Extinction and ecological retreat in a community of primates

Abstract

The lemurs of Madagascar represent a prodigious adaptive radiation. At least 17 species ranging from 11 to 160 kg have become extinct during the past 2000 years. The effect of this loss on contemporary lemurs is unknown. The concept of competitive release favours the expansion of living species into vacant niches. Alternatively, factors that triggered the extinction of some species could have also reduced communitywide niche breadth. Here, we use radiocarbon and stable isotope data to examine temporal shifts in the niches of extant lemur species following the extinction of eight large-bodied species. We focus on southwestern Madagascar and report profound isotopic shifts, both from the time when now-extinct lemurs abounded and from the time immediately following their decline to the present. Unexpectedly, the past environments exploited by lemurs were drier than the protected (albeit often degraded) riparian habitats assumed to be ideal for lemurs today. Neither competitive release nor niche contraction can explain these observed trends. We develop an alternative hypothesis: ecological retreat, which suggests that factors surrounding extinction may force surviving species into marginal or previously unfilled niches.

Stable Isotopes from Museum Specimens May Provide Evidence of Long-Term Change in the Trophic Ecology of a Migratory Aerial Insectivore

“…While initially applied to bone collagen to identify shifts in prehistoric human diets (Ambrose, 1986), this technique has also been applied to animal bones and keratinized tissues to explore changes in marine and terrestrial food webs (Thompson et al, 1995;Farmer and Leonard, 2011;Crowley et al, 2012;Wiley et al, 2013;Moreno et al, 2016) and linkages between them (Darimont and Reimchen, 2002;Chamberlain et al, 2005;Blight et al, 2015;Matsubayashi et al, 2015). Shifts in diet between types of mammal carrion (marine, terrestrial herbivores, and grainfed livestock) by California Condors (Gymnogyps californianus; Chamberlain et al, 2005) and from vertebrate herbivores and toward plant materials by Brown Bears (Ursus arctos; Matsubayashi et al, 2015) have been detected by comparing both the δ 15 N and δ 13 C values of museum specimen tissues from the predators and potential prey types during different time periods.…”

Patterns of Dental Macrowear in Subfossil Lemur catta from Ankilitelo Cave, Madagascar: Indications of Ecology and Habitat Use over Time

“…These data show the value of a dental ecology approach to reconstruct the habitats and feeding ecology of extinct primates, when viewed in the context of the feeding ecology of extant forms. Our results also have implications regarding the ongoing debate as to whether climate change, human effects or a combination of both caused the demise of the larger subfossil lemurs [Burney et al, 2004;Crowley, 2010;Crowley et al, 2012]. Given that the Ankilitelo forest, whether based on known dates for its primates at ∼ 500 to ∼ 600 BP or an earlier Holocene assemblage, appears to have been intact and supporting a vibrant animal community including the large, highly suspensory Paleopropithecus , today the area is completely denuded ( L. catta has been extirpated from the area and E. rufifrons exists in only a few dry forest parcels) [Muldoon, 2010].…”

“…Crowley et al [2012] suggest that the past 2 millennia have witnessed an 'ecological retreat' of southwestern Madagascar's lemurs, with the surviving taxa having moved into either marginal habitats or those previously unused. Our working hypothesis is that ring-tailed lemurs living in the riverine gallery forests dominated by tamarind trees are in evolutionary disequilibrium, relying on a fallback food for which they are not dentally adapted [Cuozzo and Sauther, 2006;Sauther and Cuozzo, 2009;Cuozzo and Sauther, 2012a, b].…”

“…Martin [1972] earlier noted that the extant and subfossil lemurs of Madagascar once formed a richer primate community than exists today, and that the extinction of the larger lemur forms may have created new niches for the remaining lemur species. This argument has recently been evoked by Crowley et al [2012], suggesting that some extant lemurs in southwestern Madagascar have been forced into marginal or previously unused habitats, following the recent extinction of the larger forms.…”

“…Thus, one of the major questions concerning Madagascar's remaining, endangered lemurs is how their ecology may have changed with both environmental and human-induced habitat change over the past 4 millennia since human arrival [Crowley et al, 2012]. One way to assess this is to examine recent subfossil examples of the remaining lemurs [Godfrey et al, 1999].…”