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Ecosystem Services 58 (2022) 101490
2212-0416/© 2022 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
Full Length Article
Inuence of seagrass meadows on nursery and sh provisioning ecosystem
services delivered by Ria Formosa, a coastal lagoon in Portugal
Karim Erzini
a
,
*
, Filipe Parreira
a
, Zineb Sadat
b
, Margarida Castro
a
, Luís Bentes
a
, Rui Coelho
a
,
c
,
Jorge M.S. Gonçalves
a
, Pedro G. Lino
c
, Bego˜
na Martinez-Crego
a
, Pedro Monteiro
a
,
Frederico Oliveira
a
, Joaquim Ribeiro
d
, Carmen B. de los Santos
a
, Rui Santos
a
,
e
a
Centro de Ciˆ
encias do Mar (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
b
Universit´
e Cˆ
ote d’Azur, Grand Chˆ
ateau, 28 Avenue Valrose, 06103 Nice, France
c
Instituto Portuguˆ
es do Mar e da Atmosfera (IPMA), Av. 5 de Outubro, 8700-305 Olh˜
ao, Portugal
d
No current afliation
e
Program in Genomics, Biodiversity and Land Planning (BIOPOLIS), CIBIO-InBIO, Centro de Investigaç˜
ao em Biodiversidade e Recursos Gen´
eticos, Vair˜
ao, Portugal
ARTICLE INFO
Keywords:
Vegetated habitat
Nursery
Production
Fish provisioning
Fisheries enhancement
Coastal lagoon
ABSTRACT
This study is the rst to evaluate the sh provisioning services of a whole transitional landscape (Ria Formosa
lagoon, Portugal), in parallel with the enhancement of growth, survival and production of single cohorts of the
most important commercial sh species by vegetated and unvegetated sub-tidal habitats. Based on monthly
beach seine samples, total density and biomass of 96 species of shes were 1.89 and 3.03 times greater in
vegetated habitats than unvegetated habitats, respectively. Vegetated habitat enhanced survival in six of eight
commercial species for which survival could be estimated in both habitats. The total production of all 12
commercially important species within vegetated habitat was approximately double that of unvegetated habitat,
with production enhancement in 7 of 12 species ranging from 1.8 to 169-fold for the vegetated habitats. Within
the lagoon, vegetated sub-tidal habitat covers an area 5-fold smaller than unvegetated habitat, yet it accounts for
27.1 % of sh production. Estimated total lifetime economic values of the single cohorts of the 12 commercial
species were between 30 million and 59 million EUR. An exceptionally strong year class of the European seabass
(Dicentrarchus labrax), a species with higher density and biomass in unvegetated habitat, accounts for the higher
overall values per hectare for unvegetated habitat (Low natural mortality (M): EUR 32,844 ha
−1
; High M: EUR
16,751 ha
−1
) than for vegetated habitat (Low M: EUR 22,028 ha
−1
; High M: EUR 10,700 ha
−1
). These results
highlight the enormous importance of temperate coastal lagoons as a nursery and source of recruits for coastal
sheries. Our evaluation of sh provisioning services based on data for individual cohorts of sh for a whole
transitional landscape is a stronger and more valid approach for estimating future biomass and value than
previous studies based on mean densities and biomasses of sh that did not distinguish between cohorts.
1. Introduction
Transitional landscapes such as coastal lagoons and estuaries are
widely recognized as important habitats for juvenile sh, with numerous
studies on their role and importance as nursery areas for marine species
that contribute to subsistence, commercial and recreational sheries in
adjacent coastal waters (Whiteld, 2017; Baker et al., 2020). The in-
clusion of habitat that is necessary to maintain a sustainable shery
(Essential Fish Habitat; EFH), in the law governing marine sheries
management in the U.S. (Magnuson-Stevens Act) and in the Common
Fisheries Policy of the European Union (CFP, 2013) highlights the
importance of specic areas for conservation and management.
Over time, the denition of nursery areas has shifted (Whiteld,
2017), with the mere presence of juveniles in particular habitats
considered insufcient by Beck et al. (2001), who proposed the Nursery
Role Habitat (NRH) criterion based on differences in density of juveniles
between habitats. Dahlgren et al. (2006) introduced the concept of
Effective Juvenile Habitat (EJH), differentiating the importance of ju-
venile habitats by their relative contributions to adult populations.
Sheaves (2009) broadened the denition by advocating the importance
* Corresponding author.
E-mail address: kerzini@ualg.pt (K. Erzini).
Contents lists available at ScienceDirect
Ecosystem Services
journal homepage: www.elsevier.com/locate/ecoser
https://doi.org/10.1016/j.ecoser.2022.101490
Received 7 August 2021; Received in revised form 9 September 2022; Accepted 7 October 2022
Ecosystem Services 58 (2022) 101490
2
of connectivity within the framework of a coastal ecosystem mosaic
(CEM), with a focus on the ecology of key connections during different
life history stages rather than on specic habitats. Within estuarine or
lagoon systems, this implies studying landscape ecology, the use by ju-
venile shes of a mosaic of fragmented habitats, the movements be-
tween habitats such as vegetated and unvegetated areas and of edge
effects (Sheaves, 2009; Nagelkerken et al., 2015; Whiteld, 2017).
Fodrie et al. (2009) stressed the implications of linking location-specic
differences in demographic parameters such as growth and mortality
rates with overall population tness and contributions to adult stocks.
Nursery value of different coastal habitats has been measured and
compared using density, growth, condition factor, feeding, survival and
production per unit area of juveniles (age class 0 or 0-group sh) as
proxies of habitat quality. Increased production and recruitment to adult
populations is associated with greater density, survival, condition and
growth in nurseries (Nelson, 1998; Franco et al., 2010; Janes et al.,
2019).
Studies on sh provisioning ecosystem services in coastal and tran-
sitional landscapes have focused mainly on sheries enhancement by
particular habitats, especially seagrass, rather than on the whole land-
scape. The value of sheries enhancement of seagrass habitat has been
quantied using different approaches. Blandon and zu Ermgassen
(2014a), Blandon and zu Ermgassen (2014b) carried out a meta-analysis
based on 11 studies across southern Australia where juvenile shes were
sampled in vegetated and unvegetated areas with ne mesh gear, mainly
beach seines. They estimated enhancement by seagrass as the difference
in density (individuals m
−2
) of 0.5-year-old shes between seagrass and
unvegetated habitats. Using species-specic natural mortality rates (M),
age at rst harvest, maximum age, von Bertalanffy growth parameters
and weight-length relationship parameters for 12 commercial species,
they calculated the total annual enhancement of each species (g m
−2
) by
summing the incremental increase in weight for an average sh of each
species in each year class i multiplied by the density of sh in each age
class:
Ni=N0.5×e(M×(i−0.5)) (1)
The estimated total annual seagrass enhancement was 980 g m
−2
,
corresponding to 9.8 t per hectare for the commercial sheries. The
value of seagrass nurseries was estimated at AUD 31,650 ha
−1
y
−1
(approximately EUR 19,840 ha
−1
y
−1
). J¨
anes et al. (2020) used the same
approach to estimate the average enhancement in annual sh biomass
production from seagrass, mangrove and tidal marsh habitats in
Australia and found that compared to unvegetated areas, seagrass hab-
itats were the most productive, with 55,000 more sh per hectare, while
mangroves and tidal marshes provided 19,000 and 1,700 more sh,
respectively. Jackson et al. (2015) used a seagrass residency index to
calculate the contribution of seagrass habitat provisioning service to the
Mediterranean commercial sheries landings value (CFV) and recrea-
tional sheries value (RFV), estimating that approximately 4 % of CFV
and 6 % of RFV were directly linked to seagrass, corresponding to
approximately EUR 77.7 million (CFV) and EUR 112.6 million (RFV).
