Highly variable movements by Andean Flamingos ( Phoenicoparrus andinus ): implications for conservation and management

. The Andean Flamingo ( Phoenicoparrus andinus ) is endemic to the central Andes Mountains, with the majority of the population distributed between Argentina, Bolivia, and Chile. It is the rarest of the six flamingo species on the planet and is one of the least studied flamingos. Little information exists about its annual cycle, including which wetlands individual Andean Flamingos use at different times of year, posing an obstacle to developing effective conservation planning for its populations. In 2020 and 2022, we attached GPS-enabled satellite transmitters to four Andean Flamingos in northwestern Argentina, tracking their movements throughout the year to provide an initial assessment of their movement patterns, including timing, rate, and distances of movements between wetlands. We found highly variable movement patterns between individual flamingos. After the breeding season, which they spend at high elevations, some flamingos moved northwards to overwinter in the central


INTRODUCTION
The Andean Flamingo (Phoenicoparrus andinus) is endemic to the central Andes and is one of the rarest waterbirds on the planet, with a global population size estimated at less than 80,000 individuals (Marconi et al. 2020).It is categorized as vulnerable (IUCN 2022) and is listed by the Convention of Migratory Species as "facing a very high risk of extinction in the wild in the near future" (CMS 2018) in large part because the highland lakes they depend upon to breed and forage are drying up and becoming increasingly polluted by mining activities (Caziani et al. 2007, Derlindati et al. 2014, Marconi et al. 2022) and overgrazing (Caziani et al. 2001(Caziani et al. , 2007)).Additionally, Andean Flamingos overwinter in lowland wetlands that are increasingly threatened by industrial agriculture (Valqui et al. 2000, Romano et al. 2006, Roberts et al. 2020).Furthermore, a recent study conducted in Chile showed that Andean Flamingos are negatively impacted by both lithium mining and climate change (Gutiérrez et al. 2022).
Effective conservation measures are therefore urgently needed to ensure that this species is protected across its range and throughout the year; yet Andean Flamingos are one of the least studied of the planet's six flamingo species (Delfino and Carlos 2021a).To date, most research on Andean Flamingos has focused on foraging habits (Derlindati et al. 2014), population size, and habitat use (Caziani and Derlindati 2000, Caziani et al. 2001, Romano et al. 2006, Caziani et al. 2007).One critical knowledge gap and conservation priority is to identify wetlands used by Andean Flamingos throughout their full annual cycle, which has been identified as a priority for research (Caziani et al. 2007).Research on flamingos in Africa and Europe has shown that knowing which wetlands flamingos use at different times of year is critical to developing effective conservation measures (McCulloch et al. 2003, Amat et al. 2005).If flamingo movements are directional and predictable, a site-based conservation strategy (i.e., in which a handful of sites are targeted for conservation) is appropriate, whereas if their movements are highly variable, the best conservation approach may be one that focuses on protecting the species across its entire range (Roshier andReid 2003, Caziani et al. 2007).
Andean Flamingos are thought to be primarily altitudinal migrants, breeding in the high Andes and overwintering in the lowlands, although the strength of their migratory connectivity (i.e., the amount of overlap between individuals as a result of migration; see review by Fudickar et al. 2021) remains unknown (Caziani et al. 2007).Nevertheless, a portion of the Andean Flamingo population spends the entire year at some Andean lakes where geothermal activities or the lower elevation prevents water from freezing; hence, they are also considered partial elevational migrants (Caziani et al. 2007).Because of the rapid transformation of the Andean Flamingo's environment as a result of agriculture, lithium mining and climate change, research on their full annual cycle would provide vital data for conservation planning (Marra et al. 2015).In particular, identifying the network of wetlands these birds use throughout the year would help identify which wetlands should be prioritized for Andean Flamingo conservation.Our objectives were therefore to identify the following: (1) sites used by individual Andean Flamingos throughout the year and (2) the timing, rate, and distance of their movements between sites.

