changes in migratory behaviour and routes

Avian migration can be broadly defined as the regular, seasonal movement of individuals between wintering habitat and breeding grounds. Although migratory behaviour and routes are subject to genetic (Berthold et al., Reference BERTHOLD, WILTSCHKO, MILTENBERGER and QUERNER1990; Helbig, Reference HELBIG1991; Mueller et al., Reference MUELLER, PULIDO and KEMPENAERS2011; Pulido, Reference PULIDO2007) or cultural constraints (i.e. learned migration) (Sutherland, Reference SUTHERLAND1998), migratory birds demonstrate a remarkable ability to modify migratory behaviour in response to changes in their environment (Berthold, Reference BERTHOLD1990; Pulido, Reference PULIDO2007). These adaptations can be partly credited to individual plastic response, as well as evolutionary changes via natural selection (Pulido, Reference PULIDO2007). For instance, in some species, migratory behaviour has a genetic component and therefore, migration can be selectively bred out of a population within a few generations (Alerstam and Hedenstrom, Reference ALERSTAM and HEDENSTROM1998), or conversely, increased migratory propensity can develop in a population over time (Able and Belthoff, Reference ABLE and BELTHOFF1998; Pulido, Reference PULIDO2007). Consequently, migration routes and patterns are subject to change when selective pressure favours an adjustment. Although adult birds generally demonstrate considerable site fidelity (Berthold, Reference BERTHOLD2001), juvenile birds will use a variety of routes (Berthold, Reference BERTHOLD2001; Fransson and Stolt, Reference FRANSSON and STOLT2005; Salewski and Bruderer, Reference SALEWSKI and BRUDERER2007), which might be the process by which birds change migratory routes when conditions favour an adjustment (Salewski and Bruderer, Reference SALEWSKI and BRUDERER2007). Each new generation will sample new habitats, potentially leading to slight changes in migration routes and/or species dispersal (DeSante, Reference DESANTE1973). Berthold (Reference BERTHOLD2001) outlines four basic types of modification that can be applied to migratory behaviour including: 1) changes in the timing of migratory movement; 2) changes in migration patterns and migratory direction; 3) changes in the intensity of migratory activity within populations; and 4) changes in the proportion of individuals displaying migratory behaviour (Berthold, Reference BERTHOLD2001).

It is anticipated that the impact of climate change on migrants will be more severe than the impact on resident species (Huntley et al., Reference HUNTLEY, COLLINGHAM, GREEN, HILTON, RAHBEK and WILLIS2006). Of the 298 migratory bird species listed in the Convention on the Conservation of Migratory Species of Wild Animals Appendices, approximately 84% were identified as being affected by climate change (Robinson et al., Reference ROBINSON, CRICK, LEARMONTH, MACLEAN, THOMAS, BAIRLEIN, FORCHHAMMER, FRANCIS, GILL, GODLEY, HARWOOD, HAYS, HUNTLEY, HUTSON, PIERCE, REHFISCH, SIMS, SANTOS, SPARKS, STROUD and VISSER2009). Although it is difficult to predict how climate change will affect avian migration routes, it is anticipated that many birds will modify migration routes corresponding to species-specific factors including, but not limited to, location of breeding grounds; location of wintering sites; historical stopover sites; ecological barriers; traditional migration routes; and mechanisms governing migration for that species (Berthold, Reference BERTHOLD1996). Climate-driven changes in migratory routes have been previously documented in birds (Fiedler, Reference FIEDLER2003); however, it is important to note that for some species, adaptive modification of migratory behaviour and routes might be slow or absent altogether (Pulido, Reference PULIDO2007).

