skip to main content


Title: Birds advancing lay dates with warming springs face greater risk of chick mortality

In response to a warming planet with earlier springs, migratory animals are adjusting the timing of essential life stages. Although these adjustments may be essential for keeping pace with resource phenology, they may prove insufficient, as evidenced by population declines in many species. However, even when species can match the tempo of climate change, other consequences may emerge when exposed to novel conditions earlier in the year. Here, using three long-term datasets on bird reproduction, daily insect availability, and weather, we investigated the complex mechanisms affecting reproductive success in an aerial insectivore, the tree swallow (Tachycineta bicolor). By examining breeding records over nearly half a century, we discovered that tree swallows have continuously advanced their egg laying by ∼3 d per decade. However, earlier-hatching offspring are now exposed to inclement weather events twice as often as they were in the 1970s. Our long-term daily insect biomass dataset shows no long-term trends over 25 y but precipitous drops in flying insect numbers on days with low ambient temperatures. Insect availability has a considerable impact on chick survival: Even a single inclement weather event can reduce offspring survival by >50%. Our results highlight the multifaceted threats that climate change poses on migrating species. The decoupling between cold snap occurrence and generally warming spring temperatures can affect reproductive success and threaten long-term persistence of populations. Understanding the exact mechanisms that endanger aerial insectivores is especially timely because this guild is experiencing the steepest and most widespread declines across North America and Europe.

 
more » « less
NSF-PAR ID:
10195179
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
ISSN:
0027-8424
Page Range / eLocation ID:
Article No. 202009864
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. BACKGROUND The availability of nitrogen (N) to plants and microbes has a major influence on the structure and function of ecosystems. Because N is an essential component of plant proteins, low N availability constrains the growth of plants and herbivores. To increase N availability, humans apply large amounts of fertilizer to agricultural systems. Losses from these systems, combined with atmospheric deposition of fossil fuel combustion products, introduce copious quantities of reactive N into ecosystems. The negative consequences of these anthropogenic N inputs—such as ecosystem eutrophication and reductions in terrestrial and aquatic biodiversity—are well documented. Yet although N availability is increasing in many locations, reactive N inputs are not evenly distributed globally. Furthermore, experiments and theory also suggest that global change factors such as elevated atmospheric CO 2 , rising temperatures, and altered precipitation and disturbance regimes can reduce the availability of N to plants and microbes in many terrestrial ecosystems. This can occur through increases in biotic demand for N or reductions in its supply to organisms. Reductions in N availability can be observed via several metrics, including lowered nitrogen concentrations ([N]) and isotope ratios (δ 15 N) in plant tissue, reduced rates of N mineralization, and reduced terrestrial N export to aquatic systems. However, a comprehensive synthesis of N availability metrics, outside of experimental settings and capable of revealing large-scale trends, has not yet been carried out. ADVANCES A growing body of observations confirms that N availability is declining in many nonagricultural ecosystems worldwide. Studies have demonstrated declining wood δ 15 N in forests across the continental US, declining foliar [N] in European forests, declining foliar [N] and δ 15 N in North American grasslands, and declining [N] in pollen from the US and southern Canada. This evidence is consistent with observed global-scale declines in foliar δ 15 N and [N] since 1980. Long-term monitoring of soil-based N availability indicators in unmanipulated systems is rare. However, forest studies in the northeast US have demonstrated decades-long decreases in soil N cycling and N exports to air and water, even in the face of elevated atmospheric N deposition. Collectively, these studies suggest a sustained decline in N availability across a range of terrestrial ecosystems, dating at least as far back as the early 20th century. Elevated atmospheric CO 2 levels are likely a main driver of declines in N availability. Terrestrial plants are now uniformly exposed to ~50% more of this essential resource than they were just 150 years ago, and experimentally exposing plants to elevated CO 2 often reduces foliar [N] as well as plant-available soil N. In addition, globally-rising temperatures may raise soil N supply in some systems but may also increase N losses and lead to lower foliar [N]. Changes in other ecosystem drivers—such as local climate patterns, N deposition rates, and disturbance regimes—individually affect smaller areas but may have important cumulative effects on global N availability. OUTLOOK Given the importance of N to ecosystem functioning, a decline in available N is likely to have far-reaching consequences. Reduced N availability likely constrains the response of plants to elevated CO 2 and the ability of ecosystems to sequester carbon. Because herbivore growth and reproduction scale with protein intake, declining foliar [N] may be contributing to widely reported declines in insect populations and may be negatively affecting the growth of grazing livestock and herbivorous wild mammals. Spatial and temporal patterns in N availability are not yet fully understood, particularly outside of Europe and North America. Developments in remote sensing, accompanied by additional historical reconstructions of N availability from tree rings, herbarium specimens, and sediments, will show how N availability trajectories vary among ecosystems. Such assessment and monitoring efforts need to be complemented by further experimental and theoretical investigations into the causes of declining N availability, its implications for global carbon sequestration, and how its effects propagate through food webs. Responses will need to involve reducing N demand via lowering atmospheric CO 2 concentrations, and/or increasing N supply. Successfully mitigating and adapting to declining N availability will require a broader understanding that this phenomenon is occurring alongside the more widely recognized issue of anthropogenic eutrophication. Intercalibration of isotopic records from leaves, tree rings, and lake sediments suggests that N availability in many terrestrial ecosystems has steadily declined since the beginning of the industrial era. Reductions in N availability may affect many aspects of ecosystem functioning, including carbon sequestration and herbivore nutrition. Shaded areas indicate 80% prediction intervals; marker size is proportional to the number of measurements in each annual mean. Isotope data: (tree ring) K. K. McLauchlan et al. , Sci. Rep. 7 , 7856 (2017); (lake sediment) G. W. Holtgrieve et al. , Science 334 , 1545–1548 (2011); (foliar) J. M. Craine et al. , Nat. Ecol. Evol. 2 , 1735–1744 (2018) 
    more » « less
  2. Abstract

