Threatened by Legislative Conservationism? The Case of the Critically Endangered Aeolian Lizard
Spartaco Gippoliti
Massimo Capula2 
Daniele Salvi
Franco Andreone- 1Società Italiana per la Storia della Fauna “G. Altobello”, Rome, Italy
- 2Museo Civico di Zoologia, Rome, Italy
- 3Department of Environmental Sciences and Policy, Università degli Studi di Milano, Milan, Italy
- 4Laboratoire d'Ecologie Alpine, Centre National de la Recherche Scientifique, University of Grenoble Alpes, Grenoble, France
- 5Department of Health, Life and Environmental Sciences, University of L'Aquila, L'Aquila, Italy
- 6CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Porto, Portugal
- 7Museo Regionale di Scienze Naturali, Turin, Italy
Species-based conservation legislation needs to be based on sound scientific data and updated taxonomic knowledge. European Union environmental legislation is among the most advanced in the world, yet there is not a clear and regular mechanism to update species' lists of Habitats Directive Annexes according the latest available scientific data. Here we reviewed the situation of the endemic Aeolian lizard Podarcis raffonei and indicate it as a case-study of possible ongoing species extinction into the Mediterranean biodiversity hotspot as the result of failure to update lists of EU protected species. We recommend to implement a mechanism of periodical revision of the Annexes of the Habitats Directive with particular attention to endemic EU species included in the IUCN Red List as Critically Endangered.
Introduction
Islands are well-known in shaping the perception and understanding of evolutionary processes (Lomolino, 2005). In fact, speciation and endemism of insular species are often linked to conservation priorities and are not only limited to well-known and celebrated tropical islands or archipelagos, but are also relevant in temperate environments. In such a context, lizards of the genus Podarcis show a remarkable pattern of diversity in the Mediterranean Region. Six endemic island species are currently recognized in the Western sector of the Mediterranean Region, while tens of endemic subspecies were described during the last century (Corti et al., 2011). Apart from their biological and ecological importance, Podarcis species are witnessing a relevant historical, cultural, and scientific value, since their study provided key insights to our understanding of evolutionary theory (Wallace, 1878) and for the identification of phylogenetic lineages (Arnold, 1989).
In the last years the amazing advances of molecular biology and integrative taxonomy are boosting our understanding of species evolution. As a consequence, hundreds of new species are described thanks to our ability to detect distinct evolutionary units, which were hardly identified on the basis of morphological characters only. However, the complexity of evolutionary dynamics is sometimes not fully appreciated by the legislative tools which are at the basis of biodiversity conservation (Marris, 2007). Indeed, there is the perception that legislation runs at a considerable lower velocity and, often, creates resistance in terms of taxonomic updates. This could lead to deleterious effects in terms of conservation, particularly for narrow-range species.
In the present paper, we review the peculiar case of the Critically Endangered Aeolian wall lizard (Podarcis raffonei) that highlights the limits of legislative mechanisms' ability to integrate conservation policy in Europe in light of scientific advancements in taxonomy. Since the improvement of taxonomic and evolutionary knowledge is quickly increasing or refining the number and the geographic distribution of recognized species (and genera), it is highly probable that similar considerations may be applied to other taxa and regions.
The Aeolian Lizard: A Taxonomic and a Biogeographic History
Podarcis raffonei (or P. raffoneae as it was also named after some recent nomenclatural discussions) (Figure 1) is endemic to the Aeolian Archipelago (Sicily, Italy). This lizard was first considered to be conspecific with congeneric P. waglerianus or P. siculus, but it has been recognized as a distinct species on the basis of genetical aspects and morphological comparisons (Capula, 1994, 2004). Currently, it survives with just four small isolated populations, and it was assessed as CR (Critically Endangered) by the IUCN Red List because its extent of occurrence is <100 km2, its area of occupancy is <10 km2, its distribution is severely fragmented, and there is continuing decline in the number of individuals (IUCN, 2009). The competition and hybridization with P. siculus, likely introduced in the archipelago by humans, is likely the major threat to its long-term existence.
