4. DISCUSSION
The four species of Arctic-breeding birds in our comparison exhibited
strong variation, both within years across species and within species
across years, in multiple metrics related to the timing of and
investment in reproduction. This variation was also expressed during the
period of chick growth, but the species-specific responses during this
phase of the breeding cycle often contrasted with those expressed during
the pre-lay and nesting phases. Our prediction that spring temperatures
and snow cover would have a greater effect on the timing of nest
initiation and clutch size in geese compared to semipalmated sandpipers
and longspurs was generally supported and may reflect the differing role
that endogenous reserves play among the taxa during reproduction (see
below). Our prediction that arthropod abundance would have relatively
little effect on the growth of altricial longspur chicks was also
supported, but we found no evidence that resource abundance influenced
the growth of semipalmated sandpiper chicks or snow goose goslings.
Furthermore, the effects of subspathacea biomass on the growth of
brant goslings were opposite of our predictions, emphasizing the role of
factors other than resource abundance in juvenile growth.
4.1 Annual adjustments to reproductive phenology and
investment
Of the four species in our comparison, only semipalmated sandpipers
meaningfully adjusted their arrival date in response to environmental
conditions (snow cover), likely a reflection of the species’ dependence
on exogenous reserves derived from arthropod prey that only become
available as snow melts and temperatures warm (Holmes & Pitelka, 1968;
MacLean & Pitelka, 1971). In contrast, snow geese and longspurs
consistently arrived the earliest at our study site each spring. Snow
geese employ their robust bill and specialized foraging techniques to
access nutritious sub-surface roots and shoots (Iacobelli & Jefferies,
1991), while longspurs can subsist on seeds (Custer & Pitelka, 1978)
prior to the emergence of arthropods. Brant are relatively dependent on
food resources that emerge only as temperatures warm and melting snow
exposes appropriate foraging substrates (Lewis et al., 2020), but unlike
semipalmated sandpipers, brant also carry significant endogenous
reserves that can serve as buffers when food resources are inaccessible
(Hupp et al., 2018).
Subsequent phases of the reproductive cycle of the species in our
comparison further reflected the species’ positions on the
endogenous-exogenous continuum. Larger bodied geese are capable of
carrying comparatively larger endogenous reserves to the Arctic that
they can then invest in egg production and incubation (Klaassen et al.,
2006). Conversely, shorebirds and passerines derive virtually all egg
nutrients and reserves for self-maintenance after their arrival to the
breeding area. All species advanced nest initiation with earlier
snowmelt, but the effect was strongest for geese. Likewise, warmer
spring temperatures resulted in earlier nest initiation by geese, but
not for semipalmated sandpipers and longspurs. In years when Arctic
phenology is advanced, geese can use their reserves to begin egg
development in late migration or shortly after their arrival on the
nesting area so as to initiate nests early and better time the hatch of
offspring with peak nutrient availability (Klaassen et al., 2006; Nolet
et al., 2020). Compared to the large-bodied goose species that can rely
on endogenous reserves, the pre-lay periods for semipalmated sandpipers
and longspurs were relatively long, reflecting the fact that individuals
of both species must first forage to acquire the necessary exogenous
resources prior to producing eggs. Relative to snow geese, brant invest
more exogenous nutrients into eggs, and in years when spring is advanced
are more likely to initiate follicle development during migration (Hupp
et al., 2018). The shorter pre-lay durations in brant during years of
earlier snowmelt likely reflected the species’ tendency to initiate
follicle development prior to arrival on the nesting area. Follicle
development in snow geese breeding on the Colville River Delta mainly
occurs after arrival in the Arctic (Hupp et al., 2018), and their
pre-lay interval is less variable relative to environmental conditions.
Although endogenous investment in eggs gives geese an advantage in
advancing egg development and nest initiation when Arctic phenology is
advanced, female geese may use reserves for self-maintenance at the
expense of reproductive investment in years when snow and cold
temperatures persist (Barry, 1962; Raveling, 1978; Reed et al., 2004).
