Hippocampal neurogenesis and volume in migrating and wintering semipalmated sandpipers (Calidris pusilla)

Nara Gyzely De Morais Magalhães,Cristovam Wanderley Picanço Diniz,Cristovam Guerreiro Diniz,Ediely Pereira Henrique,Patrick Douglas Corrêa Pereira,Isis Ananda Matos Moraes,David Francis Sherry,Mauro André Damasceno De Melo,Daniel Guerreiro Diniz

doi:10.1371/journal.pone.0179134

Abstract

Long distance migratory birds find their way by sensing and integrating information from a large number of cues in their environment. These cues are essential to navigate over thousands of kilometers and reach the same breeding, stopover, and wintering sites every year. The semipalmated sandpiper (Calidris pusilla) is a long-distance migrant that breeds in the arctic tundra of Canada and Alaska and winters on the northeast coast of South America. Its fall migration includes a 5,300-kilometer nonstop flight over the Atlantic Ocean. The avian hippocampus has been proposed to play a central role in the integration of multisensory spatial information for navigation. Hippocampal neurogenesis may contribute to hippocampal function and a variety of factors including cognitive activity, exercise, enrichment, diet and stress influence neurogenesis in the hippocampus. We quantified hippocampal neurogenesis and volume in adult migrating and wintering semipalmated sandpipers using stereological counts of doublecortin (DCX) immunolabeled immature neurons. We found that birds captured in the coastal region of Bragança, Brazil during the wintering period had more DCX positive neurons and larger volume in the hippocampus than individuals captured in the Bay of Fundy, Canada during fall migration. We also estimate the number of NeuN immunolabeled cells in migrating and wintering birds and found no significant differences between them. These findings suggest that, at this time window, neurogenesis just replaced neurons that might be lost during the transatlantic flight. Our findings also show that in active fall migrating birds, a lower level of adult hippocampal neurogenesis is associated with a smaller hippocampal formation. High levels of adult hippocampal neurogenesis and a larger hippocampal formation found in wintering birds may be late occurring effects of long distance migratory flight or the result of conditions the birds experienced while wintering.

Highlights

The semipalmated sandpiper is a long-distance migrant that breeds in the arctic and undertakes an annual fall migration to South America
We found a major difference between migrating and wintering birds in the number of DCXimmunolabeled hippocampal cells and in hippocampal volume (Fig 4, Tables E-G in S1 File)
We have shown for the first time in the present report that levels of neurogenesis and volume of the hippocampal formation of a long-distance migrant are lower during fall migration than while wintering

Summary

Introduction

The semipalmated sandpiper is a long-distance migrant that breeds in the arctic and undertakes an annual fall migration to South America. There is evidence for hippocampal involvement in the spatial and navigational components of migration and homing [11, 18,19,20]. Adult neurogenesis in the avian hippocampus is associated with migratory behavior [15, 21] and migratory birds have been shown to have better long term memory [22] and better spatial memory [19, 20] than non-migrants. Enhanced adult hippocampal neurogenesis is a strong candidate as one of the mechanisms underlying spatial ability and navigation in migrants [15] and there is recent evidence for glial cell involvement as well [16]

Methods

Results

Conclusion