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Article

A High Abundance of Holothuria (Halodeima) atra (Holothuroidea Aspidochirotida) in a Halimeda Dominated Habitat

by
Vanyarat Kongsap
1,
Ekkalak Rattanachot
2,*,
Anchana Prathep
2,3,
Witthaya Buaphol
4 and
Jaruwan Mayakun
1,3,*
1
Molecular Evolution and Computational Research Unit, Faculty of Science, Prince of Songkla University, Hat Yai 90110, Songkhla, Thailand
2
Excellence Center for Biodiversity of Peninsular Thailand, Faculty of Science, Prince of Songkla University, Hat Yai 90110, Songkhla, Thailand
3
Division of Biological Science, Faculty of Science, Prince of Songkla University, Hat Yai 90110, Songkhla, Thailand
4
Mu Ko Phetra National Park, Department of National Parks, Wildlife and Plant Conservation, Langu 91110, Satun, Thailand
*
Authors to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(2), 451; https://doi.org/10.3390/jmse11020451
Submission received: 17 January 2023 / Revised: 14 February 2023 / Accepted: 15 February 2023 / Published: 18 February 2023
(This article belongs to the Topic Marine Ecology, Environmental Stress and Management)
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Abstract

:
High-value sea cucumber species are overexploited, and the focus of fishing has shifted to low-value species, e.g., Holothuria (Halodeima) atra. In this study, the population of H. atra was investigated in three different habitats: a seagrass habitat, a seaweed habitat, and bare sand, at an intertidal zone of Lidee Island, Mu Ko Phetra National Park, Satun Province, Thailand. The habitat type was the predictor which had a significant impact on the density and frequency distribution of the body length of H. atra individuals. H. atra was only found in the seaweed and seagrass habitats. The highest density of this species, 91.1 ± 9.6 inds 100 m−2, was found in the seaweed habitat. The frequency distribution of the body length of H. atra individuals in the seagrass habitat showed no significant change throughout the study period, but the mode of the length frequency distribution in the seaweed habitat gradually rose from 9 to 22 cm from January−September 2019. Asexual reproduction was the major source of recruitment. The occurrence of recently fissioned individuals was slightly higher in the seaweed habitat than in the seagrass habitat (6.0 ± 1.1% and 2.2 ± 0.6%, respectively). This study showed that H. atra was most abundant in the seaweed habitat, which is likely because of the greater availability in this habitat of food sources, microhabitats, and protection against sun irradiance, desiccation, and stress during low tides.

1. Introduction

Sea cucumber (Class Holothuroidea, Phylum Echinodermata) are important and common marine invertebrates with 1775 species reported worldwide [1]. They are widely distributed throughout the world and are most diverse in tropical shallow water zones, ranging from the intertidal zone to the abyssal depths [2]. They play many important ecological roles, such as bioturbation, sediment cleaning and mixing, and nutrient recycling in benthic communities [3,4,5,6].
Besides their ecological importance, sea cucumbers are also economically important as medical and luxury foods [7,8]. Holothuroids are commercially exploited worldwide and around 20,000 to 40,000 tons of sea cucumbers are sold each year, mostly to Asian markets [2]. In Hong Kong stores, the prices for high-value sea cucumber species can reach up to USD 3583 kg−1 [7,9]. Overfishing of sea cucumbers around the world has caused the average harvested body size and density to decrease [2,10,11,12]. This overexploitation has led to a severe decline in the wild stocks of high-economic-value species and fishing targets have shifted from high-value to low-value species [11,12]. The overexploitation of high-commercial-value species of sea cucumbers, e.g., Holothuria (Metriatyla) scabra Jaeger, 1833 is a common occurrence. Furthermore, fisheries seem to have shifted towards the low-value species [2,12]. In tropical areas, especially in Thailand, H. scabra is the most important and economically valuable species that is overexploited and illegally harvested without regulation. The low-value species, H. atra, then tends to be harvested after the stocks of H. scabra begin to deplete.
H. atra is widespread in the tropical Indo-Pacific region [13]. It is a heavily exploited species in many countries in Asia [14] even though it has low commercial value. It is a high-yielding species in the Chinese market [15] because it commonly occupies shallow intertidal areas where it can be easily harvested, with the potential for future commercialization [13,16,17,18,19,20]. However, in Thailand, H. atra is overexploited and harvested without management or regulations [21]. Smaller enterprises, such as culture ponds and sea ranching systems, are ongoing in Thailand; however, the essential baseline knowledge of the biology, reproduction, population, ecology, and behaviour of H. atra is still insufficient for successful aquaculture and fishery management.
The population of H. atra might be affected by various factors, such as environmental stresses, the availability of food, human disturbances, and habitat preference [17,18,22]. Previous studies have reported that the density, body size, biomass, fission rate, and abundance of H. atra varies between habitats, such as between shallow- and deep-tide pools, back reef and front reef, and protected and unprotected areas [17,18,22]. Recently, coastal development, pollution, and nutrient inputs have resulted in the degradation of nearshore habitats [23,24,25]. Habitat degradation can result in population loss and affect the structure of H. atra populations [21,26].
However, in Thailand, the population structures, dynamics, and habitat preferences of sea cucumbers in different habitats still remain unclear and more information is needed. A thorough investigation of H. atra populations will provide a better understanding of the needs of a sustainable sea cucumber population. Therefore, the main objective of this study is to investigate the population of H. atra in three nearby different habitat types: seagrass beds, seaweed beds, and bare sand. It is hypothesized that the abundance of H. atra in seaweed and seagrass habitats is higher than in a bare sand habitat which is likely because the availability of food sources and microhabitats.

