RESEARCH ARTICLE
Seagrass Ecosystem Services and Their
Variability across Genera and Geographical
Regions
Lina Mtwana Nordlund
1
*, Evamaria W. Koch
2†
, Edward B. Barbier
3
, Joel C. Creed
4
1 Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91, Stockholm,
Sweden, 2 Horn Point Laboratory, University of Maryland Center for Environmental Science, Cambridge,
MD, 21613, United States of America, 3 Department of Economics and Finance, University of Wyoming,
1000 E. University Ave., Laramie, WY, 82071, United States of America, 4 Laborato
´
rio de Ecologia Marinha
Bêntica, Departamento de Ecologia, Instituto de Biologia Roberto Alca
ˆ
ntara Gomes, Universidade do
Estado do Rio de Janeiro – UERJ, PHLC Sala 220, Rua São Francisco Xavier 524, CEP 20559-900, Rio de
Janeiro, RJ, Brazil
† Deceased.
*
lina.mtwana.nordlund@su.se
Abstract
Threats to and loss of seagrass ecosystems globally, impact not only natural resources but
also the lives of people who directly or indirectly depend on these systems. Seagrass eco-
systems play a multi-functional role in human well-being, e.g. food through fisheries, control
of erosion and protection against floods. Quantifying these services reveals their contribu-
tions to human well-being and helps justify seagrass conservation. There has been no com-
prehensive assessment as to whether seagrass ecosystem services are perceived to vary
over the globe or amongst genera. Our study compiles the most complete list of ecosystem
services provided by seagrasses so far, including bioregional- and genus-specific informa-
tion from expert opinion and published studies. Several seagrass ecosystem services vary
considerably in their (known) provision across genera and over the globe. Seagrasses gen-
era are clearly not all equal with regard to the ecosystem services they provide. As sea-
grass genera are not evenly distributed over all bioregions, the presence of an ecosystem
service sometimes depends on the genera present. Larger sized seagrass genera (e.g.
Posidonia, Enhalus) are perceived to provide more substantial and a wider variety of eco-
system services than smaller species (e.g. Halophila, Lepilaena). Nevertheless, smaller
species provide important services. Our findings point out data gaps, provide new insight
for more efficient management and recommend caution in economic valuation of seagrass
services worldwide.
Introduction
Humans are dependent on ecosystem services (ES), so understanding which ecosystem services
are provided by seagrasses and how these services are distributed in space is important.
PLOS ONE | DOI:10.1371/journal.pone.0163091 October 12, 2016 1 / 23
a11111
OPEN ACCESS
Citation: Mtwana Nordlund L, Koch EW, Barbier
EB, Creed JC (2016) Seagrass Ecosystem Services
and Their Variability across Genera and
Geographical Regions. PLoS ONE 11(10):
e0163091. doi:10.1371/journal.pone.016309 1
Editor: Kurt O. Reinhart, USDA-ARS Fort Keogh
Livestock and Range Research Laboratory,
UNITED STATES
Received: August 28, 2015
Accepted: September 2, 2016
Published: October 12, 2016
Copyright: © 2016 Mtwana Nordlund et al. This is
an open access article distributed under the terms
of the
Creative Commons Attribution License,
which permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All data is presented
in the manuscript or if data is from elsewhere the
appropriate reference for the data source is
indicated.
Funding:
http://www.formas.se/en/ received by
LMN. The funders had no role in study design, data
collection and analysis, decision to publish, or
preparation of the manuscript.
http://wsa.
seagrassonline.org/
. LMN received financial
support to arrange and attend the workshop.
Seagrasses are marine flowering plants, which form extensive meadows in shallow coastal
waters on all continents except Antarctica [
1], [2] (Fig 1). The intertidal to shallow subtidal
location of most seagrasses allows relatively easy access and multiple uses as well as exposing
seagrass ecosystems to both terrestrial and marine based threats [
3], [4], [5]. The many threats
to seagrass are causing it to rapidly disappear globally [
3], [5], [6], [7]. Still, seagrass receives
less attention than other habitats (e.g. mangrove and coral reefs) and is often not considered in
coastal management decisions [
3], [8], [9].
Seagrasses undoubtedly provide many ecosystem services [
4], [10], defined here as natural
processes and components that benefit human needs, directly or indirectly [
11]. However, the
variability in the provision of ecosystem services by different genera of seagrasses is largely
unknown. Although seagrasses are structurally similar, they vary widely in size and productiv-
ity [
12]. For example, the leaves of some genera may reach just a centimetre above the sediment
surface while others extend canopies several meters into the water column. Rhizomes and roots
may also penetrate and modify different depths of sediments depending on the genera. These
differences in the size and productivity of seagrasses can influence all key ecosystem services,
especially important services such as coastal protection, nursery habitats, and sediment accre-
tion and stabilization [
13], [14], [15].
