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The Condor 111(1):111–119 ¡The Cooper Ornithological Society 2009

CHANGES IN SEASONAL EVENTS, PEAK FOOD AVAILABILITY, AND CONSEQUENT BREEDING ADJUSTMENT IN A MARINE BIRD: A CASE OF PROGRESSIVE MISMATCHING A NTHONY J. GASTON1,3, H. GRANT GILCHRIST1, M ARK L. M ALLORY 2 , 1

AND

PAUL A. SMITH1

Environment Canada, National Wildlife Research Centre, Carleton University, Ottawa, ON K1A 0H3, Canada 2 Canadian Wildlife Service, Box 1714, Qimugjuk Bldg 969, Iqaluit, NU X0A 0H0, Canada

Abstract. The breeding schedules of birds may not change at a rate sufficient to keep up with the current pace of climate change, causing reduced reproductive success. This disruption of synchrony is called the “mismatch hypothesis.” We analyzed data on the breeding of Thick-billed Murres (Uria lomvia) at a colony in northern Hudson Bay, Canada, to examine the relative importance of matched and mismatched timing in determining the growth rates of nestlings. From 1988 to 2007 the date of break-up and 50% clearance of sea ice in surrounding waters advanced by 17 days, and the date on which the count of murres at the colony peaked, an index of food availability, advanced by the same amount. However, the median date of egg-laying advanced by only 5 days so that the number of days between the date of hatching and the date of peak attendance and 50% ice cover increased over the study period. Nestlings’ growth was reduced in years when the counts of attending adults peaked early in the season and early relative to the date of hatching. These observations suggest that the timing of breeding is not advancing to keep pace with changes in the timing of events in the arctic marine environment, leading to greater difficulty in provisioning nestlings. We also demonstrate a relationship between the state of the North Atlantic Oscillation and both the date of peak colony attendance and the growth of nestlings. This relationship suggests that large-scale ocean–atmosphere interactions influence the availability of prey for murres, although the mechanism by which this occurs is not yet understood. Our results support the idea that mismatching of avian breeding cycles with peaks in food abundance is an important consequence of global climate change. Key words:

Arctic, breeding, mismatch, NAO, sea ice, Thick-billed Murre, Uria lomvia

Cambio de Eventos Estacionales, de Disponibilidad Máxima de Alimento, y de Ajuste Consiguiente en Reproducción de un Ave Marina: Un Caso de Desajuste Progresivo Resumen. Los cronogramas de reproducción de las aves podrían no cambiar a una tasa suficientemente rápida como para seguir el patrón actual de cambio climático, lo que causaría una reducción en su éxito reproductivo. Esta perturbación de la sincronía se conoce como la “hipótesis del desajuste.” Analizamos datos de la reproducción de Uria lomvia en la parte norte de la bahía de Hudson, Canadá, para examinar la importancia relativa del ajuste y desajuste temporal de la reproducción en determinar las tasas de crecimiento de los pichones. Entre 1988 y 2007, la fecha de ruptura y desaparición del hielo oceánico en las áreas circundantes se adelantó en 17 días, y la fecha en que los conteos de U. lomvia exhibieron un pico (un índice de la disponibilidad de alimento) se adelantó en la misma cantidad de tiempo. Sin embargo, la fecha mediana de postura de huevos se adelantó en sólo cinco días, de modo que el número de días entre la fecha de eclosión y las fechas de asistencia pico y de 50% de cobertura de hielo aumentó durante el período de estudio. El crecimiento de los pichones se redujo en aquellos años en los que los conteos de los adultos que los atendían presentaron picos a inicios de la temporada y temprano en relación con la fecha de eclosión. Estas observaciones sugieren que el momento en que tiene lugar la reproducción no se está adelantando para seguir la tasa de cambio de los eventos que suceden en el ambiente marino ártico, lo que conduce a una mayor dificultad en el aprovisionamiento de las crías. También demostramos que existe una relación entre el estado de la Oscilación del Atlántico Norte con la fecha de asistencia máxima de aves a la colonia, así como con el crecimiento de los pichones. Esto sugiere que las interacciones océano–atmósfera de gran escala influencian la disponibilidad de presas para U. lomvia, aunque el mecanismo a través del cual sucede esto todavía es desconocido. Nuestros resultados apoyan la idea de que el desajuste de los ciclos reproductivos de las aves con los picos en la abundancia de alimento es una consecuencia importante del cambio climático global.

