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Large-Scale Distribution of the European Seahorses (Hippocampus

Rafinesque, 1810): A Systematic Review

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DOI: 10.3390/biology11020325

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 biology
Review
Large-Scale Distribution of the European Seahorses
(Hippocampus Rafinesque, 1810): A Systematic Review
Cataldo Pierri 1 , Tamara Lazic 1 , Michele Gristina 2, *, Giuseppe Corriero 1 and Mauro Sinopoli 3

1 Department of Biology, University of Bari Aldo Moro, 70125 Bari, Italy; [email protected] (C.P.);
[email protected] (T.L.); [email protected] (G.C.)
2 National Research Council of Italy IAS—Institute of Anthropic Impacts and Sustainability in Marine
Environment, 90149 Palermo, Italy
3 Stazione Zoologica Anton Dohrn, Department of Integrative Marine Ecology, 90149 Palermo, Italy;
[email protected]
* Correspondence: [email protected]

Simple Summary: Populations of many marine species are threatened by a number of interacting
factors, including anthropogenic activities, climate change, and biodiversity loss. The assessment
of the conservation status of such populations relies heavily on several types of data, such as
large-scale geographical and ecological distribution. Seahorses are charismatic fish sensitive to
environmental pressures, and according to the IUCN directive 95/2020, they should be considered a
model for environmental quality assessment. As in many other areas, the data on seahorse ecological
distribution in Europe are scattered, patchy, and mainly focused on small-scale studies. Therefore, we
undertook a systematic review using the PRISMA protocol to identify the current knowledge status,
detect gaps, and propose future research priorities. We analyzed 32 years of published studies and
described the distribution of Hippocampus guttulatus and H. hippocampus across 176 sites in the Atlantic





 Ocean, Mediterranean Sea, and Black Sea as a function of habitat, depth, and degree of confinement.
Citation: Pierri, C.; Lazic, T.; Gristina, The applied method evidenced the overall lack of a detailed habitat description in published studies.
M.; Corriero, G.; Sinopoli, M. Seahorse conservation would benefit from an analytical description of habitats, such as data on
Large-Scale Distribution of the the depth, nature of the substrate, and associated biological communities, as well as the use of a
European Seahorses (Hippocampus standardized habitat classification system, such as formally recognized EUNIS habitat codes.
Rafinesque, 1810): A Systematic
Review. Biology 2022, 11, 325.
Abstract: Human pressures on marine ecosystems have caused extensive degradation of marine habi-
https://doi.org/10.3390/
tats and several local extinctions. Overexploitation and destructive fishing practices are responsible
biology11020325
for biodiversity loss in many coastal ecosystems. The definition of conservation programs in marine
Academic Editor: John R. Turner fish requires comprehensive knowledge on large-scale geographical distribution, while considering
distribution/abundance patterns in relation to key environmental variables. Due to their life-cycle
Received: 1 December 2021
Accepted: 16 February 2022
traits, the two European seahorses (Hippocampus guttulatus and H. hippocampus), as with other con-
Published: 18 February 2022 generic species, are particularly sensitive to the effects of anthropogenic activities and habitat changes.
However, information on the ecological distribution of these two species is scattered, patchy, and
Publisher’s Note: MDPI stays neutral
mainly focused on small-scale studies. In this paper, we followed an international standard protocol
with regard to jurisdictional claims in
for systematic reviews (the PRISMA protocol) to provide a detailed assessment of the two species’ ge-
published maps and institutional affil-
ographical distribution in relation to the environmental characteristics. According to the 134 analyzed
iations.
studies, Hippocampus guttulatus is more common in confined areas, while H. hippocampus is found in
marine shelf waters. With several interspecific differences, seagrasses were the most used holdfasts
of both species. The EUNIS codes (European nature information system) referring to a specific and
Copyright: © 2022 by the authors. unique habitat were discussed as a potential tool for defining the ecological distribution of the two
Licensee MDPI, Basel, Switzerland. species. The obtained results and their future implementation could help plan conservation actions.
This article is an open access article
distributed under the terms and Keywords: syngnathids; PRISMA; long-snouted seahorse; short-snouted seahorse; Hippocampus
conditions of the Creative Commons distribution; ecological assessment
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).

