Vansteenbrugge, Lies

Vansteenbrugge, L.

Open Marine Archive

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The non-indigenous ctenophore Mnemiopsis leidyi in the 
southern North Sea: Ecological and socio-economic effects 
related to its trophic position and the current distribution of 
gelatinous zooplankton 
Vansteenbrugge Lies 
ILVO, Ankerstraat 1, 8400 Oostende, Belgium 
E-mail: lies.vansteenbrugge@ilvo.vlaanderen.be  
In recent years, abundances of gelatinous zooplankton are thought to have increased all over the 
world, resulting in jellyfish-dominated ecosystems and food webs. This trend, also referred to as 
‘jellification’, is mainly based on a few local case studies and media-driven public perception, 
because long-term jellyfish datasets are scarce. Sudden increases in jellyfish densities (blooms) are 
a common life cycle characteristic, mainly driven by natural fluctuations in the climate. However, 
certain anthropogenic pressures, such as overfishing, eutrophication, non-deliberate transport of 
non-indigenous species can be correlated with varying jellyfish abundances. Moreover, gelatinous 
zooplankton blooms can directly interfere with anthropogenic activities, for example by clogging 
and rupturing of commercial fishing nets, by stinging beach tourists or by killing fish in sea farms. 
To be able to manage and reduce the potential problems and economic costs related to jellyfish 
outbreaks, understanding the mechanisms driving these outbreaks is imperative.  
 
In the 1980s, the ctenophore Mnemiopsis leidyi A. Agassiz 1865, indigenous to the Atlantic coast of 
North and South America, was introduced in the Black Sea through ballast water of ships. The 
densities of this invasive species rapidly increased in the Black Sea, and in addition to overfishing 
and eutrophication led to a collapse of the major fisheries, causing vast ecological and socio-
economic losses. Consequently, the first observations of M. leidyi in northern European marine 
waters in 2005, and the subsequent sightings of this non-indigenous ctenophore in Belgian marine 
waters in 2007 caused the appropriate concern. This PhD thesis, as part of the Interreg Iva 2 Seas 
MEMO project, aimed to assess the structural and functional role of the non-indigenous ctenophore 
Mnemiopsis leidyi in the southern North Sea. More specifically, we focussed on (1) the current 
distribution of M. leidyi in Belgian marine waters, the adjacent ports and the Westerschelde estuary, 
related to other gelatinous zooplankton, (2) the trophic ecology and interactions of M. leidyi in the 
planktonic food web, (3) the potential ecological and socio-economic effects of the presence of M. 
leidyi and other gelatinous zooplankton in these waters, and (4) the overall threat of M. leidyi and 
the implications for non-indigenous species’ management. 
 
After a general introduction (Chapter 1) on jellyfish and gelatinous zooplankton, the potential 
introductory pathways of invasive species and the life cycle characteristics of M. leidyi, the data and 
results are presented in seven chapters. Different approaches were used to tackle the research 
questions and objectives, including field studies, experimental and laboratory work, database 
analyses and public questionnaires. In this PhD study, the term ‘gelatinous zooplankton’ was 
narrowed down to the planktonic medusa phase (jellyfish) of the phylum Cnidaria (classes Hydrozoa 
and Scypohozoa) and the phylum Ctenophora.  
 
In the southern North Sea, long-term data on gelatinous zooplankton are scarce, which is partly 
driven by the difficulties to sample and preserve these often ‘fragile’ organisms, M. leidyi in 
particular. Therefore, in Chapter 2, methodological issues concerning sampling and preservation 
were investigated. We focused on two different types of plankton nets: a WP2 net (mesh size 200 
µm) and ring trawl net (mesh size 1000 µm). Based on their different mesh size and way of 
deployment (vertical versus undulating trawl), we evaluated whether they can be compared in terms 
of M. leidyi density and size distribution. Mnemiopsis leidyi densities from 245 sampling events 
were analysed according to net type and revealed that WP2 nets do not provide a good estimate of 
its presence compared to ring trawl nets. Moreover, when M. leidyi was present in both nets, much 
larger density estimates were found by the WP2 net (45.2 ± 114.0 ind.m-3 for WP2 net versus 12.8 ± 
28.5 ind.m-3 for ring trawl net). The ring trawl net gave a good overview of adult population 
structure, but may underestimate some of the small ctenophores. Consequently, both the filtered 
volume and the mesh size largely determine the catch. We also tested different preservation 
solutions and methods with respect to morphological and genetic identification of M. leidyi and in 
function of stable isotope analyses. From our experiments it became clear that unpreserved 
samples are preferred for any type of analysis. However, in many situations, direct identification in 
the field is not possible and preserving the sample is inevitable. Then, short-term preservation in 
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Lugol's solution or RCL2® may provide a good alternative, but shrinkage was observed in both 
preservatives. For stable isotope analyses, different preservation methods resulted in significant 
differences in both δ13C and δ15N, which should be considered when comparing different isotopic 
compositions. The findings and recommendations formulated in this study should be considered in 
future M. leidyi monitoring. Zooplankton samples collected during this PhD were analysed on board 
and M. leidyi was morphologically identified and measured alive (except for Tentaculata larvae 
which were genetically identified).  
 
