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- Materials and methods
- Supporting Information
Throughout the world, conservation and harvest management of waterbirds rely on flyway populations as the basic management unit, for example, in the African-Eurasian Waterbird Agreement, the Ramsar Convention and the North American Waterfowl Management Plan (for an overview, see Boere, Galbarith & Stroud 2006). Hence, in cases where a species has been divided into more than one population, knowledge of delineation of populations, rate of exchange and gene flow between populations is a fundamental prerequisite for population conservation, harvest management, designation of networks of key sites and disease transmission risk assessments. With the unprecedented current rate of global climate and land-use change, many populations undergo dramatic range contractions or expansions (McCarty 2001; Bohning-Gaese & Lemoine 2004; McDonald et al. 2012), increasing the need for up-to-date information on population structures and distributions and understanding underlying drivers, including potential dispersal between populations. Assessments of population delineation have traditionally been based on direct methods such as recoveries of dead ringed birds, observations of marked individuals, tracking of birds marked with transmitters and, more recently, by indirect and direct genetic methods. However, with few exceptions where marking and genetic sampling have systematically covered the geographic populations of a species (e.g. Williams et al. 2008; Shorey et al. 2011; Kraus et al. 2013), existing information remains too patchy to make other than qualitative judgements about connectivity between flyway populations.
The pink-footed goose Anser brachyrhynchus (hereafter pinkfeet) is an Arctic and sub-Arctic breeding species, which is divided into two flyway populations: the Iceland/Greenland population wintering in the British Isles (western population) (Mitchell et al. 1999) and the Svalbard population migrating via Norway to wintering grounds in Denmark, the Netherlands and Belgium (eastern population) (Madsen et al. 1999). The two populations follow different migration routes and spend the winter in Britain and continental Europe, respectively. As most western Palaearctic goose populations, the two populations of pinkfeet have increased dramatically in numbers during recent decades (Fox et al. 2010). Large concentrations winter relatively close to each other in Norfolk in south-east England and Flanders in Belgium (c. 150 km apart across the English Channel). Resightings of marked individuals have revealed that a small number of pinkfeet move from east to west at least in some years, roughly representing a few hundred individuals (Madsen et al. 1999). Exchange is possibly related to winter severity. Thus, in cold winters in north-western Europe, ringed individuals of eastern pinkfeet may move to France (Holgersen 1960; J. Madsen, unpublished data) and Britain (Madsen et al. 1999), and heavy snow cover in Belgium can split large aggregations of geese into smaller flocks that spread over a larger area (Madsen et al. 1999).
Genetic analyses based on mitochondrial DNA (mtDNA) have shown a population structure, but also suggested gene flow between the two populations of pinkfeet, with a low level of female gene flow from west to east, but a relatively higher flow from east to west (Ruokonen, Aarvak & Madsen 2005). These analyses provide information about genetic connectivity, defined as the degree to which gene flow affects evolutionary processes within populations, but they do not give precise information on demographic connectivity, defined as the degree to which population growth and vital rates are affected by exchange of individuals (Lowe & Allendorf 2010). Precise estimates of demographic exchange rates in pinkfeet are needed because the Svalbard population has recently been selected as the first European case for implementing adaptive harvest management at the flyway scale, under the auspices of the African-Eurasian Waterbird Agreement (Madsen & Williams 2012). This will require fine-tuned monitoring of demographic variables and modelling of an optimal harvest strategy.
The aim of this paper is to quantify the demographic connectivity between the two populations of pinkfeet based on resightings of individually marked birds in both populations. We hypothesize that exchange from east to west increases with cold winter spells in continental north-west Europe. Furthermore, to see whether there is evidence of permanent emigration (dispersal), temporary movements or alternative migration strategies in the populations, we describe the fate of individuals that switch between populations in terms of their subsequent life histories. We compare the direct observations with the indirect evidence of genetic connectivity and discuss the results in relation to international waterbird management needs.
- Top of page
- Materials and methods
- Supporting Information
The delineation of populations is an important prerequisite for the conservation and management of waterbirds. Taking the western Palaearctic swans, geese and ducks as an example, a total of 43 native species and subspecies breed and winter in the region, among which 21 occur as one defined population, while 22 species or subspecies occur in two or more (up to seven) defined populations (derived from Scott & Rose 1996; Wetlands International 2013). Our study is the first to quantitatively assess the rate of exchange between flyway populations of a western Palaearctic waterfowl species and the fate of individuals that switch. It is unique because we were able to make use of data from two recent marking and resighting schemes, coinciding in time and methodology, although not designed with a common purpose. Such parallel schemes have existed for other western Palaearctic goose populations as well (see Fox & Madsen 1999); however, except for a few long-term studies such as the barnacle goose Branta leucopsis (e.g. Owen & Black 1991), there is no sufficient information to perform quantitative analyses of exchange. Hence, for populations such as white-fronted geese Anser a. albifrons and greylag geese Anser anser, delineation of flyways and emigration/immigration rates remain unresolved. In the case of greylag geese, the current growth of populations and expansion of ranges, including re-established stocks in Scotland and continental Europe, blur the interpretability even further.
