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Communication

The Effect of Salinity on the Egg Production Rate of the Sac-Spawning Calanoid Copepod, Pseudodiaptomus hessei, in a Temporarily Open/Closed Southern African Estuary

by
Pierre William Froneman
Department of Zoology and Entomology, Rhodes University, Makhanda 6140, South Africa
Diversity 2023, 15(2), 263; https://doi.org/10.3390/d15020263
Submission received: 3 November 2022 / Revised: 3 February 2023 / Accepted: 9 February 2023 / Published: 13 February 2023
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Abstract

:
Global climate change is anticipated to be associated with changes in the salinity regimes of southern African estuaries as a result of the increased frequency of occurrences of extreme weather events (droughts and coastal storms) and the rise in sea level. The current investigation assessed the impact of salinity on the egg production rate (EPR) of the numerically important sac-spawning calanoid copepod, Pseudodiaptomus hessei, in a temporarily open/closed southern African estuary. The EPR of the copepod was determined using in vitro incubations during three distinct salinity regimes corresponding to the freshwater-deprived (hypersaline-salinity 38 PSU), freshwater-dominated (mesohaline-salinity 5 PSU), and polyhaline water phase (salinity 24 PSU). The egg production rate (EPR) and clutch size of P. hessei during the study ranged from 5.9 to 28.1 eggs F−1 d−1 and between 12 and 36 eggs sac−1, respectively. The EPR and clutch size of P. hessei during the polyhaline phase was significantly higher than during the freshwater-dominated and freshwater-deprived phases (p < 0.05). There were no significant differences in prosome length, egg size, or the hatching success of P. hessei during the three salinity regimes (p > 0.05 in all cases). The results of the current study suggest that the salinity changes in TOCEs in response to global climate warming are likely to be associated with a decrease in the reproductive success of P. hessei along the southeastern coastline of South Africa.

1. Introduction

Temporarily open/closed estuaries (TOCEs) account for ~70% of all estuaries along the southern African coastline [1,2]. Under natural conditions, these systems are periodically separated from the marine environment by the presence of a sandbar at the mouth [1,2,3]. A link to the marine environment is established through the overtopping of marine waters over the sand bar, which separates the estuary from the marine environment during winter storm events, or following heavy rainfall within the catchment area, which results in estuary breeching [1,2,3,4]. During the close phase of the estuary, temperature and salinity regimes reflect local climatic conditions and variations in the inflow of freshwater or marine waters during overtopping events [1,2]
The ecosystem functioning of TOCEs is strongly linked to the inflow of freshwater, which provides the necessary macronutrients to sustain elevated levels of primary and secondary production within these systems [1,2]. On the other hand, the establishment of a link to the marine environment is critical for the recruitment of marine breeding species into these systems, which facilitates increased biological diversity within these estuarine types [1,5]. Similar to their larger permanently open counterparts, TOCEs represent important nursery and feeding grounds for a variety of predators (estuarine, freshwater, and marine-breeding vertebrates and invertebrates) due to elevated food (mainly phytoplankton, zooplankton, and macrofauna) and habitat availability and access to refugia such as submerged macrophytes [5,6,7,8].
The calanoid copepod, Pseudodiaptomus hessei (Mrázek, 1894), is a major contributor to total copepod abundances and biomass in southern African estuaries, including TOCEs [3,4,9,10]. The copepod plays a vital role in estuarine ecosystems, functioning as a grazer of primary production and as an important prey item for a variety of invertebrate and vertebrate predators [3,4,6,7]. Pseudodiaptomus hessei is an egg-carrying calanoid copepod that exhibits a wide salinity tolerance which, in part, contributes to its extensive distribution and success in estuaries within the region [4,9,11]. The population dynamics of P. hessei is tightly coupled with freshwater pulses, with peaks in abundance typically recorded in the middle reach of estuaries following freshwater inflow [10,12,13]. Studies indicate that P. hessei reproduces throughout the year and that variations in the egg production rate of the copepod in a permanently open southern African estuary were largely moderated by changes in food quality and quantity, thus reflecting differences in freshwater inflow into the estuary [14].
Recent model simulations indicate that global climate change is likely to coincide with an increased occurrence of extreme weather events such as droughts and coastal storms and an increase in sea level and wave height along the southeastern coastline of South Africa [15,16]. These changes are expected to have an adverse effect on the ecosystem functioning of TOCEs within the region through changes in salinity regimes due to prolonged mouth closure and changes in the availability of macronutrients derived from freshwater runoff [1,2,4]. The current investigation was conducted to assess the influence of salinity during three distinct hydrological phases on the egg production rate of the calanoid copepod, Pseudodiaptomus hessei, in a TOCE along the southeastern coastline of South Africa.

