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No effects of asynchrony between hatching and peak food availability on chick growth in Semipalmated Plovers (Charadrius semipalmatus) near Churchill, Manitoba

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Birds rely on consistent patterns of food availability on their breeding grounds to successfully complete their breeding cycle. Due to ongoing warming of the sub-Arctic, there is potential for a mismatch between the peak in available invertebrate biomass and the peak in food demand for shorebird chicks. During the summers of 2010 and 2011, we investigated the relationship between temperature and benthic and terrestrial invertebrate biomass, measured using three sampling techniques in Churchill, Manitoba. We also investigated the relationship between timing of breeding of Semipalmated Plovers (Charadrius semipalmatus) and timing of peaks in invertebrate biomass. In 2011, chick growth rates were also measured to examine whether hatching in synchrony with the peak in invertebrate biomass during the brood rearing period affected growth rates. In 2010, emergent and core invertebrate biomass were negatively related to soil degree days, whereas in 2011, core biomass increased with soil degree days and pitfall biomass increased with air temperature. Total invertebrate biomass (summed over trap types) peaked from 25 to 31 days before the median chick hatch date in 2010 and 10 days after the median chick hatch date in 2011. In 2011 we did not detect any effects of asynchrony on the growth of Semipalmated Plover chicks. These results may indicate that food resources in their environment remain adequate throughout the breeding season, despite inter-annual fluctuations in the timing of invertebrate peaks.
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Polar Biology (2019) 42:593–601
https://doi.org/10.1007/s00300-019-02456-w
ORIGINAL PAPER
No eects ofasynchrony betweenhatching andpeak food availability
onchick growth inSemipalmated Plovers (Charadrius semipalmatus)
nearChurchill, Manitoba
C.AnneCorkery1· EricaNol1· LauraMckinnon2
Received: 26 March 2018 / Revised: 4 January 2019 / Accepted: 5 January 2019 / Published online: 22 January 2019
© Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Birds rely on consistent patterns of food availability on their breeding grounds to successfully complete their breeding cycle.
Due to ongoing warming of the sub-Arctic, there is potential for a mismatch between the peak in available invertebrate
biomass and the peak in food demand for shorebird chicks. During the summers of 2010 and 2011, we investigated the rela-
tionship between temperature and benthic and terrestrial invertebrate biomass, measured using three sampling techniques in
Churchill, Manitoba. We also investigated the relationship between timing of breeding of Semipalmated Plovers (Charadrius
semipalmatus) and timing of peaks in invertebrate biomass. In 2011, chick growth rates were also measured to examine
whether hatching in synchrony with the peak in invertebrate biomass during the brood rearing period affected growth rates.
In 2010, emergent and core invertebrate biomass were negatively related to soil degree days, whereas in 2011, core biomass
increased with soil degree days and pitfall biomass increased with air temperature. Total invertebrate biomass (summed over
trap types) peaked from 25 to 31days before the median chick hatch date in 2010 and 10days after the median chick hatch
date in 2011. In 2011 we did not detect any effects of asynchrony on the growth of Semipalmated Plover chicks. These results
may indicate that food resources in their environment remain adequate throughout the breeding season, despite inter-annual
fluctuations in the timing of invertebrate peaks.
Keywords Charadrius semipalmatus· Invertebrates· Shorebird· Chick growth· Phenology· Weather
Introduction
Migratory species time their movements in part to take
advantage of seasonal flushes in food resources on their
breeding grounds (Johansson and Jonzen 2012). The phe-
nology of migration in many long-distance migrant birds
is primarily driven by day length, an environmental factor
that is not influenced by weather (Both and Visser 2005).
As climate change affects northern latitudes at a more accel-
erated pace than southern latitudes, differential changes in
climate may outpace the ability of populations to adapt to
climate-induced changes in the timing of resource peaks
on their breeding grounds (Both and Visser 2001; Stenseth
and Mysterud 2002; Senner 2012). A delayed migratory
response to changes in climate on the breeding grounds
could result in a later start to breeding, lower breeding suc-
cess, and a subsequent decline in population size (Both and
Visser 2001; Drever etal. 2012).
