Ecological Engineering 120 (2018) 585–594

Contents lists available at ScienceDirect

Ecological Engineering
journal homepage: www.elsevier.com/locate/ecoleng

Marine ecosystem restoration and biodiversity offset T

a,⁎ b d c
Céline Jacob , Anaïs Buffard , Sylvain Pioch , Sébastien Thorin
a
CEFE UMR 5175, CNRS – Université de Montpellier – Université Paul-Valéry Montpellier – EPHE – Université Paul-Valéry Montpellier, Route de Mende 34 199,
Montpellier Cedex 5, France
b
CEFE UMR 5175, CNRS – Université de Montpellier – Université Paul-Valéry Montpellier – EPHE – Université Paul-Valéry Montpellier, Route de Mende 34 199,
Montpellier Cedex 5, France
c
Les Belvédères, Bâtiment B, 128, avenue de Fès, 34080 Montpellier, France
d
CEFE UMR 5175, CNRS – Université de Montpellier – Université Paul-Valéry Montpellier – EPHE – Université Paul-Valéry Montpellier, Route de Mende 34 199,
Montpellier Cedex 5, France

A R T I C L E I N F O A B S T R A C T

Keywords: The mitigation hierarchy is increasingly used in environmental policy as a way of reconciling economic de-
Restoration velopment and biodiversity conservation. The principle of the mitigation hierarchy is to avoid, reduce and offset
Marine ecosystems the environmental impacts arising from development projects by providing ecological gains through con-
Mitigation hierarchy servation or restoration measures. Most of the research on its implementation to date has focused on terrestrial
Offsetting
ecosystems. In this study, we investigated the relevance of marine ecosystem restoration in meeting offset re-
Environmental impact assessments
quirements. Stemming from a brief literature review on existing restoration techniques for marine ecosystems
(e.g. coral reefs, seagrass meadows, macroalgae beds, ‘green’ marine construction, and marine sediment re-
mediation) and our experience on Environmental Impact Assessments undertaken in mainland France and in its
oversea territories, we discuss the main criteria ensuring a suitable use of ‘restoration’ practice regarding offset
requirements. We then clarify the different levels of equivalence that should be met when designing offsets
relying on ‘restoration’ techniques. This study aims to clarify to what extent the environmental impacts of
economic activity on marine biodiversity can be offset through marine ecosystem restoration.

1. Introduction undertake on-site restoration, and lastly to offset residual impacts so

Currently, more than half of the world’s population lives within
60 km of the coast (United Nations Environment Programme). This has
led to an increase in marine environmental damage due to a number of
causes: exploitation of renewable resources (fisheries), non-renewable
resources (mineral and energy extraction), coastal artificialization, and
the discharge of pollutants and marine debris. According to Halpern
et al. (2015), 66% of the ocean show increased human impact over 5
years (2008–2013). As stated by Dulvy et al. (2003), the second leading
cause of marine extinction is habitat loss at 37% (the leading cause is
exploitation at 55%).
In light of these important environmental stakes, numerous policies
could be regarded as tools aiming at halting marine biodiversity loss.
One of these, based on the No Net Loss principle, that emerged at the
end of the 1980s in the United States,1 consists of ensuring that the
biodiversity impacts caused by a project are balanced or outweighed by
measures taken firstly to avoid or minimize these impacts, secondly to
that no loss results (BBOP, 2012).
As very few studies have examined the implementation of offsets in
the marine realm, in this paper, we rely on the observation made by
Jacob et al. (2016a) within the framework of French marine Environ-
mental Impact Assessments (EIAs). Indeed, they showed that offset
measures proposed in the studied EIAs fell into the following categories,
in line with “Offset activities” as defined by the BBOP2:
1. Undertaking positive management interventions such as restoration
of degraded habitat (referred to as “active restoration” thereafter)
(e.g. restoration of coral reefs using larvae collected from colonies
after spawning and grown in nurseries before transplantation,
creating artificial habitats with the same ecological function as the
one lost, planting seagrass from nurseries) or reducing/removing
current threats or pressures (referred to as “passive restoration”
thereafter)
2. Averting risk (e.g. the creation of marine protected areas – MPAs)

⁎
Corresponding author.
E-mail addresses: celine.jacob@cefe.cnrs.fr (C. Jacob), anais.buffard@gmail.com (A. Buffard), sylvain.pioch@gmail.com (S. Pioch), thorin@creocean.fr (S. Thorin).
1
Recommended at the National Wetland Policy Forum in 1987 and adopted by George H. W. Bush’s administration in 1989.
2
An international collaboration between companies, institutions and organizations, both private and public, that develops best practice in biodiversity offset.

