Breeding Biology of Arctic Terns (Sterna Paradisaea) in the Canadian High Arctic

Polar Biol DOI 10.1007/s00300-016-2072-1

ORIGINAL PAPER

Breeding biology of Arctic terns (Sterna paradisaea) in the Canadian High Arctic

Mark L. Mallory1 · Kelly A. Boadway2 · S. E. Davis3 · M. Maftei3 · Antony W. Diamond2

Received: 2 May 2016 / Revised: 28 December 2016 / Accepted: 28 December 2016 © Springer-Verlag Berlin Heidelberg 2017

Abstract The Arctic tern (Sterna paradisaea) is a well- Keywords Arctic · Clutch size · Polynya · Predation · known polar seabird which breeds around the circumpolar Seabird Arctic, and which undertakes the longest known annual migration of any organism. Despite its familiarity, there is little information on its breeding biology in the High Introduction Arctic, an important baseline against which future studies of climate change impacts on northern wildlife can The Arctic tern (Sterna paradisaea) is an iconic Arctic be compared. We studied the breeding biology of Arctic species with a circumpolar breeding distribution (Hatch terns in the Canadian High Arctic during five field sea- 2002). It is also a trans-equatorial migrant that winters sons, and compared this to breeding biology of terns from around Antarctica, and, consequently, this species travels more southern parts of its range. Because our field site farther each year than any other organism (Egevang et al. was beside a productive polynya, we expected that repro- 2010), potentially in excess of 90,000 km (Fijn et al. 2013). ductive metrics for terns nesting there would be relatively The breeding range of the Arctic tern extends from 84°N high. However, mean clutch size (1.7 eggs), mean egg size in coastal Greenland south to 42°N on the eastern coast (40.2 mm × 29.0 mm), mean nest initiation dates (6 July) of North America (Hatch 2002), with the majority of its were similar to Arctic terns breeding elsewhere. With our breeding population within the Subarctic through High data, we could not assess the independent effects of preda- Arctic marine zones (Salomonsen 1965). Despite this, most tion pressure, poor weather or low food supplies, but two research on this bird has focused on colonies in the south- years with low tern reproduction were also years with low ernmost, temperate regions of the Boreal marine zone (e.g., adult body mass and low clutch size (indicating poor food Hawksley 1957; Lemmetyinen 1973b; Gaston et al. 2009a). supplies), as well as low hatching success and high nest To date, few studies of Arctic tern breeding biology have abandonment (possibly due to high predation pressure). been conducted in High Arctic Europe (e.g., Bengtson 1971; Węsławski et al. 1994, 2006; Egevang 2010; Ege- vang et al. 2010) and even fewer, often partial seasons with a very specific focus, have been conducted in the North American Arctic (e.g., Drury 1960; Boekelheide 1980). * Mark L. Mallory Recently, concern has been expressed by management [email protected] agencies over a perceived decline in international Arc- tic tern populations in some parts of their range (CBIRD 1 Department of Biology, Acadia University, 33 Westwood Avenue, Wolfville, NS B4P 2R6, Canada 2014), which has been supported by some survey work (e.g., Gilchrist and Robertson 1999; Barrett et al. 2006), 2 Atlantic Laboratory for Avian Research, University of New Brunswick, P.O. Box 45111, Fredericton, NB E3B 6E1, although tern colonies are notoriously difficult to census Canada (e.g., Egevang and Frederiksen 2011). 3 High Arctic Gull Research Group, Bamfield, BC B0R 1V0, Seabirds are generally recognized as sensitive indi- Canada cators of marine ecosystem conditions (Cairns 1987;

