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THE FIRST RECORD OF THE NORTH AMERICAN FRESHWATER LIMPET FERRISSIA CALIFORNICA (MOLLUSCA, GASTROPODA) IN MOROCCO
Youness Mabrouki1 , Peter Gloer2 , Abdelkhaleq F. Taybi3
1Sidi Mohamed Ben Abdellah University, Morocco e-mail: younes_mab@hotmail.fr 2Biodiversity Research Laboratory, Germany e-mail: gloeer@malaco.de 3Mohammed First University, Morocco e-mail: taybiaf@gmail.com
Received: 05.06.2022. Revised: 13.09.2022. Accepted: 17.09.2022.
Invasive species are a major threat to global biodiversity. One of the most effective invaders among freshwater snails is the North American ancyline gastropod Ferrissia californica (= fragilis). A new population of this species has been found in Lake Zerrouka (Northern Morocco), a Protected Area, which is also a site of ecological and biological interest (known as SIBE). Thus, this record expands the known distribution range of this invasive species in the Mediterranean area. Despite the fact it is located in only one out of more than 150 localities sampled by us, ongoing investigations could soon reveal more finds of the species in Morocco. Lake Zerrouka is known for recently described endemic snail species, i.e. Ifrania zerroukansis and Gyraulus marocana. Therefore, the monitoring of the presence and expansion of F. californica within invaded areas, as well as studies improving the knowledge on its biology and ecology is an urgent need.
Key words: alien ancyline, aquarium trade, invasive species, Lake Zerrouka, new arrival, non-native Planorbi-dae, Protected Area
Introduction
Invasions by non-native species are significant threats to the global biodiversity and ecosystem functioning worldwide (Taylor et al., 2006; Gonzalez et al., 2008). They threaten the survival of autochthonous species, populations, and communities through hybridisation, competition, parasitism, predation, and the structural changes they cause to the colonised habitats (Simberloff et al., 2013; Marrone & Naselli-Flo-res, 2015). Freshwater environments being particularly vulnerable to this phenomenon are considered the most invaded and threatened ecosystem worldwide, with proportionally more invaders than terrestrial ecosystems (Vitousek et al., 1997; Pysek et al., 2010; Strayer, 2010). Moreover, the negative impacts of invaders on native species appear to be more frequent in freshwater ecosystems than in marine ones (Ricciardi & Kipp, 2008; Ricciardi & Maclsaac, 2011). In addition, aquatic invasive species are frequently involved in economic damages and can affect the human health (Pimentel et al., 2005; Keller et al., 2011).
Within the class of Gastropoda, many species have been considered as invasive in freshwater ecosystems, such as the New Zealand mudsnail Potamopyrgus antipodarum (J.E. Gray, 1843), the
apple snail Pomacea canaliculata (Lamarck,1828) (Estebenet & Martin, 2002; Karatayev et al., 2009), and the American limpet Ferrissia californica (Rowell, 1863). The native range of F. californica lies in North America, where it is widespread throughout the United States up to southern Canada. During several decades, it has widely invaded Europe, Asia, South America, Africa and Oceania (Brown, 1965; Lacerda et al., 2015; Vecchioni et al., 2017; Vinarski & Palatov, 2018; Coote et al., 2018; Gloer, 2019). In the neighbouring countries of North Africa, Ferrissia californica has been recorded in Tunisia (Khalloufi & Boumaiza, 2007) and recently in Algeria (Gloer & Ramdini, 2019).
The aim of this paper was to provide the first record of F. californica from Morocco, in Lake Zerrouka, a Protected Area, also recognised as a site of ecological and biological interest, located in the Middle Atlas Mountains, a geographical barrier known as a habitat of endemic molluscs.
Material and Methods
Sampling area
In order to promote knowledge on the malaco-fauna of Morocco, several field expeditions have
been conducted since 2014 in the northern part of Morocco, with a focus on Protected Areas, especially on great geographical barriers as the Middle Atlas Mountains. More than 150 localities have been investigated and most of these sampling sites were visited at least three times.
