Ecological Indicators 129 (2021) 107867

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Review

The key role of zooplankton in ecosystem services: A perspective of

interaction between zooplankton and fish recruitment
Silvia Lomartire a, João C. Marques a, Ana M.M. Gonçalves a, b, *
a
University of Coimbra, MARE-Marine and Environmental Sciences Centre, Department of Life Sciences, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal
b
Department of Biology and CESAM, University of Aveiro, 3810-193 Aveiro, Portugal

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

Keywords: Marine biota is a great source of ecosystem services. Recently, the involvement of marine organisms in
Ecosystem services biotechnological applications has been discovered and become useful for the development of alternative and
Zooplankton healthy food, natural medicine and cosmetics. The most known ecosystem service is the provision of seafood;
Fish stock
however, fishery management has to be implemented in order to avoid fishing exploitation, depletion of the sea
Aquaculture
and assure the recruitment by fish larva. This review put in relation the role of zooplankton in the ecosystem and
Trophic interactions
its importance in fish recruitment. Zooplankton and fish are close connected; indeed, their prey-predator relation
is an important factor for fish recruitment. Understanding the dynamic and trophic relation among different
groups (phytoplankton – zooplankton – fish) and the ecosystem services they give to us, may increase the
awareness of the importance to preserve marine environments. Furthermore, this relation is also important for
fish aquaculture practices, as it is discussed in the present review. Further researches on potential zooplankton
species that may be involved in fish farms may also ameliorate aquaculture services.
To preserve the seas from fish depletion and to assure seafood provision, it is fundamental to have deep
knowledge about the ecological connections in the marine environment and to obtain fishery management
respectful for the environment.

1. Introduction in the food industry (Fradique et al., 2010), but they can also assure
several benefits in different biotechnological applications, such as nu­
Marine ecosystems are among the most populated habitats in the traceutical, pharmaceutical or cosmetic industry, as it happens recently
world; their richness is given by an incredible number of marine or­ with further studies on seaweeds (Lee et al., 2020; Miyashita et al.,
ganisms that provide us ecosystem services. The Millennium Ecosystem 2020) and microalgae (Galasso et al., 2019; Matos, 2019). Among
Assessment defined “ecosystem services” as “the benefits that people benthonic organisms, mussels are also used in different sectors, for
obtain from ecosystems”. Ecosystem services are divided into four cat­ example the anti-inflammatory agent contained in Lyprinol may be
egories: supporting, provisioning, regulating and cultural services extracted from a green-lipped mussel originated from New Zeland
(Millennium Ecosystem Assessment, 2005). (Benkendorff, 2009). Moreover, sponges and coral are also rich in
Ecosystem services are dependent from natural ecosystem functions, bioactive compounds that could be useful for forward studies and
thus it is important to preserve our planet and its habitats. For example, development of new human services (Leal et al., 2013; Munro et al.,
provision of seafood is the most exploited ecosystem service, which is 1999).
result of a combination of primary and secondary production, biogeo­ Ecosystem services offered by marine resources are diverse. For
chemical cycling, food web dynamics, etc (Austen et al., 2011). The example, mangrove ecosystems are important to ensure nursery and
economic part is also encouraging: it has been estimated that marine breeding habitat for many important fish species that can be exploited
ecosystem services are valued at $50 trillion per year (Costanza et al., for aquaculture, providing other important services associated with
2014). habitat functions and protection (Barbier, 2017).
Marine species mostly used for human benefits are principally known Activities related to tourism, religion and culture are also strictly

* Corresponding author at: University of Coimbra, Marine and Environmental Sciences Centre (MARE), Department of Life Sciences, 3000-456 Coimbra, Portugal.
Tel.: +351 239 240 700 (ext. 262-286).
E-mail address: amgoncalves@uc.pt (A.M.M. Gonçalves).

