisation of their respective visual systems (Martin & Osorio, 2008; Martin, 2011). There are, for example, significant differences in the perception of colour, the degree of resolution (acuity) achieved, determination of the position of an object relative to the animal, and in field of view.
The use of small sheets of glass as window panes can be traced back to at least 290 ce, but it was not until 1903 that the production of large sheets of glass for windows became commonplace. These appear to be effectively invisible to an approaching bird and many individuals collide with them at velocities that are likely to result in the collision being fatal. It has been suggested that fatal velocity may be reached at distances of substantially less than a metre (Klem, 1989). Although window collisions occur throughout the year, across many different types of window and under a range of different circumstances, there are some general patterns, providing insight into why such collisions can occur.
FIG 86. Large patio windows, particularly those with bird feeders positioned close by, pose a risk to garden birds and can result in window strikes. (Mike Toms)
Examination of published studies suggests that half of all bird/window collision events result in mortality (Burton & Doblar, 2004; Gelb & Delacretaz, 2006; Bracey, 2011). Mortality rate does not appear to be influenced by the age or gender of the bird, but there is a suggestion that both behaviour and species – the two are linked – can play a role. For example, Drewitt & Langston (2008) found that species that are more active closer to the ground are more likely to collide with a window than those that are active higher within the canopy. Those (typically granviorous) species that are attracted to garden feeding stations, which are often positioned close to windows, are likely to be at greater risk of collision than insectivorous species that feed within vegetation.
Birds may not see a window, either because they can see straight through it to what is on the other side or because they can see the sky, vegetation or something else reflected in the window and fly towards this. It has been suggested that there are more collisions when the glass reflects nearby vegetation (Gelb & Delacretaz, 2009). The quality of this reflection will be determined by the nature of the glass itself and by local conditions, the latter including both local weather conditions and the degree of shading that the window receives. A particular problem may be where a bird can see through one window to another and beyond, thus establishing the illusion of a ‘passageway’ through the building. A special class of window strikes are those relating to birds attracted to lit windows at night – this particular problem is only really associated with high-rise office buildings (and lighthouses) and not with domestic properties, so will not be covered here. It is, however, likely to be an important cause of mortality for some species of nocturnally migrating bird.
If a bird moves towards a window, either from a starting position on a nearby bird feeder or from vegetation, then you might imagine that the distance from the bird to the window at the point at which it takes flight might influence whether or not a fatal collision will result. As we have already seen, Daniel Klem suggests that fatal velocity is achieved within a short distance (perhaps as little as 30 cm). Other researchers have found an increasing collision risk, and associated mortality, with distance from the window. Hager et al. (2013), for example, found an increase in collisions with feeders positioned from 5 to 10 m from the window, with a peak in fatalities when the feeders were positioned at 10 m from the window. Evans Ogden (1996) suggests a distance of from 4 to 10 m as being fatal for small birds.
Fatalities are thought to be the result of internal haemorrhaging, the bird typically striking the window head first (Klem, 1990b). Despite the ‘loose-necked’ appearance of a freshly dead bird, there is nothing to suggest that a broken neck is a common cause of death in such collisions. Of those birds that do survive the collision, at least initially, some may subsequently die from internal injuries, while others may be predated while they are lying prone and stunned on the ground beneath the window. It is likely that a sizeable proportion of window-strike casualties will be scavenged by predators; this suggests that the levels of mortality recorded in published studies are conservative estimates, with the true impact of window collisions potentially that much greater.
When it comes to attempts to reduce the incidence of collisions, there have been various recommendations and a number of commercially available ‘solutions’. Avery (1979) concluded that the presence of drawn curtains and/or net curtains could reduce collision risk, but the work of Evans Ogden (1996) and Stanyon (2014) suggests that this might not be the case. One of the most commonly used commercial ‘solutions’ is the use of sticker silhouettes, usually presented in the shape of a flying falcon or ultraviolet reflecting shape. The generally accepted wisdom within the published literature is that such devices are ineffective, the bird simply avoiding the sticker but still colliding with a different part of the window. There is even the suggestion that such stickers might make a collision more likely, since the bird will be distracted by the sticker and less likely to spot the presence of the glass (Stanyon, 2014). Other potential solutions, for example changing the angle of the window to 20–40° from vertical or adding a grid of dots or lines to the glass, may be more effective. While the former may cause engineering or design issues, the latter option could be more acceptable to homeowners, who see windows as a view into the outside world. Since humans cannot detect UV light but birds can, these patterns of dots or lines could be created from UV-absorbing or UV-reflecting materials, making them invisible to the human eye – unless light conditions inside the house are stronger than those seen outside (Buer & Regner, 2002; Klem & Saenger, 2013). Since the placement close to a window of features attractive to birds, such as bird feeders, berry-bearing vegetation or water, increases the risk of a window strike, it follows that removing such features should reduce the risk of a collision (Klem, 1991).
