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Patterns o f Diversity in Soft-B odied M eiofauna: Dispersal
Ability and Body Size Matter
Marco C urini-G alletti1, Tom Artois2, V alentina Delogu1, Willem H. De Smet3, Diego Fontaneto4'5,
Ulf Jondelius4, Francesca Leasi5'6, A lejandro M artin ez7, Inga M eyer-W achsm uth4, Karin Sara Nilsson4,
Paolo Tongiorgi6, Katrine Worsaae7, M . Antonio Todaro6*
1 D ipartim ento di Z oología e G enetica Evoluzionistica, U niversité di Sassari, Sassari, Italy, 2 C en tre fo r E nvironm ental S ciences, H asselt University, D iep en b eek , Belgium,
3 D e p a rtm e n t o f Biology, U niversity o f A ntw erp, Wilrijk, Belgium , 4 D e p a rtm e n t o f In v erteb rate Z oology, S w edish M useum o f N atural History, S tockholm , S w ed en ,
5 Division o f Biology, Im perial C ollege L ondon, A scot, U nited K ingdom , 6 D ip artim en to di Biología, U niverstità di M o d en a e R eggio Emilia, M o dena, Italy, 7 M arine
Biological S ection, University o f C o p e n h a g e n , H elsingor, D enm ark
Abstract
Background: Biogeographical and macroecological principles are derived from patterns o f distribution in large organisms,
whereas microscopic ones have often been considered uninteresting, because o f their supposed wide distribution. Here,
after reporting the results of an intensive faunistic survey o f marine microscopic animals (meiofauna) in Northern Sardinia,
we test for the effect o f body size, dispersal ability, and habitat features on the patterns o f distribution of several groups.
M e tho d o lo g y/P rincip a l Findings: As a dataset we use the results o f a workshop held at La Maddalena (Sardinia, Italy) in
September 2010, aimed at studying selected taxa o f soft-bodied meiofauna (Acoela, Annelida, Gastrotricha,
Nemertodermatida, Platyhelminthes and Rotifera), in conjunction with data on the same taxa obtained during a previous
workshop hosted at Tjärnö (Western Sweden) in September 2007. Using linear mixed effects models and model averaging
while accounting for sampling bias and potential pseudoreplication, we found evidence that: (1) meiofaunal groups with
more restricted distribution are the ones with low dispersal potential; (2) meiofaunal groups with higher probability of
finding new species for science are the ones with low dispersal potential; (3) the proportion o f the global species pool of
each meiofaunal group present in each area at the regional scale is negatively related to body size, and positively related to
their occurrence in the endobenthic habitat.
C onclusion/S ignificance: Our macroecological analysis o f meiofauna, in the framework o f the ubiquity hypothesis for
microscopic organisms, indicates that not only body size but mostly dispersal ability and also occurrence in the endobenthic
habitat are important correlates o f diversity for these understudied animals, with different importance at different spatial
scales. Furthermore, since the Western Mediterranean is one o f the best-studied areas in the world, the large number of
undescribed species (37%) highlights that the census o f marine meiofauna is still very far from being complete.
C ita tio n : Curini-Galletti M, Artois T, D elogu V, De S m et WH, F o n ta n e to D, e t al. (2012) P attern s o f Diversity in Soft-B odied M eiofauna: Dispersal Ability a n d Body
Size M atter. PLoS ONE 7(3): e33801. doi:10.1371/journal.pone.0033801
E d ito r: Philippe A rcham bault, U niversité d u Q u é b e c à Rimouski, C anada
R e c e iv e d A ugust 2, 2011; A c c e p te d F ebruary 17, 2012; P u b lis h e d M arch 23, 2012
C o p y r ig h t: © 2012 Curini-Galletti e t al. This is an o p en -ac cess article d istrib u te d u n d e r th e te rm s o f th e C reative C o m m o n s A ttrib u tio n License, w hich perm its
u n restricted use, distrib u tio n , a n d re p ro d u c tio n in an y m ed iu m , p ro v id ed th e original a u th o r a n d so u rc e a re cred ited .
F u n d in g : The w o rk sh o p a t La M addalena w as s u p p o rte d by a g r a n t fro m R egione S ard eg n a - P ro m o zio n e della ricerca scientifica e d ell'in n o v azio n e te cn o ló g ica
in S ard eg n a - a n d by c o n trib u tio n s from P arco N azionale A rcipelago di La M ad d alen a. T he fu n d e rs h ad n o role in s tu d y d esig n , d a ta co llection a n d analysis,
decision to p ublish, o r p re p a ra tio n o f th e m an u scrip t.
C o m p e tin g In te re s ts : T he au th o rs h av e d ec lared th a t n o c o m p e tin g in terests exist.
* E-mail: an to n io .to d aro @ u n im o re.it
Introduction
identify generalities in m acroecology a n d biogeography, regardless
o f phylogenetic constraints.
D u e to th eir taxonom ic diversity a n d species richness,
m icroscopic anim als (meiofauna) represent a n im p o rta n t b u t often
neglec ted c o m p o n e n t o f m arin e biodiversity [1]. M oreover, to date
large-scale taxonom ic surveys o f the actual con trib u tio n o f these
organism s to local diversity a n d analyses o f their correlates o f
diversity have rarely b e en attem p ted . T his is a n unfo rtu n ate
situation: m ost o f the m arin e biodiversity m ay reside in m eiofauna,
b u t th eir actual diversity is unknow n a n d so it is im possible to infer
the drivers o f diversity in the group. A dditionally, m ost o f the
anim al p hyla are rep resen ted in the m eiofauna [2]; therefore,
suites o f organism s from com pletely different evolutionary histories
are presen t in the sam e habitats, p roviding a n invaluable tool to
T h e aim o f this research is twofold. First, we provide an
a n n o ta te checklist o f soft-bodied m eiofauna from a m arine
p ro tec te d a re a o f the W estern M e d ite rran e a n s sea, a region
recognized as a m arin e biodiversity hotspot [3], Second, we
p erfo rm the first analysis o n the ecological a n d biological
correlates o f p attern s o f diversity in m arin e m eiofauna in a
m acroecological fram ew ork. Such analysis m ay be able to shed
light o n the generality o f the processes governing biodiversity in
o u r c hanging w orld.
T h e faunistic survey was carried out at L a M a d d a le n a M arine
N atio n al P ark (N orthern S ardina, Italy) in S eptem ber 2010 in the
course o f a 10-day w orkshop d u rin g w hich the follow ing tax a w ere
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studied: A coela, A nnelida, G astrotricha, N em erto d erm atid a,
Platyhelm inthes a n d R otifera. I t should be highlighted th a t
taxonom ical w ork o n these anim als relies o n observations o n live
m aterial; consequendy, the c u rre n t know ledge o n th em is
p articularly poor.
T h e m acroecological analyses, in addition to the S ard in ian data,
include d a ta o b tain e d on the sam e taxonom ic groups du rin g a
previous w orkshop held in S eptem ber 2008 in W estern Sw eden.
T h e Sw edish w orkshop was hosted a t T h e Sven L ovén C e n tre for
M a rin e Sciences o n the island o f T jä rn ö a n d saw the particip atio n
o f experts o f m ost m eiobenthic tax a including m ost o f the authors
[4], In a tw o-w eek p e rio d in T jä rn ö , 430 species o f m eiofauna
w ere found, w ith the discovery o f 157 species new to Sw eden a n d
27 new to science. By analysing two d a ta sets using identical
m ethods b u t covering different biogeographical areas (N orthern
Sardinia+ W estern Sw eden), we are able to search for generalities.
If generalities are p re sen t in the m acroecological processes driving
diversity in the different groups o f m eiofauna, we should observe
sim ilar p attern s in the two sam pling areas, n o tw ithstanding the
eco-physiographic differences b etw een them . A lternatively, if
correlates o f diversity are different b etw een the tw o areas, we
can infer th a t local forces outco m p ete global drivers in p ro d u cin g
p attern s o f diversity in m eiofauna.
A ccording to the ubiquity th eo rem , m icroscopic organism s are
m ore w idely distributed th a n larger ones, a n d the p ro p o rtio n o f
local species richness to the global species pool is negatively related
to b o d y size [5]; thus, the p robability to find new species w ith
restricted distribution should be low er in sm aller th a n in larger
organism s. Such a strong relationship betw een body size a n d
biodiversity p a tte rn s m ay be a m isrepresentation o f reality, a n d
o th er features o f th e organism s them selves or o f the env iro n m en t
m ay play a m ajo r role in driving diversification a n d distribution in
space [6]. T h u s, we used the tw o highly detailed faunistic lists o f
different phyla o f m arin e m eiofauna from N o rth e rn S ard in ia a n d
from W estern Sw eden to address the issue o f the im p o rtan ce o f
body size a n d o th er correlates o f diversity, using lin ear m ixed
effects m odels (LM EM s) to a cc o u n t for p otential pseudoreplication
[7], a n d m odel averaging [8] to asses the im p o rtan ce o f the
potential correlates.
m ark ed seasonality in the w ater tem p eratu re: w inter surface
tem p eratu res m ay reach the freezing p o in t a n d th ere is frequently
ice form ation, w hereas sum m er surface tem p eratu res m ay exceed
20°C. Salinity in the surface layer dow n to 20 m is affected by
currents a n d p recipitation. It varies b etw een 10 a n d 34%o. T h e
sedim ents are generally m ixed, ran g in g from fine m u d to coarse
gravel. T h ere are deep w ater Lophelia coral reefs in the n o rth ern
p a rt o f the area. N u m erous islands a n d islets provide exposed as
well as sheltered conditions; sandy coves a n d sandbars are presen t
in m an y places.
