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Influence of seagrass meadows on nursery and fish provisioning ecosystem services delivered by Ria Formosa, a coastal lagoon in Portugal

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This study is the first to evaluate the fish 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 fish species by vegetated and unvegetated sub-tidal habitats. Based on monthly beach seine samples, total density and biomass of 96 species of fishes 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 fish 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 fisheries. Our evaluation of fish provisioning services based on data for individual cohorts of fish 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 fish that did not distinguish between cohorts. 1.
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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-
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Full Length Article
Inuence 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 dAzur, 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 afliation
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 (Whiteld, 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 specic areas for conservation and management.
Over time, the denition of nursery areas has shifted (Whiteld,
2017), with the mere presence of juveniles in particular habitats
considered insufcient 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 denition 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 specic 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; Whiteld, 2017).
Fodrie et al. (2009) stressed the implications of linking location-specic
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
quantied 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-specic 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×(i0.5)) (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 signicant 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, identication, measuring and weighing.
Following Monteiro et al. (1990), species were classied 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 scorpionsh),
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 simplies 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 identiable 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
conrmed using data on month of capture with a 1 mm mesh codend
Riley pushnet of the earliest post-larval juvenile stages (12 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×(1e(− 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-specic 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 signicant 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=eZ(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=
T1
t=0Nt+Nt+1
2.(Wt+1Wt)(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 ×tmax0.916(9)
M=4.118 ×K0.73×L0.33 (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-specic
survival rate St=eMt, the evolution in numbers of the cohort was
calculated by Nt=Nt1×St1. 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 ofcial
auctions where landings and rst sale prices are recorded. Ofcial 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. Speciesdensities 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).
Signicant differences in growth parameters between V and UV habitats
were found for D. sargus, D. vulgaris, S. cantharus and S. porcus (Hotel-
lings 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 condence 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 100500 m 5002000 m 20005000 m >5000 m Total
<1 week 34 39 73
12 weeks 20 31 1 52
2 weeks to 1 month 26 66 6 98
13 months 28 30 17 2 77
36 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 reected
in the Algarve ofcial 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, signicant 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% condence 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
20042005 and contributed signicantly to the landings for the next 4 to
5 years, as can be seen in the increase in landings from 2004 to 2005 to
20092010.
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 reected 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 afnity 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
cuttlesh (Sepia ofcinalis), 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 signicant 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
pinsh, 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, reected 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; Whiteld, 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 ofcial auction statistics group all the different scorpionshes, 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 Whiteld (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 inuence
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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K. Erzini et al.
... A number of studies have estimated the fish provisioning services or value of seagrass and other coastal habitats such as oyster beds and mangroves to fisheries by modelling adult fish biomass from juvenile abundance and life history parameters, combined with market or auction values (Peterson et al., 2003;Blandon et al., 2014a,b;zu Ermgassen et al., 2016;Jänes et al., 2020;Lai et al., 2020, zu Ermgassen et al., 2021, Erzini et al., 2022. Based on evidence of high site fidelity from mark-recapture (tagging) of juveniles in the Ria Formosa lagoon, Erzini et al. (2022) estimated juvenile densities in vegetated (V) and unvegetated (UV) habitats in the Ria Formosa lagoon and calculated the fish provisioning services of each habitat as the cohort lifetime or total biomass (TB), in the absence of fishing mortality. ...
... A number of studies have estimated the fish provisioning services or value of seagrass and other coastal habitats such as oyster beds and mangroves to fisheries by modelling adult fish biomass from juvenile abundance and life history parameters, combined with market or auction values (Peterson et al., 2003;Blandon et al., 2014a,b;zu Ermgassen et al., 2016;Jänes et al., 2020;Lai et al., 2020, zu Ermgassen et al., 2021, Erzini et al., 2022. Based on evidence of high site fidelity from mark-recapture (tagging) of juveniles in the Ria Formosa lagoon, Erzini et al. (2022) estimated juvenile densities in vegetated (V) and unvegetated (UV) habitats in the Ria Formosa lagoon and calculated the fish provisioning services of each habitat as the cohort lifetime or total biomass (TB), in the absence of fishing mortality. The economic value of a cohort was obtained by multiplying the lifetime biomass (kg) by the average first sale at auction price (€ kg − 1 ). ...
... The economic value of a cohort was obtained by multiplying the lifetime biomass (kg) by the average first sale at auction price (€ kg − 1 ). Vegetated habitat enhancement of fish provisioning services in biomass and economic value were calculated by dividing the total lifetime biomass and value per unit area of V habitat by the total lifetime biomass and value per unit area of UV habitat for each cohort (Erzini et al., 2022). ...