We detected reduced clutch size in response to delayed snowmelt in both
brant and snow geese, and to lower temperatures in brant (Fig. 3).
Because brant invest relatively more endogenous reserves into eggs than
the other species we studied, they are more likely to reduce clutch
sizes in colder springs or when late snowmelt delays nest initiation and
induces females to use reserves for self-maintenance (Barry, 1962). Late
springs likely delayed new plant growth that brant also rely on for egg
nutrients (Hupp et al., 2018). In contrast, phylogenetic constraints
(MacLean, 1972) likely preclude semipalmated sandpipers from varying
clutch sizes (Sandercock et al., 1999), although previous research
indicates that shorebirds can regulate egg size within clutches in
response to seasonal variation (Martin et al., 2018; Sandercock et al.,
1999). Longspurs exhibited the greatest variation in clutch size during
our study (1–7 eggs), but this variation was not related to
environmental conditions. Such variation may instead reflect the
influence of other factors (e.g., female age or breeding experience;
Sæther, 1990; Stearns, 1976) that we did not measure.
In addition to adjusting investment in clutches, Arctic-breeding birds
may forego breeding altogether in response to extreme environmental
conditions (Ganter & Boyd, 2000; Schmidt et al., 2019), a response
believed to reflect a trade-off between current reproductive investment
and future survival (Linden & Møller, 1989; Roff, 2002). The nesting
effort of semipalmated sandpipers was greatest in years with warm
temperatures and early snow melt, but the other three species did not
meaningfully moderate nesting efforts in response to these variables.
This variation again suggests the likely role of exogenous reserves in
modulating the reproductive output of semipalmated sandpipers.
Shorebirds lay clutches that constitute a relatively high proportion of
their body mass (Rahn et al., 1975; Ricklefs, 1984), and semipalmated
sandpiper females at our study site were apparently unable to acquire
sufficient arthropod resources to initiate nests in cold springs with
extensive snow cover. In contrast, brant and snow geese could rely on
endogenous reserves, and longspurs seed resources in lieu of arthropods,
to ensure nesting opportunities.
Notably, the four species in our study share the overarching
life-history trait of being migratory animals. Previous research has
suggested that migratory species are more vulnerable to climate change
due to the potential decoupling of relevant seasonal cues across a
species’ range (Both et al., 2010; Møller et al., 2008; Robinson et al.,
2009). We documented interannual responses among these four migratory
species, however, that demonstrated a high degree of interspecific
response to shared stimuli among diverse taxa. The species at our study
site use two flyways (Pacific [brant and snow geese] and Central
[snow goose, semipalmated sandpiper, and longspur] Americas flyways)
across a mix of marine (brant and semipalmated sandpiper), seasonal
wetland (snow goose and semipalmated sandpiper), and agriculture/prairie
landscapes (snow goose and longspur) to migrate to Arctic breeding
grounds. Despite the use of varied migratory routes and habitats, these
species nonetheless adjusted their timing of breeding in ways that
tracked spring environmental conditions at the breeding site. Indeed,
long-term information for these and other species at this site exhibit a
general advancement of arrival dates in concert with warming spring
conditions (Ward et al., 2016), patterns noted more broadly in other
studies (Jonzén et al., 2006; Thorup et al., 2007; Van Buskirk et al.,
2009). Migratory birds exhibit life histories that are predicated on
exploiting diverse, ephemeral landscapes (Greenberg & Marra, 2005;
Newton, 2008), and employ flexible physiologies that permit the rapid
hypertrophy and subsequent atrophy of respiratory, digestive, and
circulatory functions (Piersma & van Gils, 2011). Such behavioral and
physiological adjustments enable large-scale movements and undoubtedly
also serve as buffers in a changing world. So although migratory species
may theoretically be predisposed to a decoupling of seasonal cues across
their large ranges, these four species responded predictably to
prevailing environmental conditions by adjusting their reproductive
timing and investment. Migratory birds, by virtue of their intrinsic
life histories, may thus accommodate the effects of a warming Arctic
better than previously appreciated.
