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Bye-Bye Birdie – Climate Change as an influence on avian migratory patterns




An estimated 2000 species of bird migrate throughout the year, approximately 19% of all bird species. Like all avian species, migratory birds contribute a range of ecosystem services: they provide direct and indirect benefits to the environments they are part of and are culturally significant for many indigenous and rural communities. The ever-increasing effects of climate change are having widespread negative impacts on the planet, it’s resources and wildlife however, these birds particularly are under disproportionate levels of pressure to adapt rapidly for survival. Climate change is affecting migration timings, migration distances and native ranges as well as habitat availability and is making annual journeys more energy costly and perilous year on year. Moving forward, dynamic conservation strategies, habitat protection, adequate monitoring/tracking and education are likely to prove essential in maintaining migration equilibrium and protecting bird populations.



Article Highlights

· The recent uncertainties of spring arrival times in recent years brings problems for many species of migratory bird.

· On average, migratory birds are reaching their breeding grounds one day earlier for every °C rise in global temperature.

· The extent to which migration disequilibrium is affecting resident species remains largely unknown in many cases.

· Climate change is affecting birds around the globe disproportionately due to the non-uniform nature of its effects.

· Although most migratory species are threatened by climate change, evidence suggests that some species might remain unaffected and others could even prosper.



Flying on the spot

The human population has been increasing at an exponential rate, most notably in the last century (Henderson and Loreau 2018). From 1950 to 2005, the population more than doubled from 2.5 billion to 6.5 billion and is expected to grow at a similar rate before exceeding 10 billion later in the 21st century (Bongaarts 2009). This unprecedented population growth is mounting pressure on biota to find ways to co-exist with humans, with many inevitably unable to do so. The wildlife decline has been so severe in that, according to the Living Planet Index report (2018), vertebrate abundances have declined by an average of 60% in the past 40 years. Perhaps even more concerning, it is predicted that by the year 2050, 15-37% of existing flora and fauna species are to become extinct (Thomas et al. 2004), with the figure potentially rising to half of all species by 2100 (Myers and Knoll 2001). This alarming loss of biodiversity has led many researchers to suggest that the sixth mass extinction is currently underway (Barnosky et al. 2011), prompting the worldwide consensus to be that if action is not taken quickly to lessen anthropogenic influence, significant and irreparable damage will occur. A major consequence of human population growth is that the planet’s climate is changing, predominantly due to excessive consumption of resources and the expulsion of greenhouse gases into the atmosphere (Coffin et al. 2019). It has been calculated that the global mean surface temperature increased by 0.87°C between 2006-2015, the trajectory past 2015 suggests that this rate of warming is rising exponentially (IPCC 2018). This rapid anthropogenic climate change brings with it the risk of many biological abnormalities, such as rising sea levels, an increase of extreme weather events and changes in the hydrological cycle (Kundzewicz 2008; Mahmoud and Gan 2018). All of which put numerous flora and fauna at risk of major population depletion or extinction.


Many birds are included in the long list of animals at risk from climate change. This report will focus on the challenges faced by birds that migrate annually in the continuously warming global climate and the direct or indirect consequences they could face if their migratory destinations, times or flyways were to change.


Many migratory birds travel long distances to reach breeding grounds and seek respite from cold winters in their native lands (Zúñiga et al. 2017). For the birds that rely on these non-breeding grounds, environmental variation has been shown to influence future reproductive success (Norris et al. 2004), as well as individual physical condition (Studds and Marra 2007). This review aims to describe avian migration and summarise the threats birds face at every stage of their journey as a result of climate change. Among influences that will be discussed are the alterations in migration timing, transformed journey distances, shifting of native ranges and loss of habitat. In addition to these threats being addressed, within this review, potential human-led adaptation strategies that could be deployed to aid conservation of migratory species will be touched on.



Importance of birds

There are approximately 10,000 species of bird on the planet, with an estimated 19% of these being migratory (Kirby et al. 2008). Migratory behaviour is more widespread in species that live in temperate areas, where food sources fluctuate considerably throughout the year, 80% of birds in these environments are thought to be migratory (Martin et al. 2007; Hedenstrom 2008). Of the tropical birds that do migrate, altitudinal migration is more common compared to movement latitudinally (Boyle et al. 2010).