S a m p l in g
Northern Sardinia. Sam ples w ere collected betw een
S eptem ber 5th a n d 15th, 2010; m ost o f th em w ere collected from
the islands form ing the archipelago o f L a M addalena; additional
sam ples w here collected from stations located along the
no rth w estern coast o f S ardinia, i.e. C osta Paradiso a n d C apo
C accia (Figure SI). T h e investigated h abitats ra n g ed from littoral
beaches a n d rock pools to sublittoral sedim ents to a b o u t —37 m,
including m arin e caves. Sam ples from this a rea consisted m ostly o f
clean fine a n d coarse sand, w ithout m u d o f silt. L ittoral sam ples
w ere taken by h a n d o r w ith a p lankton net, sublittoral sam ples
w ere taken by scuba divers. D etailed inform ation o n sam pling
localities is given in T ab le S I.
Western
Sweden. Sam ples
w ere
collected
betw een
S eptem ber 2nd a n d 13th, 2007 m ostly a ro u n d the island o f
T jä rn ö (K oster archipelago); the sam pled habitats ra n g ed from
littoral beaches a n d rock pools to sublittoral m udflats, m ostly at
depths b etw een 0 a n d —38 m . L ittoral sam ples w ere m ostly taken
by h a n d or a p lan k to n -n et w hereas sublittoral sam ples w ere taken
by b o a t using a dredge o r W a ré n sledge. T h e m ajority o f the
sedim ent sam ples w ere rich in silt a n d m ud, a n d even sandy
sam ples h a d a strong co m p o n e n t o f silt, w ith som e noticeable
exceptions. D etails o n sam pling techniques a n d characteristics the
sam pling sites can b e found in W illem s et al. [4].
E xcept for sam pling w ithin L a M a d d a le n a M a rin e N ational
P ark (Ente P a rc o -p ro to c o llo /p erm it n. 2 7 6 8 /1 1 ), no special
p e rm issio n /p e rm its w ere need ed to collect these anim als, because
m eiofauna are m icroscopic, n o n -pathogenic anim als, field study
did n o t involve e n d an g ered species a n d sam pling was carried out
in public beaches. M oreover, no m eiofauna species are u n d e r
special conservation concerns.
M aterials and Methods
S tu d y A reas
S a m p l e a n d o r g a n i s m p r o c e s s in g
Northern Sardinia. T h e sam pling a rea is located in the
S trait o f Bonifacio, betw een S ardinia a n d C orsica (W estern
M e d ite rran e a n Sea; see Figure SI). W ater circulation in the
S trait is strongly controlled b y winds: c u rre n t intensity varies
betw een 0.10 a n d 0.50 m /s , w ith h igher values in shallow er areas
d u rin g the prevailing N -W M istral w ind [9]. W ater tem p e ra tu re
varies from 15°C in early spring to 25°C in sum m er. Salinity in the
a rea is co n stan t du rin g the year, ra nging 37.7-38.8% o. M axim um
tidal range is a b o u t 0.25 m [10].
T h e strong hydrodynam ics a n d the presence o f extensive
Posidonia oceanica seagrass m eadow s, dow n to a d e p th o f —40 m,
influence the sedim ents in the area, w hich show a gravelly-sand
com position, w ith m u d c o n te n t generally < 5 % , a n d a high C a C o 3
content, w ith m axim um values > 7 5 % [9]. Locally, less sever
h ydrodynam ic conditions favour the presence o f small sandy
beaches th a t in good n u m b e r characterize the coastline o f the
islands.
Western Sweden. T h e investigated areas is located in
n o rth e rn Skagerrak o n the b o rd e r b etw een N orw ay a n d
Sw eden. T id al am plitudes are 0 .1 -0 .4 m . T h e w ater circulation
is largely d e term in ed b y w inds a n d large-scale currents. T h e re is a
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D u rin g b o th w orkshops, sam ples w ere taken to the lab o rato ry
soon after collection a n d processed w ithin few days. Specim ens
w ere ex tracted daily using two different m ethods: b o th b y M g C l2d e can tatio n a n d by siphoning off the w ater ju st above the sedim ent
[2,4], Algae sam ples w ere rinsed w ith M gC l2. Live m aterial was
studied using dissecting a n d light m icroscopes. A dditional m aterial
for identification a n d /o r descriptive purposes was preserved using
m ethods ap p ro p ria te for the respective tax o n [11-16].
A detailed description o f the faunistic results from the S ardinian
w orkshop is provided in the first p a rt o f the results section; a
sum m ary list o f the soft-bodied m eiofaunal tax a found d u rin g the
Sw edish w orkshop is p rovided in T ab le S2 while exhaustive
in form ation c an be found in W illem s et al [4].
Statistical a n a ly s e s
T ak in g advan tag e o f the robust a n d com p arab le datasets offered
by the tw o w orkshops, we aim ed a t identifying the relevant
correlates o f the diversity p attern s in m eiofaunal organism s. W e
used linear m ixed effects m odels [17] a n d m odel averaging [8] to
investigate the effect a n d the im p o rtan ce o f a set o f biological a n d
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e nvironm ental variables as predictors o f different response
variables describing different facets o f biological diversity. W e
im plem ented four separate statistical analyses, each one using a
different response variable, acco u n tin g for geographic ran g e size,
n u m b e r o f new species unknow n to science, a n d ratio o f regional
to global a n d o f local to regional species richness, explained in
details below from (i) to (iv). As e x planatory variables, we used the
ones th a t could b e ecologically relevant a n d we o b tain e d estim ates
for six variables (explained in details below , from 1 to 6), from
m easurem ents taken from the organism s we collected, a n d /o r
from the literature. B oth the explan ato ry a n d th e response
variables w ere m easured separately for the two surveys in
N o rth e rn S ardinia a n d W estern Sw eden.
Explanatory variables. T h e y acc o u n te d for biological
(body size, dispersal p o tential, rep ro d u ctiv e m ode) a n d
e n v iro n m en ta l variables (habitat, substrate a n d depth). A n
estim ate o f (1) b o d y size (m edian b o d y length) for each species
was o b tain e d from the a d u lt individuals collected in the field
a n d /o r from lite ratu re d a ta (T able S2). T o estim ate the (2)
p o ten tial for dispersal, we collected in fo rm atio n o n p re se n c e /
absence o f resting or dispersing stages (T able S2); for the (3)
rep ro d u ctiv e m ode, we categorised organism s as exclusively
p a rth e n o g en e tic or n o t (T able S2). T o estim ate enviro n m en tal
variables, we used th ree different m etrics: (4) h a b ita t specificity,
(5) k ind o f substrate a n d (6) depth. F o r h a b ita t specificity, species
w ere g ro u p e d as exclusively en d o b en th ic (living only in the
sedim ents, either as interstitial o r borrow er) o r n o t (T able S 2); for
k ind o f substrate, we identified 18 categories d ep en d in g o n the
type o f sam ple (e.g. sedim ents w ith different g ra n u lo m etry such as
pebble, coarse sand, m ed iu m sand, fine sand, m ud, sût, or o th er
h abitats such as p erip h y to n , epibiont, etc.); as for depth, the
m ea su re d d e p th o f the sam ple was used (T able SI) a n d [4], T h en ,
we o b tain e d sum m ary statistics for these six variables for six
taxonom ic groups (Acoela, A nnelida, G astro trich a, P roseriata,
R h a b d o co e la a n d R otifera), w hereas N e m e rto d e rm a tid a w ere n o t
included, d u e to the taxonom ic uncertainties in the g roup a n d the
p au city o f in form ation in the lite ratu re. F or each v ariable we
calculated the follow ing sum m ary statistics, separately for
W estern Sw eden a n d N o rth e rn S ardinia: for b o d y size, the
m ed ia n value o f all species for each gro u p (no m easure o f
variability was included, because the coefficient o f variation,
sta n d a rd d e v ia tio n /m e a n , was well below 1 in all cases, except for
annelids in S ard in ia a n d rotifers in Sw eden); for dispersal
poten tial, the p ro p o rtio n o f species w ith resting o r dispersing
stages; for rep ro d u ctiv e m ode, the p ro p o rtio n o f species w ith
p a rth e n o g en e tic re p ro d u c tio n ; for h a b ita t specificity, the
p ro p o rtio n o f exclusively en d o b en th ic species; for k ind o f
h a b ita t, th e p ro p o rtio n o f types o f h a b ita t w here eac h group
was found, in co m p ariso n to the total n u m b e r o f types; for d epth,
the d e p th ran g e for each group, in co m p ariso n to the overall
d e p th range.
Response variables. D ifferent aspects o f biodiversity for
each o f the six taxonom ic groups could be influenced b y the
ex planatory variables th a t we assessed; we included four different
response variables for four different theoretical rationales in our
m odels, listed below from (i) to (iv).
G eographic distribution o f anim als is a function o f ecological
a n d historical variables; thus, we tested w h e th er the (i) geographic
range size o f the different taxonom ic groups was influenced b y the
six ecological variables we m easured. T o do so, we gro u p ed the
species we found acco rd in g to w h e th er they have w ide o r lim ited
biogeographical range, lim ited to the M e d ite rran e a n (for the
S ard in ian dataset) o r to the N o rth Sea - Baltic a rea (for the
Sw edish dataset); we th en used the p ro p o rtio n o f species w ith
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lim ited range as a response variable. T h e expectation is th a t
sm aller organism s w ith high dispersal poten tial are m ore widely
d istributed th a n larger ones w ith o u t dispersing stages.