https://doi.org/10.1016/j.ecolind.2021.107867
Received 11 February 2021; Received in revised form 31 May 2021; Accepted 1 June 2021
Available online 5 June 2021
1470-160X/© 2021 Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
S. Lomartire et al. Ecological Indicators 129 (2021) 107867

connected with extraction and harvesting of natural marine resources. (Cavan et al., 2017).
Commercial fishing and marine tourism are both highly dependent on Zooplankton has also a strong effect on biomass stocks of other
ecosystems, but marine tourism has been identified as having lower planktonic groups, in fact zooplankton can alter the concentration of
impact on the environment and higher monetary value (Bryhn et al., prey populations (by consumption) and predator populations (by being
2020). Cultural ecosystems services provided by marine resources are consumed), consequently having effects on fish biomass (Vanni, 2002).
included in different categories: (1) aesthetic experience, which relates The predominant anthropogenic disturbance for fish is the bottom
with the vision of natural beauties; (2) recreation, as it is noticed sea and trawling practice. However, it has also strong impact on the biogeo­
beaches are considered a holiday location where is possible to practice chemical cycling of carbon and nutrient. Dissolved and particulate nu­
different activities such as swimming, snorkelling or diving; (3) inspi­ trients may be transferred from benthic to pelagic systems, favouring the
ration for art and culture, as many artists use the sea as source of occurrence of algal blooms (Pilskaln et al., 1998). This increase of pri­
inspiration; (4) cultural heritage and identity, such as the identification mary productivity could have significant effects for eutrophication of
of local connection or family link (Fletcher et al., 2014). the water column, causing stress for the marine communities, such as
Unfortunately, anthropogenic impact affects our ecosystems, zooplankton (Dounas et al., 2007).
bringing up habitat degradation, pollution, overfishing etc. Due to the Zooplankton species are widely used as live feed for farmed fish. Fish
unsustainable human exploitation of natural resources, ecosystem ser­ feed is one the main expensive cost in aquaculture (Lupatsch et al.,
vices are limited (Gentry et al., 2020). 2001), but the most important as well: quality and quantity of feed
Thus, to avoid the complete depletion of marine environments and to directly affect growth and, indirectly, maturation and mortality in fish
have functional ecosystem services along time, it is necessary to preserve (Wotton, 1990). Therefore, it is possible to alleviate this cost by utilizing
and to adopt sustainable uses of the environment. The Marine Strategy live-feed. Traditional live-feed products are rotifers (e.g., Brachionus
Framework Directive suggests the use of biological indicators to recog­ spp.) and brine shrimp (Artemia spp.), both with non-marine origins,
nize stressed ecosystems, in order to facilitate the process of restoration thus they sometimes need added enrichment before use (Hansen, 2017).
(Hattam et al., 2015). Copepods represent an important alternative live-feed in marine fish
In the following sections, the importance of zooplankton groups and production, as they improve survival, growth and development of fish
their contribution in ecosystem services is mentioned through the larvae (Hansen, 2017). Biochemical profile of copepods and their size
description of zooplankton ecological roles and its impact on fish range make them appropriate feed for fish farm larvae (Hansen, 2017).
recruitment and fishery management. It has been demonstrated that in lakes zooplankton is fundamental as
food for young fish, which represents an important element in human
2. Zooplankton contribution in marine ecosystems and diet (Mavuti, 1990). This is a suitable example of ecosystem service and
aquaculture how the ecological role is related to the ecosystem service.