Birds can plan their circannual programmes by combining immediate responses to environmental changes with internal body-clock mechanisms (Akesson et al. 2017). These adaptions are so evolutionarily hard-wired that even birds in captivity display changes of behaviour periodically at certain times of the year without being exposed to environmental factors (Gwinner 1996). Many species travel to overwintering areas with milder temperatures, so regions higher in geographical latitudes, particularly in the Northern Hemisphere, have the largest seasonal species turnover (Figure 1; Somveille et al. 2013). Birds utilise suitable, established routes for their journeys that offer appropriate ‘pit stop’ sites where rest and socialisation occur. These locations allow flocks to last the full migratory journey. Avian flyways vary from species to species and can range from hundreds to thousands of kilometres long and span across multiple countries and continents (Palm et al. 2015). That said, migration journeys can be loosely categorised into eight major identified routes (Figure 2).


In many cases, the cost of undertaking these journeys can be extreme. Migration is always energy costly (The Arctic tern (Sterna paradisaea), the bird that migrates longest in distance covers 40,000km from it’s native Greenland to Antarctica and back annually (Møller et al. 2006)) and is often perilous. Some longer journeys have been documented to cause a six-fold increase in mortality rates (Klaassen et al. 2014). The cost of these journeys can have an impact in the short-term, during the present season, resulting in a reduction of individuals making it to the feeding/breeding sites or could affect the following season(s), potentially shrinking the population via reduced reproductive output (Lok et al. 2015). Despite the considerable task of migration and associated risks, migratory birds continue this behaviour year after year as it is crucial to their survival.


Figure 1. Map representing global patterns for migratory species. Values highlighted in red signify areas that have a higher local species richness in July. Areas in blue signify areas that have a higher species richness in January. Figure taken from Somveille et al. (2013).



Figure 2. Map representing the eight major global flyways travelled along by migratory birds. (Blue = Pacific Americas, brown = Central Americas, cyan = Atlantic Americas, yellow = East Atlantic, red = Black Sea-Mediterranean, purple = East Asia-East Africa, orange = Central Asia, green = East Asia-Australasia. Figure taken from Birdlife (2019).



In addition to migrations importance to the birds themselves, this behaviour is also vital to the locations utilised throughout migration journeys due to the important ecosystem services seasonal arrival of these species provides (e.g., Box 1; Sekercioglu 2006). An increase in the number of papers regarding the subject in the last few decades has highlighted migratory birds as some of the most diverse ecosystem providers (Sekercioglu 2006; Whelan et al. 2008). Amongst these services provided include the cycling of resources, transport of seeds and pollen, food web maintenance, plant fertilisation, scavenging and pest control to name a few (Bauer and Hoye 2014). Not only are the services they provide diverse and substantial, but these services are also provided to multiple locations rather than a singular one due to the birds’ nomadic nature. Without the influence of migratory birds, the ecosystems they contribute towards at stages throughout their journeys would struggle to function as they did before.


Migratory birds might be considered as part of telecoupling frameworks as their influence encompasses both socioeconomic and ecological implications that are felt at several different sites (Liu and Yang 2013; Hulina et al. 2017). Due to migratory birds being found at multiple locations throughout the year, the ecosystem services they provide in one region can depend hugely upon ecological conditions in another (López-Hoffman et al. 2017). For instance, the black kite (Milvus migrans), a generalist trans-Saharan migrant who winters in northern Africa, feeds on swarms of desert locusts (Schistocerca gregaria) commonly found here in substantial numbers when they arrive to this region (Sánchez‐Zapata et al. 2007). This pest control is important for local farmers whose crops are destroyed by these locust swarms. When breeding conditions in the Palearctic region are sub-par, crop damage increases due to fewer individuals migrating to Africa and acting as pest control (Panuccio and Agostini 2010). Therefore, the management of the destination is as crucial as the management of their origin.



Table 1. Examples demonstrating migratory birds’ contributions towards the four ecosystem services



Threats to migratory birds

In 2008, 11% of migratory avian species were classified as threatened or near-threatened according to the IUCN Red List (Both et al. 2006; Kirby et al. 2008), and populations are declining at a rate that far exceeds their non-migratory counterparts (Bairlein 2016). In fact, in the last 30 years, more than half of migratory bird species across all major flyways have disappeared (Kirby et al. 2008; Reynolds et al. 2017). Migratory species across the globe are increasingly threatened by stressors such as climate change (Both et al. 2006), habitat loss (Faaborg et al. 2010) and direct anthropogenic actions such as hunting (Box 2; Jenkins et al. 2017). Their reliance on independent, spatially separated habitats renders migratory birds particularly susceptible to the stressors of climate change due to them being reliant on the health of several different habitats as opposed to one (Robinson et al. 2005).



