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First Data on the Helminth Community of the Smallest Living Mammal on Earth, the Etruscan Pygmy Shrew, Suncus Etruscus (Savi, 1822) (Eulipotyphla: Soricidae)

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First Data on the Helminth Community of the Smallest Living Mammal on Earth, the Etruscan Pygmy Shrew, Suncus Etruscus (Savi, 1822) (Eulipotyphla: Soricidae) animals Article First Data on the Helminth Community of the Smallest Living Mammal on Earth, the Etruscan Pygmy Shrew, Suncus etruscus (Savi, 1822) (Eulipotyphla: Soricidae) María Teresa Galán-Puchades 1,* , Santiago Mas-Coma 2, María Adela Valero 2 and Màrius V. Fuentes 1 1 Parasite and Health Research Group, Department of Pharmacy and Pharmaceutical Technology and Parasitology, Faculty of Pharmacy, University of Valencia, 46100 Burjassot, Valencia, Spain; [email protected] 2 Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, 46100 Burjassot, Valencia, Spain; [email protected] (S.M.-C.); [email protected] (M.A.V.) * Correspondence: [email protected] Simple Summary: The Etruscan shrew, Suncus etruscus, is the smallest living mammal on Earth. Its minute size (most adults weigh 1.8–3 g with a body length of 35–48 mm) makes it extremely difficult to catch in small mammal traps. The French scientist Dr Roger Fons (1946–2016) developed a particular trapping method which allowed him to assemble the largest collection of S. etruscus in the world. We had the unique opportunity of studying, for the first time, the helminth community of a total of 166 individuals of the Etruscan shrew. We found six cestode species, specifically, two extraintestinal larvae, and four intestinal adult tapeworms, as well as one adult nematode species in the stomach and several nematode larvae. Neither trematode nor acanthocephalan species were Citation: Galán-Puchades, M.T.; detected. Approximately 50% of the individuals harbored tapeworms presenting a two-host life Mas-Coma, S.; Valero, M.A.; Fuentes, cycle with arthropods as intermediate hosts, a fact that is consistent with its insectivorous diet. The M.V. First Data on the Helminth adult helminth community found is highly specific of this shrew whose numerous physiological Community of the Smallest Living adaptations due to its small size have probably influenced its helminth spectrum as well as its Mammal on Earth, the Etruscan helminth specificity. Pygmy Shrew, Suncus etruscus (Savi, 1822) (Eulipotyphla: Soricidae). Abstract: Suncus etruscus is the smallest living mammal on Earth by mass. Most adults weigh 1.8–3 g Animals 2021, 11, 2074. https:// with a body length of 35–48 mm. Catching it in small mammal traps in nature is extremely difficult doi.org/10.3390/ani11072074 due to its minute size, and therefore special trapping methods must be used. We had the unique Academic Editor: Stefania Perrucci opportunity of studying, for the first time, the helminth parasites of 166 individuals of S. etruscus, part of the largest collection in the world, which belonged to the French scientist Dr Roger Fons Received: 15 June 2021 (1942–2016). A total of 150 individuals were captured in the Banyuls-Cerbère area (France) and Accepted: 9 July 2021 16 in the island of Corsica (France). We found seven helminth species, specifically, the cestodes Published: 12 July 2021 Joyeuxiella pasqualei larvae, Mesocestoides sp. larvae, Staphylocystis claudevaucheri, S. banyulsensis, S. cerberensis, and Pseudhymenolepis sp., and the nematodes Aonchotheca sp. and Nematoda gen. sp. larvae. Publisher’s Note: MDPI stays neutral Neither trematodes nor acanthocephalans were detected. We provide prevalences, infracommunity with regard to jurisdictional claims in compositions, and helminth associations. The adult helminth community of S. etruscus seems to be published maps and institutional affil- highly specific, i.e., oioxenous, and linked to its insectivore diet. Due to its small size, S. etruscus has iations. undergone numerous physiological adaptations that have probably influenced its helminth spectrum as well as its helminth specificity. Keywords: Suncus etruscus; Mesocestoides sp. larvae; Joyeuxiella pasqualei larvae; Staphylocystis claude- Copyright: © 2021 by the authors. vaucheri; S. cerberensis; S. banyulsensis; Pseudhymenolepis sp.; Aonchotheca sp.; helminth community Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons 1. Introduction Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ Suncus etruscus, the Etruscan shrew, also known as the Etruscan pygmy shrew, the 4.0/). Pygmy white-toothed shrew, or the Savi’s pygmy shrew, is, by mass, the smallest living Animals 2021, 11, 2074. https://doi.org/10.3390/ani11072074 https://www.mdpi.com/journal/animals Animals 2021, 11, x 2 of 19 Animals 2021, 11, 2074 1. Introduction 2 of 18 Suncus etruscus, the Etruscan shrew, also known as the Etruscan pygmy shrew, the Pygmy white-toothed shrew, or the Savi’s pygmy shrew, is, by