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This study aimed to assess the impact of physicochemical parameters, serving as indicators of eutrophication, on the abundance of Oikopleura dioica in Kuwait Bay due to urbanization and sewage runoff. Seasonal variations and the abundance of O. dioica, along with physicochemical parameters (temperature, salinity, dissolved oxygen concentration, and nutrient concentrations), and chlorophyll-a concentrations were investigated at three stations—KB1, KB2, and KB3—separated by approximately 18–20 km in the eutrophic seawater of Kuwait Bay. The abundance of O. dioica measured 35.3 ± 28.60 × 103, 48.2 ± 45.11 × 103, and 43.4 ± 15.46 × 103 ind m−3 in KB1, KB2, and KB3, respectively. Statistical analysis showed no significant variation in O. dioica abundance among the three stations (F = 0.123; d.f = 11, p > 0.05). Moreover, the abundance of O. dioica exhibited positive correlations with salinity, chlorophyll-a, and nitrates (r = 0.9; p > 0.05), while being negatively affected by dissolved oxygen concentration (r = − 0.64; p > 0.05). During summer, O. dioica showed the highest abundance at each station, with a peak of 125 × 103 ind.m−3 in KB2. Principal Component Analysis (PCA) revealed a strong association between O. dioica density, chlorophyll-a, and salinity during summer, suggesting that adequate food quality and quantity may contribute to the growth and reproduction of O. dioica in Kuwait Bay.
Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, Safat, Kuwait
Matrah Al-Mutairi
Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, Safat, Kuwait
M.N.V. Subrahmanyam
Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, Safat, Kuwait
Regional Organization for the Protection of the Marine Environment (ROPME), Safat, Kuwait
*Address all correspondence to: mohalikisr@gmail.com
1. Introduction
Appendicularians, classified under Tunicata: Appendicularia, are widely distributed holoplanktonic tunicates [1] and constitute a significant mesozooplankton group in marine ecosystems [2]. They rank as the second most abundant marine zooplankton group, outnumbered only by copepods [3]. Oikopleura dioica, a member of the appendicularian species, exhibits a broad zoogeographic range, inhabiting coastal waters across Europe, Asia, and the Americas. It demonstrates adaptability to various temperature and salinity conditions [1, 4]. In the Northwest Arabian Gulf, Appendicularia represents a minor proportion of the zooplankton community, accounting for 6.39%, with O. dioica being the primary representative [5]. However, the abundance of O. dioica in Kuwait waters surpasses that in other parts of the Arabian Gulf by at least threefold [6].
Members of this species reside within a gelatinous house that they secrete around their bodies every 3–4 hours. They construct a mucus-feeding net within this house to filter food from seawater pumped through the gelatinous housing. These houses, along with fecal pellets, constitute a major component of marine snow, dominating the annual vertical carbon flux of zooplankton [7]. Both occupied and abandoned houses serve as vital food sources for copepods, medusae, chaetognaths, ctenophores, and fish larvae [3, 8, 9, 10]. The wide range of diets, encompassing both living and dead organic matter, contributes to their high survival rates [11, 12]. Appendicularians possess the capacity to significantly alter the composition of small autotrophs and heterotrophs within a community, as they can ingest over 60% of suspended particles in seawater [13]. They are associated with phytoplankton blooms and may account for nearly 40% of total mesozooplankton grazing [14].
The population dynamics of appendicularians are heavily influenced by temperature and nutrient levels [4]. In coastal regions, the prevalence of appendicularians is notably impacted by discharges from continental waters [15]. The introduction of a significant quantity of nutrients into the marine environment is absorbed by primary producers, resulting in increased chlorophyll-a concentration [16], which serves as the primary food source for filter organisms [2].
The objective of this study was to examine the impact of physicochemical parameters as indicators of eutrophication on the abundance of O. dioica in Kuwait Bay due to urbanization, including sewage runoff, and to offer an ecological perspective on factors influencing their abundance.