Climate change induced gaps between the timing of hatch
and peaks in food availability on the breeding grounds, here-
after “mismatch” (Stenseth and Mysterud 2002), has been
noted as one the of the possible mechanisms driving popu-
lation declines in insectivorous Arctic-nesting shorebird
populations (Tulp and Schekkerman 2008). In the Arctic,
short peaks in invertebrate abundance during mid-summer
(MacLean and Pitelka 1971; McKinnon etal. 2012; Bolduc
etal. 2013) are driven largely by temperature (Hodkinson
etal. 1998; Danks 2004). Short summer and weather-related
resource availability translates into a small window during
which there is adequate food available for reproduction and
the growth and survival of young. As such, birds breeding
* Laura Mckinnon
lmck@glendon.yorku.ca
1 Environmental andLife Sciences Graduate Program,
Trent University, 2140 East Bank Drive, Peterborough,
ONK9J7B8, Canada
2 Department ofMultidisciplinary Studies, York University
Glendon Campus, 2275 Bayview Avenue, Toronto,
ONM4N3M6, Canada
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... However, there is no clear link between degree of mismatch that a population experiences and its fitness reduction (Zhemchuzhnikov et al., 2021), and some studies found no effects on fitness at all (e.g. Reneerkens et al., 2016;Corkery et al., 2019). ...
... Growth and survival of chicks are considered to depend on the biomass of all available arthropod species. Chicks growing up after the overall biomass peak generally experience reduced growth rates (Lameris et al., 2022) and survival chances (Meyer et al., 2021), yet other studies do not find fitness reductions for late-hatching chicks (Corkery et al., 2019;Reneerkens et al., 2016). Before we can conclude that not all populations are equally sensitive to mismatches, it is essential to know which part of the total arthropod biomass is relevant to a certain bird species, as chicks of different shorebird species may not all rely on the same type of prey (Baker, 1977;Gerik, 2018;Holmes and Pitelka, 1968). ...
Article
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With rapid climate change over the past decades, organisms living in seasonal environments are suggested to increasingly face trophic mismatches: the disruption of synchrony between different trophic levels due to a different phenological response to increasing temperatures. Strong effects of mismatches are especially expected in the Arctic region, where climatic changes are most pronounced. Nevertheless, relatively few studies have found strong evidence for trophic mismatches between the breeding period of Arctic-breeding shorebirds and the arthropod prey on which they rely. Here we argue that this is potentially caused by a generalization of trophic interactions. While many studies have measured the mismatch relative to the peak in abundance of all available arthropod species, we use metabarcoding of prey items in faeces to show that chicks of four different shorebird species (red knot, curlew sandpiper, little stint, and red phalarope) strongly differ in their arthropod diet. We found that two arthropod families, Tipulidae and Chironomidae, on average contributed >50% to the diet of chicks. While red knot chicks were relying mainly on Tipulidae (70% in 2018 and 39% in 2019), the chicks of the other three shorebird species were mainly preying on Chironomidae (43% for red phalarope, 37% for curlew sandpiper and 44% for little stint). We found that taking into account the species-specific diet changed our measure of trophic mismatch for two out of four shorebird species. We conclude that ignoring diet data may hamper our understanding of trophic mismatches.
... To measure the degree of a trophic mismatch, and to be able to make comparisons of mismatches among species and populations, it is necessary to view the advancement in timing of reproduction of the consumer relative to a yardstick which describes the phenology of its main food sources (Visser & Both, 2005). This yardstick most often is timing of the food peak, either expressed | 3 ZHEMCHUZHNIKOV Et al. in abundance (Corkery et al., 2019;Regular et al., 2014) or quality (Gauthier et al., 2013;Ross et al., 2017Ross et al., , 2018. Besides the timing of the food peak relative to the timing of the consumer's peak demand, a trophic mismatch can be defined relative to other parameters that describe food availability (Box S1). ...
