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Article

Understanding Cassiopea andromeda (Scyphozoa) Invasiveness in Different Habitats: A Multiple Biomarker Comparison

by
Jorge Thé
1,†,
Marta Mammone
2,*,†,
Stefano Piraino
3,4,5,
Antonio Pennetta
6,
Giuseppe Egidio De Benedetto
6,
Tatiane Martins Garcia
1,
Marcelo de Oliveira Soares
1,7 and
Sergio Rossi
1,3
1
Instituto de Ciências do Mar (LABOMAR), Universidade Federal do Ceará (UFC), Fortaleza 60165-081, Brazil
2
Biology Department, Penn State University, State College, PA 16802, USA
3
Dipartimento di Scienze e Tecnologie Ambientali, Università del Salento, 73100 Lecce, Italy
4
Research Unit Lecce, Consorzio Nazionale Interuniversitario per le Scienze del Mare (CoNISMa), 73100 Lecce, Italy
5
National Biodiversity Future Center, S.c.a.r.l., 90133 Palermo, Italy
6
Dipartimento di Beni Culturali, Università del Salento, Via Monteroni, 73100 Lecce, Italy
7
Reef Systems Group, Leibniz Center for Tropical Marine Research (ZMT), 28359 Bremen, Germany
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Water 2023, 15(14), 2599; https://doi.org/10.3390/w15142599
Submission received: 2 June 2023 / Revised: 8 July 2023 / Accepted: 12 July 2023 / Published: 17 July 2023
(This article belongs to the Special Issue Implementation of Biodiversity and Ecosystem Services in Marine Ecosystem Management, Volume II)
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Abstract

:
A dual nutrition mode (i.e., mixotrophy) can be advantageous for alien species in a new environment. In Cearà (Brazil), the symbiotic jellyfish Cassiopea andromeda is rapidly spreading under diverse environmental conditions across natural and human-altered coastal habitats, such as mangroves and shrimp farms. Here we report on the trophic ecology of the alien upside-down jellyfish sampled in these two contrasting coastal habitats during the dry (July–October) and rainy (January–April) seasons, investigated by means of organic biomarkers (lipids, carbohydrates) and bulk tissue stable isotope (δ15N and δ13C) analyses. Total lipid content of jellyfish gonads was generally higher in shrimp farms, whereas no significant difference in carbohydrate concentration was found in jellyfish tissues from the two different habitats. Similarly, there were no significant differences in the δ15N values of jellyfish tissues from the two contrasting habitats, whereas the δ13C values were higher in jellyfish from shrimp farms. Overall, the higher carbon-enriched value in aquaculture ponds supports the hypothesis of differences of available food sources compared to the natural mangrove habitats, where food availability exhibits a stronger seasonality. In fact, aquaculture ponds are characterized by human-driven regular food supply, leading to more stable trophic conditions and to enhanced growth, lipid production, and gonadal output of C. andromeda jellyfish. This investigation may contribute to predicting how Cassiopea mixotrophy may contribute to explaining its differential success in different habitats.

1. Introduction

Anthropogenic pressures, such as overfishing, eutrophication, aquaculture, alien species introduction, and urbanization as well as climate change, have been proposed as multiple interacting drivers of increasing jellyfish populations worldwide [1]. Jellyfish outbreaks gain even more attention when considering invasive species and their ecological and socioeconomic impacts [2]. Invasiveness is the sum of synergic traits such as environmental tolerance, trophic plasticity, and life history strategies, and has been considered one of the most relevant aspects of ecosystem transformation during the last decades [2,3]. Understanding the trophic ecology of invasive organisms is thus essential to understanding their potential impact on the coastal ecosystems and, hence, having quantitative information for actions for their control or exploitation. The upside-down jellyfish Cassiopea andromeda [4] is commonly found in shallow-water ecosystems, such as mangroves, coral reefs, and seagrass beds as well as in aquaculture facilities, and displays frequent population outbreaks [5,6,7]. In addition, it has been increasingly recorded as a non-indigenous, outbreak-forming species across different countries [8,9,10,11]. C. andromeda has a relatively sessile behavior (epibenthic jellyfish), resting upside-down on the benthos to expose its endosymbionts to the light in calm waters. It is characterized by a mutualistic association with dinoflagellate microalgae (Symbiodiniaceae), which are able to adapt to different light conditions and provide the jellyfish with carbohydrates and lipids of photosynthetic origin, in return for a sheltered area with a regular supply of inorganic molecules [12,13,14]. The possibility of relying on different energy inputs (i.e., photosynthates from symbionts and heterotrophic input) allows C. andromeda to adapt to different environmental conditions with cascading consequences on primary productivity, nutrient cycling, and local food webs as observed in other symbiotic jellyfish species [15]. The study of animal diet (heterotrophic input) has been widely applied to understand the metazoan trophic interactions in food webs [16,17,18,19,20]. Many studies investigating the trophic position of several jellyfish species rely on direct approaches such as gut content [21]. However, this methodology delivers inaccurate or incomplete information, and discerning between autotrophic and heterotrophic energy inputs outside controlled experimental conditions (i.e., aquaria) is certainly a major issue [22,23,24,25,26,27]. Indirect combined approaches, such as stable isotopes, C:N ratios, lipid, carbohydrate, and fatty acid analyses, may help to disentangle the puzzle of direct diet and food capture rate observations, as these tools may integrate seasonal energy inputs as well as differences between different habitats or ecozones [28], and may also be used to discern the dominance of autotrophic or heterotrophic inputs in mixotrophic species [18,29]. This may be the case with C. andromeda. A combination of biomarkers (δ13C and δ15N, fatty acids, and lipid–carbohydrate storage) has been already used to understand the trophic position and the nutritional condition of both Semaeostomeae and Rhizostomeae jellyfish species such as Aurelia aurita, Stomolophus meleagris, and Cyanea nozakii [30]; Chrysaora melanaster [31]; Catostylus mosaicus [27]; Pelagia noctiluca [19,32,33]; and Mastigias papua [15]. It has thus been demonstrated to be a reliable and robust approach, especially in the understanding of jellyfish invasiveness potential under contrasting coastal habitats or environmental conditions. As elsewhere in the world, Brazilian mangroves are increasingly impacted by construction of harbors, city expansion, or multiple economic activities such as shrimp farms, causing a deep impact on biodiversity and the population dynamics of wild organisms [34,35,36]. The shrimp farm expansion on the Brazilian coast has oversimplified the functioning of the ecosystem, mainly impacting mangroves which have been eradicated to build up controlled ponds for shrimp aquaculture [35]. These ponds are deeply transformed, with much higher nutrient and particulate organic matter concentration compared to the mangrove areas [34]. Recently, C. andromeda was found to possess different invasiveness and physiological potentials in natural (mangrove) and artificial (aquaculture shrimp facility) habitats [7,10]. A greater number of jellyfish was found in the mangroves during the dry season (July: n = 546; October: n = 158) compared to the shrimp farms (July: n = 207; October: n = 119). However, while the abundance of C. andromeda was nearly stable in shrimp farms in both seasons, jellyfish in the mangroves disappeared during the rainy season. Moreover, C. andromeda in shrimp farms were three times larger (24.7 ± 5.8 cm) than those found in mangrove habitats (8.2 ± 3.4 cm) [37]. In the present study, we investigated the trophic ecology of C. andromeda in the two contrasting habitats (mangroves and shrimp farms), using a combination of analyses of macromolecules (lipids, carbohydrates, and total fatty acids) and stable isotopes (δ15N and δ13C), with the final aim of understanding how its nutritional condition is linked to its differing invasion success and population stability in the two environments.