W e acknow ledge th a t this analysis could be biased b y the large
am o u n t o f unknow n diversity in m eiofauna; thus, we applied also
an alternative rationale: (ii) if species have m o re restricted
distribution, the chance th a t a research er can find it is low er th an
for species w ith larger geographic ranges. T h u s, we m easu red also
the p ro p o rtio n o f species new to science for each taxonom ic group.
T h e expectation is, again, th a t organism s w ith high dispersal
poten tial are less likely to provide new species for science w hen
studying new areas.
O n e o f the expectations o f the u biquity th eo re m [5] is that,
locally, a large rep resen tatio n o f the global species pool is present:
if species are widely distributed, they also occur (almost) in any
place w here the en v ironm ental features suite them . T h u s, we
tested this assum ption a t two spatial scales: (iii) regionally, using as
response variable the p ro p o rtio n o f species found in the survey,
N o rth e rn S ardinia o r W estern Sw eden (regional diversity)
c o m p a red to the total n u m b e r o f species know n w orldw ide for
the tax o n (global diversity); (iv) locally, using the p ro p o rtio n o f
species found in each single sam ple (local diversity) c o m p a red to
the total n u m b e r o f species in the species pool for each a rea
(regional diversity), identified as the total n u m b e r o f species found
in each survey (N orthern S ardinia o r W estern Sw eden). T o reduce
the effect o f poten tial sam pling bias for hypotheses (iii) a n d (iv), we
re p ea te d the analyses using estim ates o f species richness instead o f
the actual observed richness, using the C h a o i estim ator from
incidence d a ta [18]. T his estim ator is able to reliably extrapolate
the poten tial n u m b e r o f additional species th a n can b e found in
the a rea b y fu rth er sam pling, given the actual observed n u m b e r o f
species a n d how m an y o f these have b e en found only once or
twice.
Statistical models. O th e r variables th a t could influence the
results o f the statistical analyses, w ith poten tial pseudoreplication,
are the tax a them selves a n d the sam pling site. T o be able to
acco u n t for a co m b in atio n o f such fixed a n d ra n d o m effects in the
m odels, we used L inear M ixed Effect M odels (LM EM s) th a t have
b e en designed exactly for these kinds o f analyses, w ith violations o f
the assum ption th a t d a ta are in d ep e n d en t [19]. T h u s, we
im plem ented several m odels, one for each o f the four response
variables, each one a ccounting for a different p roxy o f diversity,
nam ely (i) p ro p o rtio n o f species w ith restricted distribution, (ii)
p ro p o rtio n o f new species for science, (iii) p ro p o rtio n o f global
species pool found regionally a n d (iv) p ro p o rtio n o f regional
species pool found locally. A m ong the e x planatory variables, we
d isregarded the uninform ative ones th a t h a d no, o r alm ost no
variability in the dataset, or th a t w ere highly co rrelated w ith other,
m ore inform ative variables: thus, two variables w ere n o t included
in the m odels. T h e p ro p o rtio n o f parth en o g en etic species was not
included because it was co rrelated w ith b o d y size: only the groups
w ith the sm allest b o d y size, G astrotrichs a n d R otifers, h a d strictly
p arth en o g en etic species. D e p th was n o t re ta in e d because o f its low
variability am o n g taxonom ic groups: all groups h a d the sam e
d e p th range, from 0 to a b o u t —35 m , a n d only one sam ple at
—70 m co n tain ed acoels a n d one sam ple a t —50 m con tain ed
gastrotrichs. T h e structure o f the m odel was the sam e in the four
cases, w ith the ecologically m eaningful ex planatory variables for
each taxonom ic group a ccounting for four fixed effects: b o d y size,
p ro p o rtio n o f e ndobenthic species, p ro p o rtio n o f species w ith
dispersing stages, a n d p ro p o rtio n o f occupied h a b ita t types. T h e
taxonom ic group was included as a ra n d o m effect; the sam pling
site, w ith two levels only (N orthern S ardinia o r W estern Sw eden),
was included in the m odel as a fixed effect in o rd e r to obtain
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T h e tax o n o m y o f A coela a n d N e m erto d erm a tid a is p lagued by
the vague (by m o d ern standards) original descriptions o f m any
taxa. G iven the lim ited a m o u n t o f m orphological diagnostic
features, the topic o f species delim itation in the two tax a should be
readdressed, and, in m an y instances, recourse to m olecular
in form ation is deem ed fundam ental. T herefore, a t this tim e,
reports o f species outside the type locality should b e considered
w ith caution unless c o rro b o ra ted by nucleotide sequences.
Platyhelminthes: Proseriata (Table S4). T h e com position
o f P roseriata in the M e d ite rran e a n has received particu lar
attention. Fifty-seven p roseriate species are c u rren d y re p o rte d
from the n o rth e rn sector o f the central-w estern a rea o f the
M ed ite rran e a n , w here L a M a d d a le n a N atio n al p a rk is located
[31]. Intensive research in o th er areas o f S ardinia, C orsica, a n d
T u scan y [32] m akes the sector am o n g the b est studied in the
w orld.
N onetheless, o f the 34 species found, m ore th a n 50% (18) are
undescribed. M ost o f the new species belong to the g enera
Archimonocelis M eixner, 1938, Duplominona K arling, 1966, a n d
Parotoplana M eixner, 1938. Paradoxically, research o n these three
g enera has b e en particularly intense, even w ith the p ro d u c tio n o f
m o nographs based o n species from the central M e d ite rran e a n
[33-36]. O n e genus, Parotoplana, was p articularly well rep resen ted
in the sam ples, a n d m ost (7 o u t o f 10) o f the species found are new.
T w o o f th em b elong to the com plex Parotoplana renatae /macrostyla,
w hich includes a n u m b e r o f sim ilar, poorly delim ited tax a [28],
w hose taxonom ical resolution w ould benefit from the c o ntribution
o f m olecular inform ation.
T h e distribution o f m ost o f the know n species appears lim ited to
central-w estern M e d ite rran e a n . Indeed, the type locality (and, in
som e instances, the only locality from w hich the species was
know n) o f quite a few o f th em is located w ithin the L a M a d d a le n a
A rchipelago (Parotoplana geminispina D elogu & C urini-G alletti,
2009) o r in n e arb y C orsica (.Nematoplana corsicana C urini-G alletti
& M artens, 1992, Archimonocelis staresoi M artens & C urini-G alletti,
1993, A. meixneri M arten s & C urini-G alletti, 1993, Duplominona
corsicana M artens, 1984, D. longicirrus M artens, 1984) [33,34,37,38].
T w o o f the species o f u n c ertain taxonom ic attrib u tio n [i.e.
Coelogynopora c f gynocotyla Stem boek, 1924 a n d Monotoplana c f diorchis
M eixner, 1938) have a range th a t encom passes the A dantic coasts
o f E u ro p e [39,40]. H ow ever, specim ens o f M . cf. diorchis from the
M e d ite rran e a n differ in chrom osom e n u m b e r [4] from p o p u la ­
tions from n o rth e rn A tlantic, w here the type-locality (Kieler Bucht)
is placed [41]. C. gynocotyla is the only Coelogynopora Stem boek, 1924
w ithout copulatory a n d /o r accessory sclerotised structures, a n d
therefore lacks one o f the basic inform ation for species
discrim ination. A th o ro u g h revision o f the tw o taxa, w ith the
inclusion o f m olecular d ata, is therefore need ed before any
decision o f the status o f the populations from L a M a d d a le n a can
be attained.
Boreocelis cf. urodasyoides Ax, 1963 is tentatively a ttrib u te d to a
species w hose original description lacks crucial details o n the
m orphology o f the sclerotised structures a n d should be im ple­
m en te d w ith m ore inform ation o n specim ens from the type locality
(gulf o f Naples) [41]. O n e single specim en o f Philosyrtis sp. was
found, in b a d state o f preservation, m aking identification
impossible.
O verall, d a ta confirm the incom plete state o f know ledge o f the
P roseriata even in one o f the m ost studied areas o f the
M ed ite rran e a n . F u rth e rm o re , the finding o f num erous species
w hose distribution appears lim ited to the n o rth e rn sector o f the
central-w estern a rea suggests a high level o f endem ism o f
p roseriate taxa.
reliable estim ates o f v ariance [7,20,21]. All explanatory variables
w ere always re ta in e d in each analysis, a n d no m odel sim plification
was perform ed.
A binom ial distribution was assum ed in all m odels, as the
response variables are p ro p o rtio n d a ta . V alues o f C h ao estim ates
o f local a n d global diversity w ere ro u n d e d to the n earest integer to
allow the use o f binom ial distribution in all models.
T h e significance a n d im p ortance o f each explanatory variable in
the m odels w ere evaluated using m odel averaging as described in
B u rn h am a n d A nderson [8]. First, for each o f the four analyses, the
full m odel was generated; then, the set o f sub-m odels including all
possible com binations o f the ex planatory variables was generated,
a n d the relative im portance o f each variable was calculated, on a
scale from 0 to 1, as the sum o f the Akaike weights o f the sub-m odels
in w hich the variable appears; b e tte r m odels have larg er Akaike
weights, a n d a variable th a t contributes m ore to m odel fit will thus
have a higher relative-im portance value. P a ra m e te r estim ates a n d
unconditional stan d ard errors for each explanatory variable w ere
calculated by averaging over all sub-m odels in w hich the variable
appears, w eighting values from individual sub-m odels by the sub­
m odels’ Akaike weights. W e will base the significance o f the results
o n the m ore robust relative-im portance values from m odel
averaging, a n d n o t o n the p-values, m ore easily affected by the
structure o f the statistical m odels; nevertheless, w e will re p o rt b oth
values a n d discuss discrepancies, w hen present.