Based on sh abundance data, Tuya et al. (2014) estimated that seagrass
value to inshore sheries was EUR 606,239 y
−1
for Gran Canaria Island
(NE Atlantic).
While the value of ecosystem services provided by individual habi-
tats has a rich history (Campagne et al., 2015; Tuya et al., 2014; United
Nations Environment Programme, 2020), valuing the services from an
entire coastal lagoon is infrequent (Lillebø et al, 2016; Newton et al.,
2018). For the evaluation of sh provisioning services, a whole lagoon
approach is important because during their nursery phase, juveniles may
not generally experience single habitats but the entire landscape
(Sheaves, 2009).
Coastal lagoons account for approximately 11 % of the global
coastline (Kjerfve, 1994) and are important nurseries for many coastal
commercial species, providing recruits and enhancing sh yields
(Monteiro et al., 1990; Erzini et al., 2002; Tournois et al., 2017). The Ria
Formosa is the largest coastal lagoon in Portugal, with the greatest area
of vegetated sub-tidal habitat (Cunha et al., 2013) and high juvenile sh
diversity and densities, especially of commercially important coastal
species (Monteiro et al., 1990; Erzini et al., 2002; Ribeiro et al., 2012).
In this study, we use a multi-method approach to evaluate the
nursery function and sh provisioning services of the whole Ria Formosa
lagoon. Unlike previous, questionnaire-based studies (e.g. Sousa et al.,
2013), or studies that did not evaluate the lifetime contribution of
distinct cohorts (e.g. Tuya et al. 2014; J¨
anes et al., 2020), we used time
series of length frequency distributions, density and biomass of single
cohorts of 12 marine commercial species to estimate population dy-
namics parameters, and biomass modelling to estimate the sh provi-
sioning services of the Ria Formosa lagoon. The main objectives of the
study were: 1) to estimate the potential economic contribution of the
whole lagoon to coastal sheries, and 2) to compare density, biomass,
survival, production and the economic value of sub-tidal vegetated and
unvegetated habitat within the lagoon.
2. Methods
2.1. Ria Formosa lagoon
Ria Formosa is a mesotidal coastal lagoon located in southern
Portugal with minor contributions of freshwater tributaries, which ex-
tends 56 km along the coast (Fig. 1). The semi-diurnal tide amplitude
ranges from 1.3 to 3.5 m on neap and spring tides, respectively, exposing
large intertidal areas where the seagrass Zostera noltei develops. The
seagrasses species Z. marina and Cymodocea nodosa occupy the shallow
subtidal areas.
2.2. Sampling of juveniles
Sampling of the ichthyofauna took place in the Ria Formosa lagoon
over a 17-month period from September 2000 to January 2002 at 24
unvegetated (UV) and 17 vegetated (subtidal seagrass meadows, V) sites
in the major and minor channels of the lagoon (Fig. 1) with beach seines.
While we have carried out seasonal annual monitoring in a subset of our
41 sampling locations since 2001, we selected these data because sam-
pling was monthly, allowing a cohort-based approach. There have been
no signicant changes in the relative importance of the 12 main species
used in the analysis, and no substantial change in habitat type or cover at
our sampling sites since 2001 (Ribeiro et al. 2006, Ribeiro et al., 2008,
2012, unpublished data).
Beach seines are the gear of choice for quantifying juvenile sh
density as they are encircling gear that sh the whole water column and
sample a relatively large area. Two types of beach seine were used: a 50
m, 14 mm stretched mesh size beach seine from January 2001 to
January 2002 at 4 sites and a 25 m, 9 mm beach seine from September
2000 to October 2001 at 37 sites. Both nets were 3.5 m high in the
middle and sampling always took place during a period 2 h before to 2 h
after low tide, in days when the amplitude of the tide was<2 m. The two
nets were deployed differently: following Monteiro (1990), one end of
the 50 m net was held on shore and a boat was used to set the net in a
circle, while the 25 m beach seine was towed parallel to the shore by the
boat and researchers on the shore before being hauled to the shore.
Based on GPS measurements the average sampled area with the 25 m
beach seine was 1,087 m
2
, while that of the 50 m beach seine was 295
m
2
. However, three 50 m beach seine sets were made in succession at
each location and the catches pooled, resulting in a total sampled area of
885 m
2
. The catches were placed in labelled bags and transported to the
laboratory for sorting, identication, measuring and weighing.
Following Monteiro et al. (1990), species were classied as resident,
occasional or migratory, with the latter consisting of young-of-the-year
of species using the Ria Formosa as a nursery. The monthly beach seine
samples in unvegetated and vegetated sites were used to obtain sh
K. Erzini et al.
Ecosystem Services 58 (2022) 101490
3
density and biomass per unit of sampled area and lengths and weights of
juveniles of marine commercial species that use the lagoon as a nursery.
2.3. Tagging (site delity)
To compare habitats in terms of growth, mortality and production, it
was necessary rst to evaluate site delity and the association of in-
dividuals of the different species with each habitat. Tagging was used to
study site delity and spatio-temporal dynamics. Tagging of sh
occurred from September 2000 to January 2002 with a total of 73 beach
seine sets over 19 shing days at 26 locations devoted exclusively to
tagging. Depending on the location, either the 25 m or the 50 m beach
seine was used to catch sh for tagging. After capture, sh were placed
in a oating cage besides the boat and teams of researchers measured,
tagged (Floy T- tags) and recorded the data (date, location, species, total
length, and tag number). Tag wounds were treated with a providone-
iodine solution (Betadine) and the tagged sh were placed in the
oating cage for a recovery period of approximately 30 min before being
released back into the Ria at the location of capture.