The term “plankton” was attributed in 1884 by Hensen to indicate 2.1. Main contributions of zooplankton long time series
organisms randomly disposed in the space (Hensen, 1884); further, the
plankton distribution was assumed as uniformly distributed in space Oceans are unpredictable environments and their physical and
(Lussenhop, 1974). Studying the physical structure of lakes, expert chemical conditions are continuously changing. To collect reliable data
limnologists noticed a vertical and horizontal distribution for the about these variables, it is important to follow a long time-series
zooplankton that is appliable on every environment, and Hutchinson in approach and to have replicates of physical, biological and chemical
the 50 s developed different patterns of distribution: clumps, swarms or measurements collected during the years and perform statistical analysis
aggregates (Hutchinson, 1953). Zooplankton is directly connected to (Valdés et al., 2007).
higher trophic levels, thus knowing how its distribution influences the Long-term series is the best way to have reliable information
entire ecosystem and the interactions with other planktonic organisms (Beaugrand et al., 2003; Omori et al., 1994; Perry et al., 2004) about the
(Pinel-Alloul et al., 1988) may be helpful to understand ecological status of an ecosystem, considering the combined effect of anthropo­
models related to other planktonic groups (Pinel-Alloul et al., 1988). genic pressure on biota (Serranito et al., 2016).
Perissinotto and McQuaid (1992) found a connection between diurnal Valdés et al. (2007) showed that long repeated time-series samplings
vertical migration of zooplankton and fish feeding habits. The stomach of zooplankton increase the likelihood to detect changes in the envi­
content of Kreffrichthys anderssoni, local fish of the Prince Edward Ar­ ronment (Valdés et al., 2007). The time-series from 1992 to 2007 in the
chipelago (South Africa), showed the presence of the euphausiid Northern and Western coast of Spain studied the responses of
Euphausia vallentini, Microcalanus pygmaeus and the copepod Rhincalanus zooplankton to environmental conditions, such as temperature, distri­
gigas. Kreffrichthys anderssoni spend the daytime 300–400 m below the bution and water column stratification. Through the years, the seasonal
surface, shifting to the upper 50–100 m at nigh time, when zooplankton cycle of zooplankton populations has been observed to change with
is in surface water (Perissinotto and McQuaid, 1992). It is clear that the temperature (Edwards and Richardson, 2004; Greve et al., 1996).
vertical migration of zooplankton influences fish migration and food Indeed, zooplankton species distribution also have been affected by
availability. global warming (Southward et al., 1995).
Zooplankton presence affects the ecosystem dynamics (Bruce et al., Long time-series study can be utilized in fishery management to
2006). Zooplankton have a position as grazers for algae and bacteria, assess or to predict the presence of fish stocks in relation with the
influencing their community population (Lehman and Sandgren, 1985; presence of zooplankton. Mackas et al. (2013) analysed zooplankton
Sterner, 2009), but they also provide phytoplankton with nitrogen and data between 1990 and 2010. The sampling points are in the Strait of
phosphorous (Hudson et al., 1999; Hudson and Taylor, 1996; Lehman Georgia, sites rich in salmon and herring. The community composition
and Sandgren, 1985; Sterner, 2009; Urabe et al., 1995) having a perfect of zooplankton included abundance of large copepods, euphausiids and
cycle of nutrient recycling. amphipods, and non-crustacean gelatinous predators such as chaeto­
Furthermore, zooplankton have a crucial role in the efficiency of the gnaths, hydromedusae, and siphonophores. From this time-series anal­
Biological Carbon Pump (BCP) that regulates the atmospheric carbon ysis, Mackas et al. (2013) discovered a big fluctuation in zooplankton
dioxide levels (Kwon et al., 2009; Parekh et al., 2006). Cavan et al. biomass during the 20 years: in the very early 1990s and 1999–2002 the
(2017) underline the roles of zooplankton in improving the effectiveness biomass of zooplankton was at the maximum, while minimum biomass
of the BCP through the control of particles export by grazing, by frac­ was showed in 1994–1995 and 2004–2007 with a following recovery of
tioning large and fast sinking particles in slower ones and moving Par­ the average biomass in 2008–2010. In the years 2005 and 2007 the ef­
ticulate Organic Carbon (POC) to depth via diel vertical migration fect of lower zooplankton biomass affected largely an impoverished