All analyses w ere p erfo rm ed w ith the statistic software R 2.13.2
(R D evelopm ent C ore T e a m 2011: h ttp ://w w w .R -p ro je c t.o rg ),
L M E M s w ith package lme4 0.999375-39 [22], C h a o estim ates w ith
package vegan 1.15-4 [23], a n d m odel averaging w ith package
M uM In 1.6.5 [24],
Results
S a rd in ian f a u n a a n d r e m a rk s
D etails on the selected soft-bodied m eiofaunal groups (Figure 1)
from the N o rth e rn S ard in ia w orkshop are p rovided below . T h e
com plete list o f species found in N o rth e rn S ardinia is given in
T ables S3, S4, S5, S6, S7, S8.
Acoela and Nemertodermatida (Table S3). T hese two
taxa, form erly classified w ithin Platyhelm inthes, are c u rren d y
re g ard e d as basal bilaterian clades [25-27], or, alternatively, as
dram atically red u ced deuterostom es [28].
By D ecem b er 2010, th ere w ere published records o f 56 species
o f A coela from the M e d ite rran e a n , 22 o f w hich from Italian
w aters. In com parison, 57 acoel species w ere re co rd e d ju st from
the littoral zone o f the 99 k m 2 G e rm an island Sylt, a n d 47 species
w ere re co rd e d from the 57 k m 2 G ullm aren fiord o n the Sw edish
w est coast (see h ttp ://a c o ela.m y sp ec ies.in fo a n d U J unpublished).
C learly acoel diversity in the M e d ite rran e a n is understudied, a n d
th ere is a n enorm ous poten tial for finding new species. T h e tw enty
species o f A coela found du rin g the w orkshop are, w ith the
exception o f two, new to science. T h e exceptions are Symsagittifera
corsicae G schw entner, B aric & R ieger, 2002, w hose type locality is
a t the n e arb y island o f C orsica [29], a n d Paratomella rubra R ieger &
O tt, 1971, a poten tial w idely distributed acoel.
N e m erto d erm a tid a w ere revised by S terrer [30]. T h e taxonom y
o f N e m erto d erm a tid a is particularly problem atic, w ith b roadly
defined n om inal species o f w hich th ree w ere previously re p o rte d
from the M e d ite rran e a n [30]. O f the five species o f N e m erto ­
d e rm a tid a found, only Nemertinoides elongatus R iser 1 9 8 7 - re p o rte d
by S terrer [30] from the M e d ite rran e a n (Rovinj, C roatia) - could
be d e term in ed w ith som e degree o f reliability. T h e others could
only be identified to genus level, p en d in g a revision o f the taxon
w hich takes into a cco u n t m olecular data.
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M eio fau n a B iodiversity
Figure 1. Representatives o f the soft-bodied m eiofaunal taxa considered in th e analyses. A, F la g e llo p h o ra sp. -N e m e re to d e rm a tid a ; B,
P ro po ru s sp. -A co e la ; C, Polycystis n a e g e lii -R h a b d o c o e la : D, P a ro to p la n a re n a ta e -P ro s e ria ta ; E, U rodasys v iv ip a ru s -G a s tro tric h a ; F, B ra c h io n u s ib e ricus R otifera ; M e so n e rilla in te rm e d ia -A n n e lid a . L ig h t m ic ro s c o p y p h o m ic ro g ra p h s , scale b ars A, C, E = 100 p m , B, D, G = 2 5 0 p m , F = 2 0 p m .
d o i:1 0.1371 /jo u r n a l, p on e .0 0 3 38 0 1 ,g001
Platyhelminthes: Rhabdocoela (Table S5). R h ab d o co ela
is a very species-rich tax o n o f rh a b d ito p h o ra n flatw orm s, w hich
can be recognised by a tru e p h a ry n x bulbosus a n d a specific
construction o f the p ro to n ep h rid ial flam e cell [13,42]. W orldw ide
ab o u t 1550 species are described, 60 p e rce n t o f w hich (about 930
species) are from m arin e o r brackish w ater. O n e h u n d re d a n d
seventy nine m arin e rh abdocoel species are know n from the
PLoS ONE I w w w .p lo s o n e .o rg
M ed ite rran e a n , 97 o f w hich are M e d ite rran e a n endem ics. N ot
included in these counts are the 17 species know n only from the
Black Sea. O f the 179 M e d ite rran e a n species, 146 occur in the
W estern M e d ite rran e a n , as defined b y Spalding et al. [43]. O f
these 146 species, 75 are endem ic for the W estern M ed ite rran e a n ,
at least as far as is know n a t present. T h e relative high n u m b e r o f
species know n from the W estern M e d ite rran e a n as c o m p a red to
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M eio fau n a B iodiversity
the rest o f the M e d ite rran e a n is clearly because o f sam pling bias,
as the coastal a rea o f M arseille was intensively sam pled by M ichel
B runet in the sixties a n d seventies o f the form er century, a n d m any
species, albeit only kalyptorhynchs, w ere described b y him in a
series o f papers [44-54], M oreover, a large study was published by
A x [55], in w hich he described several species from coastal salt
m arshes betw een N a rb o n n e a n d P erpignan. In literature, only
th ree species a re m en tio n ed from S ardinia: Trigonostomum
penicillatum (Schm idt, 1857), T. venenosum (U ljanin, 1870) a n d
Djeziraia euxinica (M ack-Fira, 1972) [14,56],
In the m aterial collected d u rin g the w orkshop at L a M add alen a,
54 species o f rhabdocoels w ere collected. T hirty-tw o o f these
species belong to the K alyptorhynchia, 22 to its sister taxon
D alytyphloplanida (for a taxonom ical overview o f the taxon
R h ab d o co e la see W illem s et al. [13]). A dditionally, a n unknow n
m em b e r o f (probably) the genus Ciliopharyngiella Ax, 1952, a taxon
o f un certain affinities, was also found. T his species is m en tio n ed in
T ables 1 a n d S5, b u t n o t furth er considered in the follow ing text.
O nly 20 o f the species found could b e identified as already
described. T h irte e n species w ere rep resen ted b y juveniles, o r by
specim ens th a t do n o t allow identification. It is therefore likely th at
the n u m b e r o f species new to science found (21) is to be considered
as a conservative estim ate.
Several o f the know n species found have a w ide distribution
across the M e d ite rran e a n a n d the A tlantic coasts o f E urope, the
m ost-studied areas in the w orld for turbellaria. H ow ever, one o f
these w ide-ranged species, Gyratrix hermaphroditus E hrenberg, 1831,
is a notorious exam ple o f cryptic diversity, p ro b ab ly co n tain in g a
large a m o u n t o f separate sibling species [57]. A detailed
know ledge o f the com position a n d range o f the siblings is still
lacking, a n d the specim ens found at la M a d d a le n a can only be
reliably identified in a m olecular revision o f the group, w hich is
presently u n d e r way.
Five o f the know n species a re W estern M e d ite rran e a n endem ics:
Austrorhynchus bruneti K arling, 1977, -4. karlingi B runet, 1965,
Carcharodorhynchus multidentatus B runet, 1979, Duplacrorhynchus mega­
lophallus Artois & Schockaert, 1999 a n d Rogneda colpaerti Artois,
2008, while six are re co rd e d for the first tim e for the
M e d ite rran e a n p ro p e r (excl. the Sea o f M arm ara). F o u r o f these
six w ere previously only fo und in the Black Sea a n d the Sea o f
M a rm ara , a n d p resum ably have a m o re w idespread, circum M e d ite rran e a n distribution: Baltoplana valkanovi A x , 1959, Progyrator
mamertinus G ra ff (1874) R eisinger, 1926, Promesostoma ensifer
(LHjanin, 1870) Pereyaslaw sew a, 1892 a n d Promesostoma maculosum
Ax, 1956. Cystiplana paradoxa Ax, 1954 was previously found in the
Black Sea, the Sea o f M a rm a ra a n d the island o f Sylt (E uropean
N . Atlantic), a n d p ro b ab ly has a n even w ider distribution. T h e
sixth species new to the M ed ite rran e a n , Trigonostomum australis
W illem s et al, 2004, was u p to now only found along the
A ustralian E ast C oast [56] a n d therefore ap p are n tly has an
extrem e disjunct distribution. H ow ever, the w orldw ide distribution
o f m icro tu rb ellaria is very poorly know n, a n d it could well be th at
the species is m u ch m ore w idespread. O n the o th er h a n d , it could
also be th a t the populations from the M e d ite rran e a n a n d A ustralia
will a p p e a r to be genetically separated, a n d actually represent
cryptic species. A sim ilar case is the finding o f Gyratrix proaviformis
S chockaert & K arling, 1977, a species hitherto only know n from
the Pacific coast o f the LTS (Oregon), in P u n ta N eg ra (Sardinia) in
M a rc h 2010 (B. S. Tessens & W . R . W illem s, pers. com m .). O n ly a
th o ro u g h b ro a d scale sam pling a n d the use o f m olecular
techniques can help to solve these intriguing cases o f widely
separated, ap p are n tly conspecific, populations, w hich are illustra­
Table 1. Number of species found in Northern Sardinia and in Western Sweden for each taxon.
N o . sp e c ie s fo u n d
U n d e s c r ib e d sp e cies
U n c e r ta in s ta tu s
Acoela
23
21
0
N em e rto d erm a tid a
5
0
4
1
N o r th e r n S a rd in ia
Taxon
Proseriata
34
18
R habdocoela
55
21
13
G astrotricha
60
17
6
Annelida*
13
2
4
Rotifera
16
0
5
203
76
33
Acoela
21**
6**
0
N em e rto d erm a tid a
6
2
0
Proseriata
21
3
0
R habdocoela
35
3
1
G astrotricha
43**
11
0
Annelida*
6
0
0
Rotifera
23
0
2
154
25
3
TOTAL N Sardinia
W e s te r n S w e d e n
Taxon
TOTAL W S w e d en
^Include only records from exclusively e n d o b e n th ic fam ilies.