2.4. Population dynamics
Monthly length frequency distributions for 2001 were used to esti-
mate population dynamics parameters and production for 12 of the most
abundant commercial species using the lagoon as a nursery, that had a
single, main cohort of juveniles (i.e. age class 0) that could be clearly
followed over time: Boops boops (bogue), Diplodus bellottii (Senegal
seabream), D. puntazzo (sharpsnout seabream), D. sargus (white seab-
ream), D. vulgaris (two-banded seabream), Dicentrarchus labrax (Euro-
pean seabass), Mullus surmuletus (striped red mullet), Sardina pilchardus
(sardine), Sarpa salpa (salema), Scorpaena porcus (black scorpionsh),
Sparus aurata (gilthead seabream) and Spondyliosoma cantharus (black
seabream). These species recruit to the lagoon in the late winter or
spring and leave by the end of the year.
Analysis of single cohorts, with large sample sizes simplies the
analysis of growth, mortality and production (Hayes et al., 2007; Rigler
and Downing, 1984). Unlike other studies (Dolbeth et al., 2008; Franco
et al. 2010; Verdiell-Cubedo et al., 2013), there was no need for the use
of length frequency analysis to decompose length frequency distribu-
tions as there was a single clearly identiable 0-group for all 12 species,
as can be seen in the example of monthly length frequency distributions
of a single cohort of S. cantharus from vegetated habitat, in Appendix A
(Supplementary materials).
From the time series of length frequency distributions for vegetated
(V), unvegetated (UV) and total (V +UV) habitats, the following were
determined: month of birth (t =0), month of recruitment (settlement),
length-at-age (L
t
), numbers at age (N
t
), densities (n m
−2
) and biomass (g
m
−2
). Month of birth was estimated by extrapolating L
t
backwards and
conrmed using data on month of capture with a 1 mm mesh codend
Riley pushnet of the earliest post-larval juvenile stages (1–2 cm) found in
the lagoon, under the assumption that post-larval juveniles of this size
are at most 4 to 8 weeks old (Nelson, 1998, Erzini et al. 2002, Ribeiro
et al. 2012). The Gompertz model:
Lt=L0×e(G1×(1−e(− g2×t)))(1)
considered to be the most appropriate for describing age class 0 growth
(Gamito 1998, Diouf et al. 2009) was tted to the length-at-age data. L
t
is the total length, t the age in months, L0 is the hypothetical length at t
=0, G1 and g2 are growth parameters, G1g2 is the size-specic instan-
taneous rate of growth at t =0 and g2 is the instantaneous rate of
decrease of G1g2 (Saila et al., 1988). The Hotelling T
2
test was used to
test the null hypothesis that there is no difference between the growth
parameters of sh from vegetated and unvegetated habitats (Bernard,
1981; Srivastava and Carter, 1983). The SAS software was used to t the
Gompertz model (NLIN procedure) and to carry out the Hotelling T
2
test
(SAS Institute Inc., 2013). The instantaneous monthly growth rate (G)
was also estimated from.
ln(Lt) = ln(L0) + G×t(2)
where t is age in months (Nelson, 1998).
Instantaneous total mortality (Z) was estimated by tting a regres-
sion to the descending limb of the plot of the natural logarithm of
numbers-at-age against age in months (Ricker, 1975):
Fig. 1. Map of the western part of the Ria Formosa with the 41 beach seine sampling locations: 24 unvegetated (open circles), 17 vegetated (lled circles).
K. Erzini et al.
Ecosystem Services 58 (2022) 101490
4
ln(Nt) = (Z×t) + c(3)
Given that there is no signicant shing mortality during the lagoon
juvenile phase, the estimates of total mortality (Z) can be considered
equal to natural mortality, M. For all species, densities increased after
initial recruitment to the lagoon at sizes of<2 cm, reaching maximum
numbers between 5 and 7 months of age. Thus, the estimates of Z, based
on the descending part of the catch curve, correspond to natural mor-
tality of the older juveniles in the period before emigration from the
lagoon to the adjacent coastal zone. Under the assumption of a steady-
state condition and negative exponential mortality, Z equals the pro-
duction to biomass ratio (P/B) (Allen, 1971). Catch curve analysis was
carried out for each of the species separately for V and UV habitats as
well as for the combined data (V +UV). Seagrass enhancement of sur-
vival (S) was calculated as S
V
/S
UV
, where.
S=e−Z(4)
and values of S
V
/S
UV
>1 correspond to seagrass enhancement of
survival.
2.5. Production
Production of a cohort is the generation of biomass per unit area per
unit time, integrating biomass, recruitment, growth and mortality into a
single dynamic measure that is the best indicator of quantitative per-
formance of a sh population (Ricker 1975, Randall and Minns 2000,
Hayes et al. 2007). Production was estimated from growth increments
for single cohorts for vegetated and unvegetated habitats (Rigler and
Downing, 1984; Hayes et al., 2007; Dolbeth et al., 2008):
P=
T−1
t=0Nt+Nt+1
2.(Wt+1−Wt)(5)
where N
t
is density (numbers per m
2
) and Wt is mean weight of the
cohort in month t. Densities were calculated by dividing the numbers
caught in each month in each habitat by the total area sampled each
month (25,886 m
2
for 24 unvegetated habitat locations and 17,873 m
2
for 17 vegetated habitat locations). Weight-length relationships:
W=a×Lb(6)
were tted and used to calculate the mean weights-at-age of the cohort
(Wt)from the cohort length frequency distributions for each month from
the time of recruitment to the lagoon until migration from the lagoon to
the coastal waters. Total production per cohort for the whole lagoon was
calculated using the estimated cohort production per m
2
and the total
estimated subtidal areas of seagrass and unvegetated habitats
(3,060,000 m
2
and 15,940,000 m
2
, respectively; unpublished data).
2.6. Economic valuation
Calculation of the lifetime economic value of each cohort to coastal
sheries was based on the methodologies of Blandon and zu Ermgassen
(2014a), Blandon and zu Ermgassen (2014b), zu Ermgassen et al. (2016)
and J¨
anes et al. (2020). Von Bertalanffy growth parameters, maximum
age, and weight-length relationship parameters were compiled for each
species (Appendix E). For the majority of the species these were from our
own studies in the Algarve or other regions from continental Portugal
(Appendix E). For species lacking sheries biology parameters from
Portugal (D. labrax, D. puntazzo, S. porcus, S. aurata) we used age and
growth studies from nearby areas, namely the Gulf of Cadiz for D. labrax
and S. aurata, the Canary Islands for D. puntazzo, and Algeria for
S. porcus. The instantaneous natural mortality rate (M) for fully shery
recruited age classes was estimated using four empirical models: Pauly
(1980):
log10(M) = − 0.0066 − (0.279
×log10L∞) + (0.6543×log10 K) + (0.4634×log10T)(7)
Djabali et al. (1994):
log10(M) = 0.0278 − (0.1172×log10 L∞) + (0.5092×log10K)(8)
Then et al. (2015):
M=4.899 ×tmax−0.916(9)
M=4.118 ×K0.73×L∞−0.33 (10)
where K and L
∞
are von Bertalanffy growth parameters, tmax is
maximum age and T is the mean annual water temperature in southern
Portugal (16 ◦C). In addition, size-dependent natural mortality rates for
pre-recruit ages were calculated using the Lorenzen (2000) model:
Mt=M× (Lm/Lt)(11)
where M is natural mortality calculated using the above-mentioned
empirical models, L
t
is length at age t and L
m
is the minimum legal
landing size (MLS; https://www.dgrm.mm.gov.pt/peixes). For S. porcus
the size at rst maturity was used for L
m
as there is no minimum legal
landing size.
