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Article

The Symbiotic Relationship between the Antarctic Limpet, Nacella concinna, and Epibiont Coralline Algae

by
Boongho Cho
1,2,†,
Hyeonmi Bae
1,2,† and
Taewon Kim
1,2,*
1
Department of Ocean Sciences, Inha University, 100 Inha-ro, Michuhol-gu, Incheon 22212, Korea
2
Program in Biomedical Science and Engineering, Inha University, 100 Inha-ro, Michuhol-gu, Incheon 22212, Korea
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
J. Mar. Sci. Eng. 2022, 10(4), 496; https://doi.org/10.3390/jmse10040496
Submission received: 26 February 2022 / Revised: 26 March 2022 / Accepted: 28 March 2022 / Published: 2 April 2022
(This article belongs to the Special Issue Adaptation of Marine Animals to Extreme Environments)
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Abstract

:
The Antarctic limpet, Nacella concinna, is one of the most abundant benthic marine invertebrates found in the intertidal zone of King George Island, Antarctica. The shell of N. concinna is often encrusted with the coralline algae Clathromorphum obtectulum. In this study, to reveal the relationship between the limpet and coralline algae, we examined how the coralline algae affect the physical condition (survival and health) and morphology of the limpet. We cultured the limpets for 22 days and compared mortality, weight, condition factor (CF), fatty acid content, and the structure of the shell surface between limpets both with and without coralline algae in the laboratory. We also measured the environmental factors (i.e., temperature, pH, and salinity) of the seawater at each sampling site and the CF of the limpets and correlated them with coverage of coralline algae. The presence of coralline algae significantly increased the mortality of the limpets by 40% and the shell weight by 1.4-fold but did not affect the CF. Additionally, coralline algae altered the fatty acid profiles related to the limpet’s lipid metabolism (saturated fatty acids (SFA) and some polyunsaturated fatty acids (PUFA)). Specifically, C16:0, C17:0, C18:0, and total SFA increased, whereas C18:2 and C18:3 decreased. However, observations with a scanning electron microscope showed that shell damage in limpets with coralline algae was much less than in limpets without coralline algae, suggesting that coralline algae may provide protection against endolithic algae. The area of coralline algae on the limpet shell was positively correlated with the pH and temperature of the seawater. The results suggest that although coralline algae are generally assumed to be parasitical, the relationship between N. concinna and coralline algae may change to mutualism under certain conditions.

1. Introduction

Epibiosis is a phenomenon that is common in marine benthos [1,2], where the basibiont acts as the substrate to which a sessile epibiont can attach [2]. Numerous epibiotic studies have been conducted [3,4,5]. For example, Manning and Lindquist [6] studied the interaction between clams and hydroids on sandy beaches and found that the hydroid, as the epibiont, adversely affected the movement of the clams. Marin and Belluga [7] analyzed whether epibiotic sponges protected clams against predation and found that bivalves fouled with sponges survived significantly longer than unfouled bivalves. Wahl and Hay [8] examined the relationship between seaweeds, epibiotic plants, and the predatory sea urchin. They found that the sea urchins’ preference for seaweed changed according to the presence or absence of epibionts. However, thus far, there have only been a few studies of epibiosis in more extreme environments [9,10,11].
Antarctica is one of the most sensitive regions of the world to climate change [12,13], and research on ocean acidification and ocean freshening in the area is ongoing [14,15,16,17]. The Antarctic limpet, Nacella concinna, is one of the most conspicuous of the macrobenthos in the rocky intertidal and subtidal zones of Antarctica [18]. The shell of the limpet (the basibiont) can provide a habitat for the epibiont, and N. concinna that were fouled with coralline algae (epibiont) are commonly found [19,20]. The coralline algae, Clathromorphum obtectulum, is one of the most abundant non-geniculate coralline algae found throughout the Arctic and Antarctic regions and live on the rigid substrates and shells of various organisms [21,22,23,24]. McClintock et al. [19] showed that coralline algae can produce Mg-calcite skeletons when they cover the shell of N. concinna, providing protection to the shell in low pH environments. Schoenrock et al. [22] conducted experiments on culturing calcified species (C. obtectulum) and Antarctic crustose macroalgae (Hildenbrandia sp.) under the conditions of increased seawater temperature and pCO2 according to near-future climate change. They reported Hildenbrandia sp. would have potential competitive advantages for intertidal space. However, until now, there have been no studies on how epibiotic coralline algae directly affects the limpet itself.
In this study, we aimed to understand the relationship between the limpet (N. concinna) and coralline algae (C. obtectulum) in Antarctica for the first time. We hypothesized that epibiotic coralline algae on the shell would adversely affect the limpet. Accordingly, we predicted that the coralline algae would decrease the survival condition factor (CF), increase shell weight, and change the fatty acid content in the tissue of the limpet.