4.2 Variation in chick
growth
Interannual adjustments in the timing of and investment in breeding may
reflect adaptive responses to prevailing environmental conditions, but
nests must hatch and chicks must grow and survive in order for such
adjustments to be propagated in an evolutionary context (see Charmantier
& Gienapp, 2014). The rate of chick growth provides insights into
fitness-related variables (e.g., survival, recruitment, lifetime
reproductive output) that are otherwise extremely difficult to measure
in most bird species. Curiously, resource abundance was not a meaningful
predictor of chick mass of either insectivore species in our study.
Obviously, food abundance directly affects chick growth, which suggests
that either we did not measure arthropod abundance in a way that
reflected real abundance or that the range of abundances that we
measured at our site did not limit growth. For the former supposition,
this same sampling protocol has been successfully employed by others
(see Kwon et al., 2019 for overview), and Saalfeld et al. (2019)
specifically determined that this sampling technique described
variations in arthropod abundance that predicted the chick mass of two
shorebird species (dunlin Calidris alpina and pectoral sandpiperCalidris melanotos ) that are closely related to semipalmated
sandpipers. Thus, it is more likely that arthropod abundances were not
limiting during our period of study. Despite measuring a nearly 300-fold
variation in arthropod abundance (1.5–427.3 mg
3-day-1 sample) during periods of chick growth from
2015–2017, our measurements did not apparently reflect conditions that
affected the growth of insectivore chicks. For semipalmated sandpipers,
warmer temperatures in the 3-day period prior to recapture were
associated with larger same-age chicks, and there was a positive
relationship between temperature and arthropod abundance at our study
site (Pearson’s r = 0.62, P <0.001). In general,
arthropod abundance was low at lower temperatures and increased at
temperatures >5°C, but, importantly, we also documented
periods of high temperature that coincided with low arthropod abundance
(see Results) during which we nonetheless observed high age-specific
chick masses. Further, we documented mass loss or static growth of
recaptured semipalmated sandpiper chicks during a period of unusual cold
(average 3.4°C from 7–13 July 2015), and encountered dead and emaciated
chicks of red phalaropes (Phalaropus fulicarius ) that presumably
had starved. This suggests a thermogenic trade-off for semipalmated
sandpiper chicks at higher temperatures wherein the high cost of
thermogenesis (Bakken et al., 2002; Schekkerman et al., 2003) may be
minimized and growth maximized (McKinnon et al., 2013), permitting rapid
chick growth even during periods of relatively low food abundance.
Resource abundance was a meaningful predictor of the growth of only
brant, but the negative parameter estimate of this metric (Table 4) was
counterintuitive. Previous research has demonstrated an inverse
relationship between forage biomass and forage quality (i.e., nitrogen
content) in graminoids like subspathacea (Doiron et al., 2014;
Lameris et al., 2017), a relationship which may account for this
finding. There is a strong positive relationship between nitrogen
content and demographic variables like gosling growth and survival
(Doiron et al., 2015; Manseau & Gauthier, 1993; Person et al., 2003;
Sedinger & Raveling, 1986), and in our study it may be that periods of
high subspathacea biomass had correspondingly low values for
nitrogen content. The NDVI-based techniques of Hogrefe et al. (2017) are
not suitable for detecting the small but meaningful differences in the
nitrogen content of subspathacea . Anecdotally, Hogrefe et al.
(2017) determined the biomass and percent nitrogen of 221 samples ofsubspathacea from 2012–2015 at our study site, and although NDVI
values could not accurately predict the nitrogen content of these
samples, there was a strong negative relationship between biomass and
nitrogen content (Pearson’s r = -0.52, P <0.001). Thus,
higher age-specific body mass of brant goslings associated with lower
forage biomass may reflect aspects of forage quality that we were unable
to measure. In contrast, we did not find that higher subspathaceabiomass negatively affected the growth of snow goose goslings. The
larger snow goose goslings may be able to accommodate lower qualitysubspathacea compared to smaller brant goslings due to a greater
intake and processing capacity (e.g., Lesage & Gauthier, 1997; Manseau
& Gauthier, 1993; Richman et al., 2015). Further, larger snow goose
goslings were associated with cooler temperatures, a result contrasting
with semipalmated sandpipers. This may again indirectly reflect aspects
of food quality (Dickey et al., 2008) rather than thermal constraints on
growth per se (but see Fortin et al., 2000), as subspathacearesponds to warm temperatures with increased vegetative growth (i.e.,
resource biomass) and decreased nitrogen content (i.e., resource
quality; Doiron et al., 2014; Lameris et al., 2017). Although we do not
fully understand the mechanisms, our study does demonstrate that warmer
temperatures during brood rearing can differentially affect growth rates
of avian herbivores versus insectivores.