The von Bertalanffy parameters were used to calculate lengths-at-age
from t =0.5 to t =tmax +0.5 and the mean weights-at-age (Wt)
calculated with the weight-length relationships. Natural mortality rates
(Mt) for age classes with mean sizes below the MLS were calculated
using the Lorenzen (2000) model, while a constant M calculated using
the four empirical models was used for all the age classes of sh equal to
or greater than the MLS.
The maximum monthly abundance for each species was obtained
from the length frequency distributions for V and UV habitats (see for
example Appendix A) and used as N
0.5
in the life table analysis to
calculate numbers-at-age up to the maximum age. Given the age-specic
survival rate St=e−Mt, the evolution in numbers of the cohort was
calculated by Nt=Nt−1×St−1. The total biomass by age class was
calculated by multiplying the numbers-at-age by the corresponding
mean weights-at-age. The cohort lifetime or total biomass (TB), in the
absence of shing mortality, was obtained by summing the biomasses of
all fully recruited age classes: TB =t=tmax
t=rNt×Wt, where r is the
youngest age class with a mean length equal to or greater than the MLS.
In Portugal, commercial shermen must sell their catches in ofcial
auctions where landings and rst sale prices are recorded. Ofcial data
for all species sold at auction in Algarve ports from 1997 to 2017 was
obtained and average rst sale prices of the 12 species calculated. The
average prices were used to calculate the total value and the value per
hectare of each cohort for the whole lagoon and for each habitat sepa-
rately. Finally, the vegetation economic enhancement per hectare of the
vegetation habitat was calculated by dividing the value obtained for the
vegetated area by the one of the unvegetated area.
3. Results
3.1. Site delity
A total of 4,315 sh were tagged and released, with 4 species ac-
counting for 95.9 % of the total tagged sh, namely Diplodus vulgaris
(60.4 %), Dicentrarchus labrax (13.3 %), Diplodus sargus (11.8 %) and
Spondyliosoma cantharus (10.4 %) (Appendix B). During the monthly
beach seine sampling at the 41 sites, a total of 305 (7.1 %) tagged sh
were recaptured (Table 1). Some of these sh were recaptured several
times (some up to 5 and 6 times) (Table 1), with a total of 225 (5.2 %)
different sh recaptured at least once. Although recapture percentage is
relatively high, most of these shes were recaptured during the course of
K. Erzini et al.
Ecosystem Services 58 (2022) 101490
5
the shing trials for this project, and only 6 specimens were returned by
commercial and sports shermen.
Of 225 recaptured individuals, 35.7 % were recaptured within 100 m
of the tag and release location and were considered to have high site
delity, while 54.4 % of the recaptures occurred between 100 and 500 m
of the tagging location (Table 2). Only 25 individuals (8.2 %) travelled
from 500 m to 2 Km, 3 individuals (1.0 %) from 2 to 5 Km and 1 indi-
vidual>5 Km. In terms of time spent between capture and recapture, the
majority of the sh (98.4 %) were recaptured in the rst 3 months after
being tagged (Table 2).
3.2. Vegetated habitat enhancement of density and biomass
A total of 155,064 sh of 96 species were caught in the monthly
sampling from September 2000 to January 2002 (Appendices C and D).
Seventeen (8 migratory, 9 resident) and 21 species (10 migratory, 11
resident) accounted for 95 % of the total catch in numbers and biomass
respectively.
Based on an estimated total sampled area of 609,086 m
2
(vegetated:
247,567 m
2
; unvegetated: 361,519 m
2
) density and biomass were 0.354
sh m
−2
and 1.792 g m
−2
in the vegetated habitat, and 0.187 sh m
−2
and 0.881 g m
−2
in the unvegetated habitat. Vegetated habitat enhanced
density by 89.3 % (V/UV =1.893) and biomass by 103.7 % (V/UV =
2.037) in the Ria Formosa for all species. Of the 96 species, 67.7 % (65
species) had a higher density in vegetated habitat, while 64.6 % (62
species) had a higher biomass in vegetated habitat. The sh density and
biomass enhancement in vegetated habitats was more than twice for 63
% and 60 % of the species, respectively. At the individual species level
there was considerable variation, with the herbivorous Sarpa salpa
having density and biomass 130 and 174 times greater in vegetated than
in unvegetated habitats. Species’ densities and biomasses were higher at
unvegetated than vegetated habitats (V/UV <1.0) for several of the
most abundant species. The lowest V/UV values were for the anchovy
(Engraulis encrasicolus), with density and biomass 15 and 21 times
greater in unvegetated than in vegetated habitats (Supplementary ma-
terials appendices C and D). Density and biomass enhancement results
for the 12 selected species are given in Table 3. Vegetated habitat
enhanced density and biomass for 8 of the 12 commercial species, most
notably for S. salpa, S. porcus, P. puntazzo and D. bellottii, but not for
D. labrax, M. surmuletus, S. pilchardus and S. aurata (Table 3).
3.3. Vegetated habitat enhancement of growth and survival
For the study of growth, mortality and production of the cohorts of
the 12 selected species, the months of January 2001 to January 2002
were used as all the selected species recruited in late winter or spring
and left the lagoon by November and December. The Gompertz model
could be tted to both V and UV data for 6 of the 12 species (Table 4).
Signicant differences in growth parameters between V and UV habitats
were found for D. sargus, D. vulgaris, S. cantharus and S. porcus (Hotel-
ling’s T
2
; P >0.05). For S. salpa, the growth model could only be t to
data for V, while for D. bellotii, D. labrax and D. puntazzo, the parameters
could only be estimated for UV. The model could not be tted to U and
UV age-length data for B. boops and M. surmuletus. The instantaneous
growth rate per month (G) was greater for V for only 4 species (D. sargus,
D. vulgaris, S. aurata and S. pilchardus). However, differences in G were
small, with overlapping V and UV condence intervals for G for all
species (Fig. 2).
The estimated total mortality rates for individual cohorts were esti-
mated for 10 of the 12 species in V and for 9 species in UV (Table 5).
Vegetated habitat enhanced survival for 6 out of 8 species for which it
was possible to calculate mortality and survival for both V and UV
habitats, especially for D. sargus (72 %) and S. aurata (43 %) (Table 5).