2. Materials and Methods

2.1. Study Site

This investigation was conducted in the temporarily open/closed (TOCE) Kasouga Estuary in the warm temperate ecozone along the southeastern coastline of South Africa (Figure 1). The estuary is approximately 2.5 km in length and is generally shallow (<1.5 m depth). Water temperatures within the estuary typically range from 14 to 28 °C and demonstrate a seasonal pattern, with maximum temperatures in summer (December to February) and minima during winter (June to August) [3,4]. Salinities within the estuary are highly variable (0 to 60 psu), reflecting regional climatic conditions (e.g., droughts and rainfall) and the presence of a sand bar at the mouth, which may result in the estuary being separated from the marine environment for periods exceeding 1 year [3]. The overtopping of marine waters during storm events also contributes to variations in salinity within the estuary. Due to the shallow water depth and strong coastal winds that facilitate the vertical and horizontal mixing of the water column, the estuary is characterized by the virtual absence of horizontal patterns in physico-chemical variables during the closed phase [3,4].
Due to the small catchment area (~49 km2) and sporadic rainfall, which contributes to low freshwater inflow, the system is regarded as oligotrophic. As a consequence, total chlorophyll-a (Chl-a) concentrations within the estuary are generally <2.00 µg L−1 and typically dominated by the small nano- (2–20 μm) and picophytoplankton (<2.0 μm) phytoplankton size classes [3,4]. Studies conducted within the estuary indicate that the zooplankton community dominated almost entirely (>95%), both numerically and in terms of biomass, by calanoid and cyclopoid copepods of the genera Psuedodiaptomus, Paracartia, and Oithona [3,4,17]. The maximum biomass of zooplankton is attained during the closed phase following freshwater inflow into the system [3,4,17].
Zooplankton and water samples were collected at night from the lower reach of the estuary during the closed phase during three distinct hydrological phases that corresponded to the freshwater-dominated (September 2017, mesohaline, salinity 5), polyhaline (November 2017, salinity 24) and freshwater-deprived (February 2018, hypersaline, salinity 38) phases. On each occasion, temperature and salinity were recorded at 0.5 m depth using an Aquaprobe (YSI Incorporated, model 550A).

2.2. Chlorophyll-a Analysis

To determine size-fractionated Chl- a concentrations, 250 mL of water collected at the surface (0.5 m depth) was serially filtered (vacuum < 5 cm Hg) through a 20 μm nylon net filter, 2 μm isopore membrane, and 0.2 μm nucleopore filter. The filters were extracted in 90% acetone in the dark at −20 °C for 24 h. Three replicate samples were prepared during each survey. Fluorescence was then measured before and after acidification using a Turner designs 10 AU Fluorometer [3,4]. Results were expressed as μg L−1.

