Impacts of biological globalization in the Mediterranean: Unveiling the deep history of human-mediated gamebird dispersal Giovanni Forcinaa, Monica Guerrinia, Hein van Grouwb, Brij K. Guptac, Panicos Panayidesd, Pantelis Hadjigeroud, Omar F. Al-Sheikhlye, Muhammad N. Awanf, Aleem A. Khang, Melinda A. Zederh,1, and Filippo Barbaneraa,1 aDepartment of Biology, Zoology and Anthropology Unit, University of Pisa, 56126 Pisa, Italy; bBird Group, Department of Life Sciences, The Natural History Museum, Herts HP23 6AP, United Kingdom; cCentral Zoo Authority, Ministry of Environment, Forests and Climate Change, New Delhi 110001, India; dGame Fund Department, Ministry of Interior, 1453 Nicosia, Cyprus; eDepartment of Biology, University of Baghdad, Al-Jadriya, 10071 Baghdad, Iraq; fHimalayan Nature Conservation Foundation, Conservation Department, Muzaffarabad 13100, Azad Kashmir, Pakistan; gInstitute of Pure and Applied Biology, Zoology Division, Bahauddin Zakariya University, Multan 60800, Pakistan; and hProgram in Human Ecology and Archaeobiology, Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012 Contributed by Melinda A. Zeder, January 15, 2015 (sent for review September 5, 2014; reviewed by Nicole Boivin and Greger Larson) Humans have a long history of moving wildlife that over time has especially profound and lasting impact on native biotas in the resulted in unprecedented biotic homogenization. It is, as a result, Mediterranean Basin. Species translocations have led to sub- often unclear whether certain taxa are native to a region or na- stantial if not complete replacement of insular endemics (6). At turalized, and how the history of human involvement in species the same time, human-mediated species movement and landscape dispersal has shaped present-day biodiversity. Although currently management have helped preserve high biodiversity in present- an eastern Palaearctic galliform, the black francolin (Francolinus day anthropogenic, yet threatened Mediterranean environments francolinus) was known to occur in the western Mediterranean (7). The impressive pace and extent of present-day wildlife relo- “ ” from at least the time of Pliny the Elder, if not earlier. During cations raises concerns about biotic homogenization, the loss of Medieval times and the Renaissance, the black francolin was a biological distinctiveness in regions following replacement of native courtly gamebird prized not only for its flavor, but also its curative, biotas by locally expanding nonnatives (8). Achieving a compre- and even aphrodisiac qualities. There is uncertainty, however, hensive understanding of the antiquity and impact of humans on whether this important gamebird was native or introduced to the Mediterranean biodiversity promises significant insight into on- region and, if the latter, what the source of introduction into the going conservation issues, and sheds new light on the role of long- western Mediterranean was. Here we combine historical documen- distance trade and exchange in shaping the cultural identities and tation with a DNA investigation of modern birds and archival (13th– national destinies of people across the Mediterranean Basin. With their colorful plumage, small size, and relative ease of 20th century) specimens from across the species’ current and histor- transport and management, birds are likely candidates for long- ically documented range. Our study proves the black francolin was distance exchange and were often the animal of choice in European nonnative to the western Mediterranean, and we document its in- menageries (9, 10). The peacock (Pavo cristatus), for example, is troduction from the east via several trade routes, some reaching as thought to have been imported from Asia to Greece during the far as South Asia. This finding provides insight into the reach and time of Alexander the Great, and perhaps even earlier (11). In his scope of long-distance trade routes that serviced the demand of De Arte Venandi cum Avibus, Frederick II referred to the impor- European aristocracy for exotic species as symbols of wealth and tation of the Guinea fowl (Numida meleagris) from the Levant to prestige, and helps to demonstrate the lasting impact of human- Sicily (12). Chronicles of European adventurers in Asia, such as mediated long-distance species dispersal on current day biodiversity. Significance globalization | species dispersal | wildlife trade | Mediterranean | DNA Human-mediated species dispersal stretching back at least uman-mediated species translocations have played a central 10,000 y has left an indelible stamp on present day biodiversity. Hrole in shaping global biodiversity for thousands of years (1). A major contributing factor to this process was the trade