Biology 2022, 11, 325. https://doi.org/10.3390/biology11020325 https://www.mdpi.com/journal/biology

Biology 2022, 11, 325 2 of 15

1. Introduction
Worldwide, human pressures on marine ecosystems have caused extensive degrada-
tion of marine habitats, and by impacting many communities, have also caused several
local extinctions [1,2]. Indeed, overexploitation of fish and other seafood resources, coupled
with destructive fishing practices, pollution, introductions of alien species, and climate
change, are mainly responsible for biodiversity loss in coastal ecosystems [3]. In this
scenario, species with unique life-cycle traits (such as low swimming capacities, mate
fidelity, lengthy parental care, and high site fidelity) and close trophic relationships with
local communities seem much more sensitive to environmental changes, and this could
especially refer to seahorses [4–8].
The success of specific conservation actions will rely heavily on the quantity and
quality of data available on the large-scale geographical and ecological distribution, as well
as on the environmental drivers that underlie the ecological dynamics of communities [9,10].
The relationship between the distribution/abundance patterns and features of habitats is
well known, and features such as depth, bottom type, and physical characteristics [11] are
correlated to the spatial distribution of many species [12,13]. Unfortunately, comprehensive
knowledge of these data in marine fish are available in only a limited number of cases, such
as commercially important species, whereas for most other species, even if of conservation
interest, there is very often an information gap.
Seahorses are charismatic fish considered flagship species of the conservation ef-
forts [14,15], the populations of which tend to be patchily distributed and occur at low den-
sities worldwide [4]. These fish are characterized by sedentary behaviour, low swimming
capacities, and small home ranges [4,8,16–18]. Furthermore, seahorses live in vulnerable
coastal habitats that, together with their unusual life cycle traits, make them sensitive to
the effects of anthropogenic activities and habitat change [4,6,7].
The two seahorse species Hippocampus guttulatus and H. hippocampus have a wide
geographic range extending across most of Europe and North Africa, including the Atlantic
Ocean, Mediterranean Sea, and Black Sea [19]. Like other congeneric, both species are listed
on Appendix II CITES (Appendix II) and the IUCN Red List where they are classified as
“Data Deficient” at a global level [14,15]. Declines in several populations across Europe
have been recently reported [5,17,20–22]. Although the exact causes remain unknown,
there are some indications of a decrease in suitable habitats [20] or even illegal traffick-
ing [20,21]. Such a status for the two species, indeed, indicates the urgent need for specific
conservation actions to preserve populations. However, due to their cryptic nature and
sedentary behavior, seahorses are difficult to survey, and this poses serious challenges to
their conservation [23].
Estimating the conservation status of populations could benefit from knowledge about
their distribution [24], and could help identify species hotspots [25]. A systematic review of
the available literature could be useful to achieve this goal, as systematic reviews synthesize
evidence, identify gaps in the literature, and can suggest future lines of research [26]. In
recent years, several reviews on seahorses [27,28] and a specific one on two European
species [23] have been published. Indeed, a literature search may help gain a more complete
picture of the species distribution, demographics, and thus conservation status [29]. In the
present paper, we used the methodology of systematic reviews, well established in ecology
and conservation [30,31], to summarize 32 years of published studies on H. guttulatus
and H. hippocampus so as to provide an increasingly fine and detailed assessment of the
geographical and ecological distribution in relation to the environmental characteristics. By
providing data on spatial distribution and its correlation with environmental features, the
results of this study will help with better conservation of the two seahorse species.
Biology 2022, 11, 325 3 of 15

2. Materials and Methods

The systematic review was carried out according to the orientations of Preferred Re-
porting Items for Systematic Reviews and Meta-Analyses (PRISMA) [32], which is used as
a guide for study selection, screening, and eligibility. Studies were identified using several
search engines, including Elsevier’s Scopus (www.scopus.com (accessed on 1 November
2021)), Clarivate Web of Science (www.webofknowledge.com (accessed on 1 November
2021)), and Google Scholar (scholar.google.com (accessed on 1 November 2021)). The
bibliographic search included peer-reviewed literature, theses, books, and other related
scientific reports published between 1989 and 2021. Several combinations of keywords were
used to identify relevant publications: “Hippocampus guttulatus”, Hippocampus hippocampus”,
“Hippocampus ramulosus”, “seahorse”, “long-snouted”, and ”short-snouted”. Reference lists
of publications were also used as bibliographic sources. Potentially relevant papers were
read in full, and information and data that were relevant for this review were extracted.
Studies considered duplicates and those that included animals raised in captivity were
excluded from the analysis. In order to represent the comprehensive spatial distribution
of seahorses, studies without clear toponymic references were used in the case of data-
poor countries (e.g., the Maghreb and North/East Africa). Furthermore, regarding the
same areas, additional searches were made to recover reliable sources (i.e., peer-reviewed
publications, scientific reports, and congress communications) by using digital platforms
not included in the initial PRISMA strategy. When available, information on study type
(biodiversity/other), target species (H. guttulatus or H. hippocampus), year of record, study
site, country, sea (Mediterranean Sea, Atlantic Ocean, or the Black Sea), coordinates, con-
finement (marine environment or lagoon), abundance, density, sex (abundance/density of
males, females, and juveniles), habitat (e.g., Posidonia oceanica or sandy bottom), and depth
were collected. Several publications did not report the entire set of required information
(such as studies on commercial catches or checklists); in such a case, we used the available
data, which were combined together and expressed as percentages. The only exceptions
were EUNIS habitat codes [33]; if possible, they were obtained by comparing the described
habitat characteristics with the analytical descriptions of the EUNIS codes at the highest
possible level (level 4).