The Zerrouka Lake is a Protected Area located in the province of Ifrane in the heart of the Middle Atlas at an altitude of 1613 m a.s.l., considered a site of Biological and Ecological Interest (SIBE) (https://ma.chm-cbd. net/ manag_cons/esp_prot/sibe_ma/sibe_cont_hum/ plan-d-eau-zerrouka-i-h16/sibe_h16) by the Moroccan government. This area is an integral part of the Oued Tizguite Wetland, of which the River Zerrouka is a tributary, classified as a Ramsar Site from 22.05.2019 (for more details, see Mabrouki et al., 2022).
Fieldwork and laboratory processing
The samples of benthic fauna (including gastropods) were collected by a kick net and clamps during 2014-2022. The samples have been fixed in 75% ethanol. Photographs were made with a Leica M205C Microscope with a digital camera Leica DMC5400. The voucher specimens are deposited in the authors' collections. Conductivity, pH, and dissolved oxygen were measured in situ with a multiparametric measuring device (WTW, Multi-Line P4). The other parameters (ammonium and biological oxygen demand) were measured in the laboratory. The distribution map of F. californica in the West Palearctic was performed according to Gloer (2019).
Results
The first Moroccan records of the North American freshwater limpet Ferrissia californi-ca is a sample including about twenty individuals collected in Lake Zerrouka (33.5437157° N, 05.095078° W) in 14.02.2020, 24.10.2021, and 06.03.2022 (Fig 1, Fig. 2). The site is situated in the River Sebou basin near the city of Ifran. The
analysis of the physicochemical parameters of the water, such as ammonium and biological oxygen demand, revealed a good environmental quality of the habitat (Table 1), according to the Moroccan surface water guidelines of good to excellent quality (MSWG).
The individuals of Ferrissia californica were found attached to the submerged aquatic vegetation present in Lake Zerrouka. It consists of Myriophyl-lum spicatum L., Ranunculus aquatilis L., Persicaria amphibia (L.) Delarbre, Potamogeton spp., Elodea sp., and Ceratophyllum sp., sometimes attached to submerged parts of Typha latifolia L. The bottom substrate consists of sand, slit and mud. The density of F. californica ranged between 5-7 individuals per 0.5 m2.
0°0'0" 30°0'0"E 60°0'0"E
Zerrouka (Morocco).
Fig. 2. Fixed specimens of Ferrissia californica found in Lake Zerrouka (Morocco). Designations: A - dorsal view, B - lateral right view, C - lateral left view.
Table 1. The mean and limit values of Moroccan surface water guidelines of good to excellent quality, minimum and maximum values of the physical and chemical water parameters measured at the sampling locality (Lake Zerrouka, Morocco)
Parameter pH Conductivity, mg/l Dissolved oxygen, mg/l Ammonium, mg/l BOD5, mg/l
M 7.5 150 10 0.05 1.5
MSWG 6.5-8.5 100-1300 > 7-5 < 0.1-0.5 < 3-5
min 7.0 125 9.5 0.03 1
max 8.0 170 10.5 0.1 3
Note: M - mean, MSWG - Moroccan surface water guidelines of good quality, min - minimum value, max - Maximum value, BOD5 -Biological oxygen demand.
Discussion
Freshwater molluscs disperse over short or long distances, various vectors, such as current of streams and rivers during floods, birds and animals or boats and ships, in addition to aquarium trades (Alexandro-wicz, 2003). The invasion pathways ofF. californica in Morocco are unknown. However, it has been verified that the aquarium trade is the main responsible for the establishment of this invasive species into non-native areas (Boettger, 1949; Tokinova, 2012; Vecchioni et al., 2017). Ornamental aquarium pet trade starts to become a leading pathway for the introduction of aquatic invasive species in Morocco (Mabrouki et al., 2020; Taybi et al., 2020a, 2021, 2023). Perhaps, aquarists from the surrounding cities (i.e. Ifran) are behind this introduction of F. californica in Morocco, too.