2. Materials and Methods

2.1. Study Site

The study site was located in an intertidal zone of the Andaman Sea between Lidee Lek Island and Lidee Yai Island which are located in Mu Ko Phetra National Park (6°47′09.7” N 99°45′56.3” E), Satun Province, in south-western Thailand (Figure 1). There are two main seasons, both monsoon-dominated. The rainy season is dominated by the Southwest monsoon from May to October and the dry season is dominated by the Northeast monsoon from November to April. Salinity in the study area varies from 28−35 psu. In this area, Halimeda macroloba Decaisne is the dominant calcified green algal species, with a density of 55.6 ± 7.5 thalli m−2. The dominant seagrass species, with a cover of 47.6 ± 29 %, is Halophila ovalis (R. Br. Hook. J. H. (Halodeima) atra is common and abundant, with a density of 72.0 ± 4.5 inds 100 m−2.
The study site was surveyed and divided into three habitat types: a seaweed habitat with dominant H. macroloba, a agrass habitat with dominant H. ovalis, and a bare sand habitat. The estimated area of each habitat was around 1 km2.

2.2. Field Sampling Periods

The field studies were carried out monthly from November 2018 to March 2020 except during March, May, August 2019, and February 2020 due to unfavourable weather. The recruitment of H. atra was carried out on a monthly basis from September 2019 to March 2020.

2.3. Density, Size, and Recruitment from Asexual Reproduction of H. atra

In each habitat type, three permanent belt transects, each 50 m long and 10 m apart, were laid perpendicular to the shoreline of Lidee Yai Island. The number of H. atra were counted along a 1 m strip on each side of the transect line and the total length (from mouth to anus) of counted individuals was measured. Asexual reproduction by fission was observed as per Conand [18] to categorize H. atra into 3 groups: normal, fissioning, and recently fissioned. Then, the occurrence of the recently fissioned individuals was calculated.

2.4. Recruitment from Sexual Reproduction of H. atra

In this survey area, the aboveground part of seaweed and seagrass were examined as substrates for newly settled H. atra. The aboveground part of macrophytes were collected using a quadrat which was placed on its natural percent cover or density. For H. macroloba, the aboveground parts in the 20 × 20 cm quadrat were cut and kept in bottles. The aboveground part of H. ovalis was collected by cutting the sediment in a 10 × 10 cm quadrat to cut the rhizome. Then, the content was scooped and gently washed to remove the sediment and retain only the seagrass. The petioles and leaves of H. ovalis were collected. There were 10 replicates for each substrate type. After a few minutes, 99% ethanol was added to the bottle and then gently shaken every 15 min. for 1 h. The contents of the bottle were poured through a 63 µm sieve. The aboveground parts were washed thoroughly with fresh water to detach all remaining larvae from the leaves. The material that remained on a sieve was stored in 99% ethanol before observing for juvenile (adapted from Mercier [27]). The contents of a bottle were observed under a light microscope using a Sedgewick rafter counting chambers. The juveniles were measured (contracted length) under the microscope using an eyepiece micrometre. The remaining content was observed under stereomicroscope to find the small juveniles.