2. Materials and Methods

2.1. Sampling (Culture and Field Survey)

The limpets (Nacella concinna) for the culture experiments were collected in 12 January 2019 by hand from the outer side of Marian Cove on King George Island (latitude 62°14.531′ S, longitude 58°44.783′ W; water temperature: 2.8 °C ± 0.2, salinity: 33.3 psu ± 0.2, pH: 8.3 ± 0.004, mean ± standard error (SE); Figure 1). The limpets were selected based on shell length (32.7 ± 0.2, mean ± SE). To determine the area of coralline algae on the shells of the limpets, we analyzed the images (camera: Olympus TG-5, Olympus, Tokyo, Japan) using ImageJ®. We then divided the limpets into groups depending on whether they had more than 10% coralline algae coverage (present) or not (absent) (N = 20 per each treatment).
The limpets (N = 69) for the field survey for determining the relationships between the limpets and environmental factors (pH, temperature, and salinity) were collected from 19 different points both inside and outside the ice wall from 25 December 2018, to 8 February 2019 (Figure 1). Each sampling was conducted within a 30 cm radius of a sampling spot. The temperature, salinity, and dissolved oxygen content were measured using multiple water quality sensors (YSI pro2030, Yellow Spring Instruments Inc., Yellow Springs, OH, USA), while pH was measured with a pH meter (Seven2Go pH/Ion meter S8, Mettler Toledo, Columbus, OH, USA).

2.2. Experiment Setup and Acclimation

Acclimatizing the limpets to the experimental conditions was conducted in a water tank (80 × 45 × 20 cm) using seawater (pH 8.0, salinity 34 psu) taken from in front of King Sejong Station over seven days from 12 to 19 January 2019. To control salinity, the frozen part was melted for use in low-saline seawater after freezing, and the rest was used for high-saline seawater [17]. pH was controlled using CO2 tablets (SERA, Heinsberg, Germany) [17,25].
The culture experiment was conducted over 22 days from 19 January to 9 February 2019. The limpets were divided into two groups according to the presence or absence of coralline algae on their shells. The limpets were positioned separately, and the seawater was replaced every 24 h to maintain water quality. To maintain experimental accuracy, the top of the beaker was sealed by parafilm, and there was no food supply during the experiment. We used a low-temperature incubator (Plant Growth Chamber SH-303, Seyoung Scientific CO., Bucheon, Korea) to keep a stable temperature and humidity. The temperature, salinity, dissolved oxygen content, and pH were measured once every 24 h.

