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

Abstract

Context Evidence 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. Objectives We 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. Methods We analysed the herbs’ landscape-scale population genetic structure based on microsatellite markers from replicate forest fragments across seven European agricultural landscapes. Results All 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. Conclusions 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. 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.

Context matters: the landscape matrix determines the population genetic structure of temperate forest herbs across Europe

“…Oxalis acetosella has been found to produce most of its seeds from cleistogamous flowers (Berg and Redbo-Torstensson 1998 ), thus it is less dependent on insect pollinators for sexual reproduction. According to our own research, however, O. acetosella is mainly outcrossing (Naaf et al 2021 ). Anemone nemorosa and Polygonatum multiflorum are mainly and strictly outcrossing, respectively (Müller et al 2000 ; Kosiński 2012 ).…”

“…Anemone nemorosa and Polygonatum multiflorum are mainly and strictly outcrossing, respectively (Müller et al 2000 ; Kosiński 2012 ). Oxalis acetosella and A. nemorosa are pollinated by a wide range of pollinators, including hoverflies, wild bees and honey bees (Shirreffs 1985 ; Redbo-Torstensson and Berg 1995 ; Stehlik and Holderegger 2000 ; Naaf et al 2021 ). In contrast, P. multiflorum is mostly pollinated by long-tongued bumblebees (Kosiński 2012 ; Naaf et al 2021 ).…”

“…Oxalis acetosella and A. nemorosa are pollinated by a wide range of pollinators, including hoverflies, wild bees and honey bees (Shirreffs 1985 ; Redbo-Torstensson and Berg 1995 ; Stehlik and Holderegger 2000 ; Naaf et al 2021 ). In contrast, P. multiflorum is mostly pollinated by long-tongued bumblebees (Kosiński 2012 ; Naaf et al 2021 ). All three species have a low seed-dispersal potential and are classified as autochorous (Müller-Schneider 1986 ).…”

“…While O. acetosella and P. multiflorum are diploid, A. nemorosa was treated as tetraploid (Stehlik and Holderegger 2000 ). For details on genetic analyses and the calculation of population genetic variables see Naaf et al ( 2021 ), in which we studied the effects of habitat loss and fragmentation per se.

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“…Numerous population genetic studies revealed that the functional connectivity among temperate forest herb populations may be strongly reduced in landscapes with a high degree of forest fragmentation. For instance, small, spatially isolated populations often exhibit a reduced allelic richness (Vellend 2004 ; Jacquemyn et al 2006 ; Vandepitte et al 2007 ; Kolb and Durka 2013 ; Naaf et al 2021 ) and are strongly genetically differentiated from each other (Jacquemyn et al 2006 ; Schmidt et al 2009 ; Gentili et al 2018 ). However, local populations may maintain a high level of genetic diversity (Culley et al 2007 ; Toma et al 2015 ) and a low level of genetic differentiation among them (Van Rossum et al 2002 ; Tomimatsu and Ohara 2003 ; Jacquemyn et al 2009 ) if they are functionally connected by steady gene flow.…”