Manuscript received 29 May 2008; accepted 12 November 2008. 3 E-mail: [email protected] The Condor, Vol. 111, Number 1, pages 111–119. ISSN 0010-5422, electronic ISSN 1938-5422. ‘2009 by The Cooper Ornithological Society. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals.com/ reprintInfo.asp. DOI: 10.1525/cond.2009.080077

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ITRODUCTION

METHODS

Climate changes observed world-wide over the past 50 years have had significant consequences for many plant and animal populations (Crick et al. 1997, Frederikson et al. 2004, Ainley et al. 2005, Gordo and Sanz 2005, Barbraud and Weimerskirch 2006, Menzel et al. 2006). Organisms living in seasonal environments must adjust their behaviors so that breeding and other seasonal activities track the ecosystem’s consequent changes. Avian breeding schedules are synchronized with the phenology of their food supplies to meet energetic demands at each stage of breeding (Lack 1954, Perrins 1970, Brooke 1978). Failure to adjust to changes in the timing of seasonal events, such as peaks in the availability of food, may affect reproductive success adversely. This disruption of synchrony is known as the “mismatch hypothesis” (Visser et al. 1998, Bertram et al. 2001, Thomas et al. 2001, Winkler et al. 2002, Stenseth and Mysterud 2002, Both et al. 2005). The breeding biology of the Thick-billed Murre (Uria lomvia), a marine pursuit diver, has been monitored annually at Coats Island (63° N, 82° W), northern Hudson Bay, Canada, from 1988 to 2007. In recent decades the sea ice of Hudson Bay has tended to break up and melt earlier in the year (Gagnon and Gough 2005, Stirling and Parkinson 2006). The timing of ice breakup and the position of the ice–water interface is an extremely important factor in the ecology of seasonally ice-covered waters (Welch et al. 1992). Breakup of sea ice initiates a phytoplankton bloom that generates a flush of herbivorous zooplankton, which provides abundant food for upper trophic levels, setting the clock for the whole marine ecosystem (e.g., Le Fouest et al. 2005, Wang et al. 2005). Moreover, variation in the schedule of these events can create year-to-year variation in primary production that can affect growth and reproduction at higher trophic levels (Arigo and van Dijken 2004, Johnston et al. 2005). Gaston and Hipfner (1998) and Gaston et al. (2005) presented evidence that over recent decades a trend toward earlier break-up of sea ice in surrounding waters has led to a deterioration in conditions for adult Thick-billed Murres provisioning nestlings at Coats Island. In this paper, we examine how adjustments to the schedule of breeding of the Thickbilled Murre population compare with changes in other seasonal events and whether insufficient adjustment contributes to the observed deterioration in conditions for chick-rearing at the colony. Ocean–atmosphere oscillations influence the marine environment on a large scale, and a number of studies have shown these oscillations affect reproduction and survival among marine birds (Durant et al. 2004, Irons et al. 2008). Here, we contrast the effects of ice cover with those captured by the index of the North Atlantic Oscillation (NAO; Hurrell et al. 2003) to better understand the conditions that influence the timing of breeding and success of chick-rearing of the Thick-billed Murre.

In previous analyses (Hipfner and Gaston 2002, Gaston and Hipfner 2006a, Gaston et al. 2005), mean mass of nestlings at 14 days was used as a measure of nestling growth rate and as an integrator of environmental conditions relating to nestling provisioning (chicks begin to depart from the nest at 15 days of age; Gaston and Hipfner 2000). Here we use the number of birds attending the colony as a measure of environmental conditions that is independent of timing of breeding. Changes in numbers during the incubation and nestling periods depend principally on the attendance of pre-breeding birds, aged 2–6 years (Gaston et al. 1994, Gaston 2002). These cohorts spend progressively greater amounts of time at the colony as they get older, initially prospecting for sites and later occupying sites without laying eggs. The number of birds present at any time depends partly on the spare time available after nutritional needs have been satisfied and is therefore sensitive to environmental conditions (Gaston and Nettleship 1982, Cairns 1987, Gill and Hatch 2002). We interpret the date of peak attendance as the time when suitable prey are most readily available to the murres in the waters surrounding the colony. Note that no annual fisheries or oceanographic survey data are available for the waters of northern Hudson Bay. Consequently, we have no independent source of information on the state of the marine environment from year to year except for the physical climate and ice data. TIMING OF BREEDING AND NESTLING GROWTH