''T h e original e s tim a te re p o rte d by Willems e t al [4] w ere low er. The c u rren t n u m b e rs are th e result o f s u b s e q u e n t ta x o n o m ic stu d ies o n add itio n al m aterial.
dol:10.1371 /journal, pone.0033801 .t001
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M eio fau n a B iodiversity
tive o f o u r lack o f know ledge as it com es to biogeography a n d
biodiversity o f m icroturbellaria.
Gastrotricha (Table S6). T h e phylum G a stro tric h a is
cosm opolitan w ith a pproxim ately 780 species divided into two
orders: M acrodasyida, w ith a b o u t 324 strap-shaped species, all b u t
two o f w hich are m arin e or estuarine a n d C h a eto n o tid a w ith
a b o u t 455 ten p in -sh ap ed species, over 30% o f w hich occur in salty
environm ents [58,59-63]. T h e Italian m arin e gastrotrich fauna
has b e en the focus o f m u ch research a n d nu m ero u s sam pling
cam paigns, and, w ith a pproxim ately 180 species re co rd e d in m ore
th a n 230 localities [64-66], ranks a m o n g the best know n in the
w orld. Indeed, am o n g m eiobenthic phyla, none enjoys such a
detailed know ledge o f species com position a n d distribution a ro u n d
the Italian coasts. Yet, o f the 60 species o f the phylum found
d u rin g the w orkshop, 17 species are still undescribed. T his n u m b er
includes also species found previously in the M ed iterran ean ,
aw aiting form al description, a n d does n o t entirely reflect species
unique to L a M a d d a le n a area. H ow ever, the discovery o f two new
species, belonging to two undescribed g enera th a t could n o t be
easily placed into any e x ta n t family, has b e en surprising, a n d
witnesses the incom plete state o f know ledge in the M e d ite rran e a n
even o f the G astrotricha. B oth these species w ere found in sam ples
collected into m arin e caves, w hich are confirm ed as hot-spots o f
diversity for the g roup [67,68].
F ro m a biogeographical p o in t o f view, m ost species a p p e a r to
have a w ide distribution across the M e d ite rran e a n [69] a n d the
A tlantic coasts o f E u ro p e w ith som e know n to b e regional
cosm opolitans (e.g. M acrodasyida: Acanthodasys aculeatus R em an e,
1927, Dactylopodola typhle (R em ane, 1927), Urodasys viviparus W ilke,
1954 etc.; C haeto n o tid a: Aspidiophorus paramediterraneus H u m m o n ,
1974, Heteroxenotrichula pygmaea (R em ane, 1934) etc.). T w o species
are re p o rte d here for the second tim e along the Italian coasts: one
species, Diplodasys sanctaemariae H u m m o n & T o d aro , 2009,
originally described from A pulia b u t know n also from the
L evantine B asin [65]; the other, Tetranchyroderma aapton D al Z otto,
G hiviriga & T o d aro , 2010, recently described from C ap o C accia
[66], a S ardinian locality n o t too far from the c u rre n t sam pling
area; how ever, a t C osta Paradiso the species appears m ost
a b u n d an t. O f p a rticu la r interest is the finding o f Acanthodasys cf
caribbeanensis H o c h b e rg & A th erto n , 2010, w hich constitutes the
first re p o rt o f the species for the M e d ite rran e a n [70]. T h e
taxonom ic status o f the pop u latio n found a t L a M ad d alen a, will
how ever b e assessed o n com parison w ith the C a rib b e an w orm s on
the basis o f m olecular genetics.
A t h igher taxonom ic level it m ay be noticed th a t w hile the
highly diversified T h au m asto d erm atid ae [71] is well rep resen ted
in o u r sam ples, it is n o t so for the second- a n d third-m ost speciose
m arin e g astrotrich families, as T u rb an e llid ae a n d M acrodasyidae
are p re sen t a t L a M a d d a le n a w ith only five species each. W ithin
these tax a the genus Macrodasys R em an e, 1924 (M acrodasyidae) is
especially u n d er-rep resen ted w hilst Turbanella Schultze, 1853
(T urbanellidae) is a b sen t altogether.
M a rin e gastrotrichs are strictly interstitial organism s (with few
exceptions), consequently o u r sam pling efforts usually focus on
clean sandy sedim ents collected from very shallow areas (1-3 m
w ater depth); the relevance o f the a b u n d a n t a n d diverse fauna
yielded b y som e o f the sedim ents collected d u rin g the w ork-shop
held a t L a M a d d a le n a strongly calls for w idening the surveys to
d eep er sedim ents usually neglected in gastrotrich faunistic
investigations.
Annelida (Table S7). A nnelida contains m o re th a n 17000
species w orldw ide, w idely spread am o n g m arine, lim nic a n d
terrestrial environm ents [72,73]. M ost m arin e representatives o f
the group belong to the m acrofauna, a n d their com position a n d
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distribution along the Italian coasts is considered to be adequately
know n [74], M eiofaunal tax a b elong to several, u n re la te d groups
[75], a n d have b e en studied far less [74],
T his investigation focused o n exclusively interstitial families, a n d
did n o t com prise the interstitial representatives o f m acrofaunal
families. M em bers o f N erillidae, P rotodrilidae, Psam m odrilidae
a n d Polygordiidae w ere recorded, w ith a total o f th irteen species.
Seven species w ere collected a t the coastal stations a t L a
M a d d a le n a a n d C osta P aradiso a n d eight a t C ap o C accia (Nereo
cave). O nly four o f these are previously re p o rte d from the
M e d ite rran e a n Sea [74], in dicating a hitherto unseen diversity o f
b o th know n a n d unknow n m eiofaunal A nnelida in the M e d ite r­
ranean.
A m ong N erillidae, Nerillidium mediterraeum R em an e, 1928 a n d
Mesonerilla intermedia W ilke, 1953 w ere the m ost a b u n d a n t taxa.
B oth species have b e e n re p o rte d previously from several E u ro p ea n
locations in the A tlantic a n d M ed ite rran e a n . In the p re sen t study
Nerillidium mediterraneum was collected a t six stations, M . intermedia at
five, a n d M . armoricana Sw edm ark, 1959 a n d M . biantennata Jo u in ,
1963 a t two. T h e m ost rem arkable findings o ccurred in the N ereo
C ave, w hich show ed a g reat diversity o f nerillids. T hese included a
new species o f Mesonerilla w ith long palps a n d pygidial cirri.
Mesonerilla spp. have previously b e en re co rd e d in o th er cave
systems o f the A tlantic [15,76] as well as in Pacific hyd ro th erm al
deep sea vent areas [77]. T ak in g into acc o u n t th a t this genus is
p e n d in g revision [78] a n d m ay tu rn o u t paraphyletic, it still seems
highly plastic a n d suggesting a n interesting zoogeographical
history. Single ju venile specim ens o f Meganerilla B oaden, 1961
a n d Trochonerilla T zetlin a n d S aphonov 1992 w ere also reco rd ed at
the N ereo cave. Meganerilla sp. resem bles the N o rth A tlantic M .
swedmarki B oaden, 1961 by the lack o f m edian an te n n a.
Trochonerilla is so far m onospecific, how ever, furth er m aterial is
necessary to determ in e the species status. It is n otew orthy th a t this
is the first finding o f Trochonerilla outside tropical aquarium s
(including the type locality o f the M oscow A quarium ). T his
M e d ite rran e a n finding therefore m ost likely represents a new
species, geographically d istant from the presu m ed n atural, far-east,
tropical h a b ita t o f T. mobilis T zetlin a n d Saphonov, 1992.
Several specim ens belonging to Polygordius w ere also found in the
N ereo cave gravel sedim ents, w hich is the first reco rd o f
Polygordiidae from a cave. T h e lack o f specim ens w ith the
pygidium in ta c t p re v en ted fu rth er identification, how ever, several
species o f Polygordius are previously rep o rte d from the M e d ite rra ­
n ean, including Italy [7 9].
T h re e species o f P ro to d rilid ae w ere found, always w ith low
ab u n d an ces: P. gracilis V o n N o rd h e im , 1989, P. similis Jo u in , 1970
a n d P. purpureus (Schneider, 1868). Protodrilus gracilis was re co rd e d
a t th ree stations a t L a M a d d a le n a, always in coarse sandy
environm ents. T h is species w as previously re p o rte d from the
M e d ite rra n e a n b a y o f N aples (Italy) a n d B anyuls-sur-M er
(France), as well as from the A tlantic coasts o f n o rth e rn E u ro p e
[80]. Protodrilus similis, from in tertid al fine sandy sedim ents at
P u n ta R ossa, was previously re p o rte d from sou th ern M e d ite rra ­
n e a n a t G u lf o f T u n is (Tunisia) a n d the A tlantic a t A rc h ac h o n
b a y (France). Protodrilus purpureus is here re co rd e d for the first tim e
from m arin e caves, how ever several M e d ite rra n e a n records exist
[8 1 ].
Psammodrilus from C avaliere b a y represents the second re co rd o f
the genus in the M e d ite rran e a n besides P. balanoglossoides Sw ed­
m ark, 1952 [81]. Psammodrilus sp. differs significantly from the
sim ilarly small sized A tlantic E u ro p ea n P. fauveli (Sw edm ark,
1958), b u t is surprisingly sim ilar in b o th m orphology a n d
p relim in ary D N A com parisons to the recently described W est
A tlantic, B erm udian, P. moebjergi W orsaae a n d S terrer, 2006.