Figure 1. Podarcis raffonei raffonei from Strombolicchio Island (photograph by D. Salvi) and P. r. alvearioi from Vulcano Island, Aeolian Archipelago (Italy) (photograph by G. F. Ficetola).
The conservation emergency of P. raffonei is also coped with a taxonomic complexity, as witnessed by the occurrence of several phenotypically distinct allopatric populations. In fact, it inhabits one island (Vulcano) and three islets (Figure 2), and each of these populations was originally described as a distinct taxon. The nominal subspecies raffonei was described from the Strombolicchio Islet as Lacerta sicula raffonei by Mertens (1952), alvearioi from the Scoglio Faraglione Islet as Lacerta sicula alvearioi by Mertens (1952), antoninoi from the Vulcano Island as Lacerta wagleriana antoninoi by Mertens (1955), and cucchiarai from the La Canna Islet as Podarcis sicula cucchiarai by Di Palma (1980) (Figures 1, 2).
Figure 2. Distribution of extant populations of Podarcis raffonei in the Aeolian Archipelago (green) and of extinct populations with uncertain taxonomic status (orange).
The population size for P. raffonei is also apparently very small: estimated numbers are of around 500–700 individuals for Strombolicchio Islet, 200–400 individuals from Scoglio Faraglione Islet, while in the diminutive La Canna Islet the population is likely <30 individuals (Capula and Lo Cascio, 2006; Lo Cascio, 2010a). On Vulcano the species is reported to survive in one tiny peninsula only, with perhaps <200 individuals (Lo Cascio, 2010b). Last but not least, the regular observation of hybrids between P. raffonei and P. siculus also suggests that P. raffonei was originally present in most of the Aeolian archipelago (Figure 2), but went extinct in most of the range because of interspecific interactions with P. siculus (Capula, 1993). Currently, the invasive P. siculus is the only lacertid occurring on the large islands of the archipelago (Capula et al., 2002), and ecological competition with exclusion has been demonstrated on Vulcano, where P. siculus is currently widespread and very abundant, whereas P. raffonei was no more found in the historical localities quoted by Mertens (1955) and Capula and Lo Cascio (2006), and is obviously close to extinction.
The Habitats Directive and the Launch of An Urgent Action Plan
The scenario here depicted clearly shows that P. raffonei is one of the most threatened terrestrial vertebrates in Europe. For this, immediate and urgent conservation actions and efficient legislative tools are badly needed and expected. The Habitats Directive (HD) of the European Union (EU) (Council Directive 92/43/EEC), first enacted in 1992, is one of the most powerful legislative tools for conservation in Europe, since it protects >1,200 species and their habitats. The HD lists in its Annex IV both P. siculus and P. waglerianus, which are consequently strictly protected. Until its recognition as a separate species in 1994 P. raffonei was implicitly protected as a subspecies of P. waglerianus. Surprisingly enough, when recognized as a different species, P. raffonei was not explicitly stated and named in the HD. According to the HD, anyhow, when a species is separate from another species and gains taxonomic identity (as it is the case of P. raffonei) it keeps the original conservation status. In other words, P. raffonei since the moment of being recognized as a separate species maintained the legal protection that it had when considered a subspecies of P. waglerianus or P. siculus. The European Commission has long accepted the principle that when a taxon listed on one of the annexes is split as a result of a taxonomic revision, then all the new taxa are also considered as listed (Evans and Arvela, 2011).