Fortunately, the number of publications about seagrass is rapidly increasing but findings are
not always presented in the context of an ecosystem service, likely due to the fact that often the
focus of a study is not strictly on ecosystem services. For example, a study about trophic impor-
tance of diatoms in seagrass or research on seagrass wrack as fertilizer in the coastal areas may
not present their finding as an ecosystem service [16], [17]. Thus, it remains a challenge to get
an overview of existing seagrass ecosystem services, and which services arise from different
genera and bioregions, from the literature.
Seagrass ecosystem services, like all other ecosystem services, are difficult to value and rank
as the benefits to humans are difficult to quantify. In some areas seagrass ecosystem services,
Fig 1. Seagrass meadow exposed during low tide. Patchy seagrass meadow dominated by Thalassodendron ciliatum
during low tide in Zanzibar, Tanzania. Photo credit: Lina Mtwana Nordlund.
doi:10.1371/journal.pone.0163091.g00 1
Seagrass Ecosystem Services
PLOS ONE | DOI:10.1371/journal.pone.0163091 October 12, 2016 2 / 23
Competing Interests: The authors have declared
that no competing interests exist.
such as fish and invertebrate habitat, are crucial to the lives of the local community [4], [18],
while in other areas those services are valuable but their loss would not directly affect the local
communities. For accurate valuation of coastal and marine ecosystems, including seagrass eco-
systems, spatial and temporal variation in the provision of services as well as synergies among
ecosystem functions need to be understood and evaluated [
13], [19], [20]. There have been
some attempts to estimate the economic value of seagrass ecosystem services, but with limited
available information accurate estimates are very difficult to obtain [
10], [15], [21], [19], [22].
This suggests that there is a considerable gap in the literature when it comes to determining the
contribution of seagrasses worldwide in terms of the provision of ecosystem services, or bene-
fits, to humankind.
Here we review global seagrass ecosystem services and contrast seagrass genera to demon-
strate variability in the provisioning of ecosystem services and to identify important gaps in
our existing knowledge. To address this we used two approaches, a workshop that elicited
information from experts and a selective literature search. Based on the expert workshop, we
first identify ecosystem services known to be provided by each seagrass genus in the six differ-
ent seagrass bioregions [
2]. With these data, we analyze frequency and variation of seagrass
ecosystem services. Based on the selective literature search, we enhance the findings from the
expert workshop and create an overview with example references of ecosystem services. We
thereafter discuss the variation of seagrass ecosystem services and highlight potential problems
with limited knowledge about these services.
Materials and Methods
Definitions of the Concepts
The definition used for ecosystem services is based on the standardized framework by De
Groot et al. 2002 [
11]; they identified 23 ecosystem functions that provide a much larger num-
ber of goods and services, hereafter called services. They define ecosystem functions as ‘the
capacity of natural processes and components to provide goods and services that satisfy human
needs, directly or indirectly’ [11]. The bioregions used in this study are the six seagrass biore-
gions according to Short et al. (2007) [2] which is the current standard used by the interna-
tional seagrass research community. These six bioregions are Temperate North Atlantic (I),
Tropical Atlantic (II), Mediterranean (III), Temperate North Pacific (IV), Tropical Indo-
Pacific (V), and Temperate Southern Ocean (VI), and are based on assemblages of taxonomic
groups of seagrasses in temperate and tropical areas and the physical separation of the world's
oceans.
Survey of Experts
Expert knowledge is used widely in the science and practice of conservation, and eliciting opin-
ions and information from experts is commonly used to fill knowledge gaps [
8], [23], [24],
[
25], [26]. In this study, we have followed the five step expert-elicitation approach [25]. We use
the definition of an expert proposed by Krueger et al. [
24], namely “an expert can be anyone
with relevant and extensive or in-depth experience in relation to a topic of interest”. Based on
these criteria, we define experts as managers, practitioners and researchers working with (a)
questions related to the natural or social environment of seagrass, and/or (b) questions relevant
to seagrass ecosystems. Our goal for selecting seagrass experts was to include a broad range of
expertise from many different fields.
To gather expert knowledge we held a workshop entitled “Seagrass ecosystem services:look-
ing back for existing knowledge and into the future for new approaches” during the 10
th
Inter-
national Seagrass Biology Workshop (ISBW), in Buzios, Brazil in 2012. The ISBW attracts
Seagrass Ecosystem Services
PLOS ONE | DOI:10.1371/journal.pone.0163091 October 12, 2016 3 / 23
participants from academic institutions, government agencies and non-government organiza-
tions with expertise in seagrass biology, ecology, management, monitoring and social aspects
of seagrass research. ISBWs take place every other year with participants from all over the
world. The 91 workshop participants from 25 nations constituted most of the 101 ISBW
attendees (i.e. 90%), as there were no other parallel sessions. The participation in the workshop
was voluntary and before starting all participants were made aware that the results would be
published in a scientific journal.
