Differences in Light Attenuation Patterns of Sargassum horneri Beds and Their Influences on Sebastiscus marmoratus Juveniles: A Case Study of Gouqi Island, Ma’an Archipelago, China

Abstract

Sargassum beds ensure sustainable environmental, social, and economic benefits in the coastal areas around the world. They can provide shelter ground to different species of fish juveniles. To investigate these, we conducted field surveys in a peaking growth period of Sargassum horneri from May to June 2010 to evaluate them on Gouqi Island, Ma’an archipelago, China. The study indicated that the light attenuation rate inside the S. horneri beds was higher than that in the surrounding areas. The light attenuation rate was highest in Ganxie, the second highest in Huangshidong, and the lowest in Houtouwan. We found that the average length of Sebastiscus marmoratus corresponded to the average height of S. horneri. This study improves our understanding of the function of sheltering grounds provided by Sargassum beds. Additionally, this study is relevant to the development of the regulations and directives to ensure the sustainable exploitations and protection of wild seaweeds and the accompanying organisms resources.

1. Introduction

Aquatic animal behavior changes according to different light intensities, especially in predator–prey relationships [1]. Kenyon et al. examined the sheltering behavior of juvenile tiger prawns (Penaeus esculentus) and found that their behavior also changed according to the amount of light. They studied three habitats including bare silt substratum, short and thin-leaved seagrass (Halodule uninervis), and tall broad-leaved seagrass (Cymodocea serrulata) during light and dark periods and found that small prawns remained on the seagrass during both the light and dark periods, whereas the large prawns spent more time above the substratum during the dark periods [2]. Vinyard and O’Brien demonstrated that as the light level was reduced, the reactive distance of the fish to prey of a certain size was diminished and their consumption rate was depressed [3]. James and Heck et al. evaluated the influence of light intensity and seagrass density on the predation rates of lined seahorse on shrimp [4]. The effects of floating leaves with the vesicles on the intensity, direction, and spectral composition of light are all factors that can affect the feeding efficiency of fish [5,6,7]. The light environment underneath the leaves is unpropitious for prey detection because of the effects of the leaves on the spectral composition, direction, and intensity of the light [8]. Similar results were reported for Ammodytes marinus [9], Onchidoris bilamellata [10], and Penaeus merguiensis [11].

Light intensity has been hypothesized to play a key role in determining the outcomes of predator–prey interactions in aquatic ecosystems. Many indoor experiments that were designed to study fish behaviors in response to light intensities have been performed. These studies focused on sheltering behavior [2], habitat selection [11], increased reaction distance [3], and turbidity [12,13]. However, none of them have identified the mechanism of selecting a sheltering ground for fish juveniles by field observations, especially in the case of Sargassum beds.

Sargassum beds are one of the most productive coastal ecosystems, and the habitat of many economically important fishery species such as abalones, sea-urchins, and rockfish. One of the important ecological functions of Sargassum beds is to provide a sheltering ground for fish juveniles and larvae. A large mass and complex stem and leaf structures create an abundance of hiding places with low light intensity. The use of poorly illuminated habitats can reduce the predation pressure, as visual predators hunt less efficiently under low light conditions. During feeding periods, light is a limiting factor for species depending on visual predation, with it reaching the critical point between 0.01–1 lux [14].

In China, Sargassum horneri beds had been known by local fishermen as sheltering grounds for fish juveniles. Sun [15] found that when S. horneri was sampled in Nanji Island (China), a huge number of small fish sprang out of the surface and one Harengula zunasi and three Agrammus agrammas were caught by hand. Zhang et al. [16] found a group of juvenile and adult Sebastiscus marmoratus living in S. horneri beds around Gouqi Island, and these fish mainly fed on Orchestia sp., caprellid species, and Ligia exotica, whose biomasses were deeply influenced by the growth of thalli during May–June every year. In this study, to understand the light attenuation patterns of S. horneri beds, we compared the light attenuation rates k inside and outside the S. horneri beds among Houtouwan, Ganxie, and Huangshidong. We also compared k and the slope dk/dD (the ratio of delta k and delta D) during the peak period of S. horneri on the 17 May and the declining period of S. horneri on the 10 June. Finally, we evaluated the population structure of S. horneri, the characteristics of the beds and how they vary with sea surface irradiance percentage, and the relationships between the light attenuation patterns of the S. horneri beds and fish juveniles.