http://dx.doi.org/10.1016/j.ecoleng.2017.09.007
Received 7 July 2016; Received in revised form 22 August 2017; Accepted 9 September 2017
Available online 19 September 2017
0925-8574/ © 2017 Elsevier B.V. All rights reserved.
C. Jacob et al.
3. Knowledge acquisition measures (e.g. monitoring programs) or
awareness-raising measures (e.g. exhibition on the ecological role of
Posidonia oceanica)
4. Compensation packages3 for local stakeholders affected by the de-
velopment project (e.g. post-larvae capture and culture; the creation
of artificial reefs; beach reprofiling and nourishment for tourism;
supporting a development program, communication initiatives or
product valorization for aquaculture; the eradication of invasive
species)
Moreover, alternative measures, not encountered in these EIAs and
still subject to debate and discussion, may prove effective in terms of
biodiversity offset. These deal with the enhancement of coastal infra-
structures aiming at improving “conditions for species through the
modification of development activities undertaken primarily for non-
ecological reasons” to increase the ecological value of structures
(Naylor et al., 2012). This could be undertaken through ecological
engineering of coastal structure such as breakwaters, seawalls, jetties,
pilings (Dafforn et al., 2015) or eco-design or ‘green’ marine con-
struction (Pioch et al., 2011). Other types of enhancements can be
found in the marine coastal realm such as “removing structures and
impediments to natural ecosystem processes that are most likely to
promote successful and sustainable ecology” (Elliott et al., 2016), not
addressed in this paper and pollution removal via discharge controls,
treatment and bioremediation.
Thus offset measures proved to rely heavily on solutions based on
marine ecosystem restoration.
Strictly speaking, ecological restoration refers to the process of as-
sisting the recovery of a damaged ecosystem so that the latter can be
self-supporting, resilient to perturbation without further assistance and
displays a historical continuity in terms of its structure, functioning and
biological composition (Clewell et al., 2010; SER Primer, 2004). This is
thus an intentional activity that initiates or accelerates an ecological
pathway—or trajectory through time—towards a reference state. In the
case of ecological engineering, particular attention is paid to the ef-
fectiveness of a solution in economic terms through “manipulation of
natural materials, living organisms and the physico-chemical environ-
ment to achieve specific human goals and solve technical problems”
(SER Primer, 2004). This discipline is related to ecological restoration,
but differs in that it can also involve the creation of surrogate ecosys-
tems, services supplied by an ecosystem take priority over biodiversity
and historical continuity. Other terms are often found in the literature
(Abelson et al., 2016; Elliott et al., 2007) such as enhancement for “a
management approach which directly or indirectly increases the eco-
logical value, goods and services of the habitat” or rehabilitation for
“practices which lead to partial recovery” and reclamation for “prac-
tices that improve either or both the ecosystem structure or function but
not toward the original state”. Enhancement and reclamation are
usually related to ecological engineering. Here, we will use the term
‘restoration’ in a broad meaning.
Adopting an environmental management perspective, we in-
vestigate to what extent ‘restoration’ can provide relevant offset solu-
tions, that is to say meeting offset requirements. To that end, we
compare the results of existing ‘restoration’ techniques with offset
principles. We base our analysis on a brief literature review of available
‘restoration’ techniques to get a representative (but not exhaustive)
overview of current techniques and their relative degree of im-
plementation and on the experience developed mainly in mainland
France and in its oversea territories but also in California. This review
3
Compensation is a recompense for some loss or service, and is something which
constitutes an equivalent to make good the lack or variation of something else. It can
involve something (such as money) given or received as payment or reparation (as for a
service or loss or injury) (BBOP, 2012). BBOP defines compensation as reparation of
biodiversity offset that falls short of achieving a No Net Loss conservation outcome (that
is No Net Loss of biodiversity).
586
Ecological Engineering 120 (2018) 585–594
enables us to assess the effectiveness of such techniques in meeting
offset requirements (the definitions and standards used are widely ad-
mitted, mostly arising from the BBOP) and to present the main criteria
that should be informed in order to ensure a suitable utilization of
‘restoration’. In this review, compliance with the equivalence criterion
appears to be a crucial element for using ‘restoration’ solutions as off-
sets. Thus we clarify the different levels of equivalence that should be
met when designing offsets relying on ‘restoration’ techniques. This
approach tend to better inform the numerous trade-offs practitioners
and policy-makers face when suggesting or monitoring current offset
practice.
2. The relevance of ‘restoration’ techniques for offsetting
We performed a brief literature review on existing ‘restoration’
techniques (defined in broad terms) available in the marine realm
(including marine coastal ecosystems) using the Web of Science (WoS)
(the search criteria is listed in Appendix 1 and topics addressed in ar-
ticles are in Appendix 2). In this study, we decided to analyze techni-
ques strictly related to marine systems. The following systems were not
included: mangroves (since these are interface ecosystems between
fresh and salt water), estuaries and coastal wetlands (since these are
transitional water ecosystems and have been already widely discussed).
Among techniques used for pollution removal, only marine sediment
remediation was analyzed (eutrophication was out of the scope since
mainly related to controlling telluric inputs: e.g. wastewater treatment
plants and wetlands). As very few publications were available on deep-
sea ecosystems, they were not covered. As regards artificial reefs, we
examined these in the related category when they were used as a
substrate for restoring specific ecosystems or to replace the ecosystem
function of providing a habitat for particular species; otherwise, they
have not been addressed.
Only 155 articles were found to be relevant to the subject of our
study, representing 23% of the total results. These were then classified
according to a typology based on the environmental issue targeted by
the solution: coral reefs, seagrass meadows, invertebrates, artificial
habitats, ‘green’ marine construction, eutrophication, marine sediment
remediation, mangroves, macroalgae beds, deep-sea ecosystems, or
ichthyofaunal Fig. 1.
The results of the literature review (monitoring parameters, dura-
tion of monitoring and the effectiveness of the technique) are displayed
in Appendix 3 but Table 1 presents the principle of the technique and