2.3. Analysis Method

During the experiment, limpet mortality was checked every 12 h and any dead limpets were immediately removed. Mortality was checked by foot muscle and tentacle movements [25]. Digital calipers (CD-15PSX, Mitutoyo Corp., Kanagawa, Japan) were used for measuring the length, height, and width of the limpets, and an electronic micro-scale (PG2002-S, Mettler Toledo, Columbus, OH, USA) was used to measure wet weight.
The CF was used as a bioindicator to measure limpet health [26,27]. After the experiment, CFs were calculated with only live individuals using the following formula [25].
CF = tissue   wet   mass   × shell   volume − 1
Fatty acid analysis was performed on the foot tissue of the limpet (N = 20 per each treatment). The extraction of fatty acid methyl esters (FAMEs) was performed according to the methodology of Gracés and Mancha [28]. Twenty limpets were used for each treatment. The tissue samples were freeze-dried at −95 °C using freeze dryers (CoolSafe 4–15 L, LaboGene, Lillerød, Denmark). All samples were then stored at −20 °C [29,30] before being crushed and placed in tubes with Teflon caps.
The samples were mixed 2 mL of a methylation mixture (MeOH: Benzene: DMP (2,2-Dimethoxy-propane): H2SO4, 39:20:5:2) and 1 mL of heptane. The samples were extracted at 80 °C for two hours. After heating, the samples were cooled at room temperature before being divided into two layers. The upper layer of each sample was transferred to a vial for gas chromatography (GC) injection. The fatty acid composition was analyzed using a Gas Chromatograph (GC; Agilent 7890 A, Santa Clara, CA, USA) equipped with a 120 mm × 0.25 mm × 0.25 μm capillary column (DB-23, Agilent, Santa Clara, CA, USA) and a flame ionization detector (FID). The injector temperature was 250 °C. The fatty acid content was calculated using the internal injection standard (C15:0) of known concentration. The results were expressed as mg FA/g lipid.
Using field emission-scanning electronic microscopy (FE-SEM; S-4300SE, Hitachi, Ltd., Tokyo, Japan), species identification of the coralline algae on the shell was conducted based on the shape (N = 1; Figure 2a). The cross section of the shell was then analyzed to identify the direct effect of coralline algae on the limpet shell (Figure 2b).

2.4. Statistical Analysis

We tested for significant differences in mortality, CF, shell weight, coverage, and fatty acid content using the two-tailed independent t-test for normally distributed data and the Mann–Whitney U test for non-normally distributed data. Significance probability levels of the fatty acid analysis were recalculated using the sequential Bonferroni correction for multiple comparisons [31]. We used Spearman’s rank correlation coefficient to investigate the relationship between coralline algae coverage on the limpet shells and environmental factors (pH, salinity, and temperature) or the CF of the limpet. All statistical analyses were performed using SPSS software (version 19.0; SPSS, Inc., Armonk, NY, USA), with a p-value of ≤0.05 denoting statistical significance.

3. Results

3.1. Mortality, Shell Weight, and CF

Mortality rate (%) and shell weight (g) was significantly higher in limpets with coralline algae on their shell (50% and 1.99 ± 0.10 g) compared to limpets without coralline algae on their shell (10% and 1.44 ± 0.071 g) (Two-tailed Mann–Whitney U test; U = 120, n1 = 20, n2 = 20, p = 0.006; Figure 1a; Two-tailed independent t-test, t = 4.331, df = 38, p < 0.001; Figure 3a,b). However, there was no significant difference in the CF between the two groups (Two-tailed independent t-test, t = −0.389, df = 26, p = 0.700; Figure 3c). Additionally, the area of algae coverage (%) did not significantly influence mortality (Two-tailed independent t-test, t = 1.447, df = 18, p = 0.165; Figure 3d).

3.2. Fatty Acid Content

As a result of analyzing the fatty acids of two groups with the presence or absence of coralline algae, significant differences were found in SFA among the main groups, SFA, MUFA, and PUFA (Table 1). The group in which coralline algae was present on the shell had a higher content of SFA (C16:0, C17:0, C18:0) and lower content of PUFA (C18:2, C18:3) than that of the group without coralline algae.

3.3. Scanning Electron Microscope (SEM) Analysis

SEM observation showed that the algae had no direct effect on the shell. No damage was observed to the surface shells from which the algae were removed (Figure 2c). However, the surfaces of the shells without algae were damaged, with irregular holes observed (Figure 2d).

3.4. Environmental Factors and Limpet

A significantly positive correlation was found between the coverage (%) of coralline algae on the limpet and the temperature and pH of the habitat seawater (Figure 4 and Table 2).

