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Finfish vs jellyfish: complimentary feeding patterns allow threespine stickleback Gasterosteus aculeatus and common jellyfish Aurelia aurita to co-exist in a Danish cove

DOI:10.1007/s00227-018-3407-y
Authors:
Anastasia Yurtseva at Zoological Institute of Russian Academy of Sciences
Anastasia Yurtseva
  • Zoological Institute of Russian Academy of Sciences
Florian Lüskow at University of British Columbia - Vancouver
Florian Lüskow
Marion Hatton
Marion Hatton
Marion Hatton
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Adèle Doucet
Adèle Doucet
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Abstract and Figures

The threespine stickleback Gasterosteus aculeatus and the common jellyfish Aurelia aurita are keystone species in many marine ecosystems, including the shallow cove Kertinge Nor, in Denmark. Both species feed on zooplankton, raising the potential for competition between them. While jellyfish are tactile filtering planktivores, sticklebacks are visual feeders that actively detect, attack and capture prey. The study compared clearance rates (Cl) and tested the hypothesis that jellyfish are more efficient in feeding on small prey and sticklebacks on larger prey animals. Individual (Clind) and population (Clpop) feeding characteristics were studied under good visual conditions. Individual sticklebacks (TL = 44 mm) demonstrated 14–51-fold higher Clind than jellyfish (d = 27 mm) when feeding on small (< 1 mm) and medium (1–4 mm) sized prey and threefold higher Clind when feeding on larger prey (4–11 mm). Clpop was calculated for both species based on their densities in the cove. When consuming small- and medium-sized prey in May–July, Clpop for stickleback was 2–20-fold higher than for jellyfish, but in August following a decrease in fish density, Clpop was higher for jellyfish. This may imply higher predation pressure from stickleback on zooplankton in Kertinge Nor at the beginning of the season, though the common jellyfish was considered earlier as a species controlling zooplankton there. The two competing species likely coexist in the cove due to different seasonal cycles of abundance and thus different seasonal patterns of plankton consumption.
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Vol.:(0123456789)
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Marine Biology (2018) 165:148
https://doi.org/10.1007/s00227-018-3407-y
ORIGINAL PAPER
Finsh vs jellysh: complimentary feeding patterns allow threespine
stickleback Gasterosteus aculeatus andcommon jellysh Aurelia aurita
toco‑exist inaDanish cove
AnastasiaYurtseva1,2 · FlorianLüskow3,4· MarionHatton5· AdèleDoucet6· DmitryLajus2
Received: 26 February 2018 / Accepted: 14 August 2018 / Published online: 24 August 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
The threespine stickleback Gasterosteus aculeatus and the common jellyfish Aurelia aurita are keystone species in many
marine ecosystems, including the shallow cove Kertinge Nor, in Denmark. Both species feed on zooplankton, raising the
potential for competition between them. While jellyfish are tactile filtering planktivores, sticklebacks are visual feeders that
actively detect, attack and capture prey. The study compared clearance rates (Cl) and tested the hypothesis that jellyfish are
more efficient in feeding on small prey and sticklebacks on larger prey animals. Individual (Clind) and population (Clpop)
feeding characteristics were studied under good visual conditions. Individual sticklebacks (TL = 44mm) demonstrated
14–51-fold higher Clind than jellyfish (d = 27mm) when feeding on small (< 1mm) and medium (1–4mm) sized prey and
threefold higher Clind when feeding on larger prey (4–11mm). Clpop was calculated for both species based on their densities
in the cove. When consuming small- and medium-sized prey in May–July, Clpop for stickleback was 2–20-fold higher than
for jellyfish, but in August following a decrease in fish density, Clpop was higher for jellyfish. This may imply higher preda-
tion pressure from stickleback on zooplankton in Kertinge Nor at the beginning of the season, though the common jellyfish
was considered earlier as a species controlling zooplankton there. The two competing species likely coexist in the cove due
to different seasonal cycles of abundance and thus different seasonal patterns of plankton consumption.
Introduction
One of the most obvious changes in many marine ecosys-
tems in recent decades is the considerable increase in bloom
frequency and intensity of gelatinous zooplankton (com-
monly referred to as ‘jellyfish’) in many locations world-
wide (Graham etal. 2001; Purcell 2005). Researchers often
link this increase with various anthropogenic activities that
disrupt the structure and function of marine ecosystems,
such as climate change, pollution and fisheries (Arai 2001;
Richardson etal. 2009; Conley and Sutherland 2015). Fol-
lowing a positive feedback loop (Gershwin 2013), growing
jellyfish populations can further alter marine ecosystems and
thus reduce ecosystem services (Hansson etal. 2005; Flynn
etal. 2012).
