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Rapid Dwarfing of an Insular Mammal – the Feral Cattle of Amsterdam

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Rapid Dwarfing of an Insular Mammal – the Feral Cattle of Amsterdam www.nature.com/scientificreports OPEN Rapid Dwarfng of an Insular Mammal – The Feral Cattle of Amsterdam Island Received: 9 March 2017 Roberto Rozzi1 & Mark V. Lomolino2 Accepted: 19 July 2017 The island rule describes a graded trend in insular populations of vertebrates from gigantism in small Published: xx xx xxxx species to dwarfsm in large species. The dwarfng of large mammals on islands has been observed both in the present fauna and in the fossil record. Elephants, hippopotami, deer, and other species became dwarfed on islands scattered all over the world, from the Mediterranean Sea to Indonesia, from the Eastern to Western Pacifc Ocean, from the Caribbean to Canary Islands. The most rapid and well documented cases of island dwarfng known thus far took place over thousands of years. Here, we describe a rapid example of dwarfng of a large mammal - the feral cattle of Amsterdam Island, southern Indian Ocean, which dwarfed to about three quarters of its body size in slightly more than one century. This population provides us with a rare opportunity to assess the rapidity of demographic, life history, and morphological responses of large mammals to a very isolated and ecologically simple, insular environment. Te island rule describes a graded trend from gigantism in small species of vertebrates to dwarfsm in large species1–6, and it is part of a more general suite of responses to the geographic isolation and ecological simplicity of islands known as the island syndrome7. In addition to shifs in body size towards that of intermediate-sized mammals, the island syndrome (sensu lato)8 includes demographic and ecological responses (insular populations exhibiting abnormally high densities and occurring in an unusually broad range of habitats), shifs in life history characteristics (e.g., altered generation times and reproductive potentials), and modifcations of bauplans9 (e.g., towards that supporting low-gear locomotion in large mammals such as insular elephants and hippos). Tese sometimes remarkable shifs in morphological, physiological, behavioral, and ecological characteristics of insular populations of mammals may ultimately be the products of the ecological simplicity of the islands they inhabit3, 4. Essentially, the island syndrome may well evidence reversals in natural selection from ecolog- ical displacement favouring diversifcation and adaptive radiations in species-rich communities, to ecological release in species-poor insular communities (in particular, those lacking mammalian competitors and predators) and convergence on the intermediate but absent phenotypes2–4, 8. Furthermore, the various features of the island syndrome may be expected to occur in a fairly regular chronology, with each change being the precursor to sub- sequent changes in characteristics of the insular lineage7. Once established, the descendants of a founding popu- lation may undergo rapid increases in their populations, quickly followed by expansions into habitats, diets, and other ecological strategies considered atypical for the species on the mainland (invading niches lef vacant in the absence of their mammalian competitors and predators)8. Following these early phases of the island syndrome, which may occur within just a few generations, descendants of these initial populations may undergo phyletic evolution which allows them to progressively adapt to their new niches and insular environments8, 10. For large mammals, with their relatively long generation times, the latter, evolutionary phases of the island syndrome may be expected to require extremely long periods of ecological isolation. Tere is, however, some limited but intriguing indication that at least the initial stages of dwarfsm in very large mammals can be remark- ably rapid (e.g., some artiodactyls and proboscideans decreasing to between 25–50% of the mass of the ancestors in just a few millennia)5, 6. Lister hypothesized that this represented the frst of a two-stage process of body size evolution in large mammals – this frst, very rapid stage being followed by one of slower but more prolonged dwarfsm which, providing persistence of the insular lineage, ofen produced the true marvels of island evolu- tion including hippos and elephants that dwarfed to just 5% of the mass of their mainland ancestors10. Lister’s 1Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, 10115, Berlin, Germany. 