7
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M eio fau n a B iodiversity
Rotifera (Table S8). R o tifera are gro u p o f m icroscopic
aqu atic anim als w ith a b o u t 2000 described species. M ost rotifers
live in freshw ater a n d lim no-terrestrial habitats, a n d only ab o u t
400 species have b e en found in saline w aters so far [16,82,83].
Surprisingly, very few taxonom ic a n d faunistic studies have dealt
w ith m arin e rotifers, a n d m ost o f the p re sen t know ledge on rotifer
distribution is lim ited to the freshw ater h abitat.
T h e geographical distribution o f the brackish a n d m arine
rotifers (as well as th a t o f m ost freshw ater ones) largely reflects the
distribution o f rotifer investigators [84,85], consequently lim iting
biogeographical com parisons. N evertheless, the M e d ite rran e a n is
one o f the best know n areas in the w orld, b u t few specific
investigations have b e en c arried o u t in Italy [86]. A lm ost every
new study dealing w ith m arin e rotifers from the M e d ite rran e a n
a n d Italian coasts is likely to reveal new species to the a rea o r to
science [87,88].
T h e habitats we sam pled in N o rth e rn S ardinia (T able SI)
p rovided 16 species o f rotifers based on m orphological criteria.
Five o f th em w ere identified to genus level only, a n d can be
potential new species to the a rea or to science. A m ong the o th er 11
species, two are new for the Italian m arin e fauna, b u t w ere already
know n from the M e d ite rran e a n (T able S8).
R otifers notoriously host a large h id d en diversity, w ith several
cryptic species for m an y m orphospecies [89]. T hus, we used D N A
taxonom y to identify som e o f th em a n d to look for p otential
cryptic taxa, by am plifying a n d sequencing a fragm ent o f the
cytochrom e c oxidase subunit I (COI) from few individuals o f each
sam ple.
T h e species com plex Brachionus plicatilis M üller, 1786 is presen t
in the M e d ite rran e a n a n d it m ay b e difficult a n d am biguous if not
im possible to identify som e o f its cryptic tax a from m orphology
only. D N A taxonom y identified one o f o u r sam ples as belonging to
B. ibericus C iros-Peréz, G óm ez & S erra, 2001 (T able S8, G enB ank
accession num bers H Q 4 4 4 1 7 1 -H Q 4 4 4 1 7 2 ), a m em b e r o f the
group o f small-sized species in the com plex. U n c o rrec ted genetic
distances betw een o u r sequences a n d the ones available in
G e n b an k ra n g ed from 0.0 to 3.7% . T his species has never been
found in Italy before, a n d was know n only from Spain, G reece a n d
the U n ite d K in g d o m so far [90-92].
B oth Brachionus urceolaris M üller, 1773 a n d Lecane bulla (Gosse,
1851) are euryhaline species [82], a n d the C O I sequences o f b o th
confirm ed th a t o u r m arin e sam ples b elong to these m orphospecies
(G enB ank accession n u m b ers for B urceolaris: H Q 4 4 4 1 6 9 H Q 4 4 4 1 7 0 ; for L. bulla-, H Q 444174). N evertheless, D N A
taxonom y suggested also th a t o u r m arin e populations m ay be
cryptic tax a different from the ones previously sequenced from
freshw ater habitats, as u n co rre c te d genetic distances betw een the
m arin e a n d freshw ater ones a re com p arab le to the distances
betw een cryptic tax a o f o th er rotifer species com plexes th a t have
b e en tested for reproductive incom patibility [93,94], D istances
w ere betw een 18 a n d 21% for B. urceolaris [95-97] a n d betw een 8
a n d 17% for L. bulla [96,98,99].
T h e sequences we obtained for Testudinella clypeata (Müller, 1786)
are the first ones available (GenBank accession num bers H Q 4 4 4 1 6 6 H Q 444168), so we cannot test its identification using D N A
taxonom y. All individuals we found w ere m orphologically hom oge­
neous; nevertheless, we could identify two cryptic species, w ith genetic
distances o f 20% . T his is quite a high distance, as the distance
betw een the latter two cryptic species a n d the only other species with
available C O I sequences, T. pedina (H erm ann, 1783), is 28%.
in T ab le 1. T h e com plete list o f species found in W estern Sw eden
is re p o rte d in T ab le S2; for general com m ents on these tax a refer
to [4],
In general, soft-bodied m eiofauna is richer in N o rth e rn S ardinia
th a n in W estern Sw eden (203 vs 154 species); this is particularly
tru e for strictly interstitial tax a such as G astro trich a (60 vs 43 spp);
on the o th er h a n d , tax a know n to p refer fresh- o r brackish w aters,
such as rotifers, are less a b u n d a n t in the M e d ite rran e a n sam ples
(16 vs 23 spp). A coela a n d N e m erto d erm a tid a a re p re sen t in the
two areas w ith a vey sim ilar n u m b e r o f species (23 vs 21 spp a n d 5
vs 6 spp respectively). O v e r 37% o f the species found in S ardinia
ap p e a r to be undescribed taxa, a lthough h a lf o f th em require
ad ditional studies; in co n trast to the status o f only 16% o f the
species found in Sw eden considered as undescribed.
C o rre l a te s o f b iolo gic al d iv ersity
T h e potential ex planatory variables included in the m odels,
nam ely body size, p ro p o rtio n o f end o b en th ic species, p ro p o rtio n
o f species w ith poten tial for dispersal, a n d p ro p o rtio n o f o ccupied
ha b ita t types, controlling for sam pling site a n d taxonom ic group,
pro v id ed evidence o f significant global forces driving p attern s o f
diversity, acting in the sam e w ay in different geographical areas.
T h e statistical m odels significantly explained v ariance in the four
descriptors o f diversity we used as response variables (T able 2),
nam ely p ro p o rtio n o f species w ith restricted geographic range,
p ro p o rtio n o f new species, regional to global p ro p o rtio n a n d local
to regional pro p o rtio n .
T h e p ro p o rtio n o f species w ith restricted distribution in each
taxonom ic group ra n g ed from 0 to 95% a n d was significantly
negatively related to the p ro p o rtio n o f species w ith dispersal
abilities (T able 2-i): taxonom ic groups w ith m ore species able to
disperse (e.g. rotifers a n d annelids) are the groups w here less
species are restricted in their distribution a n d w here m ore species
have w ide distributions. T h e p ro p o rtio n o f species w ith restricted
distribution was overall higher, b u t only m arginally significantly, in
S ardinia (69%) th a n in Sw eden (41%) (T able 2-i); m oreover, the
low relative-im portance value for this p re d ic to r dem onstrates a
low effect o f the differences b etw een N o rth e rn S ard in ia a n d
w estern Sw eden o n the p attern s o f d istribution o f m eiofauna.
T h e p ro p o rtio n o f species new to science ra n g ed from 0 to 90%
in different taxonom ic groups a n d show ed a sim ilar scenario,
negatively related to the p ro p o rtio n o f species w ith dispersal
abilities (T able 2-ii): the probability o f finding new species in new
surveys is h igher in taxonom ic groups w here dispersing stages are
n o t present, e.g. acoels, proseriates a n d gastrotrichs. T h e
p ro p o rtio n o f new species for science for the soft-bodied
m eiofauna was significantly higher in S ardinia th a n in Sw eden
(T able 2-ii), especially for tax a such as A coela (91% vs 29%),
P roseriata (55% vs 14%) a n d R h a b d o co e la (50% vs 9%).
T h e p ro p o rtio n o f the global species pool rep resen ted a t the
regional scale show ed significant p attern s w ith high relativeim p o rtan ce values only w h en a ccounting for potential sam pling
bias by using C h ao estim ates instead o f the actu al observed
n u m b e r o f species (T able 2-iii, iii a). U sing C h ao estim ates as
descriptors o f regional species diversity, body size h a d a negative
influence, w hereas the p ro p o rtio n o f species th a t are exclusively
end o b en th ic h a d a positive influence. T h e regional representation
o f the global species pool is h igher in groups w ith small body size
a n d m ostly living as endobenthic.
T h e p ro p o rtio n o f the regional species pool found in each single
sam ple show ed significant p a tte rn s related to body size a n d
dispersal abilities only w hen a ccounting for poten tial sam pling bias
by using C h ao estim ates for regional richness (T able 2-iv, iv a),
O v e rv ie w o f t h e t w o w o r k s h o p s
A sum m ary o f the faunistic results from b o th sam pling
cam paigns in N o rth e rn S ardinia a n d in W estern Sw eden is given
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Table 2. Model-averaged parameter estimates.