Vol.:(0123456789)1 3 Polar Biol

Montevecchi 1993). Aside from their tissues serving as Methods key biomonitors of levels of environmental contamina- tion (Mallory and Braune 2012), their annual reproduc- Study site tive success and longer-term population trajectories have been used to track effects of environmental stressors We studied the breeding biology of Arctic terns at a large like climate variation for some species in Arctic Canada colony on Nasaruvaalik Island in Penny Strait, Nunavut (e.g., Gaston et al. 2009a). In this region, however, we (75° 49′N, 96° 18′W; Fig. 1), between 15 June–9 August currently lack knowledge about the breeding ecology of 2007, 16 June–17 August 2008, 16 June–29 July 2009, 15 many seabird species (Gaston et al. 2012; Mallory and June–7 August 2010, and 3 June–30 July 2011. There are Braune 2012), including terns, limiting their utility as several other tern colonies within 100 km (Maftei et al. indicators. This is unfortunate, because Arctic terns for- 2015), but Nasaruuvalik is the largest colony in the region. age at the water surface relatively high in the marine food The island is approximately 3 km × 1 km in size (Mallory web and have limited phenotypic flexibility (Durant et al. and Gilchrist 2003), is crescent-shaped, and is made of 2009; Grémillet and Charmantier 2010) and, thus, should alluvial gravel that has risen from the surrounding sea due prove particularly responsive to annual fluctuations in to isostatic rebound from historic glaciation. Terns nested food supplies. Certainly farther south in their breeding in two colonies among old beach ridges on the low, south- range, Arctic tern breeding effort and success have exhib- western and northeastern ends of the island (separated by ited marked variation and declines in the Bay of Fundy, 1.5 km), typically at elevations <5 m above sea level (asl). Canada, due in part to changing food availability (Dia- Our base camp was located on a central plateau of the mond and Devlin 2003). Furthermore, marine bird spe- island approximately 30 m asl, and out of view of nesting cies may differ in their breeding ecology in different parts terns; this was approximately 1 km north of the main south- of their range (Mallory et al. 2008), and there may also be western colony where we conducted our studies (hereafter marked natural variability in annual reproductive metrics “colony”). This colony supported about 300 pairs of nest- for seabird colonies (Grémillet and Charmantier 2010); ing terns within 0.17 km2, with nests 1–15 m from the next thus, it is important to evaluate whether knowledge gath- closest nest. We walked from the camp to the colony several ered from short-term studies or studies from various parts times daily (except in periods of rain or heavy fog), arriv- of a species’ range can be extrapolated elsewhere, such as ing at blinds (below) that were >50 m from the main nest- the Canadian Arctic. Basic knowledge about the ecology ing concentration of birds. From these blinds, several nests of Arctic-breeding seabirds is especially urgent at a time could be observed using binoculars and scopes, though few when a variety of natural and anthropogenic stressors are nest contents could be recorded. Although many research- changing and perhaps increasing in intensity in the Arctic ers elevate their blinds to help increase observation effec- marine environment (ACIA 2005; Arctic Council 2009). tiveness, this was not possible on this island, as stochas- We spent five field seasons studying the reproduc- tic visits by polar bears (Ursus maritimus) resulted in the tive biology of Arctic terns at a colony on a small island destruction of anything erected vertically. Generally, our situated beside a recurrent polynya in the High Arctic of arrival did not cause an obvious change in behavior of the Nunavut, Canada, with the goal of establishing baseline birds during nesting. There are also common eiders (Soma- values and annual variability in reproductive metrics of teria mollissima borealis), long-tailed ducks (Clangula terns at these latitudes, as well as examining environ- hyemalis) and Sabine’s gulls (Xema sabini) nesting among mental factors that may have influenced annual variation. the terns (Mallory et al. 2012; Maftei et al. 2015). Each day Polynyas are hotspots for biodiversity and productivity in in 2010 and 2011, one or two observers counted all adult Arctic marine waters (e.g., Stirling 1997; Hannah et al. Arctic terns within view on the ground (i.e., not the entire 2009; Black et al. 2012; Maftei et al. 2015) and, thus, we colony, but those visible from that vantage point) from the predicted that reproductive metrics would be high and rela- main blind in the morning and evening (weather-permit- tively consistent across years at our site, compared to areas ting), and we used the maximum number observed as our considered more environmentally unpredictable (e.g., sites number of terns on the colony that day. along shorelines affected by fisheries changes, temperature or current changes). However, both high levels of preda- Measuring reproductive effort and success tion pressure and inclement weather are associated with reduced reproductive success by terns (e.g., Power 1964; Upon our arrival at the field camp, we began watching for Becker and Specht 1991; Levermann and Tottrup 2007), so terns settled on the ground, indicating nesting locations, we expected that years with bad weather or higher preda- which we checked immediately. If a nest was discovered, tor counts would have lower tern reproductive effort and we recorded geographic coordinates with a GPS, erected a success. nest marker (numbered wooden stick) 1 m from the nest,

1 3 Polar Biol

Fig. 1 Location of the study site at Nasaruvaalik Island in Penny Strait, Nunavut (75° 49′N, 96° 18′W), in the Cana- dian High Arctic

and revisited the nest daily until a second egg was laid (or otherwise the methods from 2007 to 2011 were unchanged. five successive days had passed; Hatch2002 ) to establish We defined nests as successful if >1 egg hatched. egg-laying dates and sequence. When eggs were found, Any time after the first week of incubation, we trapped they were marked “A” or “B”, weighed (±0.2 g) using adult terns on their nest using a bownet (Salyer 1962). We a 50-g Pesola spring scale, and length and breadth were then weighed terns with a 300-g Pesola spring scale, took a measured (±0.01 mm) using digital calipers. Starting 20 variety of morphometric measures of body size (see Dev- days after the first egg was laid, we made daily visits to lin et al. 2004), and then attached a stainless steel, uniquely each nest to determine date of hatching of each egg where numbered band to the tarsus and released the birds. We possible. Note that in 2007 we found nests with 1 or 2 eggs conducted several preliminary analyses to correct body and followed the nest fate without knowing egg laying mass for structural size (e.g., Peig and Green 2009), but order. In 2009, we established a study plot containing ~100 most structural measures had low correlation or explained nests, encompassing most habitat types found within the minimal variation in body mass. Therefore, we used first- colony including the periphery and the centre to ensure capture body mass itself as a proxy of body condition of the no bias with regard to nest location in the colony (Coul- terns (Monaghan et al. 1992). son 1968; Anotolos et al. 2006). This plot was the only sec- Each day, we walked to the colony and elsewhere on the tion of the colony searched for new nests in 2009–2011, but small island to work on marine birds (e.g., Mallory et al.

1 3 Polar Biol

2012), and at the end of each day, field teams pooled information on how many potential predators were observed on the island, irrespective of their behavior (polar bear, Ursus maritimus; arctic fox, Vulpes lagopus; common raven, Cor- vus corax; glaucous gull, Larus hyperboreus; long-tailed jaeger, Stercorarius longicaudus; parasitic jaeger, Sterc- orarius parasitica; pomarine jaeger, Stercorarius pomari- nus; peregrine falcon, Falco peregrinus; gyrfalcon, Falco rusticolus), adjusting counts for likely duplication of individuals based on times of observations. We used total avian predators observed daily as our index of predation levels on the colony, divided into pre-breeding (before mean nest initiation date) and incubation periods. The mammalian predators occurred infrequently, so we did not include them in our predator index but we comment on specific instances of mammalian predation on the terns. We recorded maximum daily temperatures and total pre- Fig. 2 Timing of adult Arctic tern attendance at the colony during cipitation using a Davis Vantage Pro2® weather station, set the breeding season in 2010 and 2011 (160 = 9 June). Counts are for all individuals on the ground visible from a blind, but do not repre- to record hourly measurements. sent the entire colony

