diversity Article An Alien Invader is the Cause of Homogenization in the Recipient Ecosystem: A Simulation-Like Approach Carla Morri 1,* , Monica Montefalcone 1, Giulia Gatti 2, Paolo Vassallo 1 , Chiara Paoli 1 and Carlo Nike Bianchi 1 1 DiSTAV (Department of Earth, Environmental and Life Sciences), University of Genoa, 16132 Genova, Italy 2 Mediterranean Institute of Biodiversity and marine and continental Ecology, CNRS, Station Marine d’Endoume, 13007 Marseille, France * Correspondence: [email protected] Received: 6 July 2019; Accepted: 23 August 2019; Published: 26 August 2019 Abstract: Biotic homogenization is an expected effect of biological invasions. Invasive alien species typically show great adaptability to a wide range of environmental conditions and may expand into different habitats, thus reducing the dissimilarity among the recipient communities. We tested this assumption by analyzing a comprehensive database (78 species 229 samples) collected between × 2012 and 2017 in the marine protected area of Portofino (NW Italy), where Caulerpa cylindracea, one of the worst invaders in the Mediterranean Sea, exhibits high substratum cover at depths between 1 m and 45 m in 14 different communities (identified according to the European Nature Information System EUNIS for habitat classification). Five samples for each of the eight depth zones (i.e., 5 m, 10 m, 15 m, 20 m, 25 m, 30 m, 35 m, and 40 m) were randomly re-sampled from the comprehensive database to produce a dataset of 67 species 40 samples. Then, a second dataset of 66 species × × 40 samples was simulated by excluding Caulerpa cylindracea. Both re-sampled datasets underwent multivariate analysis. In the presence of C. cylindracea, the overall similarity among samples was higher, thus indicating homogenization of the rocky reef communities of Portofino Marine Protected Area. Continued monitoring activity is needed to understand and assess the pattern and extent of C. cylindracea’s inclusion in the recipient ecosystems. Keywords: rocky reefs; biotic homogenization; Caulerpa cylindracea; EUNIS habitats; marine protected area; Mediterranean Sea 1. Introduction Biological invasions, i.e., the successful establishment and spread of species outside their native range [1,2], are a major component of global change [3–5]; they reshuffle the planet’s biota and represent a distinctive mark of the Anthropocene [6,7]. Biological invasions have been dubbed “biological pollution” [8,9] that causes biodiversity loss and alters the composition of communities and ecosystem functioning [10,11], thus compromising ecosystem services [12]. In terrestrial habitats, biological invasions have been the concern of biogeographers and ecologists for decades [13,14], whereas in marine environments they have remained less known until recently [15,16]. Today, meta-analysis and reviews are available that highlight the impact of marine invasions [12,17–19]. Studies in the Mediterranean Sea indicate that biological invasions represent a serious ecological and economical menace leading to fishery and tourism impairment [20]. In terrestrial environments, invasive alien species have been considered important agents of biotic homogenization at different spatial scales [21–23]. In the present paper, biotic homogenization means the process that diminishes floral and faunal differences among previously distinct communities within a specific region [24,25]. The rationale beyond the idea that biological invasions may cause Diversity 2019, 11, 146; doi:10.3390/d11090146 www.mdpi.com/journal/diversity Diversity 2019, 11, 146 2 of 15 Diversity 2019, 11, x FOR PEER REVIEW 2 of 16 mayhomogenization cause homogenization in the recipient in the biota recipient is simple—invasive biota is simple—invasive species typically species show typically great adaptabilityshow great adaptabilityto a wide range to a of wide environmental range of environmental conditions and co maynditions thus and enter may diff erentthus habitats,enter different often becominghabitats, oftendominant becoming [26,27 dominant]. If an abundant [26,27]. invaderIf an abundant replaces invader or simply replaces adds toor thesimply native adds species to the that native used speciesto characterize that used the recipientto characterize communities, the recipient then the dissimilaritycommunities, among then communitiesthe dissimilarity is expectedly among communitiesreduced (Figure is expectedly1). This rather reduced simplistic (Figure scheme 1). This just rather aims simplistic at illustrating scheme the just rationale aims at of illustrating our study, thewhile rationale more complete of our study, schemes while illustrating more complete the many schemes ways invaders illustrating can the impact many recipient ways invaders communities can impactcan be foundrecipient in reviewcommunities papers can [24 ,be28 ,found29]. in review papers [24,28,29]. FigureFigure 1. 