METHODS
We captured Andean Flamingos in February 2020 at the Salar de Llullaillaco, Salta Province, Argentina (24.76° S, 68.34° W, 3759 m) and in February 2022 at Laguna de Vilama (22.58° S, 66.91°W , 4493 m), Jujuy Province, Argentina (Fig. 1).These sites were being used for foraging by flamingos, with no breeding activity observed, such that we do not know whether the flamingos we captured were breeding that season.Captures were carried out using leghold traps made of loops (17 kg test) of polyethylene fishing line positioned at 1 m intervals along a 100 m fishing line (34 kg test;McCulloch et al. 2003, Amat et al. 2005).Traps were placed underwater and held to the bottom of the lake by metal stakes in areas where Andean Flamingos were seen foraging.Traps were constantly monitored by at least two observers.When a flamingo became ensnared, it was quickly extracted and taken to the lakeshore where its mass was measured by placing it in a bag and hanging it on a Pesola spring scale (Ralph et al. 1993).A satellite transmitter (model GT-65GS-GPS, Geotrak, Inc., Apex, NC) was then attached to the flamingo using a backpack double-loop harness (Childress et al. 2004) made of tubular Teflon ribbon (Bally Ribbon Mills, Bally, PA).The mass of each transmitter plus the harness was 71 g and was 3% or less of the body mass of the flamingos to which they were attached.The birds were then released at the site of capture.Transmitters were Argos Doppler and GPS-enabled and had a duty cycle of 8 h on and 60 h off (transmitter IDs: 178851 and 178853) or 8 h on and 46 h off (transmitter 178857 and 178860).

Data analysis
We summarized the following: (1) start and end dates of movements between wetlands, (2) distance and duration of movements between individual wetlands, (3) cumulative distance (the sum of distances along the full path between start and end points along multiple wetlands used throughout the year), (4) movement persistence (a combined measure of speed and directionality of movements; Jonsen et al. 2019), ( 5) annual movement rate (the cumulative distance/duration), and (6) elevational change between seasons.The small number of tracked flamingos precluded inferential statistical analysis.Unless noted otherwise, all values represent means ± SD, combining data from 2020 and 2022.
We estimated locations using a correlated random walk model that included the uncertainty in location class (Table 1) provided by the transmitters, using the foieGras R package (Jonsen et al. 2019, 2020, Jonsen and Patterson 2021) and predicted locations using a 48-hour time step.We estimated the movement persistence parameter (Jonsen and Patterson 2021) where small values indicate slow, undirected movements related to foraging, and larger values are indicative of faster, directed movements, such as those between wetlands.We associated locations with wetlands and used the wetland complex Table 1.Number of fixes by Argos location class for each individual after applying speed, distance, and angle filtering (see Methods).The total number of fixes within each location class for each individual over the tracking period is presented in parentheses.The fraction of fixes (mean percent and standard error) that were retained for analysis for each location class after applying filters is shown in the last row.in combination with the movement persistence parameter to demarcate stationary periods.We extracted elevation (in meters; Farr et al. 2007) and land-cover classes (year = 2019; Buchhorn et al. 2020) for each position estimate using Google Earth Engine (Gorelick et al. 2017) via the rgee R package (Aybar et al. 2020).

RESULTS
We captured and outfitted transmitters on two adult (i.e., more than one year old) male Andean Flamingos on 21 February 2020 at Salar de Llullaillaco (flamingos 178853 and 178857).We captured and outfitted transmitters on another two adults for which we were uncertain of sex (flamingo 178860 on 24 February and flamingo 178851 on 25 February 2022) at Laguna de Vilama.We obtained fixes from all four flamingos, which allowed a description of most parameters we set out to measure, including cumulative movement distance (Fig. 2).