3. Results
The PRISMA search strategy found 2375 preliminary studies. After validation proce-
dures and the removal of duplicates and non-informative studies, 125 studies were chosen
(Figure 1). An analysis of the bibliographic sources from alternative search engines (not
included in the initial PRISMA strategy) and referred to the data-poor regions revealed six
peer-reviewed publications, two technical reports, and one congress paper, accounting for
134 studies used for the distribution analysis.

3.1. Research Trends and Publication Metrics on Seahorses

The first scientific publication on European seahorse species dates back to 1989, al-
though the first observation dates as far back as 1948. The number of scientific publications
increased only in the mid-2000s, and the number of published papers reached a maximum
between 2011 and 2015 (Figure 2a). Most papers focused on H. guttulatus and referred
to many scientific areas (Figure 2b). Both species were rarely reported in biodiversity
studies (Figure 2b). Regarding the type of publications, peer-reviewed papers were the
most abundant for both species (Figure 2c), while the other types (e.g., theses, books, and
technical reports) accounted for 10% of publications.
Biology 2022,11,
Biology2022, 11,325
x FOR PEER REVIEW 44 of
of 15
15

Figure1.1.Flow
Figure Flowchart
chartdetailing
detailingthe
the process
process of of identification,
identification, screening,
screening, andand eligibility
eligibility of references
of references for
for the systematic review.
the systematic review.

3.1.Geographical
3.2. Research Trends
and and Publication Metrics
Macroecological on Seahorses
Distribution
The first scientific
According publication
to the PRISMA on European
strategy, seahorse
publications species
referred to 167dates
sites back
acrosstothe
1989,
entirealt-
hough the
species first observation
distribution dates as farthe
range, including back as 1948.Atlantic
Northern The number
Ocean of scientific
(namely publications
the English
increased
Channel only
and theinNorth
the mid-2000s, and the Ocean,
Sea), the Atlantic numberMediterranean
of published papers
Sea, and reached a maximum
Black Sea (Table 1
and Figure2011
between 3). Most of the
and 2015 recorded
(Figure 2a).sites
Mostwere in the
papers Mediterranean
focused Sea (n =and
on H. guttulatus 82),referred
followed to
by the scientific
many NorthernareasAtlantic Ocean
(Figure 2b).(n = 34),
Both Atlantic
species wereOcean
rarely(n = 33), and
reported Black Sea (nstudies
in biodiversity = 18).
Sites were
(Figure located
2b). in 22 countries,
Regarding the type of and more than 65%
publications, were relatedpapers
peer-reviewed to the were
following five
the most
countries:
abundant Turkey
for both(nspecies
= 39), Spain
(Figure (n2c),
= 24), the the
while United
otherKingdom (n =theses,
types (e.g., 18), Italy (n =and
books, 16), tech-
and
France (n = 13).accounted
nical reports) An analysisforof10%
theof
alternative search engines revealed nine additional sites
publications.
in the Mediterranean Sea, located in Italy (n = 3), Croatia (n = 1), Libya (n = 2), Morocco
(n = 1), Egypt (n = 1), and Lebanon (n = 1).
 Biology2022,
Biology 11, x325
2022, 11, FOR PEER REVIEW 5 of 15 5 of 15

Figure2. 2.
Figure (a)(a)
TheThe number
number of publications
of publications on H. guttulatus
on H. guttulatus (in blue)(in
andblue) and H. hippocampus
H. hippocampus (in orange)
(in orange) per
year. (b) The number of publications on H. guttulatus and H. hippocampus per research topic. (c) Thetopic. (c)
per year. (b) The number of publications on H. guttulatus and H. hippocampus per research
The number
number of publications
of publications on H. guttulatus
on H. guttulatus and H. hippocampus
and H. hippocampus per publication
per publication type. type.