... The authors highlight that Tarwhine catches made up most of this value. Finally, Erzini et al. (2022) investigated the influence of seagrass meadows on nursery and fish provisioning ecosystem services delivered by Ria Formosa, a coastal lagoon in Portugal. Based on monthly beach seine samples, total density and biomass of 96 species of fishes were 1.89 and 3.03 times greater in vegetated habitats than unvegetated habitats. ...
... Based on monthly beach seine samples, total density and biomass of 96 species of fishes were 1.89 and 3.03 times greater in vegetated habitats than unvegetated habitats. Erzini et al. (2022) found a relatively greater economic importance of vegetated habitat when considering annual production values of 12 commercially important species. The value of vegetated habitat to production of this cohort of fish species recruited from seagrass was estimated to be €78.60/ha/year. ...
Technical Report
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This report provides an assessment of the social and economic benefits of ecosystem services generated by macroalgal restoration. It presents a case study for the Mediterranean Sea from the AFRIMED project. Key messages from the assessment are that ecosystem restoration will play a significant role for delivering on the European Union’s Green Deal and Blue Economy Strategy. Cystoseira restoration in the Mediterranean Sea has the potential to contribute to multiple Sustainable Development Goals for biodiversity conservation (SDG 14), climate change adaptation and mitigation (SDG 13) job security and economic development (SDG 8), food security (SDG 2) and good health and well-being (SDG 3). Future assessment of cost effectiveness of Cystoseira restoration would be improved by more consistent reporting on different costs and restoration outcomes. Evidence to quantify and value ecosystem services associated with Cystoseira remains limited. The AFRIMED Cost Benefit Analysis (CBA) of Cystoseira restoration demonstrates the economic case for restoration. It also provides an example of how marine ecosystem services can be integrated into economic decision making. The CBA case study also highlights many uncertainties with respect to restoration profiles, ecosystem service responses and how to monetise them.
... Protection from predators and more stable environmental conditions in the bay also support more optimal fish growth (Erzini et al. 2022;Siriwattanarat et al. 2024). The inside of the bay offers better protection from predators than the more open areas outside the bay. ...
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Awaluddin, Budimawan, Nadiarti, Nafie YAL. 2024. Biodiversity and distribution of rabbitfish (Siganidae) in Tanakeke Island, South Sulawesi, Indonesia. Biodiversitas 25: 2756-2762. The purpose of this research is to analyze the biodiversity of rabbitfish (Siganidae) in Tanekeke Island, South Sulawesi, Indonesia including species diversity, richness, evenness, and dominance. Data on Siganidae fish catches were collected from four different stations on Tanakeke Island, where each consisting of inside and outside bay zones. The data collection involved recording the total number of Siganidae fish caught with gillnet in each zone every month for a year. The caught fish were identified and categorized by species. A total 1,7421 were collected, with 1,5181 from inside the bay and 224 from outside the bay. The result indicated that species was dominated by Siganus canaliculatus (Park, 1797) with a frequency of 952 individuals (62.70%) inside the bay and 173 individuals (77.50%) outside the bay. Siganus guttatus (Bloch, 1787) ranks second, with 155 individuals (10.20%) inside the bay and 16 individuals (97.20%) outside the bay, followed by Siganus javus (Linnaeus, 1766), Siganus fuscescens (Houttuyn, 1782), Siganus punctatus (Schneider & Forster, 1801), and Siganus virgatus (Valenciennes, 1835). This research provides important insights that could greatly influence social and cultural aspects of local communities that depend on fisheries resources. The findings suggest that the bay provides more stable conditions that support the growth of rabbitfishes, allowing local communities for manage and conservation their fisheries resources.
... In the global ocean, essential marine ecosystem services are provided by seagrasses, as they create a habitat for mating, nursery (Nordlund et al. 2018), food and shelter for numerous associated species, including those with high commercial value. They are efficient in carbon sequestration, nutrient cycling, and coastal protection (Erzini et al. 2022;Mtwana Nordlund et al. 2016) and serve as biological and ecological indicators of the wellbeing of their connected communities and ecosystems (Purvaja et al. 2018). Ongoing climate change, coupled with other human disturbances, e.g., eutrophication, has caused seagrass declines globally (Espel et al. 2019;Lafratta et al. 2019) impacting their ecological services (Macreadie et al. 2019;Pansini et al. 2021). ...