2. Materials and Methods

Figure 1 shows the study sites located around Gouqi Island in the Ma’an Archipelago, Zhejiang Province, China (Figure 1). The Ma’an archipelago lies at the mouth of the Yangtze River, an important migrating passage for marine fish, and this area has a large community of S. horneri beds, which provides seasonal habitats during the maturity stage of the thalli. The Ma’an archipelago contains archipelagic waters of the continental shelf and is a good habitat for many rock fish such as the economically valued Sebastiscus marmoratus (Cuvier, 1829), whose adults and juveniles live in these beds [16]. We chose the sites Houtouwan (HTW: 30°43′31.0″ N, 122°46′20.8″ E), Ganxie (GX: 30°42′88.2″ N, 122°45′20.3″ E), and Huangshidong (HSD: 30°42′81″ N, 122°44′43.2″ E) as the study localities. The geographical characteristics of each sites differ: HTW has a large area of rocky substratum with a stepwise rocky topography, which is beneficial for S. horneri attachment, and HSD has a favorable tide, while the distribution of the beds is smallest in GX because it is near to the corner of the island and is exposed to waves. Additionally, inside and outside the S. horneri beds means 5 m and 100 m offshore, respectively.

We explored the light attenuation properties of the S. horneri beds from May to June in 2010. We evaluated the relationship between S. horneri heights and light intensities by measuring the light quanta in the areas, and we collected samples in 0.5 × 0.5 m² quadrates to measure the thalli heights on 10 June in the laboratory. We defined the percent of surface irradiance (%) as the average light quantum arriving at each of the water layers in relation to the surface, which is expressed as μmol m⁻² s⁻¹. We calculated the percent of surface irradiance (%) at 20 cm intervals. We measured the quantum of the depth of the vertical sections in situ using multi-functional water quality parameter equipment (AQ202-F, China) to be able to measure photosynthetic effective radiation at wavelengths in the range of 400–700 nm. The sensor of a white ball with a 3 cm diameter recorded the quantum data with depth at one-second intervals gradually from the top to the bottom of the sea. We measured the depth at which the thalli were attached and the average heights of the thalli (

Table 1. The attachment average depth (unit: m), average height of Sargassum horneri (unit: m), and depth with the presence of Sargassum horneri in Houtouwan, Huangshidong, and Ganxie, respectively.

Sample Site	Attachment Average Depth	Average Height	Depth with the Presence
Houtouwan	2.47	0.73	1.5–2.5
Huangshidong	2.63	0.63	2–3
Ganxie	1.95	0.76	1–2

). The height of a single gill net was 1.5 m, with it being 15 m in length including a 2.5 cm inner and 17 cm outer net mesh size. We prepared four gill nets with the total length of 60 m to collect fish juvenile individuals at a rate of ind m⁻² per day. We defined the sexual maturity stages of fish according to the following criteria: Stage I: gonads being small and ribbon-like, not possible to determine sex by gross examination; Stage II: immature, gonads elongated, slender, but sex determinable by gross examination; Stage III: maturing, gonads enlarged, individual ova visible to the naked eye.

We calculated the light attenuation rate based on the Beer–Lambert formula as follows:

$$I_D/I_0=e^{-kD}$$

(1)

where D is the depth in meters, I_D and I₀ are light intensities at the surface and depth D measured in μmol m⁻² s⁻¹, respectively, and k is the light attenuation coefficient in m⁻¹. We also defined dk/dD = Δk/ΔD as the ratio at which k changes with depth.

3. Results

3.1. Comparsions of k and dk/dD among Sites

We compared the k values inside and outside the S. horneri beds among the HTW, HSD, and GX sites (Figure 2). At the surface (0–1 m layer), the value inside the bed was higher than the value outside for the HTW area, but the opposite was found in both the GX and HSD sites. For the 1–2 m water layer, the k value was higher inside the beds in GX, but it was higher outside the beds in HTW and HSD. The k value inside was higher than that which was detected outside the bed at all of the sites in the water layers if 2–3 m and 3–4 m. The depth range in which the k value inside the beds was higher than that outside of them at 1.5–2.5 m, 2–3 m, and 1–2 m in HTW, HSD, and GX, respectively (Table 1). The height of the column (Δk) could be represented as a cumulative value of k, and it was higher inside all of the sites in the following order: GX > HSD > HTW (Figure 2).