3.2. In
Geographical and Macroecological
the Mediterranean Sea, the twoDistribution
species frequently co-occurred at the same sites
(approximately 40%). Seahorses in other areas were distributed
According to the PRISMA strategy, publications independently
referred with
to 167 sites similar
across the entire
values (Table 1). In the Atlantic Ocean and the Black Sea, the two species co-occurred at a
species distribution range, including the Northern Atlantic Ocean (namely the English
low number of sites (36% and 11%, respectively), with H. guttulatus being the most reported
Channel and the North Sea), the Atlantic Ocean, Mediterranean Sea, and Black Sea (Table
species. On the contrary, in the English Channel and the North Sea, H. hippocampus was
1 andfrequently
more Figure 3).observed,
Most of the
andrecorded
the numbersites
ofwere
sites in the Mediterranean
at which Sea (n = 82),
the species co-occurred wasfollowed
by the Northern
also low (18%). Atlantic Ocean (n = 34), Atlantic Ocean (n = 33), and Black Sea (n = 18).
Sites were located in 22 countries, and more than 65% were related to the following five
countries: Turkey (n = 39), Spain (n = 24), the United Kingdom (n = 18), Italy (n = 16), and
France (n = 13). An analysis of the alternative search engines revealed nine additional sites
in the Mediterranean Sea, located in Italy (n = 3), Croatia (n = 1), Libya (n = 2), Morocco (n
= 1), Egypt (n = 1), and Lebanon (n = 1).
 reported species. On the contrary, in the English Channel and the North Sea, H. hippocam-
pus was more frequently observed, and the number of sites at which the species co-oc-
curred was also low (18%).
Biology 2022, 11, 325 6 of 15
Table 1. Occurrence (and co-occurrence) sites of the two species in the Northern Atlantic Ocean (the
English Channel and the North Sea), Mediterranean Sea, and the Black Sea according to PRISMA (n
Table 1. Occurrence (and co-occurrence) sites of the two species in the Northern Atlantic Ocean (the
= 167) and alternative search engines (n = 9).
English Channel and the North Sea), Mediterranean Sea, and the Black Sea according to PRISMA
(n = 167) and alternative search engines (n = 9).
H. guttulatus H. hippocampus Both Species
English Channel and North Sea 5 H. guttulatus 23
H. hippocampus 6 Species
Both
English Channel and North Sea
Atlantic Ocean 17 5 4 23 126
Atlantic Ocean 17 4 12
Mediterranean Sea Mediterranean Sea 28 28 25 25 3838
Black Sea 13 3
Black Sea 13 3 22

Figure 3. Distribution map

Figureof
3. seahorse
Distributionspecies. Whitespecies.
map of seahorse symbols indicate
White sites found
symbols indicate following
sites found the
following the
PRISMA strategy. Black symbols indicate sites found through alternative
PRISMA strategy. Black symbols indicate sites found through alternative search engines. Gray sym- search engines. Gray
symbols indicate the presence of seahorses without a clear indication on the exact position.
bols indicate the presence of seahorses without a clear indication on the exact position.
The two seahorse species had different confinement preferences among the different
The two seahorseseas
species
(Figurehad
4a,b).different confinement
In the Atlantic Ocean, both preferences among
species were mainly the different
recorded in confined
areas (lagoons, estuaries, or semi-enclosed bays). In other seas, on the contrary, both
seas (Figure 4a,b). In the Atlantic Ocean, both species were mainly recorded in confined
species were most frequently described in marine shelf areas. This trend was especially
areas (lagoons, estuaries,
evidentorfor
semi-enclosed
H. hippocampus inbays). In other seas,
the Mediterranean on theAtlantic
and Northern contrary,
Oceanboth spe-
(Figure 4b);
cies were most frequently described inthemarine
in the Mediterranean, shelf
distribution areas.
of H. Thisintrend
guttulatus was
confined and especially evi-
open sea areas was
almost overlapping.
dent for H. hippocampus in the Mediterranean and Northern Atlantic Ocean (Figure 4b); in
the Mediterranean, the3.3. distribution of H. guttulatus in confined and open sea areas was
Ecological Distribution
almost overlapping. Focusing on the considered habitat parameters, a greater amount of information was
present for substrate preferences (124 publications) rather than depth (111 publications).
Preferred categories of water depth varied according to the species and confinement. In
Biology 2022, 11, 325 7 of 15

confined areas (Figure 5a), both species were mostly found from the surface up to six
meters of depth, with weak differences between species. Indeed, although H. guttulatus was
usually reported at depths from 0 to 1 m, H. hippocampus was more frequently described at
depths ranging from 4 to 6 m. In marine shelf waters (Figure 5b), the peak of H. guttulatus
reports was found at depths between 5 and 10 m, with a low number of records at depths
Biology 2022, 11, x FOR PEER REVIEW
greater than 20 m. H. hippocampus, however, was most described at depths ranging7from of 15
5 to 30 m, and the number of specimens observed at depths greater than 30 m was low.