A special case of window collisions is those linked to anti-predator escape flights, where a bird is panicked by a predator and is flushed from its perch into the glass. Erica Dunn (1993) estimated that 16 per cent of the collisions documented in her study were the result of birds panicked by a predator. On some occasions, the pursuing predator may also collide with the window, something that is seen from time to time by those taking an interest in their garden birds here in UK gardens.
There are other objects with which birds may collide within gardens and the wider urban landscape that sits around many of them. Collision with motor vehicles, with wires, netting and with micro-turbines (generating wind energy) may also be responsible for mortality.
PREDATION
Garden birds are likely to experience predation in a similar way to that seen within the wider countryside. However, its impacts at the population level may differ because of differences in the predator species involved and in the degree of isolation of garden populations from those elsewhere. Predator populations tend to be limited by the availability of their prey but this isn’t usually the case for domestic cats, which have a ready supply of food at home, and so their impacts may be greater than those of a Stoat Mustela erminea or Magpie, for example. Similarly, a population may be able to sustain high levels of predation under certain circumstances, perhaps where the population would normally be limited by some other factor (such as competition for food), or because it is sustained by recruits from elsewhere. As we shall see in this section, the interactions between garden birds and their predators may be complex, and there is still much for us to learn about the impact of predation on those birds using the garden environment.
While predator communities are likely to differ between urban and non-urban landscapes, it is important to recognise that not all gardens are urban; many are on the urban fringe and others are entirely rural in nature. It is not possible, therefore, to make generalisations about the levels of predation encountered within gardens and about how these might compare with the wider countryside. What we can say, however, is that the pattern of predation within an individual garden – and the predators responsible for that predation – is likely to be shaped by the nature of the surrounding landscape (Thorington & Bowman, 2003). There is good evidence, for example, that urban landscapes have higher densities of cats (Gaston et al., 2005a; Sims et al., 2008) and corvids (Jerzak, 2001; Antonov & Atanasova, 2003), and this might have an impact on the levels of predation experienced within this habitat.
SPARROWHAWKS
The Sparrowhawk is a specialist predator of small birds, whose English breeding population increased by 118 per cent between 1975 and 2014. This increase in abundance has been brought about through improved breeding success, following a decline in the use of those organochlorine pesticides linked to a reduction in eggshell thickness across a number of bird of prey species (Newton & Wyllie, 1992). The recovery of the Sparrowhawk population was largely completed by the mid-1990s, with recolonisation of its former breeding range (Balmer et al., 2013) and an increased use of garden sites (Chamberlain et al., 2005). Data from the BTO/JNCC/RSPB Breeding Bird Survey indicate that the breeding population has subsequently been in decline since 2006. The recovery of the Sparrowhawk population, and in particular its timing, has led some authors to suggest a causal link with the decline in UK House Sparrow populations (Bell et al., 2010).
Sparrowhawks certainly do take House Sparrows and other garden birds, their presence in the vicinity of garden feeding stations sometimes triggering a strong emotional response from those garden birdwatchers who put out supplementary food to attract small birds into their gardens. On occasion, this has helped to feed the vigorous debate around the possible role of Sparrowhawk predation in the decline of urban House Sparrow populations. Although Sparrowhawk predation can remove a large number of individuals from a prey population, there is little evidence that this ‘harvest’ leads to any obvious depression of the breeding population the following year.
The effect of predators on their songbird prey has generally been assumed to compensate for individuals that would have otherwise succumbed to other forms of mortality. Evidence for a compensatory effect in relation to Sparrowhawk predation may be found through the analysis of data on post-breeding populations of tits, sparrows and other small birds. The work of Perrins & Geer (1980) and of Newton et al. (1998), for example, has revealed the local effects of an increasing Sparrowhawk population on non-breeding tits and other woodland species. These studies identified a shift in the seasonal pattern of songbird mortality, a reduction in the size of the post-breeding population and a change in the main agents of mortality, following recolonisation of sites by Sparrowhawks. Despite the Sparrowhawks taking up to a third of the young tits produced each year, their impact on the size of the breeding population in subsequent years was immeasurably small.
FIG 87. The Sparrowhawk is a specialist predator of small birds, and may visit garden feeding stations in search of prey. (John Harding)
Work looking at garden bird populations, and using data from the BTO’s Garden Bird Feeding Survey (see Chapter 6), provides some additional insight into the question of Sparrowhawk predation and House Sparrow decline. Chamberlain et al. (2009b) and Bell et al. (2010) both analysed Garden Bird Feeding Survey data but found contrasting results, perhaps because of the different methods used or because of a failure on one or other part to properly isolate the impact of predation from other confounding factors. Chamberlain et al. (2009b) found no significant effect of Sparrowhawks on House Sparrows, when accounting for temperature and the number of bird feeders provided at the Garden Bird Feeding Survey sites studied. Bell et al. (2010) found significant negative effects of Sparrowhawks on House Sparrows but failed to account for any additional environmental covariates in their models. A piece of work by Newson et al. (2010), using a different modelling approach and a different dataset, also failed to find any evidence that House Sparrow breeding population declines were linked to an increasing Sparrowhawk population.