2.3. Egg Production Rates

Approximately 100 L of surface estuarine water was collected in 25 L carboys during each survey. The estuarine water was pre-sieved through a 50 μm mesh size to remove the larger zooplankton. Zooplankton samples were then collected at night using a modified WP-2 net (30 cm opening diameter and 150 μm mesh size) fitted with a cod-end and towed at the surface (0.5 m depth) for 2–3 min at 1–2 knots. After the net tow, the cod-end contents were gravimetrically filtered through a submerged 1 mm sieve to eliminate any potential predators (mysids and juvenile fish larvae) of copepods. The zooplankton catches were then diluted in a 50 L container and transported back to the laboratory within 3 h of collection. All experimental manipulations were subsequently conducted in the laboratory in a constant environment (CE) room at an ambient temperature with a light:dark phase of 14:10.
The egg production rates of the copepods during the three salinity regimes were estimated by employing the method of Noyon and Froneman (2013). After dilution in estuarine water, the copepods collected were acclimated in the laboratory for 6 h. Thereafter, 50 healthy females without eggs were incubated individually in 300 mL of estuarine water at in situ water temperatures. After the first 24 h, the incubated water was gently sieved through a submerged 50 μm mesh for examination of each female using a Zeiss stereomicroscope operated at 100× magnification. The ovigerous females were anaesthetized using the chemical compound Tricaine mesylate (MS 222, Sigma, St. Louis, MO, USA) to count the number of eggs produced without damaging the egg sac or the female [14]. Anesthetized females were never kept in water for more than 2 min and no ovigerous female mortality was recorded during the incubations (data not presented). The ovigerous females were then transferred to a petri dish with fresh estuarine water at an ambient temperature in order to take a ventral picture using a Leica stereomicroscope integrated camera (capture resolution 1600 × 1200 pixels, CMOS Camera) operated at 50× magnification. The number and size of eggs within the egg sac and prosome length were then determined using image software. The females were then re-incubated into 250 mL of renewed estuarine water. The egg production rate (EPR) was calculated as the number of eggs produced during the first 24 h multiplied by the ratio of ovigerous females and expressed as the number of eggs per female per day (eggs F−1 d−1). The ovigerous females were observed every 24 h to determine if hatching had occurred. If the eggs had not hatched, the female was re-incubated in stock estuarine water collected at the beginning of the experiment and stored in 25 L carboys at in situ temperatures with a natural day/night pattern to reduce potential degradation of the water. If hatching had occurred, the total number of nauplii were counted to estimate hatching success (HS). The duration of incubation varied between 48 and 72 h. Although it is possible that cannibalism by female copepods on nauplii stages could alter HS, a review of the literature suggests that the nauplii are above the preferred particle size consumed by P. hessei adults [18].

2.4. Statistical Analysis

Differences in the estimates of total Chl-a concentration and the egg production rates and prosome length of the mature adult female P. hessei during the different salinity regimes were assessed using a One-Way Analysis of Variance (ANOVA) test. All statistical analyses were performed in R v3.5.1 [19].

3. Results

Water temperatures ranged from 21.5 to 21.7 °C (mean = 21.6 °C) during the mesohaline phase and between 20.2 and 20.8 °C (mean = 20.5 °C) during the polyhaline phase. The mean water temperature during the hypersaline phase was 22.5 °C (range of 21.9 to 23.1 °C) (Table 1). There were no significant temporal differences in water temperature during the study (F = 3.06; p = 0.12).

3.1. Chlorophyll-a Concentrations

Mean total Chl-a concentration during the mesohaline and polyhaline phase of the estuary was estimated at 4.031 µg L−1 (±0.490) and 5.060 µg L−1 (±0.812), respectively. During the hypersaline phase, the total Chl-a concentration ranged from 2.309 to 4.011 µg L−1 (mean = 3.135 µg L−1) (Figure 2). Total Chl-a concentration during the polyhaline phase was significantly higher than during the mesohaline and hypersaline phases (F = 5.147; p < 0.05). There were no significant differences in total Chl-a concentrations between the mesohaline and hypersaline phases of the estuary (p > 0.05).
The mean average contributions of picophytoplankton (<2.0 µm), nanophytoplankton (2–20 µm), and microphytoplankton (>20 µm) to total Chl-a concentration during the mesohaline phase were 53% (±7%), 27 (±5%), and 20% (±2%), respectively (Figure 2). Total Chl-a concentration during the polyhaline phase was dominated by the nanophytoplankton size class, which contributed on average 70% (±4%) of the total pigment (Figure 2). The contribution of picophytoplankton to total Chl-a concentration ranged from 12 to 20% (±4), while microphytoplankton contributed, on average, 14% (±2%) of the total pigment. Finally, during the hypersaline phase of the estuary, picophytoplankton were the dominant component of total Chl-a concentration, contributing between 62 and 66% (mean = 64%) of the total pigment. The average contribution of nanophytoplankton and microphytoplankton to the total Chl-a concentration was 26% (±3) and 20% (±4), respectively (Figure 2).