Additionally, we compared k and dk/dD during the peak period on the 17 May and the declining period on 10 June 2010. As Figure 3 shows, the dk/dD in the top and bottom layers were similar on the 17 May and 10 June. The dk/dD of the top layer was −1.45 m⁻², and that of the bottom layer was 0.014 m⁻² on 17 May. On 10 June, the values were −5.102 m⁻² and 2.319 m⁻² in the top and bottom layers, respectively.

3.2. Population Structure of S. horneri Varied with Sea Surface Irradiance Percentage

We compared the characteristics of the S. horneri population with the percentage of surface irradiance at the interval of 0.2 m, corresponding to the depth at which S. horneri were affected. The average height of S. horneri was found in HTW was 80–100 mm, with there being a maximum of 180–200 mm and a minimum of 0–20 mm (Figure 4). Most S. horneri ranged from 80–100 mm to 40–60 mm in GX and HSD, and the distributions lacked a tall group and had only a small number of short thalli. The upper limit group was situated at 100–140 mm in GX and 100–120 mm in HSD. A minimum height group of 0–20 mm which occurred in HSD and HTW, but not in GX. The sea surface irradiance percentage in HTW and HSD decreased from the surface to 1.2 m, and it declined further to 2.2 m in HTW, but it remained similar in HSD (Figure 4). In GX, the percent of surface irradiance went up and down with the depth. The heights on 17 May and 10 June were 1.14 m and 0.73 m, respectively. We estimated the depth range of S. horneri to be between 1.3–2.5 m and 1.7–2.5 m, respectively, based on the average attachment depth (Table 1).

We compared the surface irradiance percentage with the characteristics of the S. horneri beds and found that the percentage in GX increased and decreased in a disorderly manner, probably because GX is located at the corner of the island, where strong waves disturb the optical environment. Thalli with a low height (40–60 mm) were predominant in HSD because of the open tide and clean water which are provided by its distance from the inhabited island, therefore, the surface irradiance percentage decreased to 1.2 m and then, it remained unchanged. The S. horneri population in HSD occupied a large area, but the thallum height was short and therefore, did not affect the light intensity a lot. The light intensity in HTW gradually decreased with the depth.

3.3. Relationships between Light Attenuation Patterns of the Beds and Fish Juveniles

Our analysis of the total fish number density in the S. horneri beds (Figure 5) showed that more fish were present inside of the beds than outside the beds, and more fish were present in GX, which was followed by HSD and then, HTW. In addition, at the beginning of the fast-growing period of S. horneri, the length of S. marmoratus on 27 April was 69.3 mm, while during the peak period on 29 May, it was 124 mm, and during the period of decline on 10 June, the length was 72.8 mm; the lengths in other periods were in the range of 82.18–95.87 mm (Figure 6).

4. Discussion

Based on the relationship between the S. marmoratus length and the S. horneri height in HTW (Figure 6), we found that the average length of S. marmoratus corresponded to the average height of S. horneri. Zhang et al. previously reported that S. marmoratus was the dominant species in the beds throughout the year, except for during September [16]. During the peak period of the seaweed beds, the stomach contents of S. marmoratus contained Orchestia sp., Caprellidea species, and Ligia exotica, which live in the fronds [16], showing a high level of interdependency between the beds and this fish species. The swimming ability of S. marmoratus is poor, and it is usually limited to a range of 1 km [17]. We also calculated the average gonad maturity of S. marmoratus both inside and outside the S. horneri bed at each site. Except for outside in HTW, all of the individuals were juveniles (

Table 2. The number (unit: individuals) and the gonad maturity (I–III) of Sebastiscus marmoratus in Houtouwan (HTW), Huangshidong (HSD), and Ganxie (GX) inside and outside the Sargassum horneri beds.