... The timing of the food peak was suggested as a universal yardstick to describe fitness consequences of trophic mismatches between avian Rate of change in bird phenology (days per year) significant trends non-significant trends consumers and their prey (Visser & Both, 2005), although theoretical studies showed that to study fitness effects, it is important to consider the entire period during which food abundance sufficiently meets and overlaps with the food requirements of the offspring throughout the breeding season (Durant et al., 2005(Durant et al., , 2007. Several empirical studies indeed indicate that asynchrony with a food peak may not lead to fitness consequences when food is sufficiently abundant during the entire season (Corkery et al., 2019;Dunn et al., 2011;Reneerkens et al., 2016;Wesołowski & Rowiński, 2014). Vice versa, a good temporal match between offspring growth period and food peak might still result in negative fitness consequences when food availability during the entire season is low (Vatka et al., 2014). ...
Article
Full-text available
• Many organisms reproduce in seasonal environments, where selection on timing of reproduction is particularly strong as consumers need to synchronize reproduction with the peaked occurrence of their food. When a consumer species changes its phenology at a slower rate than its resources, this may induce a trophic mismatch, that is, offspring growing up after the peak in food availability, potentially leading to reductions in growth and survival. However, there is large variation in the degree of trophic mismatches as well as in its effects on reproductive output. • Here, we explore the potential causes for variation in the strength of trophic mismatches in published studies of birds. Specifically, we ask whether the changes in the degree of mismatch that have occurred over time can be explained by a bird's (a) breeding latitude, (b) migration distance, and/or (c) life‐history traits. • We found that none of these three factors explain changes in the degree of mismatch over time. Nevertheless, food phenology did advance faster at more northerly latitudes, while shifts in bird phenology did not show a trend with latitude. • We argue that the lack of support in our results is attributable to the large variation in the metrics used to describe timing of food availability. We propose a pathway to improve the quantification of trophic mismatches, guided by a more rigorous understanding of links between consumers and their resources.
... Insectivorous migratory birds breeding in the Arctic are expected to be especially prone to warming-induced mismatch (McKinnon et al., 2012;Miller-Rushing et al., 2010;Saalfeld et al., 2019; but see Corkery et al., 2019;McKinnon et al., 2013). Arthropods are resident ectotherms, and their phenology is strongly affected by local environmental conditions (Culler et al., 2015;Høye & Forchhammer, 2008a;Shaftel et al., 2021). ...
Article
Full-text available
Seasonally abundant arthropods are a crucial food source for many migratory birds that breed in the Arctic. In cold environments, the growth and emergence of arthropods are particularly tied to temperature. Thus, the phenology of arthropods is anticipated to undergo a rapid change in response to a warming climate, potentially leading to a trophic mismatch between migratory insectivorous birds and their prey. Using data from 19 sites spanning a wide temperature gradient from the Subarctic to the High Arctic, we investigated the effects of temperature on the phenology and biomass of arthropods available to shorebirds during their short breeding season at high latitudes. We hypothesized that prolonged exposure to warmer summer temperatures would generate earlier peaks in arthropod biomass, as well as higher peak and seasonal biomass. Across the temperature gradient encompassed by our study sites (>10°C in average summer temperatures), we found a 3‐day shift in average peak date for every increment of 80 cumulative thawing degree‐days. Interestingly, we found a linear relationship between temperature and arthropod biomass only below temperature thresholds. Higher temperatures were associated with higher peak and seasonal biomass below 106 and 177 cumulative thawing degree‐days, respectively, between June 5 and July 15. Beyond these thresholds, no relationship was observed between temperature and arthropod biomass. Our results suggest that prolonged exposure to elevated temperatures can positively influence prey availability for some arctic birds. This positive effect could, in part, stem from changes in arthropod assemblages and may reduce the risk of trophic mismatch.