the references. The objective was to get a representative (but not ex-
haustive) overview of current available techniques applicable to marine
ecosystems and their relative degree of implementation.
Although extensive literature on mitigation requirements is avail-
able for wetlands (Ambrose, 2010; Ambrose et al., 2007; Gardiner,
2002), marine mitigation suffers from a lack of guidelines. Here we
propose to assess the relevance of these ‘restoration’ techniques as offset
solutions, comparing socio-economic, ecological, and technological
parameters related to restoration decision (Van Dover et al., 2014) to
the issues commonly discussed in scientific literature on designing
offset measures (Bull et al., 2013; Maron et al., 2012; Quétier and
Lavorel, 2011) as well as to the recommendations of the BBOP.4 Of the
criteria used to define the feasibility of an offsetting technique, we
analyzed the following four, which we considered the most important:
• the standards used to define the ecological effectiveness of a ‘re-
storation’ technique, which enable offset gains to be assessed
• cause(s) of the failure of a technique, which leads to uncertain
the
outcomes
4
In the framework of biodiversity No Net Loss as defined by the BBOP (2012), eco-
logical equivalence can be assessed in terms of species diversity, functional diversity and
composition, ecological integrity or condition, landscape context, and ecosystem services.
C. Jacob et al.
• the costs,which affect a technique’s economic feasibility
• the resilience of the ecosystem, which influences the choice of the
relevant ‘restoration’ technique and the time of monitoring
2.1. Ecological effectiveness
According to a primer produced by the Society of Ecological
Restoration in 2004, nine attributes of measuring restoration success
are given.5 More specifically, Ruiz-Jaen and Mitchell Aide (2005) link
the restoration success of terrestrial ecosystems to diversity, vegetation
structure and ecological processes. For estuarine, coastal and marine
ecosystems, Elliott et al. (2007) link restoration success to physico-
chemical attributes and ecological structure and functioning.
In the literature reviewed in our study, the definition of restoration
objectives, enabling the effectiveness of a technique to be assessed, is
not clearly stated. Indeed, the poor definition of restoration goals as
well as the criteria used to verify their attainment is described as a
common limitation by scientists working on the subject (Borja et al.,
2010; Simenstad et al., 2006; Wortley et al., 2013). This includes both
structural species6 and functional aspects (Borja et al., 2010). Our lit-
erature review revealed that the most reported parameter for describing
restoration success is survival rate, a conclusion also drawn by
Bayraktarov et al. (2016) in their study on marine coastal restoration.
Higher survival rates following restoration were observed for coral reefs
(Kolinski and Helton, 2006; Rinkevich, 2014), seagrass (Bastyan and
Cambridge, 2008; Lee and Park, 2008) and macroalgae (Falace et al.,
2006), but survival is highly dependent on the species studied and is
strongly influenced by the transplantation technique. Growth rate was
also often mentioned as a parameter for assessing restoration success,
but species richness, species abundance and cover were seldom used.
Equally, the provision of ecosystem functions and services was hardly
ever addressed. Thus, a better definition of performance standards is
needed that relies not only on ‘item-based success’ but on an ecosys-
tem’s functions and services to allow a more complete assessment of
5
The SER Primer states that a restored ecosystem should have the following attributes:
(1) similar diversity and community structure compared to reference sites; (2) presence of
indigenous species; (3) presence of functional groups necessary for long-term stability; (4)
capacity of the physical environment to sustain reproducing populations; (5) normal
functioning; (6) integration with the landscape; (7) elimination of potential threats; (8)
resilience to natural disturbances; and (9) self-sustainability (Ruiz-Jaen and Mitchell
Aide, 2005).
6
Structural species are species that create or provide the physical structure of the
environment (Huston and Huston, 1994), they can be considered as a type of ecosystem
engineers. Structural or structuring can be equally used.
587
Ecological Engineering 120 (2018) 585–594
Fig. 1. WoS publications related to marine ecosystem
restoration, categorized by the targeted issue.
offset gains (see Section 3.1).
2.2. Causes of failure
The projects described in the reviewed articles often faced similar
problems (e.g. failure of attachment to structures, predation, storms,
pollution, etc.). Although some of them are unpredictable and outside
of the control of the scientists or managers, others could have been
prevented.
This is the case of poor site selection which was often mentioned as
a reason for project failure (see the guidelines produced by the US
National Oceanic and Atmospheric Administration for seagrass re-
storation, Fonseca et al., 2002). This encompasses different issues, such
as insufficient diagnosis pre-restoration to determine the environmental
conditions of a site (e.g. sedimentation, current), its connectivity to
existing highly functional zones, and other anthropic pressures present
(e.g. water pollution, turbidity, illegal trawling). Preliminary tests are
infrequently carried out to verify the tolerance of a species to trans-
plantation and the conditions of the site to be restored. Ensuring that
conditions are favorable on a restoration site before undertaking any
measures is essential to reduce uncertainty in its success.
Moreover, an observation made within the framework of EIAs car-
ried out in the Australia’s Great Barrier Reef but that could easily
transferred to other contexts, is the lack of independent peer review
(Bos et al., 2014; Sheaves et al., 2016), potentially increasing the risk of
failure. Indeed, peer review ensures that studies align with scientific
requirements encompassing details regarding their goal and hypothesis
formulation, survey design, data quality and statistical power (Legg and
Nagy, 2006).
2.3. Costs
As costs were rarely given in the reviewed articles, we were not able
to conduct any cost analyses. However, it is known that the restoration
of marine ecosystems is more expensive than for other types of eco-
systems (Bayraktarov et al., 2016), representing costs 10–400 times
higher than the maximum cost documented for the restoration of ter-
restrial ecosystems (see Groot et al., 2013). According to Bayraktarov
et al. (2016), for all marine ecosystems (coral, seagrass, mangroves,
saltmarshes and oyster reefs) the median cost has been estimated at
around US$80,000 ha−1 and the average cost at around US
$1,600,000 ha−1. They have also demonstrated that the survival of
restored organisms is not related to cost, but is rather linked to the
dynamic nature of marine ecosystems and to the nature of the
C. Jacob et al. Ecological Engineering 120 (2018) 585–594