2State University of New York, College of Environmental Science and Forestry, Syracuse, NY, 13210, USA. Correspondence and requests for materials should be addressed to R.R. (email: [email protected]) SCIENTIFIC REPORTS | 7: 8820 | DOI:10.1038/s41598-017-08820-2 1 www.nature.com/scientificreports/ Figure 1. Map of Amsterdam Island and general information about the feral cattle population. (a) Feral cattle distribution and breeding area of the Amsterdam albatross (map modifed afer ref. 16). (b) Location map of Amsterdam Island (map modifed from Wikimedia Commons, public domain: https://commons.wikimedia. org/wiki/Maps_of_the_world#/media/File:BlankMap-World6.svg). (c) Feral cattle population size from introduction to frst removal (data from ref. 16). initial stage of dwarfng is characterised by an interplay of plastic and genetic efects10. In particular, the genetic component of size reduction would come about in part by genetic assimilation of initial ecophenotypic stunting. Tis stage is dominated by strong selective pressure for size reduction and it is accompanied by allometric and other developmental efects10. In the second stage, mostly driven by natural selection, processes already begun in the initial stage continue much longer and produce more extreme changes10. A common feature in dwarfed island herbivores is a great shortening of the limbs, especially the distal limb elements. Tis has been explained as an adaptation for what Sondaar (1977) described as low-gear locomotion9 – a frequent phenomenon believed to be more adaptive, in the absence of predators, for climbing across rocky and hilly terrain than the ancestral (mediportal) bauplan. While the great wealth of evidence on body size evolution in large mammals is derived from palaeontological studies, anthropogenic introductions of mammals to islands in recent history can also provide key insights into the rate and nature of the island rule and, more generally, the island syndrome. Such introductions can serve as valuable manipulative experiments on the ecology and evolution of isolated biotas. Here, we describe the case of the feral cattle (Bos primigenius taurus) of Amsterdam Island (South Indian Ocean), which provides us with a rare opportunity to assess the rapidity of demographic, life history, and evolutionary (body size and bauplan) responses of large mammals to the ecological simplicity of a very isolated, insular environment. Amsterdam Island (37°40′33″S, 77°33′17″E) is a 55 km2 volcanic dome in the South Indian Ocean that arose between 0.4 to 0.2 myBP11 (Fig. 1). At the time of introduction of the cattle, its maximum elevation was 881 m above sea level and the island habitat ranged from Phylica nitida trees and grasses in the lowlands to dwarf shrubs (Acaena magellanica), sphagum bogs and mosses along the higher elevations12. Te feral herd of Bos primigenius taurus was established when fve individuals were introduced onto the island in 1871, these being translocated from Réunion Island (21°06′52″S, 55°31′57″E). Tese individuals were descendants of French stocks present on Réunion Island, which at that time included the following breeds: Jersey, Tarentaise, Grey Alpine, and Breton Black Pied12–15. From the initial founders, this unmanaged population, free from artifcial selection and natural predators and competitors, quickly increased in number (Fig. 1) and spread across the island to occupy most of the lowland habitats (those <500 m), which included grasslands, shrubs, and Phylica nitida trees and ferns. By 1950, the pop- ulation had increased to an estimated 2000 individuals – sufcient numbers such that grazing and trampling pres- sures heavily impacted the island’s native biota. In fact, at that time much of the native vegetation had disappeared in favour of introduced plants and, particularly, forage grasses16. Te population of feral cattle then experienced a collapse in 1951 due to an undetermined disease outbreak, but quickly rebounded to reach pre-collapse levels by the 1980s16. With the ecological impacts of the burgeoning population of cattle now threatening the survival of island endemics, including the endemic tree (Phylica nitida) and the Amsterdam Island albatross (Diomedea amsterdamensis), conservation measures were initiated to control the herd16. Tis included erection of fences in 1987 and 1992 to restrict the range of the cattle (Fig. 1), and culling, which began in the late 1980s but, ultimately, was followed by extermination of the herd in 2010 to protect native plants and animals. SCIENTIFIC REPORTS | 7: 8820 | DOI:10.1038/s41598-017-08820-2 2 www.nature.com/scientificreports/ Figure 2. Body masses of adult Amsterdam Island cattle and body size divergence with respect to ancestral French breeds. (a) Comparison of average body masses of adult Amsterdam Island cattle to that of the ancestral French breeds. Silhouette of cattle from Amsterdam island drawn by R.R. Images of other breeds from Wikimedia Commons, user credits from lef to right: https://en.wikipedia.org/wiki/Bretonne_Pie_ Noir#/media/File:Taureau_breton_pie_noir.JPG by Gaëlle Diabaté is licensed under
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