Statistical analysis prior to the terns departing. For the period 29 Jun – 29 Data were tested for approximation of normal distribu- Jul, which covered nest initiation and hatching each year, tions using Kolmogorov–Smirnov tests, and subsequent we counted a daily average of 235 ± 47 (n = 30 d) terns in comparisons of annual means were conducted using t tests, 2010 which was similar to that in 2011 (223 ± 48, n = 25 d; Mann–Whitney tests, analysis of variance (ANOVA) and t53 = 1.0, p = 0.3). However, daily maximum counts ranged Tukey–Kramer post hoc tests (when data approximated by >100% (141–339 terns). During 2010 and 2011, we normality) or Kruskal–Wallis nonparametric ANOVA had 35 days where we conducted counts in the morning with Dunn’s multiple comparison tests (when data did not (0830–1030) and evening (1600–1900), and mean counts in approximate normality, even after transformation). Propor- the morning (232 ± 45) were significantly higher than in the tions of nesting success were compared using Fisher exact evening (180 ± 47; paired t34 = 5.7, p < 0.001). tests, and Spearman rank correlations were used to test for trends where appropriate. A generalized linear model Weather conditions (GLM; binomial logit link) was used to test whether nesting success was predicted from nest initiation date, con- Across the five seasons, the maximum daily tem- trolling for the effect of year. All analyses were performed peratures prior to nest initiation differed significantly using R (R Development Core Team 2011), InStat (Graph- (Table 1; ANOVA; F4,50 = 12.6, p < 0.001), with tem- Pad Software Inc. 2009) or Statistica (Statsoft Inc. 2015). peratures warmer in 2010 than in 2007, 2009 and 2011 Means are reported ± SD unless otherwise noted. (Tukey–Kramer multiple comparison tests, all p < 0.01), and 2008 warmer than 2009 (p < 0.05; see Fig. 3). How- ever, during the incubation period, temperatures were simi- Results lar in all five years (F4,115 = 1.3, p = 0.28). The colony is situated beside a recurrent polynya and thus open water Colony attendance was available upon arrival from northward migration in each year. Daily maximum counts of Arctic terns in 2010 and 2011 exhibited considerable variation through the breeding Predators season (Fig. 2). Terns arrived at the colony in early June, but numbers observed on the colony increased rapidly The number of avian predators observed daily varied across in late June, then fluctuated throughout July, and slowly years, both before nest initiation (Table 1; ANOVA on declined through August. Other than 2010, when terns log-transformed data, F4,50=29.7, p < 0.001), and during abandoned the colony near the end of the incubation incubation (F4,104=132.5, p < 0.001). Prior to incubation, period, the research teams always departed (latest 2 Sep) more predators were seen daily in 2010 than in any other

1 3 Polar Biol

Table 1 Comparison of Year Mean (SD) daily avian predator Days with polar bears Mean (SD) maximum tempera- annual predator counts and count ture (°C) temperatures on Nasaruvaalik Island, Nunavut before nest Before nest During incubation Before nest During Before nest During incubation initiation (n = 11 d) and during initiation initiation incubation initiation typical incubation period across years (n = 24 d) 2007 3.6 (0.9) 3.9 (0.9) 4 1 4.3 (2.4) 5.4 (3.2) 2008 6.5 (1.5) 4.4 (1.4) 2 0 6.0 (2.8) 4.7 (2.8) 2009 3.4 (0.6) 6.4 (1.3) 2 5 2.9 (1.9) 4.2 (2.4) 2010 7.1 (1.8) 18.4 (4.9) 3 3 8.5 (3.4) 5.6 (3.6) 2011 6.8 (1.5) 5.2 (0.6) 2 1 3.9 (1.5) 5.9 (2.6)

(p < 0.001). In 2010, we observed nine adult tern carcasses, apparently killed by a peregrine falcon which we observed on three days over the island (one fresh kill on a day we saw the falcon). We did not see freshly killed adult terns in any other year. Annually, polar bears visited the island 3 ± 1 d before nest initiation (i.e., three different days) which was similar to observations during incubation (2 ± 2 d; Mann–Whit- ney test, U’=16.5, p = 0.42). Numbers of visits were more variable across years during incubation, and 2009 and 2010 experienced more incubation days with polar bears than 2007, 2008 and 2011 (Table 1). The only time we saw an arctic fox on the island was prior to tern nest initiation in 2009, but it left the island before the incubation period.

Fig. 3 Daily maximum temperatures (°C) over 5 years of monitoring Mean nest initiation and incubation period at Nasaruvaalik Island (170 = 19 June). Vertical lines represent the mean start and end of incubation across all years Tern nest initiation was relatively fixed across years, with an overall mean of 6 Jul (Table 2), although there was still year except 2011 (Tukey–Kramer tests, all p < 0.001), and significant variation among years (KW test; H4,834 = 109.8, 2007 and 2009 had similar daily numbers of predators, p < 0.001). Nests were initiated earlier in 2011 than in all which were lower than other years (all p < 0.001). Dur- other years (Dunn’s Multiple Comparisons test, p < 0.001). ing incubation, more predators were spotted daily in 2010 Overall, there was no obvious relationship between pre- than in any other year (all p < 0.01), while fewer predators nesting mean maximum temperature and median nest ini- were observed in 2007 than in any other year except 2008 tiation date (rs5=0.56, p = 0.35). There was nearly a one (all p < 0.001), and fewer were seen in 2008 than in 2009 month spread in nest initiations: the earliest nest initiation

Table 2 Reproductive parameters of Arctic terns in 2007–2011 at Nasaruvaalik Island, Nunavut Year Mean (SD), range, n of Arctic tern reproductive parameters Nest initiation date Adult mass (g) Clutch size Incubation period (d) Nesting success (%), n

2007 6 Jul (1.7), 27 Jun-9 Jul, 250* 111 (6), 111, 55 1.8 (0.4), 2, 211 2008 6 Jul (4.0), 28 Jun–21 Jul, 324 111 (7), 111, 26 1.8 (0.4), 2, 314 21.3 (0.1), 21, 90 95, 104 2009 6 Jul (5.5), 30 Jun–21 Jul, 93 104 (7), 103, 50 1.5 (0.5), 1, 167 21.2 (0.2), 21.5, 31 78, 45 2010 5 Jul (1.6), 3–17 Jul, 85 103 (7), 102, 172 1.5 (0.5), 2, 113 22.4 (0.2), 22, 36 28, 113 2011 2 Jul (4.6), 23 Jun–15 Jul, 82 110 (7), 110, 105 1.8 (0.4), 2, 108 93, 108 Overall means 6 Jul (3.9), 23 Jun–21 Jul, 834 107 (8), 107, 401 1.7 (0.4), 2, 885 21.3 (0.1), 21, 157 72, 370

