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Communication
Anthropogenic Modifications to Estuaries Facilitate the
Invasion of Non-Native Species
Enrique González-Ortegón1, * and Javier Moreno-Andrés2
Citation: González-Ortegón, E.;
Moreno-Andrés, J. Anthropogenic
Modifications to Estuaries Facilitate
the Invasion of Non-Native Species.
Processes 2021,9, 740. https://
doi.org/10.3390/pr9050740
Academic Editor:
Avelino Núñez-Delgado
Received: 25 March 2021
Accepted: 20 April 2021
Published: 22 April 2021
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4.0/).
1Instituto de Ciencias Marinas de Andalucía, ICMAN-CSIC, Campus Universitario Río San Pedro s/n Pto.
Real, 11519 Cádiz, Spain
2Department of Environmental Technologies, Faculty of Marine and Environmental Sciences,
INMAR—Marine Research Institute, CEIMAR—International Campus of Excellence of the Sea,
University of Cadiz, Campus Universitario de Puerto Real, 11510 Cádiz, Spain; javier.moreno@uca.es
*Correspondence: e.gonzalez.ortegon@csic.es
Abstract:
New observations of non-indigenous species (NIS) in coastal waters, such as the Gulf of
Cadiz (Spain) have increased since 1980 and more or less exponentially in the last five years. Ballast
water has become the most significant pathway for unintentional introductions of NIS into marine
ecosystems. For example, the marine larvae of crustacean decapods that inhabit the water column
could be transported in ballast water. Although elevated concentrations of metals are toxic to many
marine organisms, some of them have evolved effective detoxification, or avoidance mechanisms
making it possible to consider they have a superior ability to withstand exposures to these toxicants.
In this text, we try to reinforce the hypothesis that anthropogenic modifications (such as chemical
alterations and modified environments) benefit NIS with broad environmental tolerances. Taking
these risks into account, a reinforcement of efficient Ballast Water Management Systems to respond
to today’s challenging environmental conditions is discussed.
Keywords: exotic species; planktonic species; larvae; ballast water; gulf of Cadiz
1. Introduction: An Increase in the Arrival of Species
New worldwide observations of non-native invasive species (NIS) have increased
over time, for instance in the Gulf of Cadiz (Spain), GoC, since 1980 and even more in
the last five years [
1
]. Although the rate of new observations cannot be relied upon as
an indicator of introduction rate, due to such factors as: sampling bias, occurrence of
unexpected discoveries, lag time between introduction and discovery, and high variability
in sampling effort, it does indicate increasing pressure on the GoC. The overall number of
published articles about biological invasions appears, however, to be significantly biased
towards new records, the hypothesis of the entrance of NIS in the recipient environment or
the potential impacts in the native biological community; few studies analyzed the activities
which they could determine species traits that affect the success of NIS post-arrival [2].
This communication is more an essay to reinforce the hypothesis that anthropogenic
modifications (such as chemical alterations and modified environments) benefit NIS with
broad environmental tolerances and how these invasive non-natives are often better suited
to be able to survive in modified estuaries in which they are introduced (Figure 1). The
extensive and accidental introduction of organisms in waters is a direct consequence of the
intensity with which humans utilize this via for worldwide commerce [
3
]. Although, it is
not possible to tease apart the invasion of species from 40 years ago due to the lack of records
and long-term series, it is likely that the GoC present continues pressure at least since
1492, when Columbus sailed between this gulf and The Americas by wooden-hulled ships.
From the 1500s, wooden-hulled ships could be colonized by marine organisms, which have
been carried to many parts of the world, resulting in broad geographic distributions [
4
,
5
].
The use of steel as the primary ship-building material in vessels forced to use anti-fouling
Processes 2021,9, 740. https://doi.org/10.3390/pr9050740 https://www.mdpi.com/journal/processes
Processes 2021,9, 740 2 of 9
paints which resulted in significant impacts to marine communities such as TBT or tri-butyl
tin [
6
]. However, other constituents of antifouling paints to prevent the spread of species
on vessel and boat hulls such as copper and zinc, which are common, seems to confer a
competitive advantage on some non-indigenous marine invertebrates [
7
]. For instance,
invasive bryozoans display a high tolerance to the toxic heavy metal copper [
8
] being
a mechanism for the selection of toxicant tolerance in non-native species
(see Section 3).
Finally, although it is likely that the main transport of species could be associated to
merchant vessels, we should take into account the situation for non-merchant vessels. For
instance, recreational vessels are commonly transported to new locations by water without
any attempt at cleaning.