The reproduction of Thick-billed Murres was observed annually at Coats Island, northern Hudson Bay, from 1988 to 2007 (for methods, see de Forest and Gaston 1996). Thickbilled Murres lay a single egg on bare rock ledges and incubate it continuously for 30 to 34 days (Gaston and Hipfner 2000). During incubation, and immediately after hatching, it is difficult to see whether or not an egg or chick is present. Consequently, where birds are left undisturbed, prolonged observations are required to establish the date of hatching. Observations of breeding birds were carried out daily from plywood blinds close to breeding areas. Observers used maps of known breeding sites on pre-defined study plots to record the presence or absence of an egg or chick daily, beginning before the start of hatching. Eggs or chicks were not seen every day on every site. Dates of hatching were recorded when an egg was present one day and a chick was seen within the following 72 hr (90% of eggs in all years). If an egg was present on day i and a chick was seen on days i 1 or i 2, date of hatching was recorded as i 1. If a chick was present on day i 3, date of hatching was recorded as i 2. Otherwise, hatching dates were considered unknown. Mean dates of hatching based on these observations are referred to as “the undisturbed sample” (Hu). In a separate part of the colony, we determined date of hatching by disturbing adult birds every 2–3 days during the

MISMATCHING OF BREEDING BY THE THICK-BILLED MURRE

hatching period to check if eggs had hatched. Mean dates of hatching based on this sample are referred to as “the disturbed sample” (Hd). We used a Pesola spring balance, accurate to o 1 g, to weigh chicks hatched in this area at 3-day intervals until they were at least 14 days old. We used mass at 14 days, either measured directly or interpolated linearly from weights taken no more than 4 days apart, as a standard measure of nestlings’ growth rate (Hipfner and Gaston 2002, Gaston and Hipfner 2006a). Observations of timing of breeding for the Hd sample were available for all years of the study, and those for the Hu sample were available for all years except for 2000–2002. We used Hd, rather than Hu, in comparisons of timing of ice break-up and murres’ attendance patterns because Hd covered more years. ATTENDANCE PATTERNS OF ADULT BIRDS

Counts of all birds visible on 10 pre-defined study plots were carried out daily from 17:00 to 18:00 each year while observers were present (see Gaston 2002). In most years, peak counts occurred during the nestling period, from mid-July onward. We used data only for years when observations began on or before 16 July and calculated 7-day running means for the total of all plot counts to smooth out variation caused by weather. We estimated the date of peak attendance as the date with the highest 7-day mean. Because data were missing for some days, not all means were based on seven days of data. Only those based on four or more days of counts were considered in this analysis. Information on 7-day mean attendance from 16 July to 15 August was available for all years except 2000–2002. To illustrate changes in the pattern of attendance over the study period, we plotted the mean of our 7-day means for each year we gathered data at least from early incubation, dividing the sample into the nine earliest (1988–1996) and eight later years (1997–1999, 2003–2007). ICE CONDITIONS AND NORTH ATLANTIC OSCILLATION

During winter, Hudson Bay is almost 100% ice-covered. However, the ice remains mobile over most of the bay, with only small areas around the coasts forming static, land-fast ice. This cover begins to open in April, and marine waters are generally completely ice-free by early August (Prinsenberg 1986). Previous publications relating ice conditions to reproduction of murres at Coats Island used percentage of ice cover at standard dates as a measure of the timing of ice clearance (Gaston and Hipfner 1998, Gaston et al. 2005). However, given the need to determine a specific annual date, we chose the date of 50% ice cover in Hudson Bay each year, provided by the Canadian Ice Service (R. Gagnon, pers. comm.) and based on the interpretation of weekly aerial surveys and radar satellite images. We chose the date of 50% cover as our index of the timing of ice break-up because conditions change rapidly at that point of the year, making it a more sensitive measure than dates closer to the start or end of the clearance