4. Discussion

In this study, we found that Antarctic limpets with coralline algae epibionts had higher mortality and greater shell weight than limpets without coralline algae and identified variations in the ratio of fatty acids between the two groups. However, the CF did not differ significantly between the two groups. These results suggest that coralline algae act as a parasite under normal conditions, with their presence negatively affecting behavior and metabolic activity by increasing the shell weight of the host and by decreasing drag speed [32], eventually jeopardizing their survival [33]. Our study showed that the shell weight of the limpet was higher in the group with coralline algae than in the group without coralline algae. An increase in shell weight can increase the metabolic burden of the host organism, eventually leading to energy exhaustion [32].
Although the CF could be a sensitive indicator for other organisms that generally inhabit the intertidal zone, the CF of N. concinna did not respond sensitively to pH [25] and temperature [34] in previous studies. Therefore, it appears that epibionts do not affect the CF of the limpet.
The fatty acid composition, which can be an indicator of stress (temperature, salinity, pollutants, etc.) in living organisms, was found to vary significantly depending on the presence or absence of epibionts [35,36]. In the group with coralline algae, the C16:0, C17:0, C18:0, and total SFA values were higher than in the group without coralline algae. The PUFA values of C18:2n6c, C18:3n3, and PUFA: SFA were lower in the group with coralline algae. It is well known that changes in the fatty acid composition are one of the cell-unit protection strategies that protect against environmental changes [37]. Changes in fatty acids were also seen in the military turban sea snail (Turbo militaris) [38] with increasing temperature and in the blue mussel (Mytilus edulis L.) [39] with increasing salinity.
Changes in SFA and PUFA are characteristics that regulate membrane structure and features in organisms to resist environmental stress, respectively [37,40,41,42]. This study has shown that the presence of an epibiont can change the fatty acid composition of the host and may also influence the cell functioning.
SEM analysis showed that the degree of damage to the surface of the limpet shell was different depending on the presence or absence of coralline algae. Limpet shells can be damaged by environmental factors such as waves and glaciers, as well as biological factors such as endolithic algae [43]. Endolithic algae are very important microborers for organisms with carbonate exoskeletons [44,45,46]. However, our study could not confirm whether the coralline algae directly affected the shell of the limpet.
Interactions between epibionts and hosts can be altered by environmental changes [47,48]. For instance, while branchiobdellids, which are epibionts of crayfish, act as commensals in clean water, their relationship changes to mutualism under a fouling environment [47]. The limpets and coralline algae are sensitive to ocean acidification in Antarctica because calcium carbonate (CaCO3) makes up the main component of their shell [19,49]. When the temperature and pH of the seawater fluctuate due to climate change, the epibiotic relationship between limpet and coralline algae will also be affected. In our study, the area of coralline algae on the limpets showed an opposite trend with decreasing pH and increasing temperature. Despite this, studies have shown that endolithic algae can thrive when seawater pH decreases and water temperature increases [50,51,52]. In addition, it was suggested that increasing the biomass of microborers can partially improve the dissolution rate (%) of coral exoskeletons [53]. Therefore, if endolithic algae are more likely to proliferate on limpets because of climate change, coralline algae can protect the shell because they adhere to the outermost surface of the limpet shell. This can lead to a mutually beneficial symbiosis as the benefits received by the limpets in the existing parasitic relationship will be substantially increased.

5. Conclusions

This study evaluated the interactions between the Antarctic limpet, representative intertidal macrofauna living in the Antarctic intertidal zone, and coralline algae fouled on the shells. Negative effects of this relationship were that the mortality and shell weight of the limpets were increased, and the distribution of the fatty acids was altered. As a positive effect, the algae physically protected the limpet shell from external stressors (scratches, penetration, etc.). We provide the first evidence that the relationship between the Antarctic limpet (N. concinna) and coralline algae is parasitic. However, future climate change may alter this relationship. Further studies on the effects of climate change on the interactions between these two species would help understand how symbiotic relationships can develop between species.