The development of new statistical approaches has enabled us to look again at the Garden Bird Feeding Survey data, which is probably the best dataset available to address the question of Sparrowhawks and garden bird populations (Swallow et al., 2016a; 2016b). The results of this work suggest that, after controlling for the effects of environmental factors such as weather and surrounding habitat, there is still an additional negative effect of Sparrowhawks on House Sparrow populations using Garden Bird Feeding Survey sites (Swallow et al., in prep). However, in practical terms the effect is extremely small and it is likely that Sparrowhawk predation is a very minor contributory factor to the decline of House Sparrows (and Starlings) rather than the main cause.
In addition to any possible direct effect of Sparrowhawk predation – i.e. small birds being killed – the presence of a Sparrowhawk in the vicinity of a garden feeding station may have an indirect effect on small birds by deterring them from accessing the food on offer. It is known that many small birds are reluctant to feed far from cover, something that has been attributed to the greater risk of predation facing birds feeding out in the open. Work in a Cardiff garden, for example, has found that the consumption of supplementary food provided in feeders adjacent to cover is double that of feeders placed 7.5 m away (Cowie & Simons, 1991).
A study by Hinsley et al. (1995) shows that older tits are more likely to use bird feeders positioned close to cover, forcing younger, subordinate individuals to take their chances on feeders positioned further away and at greater risk of Sparrowhawk predation. Similar findings have been found for other tit species and also in mixed-species flocks, where smaller and less dominant species are forced to feed in more exposed locations (Ekman, 1986; Suhonen et al., 1993). Such studies underline that small birds are able to weigh up the risk of predation and to balance this against the need to feed. The vulnerability of particular species to Sparrowhawk predation has been found to be due to both the characteristics of the prey species themselves – such as habitat use and behaviour – and those of the predator (Solonen 1997; 2000).
Sparrowhawks deploy a number of different hunting techniques, the most commonly used of which is ‘short-stay-perch-hunting’ (Newton, 1986). This technique sees the Sparrowhawk make short flights from one perch to another, pausing on each to scan the local area from cover, before moving on. The use of cover, both while perched and during flight, underlines that the hawk is a stealth hunter, seeking to take prey by surprise in order to increase its chances of making a kill. Garden birdwatchers often report how hunting Sparrowhawks make use of the cover provided by hedgerows, fences, shrubby borders and other features in order to get as close as possible to hanging feeders or bird tables. The use of such features is sometimes referred to as ‘contour hunting’. The difference in size between male and female Sparrowhawks – the female is the bigger sex – sees male Sparrowhawks typically take prey up to the size of a Mistle Thrush or Fieldfare, while females regularly tackle larger birds, such as Collared Dove and Woodpigeon. Although both sexes favour wooded habitats when hunting, females make greater use of open country than males and have larger hunting ranges (Marquiss & Newton, 1982). Whether this results in a greater use of gardens by females is unclear – this may be the case in rural gardens – and more work is needed to look at Sparrowhawks breeding within urbanised landscapes.
MAGPIES
The Magpie is a generalist and is known to use a broad range of food types. Animal prey, which is dominated by invertebrates, is most important during the breeding season when Magpies have young of their own to feed, while plant material dominates at other times of the year (Tatner, 1983). There are occasional records of Magpies killing frogs, moles and snakes, with small rodents and small birds taken more frequently – Magpies are even agile enough to catch adult birds, including House Sparrow and Dunnock. However, it is often the conspicuous predation of the eggs and young at songbird nests that has given rise to the assertion that Magpies might be responsible for the declines seen in certain songbird populations. There is relatively little quantitative information on the predation of songbird nests by Magpies, and even less on how such predation might impact on the breeding populations of the songbird species concerned.
FIG 88. Although happy to visit garden feeders in search of peanuts and suet pellets, Magpies may also visit gardens to search for the eggs and chicks of other garden birds. (John Harding)
Møller (1988), working on nest predation in Danish Blackbirds, found that the Magpies in his study area were responsible for 96 per cent of nest predation events recorded and that the presence of a breeding pair of Magpies in a wood resulted in an increased predation rate. In respect of urban Magpies, Mizera (1988) has suggested that Magpies were responsible for the breeding failure of most of the open-nesting songbirds in his Polish study area; as Magpie populations increased from 2 pairs in 1963 to 13 pairs in 1982, so the breeding success and numbers of Blackbirds declined. However, another urban study – this time in Berlin – found no evidence that increasing Magpie numbers had any effect on songbird numbers (Witt, 1989). There has been a small amount of work on urban Magpies and nest predation here in the UK. Groom (1993), working in urban Manchester, found that fewer than one in twenty of his Blackbird nests were successful, with Magpie thought to be the main nest predator. However, there was no apparent change in the numbers of breeding Blackbirds over the three years of this study, despite the high Magpie densities, and Groom concluded that habitat quality was probably the main factor determining the size of his urban Blackbird population.