Table 1
Total numbers of tagged and recaptured sh of each species, total number of recaptures per species and the number of times individual sh were recaptured.
Total Number Total Number of times recaptured
Species tagged recaptured recaptures 1 2 3 4 5 6
Diplodus vulgaris 2606 189 261 143 31 8 4 2 1
Spondyliosoma cantharus 448 17 23 13 3 1
Diplodus sargus 511 15 17 13 2
Dicentrarchus labrax 575 3 3 3
Sparus aurata 11 1 1 1
Total 4151 225 305 173 36 8 5 2 1
Table 2
Number of recaptures by interval of time and distance (m) travelled between tagging and recapture locations, for all species.
Time between Distance
tagging and recapture <100 m 100–500 m 500–2000 m 2000–5000 m >5000 m Total
<1 week 34 39 73
1–2 weeks 20 31 1 52
2 weeks to 1 month 26 66 6 98
1–3 months 28 30 17 2 77
3–6 months 1 1 2
>6 months 1 1 2
Total 109 166 25 3 1 304
Table 3
Density (n m
−2
) and biomass (g m
−2
) for vegetated (V) and unvegetated (UV)
habitats, with enhancement ratios (V/UV). Enhancement due to vegetation (V/
UV >1) in bold.
Species UV (n
m
−2
)
V (n
m
−2
)
V / UV
(n m
−2
)
UV (g
m
−2
)
V (g
m
−2
)
V / UV
(g m
−2
)
B. boops 0.0005 0.0009 1.7 0.0017 0.0027 1.6
D. labrax 0.0155 0.0052 0.3 0.1108 0.0809 0.7
D. bellottii 0.0006 0.0048 8.1 0.0009 0.0079 9.2
D. puntazzo 0.0001 0.0018 15.7 0.0012 0.0064 5.1
D. sargus 0.0019 0.0040 2.1 0.0088 0.0208 2.4
D. vulgaris 0.0070 0.0175 2.5 0.0738 0.1473 2.0
M. surmuletus 0.0011 0.0007 0.7 0.0117 0.0102 0.9
S. pilchardus 0.0213 0.0188 0.9 0.0455 0.0332 0.7
S. salpa 0.0001 0.0069 130.3 0.0001 0.0242 173.5
S. porcus 0.0003 0.0040 13.9 0.0080 0.1157 14.5
S. aurata 0.0010 0.0005 0.5 0.0251 0.0186 0.7
S. cantharus 0.0058 0.0157 2.7 0.0429 0.0685 1.6
K. Erzini et al.
Ecosystem Services 58 (2022) 101490
6
3.4. Enhancement of production
The production (g m
−2
y
−1
) of single cohorts in vegetated habitat
was higher than for the unvegetated one for 7 out 12 species of the most
important commercial species (Fig. 3). Particularly noteworthy in terms
of seagrass enhancement of production is the herbivorous S. salpa, with
vegetated habitat being 169.1 times more productive than unvegetated.
Of the 8 Sparidae, only B. boops and S. aurata had lower productivity in
vegetated habitat than in the unvegetetated one. The European seabass
(D. labrax), sardine (S. pilchardus) and red mullet (M. surmuletus) were
also more productive in unvegetated habitat. The vegetation enhance-
ment ratio (V
production
/ UV
production
) was higher than 1 in 6 species
(Fig. 4), ranging from 1.8 for the black seabream (S. cantharus) to 169.1
for S. salpa (not shown in the gure).
Total annual production estimated for the whole Ria Formosa lagoon
based on total vegetated and unvegetated subtidal surface areas was
20,569.1 kg (Table 6) and ranged from 5,072 Kg for the most productive
species (D. vulgaris) to 193 kg for B. boops. Overall, the seagrass habitat
was almost twice as productive (1.824 g m
−2
y
−1
) as unvegetated
habitat (0.940 g m
−2
y
−1
), but it only accounted for 27.1 % of the total
annual production as its total area was 5-fold lower (19.2 %) than
unvegetated habitat. The total annual production of the 12 cohorts of
juveniles was worth 129,353
€
(Table 6). This total value corresponds to
78.6
€
ha
−1
for vegetated habitat and 66.1
€
ha
−1
for unvegetated
habitat.
3.5. Cohort lifetime economic value
The results of the economic evaluation are given in Table 7. Given
the wide range of natural mortality (M) values obtained with the four
empirical models, results are presented only for the lowest and the
highest natural mortality (M) for each species. For low values of M, the
total contribution of the single cohorts of the 12 species over their
lifetime is almost EUR 59.2 million, with the seagrass habitat accounting
for 11.4 %. For high M, the corresponding values are EUR 30.0 million
and 10.9 %. The far greater importance of unvegetated habitats is
largely due to the overwhelming contribution of the high value, long-
lived European seabass (D. labrax) that is not V-enhanced, and to a
lesser extent to two other high value species, the gilthead seabream
(S. aurata) and red mullet (M. surmuletus) that are also not V-enhanced.
Total value per hectare of V habitat ranged from EUR 10,700 (high M) to
EUR 22,028 (low M), with corresponding values of EUR 16,751 and EUR
32,844 for UV habitat. Nine out of 12 species were V-enhanced (EUR
ha
−1
), with greatest enhancement (224.4) for the herbivorous S. salpa.
The importance of the strong cohort of European seabass is reected
in the Algarve ofcial landings data (Fig. 5). Based on the length-at-age
relationship and the minimum legal size of 36 cm total length, seabass
Table 4
Gompertz model parameters parameters (L0, G1 and g2) for vegetated (V) and unvegetated (UV) habitat, with results of the Hotelling T
2
test. *: Gompertz model
parameters could not be estimated. In bold, signicant differences between V and UV.
Gompertz (V) Gompertz (UV) Hotelling
Species Code L0 G1 g2 L0 G1 g2 T
2
P
B. boops Bb * * * * * *
D. bellottii Db * * * 0.1522 4.163 0.212
D. labrax Dl * * * 0.0004 10.285 0.518
D. puntazzo Dp * * * 0.9420 3.508 0.187
D. sargus Ds 0.002 8.383 0.392 0.0640 5.084 0.303 0.263 0.850
D. vulgaris Dv 1.726 6.180 0.035 1.1920 3.321 0.106 1.359 0.302
M. surmuletus Ms * * * * * *
S. aurata Sa 0.033 6.619 0.314 0.0220 6.845 0.352 8.729 0.013
S. cantharus Sc 0.035 5.423 0.259 0.0073 7.161 0.407 0.071 0.974
S. pilchardus Spil 2.034 1.249 0.351 3.3940 0.883 0.165 3.819 0.032
S. porcus Spor 3.336 3.212 0.055 2.8055 2.751 0.084 1.557 0.244
S. salpa SS 2.008 2.734 0.131 * * *
Fig. 2. Instantaneous growth rates (G) with 95% condence intervals for
vegetated and unvegetated habitats. Species codes are given in Table 4.
