Aquatic Botany 185 (2023) 103615
Available online 27 December 2022
0304-3770/© 2022 Elsevier B.V. All rights reserved.
Marinomyxa marina presence in a Halophila stipulacea meadow near a fsh
farm in south Evoikos Gulf (Greece)
Nefeli Zervou
a
, Varvara Podia
a
, Sarah Faulwetter
b
, Alexis Ramfos
c
, Savvas Genitsaris
d
,
Kosmas Haralampidis
a
, Ioannis-Dimosthenis S. Adamakis
a, *
a
Section of Botany, Department of Biology, National and Kapodistrian University of Athens, Zografou Campus, 15784 Athens, Greece
b
Department of Geology, University of Patras, 26504 Patras, Greece
c
Department of Biology, University of Patras, 26504 Patras, Greece
d
Section of Ecology and Taxonomy, Department of Biology, National and Kapodistrian University of Athens, Zografou Campus, 15784 Athens, Greece
A R T I C L E INFO
Keywords:
Aegean Sea
Endosymbiont
Invasive species
Parasite
Phytomyxean
ABSTRACT
Halophila stipulacea (Forsskål) Ascherson [Order: Alismates, Family: Hydrocharitaceae] is an autochthonous
seagrass of the Indo-Pacifc and Red Sea; however, it has invaded two distinct geographical areas: the Medi-
terranean and Caribbean Sea. It is a known carrier of a phytomyxean endosymbiont which forms galls in the
petioles of the leaves. In the present study we investigated its presence in a H. stipulacea meadow located
proximal to a fsh farm in the Southern Evoikos Gulf (Aegean Sea, Greece). Seagrass samples were collected
seasonally from July 2021 until May 2022 from three sites of the meadow. A seasonal pattern was observed with
the highest infection rates in summer (July), fewer in autumn (October) and absence of the marine phytomyxean
species during winter (January) and spring (May). Moreover, pressure posed from the fsh farm seemed to
interfere with the gall abundances as statistically important differences in the infection rates were obvious.
Morphological and anatomical traits of the formed galls confrmed that mature resting spores inside the galls are
arranged in dyads. Molecular and phylogenetic analysis confrmed that the phytomyxean endosymbiont
belonged to Marinomyxa marina and suggested minimal evolutionary divergence between invasive M. marina
populations. In the Aegean Sea this is northernmost record of this phytomyxean endosymbiosis following the
expansion of H. stipulacea.
1. Introduction
The Mediterranean Sea is home to four autochthonous marine sea-
grass species (namely: Cymodocea nodosa (Ucria) Asch., Posidonia oce-
anica (L.) Delile, Zostera marina L. and Z. noltii Hornem) as well as to the
exotic Halophila stipulacea (Forsskål) Ascherson [Order: Alismates,
Family: Hydrocharitaceae]. H. stipulacea was introduced into the Med-
iterranean Sea via the Suez Canal opening more than a century ago
(Lipkin, 1975) and still remains the only non-indigenous seagrass in the
Mediterranean (García-Escudero et al., 2022). It is one of the frst Les-
sepsian migrants to cross the Suez Canal, originating from the
Indo-Pacifc (Winters et al., 2020), and since its frst Mediterranean
sighting, (Rhodes Island, in 1894) (Lipkin, 1975) it has been colonizing
the Mediterranean basin. H. stipulacea has been found south of the
Adriatic Sea and south of the Tyrrhenian Sea: Albania, Cyprus, Egypt,
Greece, Israel, mainland Italy (northernmost limit: Porto Palinuro,
Salerno), Lebanon, Libya, Malta, Sardinia, Syria, Tunisia and Turkey
(Winters et al., 2020), while recently, it has been discovered along the
French Riviera (France). This represents a big leap in its known distri-
bution several hundred kilometers from its previously known north-
ernmost localities in the western Mediterranean (Thibaut et al., 2022).
Over the last years, the species is expanding increasingly, possibly due to
its superior ability to tolerate a wide range of environmental conditions
(Winters et al., 2020). Since 2002, H. stipulacea is also found in the
biogeographic area of the Caribbean Sea (Winters et al., 2020). Future
predictions of H. stipulacea distribution suggest that the species will have
the opportunity to expand into the 83 % of the Mediterranean coastal
areas within the next 100 years (Beca-Carretero et al., 2021). Thus, it
comes to no surprise that concerns about its impact on current biodi-
versity have been voiced (Williams, 2007; Tsirintanis et. al, 2022).
H. stipulacea is also a known host of an endosymbiont of the Phyto-
myxea class (SAR: Rhizaria, Endomyxa), which has been characterized
* Corresponding author.
E-mail address: iadamaki@biol.uoa.gr (I.-D.S. Adamakis).
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Aquatic Botany
journal homepage: www.elsevier.com/locate/aquabot
https://doi.org/10.1016/j.aquabot.2022.103615
Received 23 July 2022; Received in revised form 9 December 2022; Accepted 26 December 2022