The species seems to require good water quality such as the water of Lake Zerrouka (Barakat et al., 2016; Taybi et al., 2020b). The number of the collected F. californica individuals was relatively low in this first study. This suggests that the invasion could be at its initial stage, as also observed for introduction of Physa acuta (Draparnaud, 1805) in Ilha Grande (Miyahira et al., 2021). It is expected that the species range will increase exponentially across Morocco as has happened in Europe (Gloer, 2019).
Migratory water birds, abundant in Lake Zerrou-ka (personal observations), like members of families Anatidae and Rallidae have also been suggested as a potential invasion vector for F. californica (Raposeiro et al., 2011). Waterfowl may be the main vectors for inland spread in Morocco and North Africa, since many routes of bird migration between Europe and Africa cross the Iberian Peninsula and Morocco (Pérez-Tris & Santos, 2004; Alonso et al., 2019), as it might have happened with Potamopyrgus antipodarum, which is also present in Morocco (Taybi et al., 2021). Lake Zer-rouka is a nesting site for several aquatic birds including members of Anatidae (Anas ferina Linnaeus, 1758, A. fuligula Linnaeus, 1758, and A. nyroca Guldenstad, 1770) and Rallidae (Fulica cristata Gmelin, 1789, F. atra Linnaeus, 1758) (Chillasse et al., 2001).
Ferrissia californica has now a near-cosmopolitan distribution owing to multiple capacities of this snail. It is a eurybiontic species and is capable of adaptation to tolerating a wide range of various habitat types (Dillon & Herman, 2009). The high abundance of F. californica has been discovered recently, living even in parts of the cave habitats differing by light regime. This indicates that the species has established a stable underground population able to reproduce (Vinarski & Palatov, 2018). Once arriving in new environments, the success
key for establishment of this hermaphroditic gastropod might be the capacity for self-fertilisation (Raposeiro et al., 2011; Vecchioni et al., 2017) in addition to its small body size and the ability to live in stagnant water (Walther et al., 2006).
No clear data are currently available on the possible impact of F. californica on native molluscan communities, and especially those, which have similar ecological niches, such as the autochthonous Ancy-lus sp., with which the species often co-exists in the invaded areas (Marrone et al., 2011). In addition to the newly discovered F. californica, Lake Zerrouka is a home for endemic freshwater snails, which been recently described, namely Gyraulus marocana Mabrouki, Gloer & Taybi 2022 (Planorbidae), and Ifra-nia zerroukansis Gloer, Mabrouki & Taybi 2020 (Hy-drobiidae) known only from their type locality (Gloer et al., 2020; Mabrouki et al., 2022).
Conclusions
This paper reports the first finding of an acclimated population of F. californica in Morocco. The species seems to be at the initial stage invasion, by requiring good quality of water such as that in the invaded area of Lake Zerrouka. Despite the fact it is located in only one out of more than 150 localities sampled by the authors, the on-going investigations can soon reveal more finds of this species in the country and on the rest of the continent.
The trade of exotic species appears as a major source favouring the invasion in Moroccan freshwater habitats by non-native species. Strict law enforcement policies and procedures must be established in the trade of aquatic species as a preventive measure to preserve the native biodiversity.
Being located in the Middle Atlas Mountains, which is a geographical barrier, known as a habitat of endemic molluscs, Lake Zerrouka has a major importance for conservation of the autochthonous aquatic biodiversity. This requires urgent actions to prevent its unique biota from potential alteration and to prevent extinctions of native species. The realisation of careful monitoring programmes throughout the invasive range of F. californica is thus advisable.
Acknowledgements
We thank the editor and reviewers, whose helpful comments have improved the present paper.