2.5. Abundance and Aboveground of Macrophytes

Quadrats (50 × 50 cm) were placed at 5 m intervals along each line transect to estimate the percentage cover of H. ovalis and density of H. macroloba. Seagrass and seaweed specimens were identified as per Coppejans et al. [28]. For aboveground biomass of macrophytes, a quadrat, 20 × 20 cm, was placed randomly at 0 m, 25 m, and 50 m of each line transect in each seagrass and seaweed habitat; then, all macrophytes in the quadrat were collected. The above ground part of macrophytes was cleaned, dried in the oven at 60 °C for 48 h, and weighted, respectively.

2.6. Properties of Sediment

Sediment samples (2.5 cm depth) were randomly collected at 0 m, 25 m, and 50 m along each line transect using a 7 cm diameter core drill. Samples were kept in an ice box during the transportation to the laboratory at Faculty of Science, Prince of Songkla University [29]. In the laboratory, sediment samples were dried in an oven at 60 °C for 48 h. To analyse organic matter and grain size, 10 g of dry sediment was sieved through a 1 mm mesh sieve, then ground until homogeneous and weighed to 3 g. The sample was then burned at 450 °C for 5 h, and reweighed. Organic matter was calculated by loss of weight on ignition (LOI; adapted from Storer [30]). For grain-size analysis, the rest of the dried sediments were sieved through 2 mm, 1 mm, 500 μm, 250 μm, 125 μm, and 63 μm mesh sieves and then sediments in each sieve were weighed and mean grain size calculated by using GRADISTAT v.9.1 [31,32].

2.7. Environmental Factors

Water temperature and light intensity were recorded using the Onset Hobo LI light logger (Onset Computer Corporation, Bourne, MA, USA) that was set up at 10 cm from aboveground at each habitat site (from 7 am to 4 pm). Light intensity in Lux was transformed into µmole photon m−1 s−1 [33]. Salinity was measured using a refractometer. Gypsum balls were used to indirectly measure water velocity [34]. Gypsum balls were dried at 60 °C until a constant weight was achieved and weighed before exposure. In the field, the gypsum balls were set at 10 cm above the ground in each transect line for one tide (6–8 h) when the water level was at least 1 m height; then, they were collected and brought back to the laboratory. Used gypsum balls were weighed and the dissolution rate calculated (g h−1).

2.8. Statistical Analyses

A two-way analysis of variance (ANOVA) was used to test the difference in density of H. atra, the occurrence of recently fissioned individuals of H. atra, and mean grain size among the habitat types and months. A one-way analysis of variance (ANOVA) was used to test the difference of percentage cover of H. ovalis, the biomass of H. ovalis, the density of H. macroloba, the biomass of H. macroloba, light intensity, and temperature between months. A Scheirer-Ray-Hare test was used to test the difference in length of H. atra and organic matter among habitat types and months. A Kruskal-Wallis test was used to test the distribution of sediment size among habitat types and dissolution rate of gypsum balls between months. Post hoc comparisons were made using Tukey’s post hoc test and Dunn’s Kruskal−Wallis multiple comparisons. Simple linear regression was used to test the relationship between the density of H. atra and the abundance of seaweed and seagrass. Multiple regression was used to test the relationship between density and 2 habitat types (seaweed and seagrass), sediment properties, and physical factors. The R statistical software was used for statistical analysis [35].

3. Results

3.1. Abundance and Aboveground Biomass of Macrophyte Vegetation

In the seagrass habitat, there was a significant difference in the percentage cover of H. ovalis between months, with a mean of 46.8 ± 2.7% (one-way ANOVA, F12,26 = 4.863, p < 0.001, Figure 2A). The lowest percentage cover of H. ovalis was found in December 2018 and January 2020, with 17.7 ± 2.8% and 30.0 ± 0.9%, respectively. The highest was found in November 2019, with 67.8 ± 8.5%. For the aboveground biomass of H. ovalis, there was a significant difference between months, with mean 8.4 ± 0.6 gdw m−2 (one-way ANOVA, F10,88 = 14.55, p < 0.001; Figure 2B). The lowest aboveground biomass of H. ovalis was in December 2019 and January 2020: 3.2 ± 1.1 and 3.8 ± 0.5 gdw m−2, respectively. The highest was found in June 2019: 19.5 ± 1.8 gdw m−2.
In the seaweed habitat, the highest densities of H. macroloba were found in November 2018 until July 2019: 57.8 ± 4.1 to 85.7 ± 2.0 thalli m−2. Interestingly, the density of H. macroloba dramatically decreased in September 2019 from 75.3 ± 22.9 thalii m−2 in July 2019 to 17.2 ± 7.1 thalii m−2 in September 2019 (one-way ANOVA, F12,26 = 2.497, p < 0.05; Figure 2C). For the aboveground biomass of H. macroloba, there was a significant difference between the months, with a mean of 22.4 ± 5.2 gdw m−2 (one-way ANOVA, F10,88 = 2.059, p < 0.05; Figure 2D). The lowest aboveground biomass of H. macroloba was found in December 2019 (3.2 ± 1.1 gdw m−2) and the highest was found in June 2019 (19.5 ± 1.8 gdw m−2). Sexual reproduction of H. macroloba was observed in September 2019.