Probably one of the most important consequences of
these changes is increasing trophic competition between
jellyfish and small pelagic fish for zooplankton (Purcell and
Arai 2001; Shoji etal. 2005). Therefore, small pelagic fish
would be among the first to suffer in the whole cascade of
changes in marine ecosystems dealing with growing jellyfish
populations. Often, the small pelagic fish themselves have
Responsible Editor: J. Purcell.
Reviewed by A. Malzahn and an undisclosed expert.
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s0022 7-018-3407-y) contains
supplementary material, which is available to authorized users.
* Anastasia Yurtseva
ayurtseva@gmail.com
1 Laboratory ofIchthyology, Zoological Institute RAS,
199034St.Petersburg, Russia
2 Department ofIchthyology andHydrobiology,
Saint-Petersburg State University, 199178St.Petersburg,
Russia
3 Marine Biological Research Centre, Department ofBiology,
University ofSouthern Denmark, 5300Kerteminde,
Denmark
4 Department ofEarth, Ocean andAtmospheric Sciences,
University ofBritish Columbia, Vancouver, BCV6T1Z4,
Canada
5 Johnson andJohnson Campus de Maigremont,
27100ValdeReuil, France
6 École de Biologie Industrielle, 95800Cergy, France
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... In contrast, Kiel Bight experiences even stronger fluctuations, including years with strong blooms but also years with very low abundance over time. This has resulted in more consistent and stronger predation impacts of Aurelia aurita on mesozooplankton compared with Kiel Bight, which is controlling the zooplankton biomass at least during late summer (Olesen 1995;Yurtseva et al. 2018) with calculated 1-4 days of half-life expectancies (Lüskow and Riisgård 2016). During years of high abundance of small jellyfish, predation-induced declines in prey have resulted in a feedback loop leading to shrinkage and mortality of jellyfish (Goldstein and Riisgård 2016). ...
... Temporal and spatial dynamics further complicate this picture. For example, in Kertinge Nor, sticklebacks (Gasterosteus aculeatus Linnaeus, 1758) and jellyfish both reach high abundances, but at different times of the year, which limits the potential for competition (Yurtseva et al. 2018). However, knowing about effects of fish on jellyfish are crucial in order to understand jellyfish population dynamics in the Baltic Sea. ...
Review of jellyfish trophic interactions in the Baltic Sea
Article
Full-text available
  • Sep 2021
Despite the diversity and oftentimes large biomass of jellyfish in marine systems, their ecological role remains poorly understood. We here provide the first systematic review of studies on jellyfish trophic ecology in the Baltic Sea (a regional marine system under strong multiple global and regional anthropogenic pressures). In total, we identified 57 peer-reviewed publications, with notable taxonomic bias towards two species (Aurelia aurita; non-indigenous Mnemiopsis leidyi) and spatial bias towards five areas (Bornholm Basin, Kiel Bight, Kertinge Nor, Lim- and Gullmarsfjord). The studies provide evidence for diverse trophic roles of jellyfish as predators and as competitors of other jellyfish, zooplankton and fish species. In combination, the studies also highlight potentially large impacts via top-down (grazing) and bottom-up (nutrient excretion) effects, but also, strong spatio-temporal variability in the magnitude of these effects, depending on the occurrence of jellyfish blooms. Studies on the role of jellyfish as prey for fish, seabirds or marine mammals, and for benthic systems via food-falls, were limited or lacking for the Baltic Sea, despite increasing focus on these topics globally. Improved understanding of the temporal (seasonal, inter-annual, long-term) and spatial variability of blooms and corresponding trophic effects, would provide more systematic understanding of the ecological role of jellyfish in the spatio-temporally variable Baltic Sea. A broader spatial coverage, inclusion of more jellyfish taxa and under-studied early life history stages, as well as the implementation and continuation of long-term data series would represent important steps towards this goal.
