Reduced Breeding Success Suggests Trophic Mismatch Despite Timely Arrival in an Alpine Songbird

A steady advance in the onset of spring is one of the most prominent footprints of climate warming and requires organisms, including migratory birds, to adapt their annual routines. As lower trophic levels typically adapt faster than higher trophic levels, observations of reduced fitness due to trophic mismatches are becoming more frequent, especially in long-distance migratory birds. We aimed to identify key phenological events, and quantify potential mismatches and their consequences in a migratory songbird population of the Northern wheatear (Oenanthe oenanthe) breeding at high elevations in the European Alps.We used light-level geolocators to track wheatears, and collected information on individual breeding activity and breeding success as well as environmental conditions during the reproductive season. In addition, we used citizen science data and remote sensed images to quantify longer term phenological trends.Snow melt and green-up showed an exceptionally early spring in the study region in 2020, preceded by a relatively average year in 2019. Yet, tracked individuals arrived well before the snowmelt in 2020 and clutch initiation dates across the population were earlier in 2020 compared to 2019. However, this shift lagged behind the advance in environmental conditions. While hatching success was similar in both years, fledging success and overall nest success was significantly reduced in 2020.Our results show that, despite the timely arrival at the breeding grounds, wheatears did not advance breeding activities in synchrony with environmental conditions during the exceptionally early year in 2020. The reduced fledging success suggests a trophic mismatch. However, the underlying mechanisms for hatchling mortality and nest failure remain unknown. Earlier reproductive seasons are expected to become more frequent in the future. We show that the negative effects of changing seasons in Alpine migratory birds might be similar to birds breeding at high latitudes, despite their shorter migratory distance.

The influence of climate variability on demographic rates of avian Afro-palearctic migrants

Climate is an important driver of changes in animal population size, but its effect on the underlying demographic rates remains insufficiently understood. This is particularly true for avian long-distance migrants which are exposed to different climatic factors at different phases of their annual cycle. To fill this knowledge gap, we used data collected by a national-wide bird ringing scheme for eight migratory species wintering in sub-Saharan Africa and investigated the impact of climate variability on their breeding productivity and adult survival. While temperature at the breeding grounds could relate to the breeding productivity either positively (higher food availability in warmer springs) or negatively (food scarcity in warmer springs due to trophic mismatch), water availability at the non-breeding should limit the adult survival and the breeding productivity. Consistent with the prediction of the trophic mismatch hypothesis, we found that warmer springs at the breeding grounds were linked with lower breeding productivity, explaining 29% of temporal variance across all species. Higher water availability at the sub-Saharan non-breeding grounds was related to higher adult survival (18% temporal variance explained) but did not carry-over to breeding productivity. Our results show that climate variability at both breeding and non-breeding grounds shapes different demographic rates of long-distance migrants.

Strengthening the evidence base for temperature-mediated phenological asynchrony and its impacts

Climate warming has caused the seasonal timing of many components of ecological food chains to advance (Thackeray et al. 2010, 2016). Differential shifts lead to phenological asynchrony, often referred to as trophic mismatch when it is detrimental for consumers (Cushing 1990). In the context of trophic interactions, it has been suggested that consumers will shift their phenology to adapt to shifts in the availability of their food source (Visser and Both 2005), but they rarely do so in practice (Thackeray et al. 2016; Kharouba et al. 2018). Whether such unequal shifts are detrimental or not is unresolved (Johansson and Jonzén 2012; Reed et al. 2013a; Samplonius et al. 2016; Radchuk et al. 2019; Visser and Gienapp 2019). At present there has been no consistent analysis of the links between temperature change, phenological asynchrony, and individual-to-population level impacts across taxa, trophic levels and biomes at a global scale. Instead, many of our insights into mismatch and its impacts stem from a handful of independent single-system studies, varying greatly in their conceptual basis and methodological approach. Here, we propose five criteria that all need to be met to demonstrate that temperature-mediated trophic mismatch poses a growing risk to consumers. These criteria are: 1) an ephemeral resource contributes a large proportion of the consumer’s diet; 2) asynchrony between phenology of consumer and resource is increasing over time; 3) interannual variation in asynchrony is driven by interannual variation in temperature; 4) asynchrony reduces consumer fitness, 5) mismatch impacts negatively on consumer population size or growth. We conduct a literature review of 109 papers studying 132 taxa, and find that for most taxa only two of the five criteria are met. Moreover, all five criteria are only assessed for two taxa. The most commonly-tested criteria are 1 and 2, and few studies further examined evidence for criteria 4 or 5. Furthermore, effects of mismatch are heavily skewed towards juvenile stages rather than adults. Crucially, nearly every study was conducted in Europe or North America, and most studies were on terrestrial secondary consumers. We thus lack a robust evidence base from which to draw general conclusions about the risk that climate-mediated trophic mismatch may pose to populations worldwide.

Understanding temperature effects on recruitment in the context of trophic mismatch

Understanding how temperature affects the relative phenology of predators and prey is necessary to predict climate change impacts and recruitment variation. This study examines the role of temperature in the phenology of a key forage fish, the lesser sandeel (Ammodytes marinus, Raitt) and its copepod prey. Using time-series of temperature, fish larval and copepod abundance from a Scottish coastal monitoring site, the study quantifies how thermal relationships affect the match between hatching in sandeel and egg production of its copepod prey. While sandeel hatch time was found to be related to the rate of seasonal temperature decline during the autumn and winter through effects on gonad and egg development, variation in copepod timing mostly responded to February temperature. These two temperature relationships defined the degree of trophic mismatch which in turn explained variation in local sandeel recruitment. Projected warming scenarios indicated an increasing probability of phenological decoupling and concomitant decline in sandeel recruitment. This study sheds light on the mechanisms by which future warming could increase the trophic mismatch between predator and prey, and demonstrates the need to identify the temperature-sensitive stages in predator-prey phenology for predicting future responses to climate change.

Building a DNA barcode library of Alaska’s non-marine arthropods

Climate change may result in ecological futures with novel species assemblages, trophic mismatch, and mass extinction. Alaska has a limited taxonomic workforce to address these changes. We are building a DNA barcode library to facilitate a metabarcoding approach to monitoring non-marine arthropods. Working with the Canadian Centre for DNA Barcoding, we obtained DNA barcodes from recently collected and authoritatively identified specimens in the University of Alaska Museum (UAM) Insect Collection and the Kenai National Wildlife Refuge collection. We submitted tissues from 4776 specimens, of which 81% yielded DNA barcodes representing 1662 species and 1788 Barcode Index Numbers (BINs), of primarily terrestrial, large-bodied arthropods. This represents 84% of the species available for DNA barcoding in the UAM Insect Collection. There are now 4020 Alaskan arthropod species represented by DNA barcodes, after including all records in Barcode of Life Data Systems (BOLD) of species that occur in Alaska — i.e., 48.5% of the 8277 Alaskan, non-marine-arthropod, named species have associated DNA barcodes. An assessment of the identification power of the library in its current state yielded fewer species-level identifications than expected, but the results were not discouraging. We believe we are the first to deliberately begin development of a DNA barcode library of the entire arthropod fauna for a North American state or province. Although far from complete, this library will become increasingly valuable as more species are added and costs to obtain DNA sequences fall.