Article
The potentially cascading consequences of climate changes on redistribution of habitat-forming species, like seagrasses, remain a major research gap. Empirical demonstrations of local population changes are increasingly reported without a globally integrated predictive framework as a leading testable hypothesis. Therefore, here, we aimed to estimate changes in species richness , community composition, and areas of climatic refugia under future climate scenarios. Location: Global scale. Time Period: Present-day conditions (from 2010 to 2020) and for three Shared Socioeconomic Pathway (SSP) scenarios of future climate change (from 2090 to 2100). Major Taxa Studies: Seagrasses (plantae). Methods: We coupled seagrass occurrences with environmental predictors (temperature, salinity, nitrate, wave energy, and ice) in stacked species distribution modelling. Results: Models estimated a present global extent of 917,169 km 2 with high species richness in Temperate Australasia, Indo-Pacific, and Temperate North Pacific. Future projections predicted widespread spatial redistribution, with Arctic expansions, losses in lower latitudes, and deeper vertical ranges, while globally maintaining the area extent occupied worldwide by seagrass species (only 5% of change). Species richness increased poleward under more drastic scenarios (SSP3-7.0 and SSP5-8.5), with losses in tropical zones (30 o N to 30 o S). Local climatic refugia are retained in all scenarios but decrease under higher emissions. Additionally, even where seagrass species remain, widespread community composition changes were predicted. Main Conclusions: Our findings serve as baselines to inform, anticipate, and mitigate cascading consequences of shifts in sea-grass ecosystems that provide essential services for humanity.
... This valuable transition water body of regional, national, and international ecological importance is a site of Natura 2000 network (PTZPE0017), EU Birds Directive Special Protection Area and has been part RAMSAR wetland convention since 1980. This coastal lagoon is an important ecosystem with high biodiversity and serves as a nursery area for several species, including several commercial species (Erzini et al., 2022). The lagoon has several seagrass meadows with associated species, including several endangered species, such as Hippocampus guttulatus and H. hippocampus (Caldwell and Vincent, 2012). ...
Article
This study describes the presence of the royal cucumber Parastichopus regalis (Cuvier, 1817) in The Natural Park of Ria Formosa (NPRF), Portugal. A single individual was observed during a monitoring scuba dive at a depth of 3 m inside this shallow mesotidal lagoon. The most plausible explanation for this occurrence is attributed to the rejection by trawlers when returning to their home port from their fishing grounds. This marine species has a deeper distribution outside the lagoon and is commonly captured as by-catch and subsequently discarded. This study also alerts us to the growing presence of non-indigenous species and the emergent threat of new invasions, highlighting the need to adopt biosecurity measures, like good practices for fishers when dealing with discards to avoid new species introductions in this fragile coastal marine habitat.
... Therefore, the catches estimated in this study were higher than the historical catches. In other lagoons, quantification of provisioning services from the biomass of several commercial fish in vegetated and unvegetated areas of eelgrass beds has been reported 48 . In this study, a significant feature is that the spatial distribution relationship between eelgrass beds and shrimp was shown and the potential map was created to calculate the provisioning services. ...
Article
Full-text available
Eelgrass beds provide a habitat for many high-value fishery resources, and provisioning services, one of the ecosystem services, need to be quantified. However, few examples have been evaluated spatially. We determined the distribution of eelgrass beds in Lake Notoro, a marine lagoon in Hokkaido, Japan, and quantified the provisioning services by the eelgrass beds in relation to Pandalus latirostris, a fishery resource. Acoustic measurement surveys of the eelgrass beds and catch surveys of the shrimp were conducted in July and August 2015. The relationship between catch per unit effort (CPUE) of shrimp and the distribution of eelgrass beds was shown. The estimated distribution area of eelgrass beds was 7.07 km². Shrimp was frequently caught at water depths of 3–5 m, approximately 200 m from the edge of the eelgrass beds. The expected catch of shrimp in the fishing area of Lake Notoro in 2015 was 25.37 tons and US$ 463.6 thousand. Eelgrass beds were found to affect the fisheries production not only on the inside but also at the edge and outside. The entire coastal space should be evaluated, while considering the effect of the distribution of eelgrass beds, to quantify the provisioning services.