*Nests were not checked systematically as in later years, so mean nest initiation date could have been earlier

1 3 Polar Biol was 23 Jun and the latest was 21 Jul. Terns spent about statistically larger than that of second laid eggs (34.5 ± 3.0, 21 d incubating, although this differed among years paired t test, t373 = 1.7, p = 0.097). (H2,157=22.1, p < 0.001), with incubation approximately 1 d longer in 2010 (p < 0.05). Adult mass For those nests where we measured the incubation period, we controlled for mean annual nest initiation and Adult Arctic tern body mass differed among years (Table 2; then compared initiation dates among birds that incu- ANOVA; F4,410 = 30.1, p < 0.001). Body mass of terns bated for <21, 21–22, and >22 days. Terns that initiated captured during incubation was similar in 2009 and 2010 nests later in the season had a shorter incubation period (p > 0.05), and mass in those years was lower (all p < 0.001) than those that initiated their nests earlier (H3,157=10.2, than in 2007, 2008 or 2011 (which did not differ signifi- p = 0.017; <21 vs. >22 days, p < 0.05). cantly from each other; p > 0.05).

Clutch size Discussion From 2007 to 2011, terns nesting at Nasaruvaalik Island had a mean clutch size of 1.7 ± 0.4 eggs (Table 2), but this By conducting the first multi-year study of Arctic tern breeding biology in the Canadian Arctic, we established differed among years (H4,885 =115.8, p < 0.001). Clutch sizes were similar in 2007, 2008 and 2011, but smaller baseline information on breeding parameters of this spe- in 2009 and 2010 (p < 0.001). In 2008, where we had the cies in the core of the tern breeding range in Canada, which largest seasonal effort tracking clutch size and correspond- allows for broad comparisons to similar baseline studies at ing nest initiation, the mean nest initiation date for 1-egg other sites (e.g., Pettingill 1939; Hawksley 1957; Bengt- clutches (188 ± 4) did not differ from that of 2-egg clutches son 1971; Lemmetyinen 1972, 1973a, b; Chapdelaine et al. (189 ± 4; U’=7119, n = 314, p = 0.20). Only one 3-egg 1985; Egevang 2010; Vigfusdottir 2012; Table 3). We clutch (0.1%) was found in five field seasons. found that Arctic terns initiated nests in the first week of July, incubated nests for a little more than 21 days and averaged 107 g body mass during this time, and approximately Nesting success three quarters of their nests hatched. However, across years we found marked differences in adult body condi- Nesting success was not monitored in 2007, but in the tion, clutch size, nest initiation dates, incubation periods, four other years it averaged 72% and differed significantly 2 hatching success and predator numbers, all valuable data p among years ( 3 =157.8, < 0.001). Nesting success was on helping assess the range of the “normal” ebb and flow p similar in 2008 and 2011 (Fisher Exact test, = 0.56), but of tern reproduction at these latitudes (Grémillet and Char- p differed among all other year combinations (all ≤ 0.014). mantier 2010). Collectively, our data suggest that variation Using a subset of nests and controlling for year, nests initi- in predation pressure, food supplies, or the possible interac- ated earlier in the season were no more likely to be success- tion of these factors have a strong influence on Arctic tern p ful than those initiated later (GLM; = 0.11). reproduction at high latitudes. We predicted that reproductive metrics of terns would Eggs be high at our site because it is situated beside a polynya (an area of recurrent open water when other areas remain For all eggs measured, mean egg length was 40.6 ± 1.7 ice-covered; Hannah et al. 2009), and these sites are known (n = 1354), which was similar across years (F4,1350=1.6, to be highly productive and support greater biodiversity p = 0.16). However, mean egg breadth was 29.4 ± 1.0 than surrounding areas (reviewed in Stirling 1997). The (n = 1354) which differed across years (H4,1354=33.7, tern colony is the largest we know of in the Queens Chan- p < 0.001). Eggs were broadest in 2009, similar to 2007 and nel region and perhaps the Canadian High Arctic, support- 2011 (all p > 0.05), while eggs in 2008 and 2010 were slim- ing ~900 birds (Maftei et al. 2015). Contrary to our pre- mer (p < 0.001). When we restricted the analysis to only dictions, terns at Nasaruvaalik Island had a similar mean first-laid eggs in 2008–2011 (to eliminate possible influ- clutch size (1.7 eggs) compared to other colonies located in ence of pseudoreplication from individual birds), the pat- the Arctic (Table 3), laid eggs of similar size (Hatch 2002; tern held: egg length was similar in all years (H3,550=0.7, Egevang and Stenhouse 2007), and nest initiation dates and p = 0.87) but eggs were broader in 2009 than 2008 and the production of chicks (measured as nesting success) also 2010 (H3,550=13.9, p = 0.003), although egg breadth appeared to be similar to those recorded by Levermann was similar in 2009 and 2011 (p > 0.05). For 374, 2-egg and Tøttrup (2007) in northeast Greenland (another site nests, egg volumes of first laid eggs (34.8 ± 3.5) were not in the High Arctic with similar environmental conditions).