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growth and survival of juvenile salmon and herring (Mackas et al., fisheries and tourism (Dong et al., 2010; Purcell, 2012; Richardson et al.,
2013). The abundance of fish stocks is not only dependent on 2009).
zooplankton abundance, but it is also a potential factor. Pelagia noctiluca blooms, usually present in the Eastern Atlantic and
Specific zooplankton species are indicated as bioindicators sensitive the Mediterranean Sea, are very large and they interfere with several
to disturbances within the natural environments. For this reason they marine human activities, such as tourism and fishing (Canepa et al.,
are also called “sentinels of environmental changes and pressures” 2014). This species is one of the most common stinging jellyfish, as also
(Beaugrand et al., 2010; Legendre and Rivkin, 2005; Richardson, 2008). one of the primary cause of fish mortality in fishing farms. Similar cases
The Marine Strategy Framework Directive assumes that zooplankton can of gill disorders and caged fish mortality events have been reported in
identify environmental changes and anthropogenic invasion in the na­ Northern Europe (Rodger et al., 2011).
ture, such as addition of chemicals (Serranito et al., 2016). Since
zooplankton is very sensitive to changes, the response to the disturbance 3. Influence of the zooplankton on fish stocks
will appear in a short-time respect for the higher trophic level. The short
response and their ubiquity make them potential bioindicators for The fishery management processes must be sustainable and ecolog­
different wet areas all over the world (Serranito et al., 2016). A case ical, to avoid the depletion of fish abundance due to overfishing and
study conducted in Toulon Bay in the Mediterranean presents a times- wrong fishery policy.
series approach from 2002 to 2013. The aim of the study was to quan­ It is important to consider the effects of environmental changes and
tify the biomass abundance of copepods and to evaluate the possibility stressors on stock recruitment. To provide future stocks may be useful
to use them as bioindicators for chemicals in the environment. Results combining the use of biological indicators and recruitment models
showed a great abundance of species from fam. Oithonidae was present (Pershing et al., 2005). Zooplankton are used as indicators of environ­
in the bay, and these organisms possess characteristics to be considered mental conditions, which reflect on the ecosystem status and also in the
as bioindicators of anthropogenic pollution present in the Bay (Serranito living component, giving us information about the abundance of pred­
et al., 2016). ators like fish (Sherman et al., 2002). Zooplankton organisms occupy a
crucial position in the food chain, thus they have effects also on fish
2.2. Impacts of gelatinous zooplankton on ecosystem services stocks and fish recruitment (Fig. 1). Variation of the biomass abundance
of zooplankton could trigger a cascade effect that reflect also on the fish
Zooplankton include also gelatinous organisms, which is represented stock.
by the phyla Cnidaria, Ctenophora and Chordata. Jellyfish (Cnidaria)
have positive impacts for the ecosystems services: they are widely used 3.1. Interactions between zooplankton and fish recruitment
in Asian food industry but also in other continents (Graham et al., 2014)
and in pharmaceutical industry. The extraction of collagen is already Commercial fisheries are dependent on fish stocks, which are sup­
used for the production of cosmetic products (Patwa et al., 2015). ported by the bottom of the food chain (Nixon et al., 1986): primary
From the ecological side, gelatinous zooplankton are key species for production assures the carbon production which will provide abundance
particular fish, such as blue fin tuna in Mediterranean (Cardona et al., in zooplankton biomass, the prey-resource for larval stages of fish
2012). Moreover, they also contribute to the nutrient recycling trans­ (Sherman et al., 2002).
ferring nutrients to the benthic organisms through release of faecal The correlation between zooplankton and fish recruitment was