Sample Site	Number (N)	Average Gonad	Gonad I	Gonad II	Gonad III
HTW inside	19	1.79	21%	79%	0%
HTW outside	19	1.80	0%	84%	16%
HSD inside	38	1.51	47%	50%	0%
HSD outside	—	—	—	—	—
GX inside	42	1.68	31%	67%	0%
GX outside	16	1.80	19%	75%	0%

). The average gonad maturity of this species inside the beds was lower than that of fish outside the bed at each sites, and most of the individuals were juveniles. This result indicated that S. horneri beds provide sheltering habitats for juvenile fish. Additionally, the changing direction of light propagation and light intensity are affected by the growing stages of S. horneri, which can protect S. marmoratus individuals from top predators. The length of S. marmoratus varied consistently with the average heights of S. horneri. Wang reported that S. marmoratus ranging in length from 50.0 to 79.9 mm mainly fed on amphipods, while those with a length of 80.0–99.9 mm, fed on crabs and amphipods, and those of more than 100 mm long, mainly fed on fish and amphipod [18]. This difference occurred because the diet of S. marmoratus varied as the density of the prey organisms changed with the growth of the thalli.

The diving survey revealed that small fish individuals schooled, swimming around the beds during the day. Fish schooling behavior is often an effective anti-predator tactic [19]. Because schooling is primarily a visual phenomenon, it depends on light intensity [20,21,22]. As light intensity decreases, the schools progressively break up into smaller units until all of the schooling ceases [23,24]. Thus, at high light levels, prey could use schooling as a means of reducing the risk of predation. Mark and Thomas reported that illumination that increases above 10.8 lux (=0.2 μ·E·m⁻²·s⁻¹) has a weak effect on the reactive distance [12]. One lx is equal to 0.02 μ·E·m⁻²·s⁻¹ [25], and so 1 lx is equivalent to 1.08 lux. In this study, we calculated the average quantum value on the 29 May (110 lux) and 10 June (180 lux) in HTW. Therefore, there was enough light quanta in the Sargassum beds to distinguish the small fish individuals, and they avoided predation through schooling under high light intensity conditions.

A possible explanation for why small fish individuals are frequently active in the daytime is that predatory fish themselves may be subjected to predators [26]. Thus, the threat to lower order predatory fish may be higher during the high light intensity daytime, forcing them into relative inactivity during the day. In this scenario, the small prey fish could be relatively safe during the day; the increased risk that is associated with twilight may be due to the increased active hunting by predatory fish. In our study, we also observed a large amount of suspended matter in water, which would have affected predator visibility. Small fish swam around the complex morphological structure of the fronds, which helped them avoid sudden attacks from predators.

Regarding sheltering, we argue that the structure of the habitat that limits predation may be light-dependent. The successive shadow layer provides benefits to the fish juveniles due to the suitability of the light intensity that is created by the Sargassum beds. Light attenuation patterns in Sargassum beds strengthen the fish sheltering behavior. The ability of a fish to perceive contrast in radiance generally declines with decreasing light intensity [27,28]. Complex frond structures create large numbers of shadow layers, making it more difficult for predators to locate and trace their prey. Weakly illuminated habitats can reduce the predation pressure as visual predators forage less efficiently under low-light conditions [29].

Turbidity and turbulence also influence fish sheltering, but via different mechanisms. Turbidity can diminish the contrast between the prey organisms and the background due to the scattering of light [30]. The shading effect of turbidity occurs because underwater light is absorbed and scattered by the water and by particles such as suspended matter, and their vision is sensitive to the non-image-forming scattered light, which degrades the target brightness and color contrast. Juvenile fish settled in such optical environments reduce the chance of being found by predators. Additionally, the size and shape of the fish will appear substantially different in turbulent water than it would in still water regardless of the turbidity level. Small fish in a turbulent environment appear larger, so predators may be unwilling to attack [30]. Therefore, in this condition, small fish can gain relative safety.

5. Conclusions

Seaweed including Sargassum species has a lot of roles in maintaining the balance of aquatic ecosystems and in industrial usages [31,32,33,34,35,36]. Many studies have shown that seaweed beds can provide sheltering grounds for fish, but the data for S. horneri beds are scarce. In this study, we used k as the light index to describe the pattern of the optical distribution of light in S. horneri beds. We found that the k inside the beds changed more than it did on the outside, and more fish were found inside the beds as well. We found that S. marmoratus numbers inside the beds were related to the different heights of S. horneri and that small fish inside the beds exhibited schooling behavior. This study provides a better understanding of the function of the sheltering ground that is provided by Sargassum beds. It is necessary to understand the relationships between the density of macroalga and fish schooling behavior through laboratory experiments in future. Finally, the understanding of the synergy between fisheries and environment provides a sustainable pattern for the protections of seaweed beds that accompany wild organisms worldwide.