1 3 Polar Biol

Table 3 Mean clutch sizes of Arctic terns from various locations in the circumpolar Arctic Site Latitude (ºN) Longitude (ºW) Year Mean clutch n References size (SD)

Frederickshaab Glacier, Greenland 62.5 50.2 1943 1.7 (0.5) 279 Elkund (1944) Alexander Archipelago, Alaska 56.7 133 1945 2.0 (0) 45 Williams (1947) Bylot Island, Nunavut 73 79.5 1954 1.6 (0.1) 18 Drury (1960) Devon Island, Nunavut 75.6 84.5 1967 1.6 (0.1) 22 Hussell and Holroyd (1974) Svalbard, Norway 78.2 15.2 1967 1.7 (0.5) 152 Bengtson (1971) Cornwallis Island, Nunavut 74.7 95 1969 1.5 (0.6) 4 Geale (1971) Svalbard, Norway 78.2 15.2 1970 1.8 (0.4) 46 Lemmetyinen (1972) Cooper Island, Alaska 71.3 156 1975 1.9 (0.1) 51 Boekelheide (1980) 1977 1.5 (0.1) 61 Belcher Islands, Nunavut 56.2 79.5 1997 1.6 (0.5) 270 Gilchrist and Robertson (1999) Nasaruvaalik Island, Nunavut 75.8 96.3 2002 1.8 (0.1) 25 ML Mallory, unpubl. data 2003 1.9 (0.1) 25 2004 1.9 (0.1) 20 2005 1.9 (0.1) 25 2006 1.9 (0.1) 15 Kitssissunnguit, Greenland 68.8 52 2002 1.8 (0.5) 292 Egevang and Frederiksen (2011) 2003 1.7 (0.4) 413 2004 1.8 (0.6) 446 2005 1.9 (0.4) 234 2006 2.0 (0.5) 367 Sand Island, Greenland 74.7 20.3 2007 1.4 (0.5) 109 Egevang (2010) 2008 1.6 (0.5) 60 Snaefellsnes, Iceland 64.9 23.3 2008 2.0 (0.4) 66 Vigfusdottir et al. (2013) 2009 1.7 (0.5) 272 2010 1.8 (0.4) 201 2011 1.4 (0.6) 96 Breinykskjeran, Norway 67.5 12 2013 1.6 (0.1) 99 Barrett et al. 2014

Our study and that from other locations suggest that Arc- Leopold Island (74ºN, 90ºW), another High Arctic nesting tic tern clutch size is variable across years, presumably in site 270 km to the southeast (Gaston et al. 2005). Lever- response to environmental conditions, but generally colony mann and Tøttrup (2007) suggested that annual decisions to averages are <2 eggs and, consequently, Arctic terns breed- breed by gulls and terns in northeast Greenland were made ing at Nasaruvaalik Island were not exceptional compared between 1 and 15 July. Thus, across marine bird species, to reproduction at other Arctic sites, despite being situated the last week of June and first week of July seems to be a beside the polynya. key period for nesting among High Arctic marine birds, at Arctic marine birds have a narrow window of time in least in areas where sea ice remains into July. which to pair bond and copulate, lay eggs, rear young and Arctic terns on Nasaruvaalik Island attempted to breed depart for southern waters, the timing of which is largely in each year of this study, as they have every year since at driven by temperatures and sea ice patterns (e.g., Gaston least 2002 when visits to the island began (Mallory and et al. 2005; Mallory and Forbes 2007). Terns arrived at Gilchrist 2003), and paleolimnological evidence suggests Nasaruvaalik Island in mid-June and probably departed in that Arctic terns have nested on Nasaruvaalik Island for at mid to late September each year. Depending on the year, least 100 years (Michelutti et al. 2010). However, 2009 and daily maximum temperatures were generally above 0 °C 2010 proved to be poor breeding years for the terns, with (excluding wind chill) for the entire time we observed terns the lowest clutch sizes and hatching success of all recorded at the colony. Although the range of nest initiation dates years (Fig. 4). Like most seabirds, Arctic terns experience was similar, the mean timing of nest initiation by terns was good and bad years of reproduction. These fluctuations are typically ~1 week later than that of sympatrically nesting potentially influenced by many environmental factors, but Sabine’s gulls (Mallory et al. 2012), and a few days later the most frequently invoked are weather conditions (Power than nest initiations by black-legged kittiwakes (Rissa tri- 1964; Becker and Specht 1991; Robinson et al. 2002), food dactyla) and thick-billed murres (Uria lomvia) at Prince availability (e.g., Lemmetyinen 1972, 1973b; Monaghan