Table 5
Estimated total instantaneous mortality rates (Z
V
, Z
UV
), standard errors (s.e.) of
Z, survival (S
V
, S
UV
) and vegetated habitat enhancement of survival (S
V
/S
UV
)
with higher survival in vegetated habitat (S
V
/S
UV
>1) in bold. *: Z and S could
not be estimated.
Species Z
V
s.e. S
V
Z
UV
s.e. S
UV
S
V
/S
UV
B. boops * * * * * * *
D. labrax * * * 0.44 0.16 0.65 *
D. bellottii 1.14 0.44 0.32 * * * *
D. puntazzo 0.61 0.07 0.55 * * * *
D. sargus 0.50 0.08 0.60 1.05 0.20 0.35 1.72
D. vulgaris 0.56 0.09 0.57 0.70 0.08 0.49 1.15
M. surmuletus 0.34 0.04 0.71 0.38 0.05 0.69 1.04
S. pilchardus 0.57 0.15 0.57 0.76 0.20 0.47 1.22
S. salpa 0.94 0.23 0.39 0.39 0.35 0.68 0.58
S. porcus 0.06 0.04 0.94 0.08 0.09 0.93 1.01
S. aurata 0.37 0.15 0.69 0.73 0.04 0.48 1.43
S. cantharus 0.31 0.06 0.73 0.17 0.05 0.85 0.87
K. Erzini et al.
Ecosystem Services 58 (2022) 101490
7
that were juveniles in 2001 would have recruited to the shery in
2004–2005 and contributed signicantly to the landings for the next 4 to
5 years, as can be seen in the increase in landings from 2004 to 2005 to
2009–2010.
4. Discussion
This study is the rst to evaluate the sh provisioning services of a
whole transitional landscape, the Ria Formosa lagoon, in parallel with
the enhancement of growth, survival and production of single cohorts of
Fig. 3. Production (g m
−2
y
−1
) for unvegetated (brown) and unvegetated (green) habitats. (For interpretation of the references to colour in this gure legend, the
reader is referred to the web version of this article.)
Fig. 4. Vegetation production enhancement ratios (V
production
/UV
production
). Sarpa salpa, with an enhancement ratio of 169.1 is not shown. The vertical line (V/UV
ratio =1) corresponds to no difference in production between V and UV habitats. Ratios >1 mean that vegetated habitat is more productive than unvege-
tated habitat.
K. Erzini et al.
Ecosystem Services 58 (2022) 101490
8
commercial sh species by vegetated and unvegetated sub-tidal habi-
tats. The sh provisioning services of the Ria Formosa lagoon, estimated
as the lifetime economic value (Dewsbury et al. 2016) of single cohorts
of 12 commercial species for high and low natural mortality scenarios,
ranged between 31.6 and 59.0 million EUR. The corresponding values
per hectare of sub-tidal habitat were 16,615 and 31,102 EUR ha
−1
.
These ndings highlight the importance of Ria Formosa as a nursery and
major source of recruits to local coastal sheries.
These estimates are similar to those of other studies that have esti-
mated the sheries economic value of coastal vegetated habitats such as
seagrass meadows, mangrove forests and tidal marshes (Blandon and zu
Ermgassen (2014a), Blandon and zu Ermgassen (2014b); J¨
anes et al.,
2020). J¨
anes et al. (2020) reported that 99 % of the economic value of
vegetated coastal habitats in Australia was associated with seagrass
habitat, with an average value of 21,276 AUD ha
−1
y
−1
(approximately
13,337 EUR ha
−1
y
−1
). For southern Australia, the value of seagrass
nurseries was estimated to be 31,650 AUD ha
−1
y
−1
(approximately
19,840 EUR ha
−1
y
−1
) by Blandon and zu Ermgassen (2014a), Blandon
and zu Ermgassen (2014b).
The value of transitional landscapes in terms of sh provisioning
services is supported by other studies that have provided evidence of the
link between lagoon or estuarine nurseries and coastal commercial
sheries. Based on otolith microchemical analyses Tournois et al. (2017)
found that >80 % of adult gilthead seabream (S. aurata) captured in the
coastal zone in the Gulf of Lion (France) originated from 4 coastal la-
goons, while Lett et al. (2019) reported that individual lagoons in the
south of France contributed up to 18 % of the local coastal exploited
stock of S. aurata. Otolith elemental ngerprinting was also used to
assign nursery origin of coastal species in Portugal, including D. labrax
and the D. vulgaris (Vasconcelos et al., 2008; Correia et al., 2011).
However, neither study reported estuarine or lagoon origin for
D. vulgaris, suggesting that rocky inshore areas along the coast of
Portugal are also likely to be important nurseries for this species.
Even though the cohort lifetime economic value of 9 out of the 12
species studied was enhanced by seagrass meadows, the overall eco-
nomic value of the unvegetated habitat was higher. This was due to the
exceptionally high recruitment of the European seabass, a high value,
long-lived species with higher density and biomass in unvegetated
habitat, that accounted for 76 to 81 % of the total lifetime economic
value per hectare. Our long-term, annual summer monitoring of juve-
niles (unpublished data) shows that in the year of the study, 2001, there
was a very strong recruitment of this species, which is reected in the
high commercial landings from 2004 to 2010, with age classes 3 to 9 of
the 2001 cohort dominating the landings.
The relatively greater economic importance of vegetated habitat is
apparent when considering the cohort annual production, rather than
the lifetime monetary value of the 12 species. The value of vegetated
habitat production of the cohorts of those species was 78.6
€
ha
−1
y
−1
while that of unvegetated habitat was 66.1
€
ha
−1
y
−1
. These values are
similar to those obtained by Tuya et al. (2014) for Cymodocea nodosa
meadows off Gran Canaria Island, where the economic value of the
production of juveniles of 8 commercial species was estimated to be
95.75
€
ha
−1
y
−1
, with two species (Sparisoma cretense and
M. surmuletus) accounting for 83 % of the economic value.
In this study, production of 7 of the 12 species was greater in vege-
tated habitats, with enhancement by an order of magnitude or more for
S. salpa, D. bellottii and S. porcus. Greater sh production in vegetated
habitat is expected due to the nursery role of structurally complex
habitats such as seagrass meadows that enhance survival and growth by
providing shelter from predators and rich feeding grounds (periphyton
and invertebrates) for juveniles of many sh species (Gillanders, 2006;
Wong and Dowd, 2016). In the case of the Ria Formosa, enhanced sh
production seems to be mainly due to the higher densities, biomass and
survival in vegetated habitat for most of the species, rather than to
higher growth. Heck et al. (2003) reported that 3 out of 6 sh species
had higher growth rates in vegetated habitat, while higher survival in
vegetated or structured habitat was more common. In a more recent
global meta-analysis, McDevitt-Irwin et al. (2016) found that seagrass
enhancement of survival of juvenile shes was more common than
enhancement of growth.
