Sensitivity to habitat fragmentation across European landscapes in three temperate forest herbs

Tobias Naaf,Jan Plue,Pieter Vangansbeke,Sara A O Cousins,Jonathan Lenoir,Camille Meeussen,Kenny Helsen,Pedro Poli,Martin Diekmann,Siyu Huang,Per‐Ola Hedwall ,Guillaume Decocq,Fabien Spicher,Jaan Liira,Thomas Vanneste,Sanne Govaert,Kris Verheyen,Jannis Till Feigs,Pieter De Frenne,Stephanie I J Holzhauer,Jörg Brunet,Katja Kramp

doi:10.1007/s10980-021-01292-w

Abstract

ContextEvidence for effects of habitat loss and fragmentation on the viability of temperate forest herb populations in agricultural landscapes is so far based on population genetic studies of single species in single landscapes. However, forest herbs differ in their life histories, and landscapes have different environments, structures and histories, making generalizations difficult.ObjectivesWe compare the response of three slow-colonizing forest herbs to habitat loss and fragmentation and set this in relation to differences in life-history traits, in particular their mating system and associated pollinators.MethodsWe analysed the herbs’ landscape-scale population genetic structure based on microsatellite markers from replicate forest fragments across seven European agricultural landscapes.ResultsAll species responded to reductions in population size with a decrease in allelic richness and an increase in genetic differentiation among populations. Genetic differentiation also increased with enhanced spatial isolation. In addition, each species showed unique responses. Heterozygosity in the self-compatible Oxalis acetosella was reduced in smaller populations. The genetic diversity of Anemone nemorosa, whose main pollinators are less mobile, decreased with increasing spatial isolation, but not that of the bumblebee-pollinated Polygonatum multiflorum.ConclusionsOur study indicates that habitat loss and fragmentation compromise the long-term viability of slow-colonizing forest herbs despite their ability to persist for many decades by clonal propagation. The distinct responses of the three species studied within the same landscapes confirm the need of multi-species approaches. The mobility of associated pollinators should be considered an important determinant of forest herbs’ sensitivity to habitat loss and fragmentation.

Highlights

Large parts of the Earth are covered by humanmodified, agricultural landscapes, in which only small remnants ofnatural habitats are left (Kennedy et al 2019)
All species responded to reductions in population size with a decrease in allelic richness and an increase in genetic differentiation among
Our study indicates that habitat loss and fragmentation compromise the long-term viability of slow-colonizing forest herbs despite their ability to persist for many decades by clonal propagation

Summary

Introduction

Large parts of the Earth are covered by humanmodified, agricultural landscapes, in which only small remnants of (semi-)natural habitats are left (Kennedy et al 2019). Habitat loss and fragmentation are, considered among the most important threats to biodiversity (Wilson et al 2016). In the temperate zones of the Northern Hemisphere, agricultural landscapes are dominant (Kennedy et al 2019). Many organisms are not adapted to live in small populations restricted to isolated habitat fragments. Typical temperate forest herbs, for instance, evolved during times when forests were much more common and connected than today (Honnay et al 2005) and exhibit traits associated with long-term stable conditions, such as a high age of first flowering, the production of few and heavy seeds and the absence of long-distance seed dispersal mechanisms. Plue IVL Swedish Environmental Institute, Valhallavagen 81, 10031 Stockholm, Sweden

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