2. Materials and Methods

2.1. Study Area

The study was carried out on the coast of Ceará state (Figure 1), Southwestern Atlantic (Brazil). In this area, the estuarine surface temperature is high, with a low interannual variability (27 to 34 °C) [37]. It is known as a semi-arid tropical region, where rainfall is scarce (500–1000 mm/per year) [38], with two distinct and well-defined periods: a rainy season (first half of the year, January–June) in which 90% of the precipitation occurs, while only 10% of the annual precipitation comes during the dry season (second half of the year, July-December) [39]. In the dry period—due to a combination of low rainfall, high insolation, high water residence time, and higher evaporation rates of low-latitude, shallow-water estuaries—the hypersaline condition (salinity higher than the sea) (e.g., >37 ppt) is an extreme and seasonal environmental feature [40]. The sampling was carried out in two localities 20 km apart from each other (Figure 1). In the first study area (Acaraú—2°49′59.12″ S/40°7′17.07″ W), the jellyfish C. andromeda were sampled inside the water canals of a shrimp farm (Sf) (Figure 1C). In the second area (Itarema—2°53′2.92″ S/39°54′41.95″ W), the jellyfish were sampled in a semi-enclosed, shallow-water estuary about 0.5–1 m depth, characterized by mangrove forests (M) and with no influence of shrimp farm activities (Figure 1D). Environmental parameters (temperature, salinity, and pH) as well as total nitrogen (TN) and phosphorous (TP) were measured for the two habitats [37] and are reported in Table 1. Sampling was carried out in July and October 2018 (dry period) and in January and April 2019 (rainy period).

2.2. Sample Collection and Preservation

Five C. andromeda specimens were collected for each survey (July 2018; October 2018; January 2019; April 2019) from the shrimp farm. In mangrove stations, the jellyfish population is subject to seasonality and thus specimens were found only in the dry period (n = 5 per survey). Measurements of the umbrella diameter were made using a caliper before body parts were separated to be used for biochemical analyses. The C. andromeda specimens used for this study ranged between 8 and 20 cm in diameter in both locations and during the different sampling times. All sampled specimens were then separated into oral arms, umbrella, and gonads for the study of biomarkers (carbohydrates, lipids, organic matter, FA) and for stable isotope (SI) analysis (Table 2). Immediately after excision, all body parts were frozen (−20 °C). After the freezing process, samples were lyophilized and ground into a fine powder using an agate mortar and pestle (ideal for smashing frozen samples) for biomarker analysis.

2.3. Biomarker Analysis

2.3.1. Organic Matter

Approximately ~7 mg of each sample (a total of 30 specimens considering the 3 different body parts; for the last sampling date in the Sf we used 3 samples for the gonads: n = 88) was weighed as DW (after drying for 48 h at 60 °C) and was burned in a muffle furnace for 5 h at 450 °C. Organic matter content (AFDW, i.e., ash-free dry weight) was then calculated as the difference between the DW and the ash weight [41]. AFDW was quantified for all the different body parts of all the specimens of the whole sampling period (n = 88, Table 2). AFDW was used to normalize lipid and carbohydrate data [18].

2.3.2. Total Carbohydrate Content

Total carbohydrate content was determined in the oral arms and umbrellas, where symbionts are mostly found. Oral arms and umbrellas (n = 5) were sampled for the shrimp farm (4 sampling dates) and the mangroves (2 sampling dates) (n = 60, Table 2). Approximately 6–7 mg of each sample DW was homogenized in 3 mL of distilled water following [42], adapted for cnidarians by [43]. (D)-Glucose was used as a standard and a calibration line was made prior to the sample’s analysis. Carbohydrate concentrations were expressed in µg carbohydrates/mg AFDW.

2.3.3. Total Lipid Content

The total lipid content was quantified in five samples of gonads, oral arms and umbrellas in two locations and on four sampling dates (n = 88, Table 2). For the last sampling date in the Sf we used only three samples for the gonads. Total lipid content was quantified following [18] for jellyfish. Approximately 20 mg of umbrellas, ~10 mg of oral arms and 5 mg of gonads DW were weighed with a precision balance. The tissue was ground and the powder was resuspended in 3 mL of chloroform:methanol (2:1) following [44] (colorimetry) transformed by [45]. A calibration line was made using cholesterol as a standard and the final reaction was performed using vanillin. Measurements were analyzed with a spectrophotometer (UV mini1240, Shimadzu, Kyoto, Japan). The lipid content was expressed in µg lipid/mg AFDW. The total fatty acids (FA) of jellyfish from the two habitats were analyzed only in the last sampling time (October) in which both populations were present due to a lack of DW from the July sampling; thus, the methodology and results are reported in the Supplementary Materials.

2.3.4. C:N Ratios, δ15N and δ13C Composition

Both stable isotope (δ15N and δ13C) composition and the carbon/nitrogen (C:N) mass ratio were assessed in three umbrella samples [46] collected at the shrimp farm and the mangrove estuarine ecosystem on each sampling date (n = 18, Table 2). Approximately 1.8–2 mg of DW was introduced in tin capsules to run each sample separately, and analyses were performed using the Elementar IsoPrime 100 isotope ratio–mass spectrometry (IR–MS) instrument (IsoPrime Ltd., Cheadle Hulme, UK) coupled to an N–C–S elemental analyzer (Elementar Vario Pyro Cube EA CNS; Elementar Analysensysteme GmbH, Hanau, Germany). The elemental analyzer combustion tube was at 1020 °C and the reduction tube was at 850 °C. Helium (He) was at 230 mL/min and O2 was at 35 mL/min. The CO2 sample gas stream was diluted with additional helium and the CO2 and N2 reference gases at 8 and 4 bars, respectively. The reference materials were Sulfanilamide for determination of elemental composition, Glucose (BCR-657) and Polyethylene (IAEA-CH-7) for determination of the stable carbon isotopic values (δ13C), and Potassium Nitrate (USGS32) and Ammonium Sulfate (USGS25) for determination of the stable nitrogen isotopic values (δ15N).
The δ13C and δ15N values were calculated relative to Peedee Belemnite (PDB) and Vienna Pee Dee Belemnite (VPDB) for carbon and atmospheric N2 (air), respectively, and expressed in the δ notation as parts per mille (‰).