pellets or decomposition of the entire body (Henschke et al., 2016; already discussed in the 80s. Studying the biomass abundance of
Sweetman and Chapman, 2015). Nevertheless, gelatinous zooplankton zooplankton in the North Sea, it appeared to have a huge decline during
are well-known for the formation of dense species gathering called the same period in which the abundance of commercial fish was
“bloom” that could be repetitive during the years and could have con­ diminishing (Reid, 1984). The decline of zooplankton which occurred
sequences for human health, as it happened in South Italy (Salento due to climate change, could be also a suitable explanation for reduction
seacoast) where jellyfish blooms caused skin burnt and the total cost for in stocks, since low food availability may be critical for fishery (Reid,
emergency medical aid was around 400,000€/5 years services (De 1984). Additionally, detailed studies showed that the decrease in stocks
Donno et al., 2014). Consequently, blooms provoke damages in tourism for herring and mackerel was also due to a period of overfishing and a
and economy (Boero, 2013; Kim et al., 2012; Kontogianni and Emma­ consequential impoverished recruitment (Reid, 1984). Pershing et al.
nouilides, 2014). (2005) studied zooplankton community patterns in the Gulf of Maine
Jellyfish and ctenophores (Ctenophora) are both predators for (Atlantic Ocean - east coast of North America) and their relation with the
zooplankton and juvenile fish stage (Boero, 2013; Purcell and Arai, recruitment of determined fish stocks. Researches suggested that
2001). The presence of blooms indicates a fall in the good ecosystem changes in those patterns could influenced on a large-scale the ecosys­
status or anthropogenic pressure due to overfishing and depletion of tems, with consequentially changes on the services they can provide to
predators of gelatinous zooplankton. This can bring up an over­ humans (Pershing et al., 2005). Further investigations identified strong
population of gelatinous zooplankton which will impact drastically the physical changes in the Gulf of Maine that could be stressors for the fish
fish recruitment (Lynam et al., 2004, 2005; Schneider et al., 1998). One stocks.
of the most harmful species is the invasive species Mnemiopsis leidyi Besides, shifts in zooplankton community abundance co-occurred
(Shiganova et al., 2006) which disrupted the Black Sea ecosystem at all with lower fish recruitment abundance. It is not conclusive saying that
trophic levels and affected fisheries. Mnemiopsis leidyi is native to estu­ fish recruitment is only influenced by zooplankton biomass, but among
aries and bays along temperate and subtropical coastal waters of North the varieties of factors, high prey abundance present in the timing of fish
and South America. Since the early 1980s Mnemiopsis leidyi has pene­ spawning will increase the recruitment (Beaugrand et al., 2003; Cush­
trated in new areas such as Black Sea Caspian Sea North and Baltic Sea ing, 1990; Hjort, 1914; Platt et al., 2003).
trough ballast waters contained in commercial ships (Shiganova et al., The Barents Sea is another important area to find commercial fish
2019). stocks. In the mid-1980s and mid-1990s the stock of Mallotus villosus,
The abundance of gelatinous zooplankton can affect also the clog up known as capelin, faced a severe decline in recruitment, due to the
of fishery nets, aquaculture fish mortality, or obstruction of cooling strong predation exert by young herring on capelin larvae. Since capelin
systems of coastal desalination, nuclear and coalfired power plants are a key species of the Barents Sea ecosystem, their decrease influences
(Graham et al., 2014). It happened during blooms of the jellyfish Aurelia the higher trophic level which include cod, harp seals, and guillemots
spp., which provoked clogging cooling water intakes at coastal power (Dalpadado et al., 2002).
plants, causing mortality of aquaculture species, and interfering with Among those years the zooplankton biomass has also showed

