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Article

Temperature-Dependent Food Consumption Rates of the Sea Urchin Mesocentrotus nudus and Top Shell Turbo sazae: Potential Impacts on Seaweed Beds

by
Jaehwan Seo
1 and
Bon Joo Koo
1,2,*
1
East Sea Environment Research Center, Korea Institute of Ocean Science & Technology (KIOST), Uljin 36315, Republic of Korea
2
School of Ocean Science, University of Science and Technology, Daejeon 34113, Republic of Korea
*
Author to whom correspondence should be addressed.
Animals 2023, 13(22), 3436; https://doi.org/10.3390/ani13223436
Submission received: 5 October 2023 / Revised: 4 November 2023 / Accepted: 6 November 2023 / Published: 7 November 2023
(This article belongs to the Section Aquatic Animals)
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Abstract

:

Simple Summary

Despite the expansion of barren grounds and a change in the habitats of macrograzers brought about by rising water temperatures linked to climate change, there is a lack of information regarding how this habitat alteration and grazing by macrograzers affect seaweed beds. This study assessed which species, sea urchin and top shell, would have a more significant influence on seaweed beds if the current trend of increasing water temperature continues. Our results suggest that top shell has a greater potential to cause barren ground and thus poses a greater threat than sea urchin.

Abstract

In Korea, the expansion of barren ground and a shift in macrograzer habitats due to increasing water temperatures associated with climate change are becoming increasingly problematic. This study assessed the potential effects of the sea urchin Mesocentrotus nudus and top shell Turbo sazae on seaweed beds by examining changes in their food consumption rates in response to changes in temperature. The food consumption rates of kelp (Saccharina japonica) for both species were estimated at 5 °C, 10 °C, 15 °C, 20 °C, and 25 °C in laboratory experiments. The rate for M. nudus increased with increasing water temperature, with the highest rate of 0.001 g g−1 d−1 at 15 °C and 20 °C, and the lowest at 25 °C, which killed some individual sea urchins. The rate for T. sazae also increased with increasing water temperature, with the highest being 0.087 g g−1 d−1 at 25 °C and the lowest being at 5 °C. T. sazae had a higher food consumption rate than M. nudus at all temperatures; as water temperature increased, the difference between species increased, with the largest difference occurring at 25 °C. These findings indicate that as water temperature increases, T. sazae places greater feeding pressure on macroalgae than M. nudus.

1. Introduction

Urchin barren grounds are benthic communities on rocky reefs that are predominantly inhabited by herbivorous sea urchins and coralline red algae and that lack seaweed [1]. These barrens typically occur in areas capable of supporting kelp beds, which are highly productive, providing habitat and food sources for numerous ecologically and commercially significant fish and invertebrate species [2,3,4]. Over the past four decades, a shift from kelp beds to sea urchin barrens has been extensively documented along temperate coastlines worldwide [5,6,7,8]. In Korea, barrens initially emerged domestically in localized areas during the 1960s and 1970s [9,10], and their area of occurrence has been continuously expanding since then. Since the first reported occurrence of extensive barrens covering 370 ha in 1997, such areas have expanded significantly, reaching 2413 ha in 2003–2004 and a staggering 10,518 ha in 2014 along the eastern coast of Korea. Consequently, barrens are becoming an increasingly serious problem that affects 62% of the entire rock mass area of 170,054 ha [11].
High densities of herbivores, particularly sea urchins in the family Strongylocentrotidae, play a major role in the development of barren states in subtidal ecosystems [12,13,14,15]. In particular, the sea urchin Mesocentrotus nudus (formerly known as Strongylocentrotus nudus) is ecologically significant in coastal areas worldwide. This species is found in subtidal rocky regions across East Asia, including locations such as Dalian in China, the Maritime Territory of Russia, and the East Sea around Korea and Japan. This species is dominant in subtidal rocky habitats in Korea and typically favors brown algae such as Saccharina longissima, S. japonica, and Undaria pinnatifida as food resources [16,17,18]. Considering its high food consumption rate and population density, M. nudus has a substantial grazing impact on seaweed beds. This species is thought to be a significant contributor to the formation of barrens due to the overlap between its distribution and areas where seaweed has been depleted [19,20].
Since the mid-1970s, awareness of global climate change has increased; in particular, the impacts of increasing global seawater temperatures on ecological functions of marine species, such as range expansion or contraction and local extinction, have become clear [21,22,23]. The seas around the Korean Peninsula are some of the most vulnerable to climate change, as they are currently undergoing a rapid increase in seawater temperature [24]. Because Korean marine ecosystems extend from the sub-tropical to sub-arctic zones, a variety of marine organisms have likely shifted their geographical distributions poleward with recent global climate change [25]. In particular, during the past half century, increases in mean water temperature of nearly 1.7 °C have been reported in the East/Japan Sea, 1.4 °C in the Korea Strait, and 0.3 °C in the Yellow Sea [26].
Temperature influences the metabolism of marine ectotherm species and can thereby impact their behavior and reproductive success [27,28,29]. Many biological processes directly related to metabolic rates exhibit a unimodal performance curve when assessed across a suitable temperature range [30,31,32]. Within the temperature range of 0 °C to 40 °C, metabolic rates of ectotherms first increase almost proportionally with temperature, and then decrease rapidly above a critical temperature [27,31,32]. Furthermore, at higher water temperatures, marine ectotherms face reduced oxygen concentrations, limiting their capacity to feed or reproduce [32,33].
The Korean top shell, Turbo sazae, is a marine gastropod that inhabits sub-tropical rocky subtidal environments with water temperatures of 20 °C to 25 °C. This species is predominantly found in regions influenced by the Kuroshio–Tsushima current in the northwestern Pacific [34,35,36,37]. T. sazae has long been included within Turbo cornutus [38]. However, Fukuda [39] proposed that T. cornutus should refer only to populations that are native to southern China and Taiwan, designating the Japanese/Korean populations as a distinct species, T. sazae. Historically, T. sazae was primarily found along the coast of Jeju in Korean waters, with secondary populations along the coast of Busan [40]. Recent shifts in oceanographic conditions driven by climate change have led to northward expansion of the habitat range of T. sazae, from 35° N in 2010 to beyond the 37° N line in 2016, covering a distance of 124 km in just 6 years [41]. However, information about the effects of this habitat expansion and feeding by T. sazae on seaweed beds remains limited.
This study evaluated the potential impacts of the sea urchin M. nudus and top shell T. sazae on seaweed beds based on changes in their food consumption rates in response to changing temperature.