2.3.5. Statistical Analysis

Data were tested for normal distribution by the Shapiro–Wilks test using Statistica 7.0 software. The whole dataset did not follow a normal distribution so stable isotopes, total carbohydrates and total lipids were analyzed using the nonparametric Mann–Whitney U test and Kruskal–Wallis test (Statistica 7.0 software) and also Dunn’s post hoc test (Past 4.03). Plots were generated using the “ggplot2” package.

3. Results

3.1. Organic Matter

The gonads showed the highest AFDW content (>60%) in all the sampling dates compared to the oral arms and umbrellas (Table 3). The AFDW from the gonads of C. andromeda jellyfish were significantly different between the shrimp farm and the mangroves (Kruskal–Wallis test: H = 14.46, p < 0.05). Dunn’s post hoc test (Supplementary Materials, Table S1) showed that the differences between the two places occurred in July and October (2018).

3.2. Total Carbohydrate Content

Overall, the Kruskal–Wallis test (H = 31.46, p < 0.05) and Dunn’s post hoc test showed some significant differences (Figure 2, Table S2). Considering each month independently, in July, oral arm carbohydrate content was significantly different between the mangroves and the shrimp farm (Figure 2; p < 0.05; Table S2). Carbohydrate concentrations in oral arms did not differ significantly in the shrimp farm over the sampling period (Figure 2). In October, tissue differences were observed in both the shrimp farm and the mangroves, while in July this was true only in the mangroves. The jellyfish carbohydrate content of umbrella tissue and oral arms in the mangroves exhibited significant differences between July and October (Figure S1).

3.3. Total Lipid Content

Throughout the surveys, there were significant differences in the lipid content of the gonad and umbrella tissues between the shrimp farm and the mangroves (Kruskal–Wallis test: Hgonads = 14.73 and Humbrella = 11.82, p < 0.05). The results of Dunn’s post hoc test are reported in Tables S3 and S4. The total lipid content of the gonads was higher in the shrimp farm during all the monitored period (Figure 3). In the umbrella tissues, the total lipid content was higher in the shrimp farm only in July (Figure 3). No significant differences were found in oral arm tissue throughout the sampling period.

3.4. Stable Isotopes Analysis and C:N Ratio

The isotopic δ13C values from umbrellas of C. andromeda jellyfish were significantly different between the shrimp farm and the mangroves (Kruskal–Wallis test: H = 14.59, p < 0.05) and ranged between −18.90 and −15.92‰ in the shrimp farm and between −19.75 and −17.61‰ in the mangroves. The results of the Dunn’s post hoc test (Table S5) showed differences between the two places in July and October (2018), with δ13C values significantly higher in jellyfish from the shrimp farm than those from the mangroves (Figure 4). There were no significant differences (Kruskal–Wallis test: H = 9.1, p > 0.05) between jellyfish from the two study areas in the δ15N proportions throughout the seasonal cycle with values ranging between 2.3 and 4.59‰ and between 2.41 and 4.55‰ in the shrimp farm and the mangroves, respectively (Figure 4 and Figure 5). Samples from different periods of the year and different locations showed clear separation into clusters (Figure S1).
C:N ratios (Figure 5 were significantly different between the shrimp farm (5.36 ± 0.2) and the mangroves (4.38 ± 0.09) in July. Over the sampling period they changed significantly in the shrimp farm from 5.36 ± 0.2 to 3.81 ± 0.05.

4. Discussion

In the present study, we used different trophic biomarkers to investigate the trophic ecology of the non-indigenous jellyfish Cassiopea andromeda, collected from an artificial aquaculture pond and a natural mangrove–estuarine habitat.

4.1. Nutritional Condition of Cassiopea andromeda

Within the different body compartments, gonads showed the highest amount of organic matter (AFDW) in both habitats and the difference between the two habitats was significant, with a higher lipid content in the shrimp farm. The environmental stability of the shrimp farm habitat, in terms of regular food supply for the white shrimp Litopenaeus vannamei, may be reflected by a nearly constant carbohydrate concentration in C. andromeda tissues over the year. In fact, despite the more remarkable fluctuations in salinity, nutrients, and temperature of the mangrove habitat [7,37], jellyfish tissues from mangroves revealed carbohydrate levels comparable to those from the shrimp farm medusae, except in July in the oral arms. This is the part of the jellyfish body with the highest density of microalgal symbionts [47], where higher quantities of photosynthates are produced and translocated to the host [24]. A higher level of translocation/production activity due to less turbid waters in the mangroves may explain the higher carbohydrate content in July. While carbohydrate content is nearly constant in all body compartments in the shrimp farm, in the mangroves it undergoes seasonal variations. In the oral arms it decreases from July to October, while in the umbrella we observe the opposite behavior; it increases from July to October, suggesting either a different rate of photosynthetic products in the two different tissues or a different allocation of resources that might be used for growth. The same behavior was observed for lipids in mangrove jellyfish, suggesting different energy allocation in different seasons. Compared to the specimens living in mangroves, a higher lipid content was detected throughout the whole study in the gonads of C. andromeda specimens from the shrimp farm. Individual jellyfish specimens of larger size were found throughout the year in the artificial structures (canals) of the shrimp farm, where the environmental conditions—forced by feed supply and aeration of the shrimp aquaculture farm—are more stable compared to the natural mangrove habitat ruled out by seasonal changes in environmental variables [37]. This is witnessed by the size of C. andromeda specimens, which is much larger in the shrimp farm (up to 49.2 cm of umbrella diameter) than in the mangroves (up to 26.7 cm in diameter) [37]. In shrimp farms, stable environmental conditions secure continuity of jellyfish growth throughout the year [7], paralleled by a high lipid storage in the gonads. The jellyfish disappeared just after the rainy season in the mangroves, whereas a stable jellyfish population with mature oocytes (as per [48]) was observed in the shrimp farm at the same time of the year [7]. Jellyfish growth could be promoted by increased nutrient availability [3,49] and the mixotrophic ability of Cassiopea spp. may modify benthic biogeochemical fluxes, acting as a sink of inorganic nutrients and affecting sediment microbial processes and oxygen consumption [50,51]. Surprisingly, [37] reported a higher amount of TN and TP in the mangrove estuarine system, where jellyfish specimens may achieve, on average, a smaller size. This may suggest that pulse inputs of high nutrient concentrations might not favorably sustain regular, i.e., vigorous jellyfish growth; conversely, a controlled and constant nutrient supply, such as on a shrimp farm, may be a better booster for jellyfish growth [49,52].