    Aerial insectivorous birds have experienced alarming population declines in eastern North America. Meanwhile, urbanization continues to increase rapidly, with urban land use comprising 69.4 million acres (1 acre = 0.40 ha), or 3.6% of total land area, in the contiguous United States. Multiple environmental changes are associated with urbanization, including alterations to local climate, changes in habitat structure, and potential shifts in both terrestrial and emergent aquatic flying insects on which aerial insectivorous birds rely. Here, we investigated the linkages between urbanization, water quality, and Tree Swallow (Tachycineta bicolor) reproductive success and body condition at seven river‐riparian sites representing urban and protected land use in Columbus, Ohio (USA) over five consecutive years (2014–2018). Tree Swallows at urban and protected sites relied on emergent aquatic insects for 37.4% and 30.8% (SD = 28.4% and 24.1%) of their nutritional subsidies, respectively. Despite the loss of environmental quality generally attributed to cities, Tree Swallows exhibited greater reproductive success in urban settings where climate was more amenable to egg and nestling survival, and the breeding season was longer. Urban‐nesting Tree Swallows initiated laying 7.9 d earlier and fledged 35% more young per nest than those at protected sites. Multiple characteristics of urban sites appeared to drive these patterns, including differences in mean and extreme air temperatures and measures of water quality (e.g., water temperature, nutrient concentrations, turbidity). However, chronic effects of elevated Hg concentrations, which were 482% greater in adult swallow blood at urban sites than at protected sites where swallows exhibited a 17.4% lower trophic position, may disadvantage individuals in other ways. Further, although Tree Swallows are a good model aerial insectivore bird species, characteristics of urban landscapes that benefit Tree Swallows may not advantage other aerial insectivorous birds owing to differences in life‐history and foraging strategies. These findings implicate urbanization, local climate, and water quality as important considerations in the conservation of aerial insectivorous birds.