changes in avian phenology

Climate change has had a profound effect on the seasonality of many biological systems, some of which are closely associated with the timing of avian life-cycle events. For instance, the timing of breeding activity is meant to coincide with peak food availability (Both et al., Reference BOTH, VAN TURNHOUT, BIJLSMA, SIEPEL, VAN STRIEN and FOPPEN2010; Stenseth and Mysterud, Reference STENSETH and MYSTERUD2002); a temperature-dependent factor (Visser et al., Reference VISSER, HOLLEMAN and GIENAPP2006). Spring temperatures in temperate regions have been getting progressively warmer earlier in the season, resulting in an earlier peak in food availability (Both and Visser, Reference BOTH and VISSER2001; Both et al., Reference BOTH, VAN TURNHOUT, BIJLSMA, SIEPEL, VAN STRIEN and FOPPEN2010; Visser et al., Reference VISSER, HOLLEMAN and GIENAPP2006). Consequently, many birds have advanced laying dates to accommodate the seasonal shift (Both et al., Reference BOTH, ARTEMYEV, BLAAUW, COWIE, DEKHUIJZEN, EEVA, ENEMAR, GUSTAFSSON, IVANKINA, JÄRVINEN, METCALFE, NYHOLM, POTTI, RAVUSSIN, SANZ, SILVERIN, SLATER, SOKOLOV, TÖRÖK, WINKEL, WRIGHT, ZANG and VISSER2004; Brown et al., Reference BROWN, LI and BHAGABATI1999; Crick and Sparks, Reference CRICK and SPARKS1999; Forchhammer et al., Reference FORCHHAMMER, POST and STENSETH1998; McCleery and Perrins, Reference MCCLEERY and PERRINS1998; Møller et al., Reference MØLLER, RUBOLINI and LEHIKOINEN2008; Winkler et al., Reference WINKLER, DUNN and MCCULLOCH2002). Crick and Sparks (Reference CRICK and SPARKS1999) have shown that 20 different bird species in the UK were laying eggs earlier than in previous years. However, to lay eggs earlier, many birds have modified migratory activity to be able to arrive on breeding grounds earlier (Jonzen et al., Reference JONZEN, LINDEN, ERGON, KNUDSEN, VIK, RUBOLINI, PIACENTINI, BRINCH, SPINA, KARLSSON, STERVANDER, ANDERSSON, WALDENSTROM, LEHIKOINEN, EDVARDSEN, SOLVANG and STENSETH2006). Advances in spring arrival have been recorded in both long- and short-distance migrants from a range of taxonomic groups (Austin and Rehfisch, Reference AUSTIN and REHFISCH2005; Winkler et al., Reference WINKLER, DUNN and MCCULLOCH2002). To make this adjustment, some species are wintering closer to their breeding grounds to reduce the amount of time spent migrating (Austin and Rehfisch, Reference AUSTIN and REHFISCH2005). In north-eastern North America, short-distance migrants experienced greater advances in arrival (13 days) compared to long-distance migrants (4 days) (Rainio, Reference RAINIO2008), with an overall advance in arrival date of 8 days over the course of the 20^th century (Butler, Reference BUTLER2003). Not all species of birds have adjusted the timing of live-cycle events, and even among those who have, it may not be sufficient to accommodate rapid advancement of spring conditions on the breeding grounds, leading to an ecological mismatch between the timing of breeding and peak food availability (Both et al., Reference BOTH, VAN TURNHOUT, BIJLSMA, SIEPEL, VAN STRIEN and FOPPEN2010, Møller et al., Reference MØLLER, RUBOLINI and LEHIKOINEN2008).

changes in avian distributions and migratory distances

It has been shown that many birds are changing their distribution in response to climate change, favouring shifts towards the poles (Brommer, Reference BROMMER2004; Hitch and Leberg, Reference HITCH and LEBERG2007; Huntley et al., Reference HUNTLEY, COLLINGHAM, GREEN, HILTON, RAHBEK and WILLIS2006; La Sorte and Thompson, Reference LA SORTE and THOMPSON2007; Parmesan and Yohe, Reference PARMESAN and YOHE2003; Thomas and Lennon, Reference THOMAS and LENNON1999; Zuckerberg et al., Reference ZUCKERBERG, WOODS and PORTER2009) or shifting their altitudinal range higher (Parmesan and Yohe, Reference PARMESAN and YOHE2003; Sekercioglu et al., Reference SEKERCIOGLU, SCHNEIDER, FAY and LOARIE2008; Walther et al., Reference WALTHER, POST, CONVEY, MENZEL, PARMESAN, BEEBEE, FROMENTIN, HOEGH-GULDBERG and BAIRLEIN2002). In a study by Thomas and Lennon (Reference THOMAS and LENNON1999), the range and breeding distribution of birds in Britain shifted northward by an average of 18.9 km over 20 years with no southern range expansion observed in northern species. The observed changes in distribution are consistent with climate warming (Thomas and Lennon, Reference THOMAS and LENNON1999), suggesting that climate change might be at least partly responsible. An analogous study by Hitch and Leberg (Reference HITCH and LEBERG2007) found similar results, in which North American birds shifted north by an average of 2.35 km/yr; however, the shifts observed in North America were occurring at a much faster rate compared to Britain (0.95 km/yr) (Thomas and Lennon, Reference THOMAS and LENNON1999). As with the European birds, no change in southern range margins was observed in the more northern species. There have been similar changes observed in the southern hemisphere, where many species of birds have been extending their range boundaries southward or moving to higher altitudes and contracting their northern range margins (Chambers et al., Reference CHAMBERS, HUGHES and WESTON2005; Reid, Reference REID2003). Birds serve as a valuable model when investigating the relationship between range expansion and climate change, because many birds have distributions that are correlated to temperature margins (Joseph and Stockwell, Reference JOSEPH and STOCKWELL2000).

