Conservation implications of long-distance migration routes: Regional metapopulation structure, asymmetrical dispersal, and population declines

Understanding and conserving metapopulations of long-distance migrants is challenging since breeding population structure may not be delimited simply by geography, but also by migration or wintering distributions. We present the first study of the relative importance of breeding, migration and wintering distributions for regional metapopulation processes in breeding areas. Using a species for which life-history and demography are extensively studied (common terns Sterna hirundo), we explored population genetics across eastern North America to distinguish between these potential drivers of metapopulation structure, understand recent population declines in inland areas, and direct appropriate conservation efforts. We analyzed nuclear and mitochondrial DNA to determine changes in population structure and dispersal over prehistoric, historical and contemporary time at regional, sub-regional and local spatial scales. We found evidence for conservation-relevant, hierarchical metapopulation structure within breeding areas: at (i) local and sub-regional scales resulting from restricted dispersal distances, and (ii) between inland and coastal regions as a result of non-breeding distributions. Crucially, at regional scales (ii), asymmetrical dispersal rates from inland to coastal colonies have increased ten-fold since the 1960s, contributing to recent, largely-enigmatic inland population declines. Migrating inland common terns pass over coastal colonies but the reverse is not true. Thus, asymmetrical dispersal from inland to coastal areas provides the first demonstration that migration routes, not wintering distributions, are drivers of breeding population structure in the absence of physical barriers. Our results illustrate the conservation importance of this determination for long-distance migrants: definitive evidence connecting metapopulation demographics to regional population declines for common terns, previously only speculated at despite > 100 years of banding effort.