Figure4.
Figure 4. Percentage
Percentage distribution
distribution of
of seahorses
seahorses concerning
concerning geographical
geographical area
area and
and the
the degree
degree of
of con-
con-
finement for (a) H. guttulatus and (b) H. hippocampus. EC&NS = English Channel and the North Sea.
finement for (a) H. guttulatus and (b) H. hippocampus. EC&NS = English Channel and the North Sea.

3.3. Ecological
Concerning Distribution
habitats, seahorses were found in 24 different habitat types among all sites
(Figure 6a,b). However,
Focusing in confined
on the considered environments,
habitat parameters, thea two species
greater wereofreported
amount in more
information was
habitats
present (n for=substrate
21) than inpreferences
the marine (124
environment (n = 15).
publications) At both
rather thanconfined
depth (111andpublications).
marine sites,
the two species
Preferred were of
categories most frequently
water reported
depth varied in seagrass
according to thebeds. Hippocampus
species guttulatus
and confinement. In
also showed
confined high
areas preferences
(Figure 5a), bothfor Chlorophyta
species facies
were mostly and sandy
found from thebottoms
surfaceatupboth types
to six me-
of sites,
ters and additionally
of depth, for Rhodophyta
with weak differences facies
between and mussel
species. Indeed,beds in marine
although shelf areas
H. guttulatus was
(Figure
usually6b). H. hippocampus,
reported on the0 contrary,
at depths from to 1 m, H.was rarely reported
hippocampus in association
was more frequentlywith algae,
described
but was more
at depths frequently
ranging from 4 found
to 6 m.on
In phanerogams and other
marine shelf waters substrates,
(Figure 5b), the including
peak of H.shallow
guttula-
rocky
tus reports was found at depths between 5 and 10 m, with a low number of records of
and muddy bottoms, almost always sharing the same ecological distribution at
H. guttulatus.
depths greater than 20 m. H. hippocampus, however, was most described at depths ranging
from 5 to 30 m, and the number of specimens observed at depths greater than 30 m was
low.
Concerning habitats, seahorses were found in 24 different habitat types among all
sites (Figure 6a,b). However, in confined environments, the two species were reported in
more habitats (n = 21) than in the marine environment (n = 15). At both confined and ma-
rine sites, the two species were most frequently reported in seagrass beds. Hippocampus
PEER REVIEW 8 of 15

shallow rocky and muddy bottoms, almost always sharing the same ecological distribu-
Biology 2022, 11, 325 8 of 15

tion of H. guttulatus.

Figure 5. Percentage Figure

depth5. ranges
Percentage(meter) of(meter)
depth ranges the twoof the species
two speciesin confined
in confined (a)
(a) and andshelf
marine marine shelf (b)
(b) environments.
environments.
Publications with data sufficient for the correct classification of habitats according
to the EUNIS classification system (Figure 7) permitted the identification of three types
Publications with datalevel
of EUNIS sufficient forincluding
2 habitats, the correct classification
A2 (Littoral ofA3
sediments), habitats according
(Infralittoral rock andto
the EUNIS classification
other hardsystem (Figure
substrata), and A47)(Circalittoral
permittedrocktheother
identification of and
hard substrata), threeten types
types ofof
EUNIS level 3 habitats (for the interpretation of these habitats, see EUNIS 2020 habitat
EUNIS level 2 habitats, including A2 (Littoral sediments), A3 (Infralittoral rock and other
classification). Following this classification, most of the publications reported seahorses
hard substrata), and in A4 (Circalittoral
the habitat of Littoralrock otherdominated
sediments hard substrata),
by aquatic and ten types
angiosperms (Levelof 3:EUNIS
A2.6;
level 3 habitats (forLevel
the interpretation of these
2: Littoral sediments). With habitats, see EUNIS
increasing depth 2020 habitat
and transition classifica-
from infralittoral to
circalittoral habitats, the number of seahorse reports decreased with a greater frequency for
tion). Following this classification, most of the publications reported seahorses in the hab-
H. hippocampus at greater depths.
itat of Littoral sediments dominated by aquatic angiosperms (Level 3: A2.6; Level 2: Lit-
toral sediments). With increasing depth and transition from infralittoral to circalittoral
habitats, the number of seahorse reports decreased with a greater frequency for H. hippo-
campus at greater depths.
FOR PEER REVIEW
Biology 2022, 11, 325 9 of 915
of 15

Figure 6. Percentage distribution

Figure of the
6. Percentage two species
distribution of theamong habitats
two species amongin confined
habitats (a) and
in confined (a)marine shelf
and marine shelf
environments (b). environments (b).
Biology 2022,
Biology 2022,11,
11,x325
FOR PEER REVIEW 10 of 15 10 of 1

Figure7.7. Distribution
Figure Distributionofofthe
thetwo
twospecies
species among
among thethe habitats
habitats classified
classified according
according to EUNIS
to the the EUNIS (Eu
ropean Nature
(European NatureInformation System)classification
Information System) classification system.
system.