Author Contributions

B.C., H.B. and T.K. conceived and designed the experiments; B.C. and H.B. performed the experiments; B.C. and H.B. analyzed the data; B.C. and H.B. contributed reagents/materials/analysis tools; B.C. and H.B. wrote the paper; T.K. conducted writing-review and editing; T.K. supervised the research and in charge funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Korea Polar Research Institute under grant PE22110 and Inha University research grant.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Acknowledgments

We thank Ji Hee Kim of the Korea Polar Research Institute for identifying the coralline algae species.

Conflicts of Interest

The authors declare no conflict of interest.

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Jmse 10 00496 g001 550
Figure 1. (a) The sampling site for Nacella concinna is marked by a white circle (culture experiments) and white triangles (field survey). The insert on the upper left indicates the location of Marian Cove (red square) on King George Island. (b) Sample images of N. concinna were used in this study. The upper row shows N. concinna partially covered by the coralline algae Clathromorphum obtectulum. The lower row shows N. concinna without C. obtectulum on the shell.
Figure 1. (a) The sampling site for Nacella concinna is marked by a white circle (culture experiments) and white triangles (field survey). The insert on the upper left indicates the location of Marian Cove (red square) on King George Island. (b) Sample images of N. concinna were used in this study. The upper row shows N. concinna partially covered by the coralline algae Clathromorphum obtectulum. The lower row shows N. concinna without C. obtectulum on the shell.
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Figure 2. (a) SEM images of the conceptacles of coralline algae (×250), (b) the cross section of the limpet shell with coralline algae (×100), (c) the in-plane section of the limpet shell after the coralline algae had been removed deliberately (×180), and (d) the in-plane section of limpet shell with no coralline algae (×180). The dashed yellow line indicates the boundary line between the shell and coralline algae and the white arrows indicate irregular holes.
Figure 2. (a) SEM images of the conceptacles of coralline algae (×250), (b) the cross section of the limpet shell with coralline algae (×100), (c) the in-plane section of the limpet shell after the coralline algae had been removed deliberately (×180), and (d) the in-plane section of limpet shell with no coralline algae (×180). The dashed yellow line indicates the boundary line between the shell and coralline algae and the white arrows indicate irregular holes.
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Figure 3. (a) Mortality, (b) shell weight, and (c) CF of limpets in the presence or absence of coralline algae on the shell. (d) The coverage area (%) of the coralline algae from alive or dead limpets within the group in which coralline algae are present on the shell. Values for shell weight, CF, and coverage area are indicated as mean ± SE. Asterisks indicate significant differences between groups (p < 0.05).
Figure 3. (a) Mortality, (b) shell weight, and (c) CF of limpets in the presence or absence of coralline algae on the shell. (d) The coverage area (%) of the coralline algae from alive or dead limpets within the group in which coralline algae are present on the shell. Values for shell weight, CF, and coverage area are indicated as mean ± SE. Asterisks indicate significant differences between groups (p < 0.05).
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Figure 4. Relationship between (a) pH, (b) temperature, (c) salinity, and (d) CF and the coverage of coralline algae on the limpet shell. The red line indicates the trend line.