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period. We do not imply that this date has particular significance for the initiation of breeding by murres, which must generally take place earlier. It is, however, closely correlated to similar indices (date of 25% and 75% ice cover). These data were available for 1971 to 2007. For comparison with earlier published results, the relationship between date of 50% cover and percentage of ice cover on 25 June is also presented. Ice cover on 25 June was obtained from http//ice-glaces.ec.gc.ca (accessed 1 October 2008). To examine the effects of the NAO we used the winter NAO index (WNAO; December–March) taken from http://www.cgd.ucar.edu/cas/jhurrell/indices.html (accessed 1 October 2008). Because adult murres provision their chicks mainly with fish three years old and younger (Gaston and Hipfner 2000), we also investigated lag effects of 1, 2, and 3 years in these physical variables. STATISTICAL TREATMENT

We examined trends over time in physical and biological variables with Pearson correlation and compared slopes by using the coefficients and their standard errors in the Difference Test module of Statistica 7.1 (Statsoft 2005). We developed linear models to predict date of hatching, date of peak attendance, and chick mass at 14 days on the basis of the biological and physical variables described above. Because of the large number of variables, we used an information-theoretic approach. Models were ranked with Akaike’s information criterion for small samples (AICc), and $AICc, and Akaike weights (wi) were used to infer support for models in the candidate set (Burham and Anderson 2002). We tested all variables as fixed effects and calculated AICc values using the residual sums of squares. We analyzed each of the three dependent variables (date of peak attendance, mean date of hatching (Hd), and chick mass at 14 days) independently. For each, we first assessed the influence of date of 50% ice cover and the WNAO index. We also tested 50% ice cover and WNAO index lagged by 1–3 years to include the possibility of lagged effects propagating via the food web. We allowed for a curvilinear pattern in the effect of date of 50% ice cover by adding the square of date of 50% ice cover to the models. We also evaluated interrelationships among the date of peak attendance, date of hatching, and chick mass at 14 days but used their temporal sequence to determine which models to consider. Because date of hatching is determined by date of laying, and laying precedes date of peak attendance and the nestling period, we added date of hatching to models predicting the other two variables. Peak attendance precedes the date of 14-day mass, and we added it to models predicting 14day mass. For the model predicting chick growth, we added the difference between the date of hatching and the date of peak attendance as a covariate to reflect the mismatch in these dates. To the best model with a single variable, we added the other eligible variables as defined above. We did not consider models including more than one WNAO or 50% ice cover variable. Finally, we tested year as a continuous variable to account for

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annual trends not captured by our other variables. Because values of several variables were missing for the years 2000–2002, we omitted these years from all models. Because our sample size including date of peak attendance was only 17 years, we did not consider any models with more than two independent variables. This process resulted in a total of 14 models compared for date of hatching, 16 for date of peak attendance, and 34 for chick mass at 14 days (for which models including both date of peak attendance and difference between date of peak attendance and median date of hatching were included). RESULTS

TABLE 1. Correlation of variables in the breeding phenology of the Thick-billed Murre and date of 50% ice cover with year, over the period 1988–2007. Variable Date of 50% ice WNAOa Date of hatch: Hu Date of hatch: Hd Date of peak 7-day mean Peak date: Hd Hd−50% ice cover

Regression coefficient

Correlation (r)