3.2. Properties of Sediment

The percentage of sedimentary organic matter was significantly lower in bare sand than in the seagrass and seaweed habitats (5.4. ± 0.1%, 6.9 ± 0.2% and 6.8 ± 0.1%, respectively; Table 1). In all three habitats, the highest proportion of sedimentary organic matter was found in April 2019 (8.5 ± 0.5%) and the lowest proportion was found in June 2019 (5.1 ± 0.14; Figure 3A; Table 1). There was no significant difference in the percentage of sedimentary organic matter between seagrass and seaweed habitats (6.9 ± 0.2% and 6.8 ± 0.1%, respectively; Table 1).
The mean grain size was significantly different in all three habitats. The smallest mean grain size was found in the seaweed habitat (131.6 ± 3.1 µm) compared with the seagrass habitat and bare sand (178.3 ± 3.1 µm and 166.7 ± 3.6 µm, respectively). The smallest grain size (144.1 ± 7.7 µm) was found in July 2019 in the seaweed habitat and the largest grain size was found in November 2019 in the bare sand habitat (174.0 ± 9.6 µm; Figure 3B; Table 2).
The fractions of sediment samples were significantly different among habitats (Kruskal-Wallis, p < 0.01). The highest amount of gravel (>2 mm) composed of shell and coral rubble and fine sand (125 µm) were found in the seaweed habitat. The highest amount of medium sand (250 µm) was found in the seagrass habitat. Meanwhile, the highest amounts of very coarse sand (1 mm), coarse sand (500 µm), very find sand (63 µm), and mud (<63 µm) were found in the bare sand habitat (Figure 4).

3.3. Environmental Factors

Light intensity was highest in February 2019 (1044.1 ± 75.3 µmole photon m−2 s−1), while the lowest light intensity was recorded in November 2019 (535.5 ± 75.7 µmole photon m−2 s−1; one-way ANOVA, F11,23 = 7.767, p < 0.001). The temperature ranged from a low of 28.4 °C in January 2020 to a high of 32 °C in June 2019 (one-way ANOVA, F11,23 = 15.52, p < 0.001). The water velocity varied between habitat types and months (two-way ANOVA; habitat type, F2,62 = 5.376, p < 0.01; month, F10,62 = 70.924, p < 0.001; interaction, F20,62 = 4.257, p < 0.001). The dissolution rate of gypsum balls was significantly highest in November 2019 (0.6 ± 0.04 g h−1) and lowest in October 2019 (0.3 ± 0.1 g h−1; Kruskal-Wallis, H10 = 77.969, p < 0.001).
The density of H. atra was not significantly correlated with the percentage cover of H. ovalis, the density of H. macroloba, and the aboveground biomass of H. macroloba (p > 0.05; Figure 5A,C,D). However, the density of H. atra in the seagrass habitat was significantly negatively correlated with the biomass of H. ovalis (linear regression, Y = −1.28X + 59.74, R2 = 0 18, F1,31 = 6.59, p < 0.05; Figure 5B).
For multiple regression analysis between the density of H. atra with habitat type, organic matter, grain size, and the physical factors of light, temperature, and the dissolution rate of gypsum balls, the multiple regression analysis revealed that the habitat type was the predictor which had the significantly strongest impact on the density of H. atra followed by mean grain size and temperature. The density of H. atra was significantly positively correlated with the seaweed habitat and the mean grain size, but negatively correlated with temperature (Table 3).