4.2. Trophic Strategy of Cassiopea andromeda

Cassiopea andromeda couples typical heterotrophic feeding based on zooplankton, POM (particulate organic matter), DOM (dissolved organic matter) and detritus, with an additional autotrophic energy supply from its endosymbiotic dinoflagellates [50,53,54]. In mixotrophic metazoans, stable isotope analysis and C:N ratios can contribute as nutritional indicators to unravel the predominant trophic strategy, as well as the nutrient exchanges between host and endosymbionts [15,55,56]. In our study, a significant difference was observed between the two environments, with δ13C values lower in jellyfish tissues from mangroves (July: Sf −19; M −20; October: Sf −16; M −18). This may be reflected by the carbon local sources utilized. In fact, Brazilian mangroves are characterized by a high quantity of nutrients and POM is primarily produced by mangrove detritus, which represents the dominant carbon source [57]. The shrimp farm water is enriched with OM, nutrients, and detritus due to the constant amount of feed necessary for the shrimps’ growth, which is eventually broken down along the food chain [58,59]. Jellyfish in the shrimp farm were more Carbon-enriched due to the different feed used for shrimp aquaculture in the study site [60,61,62]. Moreover, across the October, January, and April samplings, C. andromeda in the shrimp farm showed a general constancy in δ13C and δ15N values, underlying the maintenance of stable and controlled environmental conditions by the occurrence of the aquaculture facilities. However, regardless of the effort of the farm activities in buffering drastic seasonal changes, the prevalence of the trophic mode is still related to seasonal variations. As C:N ratios demonstrated, jellyfish in the shrimp farm seemed to move from an autotrophic–mixotrophic strategy (C:N 5.36 ± 0.23) to a more heterotrophic one at the end of the rainy season (C:N 3.81 ± 0.05). [15] reported a similar behavior in the symbiotic M. papua, where jellyfish populations showed instead different autotrophy/heterotrophy contributions based on the sampling location, in Palau [15].
The C. andromeda behavior may be due to a decrease in light intensity with the upcoming rainy season [39], but a constant presence of POM and nutrients is guaranteed in the shrimp farm. In specimens collected in mangroves, a shift in δ13C, from July (δ13C: −20‰) to October (δ13C: −18‰) was observed, together with a small increase in the C:N ratio and a significant decrease in δ15N values, suggesting a possible predominancy of autotrophy. This might be explained by less turbid, i.e., more transparent waters, related to increased light irradiance and enhanced photosynthesis of symbiotic dinoflagellates, thus increasing the δ13C value of the symbiotic association [63,64].

4.3. Why Did Cassiopea andromeda Disappear in the Mangroves?

Based on the measurements of carbohydrates and lipids conducted in this research, it appears that the steady availability of energy sources in various tissues enabled jellyfish in the shrimp farm to maintain a consistent energy supply for their growth and reproduction. We observed a higher proportion of saturated fatty acids in the shrimp farm jellyfish (SFAs = 46%) compared to the mangrove system jellyfish (SFAs = 35%) while a higher amount of polyunsaturated fatty acids (PUFAs) was found in the mangrove-related jellyfish. This may suggest a better quality in the origin of the food present in the estuary (C3 plants). However, due to the low number of samples, our data are not conclusive and additional studies are needed. As a result of Cassiopea’s nutritional condition, the jellyfish population is able to thrive and persist in this particular environment. On the contrary, jellyfish disappeared from the mangrove habitat at the end of the rainy season; the high turbidity of the water column during the concentrated rainfall of 2019 (546 mm/month, i.e., the largest monthly rainfall in 11 years) [37] reduced the amount of incoming light available for photosynthesis. Coupled with a drastic salinity decrease (24.4), high water turbidity may affect the autotrophic potential of Cassiopea, overshooting its adaptability to light conditions [14] and eventually leading to its seasonal disappearance from the natural mangrove habitat.

5. Conclusions

Disentangling the relative contribution of autotrophy and heterotrophy may be challenging in a symbiotic jellyfish such as Cassiopea andromeda. Here, we shed light on the differences in the nutrition mode in a natural vs. human-made environment. We show that C. andromeda seems strongly controlled by the seasonal variability of abiotic factors in the mangrove system, notwithstanding its ecophysiological plasticity and its mixotrophic potential. On the contrary, coastal systems modified for food production and subsidized by man-controlled inputs of energy and organic matter, such as shrimp aquaculture farms, may better support a stable jellyfish population. This suggests that human-controlled, modified coastal habitats may enforce the capability of C. andromeda to maintain populations in exotic areas, using artificial marinas and other coastal habitats as stepping stones for a worldwide bioinvasion.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/w15142599/s1, Figure S1: Plot of δ15N versus δ13C values of Cassiopea andromeda umbrella tissue; Table S1: Dunn’s post hoc of AFDW; Table S2: Dunn’s post hoc of total carbohydrates; Table S3: Dunn’s post hoc of total lipids in gonads; Table S4: Dunn’s post hoc of total lipid in umbrellas; Table S5: Dunn’s post hoc of isotope values; Table S6: List of C. andromeda gonad fatty acids.

Author Contributions

Conceptualization, S.R. and M.d.O.S.; methodology, S.R. and M.d.O.S.; formal analysis, M.M., J.T., T.M.G., A.P. and G.E.D.B.; investigation, M.M. and J.T.; resources, S.R., A.P. and G.E.D.B.; data curation, M.M.; writing—original draft preparation, M.M. and J.T.; writing—review and editing, all the authors; visualization, M.M.; supervision, S.P. and S.R.; project administration, S.R. and M.d.O.S.; funding acquisition, S.R. and M.d.O.S. All authors have read and agreed to the published version of the manuscript.

Funding

SR wants to thank to the XXXV Convocatòria Fons de Solidaritat de la UAB for the mobility program to Fortaleza (UAB-SOL 34566). MOS thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Research Productivity Fellowship 313518/2020-3), PELD Costa Semiárida do Brasil-CSB (No. 442337/2020-5), CAPES-PRINT, CAPES-Von Humboldt (AVH), and Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (Chief Scientist Program) for their financial support. Further support was provided to SP by the EU project number Project 101060072 “ACTNOW—Advancing understanding of Cumulative Impacts on European marine biodiversity, ecosystem functions and services for human wellbeing”.

Institutional Review Board Statement

All applicable international, national, and institutional guidelines for the care and use of animals were followed by the authors.

Data Availability Statement

Relevant data are contained within the article; raw data are available from the corresponding author M.M.