1 3 Polar Biol

obtained in the wintering grounds to maintain their body condition (Agius 2008), and must replenish these reserves on arrival at the breeding colony. The lower body weights of terns in 2009 and 2010 likely resulted from low food resources at the breeding colony on arrival (Monaghan et al. 1989; Wendeln 1997). In support of this hypothesis, we observed differences in courtship feeding across years: in 2007 and 2008, ~5 cm polychaete worms were brought to the colony frequently but, in 2009 and 2010, courtship prey was smaller (<2 cm) and, therefore, constituted lesser volumes of food delivered. We believe that several environmental conditions may have acted synergistically and deleteriously to influence Fig. 4 Comparison of breeding metrics of Arctic terns or environmental conditions during incubation across years at Nasaruvaalik tern reproduction in the poor years, but particularly in Island: filled squares mean clutch size (eggs); filled circles mean 2010. In that year, when we observed complete colony adult mass during incubation (g); open triangles mean nesting suc- failure (Fig. 4), adults abandoned the colony after sev- open bars cess (%); mean total number of avian predators daily dur- eral days of high wind, snow and sleet during the chick- ing incubation; filled bars days with polar bears during incubation hatching period in the first week of August. This island- wide abandonment was unrelated to human disturbance; et al. 1989, 1992; Avery et al. 1992; Suddaby and Ratcliffe although our main (south) colony was visited daily and 1997; Votier et al. 2008; Vigfusdottir 2012), and the pres- studied intensively, the north colony was visited only ence of predators (Lemmetyinen 1973a; Levermann and weekly or on alternate weeks in 2009 and 2010, and yet Tottrup 2007; Wojczulanis-Jakubas et al. 2008). Below we all terns abandoned there as well. During the same stormy consider how each of these factors may have contributed to period, at least one peregrine falcon visited the colony, the reduced reproductive success of the terns in 2009 and as was evident by the carcasses of a few adult terns that 2010. stayed on their nests. Moreover, throughout pre-breed- In 2009, temperatures prior to and early in breeding ing and incubation, 2010 saw the most predators at the were the coldest we recorded in this study and, while terns colony of any year. An increased presence of predators bred, reproductive effort was reduced (smaller clutch sizes), during the pre-breeding portion of the season may cause as parental investment should be lower in years when the seabirds to delay the onset of laying, or forgo breeding expectation of reproductive success may be lower, espe- entirely (Boekelheide 1980; Levermann and Tottrup cially for long-lived birds (Montgomerie and Weatherhead 2007). Finally, in addition to poor weather and high pred- 1988). Lower temperatures could be linked to late break- ator presence¸ adult body mass was lowest in 2009 and up of sea ice, and consequent delayed or reduced marine 2010, suggesting poor food supplies in the surrounding food availability (e.g., Gaston et al. 2005). In contrast, 2010 polynya (Suddaby and Ratcliffe 1997; although sufficient was a warm year but with more precipitation, and stormy to have terns attempt to breed). Collectively, it is unclear weather with heavy rains (or wet snow) early in chick- whether one factor dominates decisions by terns regard- rearing can cause widespread failure in tern colonies due ing reproductive effort and success, or whether there are to exposure and starvation (Power 1964; Becker and Spe- interactions between numerous factors. cht 1991; Robinson et al. 2002). However, at Nasaruvaalik, Not only were clutch size, hatching success and adult a major storm took place in 2010 before most chicks had mass all low in 2010, but the mean incubation period hatched, and those that had hatched were already dying, was longer that year as well. This was likely a result of most likely from starvation. Moreover, Levermann and high numbers of predators during incubation which kept Tottrup (2007) found that even when the terns abandoned flushing terns from their nests; the incubation period can breeding in Greenland, they still found food for courtship be extended when predators are present (Boekelheide pairing and had high feeding success, and we also found 1980). Our qualitative observations of colony-wide flush- that terns in poor breeding years were returning to the col- ing (‘panic flights’; Hatch 2002) noted that terns were far ony with food. more likely to flush from their nests even when a preda- Food availability could not be sampled directly in tor was not in sight in 2010. However, frequent flushing this study, but inferences can be made. Body weight of occurred most often immediately after a falcon came adult terns during incubation was approximately 8% through the colony; this species is a potential predator of lower in 2009 and 2010 compared to other years. During nesting adults rather than just nest contents. their long migrations, Arctic terns use energy reserves

1 3 Polar Biol

High Arctic colony clutch sizes References