The question of whether Magpies might be responsible for any of the widespread declines seen in songbird populations in the UK has been investigated by Gooch et al. (1991), who used BTO data for 11 common songbird species considered as being potentially vulnerable to Magpie predation. While these included several familiar garden bird species, such as Blackbird, Song Thrush, Dunnock, Robin and Chaffinch, the data were drawn mainly from woodland and farmland populations. Nest mortality was not related to Magpie density, nor did nest mortality increase with increasing Magpie density; in fact, the songbird populations actually did better (not worse) in regions where Magpie density was higher. A later study, using a larger dataset and a more advanced statistical approach, indicated that Magpie (and Sparrowhawk) was unlikely to have caused the observed songbird declines because the patterns of year-to-year population changes witnessed did not differ between sites with and without these predators (Thomson et al., 1998).
These two pieces of work strongly suggest that, at a regional or national level, Magpies have no detectable effect on songbird breeding success. However, the same may not be true for urbanised landscapes, where both habitat structure and differences in food availability might alter the levels of predation risk for nesting songbirds. This is something that, as is indicated by Chapter 3, warrants greater study.
CATS
The presence within the UK of the cat as a domesticated animal extends back over many centuries, but it has only been relatively recently that its potential impact on populations of wild birds and other animals has been recognised (Matheson, 1944; Sims et al., 2008). The large population of domestic cats present in the UK, estimated to number at least eight million pet cats and 800,000 feral individuals, coupled with frequent observations of their taking wildlife, reinforces the widespread belief that cats may have contributed to the marked declines seen in bird and amphibian populations. Despite the significant levels of bird mortality being linked to cat predation within some studies – Churcher & Lawton (1987) estimated that up to a third of the mortality they witnessed was linked to cat predation – we lack much-needed empirical evidence and simply do not know whether or not cat predation has any real impact on populations of wild birds. There is some evidence, for example, the recent work of van Heezik et al. (2010), to indicate that certain prey species may be unable to persist in habitats where levels of cat predation are high. Even within urbanised landscapes, such habitat effects may be of particular importance: there is, for example, evidence that predation rates on certain prey species may be higher within the urban/suburban fringe than they are within the core urban habitat (Gillies & Clout, 2003).
The nature of predation: compensatory or additive?
The very large figures quoted by the likes of Woods et al. (2003) and Loss et al. (2012), who estimated respectively that UK cats kill between 25 and 29 million birds annually and that US cats kill between 1.4 and 3.7 billion birds annually, may not translate into a decline in wild bird populations if this predation is ‘compensatory’ rather than ‘additive’. Where predation is compensatory, the removal of part of the population serves to reduce the level of mortality that will be experienced by the surviving component. For example, if the size of a House Sparrow breeding population is ultimately driven by density-dependent competition for food during late winter, such that more individuals die when there is greater competition for a finite food source, then cat predation earlier in the year will simply reduce the number of individuals competing and result in a lower mortality rate from starvation than would have been the case in the absence of predation. The resulting breeding population would, in this instance, be the same regardless of whether or not the predation was taking place. Another way to think of compensatory predation is to view it as the predator taking part of the annual ‘surplus’. Predation is ‘additive’ where its effects are additional to the other mortality causes.
FIG 89. Cat predation may be particularly problematic in some areas because of the numbers of free-living individuals present. (Mike Toms)
Jarvis (1990) has argued that within the UK, cat predation is compensatory rather than additive; while there is some evidence to support this view (e.g. Flux, 2007; Lilith, 2007), it is important to recognise that birds are mobile and that the presence of a population at a given site may be maintained only by the arrival of individuals from populations elsewhere – something that has been studied by those looking at source-sink dynamics. This means that just because a garden bird population isn’t declining in a locality where there is a high level of cat predation, this does not mean that predation by cats in this locality isn’t having an impact at a wider population level.
One reason why cat predation may be particularly problematic is that domestic cats, living as companion animals, are supported with supplementary food by their owners. This means that their populations are not limited by the availability of wild prey, something that enables them to live at much higher densities than those seen in wild felids, living as part of a natural system (MacDonald & Loveridge, 2010). The provision of supplementary food no doubt reduces the level of predation that actually happens, but domesticated cats still maintain and implement their predatory behaviour (Fitzgerald & Turner, 2000).