Processes 2021, 9, x FOR PEER REVIEW 3 of 9
Figure 1. Modifications of the habitat by anthropogenic factors (new artificial structures, or modi-
fication of the water quality) increase the chance of the establishment of non-native species.
2. The Suitability of an Estuarine Environment to Host Non-Native Species
The establishment of non-native species could be determined by the recurrence of an
inflow of a species to a location outside its native range, and the biotic and abiotic condi-
tions [17]. The wide variation in abiotic factors inside ballast tanks has also been reported
[18] and although generally the viable number of phytoplankton and zooplankton drops
within the holding time, it is not enough to meet the discharge standards.
Among the different aquatic ecosystems, estuaries show a wide variation in abiotic
factors and most of the big estuaries are navigable and have big ports. These ports, servic-
ing both inland waterways and oceanic shipping, are prone to inoculations of trans-oce-
anic biota and may, occasionally, promote a secondary spread of alien biota upstream. In
this way, if the viable numbers of planktonic species are becoming resistant under variable
abiotic conditions and are potentially discharged in these anthropogenic modified ecosys-
tems, they might be more suitable to develop in these port areas, which are suitable sce-
narios for opportunistic species [9]. For instance, brackish-water macroinvertebrates are
often introduced from ballast water to estuaries or coastal waters [19]. These ecosystems
present a very wide saline gradient that could allow a variety of aquatic species to settle.
In this way, ‘invasiveness’ is perceived to be particularly high in species with a broad
environmental tolerance to both salinity and temperature [20].
For instance, although crustaceans show a specific salinity optimum for survival and
development, which is related to their ecology, larvae of most euryhaline species in estu-
aries or even marine species of fish and macroinvertebrates with a strong estuary depend-
ent juvenile phase, display an optimum that is within a wide range of around 15–25%
[21,22]. The continued transport of planktonic species such as decapod crustacean larvae
in ballast water would ensure the arrival of this group of species in plankton, which might
explain the success of this group of species in coastal waters. Another example is the
prymesiphyte, Prymnesium sp., it is a euryhaline microalga, which is listed on the IOC-
UNESCO Taxonomic Reference List of Harmful Microalgae and has also been linked to
ballast waters in the Bilbao Harbor (North-Spain), which is also an estuary [23]. Toxic
blooms of this microalgae can develop and can cause mortality in shellfish. In fact, such
episodes have been detected in estuarine waters within the North Sea [24].
Thus, euryhaline species or estuarine dependent species may successfully invade a
location outside their native range if they are transported to estuaries with a significant
variability in salinity [22], these ecosystems are prone to invasion by exotic species.
Figure 1.
Modifications of the habitat by anthropogenic factors (new artificial structures, or modifica-
tion of the water quality) increase the chance of the establishment of non-native species.
Among the different ways that NIS species are introduced, ballast water has been
considered one of the main vectors. These introductions might be facilitated due to the
small pre-adult sizes (such as larval stages) and the particular risk of such transfers in
ballast has been denoted for microorganisms [
9
,
10
]. In 2004, The International Maritime Or-
ganization (IMO) published the International Convention for the Control and Management
of Ships’ Ballast Water and Sediments (BWMC) that came into force in the year 2017. The
main measure adopted was to establish a ballast water discharge standard through D-2
regulation, which was designed according to the organism’s size: zooplankton (
≥
50
µ
m)
or phytoplankton species (≥10–<50 µm) and also established three independent bacterial
indicators related to human health. However, some delays have occurred until today,
which are related to the impossibility of implementing a validated Ballast Water Treatment
System in the majority of vessels, among other factors. Despite many efforts being made
to apply BWMC efficiently, the introduction of species via ballast water is still a global
challenge [10].
Most of the exotic aquatic species are invertebrates such as decapod crustaceans, it
is probably the fact that they have a larval phase, which inhabits the water column in
the form of plankton, which ensures their transport in ballast water [
11
]. For instance,
the initial invasion of the European green crab (Carcinus maenas) is thought to have taken
place via the transport of larvae in ballast water [
12
], and they have also probably spread
via anthropogenic intraregional transport [
13
]. The difficulty in identifying these early
developmental stages (e.g., larvae and eggs) correctly is still a crucial issue, since these
pre-adult stages are all common in ballast water [
14
,
15
]. However, recent studies have
overcome this challenge with the use of advanced techniques, such as high throughput
Processes 2021,9, 740 3 of 9
sequencing, allowing the detection of pre-adult stages and other microorganisms [
14
].