The aim of the workshop was to survey the provision of ecosystem services by seagrass gen-
era in different bioregions. During the first part of the workshop the goal was to identify eco-
system services known to be provided by seagrass somewhere on the planet. Through an open
floor discussion, we encouraged participants to add, change or remove ecosystem services to a
list provided to all participants (due to time constraints we started the workshop by presenting
a preliminary list of a few ecosystem services commonly listed in the scientific literature [
15],
[
27]). The organizers also noted when specific information about a seagrass ecosystem service
was mentioned (later added to
Fig 2). A final list was agreed upon by the participants. The list
has no prioritization, but is arranged to have similar ecosystem services clumped. The
Fig 2. Ecosystem services (ES) provided by seagrass—expert eliciting. Colours represent consensus view of experts’ in
each bioregional group. Red represents service not present; grey unknown and green service present. A sum of present,
unknown, not present services scores can be seen in the table to the far right per ES and at the bottom for each genus in every
bioregion. Bioregions according to Short et al., 2007 [
2]:I = Temperate North Atlantic, II = Tropical Atlantic, III = Mediterranean,
IV = Temperate North Pacific, V = Tropical Indo-Pacific, VI = Temperate Southern Oceans. At the far left # indicates a number
that corresponds to the same ecosystem service in
Table 1 facilitate comparisons, and has no prioritization.
doi:10.1371/journal.pone.0163091.g002
Seagrass Ecosystem Services
PLOS ONE | DOI:10.1371/journal.pone.0163091 October 12, 2016 4 / 23
workshop organizers then finalised an excel file that contained the list of 25 ecosystem services
on the y-axis, and on the x-axis the six bioregions nested in each of the 13 seagrass genera (the
skeleton of
Fig 2). Even though we are aware seagrass species’ characteristics may vary (e.g.
size), we focused on seagrass genera, due to time constraints, the large amount of data, paucity
of knowledge of some species and to facilitate group work.
During the second part of the workshop, participants were divided into groups representing
the six bioregions (and into sub-groups in highly diverse bioregions) based on their geographi-
cal working experience (i.e. where their expertise was strongest). The groups were asked to add
information based on their own knowledge (through publications, ongoing research, their own
research and own observations) of seagrass ecosystem service within their bioregion. They
were asked to fill an excel spreadsheet and score each ecosystem service for each genus present
in the bioregion. Experts gave each ecosystem service a categorical score indicating the ecosys-
tem service was known to be present, might be present, not present, and unknown/unsure.
Internet searches were allowed. Each bioregion had the following number of respondents dur-
ing the second half of the workshop: seven for Temperate North Atlantic (I), eight for Tropical
Atlantic (II), five for the Mediterranean (III), eight for Temperate North Pacific (IV), eleven
for Tropical Indo-Pacific (V) and six for Temperate Southern Oceans (V). Results, the consen-
sus view of all group members, were reported by the facilitators of groups from each bioregion.
We later decided to use three instead of the original four categories, namely (1) service
known to be present; (2) service unknown (service might be present, ranging from unlikely to
likely); (3) service known to be not present (service could not be classified even in the
“unknown” category). This was done as a precaution as some experts did not distinguish
between unknown and might be present. The data from all groups were then compiled into
one table (Fig 2). After the workshop, the table was circulated via e-mail to an additional twelve
seagrass experts that did not attend the 10th ISBW and have expertise from Africa, for potential
gap filling, but the response frequency was very poor. These additional experts were also
informed that their responses were to be used in a scientific publication.
The specific hypotheses in the survey of experts part of the study was: i) some ESs are more
frequently present than others, independently of genera present; ii) variation exists in the pro-
vision of seagrass ESs among the globes bioregions; iii) more genera present per bioregion pro-
vide more ESs; iv) different seagrass ESs are provided by different genera and with varying
frequency; v) Seagrass genus size will predict the frequency of provision of ESs.
Statistical analyses. The statistical analyses are based on the expert opinion data compiled
in
Fig 2. The original four categories were converted into three categories (see above). We used
frequency of known occurrence (service present) in our analyses. Thereafter we calculated
means of frequencies across the (25) services and across the (6) bioregions and/or 13 genera to
empirically test the stated hypotheses (i-v). To account for unequal number of genera among
bioregions, means of frequencies were also calculated relative (relativized) to the number of
genera present.
Total frequencies of present, unknown and not present ES (per service) were calculated
across all genera and bioregions. Total frequencies of present, unknown and not present ES for
each per genera in each bioregion were calculated across all ES.
We used ANOVA and Tukey tests to compare the frequency of presence of the different
perceived services (as bioregional means) and compared them with genus standardised per-
ceived services (as bioregional means) as well as to analyse differences among means of fre-
quencies (only presence) of the perceived relative (known) provision of different ecosystem
services among bioregions. We also compared differences among means of frequencies of the
perceived provision of different ecosystem services among bioregions and relativized per
genus. In order to examine the multivariate relationship between frequency (only presence) of
Seagrass Ecosystem Services
PLOS ONE | DOI:10.1371/journal.pone.0163091 October 12, 2016 5 / 23