The comparisons of clutch size with other High Arctic ACIA (2005) Arctic climate impact assessment scientific report. tern colonies (Table 3) suggest that, despite the inclu- Cambridge University Press, Cambridge Agius SM (2008) Can patterns of energetic condition explain dif- sion of two poor breeding years, Nasaruvaalik Island ferences in the productivity of arctic and common terns at Petit is an average, sometimes good site for breeding Arctic Manan Island, Maine? Dissertation, University of Maine terns. One reason for the quality of the site lies with the Anotolos M, Roby D, Lyons DE, Anderson SK, Collis K (2006) proximity of nearby polynyas close to the island, and sev- Effects of nest density, location, and timing on breeding success of caspian terns. Waterbirds 29:465–472 eral more within 30–35 km (Hannah et al. 2009), within Arctic Council (2009) Arctic marine shipping assessment 2009 report. the known foraging distances of some breeding terns http://www.arctic.noaa.gov/detect/documents/AMSA_2009_ (Black 2006). Two smaller polynyas immediately north Report_2nd_print.pdf. Accessed Feb 2016. and south of Nasaruvaalik Island were also open in mid- Avery MI, Suddaby D, Ellis PM, Sim IMW (1992) Exceptionally low body-weights of arctic terns Sterna paradisaea on Shetland. Ibis June in all years of this study. As a consequence, predict- 134:87–88 able open water by the polynyas means that nest initia- Barrett RT, Lorentsen S-H, Anker-Nilssen T (2006) The status tion dates of terns at Nasaruvaalik Island may not vary of breeding seabirds in mainland Norway. Atlantic Seabirds as much as in other Arctic-nesting seabirds, which may 8:97–126 Becker PH, Specht R (1991) Body mass fluctuations and mortality in experience substantial delays or forgo breeding altogether common tern, Sterna hirundo, chicks dependent on weather and in late ice years (Boekelheide 1980; Gaston et al. 2005; tide in the Wadden Sea. Ardea 79:45–55 Mallory and Forbes 2007). Bengtson SA (1971) Breeding success of the arctic tern Sterna paradisaea Seabird breeding phenology has already been docu- (Pontoppidan) in the Kongsfjord area, Spitsbergen in 1967. Norw. J Zool 19:77–82 mented as shifting in relation to climate change in the last Black AL (2006) Foraging area characteristics of arctic terns (Sterna 30 years (e.g., Møller et al. 2006; Gaston et al. 2009b; paradisaea) and common terns (Sterna hirundo) breeding on Wanless et al. 2009), although long-distance migrants Machias Seal Island. Dissertation, University of New Brunswick appear less likely to adjust arrival dates for breeding Black A, Gilchrist HG, Allard KA, Mallory ML (2012) Incidental observations of birds in the vicinity of the Hell Gate Polynya, than short-distance migrants (Gunnarsson and Tómas- Nunavut: species, timing and diversity. Arctic 65:145–154 son 2011). Thus, data from this study that will serve Boekelheide RJ (1980) Arctic terns: breeding ecology and sea-ice as a baseline for future monitoring of Arctic terns may relationships on an arctic barrier island. Disseration, University already differ from a baseline that would have been of California Cairns DK (1987) Seabirds as indicators of marine food supplies. established based on observations collected more than Biol Oceanogr 5:261–272 30 years ago; this is often termed a ‘shifting baseline’ CBIRD (2014) Final minutes of circumpolar seabird expert group (e.g., Pinnegar and Engelhard 2008). Nonetheless, in the meeting (CBIRD). Spitzbergen Funken, Longyearbyen. 3 April absence of earlier baseline data, it is important to estab- 2014 Chapdelaine G, Brousseau P, Anderson R, Marsan R (1985) Breeding lish current, ‘typical’ parameters of reproductive ecology ecology of common and arctic terns in the Mingan Archipelago, as soon as possible, however shifted they may be (Mal- Quebec. Colon Waterbirds 8:166–177 lory et al. 2010), to enable documenting and modelling Coulson JC (1968) Differences in quality of birds nesting in centre future changes. Data from this study will allow future and on edges of a colony. Nature 217:478–479 Devlin CM, Diamond AW, Saunders GW (2004) Sexing arctic terns use of this species as a bioindicator of the marine health in the field and laboratory. Waterbirds 27:314–320 of the region as climate change continues and as human Diamond AW, Devlin CM (2003) Seabirds as indicators of changes activities become increasingly pervasive throughout the in marine ecosystems: ecological monitoring on Machias Seal Canadian High Arctic Archipelago. Island. Environ Monit Assess 88:153–175 Drury WH (1960) Breeding activities of long-tailed jaeger, herring gull and arctic tern on Bylot Island, Northwest Territories, Can- Acknowledgements We are indebted to the many field assistants ada. Bird-Banding 31:63–79 who helped with this project. K. Kuletz provided unpublished data Durant JM, Hjermann D, Frederiksen M, Charrassin JB, Le Maho on trends in Arctic Terns from Alaska, USA, and H. G. Gilchrist Y, Sabarros PS, Crawford RJM, Stenseth NC (2009) Pros and provided data from Southampton Island, NU. Financial and logistic cons of using seabirds as ecological indicators. Climate Res support were provided by Environment Canada (Canadian Wild- 39:115–129 life Service), Aboriginal Affairs and Northern Development Canada Egevang C (2010) Migration and breeding biology of arctic terns in (Northern Contaminants Program), Natural Resources Canada (Polar Greenland. Dissertation, Aarhus University Continental Shelf Program), University of New Brunswick, and Egevang C, Frederiksen M (2011) Fluctuating breeding of arctic Acadia University. All work was conducted under valid research per- terns (Sterna paradisaea) in Arctic and High-Arctic colonies in mits (EC-PNR-11-020, NUN-SCI-09-01, WL 2010-042). Finally, we Greenland. Waterbirds 34:107–111 thank the anonymous referees who provided insightful reviews of this Egevang C, Stenhouse IJ (2007) Field report from Sand Island, North- manuscript. east Greenland-2007. Greenland Institute of Natural Resources. http://www.natur.gl/fileadmin/user_upload/Publikationer/feltrap- porter/Fieldwork_Sand_Island_2007_1.pdf. Accessed Feb 2016.