Table 1
Description of the marine ecosystem ‘restoration’ techniques currently available in the literature.

Technique Principle References

Coral reefs
Transplantation Most common restoration technique, involving the transplantation of coral Abelson (2006), Gomez et al. (2011), Kolinski and Helton
colonies, juveniles or fragments to a natural or artificial substrate. Usually, (2006), Omori and Iwao (2014) and Tortolero-Langarica
epoxy is used to attach the coral to natural or artificial (e.g. concrete, steel rods) et al. (2014)
hard substrates.
Transplantation of nursery- Breeding of coral larvae or fragments before transplantation. Larvae, ova and Amar and Rinkevich (2007), Mbije et al. (2013), Rinkevich
raised corals embryos are directly collected with a funnel net or by the installation of artificial (2014) and Schopmeyer et al. (2012)
substrate near the colonies. Fragments are removed from natural colonies or
retrieved from the seafloor. Nurseries can be raised on artificial substrates such
as concrete, slate or nets.
Electro-stimulation Mineral accretion by electrolysis to improve the growth of transplanted juveniles Sabater and Yap (2002) and Schuhmacher et al. (2002)
or the colonization by larvae. A low continuous current encourages the deposit
of minerals present in seawater.
Artificial reefs Increasing the available hard substrate for natural colonization of coral larvae Al-Horani and Khalaf (2013) and Thanner et al. (2006)
(must be located close to a healthy and productive coral reef).

Seagrass meadows
Transplantation Removing the rhizome or entire plant from a seagrass donor and transplanting it Bastyan and Cambridge (2008), Bell et al. (2008), Lee and
to a natural or artificial substrate (e.g. cement base or grid) by attaching it with Park (2008), Paling et al. (2001) and Zarranz et al. (2010)
various methods (e.g. epoxy glue, props, hooks, staples, elastic bands or shells)
manually or using a machine. Posidonia oceanica (Neptune grass), Posidonia
australis, Posidonia coriacea, Amphibolis griffithi, Posidonia sinuosa, Zostera marina
(eelgrass), Halodule wrightii (shoalgrass), Thalassia testudinum (turtlegrass),
Syringodium filiforme (manatee grass)
Sowing Seeding using seeds from a donor seagrass meadow (harvested from the seafloor Bell et al. (2008), Marion and Orth (2010) and Zarranz et al.
by divers or by an underwater mower). These can be seeded directly on the site (2010)
manually or mechanically, diffused (through ‘buoys’), or cultivated in a
laboratory until germination and then planting the young seedlings directly in
the sediment on webs or on a prop. Cymodocea nodosa (slender seagrass), Z.
marina, T. testudinum.
Electro-stimulation Mineral accretion by electrolysis to improve the growth of transplanted shoots. Vaccarella and Goreau (2012)
A low continuous current encourages the deposit of minerals present in
seawater.
Micro-propagation Cloning plants axenically from terminal buds to produce a large number of Ailstock and Shafer (2006)
clonal offspring. Ruppia maritima (beaked tasselweed), H. wrihhtii, T. testudinum,
S. filiforme

Macroalgae beds
Transplantation Most common restoration technique. It involves attaching adult or juvenile thalli Carney et al. (2005), Falace et al. (2006) and Perkol-Finkel
using epoxy glue, polyurethane foam or hooks on a natural or artificial substrate. et al. (2012)
Transplantation can be undertaken on coastal structures when populations are
too remote for natural colonization (e.g. Cystoseira barbata, Cystoseira
amentacea).
Sowing Sowing of sori directly after harvesting them or the outplanting of spores or Carney et al. (2005) and Terawaki et al. (2003)
microscopic sporophytes grown in laboratory cultures on a substrate. It is also
possible to induce the fertility of male or female gametophytes to produce
microscopic sporophytes.
Artificial reef Increasing the available hard substrate for natural macroalgae colonization. Reed et al. (2006)

Ichthyofauna
Postlarval Capture and Culture Restocking ecosystems to boost biodiversity and fish density for fishing Gerard et al. (2008)
(PCC) purposes.
Artificial reef Creating an artificial reef to replace some of the degraded functions (e.g. as a Brickhill et al. (2005), Jordan et al. (2005), Pastor (2008)
habitat or feeding zone) or ecosystem services (e.g. fish provision) or to increase and Seaman (2007)
connectivity (e.g. to improve recruitment of species with limited dispersal).
Artificial algae Imitating the size, shape and density of natural macroalgae (e.g. Cystoseira spp. Fernández et al. (2009)
or Sargassum spp.). Artificial algae can be made out of polypropylene,
polyethylene or nylon and attached to an artificial reef with a steel and epoxy
anchor to replace the habitat function of macroalgae in zones where
environmental conditions prevent natural recovery.

Invertebrates: bivalves (oyster, scallop, abalone, mussel, giant clam), crustaceans (lobster), sea fans
Transplantation Transplanting adults from another site. It is used for some bivalve mollusks Katsanevakis (2009) and Linares et al. (2008)
(Pinna nobilis, noble pen shell and Tridacna spp., giant clam).
Planting hatchery-raised Releasing cultured larvae to rebuild stocks. Arnold (2008), Dinnel et al. (2009), Gerard et al. (2008),
juveniles Hansen and Gosselin (2013) and Tettelbach et al. (2013)
Artificial reef Creating an artificial reef to replace some of the degraded functions (e.g. as a Behringer and Butler (2006) and Chapman (2012)
habitat or feeding zone) or ecosystem services (e.g. crustacean provision) or to
increase connectivity (e.g. to improve recruitment of species with limited
dispersal).

‘Green’ marine construction

Modification of concrete surface: This facilitates species colonization by targeting ‘ecosystem engineers’, which influence other species by altering environmental conditions and by
providing habitats and other resources (Jones et al., 1994; Jones et al., 1997 In: Harley, 2006) (e.g. barnacles in intertidal zones).
Surface texture Modifying the texture of a construction by methods such as making grooves in Coombes et al. (2015) and Omori and Fujiwara (2004)
the surface of the concrete or by including shells, fiberglass, natural fibers or
(continued on next page)

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C. Jacob et al. Ecological Engineering 120 (2018) 585–594

Table 1 (continued)

Technique Principle References

porous granulates in the cement, or by attaching small structures to artificial

constructions to improve colonization.
Artificial cavities Creation of cavities of different sizes at different heights in a dike. These cavities Browne and Chapman (2014), Chapman and Blockley
can be integrated in the design of a dike or added to pre-existing dikes. (2009) and Firth et al. (2014)
Creation of specific structures: This technique exists mainly in pilot projects (e.g. micro-habitats to restore habitat or nursery functions and semi-floating dikes to minimize physical
footprint).