2. Materials and Methods

2.1. Animal Preparation

We obtained 50 sea urchins from the Imwon harbor fishery market in Samcheok, Korea, in September 2022. All individuals were immediately placed into containers filled with seawater and transported to the laboratory. Upon arrival, they were moved to aerated 60 L aquaria maintained at 15 °C. After 1 day, we selected 15 individuals exhibiting high mobility, rigid and upward-facing spines, and ambulacral feet that could adhere strongly to surfaces, thereby avoiding common signs of stress or disease. Each individual was transferred to an independent experimental unit and acclimated to the experimental temperature (5 °C, 10 °C, 15 °C, 20 °C, and 25 °C) without feeding for 5 days. The diameter and wet weight of each individual were measured immediately before and after the feeding assay.
In October 2022, 50 top shells were acquired from the fishery market at the Jukbyeon harbor in Uljin, Korea. The top shells were acclimated using the same method as sea urchins. The shell height and wet weight of each individual were measured immediately before and after the feeding assay. We selected a certain size of both species for the tests.

2.2. Experimental System

We manipulated seawater temperature using five main tanks from 5 °C to 25 °C at a 5 °C interval, and seawater was circulated from each main tank into three independent experimental units. A water pump and agitator were installed within each main tank to ensure homogenous mixing of the water in the main tanks and thus avoid the formation of temperature gradients. To adjust the water temperature, each main tank was equipped with electric heating and cooling units, which were controlled with electric temperature regulators. The regulators allowed the water temperature to be adjusted by a minimum interval of 0.2 °C. A temperature logger was placed within each main tank for continuous monitoring. A schematic diagram of the experimental system used for the feeding assay is presented in Figure 1.
The sea urchins and top shells were assigned to experimental units, each holding one individual of each species. These units were constructed of transparent polycarbonate (20 cm width × 30 cm height × 20 cm depth) with inflow and outflow holes at the top to maintain a constant water volume of 20 L. The experimental system was set up within a constant temperature and humidity chamber maintained at a temperature of 15 °C with a photoperiod of 12 h of light and 12 h of darkness.
Prior to the feeding assay, the sea urchins and top shells were acclimated to laboratory conditions for 1 day. During this time, they were kept at the sea surface temperature recorded during collection. Then, the water temperature was gradually increased or decreased at a rate of 5 °C per day for 3 days until the target temperature was reached. All animals were kept at the target water temperatures for 2 days, and were starved during the acclimation period.

2.3. Nutrient Analysis

Seawater samples were collected every 24 h from the main tank, transferred to polypropylene tubes, and stored at −80 °C for preservation. The concentrations of phosphate, nitrate, and nitrite were analyzed using a continuous flow analyzer (QuAAtro, SEAL Analytical, Mequon, WI, USA).

2.4. Feeding Assay and Consumption Rates

During the feeding assay, which lasted for 5 days, the sea urchins and top shells were fed kelp (S. japonica) of a specific size and weight (10 cm × 10 cm; wet weight: approximately 10 g). The kelp provided as food was replaced with fresh kelp every 24 h and this process was repeated over the entire feeding assay period. Additionally, three pieces of kelp were maintained as controls in the absence of animals to assess possible autogenic changes in kelp weight due to degradation or water saturation. The amount of kelp consumed by the sea urchins and top shells was determined based on the difference in the wet weight of kelp before and after the feeding assay, which was adjusted according to the change in kelp wet weight of controls. Then, we standardized the wet weight of consumed kelp to the wet weight of the animal and the duration of the feeding assay using the following equation:
Food consumption rate = wet weightkelp consumed [mg]/(wet weightanimal [g] × time [d])

2.5. Statistical Analysis

Differences in the diameter and wet weight of sea urchins, and in shell height and wet weight of top shells, before and after the feeding assay were determined using a two-sample t-test. The results were considered statistically significant at p < 0.05. A one-way analysis of variance (ANOVA) with Tukey’s post-hoc test was used to assess differences in these measurements as well as food consumption rates at each temperature. All statistical analyses were performed using SYSTAT software (Systat version 12.0, SPSS Inc., Chicago, IL, USA).

3. Results

3.1. Comparison of Morphometric Data

The mean diameter and mean wet weight of M. nudus and T. sazae prior to the feeding assay showed no significant differences among temperatures (Table 1 and Table 2). The values for M. nudus only differed at 25 °C (Table 3). On the third day of the feeding assay at 25 °C, two sea urchins died in two experimental units, whereas no mortality of T. sazae was observed at any temperature. The values for T. sazae did not significantly differ before/after feeding or among temperatures (Table 4).

3.2. Seawater Nutrients

The phosphate concentration in M. nudus treatments at 5 °C slightly decreased on the second day, followed by a slight increase on the fourth day and a sharp decrease on the fifth day, whereas it gradually decreased until the fourth day and then increased on the fifth day at 10 °C (Figure 2). It showed decreasing trends until the fourth day at 15 °C, 20 °C, and 25 °C, followed by rapid increases on the fifth day. The nitrite concentration gradually increased at all temperatures except 5 °C, while the nitrate concentration showed a consistent decreasing tendency over time.
In T. sazae, phosphate concentrations fluctuated until the fourth day at all temperatures except 25 °C, and rapidly increased on the fifth day at all temperatures (Figure 3). A rapid increase in nitrite was observed on the fifth day at all temperatures, while the nitrate concentration showed a fluctuating pattern with repeated decreases and increases.

3.3. Food Consumption Rates

Variation in food consumption rates was observed in both M. nudus and T. sazae in response to changes in water temperature (Figure 4 and Figure 5). The mean rate per individual was highest at 15 °C, followed by 20 °C, 10 °C, 5 °C, and 25 °C. Meanwhile, the rate per unit biomass was highest at 15 °C and 20 °C, followed by 10 °C, 5 °C, and 25 °C.
For T. sazae, the rate increased with increasing water temperature. The rate per individual was highest at 25 °C, followed by 20 °C, 15 °C, 10 °C, and 5 °C; it showed a similar trend per unit biomass. These results indicate that M. nudus had a higher mean food consumption rate per individual at 15 °C and 20 °C than T. sazae, whereas the reverse pattern was observed at 25 °C; however, the rate per unit biomass was higher in T. sazae than in M. nudus at all temperatures, and the difference between the two species increased as temperature increased (Table 5).