It is also important to recognise a second component to many urban, and indeed rural, cat populations in the form of free-roaming individuals; these are cats that are not pets but neither are they truly feral (Calhoon & Haspel, 1989; Finkler et al., 2011). Instead, the animals take advantage both of handouts, in the form of supplemental feeding by people, and of other food scraps encountered within their foraging range. Densities of such individuals may range from 0.033 cats per ha (in rural Sweden – Liberg, 1980) to 7.43 cats per ha (Maryland, US – Oppenheimer, 1980). Dards (1979) reported densities of c. 2.00 cats per ha in urban Portsmouth. Urban densities of free-roaming cats are typically significantly higher than those of equivalent rural populations, with food availability and shelter both important in determining the densities attained. It is thought by some researchers that these un-owned, free-roaming cats are responsible for the majority of the bird and small mammal mortality linked to cat predation (Loss et al., 2012). If this is true, then most of the published figures for garden bird mortality resulting from cat predation will be significant underestimates.
Many of the studies to have examined the predation of garden birds and other wildlife by domestic cats have done so indirectly, asking cat owners to collect and record the numbers and identity of prey species taken. The successful application of this method necessitates the assumption that the prey items brought home are a representative sample of the total caught and killed; some items, such as larger invertebrates, may be significantly under-represented within the sample. There is also substantial variation between individual cats in the extent to which they kill prey and take it back to the household in which they live. Tschanz et al. (2011), for example, found that 16 per cent of the cats in their study accounted for 75 per cent of the prey returned. Some researchers have found that younger (and thinner) cats bring home more prey items than older cats (e.g. Woods et al., 2003; van Heezik et al., 2010).
The approach of asking cat owners to record the prey brought home by cats is certainly a better one than simply asking cat owners to estimate the number of birds and animals killed, since it has been shown that cat owners consistently underestimate predation levels, presumably because their judgement has in some way been clouded by the emotional aspect of their cat killing another creature (Barratt, 1998). Looking across the various studies using this approach for examining cat predation and its impacts suggests that, on average, domestic cats exhibit predation rates of between 0.58 (Baker et al., 2005) and 6.57 prey items per cat per month (Calver et al., 2007). Annual figures calculated by Loss et al. (2012) for the US and Europe combined are between 23.2 and 46.2 birds per cat per year; these compare to equivalent figures for mammal prey of 134.9–328.6, underlining the seemingly greater importance of small mammals in domestic cat diet. Such figures are often then used to produce estimates of the total number of prey items taken annually, the rate extrapolated up by the number of cats known to be resident within a particular city, region or country. While small mammals, such as mice, voles and shrews, tend to be the most numerous type of prey taken and brought home by domestic cats, small birds feature prominently (Churcher & Lawton, 1987; Woods et al., 2003; Baker et al., 2005).
The study carried out in Bristol by Phil Baker and colleagues (Baker et al., 2005) used a diary approach, allowing cat owners to record what their cats brought home on a daily basis. In addition to the information collected on the species being brought home by the cats, Baker and his colleagues were also able to estimate from questionnaire returns that roughly one in five of the householders in the study area owned a cat. A Cats Protection League figure for the equivalent period suggests cat ownership could be as high as one in four homes. The most commonly recorded prey species was Wood Mouse Apodemus sylvaticus, while House Sparrow, Blue Tit, Robin and Blackbird were the most commonly taken birds (that could be identified to species). Using figures from the BTO/JNCC/RSPB Breeding Bird Survey for the Bristol region, Baker et al. (2005) were able to calculate minimum predation rates for each species; these were found to be moderately high for three of the bird species considered, namely Dunnock (46 per cent), Robin (46 per cent) and House Sparrow (45 per cent), where the percentage represents predation as a proportion of the combined total of pre-breeding density and annual productivity. House Sparrow populations have previously been considered vulnerable to cat predation, most notably through the work of Churcher & Lawton (1987). Churcher & Lawton’s work suggested that, within their English village study area, cat predation was responsible for up to 30 per cent of annual House Sparrow mortality.
FIG 90. Cat predation may be particularly important in limiting the distribution of small mammals in some locations. (John Harding)
While it might be assumed that there is a direct and negative relationship between keeping a cat and feeding wild birds in your garden, a national study by Woods et al. (2003) found evidence that cats living in households where owners fed the birds brought home fewer birds (and fewer reptiles and amphibians) than cats living in a house where food was not provided. The work of Dunn & Tessaglia (1994) and of Lepczyk et al. (2004b) contradicts this, with both research teams finding that there was no difference in predation rates between households that fed wild birds and those that did not.