With regard to Palaearctic duck populations, the flyway delineations (Scott & Rose 1996) are generally based on more patchy data than for geese. For widespread species like teal Anas crecca, the proposed western Palaearctic flyways are regarded as doubtful (Guillemain, Sadoul & Simon 2005). At the extreme end of the spectrum, for mallards Anas platyrhynchos, which have a Holarctic distribution, genetic analyses based on mtDNA as well as nuclear markers have confirmed previous evaluations based on ringing (Scott & Rose 1996) that there is no clear population structure at least at the continental scale, suggesting that continental flyway populations cannot be defined (Kulikova et al. 2005; Kraus et al. 2011, 2013). Nevertheless, for practical management purposes, biogeographical ‘stocks’ have been defined both in the Old World (Delany & Scott 2006) and the New World (e.g. U.S. Fish & Wildlife Service 2012). In North America, adaptive harvest management operates with three stocks of mallards, justified by geographic differences in their reproduction, mortality and migrations, suggesting that there may be corresponding differences in optimal levels of sport harvest. The three stocks are defined by their non-overlapping breeding distributions, while it is recognized that there is some mixing in non-breeding areas. In contrast, in the western Palaearctic, stocks are defined on the basis of winter distributions (Scott & Rose 1996), which has no true biological justification, but is a pragmatic approach taken because this is where ducks are monitored (Delany & Scott 2006).
Throughout Europe, most dabbling duck ringing has been performed on staging, moulting and wintering grounds and not on the breeding grounds. Combined with the fact that most of the resulting data are ring recoveries of shot birds and not multiple resightings of marked individuals such as for geese, this makes it difficult to decipher flyways correctly. In order to derive a better description of migration systems, it is important that future ringing, tagging or molecular sampling focuses on the breeding grounds to which waterfowl are known to show natal and breeding-site fidelity; in ducks, notably among females (Anderson, Rhymer & Rohwer 1992).
For pinkfeet, the capture–resighting analyses showed that exchange of individuals between the two populations takes place, but is a relatively rare event. Because we restricted the quantitative statistical analyses to individuals for which we have three or more neck-band resightings in a season, and because of differences in resighting probabilities in the two flyways and at certain times of the season, the rates of exchange are minimum estimates. As hypothesized, exchange from east to west increased in winters with much snow extending to the south-western part of the winter range of the eastern flyway; however, the relationship was driven by the winter of 2009/2010, when there was a thick snow cover throughout the winter range from Denmark through to Belgium. Qualitative assessments from previous winters with extensive snow cover, for example, 1996/1997, support the results of the statistical analyses (Madsen et al. 1999). In the winters of 1996/1997 and 2009/2010, the geese moved all the way to the limit of the range in south-west Belgium before crossing over to Britain. Based on a rough extrapolation of exchange rates to population level and taking into account that the rates of exchange are minimum estimates, the exchange in cold winters could constitute hundreds if not thousands of individuals, perhaps >1% of the eastern population. The general winter climate in Britain is known to be more mild and wet compared to continental Europe, and eastern birds using Britain as an alternative winter ground in severe winters might not make a ‘bad’ choice moving westwards, which is common in waterfowl in continental Europe (Ridgill & Fox 1990).
In this study, all exchanged eastern birds with known destiny reappeared in the eastern population, suggesting no permanent emigration to the western population. Eastern birds seen in Britain either crossed back to Belgium or the Netherlands or showed northward movement within Britain with a suggested direct crossover from Britain to Norway (in 2009/2010). Hence, the movements do not appear to be erratic, and the geese appear to have knowledge of their whereabouts in Britain and can orient themselves back to their original flyway. Eastern and western pinkfeet most likely mix on the staging areas in Britain, and the departure towards Norway in a north-easterly direction probably takes place when western birds are on their way towards Iceland in a north-westerly direction. The apparent crossing of the North Sea from Scotland to Norway by several individuals suggests that this is an alternative migration route, particularly used following cold winters. The appearance of eastern birds in Scotland in autumn may be a sign of a migration route established by the same group of geese using the reverse route in spring (although this has not yet been confirmed by individually marked birds). The fact that the majority of exchanged individuals were older birds supports the suggestion that the exchanges are not erratic events (as might be expected if it were younger birds), or related to young mate-searching birds, but more likely to be an alternative winter strategy. Western geese switching to the eastern flyway were not confirmed to emigrate on a permanent basis either.