3.4. Population of H. atra

The average density of H. atra in the seagrass habitat, 52.8 ± 3.2 inds 100 m−2, was significantly lower than in the seaweed habitat, 91.0 ± 5.9 inds 100 m−2 (Table 1). From June to July 2019, the average density of H. atra in the seagrass habitat was slightly lower than in other months and increased afterwards. The average density of H. atra in the seaweed habitat was considerably low during June-July 2019 but had recovered by September 2019 (Figure 6, Table 2). However, no individuals were found in the bare sand habitat during this study.
The average length of H. atra in the seaweed habitat, 13.9 ± 0.1 cm, was significantly longer than H. atra in the seagrass habitat, 12.1 ± 0.1 cm (Table 1). The longest average length of H. atra was found in September 2019, with 14.3 ± 0.3 cm, while the shortest average length was found in April 2019, with 12.5 ± 0.2 (Table 1). The monthly length-frequency distribution of H. atra showed a unimodal distribution in both the seagrass and seaweed habitats. In the seagrass habitat, the mode of length-frequency distribution did not significantly change throughout the study period, ranging from 8 to 12 cm. In the seaweed habitat, the mode of length-frequency distribution rose from 9 to 22 cm in January 2019 to September 2019, then decreased to 11 cm in October 2019 (Figure 7).

3.5. Recruitment of H. atra

For recruitment from asexual reproduction during September to December 2019, the occurrence of recently fissioned individuals of H. atra was slightly higher in the seaweed habitat than in the seagrass habitat (6.0 ± 1.1% and 2.2 ± 0.6%, respectively), but the difference was not statistically significant (Figure 8, Table 2).