Article
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https://science.sciencemag.org/content/370/6517/670.1
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Nearshore‐structured habitats—including underwater grasses, mangroves, coral, and other biogenic reefs, marshes, and complex abiotic substrates—have long been postulated to function as important nurseries for juvenile fishes and invertebrates. Here, we review the evolution of the “nursery habitat hypothesis” and use >11,000 comparisons from 160 peer‐reviewed studies to test whether and which structured habitats increase juvenile density, growth, and survival. In general, almost all structured habitats significantly enhanced juvenile density—and in some cases growth and survival—relative to unstructured habitats. Underwater grasses and mangroves also promoted juvenile density and growth beyond what was observed in other structured habitats. These conclusions were robust to variation among studies, although there were significant differences with latitude and among some phyla. Our results confirm the basic nursery function of certain structured habitats, which lends further support to their conservation, restoration, and management at a time when our coastal environments are becoming increasingly impacted. They also reveal a dearth of evidence from many other systems (e.g., kelp forests) and for responses other than density. Although recent studies have advocated for increasingly complex approaches to evaluating nurseries, we recommend a renewed emphasis on more straightforward assessments of juvenile growth, survival, reproduction, and recruitment.
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The significant role seagrass meadows play in supporting fisheries productivity and food security across the globe is not adequately reflected in the decisions made by authorities with statutory responsibility for their management. We provide a unique global analysis of three data sources to present the case for why seagrass meadows need targeted policy to recognize and protect their role in supporting fisheries production and food security. (1) Seagrass meadows provide valuable nursery habitat to over 1/5th of the world's largest 25 fisheries, including Walleye Pollock, the most landed species on the planet. (2) In complex small-scale fisheries from around the world (poorly represented in fisheries statistics), we present evidence that many of those in proximity to seagrass are supported to a large degree by these habitats. (3) We reveal how intertidal fishing activity in seagrass is a global phenomenon, often directly supporting human livelihoods. Our study demonstrates that seagrasses should be recognized and managed to maintain and maximize their role in global fisheries production. The chasm that exists between coastal habitat conservation and fisheries management needs to be filled to maximize the chances of seagrass meadows supporting fisheries, so that they can continue to support human wellbeing.
Article
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Estuaries and other coastal habitats are considered essential for the survival of early life stages of commercial, recreational, and other ecologically important species. While early designations simply referred to habitats with higher densities of juveniles as nurseries, the definition was improved by arguing that contribution per unit area to the production of individuals that recruit to adult populations is greater, on average, in nursery habitats. However, this and related approaches typically consider critical habitats as individual, homogeneous entities that are static in nature and do not specifically incorporate important dynamics that determine nursery function. The latter include environmental variability, estuarine hydrodynamics, trophic coupling, ontogenetic habitat shifts, and spatially explicit usage of habitat patches and corridors within larger seascapes. Subsequent studies have identified important factors that regulate nursery value, and researchers working independently across the globe have not only supported the advances made in defining the processes underlying nursery function but, as set forth in this narrative, have advanced it while suggesting that much work still needs to be done to improve our understanding of the links between juvenile nekton survival and the estuarine-coastal seascape. We discuss the current nursery role hypothesis and the data supporting (or refuting) it along with the implications for management of estuarine habitats for the conservation or restoration of nursery function.
Article
The genus Caulerpa has attracted much attention because many of its species were introduced into non-native regions and became notoriously invasive. This is the case of Caulerpa prolifera that has been rapidly expanding in Ria Formosa lagoon, taking over the deeper unvegetated soft bottoms and competing with seagrass meadows in the shallower areas. Here we address how C. prolifera invasion may affect the support of biodiversity, and specifically, the provision of habitat and nursery for commercial species by the native habitats of this coastal lagoon. Even though no significant differences in total species richness, diversity and evenness were found between C. prolifera and the native unvegetated habitat, the dissimilarity between these two habitats was highest, mostly driven by the extreme reduction of the gastropod Bittium reticulatum and of the tanaid Apseudopsis formosus. This may implicate changes in the trophic interactions of the ecosystem, for example decreasing the tanaid food source for seahorses, which are presently endangered in the lagoon. On the other hand, the fauna species richness, diversity and evenness were significantly higher in the native seagrass habitat than in C. prolifera. Juveniles of valuable flat and sparid fish were only observed in unvegetated sediments and seagrass meadows, respectively. The aggressive spread of C. prolifera in Ria Formosa may alter the structure of native faunal communities, with likely negative implications on fisheries. Nevertheless, the global biodiversity of the lagoon will not be likely drastically affected unless the seaweed takes over the seagrass meadows.