Acknowledgments

The authors want to thank Núria Viladrich, Andrea Gori (University of Barcelona), and Daniela Fico for technical support during the lipid, carbohydrate, and fatty acid analyses.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Purcell, J.E.; Uye, S.I.; Lo, W.T. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: A review. Mar. Ecol. Progr. Ser. 2007, 350, 153–174. [Google Scholar] [CrossRef]
  2. Bayha, K.M.; Graham, W.M. Nonindigenous Marine Jellyfish: Invasiveness, Invasibility, and Impacts. In Jellyfish Blooms; Pitt, K.A., Lucas, C.H., Eds.; Springer Science: Berlin/Heidelberg, Germany, 2014; Volume 3, pp. 45–77. [Google Scholar] [CrossRef]
  3. Stoner, E.W.; Archer, S.K.; Layman, C.A. Increased nutrient availability correlates with increased growth of the benthic jellyfish Cassiopea spp. Food Webs 2022, 31, e00231. [Google Scholar] [CrossRef]
  4. Peron, F.; Lesueur, C.A. Tableau des caractères generiques et specifiques de toutes les espèces de méduses connues jusqùà ce jour. Ann. Muséum D’histoire Nat. 1810, 14, 325–366. [Google Scholar]
  5. Holland, B.S.; Dawson, M.N.; Crow, G.L.; Hofmann, D.K. Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): Molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar. Biol. 2004, 145, 1119–1128. [Google Scholar] [CrossRef]
  6. Ohdera, A.H.; Abrams, M.J.; Ames, C.L.; Baker, D.M.; Suescún-Bolívar, L.P.; Collins, A.G.; Freeman, C.J.; Gamero-Mora, E.; Goulet, T.L.; Hofmann, D.K.; et al. Upside-Down but Headed in the Right Direction: Review of the Highly Versatile Cassiopea xamachana System. Front. Ecol. Devol. 2018, 6, 35. [Google Scholar] [CrossRef] [Green Version]
  7. Thé, J.; Gamero-Mora, E.; Silva, M.V.C.; Morandini, A.C.; Rossi, S.; Soares, M.O. Non-indigenous upside-down jellyfish Cassiopea andromeda in shrimp farms (Brazil). Aquaculture 2020, 532, 735999. [Google Scholar] [CrossRef]
  8. Cillari, T.; Andaloro, F.; Castriota, L. First documented record of Cassiopea cf andromeda (Cnidaria: Scyphozoa) in Italian waters. Cah. Biol. Mar. 2018, 59, 193–195. [Google Scholar] [CrossRef]
  9. Deidun, A.; Sciberras, A.; Formosa, J.; Zava, B.; Insacco, G.; Corsini-Foka, M.; Crandall, K.A. Invasion by non-indigenous freshwater decapods of Malta and Sicily, central Mediterranean Sea. J. Crustac. Biol. 2018, 38, 748–753. [Google Scholar] [CrossRef] [Green Version]
  10. Morandini, A.C.; Stampar, S.N.; Maronna, M.M.; Silveira, F.L. All non-indigenous species were introduced recently? The case study of Cassiopea (Cnidaria: Scyphozoa) in Brazilian waters. J. Mar. Biolog. Assoc. U. K. 2017, 97, 321–328. [Google Scholar] [CrossRef] [Green Version]
  11. Stampar, S.N.; Gamero-Mora, E.; Maronna, M.M.; Fritscher, J.M.; Oliveira, B.S.P.; Sampaio, C.L.S.; Morandini, A.C. The puzzling occurrence of the upside-down jellyfish Cassiopea (Cnidaria: Scyphozoa) along the Brazilian coast: A result of several invasion events? Zoologia 2020, 37, 1–10. [Google Scholar] [CrossRef]
  12. Mortillaro, J.M.; Pitt, K.A.; Lee, S.Y.; Meziane, T. Light intensity influences the production and translocation of fatty acids by zooxanthellae in the jellyfish Cassiopea sp. J. Exp. Mar. Bio. Ecol. 2009, 378, 22–30. [Google Scholar] [CrossRef]
  13. Verde, E.; McCloskey, L. Production, respiration, and photophysiology of the mangrove jellyfish Cassiopea xamachana symbiotic with zooxanthellae: Effect of jellyfish size and season. Mar. Ecol. Progr. Ser. 1998, 168, 147–162. [Google Scholar] [CrossRef] [Green Version]
  14. Mammone, M.; Ferrier-Pages, C.; Lavorano, S.; Rizzo, L.; Piraino, S.; Rossi, S. High photosynthetic plasticity may reinforce invasiveness of upside-down zooxanthellate jellyfish in Mediterranean coastal waters. PLoS ONE 2021, 16, e0248814. [Google Scholar] [CrossRef]
  15. Djeghri, N.; Pondaven, P.; le Grand, F.; Bideau, A.; Duquesne, N.; Stockenreiter, M.; Behl, S.; Huang, J.; Hansen, T.; Patris, S.; et al. High trophic plasticity in the mixotrophic Mastigias papua-Symbiodiniaceae holobiont: Implications for the ecology of zooxanthellate jellyfishes. Mar. Ecol. Progr. Ser. 2021, 666, 73–88. [Google Scholar] [CrossRef]
  16. Drazen, J.C.; Phleger, C.F.; Guest, M.A.; Nichols, P.D. Lipid, sterols and fatty acid composition of abyssal holothurians and ophiuroids from the north-east Pacific Ocean: Food web implications. Comp. Biochem. Physiol. 2008, 151, 79–87. [Google Scholar] [CrossRef] [PubMed]
  17. Kelly, J.R.; Scheibling, R.E. Fatty acids as dietary tracers in benthic food webs. Mar. Ecol. Progr. Ser. 2012, 446, 1–22. [Google Scholar] [CrossRef] [Green Version]
  18. Leal, M.C.; Ferrier-Pagès, C. Stable isotope as tracers of trophic interactions in marine mutualistic symbiosis. Ecol. Evol. 2018, 9, 723–740. [Google Scholar] [CrossRef]
  19. Milisenda, G.; Rossi, S.; Vizzini, S.; Fuentes, V.L.; Purcell, J.E.; Tilves, U.; Piraino, S. Seasonal variability of diet and trophic level of the gelatinous predator Pelagia noctiluca (Scyphozoa). Sci. Rep. 2018, 8, 12140. [Google Scholar] [CrossRef] [Green Version]
  20. Nagata, R.M.; Moreira, M.Z.; Pimentel, C.R.; Morandini, A.C. Food web characterization based on δ15N and δ13C reveals isotopic niche partitioning between fish and jellyfish in a relatively pristine ecosystem. Mar. Eco. Pro. Ser. 2015, 519, 13–27. [Google Scholar] [CrossRef]