This study investigated the seasonal variations in the abundance of O. dioica alongside physicochemical parameters at three stations—KB1, KB2, and KB3—located approximately 18–20 km apart in the eutrophic waters of Kuwait Bay (refer to Figure 1). KB3 is situated in the inner part of Kuwait Bay, approximately 1–2 km from Ras Asheerej and Doha, where desalination plants are situated. KB2 is positioned in the middle of Kuwait Bay, with Kuwait City, about 5–6 km away, being the nearest land point. KB1 is situated at the mouth of Kuwait Bay, approximately 5–6 km away from Ras Salmiya, known as an urban and tourist area. The study spanned all four seasons of the year 2005.
Figure 1.
Location of the study area (Kuwait Bay) and of the three sampling stations.
2.2 Physicochemical and biological parameters
In-situ measurements of physicochemical parameters (temperature, salinity, dissolved oxygen, and pH) and chlorophyll-a were obtained using a conductivity-temperature-depth (CTD) measuring device. Surface seawater samples (collected in triplicates for each season) were taken from each station and analyzed in the laboratory for nutrient concentrations (ammonium, nitrates, nitrites, and phosphates).
Zooplankton sampling involved the use of a 64 μm mesh net with a net mouth diameter of 0.5 m. Samples were collected in triplicates for each season from each station, and abundance was estimated based on the volume of water filtered, as indicated by flowmeters attached to the plankton net, as described in Thompson and Schweigert [17].
2.3 Statistics
Two-way analysis of variance (ANOVA) and paired comparisons, followed by post hoc Tukey’s test, were conducted to analyze the physicochemical parameters and the abundance of O. dioica across all stations and seasons. Pearson’s correlation coefficient was utilized to explore the relationship between the abundance of O. dioica and physicochemical parameters using Xl-stat 2019 v. 21.2 software. The data collected in this study underwent normalized Principal Component Analysis (PCA).
Table 1 presents the seasonal variations in the measured physicochemical parameters. Water temperature exhibited fluctuations, ranging from 20.1°C (winter, KB2) to 29.3°C (summer, KB3). Salinity levels ranged from 36.7 psu at station KB2 during spring to 40.5 psu at station KB3 during summer. High concentrations of nitrates, ammonium, and phosphates were consistently observed across all stations, indicative of a eutrophic condition. Among nitrogen forms, nitrates were the most prevalent, with concentrations ranging from 0.51 mg L−1 during summer at KB3 to 1.21 mg L−1 during winter at KB2.
KB1
KB2
KB3
Sp
Su
Au
Wi
Sp
Su
Au
Wi
Sp
Su
Au
Wi
Temperature (°C)
23.2
24.4
25.7
20.2
22.1
24.2
26.3
20.1
25.5
29.3
29.0
21.6
DO mg L−1
8.3
7.1
6.3
8.7
7.3
7.1
6.5
7.9
8.4
6.2
6.5
10.0
pH
8.1
8.1
8.1
8.5
8.2
8.6
8.9
7.3
8.1
8.1
8.0
8.2
Salinity psu
37.1
39.3
38.7
37.2
36.7
40.2
38.2
39.3
37.4
40.5
38.0
38.3
Ammonium mg L−1
0.6
0.1
0.0
0.4
0.6
0.1
0.3
0.4
0.8
0.0
0.1
0.5
Nitrites mg L−1
0.0
0.0
0.1
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.1
0.0
Nitrates mg L−1
0.8
0.6
0.7
1.0
0.7
0.6
0.6
1.2
0.7
0.5
0.6
1.1
Phosphates mg L−1
0.5
0.4
0.8
0.6
0.5
0.5
0.9
0.8
0.5
0.3
0.8
0.6
Table 1.
Physicochemical parameters observed in Kuwait Bay (Sp: Spring, su: Summer, Au: Autumn, Wi: Winter).
