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Landscape Genetics of Northern Crested Newt Triturus Cristatus Populations in a Contrasting Natural and Human‑Impacted Boreal Forest

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Landscape Genetics of Northern Crested Newt Triturus Cristatus Populations in a Contrasting Natural and Human‑Impacted Boreal Forest Conservation Genetics (2020) 21:515–530 https://doi.org/10.1007/s10592-020-01266-6 RESEARCH ARTICLE Landscape genetics of northern crested newt Triturus cristatus populations in a contrasting natural and human‑impacted boreal forest Hanne Haugen1 · Arne Linløkken2 · Kjartan Østbye2,3 · Jan Heggenes1 Received: 21 June 2019 / Accepted: 12 March 2020 / Published online: 19 March 2020 © The Author(s) 2020 Abstract Among vertebrates, amphibians currently have the highest proportion of threatened species worldwide, mainly through loss of habitat, leading to increased population isolation. Smaller amphibian populations may lose more genetic diversity, and become more dependent on immigration for survival. Investigations of landscape factors and patterns mediating migration and population genetic diferentiation are fundamental for knowledge-based conservation. The pond-breeding northern crested newt (Triturus cristatus) populations are decreasing throughout Europe, and are a conservation concern. Using microsatellites, we studied the genetic structure of the northern crested newt in a boreal forest ecosystem containing two contrasting landscapes, one subject to recent change and habitat loss by clear-cutting and roadbuilding, and one with little anthropogenic disturbance. Newts from 12 breeding ponds were analyzed for 13 microsatellites and 7 landscape and spatial variables. With a Maximum-likelihood population-efects model we investigated important landscape factors potentially explaining genetic patterns. Results indicate that intervening landscape factors between breeding ponds, explain the genetic diferentiation in addition to an isolation-by-distance efect. Geographic distance, gravel roads, and south/south-west fac- ing slopes reduced landscape permeability and increased genetic diferentiation for these newts. The efect was opposite for streams, presumably being more favorable for newt dispersal. Populations within or bordering on old growth forest had a higher allelic richness than populations in managed forest outside these areas. Old growth forest areas may be important source habitats in the conservation of northern crested newt populations. Keywords Landscape genetics · Triturus cristatus · Boreal forest · Composition · Migration barriers Introduction Much of the widespread decline in global biodiversity (IPBES 2018) is driven by negative impacts from anthro- pogenic habitat changes and loss. Among all vertebrates, Electronic supplementary material The online version of this amphibians is the group that currently has the highest pro- article (https ://doi.org/10.1007/s1059 2-020-01266 -6) contains portion of threatened species, mainly because of habitat loss, supplementary material, which is available to authorized users. caused by agricultural land use, logging, and the changing * Jan Heggenes of freshwater systems (Stuart et al. 2004; Becker et al. 2007; [email protected] Baillie et al. 2010). 1 Habitat loss is a negative direct efect, as smaller habitat Department of Natural Sciences and Environmental Health, patches can sustain fewer individuals (Fahrig 2003; Cush- University of South-Eastern Norway, Campus Bø, Notodden, Norway man 2006; Fischer and Lindenmayer 2007), i.e., population reduction. However, the same process, typically also leads to 2 Department of Forestry and Wildlife Management, Inland Norway University of Applied Sciences, Evenstad, Norway habitat changes and split, i.e., an increase in the amount of inhospitable environments between populations, which can 3 Department of Biosciences, Center for Ecological and Evolutionary Synthesis (CEES), University of Oslo, reduce landscape permeability and migration between suita- Oslo, Norway ble habitat patches (Wiegand et al. 2005; Becker et al. 2007; Vol.:(0123456789)1 3 516 Conservation Genetics (2020) 21:515–530 Fischer and Lindenmayer 2007). Connectivity among habi- rejuvenated by natural forest fres) and no record of recent tats is suggested to play a key role in preserving amphibian logging (Reiso 2018). populations (Lehtinen et al. 1999; Cushman 2006; Becker We suggest that such forest habitat changes by clear-cut- et al. 2007; Coster et al. 2015a). ting likely is negative for amphibian genetic connectivity. The potential for migration to counteract habitat isola- However, we also hypothesize that additional landscape fea- tion efects is connected to the balance between a given spe- tures, both natural and infrastructure associated with clear- cies ability and its propensity to move and the geographical cutting, primarily roads, may play an important role in these distance to travel [the isolation-by-distance efect (Wright generally less human-impacted landscapes. This requires 1943; Hutchison and Templeton 1999; Jenkins et al. 2010)]. more detailed data and analysis, but is important particu- However, it is also connected to the species ability to trav- larly in proactive conservation. Here, factors like aspect and erse the in-between (matrix) habitat (i.e., landscape resist- vegetation cover may be important considering the distri- ance Jenkins et al. 2010; Richardson 2012; Balkenhol et al. bution of cool and humid microclimates, and thereby the 2016), depending on the species vagility, plus the ability accessibility of suitable habitat for amphibians (Oke 2002; to cross diferent types of environments. Amphibians are Peterman and Semlitsch 2013). Streams could function as considered unlikely candidates for good dispersal, with humid dispersal corridors (Emel and Storfer 2015), steep their generally low vagility (Bowne and Bowers 2004; Alex slopes as barriers or partial barriers by evoking avoidance Smith and Green 2005), small body sizes and high water behavior or increasing energy cost (Lowe et al. 2006). Low loss rate under hot and dry conditions (Oke 1987; Wells soil productivity and the removal of forest canopy could 2007). Therefore, landscape factors determining matrix result in a lack of prey, as invertebrate abundance may be habitat likely may be important in determining the level of afected negatively by clear-cuts and low soil pH (Stuen and connectivity between habitats, and particularly for amphib- Spidsø 1988; Wareborn 1992; Atlegrim and Sjöberg 1996). ians (Compton et al. 2007; Todd et al. 2009; Goldberg and Further, forest gravel roads could act as barriers due to a Waits 2010). drier microclimate from removal of vegetation and canopy The general concept and framework of landscape genet- (Marsh and Beckman 2004), or because of steep roadside ics combines population genetics with features from land- verges that are too difcult to traverse (Marsh et al. 2005). scape ecology, ofering tools to investigate relative efects Here we use the northern newt as an amphibian model of landscape composition traits and the putatively associated to study landscape genetic relationships and identify what confguration upon gene fow and genetic drift (Balkenhol landscape features may afect the genetic diferentiation and et al. 2016). Factors reported to increase genetic diferentia- pattern of northern crested newt populations in a northern tion in an amphibian context, are roads (Richardson 2012; boreal forest breeding pond system with contrasting (near-) Sotiropoulos et al. 2013), rivers (Peter et al. 2009; Rich- natural vs. forestry impacted forest landscapes. North- ardson 2012), topography (Spear and Storfer 2008; Kersh- ern crested newt is a pond breeding amphibian. They can enbaum et al. 2014), urban areas (Emaresi et al. 2011) and become at least up to 16 years in the wild (Miaud and Cas- open felds (Greenwald et al. 2009), although efects can tanet 2011). A female can lay about 200 eggs annually (Arn- be species specifc or landscape specifc. Because most of tzen and Hedlund 1990), but because of lethal homozygotes these studies focus on landscapes afected by agriculture and there is a 50% lethality during egg development (Wallace urban development, an important observation is that forest 1987). Sexual maturity is reached at age 3–5 years (Dolmen cover appears to decrease population diferentiation (Green- 1983). Known maximum dispersal distance of the species is wald et al. 2009; Richardson 2012). However, although for- 1 km or more (e.g., 860 m Kupfer and Kneitz 2000, 1290 m ests may still constitute extensive and important habitats for Kupfer 1998). However, long distance dispersal events could amphibians (Corn and Bury 1989; Gibbs 1998; Semlitsch be difcult to observe and generalize because of the rarity and Bodie 2003; Cushman 2006; Coster et al. 2015b), few of such events, and the likely dependence on factors such as studies focus on contrasting forest ecosystems, which may corridors and matrix between ponds. be disturbed by human impacts, or remain natural. Here, we focus on a boreal northern forest ecosystem without major human impacts like urban areas, agriculture Methods or major roads. However, the study system consists of boreal forest with diferent histories of generally low, but quite vari- Study area able and contrasting impacts from forestry practices. One part of the study area has been afected by clear-cutting and Thirteen known, fshless northern crested newt breeding harvest for several decades, whereas another part of the ponds were included for feld sampling in the study area study area consists of old natural Pinus sylvestris dominated (Fig. 1), located within a forested land area of 10.5 × 3.5 km forest with long forest continuity (trees 200–300 years old, (N59° 37′, E9° 19′) in south-east Norway. The sampled 1 3 Conservation
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