4. Discussion

In the present study, the abundance of H. atra was higher in the seaweed habitat than in the seagrass habitat and absent in the bare sand habitat. This might be because of habitat structure. The structure of H. macroloba is more complex than the structure of H. ovalis based on leaf morphology, dimensions of shoots, canopy level, and leaf length [36]. H. macroloba has a large, erect thallus that protrudes approximately 5−15 cm above the substrates, and its branching is highly dimensional. H. ovalis is very short, protruding approximately 1−2 cm above the substrate, and has thin leaves compared with H. macroloba. The different structures of these habitat types might provide differences in protection and food availability for sea cucumbers.
In this study site, the sea cucumber was exposed to the air for around 3 h twice a day during the spring tide period. Therefore, the complex structure of H. macroloba can provide the sea cucumber with better protection and shelter from low-tide stress, i.e., high temperature, solar irradiance, and desiccation, than the seagrass habitat and bare sand [22,37,38,39,40,41,42,43,44]. In addition, multiple regression revealed that H. atra density was positively related to seaweed habitat, but negatively related to temperature. Furthermore, we often found H. atra tightly wreathed around H. macroloba by its tube feet (Figure 9A−D). This behaviour might help to stabilize its body firmly against tidal currents that could dislodge it. Thus, H. macroloba presents a more suitable habitat for H. atra and it acts like a pillar for sea cucumbers to attach to (personal observation). Therefore, H. atra might prefer to live in the habitats that provide better protection and shelter from low-tide stress and tidal currents.
Regarding food availability, we verified that the bare sand habitat had the lowest amount of organic matter due to less ability to trap and retain organic matter [36,45]. Moreover, the high content of organic matter in the macrophyte-dominated habitat was composed of dead matter from the macrophytes [46,47]. H. ovalis and H. macroloba both have high growth rates and fast turnover rates. H. ovalis can produce new leaf pairs in 4 days [48] and has a turnover rate of 10 leaves per shoot−1 year−1 [49] while H. macroloba produces one-two new segments per thallus−1 day−1 and a thallus turnover rate of 14.7−29.4 days [50]. Previous studies reported that H. atra shows selective feeding on the sediments rich in its food, i.e., organic matter and microalgae [51,52,53]. Therefore, H. atra might prefer to live in high-organic matter habitats, including the seaweed habitat and seagrass habitat.
In addition, this study reported that there was variation in the abundance and biomass of macrophytes between months. The abundance and biomass of H. ovalis were slightly lower in the dry season, similar to a previous study in the southern Andaman Sea [47,48]. This might be because a longer exposure period or higher irradiance in the dry season can damage the tissue and create associated stress symptoms [54]. In the seaweed habitat, a high abundance and biomass of H. macroloba was found in December 2018 until July 2019, and dramatically decreased in September 2019. This might be because of the die-off after the sexual reproduction period [50]. After that, the biomass of H. macroloba recovered in January 2020. Interestingly, the analyses of linear regression indicated that there was no relationship between the density of H. atra and the abundance of H. macroloba. This might be because during low-density periods of H. macroloba, the seaweed habitats still provide a better availability of food, shelter, and protection than the seagrass and bare sand habitats. In addition, the abundance of the seaweed will recover in a few months [50]. The regression analysis demonstrated that the density of H. atra was negatively related to the biomass of H. ovalis. However, this relationship was unclear. A possible reason might be because the belowground network of H. ovalis is compact, and their leaves are dense (two leaves per node), occupying both aboveground and belowground spaces and obstructing the sea cucumber from obtaining food from the sand. From field observation, H. atra found in the seagrass habitat always live in the sparse spots of seagrass where they can easily obtain food on the surface of substrates.
From the multiple regression analysis, it was determined that the main factors influencing H. atra density were the habitat types and temperature, as the environmental stressors that were discussed in the previous section. Moreover, grain size was positively related to the density, which might be due to the fact that sand particles were dominant in these areas, while mud (<63 μm) was less than 5%. In addition, H. atra prefers to feed on the sand more than fine sediment, which relates to a previous report showing that around 90% of sediment in H. atra intestine was composed of sand and gravel, while 10% was silt [55].
In this study, the length-frequency distribution of H. atra was different between habitats. In the seagrass habitat, the length-frequency distribution of H. atra was dominated by small individuals and the mode did not change throughout the year. This was similar to previous studies carried out in shallow waters near Ananij Island, Wanlitung, and Reunion Island [17,56,57,58]. It might be that fission produces a small individual but compensates for overall mortality and emigration [17,59,60,61,62]. In the seaweed habitat, the mode gradually rose from 8 to 22 cm from January until September 2019. After that, it rapidly decreased to 11 cm by October 2019. The findings were quite similar to a previous study by Ongkers et al. [63] which showed that the average size of H. atra in the coastal waters of Morella gradually increased from April to September 2018. Uthicke [59] also reported temporal variation in the mode of the length-frequency distribution of H. atra at Fantome Island and Brook Island. However, the reason for this phenomenon in the seaweed habitat was unclear. Therefore, for a better understanding of population dynamics, such as migration and recruitment from both sexual and asexual reproduction, and seasonal variation, long-term studies are needed.
For asexual recruitment, we hypothesized that there was a higher occurrence of recently fissioned individuals of H. atra in the seagrass habitat than in the seaweed habitat, since a triggering factor for the asexual reproduction of H. atra is a stressful environment [17,56,64,65]. Thus, the more complex structure of the seaweed habitat might reduce the trigger for fission. However, slightly higher fission in the seaweed habitat than in the seagrass habitat might be because H. atra utilized the strong-flat thallus of H. macroloba as a substrate to hold while twisting its body during fission ([17], personal observation, Figure 10A,B).
Regarding sexual recruitment, newly settled and small juveniles were not found during this study. This might be because of a failure of fertilization and an unsuitable environment [66,67]. A failure of fertilization occurs due to the low density of mature individuals [66]. Dissanayake and Stefansson [68] reported that the size of the mature individuals of H. atra were 16 cm long, which showed low abundance in this study site. Moreover, Chao et al. [66] showed that small individuals (<190 g wet wt) in the fission population showed no signs of spawning even if they showed mature gonads. Second, previous studies have reported the survivorship of sea cucumbers in these stages to depend on proper environmental conditions [69,70,71]. Stressful environments, i.e., high temperature, desiccation, and varied salinity might cause the mortality of larvae, newly settled, and small juveniles of H. atra [38,66,67]. Thus, the absence and unpredictability of the newly settling and small juveniles of H. atra can indicate that asexual reproduction might be the major source of the recruitment to maintain this population [56,66].

5. Conclusions

In this study, we studied the population structures of H. atra in three different habitats: a seagrass habitat, a seaweed habitat, and bare sand. Our studies found H. atra in the seaweed and seagrass habitats, but no H. atra individuals were found in the bare sand habitat. Different habitat types are correlated to the density and length-frequency distribution of this sea cucumber. H. atra is more abundant in vegetated areas where shelter, food, and protection are available. These findings regarding the habitat of H. atra have implications for aquaculture in terms of site selection. In addition, these results suggest that different habitats could influence the population structure and dynamics of H. atra. Therefore, habitat preservation is an important management strategy to maintain sustainable populations of H. atra and possibly other sea cucumber populations.