4. Discussion
4. Discussion
One of the fundamental challenges at the forefront of conservation biology is to under-
stand One of the fundamental
the ecological challengesofatsensitive
and spatial distribution the forefront
species ofand conservation biology
their demographic dy-is to un
derstand the ecological and spatial distribution of sensitive species
namics. This challenge becomes greater when attempting to develop conservation strategies and their demographi
dynamics.
for data-poorThis challenge
species becomes
with patchy greater when
and scattered attempting
information. to develop
Seahorses conservation strat
are a paradigmatic
egies
case of for data-poor
data-poor marinespecies
species.with patchy
In that sense,and
the scattered
systematic information. Seahorses for
review could compensate are a para
the lack of specific large-scale studies by synthesizing the available
digmatic case of data-poor marine species. In that sense, the systematic review could cominformation.
Seahorses
pensate for theare considered
lack of specificflagship species in several
large-scale studies fields
by of conservationthe
synthesizing biology [19] infor
available
and have been recently claimed to have an important role as indicators of environmental
mation.
quality [34]. The issues facing seahorses, including habitat degradation and loss, target
Seahorses are considered flagship species in several fields of conservation biology
fisheries, and by-catch, are indeed major concerns in marine conservation, and the fact that
[19]global
the and have
IUCNbeen statusrecently claimedand
of H. guttulatus to have an important
H. hippocampus, as forrole as other
many indicators of environ
seahorse
species, is Data Deficient [14,15] indicates the need for a specific implementation of currentand loss
mental quality [34]. The issues facing seahorses, including habitat degradation
target fisheries,
knowledge and by-catch,
to improve are indeed
their conservation major
status. concerns
The decline of inmany
marine conservation,
seahorse popula- and th
fact that
tions, the global
coupled with theirIUCNuniquestatus of H. guttulatus
appearance and H.has
and life history, hippocampus, as for many othe
generated considerable
interest
seahorse among many
species, is scientists,
Data Deficientwith an increase
[14,15] in the number
indicates the need of publications
for a specificinimplementation
the last
decades.
of current However,
knowledge despite the increasing
to improve theirnumber of studies
conservation and reported
status. The declinedeclines of upseahorse
of many
to 80% of the initial population abundances [22], both species are still poorly considered
populations, coupled with their unique appearance and life history, has generated con
in national directives and laws regulating their collection (with some exceptions; in the
siderable interest among many scientists, with an increase in the number of publication
UK, for instance, both species are protected by the Wild-Life and Countryside ACT and
in the
are amonglast the
decades. However,Action
UK Biodiversity despite thepriority
Plan increasing number
species) of studies
[14,15]. and reported
The necessity for de
clines
the of up
correct to 80% of of
classification thethe
initial
speciespopulation abundances
status on regional [22], both species
and international levels hasarealso
still poorly
considered
been highlightedin national
by the IUCNdirectives and laws
resolution regulating their collection
95 (WCC-2020-Res-095-EN (with some excep
the Conservation
tions;
of in the pipefishes
seahorses, UK, for instance, both species
and seadragons). are protectedstudies
Characterization by the containing
Wild-Life and bothCountrysid
eco-
logical
ACT and andare autecological
among theinformation could be
UK Biodiversity usefulPlan
Action to achieve
prioritythis scope. [14,15].
species) However, The neces
seahorses lack in-depth characterization at a global scale, as most ecological
sity for the correct classification of the species status on regional and international level studies refer
to small-scale
has also beenassessments
highlighted [7,20,27,35].
by the IUCN Using the methodology
resolution of systematic reviews, the
95 (WCC-2020-Res-095-EN the Conser
present study brings together all available information present in the scientific literature,
vation of seahorses, pipefishes and seadragons). Characterization studies containing both
thus representing the most exhaustive and up-to-date assessment of the geographical and
ecologicaldistribution
ecological and autecological
patterns information
of H. guttulatuscould
and H.behippocampus.
useful to achieve this the
Moreover, scope.
studyHowever
seahorsesthe
proposes lack
usein-depth
of EUNIScharacterization
codes, the main at a global scale,
comprehensive as most ecological
pan-European studies refe
hierarchical
to small-scale assessments [7,20,27,35]. Using the methodology of
habitat classification system, as an important tool for designing networks of protected areas, systematic reviews, th
present study
monitoring, andbrings together
management all available information present in the scientific literature
planning.
thus representing the most exhaustive and up-to-date assessment of the geographical and
ecological distribution patterns of H. guttulatus and H. hippocampus. Moreover, the study
proposes the use of EUNIS codes, the main comprehensive pan-European hierarchica
habitat classification system, as an important tool for designing networks of protected ar
eas, monitoring, and management planning.
By reporting 32 years of records and 176 sites across the entire distributional range
Biology 2022, 11, 325 11 of 15