In addition to variation in the predatory activities of individual cats, there can also be variation in the impact that such predation has at the population level. It has been shown that birds are particularly susceptible to cat predation during the breeding season, and that the intensity of predation is at its peak during this period (Lepczyk et al., 2004b; Baker et al., 2005). This seasonal peak in predation may have a wider impact on the post-breeding population, the loss of an adult bird also potentially meaning the loss of its dependent young or its clutch of eggs. Domestic cats may impact garden bird populations in two ways: as we have already seen, they may kill birds but there may also be sub-lethal effects, with the presence of hunting cats preventing individual birds from foraging or from returning to an occupied nest. This ‘fear of cats’ has been investigated by researchers at the University of Sheffield, whose modelling approach suggested that such sub-lethal impacts could depress the size of urban bird populations (Beckerman et al., 2007). Further work on this topic, also carried out at Sheffield, revealed that the brief presence of a model domestic cat at an active Blackbird nest led to a subsequent reduction in provisioning rates and increased levels of nest predation (Bonnington et al., 2013). The latter effect appeared to result from the increased levels of nest defence behaviour directed at the cat model, which presumably alerted nest predators (Grey Squirrels and corvids) to the presence of the nest.
Reducing the impact of cat predation
Various attempts have been made to reduce the impact of cat predation on populations of wild birds. These have included curtailing the movements of domestic cats (including the enactment of legislation elsewhere in the world requiring that cats are kept indoors), the use of sonic and other devices to alert potential prey to a cat’s presence (Clark & Burton, 1998; Clark, 1999; Ruxton et al., 2002), and the deployment of ‘bibs’ and other restraints that limit a cat’s ability to hunt effectively (Calver et al., 2007). Since the time of day has an influence on the types of prey taken, it is possible for cat owners to reduce the impact of their pet on particular species by modifying the time periods when a cat is allowed outside – Barratt (1997) found that cats tended to bring home birds in the morning, reptiles in the afternoon and mammals in the evening, most likely reflecting peaks in the activity patterns of these different groups.
The addition of one or (better still) two bells to a cat’s collar has been shown to reduce the number of prey items that a cat brings into its household. A study by Graeme Ruxton and his colleagues, in which 21 cats were monitored over eight weeks and carried a bell for four weeks within this period, saw the mean number of prey items delivered fall from 5.5 to 2.9 individuals. The bell had no effect on the relative numbers of different types of prey delivered and, within this study at least, no evidence that the cats adapted their hunting behaviour to reduce the effect of the bell over time (Ruxton et al., 2002). The effectiveness of a not dissimilar device, in the form of a collar-mounted sonic apparatus, has also been shown to reduce the level of predation on birds – though not on mammals (Clark, 1999).
Working in Australia, Michael Calver and colleagues have investigated the effectiveness of a more substantial device, the CatBibTM. The bib is a sizeable neoprene device that hangs from the cat’s collar and is designed to interfere with the precise timing and coordination that a cat needs for successful bird catching. Alone, or in combination with bells, the bibs were found to stop 81 per cent of the cats studied from catching birds; cats wearing the bib caught only one in four of all birds (Calver et al., 2007). While Calver found the device to be effective, continued use by those cat owners who trialled the device had dropped to 17 per cent eight months after the trial, despite nearly three-quarters saying they would continue to use the device.
In addition to the devices proposed for use on individual cats, there are also commercially available deterrents designed for use by people – typically non-cat owners – wanting to prevent cats from making use of their gardens. These range from cheap chemical sprays and pellets through to more expensive ultrasonic devices, such as ‘Catwatch’. The ultrasonic devices work by detecting movement and body heat and using this to trigger an ultrasonic alarm operating at a volume of 56 decibels (at 7 m) and a frequency of 21–23 kHz. The results of a study examining the effectiveness of the ‘Catwatch’ device suggest that it does have a ‘moderate deterrent effect’ (Nelson et al., 2006).
OTHER PREDATORS
Although a number of other predators may take the adults, young and eggs of garden birds, relatively less attention has been directed towards understanding either the scale of predation or its impact at the population level. One species that has been thought likely to be responsible for significant levels of nest predation – both to open nests and to those in nest boxes – is the Grey Squirrel. Squirrels, in general, are major nest predators, as revealed by studies in both Europe and North America (Martin, 1993; Nour et al., 1993); however, much of this evidence is linked to species other than Grey Squirrel. While we know that Grey Squirrels do eat wild birds and their eggs in both woodland and garden habitats, there has been little work – either in the UK or North America – to quantify the numbers of birds and eggs taken. Anecdotal reports hint at local impacts within a handful of sites, but a study by Newson et al. (2010) failed to find any convincing evidence for an increasing Grey Squirrel population being behind an observed decline in woodland bird populations at a national level. Newson et al. (2010) did, however, find a positive association between nest failure at the egg stage in Blackbird and Collared Dove and squirrel abundance; this may mean that nest predation by Grey Squirrels had been depressing the populations of these two species.
