Isotopic ecology and extirpation chronology of the extinct Lesser Antillean native rodent Antillomys rayi Brace et al. (2015)
Introduction
The Lesser Antillean native rodents form part of a wider mainland South-American rodent radiation, the tribe Oryzomyini (family Cricetidae, subfamily Sigmodontinae), which comprises 29 extant genera, from which around 141 species are currently recognized (Pardiñas et al., 2017). Species of this tribe are sometimes referred to as “rice rats”. Oryzomyine rodents probably colonized the island chain during the Late Miocene (Brace et al., 2015). Their skeletal remains are frequently found in both archaeological and palaeontological sites and provide evidence for the presence of around 20 separate oryzomyine populations across the Lesser Antillean islands, which include different endemic genera and species (Turvey et al., 2010, 2012; Brace et al., 2015). The Lesser Antillean native rodents are now extinct, disappearing as part of a larger Holocene Caribbean extinction event most likely driven by anthropogenic causes (Cooke et al., 2017). These extinctions probably occurred during the last millennium, with several following European contact, and the last-occurrences of Lesser Antillean native rodents documented in the late 19th or very early 20th century. Because last-occurrence dates are not available for most species and/or rarely rely on direct radiocarbon dating, the dynamics, drivers and timing of these disappearances, however, remain elusive and potentially differ between regions and populations (Turvey et al., 2010; Cooke et al., 2017). Several hypotheses have been advanced to explain them, including biological competition with introduced species and human impact on oryzomyine populations or their habitats, initially by Amerindian populations and/or by subsequent European colonists.
Several studies of oryzomyine bones recovered from archaeological sites indicate they constituted an important component of the Amerindian diet (Wing et al., 2001; Wing, 2001; Newsom and Wing, 2004). Such practices could have led to the extirpation of some populations during the region’s prehistoric period (e.g., Wing et al., 1968; Jones, 1985; Wing, 1995; Wing and Wing, 1997; Nokkert, 1999). On the contrary, several authors consider that most of these extirpations were driven either directly or indirectly by European colonists (Turvey et al., 2010). For instance, Lesser Antillean native rodents may have been overexploited for their meat. Historical accounts do, in fact, mention that they were still consumed during the historical period on several islands (Du Tertre 1667, Rochefort 1667, Labat, 1722, Turvey et al., 2010). Another potential cause could be the large-scale transformation of island’s forests into agricultural areas, potentially destroying the natural habitats of Lesser Antillean native rodents. The introduction of invasive species may have equally played a role in these extinctions. For example, the last known records of several Lesser Antillean native rodent species (Megalomys desmarestii, M. luciae and Oligoryzomys victus) all date to between 1880 and 1890 and are concomitant with the introduction of the Indian mongoose (Urva auropunctata; Horst et al., 2001; Turvey et al., 2010). The impact of the invasive black rat (Rattus rattus) as a biological competitor has equally been suspected for older extirpations (Pinchon, 1967; Wing, 2008; Turvey et al., 2010). However, all of these hypotheses are currently difficult to test in view of the paucity of data, including reliable last-occurrence dates and a precise understanding of Lesser Antillean native rodent ecology.
In Guadeloupe (Basse-Terre and Grande-Terre), Marie-Galante, Barbuda and Antigua, fossil specimens of a large Lesser Antillean native rodent have recently been described as representing a distinct species, Antillomys rayi Brace et al. (2015). Fossil remains of A. rayi have been identified from very few Amerindian archaeological sites on the Eastern coasts of Guadeloupe and Marie-Galante (Brace et al., 2015). However, this species occurrence appears to have been larger, including the pre-Columbian sites of Roseau on Basse-Terre and Folle-Anse on Marie-Galante, as well as natural accumulations preserved in the caves of Grotte des Bambous, Pointe-des-Châteaux, and Blanchard 2 (Fig. 1 and SI 1). The mechanisms underlying the extirpation of A. rayi from both islands currently remain unexplained. This is partly due to the lack of chronological data for the remains of this species from archaeological deposits.
Surprisingly, early chroniclers who described the Guadeloupe fauna do not mention any oryzomyine rodent (Ballet, 1895), raising the possibility of a relatively early extirpation during the prehistoric period. The only mentions of an oryzomyine rat on these islands come from an anonymous early 19th text indicating the persistence of a “pilori rat” on the tiny islet of Petite Terre (Anonyme, 1829) and the suspicion of its presence in the deep forests from Basse-Terre in the 1960s (Pinchon, 1967). Unfortunately, the scarcity of these observations and the lack of associated specimens make it difficult to lend credibility to these observations, therefore hinting at an early extirpation of A. rayi from the main Guadeloupe Islands.