0)
(ii)
R e s tric te d d is t r ib u t io n
N e w sp e cies
E s tim a te
E s tim a te
± SE
Rl
P
± SE
Rl
P
(Intercept)
- 0 .4 4 ± 0 .4 3
-
0.310
-0 .7 1 ± 0 .6 4
-
0.266
Body size
0.11 ± 0 .1 0
0.09
0.264
—0 .1 9 ± 0 .1 2
0.21
0.067
D ispersal
- 1 .7 1 ± 0 .5 4
0 .9 6
0 .0 0 1
H abitat ty p e s
0.32 ± 0 .9 6
0.13
0.739
E ndobenthic
0.58 ± 0 .6 3
0.09
Sam pling site
- 0 .4 6 ± 0 .2 5
0.49
- 3 . 7 8 ± 1 .6 0
0 .9 7
0 .0 1 8
- 0 .4 9 ± 1 .8 9
0.12
0.791
0.357
- 0 .7 5 ± 0 .9 9
0.05
0.450
0.041
—0 . 9 6 ± 0 . 3 4
0 .9 7
0 .0 0 4
(iii)
(iii a)
R e g io n a l/g lo b a l
R e g io n a l/g lo b a l (C h a o )
E s tim a te
E s tim a te
± SE
Rl
P
± SE
Rl
P
(Intercept)
- 3 .2 8 ± 0 .4 2
-
< 0.001
- 0 .4 4 ± 0 .4 3
-
0.001
Body size
—0 .1 9 ± 0 .1 2
0.21
0.106
- 0 . 9 1 ± 0 .1 3
1 .0 0
< 0 .0 0 1
Dispersal
—0 .2 8 ± 0 .5 5
0.07
0.615
1.82 ± 1 .1 4
0.07
0.112
H abitat ty p e s
0.95 ± 0 .3 3
0.84
0.003
0.30 ± 0 .2 0
0.10
0.130
0 .9 4
0 .0 0 2
0.00
N/A
E ndobenthic
Sam pling site
—0.07± 0.51
0.05
0.885
1 . 8 4 ± 0 .5 9
—0 1 6 ± 0 .2 4
0.18
0.510
N/A
(iv)
(iv a)
L o c a l/r e g io n a l
L o c a l/r e g io n a l (C h a o )
E s tim a te
E s tim a te
± SE
Rl
P
± SE
Rl
P
(Intercept)
- 1 .9 2 ± 0 .3 2
-
< 0.001
—3 .1 4 ± 0 .7 2
-
<0.001
Body size
0.09 ± 0 .1 5
0.11
0.523
0.39 ± 0 .1 7
0.44
0.027
Dispersal
0.50 ± 0 .5 0
0.17
0.315
1.21 ± 0 .5 4
0.49
0.027
H abitat ty p e s
-0 .2 1 ± 0 .8 4
0.09
0.803
0.74 ± 1 .4 0
0.17
0.598
E ndobenthic
0.16 ± 0 .6 3
0.09
0.795
- 0 . 1 6 ± 1.03
0.07
0.875
Sam pling site
- 0 .3 5 ± 0 .4 3
0.17
0.310
- 0 .6 5 ± 0 .3 4
0.33
0.0061
R elative-im portance values (Rl) an d p-values for th e six m odels w ith all ecologically relev an t variables retain ed in th e m odels. Identification co d e s from (i) to (iv) refer to
th e fo u r m odels explained In th e text; co d e s follow ed by 'a ' refer to analyses using C hao estim ates o f regional diversity. P aram eters w ith high relativ e-im p o rtan ce values
are h ig h lig h te d In bold.
dol:10.1371 /journal.pone.0033801 .t002
even if none o f the variables h a d high relative-im portance values
as predictors o f the m odel.
U n d e s c r i b e d d iv ersity
O f the 203 species found in N o rth e rn Sardinia, 76 (about 37%
o f the total) have b e en recognized as previously undescribed by
authorities in their field. As im pressive as the percentage m ay be, it
m ay tu rn out to be a conservative estim ate. In fact, a relatively
high, ad ditional n u m b e r o f species (33) could not b e identified w ith
certainty, due to the fact th a t the m aterial was inadequate, o r the
specim ens found belonged to groups w here revisions are pending,
a n d a p o rtio n o f th em m ay tu rn out to b e new species as well. In
com parison, du rin g the w orkshop held a t T jä rn ö in 2007, for the
sam e tax a considered here, 143 species w ere found, only 13 o f
w hich w ere new to science. T h e T jä rn ö w orkshop sp an n ed a
longer tim e, a n d the sam pling effort was rem arkably m ore intense:
d u rin g a two w eek period, alm ost 100 sam ples w ere sorted, from
littoral beaches, rock pools a n d different types o f sublittoral sand
a n d m udflats, to a d e p th o f ab o u t 90 m o n Lophelia reefs [4],
Discussion
T w o m ain results w ere p ro d u c ed by the detailed taxonom ic
surveys in N o rth e rn S ardinia a n d in W estern Sw eden. First, the
n u m b e r o f new , still undescribed species is high even in wellstudied areas; second, the p attern s o f diversity in m eiofauna have
strong m acroecological correlates, such as b o d y size, dispersal
ability a n d o ccurrence in endobenthic h a b ita t. As hypothesised,
these m acroecological correlates overcom e the effect o f local
variables; the only significant differences in the p a tte rn s o f diversity
betw een N o rth e rn S ardinia a n d W estern Sw eden refer to the
a m o u n t o f undescribed diversity. T h is issue deserves additional
explanations, w hich we provide in the follow ing p a rag ra p h .
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negatively co rrelated to b o d y size [5]. B ody size in the m eiofaunal
organism s analysed in N o rth e rn S ardinia a n d W estern Sw eden
ra n g ed from 0.08 m m to 13 m m , encom passing th ree orders o f
m agnitude. T h u s, its absence from the im p o rta n t explanatory
variables is n o t due to lack o f variabüity, b u t to a n actual p attern :
the absence o f dispersing stage b u t n o t b o d y size influences the
pro b ab ü ity o f finding new species w ith restricted distribution in
m eiofauna. T hus, furth er studies aim ed a t describing diversity in
m arin e m eiofauna should focus prim arü y o n such organism s in
o rd e r to provide new d a ta for the accu rate description o f m arine
diversity.
F u rth e rm o re , the w orkshop hosted a greater n u m b er o f research­
ers, w ho w orked on different sedim ents a n d habitats a t the sam e
tim e, sharing findings am o n g each other. Y et, the n u m b e r o f new
species in N o rth e rn S ardinia is m u ch higher, b o th in absolute a n d
in relative term s.
D ifferences in b o th the total n u m b e r o f species a n d in the
p ro p o rtio n o f undescribed species found d u rin g the w orkshops are
rem arkable. T hese differences m ay reflect reality o r m ay be
artefacts o f sam pling effort. T h e effect o f sam pling bias a n d
sam pling effort is a know n pro b lem in all biodiversity inventories,
even in w ell-know n organism s such as birds a n d g ro u n d beetles
[100,101], b u t becom es massive in inconspicuous m eiofaunal
organism s [102]. Interestingly, the p ro p o rtio n o f undescribed
diversity was different b etw een the tw o w orkshops only for acoels,
proseriates a n d rhabdocoels, a n d h igher in S ardinia. G iven th a t
Sw eden has a long history o f taxonom y on acoels a n d flatw orm s
[103-105], it is n o t surprising th a t m ost o f the species in these
th ree groups have already b e en discovered a ro u n d the island o f
T jä rn ö .
M ost o f the subtidal sam ples exam ined d u rin g the w orkshop
held a t T jä rn ö w ere taken by a dredge or a W aré n sledge [4], the
sam ples w ere later stored in large plastic boxes in a cold room , in
o rd e r to allow the anim als to craw l to the surface o f the sedim ent.
T h e w hole process, how ever, m ay have pro v ed noxious to m inute
a n d fragüe organism s. O n the c ontrary, the sedim ents studied in
L a M a d d a le n a w ere carefully a n d m anually collected by scubadivers from the oxygenated surface layers only, in o rd e r to
m inim ize a n y d am age to interstitial organism s. M icrohabitats
representing the greatest diversity o f sedim ent could therefore also
be selectively chosen b y the divers, a n d interm ixing o f habitats
avoided. T his m eth o d is also far m o re efficient for ex tracting
anim als lim ited to a co n ce n tra ted surface layer a n d allows for
im m ediate processing o f the sedim ent yielding a m ore vivid a n d
possibly rich er fauna. M oreover, there m ay be a role o f previous
know ledge in the area: the census o f m arin e fauna a t T jä rn ö is
und o u b ted ly m ore com plete th a n in a n y site o f the M ed iterran ean .
T jä rn ö lies in a n intensely studied area, w ith the presence o f
num erous, closely located M a rin e Biological Stations (to quote the
m ost fam ous, H elsingor (D enm ark), Sylt (G erm any); Sven Loven
C entres a t K ristin eb erg a n d T jä rn ö itself (Sweden). O n the
contrary, M a rin e Biological Stations in the M e d ite rran e a n are far
fewer a n d farth er a p a rt - in the case o f L a M ad d alen a, the
w orkshop was hosted in th ree ad ja ce n t re n te d flats, a n d
m icroscopes w ere personally carried by the researchers involved.
T h e lack o f suitable, coastal locations w here sam ples can be
processed affects p articularly the know ledge o f soft-bodied
m eiofauna, w hich needs to be studied alive. N evertheless, the
n u m b e r o f species in N o rth e rn S ardinia was h igher th a n in
W estern Sw eden.
D ifferences betw een the two surveys are in d eed present: in the
kind o f h a b ita t (mostly silt a n d m u d in Sw eden, a n d clean sand in
Sardinia), in sam pling techniques (mostly related to the differences
in the sedim ents them selves), in the clim ate, in the latitudinal
position a n d in the biogeographical a re a (see discussion in the last
section). N otw ithstanding these obvious differences, o u r m acro ­
ecological analyses revealed co m m o n p attern s o f diversity
correlating w ith the sam e variables in the two areas: the n u m b er
o f new, undescribed species w ith restricted distribution is higher in
taxonom ic groups w ith no dispersing stage regardless o f size o f the
organism s. T h e fact th a t size o f the organism s did n o t correlate
w ith the n u m b er o f new species p e r group is in contrast to the
ubiquity hypothesis. A ccording to this parad ig m , sm aller o rg a n ­
isms should have w ider geographical ranges, a n d thus, the
pro b ab ü ity o f finding new species in local sam ples should be
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P a t t e r n s o f div ersity in s p a c e
T h e presence o f dispersing ability, body size, a n d the
end o b en th ic h a b ita t w here the organism s live are significant
correlates o f species distribution in space a t different scales.