4. Discussion

Differences in body size and body mass among macrograzers are important factors that influence their food consumption due to corresponding differences in energetic requirements and metabolic demands [42,43,44]. The mean diameter and wet weight of M. nudus and T. sazae did not significantly differ before and after the feeding assay or among temperatures before the assay. Thus, we assumed that factors such as body size and biomass did not influence the food consumption rate of either species.
Böttger et al. [45] reported that the food consumption rate and feces production of another sea urchin, Lytechinus variegatus, decreased with increasing phosphate concentration, particularly above 0.8 mg L−1. On the other hand, an increase in food consumption by the sea urchin Loxechinus albus was observed with increasing phosphate concentration, suggesting that the effect of phosphate concentration on food consumption is species-specific [46]. Nitrate and nitrite are toxic to invertebrates, as they hinder the capacity of pigments to carry oxygen [47,48]. In addition, increases in their concentrations have been shown to lower the amount of food eaten by other gastropods [49]. Basuyaux and Mathieu [50] reported that the food consumption rate of the sea urchin Paracentrotus lividus significantly decreased when nitrate and nitrite concentrations exceeded 100 mg L−1 and 2 mg L−1, respectively. Over the entire feeding assay period of our study, these concentrations did not exceed those levels, suggesting that the food consumption rate of M. nudus was not influenced by these substances.
In T. sazae, the nitrite concentrations rapidly increased on the fifth day at all temperatures, reaching 13 mg L−1 at 25 °C, higher than the levels observed in M. nudus treatments (Figure 3). The feces of gastropods may contain high nitrogen levels due to low assimilation efficiencies for certain food sources [51]. Thus, we ascribed this change in nitrite to dissolution from feces. Watson et al. [52] reported that nitrite tolerance is species-specific, with species of the genus Turbo having higher tolerance to nitrite than other genera. They reported that mortality of two turbinid gastropods, Tectus fenestratus and Tegula eiseni, was observed at low concentrations, whereas no adverse effects were observed in Turbo bruneus at concentrations up to 5 mg L−1. In our study, the nitrite levels exceeded 5 mg L−1 on the fifth day at all temperatures, suggesting that food consumption may have been affected by excess nitrite. However, because nitrite tolerance varies among species [47,49,52], the concentration that impacts the food consumption rate of this species remains unclear. Therefore, further research is needed to assess the effects of seawater nutrient concentrations on the food consumption rates of T. sazae.
Regarding mortality, in M. nudus, there were no deaths except at 25 °C, consistent with a previous study that reported no mortality at a temperature range of 5–24 °C [53]. The food consumption rate of this species gradually increased from 5 °C to 15 °C, remained relatively constant from 15 °C to 20 °C, and then sharply decreased at 25 °C, in line with a previous study [54]. Thus, the rates were lowest at 5 °C and 25 °C, which may be attributable to limitations of effective grazing behaviors (i.e., the use of tube feet and spines to capture food and the lantern to grasp and masticate), reduced activity of digestive enzymes, and decreased nutrient absorption under conditions of temperature-induced stress [55,56,57,58]. Our findings suggest that the optimal temperature range for food consumption by M. nudus is between 15 °C and 20 °C. In contrast to M. nudus, no mortality of T. sazae was observed during the experiment. T. sazae is a sub-tropical species found in subtidal habitats with water temperatures of 14 °C to 25 °C [35,37], which suggests that it can withstand higher temperatures than M. nudus. In our study, it showed a gradual increase in the food consumption rate with an increase in temperature, with a peak at 25 °C. In such gastropods, increases in temperature lead to higher metabolic demand, thus increasing food consumption [59,60,61,62]. For example, the rate of Turbo samaticus gradually increases with increasing temperature, peaking at 25 °C [63]; in Haliotis midae, the rate doubles at 15 °C compared to 22 °C [64]. Furthermore, the oxygen consumption of T. sazae (T. cornutus) showed a gradual increase with increasing temperature, peaking at 30 °C, after which it rapidly declines [65]. Therefore, we conclude that this is the case in T. sazae. Such temperature-related changes in food consumption differed between the two species we studied. M. nudus had its highest food consumption rates at 15 °C and 20 °C, whereas T. sazae peaked at 25 °C. In addition, the difference in rate per unit biomass widened with increasing temperature. This suggests that as water temperature increases, T. sazae exerts greater feeding pressure on macroalgae than M. nudus. However, the feeding rates of macrograzers are also influenced by various factors other than temperature, including size, biomass, density, and food preference.
Because metabolic energy demands increase more rapidly with increasing body size than the amount of energy that can be supplied via consumption, and this mismatch is enhanced at elevated temperatures, the food consumption rates of sea urchins decrease as their size increases [32,44]. In contrast, the food consumption rates of turbinid gastropods show positive correlations with size, biomass, and density [42,66]. Food preference is one of the most important factors determining the food consumption rates of macrograzers. Yang et al. [20] reported that M. nudus preferred the brown alga U. pinnatifida, followed by Grateloupia elliptica and Sargassum confusum, with the consumption rate of the former being approximately double those of the other two. The high absorption efficiency of brown kelp by sea urchins is due to a high level of digestive enzymes for depolymerization of alginic acid and mannitol [67,68]. In contrast to sea urchins, turbinid gastropods have a preference for blue-green algae. For example, Turbo marmoratus primarily eats Lyngbya and Rivularia species, followed by coralline algae such as Melobesioideae and Jania species [69]. Despite the high abundance of the brown alga Dictyopteris undulata in its habitat, it does not consume it due to defensive chemicals such as sulfur compounds [20,69]. Hence, M. nudus and T. sazae probably have different preferred food sources.
Previous feeding conditions and changes in temperature can alter the food preferences of macrograzers; they tend to prefer foods that are different from what they have already consumed. For example, in one study, when M. nudus was starved before feeding, they preferred U. pinnatifida; in contrast, when fed this species and then tested, they preferred G. elliptica [20]. In another study, the green sea urchin Strongylocentrotus droebachiensis preferred S. latissima over Codium fragile but this changed depending on past feeding conditions [70]. They attributed the shift in preference to the benefits of a mixed diet, a need for different nutrients, and an attempt to avoid the accumulation of defensive chemicals [71,72,73,74,75]. The food preference of the turbinid gastropod T. sarmaticus is influenced by changes in temperature [63]. In the cited study, among six algal diets tested, T. sarmaticus consumed more Ulva rigida at 15 °C but more Corallina at 20 °C and 25 °C. The higher specific consumption rates may well equally be a result of compensation by T. sarmaticus for the lower digestibility of these algae. With all of this in mind, our study may be limited in that we offered only one species of food and thus our results may be overestimates or underestimates. Further research is required to determine the precise food consumption rates of these two species while considering their different food preferences.
The sea urchin M. nudus is one of the most abundant macrograzer species along the eastern coast of Korea, with population densities of 1 to 12 ind−1 m−2 [76]. It is believed to significantly contribute to the formation of barren ground due to overlap between its distribution and areas where seaweed has been depleted [19,20]. Recently, the habitat of T. sazae has expanded northward as seawater temperature has increased due to climate change; its population density has also increased [41]. However, information about the impacts of feeding by this species on seaweed beds remains limited. Our findings suggest that if the current trend of increasing water temperature continues, the potential impact of T. sazae on seaweed beds may become greater than the threat from M. nudus.