Of course, we agree that this is better than nothing, and theoretically warrants a certain degree of protection for P. raffonei, but there are some major constraints facing this situation. First of all, the species is not explicitly reported and visible in the HD. In our opinion this is a great obstacle and heavily hampers organizations and researchers to ask for economical supports for conservation and/or research, simply because P. raffonei is not perceived as a protected species, and even make people believe that it is not protected. Then, the change from supposed subspecies of P. siculus and P. waglerianus showed that the species gained a particular status and rank (from subspecies to species) end stressed its narrow endemicity. Since P. raffonei is declining and present in the Aeolian archipelago only reduced the area of occurrence and extent of occurrence, its Red List status (Critically Endangered) is strongly different from both P. siculus and P. waglerianus. These species are both assessed as Least Concern, and one of them (P. siculus) actually is a very widespread and locally abundant species and is also the main agent of P. raffonei lowering and potential extinction. For this, the inclusion of P. raffonei in the HD can be seen as just a casual consequence of this, and not a tailored action due to its peculiar conservation status. Conversely, we reaffirm that it would be more appropriate explicitly listing P. raffonei in the Annex II of the directive, which ensure conservation measures including habitat protection through the Natura 2000 network.
Furthermore, it must be stressed that, were the taxonomic status of the taxon raffonei not re-evaluated, very little attention would have been paid to the extinction of some other subspecies of a wide-ranging non-threatened species such as P. waglerianus (Gippoliti and Amori, 2007). Currently, the extinction of insular-endemic subspecies occurred several times, without major conservation concerns being raised. This was for instance the case with Podarcis siculus sanctistephani (Mertens, 1926), a subspecies typical of Santo Stefano Islet in the Pontine Archipelago (Latium, Italy). According to Lanza and Corti (1993), by 1954 this taxon was no more found on the islet, where it was replaced by P. s. siculus. Moreover, the case of P. raffonei is not isolate and it can be seen as a remarkable example, since many other palaeoendemic species still remain over-neglected by EU legislation (e.g., Gippoliti and Amori, 2004, 2006).
Considering the available evidence about the main cause of P. raffonei range contraction and the possible complete extinction of the species in Vulcano in a few years, we are in the urgency to act very quickly for assuring its conservation. So far, we strongly support the preparation and application of an action plan including a detailed monitoring program of the species and immediate management actions (Lo Cascio and Ficetola, 2016). The populations of P. raffonei living in the different islands are characterized by genetic and morphological differences, so they need to be managed as distinct Management Units. Moreover, captive breeding programs are to be considered in the recovery plan for the species as complementary tool to preserve as much as possible of the diversity of these lineages (Gippoliti and Capula, 2014). Furthermore, the possibility to eradicate (or at least containing) P. siculus from some islets to allow reintroduction of P. raffonei should also be taken into account. Available evidence with other lizards suggests that release of captive-bred individuals may be a viable and economically feasible option for the Aeolian wall lizard (Santos et al., 2009).
The Habitat Directive and the Fluid Taxonomy
Although, the EU has an advanced environmental policy, the complex political history and structure of the EU produced tools for biodiversity conservation that are not always able to cope with the fluid state of knowledge arising from biodiversity, ecological and evolutionary research (Battisti and Fanelli, 2015). Podarcis lizards are a good example of Mediterranean endemic diversity that is increasingly appreciated thanks to a scientific interest and to the availability of new taxonomic techniques. So far, species lists of the HD need updating and identification of new methods of species selection (Cardoso, 2012; Prie et al., 2012). The HD annexes have been the basis to establish the Natura 2000 Network, a number of conservation sites of European importance to assure the future of biodiversity on the continent. It is evident that if we fail to recognize narrow-range threatened lineages we are unsuccessful in protecting an important part of current biodiversity.
The idea that we have a definitive knowledge of European biodiversity and taxonomy is simply an implicit (but largely erroneous) assumption of European environmental legislation (Dubois, 1998), as we have to recognize today that biodiversity information is still imperfect. An accurate taxonomy reflecting current knowledge on phylogenetic systematic is crucial to indicate conservation priorities and management (Thuiller et al., 2015). In our opinion tools and legislation aimed at conserving biodiversity thus require periodical updates in order to integrate state-of-the-art knowledge from taxonomic research. It is pivotal that scientific organizations, environmental NGO's, and zoos in Europe are guided in the allocation of conservation resources by the most scientifically sound tools now available (as the periodically updated IUCN Red List) and not just by the outdated annexes of the HD, at least until they are carefully amended. In the last years, the annexes were subjected to some updates, for instance when new member states become EU members, or to take into account some taxonomic revisions. However, these updates have not been performed in a regular basis and are still heterogeneous. Nevertheless, the HD requires that, every 6 years, countries shall draw up a report on the conservation status of all the listed species. We believe that such reporting should be accompanied by a regular update of the annexes. Such updates are imperative for the conservation of European biodiversity, and must pay strong attention to taxonomic updates and to species that are identified as threatened or with decreasing conservation status.