References
Alexandrowicz S.W. 2003. Planorbella duryi (Wetherby, 1879) from the crater-lake Albano (Central Italy). Folia Mala-cologica 11(3-4): 89-93. DOI: 10.12657/folmal.011.009
Alonso А., Castro-Díez P., Saldaña-López A., Gallardo B. 2019. The New Zealand mud snail Potamopyrgus antipodarum (J.E. Gray, 1853) (Tateidae, Mollusca) in the Iberian Peninsula: temporal patterns of distribution. BioInvasions Records 8(2): 287-300. DOI: 10.3391/bir.2019.8.2.11 Barakat A., El Baghdadi M., Rais J., Aghezzaf B., Slassib M. 2016. Assessment of spatial and seasonal water quality variation of Oum Er Rbia River (Morocco) using multivariate statistical techniques. International Soil and Water Conservation Research 4(4): 284-292. DOI: 10.1016/j.iswcr.2016.11.002 Boettger C.R. 1949. Die Einschleppung Einer Nordamerikanischen Sußwasserschnecke der Gattung Ferrissia nach Deutschland. Archiv fur Molluskenkunde 78: 187. Brown D.S. 1965. Freshwater gastropod Mollusca from Ethiopia. Bulletin of British Museum Natural History. Zoology 12: 37-94. Chillasse L., Dakki M., Abbassi M. 2001. Valeurs et fonctions écologiques des Zones humides du Moyen Atlas (Maroc). Humedales Mediterráneos 1: 139-146. Coote T., Schmidt K.A., Schmidt R.E., McMullin E.R. 2018. Discovery of the freshwater limpet, Ferrissia californica (Rowell, 1863) (Gastropoda: Planorbidae), from the streams of Montserrat, West Indies, a new addition to the Caribbean fauna. American Malacological Bulletin 36(2): 291-295. DOI: 10.4003/006.036.0208 Dillon R.T.Jr., Herman J.J. 2009. Genetics, Shell Morphology, and Life History of the Freshwater Pulmonate Limpets Ferrissia rivularis and Ferrissia fragilis. Journal of Freshwater Ecology 24(2): 261-271. DOI: 10.1080/02705060.2009.9664291 Estebenet A.L., Martín P.R. 2002. Pomacea canaliculata (Gastropoda: Ampullariidae): life-history Traits and their Plasticity. Biocell 26(1): 83-89. Glöer P., Mabrouki Y., Taybi A.F. 2020. Two new valvatoid genera (Gastropoda, Hydrobiidae) from Morocco. Ecologica Montenegrina 30: 124-128. DOI: 10.37828/em.2020.30.12 Glöer P. 2019. The freshwater gastropods of the West Palaearc-tic. Vol. 1: Fresh- and brackish waters except spring and subterranean snails. Identification Key, Anatomy, Ecology, Distribution. Hetlingen: Biodiversity Research Lab. 399 p. Glöer P., Ramdini R. 2019. Hippeutis complanatus Linnaeus, 1758 in Algeria, re-found after more than 150 years. Ecologica Montenegrina 22: 226-227. Gonzalez A., Lambert A., Ricciardi A. 2008. When does ecosystem engineering cause invasion and species replacement?. Oikos 117(8): 1247-1257. DOI: 10.1111/j.0030-1299.2008.16419.x Karatayev A.Y., Burlakova L.E., Padilla D.K., Mastitsky S.E., Olenin S. 2009. Invaders are not a random selection of species. Biological Invasions 11(9): 2009. DOI: 10.1007/s10530-009-9498-0 Khalloufi N., Boumaiza M. 2007. Première citation et description de quatre pulmonés dulcicoles de Tunisie (Mollusca, Orthogastropoda). Bulletin De La Société Zoologique De France 132: 191-204. Keller R.P., Geist J., Jeschke J.M., Kühn I. 2011. Invasive species in Europe: ecology, status, and policy. Environmental Sciences Europe 23: 23. DOI: 10.1186/2190-4715-23-23