1. AA schematic schematic representation representation of of how how an an invader invader may may cause cause biotic biotic homogenization homogenization in in the the recipientrecipient communities. communities. Community Community A A is is characterized characterized by by its its exclusive exclusive species species a, a, and and community community B B is is characterizedcharacterized by by its its exclusive exclusive species species b; b; the the two two co communitiesmmunities are are evidently evidently highly highly dissimilar. dissimilar. If If an an invasiveinvasive species species enters enters both both communities communities to to flank flank or or even even replace replace the the exclusive exclusive species, species, then then the the two two communitiescommunities become become more more similar, similar, and hence homogenized. WeWe tested tested the the assumption assumption above above by by analyzing analyzing the the change change that that may may be be observed observed in in the the zonation zonation ofof communities communities along along a a sharp sharp ecological ecological gradient gradient (i.e., (i.e., depth) depth) in in the the presence presence or or absence absence of of an an alien alien invader.invader. We We used used a a comprehensive comprehensive database database collecte collectedd in in the the marine marine protected protected area area of of Portofino Portofino (NW (NW Italy),Italy), where where CaulerpaCaulerpa cylindracea cylindracea—one—one of of the the worst worst invaders invaders in in the the Mediterranean Mediterranean Sea Sea [30,31]—has [30,31]—has becomebecome abundant in recentrecent yearsyears [32[32].]. AfterAfter a a descriptive descriptive analysis analysis of of the the comprehensive comprehensive database, database, we wegenerated generated two two distinct distinct datasets datasets to go to throughgo through multivariate multivariate analysis: analysis: the firstthe first contained contained observed observed data, data,and theand second the second was a “simulated”was a “simulated” one where one C.where cylindracea C. cylindraceawas excluded was excluded from the dataset,from the under dataset, the underhypothesis the hypothesis that the latter that the dataset latter will dataset exhibit will greater exhibit dissimilarity greater dissimilarity than the formerthan the one. former We one. used We the usedterm “simulated”the term “simulated” to make it clearto make that weit clear did notthat perform we did a real,not perform physical removala real, physical experiment removal in the experimentfield. Our procedure in the field. ties inOur with procedure the so-called ties “inclusionin with the versus so-called exclusion” “inclusion approach, versus which exclusion” has been approach,said to be notwhich only has relevant been said to invasionto be not biology, only relevant but to to any invasion field where biology, the componentbut to any field of interest where is the an componentintegrated partof interest of the responseis an integrat [18,33ed]. part of the response [18,33]. 2. Materials and Methods 2. Materials and Methods 2.1. The Invader 2.1. The Invader Caulerpa cylindracea Sonder, formerly considered a variety of Caulerpa racemosa (Sonder) Verlaque, Huisman,Caulerpa and cylindracea Boudouresque, Sonder, but presentlyformerly recognizedconsidered asa anvariety independent of Caulerpa species racemosa [34,35], is(Sonder) a green Verlaque,alga with Huisman, a cylindrical and stolonBoudouresque, bearing erectbut presentl frondsy up recognized to 20 cm as high, an independent with bunches species of vesicular [34,35], isbranchlets a green alga or ramuli with (Figurea cylindrical2a). C. stolon cylindracea bearingis of erect southwest fronds Australian up to 20 origin,cm high, but with in recent bunches decades of vesicularhas expanded branchlets its range or toramuli many (Figure subtropical 2a). C. areas cylindracea of the Pacific is of andsouthwest Atlantic Australian oceans [36 origin,]. but in recent decades has expanded its range to many subtropical areas of the Pacific and Atlantic oceans [36]. Diversity 2019, 11, 146 3 of 15 Diversity 2019, 11, x FOR PEER REVIEW 3 of 16 Figure 2. Caulerpa cylindracea Sonder: (a) Typical aspect with creeping and jutting stolons and clavate Figure 2. Caulerpa cylindracea Sonder: (a) Typical aspect with creeping and jutting stolons and clavate branchlets; (b) exhibiting high cover (22%) amid infralittoral algae in shallow water; (c) invading the branchlets; (b) exhibiting high cover (22%) amid infralittoral algae in shallow water; (c) invading Codium vermilara association (EUNIS A3.231);