Marine sediment remediation

Bioaugmentation
(ex situ and in situ)
Electro-oxidation (ex situ)
Electro-biostimulation (ex situ)
Addition of exogenous bacteria or inputs that stimulate microbial activity by Haines et al. (2003) and Prince (1997)
providing oxygen, nutrients or chemical products (e.g. gaseous hydrogen,
acetate, lactate or alcohol). This technique can be used to degrade organic or
inorganic oxidized pollutants or to reduce accumulated sediments in ports (bio-
dredging). It does not require sediment excavation.
Using electro-osmosis to cause pollutants to migrate and to precipitate through a Virkutyte et al. (2002)
membrane via the action of an electric field generated by electrodes (pollutant
recovery is required after migration as the pollutants are not degraded).
Using an electrical current to stimulate microbial activity, allowing organic Li and Yu (2015) and Lu et al. (2014)
pollutants to be degraded by bacteria more quickly than in natural conditions.
Electrodes placed in contaminated sediment act as electron donors to cause
degradation through a reduction reaction (for chlorinated chemical products) or
act as electron acceptors to cause degradation through oxidation reaction (for
hydrocarbons). It does not require sediment excavation.

organisms themselves. As Van Dover et al. (2014) observe concerning
parameters contributing to decisions to undertake ecological restora-
tion, the control of restoration costs informed by previous projects is
crucial. The determination of the socio-economic “outcomes” of such
restorations could also help justify the costs of intervention (Aronson
et al., 2010; Cooper et al., 2013; Groot et al., 2013).
2.4. Resilience of marine ecosystems
To better inform decisions concerning opportunities to implement a
‘restoration’ technique, it is useful to investigate the data available on
the natural resilience of marine ecosystems.
2.4.1. Relatively short recovery time of marine ecosystems
In their study on the rapid recovery of damaged ecosystems, Jones
and Schmitz (2009) compare the average recovery times of different
types of ecosystem after both experimental and natural perturbations
and both passive and active recovery projects.7 The study shows that
marine benthic ecosystems have the shortest recovery time (less than 5
years) of all the studied ecosystems (freshwater, brackish, forest, ter-
restrial), and marine pelagic ecosystems have a recovery time similar to
freshwater ecosystems (between 10 and 15 years); the types of per-
turbation in this study were limited to overfishing, eutrophication, in-
vasive species, hurricanes, oil spills, trawling and power plants. A study
by Borja et al. (2010) is in line with this finding, but gives a qualifi-
cation regarding full recovery: “Although in some cases recovery can
take less than 5 years, the full recovery of many coastal marine and
estuarine ecosystems can take a minimum of 15–25 years from over a
century of degradation and attainment of the original biotic composi-
tion and diversity and complete functioning may lag far beyond that.”
Indeed, as marine ecosystems are highly connected communities with
large numbers of opportunist and generalist feeders, they tend to have
greater structural robustness (Dunne et al., 2004). Yet differences re-
main between high-energy regime systems and more stable areas
(Collie et al., 2000): highly variable ecosystems such as estuaries are
more resilient (Elliott and Quintino, 2007).
2.4.2. Active and passive restoration measures
Most of the restoration literature we reviewed concerns ecosystem
engineers: species that substantially modify the physical structure of the
abiotic or biotic materials forming the habitat, and thus directly or
indirectly change the availability of resources to other species (a type of
keystone species), increasing the structural complexity of the habitat,
the local biomass, and the local biodiversity (Coleman and Williams,
2002). They are mostly located within the subtidal zone. This can be
explained by the fact that current feedback on coastal, estuarine and
marine restoration has involved small-scale schemes (Perrow and Davy,
2002) in which keystone species and ecosystem engineers (such as kelp,
coral and biogenic reefs) play a central role in effecting restoration
(Fonseca et al., 2002; Hawkins, 2004). Usually “structuring species, in
sufficient quantities, allow [an ecosystem] to regain its overall nature
and thus restore [its] ecological functioning” (Elliott et al., 2007). This
analysis corroborates the review of French EIAs related to marine de-
velopment projects, in which offset measures were found only for
keystone species (Jacob et al., 2016a). So for coastal marine ecosys-
tems, active restoration should continue to be encouraged where eco-
system engineers are present, but measures relating to passive recovery
could also be proposed to complement these in order to ensure optimal
environmental conditions and the absence of anthropic pressures
(Duarte et al., 2013).
In contrast, as firstly stated by Hawkins et al. (1999) and empha-
sized by Borja et al. (2010), in an open marine system, the best ap-
proach would be to stop the cause of the impact and allow recovery. So
for offshore ecosystems, passive recovery may be the most suitable.
Even in the absence of disturbance, as mentioned by Elliott et al.
(2007), the “gradual changing of conditions (e.g. nutrient loading, cli-
mate change and habitat fragmentation) may exceed threshold levels,
resulting in an abrupt system response (Kaiser and Attrill, 2011; The
Resilience Alliance, 2002)”. Indeed, marine ecosystems display various
degrees of hysteresis8 and can change to the point that they no longer
converge at the original assemblage (Hughes et al., 2005). Although
this applies to both coastal marine and open water ecosystems (through
the “treatment” stage as identified in Westwood et al., 2014), in the
absence of active restoration solutions for open marine systems, it is
crucial to ensure that changes in environmental parameters are avoided
or reduced to maintain these ecosystems’ resilience. Special attention
should thus be paid to physico-chemical parameters, overexploitation
of biota, and habitat (Elliott et al., 2007). This could be undertaken

7
Passive recovery describes the recovery of an ecosystem once stressors have been
8
removed and according to its resilience, whereas active recovery is based on human- Hysteresis is the difference between the trajectories observed during decline and
mediated actions to enhance recovery (Elliott et al., 2007). recovery.