Of note, none of the environmental covariates that we assessed
meaningfully predicted the mass of longspur chicks, the only altricial
species in this comparison. Previous research at a nearby site in Arctic
Alaska documented seasonal declines in the growth of longspur chicks, as
well as negative effects of low arthropod abundance and cold
temperatures (Pérez et al., 2016). At our study site, however, other
factors were apparently more important in modulating the growth of
longspurs. It may be that aspects of parental quality that we did not
measure (e.g., nest-site selection [Martin et al., 2000, Lloyd &
Martin, 2004], chick provisioning [Davies, 1986; Limmer & Becker,
2009]) buffered deleterious effects of temperature and resource
abundance that affected the chicks of precocial species at our site.
An environmental variable that received wide support across our
comparisons was the timing of nest initiation with respect to snow
cover. For brant, snow geese, and semipalmated sandpipers, chicks from
nests that were initiated before or near the annual date of 50% snow
cover were larger than chicks from nests that were initiated relatively
later (Table 4). The positive effect of early initiation on chick growth
has been documented in other studies of Arctic-breeding birds (Cooch et
al., 1991; Ruthrauff & McCaffery, 2005; Sedinger & Flint, 1991), and
indicates that early nest initiation rather than resource abundance is a
more important factor in regulating chick growth at our study site. This
suggests the role of potential factors (e.g., parental quality
[Clutton-Brock, 1984; Forslund & Pärt, 1995], carry-over effects
[Harrison et al., 2011]) that we could not measure. Other
researchers, however, have specifically detected seasonal declines in
the growth of snow goose goslings related to food abundance (Lepage et
al., 1999; Lindholm et al., 1994). These studies were conducted at
breeding sites with degraded grazing lawns and low-quality food compared
to that on the Colville River (Hupp et al., 2017), emphasizing how
spatial variation in ecological factors—in this case, food quality and
abundance—can differentially affect the demographic response of the
same populations (Sedinger et al., 2001).
4.3 Conclusion
Life-history traits that afford flexible responses to variable
environmental conditions are favored in highly seasonal and
unpredictable environments like the Arctic. Traits that in turn promote
evolutionary changes in a population are further expected to be subject
to strong selection pressure under climate-warming scenarios (Berteaux
et al., 2004; Hoffmann & Sgrò, 2011; Williams et al., 2008).
Temperatures across all seasons are projected to increase on Alaska’s
Arctic Coastal Plain due to climate change (IPCC, 2013), and increases
in warming have already led to long-term advances in snow melt and
longer snow-free seasons in Arctic Alaska (Cox et al., 2017; Hinzman et
al., 2005; Stone et al., 2002). Brant and snow geese generally responded
more flexibly to variation in temperature and snowmelt during the
pre-lay and nesting periods than did semipalmated sandpipers and
longspurs. In contrast, we detected potentially deleterious effects of
increased temperature on brant and snow goose goslings, while
semipalmated sandpiper chicks responded favorably to warmer conditions.
Thus, brant and snow geese may possess traits that are beneficial during
one phase of the reproductive cycle (e.g., relative flexibility along
the endogenous-exogenous spectrum) and others which may be detrimental
at another phase (e.g., temperature-mediated sensitivity to food quality
during juvenile growth). For the Arctic-breeding birds in our study,
these contrasting responses underscore the importance of assessing the
effects of climate variability across multiple phases of the
reproductive cycle (Nolet et al., 2020).