Most migratory birds that breed in the temperate zone respond to increases and decreases in temperature; low temperatures favour an increase in migratory activity, including longer migratory distances and reduced time spent on the breeding grounds (Pulido, Reference PULIDO2007), and high temperatures favour a reduction in migratory activity (Berthold, Reference BERTHOLD2001; Pulido and Berthold, Reference PULIDO and BERTHOLD2004). For instance, short-distance migrants are benefiting from milder winters by remaining closer to their breeding grounds during the winter, or forgoing migration altogether and remaining on breeding grounds on a year-round basis (Butler, Reference BUTLER2003; Pulido and Berthold, Reference PULIDO and BERTHOLD2010). After analyzing data on 24 short-distance migrant species in Europe during the period from 1932 to 2004, it was shown that 12 of these displayed a statistically significant reduction in migration distance as wintering grounds shifted closer to breeding areas (Visser et al., Reference VISSER, PERDECK, VAN BALEN and BOTH2009). Furthermore, within the last hundred years, several species that were formerly considered partial or short-distance migrants have stopped migrating (Berthold, Reference BERTHOLD1999; Pulido and Berthold, Reference PULIDO and BERTHOLD2010).

However, the impact of climate change on long-distance migrants differs from short-distance migrants. The northward shift in breeding ranges (Hitch and Leberg, Reference HITCH and LEBERG2007; Parmesan and Yohe, Reference PARMESAN and YOHE2003; Thomas and Lennon, Reference THOMAS and LENNON1999; Zuckerberg et al., Reference ZUCKERBERG, WOODS and PORTER2009) could potentially increase migration distances for long-distance migrants (Doswald et al., Reference DOSWALD, WILLIS, COLLINGHAM, PAIN, GREEN and HUNTLEY2009). Doswald et al. (Reference DOSWALD, WILLIS, COLLINGHAM, PAIN, GREEN and HUNTLEY2009) evaluated the potential impact of climate change on the ranges and migration distances of Sylvia Warblers in Europe. The researchers found a consistent northward shift in breeding ranges, whereas the potential non-breeding range margins demonstrated no directional change. Consequently, long-distance migrants are expected to face increased migratory distances (Doswald et al., Reference DOSWALD, WILLIS, COLLINGHAM, PAIN, GREEN and HUNTLEY2009).

changes in migratory destinations and staging site usage in migrants

For those species that do adapt to climate change, survival will still be challenging due to a lack of suitable habitat combined with environmental pressures induced by climate change. These environmental stressors include increased frequency of floods, droughts and forest fires; together, these changes will likely drive birds into urban areas more regularly (Chambers et al., Reference CHAMBERS, HUGHES and WESTON2005). For instance, during 2003, when many parts of Australia were affected by drought, it was reported that large flocks of Australian White Ibis (Threskiornis molucca), a species that has been associated with the spread of disease (Epstein et al., Reference EPSTEIN, MCKEE, SHAW, HICKS, MICALIZZI, DASZAK, KILPATRICK and KAUFMAN2006), established a large nesting colony at Lake Gillawarna, a public park, to avoid inland droughts on the breeding grounds (City of Bankstown, Reference CITY OF BANKSTOWN2004; Martin et al., Reference MARTIN, FRENCH and MAJOR2010). While nomadic range shifts of this nature are only short-term, generally lasting a few years or less, these drought-induced movements are becoming more commonly observed in water-birds, in which large numbers of various species are moving to coastal regions to more hospitable environments (Martin et al., Reference MARTIN, FRENCH and MAJOR2010). Orders of avian species known to carry pathogens that can infect poultry are presented in Table 1 of Part II of this review.