For instance, Darling et al. 2020 found considerably higher ratios of arthropods (mainly
copepods) or mollusks in ballast tanks [
15
]. In this way, the transport of larvae over long
distances via ballast water could assure the transport of planktonic species or those species
with a planktonic phase, although the success of their future establishment depends on
biotic and abiotic factors upon arrival in the ecosystem.
This text focuses on how anthropogenic modifications influence the establishment
of plankton (zooplankton (
≥
50
µ
m) or phytoplankton species (10–50
µ
m)) and microor-
ganisms at a location outside their native range (Figure. 1). With regard to anthropogenic
modifications, we are referring to chemical alterations, modified environments or modifica-
tions of hydrological regimes in estuaries [
2
,
16
]. These scenarios will be discussed with
some trends observed at the global scale; however, particular cases will be presented along
the coastline of the south-west of Spain, concretely, the coastline of Cadiz. The coastal
line of the GoC has suffered many anthropogenic transformations, with the presence of
highly modified estuaries, important industrial activity and the presence of aquaculture
and shellfish culture facilities. For instance, the Port of Algeciras, one of the biggest ports
in Europe, is also present in this area.
2. The Suitability of an Estuarine Environment to Host Non-Native Species
The establishment of non-native species could be determined by the recurrence of
an inflow of a species to a location outside its native range, and the biotic and abiotic
conditions [
17
]. The wide variation in abiotic factors inside ballast tanks has also been
reported [
18
] and although generally the viable number of phytoplankton and zooplankton
drops within the holding time, it is not enough to meet the discharge standards.
Among the different aquatic ecosystems, estuaries show a wide variation in abiotic
factors and most of the big estuaries are navigable and have big ports. These ports,
servicing both inland waterways and oceanic shipping, are prone to inoculations of trans-
oceanic biota and may, occasionally, promote a secondary spread of alien biota upstream.
In this way, if the viable numbers of planktonic species are becoming resistant under
variable abiotic conditions and are potentially discharged in these anthropogenic modified
ecosystems, they might be more suitable to develop in these port areas, which are suitable
scenarios for opportunistic species [
9
]. For instance, brackish-water macroinvertebrates are
often introduced from ballast water to estuaries or coastal waters [
19
]. These ecosystems
present a very wide saline gradient that could allow a variety of aquatic species to settle.
In this way, ‘invasiveness’ is perceived to be particularly high in species with a broad
environmental tolerance to both salinity and temperature [20].
For instance, although crustaceans show a specific salinity optimum for survival
and development, which is related to their ecology, larvae of most euryhaline species in
estuaries or even marine species of fish and macroinvertebrates with a strong estuary
dependent juvenile phase, display an optimum that is within a wide range of around
15–25% [
21
,
22
]. The continued transport of planktonic species such as decapod crustacean
larvae in ballast water would ensure the arrival of this group of species in plankton, which
might explain the success of this group of species in coastal waters. Another example
is the prymesiphyte, Prymnesium sp., it is a euryhaline microalga, which is listed on the
IOC-UNESCO Taxonomic Reference List of Harmful Microalgae and has also been linked
to ballast waters in the Bilbao Harbor (North-Spain), which is also an estuary [
23
]. Toxic
blooms of this microalgae can develop and can cause mortality in shellfish. In fact, such
episodes have been detected in estuarine waters within the North Sea [24].
Thus, euryhaline species or estuarine dependent species may successfully invade a
location outside their native range if they are transported to estuaries with a significant
variability in salinity [22], these ecosystems are prone to invasion by exotic species.
Processes 2021,9, 740 4 of 9
3. Pollution-Tolerant Species: Species Likely to Be Invasive
Increasing commercial and recreational use, resulting in significant anthropogenic
impacts on estuaries because of the rapid development of coastal watersheds, threaten the
health of these ecosystems [
25
,
26
]. The excess of nutrient inputs (hypernutrification) in
estuaries is usually linked to human activities within their drainage basin [
27
]. For instance,
in the GoC, when nutrient concentrations of the Guadalquivir estuary were compared with
those from other European estuaries, a nitrogen hypernutrification similar to that of the
Westerschelde estuary (The Netherlands) [
28
] was observed [
29
]. In addition, chemical
stressors such as trace metals, mainly associated with ports, or emerging compounds in
highly modified estuaries, such as the Guadalquivir estuary or the Tinto-Odiel estuarine
zone with major industrial activity [
30
] are a threat to the native populations and allow a
favorable selection of the non-native species transported.