By reporting 32 years of records and 176 sites across the entire distributional range,
this research contributed to strengthening the ecological and geographical assessment of
European seahorses. H. guttulatus and H. hippocampus were recorded across the entire
distributional area [14,15,19], and the number of occurrence localities of the two species
reported here is greater than that of previously published datasets [4,19,23]. The data
collected during this systematic review confirmed the trend of increased scientific attention
and, although these charismatic fish have been studied for more than 30 years, the research
intensification began only recently, when several European research groups simultaneously
focused their attention on these animals. However, most studies analysed in our review
were focused on reproductive biology or physiological traits, while a smaller number
were related to autecology and population dynamics. The focal point on these biological
aspects was also common among other seahorse species, as unique life cycle traits provide
a significant opportunity to expand our understanding of reproductive ecology in animals
in general [27].
The important role of confined environments, such as lagoons and estuaries, was
particularly evident in the Atlantic, probably because they offer shelter from strong wave
motions and winter storms [36]. Furthermore, the tendency to occupy shallow habitats
could explain why many seahorses in the Atlantic Ocean were found in confined areas.
In the Mediterranean Sea, these fish seemed more equally distributed between the two
environments, although H. guttulatus showed slightly higher preferences for confined areas,
while H. hippocampus was more frequently found at marine sites, probably because of the
greater water depths, which seem preferred by the species [7]. Although in agreement
with previous small-scale studies, it should be pointed out that such findings could be an
artefact of site-specific population traits. Indeed, the results are highly dependent on the
research activities in specific areas with locations where seahorses were already known
to be present or abundant being more studied, and this could have limited our ability to
detect ecological patterns.
Regarding ecological distribution, H. guttulatus and H. hippocampus can be found
in a variety of habitats with different degrees of complexity, but prey abundance seems
an important factor in determining habitat selection [17,34]. However, according to the
available information, the most reported seahorse habitat in both marine shelf and confined
areas were marine phanerogams. Seagrasses are the preferred habitat of many temperate
syngnathid species [4], probably because they maximize prey density and capture efficiency,
and could help fish with low swimming capacities avoid predators [4]. In confined areas,
however, seahorses are also reported on incoherent (sandy or muddy) bottoms and algal
beds, supporting site-specific studies [7,20,23,37,38]. Some seahorses have been recorded
grasping artificial structures, highlighting their important role in the population dynamics
of seahorses [18,37]. It is known that artificial structures are a suitable habitat for seahorses,
probably because they host rich and diversified fouling communities, which can contribute
to the complexity of the system by providing additional microhabitats, food, and hiding
places [7,35,39].
In the present research, we attempted to standardize habitats of occurrence by applying
the European codification system used in many ecological studies. The EUNIS habitat
classification is a comprehensive pan-European system used to facilitate and harmonize
the description and collection of data using analytical criteria. There are two advantages of
using this classification: first, its use of widely accepted habitat types recognized by the
scientific community, and second, it is a reference point for the development of indicators
and environmental reporting [40]. When considering the high variability of habitats over
the entire seahorse distribution area, the use of standardized codes could be essential to map
habitats of their occurrence, support conservation strategies, and environmental assessment.
However, the performed systematic review revealed a substantial deficit in data availability,
as only half of the selected literature contained an entire set of the required information
on environmental features, which somewhat hampered our analysis. According to the
available data, most seahorses, and especially H. guttulatus, have been recorded in the
Biology 2022, 11, 325 12 of 15

habitat of Littoral sediments dominated by angiosperms (EUNIS code A2.6), confirming