3.2. Egg Production Rates

The egg production rate (EPR) and clutch size of P. hessei during the study ranged from 5.9 to 28.1 eggs F−1 d−1 and between 12 and 36 eggs sac−1, respectively (Table 2). One-Way Analysis of Variance (ANOVA) indicated that the clutch size (28 to 36 eggs sac−1; mean = 30.1 ± 2.9) and EPR (20.3 to 28.1 eggs F−1 d−1; mean = 23.5 ± 2.2) of P. hessei during the polyhaline phase were significantly higher than during the mesohaline and hypersaline phases of the estuary (F = 28.19; F = 76.39; p < 0.05 in both cases). The mean clutch size of P. hessei during the mesohaline and hypersaline phases was estimated at 18.0 (± 3.1) and 18.4 (±6.2) eggs F−1 d−1, respectively (Table 2). Similarly, the EPR of the copepods varied between 8.8 and 12.0 eggs F−1 d−1 during the mesohaline phase and between 5.9 and 11.3 eggs F−1 d−1 during the hypersaline phase. There were no significant differences in the EPR and clutch size of P. hessei between the mesohaline and hypersaline phases of the estuary (p > 0.05 in both cases).
The egg size of P. hessei during the mesohaline and polyhaline phases ranged from 68.2 to 85 µm (mean = 78.2 ± 7.2 µm) and from 68 to 91 µm (mean = 83.2 ± 9.3 µm), respectively (Table 2). The average egg size during the hypersaline phase was 72.8 ± 4.2 (range—75.3 to 86.3 µm). The mean hatching success of P. hessei during the mesohaline, polyhaline, and hypersaline phases was calculated at 64% (±13.1%), 88 (±4.7%), and 74% (±4.5%), respectively. One-way ANOVA indicated that there were no significant differences in the egg size and hatching success of P. hessei during the three salinity regimes (p > 0.05 in both cases).
The prosome length of adult female P. hessei ranged from 1.05 to 1.30 mm (mean = 1.12 ± 0.08 mm) during the mesohaline phase and between 0.78 and 1.08 mm (mean = 0.91 ± 0.08) during the polyhaline phase. During the hypersaline phase, the mean prosome length of the adult females was 0.88 mm (±0.09; range 0.76 to 1.01 mm). There were no significant temporal patterns observed in the prosome length of adult females during the study (ANOVA; p > 0.05).