The discovery of M. leidyi in Belgian waters in 2007 created a unique opportunity to enhance our 
knowledge on the distribution of gelatinous zooplankton in the southern North Sea (Chapter 3). 
Monthly and seasonal CalCOFI ring trawl plankton net samples (mesh size 1000 µm, undulating 
trawl) from the Belgian part of the North Sea and the adjacent Westerschelde estuary were gathered 
between March 2011 and February 2012. The gelatinous zooplankton in these samples consisted of 
three Scyphozoa, three Ctenophora and 27 Hydrozoa taxa, including three non-indigenous species: 
M. leidyi, Nemopsis bachei and Lovenella assimilis. In an addendum (Addendum II), we also 
described the re-discovery of larval mantis shrimp (Rissoides desmaresti), which has not been 
observed in the Belgian part of the North Sea since 1913. Average gelatinous zooplankton densities 
reached up to 18 ind.m-3 near the coast, gradually declining towards the open sea, while in the 
brackish Westerschelde, average densities remained below 3 ind.m-3. Gelatinous zooplankton 
densities were highest in summer and autumn, and the ctenophore Pleurobrachia pileus and the 
hydromedusa Clytia sp. were present year-round and at every location. Gelatinous zooplankton 
densities never outnumbered the non-gelatinous zooplankton densities from the CalCOFI net. Due 
to the larger mesh size (1000 µm) of this net, only the larger fraction of the zooplankton is 
captured. The spatial and temporal distribution patterns seemed to be mainly driven by 
temperature (season) and salinity (location). In terms of population dynamics, the predatory 
ctenophore Beroe sp. followed the three reproductive cycles of its prey P. pileus, but may profit 
from the high abundances of M. leidyi in summer and autumn by reaching higher densities. This 
study provides a firm baseline to evaluate potential gelatinous zooplankton increases in the Belgian 
part of the North Sea and the Westerschelde estuary.  
 
The analysis of the spatio-temporal distribution and population dynamics of M. leidyi in the 
southern North Sea and its main coastal ports (Chapter 4) revealed that M. leidyi occurred from 
August to December, but was never found more than 30 km offshore. Densities were generally low 
(average 0.8 ± 2.8 ind.m-3) compared to other invaded ecosystems in Europe (densities up to 867 
ind.m-3). Highest densities of M. leidyi were found in the semi-enclosed basin in the port of 
Oostende (18.4 ind.m-3) and the Westerschelde estuary (1.9 ind.m-3). The presence of larvae and the 
sudden appearance of high numbers across the size distribution in August indicated that ports and 
estuaries may act as sources, populating the adjacent coastal (sink) areas. By means of a zero-
inflated negative binomial regression model, the observed variation in M. leidyi densities was 
related to temperature (highest densities when temperature starts to decrease), wave height (higher 
densities in low energetic systems) and dissolved oxygen concentrations (higher densities at low 
oxygen concentrations). Although M. leidyi densities remained relatively low since its first 
appearance in Belgian waters in 2007, a permanent M. leidyi population has established in the 
southern North Sea. As outbreaks may happen with only small changes in environmental 
parameters, further monitoring of this notorious non-indigenous species is recommended. 
 
Knowledge on the diet of M. leidyi and its interactions with other components of the pelagic food 
web will largely contribute to assess the impact of this non-indigenous species on the ecosystem. 
Using both stable isotope (SI; δ13C and δ15N) and fatty acid (FA) analyses, we revealed spatial and 
temporal variation in the trophic ecology of M. leidyi in different ecosystems in the southern North 
Sea (Chapter 5). Based on the isotopic composition, we found that spatial differences were largely 
driven by variation at the base of the food web rather than diet changes of M. leidyi in the different 
ecosystems. Temporal variation in M. leidyi SI composition was also influenced by shifting baseline 
values and driven by seasonal changes in the associated plankton communities. In this chapter, we 
provide the first data on the FA composition of M. leidyi as compared to FA concentrations of two 
other (indigenous) ctenophores. The total FA concentration of M. leidyi was three to four times 
lower compared to Pleurobrachia pileus and Beroe sp., categorising this non-indigenous ctenophore 
as a lipid-poor organism. Trophic interactions between M. leidyi and the two co-occurring 
ctenophores (P. pileus and Beroe sp.) showed considerable resource differentiation, which could be 
the result of competition or both ctenophores could have different diets. A mixture of zooplankton 
was identified as potential food source for M. leidyi. FA markers supported the carnivorous diet of 
Beroe sp., but its SI composition did not confirm it as a predator of M. leidyi.  
 