... A greater mechanistic understanding is needed as well as identification of baselines for defining optimal food resource characteristics. For example, asynchronies with food peaks may not have consequences if food is abundant (Corkery et al., 2019;Dunn et al., 2011) or alternatively, synchronization with food peaks could have negative consequences if food abundance is low (Vatka et al., 2014). Time-series analyses relating seasonal krill availability (e.g., Nardelli et al., 2021) to foraging penguins and their reproductive performance will be critical for testing whether phenological mismatches between krill and Adélie penguins impact penguin population dynamics. ...
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Abstract Climate change is leading to phenological shifts across a wide range of species globally. Polar oceans are hotspots of rapid climate change where sea ice dynamics structure ecosystems and organismal life cycles are attuned to ice seasonality. To anticipate climate change impacts on populations and ecosystem services, it is critical to understand ecosystem phenology to determine species activity patterns, optimal environmental windows for processes like reproduction, and the ramifications of ecological mismatches. Since 1991, the Palmer Antarctica Long‐Term Ecological Research (LTER) program has monitored seasonal dynamics near Palmer Station. Here, we review the species that occupy this region as year‐round residents, seasonal breeders, or periodic visitors. We show that sea ice retreat and increasing photoperiod in the spring trigger a sequence of events from mid‐November to mid‐February, including Adélie penguin clutch initiation, snow melt, calm conditions (low winds and warm air/sea temperature), phytoplankton blooms, shallow mixed layer depths, particulate organic carbon flux, peak humpback whale abundances, nutrient drawdown, and bacterial accumulation. Subsequently, from May to June, snow accumulates, zooplankton indicator species appear, and sea ice advances. The standard deviation in the timing of most events ranged from ~20 to 45 days, which was striking compared with Adélie penguin clutch initiation that varied 30 days) than mean dates and the variability in timing was low (
... Elevated biomass of prey items near goose colonies could result in larger or higher quality eggs and even benefit chick growth rates of some species [25,26]. Any changes in invertebrate phenology due to climate change [64], however, may result in a mismatch between timing of chick hatch and prey emergence potentially offsetting any positive effects associated with the goose colony for some [26,30] but not all species [31,65]. Furthermore, invertebrate emergence cycles vary significantly across broad-geographic scales [66], potentially obscuring any larger trends. ...
Article
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Over the last 60 years, Arctic goose populations have increased while many sympatric tundra nesting bird populations have declined. Hyperabundant geese have well-documented effects on tundra habitats, which can alter habitat use by sympatric bird species. These habitat changes may also alter invertebrate communities and abundances, with potentially important, but as of yet, undocumented effects on insectivorous birds such as shorebirds. Here, we determined the effects of goose-induced habitat alteration on invertebrate communities and relate the observed changes to shorebird diet. At sites and habitat types representing a gradient of goose influence, we identified goose-related changes in ground cover and linked these factors to variation in invertebrate communities. We then used DNA metabarcoding to characterize the diet of six shorebird species across sites and identify inter-site variation in abundance, biomass, and timing of emergence of dominant shorebird prey items. Invertebrate diversity and richness did not vary either among sites or habitat types. However, for prey items identified as part of the shorebird diet, we found significantly higher abundances and biomasses at a moderately goose-influenced site than at either low or high goose-influenced sites. Biomass of Tipulidae, the dominant prey taxon for shorebirds at the study sites, was 7.5 times higher at the moderately goose-influenced site compared to the site where goose influence was minor. We attribute this enhancement of prey biomass to both the fertilizing effect of goose fecal pellets and the moderate grazing pressure. Many studies have documented adverse effects of overabundant geese, but here we show that a moderate degree of goose grazing can lead to enhanced biomass of invertebrates, with the potential for improved shorebird foraging success and chick growth. These benefits, however, might be outweighed by negative effects of goose-induced habitat alteration and predation pressure.
... Those that have done so indicate large variation in effect size (Knudsen et al., 2011;. Recently, some studies have revealed mismatches that do not impact fitness (Corkery et al., 2019;Machín et al., 2018;Reneerkens et al., 2016) and in a recent review study, Zhemchuzhnikov et al. (2021) were unable to establish a clear link between the extent of a trophic mismatch and fitness impacts. The absence of a clear relationship between trophic mismatch and population dynamics may be influenced by the large variation in the effect sizes of trophic mismatches. ...