The extent and pattern of Grey Squirrel nest predation may be very different in a garden setting to that seen within woodland or the wider countryside. Grey Squirrels are generalist feeders, exploiting a wide range of food types, and their populations may benefit from the presence of supplementary food, such as peanuts and sunflower seeds, provided at garden feeding stations. The provision of supplementary food may both increase the numbers of Grey Squirrels visiting a garden and the number of individuals foraging more widely within the garden setting. This is something that has been investigated by Hugh Hanmer, through his PhD at the University of Reading (Hanmer et al., 2017b). Hanmer used cameras to monitor artificial nests that had been placed in the area around a series of bird feeders, some of which were empty and some of which contained food – the latter divided into those that were protected by a cage and those that were not. The work set out to establish whether Grey Squirrels – and other nest predators – were attracted to garden feeding stations providing supplementary food and, if so, whether this associated with differences in rates of nest predation. Grey Squirrels (and Magpies) were frequent visitors to those feeders containing food, and predation by Grey Squirrels (and Magpies and Jays) was significantly higher when nests were located close to filled feeders. Hanmer concluded that the increased predation on the artificial nests close to filled feeders was not simply a consequence of predators being attracted to a point source; instead, he thought that the predators were perhaps also being attracted by the presence of other feeder users in the vicinity. While Hanmer’s work demonstrates the potential impacts at the level of individual nests, it remains to be determined if such predation affects the population dynamics of urban birds more widely.
Great Spotted Woodpecker, Jay, Weasel and Pine Marten Martes martes are known to be important nest predators within forest and woodland habitats across Europe, but they are unlikely to be important predators within a garden context – though all four species are regular visitors to some favoured gardens. Great Spotted Woodpeckers are known to feed on tit chicks extracted from wooden nest boxes, the woodpecker either enlarging the entrance hole or – seemingly more often – drilling a fresh hole in the side of the box. Great Spotted Woodpecker predation of nest box contents appears to be linked to the presence of vocal chicks within the box. Weasels may also take young chicks from within nest boxes, a behaviour that may be more common in those years when favoured small mammal prey populations are low (Dunn, 1977). Jay, although a less commonly reported garden visitor than Magpie, appears to be an important nest predator targeting open-nesting species. Working in woodland in Germany, Schaefer (2004) used video cameras to monitor the fate of 132 Blackcap nests; Jays were responsible for 21 per cent of nest fates and 46 per cent of nest losses.
FIG 91. Great Spotted Woodpeckers are known to predate the nests of other birds, even breaking in to nest boxes to take the chicks of Blue Tits. (John Harding)
EXPOSURE TO ENVIRONMENTAL CONTAMINANTS
Many different types of environmental toxicants – which include insecticides, rodenticides, heavy metals and molluscicides – have been documented to cause mortality or bring about sub-lethal effects in wild birds. Such incidents have tended to be reported from bird populations living within the wider countryside – think of the impacts of DDT on bird of prey populations (Ratcliffe, 1967) or the presence of second-generation rodenticides in Barn Owls (Newton et al., 1990; Gray et al., 1994) – but individuals may also be exposed to such compounds within the garden environment. Urbanised landscapes are subject to higher levels of certain environmental pollutants than is the case within the wider countryside, with contaminants from industry, transport and other activities posing a potential risk to the wildlife using gardens, parks and other areas of urban green space. Chandler et al. (2004), for example, showed that the levels of lead found in an urban House Sparrow population in Vermont, US, were significantly higher than those from a wider countryside control group. Closer to home, a study looking at Finnish House Sparrow liver samples, sampled in the 1980s, found that heavy metal levels were higher in urban than rural areas (Kekkonen et al., 2012).
Some heavy metals, including zinc, copper, manganese, chrome and iron, are essential to living organisms but become harmful if present in excess. Other heavy metals, such as cadmium, aluminium and lead, are usually not essential to living organisms. Heavy metal pollution has been shown to detrimentally affect key phases in the avian life cycle, including the development of the egg, chick growth and adult reproduction (Eeva & Lehikonen, 1995; 1996). Heavy metals and other airborne pollutants, such as combustion-derived hydrocarbon gases and biocides, are highly reactive elements which interfere with avian metabolism and key biochemical reactions. They can disrupt the activities of enzymes and alter the levels of free radicals – free radicals are by-products of cell metabolism and are usually balanced by a number of antioxidant elements. The antioxidant response to the oxidative damage caused by such pollutants has been used by some researchers as a biomarker, revealed through the blood sampling of key species – such as House Sparrow – and used to indicate the impacts of pollution on the wider environment (Herrera-Dueñas et al., 2014).