Feeding patterns of threespine stickleback, Gasterosteus aculeatus (Linnaeus, 1758) on the spawning grounds of the Kandalaksha Bay, White Sea
Conference Paper
Full-text available
  • Nov 2018
Threespine stickleback Gasterosteus aculeatus (Linnaeus, 1758) is one of the most widely distributed fish species, living both in fresh and marine waters of the northern part of the Atlantic and Pacific Oceans (Berg, 1949; Wootton, 1984). At present, the sticklebacks are the most abundant pelagic fish in the White Sea (Ivanova et al., 2016). Here stickleback spawn in shallow waters, preferring seagrass beds (Lajus et al., 2013). The Kandalaksha Bay with its extremely indented costal line and numerous shallow inlets with dense seagrass beds (primarily eelgrass Zostera marina (Linnaeus, 1753)) create favorable conditions for spawning stickleback (Ziuganov, 1991; Ivanova et al., 2016). The eggs develop in the nests, being guarded by males. Males aerate eggs and remove unfertilized and dead ones. Females sometime after spawning stay on the spawning grounds and actively feed. They often attack on the nests with a purpose to prey on eggs and larvae of their own species (Mukhomediarov, 1966). The results of the study show that the White Sea stickleback is a typical omnivorous species. They prey on benthos, eggs and juvenile fish, imago of flying insects and plankton. In summer, during spawning period, stickleback is mostly benthivores. Their stomach content is correlates with characteristics of the spawning grounds. In the traditionally “good” spawning grounds, where the density of fish, and therefore density of eggs is high (Demchuk et al., 2018), and the stickleback eggs is a preferable food item. During spawning, the diet changes accordingly to the change of availability of different food items, and by the end of the spawning, the feeding intensity increases, especially in females. Despite the wide range of food items of the stickleback and its high variability during the spawning season, not more than 2-3 components dominate at once.
Питание беломорской трехиглой колюшки Gasterosteus aculeatus (Linnaeus, 1758) на нерестилищах.
Article
Full-text available
  • Apr 2018
The feeding of spawning threespine stickleback Gasterosteus aculeatus L. during the entire spawning period (late May – early July) in 2016 has been studied in three locations of the Chupa Inlet mouth, Kandalaksha Bay, White Sea. The fish mostly feed on benthos: stickleback eggs (up to a half of stomach content), pupae and larvae of Chironomidae, Polychaeta and Amphipoda, and also on imago of Diptera. In good spawning grounds with high density of spawners, the proportion of stickleback eggs in feeding is higher. Effect of sex, spawning stage and location has been found. Females, in comparison with males, have a more diverse diet (20 food items versus 13) and show greater changes during the spawning season, in particularly, they consume more energetically-rich food items than males. This is likely because more territorial males, occupied with guarding the progeny, are more limited in changing their diet. Differences between the sexes are especially large by the end of spawning period. Females begin intensive post-spawning feeding before the males, which have to guard the nests. We also observed a decrease of condition factor during the spawning period, which is probably associated with high energetic cost of spawning.
DNA metabarcoding reveals diverse diet of the three-spined stickleback in a coastal ecosystem
Article
Full-text available
The three-spined stickleback (Gasterosteus aculeatus L., hereafter ‘stickleback’) is a common mesopredatory fish in marine, coastal and freshwater areas. In large parts of the Baltic Sea, stickleback densities have increased >10-fold during the last decades, and it is now one of the dominating fish species both in terms of biomass and effects on lower trophic levels. Still, relatively little is known about its diet—knowledge which is essential to understand the increasing role sticklebacks play in the ecosystem. Fish diet analyses typically rely on visual identification of stomach contents, a labour-intensive method that is made difficult by prey digestion and requires expert taxonomic knowledge. However, advances in DNA-based metabarcoding methods promise a simultaneous identification of most prey items, even from semi-digested tissue. Here, we studied the diet of stickleback from the western Baltic Sea coast using both DNA metabarcoding and visual analysis of stomach contents. Using the cytochrome oxidase (CO1) marker we identified 120 prey taxa in the diet, belonging to 15 phyla, 83 genera and 84 species. Compared to previous studies, this is an unusually high prey diversity. Chironomids, cladocerans and harpacticoids were dominating prey items. Large sticklebacks were found to feed more on benthic prey, such as amphipods, gastropods and isopods. DNA metabarcoding gave much higher taxonomic resolution (median rank genus) than visual analysis (median rank order), and many taxa identified using barcoding could not have been identified visually. However, a few taxa identified by visual inspection were not revealed by barcoding. In summary, our results suggest that the three-spined stickleback feeds on a wide variety of both pelagic and benthic organisms, indicating that the strong increase in stickleback populations may affect many parts of the Baltic Sea coastal ecosystem.