Article
Full-text available
In seasonal environments subject to climate change, organisms typically show phenological changes. As these changes are usually stronger in organisms at lower trophic levels than those at higher trophic levels, mismatches between consumers and their prey may occur during the consumers’ reproduction period. While in some species a trophic mismatch induced reductions in offspring growth, this is not always the case. This variation may be caused by relative strength of the mismatch, or by mitigating factors like increased temperature reducing energetic costs. We investigated the response of chick growth rate to arthropod abundance and temperature for six populations of ecologically similar shorebirds breeding in the Arctic and sub‐Arctic (four subspecies of Red Knot Calidris canutus, Great Knot C. tenuirostris and Surfbird C. virgata). In general, chicks experienced growth benefits (measured as a condition index) when hatching before the seasonal peak in arthropod abundance, and growth reductions when hatching after the peak. The moment in the season at which growth reductions occurred varied between populations, likely depending on whether food was limiting growth before or after the peak. Higher temperatures led to faster growth on average, but could only compensate for increasing trophic mismatch for the population experiencing the coldest conditions. We did not find changes in the timing of peaks in arthropod availability across the study years, possibly because our series of observation was relatively short; timing of hatching displayed no change over the years either. Our results suggest that a trend in trophic mismatches may not yet be evident; however, we show Arctic‐breeding shorebirds to be vulnerable to this phenomenon and vulnerability to depend on seasonal prey dynamics.
... www.nature.com/scientificreports/ in sampling chicks that leave nest sites within hours of hatching 24 , are highly mobile 25 , are difficult to relocate 26 , and often hide or remain motionless in the presence of a predator (or researcher) 27 . Instead, most studies have relied on growth rates of chicks when investigating the impacts of phenological mismatch 6,7,9,21,28,29 . However, the relationship between growth and survival of chicks is not necessarily straightforward; the assumption that slower growth leads to lower survival may not be true if undernourished chicks can simply grow more slowly over a longer period without compromising survival. ...
Article
Full-text available
Climate change in the Arctic is leading to earlier summers, creating a phenological mismatch between the hatching of insectivorous birds and the availability of their invertebrate prey. While phenological mismatch would presumably lower the survival of chicks, climate change is also leading to longer, warmer summers that may increase the annual productivity of birds by allowing adults to lay nests over a longer period of time, replace more nests that fail, and provide physiological relief to chicks (i.e., warmer temperatures that reduce thermoregulatory costs). However, there is little information on how these competing ecological processes will ultimately impact the demography of bird populations. In 2008 and 2009, we investigated the survival of chicks from initial and experimentally-induced replacement nests of arcticola Dunlin (Calidris alpina) breeding near Utqiaġvik, Alaska. We monitored survival of 66 broods from 41 initial and 25 replacement nests. Based on the average hatch date of each group, chick survival (up to age 15 days) from replacement nests (Ŝi = 0.10; 95% CI = 0.02–0.22) was substantially lower than initial nests (Ŝi = 0.67; 95% CI = 0.48–0.81). Daily survival rates were greater for older chicks, chicks from earlier-laid clutches, and during periods of greater invertebrate availability. As temperature was less important to daily survival rates of shorebird chicks than invertebrate availability, our results indicate that any physiological relief experienced by chicks will likely be overshadowed by the need for adequate food. Furthermore, the processes creating a phenological mismatch between hatching of shorebird young and invertebrate emergence ensures that warmer, longer breeding seasons will not translate into abundant food throughout the longer summers. Thus, despite having a greater opportunity to nest later (and potentially replace nests), young from these late-hatching broods will likely not have sufficient food to survive. Collectively, these results indicate that warmer, longer summers in the Arctic are unlikely to increase annual recruitment rates, and thus unable to compensate for low adult survival, which is typically limited by factors away from the Arctic-breeding grounds.