589
C. Jacob et al.
through the use of passive restoration measures limiting certain impacts
of activities such as fisheries, shipping, aggregate extractions, etc.
2.4.3. Time of monitoring
Monitoring duration ranged from 3 months to 5 years, but was ty-
pically less than 1 year, as observed in the study by Bayraktarov et al.
(2016), in which 47% of the studied projects dealing with the re-
storation of coastal ecosystems were assessed for less than 1 year. They
also noted that 11% of the studied projects did not provide information
on project duration, which we also observed in our literature review.
This time frame does not extend to the full duration of the operation
phase of the development project being offset, but rather is limited only
to the construction phase (see Jacob et al., 2016a). As it stands, the
duration of monitoring time is currently far below the time required (as
described by Borja et al., 2010) to determine whether a targeted en-
vironmental feature has recovered. A 5-year monitoring period should
be a prerequisite, which could then be adapted to a particular ecosys-
tem’s recovery time.
Informing these four parameters (effectiveness, causes of failure,
costs and resilience) ensures that adapted responses in terms of offset
design are provided according to the type of marine ecosystem at stake.
3. How to ensure biodiversity gains that respect the equivalency
principle?
3.1. A more relevant approach for defining equivalence in marine offsetting
Equivalence can be defined in different ways. Quétier and Lavorel
(2011) explore the target components of biodiversity and ecosystems
that can be used as metrics to measure losses and gains. Indeed, as
mentioned by Jacob et al. (2016b), “The principle of offsetting ac-
cording to the goal of No Net Loss can be applied differently depending
on what is at stake – habitat/species, ecosystem functions or ecosystem
services (Calvet et al., 2015; Levrel et al., 2012). Currently, most offset
practices focus on habitats and species, but are increasingly integrating
a functional approach.” Social and cultural aspects of ecosystems are
seldom considered in biodiversity offset implementation constituting a
potential source of injustice and inequalities (Apostolopoulou and
Adams, 2015; Gobert, 2010). One way to connect human activities and
amenities to degraded or restored ecosystems could be the integration
of the concept of ecosystem services within biodiversity offset (Jax
et al., 2013; Baker et al., 2013 In: Jacob et al., 2016b). This aims at
strengthening the consideration of social equity and result in better
acceptance of projects and proposed offsets.
In our literature review, we observed that restoration objectives can
differ greatly according to the issue targeted and the technique used.
Some techniques were able to restore a functional ecosystem similar to
the damaged ecosystem, but others were only able to restore certain
functions or services provided by the ecosystem (see reclamation con-
cept). For instance, some species have very low survival rates when
transplanted such as Posidonia oceanica, and thus they cannot be re-
stored then degraded, thus offsetting currently draws upon surrogate
ecosystems delivering similar ecosystem functions or services. Using the
example of the destruction of a Posidonia oceanica seagrass meadow by
the construction of port infrastructure, we classify the different practice
that can be currently encountered in EIAs according to the levels of
compliance with the equivalence criteria (Table 2).
Thus ‘restoration’ techniques can reach different levels of com-
pliance concerning the equivalence criteria from a systemic approach
relying on biodiversity dynamics, ecological interactions and processes
to a services’ approach based on the provision of services by species and
ecosystems (Fig. 2).
Systemic and functional approaches should be favored as biodi-
versity components are the basis of ecosystem services’ supply – in fact,
current regulations require a No Net Loss of biodiversity. As discussed
by Bas et al. (2016), in their paper on the development of an hybrid
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Ecological Engineering 120 (2018) 585–594
methodology assessing losses and gains within the framework of marine
biodiversity offset, two kinds of scaling methods can be differentiated,
the ones using a single-metric such as Habitat Equivalency Analysis
(HEA), created by the US National Oceanic and Atmospheric Admin-
istration (NOAA) in 1995 (Dunford et al., 2004) and the ones using a
multi-criteria analysis, such as the Uniform Mitigation Assessment Method
(UMAM), a Floridian type of Wetland Rapid Assessment Method (RAM)
that appeared in the United States in accordance with the Clean Water
Act (Fennessy et al., 2007). While HEA is based on an indicator that can
be one species or a group of species, representative of the state of im-
pacted habitats, UMAM relies upon 37 indicators divided into three
groups corresponding to “Location and Landscape Support”, “Water
Environment” and “Community Structure”, thus assessing both struc-
ture and functions.
The services’ approach should be used in complement to and not in
place of current systemic and functional approaches as mentioned by
Jacob et al. (2016b) in their paper investigating the inclusion of an
ecosystem services’ approach in biodiversity offsetting. They argue that
“integrating ES in the current approaches in a complementary way that
respects their different objectives and rationales is crucial for better
biodiversity outcomes. A solely ES-based approach cannot replace
current approaches based on habitat/species/function assessment, an
observation also made by the BBOP (2012)”. They also proposed a
conceptual framework where the measures that are suggested to offset
biodiversity losses “should equally be chosen to minimize residual
losses of ecosystem services” besides achieving ecological performance
standards. Then, different types of complementary offsets can be de-
veloped to address these residual losses of ecosystem services: measures
based on ecological restoration or other actions that restore nature,
human-based measures substituting natural capital with human-made
capital or financial measures compensating populations that have lost
ecosystem services. Techniques targeting ecosystem services can thus
be used to complement the ones targeting habitats/species/functions in
order to reach equivalence in terms of ecosystem services, if not at-
tained by ordinary biodiversity offsets. For instance, oyster reef im-
plementation can provide several ecosystem services (Grabowski et al.,
2007) such as water filtration and concentration of pseudofeces. As the
only hard substrate in a predominately soft-sediment environment