Nonetheless, in the early colonial period of the Lesser Antillean islands, like Guadeloupe, increased agriculture activity resulted in a massive transformation of natural habitats, with most lowland forest cleared for cane cultivation, and middle elevation forest for coffee and cocoa crops (Lasserre, 1961; Lugo et al., 1981). Furthermore, the introduction of the black rat in the Lesser Antilles is relatively old, contemporary with the arrival of the first Europeans (prior to 1647, Du Tertre 1667, Breton, 1978; Lorvelec et al., 2007). This species could have colonized Guadeloupe as early as the 16th century with the arrival of the first Spanish ships, as is the case for Hispaniola (MacPhee et al., 1999; Wing et al., 2001). In this scenario, the extinction of A. rayi could also have been driven by direct or indirect human pressure during the historical period.
Information concerning the ecology of A. rayi, as well as precise last-occurrence dates is required to further test these different scenarios. To this end, we first measured both the oxygen and carbon isotopic compositions of present-day black rat tooth enamel from different natural environments of Guadeloupe (Basse-Terre and Grande-Terre (Goedert et al., 2020); in order to establish present-day isotopic reference values and compare them with oxygen and carbon isotopic compositions of fossil A. rayi tooth enamel (Fig. 2; SI 2, 3). In parallel, we obtained radiocarbon dates from A. rayi tooth enamel samples complemented by dates from other A. rayi skeletal elements from multiple sites in Guadeloupe (Basse-Terre and Grande-Terre) and Marie-Galante (Fig. 1) in order to better constrain the extirpation chronology of this species on these Lesser Antillean islands (Fig. 3; SI 4).
Section snippets
Climatic and geographic context
Guadeloupe comprises two main islands: the volcanic and mountainous Basse-Terre Island, to the west, and the carbonated low-lying island of Grande-Terre to the east. Guadeloupe experiences a marked precipitation gradient (e.g., Lasserre, 1961); the north-eastern region of Grande-Terre receives no more than 1300 mm of mean annual precipitation compared to the 10,000 mm mean annual precipitation of the volcanic summit of La Soufrière on Basse-Terre. Variations in soil type and climatic conditions
Material and methods
Sample sizes follow Royer (2013), Royer et al. (2013a), and Peneycad et al. (2019), who found that mean isotopic values from a subsample of n ≥ 5–10 rodent individuals is accurate enough to confidently (≥90 %) reflect mean isotopic values of larger populations. Consequently, we selected five black rat lower incisors per locality and per season to establish a present-day isotopic referential and at least ten A. rayi lower incisors per locality, representing at least six different individuals.
Stable isotope compositions of present-day black rats
Overall, δ13Cc and δ18Op values of black rat lower incisor distinguish the natural environments of Guadeloupe (SI 2; SI 8; Fig. 2). Apart from the swamp forest, each natural environment displays significant seasonal isotopic variations (SI 8; Fig. 2).
Black rats living in the semi-deciduous dry forest tend to have both higher δ13Cc and δ18Op values than those living in other environments (Fig. 2a). This is consistent with the fact that semi-deciduous dry forests receive the lowest mean annual
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Correspondence and requests for materials should be addressed to A. L.
Acknowledgements
We thank the Musée Edgar Clerc (MEC) and its curator S. Guimaraes, for granting us access to the museum’s fossil collections as well as material loaned to Dr. D. Mc Farlane and Dr. M. Weksler. We also thank Donald Mc Farlane and Marcello Weksler who provided access to this. We thank the Service Régional de l’archéologie de Guadeloupe and its head D. Bonnissent, as well as the collection manager G. Robert for facilitating access to the collections housed at the Direction des Affaires Culturelles
References (127)
- et al.
Digesting the data-Effects of predator ingestion on the oxygen isotopic signature of micro-mammal teeth
Quat. Sci. Rev.
(2017) - et al.
Spatial heterogeneity in the relationship between precipitation and carbon isotopic discrimination in C3 plants: inferences from a global compilation
Global Planet. Change
(2019) Variations in the 13C/12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation
Phytochemistry
(1971)- et al.
Pleistocene seasonal temperature variations recorded in the δ18O of Bison priscus teeth
Earth Planet Sci. Lett.
(2009) - et al.
Paléoclimat des Petites Antilles depuis 4000 ans BP: l’enregistrement de la lagune de Grand-Case à Saint-Martin
Compt. Rendus Geosci.
(2004) - et al.
Oxygen isotope systematics of biologically mediated reactions of phosphate: I. Microbial degradation of organophosphorus compounds
Geochem. Cosmochim. Acta
(1997) - et al.
Robust estimates of extinction time in the geological record
Quat. Sci. Rev.
(2012) - et al.
Biologic and climatic signals in the oxygen isotopic composition of Eocene-Oligocene equid enamel phosphate
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(1996) - et al.
Carbon isotopes of trees from arid environments and implications for reconstructing atmospheric CO2 concentration
Geochem. Cosmochim. Acta
(1995) - et al.
An 85-ka record of climate change in lowland Central America
Quat. Sci. Rev.
(2008)
Oxygen isotope analyses of co-existing carbonate and phosphate in biogenic apatite: a way to monitor diagenetic alteration of bone phosphate?