5. Conclusions

We evaluated changes in the food consumption rates of the sea urchin M. nudus and top shell T. sazae with changes in temperature. T. sazae had a higher consumption rate than M. nudus at all temperatures and the difference between species became wider as temperature increased. Given the ongoing range expansion of T. sazae due to increasing water temperature, our findings indicate that this species has a greater potential to cause barren ground and thus poses a greater threat than M. nudus. However, our study had limitations, as we did not consider various factors that may influence the feeding rates of both species. Nonetheless, our findings could help inform management plans for seaweed beds and strategies for restoration of barren grounds.

Author Contributions

Conceptualization, B.J.K.; formal analysis, B.J.K. and J.S.; investigation, B.J.K. and J.S.; data curation, B.J.K. and J.S.; writing—original draft preparation, B.J.K. and J.S.; writing—review and editing, B.J.K. and J.S.; supervision, B.J.K.; funding acquisition, B.J.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the project “Development of original technology to verify factors influencing barren ground on the East Sea coast according to climate change (PEA0116)” funded by the Korea Institute of Ocean Science and Technology.

Institutional Review Board Statement

Ethical review and approval were waived for this study due to the IACUC (Institutional Animal Care and Use Committee) guideline of Korea, which states that experiments that do not use biological objects or use plants, bacteria, protozoans, and invertebrates, which are not subject to law under the current law, do not require deliberation and approval from the committee.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Pearse, J.S.; Clark, M.E.; Leighton, D.L.; Mitchell, C.T.; North, W.J. Marine waste disposal and sea urchin ecology. In Kelp Habitat Improvement Project, California Annual Report, 1969 to 1970; North, W.J., Ed.; California Institute of Technology: Pasadena, CA, USA, 1970; pp. 1–93. [Google Scholar]
  2. Konar, B.; Estes, J.A. The stability of boundary regions between kelp beds and deforested areas. Ecology 2003, 84, 174–185. [Google Scholar] [CrossRef]
  3. Ling, S.D. Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: A new and impoverished reef state. Oecologia 2008, 156, 883–894. [Google Scholar] [CrossRef] [PubMed]
  4. Bonaviri, C.; Gianguzza, P.; Pipitone, C.; Hereu, B. Micropredation on sea urchins as a potential stabilizing process for rocky reefs. J. Sea. Res. 2012, 73, 18–23. [Google Scholar] [CrossRef]
  5. Sala, E.; Boudouresque, C.F.; Harmelin-Vivien, M. Fishing, trophic cascades and the structure of algal assemblages; evaluation of an old but untested paradigm. Oikos 1998, 82, 425–439. [Google Scholar] [CrossRef]
  6. Pinnegar, J.K.; Polunin, N.V.C.; Francour, P.; Badalamenti, F. Trophic cascades in benthic marine ecosystems: Lessons for fisheries and protected-area management. Environ. Conserv. 2000, 27, 179–200. [Google Scholar] [CrossRef]
  7. Steneck, R.S.; Graham, M.H.; Bourque, B.J.; Corbett, D.; Erlandson, J.M.; Estes, J.A.; Tegner, M.J. Kelp forest ecosystems: Biodiversity, stability, resilience and future. Environ. Conserv. 2002, 29, 436–459. [Google Scholar] [CrossRef]
  8. Filbee-Dexter, K.; Scheibling, R.E. Hurricane-mediated defoliation of kelp beds and pulsed delivery of kelp detritus to offshore sedimentary habitats. Mar. Ecol. Prog. Ser. 2012, 455, 51–64. [Google Scholar] [CrossRef]
  9. Kang, J.W. Illustrated Encyclopedia of Fauna & Flora of Korea, Volume 8. Marine Algae; Ministry of Education: Seoul, Republic of Korea, 1968; 465p. [Google Scholar]
  10. KORDI. A Preliminary Marine Ecological Study for Gojeong-Ri Power Plant Site; BSPI 00014-14-3; Korea Ocean Research & Development Institute: Ansan, Republic of Korea, 1978; 138p. [Google Scholar]
  11. FIRA. Barren Grounds Spreads over 60% in Bedrock on the East Sea; Press Release; FIRA: Busan, Republic of Korea, 15 July 2015. [Google Scholar]
  12. Elner, R.W.; Vadas, R.L., Sr. Inference in ecology: The sea urchin phenomenon in the northwestern Atlantic. Am. Nat. 1990, 136, 108–125. [Google Scholar] [CrossRef]
  13. Dayton, P.K.; Tegner, M.J.; Parnell, P.E.; Edwards, P.B. Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecol. Monogr. 1992, 62, 421–445. [Google Scholar] [CrossRef]
  14. Pearse, J.S. Ecological role of purple sea urchins. Science 2006, 314, 940–941. [Google Scholar] [CrossRef]
  15. Agnetta, D.; Bonaviri, C.; Badalamenti, F.; Scianna, C.; Vizzini, S.; Gianguzza, P. Functional traits of two cooccurring sea urchins across a barren/forest patch system. J. Sea Res. 2013, 76, 170–177. [Google Scholar] [CrossRef]
  16. Machiguchi, Y.; Mizutori, S.; Sanbonsuga, Y. Food preference of sea urchin Strogylocentrotus nudus in laboratory. Bull. Hokkaido Natl. Fish. Res. Inst. 1994, 58, 35–43. [Google Scholar]