Two-way ANOVA shows that almost all parameters changed significantly among seasons. However, they are similar between stations (P > 0.05) (Table 2).
3.2 Oikopleura dioica abundance
The lowest density of O. dioica was recorded in winter in KB1 with 2 × 103 ind m−3. O. dioica, while the highest abundance was observed in summer, reaching 125 × 103 ind m−3 in KB2 (Figure 2). The abundance of O. dioica did not significantly vary between the three stations (F = 0.123; d.f = 11, p > 0.05) (Figure 2).
Figure 2.
Spatio-temporal variations of O. dioica abundance in Kuwait Bay.
To underscore the influence of physicochemical parameters on O. dioica abundance, a PCA was conducted (refer to Figures 3 and 4). The PCA results indicate that the F1 and F2 axes were highly significant, collectively explaining 100% of the variance. F1 (58.90% of total variance) positively correlated with dissolved oxygen and temperature, while phosphates, nitrites, pH, and chlorophyll-a displayed negative correlations with this axis. Hence, F1 can be interpreted as the photosynthetic gradient within Kuwait Bay. Conversely, F2 (41.10%) exhibited a positive association with O. dioica abundance, ammonium, and salinity, with nitrate displaying a negative loading on axis F2. The biplot of observations (stations) illustrates that KB2, the central station of the bay, was distinctly separated from the other two stations. KB2 exhibited the highest nutrient levels, fostering the proliferation of photoautotrophs, primarily phytoplankton. In contrast, KB1, situated at the bay entrance, displayed lower nutrient levels. During summer, O. dioica abundance strongly correlated with chlorophyll-a and salinity, suggesting that adequate food quality and quantity could support its growth and reproduction in the central area of Kuwait Bay. O. dioica abundance exhibited positive correlations with salinity (r = 0.96; p < 0.01), chlorophyll-a (r = 0.92; p < 0.02), and ammonium (r = 0.99; p < 0.01), while being negatively impacted by dissolved oxygen concentration (r = − 0.64; p < 0.05).
Figure 3.
PCA ordination of physicochemical variables and the abundance of O. dioica.
Figure 4.
PCA ordination of the abundance of O. dioica along the three stations (observations) of Kuwait Bay.
This study documented elevated nutrient concentrations (nitrogen and phosphorus enrichment), confirming the eutrophic status in the Arabian Gulf, consistent with previous research [18, 19, 20]. Kuwait Bay, receiving significant land runoff and sewage discharge, remains highly polluted despite its importance as a critical nursery area for fish and shrimp larvae. O. dioica exhibited very low densities in winter, peaking during summer, a pattern reminiscent of observations reported in Kuwait Bay by Michel et al. [6].
The seasonal abundance of O. dioica mirrors observations in the eutrophic inlet of the Inland Sea of Japan [21]. Continuous reproduction throughout the year characterizes O. dioica, which exhibits a positive correlation with salinity, chlorophyll-a, and ammonium levels. Known for its tolerance to extreme temperatures and salinity, O. dioica sustains large populations across the Arabian Gulf [6]. Rapid response to blooms triggered by nano- and pico-phytoplankton has been observed, aligning with its feeding preference for diminutive particles within the size range of 0.2 to 17 μm [22]. High chlorophyll levels, particularly in summer, suggest that food may not be a limiting factor for O. dioica population dynamics in this eutrophic area, supporting its consideration as a bioindicator of eutrophication [22, 23, 24]. The negative impact of dissolved oxygen concentration on O. dioica abundance underscores potential fluctuations observed due to pollution, nutrient variations, phytoplankton blooms, and other factors. PCA reaffirmed the strong association between O. dioica abundance, chlorophyll-a, and salinity during summer, suggesting sufficient food resources to sustain its growth and reproduction in Kuwait Bay. Furthermore, Li et al. [25] reported that early maturation of O. dioica favors the species’ rapid response to fleeting phytoplankton blooms. Although such a response was limited to blooms of small-size phytoplankton, it may help to recover micro-phytoplankton dominance in natural environments [25].