(Lenihan and Peterson, 1998; Lenihan, 1999), they can provide habitats
for epibenthic invertebrates as well as stabilize the adjacent habitats
and shoreline.
Given the limitations described above of attaining environmental
equivalency in marine ecosystems, other types of offsets are currently
implemented for these ecosystems: out-of-kind offsets, preservation
measures, passive restoration measures and enhancement.
3.2. Other types of offset measures
3.2.1. Out-of-kind offsets
When the biodiversity conserved through the offset differs in kind
from the biodiversity impacted by the project, this is called out-of-kind
offset (BBOP, 2012). As observed by Bull et al. (2013), “The fact that
biodiversity is not fungible calls into question the use of out-of-kind
offsets (Godden and Vernon, 2003; Salzman and Ruhl, 2000). The au-
thors “see a compelling argument for out-of-kind trades”when “trading
up is possible; i.e. trading losses in habitat of low conservation sig-
nificance for gains in threatened habitats (Quétier and Lavorel, 2011)”,
but this must be justified through a consensus on conservation prio-
rities. This is seldom clarified in the selection of out-of-kind offset
measures, which are generally required to be adequate in nature and
scale to offset the impact (BBOP, 2012). For example, in California,
some impacts of development projects on marine ecosystems were
offset by the restoration of coastal wetlands (see the San Onofre Nuclear
Generating Station or the Port of Los Angeles) since this was identified
as a priority in a State where 90% of wetlands of high conservation
significance have disappeared within a century (USFWS).
C. Jacob et al.
Table 2
Different ‘restoration’ solutions proposed for the destruction of a P. oceanica meadow.
Type of approach Technique used
Systematic approach Restoration of a functional P. oceanica seagrass meadow through
transplantation
Functional approach Restoration of the ecological function as a habitat for fish through
the implementation of artificial reefs
Services approach Restoration of carbon storage (regulation service) through the
construction of ‘zero carbon’ buildings in the port
Implementation of artificial reefs (provisioning service – fish)
Restoration of wave attenuation (regulation service) through the
implementation of a swell attenuation system
The most striking example in the marine realm is the replacement of
soft substrate by hard substrate. The creation of new artificial habitats
improve overall biodiversity, but the restored communities are often
different than those impacted. Emu Ltd. (2004) considers that artificial
reef implementation is habitat enhancement, whereas Elliott et al.
(2007) argue that this “implies a quality judgement by presuming that a
three-dimensional reef structure is preferable to the two-dimensional
seabed previously in the area”. According to these authors, artificial
reefs should be regarded as the creation of a new habitat, augmenting
the biodiversity of an area, rather than a replacement of a lost habitat.
Debate continues regarding whether or not this represents an en-
hancement of the overall system. We stress out that this could be
considered as a good example of an offset for the provisioning service of
fisheries. In an example borrowed from Levrel et al. (2012) in Florida
where artificial reefs were implemented to limit social conflicts be-
tween divers and fishermen, Jacob et al. (2016b) highlight that boulder
reefs (a type of artificial reefs) “favor an abundance of big fish (pro-
viding cultural services), but do not compensate for the ecological im-
pacts of projects or accidents (for instance, by providing regulation
services such as playing the role of a nursery)”. This illustrates the case
where the ecosystem services’ approach is used without ensuring a No
Net Loss of biodiversity in the first place but providing surrogate eco-
systems delivering ecosystem services falling into the “Compensation
packages for local stakeholders” category. Thus, if artificial reefs are
considered as a mean to enhance ecosystems’ value (See 3.2.4), gains
should be appropriately demonstrated.
3.2.2. Preservation measures
In the context of marine ecosystems, the temptation is great to
propose the implementation of preservation measures as offsets. This is
particularly true since, as reported by Bayraktarov et al. (2016), “The
upper range of total costs reported for marine coastal restorations … are
up to 8 times higher than the maximum costs estimated by conservation
organizations for acquisition and management of terrestrial protected
areas of 10,000–50,000 US$ ha−1 (2012) Armsworth (2014).” This is
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Ecological Engineering 120 (2018) 585–594
Examples of performance criteria (indicating gain)
Survival rate, leaves’ length, density, cover and associated species equivalent to the
destroyed seagrass
Development of physical properties of a habitat, organic matter production, trophic
relationships equivalent to habitat function of the destroyed seagrass
Avoided CO2 production of the new buildings equivalent to carbon storage of the
destroyed meadow
Exploited fish biomass equivalent to that provided by the destroyed meadow
Attenuation equivalent to that provided by the destroyed meadow
an important point, even if it would have been more meaningful to
compare the costs of marine restoration with costs related to Marine
Protected Areas.
In the case of preservation, the concept of additionality is crucial;
this means that offsets should deliver conservation gains over and
above planned or predicted conservation measures taken by other
parties (BBOP, 2012). Otherwise, it can lead to the financing of mea-
sures already covered by commitments made in the framework of other
environmental policies (Maron et al., 2015).
3.2.3. Passive restoration measures
These measures reduce other anthropic pressures jeopardizing the
survival of species or the success of restoration projects. For instance, as
mentioned by Orth et al. (2006), seagrass meadows are threatened by
sediment and nutrient runoff, physical runoff, physical disturbance,
invasive species, disease, commercial fishing practices, aquaculture,
overgrazing, algal blooms and global warming. Implementation of
ecological moorings, eradication of invasive species and creation of no-
trawling zones by introduction of anti-trawling reefs can also be sug-
gested. Nevertheless, demonstration of gains should be made explicit as
displayed in Bas et al. (2016) in the case of offset sizing related to the
impact of the creation of a no-trawling zone through anti-trawling reefs
on Posidonia meadows.
This approach should be favored in particular for offshore ecosys-
tems, where ‘restoration’ techniques are rare, and the focus should be
on the maintenance or improvement of the ecosystem’s resilience (see