  17. Kawamata, S. Modelling the feeding rate of the sea urchin Strongylocentrotus nudus (A. agassiz) on kelp. J. Exp. Mar. Biol. Ecol. 1997, 210, 107–127. [Google Scholar] [CrossRef]
  18. Kim, S.K.; Kim, Y.D.; Jeon, C.Y.; Gong, Y.G.; Kim, D.S.; Kim, J.H.; Kim, M.L.; Han, H.K. Algal consumption and preference of sea urchins, Strongylocentrotus nudus, S. intermedius and abalone, Haliotis discus hannai. J. Korean Fish. Soc. 2007, 40, 133–140. [Google Scholar]
  19. Yoo, J.W.; Kim, H.J.; Lee, H.J.; Lee, C.G.; Kim, C.S.; Hong, J.S.; Hong, J.P.; Kim, D.S. Interaction between invertebrate grazers and seaweeds in the East Coast of Korea. J. Korean Soc. Oceanogr. 2007, 12, 125–132. [Google Scholar]
  20. Yang, K.M.; Jeon, B.H.; Kim, H.G.; Kim, J.H. Feeding behaviors of a sea urchin, Mesocentrotus nudus, on six common seaweeds from the east coast of Korea. Algae 2021, 36, 51–60. [Google Scholar] [CrossRef]
  21. Poloczanska, E.S.; Hawkins, S.J.; Southward, A.J.; Burrows, M.T. Modeling the response of populations of competing species to climate change. Ecology 2008, 89, 3138–3149. [Google Scholar] [CrossRef]
  22. Hawkins, S.; Sugden, H.; Mieszkowska, N.; Moore, P.; Poloczanska, E.; Leaper, R.; Herbert, R.J.; Genner, M.; Moschella, P.; Thompson, R. Consequences of climate-driven biodiversity changes for ecosystem functioning of North European rocky shores. Mar. Ecol. Prog. Ser. 2009, 396, 245–259. [Google Scholar] [CrossRef]
  23. Noke, R. What Is Driving the Range Extension of Gibbula umbilicalis (Gastropda, Trochidae) in the Eastern English Channel? Master’s Thesis, Bournemouth University, Bournemouth, UK, 2016. [Google Scholar]
  24. Team, G. GISS Surface Temperature Analysis (GISTEMP); NASA Goddard Institute for Space Studies: New York, NY, USA, 2017.
  25. Jung, S.; Pang, I.-C.; Lee, J.-H.; Choi, I.; Cha, H.K. Latitudinal shifts in the distribution of exploited fishes in Korean waters during the last 30 years: A consequence of climate change. Rev. Fish Biol. Fish. 2014, 24, 443–462. [Google Scholar] [CrossRef]
  26. KMA. Report of Global Atmosphere Watch 2018; National Institute of Meteorological Sciences: Seogwipo, Republic of Korea, 2019; p. 268. [Google Scholar]
  27. Gillooly, J.F.; Brown, J.H.; West, G.B.; Savage, V.M.; Charnov, E.L. Effects of size and temperature on metabolic rate. Science 2001, 293, 2248–2251. [Google Scholar] [CrossRef]
  28. Byrne, M.; Ho, M.; Selvakumaraswamy, P.; Nguyen, H.D.; Dworjanyn, S.A.; Davis, A.R. Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proc. R. Soc. B 2009, 276, 1883–1888. [Google Scholar] [CrossRef] [PubMed]
  29. Tagliarolo, M.; Porri, F.; Scharler, U.M. Temperature-induced variability in metabolic activity of ecologically important estuarine macrobenthos. Mar. Biol. 2018, 165, 23. [Google Scholar] [CrossRef]
  30. Huey, R.B.; Stevenson, R.D. Integrating thermal physiology and ecology of ectotherms: A discussion of approaches. Am. Zool. 1979, 19, 357–366. [Google Scholar] [CrossRef]
  31. Dell, A.I.; Pawar, S.; Savage, V.M. Systematic variation in the temperature dependence of physiological and ecological traits. Proc. Natl. Acad. Sci. USA 2011, 108, 10591–10596. [Google Scholar] [CrossRef]
  32. Lemoine, N.P.; Burkepile, D.E. Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 2012, 93, 2483–2489. [Google Scholar] [CrossRef]
  33. IPCC. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; Pachauri, R.K., Meyer, L., Eds.; The Core Writing Team, IPCC: Geneva, Switzerland, 2014; p. 151. [Google Scholar]
  34. Rho, S. Studies on the propagation of top shell-I. Spawning and early development of the top shell, Turbo cornutus SOLANDER. Korean J. Fish. Aquat. Sci. 1976, 9, 43–55. [Google Scholar]
  35. Cha, B.Y.; Kim, D.H.; Kim, B.Y. Growth of Batillus cornutus by capture-recapture method. Korean J. Malacol. 2007, 23, 227–233. [Google Scholar]
  36. Cheung, W.W.; Watson, R.; Pauly, D. Signature of ocean warming in global fisheries catch. Nature 2013, 497, 365–368. [Google Scholar] [CrossRef]
  37. Lee, J.Y.; Yang, H.S.; Kang, D.H.; Jeung, H.D.; Hong, H.K.; Lee, H.J.; Kang, H.S.; Choi, K.S. Spatial variation in the annual reproductive cycle of Turbo (Batillus) cornutus (Gastropoda: Trochidae) at Jeju Island, Korea. Invertebr. Reprod. Dev. 2014, 58, 23–33. [Google Scholar] [CrossRef]
  38. Lightfoot, J. A Catalogue of the Portland Museum, Lately the Property of the Dutchess Dowager of Portland, Deceased; Which Will Be Sold by Auction by Mr. Skinner & Co, London; Forgotten Books: London, UK, 1786. [Google Scholar]
  39. Fukuda, H. Nomenclature of the horned turbans previously known as Turbo cornutus (Lightfoot, 1786) and Turbo chinensis Ozawa & Tomida, 1995 (Vetigastropoda: Trochoidea: Turbinidae) from China, Japan and Korea. Molluscan Res. 2017, 37, 268–281. [Google Scholar]