−0.85 −0.16 −0.25 −0.27 −0.85 −0.39 0.64

−0.54 −0.43 −0.56 −0.60 −0.46 −0.31 0.47

n

P

20 0.01 20 0.06 16 0.02 20 0.005 17 0.07 17 0.22 20 0.03

a

TREND IN ICE CONDITIONS

From 1971 to 2007 the first date at which ice cover in Hudson Bay was reduced to 50% varied between 12 June (2006) and 19 July (1983), dates that correspond approximately to the period of first egg-laying to first hatching of murres at Coats Island (pers. obs.). Little trend in the date of 50% ice cover was apparent from 1971 to 1994 (R2  0.01), after which the date advanced rapidly (Fig. 1). During the period of this study (1988–2007) the date of 50% ice cover was negatively correlated with year (Table 1), suggesting an advance of 17 days from 1988 to 2007. During the same period, the date of 50% ice cover was strongly correlated with percentage of ice cover on 25 June (r18  0.90, P  0.001), the index of ice conditions used in previous analyses of the Coats Island colony (Gaston et al. 2005). TREND IN DATE OF HATCHING

Mean dates of hatching based on Hu and Hd were correlated (r15  0.86, P  0.001), and both samples indicated that murre chicks hatched earlier in more recent years (Table 1), advancing

FIGURE 1. Earliest date of 50% ice cover in Hudson Bay from 1971 to 2007 (data courtesy R. Gagnon, Canadian Ice Service). The solid line represents the fitted cubic polynomial ( y  0.0003x3 − 1.5197x 2 3073.6x − 2 r 106, R 2  0.36). For the years of this study, 1988–2007, the linear regression is y  1728.8 − 0.853x; adjusted R 2  0.26, F 1,18  7.60, P  0.01.

Winter North Atlantic Oscillation index.

over the period 1988–2007 by about 5 days (Fig. 2). Our best model combined the effect of an advancing date of hatching each year with the effect of earlier dates of hatching for years with earlier dates of 50% ice cover (Table 2). Two models incorporating the WNAO index, one for the year of study and one for a lag of 3 years, had $AICc values of 1.3 and 1.4 respectively. The combined Akaike weight (wi) for these three models was 0.92 (Table 2). Over the course of the study, our regression models predict 17 days of advancement in the date of 50% ice cover and 5 days of advancement in the date of hatching, meaning that date of hatching was approximately 12 days later relative to the date of 50% ice cover in 2007 than in 1988 (Fig. 3). TREND IN DATE OF PEAK ATTENDANCE

Dates of peak attendance of murres at the colony varied from 11 August in 1991 to 24 June in 2004; the mean for all years was 28 July (o 12 days SD). Generally, numbers of birds increased during the egg-laying and incubation periods, with the peak occurring after the median date of hatching. However, this pattern changed over the study period. In the first half of the study (1988–1996), attendance peaked approximately 10 days after the median date of hatching, and numbers remained at 90% of the peak value until 18 days after the mean date of hatching (Fig. 4). In the later years (1997–2007) the peak occurred earlier in the season and was followed by a sharper fall in relative numbers. The rate of increase before the date of peak attendance (29 July) was greater during the early period (0.24% day−1) than during the later period (0.17% day−1, difference test, P  0.009). Among the models with a single variable, a quadratic effect of the date of 50% ice cover received the best support (Table 2). However, the addition of the current year’s WNAO index to this model reduced the AICc by 4 units. The model relating peak attendance to the date of 50% ice cover2 WNAO had an Akaike weight five times that of the next best model (Table 2). This result suggested that later ice clearance resulted in later peak attendance but that the delay in peak attendance was moderated in years of very late ice cover (Fig. 5), while attendance tended to be later in years with a positive WNAO index.

MISMATCHING OF BREEDING BY THE THICK-BILLED MURRE

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TABLE 2. Model comparisons for covariate effects on date of hatching (Hd), date of peak attendance (peak date), and mean nestling mass at 14 days (chick mass). Covariates in models include the date of 50% ice cover (50% ice), winter North Atlantic Oscillation index (WNAO), these variables lagged by up to 3 years (lag 1–3), year, date of hatching, date of peak attendance, and the difference between the date of hatching and the date of peak attendance (mismatch). K is the number of variance parameters estimated; $AICc is the difference in second-order Akaike’s information criterion (AICc) of a given model relative to the smallest AICc in the model set, wi is Akaike weight, a measure of relative support for the model, and RSS is residual sums of squares. A indicates additive effects. The three predicted variables were analyzed separately. Results are presented for the null model and all models where $AICca 4. Predicted Hd

a

Date of peak attendanceb

Chick massc

Covariate(s)