Lacerda L.E.M., Richau C.S., Amaral C.R., Silva D.A., Car-valho E.F., Santos S.B. 2015. Ferrissia fragilis (Tryon, 1863): a freshwater snail cryptic invader in Brazil revealed by morphological and molecular data. Aquatic Invasions 10(2): 157-168. Mabrouki Y., Taybi A.F., Bahhou J., Doadrio I. 2020. The first record of the swordtail Xiphophorus hellerii Heck-el, 1848 (Poeciliidae, Actinopterygii) established in the wild from Morocco. Journal of Applied Ichthyology 36(6): 795-800. DOI: 10.1111/jai.14105 Mabrouki Y., Gloer P., Taybi A.F. 2022. Gyraulus marocana sp. nov., a new freshwater snail species (Mollusca, Gastropoda, Planorbidae) from Morocco. Nature Conservation Research 7(1): 96-100. DOI: 10.24189/ncr.2022.007 Marrone F., Naselli-Flores L. 2015. A review on the animal xenodiversity in Sicilian inland waters (Italy). Advances in Oceanography and Limnology 6(1-2): 2-12. DOI: 10.4081/aiol.2015.5451 Marrone F., Lo Brutto S., Arculeo M. 2011 Cryptic invasion in Southern Europe: The case of Ferrissia fragilis (Pul-monata: Ancylidae) Mediterranean populations. Biologia 66(3): 484-490. DOI: 10.2478/s11756-011-0044-z Miyahira I.C., Gongalves I.C.B., Lacerda L.E.M., Ximenes R.F., Santos S.B. 2021. The introduction of Physa acuta (Gastropoda: Physidae) on Ilha Grande, Southeast Brazil, from initial stages to an established population. Brazilian Journal of Biology 83: e243801. DOI: 10.1590/1519-6984.243801 Pérez-Tris J., Santos T. 2004. Spanish research on avian migration: historical trajectory and future perspectives. Ardeola 51(1): 71-89. Pimentel D., Zuniga R., Morrison D. 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52(3): 273-288. DOI: 10.1016/j.ecolecon.2004.10.002 Pysek P., Bacher S., ChytryfM., Jarosík V., Wild J., Celes-ti-Grapow L., Gassó N., Kenis M., Lambdon P.W., Nentwig W., Pergl J., Roques A., Sádlo J., Solarz W., Vilá M., Hulme P.E. 2010. Contrasting patterns in the invasions of European terrestrial and freshwater habitats by alien plants, insects and vertebrates. Global Ecology and Biogeography 19(3): 317-331. DOI: 10.1111/j.1466-8238.2009.00514.x Raposeiro P.M., Costa A.C., Martins A.F. 2011. On the presence, distribution and habitat ofthe alien freshwater snail Ferrissia fragilis (Tryon, 1863) (Gastropoda: Planorbidae) in the oceanic islands of the Azores. Aquatic Invasions 6(1): 13-17. DOI: 10.3391/ai.2011.6.S1.003 Ricciardi A., Kipp R. 2008. Predicting the number of ecologically harmful exotic species in an aquatic system. Diversity and Distributions 14(2): 374-380. DOI: 10.1111/j.1472-4642.2007.00451.x Ricciardi A., MacIsaac H.J. 2011. Impacts of Biological Invasions on Freshwater Ecosystems. In: D.M. Richardson (Ed.): Fifty Years of Invasion Ecology: The Legacy of Charles Elton. New Jersey: Wiley-Blackwell. P. 211224. DOI: 10.1002/9781444329988.ch16 Simberloff D., Martin J.L., Genovesi P., Maris V., Wardle D.A., Aronson J., Courchamp F., Galil B., García-Berthou E.,
Pascal M., Pysek P., Sousa R., Tabacchi E., Vilá M. 2013. Impacts of biological invasions: what's what and the way forward. Trends in Ecology and Evolution 28(1): 58-66. DOI: 10.1016/j.tree.2012.07.013 Strayer D.L. 2010. Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biology 55(s1): 152-174. DOI: 10.1111/j.1365-2427.2009.02380.x Taybi A.F., Mabrouki Y., Doadrio I. 2020a. The occurrence, distribution and biology of invasive fish species in fresh and brackish water bodies of NE Morocco. Arxius de Miscellania Zoológica 18: 59-73. DOI: 10.32800/ amz.2020.18.0059 Taybi A.F., Mabrouki Y., Legssyer B., Berrahou A. 2020b. Spatio-temporal typology of the physico-chemical parameters of a large North African river: the Mou-louya and its main tributaries (Morocco). African Journal of Aquatic Sciences 45(4): 431-441. DOI: 10.2989/16085914.2020.1727832 Taybi A.F., Mabrouki Y., Gloer P. 2021. First record of the New Zealand Mudsnail Potamopyrgus antipodarum (J.E. Gray, 1843) (Tateidae, Mollusca) in Africa. Graell-sia 77(2): e140. DOI: 10.3989/graellsia.2021.v77.303 Taybi A.F., Mabrouki Y., Gloer P. 2023. First record of the exotic Seminole rams-horn Helisoma duryi (Wetherby, 1879), (Gastropoda: Planorbidae) in Morocco. Graell-sia 79(1). In print.