the results of site-specific studies on arbitrarily defined habitats [7,17,23,28,34,35].
Following the results of the present systematic review and previous site-specific
studies [14,15,19], both species have a wide and mainly overlapping geographic range
extending across most of the Atlantic Ocean, Mediterranean Sea, and Black Sea. However,
parts of the two species distribution areas appear poorly represented according to the
peer-reviewed bibliographic sources, although numerous unpublished expert opinions
and observations have testified the presence of seahorses. The presence of populations,
their abundance, and other survey information, for instance, seem incomplete at the
southern limit of the seahorses’ range, including broad areas along the African coast
(e.g., Algeria, Egypt, Libya, and Morocco). In line with accepted principles of literature
searches for systematic reviews, this approach uses specific bibliographic databases to
identify adequate literature. However, the search engine can prevent finding all pertinent
records, as literature is often found outside of the required bibliographic databases and
might involve websites or online repositories that typically require specific data searching
and browsing. Therefore, keyword-based research on specific databases may miss items
potentially relevant to the research question. Furthermore, although journal articles are
usually easily identifiable via database searches, other research items such as research
reports and conference papers are often not [34]. Indeed, when the literature analysis
was expanded in specific geographic areas, the search produced new records of seahorse
occurrence, mainly referring to ichthyofauna checklists and unpublished sources (such as
technical reports of scientific projects and congress abstracts). Assessing material published
on the Internet represents a challenge, given the vast amount of information, lack of
standard indexing, and controlled vocabulary, but it can make important contributions
to a systematic review [41] as much research is unpublished or not disseminated through
peer-reviewed, commercial media [42,43]. The results of the systematic review presented
in this paper revealed some important findings that would not have been apparent without
a search on these non-standard sources. Indeed, the use of additional research platforms
provided a greater definition of seahorse occurrence data. However, this review revealed
that many bibliographic sources did not report the information useful for georeferencing
seahorses, such as toponyms or geographical coordinates of sites. Such constraints imposed
a challenge to the comprehensive review of seahorse distribution. Although usually
excluded as non-informative in the screening process, in the case of countries with no
data, we decided to insert the generic report on the distribution map (Figure 3) in order to
present the information as complete as possible.
The outcome of the systematic review will depend not only on the ability of search
strategy to locate relevant data, but also on the quality and quantity of those sources and the
information they contain. When dealing with systematic reviews, an aspect that should not
be underestimated is the identification of the weight that should be given to each record in
relation to the research effort, as collected information could seem unbalanced—abundant
and detailed in the countries where the research teams are historically involved, while
rare or scanty in other regions, possibly because of a lack of research interest or funding
to study the species. The results of this review were probably influenced by the presence
of research groups that actively studied the two species on a local scale. Furthermore,
the lack of studies following the same populations over time, thus providing historical
series of repeated observations, rendered any systematic representation of the information
incomplete. This applies to a series of sites at which seahorses were claimed to be present,
but there were no indications of their past or contemporary abundance nor eventual
population fluctuations through time. In the case of several sites, such as Mar Piccolo
di Taranto (Southern Italy) and Ria Formosa (Southern Portugal), there was repeated
information confirming a constant seahorse presence, albeit with numerical fluctuations.
According to some anecdotal evidence, several populations were abundant in the past,
but have now completely disappeared, as is the case with Marsala lagoon (Sicily). This
situation is probably shared by other populations, but the available literature does not
Biology 2022, 11, 325 13 of 15

contain sufficient information that would permit the assessment of abundance changes,
thus rendering any restoration and conservation actions difficult.
The conservation of seahorses should be a priority for ecological, biological, and eco-
nomic reasons, as well as for their intrinsic value [28]. Although there are a relatively high
number of papers on the two European seahorses that have been published in recent years,
some aspects of seahorse ecology and biology seem poorly represented. The assessment of
the conservation status is influenced by data availability and the possibility of their effective
use [44]. Indeed, according to the FAIR principles, information needs to be findable, acces-
sible, interoperable, and reusable in order to be used as a basis for decision-making when
converted into knowledge [45]. If conforming to recognized and standardized protocols,
uniform characterization of the information would allow for the application of artificial
intelligence tools for the search, interpretation, and cleaning of large amounts of data. This
review highlights advances in our understanding of seahorse distribution, but perhaps
more importantly, it highlights important gaps to be filled. Therefore, we suggest that
future research should be oriented to locate and characterize hitherto unknown popula-
tions, especially in poorly studied areas, which would be valuable for understanding the
distribution and ecology, and could help at preserving the two seahorse species.

Author Contributions: Conceptualization, C.P., T.L., M.G. and M.S.; methodology, T.L. and M.S.; for-
mal analysis, C.P., T.L. and M.S.; investigation, T.L., M.G. and M.S.; data curation, T.L.; writing—original
draft preparation, C.P. and M.S.; writing—review and editing, C.P., T.L., M.G., G.C. and M.S.; supervi-
sion, C.P., M.G. and G.C. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: In light of recent threats posed by illegal harvesting, the authors
believe that they should not publish the exact list and related locations of sites of seahorse occurrence.
However, the data will be made available to anyone with a scientific or political interest after a
justified request to the corresponding author.
Acknowledgments: The authors thank the two anonymous reviewers who contributed to enriching
this review with their advice.
Conflicts of Interest: The authors declare no conflict of interest.

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