Author Contributions

Conceptualization, J.M., E.R. and A.P.; methodology, V.K., E.R., J.M. and W.B.; formal analysis, V.K.; investigation, V.K.; writing−original draft preparation, V.K.; writing−review and editing, J.M. and E.R.; visualization, E.R. and J.M.; supervision, J.M., E.R. and A.P.; project administration, J.M. and E.R.; funding acquisition, E.R., J.M. and V.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Faculty of Science Research Fund, Prince of Songkla University (PSU) (J.M., Research Grant, 2020, contract no. 163003) and the Faculty of Science Research Fund, Prince of Songkla University (PSU) (V.K., contract no. 1-2562-02-007). Financial support to E.R. from The Thailand Research Fund and Office of the Higher Education Commission (contract no. MRG6180174) is acknowledged.

Institutional Review Board Statement

The license to use animals for scientific purposes, ID U1-07886-2561, was provided by the Institute of Animals for Scientific Purpose Development (IAD), National Research Council of Thailand (NRCT).

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors would like to thank the Seaweed and Seagrass Research Unit TEAM, Prince of Songkla University, Watana Chaithongkeaw, and the staff of Mu Ko Phetra National Park, Langu, Satun, Thailand for field assistance. Thanks to Thomas Duncan Coyne for assistance with the English.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Figure 1. Study site at Lidee Islands, Mu Ko Phetra National Park, in the Andaman Sea, Satun Province. SW: seaweed habitat; SG: seagrass habitat; BS: bare sand habitat.
Figure 1. Study site at Lidee Islands, Mu Ko Phetra National Park, in the Andaman Sea, Satun Province. SW: seaweed habitat; SG: seagrass habitat; BS: bare sand habitat.
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Figure 2. Abundance of macrophyte (mean ± SE) from November 2018 to March 2020 except March, May, and August 2019, and February 2020, and biomass of macrophytes (mean ± SE) from December 2018 to March 2020 except January, March, May, and August 2019, and February 2020: (A) percentage cover of H. ovalis in seagrass habitat; (B) aboveground biomass of H. ovalis in seagrass habitat; (C) density of H. macroloba in seaweed habitat and (D) aboveground biomass of H. macroloba in seaweed habitat.
Figure 2. Abundance of macrophyte (mean ± SE) from November 2018 to March 2020 except March, May, and August 2019, and February 2020, and biomass of macrophytes (mean ± SE) from December 2018 to March 2020 except January, March, May, and August 2019, and February 2020: (A) percentage cover of H. ovalis in seagrass habitat; (B) aboveground biomass of H. ovalis in seagrass habitat; (C) density of H. macroloba in seaweed habitat and (D) aboveground biomass of H. macroloba in seaweed habitat.
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Figure 3. Properties of sediment (mean ± SE): (A) organic matter and (B) grain size in seagrass, seaweed, and bare sand habitats from November 2018 to March 2020.
Figure 3. Properties of sediment (mean ± SE): (A) organic matter and (B) grain size in seagrass, seaweed, and bare sand habitats from November 2018 to March 2020.
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Figure 4. Distribution of sediment size (mean ± SE) in (A) seagrass; (B) seaweed; and (C) bare sand habitats from November 2018 to March 2020.
Figure 4. Distribution of sediment size (mean ± SE) in (A) seagrass; (B) seaweed; and (C) bare sand habitats from November 2018 to March 2020.
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Figure 5. Relationship between density of H. atra and abundance of macrophytes: (A) percentage cover of H. ovalis; (B) aboveground biomass of H. ovalis; (C) density of H. macroloba; and (D) aboveground biomass of H. macroloba.
Figure 5. Relationship between density of H. atra and abundance of macrophytes: (A) percentage cover of H. ovalis; (B) aboveground biomass of H. ovalis; (C) density of H. macroloba; and (D) aboveground biomass of H. macroloba.
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Figure 6. H. atra densities (mean ± SE) in the seagrass (SG) and seaweed (SW) habitats from November 2018 to March 2020.
Figure 6. H. atra densities (mean ± SE) in the seagrass (SG) and seaweed (SW) habitats from November 2018 to March 2020.