Alteration of migration timing

Rising global temperatures have distorted the phenology of migratory birds in a number of ways (Cotton 2003; Visser 2013). Migration is a process controlled by endogenous mechanisms that have been refined over millennia to synchronise with suitable temperatures and peak food availability (Carey 2009). The extreme rate of warming is taking a toll on current species and they are under increasing pressure to adapt rapidly (Bairlein 2016) and to reverse the hard-wired behaviours that have been established over a vast period. While there is variation among species, Marra et al. (2005) postulated that on average, with every 1°C increase in temperature, birds would begin their migration one day earlier. This is leaving the phenology of some species and their prey ecologically mis-matched, leading to reduced fitness, less reproduction, and increased mortality (Thackeray et al. 2010).


Many species use local climatic cues to begin their migration which creates these mismatches between predator and prey (Robinson et al. 2009). For example, Dutch pied flycatchers (Ficedula hypoleuca) have not advanced their arrival to feeding grounds in response to warmer spring temperatures (Both and Visser 2001). The caterpillars they feed on, however, have adapted to emerge early resulting in the birds missing key provisioning opportunities. In fact, in areas with the earliest seasonal (and therefore most mismatched) food peaks, populations of the pied flycatcher have declined by up to 90% (Both et al. 2006). For insectivorous birds that feed on caterpillars such as these, flourishes of insect availability dictated by warming are short-lived and are vital to the survival of individuals and reproductive success (Visser et al. 2006). This imbalance of predator-prey relationships likely has a cascading effect on the trophic system (Morris and Letnic 2017). The increase in insect herbivory from reduced bird predation could have detrimental effects on both natural and agricultural flora, ultimately placing natural ecosystem out of balance and farmers out of pocket (Wenny et al. 2011).


As well as the premature advancement of spring from winter affecting prime feeding times, breeding patterns and success have also been affected (Charmantier and Gienapp 2014). Some birds that have been able to adapt are nesting earlier to coincide with advanced prey abundance (Crick et al. 1997), others have been shown unable to do so (Visser et al. 1998). Regional climates are fluctuating at differential rates, so migrants who use cues in one region to calculate the timing of arrival in another often mistime their movements (Robinson et al. 2005). This global variation in warming likely makes it incredibly difficult for many migratory species to accurately account for food availability and therefore ideal nesting times, this will result in maladaptive behavioural responses.


Increasing temperatures could be extending the entire breeding season for many bird species (Halupka and Halupka 2017), which could have varying effects. If a bird has the potential to produce multiple broods in a single breeding season, such as the Eurasian hoopoe (Upupa epops), then prolonged suitable weather may increase the chances of raising their young successfully (Hoffmann et al. 2015). This said, if climate warming were to alter parental decision making from having one clutch to two as a result of these conditions, this could result in insufficient energy for forthcoming return migration journeys and result in lower parental survival rates (Hoffmann et al. 2015).


Species with longer migration routes are more susceptible to phenological mismatches than those with shorter routes (Møller et al. 2008). This can result in population declines due to losing their competitive ability and access to resources (Howard et al. 2018). For example, species that breed in temperate regions and winter in the tropics, such as Afro-Palearctic birds have seen more considerable population declines over recent decades compared to resident or short-distance migrants who have seen lesser declines (Sanderson et al. 2006). Milder winters have increased the survival rate of resident, overwintering species, meaning there is more competition for resources when migrants arrive (Lemoine and Böhning‐Gaese 2003). This general pattern of population declines is evident in long-distance migrants that winter in arid habitats such as the Sahel, where drought-induced desertification and intensive agriculture have had detrimental effects on food availability and nesting site locations for European migrants (Baillie and Peach 1992; Szep 1995). Where short-distance migrants and permanent residents have demonstrated phenotypic plasticity in response to local temperature changes such as in this example (Tryjanowski et al. 2005), long-distance migrants have struggled more distinctly in altering their behaviours to suit new and climatically altered environments.



Transformed journey distance and shifting of ranges

Due to warming global temperatures, migratory bird species are beginning to expand their ranges poleward to areas resembling pre-warming temperatures, in their previous, more equatorial native ranges (e.g., Figure 3; Brommer et al. 2012; Virkkala and Lehikoinen 2017). As a result of this, many migratory birds that have relocated are now further away from their migration destinations than they were before moving. The result of this is that these birds must travel further distances and consume more energy to migrate annually. Not only this, these birds may also arrive later at their destinations, potentially missing out on resources vital for survival and reproduction (Schmaljohann 2019). An example of a species that would be severely affected by this that migrates along the Eurasian-African flyway is the thrush nightingale (Luscinia luscinia). The distance between their breeding and non-breeding grounds could grow by approximately 773km (±30.3km), increasing their journey time by a minimum of five days (Howard et al. 2018). As this review has previously mentioned, migration is a period of increased mortality for birds due to increased energy expenditure and predation risk (Alerstam et al. 2003; Newton 2006; Hewson et al. 2016). Therefore, any increase in journey distance escalates the risk of injury or mortality.