Population predation impact of jellyfish (Aurelia aurita) controls the maximum umbrella size and somatic degrowth in temperate Danish waters (Kertinge Nor and Mariager Fjord)
Article
Full-text available
The population density and individual size of the common jellyfish Aurelia aurita were studied during 2014 and 2015 in two Danish fjord systems, Kertinge Nor and Mariager Fjord in order to obtain a better understanding of the driving forces for somatic degrowth (shrinkage) of medusa during late summer and autumn. In both fjord systems the numerous medusae were characterized by their small body size and by a distinct phase of degrowth. The population predation impact of A. aurita, with estimated zooplankton half-lives of only about 1 to 3 d, indicated that shortage of prey controls the maximum umbrella size of only 60 (Kertinge Nor) to 100 mm (Mariager Fjord) and the subsequent degrowth. When jellyfish were brought into the laboratory in early spring and the late degrowth period and continuously fed with zooplankton (Artemia salina), equivalent to 5.8 μg C l–1, this resulted in initial growth rates of 11.3 and 24.4 % d–1 in two series of experiments with 56.9 and 5.5 mm umbrella diameter, respectively, and considerably longer survival than of jellyfish in their natural environment. The degrowth rates in Kertinge Nor (–1.2 % d–1) and Mariager Fjord (−1.5 and −0.7 % d−1 in 2014 and 2015, respectively) were slightly lower than observed in laboratory starvation experiments (−3.2 and −4.2 % d−1), indicating that the starvation of jellyfish in nature was less pronounced, i.e. some prey organisms may have been available although the short estimated half-lives of zooplankton suggested a pronounced predation impact exerted by the jellyfish.
The effect of temperature on predation rates of a fish (Gasterosteus aculeatus) and a jellyfish (Aurelia aurita) on larval capelin (Mallotus villosus)
Article
  • Jan 1996
Field studies have shown that temperature influences larval fish mortality rates. In laboratory experiments conducted in microcosms (38 L) and mesocosms (3100 L), we tested the effect of three temperatures (3.9, and 15°C) on the mortality rates of newly emerged larval capelin (Mallotus villosus) in the presence and absence of predators: the stickleback, Gasterosteus aculeatus, and the jellyfish Aurelia aurita. Predation rates by sticklebacks were positively correlated with temperature in microcosm trials, but not in mesocosm trials; this difference was related to the duration of the experiments and the level of satiation of the sticklebacks. Predation rates by jellyfish were significantly lower at 3°C than at 9 and 15°C in microcosm trials, and significantly more larvae were found dead, though not consumed, at 3°C. As a result, there was no difference in the total mortality rate of capelin among temperatures in microcosm trials with jellyfish. Mesocosm trials with jellyfish also resulted in no significant differences in larval mortality rates among temperatures. In the field, mass emergence of capelin larvae probably swamps small fish predators such as sticklebacks that have high capture rates and small gut capacities, but not jellyfish, which have relatively low capture rates and large gut volumes.