D ispersal abüities influence the p a tte rn s o f distribution, as
expected from the ubiquity hypothesis [5,6]; this result is robust
a n d consistent, given the high relative-im portance values in the
m odels (T able 2-i, ii) a n d the fact th a t such capabüity is an
im p o rta n t p re d ic to r for b o th the p ro p o rtio n o f species w ith
restricted distribution a n d for the p ro p o rtio n o f species new to
science. O n the o th er h a n d , small, strictly end o b en th ic species,
b o th in N o rth e rn S ard in ia a n d in W estern Sw eden, have a high
rep resen tatio n o f the global species pool a t the regional scale. T h e
fact th a t small organism s have a high regional to global p ro p o rtio n
is in accordance w ith the u biquity hypothesis [5,6]: o u r results
support the scenario that, if organism s are small, m ost the
avaüable global species pool wül be found sam pling different
h abitats a t a regional scale. A t the largest scale, th a t is c o m paring
N o rth e rn S ardinia a n d W estern Sw eden (regional diversity) w ith
the overall w orldw ide diversity (global species pool) o f each
m eiofaunal group, a larg er rep resen tatio n o f the global species
pool is p re sen t in sm aller m eiofaunal groups, as expected from the
ubiquity hypothesis [102]. Still this significant correlation could be
due to taxonom ic bias, w ith a b e tte r taxonom ic resolution in larger
organism s, a n d a h igher degree o f hid d en diversity in sm aller th an
in larg er m eiofaunal organism s [89,106,107].
T h e relative influence o f body size in structuring diversity in
space changes a t different spatial scales. A t the local spatial scale,
the n u m b e r o f species found in each sam ple in p ro p o rtio n to the
potentially avaüable ones for each o f the two areas (regional
species pool) is n o t related to any o f the analysed predictor, not
even to body size or to the end o b en th ic habit. T hus, b o d y size,
negatively related to spatial distribution a t the regional to global
scale, becom es non-influential a t the local to regional scale. T his
fact could be explained by the following scenarios: m eiofaunal
groups w ith larger b o d y size can m ove freely a t the local to
regional spatial scale, a t least as m u ch as the ones w ith sm aller
body size. O n the o th er h a n d body size m ay becom e a lim iting
factor to dispersal from the regional to global spatial scale. T his
p a tte rn is consistent b etw een N o rth e rn S ardinia a n d W estern
Sw eden, w ith no differences b etw een the two areas.
D iffere n c es b e t w e e n N o r th e r n Sardinia a n d W e s t e r n
Sw eden
W hilst sim ilarities exist in the diversity p a tte rn s in m eiofauna in
these two areas, several differences are in d eed present. O th e r th an
sam pling effort a n d poten tial bias in taxonom ic know ledge already
discussed, th ere are differences in the kind o f h abitat. M ost o f
sedim ents collected in N o rth e rn S ardinia ra n g ed from clean, fine
to coarse sand, to shelly gravel, including m arin e caves. T h is type
o f sedim ent favours tax a such as P ro seriata [108], G astrotricha
[12], A nnelida [75] a n d A coela [4], C onversely, m ost o f the
10
M arch 2 0 1 2 | V o lu m e 7 | Issue 3 | e33801
M eio fau n a B iodiversity
sedim ents collected a t T jä rn ö w ere m u ch siltier, consisting, in
m an y cases, o f m u d d y sand [4], W ater salinity is also different
betw een the two investigated areas a n d m ay acco u n t for the
re co rd e d faunistic differences. L ow salinity values a n d am ple
v a riation o f this physicochem ical factor are know n to have an
adverse im p act o n m eiofauna biodiversity [2]. T h e salinity a t the
littoral a n d shallow sublittoral stations o f T jä rn ö m ay vary from 10
to 34%o over the y ear while in S ardinia it is a b o u t 38%o the year
aro u n d , w ith little difference b etw een the littoral a n d the
sublittoral sites. O verall species richness in soft-bodied m eiofauna
undeniably was higher in Sardinia, b u t w e c an n o t infer w h eth er
this could b e due to the effect o f salinity o r to the effect o f different
species pools in different biogeographical a re a a t different
latitudes.
L atitudinal gradients in diversity indeed exist for m ost
organism s: diversity gradients, peaking in the tropics a n d tailing
off tow ard the poles, are well know n biological p h e n o m e n a, a n d
are shared by b o th m arin e a n d terrestrial systems [109]. L atitude
is m erely a description o f location; nevertheless, it often correlates
w ith o th er variables th a t are biologically relevant [110], such as: i)
historical events, i.e. the destructive effect o f glaciations acting at
high latitudes [111]; ii) R a p o p o rt’s rule, w hich attributes the
grad ien t to a decrease in species’ ranges to w ard low latitudes
[112]; a n d iii) differential solar energy in p u t a n d w ater availability,
linked to biodiversity th ro u g h productivity [109,113]. T h e
co m bined actions o f the three factors above a n d o f salinity can n o t
be ru led out: Sea Surface T em p era tu res (SST) a re indeed
m arkedly different betw een the two sites. T jä rn ö , latitude
58 °5 2 ,29.12"N , has average offshore SS T included b etw een the
isotherm s o f 9°C a n d 10°C; L a M a d d a le n a tow n (latitude
41°12'45.94"N ) has average SS T included b etw een 17°C a n d
18°C (N O A A , N atio n al O cea n o g ra p h ic D a ta C enter: w w w .nodc.
noaa.gov). F u rth e rm o re , it has b e en show n th a t som e organism s o f
the m eiofauna m ay have recolonized the N o rth e rn A dantic from
southern refugia [114], w itnessing the action o f glaciations on
boreal m arin e biodiversity. Finally, the finding a t L a M a d d a le n a o f
species only know n from neig h b o u rin g areas (in cases, w ith ranges
ap p aren tly lim ited to the C o rsican-S ardinian com plex), also hints
th a t a greater percentage o f n arro w -ran g e endem ics in the
M e d ite rran e a n c an n o t be ruled out.
Flow ever, the latitudinal influence o n diversity o f m icroscopic
organism s as m eiofauna is still highly d e b ated [102,115,116].
M oreover, no differences in the m acroecological correlates o f
diversity could b e observed b etw een S ardinia a n d Sw eden, even if
th ere are differences in h a b ita t heterogeneity, a n d th ere is a
general shortage o f suitable well sorted, coarse, a n d possibly
calcareous sedim ents in the N o rth A dantic. Poorly sorted
sedim ents provide less p o re volum e a n d consequently a low
potential for the presence o f interstitial m eiofauna [2,108].
M oreover, the fact th a t the sedim ent type m ay b e far m ore
restrictive th a n latitude for m eiofauna is supported by several
exam ples o f extrem ely diverse m eiofauna in the N o rth A tlantic
found in e.g., shell gravel o f the F aroe B ank [117,118], a n d the
coarse sand o f Flakkerhuk, W est G re en la n d [77,119-121].
In conclusion, the w orkshops held a t L a M a d d a le n a a n d at
T jä rn ö , in ad d itio n to the w ealth o f new species found, w hich will
be independently described by the researchers involved, high-
lighted the very lim ited know ledge o f soft-bodied m eiofauna, even
in w ell-studied areas. T his result has a n im p act on the evaluation
o f the m agnitude o f the con trib u tio n o f m eiofauna to m arine
biodiversity, surely und erestim ated w ith so m an y tem p erate to
tropical areas o f the p lan e t poorly studied [122] (see also h t t p : / /
co m l.o rg /ab o u t).
Supporting Inform ation
Figure SI
(TIF)
Sam pling localities in Northern Sardinia.
Table SI D etailed inform ation on sam pling localities in
Northern Sardinia.
(D O C)
Table S2 Ecological and biological attributes (adult
body length, distribution, endobenthic habitat) for each
species included in the analyses.
(D O C)
Tables S3 Acoela and N em ertoderm atida. Species list
and occurrence in Northern Sardinia.
(D O C)
Tables S4 Proseriata. Species list and occurrence in
Northern Sardinia.
(D O C)
Tables S5 Rhabdocoela. Species list and occurrence in
Northern Sardinia.
(D O C)
Tables S6 Gastrotricha. Species list and occurrence in
Northern Sardinia.
(D O C)
Tables S7 Annelida. Species list and occurrence in
Northern Sardinia.
(D O C)
Tables S8 Rotifera.
Northern Sardinia.
(D O C)
Species list and occurrence in
Acknowledgments
W e thank Agostino Bifulco for m aking samplings in the far-off islands of
the archipelago possible. Collection o f samples in m arine caves was only
possible thanks to the professional assistance o f Elisabetta Lutzu (Diving
C enter Costa Paradiso) and Elisabetta Pischedda (Blue Service Alghero),
who allowed the divers (M CG and AM) to rem ain within the borders of
safe-diving conditions. T he authors thank Nils Bunnefeld for advice on
statistical analyses and K avin Balbi for im proving the English text.
Author Contributions
Conceived and designed the experiments: M C G T A D F U J K W M A T.
Perform ed the experiments: M C G T A V D W H D S D F UJ FL A M IM W
K SN PT K W M A T. Analyzed the data: M C G T A VD W H D S D F UJ FL
AM IM W K SN P T K W M A T. C ontributed reagents/m aterials/analysis
tools: M C G T A D F UJ A M K W M A T. W rote the paper: M C G T A DF
UJ A M K W M AT.
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