The density and biomass of most of the commercially important sh
species were higher in vegetated habitats (i.e. 8 of 12 species), though
dependence on vegetated habitats varied with diet. The greatest differ-
ence was for the herbivorous S. salpa, which feeds on seagrasses and
algae (Goldenberg and Erzini, 2014), followed by S. porcus. As an
ambush predator feeding mainly on decapod crustacea and sh
(Compaire et al. 2018), higher densities of S. porcus in vegetated habitat
is to be expected. Juveniles of the 6 other species, all Sparidae, with
higher densities and biomass in vegetated habitat, are omnivores,
feeding mainly on invertebrates associated with seagrass and algae
(Gonçalves and Erzini, 1998; Pita et al., 2002; Müller et al., 2020). Of the
four species that had higher density and biomass in unvegetated habitat,
S. pilchardus is a pelagic lter feeder, schooling in open water and thus
not expected to have an afnity for seagrass, while M. surmuletus and
S. aurata feed mainly on benthic invertebrates on unvegetated bottoms
(Bentes, 1996; Mazzola et al., 1999; Pita et al., 2002). D. labrax density
and biomass were also greater in unvegetated habitat, in contrast to
what was observed in seagrass habitats of estuaries along the Portuguese
coast (Vasconcelos et al., 2010) and of the Adriatic Sea (Bussotti and
Guidetti, 2011). However, D. labrax juveniles in salt marshes of Mont
Saint Michel Bay (France) did not depend exclusively on vegetated tidal
ats, feeding mainly on mysids and amphipods in different habitats,
including tidal creeks (Laffaille et al. 2001).
Higher densities in vegetated habitat are associated not only with
Table 6
Production estimates (g m
−2
y
−1
) and values (
€
) for vegetated (V), unvegetated (UV) habitats and for the whole Ria Formosa for single cohorts (age class 0) of each
species.
Vegetated habitat (V) Unvegetated habitat (UV)
Species Production (g
m
−2
y
−1
)
Annual
production (kg)
Production (g
m
−2
y
−1
)
Annual
production (kg)
V/UV
production
Total annual
production (kg)
€
kg
−1
V (
€
) UV(
€
) Total
value (
€
)
D. labrax 0.122 372.5 0.188 2994.2 0.648 3366.7 12.4 4619.0 37128.1 41747.1
S. aurata 0.104 319.0 0.159 2527.5 0.657 2846.5 10.41 3319.8 26303.2 29623.0
D. vulgaris 0.496 1518.5 0.223 3553.6 2.226 5072.0 3.8 5770.3 13503.7 19273.6
M. surmuletus 0.052 158.5 0.066 1051.8 0.785 1210.4 12.38 1962.7 13024.1 14988.0
D. sargus 0.099 303.3 0.046 738.1 2.141 1041.4 8.07 2448.8 5959.4 8408.2
S. cantharus 0.220 672.4 0.124 1983.2 1.766 2655.6 2.85 1916.3 5652.1 7568.5
S. porcus 0.408 1249.5 0.030 483.7 13.456 1733.2 2.00 2499.0 967.4 3466.4
D. puntazzo 0.042 129.7 0.011 172.4 3.917 302.1 5.8 753.6 1001.6 1755.2
S. pilchardus 0.047 142.8 0.077 1234.5 0.603 1377.3 1.01 144.9 1252.9 1397.9
B. boops 0.007 20.2 0.011 172.8 0.608 193.0 2.42 48.8 417.9 466.7
S. salpa 0.169 517.5 0.001 15.9 169.179 533.4 0.63 325.9 10.0 336.0
D. bellottii 0.058 179.0 0.004 58.6 15.917 237.5 1.36 243.2 79.6 322.7
TOTAL 1.824 5582.7 0.940 14,986.4 20,569.1 24,052 105,300 129,353
K. Erzini et al.
Ecosystem Services 58 (2022) 101490
9
increased food supply but also with shelter from strong tidal currents
and protection from predators, which in the Ria Formosa lagoon include
cuttlesh (Sepia ofcinalis), larger sea bass (D. labrax) and diving birds
such as the great cormorant (Phalacrocorax carbo). In contrast, Franco
et al. (2006) reported a minor nursery role of seagrass habitat in Venice
lagoon, Italy, compared to other lagoon habitats, attributing this in part
to a higher abundance of predators in seagrass meadows and a juvenile
preference for patches of unvegetated habitat near seagrass.
Fish survival rates were also higher in seagrass than in unvegetated
habitats for 6 out of 8 species, with survival enhanced by up to 72 % in
the case of D. sargus. These ndings are in line with the meta-analysis of
survivorship data of Heck et al. (2003) who reported signicant differ-
ences between seagrass habitat and unstructured habitat, but not be-
tween seagrass and other structured habitat, and of Lefcheck et al.
(2019) who reported that submersed aquatic vegetation (SAV) enhanced
survival. Anomalously low mortality values for S. porcus are probably
due to its cryptic, spiny and venomous characteristics, in common with
other Scorpaenidae (Santhanam, 2019).
Analysis of differences in growth between habitats were inconclu-
sive, suggesting that the species that prefer the seagrass habitat also use
the unvegetated habitat but in lower numbers, despite a certain degree
of site delity as indicated by the tagging study. High site delity and
relatively small home ranges of juveniles within the Ria Formosa are in
line with other studies such as those of Potthoff and Allen (2003) who
reported strong site delity within salt marsh creeks of juveniles of the
pinsh, Lagodon rhomboides (Sparidae) and of Ventura et al. (2015) for
four Sparids from a rocky coastline in Italy, three of which are among the
12 of the present study (D. puntazzo, D. sargus and D. vulgaris). However,
expansion of the home ranges of juveniles, reected in the mark-
recapture data and the acoustic telemetry studies of Abecasis and
Erzini (2008), Abecasis et al. (2012), is to be expected as the sh grow
(Ventura et al., 2015) and move towards the inlets and eventually out of
the Ria Formosa lagoon in the autumn. The patchy distribution of
vegetated habitat and information on the movement ecology of juveniles
derived from tagging and acoustic telemetry studies supports the
“seascape nursery” approach advocated by Nagelkerken et al. (2015),
with species strongly associated with vegetated habitat, but using a
mosaic of habitats (Sheaves, 2009; Whiteld, 2017) as they expand their
Table 7
Average rst sale price at auction (EUR kg
−1
), cohort biomass (t) for vegetated (V) and unvegetated (UV) habitat for lowest and highest M values for each species, total value of each cohort (EUR) and vegetation
enhancement per hectare (EUR ha
−1
). V (EUR ha
−1
)/UV EUR ha
−1
ratios >1.0 are in bold. Since ofcial auction statistics group all the different scorpionshes, the auction price for S. porcus was based on personal
observation of sh market prices (average of 4 EUR kg
−1
), with auction price assumed to be half the market price.