  21. Purcell, J.E. Extension of methods for jellyfish and ctenophore trophic ecology to large-scale research. Hydrobiologia 2009, 616, 23–50. [Google Scholar] [CrossRef] [Green Version]
  22. Alfaro, A.C.; Thomas, F.; Sergent, L.; Duxbury, M. Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuar. Coast. 2006, 70, 271–286. [Google Scholar] [CrossRef]
  23. Calado, R.; Leal, M.C. Trophic Ecology of Benthic Marine Invertebrates with Bi-Phasic Life Cycles: What Are We Still Missing? In Advances in Marine Biology; Academic Press: Orlando, FL, USA, 2015; Volume 71, pp. 1–70. [Google Scholar] [CrossRef]
  24. Freeman, C.J.; Stoner, E.W.; Easson, C.G.; Matterson, K.O.; Baker, D.M. Symbiont carbon and nitrogen assimilation in the Cassiopea-Symbiodinium mutualism. Mar. Ecol. Progr. Ser. 2016, 544, 281–286. [Google Scholar] [CrossRef] [Green Version]
  25. Freeman, C.J.; Stoner, E.W.; Easson, C.G.; Matterson, K.O.; Baker, D.M. Variation in δ13C and δ15N values suggests a coupling of host and symbiont metabolism in the Symbiodinium-Cassiopea mutualism. Mar. Ecol. Progr. Ser. 2017, 571, 245–251. [Google Scholar] [CrossRef]
  26. Leal, M.C.; Ferrier-Pagès, C. Molecular trophic markers in marine food webs and their potential use for coral ecology. Mar. Genom. 2016, 29, 1–7. [Google Scholar] [CrossRef]
  27. Pitt, K.A.; Clement, A.L.; Connolly, R.M.; Thibault-Botha, D. Predation by jellyfish on large and emergent zooplankton: Implications for benthic pelagic coupling. Estuar. Coast. Shelf Sci. 2018, 76, 827–833. [Google Scholar] [CrossRef] [Green Version]
  28. Rossi, S.; Coppari, M.; Viladrich, N. Benthic-Pelagic Coupling: New Perspectives in the Animal Forests. In Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots; Rossi, S., Bramanti, L., Gori, A., Orejas, C., Eds.; Springer: Berlin/Heidelberg, Germany, 2017; pp. 855–886. [Google Scholar]
  29. Houlbrèque, F. Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J. Exp. Biol. 2004, 207, 1461–1469. [Google Scholar] [CrossRef] [Green Version]
  30. Ying, C.; Ying, W.; Jing, Z.; Na, W. Potential dietary influence on the stable isotopes and fatty acid compositions of jellyfish in the Yellow Sea. J. Mar. Biol. Assoc. U. K. 2012, 92, 1325–1333. [Google Scholar] [CrossRef]
  31. Brodeur, R.D.; Sugisaki, H.; Hunt, G.L., Jr. Increases in jellyfish biomass in the Bering Sea: Implications for the ecosystem. Mar. Ecol. Prog. Ser. 2002, 233, 89–103. [Google Scholar] [CrossRef] [Green Version]
  32. Milisenda, G. Ecophysiology, Trophic Ecology, Reproductive Biology and Bioenergetics of Pelagia noctiluca (Forskål, 1775). Ph.D. Thesis, Universitá del Salento, Lecce, Italy, 2014. [Google Scholar]
  33. Tilves, U.; Fuentes, V.L.; Milisenda, G.; Parrish, C.C.; Vizzini, S.; Sabatés, A. Trophic interactions of the jellyfish Pelagia noctiluca in the NW Mediterranean: Evidence from stable isotope signatures and fatty acid composition). Mar. Ecol. Progr. Ser. 2018, 591, 101–116. [Google Scholar] [CrossRef]
  34. Lacerda, L.D.; Borge, R.; Ferreira, A.C. Neotropical mangroves: Conservation and sustainable use in a scenario of global climate change. Aquat. Conserv. Mar. Freshw. Ecosyst. 2019, 29, 1347–1364. [Google Scholar] [CrossRef]
  35. Queiroz, L.; Rossi, S.; Meireles, J.; Coelho, J. Shrimp aquaculture in the state of Ceará during the period 1970–2012: Trends of the privatization of mangrove forest in Brazil. Ocean Coast. Manag. 2013, 73, 54–62. [Google Scholar] [CrossRef]
  36. Sousa, O.V.; Macrae, A.; Menezes, F.G.R.; Gomes, N.C.M.; Vieira, R.H.S.F.; Mendonça-Hagler, L.C.S. The impact of shrimp farming effluent on bacterial communities in mangrove waters, Ceará, Brazil. Mar. Pollut. Bull. 2006, 52, 1725–1734. [Google Scholar] [CrossRef]
  37. Thé, J.; Barroso, H.; Mammone, M.; Viana, M.; Melo, C.; Banha, T.; Mies, M.; Morandini, A.C.; Rossi, S.; Soares, M.O. Aquaculture facilities promote population stability throughout seasons and increase medusae size for the invasive jellyfish Cassiopea andromeda. Mar. Environ. Res. 2020, 162, 105161. [Google Scholar] [CrossRef] [PubMed]
  38. Soares, M.; Rossi, S.; Martins, F.; Carneiro, P. The forgotten reefs: Benthic assemblage coverage on a sandstone reef (Tropical South-western Atlantic). J. Mar. Biol. Assoc. U. K. 2017, 97, 1585–1592. [Google Scholar] [CrossRef]
  39. Soares, M.O.; Campos, C.C.; Carneiro, P.B.M.; Barroso, H.S.; Marins, R.V.; Teixeira, C.E.P.; Menezes, M.O.B.; Pinheiro, L.S.; Viana, M.B.; Feitosa, C.V.; et al. The Brazilian semi-arid coast in times of global environmental changes. Perspect. Ecol. Conserv. 2021, 19, 267–278. [Google Scholar] [CrossRef]
  40. Barroso, H.S.; Tavares, T.C.L.; Soares, M.O.; Garcia, T.M.; Rozendo, B.; Vieira, A.S.C.; Viana, B.; Pontes, T.M.; Ferreira, T.J.; Filho, J.P.; et al. Intra-annual variability of phytoplankton biomass and nutrients in a tropical estuary during a severe drought. Estuar. Coast. 2018, 213, 283–293. [Google Scholar] [CrossRef]
  41. Slattery, M.; Mcclintock, J.B. Population structure and feeding deterrence in three shallow-water antarctic soft corals. Mar. Biol. 1995, 122, 461–470. [Google Scholar] [CrossRef]
  42. Dubois, M.; Gilles, K.A.; Hamilton, J.K.; Rebers, P.A.; Smith, F. Colorimetric method for the determination of sugars and related substances. Anal. Chem. 1956, 28, 350–356. [Google Scholar] [CrossRef]