mass, the smallest living mammalmammal on Earth. on Earth. Most Most adults adults weigh weigh 1.8–3 1.8–3 g with g with a body a body length length of 35–48 of 35–48 mm, mm, being being 20 times20 lighter times lighter than the than average the average adult adult mouse mouse [1] [(Figure1] (Figure 1).1 ).This This miniscule miniscule mammal mammal speciesspecies is widespreadis widespread throughout throughout Southern Southern Euro Europe,pe, Northern Northern Africa, Africa, and and Central Central Asia. Suncus etruscusetruscus has hasindeed indeed one one of ofthe the largest largest distribution distribution ranges ranges among among insectivore insectivore mammals encompassingencompassing the territory the territory from from the Iberian the Iberian Peninsula Peninsula to Kalimantan to Kalimantan (Borneo) (Borneo) Island Island (In- donesia),(Indonesia), where where they occupy they occupy abandoned abandoned oliv olivee groves groves and and vineyards vineyards with with old old dry dry stone wallswalls and andstone-piles stone-piles as well as well as low as lowmaquis maquis shrubs shrubs and andMediterranean Mediterranean oak oakand andpine pine for- ests forests[2]. Recently, [2]. Recently, the Etruscan the Etruscan shrew shrew has also has alsobeen been detected detected in Russia in Russia [3]. [ 3]. (a) (b) FigureFigure 1. Suncus 1. Suncus etruscus etruscus: (a):( Comparativea) Comparative size size of ofthe the smallest smallest living living mammal mammal on on Earth Earth (illustration (illustration by Angelaby Angela Debenedetti, Debenedetti, PhD); PhD); (b) (Anb) Anindividual individual of ofthe the Etruscan Etruscan shrew shrew ingesting ingesting a a yellow yellow mealworm mealworm (Tenebrio(Tenebrio molitor molitor) larva) larva (R. (R.Fons Fons photo photo collection). collection). DespiteDespite its large its large geographical geographical distribution, distribution, on onlyly a asmall small number number of of individuals individuals of this speciesspecies have have been been caught caught in inthe the world, world, since since catching catching S. etruscusetruscusin in small small mammal mammal traps traps in in naturenature is is extremely extremely difficult difficult due to itsits minuteminute size, size, and and therefore therefore special special trapping trapping methods meth- ods must bebe used.used. InIn fact,fact, its its existence existence was was only only known known thanks thanks to to the the findings findings of itsof predatorits pred- ator(the (the barn barn owl owlTyto Tyto alba alba) pellets) pellets [4]. [4]. Roger Fons (1942–2016), Directeur de Recherche at the French CNRS (Centre National Roger Fons (1942–2016), Directeur de Recherche at the French CNRS (Centre Na- de la Recherche Scientifique), was the only specialist of the Etruscan pygmy shrew in tional de la Recherche Scientifique), was the only specialist of the Etruscan pygmy shrew the world, carrying out his scientific activity at Laboratoire Arago (University Pierre et in the world, carrying out his scientific activity at Laboratoire Arago (University Pierre et Marie Curie, Paris VI, Banyuls-sur Mer, France). He published numerous scientific articles Mariedealing Curie, with ParisS. VI, etruscus, Banyuls-suras for Mer, instance France). those He concerning published trapping numerous and scientific breeding articles meth- dealingods [with4,5], morphologyS. etruscus, as [6 for–11 ],instance evolution those and concerning systematics trapping [12], biology/ecology and breeding[5 ,methods6,13–17], [4,5],ethology morphology [14,18 –[6–11],20], and evolution physiology and [14 ,21systematics–30], among [12], others. biology/ecology [5,6,13–17], ethologyDue [14,18–20], to our, not and only physiology scientific [14,21–30], collaboration, among but also others. friendship with Dr Fons, we had theDue unique to our, opportunity not only scientific of studying, collaboration, for the first but time, also the friendship helminth parasiteswith Dr Fons, of S. etruscuswe had, the uniquesince he opportunity owned the largestof studying, collection for the of thisfirst shrew time, inthe the helminth world. parasites In fact, in of the S. 1980s etruscus we, sincejointly he owned published the largest the finding collection of three of new this intestinal shrew in cestodes, the world. namely In fact, the hymenolepididsin the 1980s we jointlyHymenolepis published claudevaucheri the finding of[31 three], H. cerberensisnew intestinal[32], andcestodes,H. banyulsensis namely the[33 hymenolepidids]. HymenolepisIn addition claudevaucheri to the three [31], new H. cerberensis tapeworm [32], species, and we H. found banyulsensis some other [33]. helminths in the studiedIn addition individuals. to the three Herein, new we presenttapeworm the firstspecies, data we on thefound global some helminth other communityhelminths ofin the studiedthe Etruscan individuals.
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