4. Discussion

The current investigation was conducted to assess the potential effect of salinity changes on the egg production rate of the sac-spawning calanoid copepod Psuedodiaptomus hessei in a temporarily open/closed estuary (TOCE) located along the southeastern coastline of southern Africa.
The inflow of freshwater into TOCEs during the closed phase contributes to elevated levels of primary production as a result of the increased availability of macronutrients [1,2,3]. It is therefore not surprising that the highest total Chl-a concentration was recorded during the polyhaline phase [Table 1]. During the hypersaline phase, total Chl-a concentrations were lower and dominated by the small picophytoplankton (<2.0 µm) size class. Reduced Chl-a concentrations and the predominance of small picophytoplankton during this phase reflect the oligotrophic nature of the system in the absence of freshwater inflow into the system [1,2]. Similarly, the reduced total Chl-a concentrations during the mesohaline phase are likely the result of the unfavorable light environment conferred by the re-suspension of sediments following freshwater inflow into the system [2]. The unfavorable light environment would favor the growth of the smaller picophytoplankton due to their enhanced light absorption abilities under unfavorable conditions. Estimates of total Chl-a concentration during the three salinity regimes are in the range previously reported for Kasouga Estuary and, indeed, in other TOCEs within the same ecoregion [1,2,4,5].
Field studies indicate that P. hessei can tolerate salinities from <1 to 74, which explains the ability of the copepod to rapidly recolonize estuaries after flushing events and predominate during hypersaline conditions [9]. A previous study indicated that, at a constant temperature, salinity had no marked effect on the respiration rate of P. hessei [20]. The results suggest that variations in salinity alone cannot account for the temporal patterns in egg production rate observed for P. hessei during the current investigation. Variations in egg production rate (EPR) and clutch size in sac spawner copepods have been linked to temperature and the quality and quantity of food [14,21,22]. Given that water temperatures were broadly similar during the different salinity regimes (Table 1), the effect of temperature in accounting for the differences in the clutch size and EPR of P. hessei can largely be discounted. The elevated EPR and clutch size recorded during the polyhaline phase coincided with the highest total Chl-a concentrations (Figure 2 and Table 2). Moreover, during this phase, total Chl-a concentration was dominated by the nanophytoplankton size class (2–20 µm), which is considered to be the optimum size particle for adult P. hessei [18]. In contrast, during the mesohaline and hypersaline phases, total Chl-a concentration was lower and dominated by the picophytoplankton (<2.0 µm) size class, which is considered too small to be efficiently fed on by adult copepods [18]. These results highlight the importance of the quality and quantity of food in regulating the reproductive activities of P. hessei within the estuary. It should be noted that the current investigation only employed Chl-a concentration as a measure of food availability. Within estuarine systems, detritus contributes significantly to the available carbon pools in freshwater-deprived estuaries and is therefore also likely to be an important additional food source for P. hessei within the estuary, particularly during periods of reduced total Chl-a concentration [23].
The egg production rate (EPR) of P. hessei during the various salinity regimes varied from 5.9 to 28.1 eggs F−1 d−1 (Table 2). These estimates are in the range previously reported for the copepod in the nearby permanently open Kariega Estuary within the same ecoregion [14]. The estimates are also in the range reported for other sac spawner copepods. For example, the EPR of Pseudodiaptomus annandalei was 12 eggs F−1 d−1 [24], while that of Eurytemora affinis reached 37.8 eggs F−1 d−1 under laboratory conditions [25]. It is worth noting that the mean clutch size of 30.1 ± 2.9 eggs per sac (range of 28–36 eggs) measured for P. hessei during the polyhaline phase is amongst the highest recorded for egg-carrying copepods. For instance, the clutch size of Pseudodiaptomus pelagicus ranged from 10.9 ± 6.4 to 25.2 ± 1 eggs sac−1 [26]. The highest clutch size for Pseudocalanus newmani was 34 eggs [27], while that of E. affinis was 110 eggs [25].
In contrast to the clutch size and EPR, there were no significant differences in the egg size and hatching success (HS) of P. hessei during the different salinity regimes (Table 2; p > 0.05 in both cases). Differences in egg size within copepod species have been linked to female size and reproductive strategy, with diapause eggs being significantly larger than subitaneous eggs [28]. Since there were no significant differences in the prosome length of adult female P. hessei during the study (Table 2), the absence of any significant differences in the egg size of sac spawning P. hessei during the three salinity regimes is not unexpected. The egg size and high HS (>75%) of P. hessei (>75%) reported here are in the range for other egg-carrying copepods, both locally and internationally [14,29,30].

5. Conclusions

The results of the current investigation indicate that variations in the quantity and quality of food availability mediated by salinity changes have a significant effect on the clutch size and egg production rate of P. hessei in the temporarily open/closed Kasouga Estuary on the southeast coastline of South Africa. Psuedodiaptomus hessei represents an important prey item in the diet of numerous invertebrates and vertebrates in southern African estuaries [6,7]. The high EPR and clutch size of P. hessei recorded during the study may therefore be an adaptation to high predation risk [30,31]. The change in salinity regimes in TOCEs that is anticipated to take place as a result of global warming is thus likely to coincide with the reduced reproductive success of P. hessei within these systems. Given the important ecological role that P. hessei plays within TOCEs, both in terms of grazers of phytoplankton and as a carbon source for a variety of predators [6,7,13,32], a reduction in the reproductive success of the copepod is likely to have far-reaching cascading effects on the ecosystem functioning of TOCEs within the region.

Funding

Funds for this study were obtained from a Rhodes University science grant, fund number IF 2108.

Institutional Review Board Statement

All necessary permits for collection and experimentation were acquired for the described field study from the Department of Agriculture, Forestry and Fisheries, Republic of South Africa (permit reference number: RES2017/46).