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Fig. 1. Illustration of the aquatic food chain.

variations (Skjoldal and Rey, 1989) possible due to differences in hori­ the sustainability fisheries in the Mediterranean Sea (European Com­
zontal transportation and big predation pressures. These variations may mission, 2006). In light of this close relation between zooplankton
be signals for further changes in the ecosystem, as studies demonstrated communities and fish stocks, it is important to apply an approach in
some interactions among cod (Gadus morhua), herring (Clupea harengus), fishery management that recognize and include the knowledge of the
and capelin and between fish and zooplankton (Bogstad and Mehl, 1997; status of the ecosystem.
Dalpadado and Skjoldal, 1996; Gjøsæter, 1998; Ponomarenko and Yar­
agina, 1979). Zooplankton is the major nutriment in capelin and herring 4. Zooplankton as primary fish feed source
diets (Dalpadado et al., 2002), while cod consume krill, amphipods,
shrimps (Pandalus borealis), capelin, herring, polar cod (Boreogadus Fish, like other animals, need a nutritional diet rich in protein con­
saida), redfish (Sebastes spp.), cod, and haddock (Melanogrammus tent for optimizing growth and reproduction (Weatherley and Gill,
aeglefinus) (Bogstad and Mehl, 1997; Ponomarenko and Yaragina, 1983); they cannot synthesize essential amino acids (EAAs) (Ketola,
1979). 1982), thus they need to keep it from external sources (Taipale et al.,
The Barents Sea food chain is characterized by few dominant species, 2018).
they could be resumed such as: diatom → krill → capelin → cod. Shifts For example, eicosapentaenoic acid (EPA) and docosahexaenoic acid
among different trophic levels are the proof of the strength of these (DHA) are required in the juvenile stage of fish – as well as mammals and
biological interactions and how they can easily change the ecosystem birds – for growth, eye and brain tissue development and immunity
status (Dalpadado et al., 2002). function (Tocher, 2010). The omega-3 fatty acids EPA and DHA are
An interesting example of the negative influence of gelatinous synthesized only by few phytoplankton taxa such as dinoflagellates,
zooplankton on fish recruitment is given by the case study conducted in golden algae, diatoms, and cryptomonads (Galloway and Winder, 2015;
the Black Sea. In the time-series observations during 1960–2001 the Taipale et al., 2016), thus fish assimilates those biomolecules through
Black Sea faced significant changes that affected the ecosystem health the consumption of zooplankton which feed on phytoplankton or con­
that appeared weak and less stable (Grishin et al., 2007). verting the precursor of fatty acid, the α-linolenic acid (Taipale et al.,
These conditions favoured the outburst of gelatinous zooplankton 2018).
Mnemiopsis leidyi and jellyfish Aurelia aurita. Since 1988 until the late Zooplankton groups are characterized by different feeding prefer­
1990s, Mnemiopsis leidyi has the control on the zooplankton biomass, its ences and metabolism; cladocerans prefer phytoplankton species
favourite prey, affecting also the stocks of some abundant commercial abundant in EPA (e.g., Daphnia magna) whereas copepods prefer
fish species (Grishin et al., 2007). phytoplankton species rich in DHA, indeed copepods present abundance
The decrease of fish stocks in the early 1990s was mainly affected by of DHA, such as Eudiaptomus (Taipale et al., 2018). DHA is highly pre­
overfishing due to unregulated fisheries, even though the presence of the sent in many aquatic food webs (Strandberg et al., 2015) because of the
invasive non-indigenous species Mnemiopsis leidyi negatively contrib­ great assumption by copepods and the predation of copepods by fish.
uted as food competitor of planktivorous fish (Daskalov, 2003, 2002). A common procedure in fish aquaculture is to add microalgae to
The outburst of gelatinous zooplankton also produces indirect effect on culture system of zooplankton prey for fish larvae (Tamaru et al., 1994).
the ecosystem, leading to the increase in phytoplankton and detritus The most popular microalgae used for feeding zooplankton for aqua­
with a consequential reduced water quality, hypoxia and negative ef­ culture purposes are Nannochloropsis oculate, Tetraselmis suecica, Pavlova
fects on fishes and other organisms (Grishin et al., 2007). lutheri and Isochrysis sp., which are PUFAs-rich and they enrich
In order to avoid further increases in mortality rates for juveniles and zooplankton in DHA (Nichols et al., 1989).
to substantially reduce the number of juveniles by overfishing vessels, Nutritional quality of phytoplankton has a cascade effect along the
the European Union provides the Council Regulation (EC) N. 1967/2006 food chain, influencing through zooplankton all the trophic web (Brett
of 21 December 2006. This regulation determines the minimum landing and Müller-Navarra, 1997; Elser et al., 2000; Müller-Navarra et al.,
sizes of certain marine organisms (Annex III) (European Commission, 2000). Thus, in fishery management it should be mandatory to consider
2006). In this way, the selectivity of fishing gear should correspond as always the trophic relation between phytoplankton, zooplankton and
closely as possible to the minimum landing size established for a certain fish, in order to have an efficient stock and make a better use of fishery
species or group of species caught by that gear. Gears should be adapted resources (Waya et al., 2017).
base on the fishing zone: for example, part of the coastal zone should be
reserved for selective fishing gears used by small-scale fishermen, in
order to protect nursery areas and sensitive habitats and enhance the 4.1. Use of zooplankton in fish farming
social sustainability of Mediterranean fisheries. Management plans may
also include measures to monitor the fishing effort, in order to safeguard Aquaculture is nowadays one of the most exploited sectors around
the world (FAO, 2018) and this phenomenon is co-occurring with