The feeding ecology of M. leidyi was further investigated as its invasive success is partly related to a 
broad and flexible planktivorous diet. In Chapter 6, we investigated the feeding rates and carbon 
assimilation of M. leidyi by means of grazing experiments with a pelagic diatom species 
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Phaeodactylum tricornutum and three potential mesozooplankton prey species: nauplii from brine 
shrimp Artemia salina, a copepod Acartia tonsa, and eggs and larvae of European sea bass 
Dicentrarchus labrax. Clearance rates were on average 0.2 ± 0.1 L.mL
M.leidyi
-1.h-1, with no significant 
differences in clearance rates between prey type or prey size. The assimilation of carbon by M. leidyi 
for these different prey types was determined using 13C tracer experiments. Highest carbon 
assimilation was observed for Acartia and sea bass larvae (most efficiently assimilated), and lowest 
for the pelagic diatom P. tricornutum. To further elucidate the prey-dependent variation in carbon 
uptake, we investigated the effect of each prey type in terms of fatty acids as a proxy for food 
quality. The consumption of sea bass larvae, characterised by higher levels of DHA (an essential 
fatty acid), resulted in significantly higher FA concentrations in M. leidyi. As M. leidyi does not 
convert excess food into storage lipids, survival, growth and reproduction are likely enhanced by 
the higher food quality, which might contribute to its invasive success. As global warming may 
result in an earlier appearance of M. leidyi and thus temporal overlap with high quality prey such as 
fish larvae, a substantial impact on the ichthyoplankton community in the southern North Sea might 
be expected. 
 
The third aim of this PhD study was to determine the potential ecological and socio-economic 
effects of the presence of M. leidyi in Belgian waters. For the latter, we needed to broaden our scope 
by focusing on the impact of all prevailing jellyfish on beach tourism in Belgium, as M. leidyi is too 
small and fragile, and thus rarely noticed by tourists (except for divers). In Chapter 7, we examined 
to what extent the main jellyfish messages in the Flemish media corresponded with the knowledge 
and perception in the tourism sector along the Belgian coast. We searched Flemish newspapers for 
jellyfish-related articles issued between January 2000 and September 2012 and executed 
questionnaires at the Belgian coast in the summer of 2012. The number of Flemish newspaper 
articles increased from less than 5 in 2000 to 27 articles in 2010. Almost 75 % of these articles 
reported on the causes and economic consequences of jellyfish blooms, and many articles 
mentioned the dramatic consequences of stinging, poisonous and invasive species. The analysis of 
the questionnaires showed that the perception of beach tourists on jellyfish is only partly driven by 
the general media (mainly related to the causes of jellyfish blooms), while personal experience (e.g. 
stinging, slimy organisms) was at least an equally important driver. As public perception is a key 
driver for certain policy decisions, integrated coastal zone managers should consider the provision 
of simple and good information concerning jellyfish (e.g. billboards or aquaria) at the beach. The 
results of this socio-economic study might serve as a baseline for future citizen science programs. 
 
Finally, the main results of this PhD study were discussed in a broader perspective to manage the 
introduction and presence of non-indigenous or invasive species (Chapter 8). We performed a risk 
assessment for M. leidyi in the southern North Sea by means of the online Harmonia+ tool, which 
generates exposure (introduction, establishment and spread) and impact (on the environment and 
human activities) scores. An overall risk of 0.286 was calculated for the non-indigenous ctenophore 
M. leidyi in the southern North Sea, which is considered to be low. Up to 2012, M. leidyi showed a 
clear seasonal outbreak between summer and autumn. Relatively high densities (up to 18 ind.m-3) 
were only observed in the ports, which are considered to be of lower ecological value compared to 
the ‘richer’ coastal zone or Westerschelde estuary, where M. leidyi densities mostly remained below 
1 ind.m-3. The combination of periods with unfavourable environmental conditions, the diverse 
gelatinous zooplankton community (potential competition) and the presence of predators such as 
Beroe sp., probably has limited the success of M. leidyi in the southern North Sea. However, this 
PhD study (including the more recent observations in 2014) showed that the population of M. leidyi 
is fully established in the different southern North Sea ecosystems. Therefore, M. leidyi should 
remain under close observation by means of regular monitoring surveys, and management actions 
should not be postponed in order to safeguard the current ecosystem services. As such, trying to 
keep the population under control is most probably the only way forward for a proper management 
of this non-indigenous species. Ratification of the Ballast Water Convention by all countries around 
the world is another key issue to at least prevent the introduction of new species and to avoid 
potential re-introduction of M. leidyi in our waters. In light of the Marine Strategy Framework 
Directive, the early detection (and subsequent eradication) of non-indigenous species (many of them 
appearing in the water column as some sort of zooplankton stage), for example by means of 
automated sampling tools, needs to be promoted. This PhD study is a baseline for future 
(gelatinous) zooplankton monitoring in the Belgian part of the North Sea and Westerschelde estuary 
(and by extension the southern North Sea). 
 


The non-indigenous ctenophore <i>Mnemiopsis leidyi</i> in the southern North Sea: ecological and socio-economic effects related to its trophic position and the current distribution of gelatinous zooplankton

Ghent University Academic Bibliography

The non-indigenous ctenophore Mnemiopsis leidyi in the southern North Sea : ecological and socio-economic effects related to its trophic position and the current distribution of gelatinous zooplankton

https://biblio.ugent.be/publication/6965950/file/6965996.pdf

The non-indigenous ctenophore Mnemiopsis leidyi in the southern North Sea : ecological and socio-economic effects related to its trophic position and the current distribution of gelatinous zooplankton

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