Author Contributions
All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Acknowledgments
The authors thank A. Nistri, D. Fontaneto, L. M. Luiselli, and G. Amori for useful discussions on Directive Habitats and P. Lo Cascio for updates about the conservation status of P. raffonei. C. Rondini was much helpful in commenting a first draft of this paper. GF and DS received funding from the Mohamed bin Zayed Species Conservation Fund (Eolizard Project, 162514415). DS is currently supported by the program “Rita Levi Montalcini” for the recruitment of young researchers at the University of L'Aquila.
References
Arnold, E. N. (1989). Towards a phylogeny and biogeography of the Lacertidae: relationships within an Old-World family of lizards derived from morphology. Bulletin of the British Museum (Natural History). Zoology 55, 209–257.
Battisti, C., and Fanelli, G. (2015). Don't think local! Scale in conservation, parochialism, dogmatic bureaucracy and the implementing of the European Directives. J. Nat. Conserv. 24, 24–30. doi: 10.1016/j.jnc.2015.01.005
Capula, M. (1993). Natural hybridization in Podarcis sicula and P. wagleriana (Reptilia: Lacertidae). Biochem. Syst. Ecol. 21, 373–380. doi: 10.1016/0305-1978(93)90028-P
Capula, M. (1994). Genetic variation and differentiation in the lacertid lizard, Podarcis wagleriana (Reptilia: Lacertidae). Biol. J. Linn. Soc. 52, 177–192. doi: 10.1111/j.1095-8312.1994.tb00986.x
Capula, M. (2004). Low genetic variation in a critically endangered Mediterranean lizard: conservation concerns for Podarcis raffonei (Reptilia, Lacertidae). Ital. J. Zool. 1, 161–166. doi: 10.1080/11250003.2004.9525553
Capula, M., and Lo Cascio, P. (2006). “Podarcis raffonei (Mertens, 1953)” in Atlas of Italian Amphibians and Reptiles, eds R. Sindaco, G. Doria, E. Razzetti, and F. Bernini (Firenze: Polistampa), 480–485.
Capula, M., Luiselli, L., Bologna, M. A., and Ceccarelli, A. (2002). The decline of Aeolian wall lizard, Podarcis raffonei: causes and conservation proposals. Oryx 36, 66–72. doi: 10.1017/S0030605302000108
Cardoso, P. (2012). Habitat Directive species lists: urgent need of revision. Insect Conserv. Divers. 5, 169–174. doi: 10.1111/j.1752-4598.2011.00140.x
Corti, C., Capula, M., Luiselli, L., and Sindaco, R. (2011). Reptilia. Fauna d'Italia, Vol. XLV. Bologna: Il Sole 24 ore Edagricole.
Di Palma, M. G. (1980). La Lucertola del Faraglione “La Canna” nelle Isole Eolie: Podarcis sicula cucchiarai subsp. nova (Reptilia, Lacertidae). Nat. Sic. 3–12.
Dubois, A. (1998). Lists of European species of amphibian and reptiles: will we soon be reaching “stability”? Amphib. Reptil. 19, 1–28. doi: 10.1163/156853898X00304
Evans, D., and Arvela, M. (2011). Assessment and Reporting under Article 17 of the Habitats Directive - Explanatory Notes & Guidelines for the Period 2007–2012. Final version, July 2011. Paris: European Topic Centre on Biological Diversity.