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dramatical decrease of functionality of our ecosystems and habitat (Bhaskaran and Imelda, 2020; Khan et al., 2020).
changes due to anthropogenic exploitation of natural resources, envi­ Live food that is also recommended for aquaculture is Daphnia magna
ronmental pollution and spread of invasive species (Naeem et al., 2012). which can be easily cultured with low-cost expenses. Daphnia magna is
Feed used for aquaculture releases an amount of organic matter, considered a natural source of proteins, vitamins, carbohydrates and
nutrients and suspended solids (Edwards, 2015) which may have lipids (Jorge et al., 2016) and with the 45–70% protein content and
negative impact on the aquaculture but also on the environment, due to 11–27% lipid content (Macedo and Pinto-Coelho, 2001), it represents a
the discharge of nutrients from the aquaculture implants (Naylor et al., nutritional food for fish (Khan et al., 2020). Cladocerans in general have
2000). Nitrogen and phosphorus are often released in high concentra­ the advantage of high reproduction rates, wide temperature tolerance
tion causing eutrophication, oxygen depletion and siltation in the and the ability to regulate the presence of phytoplankton and organic
environment (Burford et al., 2003). To minimize the impacts of nutri­ wastes (Khan et al., 2020) and they meet the nutritional requirement of
ents, several countries are developing Integrated Multi-Trophic Aqua­ fish larvae (Evjemo et al., 2003). Among other species, Brachionus pli­
culture (IMTA) systems, which imply the wastewaters for cultivation of catilis, Brachionus rotundiformis, Pseudodiaptomus annendeli, Pseudo­
macro- and microalgae. In this way, aquaculture wastewater will pro­ diaptomus serricaudatus and Moina sp. have been discovered as the most
vide the right amount of nutrients (ammonia, nitrite, nitrate, dissolved successfully species to cultivate in small and large scale in the mari­
organic nitrogen and phosphate) discharged (Abe et al., 2002; Converti culture hatchery, as they possess high reproductive rate, short genera­
et al., 2006; Soletto et al., 2005). tion time, and the ability to live and grow in crowded culture conditions
Studies demonstrate that it is possible to employ microalgae to (Bhaskaran and Imelda, 2020).
remove nutrients from aquaculture wastewaters (Gao et al., 2016; In Taiwan, the calanoid copepod Pseudodiaptomus annandalei is
Lefebvre et al., 2004). Bioremediation with microalgae is ecological and commonly used as live feed for commercially important species such as
low-cost (Mulbry et al., 2008). The most valid candidates to utilize for grouper larvae (Chen et al., 2006; Lee et al., 2010). This copepod has
aquaculture bioremediation wastewater are Tetraselmis suecica and been cultivated successfully in Taiwan in ponds for several decades at
Dunaliella tertiolecta (Borges et al., 2005; Michels et al., 2014). relatively high densities, in order to have huge disposal of live-feed for
Due to the high market demand, is emerging the need to have the feeding fish larvae (Blanda et al., 2015). Kar et al. (2017) carried out the
highest yields achieved with the least nutrient loading. In semi-intensive cultivation of the species Moina micrura, Scapholeberis kingi and Bra­
fishpond systems, cereals are often replaced by complex fertilizers that chionus calyciflorus; the growth and the reproduction of the three species
increase the natural productivity of fish (Kaushik, 1995; Pechar, 2000; were satisfactory to sustain the mass culture and the supply as live feed
Potužák et al., 2007; Tacon, 1996) without compromising fish flesh fish (Kar et al., 2017). Moreover, zooplankton organisms are often
quality (Dickson et al., 2016). Unfortunately, traditional fish feeds are considered as bioindicators to assess the ecosystem quality of fishponds
often made from fishmeal and oil, and the use of such ingredients is (Marbà et al., 2013) and fishery health (Ejsmont-Karabin, 2012; Ersoy
unsustainable (Welker et al., 2014), thus their use has been reduced in et al., 2019; Pociecha et al., 2018).
the last decade (Tacon and Metian, 2015).
There are many alternative sources available, which are not only 5. Conclusion
comparatively cheaper but are nutritionally enriched. For example,
poultry by-product meal (Bureau et al., 1999; Rawles et al., 2006) may The present review underlines the importance of ecosystem services