  40. Choe, B. Illustrated Encyclopedia of Fauna and Flora of Korea, Volume 33, Mollusca (II); National Textbook Company: Seoul, Republic of Korea, 1992; p. 860. [Google Scholar]
  41. Son, M.H.; Lee, C.I.; Park, J.M.; Kim, H.J.; Riedel, R.; Hwang, I.; Lim, Y.N.; Jung, H.K. The Northward Habitat Expansion of the Korean Top Shell Turbo sazae (Gastropoda: Vetigastropoda: Turbinidae) in the Korean Peninsula: Effects of Increasing Water Temperature. J. Mar. Sci. Eng. 2020, 8, 782. [Google Scholar] [CrossRef]
  42. Wernberg, T.; White, M.; Vanderklift, M.A. Population structure of turbinid gastropods on wave-exposed subtidal reefs: Effects of density, body size and algae on grazing behavior. Mar. Ecol. Prog. Ser. 2008, 362, 169–179. [Google Scholar] [CrossRef]
  43. Suskiewicz, T.S.; Johnson, L.E. Consumption rates of a key marine herbivore: A review of the extrinsic and intrinsic control of feeding in the green sea urchin. Mar. Biol. 2017, 164, 131. [Google Scholar] [CrossRef]
  44. Roma, J.; Schertenleib, K.; Ramalhosa, P.; Gestoso, I.; Canning-Clode, J.; Lenz, M. Moderately elevated temperatures increase macroalgal food consumption in two sea urchin species from coastal waters of Madeira. J. Exp. Mar. Biol. Ecol. 2021, 542, 151603. [Google Scholar] [CrossRef]
  45. Böttger, S.A.; McClintock, J.B.; Klinger, T.S. Effects of inorganic and organic phosphates on feeding, feeding absorption, nutrient allocation, growth and righting responses of the sea urchin Lytechinus variegatus. Mar. Biol. 2001, 138, 741–751. [Google Scholar] [CrossRef]
  46. Pulgar, J.; Moya, A.; Fernández, M.; Varas, O.; Guzmán-Rivas, F.; Urzúa, Á.; Quijón, P.A.; García-Huidobro, M.R.; Aldana, M.; Duarte, C. Upwelling enhances seaweed nutrient quality, altering feeding behavior and growth rates in and intertidal sea urchin, Loxechinus albus. Sci. Total Environ. 2022, 851, 158307. [Google Scholar] [CrossRef]
  47. Cheng, S.; Chen, J. Hemocyanin oxygen affinity and the fractionation of oxyhemocyanin and deoxyhemocyanin for Penaeus monodon exposed to elevated nitrite. Aquat. Toxicol. 1999, 45, 35–46. [Google Scholar] [CrossRef]
  48. Soucek, D.; Dickinson, A. Acute toxicity of nitrate and nitrite to sensitive freshwater insects, mollusks and a crustacean. Arch. Environ. Contam. Toxicol. 2012, 62, 233–242. [Google Scholar] [CrossRef]
  49. Harris, J.; Maguire, G.; Edwards, S.; Hindrum, S. Effect of ammonia on the growth rate and oxygen consumption of juvenile greenlip abalone, Haliotis laevigata Donovan. Aquaculture 1998, 160, 259–272. [Google Scholar] [CrossRef]
  50. Basuyaux, O.; Mathieu, M. Inorganic nitrogen and its effect on growth of the abalone Haliotis tuberculata Linnaeus and the sea urchin Paracentrotus lividus Lamarck. Aquaculture 1999, 174, 95–107. [Google Scholar] [CrossRef]
  51. Cox, T.E.; Murray, S.N. Feeding preferences and the relationships between food choice and assimilation efficiency in the herbivorous marine snail Lithopoma undosum (Turbinidae). Mar. Biol. 2006, 148, 1295–1306. [Google Scholar] [CrossRef]
  52. Watson, G.; Davies, J.; Wood, H.; Cocks, A. A comparison of survivourship and function (grazing and behaviour) of three gastropod species used as clean-up crew for the marine aquarium trade. PLoS ONE 2018, 13, e0199516. [Google Scholar] [CrossRef] [PubMed]
  53. Gao, X.; Sun, M.; Hu, Q.; Li, G. Influence of temperature on various development stages of the sea urchin Strongylocentrotus Nudus A. Oceanol. Limnol. Sin. 1993, 24, 634–640. [Google Scholar]
  54. Feng, W.; Nakabayashi, N.; Narita, K.; Inomata, E.; Aoki, M.N.; Agatsuma, Y. Sexually unbalanced gonad development and nutrition of the newly range-extended sea urchin Heliocidaris crassispina in the northeastern Honshu, Japan. Estuar. Coast. Shelf. Sci. 2021, 249, 107120. [Google Scholar] [CrossRef]
  55. De Ridder, C.; Lawrence, J.M. Food and feeding mechanisms: Echinoidea. In Echinoderm Nutrition; Jangoux, M., Lawrence, J.M., Eds.; A.A. Balkema Publishers: Rotterdam, The Netherlands, 1982; pp. 57–92. [Google Scholar]
  56. Klinger, T.S.; Hsieh, H.L.; Pangallo, R.A.; Chen, C.P.; Lawrence, J.M. The effect of temperature on feeding, digestion, and absorption, of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea). Physiol. Zool. 1986, 59, 332–336. [Google Scholar] [CrossRef]
  57. Sawabe, T.; Oda, Y.; Shiomi, Y.; Ezura, Y. Alginate degradation by bacteria isolated from the gut of sea urchins and abalones. Microb. Ecol. 1995, 30, 193–202. [Google Scholar] [CrossRef] [PubMed]
  58. Azad, A.K.; Pearce, C.M.; McKinley, R.S. Effects of diet and temperature on ingestion, absorption, assimilation, gonad yield, and gonad quality of the purple sea urchin (Strongylocentrotus purpuratus). Aquaculture 2011, 317, 187–196. [Google Scholar] [CrossRef]
  59. Edwards, D.C.; Huebner, J.D. Feeding and growth rates of Polinices duplicatus preying on Mya arenaria at Barnstable Harbour, Massachusetts. Ecology 1977, 58, 1218–1236. [Google Scholar] [CrossRef]