Figure 3. Representation of the northward shift of breeding ranges for 305 bird species assessed in North America between 1966-2013. The middle line represents the average shift northwards (40 miles), the shaded area represents the range of values from the species observed. Figure taken from Mass Audobon (2019).



In the UK from 1972-91, Thomas and Lennon (1999) not only concluded that some bird species had shifted their breeding ranges northwards by an average of 18.9 km, they found that some migrating species were extending their temporary stay and in extreme cases even became permanent residents in response to warming. Individual populations of Eurasian blackcaps (Sylvia atricapilla) previously summer visitors to the UK, were reported to have remained in the UK overwinter in response to warmer conditions and had even micro-evolved as a result to garner fitness advantages (Berthold et al. 1992). Entire species have since been found to alter their behaviour and remain in Britain permanently rather than migrate (Clark et al. 2004).


As a result of this reduced migratory behaviour, wintering ranges for bird species can be altered as they preferentially spread locally/regionally rather than over vaster distances (Robinson et al. 2005). This phenomenon is likely to occur more often in short-distance migrants who would be less inclined to migrate due to being less well adapted to long journeys. Smaller species are unable to fly at the same speeds as larger birds or to conserve energy as efficiently (Hedenström 2003) meaning their migration efficiency is lower relative to larger species. This could be forcing the long-distance migrators to travel even further as competition for resources increases at areas they once travelled to (Lemoine and Böhning‐Gaese 2003).



Loss of habitat

As migratory birds depend on multiple habitats at different stages in time, a reduction in quality/loss of one location, regardless of the quality at others, can have severe negative impacts (Jackson et al. 2019). Habitat loss has been observed to manifest in a number of different ways for a host of different bird species (e.g., Table 2).


One example, and perhaps the most pressing of all habitat loss factors for birds is the effects from sea-level rises as a result of warming-induced glacial melting (Mimura 2013). Shorebirds specialised towards littoral ecosystems are thought to be most at threat from this due to rising sea levels compromising their preferred habitats (Iwamura et al. 2013; Galbraith et al. 2014). The effects of sea level rise on migratory birds are most pronounced on those that require stop-over sites during their journeys. Stop-over sites are of major importance for several migratory species, with some spending up to 70% of their annual migration time at these locations (Hedenström and Alerstam 1997). The disappearance of these could lead to birds becoming exhausted and unable to survive their journeys. These sites are often in the form of low-elevation islands, which are most at risk from sea level rises (Reynolds et al. 2015).


Another example of climate change destroying bird habitat is the increasing frequency and intensity of forest fires due to vegetation drying. Though forest fires are becoming very problematic planetwide, the most severe impacts are being felt in tropical landscapes such as Amazonia due to increasing drought regularity (Marengo et al. 2008; Devisscher et al. 2016). When they occur in moderation, forest fires are important in maintaining ecosystem dynamics and generate high habitat heterogeneity (Rey et al. 2019), however, the frequency and intensity to which these fire events are now occurring are now posing far more problems than benefits (Devisscher et al. 2016). Whilst being advantageous to a limited pool of bird species such as woodpeckers, who can utilise the new open spaces and burnt wood to feed on insects and create nests in snags (Walsh et al. 2019), fires can decimate bird populations and act as a major driver for population losses. Directly, these fires can catch birds in the flames (most notably affecting young, who are unable to fly away to escape danger), Indirectly, fires cause habitat destruction, meaning resources in the remaining, condensed habitable areas are subject to greater competition.



Table 2. Examples of species affected by habitat loss triggered by climate change



Conservation strategies

Migratory birds are difficult to monitor and devise solutions for in response to population declines as they move between and depend on multiple locations and resources – their initial site and destination as well as various stopover sites (Klaassen et al. 2014; Howard et al. 2018). This could explain why so few are safeguarded compared to sedentary species. 9% of migratory birds are adequately protected throughout all stages of their journey, as opposed to 45% of non-migratory species (Runge et al. 2015).