Figure 4. Relationship between (a) pH, (b) temperature, (c) salinity, and (d) CF and the coverage of coralline algae on the limpet shell. The red line indicates the trend line.
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Table
Table 1. Fatty acids composition (mg/g) of groups. Values are mean ± SE. ‘Presence’: the limpet partially covered by the coralline algae, ‘Absence’: the limpet without the coralline algae on the shell.
Table 1. Fatty acids composition (mg/g) of groups. Values are mean ± SE. ‘Presence’: the limpet partially covered by the coralline algae, ‘Absence’: the limpet without the coralline algae on the shell.
Fatty AcidTrivial NamePresenceAbsencep-Value
N = 20N = 20
C14:0Myristic acid
(tetradecanoic acid)		0.192 (±0.007)0.178 (±0.006)0.145
C16:0Palmitic acid
(hexadecanoic acid)		3.463 (±0.061)3.228 (±0.038)0.002 *
C17:0Margaric acid
(heptadecanoic acid)		0.248 (±0.010)0.179 (±0.004)<0.001 *
C18:0Stearic acid
(octadecanoic acid)		0.952 (±0.020)0.868 (±0.011)0.001 *
Ʃ SFA 1-4.855 (±0.090)4.452 (±0.050)<0.001 *
C18:1Oleic acid0.531 (±0.021)0.536 (±0.016)0.84
C20:1Eicosenoic acid0.992 (±0.027)1.065 (±0.025)0.052
Ʃ MUFA 2-1.523 (±0.044)1.602 (±0.031)0.153
C18:2Linoleic acid0.062 (±0.006)0.093 (±0.006)0.001 *
C18:3Alpha-linolenic acid (ALA)0.131 (±0.015)0.222 (±0.014)<0.001 *
C20:2Eicosadienoic acid0.928 (±0.039)0.951 (±0.026)0.613
C20:3Eicosatrienoic acid (ETE)0.817 (±0.028)0.842 (±0.019)0.478
C20:4Arachidonic acid (AA)2.240 (±0.089)2.451 (±0.061)0.058
C20:5Eicosapentaenoic acid (EPA, Timnodonic acid)4.039 (±0.174)3.948 (±0.091)0.648
Ʃ PUFA 3-8.217 (±0.281)8.507 (±0.091)0.337
Ʃ n–3 4-1.662 (±0.072)1.671 (±0.041)0.912
Ʃ n–6 5-1.077 (±0.044)1.165 (±0.031)0.089
n–3:n–6-1.565 (±0.063)1.457 (±0.056)0.212
1 SFA, Saturated Fatty Acid; 2 MUFA, Monounsaturated Fatty Acid; 3 PUFA, Polyunsaturated Fatty Acid; 4 n–3, n–3 Fatty acid; 5 n–6, n–6 Fatty acid; * Significant p values with sequential Bonferroni correction (p < 0.05).
Table
Table 2. Spearman’s rank correlation analysis examines the relationship between pH, temperature, salinity, and the CF of the limpets and the coverage of coralline algae on the limpet shell. Description of symbols: r—Spearman’s Rank Correlation Coefficient; N—number of data; p—the p-value of the correlation.
Table 2. Spearman’s rank correlation analysis examines the relationship between pH, temperature, salinity, and the CF of the limpets and the coverage of coralline algae on the limpet shell. Description of symbols: r—Spearman’s Rank Correlation Coefficient; N—number of data; p—the p-value of the correlation.
pHTemperatureSalinityCondition Factor × 1000
Coveragey = 31.876x − 258.95
r = 0.664, N = 69, p < 0.001		y = 2.5621x − 4.0368
r = 0.539, N = 69, p < 0.001		y = −0.0349x + 7.1865
r = 0.036, N = 69, p = 0.772		y = 7.1391x − 3.1859
r = −0.055, N = 69, p = 0.654
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Cho, B.; Bae, H.; Kim, T. The Symbiotic Relationship between the Antarctic Limpet, Nacella concinna, and Epibiont Coralline Algae. J. Mar. Sci. Eng. 2022, 10, 496. https://doi.org/10.3390/jmse10040496

AMA Style

Cho B, Bae H, Kim T. The Symbiotic Relationship between the Antarctic Limpet, Nacella concinna, and Epibiont Coralline Algae. Journal of Marine Science and Engineering. 2022; 10(4):496. https://doi.org/10.3390/jmse10040496

Chicago/Turabian Style

Cho, Boongho, Hyeonmi Bae, and Taewon Kim. 2022. "The Symbiotic Relationship between the Antarctic Limpet, Nacella concinna, and Epibiont Coralline Algae" Journal of Marine Science and Engineering 10, no. 4: 496. https://doi.org/10.3390/jmse10040496

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