be included in the feed of carnivorous fish species such as rainbow trout provided by marine systems. The provision of seafood has crucial
because of its relatively high protein content and lower price compared importance; fish add nutritional value to our daily diet, moreover,
to fishmeal (Shapawi et al., 2007). Therefore, some microalgae (e.g., fishing and aquaculture farms represent economic entrances in different
Spirulina) are rich in amino acids and omega-3 and omega-6 fatty acids, countries. Therefore, fishery management has to consider all the
which make them potential natural replacement of fishmeal, adding ecological roles of marine organisms and their trophic connections, in
nutritional value and benefits to animal health (Hodar et al., 2020). order to preserve the environment but also assure fish stocks. The pre­
Zooplankton organisms can contribute to the growth of fish economi­ sent review discusses about the roles of zooplankton in marine systems,
cally important: they support the nutrient flows between phytoplankton showing how its presence is essential for the good functioning of the
and fish (Howick and Wilhm, 1984), are source of amino acids, protein, ecosystem and fish recruitment. Zooplankton has a pivotal role in the
fatty acids, lipids, enzymes and minerals (Watanabe et al., 1983) and food chain since it allows income of nutrient to the lower level and
they are rich in protein and carbohydrate-poor, while using cereal feed guaranteeing food to the upper levels. Malfunctions of each trophic level
the uptake of protein is lower (Tóth et al., 2020). affect even the predator–prey interaction, leading a severe degradation
The implication of live feed in aquaculture may be risky considering of the ecosystem. To avoid the collapse of the food web, it is important to
mortality probability of specimen, but it is also one of the most profit­ preserve zooplankton as it is fundamental for the existence of ecosystem
able venture (Khan et al., 2020). Moreover, due to their nutritional services, such as fishery and aquaculture.
properties, zooplankton organisms are the feeding source more appre­ Fish preferred feed items are zooplankton organisms, thus a long-
ciated by fish larvae (Rønnestad et al., 1999). Due to their high nutri­ time series monitoring of zooplankton is useful to know not only the
tional value, zooplankton has been exploited in fish farms. Hassan et al. environmental status since zooplankton is also implied as bioindicator,
(2020) evaluated the growth performance of European sea bass but also if the relation predator–prey is efficient to assure fish recruit­
(Dicentrarchus labrax) in relation with replacement of zooplankton ment. In light of this assumption, it is fundamental to develop public
biomass in fish diet. The experiment was carried out replacing policies in fishery management aimed to guarantee sustainable fishing,
zooplankton biomass in commercial fishmeal with five different con­ recruitment of fish and the preservation of the environment as well as
centrations (from 25% to 100%). Results showed that fish feed by 100% the fishing stock.
replaced meal gained higher body length, body weight and showed the
major feed intake (Hassan et al., 2020). Declaration of Competing Interest
The assumption of proteins from live food assures a better growth,
efficient breeding and survival (Mandal et al., 2009). Live food is The authors declare that they have no known competing financial
available in the market but it is quite expensive, thus to reduce the interests or personal relationships that could have appeared to influence
production costs a good alternative is to cultivate zooplankton species at the work reported in this paper.
low-costs venture (Khan et al., 2020). Artemia nauplii has been used for
aquaculture implants for a long time (Agadjihouèdé et al., 2011), but the
high cost of Artemia nauplii cysts led to search for other species

5
S. Lomartire et al. Ecological Indicators 129 (2021) 107867

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04292/2020 – MARE – Marine and Environmental Sciences Centre and pone.0031329.g00510.1371/journal.pone.0031329.g00610.1371/journal.
pone.0031329.g00710.1371/journal.pone.0031329.g00810.1371/journal.
UIDP/50017/2020 + UIDB/50017/2020 (by FCT/MTCES) granted to pone.0031329.g00910.1371/journal.pone.0031329.t00110.1371/journal.
CESAM – Centre for Environmental and Marine Studies. Silvia Lomartire pone.0031329.t00210.1371/journal.pone.0031329.t003.
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