K

RSS

50% ice year 50% ice WNAO 50% ice WNAO lag 3 50% ice Null 50% ice (50% ice) 2 WNAO 50% ice (50% ice) 2 hatch date 50% ice (50% ice) 2 WNAO lag 3 50% ice (50% ice) 2 year 50% ice (50% ice) 2 WNAO lag 2 Null Mismatch WNAO lag 2 Peak date Mismatch Peak date WNAO lag 2 Mismatch 50% ice lag1 Peak date 50% ice lag1 Peak date WNAO Mismatch 50% ice lag 3 Mismatch 50% ice Peak date 50% ice lag 3 Peak date WNAO lag 1 Mismatch year Peak date 50% ice Peak date WNAO lag 3 Peak date hatch date Peak date 50% ice lag 2 Peak date year Null

3 3 3 2 1 3 3 3 3 3 1 3 2 2 3 3 3 3 3 3 3 3 3 3 3 3 3 3 1

47.2 50.8 51.3 65.3 113.5 351.0 426.6 430.9 434.4 439.7 1092.0 722.2 908.4 922.9 777.1 811.4 825.0 854.2 866.2 870.3 886.3 886.8 902.0 902.4 904.4 904.7 908.3 908.4 1844

$AICc 0.0 1.3 1.4 2.5 9.4 0.0 3.3 3.5 3.6 3.8 13.7 0.0 0.9 1.2 1.2 2.0 2.3 2.9 3.1 3.2 3.5 3.5 3.8 3.8 3.8 3.8 3.9 3.9 10.4

wi 0.40 0.21 0.19 0.11 0.00 0.51 0.10 0.09 0.08 0.07 0.00 0.17 0.11 0.09 0.09 0.06 0.05 0.04 0.04 0.03 0.03 0.03 0.03 0.03 0.02 0.02 0.02 0.02 0.00

a

Lowest AICc  73.4 Lowest AICc  107.6 c Lowest AICc  119.8 b

MODELS EXPLAINING NESTLING MASS AT 14 DAYS

We found no support for models relating nestling mass at 14 days to date of hatching, and a model relating nestling mass to the date of 50% ice cover was only a marginal improvement (1.9 AICc units) over the null model. The model best supported by the data suggested that nestlings were heavier in years when the date of peak attendance was later relative to date of hatching (i.e., a smaller mismatch) and when the WNAO index, lagged by two years, was negative (Table 2, Fig. 6). However, models including the degree of mismatch alone, the date of peak attendance alone, or the date of peak attendance the WNAO index lagged by two years received similar support ($AICc  2, Table 2). Because we interpret peak attendance as an index of the local abundance of prey,

the results suggest that chick growth is better in years when food abundance peaks relatively later in the season or closer to the mean date of hatching. DISCUSSION As documented previously, the clearance of ice in Hudson Bay has become earlier over the past few decades, with most of the change taking place since 1994 (Fig. 1; Stirling and Parkinson 2006). Presumably as a consequence of the earlier ice clearance, the Thick-billed Murres breeding at Coats Island have advanced their date of egg-laying (Fig. 2). However, the advance in the date of laying has not been as great as the advance in the timing of ice clearance. On average ice clearance has advanced 12 days more than timing of breeding. Conversely,

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FIGURE 2. Mean dates of hatching of Thick-billed Murres at undisturbed (Hu) and disturbed (Hd) study plots at Coats Island from 1988 to 2007.