Individual patterns
Flamingo 178851 departed from Laguna de Vilama, Jujuy Province, Argentina in March 2022 to spend the rest of the year in the vicinity of Lago Poopó and nearby Lago Uru Uru in Bolivia at ~3700 m (Fig. 3).It visited Laguna de los Pozuelos in January 2023 for two days, returned to Lago Uru Uru and Lago Poopó and then moved to a system of lowland wetlands (< 200 m elevation) in Santiago del Estero Province, Argentina in April 2023, remaining there until May, which is the end of its current tracking period.
Flamingo 178853 first moved to Laguna Mar Chiquita, Córdoba Province, Argentina in May 2020, remained there until 8 June and then used smaller wetlands in Santa Fe Province, Argentina (Fig. 3).In September 2021, it started sending fixes that suggested large, irregular movements across the landscape and away from water.Fixes then originated from a nearby urban area, suggesting that the flamingo had been killed by hunters or that the transmitter had been found by people after it had fallen off the flamingo or after it had died of natural causes.We therefore only analyzed data for that bird up to 16 September 2021.Flamingo 178860 briefly moved to Laguna de los Pozuelos in March 2022 and then returned to Laguna de Vilama where it remained at least until April.In April, it returned to Laguna de los Pozuelos and then to Laguna Mar Chiquita, Córdoba Province, where it remained at least until June (Fig. 3).It visited Laguna Santana in Córdoba Province until September and then moved to Laguna Mar Chiquita (a different lake than the previous with the same name), near the town of Junín in Buenos Aires Province, Argentina.Notably, this lake is outside of the current described range of the species (Roberts et al. 2020).It remained there until early October when it departed on a non-stop flight of

Seasonal movement rate and persistence
The mean daily movement rate throughout the study and across flamingos ranged from 0.37 km/h in winter to 0.89 km/h during post-breeding (Table 2), with a maximum recorded rate of 31 km/ h by flamingo 178860 on 10 October 2022, during its long, nonstop flight.Mean movement persistence was highest during the pre-breeding season and lowest during the post-breeding season (Table 2).

Seasonal elevational movements
Flamingos 178853 and 178860 exhibited elevational migration, spending the breeding season at >3000 m, sometimes >4000 m, and most of the non-breeding season near sea level in Argentina (Fig. 3).In contrast, flamingo 178857 spent both the breeding and non-breeding seasons at >3000 m (in Argentina and Bolivia, respectively; Fig. 3), and flamingo 178851 exhibited both strategies, overwintering at altitude in one year and moving closer to sea level during the post-breeding period of the following year.On average, flamingos spent the pre-breeding and breeding seasons at higher elevations than during the rest of the year, with mean breeding season elevation almost at 4000 m (Table 2).Variation in seasonal mean elevation was more than twice as high during post-breeding and winter relative to pre-breeding and breeding (Table 2).

Seasonal wetland use
Flamingos used fewer wetlands during the pre-breeding and breeding seasons than during the rest of the year, with the number of wetlands used highest during the post-breeding period (Table 2).The vast majority of locations used by flamingos were within permanent water bodies (n = 2810 locations; 48%), followed by areas classified as bare ground or sparse vegetation (n = 1936; 33%), and herbaceous vegetation (n = 528; 9%).Given that flamingos almost exclusively use water bodies, the use of areas classified as bare ground and vegetation likely represent sites where water is only seasonally present, i.e., on the dates the flamingos were at those sites, there would have been water present.