... However, it remains unclear whether this increased temporal asynchrony is harmful to young. McKinnon et al. (2013) and Corkery et al. (2019) both reported chicks growing sufficiently well even under depressed food conditions caused by phenological mismatch, perhaps due to lower thermoregulatory needs during the warmer springs. In contrast, Saalfeld et al. (2019) found that shorebirds experienced increased phenological mismatch with earlier snowmelt, and that, in general, chicks that hatched from nests initiated earlier experienced greater food availability and grew at faster rates than chicks from nests that hatched later. ...
Article
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While increases in overall temperatures are widely reported in the Arctic, large inter-annual variation in spring weather, with extreme early and late conditions, is also occurring. Using data collected from three sites in Arctic Alaska, we explored how shorebird breeding density, nest initiation, nest synchrony, nest survival, and phenological mismatch varied between two exceptionally early (2015 and 2016) and late (2017 and 2018) springs. We assessed these differences in the context of long-term data from each site and whether species exhibited conservative or opportunistic reproductive strategies. Conservative shorebirds typically display nest-site fidelity and territoriality, consistent population densities, relatively even individual spacing, and monogamous mating systems with bi-parental incubation. In contrast, opportunistic shorebirds display the opposite traits, and a polygamous mating system with uniparental incubation. In this study, we evaluated 2,239 nests from 13 shorebird species, 2015–2018, and found that shorebirds of both strategies bred earlier and in higher numbers in early, warm springs relative to historic levels (based on 3,789 nests, 2005–2014); opposite trends were observed in late springs. In early springs, nests were initiated less synchronously than in late springs. Nest survival was unrelated to spring type, but was greater in earlier laid nests overall. Invertebrate food resources emerged earlier in early springs, resulting in a greater temporal asynchrony between invertebrate emergence and chick hatching in early than late springs. However, invertebrate abundance was quite variable among sites and years regardless of spring type. Overall, our results were generally consistent with predicted relationships between spring conditions and reproductive parameters. However, we detected differences among sites that could not be explained by other ecological factors (e.g., predators or alternative prey). Differences in shorebird community composition and other subtler methodological/ecological differences among sites highlight the difficulty of understanding the complex nature of these ecological systems and the importance of evaluating questions at multiple sites across multiple years. Our study demonstrates that shorebirds exhibit a high degree of behavioral flexibility in response to variable Arctic conditions, but whether this flexibility is enough to allow them to optimally track changing environmental conditions or if evolutionary adjustments will be necessary is unknown.
... Some species have responded by advancing laying dates, whereas others have not, suggesting there are migratory constraints to an advancement (McKinnon et al. 2012, Liebezeit et al. 2014, Reneerkens et al. 2016 In Red Knots (Calidris canutus canutus) body size of juveniles is positively related to date of snow melt in the Arctic, suggesting that their body size at fledging is smaller following a mismatch in early springs, resulting in a lower subsequent survival (van Gils et al. 2016). In general, however, evidence for a phenological mismatch for shorebirds is rare, perhaps because arthropod abundance, more than plant growth, is strongly affected by weather conditions following snowmelt (McKinnon et al. 2012, Reneerkens et al. 2016, Leung et al. 2018, Corkery et al. 2019, Saalfeld et al. 2019). While only a few studies investigated the connection between proportion of juveniles and climatic conditions in the breeding grounds and none of these included onset of spring, most of these studies found a higher proportion of juveniles following warm breeding seasons (Schekkerman et al. 1998, Beale et al. 2006, Aharon-Rotman et al. 2015. ...
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... These changes could significantly influence populations of Arctic-breeding birds, the most diverse and vertebrate taxa of the circumpolar Arctic [2]. Northward shifts in vegetation communities have already influenced the availability of nesting habitat for sub-arctic breeding shorebirds [3], and advances in peak prey availability have created a mismatch with the phenology of chick hatch [4], and lower growth and chick survival in some [5,6] but not all cases [4,7,8]. While at large scales these changes have the potential to alter bird distribution, phenology, and demography, at smaller spatial scales the trophic interactions among predators and their prey may play a more dominant role in structuring communities [9,10]. ...
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