Seawater temperature, water currents, and algal distribution were the most relevant environmental factors affecting the abundance and distribution of Tunicata in Korea Bay (also called West Korea Bay), the North Yellow Sea, China [26]. In this study, phytoplankton were not considered; however, Kuwait Bay is a eutrophic area with high nutrient input (Tables 1 and 2; Figure 3) and that logically supports primary producers and could be one of the reasons that explain the high abundance of O. dioica. It has been reported that tunicates tend to gather in places of high plankton abundance [27], and they can feed on small particles, which makes them a basic link in the microbial food web [28]. As for currents, it was not considered in this study, which needs further investigation in the future. It is also important to note that Korea Bay is also a eutrophic area where it receives many of China’s smaller rivers in addition to three of North Korea’s major rivers: The Yalu (which rises on Mount Paektu and forms much of the border between China and North Korea), the Ch’ŏngchŏn, and the Taedong [29]. As for the depth, Koreas Bay is considered shallow (deepest depth is 50 m) [29], while Kuwait Bay is even shallower.
Two-way ANOVA results on the influence of stations and seasons on the physicochemical parameters within the three sampled stations (KB1, KB2, and KB3). SS, MS, df, and F are test parameters.
P < 0.05.
P < 0.01.
p < 0.001.
Paired comparisons using Tukey’s test were assessed to evaluate differences among stations and seasons: Su: Summer, Au: Autumn, Wi: Winter, Sp: Spring.
Predation can also impact the abundance of O. dioica [30]. Unlike this study, Sato et al. [30] reported that the lowest abundance of O. dioica was during summer fall and related that to the predation of the scyphomedusa Aurelia aurita on them. The factor of predators was not considered in the study herein but logically, if such heavy predation existed, the abundance would have definitely decreased (Figure 2). It is also noteworthy to mention that Sato et al. [30] study was in Tokyo Bay, Japan, a eutrophic area like Kuwait Bay in this study.
The abundance of O. dioica was documented as 35.3 ± 28.60 × 103, 48.2 ± 45.11 × 103, and 43.4 ± 15.46 × 103 individuals per cubic meter in KB1, KB2, and KB3, respectively. No significant variation in O. dioica abundance was observed among the three stations (F = 0.123; d.f = 11, p > 0.05). Correlation analysis revealed a positive relationship between O. dioica abundance and salinity, chlorophyll-a, and nitrates (r = 0.9; p > 0.05). However, abundance showed a negative correlation with dissolved oxygen concentration (r = − 0.64; p > 0.05). Throughout summer, O. dioica displayed its highest abundance at each station, peaking at 125 × 103 individuals per cubic meter in KB2. PCA underscored a robust association between O. dioica density, chlorophyll-a, and salinity during summer, suggesting that sufficient food quality and quantity may facilitate the growth and reproduction of O. dioica in Kuwait Bay. Additionally, future studies should encompass multiple years and diverse locations (eutrophic and oligotrophic), considering seasonal variations in physicochemical parameters, pollution levels, and types, predation on O. dioica by larval fish and other planktivorous species, phytoplankton abundance, and O. dioica’s feeding on phytoplankton.
The authors express gratitude to Mr. Yousef Alenezi, our colleague from the Kuwait Institute for Scientific Research, for providing the map. Special thanks are extended to Dr. Neila Annabi-Trabelsi and Dr. Wassim Guermazi from the University of Sfax, Tunisia, for their valuable review of the manuscript.
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Written By
Mohammad Ali, Matrah Al-Mutairi and M.N.V. Subrahmanyam
Submitted: 23 February 2024Reviewed: 02 April 2024Published: 08 May 2024
Open access peer-reviewed chapter - ONLINE FIRST