Estuarine and marine diets of out-migrating Chinook Salmon smolts in relation to local zooplankton populations, including harmful blooms
Article
  • Nov 2017
A cross-scale trophic cascade from large predatory fish to algae in coastal ecosystems
Article
  • Jul 2017
Trophic cascades occur in many ecosystems, but the factors regulating them are still elusive. We suggest that an overlooked factor is that trophic interactions (TIs) are often scale-dependent and possibly interact across spatial scales. To explore the role of spatial scale for trophic cascades, and particularly the occurrence of cross-scale interactions (CSIs), we collected and analysed food-web data from 139 stations across 32 bays in the Baltic Sea. We found evidence of a four-level trophic cascade linking TIs across two spatial scales: at bay scale, piscivores (perch and pike) controlled mesopredators (three-spined stickleback), which in turn negatively affected epifaunal grazers. At station scale (within bays), grazers on average suppressed epiphytic algae, and indirectly benefitted habitat-forming vegetation. Moreover, the direction and strength of the grazer–algae relationship at station scale depended on the piscivore biomass at bay scale, indicating a cross-scale interaction effect, potentially caused by a shift in grazer assemblage composition. In summary, the trophic cascade from piscivores to algae appears to involve TIs that occur at, but also interact across, different spatial scales. Considering scale-dependence in general, and CSIs in particular, could therefore enhance our understanding of trophic cascades. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
Population predation impact of jellyfish (Aurelia aurita) controls the maximum umbrella size and somatic degrowth in temperate Danish waters (Kertinge Nor and Mariager Fjord)
Article
The population density and individual size of the common jellyfish Aurelia aurita were studied during 2014 and 2015 in two Danish fjord systems, Kertinge Nor and Mar-iager Fjord in order to obtain a better understanding of the driving forces for somatic degrowth : (shrinkage) of medusa during late summer and autumn. In both fjord systems the numerous medusae were characterized by their small body size and by a distinct phase of degrowth. The ( population predation impact of A. aurita, with estimated zooplankton half-lives of only about 1 ; to 3 d, indicated that shortage of prey controls the maximum umbrella size of only 60 (Kertinge Nor) to 100 mm (Manager Fjord) and the subsequent degrowth. When jellyfish were brought into the laboratory in early spring and the late degrowth period and continuously fed with zoo-plankton (Artemia salina), equivalent to 5.8 μg C l⁻¹, this resulted in initial growth rates of 11.3 and 24.4 % d⁻¹ in two series of experiments with 56.9 and 5.5 mm umbrella diameter, respectively, and considerably longer survival than of jellyfish in their natural environment. The degrowth rates in Kertinge Nor (-1.2 % d⁻¹) and Manager Fjord (-1.5 and -0.7 % d⁻¹ in 2014 and 2015, respectively) were slightly lower than observed in laboratory starvation experiments (-3.2 and -4.2 % d⁻¹), indicating that the starvation of jellyfish in nature was less pronounced, i.e. some prey organisms may have been available although the short estimated half-lives of zooplankton suggested a pronounced predation impact exerted by the jellyfish.
Seasonal dynamics in the diet of pelagic fish species in the southwest Baltic Proper
Article
  • Dec 2016
There is accumulating evidence of the significant role of three-spined sticklebacks (Gasterosteus aculeatus) for ecosystem structure and functioning in coastal areas of the Baltic Sea, but little is known about the role of the species in the pelagic foodwebs of the Baltic and its interaction with other planktivorous fish species. In this study, we assess the feeding niche, diet overlap, and prey selectivity of sticklebacks, herring (Clupea harengus), and sprat (Sprattus sprattus) in an area of the southwest Baltic Sea (Kalmar Sound) in relation to the seasonal abundance of zooplanktonic prey during 2009–2011. The main prey items for all fish species studied were the calanoid copepods Eurytemora affinis, Temora longicornis, and Acartia spp. during spring and summer, and the cladoceran Bosmina spp in autumn. The diet of all the three fish species overlapped considerably, especially during summer and autumn. A substantial diet overlap was even present between sticklebacks and larger (>10 cm) herring and sprat. We also found evidence for an overlap in feeding preferences, i.e. certain zooplankton species were selected by all the three fish species in each given season. Overall, these results indicate potential resource competition between sticklebacks and clupeids. With an increasing abundance of sticklebacks in the Baltic Sea, their role should not be neglected when investigating pelagic foodweb dynamics, and management of herring and sprat may have to account for sticklebacks by considering that sticklebacks, via food competition, might affect clupeid stocks.
Moon Jellyfish, Aurelia Aurita, in the Gulf of Gdansk: Threatening predator or not?
Article
  • Jan 2016
The seasonal population dynamics and feeding preferences of the moon jellyfish, Aurelia aurita, in the Gulf of Gdansk (southern Baltic Sea) were investigated. Medusae were present in the water column from June to November, with maximum occurrence in August and September. The medusa bell diameter and weight increased during the study period reached maximum values in October. The relationship between bell diameter and wet weight was strong. No ephyrae were observed during the study period. Gastric content analysis revealed that the medusae fed mainly on copepods and cladocerans. Rotifers that dominated the water column throughout the study period were not found in the jellyfish guts, but the stable isotope signature indicated that they could have been a significant source of derived carbon. Low numbers of plankton prey and the lack of fish larvae in A. aurita guts suggest that the jellyfish is of minor relevance as a predator and competitor in the Gulf of Gdansk.