It is likely that similar situations will occur in North America with climate change, especially in the Prairie Pothole Region (PPR). The PPR is located in the Northern Great Plains and serves as one of the most important breeding sites for waterfowl (Batt et al., Reference BATT, ANDERSON, ANDERSON and CASWELL1989; Bethke and Nudds, Reference BETHKE and NUDDS1995). Although the PPR constitutes only a small portion of the available breeding habitat in North America, it generates between 50-80% of the duck population (Batt et al., Reference BATT, ANDERSON, ANDERSON and CASWELL1989). There is concern that climate change could decrease the quality and abundance of shallow wetlands that serve as a breeding habitat for several waterfowl species (Murkin et al., Reference MURKIN, MURKIN and BALL1997; Sorenson et al., Reference SORENSON, GOLDBERG, ROOT and ANDERSON1998). These changes could influence waterfowl population dynamics (Batt et al., Reference BATT, ANDERSON, ANDERSON and CASWELL1989; Poiani and Johnson, Reference POIANI and JOHNSON1991; Swanson and Duebbert, Reference SWANSON and DUEBBERT1989), potentially causing birds to relocate to new breeding grounds, depend more substantially on semi-permanent wetlands, forgo breeding altogether, or experience failure when re-nesting (Poiani and Johnson, Reference POIANI and JOHNSON1991; Swanson and Duebbert, Reference SWANSON and DUEBBERT1989).

When precipitation and temperature create ideal breeding conditions, waterfowl will settle to breed in the prairies (Johnson and Grier, Reference JOHNSON and GRIER1988). However, during years of widespread drought, waterfowl forgo breeding, experience reduced reproductive success, or move farther north into Canada where wetlands are less abundant but water levels experience fewer fluctuations (Johnson et al., Reference JOHNSON, MILLETT, GILMANOV, VOLDSETH, GUNTENSPERGEN and NAUGLE2005; Sorenson et al., Reference SORENSON, GOLDBERG, ROOT and ANDERSON1998). When considering how closely duck populations correspond to the number of ponds in the PPR at the beginning of the breeding season (Johnson et al., Reference JOHNSON, MILLETT, GILMANOV, VOLDSETH, GUNTENSPERGEN and NAUGLE2005), there will likely be a decrease in duck populations as drought frequency increases (Sorenson et al., Reference SORENSON, GOLDBERG, ROOT and ANDERSON1998). Using computer modelling, Sorenson et al. (Reference SORENSON, GOLDBERG, ROOT and ANDERSON1998) predicted that by the year 2050, the number of ponds in May in the PPR will decrease by 38% and duck populations will decrease by 46% (Sorenson et al., Reference SORENSON, GOLDBERG, ROOT and ANDERSON1998).

The effects of climate change on the PPR and its subsequent impact on migrants is not isolated to North America; other important migrant habitats, including breeding, wintering, and stopover sites, will be vulnerable to the effects of climate change (Bairlein and Hüppop, Reference BAIRLEIN and HÜPPOP2004; Sehgal, Reference SEHGAL2010). For instance, rising sea levels could potentially render many sites unusable for migrant stopovers (Huntley et al., Reference HUNTLEY, COLLINGHAM, GREEN, HILTON, RAHBEK and WILLIS2006). If the availability of suitable habitat decreases substantially, birds might begin crowding on substandard sites (Wobeser, Reference WOBESER1992). With additional stress on staging sites caused by depletion of natural habitats, coastal erosion, development of man-made barricades, changes in land-usage, and the introduction of invasive species (Mehlman et al., Reference MEHLMAN, MABEY, EWERT, DUNCAN, ABEL, CIMPRICH, SUTTER and WOODREY2005; Sehgal, Reference SEHGAL2010), some migrants might be pressured into changing migration routes and stopover site usage (Bairlein and Hüppop, Reference BAIRLEIN and HÜPPOP2004; Huntley et al., Reference HUNTLEY, COLLINGHAM, GREEN, HILTON, RAHBEK and WILLIS2006).