  43. Rossi, S.; Sabatés, A.; Latasa, M.; Reyes, E. Lipid biomarkers and trophic linkages between phytoplankton, zooplankton and anchovy (Engraulis encrasicolus) larvae in the NW Mediterranean. J. Plankton Res. 2006, 28, 551–562. [Google Scholar] [CrossRef] [Green Version]
  44. Barnes, H.; Blackstock, J. Estimation of lipids in marine animal tissues: Detailed investigation of the sulphophosphovanillin method for ‘‘total’’ lipids. J. Exp. Mar. Biol. Ecol. 1973, 2, 103–118. [Google Scholar] [CrossRef]
  45. Rossi, S.; Gili, J.M.; Coma, R.; Linares, C.; Gori, A.; Vert, N. Temporal variation in protein, carbohydrate, and lipid concentrations in Paramuricea clavate (Anthozoa, Octocorallia): Evidence for summer–autumn feeding constraints. Mar. Biol. 2006, 149, 643–651. [Google Scholar] [CrossRef]
  46. D’Ambra, I.; Carmichael, R.H.; Graham, W.M. Determination of δ13C and δ15N and trophic fractionation in jellyfish: Implications for food web ecology. Mar. Biol. 2014, 161, 473–480. [Google Scholar] [CrossRef]
  47. Lampert, K.P.; Bürger, P.; Striewski, S.; Tollrian, R. Lack of association between color morphs of the Jellyfish Cassiopea andromeda and zooxanthella clade. Mar. Ecol. 2012, 33, 364–369. [Google Scholar] [CrossRef]
  48. Mammone, M.; Bosch-Belmar, M.; Milisenda, G.; Castriota, L.; Sinopoli, M.; Allegra, A.; Falautano, M.; Maggio, T.; Rossi, S.; Piraino, S. Reproductive cycle and gonadal output of the Lessepsian jellyfish Cassiopea andromeda in NW Sicily (Central Mediterranean Sea). PLoS ONE 2023, 18, e0281787. [Google Scholar] [CrossRef]
  49. Stoner, E.W.; Yeager, L.A.; Sweatman, J.L.; Sebilian, S.S.; Layman, C.A. Modification of a seagrass community by benthic jellyfish blooms and nutrient enrichment. J. Exp. Mar. Biol. Ecol. 2014, 461, 185–192. [Google Scholar] [CrossRef]
  50. Welsh, D.T.; Dunn, R.J.K.; Meziane, T. Oxygen and nutrient dynamics of the upside-down jellyfish (Cassiopea sp.) and its influence on benthic nutrient exchanges and primary production. Hydrobiologia 2009, 635, 351–362. [Google Scholar] [CrossRef]
  51. Zarnoch, C.B.; Hossain, N.; Fusco, E.; Alldred, M.; Hoellein, T.J.; Perdikaris, S. Size and density of upside-down jellyfish, Cassiopea sp., and their impact on benthic fluxes in a Caribbean lagoon. Mar. Environ. Res. 2020, 154, 104845. [Google Scholar] [CrossRef]
  52. Todd, B.D.; Thornhill, D.J.; Fitt, W.K. Patterns of inorganic phosphate uptake in Cassiopea xamachana: A bioindicator species. Mar. Pollut. Bull. 2006, 52, 515–521. [Google Scholar] [CrossRef]
  53. Jantzen, C.; Wild, C.; Rasheed, M.; El-Zibdah, M.; Richter, C. Enhanced pore-water nutrient fluxes by the upside-down jellyfish Cassiopea sp. in a Red Sea coral reef. Mar. Ecol. Progr. Ser. 2010, 411, 117–125. [Google Scholar] [CrossRef]
  54. Pitt, K.A.; Connolly, R.M.; Meziane, T. Stable isotope and fatty acid tracers in energy and nutrient studies of jellyfish: A review. Hydrobiologia 2009, 616, 119–132. [Google Scholar] [CrossRef]
  55. Djeghri, N.; Stibor, H.; Lebeau, O.; Pondaven, P. δ13C, δ15N, and C:N ratios as nutrition indicators of zooxanthellate jellyfish: Insights from an experimental approach. J. Exp. Mar. Biol. Ecol. 2020, 522, 151257. [Google Scholar] [CrossRef]
  56. Phillips, D.L. Converting isotope values to diet composition: The use of mixing models. J. Mammal. 2012, 93, 342–352. [Google Scholar] [CrossRef] [Green Version]
  57. Giarrizzo, T.; Schwamborn, R.; Saint-Paul, U. Utilization of carbon sources in a northern Brazilian mangrove ecosystem. Estuar. Coast. Shelf Sci. 2011, 95, 447–457. [Google Scholar] [CrossRef]
  58. Junior, A.P.B.; Flickinger, D.L.; Henry-Silva, G.G. Sedimentation rates of nutrients and particulate material in pond mariculture of shrimp (Litopenaeus vannamei) carried out with different management regimes. Aquaculture 2021, 534, 736307. [Google Scholar] [CrossRef]
  59. Poersch, L.H.; Bauer, W.; Kersanach, M.W.; Wasielesky, W. Assessment of trace metals, total organic carbon and total nitrogen of a shrimp farm system in Southern Brazil. Reg. Stud. Mar. Sci. 2020, 39, 101452. [Google Scholar] [CrossRef]
  60. Barcellos, D.; Queiroz, H.M.; Nóbrega, G.N.; Filho, R.L.O.; Santaella, S.T.; Otero, X.L.; Ferreira, T.O. Phosphorus enriched effluents increase eutrophication risks for mangrove systems in northeastern Brazil. Mar. Pollut. Bull. 2019, 142, 58–63. [Google Scholar] [CrossRef]
  61. Marins, R.V.; Lacerda, L.D.; Araújo, C.S.; Fonseca, L.V.; Silva, F.A.T.F. Phosphorus and suspended matter retention in mangroves affected by shrimp farms effluents in NE Brazil. An. Acad. Bras. Ciênc. 2020, 92, e20200758. [Google Scholar] [CrossRef] [PubMed]
  62. Tacon, A.G.J.; Jory, D.; Nunes, A. Shrimp feed management: Issues and perspectives. In On-Farm Feeding and Feed Management in Aquaculture; Hasan, M.R., News, M.B., Eds.; FAO Fisheries and Aquaculture Technical Paper: Rome, Italy, 2013; pp. 481–488. [Google Scholar]
  63. Baker, D.M.; Kim, K.; Andras, J.P.; Sparks, J.P. Light-mediated 15N fractionation in Caribbean gorgonian octocorals: Implications for pollution monitoring. Coral. Reefs 2011, 30, 709–717. [Google Scholar] [CrossRef]
  64. Heikoop, J.M.; Dunn, J.J.; Risk, M.J.; Sandeman, I.M.; Schwartz, H.P.; Waltho, N. Relationship between light and the S15N of coral tissue: Examples from Jamaica and Zanzibar. Limnol. Oceanog. 1998, 43, 909–920. [Google Scholar] [CrossRef] [Green Version]
Water 15 02599 g001 550