FIGURE 3. Trend in the difference between mean date of hatching (Hd) and earliest date of 50% ice cover in Hudson Bay between 1988 and 2006.

the date of peak 7-day mean attendance at the colony has advanced by the same number of days (17) as the date of 50% ice cover. This correspondence suggests that peak availability of food is closely tied to ice conditions, supporting the contention of Welch et al. (1992) that ice break-up sets the clock for seasonal events in the arctic marine environment. Growth of nestlings may be affected by a wide range of environmental factors, such as weather, ice, visibility, prey abundance, and prey distribution (Elliott et al. 2007). However, we assume that the realized growth of the chicks integrates all of this variation, providing a single index of the quality of conditions in a particular year. Likewise, our results do not address

the issue of whether any restraint on the part of parents occurs. A strong correlation between nestling mass and adult mass while provisioning nestlings (Gaston and Hipfner 2006a) suggests that adults adjust their provisioning efforts progressively: there is no threshold beyond which adults devote all surplus energy to provisioning, at least under conditions existing at Coats Island. Although we have seen a striking change in chicks’ diets through the study, we do not ascribe the mismatch effect to any particular cause; the effect may result from the combined changes of many aspects of the marine environment. The evidence presented here requires some revision of earlier conclusions about the relationship of ice cover to

FIGURE 4. Average seasonal trends in smoothed (7-day mean) counts of adult Thick-billed Murres at study plots on Coats Island for years 1988–1996 (n  8, solid line) and 1997–2007 but excluding 2000–2002 (n  8, broken line). Each point is the mean of annual 7-day running means. Upward arrows show dates of mean laying and hatching for the earlier period, downward arrows for the later period.

FIGURE 5. Changes in the date of annual peak 7-day mean counts of adult Thick-billed Murres at Coats Island in relation to date of 50% ice cover 1988–2007. Fitted curve, date of peak attendance  23.10 2.43x − 0.0334x2.

MISMATCHING OF BREEDING BY THE THICK-BILLED MURRE

FIGURE 6. Mean nestling mass at 14 days in relation to the date of peak 7-day mean count. Dotted lines show 95% confidence interval on least-squares regression.

reproduction of murres at Coats Island. Previous work suggested that the role of ice in restricting access to open water was the most important factor affecting timing of breeding. This was probably true at the high arctic breeding site at Prince Leopold Island over the past two decades (Gaston et al. 2005). As the timing of break-up has advanced in northern Hudson Bay, however, the advance of laying has not kept pace. At the same time changes in the marine food web have appeared. The pagophilic arctic cod (Boreogadus saida), which dominated nestlings’ diet in the early years of the study, has been replaced by the low arctic capelin (Mallotus villosus) (Gaston et al. 2003). This change has altered the relationship between ice conditions and the biology of breeding birds. Evidence from the timing of peak attendance suggests that ice conditions still set the timetable for production in local waters; hence the murres appear to be falling behind the optimal schedule for laying. The current data, unlike earlier results based on data to 2002 (Gaston et al. 2005), show no significant relationship between chick mass at 14 days and either year or ice conditions. This difference may be because, in recent years, birds have adjusted their foraging behavior to changes since the mid-1990s in the composition of their prey. After an abrupt switch from predominantly arctic cod to predominantly capelin in the mid1990s, the composition of nestlings’ diet at Coats Island has remained unchanged since 1998 (Gaston et al. 2003 and unpubl. data). The present study, however, found chick mass to be strongly positively influenced by the date of peak attendance and negatively influenced by the difference between dates of hatching and peak attendance. Chick mass was highest when peak attendance occurred late in the season. The simplest explanation for these effects is that ice break-up and clearance determine the timing of prey availability and in years of earlier