Taylor B.W., Flecker A.S., Hall R.O. 2006. Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 313(5788): 833-836. DOI: 10.1126/science.1128223 Tokinova R.P. 2012. The First Finding of the North American Freshwater Limpets Ferrissia fragilis (Tryon, 1863) (Mollusca, Gastropoda) in the Middle Volga Basin. Russian Journal of Biological Invasions 3(1): 52-55. DOI: 10.1134/S2075111712010134 Vecchioni L., Marrone F., Arculeo M., Arizza V. 2017. Are there autochthonous Ferrissia (Mollusca: Planorbidae) in the Palaearctic? Molecular evidence of a widespread North American invasion of the Old World. European Zoological Journal 84(1): 411-419. DOI: 10.1080/24750263.2017.1350759 Vinarski M.V., Palatov D.M. 2018. Ferrissia californica (Gastropoda: Planorbidae): the first record of a global invader in a cave habitat. Journal of Natural History 52(17-18): 1147-1155. DOI: 10.1080/00222933.2018.1450904 Vitousek P.M., D'Antonio C.M., Loope L., Rejmanek M., Westbrooks R.G. 1997. Introduced species: a significant component of human-caused global change. New Zealand Journal of Ecology 21: 1-16. Walther A.C., Lee T., Burch J.B., Foighil D.O. 2006. Confirmation that the North American ancylid Ferrissia fragilis (Tryon, 1863) is a cryptic invader of European and East Asian freshwater ecosystems. Journal of Mollus-can Studies 72: 318-321. DOI: 10.1093/mollus/eyl009
ПЕРВАЯ НАХОДКА СЕВЕРОАМЕРИКАНСКОГО ПРЕСНОВОДНОГО БЛЮДЕЧКА FERRISSIA CALIFORNICA (MOLLUSCA, GASTROPODA) В МАРОККО
Ю. Мабруки1 , П. Глёэр2 , А. Ф. Тайби3
Университет Сиди Мохамеда бен Абдаллы, Марокко e-mail: younes_mab@hotmail.fr 2Лаборатория исследования биоразнообразия, Германия e-mail: gloeer@malaco.de 3Первый университет Мохаммеда, Марокко e-mail: taybiaf@gmail.com
Инвазионные виды представляют серьезную угрозу глобальному биоразнообразию. Среди пресноводных улиток одним из наиболее активных инвайдеров является североамериканский вид анцилин Ferrissia californica (= fragilis). Новая популяция этого вида была обнаружена в оз. Зерроука (север Марокко), на особо охраняемой природной территории, которая также является областью экологического и биологического интереса (известной как SIBE). Таким образом, эта находка расширяет известный ареал этого инвазионного вида в Средиземноморье. Несмотря на то, что находка сделана только в одном из более чем 150 изученных авторами локалитетов, текущие исследования могут вскоре выявить больше находок этого вида в Марокко. Для оз. Зерроука известны описанные эндемичные виды улиток, Ifrania zerroukansis и Gyraulus marocana. Поэтому мониторинг распространения F. californica в пределах инвазионного ареала, а также исследования, пополняющие знания о биологии и экологии вида являются насущной необходимостью.
Ключевые слова: инвазионный вид, новый занос, озеро Зерроука, особо охраняемая природная территория, торговля аквариумными организмами, чужеземная анцилина, чужеземные Planorbidae