  60. Stickle, W.B.; Moore, M.N.; Bayne, B.L. Effects of temperature, salinity and aerial exposure on predation and lysosomal stability of the dogwelk Thais (Nucella) lapillus (L.). J. Exp. Mar. Biol. Ecol. 1985, 93, 235–258. [Google Scholar] [CrossRef]
  61. Lee, Y.J.; Yoo, S.K.; Rho, S.; Kim, S.H. The stocking density and growth of young abalone Haliotis discus hannai Ino cultured in the hanging net cage. Bull. Nat. Fish. Res. Dev. Agency 1988, 42, 59–69. [Google Scholar]
  62. Gao, X.; Liu, Y.; Liu, Y.; Liu, J. Influence of temperature on feeding and growth of young abalone. Oceanol. Limnol. Sin. 1990, 21, 20–26. [Google Scholar]
  63. Foster, G.G.; Hodgson, A.N. Consumption and apparent dry matter digestibility of six intertidal macroalgae by Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae). Aquaculture 1998, 167, 211–227. [Google Scholar] [CrossRef]
  64. Dixon, M.G. The Effect of Temperature and Photoperiod on the Digestive Physiology of the South African Abalone, Haliotis Midae. Master’s Thesis, Rhodes University, Grahamstown, South Africa, 1992. [Google Scholar]
  65. Matoto, S.V.; Shimizu, T.; Mita, H.; Tsuchiya, K.; Segawa, S. Reproduction and metabolism of Turbo (Batillus) cornutus in Chiba, Japan. Fish. Sci. 2002, 68, 330–333. [Google Scholar] [CrossRef] [PubMed]
  66. Davis, A.R.; Benkendorff, K.; Ward, D.W. Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp. Mar. Biol. 2005, 146, 859–868. [Google Scholar] [CrossRef]
  67. Eppley, R.W.; Lasker, R. Alginase in the sea urchin Strongylocentrotus purpuratus. Science 1959, 129, 214–215. [Google Scholar] [CrossRef]
  68. Boolootian, R.A.; Lasker, R. Digestion of brown algae and the distribution of nutrients in the purple sea urchin Strongylocentrotus purpuratus. Comp. Biochem. Physiol. 1964, 11, 273–289. [Google Scholar] [CrossRef]
  69. Kikutani, K.; Ohba, H.; Yamakawa, H. Distribution and gut contents of the green snail Turbo marmoratus in Tokunoshima Island, Ryukyus (southern Japan). J. Tokyo Univ. Fish. 2002, 88, 47–52. [Google Scholar]
  70. Lyons, D.A.; Scheibling, R.E. Effect of dietary history and algal traits on feeding rate and food preference in the green sea urchin Strongylocentrotus droebachiensis. J. Exp. Mar. Biol. Ecol. 2007, 349, 194–204. [Google Scholar] [CrossRef]
  71. Freeland, W.J.; Janzen, D.H. Strategies in herbivory by mammals: The role of plant secondary compounds. Am. Nat. 1974, 108, 269–289. [Google Scholar] [CrossRef]
  72. Vadas, R.L. Preferential feeding: An optimization strategy in sea urchins. Ecol. Monogr. 1977, 47, 337–371. [Google Scholar] [CrossRef]
  73. Rapport, D.J. Optimal foraging for complementary resources. Am. Nat. 1980, 116, 324–346. [Google Scholar] [CrossRef]
  74. Pennings, S.C.; Nadeau, M.T.; Paul, V.J. Selectivity and growth of the generalist herbivore Dolabella auricularia feeding upon complementary resources. Ecology 1993, 74, 879–890. [Google Scholar] [CrossRef]
  75. Cruz-Rivera, E.; Hay, M.E. Macroalgal traits and the feeding and fitness of an herbivorous amphipod: The roles of selectivity, mixing, and compensation. Mar. Ecol. Prog. Ser. 2001, 218, 249–266. [Google Scholar] [CrossRef]
  76. Jung, S.W.; Rho, H.S.; Choi, C.G. Seaweed beds and community structure in the East and South Coast of Korea. J. Mar. Sci. Eng. 2022, 10, 689. [Google Scholar] [CrossRef]
Animals 13 03436 g001
Figure 1. Schematic diagram of the experimental system used for the feeding assay with one main tank and three experimental units.
Figure 1. Schematic diagram of the experimental system used for the feeding assay with one main tank and three experimental units.
Animals 13 03436 g001
Animals 13 03436 g002
Figure 2. Comparison of nutrient concentrations in M. nudus treatments: (a) phosphate, (b) nitrite, and (c) nitrate.
Figure 2. Comparison of nutrient concentrations in M. nudus treatments: (a) phosphate, (b) nitrite, and (c) nitrate.
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Animals 13 03436 g003
Figure 3. Comparison of nutrient concentrations in T. sazae treatments: (a) phosphate, (b) nitrite, and (c) nitrate.
Figure 3. Comparison of nutrient concentrations in T. sazae treatments: (a) phosphate, (b) nitrite, and (c) nitrate.
Animals 13 03436 g003
Animals 13 03436 g004
Figure 4. Comparison of food consumption rate of M. nudus by temperature: (a) food consumption rate per individual and (b) food consumption rate per unit biomass. Different letters indicate significant differences among temperatures at p < 0.05.
Figure 4. Comparison of food consumption rate of M. nudus by temperature: (a) food consumption rate per individual and (b) food consumption rate per unit biomass. Different letters indicate significant differences among temperatures at p < 0.05.
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Animals 13 03436 g005