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Previous laboratory feeding experiments, representing the state-of-the-art methodology to investigate micro-plastic (MP) ingestion and its impact for fish, tend to disregard both the significance of applying realistic MP densities and the potential relevance of biofilm-coating for ingestion probability. This experiment assessed the uptake of either pristine or biofilm-coated MP particles and the physiological impacts for juvenile white seab-ream for MP concentrations consistent with those found in the field along with natural prey over a course of 3.5 weeks. Results indicate the ability of juvenile D. sargus to discriminate between edible and non-edible prey. A distinct preference for biofilm-coated over pristine particles could not be verified. No significant impact on growth and condition was found except for high levels of MP ingestion. The outcomes highlight the importance of performing MP feeding experiments mimicking natural conditions to reliably assess the impact of MP on early life stages of fish.
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Coastal ecosystems are estimated to support 95% of the world’s commercially-important fish, owing largely to their provision of nursery habitat for juveniles; however, systematic databases with such data are scarce. By systematically reviewing the literature across Australia, we quantified fisheries enhancement from three key coastal vegetated habitats: seagrass meadows, mangrove forests, and tidal marshes. From juvenile densities, we modelled adult fish biomass enhancement resulting from these structured habitats and linked fish of economic importance with market values. We found that seagrass displayed higher per hectare abundance, biomass and economic enhancement compared to mangroves and tidal marshes. On average, one hectare of seagrass supported 55,000 more fish annually compared to unvegetated seabed, resulting in an additional biomass of 4000 kg and a value increase of AUD 21,200 annually. Mangroves supported 19,000 more fish, equivalent to 265 kg⁻¹ ha⁻¹ y⁻¹, and tidal marshes provided a modest 1700 more fish, equivalent to 64 kg⁻¹ ha⁻¹ y⁻¹. The most abundant fish across all ecosystems were small, non-commercial species (e.g. gobies and glassfish), but the highest biomass and economic value originated from larger, longer-lived fish that are regularly targeted by fisheries (e.g. breams and mullets). By quantifying enhancement value across Australia, our findings provide further evidence for, the benefit these critical habitats provide in supporting coastal fisheries and human well-being.
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To investigate dispersal and connectivity between spawning and lagoon nursery habitats of the gilthead seabream, Sparus aurata, in the Gulf of Lions (northwestern Mediterranean Sea), we modeled the potential transport of the species' larvae between its supposed main spawning site in the region (the Planier Island) and two of its main local nursery areas (the coastal lagoons of Thau and Salses-Leucate). Passive larval drift simulations using a dispersal biophysical model showed a large variability in the possible trajectories from spawning to nursery areas and in the predicted ages for larvae arrival on the two nursery sites. The most common ages at arrival obtained in the simulations (20-60 days) are broadly consistent with previous modeling studies but contrast with the actual ages of the S. aurata post-larvae collected in 2016 and 2017 at time of the lagoon entrances (60-90 days, from otolith readings). The period between 25 and 70 days being critical for gilthead seabream larvae to acquire sufficient swimming, osmoregulatory, and olfactory abilities to enter coastal lagoons, we argue that ontogenic development plays a crucial role in the transport and local retention of S. aurata larvae in the studied region, explaining the discrepancy between simulation results and observed data.
Article
Estuarine-dependent marine fish species rely on shallow, sheltered and food rich habitats for protection from predators, growth and ultimately recruitment to adult populations. Hence, habitats within estuaries function as critical nursery areas for a variety of fish species. Results from stomach content analysis and dietary diatom composition of a ubiquitous estuarine-dependent species Rhabdosargus holubi (Steindachner, 1881) in the main vegetated and un-vegetated habitats in the Bushmans Estuary, South Africa, were interpreted along with published information on habitat complexity, relative abundance and behaviour of this species. Although the complexity of seagrass, together with the higher abundance and behaviour of R. holubi in seagrass suggests that this is the main nursery habitat (in terms of both feeding and protection from predation), the dominance of red filamentous algae and the presence of some invertebrates mainly in the diet of fish from un-vegetated habitats indicates that this species is using a mosaic of habitats, including un-vegetated areas, for foraging. Based on the above findings, and results from other studies, it is concluded that juvenile R. holubi in permanently open estuaries makes use of a range of habitats according to macrophyte shelter from predators, the availability of preferred food resources and physical drivers such as water depth and tidal phase. This study demonstrated that a multi-method approach, as opposed to a single method approach (diet alone) is useful to assess the nursery value of juvenile fish habitats.