At first glance, the capture–resighting analyses appear to support the genetic analyses, suggesting gene flow between the two populations and primarily from east to west (Ruokonen, Aarvak & Madsen 2005). However, detailed examination of the life histories of exchanged individuals raised some interesting questions about this interpretation. While the mtDNA-based genetic analysis suggested effective dispersal, that is, reproduction in the foreign population, the direct observations did not confirm this. There may be several reasons for this discrepancy:
- The sampling of birds used for genetic analyses may accidentally have included birds from the eastern or western population that were temporarily visiting the foreign population, thus leading to a false expression of gene flow. However, in the genetic study, samples were taken in both of the two breeding and non-breeding ranges and the fact that haplotypes in Britain and Iceland (representing the non-breeding and breeding grounds of the western population) were similar contradicts this hypothesis and suggests that gene flow has occurred.
- Dispersal takes place, but is not captured by the direct observations. Because resighting effort is very low in Iceland and on Svalbard, we cannot exclude that some foreign individuals have escaped observation and have bred in the ‘wrong’ flyway.
- The genetic analyses estimate gene flow in a historic time perspective, while the mark–resightings express the current situation of exchange. Hence, in a longer time perspective, there has been effective dispersal between the two populations.
It should also be borne in mind that the statistical analyses based on the mtDNA genotype frequencies have their limitations in quantifying population structure and gene flow (e.g. Abdo, Crandall & Joyce 2004). With the recent advances in the use of molecular markers and population genomics, analytical options have now become much more powerful, and exchange can be measured directly, potentially assigning individuals to their parents (Broquet & Petit 2009). For the moment, we conclude that in terms of present demography, the two populations of pinkfeet are virtually closed, although they partially overlap in time and space, particularly following cold winters, but there is a genetic connectivity due to low levels of dispersal (earlier or present) between populations. Higher future rates of exchange will not necessarily imply a higher genetic mixing of the two populations, because individuals are likely to find their way back to their original flyway. More regular exchange may lead to the evolution of alternative migration routes, for example, birds migrating from Svalbard via staging sites in Norway across to wintering sites in Britain.
Perspectives and implications for management
In relation to the current plans to introduce adaptive harvest management of the Svalbard population of pinkfeet (Madsen & Williams 2012), this study shows that there is no imminent need to consider emigration and immigration in demographic models that are developed to predict an optimal harvest. In the case of cold winter movements to Britain, eastern geese may be exposed to additional harvest mortality; in Britain, the inland hunting season closes on 31 January and shooting on the foreshore closes on 14 February, while pinkfeet are fully protected in Belgium and the Netherlands and have a hunting season in Denmark closing on 15 January. However, even at the current peak rates of exchange (in total up to a few thousand individuals), harvest in Britain is unlikely to have a critical impact at the population level.
In essence, existing information about the connectivity of western Palaearctic flyway populations is insufficient for population management, except for taking a very prudent conservation approach. The majority of marking schemes for waterbirds in Europe have been set up by individual researchers or teams, rarely coordinated between flyway populations and mostly without a clearly stated purpose to underpin management. Several of the marking schemes on geese, ducks and swans have been difficult to maintain in the long term and thus cannot help explain recent dramatic changes in population sizes and ranges. There is a growing wish to internationally coordinate management of waterbirds in Europe and in the African-Eurasian region, as manifested by the recent strategy of the African-Eurasian Waterbird Agreement (AEWA 2008). This is exemplified with the international management plan for the Svalbard population of pinkfeet (Madsen & Williams 2012) and plans in progress for cormorants Phalacrocorax carbo (Behrens, Rauschmayer & Wittmer 2008). If this approach is to be applied more widely, there is an urgent need to rethink waterbird marking schemes, to design and sustain them in order to better underpin management needs.
New population genomic tool kits give promise for making quick and cost-effective advances in understanding population structures and dispersal, such as has been shown for mallards A. platyrhynchos (Kraus et al. 2013). Future studies should take advantage of combining the classic and the molecular tools. As demonstrated for pinkfeet, the combination of methods leads to supplementary insights, which would otherwise not be possible.
Genetic analyses in pinkfeet and North American mallards show gene flow, while demographic analyses give justification for separation in stocks or demographic populations. In both cases, a demographically based population definition is needed for current management planning, while for longer-term conservation of the species, the genetic definition has more bearing. We recommend that to support management decisions at population levels, future studies of connectivity should use classic marking in combination with molecular methods and focus sampling on waterbird breeding grounds.