Figure 5. Comparison of food consumption rate of T. sazae by temperature: (a) food consumption rate per individual and (b) food consumption rate per unit biomass.
Figure 5. Comparison of food consumption rate of T. sazae by temperature: (a) food consumption rate per individual and (b) food consumption rate per unit biomass.
Animals 13 03436 g005
Table 1. Comparison of morphometric data for M. nudus among temperatures prior to the feeding assay (mean ± standard deviation).
Table 1. Comparison of morphometric data for M. nudus among temperatures prior to the feeding assay (mean ± standard deviation).
5 °C10 °C15 °C20 °C25 °C
Diameter (mm)64.8 ± 2.765.6 ± 7.466.6 ± 6.662.4 ± 2.266.5 ± 6.1
Wet weight (g)91.1 ± 8.188.8 ± 30.093.5 ± 27.578.9 ± 8.292.6 ± 24.4
Table 2. Comparison of morphometric data for T. sazae among temperatures prior to the feeding assay (mean ± standard deviation).
Table 2. Comparison of morphometric data for T. sazae among temperatures prior to the feeding assay (mean ± standard deviation).
5 °C10 °C15 °C20 °C25 °C
Shell height (mm)75.0 ± 2.777.2 ± 1.175.5 ± 6.470.3 ± 0.373.7 ± 3.9
Wet weight (g)91.8 ± 8.2101.5 ± 2.591.6 ± 14.584.6 ± 1.389.8 ± 18.2
Table 3. Comparison of morphometric data for M. nudus among temperatures and between measurements before and after the feeding assay (mean ± standard deviation). Significant differences are based on t-test at p < 0.05.
Table 3. Comparison of morphometric data for M. nudus among temperatures and between measurements before and after the feeding assay (mean ± standard deviation). Significant differences are based on t-test at p < 0.05.
5 °C10 °C15 °C20 °C25 °C
Diameter
(mm)		Wet Weight (g)Diameter
(mm)		Wet Weight (g)Diameter
(mm)		Wet Weight (g)Diameter
(mm)		Wet Weight (g)Diameter
(mm)		Wet Weight (g)
Before 64.8 ± 2.794.1 ± 8.165.6 ± 7.488.8 ± 30.066.6 ± 6.693.5 ± 27.562.4 ± 2.378.9 ± 8.367.7102.4
After 66.0 ± 2.794.1 ± 8.767.8 ± 8.287.8 ± 37.067.7 ± 5.391.6 ± 22.864.1 ± 3.078.3 ± 3.970.3102.3
p value0.05<0.05<0.05<0.05<0.05<0.05<0.05<0.05<ndnd
nd: not determined.
Table 4. Comparison of morphometric data for T. sazae among temperatures and between measurements before and after the feeding assay (mean ± standard deviation). Significant differences are based on t-test at p < 0.05.
Table 4. Comparison of morphometric data for T. sazae among temperatures and between measurements before and after the feeding assay (mean ± standard deviation). Significant differences are based on t-test at p < 0.05.
5 °C10 °C15 °C20 °C25 °C
Diameter
(mm)		Wet Weight (g)Diameter
(mm)		Wet Weight (g)Diameter
(mm)		Wet Weight (g)Diameter
(mm)		Wet Weight (g)Diameter
(mm)		Wet Weight (g)
Before 64.9 ± 2.991.8 ± 8.267.8 ± 0.8101.5 ± 2.565.8 ± 3.491.6 ± 14.570.3 ± 0.384.6 ± 1.373.7 ± 3.989.8 ± 18.2
After 65.5 ± 2.387.8 ± 6.467.6 ± 0.8100.3 ± 2.966.0 ± 3.491.2 ± 14.170.5 ± 0.5784.7 ± 1.67.3 ± 4.490.0 ± 18.5
p value0.05<0.05<0.05<0.05<0.05<0.05<0.05<0.05<0.05<0.05<
Table 5. Comparison of food consumption rate between M. nudus and T. sazae (mean ± standard deviation). Significant differences are based on t-test at p < 0.05.
Table 5. Comparison of food consumption rate between M. nudus and T. sazae (mean ± standard deviation). Significant differences are based on t-test at p < 0.05.
5 °C10 °C15 °C20 °C25 °C
Ind.
(g ind−1 d−1)		Biomass
(g g−1 d−1)		Ind.
(g ind−1 d−1)		Biomass
(g g−1 d−1)		Ind.
(g ind−1 d−1)		Biomass
(g g−1 d−1)		Ind.
(g ind−1 d−1)		Biomass
(g g−1 d−1)		Ind.
(g ind−1 d−1)		Biomass
(g g−1 d−1)
M. nudus0.46 ± 0.590.002 ± 0.0041.41 ± 1.070.007 ± 0.0133.19 ± 1.970.010 ± 0.0132.73 ± 1.270.010 ± 0.0130.37 ± 0.560.002 ± 0.004
T. sazae0.29 ± 0.460.003 ± 0.0031.45 ± 1.700.032 ± 0.0241.70 ± 1.140.061 ± 0.0531.96 ± 2.040.062 ± 0.0752.54 ± 3.070.087 ± 0.127
p value0.05<0.05<0.05<0.05<0.05<0.05<0.05<0.05<0.05<0.05<
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Seo, J.; Koo, B.J. Temperature-Dependent Food Consumption Rates of the Sea Urchin Mesocentrotus nudus and Top Shell Turbo sazae: Potential Impacts on Seaweed Beds. Animals 2023, 13, 3436. https://doi.org/10.3390/ani13223436

AMA Style

Seo J, Koo BJ. Temperature-Dependent Food Consumption Rates of the Sea Urchin Mesocentrotus nudus and Top Shell Turbo sazae: Potential Impacts on Seaweed Beds. Animals. 2023; 13(22):3436. https://doi.org/10.3390/ani13223436

Chicago/Turabian Style

Seo, Jaehwan, and Bon Joo Koo. 2023. "Temperature-Dependent Food Consumption Rates of the Sea Urchin Mesocentrotus nudus and Top Shell Turbo sazae: Potential Impacts on Seaweed Beds" Animals 13, no. 22: 3436. https://doi.org/10.3390/ani13223436

APA Style

Seo, J., & Koo, B. J. (2023). Temperature-Dependent Food Consumption Rates of the Sea Urchin Mesocentrotus nudus and Top Shell Turbo sazae: Potential Impacts on Seaweed Beds. Animals, 13(22), 3436. https://doi.org/10.3390/ani13223436

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