     
    more » « less
  3. Abstract

    Savannah Sparrows (Passerculus sandwichensis) and Tree Swallows (Tachycineta bicolor) breed and forage in the same habitat on Kent Island, a boreal island in the Bay of Fundy, New Brunswick, but respond differently to the same weather conditions. The 2 passerines are similar in body size but because Tree Swallows depend upon small flying insects captured on the wing, they may be more sensitive to weather than Savannah Sparrows, which forage on insects and seeds on the ground and in shrubs and trees. To compare how reproductive success in the 2 species was affected by weather conditions, we took advantage of an 18-year dataset and used a model-building approach that controlled for year, adult sex and age, and field where they nested. We focused on 3 measures of reproductive success (hatching success, fledging success, and nestling condition) and different time periods (3- to 18-day time windows) before hatching or fledging. The responses of the 2 species differed in magnitude and direction. In Tree Swallows, adding weather variables to the basic model increased the explanatory power of fixed effects by 19.1%, illustrating the swallows’ sensitivity to weather. In contrast, in Savannah Sparrows, the addition of weather variables only increased the model’s explanatory power by 0.4% and the proportion of variation attributed to fixed factors by only 1.5%, which reflected the species’ hardiness in the face of inclement weather. Our results suggest that how a bird species forages and the nature of its prey may influence its sensitivity to weather and indicate that increased rainfall, strong winds and other events associated with climate change may affect Tree Swallows and other aerial insectivores more than ground-foraging birds such as Savannah Sparrows.

     
    more » « less
  4. Abstract

    Warming temperatures and advancing spring are affecting annual snow and ice cycles, as well as plant phenology, across the Arctic and boreal regions. These changes may be linked to observed population declines in wildlife, including barren‐ground caribou (Rangifer tarandus), a key species of Arctic environments. We quantified how barren‐ground caribou, characteristically both gregarious and migratory, synchronize births in time and aggregate births in space and investigated how these tactics are influenced by variable weather conditions. We analyzed movement patterns to infer calving dates for 747 collared female caribou from seven herds across northern North America, totaling 1255 calving events over a 15‐year period. By relating these events to local weather conditions during the 1‐year period preceding calving, we examined how weather influenced calving timing and the ability of caribou to reach their central calving area. We documented continental‐scale synchrony in calving, but synchrony was greatest within an individual herd for a given year. Weather conditions before and during gestation had contrasting effects on the timing and location of calving. Notably, a combination of unfavorable weather conditions during winter and spring, including the pre‐calving migration, resulted in a late arrival on the calving area or a failure to reach the greater calving area in time for calving. Though local weather conditions influenced calving timing differently among herds, warm temperatures and low wind speed, which are associated with soft, deep snow, during the spring and pre‐calving migration, generally affected the ability of female caribou to reach central calving areas in time to give birth. Delayed calving may have potential indirect consequences, including reduced calf survival. Overall, we detected considerable variability across years and across herds, but no significant trend for earlier calving by caribou, even as broad indicators of spring and snow phenology trend earlier. Our results emphasize the importance of monitoring the timing and location of calving, and to examine how weather during summer and winter are affecting calving and subsequent reproductive success.

     
    more » « less
  5. Abstract

    Anthropogenic changes are often studied in isolation but may interact to affect biodiversity. For example, climate change could exacerbate the impacts of biological invasions if climate change differentially affects invasive and native species. Behavioural plasticity may mitigate some of the impacts of climate change, but species vary in their degree of behavioural plasticity. In particular, invasive species may have greater behavioural plasticity than native species since plasticity helps invasive species establish and spread in new environments. This plasticity could make invasives better able to cope with climate change.

    Here our goal was to examine whether reproductive behaviours and behavioural plasticity vary between an introduced and a nativeOnthophagusdung beetle species in response to warming temperatures and how differences in behaviour influence offspring survival.

    Using a repeated measures design, we exposed small colonies of introducedO. taurusand nativeO. hecateto three temperature treatments, including a control, low warming and high warming treatment, and then measured reproductive behaviours, including the number, size and burial depth of brood balls. We reared offspring in their brood balls in developmental temperatures that matched those of the brood ball burial depth to quantify survival.

    We found that the introducedO. taurusproduced more brood balls and larger brood balls, and buried brood balls deeper than the nativeO. hecatein all treatments. However, the two species did not vary in the degree of behavioural plasticity in response to warming. Differences in reproductive behaviours did affect survival such that warming temperatures had a greater effect on survival of offspring of nativeO. hecatecompared to introducedO. taurus.

    Overall, our results suggest that differences in behaviour between native and introduced species are one mechanism through which climate change may exacerbate negative impacts of biological invasions.

     
    more » « less