Population genetics and abundance of the Endangered grey-headed lemurEulemur cinereicepsin south-east Madagascar: assessing risks for fragmented and continuous populations

Abstract

Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations R i c k A . B r e n n e m a n , S t e i g E . J o h n s o n , C a r o l y n A . B a i l e y C h r i s t i n a I n g r a l d i , K i r a E . D e l m o r e , T r a c y M . W y m a n H u b e r t E . A n d r i a m a h a r o a , F i d i m a l a l a B . R a l a i n a s o l o J o n a h H . R a t s i m b a z a f y and E d w a r d E . L o u i s , J rAbstract Knowledge of both population size and genetic diversity is critical for assessing extinction risk but few studies include concurrent estimates of these two components of population biology. We conducted an investigation of population density and size, and genetic variation and past demographic events, of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar. We estimated lemur density using line-transect surveys and used satellite imagery to calculate forest fragment area in three localities. We collected tissue samples from 53 individuals and used 26 polymorphic microsatellite loci to obtain measures of population structure (divergence and diversity) across these localities. We tested the probability of past bottleneck events using three models. Contrary to expectation, there were no significant differences in population density across localities. Genetic diversity decreased, but not significantly, with decreasing habitat area and population size. We found a higher likelihood of past bottleneck events in the fragmented coastal populations. The low population size and prior decline in diversity in coastal patches are consistent with their isolation, anthropogenic disturbance, and exposure to cyclone activity. The similarities in the estimates of density between continuous and fragmented sites may indicate recent population growth in the fragments but these populations nevertheless remain at risk from reduced levels of genetic variation. These patterns should be confirmed with more extensive sampling across the limited range of E. cinereiceps.This paper contains supplementary material that can be found online at

Stuck in fragments: Population genetics of the Endangered collared brown lemurEulemur collarisin the Malagasy littoral forest

“…This pattern is supported by the overall association between genetic diversity and patch size, which, in turn, is a good proxy of population size (Arroyo‐Rodrıguez and Dias, ; Holmes et al, ; Knaepkens, Bervoets, Verheyen, & Eens, ). A similar trend towards low genetic diversity in fragmented populations was recently observed in one congeneric species ( Eulemur cinereiceps , Brenneman et al, ) as well as in other genera of the family Lemuridae ( Varecia variegata , Holmes et al, ; Lemur catta , Clarke, Gray, Gould, & Burrell, ). However, the genetic diversity of the collared brown lemurs from Fort Dauphin's littoral forest appears even lower than that observed in other lemur populations.…”

“…A previous genetic assessment of four populations of E. collaris in three continuous forests located in the central and northern part of the species range revealed higher mean H e , 0.58 (10 loci; Ranaivoarisoa et al, ) than that observed in our populations, 0.45 (8 loci). The mean H e of littoral E. collaris is also low when compared to the Critically Endangered, congeneric E. cinereiceps , 0.53 (26 loci), that also has part of its range occurring in littoral forest fragments (Brenneman et al, ). Such a pattern holds even when compared with other lemurids living in fragmented forests ( Varecia variegata : 0.57 [10 loci; Baden et al, ] and Lemur catta : 0.80 [8 loci; Parga et al, ]), and other lemur families ( Propithecus coquereli : 0.77 [20 loci; Rakotoarisoa et al, ]; Microcebus revelobensis : 0.60 [8 loci; Olivieri, Sousa, Chikhi, & Radespiel, ] ; Propithecus tattersalli : 0.72 [13 loci; Quéméré, Louis, Ribéron, Chikhi, & Crouau‐Roy, ]; Propithecus perrieri : 0.64 [24 loci; Salmona et al, ]).…”

Trends in forest fragment research in Madagascar: Documented responses by lemurs and other taxa

“…For LA, other tests of fragmentation employed included the impact of landscape changes over time (percent forest loss: Marrocoli, Hamann, & Allison, 2013; pre‐ and with forest corridor: Montero et al, 2019), percent canopy cover (e.g., Raharivololona & Ganzhorn, 2009), and qualitative assessments of the extent of fragmentation (e.g., Brenneman et al, 2012; Campera et al, 2014), among others (Supporting Information Appendix S3). Two LA examined fragmentation per se: Salmona et al (2017) by a population genetics analysis determining whether habitat loss, fragmentation, or a combination best explained the demographic history of two sifaka species ( P. tattersalli and Propithecus perrieri ) and Steffens and Lehman (2018) by the impact of the simulated removal of fragments or alteration of interfragment distance on lemur species in Ankarafantsika National Park, northwestern Madagascar.…”

“…Two studies additionally report lower genetic diversity for Milne‐Edwards’ sportive lemur ( Lepilemur edwardsi ; Craul et al, 2009) and golden‐brown mouse lemur ( Microcebus ravelobensis : Guschanski, Olivieri, Funk, & Radespiel, 2007) in forest fragments than in Ankarafantsika National Park but do not explicitly link these findings to fragment size. Five species living in fragmented landscapes displayed evidence of genetic bottlenecks within their studied range (white‐collared lemur, Eulemur cinereiceps : Brenneman et al, 2012; L. edwardsi : Craul et al, 2009; V. variegata : Holmes et al, 2013; Perrier's sifaka, P. perrieri , and Tattersall's sifaka, P. tattersalli : Salmona et al, 2017). Evidence for contemporary gene flow between fragments was also reported for Microcebus ganzhorni , indicating the species’ ability to access the matrix (Montero et al, 2019).…”

Decline and demographic changes in the population of the Near Threatened brown lemur Eulemur fulvus on Mayotte

“…Such data would facilitate the modelling of population dynamics and the examination of any density-dependency. A concurrent examination of genetic diversity, as in a recent study of the grey-headed lemur Eulemur cinereiceps in Madagascar (Brenneman et al, 2012), would facilitate a more detailed examination of extinction risk.…”