Figure 1. Study area in the Cearà State (northeastern Brazil, SW Atlantic) (A) with highlights indicating sampling stations (B) in a shrimp farm (Acaraù) (C) and a mangrove-estuarine ecosystem (Itarema) (D).
Figure 1. Study area in the Cearà State (northeastern Brazil, SW Atlantic) (A) with highlights indicating sampling stations (B) in a shrimp farm (Acaraù) (C) and a mangrove-estuarine ecosystem (Itarema) (D).
Water 15 02599 g001
Water 15 02599 g002 550
Figure 2. Carbohydrate content (µg carbohydrates/mg AFDW) of C. andromeda (n = 60) in oral arm tissues and umbrellas from shrimp farm (Sf) and mangroves (M) in Ceará State (Brazil, SW Atlantic).
Figure 2. Carbohydrate content (µg carbohydrates/mg AFDW) of C. andromeda (n = 60) in oral arm tissues and umbrellas from shrimp farm (Sf) and mangroves (M) in Ceará State (Brazil, SW Atlantic).
Water 15 02599 g002
Water 15 02599 g003 550
Figure 3. Total lipid contents (µg lipid/mg AFDW) of Cassiopea andromeda in gonad, umbrella and oral arm tissues (n = 88) from shrimp farm and mangroves in Ceará State (Brazil, SW Atlantic).
Figure 3. Total lipid contents (µg lipid/mg AFDW) of Cassiopea andromeda in gonad, umbrella and oral arm tissues (n = 88) from shrimp farm and mangroves in Ceará State (Brazil, SW Atlantic).
Water 15 02599 g003
Water 15 02599 g004 550
Figure 4. Boxplot representing δ13C and δ15N values of C. andromeda umbrella tissue from shrimp farm (Sf) and mangroves (M) in Ceará State (Brazil, SW Atlantic). Sample size (n = 18).
Figure 4. Boxplot representing δ13C and δ15N values of C. andromeda umbrella tissue from shrimp farm (Sf) and mangroves (M) in Ceará State (Brazil, SW Atlantic). Sample size (n = 18).
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Water 15 02599 g005 550
Figure 5. C:N mass ratio of C. andromeda umbrella tissue from shrimp farm (Sf) and mangroves (M) in Ceará State (Brazil, SW Atlantic). Sample size (n = 18). In January and April (2019), no C. andromeda jellyfish were found in the mangrove ecosystem.
Figure 5. C:N mass ratio of C. andromeda umbrella tissue from shrimp farm (Sf) and mangroves (M) in Ceará State (Brazil, SW Atlantic). Sample size (n = 18). In January and April (2019), no C. andromeda jellyfish were found in the mangrove ecosystem.
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Table
Table 1. Environmental parameters adapted from [37].
Table 1. Environmental parameters adapted from [37].
Temperature °CpHSalinityTN (µM)TP (µM)
Shrimp farm27.8–31.57.9–8.431.6–46.213–420.3–1.8
Mangroves30.4–347.9–8.324.4–46.942–641.8–2.8
Table
Table 2. Summary of analysis performed on the upside-down jellyfish C. andromeda in contrasting coastal environments (shrimp farm and mangroves). N = number of samples; J = July; O = October; Ja = January; A = April; SF = shrimp farm; M = mangroves; U = umbrella; OA = oral arms; G = gonad. * For the last sampling date in the Sf we used only three samples for the gonads.
Table 2. Summary of analysis performed on the upside-down jellyfish C. andromeda in contrasting coastal environments (shrimp farm and mangroves). N = number of samples; J = July; O = October; Ja = January; A = April; SF = shrimp farm; M = mangroves; U = umbrella; OA = oral arms; G = gonad. * For the last sampling date in the Sf we used only three samples for the gonads.
AnalysisTotal NN Replicates/TreatmentMonth and AreaBody Part
Stable isotopes183J (SF, M); O (SF, M); Ja (SF); A (SF)U
Organic matter885 *J (SF, M); O (SF, M); Ja (SF); A (SF)U, OA, G
Carbohydrates605J (SF, M); O (SF, M); Ja (SF); A (SF)U, OA
Lipids885 *J (SF, M); O (SF, M); Ja (SF); A (SF)U, OA, G
Fatty acids105O (SF, M)G
Table
Table 3. Organic matter content (%) in specimens from the shrimp farm (Sf) and mangroves (M) in different body compartments (umbrella, oral arms and gonads) during the sampling periods. Data represent mean ± SD.
Table 3. Organic matter content (%) in specimens from the shrimp farm (Sf) and mangroves (M) in different body compartments (umbrella, oral arms and gonads) during the sampling periods. Data represent mean ± SD.
LocationMonthUmbrella (%)Oral Arms (%)Gonads (%)
SfJul39 ± 240 ± 378 ± 7
MJul39 ± 448 ± 263 ± 6
SfOct46 ± 1342 ± 777 ± 1
MOct52 ± 1537 ± 779 ± 4
SfJan28 ± 228 ± 579 ± 3
MJanabsentabsentabsent
SfApr41 ± 444 ± 769 ± 1
MAprabsentabsentabsent
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Thé, J.; Mammone, M.; Piraino, S.; Pennetta, A.; De Benedetto, G.E.; Garcia, T.M.; de Oliveira Soares, M.; Rossi, S. Understanding Cassiopea andromeda (Scyphozoa) Invasiveness in Different Habitats: A Multiple Biomarker Comparison. Water 2023, 15, 2599. https://doi.org/10.3390/w15142599

AMA Style

Thé J, Mammone M, Piraino S, Pennetta A, De Benedetto GE, Garcia TM, de Oliveira Soares M, Rossi S. Understanding Cassiopea andromeda (Scyphozoa) Invasiveness in Different Habitats: A Multiple Biomarker Comparison. Water. 2023; 15(14):2599. https://doi.org/10.3390/w15142599

Chicago/Turabian Style

Thé, Jorge, Marta Mammone, Stefano Piraino, Antonio Pennetta, Giuseppe Egidio De Benedetto, Tatiane Martins Garcia, Marcelo de Oliveira Soares, and Sergio Rossi. 2023. "Understanding Cassiopea andromeda (Scyphozoa) Invasiveness in Different Habitats: A Multiple Biomarker Comparison" Water 15, no. 14: 2599. https://doi.org/10.3390/w15142599

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