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Figure 7. H. atra length-frequency distribution, sampled monthly from November 2018 to March 2020 in seagrass (dash line) and seaweed habitats (solid line).
Figure 7. H. atra length-frequency distribution, sampled monthly from November 2018 to March 2020 in seagrass (dash line) and seaweed habitats (solid line).
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Figure 8. Occurrence of recently fissioned individuals (mean ± SE) in the seagrass habitat (SG) and seaweed habitat (SW), from September 2019 to March 2020.
Figure 8. Occurrence of recently fissioned individuals (mean ± SE) in the seagrass habitat (SG) and seaweed habitat (SW), from September 2019 to March 2020.
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Figure 9. H. atra attaches and wreathes its body around H. macroloba (A−D).
Figure 9. H. atra attaches and wreathes its body around H. macroloba (A−D).
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Figure 10. Using its tube feet (TF), H. atra holds H. macroloba to help twist its body (A,B).
Figure 10. Using its tube feet (TF), H. atra holds H. macroloba to help twist its body (A,B).
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Table
Table 1. Results of Scheirer-Ray-Hare testing of data of the effects of habitat type and month on total length of H. atra and sedimentary organic matter.
Table 1. Results of Scheirer-Ray-Hare testing of data of the effects of habitat type and month on total length of H. atra and sedimentary organic matter.
Source of VariationTotal Length of H. atraOrganic Matter
dfSSHDfSSH
Habitat type14,006,900153.930 ***2851,28084.595 ***
Month121,921,40073.815 ***121,046,093103.954 ***
Habitat type × month121,304,30050.106 ***24427,82542.515 *
Residuals557313,849,000 308
df, degrees of freedom; SS, sum of squares; ns, no significant differences; ‘*’, p < 0.05; ‘***’, p < 0.001.
Table
Table 2. Results of two-way ANOVA testing of data of the effects of habitat type and month on density, occurrence of recently fissioned individuals of H. atra, and mean grain size.
Table 2. Results of two-way ANOVA testing of data of the effects of habitat type and month on density, occurrence of recently fissioned individuals of H. atra, and mean grain size.
Source of VariationDensityOccurrence of
Recently Fissioned
Individual		Mean Grain Size
dfMSFdfMSFdfMSF
Habitat type128,42545.187 ***110.810.575 ns268,82061.713 ***
Month1221593.433 ***540.892.176 ns1230392.725.**
Habitat type × month126591.048 ns56.270.334 ns2419671.764 *
Residuals52629 2418.79 3081115
df, degrees of freedom; MS, mean squares; ns, no significant differences; ‘*’, p < 0.05; ‘**’, p < 0.01; ‘***’, p < 0.001.
Table
Table 3. Results of multiple regression analysis testing the influence of habitat type, organic matter, mean grain size, light, temperature, and dissolution rate of gypsum ball on the density of H. atra.
Table 3. Results of multiple regression analysis testing the influence of habitat type, organic matter, mean grain size, light, temperature, and dissolution rate of gypsum ball on the density of H. atra.
VariableCoefficientSEt-ValueVIF
Intercept351.171194.5611.805 ns
Habitat type67.64711.6315.816 ***2.84
Organic matter4.8343.4581.398 ns1.54
Mean grain size0.5710.2072.754 **2.71
Light0.0240.0250.962 ns1.25
Temperature−14.7495.837−2.527 *1.41
Dissolution rate of gypsum ball−7.34843.969−0.167 ns1.65
ns, no significant differences; ‘*’, p < 0.05; ‘**’, p < 0.01; ‘***’, p < 0.001.
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Kongsap, V.; Rattanachot, E.; Prathep, A.; Buaphol, W.; Mayakun, J. A High Abundance of Holothuria (Halodeima) atra (Holothuroidea Aspidochirotida) in a Halimeda Dominated Habitat. J. Mar. Sci. Eng. 2023, 11, 451. https://doi.org/10.3390/jmse11020451

AMA Style

Kongsap V, Rattanachot E, Prathep A, Buaphol W, Mayakun J. A High Abundance of Holothuria (Halodeima) atra (Holothuroidea Aspidochirotida) in a Halimeda Dominated Habitat. Journal of Marine Science and Engineering. 2023; 11(2):451. https://doi.org/10.3390/jmse11020451

Chicago/Turabian Style

Kongsap, Vanyarat, Ekkalak Rattanachot, Anchana Prathep, Witthaya Buaphol, and Jaruwan Mayakun. 2023. "A High Abundance of Holothuria (Halodeima) atra (Holothuroidea Aspidochirotida) in a Halimeda Dominated Habitat" Journal of Marine Science and Engineering 11, no. 2: 451. https://doi.org/10.3390/jmse11020451

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