Earth Planet Sci. Lett.
Influences on the stable oxygen and carbon isotopes in gerbillid rodent teeth in semi-arid and arid environments: implications for past climate and environmental reconstruction
Earth Planet Sci. Lett.
The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite
J. Archaeol. Sci.
Oxygen isotope evidence of little ice age aridity on the caribbean slope of the cordillera central, Dominican Republic
Quat. Res.
Thermal excursions in the ocean at the Cretaceous—tertiary boundary (northern Morocco): δ18O record of phosphatic fish debris
Palaeogeogr. Palaeoclimatol. Palaeoecol.
Oxygen isotope exchange between dissolved phosphate and water at temperatures ≤135°C: inorganic versus biological fractionations
Geochem. Cosmochim. Acta
Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet
J. Archaeol. Sci.
Oxygen isotopes in mammal bone phosphate: a new tool for paleohydrological and paleoclimatological research?
Geochem. Cosmochim. Acta
Fractionation of oxygen isotopes between mammalian bone-phosphate and environmental drinking water
Geochem. Cosmochim. Acta
Blanchard Cave 2: a historic period Audubon’s shearwater (Puffinus lherminieri) nesting site in Marie-Galante (Guadeloupe islands, FWI)
J. Archeol. Sci.: Rep.
Combined records from a stalagmite from Barbados and from lake sediments in Haiti reveal variable seasonality in the Caribbean between 6.7 and 3 ka BP
Quat. Sci. Rev.
Magma-derived CO2 emissions recorded in 14C and 13C content of plants growing in Furnas caldera, Azores
J. Volcanol. Geoth. Res.
Variability in the oxygen isotope compositions of modern rodent tooth carbonate: implications for palaeoclimate reconstructions
Palaeogeogr. Palaeoclimatol. Palaeoecol.
Bone collagen preservation in the tropics: a case study from ancient Puerto Rico
J. Archaeol. Sci.
Turnover of oxygen and hydrogen isotopes in the body water, CO2, hair, and enamel of a small mammal
Geochem. Cosmochim. Acta
Description des îles d’Amérique en l’estat qu’elle estoient l’année 1660. Archives of the French State Secretary for the Navy. ANOM, C/8B/1
Notices historiques et statistiques sur la Guadeloupe et dépendances. Pages 117 (3)-155 (41) Almanach de la Guadeloupe et dépendances pour l’année commune 1829
Can C3 plants faithfully record the carbon isotopic composition of atmospheric carbon dioxide?
Paleobiology
La Guadeloupe. Renseignements sur l’histoire, la flore, la faune, la géologie, la minéralogie, l’agriculture, le commerce, l’industrie, la législation, l’administration
Le programme ARTEMIS: nouvel outil pour la datation radiocarbone AMS (Spectromètre de Masse par Accélérateur) et nouvelles problématiques
The “Cayo” Site of Roseau: Ceramic, Vertebrate and Isotopic Analysis of a Guadeloupe Late Ceramic Archaeological Assemblage
Invasive mammals in Cuba: an overview
Biol. Invasions
Unexpected evolutionary diversity in a recently extinct Caribbean mammal radiation
Proc. Biol. Sci.
Relations de l’île de la Guadeloupe
Isotopic partitioning by small mammals in the subnivium
Ecol. Evol.
Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies
Oecologia
Folle-Anse (Grand-Bourg de Marie-Galante). Pages 19–21 Bilan scientifique de la région Guadeloupe 1997. Ministère de la Culture et de la Communication, direction régionales des affaires culturelles Guadeloupe
Population ecology of Rattus Rattus across a desert-montane forest gradient in the galapagos islands
Ecology
Biology of the bahaman hutia, geocapromys ingrahami
J. Mammal.
Histology of the mouse incisor
J. Dent. Res.
Grotte des Bambous, commune du Moule. Rapport de sondage archéologique. Direction des Affaires Culturelles
Deciphering the isotopic niches of now-extinct Hispaniolan rodents
J. Vertebr. Paleontol.
Anthropogenic extinction dominates Holocene declines of West Indian mammals
Annu. Rev. Ecol. Evol. Syst.
After two decades a second anchor for the VPDB δ13C scale
Rapid Commun. Mass Spectrom.: Int. J. Devoted Rapid Dissem. Min. Res. Mass Spectro.
Preparation of phosphate samples for oxygen isotope analysis
Anal. Chem.
Stable isotopes in precipitation
Tellus
Pre-Columbian social organisation and interaction interpreted through the study of settlement patterns
Cycle de reproduction du rat noir (Rattus rattus) et du surmulot (Rattus norvegicus) dans différents milieux de la Guadeloupe (Antilles françaises): Mammalia
Mammalia
Cited by (4)
The pre-Columbian site of Roseau (Guadeloupe, F. W. I.): intra-site chronological variability of the subsistence strategies in a Late Ceramic archeological vertebrate assemblage
2021, Archaeological and Anthropological Sciences