2.4) and on reducing the impacts of human activities.
3.2.4. Enhancement
Pollution removal can be regarded as a type of ecosystem en-
hancement through limitation of contaminant discharge, reduction of
nutrient and organic matter enrichment and eutrophication. Marine
sediment remediation (for ex situ experiments, see Virkutyte et al., 2002
on heavy metals and Li and Yu, 2015 on PCB and hydrocarbons) is a
possible alternative for port sites, where issues relative to pollutants are
Fig. 2. Trade-offs between the degrees of equivalence
and the degrees of ecological complexity.
source: Calvet et al. (2015).
C. Jacob et al.
frequent (many marine development projects involve port infra-
structure, where poor sediment quality is often encountered). Before
designing measures aimed at increasing biodiversity, it is crucial to
ensure good environmental quality.
Ecological engineering of coastal structure could be considered as
measures to increase the ecological value of structures providing that
ecological gains are properly assessed. The modification of concrete
surface such as grooved surface increases colonization, cover and spe-
cies richness (Coombes et al., 2015) or the addition of rock pools im-
proves species richness on pre-existing dikes compared to smooth walls
(Browne and Chapman, 2014; Firth et al., 2014).
3.3. Misuse of ‘restoration’ techniques as offsets
The transplantation of species that would otherwise be destroyed by
a development project is often presented as an offset measure, although
strictly speaking this constitutes a reduction measure. Depending on the
success of transplantation and potential temporal loss (the time be-
tween the beginning of the impact and successful restoration), off-
setting may be required. One of the ecological-equivalence scaling
method mentioned earlier, HEA, takes into account the temporal di-
mension: timeline of the injury, the service reduction, the shape of the
recovery curve, the percent services provided by the restored habitat,
and the duration of restored services (Strange et al., 2002). In addition,
as emphasized by Bas et al. (2016), the amount of loss or gain per acre
for a specific year is corrected by a ratio (discounted) to take into ac-
count human and societal preferences for present offset projects rather
than delayed ecological restoration.
Although artificial reefs are often suggested as biodiversity offsets,
they should be regarded as reduction measures in some cases (e.g. by
reducing habitat fragmentation) or as ‘accompanying measures’.9 or
‘community benefits’10; These measures aim at providing compensation
of some kind to the people affected by the negative environmental
impacts of a project and/or to improve its social acceptance
(Kermagoret et al., 2015). In fact, measures based on ecological en-
gineering of coastal structures but where ecological gains cannot be
properly assessed could be considered as such measures.
4. Conclusion
Given the alarming observation made in a review of 55 environ-
mental impact studies related to marine development projects in France
(Jacob et al., 2016a), which found that “only 7% of the proposed
measures had the aim of offsetting predicted degradation”, that these
measures all related to ‘remarkable biodiversity’, and that none were
properly designed (absence of offset-sizing, lack of performance stan-
dards and insufficient monitoring), it is quite urgent to call for a better
use of ‘restoration’ techniques. This means clarifying trade-offs between
the different approaches used to determine the equivalence, especially
in the context where the temptation is great to simplify the current
processes, which are seen as complicated, costly and leading to un-
certain outcomes. Indeed, the gains obtained by the implementation of
‘restoration’ techniques should be carefully assessed to ensure No Net
Loss of biodiversity in priority.
Further studies of ‘restoration’ techniques should be encouraged to
supplement the limited literature on the subject. This can be under-
taken through specific programs associating different stakeholders
drawing upon experiences led on wetlands’ ecosystems benefiting from
9
Examples of accompanying measures are knowledge acquisition, the definition of a
broader conservation strategy, the implementation of a biotope protection order overseen
by national, regional or local governments, etc. They can be defined to improve the ef-
ficacy of or give additional safeguards to the environmental success of offset measures.
They can also target socioeconomic activities (MEDDE, 2013).
10
Community benefits are defined as “some form of additional, positive provisions for
the area and people affected by major development” (Bristow et al., 2012).
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Ecological Engineering 120 (2018) 585–594
extensive feedbacks. For example, the Southern California Coastal
Water Research Project – SCWRP, consists in a broad-based partnership
of 18 state and federal agencies working in concert with scientists, local
governments, environmental organizations, business leaders, and edu-
cators. This project provides innovative ways to develop environmental
monitoring methods, to communicate among scientists, methods de-
velopers and water quality managers. This kind of partnership will also
help defining restoration targets that better align with the priorities of
conservation policies.
Our review found that studies are increasingly being carried out by
environmental consultancy firms, but these results are not always
shared through publications. This has also been observed in the context
of EIAs conducted in the Great Barrier Reef where development projects
“generate a voluminous “gray” literature, with limited distribution
making them difficult to obtain, and short time-frames available for
review limiting scrutiny by the scientific community” (Sheaves et al.,
2015). One way to overcome this limitation would be to encourage
centralized compilation of metadata (Sheaves et al., 2015) and even to
request them through permits issued by regulatory authorities as
mentioned in the case of French EIAs (Jacob et al., 2015, 2016a).
Although knowledge gaps remain, it is possible to improve offset
practice in the marine realm, building on the existing data. It is crucial
to counteract current approaches that justify poorly designed offset
solutions by claiming lack of knowledge.
Acknowledgements
Adeline Bas provided commentary and advice in the preparation of
this manuscript. We gratefully acknowledge the efforts of the anon-
ymous reviewers; these contributed significantly to improving this ar-
ticle. This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the
online version, at http://dx.doi.org/10.1016/j.ecoleng.2017.09.007.
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