Low M High M EUR ha
−1
Cohort biomass (t) Value (EUR) Cohort biomass (t) Value (EUR) Low M High M
Species
€
/kg V UV V UV U +UV V UV V UV U +UV V UV V UV V/UV
B. boops 2.42 9.7 8.3 23,440 20,110 43,550 3.2 2.7 7,696 6,603 14,298 77 13 25 4 6.1
D. labrax 12.40 427.9 3273.7 5,305,421 40,592,720 45,898,141 214.4 1,640.2 2,658,180 20,338,208 22,996,389 17,338 25,466 8,687 12,759 0.7
D. bellottii 1.36 13.2 7.1 17,967 9,698 27,666 2.3 1.2 3,102 1,674 4776 59 6 10 1 9.7
D. puntazzo 5.81 50.0 21.6 290,178 125,234 415,411 30.7 13.3 178,343 76,969 255,312 948 79 583 48 12.1
D. sargus 8.07 54.2 199.7 437,758 1,612,406 2,050,164 25.5 93.9 205,781 757,958 963,739 1,431 1,012 672 476 1.4
D. vulgaris 3.80 26.2 60.7 99,508 230,479 329,987 5.2 12.2 42,374 46,140 88,514 325 145 138 29 2.2
M. surmuletus 12.38 0.8 7.1 9.857 88,239 98,096 0.7 5.6 8,197 68,910 77,107 32 55 27 43 0.6
S. pilchardus 1.01 15.2 44.8 188,726 45,435 234,160 3.5 10.2 43,125 10,382 53,507 617 29 141 7 21.6
S. salpa 0.63 77.3 2.9 78,429 1,821 80,250 20.8 0.8 21,149 491 21,640 256 1 69 0.3 224.4
S. porcus 2.00 2.9 1.2 1,813 2,393 4,206 0.1 0.0 47 62 110 6 2 0.15 0.04 3.9
S. aurata 10.41 70.5 922.9 141,061 9,604,597 9,745,658 39.5 516.8 78,983 5,377,798 5,456,780 461 6,025 258 3,374 0.1
S. cantharus 2.85 14.1 29.5 146,287 83,935 230,222 2.6 5.5 27,325 15,678 43,003 478 53 89 10 9.1
Total 762 4,580 6,740,444 52,417,068 59,157,512 348 2302 3,274,302 26,700,873 29,975,175 22,028 32,844 10,700 16,751
Fig. 5. Total annual landings of the European sea bass, D. labrax sold at auction
in southern Portugal (Algarve). MLS =minimum legal landing size. Source of
data: DGRM (Direç˜
ao-Geral de Recursos Naturais, Segurança e Servi-
ços Marítimos).
K. Erzini et al.
Ecosystem Services 58 (2022) 101490
10
range within the lagoon.
We showed here that seagrass meadows contribute to sh provi-
sioning of Ria Formosa through their role as nurseries or in terms of food
production as habitat for exploitable life history stages (Almeida et al.,
2008; Baker et al., 2020; Dewsbury et al., 2016; Costanza et al., 2017;
Nordlund et al., 2018; Unsworth et al., 2019). The Ria Formosa lagoon is
by far the most extensive vegetated transitional zone and juvenile sh
nursery in southern Portugal, where most of the coast consists of
exposed, sandy beaches that are not a suitable habitat for young-of-the-
year of most of the commercial sh species assessed in this study. The
importance of the Ria Formosa lagoon and its vegetated habitat as a
nursery are clear from the high site delity, high density and biomass,
evidence for growth, low mortality, and high production. In combina-
tion, our results support classifying the vegetated subtidal habitat of the
Ria Formosa lagoon as Nursery Role Habitat (NRH), Effective Juvenile
Habitat (EJH) and Essential Fish Habitat (EFH) for the majority of the
species, following the criteria of Beck et al. (2001), Dahlgren et al.
(2006) and Litvin et al. (2018).
5. Conclusion
The landscape approach used here to assess the sh nursery
ecosystem service of Ria Formosa lagoon, as advocated by Sheaves
(2009), Nagelkerken et al. (2015) and Whiteld (2017), combined with
the rst-time evaluation of sh provisioning services based on individ-
ual cohorts revealed the highly relevant economic contribution of Ria
Formosa to local coastal sheries. As well, our study highlighted the role
of subtidal seagrass meadows that enhance density, biomass, survival
and production of the majority of the species, which emphasizes the
importance of preserving and restoring this habitat in the Ria Formosa
lagoon. In fact, seagrasses have been declining in Ria Formosa, espe-
cially in the inter-tidal zone, due to meadow destruction and fragmen-
tation caused by the cultivation of bivalves and harvesting of
invertebrates for consumption and bait (Cunha et al., 2013).
On the other hand, some important commercial species are more
dependent on unvegetated habitat than vegetated habitat. A recent
threat to this ecosystem service of the unvegetated sub-tidal habitat of
the Ria Formosa is the aggressive takeover by the green algae Caulerpa
prolifera which may alter the structure of native faunal communities,
with likely negative implications for sheries (Parreira et al., 2021).
Given there are threats to all habitats in the Ria Formosa supports the
importance of using a whole lagoon landscape approach to assess
nurseries and sources of recruits to coastal sheries.
We hope that this study will contribute to improving the conserva-
tion and management of the Ria Formosa lagoon, the largest and most
important in Portugal, and to the sustainability of the small-scale coastal
sheries of southern Portugal.
Declaration of Competing Interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgements
This work was funded by the following projects: RIAVALUE (Valu-
ation of the ecosystem services delivered by Ria Formosa lagoon), FCT –
Foundation for Science and Technology (Portugal), ref. PTDC/MAR-
EST/3223/2014; ICTIORIA (Recruitment of sea breams (Sparidae) and
other commercially important species in the Algarve (southern
Portugal). Commission of the European Communities, DG XIV C1/99/
061; Portuguese national funds from FCT - Foundation for Science and
Technology through projects UIDB/04326/2020, UIDP/04326/2020
and LA/P/0101/2020 to CCMAR and 2020.03825.CEECIND to C.B.d.l.S.
We are grateful to the Direcç˜
ao-Geral de Recursos Naturais, Segurança e
Serviços Marítimos (DGRM) for providing landings and economic data.
We would like to thank our skipper and master sher, Isidoro Costa, and
all the students and volunteers who participated in the eldwork and
laboratory processing of the samples. A particular acknowledgment is
due to the referee for the extremely thoughtful and thorough reviews
that contributed greatly to improving the manuscript.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ecoser.2022.101490.
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