1 3 Polar Biol

Egevang C, Stenhouse IJ, Phillips RA, Petersen A, Fox JW, Silk JRD Mallory ML, Gilchrist HG (2003) Marine birds breeding in Penny (2010) Tracking of arctic terns Sterna paradisaea reveals longest Strait and Queens Channel, Nunavut, Canada. Polar Res animal migration. P Natl Acad Sci-Biol 107:2078–2081 22:399–403 Elkund CR (1944) Nesting notes on the arctic tern. Auk 61:648 Mallory ML, Gaston AJ, Forbes MR, Gilchrist HG, Cheney B, Fijn RC, Hiemstra D, Phillips RA, van der Winden J (2013) Arctic Lewis S, Thompson PM (2008) Flexible incubation rhythm in terns Sterna paradisaea from the Netherlands migrate record northern fulmars: a comparison between oceanographic zones. distances across three oceans to Wilkes Land, East Antarctic. Mar Biol 154:1031–1040 Ardea 101:3–12 Mallory ML, Robinson SA, Hebert CE, Forbes MR (2010) Sea- Gaston AJ, Gilchrist HG, Mallory ML (2005) Variation in ice condi- birds as indicators of aquatic ecosystem conditions: a case for tions has strong effects on the breeding of marine birds at Prince gathering multiple proxies of seabird health. Mar Pollut Bull Leopold Island, Nunavut. Ecography 28:331–344 60:7–12 Gaston AJ, Bertram DF, Boyne AW, Chardine JW, Davoren G, Dia- Mallory ML, Boadway KA, Davis SE, Maftei MT (2012) Breeding mond AW, Hedd A, Montevecchi WA, Hipfner JM, Lemon biology of Sabine’s gull (Xema sabini) in the Canadian High MJ, Mallory ML, Rail JF, Robertson GJ (2009a) Changes in Arctic. Polar Biol 35:335–344 Canadian seabird populations and ecology since 1970 in rela- Michelutti N, Blais JM, Mallory ML, Brash J, Thienpont J, Kimpe tion to changes in oceanography and food webs. Environ Rev LE, Douglas MSV, Smol JP (2010) Trophic position influences 17:267–286 the efficacy of seabirds as metal biovectors. P Natl Acad Sci- Gaston AJ, Gilchrist HG, Mallory ML, Smith PA (2009b) Changes in Biol 107:10543–10548 seasonal events, peak food availability, and consequent breeding Møller AP, Flensted-Jensen E, Mardal W (2006) Rapidly advancing adjustment in a marine bird: a case of progressive mismatching. laying date in a seabird and the changing advantage of early Condor 111:111–119 reproduction. J Anim Ecol 75:657–665 Gaston AJ, Mallory ML, Gilchrist HG (2012) Populations and trends Monaghan P, Uttley JD, Burns MD, Thaine C, Blackwood J (1989) of Canadian Arctic seabirds. Polar Biol 35:1221–1232 The relationship between food supply, reproductive effort and Geale J (1971) Birds of Resolute, Cornwallis Island, NWT. Can Field breeding success in arctic terns, Sterna paradisaea. J Anim Nat 85:53–59 Ecol 58:261–274 Gilchrist HG, Robertson GJ (1999) Population trends of gulls and Monaghan P, Uttley J, Burns MD (1992) Effect of changes in food arctic terns nesting in the Belcher Islands, Nunavut. Arctic availability on reproductive effort in arctic terns Sterna paradi- 52:325–331 saea. Ardea 80:71–81 GraphPad Software Inc (2009) Instat. GraphPad Software Inc, La Montevecchi WA (1993) Birds as indicators of change in marine Jolla prey stocks. In: Furness RS, Greenwood JD (eds) Birds as Grémillet D, Charmantier A (2010) Shifts in phenotypic plasticity monitors of environmental change. Chapman and Hall, Lon- constrain the value of seabirds as ecological indicators of marine don, pp 217–265 ecosystems. Ecol Appl 20:1498–1503 Montgomerie RD, Weatherhead PJ (1988) Risks and rewards of nest Gunnarsson TG, Tómasson G (2011) Flexibility in spring arrival of defence by parent birds. Q Rev Biol 63:167–187 migratory birds at northern latitudes under rapid temperature Peig J, Green AJ (2009) New perspectives for estimating body condi- changes. Bird Study 58:1–12 tion from mass/length data: the scaled mass index as an alterna- Hannah CG, Dupont F, Dunphy M (2009) Polynyas and tidal currents tive method. Oikos 118:1883–1891 in the Canadian Arctic archipelago. Arctic 62:83–95 Pettingill O (1939) History of one hundred nests of arctic tern. Auk Hatch JJ (2002) Arctic tern (Sterna paradisaea). In: Poole A (ed) 56:420–428 The birds of North America online. Cornell Lab of Ornithology, Pinnegar JK, Engelhard GH (2008) The ‘shifting baseline’ phenom- Ithaca. http://bna.birds.cornell.edu/bna/species/707. Accessed enon: a global perspective. Rev Fish Biol Fisher 18:1–16 Feb 2016. Power G (1964) Breeding success of the common tern on the North Hawksley O (1957) Ecology of a breeding population of arctic terns. Shore of the Gulf of St. Lawrence in 1961 and 1962. Arctic Bird-Banding 28:57–92 17:51–53 Hussell DJT, Holroyd GL (1974) Birds of the Truelove Lowland and R Development Core Team (2011) R: A language and environment adjacent areas of northeastern Devon Island, NWT. Can Field for statistical computing. R Foundation for Statistical Comput- Nat 88:197–212 ing, Vienna. URL http://www.R-project.org Lemmetyinen R (1972) Growth and mortality in the chicks of arctic Robinson JA, Hamer KC, Chivers LS (2002) Developmental plas- terns in the Kongsfjord area, Spitsbergen in 1970. Ornis Fenn ticity in Arctic terns Sterna paradisaea and Common Terns S. 49:45–51 hirundo in response to a period of extremely bad weather. Ibis Lemmetyinen R (1973a) Clutch size and timing of breeding in the 144:344–346 arctic tern in the Finnish archipelago. Ornis Fenn 50:18–26 Salomonsen F (1965) The geographical variation of the fulmar (Ful- Lemmetyinen R (1973b) Breeding success in Sterna paradisaea and mar glacialis) and the zones of marine environment in the North Sterna hirundo in Southern Finland. Ann Zool Fenn 10:526–535 Atlantic. Auk 82:327–355 Levermann N, Tottrup AP (2007) Predator effect and behavioural Salyer JW (1962) A bow-net trap for ducks. J Wildl Manag patterns in arctic terns (Sterna paradisaea) and Sabine’s 26:219–221 gulls (Xema sabini) during a failed breeding year. Waterbirds StatSoft, Inc. (2015) Statistica 12. http://www.statsoft.com/Products/ 30:417–420 STATISTICA-Features/version-12. Tulsa, Oklahoma, USA Maftei M, Davis SD, Mallory ML (2015) Assessing regional popula- Stirling I (1997) The importance of polynyas, ice edges, and leads to tions of ground-nesting marine birds in the Canadian High Arc- marine mammals and birds. J Mar Syst 10:9–21 tic. Polar Res 34:25505 Suddaby D, Ratcliffe N (1997) The effects of fluctuating food avail- Mallory ML, Braune BM (2012) Tracking contaminants in seabirds ability on breeding arctic terns (Sterna paradisaea). Auk of Arctic Canada: temporal and spatial insights. Mar Pollut Bull 114:524–530 64:1475–1484 Vigfusdottir F (2012) Drivers of productivity in a subarctic seabird: Mallory ML, Forbes MR (2007) Does sea ice constrain the breeding Arctic Terns in Iceland. PhD thesis. University of East Anglia, schedules of High Arctic northern fulmars? Condor 109:894–906 Norwich, UK

1 3 Polar Biol

Vigfusdottir F, Gunnarsson TG, Gill JA (2013) Annual and between- Węsławski JM, Stempniewicz L, Galaktionov K (1994) Summer diet colony variation in productivity of Arctic Terns in West Iceland. of seabirds from the Franz-Josef-Land archipelago, Russian Arc- Bird Study 60:289–297 tic. Polar Res 13:173–181 Votier SC, Heubeck M, Furness RW (2008) Using inter-colony varia- Węsławski JM, Kwaśniewski S, Stempniewicz L, Błachowiak- tion in demographic parameters to assess the impact of skua pre- Samołyk K (2006) Biodiversity and energy transfer to top dation on seabird populations. Ibis 150:45–53 trophic levels in two contrasting Arctic fjords. Polish. Polar Res Wanless S, Frederiksen M, Walton J, Harris MP (2009) Long-term 27:259–278 changes in breeding phenology at two seabird colonies in the Williams RB (1947) Notes on the arctic tern in Alexander Archipel- western North Sea. Ibis 151:274–285 ago, southeastern Alaska. Auk 64:143–144 Wendeln H (1997) Body mass of female common terns (Sterna Wojczulanis-Jakubas K, Jakubas D, Stempniewicz L (2008) Avifauna hirundo) during courtship: relationships to male quality, egg of Hornsund area, SW Spitsbergen: present state and recent mass, diet, laying date and age. Colon Waterbirds 20:235–243 changes. Polish. Polar Res 29:187–197

1 3