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ice clearance prey availability peaks before the time of chick hatching. With less food available, parents must reduce rates of food delivery to nestlings, resulting in lower rates of growth. The inclusion of WNAO indices in well-supported models for all three dependent variables strongly suggests that this largescale ocean–atmosphere oscillation has detectable effects on the breeding biology of the murres on Coats Island. The effect of WNAO on hatching date and date of peak attendance is additional to the effect of ice break-up and may relate to variation in conditions during winter or migration. This connection deserves further study. At Coats Island, ice cover in waters within the foraging range of the colony was 10% in all years by the median date of hatching (Canadian Ice Service, unpubl. data). Consequently, it is unlikely that effects observed on chick growth were caused directly by differences in access to food caused by changes in ice. Rather, we assume that changes set in train by ice break-up move through the food web to create part of the variation in food availability manifested as variation in chick growth. As generation time in Thick-billed Murres is about 10 years (Gaston and Hipfner 2000), the observed advance in timing of breeding at Coats Island since 1988 is unlikely to be the result of selection and presumably represents phenotypic adjustment. The fact that Thick-billed Murres at Coats Island have not adjusted their breeding to match the entire change in the phenology of other ecosystem events could have resulted from several causes: 1. Females may be unable to lay at the optimal date because of constraints on egg production (e.g., Perrins 1970); 2. Events on the wintering areas or staging grounds may delay the murres’ arrival at the breeding colony; or 3. Time of egg-laying may be determined partly by inherited mechanisms regulated by day length, or other invariant cues. Of these possibilities, the first seems unlikely, as egg size, a likely indicator of constraints on egg production, does not vary with timing of laying at the Coats Island colony (Hipfner et al. 2005). We cannot discount the possibility that timing of breeding is constrained by conditions in the winter range or during migration. However, it is notable that since 1994 ice conditions in the wintering areas off Newfoundland and Labrador have changed even more radically than those in Hudson Bay, with winter ice cover being much less extensive in recent years (Johnston et al. 2005, Canadian Ice Service, unpubl. data). A recent reduction in band recoveries of Thick-billed Murres in Newfoundland and Labrador suggests that the Coats Island population may be wintering farther north, closer to its breeding area (AJG, unpubl. data). To investigate further a possible link between adults’ condition at egg-laying and the timing of ice break-up, we reexamined data for adults’ mass changes 1988–2001 presented

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ANTHONY J. GASTON

ET AL .

by Gaston and Hipfner (2006b, Table 2) with the addition of data from two more years (2003 and 2004, the only additional years for which such data were available). We compared the rate of change in adults’ mass during incubation (regression slope of mass on date for incubating adults) with date of 50% ice cover, date of peak attendance, and difference between Hd and date of 50% cover. No significant relationships were detected with any of these variables (n  11, all P  0.2; AJG, unpubl. data). If conditions preceding the murres’ arrival in northern Hudson Bay were responsible for the correlations we have presented in our results, we would expect them to be expressed in mass change during incubation (Gaston and Hipfner 2006b). The lack of any relationship between adult mass during incubation and the above three variables suggests that conditions during chick-rearing, rather than those earlier in the season, determined the relationships presented here. There has been little change in the demographics of the colony, although the population increased by about 1% annually until 1997 and then became more or less stable (Gaston 2002; AJG, unpubl. data). Likewise, reproductive success has not varied greatly, fluctuating from 0.55 to 0.65 chicks reared per pair over the study period (AJG, unpubl. data). The observed trends in attendance and nestling growth cannot be accounted for by demographic changes. Consequently, the most likely explanation at present is that timing of breeding is constrained by intrinsic factors, such as photoperiod. Our results suggest that Thick-billed Murres at Coats Island have responded to changes in marine conditions by breeding earlier, but these adjustments have been insufficient to match the rate of change in the ecosystem phenology over the past two decades. Year-to-year variation in the growth of nestlings suggests that conditions for chick-rearing are worse in years when the abundance of food peaks late in the season, or when murres are least in synchrony with the rest of the ecosystem. This mismatch has increased with recent changes in the timing of ice clearance. If current trends continue, the consequent reduction in nestlings’ growth may contribute to a reduction in recruitment, as lighter chick mass reduces apparent survival (chance of return to the colony; U. Steiner, unpubl. data). Our observations support the idea that mismatching of avian breeding cycles can be an important consequence of rapid global climate change. ACKNOWLEDGMENTS We are most grateful to all those, too numerous to name individually, who contributed to our study over the years. We particularly thank those who supervised fieldwork when we were absent: Garry Donaldson, Richard Elliot, Kyle Elliott, Graeme Gissing, Mark Hipfner, David Noble, Uli Steiner, and Kerry Woo. We thank Christine Eberl for being our southern agent and Myra Robertson for handling permits. None of this work would have been possible without the logistic support of the Polar Continental Shelf Project of Natural Resources

Canada and the Nunavut Research Institute, as well as the financial support of Environment Canada, the Northern Ecosystem Initiative of Environment Canada, Natural Sciences and Engineering Research Council of Canada, and Northern Studies Trust Program.

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