in The dispersal of early agricultural economies out of the centers a wide range of exotic species that was fueled by elite demand. of initial domestication more than 10,000 y ago marks an ac- The black francolin—now extinct in the western Mediterranean celeration of human-directed species range expansions involving but once a courtly gamebird prized for its flavor, curative, and both domesticates and a wide range of nondomesticated species (2, aphrodisiac qualities by European aristocracy—was one of these 3). The maritime and overland trade routes of the third millennium species. Using historical sources and DNA analysis of modern and B.C. that linked major urban centers across South and Central Asia, archival specimens, we show that this bird was not native to the Mesopotamia, the Arabian Peninsula, and North Africa expanded western Mediterranean, and document its introduction to the geographic distribution and diversity of species through long- Cyprus and westward through the Mediterranean Basin via distance translocations (4). The range and impact of this process several trade routes that reached as far east as South Asia. continued to increase as transportation technology improved and as demand for both staple and rare exotic species from faraway places Author contributions: F.B. designed research; G.F. performed research; G.F., M.G., A.A.K., M.A.Z., and F.B. analyzed data; G.F., M.A.Z., and F.B. wrote the paper; and H.v.G., B.K.G., grew among ruling elites and rising mercantile classes across the P.P., P.H., O.F.A.-S., M.N.A., and A.A.K. performed biological sampling. increasingly vast territory connected in these exchanges. The post- Reviewers: N.B., University of Oxford; and G.L., University of Oxford. A.D. 1000 period in particular saw a surge in species translocations The authors declare no conflict of interest. as emerging nation states in Medieval and Renaissance Europe Data deposition: The sequences reportedinthispaperhavebeendepositedinthe received a staggering diversity of plants and animals through trade GenBank database (accession nos. LK871783–LK871855). routes that linked an expansionist Islamic world with major empires 1To whom correspondence may be addressed Email: [email protected] or filippo.barbanera@ in central Asia and China (1, 5). unipi.it. This process of biological globalization resulted in large-scale This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. reshuffling of both wildlife and domesticates that has had an 1073/pnas.1500677112/-/DCSupplemental. 3296–3301 | PNAS | March 17, 2015 | vol. 112 | no. 11 www.pnas.org/cgi/doi/10.1073/pnas.1500677112 Downloaded by guest on October 1, 2021 Marco Polo (13), often contained references to gamebirds. Since featured in a poem (Xenia, “Gifts”) by the Roman epigrammatist the first centuries B.C., travelers along the Silk Road are known to Martial (ca. 85 B.C.), where it is referred to as a particularly tasty have carried and bred chukar partridges (Alectoris chukar)as bird included among the presents sent home with party guests at a source of food on the way to Europe (14). the festival of the Saturnalia. Later still, it is mentioned by the Another species of gamebird that may well have been included Roman lyric poet Horace (30 B.C.) in his iambic poetry (Epodes, in these exchanges is the black francolin (Francolinus francolinus, “The Epodes”)asfollows:“Non Afra avis descendat in ventrem Phasianidae). No longer found in the western Mediterranean, meum, non attagen Ionicus iucundior quam lecta de pinguissimis the black francolin is known from textual and iconographic olive ramis arborum (Not African fowls, nor Ionian Attagen could sources as a species that figured prominently in courtly life in pass my lips more happily than the fruit collected from the most Medieval and Renaissance Europe (5, 15). Here we combine heavily loaded branches of the olive).” In his Naturalis Historia historical documentation with the genetic study of modern, (77 A.D.), Pliny the Elder reported: “Attagen maxime Ionius archaeozoological, and archival collections of this bird to assess celeber et vocalis alias, captus vero obmutescens quondam extimatus whether the black francolin represents an example of the extir- inter raras aves, iam et in Gallia Hispanique (the most reputed pation of a native or an introduced species in the western Attagen is that from Ionia; it usually sings but is silent in captivity; Mediterranean, thus exploring what this species can tell us about once considered a rare bird, but now it is also found in Gaul and the nature of human-mediated dispersals in the region. Spain)” (19). No additional textual documentation of the black francolin in The Black Francolin in the Mediterranean the Mediterranean