The majority of non-native marine species are transported in ballast water (mainly
as larval stages) or as hull fouling as adult organisms [
10
,
31
], highly contaminated with
metals [
32
]. In fact, certain amounts of heavy metals have been reported in ballast wa-
ter [
33
,
34
]. More specific studies have detected a high metal concentration inside tanks
when compared with the harbor water along the Persian Gulf [
35
]. A particular case is
ballast sediments, which have been shown to be a reservoir of the resting stages of several
invertebrates [
36
] but also an important area where certain amounts of metals accumu-
late [
34
]. Hulls and ballast water tanks are also painted with metal-based biocides leading
to internal corrosion [
37
]. This is significant because NIS seem to acquire greater resistance
to pollutants than native species [
38
] as a result of their stay in the hull. The transportation
process may therefore select for metal tolerance, and the major contaminants in ports and
harbors are metals [39].
The presence and effects of these emerging contaminants in these scenarios need
further research: although some recent studies have detected antibiotic resistance genes
in ballast waters [
40
,
41
], few experimental studies have combined the effects of emerging
compounds or metals, together with environmental variability in terms of salinity and tem-
perature, on survival and larval traits of marine and estuarine macroinvertebrates
[42,43].
In addition, there is a lack of data on the effects of long-term low-dose exposure to phar-
maceuticals and, especially, on the early developmental stages of marine and estuarine
species [
44
,
45
], and even fewer studies take into account that organisms are exposed
to these compounds in a context of environmental variability, such as estuaries [
46
,
47
],
or the mode of action of those compounds which may differ depending on the species
affected [
48
,
49
]. Overall, the contaminants tested did not show any clear effects on the
survival and development of larvae exposed to environmental concentrations [
42
,
43
]. How-
ever, other studies on euryhaline species, which manipulated the access to food combined
with emerging compounds considered sublethal under optimal food conditions, elicited
lethal effects under conditions of food limitation [
50
]. Nevertheless, species that arrive at
estuaries benefit from the rich feeding-grounds provided by these ecosystems, compared
to other aquatic ecosystems. That is, overall, estuaries have a food web based on partic-
ulate and dissolved organic matter which includes bacteria and large mesozooplankton
populations of detritivorous consumers, which are food for zooplankton predators such
as juvenile fish and decapod crustaceans [
29
,
51
]. After exposure to contaminants and the
associated stress, it is clear that NIS species benefit from the rich feeding-grounds provided
by estuaries, increasing the likelihood of their successful introduction.
Coastal lines and estuaries, in many cases, have been completely modified and ship-
ping selects for tolerant species thereby increasing the occurrence and densities of non-
native species delivered in ballast water to contaminated locations. The majority of NIS
are transported in ballast water or as hull-fouling organisms [
31
]. Metals are toxic to
many marine organisms [
52
], but some organisms are able to withstand exposures to these
toxicants [
53
]. This physiological stress would allow a selection in the transportation of
those species, in such a way that those with efficient detoxification mechanisms or more
resistant could survive their transportation better [
2
]. Thus, the coastal waters of the Gulf of
Processes 2021,9, 740 5 of 9
Cadiz, rich with chemical alterations, such as the Guadalquivir and Tinto-Odiel estuaries,
could be a mechanism for the selection of toxicant tolerance in non-native species.
4. Modifications to the Coastal Habitat: Increasing the Substrate of Non-Native Species
In addition to the modification of water quality and aquatic environment contamina-
tion, modified environments such as marinas or artificial structures on the coast increase
retention of non-native species propagules and provide a substratum for their establish-
ment [
53
–
55
]. Historically, the coastal line of the GoC has suffered several anthropogenic
transformations such as the construction of four main harbors (in Algeciras, Cadiz, Seville
and Huelva), reconstructed beaches (e.g., in Algeciras, Cadiz and Huelva) and wetlands
(in the Guadalquivir river basin). The increasing transformation of natural to urbanized
coastlines has promoted the establishment and spread of NIS [
56
]. Recently, a catas-
trophic bloom of Rugulopterix okamurae caused a significant impact throughout the Strait
of Gibraltar (Spain). This species of algae had likely been introduced via ballast waters
(although it cannot fully demonstrate), and its spread has increased, possibly due to global
warming [57].
The global increase in anthropogenic activities results in hydrological modifications,
creating environmental novelty and newly available artificial habitat [58,59].
Aquaculture has expanded greatly in the last few decades and deserves special atten-
tion. These activities can provide the substrate for potentially invasive species to settle and
grow in the vicinity of areas with high maritime traffic, i.e., harbors, but they can also serve
as a source of biofouling organisms that can attach to a new substrate, permitting them to be
transported to a location where they can become invasive. These, together with the occur-
rence of other contaminants such as nutrients, pathogens or emerging contaminants may
also be transferred to another area. For these reasons, harbors can be considered a point of
transfer between aquaculture and shipping [
60
,
61
]. Some examples of this transference are
the amoebic gill disease (N. pemaquidensis) [62] or the oyster parasite B. ostreae [63].