DISCUSSION
Although these results are based on a small sample size that precludes general conclusions, they are the first to show that Andean Flamingos are capable of moving rapidly across hundreds of kilometers with highly variable movement timing and direction, which is typical of other flamingo species (Childress et al. 2004, 2007, Béchet 2017, Pretorius et al. 2020, Delfino and Carlos 2021b).The flamingos we tracked moved extensively between wetlands in Argentina, Bolivia, and Chile, overwintering in the Andes of Bolivia or descending to overwinter close to sea level in central Argentina.Flamingos also moved extensively between wetlands during the winter.
Flamingos used a smaller number of wetlands during the prebreeding and breeding seasons, whereas they used a larger set of wetlands during the post-breeding and winter seasons.Their higher movement persistence (i.e., faster, directed movements) during pre-breeding and breeding seasons is likely a consequence of the spacing of suitable water bodies in the high Andes, requiring rapid movements between distantly separated sites.In contrast, during post-breeding and winter, they may be able to access a larger set of wetlands, requiring fewer long-distance flights, and be energetically less prepared to undertake fast movements as a result of having invested in breeding.Thus, during the breeding season at elevation, Andean Flamingos may be more limited by availability of water bodies that offer the appropriate conditions for reproduction versus during winter, when they may be more tolerant of a variety of conditions.That Andean Flamingos use a specific set of wetlands during breeding is reflected in the variation in elevation of sites they use during pre-breeding and breeding, which was much lower than at other times of year.Why some flamingos overwinter at altitude whereas others descend to near sea level could be in part due to individuals in poorer physical condition moving to the lowlands, where winter conditions are less extreme (see review by Barçante et al. 2017).That they can overwinter at altitude in some years but descend to the lowlands in others, as demonstrated by flamingo 178851, is likely a result of yearspecific environmental conditions across their range (e.g., as a function of the El Niño/La Niña cycle) and the condition of a given bird during that period (e.g., as a result of whether it attempted to breed).
The irregular movements of Andean Flamingos stand in contrast to those of Lesser Flamingos (Phoeniconaias minor) in southern Africa.The movements of the latter are more similar to migration than to nomadism because they are often characterized by a regular, repeated pattern between two primary locations (Pretorius et al. 2020).Likewise, Greater Flamingos (Phoenicopterus roseus) show high levels of connectivity between specific sites (Javed 2006) and may prefer to use specific parts of wetlands (Baker et al. 2006).
Developing effective conservation plans for species that exhibit such long-distance, highly variable movement patterns can be challenging.For the Andean Flamingo, it will require coordinated, international research and conservation cooperation to ensure adequate protection throughout their range and across the entire year.Andean Flamingo is included in Appendix I of the Convention on the Conservation of Migratory Species of Wild Animals, for which a memorandum was signed in 2008 by Bolivia, Chile, and Peru, but not Argentina.Such a disjointed international flamingo conservation effort, which has also been highlighted for Old World flamingos (e.g., McCulloch et al. 2003, Amat et al. 2005), is worrisome, given the fluid nature of the movements by Andean Flamingos that we detected between Argentina, Bolivia, and Chile (with one flamingo visiting all three countries).Additionally, Andean Flamingos use only a few breeding sites, with the Salar de Llullaillaco being one of only six known breeding sites in Argentina (Torres et al. 2019;E. Derlindati, personal observation).Recent lithium mining near that site is a potential threat to their ability to breed (E.Derlindati, personal observation), underscoring the urgent need for more research, monitoring, and conservation measures (see review by Marconi et al. 2022).
Future research priorities for Andean Flamingos include collection of detailed movement data from across their range, throughout the year, and from different ages and sexes.Additionally, mortality can be driven by mechanisms operating within a given season (e.g., nest predation) or between seasons (e.g., winter habitat quality affecting reproductive success in summer), so quantifying such seasonal interactions will be essential to understand the drivers of flamingo population dynamics (Rushing et al. 2017).

Fig. 1 .
Fig. 1.Overview of movement trajectories and sites (left panel) visited by four Andean Flamingos (Phoenicoparrus andinus), including names of major and minor sites (right panel).See Fig. 3 for explanation of individual flamingo movement trajectories.Arrows do not necessarily show routes used by flamingos.

Fig. 2 .
Fig. 2. Time series showing the cumulative distance traveled by individuals over the tracking period.The dots indicate when fixes were obtained for each individual.Transmitters had a duty cycle of 8 h on and 60 h off (transmitter/PTT IDs: 178851 and 178853) or 8 h on and 46 h off (178857 and 178860).The different phases of the annual cycle, Breeding (B), Postbreeding (Post-B), Winter (W), and Pre-breeding (Pre-B) are highlighted along the bottom and demarcated with vertical lines.Flamingo image by Lee Harding, John E. McCormack, Michael G. Harvey, Brant C. Faircloth, Nicholas G. Crawford, Travis C. Glenn, Robb T. Brumfield, and T. Michael Harvey.Attribution 3.0 Unported, courtesy of PhyloPic.org.

Fig. 3 .
Fig. 3. Movement trajectories and dates of visits to sites by four Andean Flamingos (Phoenicoparrus andinus).Number at the top right of each panel corresponds to an individual flamingo transmitter ID.Numbers before dates correspond to the chronological sequence of visits to each site.Site codes are: SL-Salar de Llullaillaco, Salta Province, Argentina; LVP-Laguna de Vilama and Laguna de los Pozuelos, Jujuy Province, Argentina; LP-Lago Poopó and Lago Uru Uru, Bolivia; and LMC-Laguna Mar Chiquita, Cordoba Province, Argentina.

Table 2 .
Mean (1 sd) movement parameters by season for four tracked flamingos.
** Total number of wetlands used by all tracked flamingos.