Considering the economic and ecological importance of migratory birds, efforts to conserve them more effectively must be introduced. In Reynolds et al. (2017), three obstacles preventing adequate conservation action for migratory species were identified. These must be addressed if adequate habitats are to be provided in anticipation for where and when these species will need them. These three obstacles are: 1) conservationists need to be able to predict where a species will be throughout the year, 2) be able to identify regions that can be modified to render them suitable for migrants, and 3) create economically viable mechanisms that ensure the habitat is ready and suitable for when the migrants arrive.


Rather than a more conventional preservation approach, dynamic conservation is likely a more appropriate tactic to employ when considering migratory birds (Bull et al. 2013). This means that specific efforts would be employed when species arrive at a particular area, rather than all year-round-protection. This conservation approach has certain benefits attached to it and would allow for increased flexibility and better utilisation of finite conservation resources if used correctly. If (for example) NGO’s wanted to create new nesting spots for migrants with private landowners, short-term agreements coinciding with migration movements could be struck as opposed to any deals

that would involve permanently owning land. Due to this, NGO’s would not be burdened with management costs all year round (Reynolds et al. 2017), making this approach more cost-effective than permanent safeguarding. Moreover, private landowners might prove more inclined to enter short-term agreements rather than selling their land completely due to the lesser commitment (Reynolds et al. 2017).


Concerning habitat provision, the preservation of intact habitats is generally more economically viable than the restoration of degraded or non-existent ones (Possingham et al. 2015). Although both restoration and protection would be ideal in conjunction (as restoration can improve biodiversity and increase ecosystem service provision (Benayas et al. 2009)), the latter should be the preferred approach as it incurs lesser costs (Possingham et al. 2015). Not only this, restoration ecology can take decades to regain the properties that were originally present, therefore these projects are often not immediate in providing results (Palmer and Filoso 2009; Possingham et al. 2015). For defined protected areas, conservation efforts only prove effective with strict regulation and management (Joppa et al. 2008) so funding allowing for the hire of rangers and provision of equipment must be provided. Even where sufficient resources are given, it is often difficult to quantify the success of conservation strategies in protected areas compared to non-target areas (Gaston et al. 2008), as a result, long-term monitoring is essential to gauge whether intervention is having an impact. A factor making the logistics for migratory bird conservation difficult specifically is that multiple locations must be protected. If this is to be achieved conservation organisations at several sites must effectively work with one another, this means transparent and efficient communication of tracking and monitoring data.


Public education regarding the urgency for action is necessary for future change, therefore information regarding how climate change is affecting migratory birds must be spread. Direct practical engagement with nature via community-driven projects must take place in conjunction with class-taught initiatives to shift public attitudes and encourage sustainable lifestyle changes more effectively (Sousa et al. 2016). Though connecting with nature is growing increasingly difficult due to the recent trends showing an exodus of human populations from rural to urban areas, rural excursions should be encouraged particularly for school children, many of whom are rarely exposed to the countryside. Reassuring locals that recovery is possible through the use of specific examples might additionally act as a useful tool to illustrate that change is possible. For example, the white-tailed eagle (Haliaeetus albicilla)(for example) went extinct in Britain in 1916 due to persecution and environmental pollutants but made a remarkable recovery in the 1970s following intensive conservation efforts which prohibited the use of certain agricultural chemicals (Hailer et al. 2006).


Conservation bodies should take advantage of volunteers to bolster monitoring and tracking efforts. Other countries might use the UK as an example of this, where professionals rely heavily upon keen, passionate birdwatching communities to map changes in movements and range shifts. These individuals might also be used as a tool to boost funding for related conservation efforts through ecotourism. Maintaining species-rich habitats with high bird biodiversity is likely to attract more tourists which adds incentive to maintaining conservation efforts.



Conclusion

Many avian species are under threat of population decline and extinction due to climate change, migratory birds even more so are at risk due to their reliance on spatiotemporal patterns and multiple habitats (Robinson et al. 2005). Although some species have demonstrated behavioural changes and microevolution to suit the rapidly changing conditions, others have been unable to adapt, it is these species that are at primary risk of extinction (Møller et al. 2008). Moving forward, ongoing conservation work by organisations such as the IUCN and BirdLife will prove crucial in conserving migratory bird species. This said, combatting climate change to address the devastating impact it is having on migratory birds is essential. Continued public education regarding the wider topic is needed and policy to reflect this adopted for long-term results. Success stories in species such as the white-tailed eagle and the red kite (Milvus milvus) demonstrate an ability for vulnerable bird species to recover (Hailer et al. 2006; Heneberg et al. 2016), yet time is quickly running out, not only for this category of organisms but for a host of other taxa alike.



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