Gippoliti, S., and Amori, G. (2004). Mediterranean Island mammals: are they a priority for biodiversity conservation? Biogeographica 25, 135–144. doi: 10.21426/B6110135
Gippoliti, S., and Amori, G. (2006). Ancient introductions of mammals in the Mediterranean Basin and their implications for conservation. Mamm. Rev. 36, 37–48. doi: 10.1111/j.1365-2907.2006.00081.x
Gippoliti, S., and Amori, G. (2007). The problem of subspecies and conservation lists: the case of mammals. Folia Zool. 56, 113–117.
Gippoliti, S., and Capula, M. (2014). Local biodiversity and European zoos. Does it matter? Italy as a case study. Intern. Zool. News 61, 117–125.
Lanza, B., and Corti, C. (1993). Erpetofauna italiana: “acquisizioni” ed estinzioni nel corso del Novecento. Suppl. Ric. Biol. Selvaggina 21, 5–49.
Lo Cascio, P. (2010a). Attuali conoscenze e misure di conservazione per le popolazioni relitte dell'endemica lucertola delle Eolie, Podarcis raffonei (Squamata Sauria). Nat. Sic. 34, 295–317.
Lo Cascio, P. (2010b). Aspetti ecologici e problemi di conservazione di una popolazione di Podarcis raffonei (Mertens, 1952) (Reptilia: Lacertidae). Nat. Sic. 30, 495–521.
Lo Cascio, P., and Ficetola, G. F. (2016). “Podarcis raffoneae (Mertens, 1952) (Lucertola delle Eolie),” in Manuali per il Monitoraggio di Specie e Habitat di Interesse Comunitario (Direttiva 92/43/CEE) in Italia: Specie Animali, eds F. Stoch and P. Genovesi (Rome: ISPRA), 280–281.
Lomolino, M. V. (2005). Body size evolution in insular vertebrates: generality of the island rule. J. Biogr. 32, 1683–1699. doi: 10.1111/j.1365-2699.2005.01314.x
Mertens, R. (1955). Die Mauereidechsen der Liparischen Inseln, gesammelt von Dr. Antonino Trischitta. Senckenb. Biol. 36, 25–40.
Prie, V., Puillandre, N., and Bouchet, P. (2012). Bad taxonomy can kill: molecular reevaluation of Unio mancus Lamarck, 1819 (Bivalvia: Unionidae) and its accepted subspecies. Knowl. Manage. Aquat. Ecosyst. 405, 08p1–08p18. doi: 10.1051/kmae/2012014
Santos, T., Pérez-tris, J., Carbonell, R., Tellería, J. L., and Díaz, J. A. (2009). Monitoring the performance of wild-born and introduced lizards in a fragmented landscape: implications for ex-situ conservation programmes. Biol. Conserv. 142, 2923–2930. doi: 10.1016/j.biocon.2009.07.017
Thuiller, W., Maiorano, L., Mazel, F., Guilhaumon, F., Ficetola, G. F., Lavergne, S., et al. (2015). Conserving the functional and phylogenetic trees of life of European tetrapods. Philos. Trans. R. Soc. B 370:20140005. doi: 10.1098/rstb.2014.0005
Keywords: Podarcis raffonei, habitat directive, legislation, conservation, taxonomy
Citation: Gippoliti S, Capula M, Ficetola GF, Salvi D and Andreone F (2017) Threatened by Legislative Conservationism? The Case of the Critically Endangered Aeolian Lizard. Front. Ecol. Evol. 5:130. doi: 10.3389/fevo.2017.00130
Received: 28 July 2017; Accepted: 05 October 2017;
Published: 20 October 2017.
Edited by:
David Jack Coates, Department of Parks and Wildlife, AustraliaReviewed by:
Stéphane Aulagnier, Université Toulouse III Paul Sabatier, FranceViorel Dan Popescu, Ohio University, United States
Copyright © 2017 Gippoliti, Capula, Ficetola, Salvi and Andreone. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Franco Andreone, franco.andreone@regione.piemonte.it; franco.andreone@gmail.com