5. Climate-Related Invasion of Non-Native Species
Many Mediterranean river discharges have declined more than the levels expected
due to reductions in precipitation, and this is due to the flow regime of the water controlled
by dams [
64
]. For instance, these effects have occurred clearly in the Guadiana and the
Guadalquivir estuaries in the GoC [
65
,
66
]. In the case of the Guadalquivir estuary, the
annual freshwater discharge since the construction of the Alcala del Rio dam (1930) has
shown a significant long-term decreasing trend in dam discharges [
64
]. This anthropogenic
reduction of freshwater discharge from Mediterranean rivers may create a different habitat,
thus increasing the suitable habitat available for colonization by non-native species [
67
].
For instance, the Guadalquivir estuary and the adjacent salt marshes have recorded a high
number of non-native species since the 1970s, even zooplankton species such as Acartia
tonsa [
68
]. The interaction of water-usage practices and climate change anomalies has
the potential to create events of new invasions, such as the co-occurrence of increased
freshwater extraction and the resulting increased saline conditions in the San Francisco
estuary that benefitted a non-indigenous zooplankton species (e.g., [69]).
Thus, introduction or invasions may be accelerated by global warming and enhanced
by anthropogenic forces such as ballast water or aquaculture as previously discussed.
Global warming has a direct effect on the proliferation of harmful algal blooms (HABs),
which may also be promoted because of the contents of ballast water. These are of partic-
ular interest and concern because of their economic and health consequences [
70
]. Most
of the related studies have been focused on the role of global warming in freshwater
cyanobacterial invasion patterns [
71
]; however, further research is encouraged concerning
marine HABs and the role of global warming in their spread. For instance, a HAB related
paralytic shellfish poisoning event affected mussel aquaculture along the Cádiz coastline
in the Algeciras Bay [
72
], which is an area that experiences high maritime traffic and
industrial pressure.
Processes 2021,9, 740 6 of 9
Finally, climate warming will expand northward along the European Atlantic coast
through the gulf of Cadiz and will benefit non-native species with wide environmental
tolerances, as has already occurred with other macroinvertebrates [1].
6. Conclusions
Ballast water is an important vector for the dispersal of pre-adult stages and other
microorganisms from different geographical areas that are not naturally connected. It has
been observed that microscopic organisms and early development stages can develop and
become invasive in over-exploited ecosystems that are highly influenced by anthropogenic
perturbations, such as harbors and also modified environments, such as estuaries. Many
efforts have been made to diminish the high impact of the NIS related to ballast water.
However, due to advances in new techniques for species detection, the detection of many
microscopic organisms is increasing, also including the early stages of the development
of macroscopic organisms. In this scenario, a high abundance of microorganisms (includ-
ing those below 10
µ
m in size) has been demonstrated in ballast waters and may have
a significant impact on the receiving environment. Consequently, this fact should, per-
haps, be taken into account in the discharge standards [
9
]. Additionally, it has also been
demonstrated that the abiotic factors in ballast waters and receiving environments can vary
widely and organisms in ballast waters are not fully decay by these abiotic factors [
18
]. In
order to overcome these challenging conditions properly, the assessment and validation of
ballast water treatment systems that can efficiently overcome these two factors (biotic and
abiotic) is encouraged. Thus, it should involve a “worst case scenario” that could occur
in real water conditions [
18
,
73
]. Additionally, the development of efficient ballast water
management systems in these scenarios would also benefit some related industries, such as
aquaculture, which is also, potentially, affected by possible spread of organisms resulting
from an inadequate ballast water management [61,70].
Author Contributions:
Conceptualization, E.G.-O. and J.M.-A.; writing—original draft preparation,
E.G.-O. and J.M.-A.; writing—review and editing, E.G.-O. and J.M.-A. All authors have read and
agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: This essay did not report any data.
Acknowledgments:
This essay was developed in the framework of the InvBlue project (PID2019-
105978RA-I00) from the Spanish “Ministerio de Economía y Competitividad (MINECO), Plan Na-
cional I + D”, and within the 2014–2020 ERDF Operational Programme and Department of Economy,
Knowledge, Business and University of the Regional Government of Andalusia (Spain). Project Ref.:
FEDER-UCA18 -108023. We thank Jon Nesbit for the English revision. We are also grateful to two
anonymous referees for their critiques and suggestions that improved the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
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