The presence of lead within the urban environment has been linked to the use of lead-based paint and leaded petrol, the former banned from sale to the general public in 1992 in the UK – though continuing for some specialist uses – and the latter phased out from general sale from 1999. However, lead is persistent within the environment and concentrations in soil remain high in many urbanised landscapes. Birds may come into contact with this lead through inadvertent consumption of soil particles when feeding on soil-dwelling invertebrates, such as earthworms (Beyer et al., 1988). Labere et al. (2004) reported that earthworms sampled from a lead-contaminated area at West Point, US, had up to 90 per cent higher concentrations of lead compared to an uncontaminated control site, while Weyers et al. (1985) found significantly higher levels of lead in the feathers and organs of Blackbirds feeding at contaminated sites in Germany. Lead poisoning in birds can have both physiological and behavioural effects: from anaemia, emaciation and brain damage, through to increased aggression and difficulties in walking, flying and landing. Work by Karin Roux and Pete Marra (2007) has revealed a gradient in lead pollution from urban to rural landscapes, which is matched by a similar gradient in lead levels within the blood of sampled adult and nestling birds, including American Robin, Gray Catbird Dumatella carolinensis, Song Sparrow, Northern Cardinal and House Sparrow.
The birds inhabiting gardens located closer to busy roads are likely to be at greater risk from pollutants associated with transport than gardens located within more leafy suburbs; it has also been speculated that changing levels of such pollutants might be behind the observed declines in urban House Sparrow populations. In addition to heavy metals like lead, other particulates, nitrogen oxides, polycyclic aromatic hydrocarbons and volatile organic compounds may also pose a risk to House Sparrows and other birds (Bignal et al., 2004). There is also concern about some of the anti-knock agents – such as MTBE – introduced as a replacement to lead in petrol. Working along an urban gradient in Leicester, Kate Vincent and colleagues found that House Sparrow chicks reared at sites with high NO2 levels tended to be smaller and lighter than those at other sites. The observed difference in body mass was sufficient to have had a relatively large impact on chick survival once they had left the nest (Hole, 2001; Peach et al., 2008). The most likely route for emissions to impact on the growth of House Sparrow chicks is by reducing the availability of favoured invertebrate prey, and Vincent’s work did find direct evidence for an influence of prey availability on reproductive success.
Large increases in the use of molluscicides in gardens, and more widely within lowland farmland (Garthwaite & Thomas, 1996), may have reduced prey availability for species like Song Thrush; they may have also caused direct mortality through secondary poisoning. However, despite the fact that snails form a large component of Song Thrush diet, particularly when other food is scarce, there has been little work done to evaluate the extent to which molluscicides might have played a role in the decline of Song Thrush populations here in the UK. The use of other forms of pesticide within the garden environment may impact on garden birds by reducing the availability of favoured invertebrate prey, something that has already been demonstrated for some of the heavy metals already mentioned (Pimental, 1994; McIntyre, 2000).
FIG 92. Song Thrushes may be exposed to environmental contaminants through their diet. (John Harding)
OTHER CAUSES OF MORTALITY
A handful of reports suggest that ethanol poisoning may occasionally result in the deaths of berry-eating garden birds, which had presumably fed on fermenting berries or fruit (Fitzgerald et al., 1990; Duff et al., 2012). Cases of such mortality have been documented in Blackbirds and Redwings here in the UK, the former having fed on rowan berries Sorbus sp. and the latter on Holly. There are also a number of reports of birds being found drowned. In some instances, these incidents have involved multiple individuals of the same species. For example, Lawson et al. (2015b) reported on 12 incidents (from a 21-year period) of mass drownings with Starlings. These incidents always occurred in spring and early summer and usually involved juvenile birds. There was no evidence of underlying disease or other mortality cause and the authors concluded that the most likely explanation was that these were inexperienced birds getting into difficulty.
A small number of studies have highlighted a potential risk to urban bird populations from mobile phone base stations – a topic that has seen parallel concerns raised in relation to human health. Although more detailed work is needed, in part to control for other confounding factors, it would be wrong to dismiss the possibility of such effects out of hand. Non-thermal effects of microwaves on birds have already been documented (Tanner 1966; Fernie & Reynolds, 2005), suggesting, for example, that electromagnetic radiation from mobile phones may negatively impact on the development and survival of bird embryos (Farrel et al., 1997) and disrupt magnetic navigation in several bird species (Thalau et al., 2005). Demonstrating such effects within wild birds living within urban environments is likely to prove challenging.
CONCLUDING REMARKS
As we have seen through the work reported in this chapter, gardens have both opportunities and risks associated with their use. While we have a good understanding of some of these, our knowledge of others is far from complete. The challenges of working within the garden environment – something to which we will return in Chapter 6 – have been overcome in some of the areas of research (notably disease) that have been the focus of the current chapter. We have seen how risks and opportunities may vary between species and individuals, sometimes the result of physiology or ecology, sometimes shaped by behaviour. And it is behaviour to which we will turn our attention now.