Data Availability Statement

Data for the study are available from the author on request.

Acknowledgments

The author would like to acknowledge Rhodes University for providing the facilities to conduct the study.

Conflicts of Interest

The author declares no conflict of interest.

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Figure 1. Geographic location of the temporarily open/closed Kasouga Estuary located along the southeastern coastline of South Africa.
Figure 1. Geographic location of the temporarily open/closed Kasouga Estuary located along the southeastern coastline of South Africa.
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Figure 2. Size-fractionated total chlorophyll-a concentration during the three salinity regimes of the temporarily open/closed Kasouga Estuary on the southeastern coastline of South Africa. Error bars are standard deviation (n = 3).
Figure 2. Size-fractionated total chlorophyll-a concentration during the three salinity regimes of the temporarily open/closed Kasouga Estuary on the southeastern coastline of South Africa. Error bars are standard deviation (n = 3).
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Table
Table 1. Mean water temperature and salinity in the three hydrological phases of the temporarily open/closed Kasouga Estuary located along the southeastern coastline of South Africa. Error bars are standard deviation (n = 3).
Table 1. Mean water temperature and salinity in the three hydrological phases of the temporarily open/closed Kasouga Estuary located along the southeastern coastline of South Africa. Error bars are standard deviation (n = 3).
SalinityTemperatureSalinity
Mesohaline21.6 (±0.1)5 (±0.2)
Polyhaline20.5 (±0.3)24 (±0.5)
Hypersaline22.5 (±0.6)38 (±0.5)
Table
Table 2. Estimates of egg production rate, clutch and egg size, hatching success, and prosome length for the egg sac-spawning calanoid copepod Pseudodiaptomus hessei under varying salinity conditions in the temporarily open/closed Kasouga Estuary located on the southeastern coastline of South Africa. Values in brackets are the mean and SD values; n = number of replicates.
Table 2. Estimates of egg production rate, clutch and egg size, hatching success, and prosome length for the egg sac-spawning calanoid copepod Pseudodiaptomus hessei under varying salinity conditions in the temporarily open/closed Kasouga Estuary located on the southeastern coastline of South Africa. Values in brackets are the mean and SD values; n = number of replicates.
VariableMesohalinePolyhalineHypersaline
Egg production rate (F d−1)
(n = 20)		6.8–12.0
(8.81 ± 2.2)		20.3–28.1
(23.5 ± 2.2)		5.9–11.3
(8.3 ± 2.5)
Clutch size
(n = 20)		13–25
(18.0 ± 3.1) 		26–36
(30.1 ± 2.9)		12–25
(18.4 ± 6.2)
Egg size (µm)75–86
(80.4 ± 4.1)		68–91
(83.2 ± 9.3)		57–85
(78.2 ± 7.2)
Hatching success (%)65–78
(72.8 ± 4.5)		81–94
(88.8 ± 4.7)		48–84
(63.0 ± 13.2)
% spawning females527846
Prosome length (mm)0.91–1.08
(1.12 ± 0.81)		1.05–1.33
(0.91 ± 0.79)		0.76–1.01
(0.88 ± 0.89)
Numbers in bold indicate significant difference (ANOVA; p < 0.05 in both cases).
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Froneman, P.W. The Effect of Salinity on the Egg Production Rate of the Sac-Spawning Calanoid Copepod, Pseudodiaptomus hessei, in a Temporarily Open/Closed Southern African Estuary. Diversity 2023, 15, 263. https://doi.org/10.3390/d15020263

AMA Style

Froneman PW. The Effect of Salinity on the Egg Production Rate of the Sac-Spawning Calanoid Copepod, Pseudodiaptomus hessei, in a Temporarily Open/Closed Southern African Estuary. Diversity. 2023; 15(2):263. https://doi.org/10.3390/d15020263

Chicago/Turabian Style

Froneman, Pierre William. 2023. "The Effect of Salinity on the Egg Production Rate of the Sac-Spawning Calanoid Copepod, Pseudodiaptomus hessei, in a Temporarily Open/Closed Southern African Estuary" Diversity 15, no. 2: 263. https://doi.org/10.3390/d15020263

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