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closed southern African estuary
Estuarine, Coastal and Shelf Science 63 (2005) 73–81 www.elsevier.com/locate/ECSS
Population dynamics of the caridean shrimp Palaemon peringueyi in a temperate temporarily open/closed southern African estuary A.T.F. Bernard*, P.W. Froneman Coastal Research Group, Department of Zoology, Rhodes University, PO Box 94, Grahamstown 6140, South Africa Received 28 June 2004; accepted 22 October 2004
Abstract The population dynamics of the caridean shrimp Palaemon peringueyi were investigated bimonthly over an 11-month period (May 2003–March 2004) in the upper, middle and lower reaches of the temporarily open/closed West Kleinemonde estuary situated on the Eastern Cape coastline of South Africa. Temperature and dissolved oxygen displayed little spatial variability within the estuary ( p O 0.05), while a horizontal gradient in salinity was present ( p ! 0.05). Seasonal variability in the physico-chemical variables was marked ( p ! 0.05). The flood conditions associated with breaching of the estuary at the onset of the study coincided with the lowest abundance (0.08 G 0.05 ind mÿ2) and biomass values (0.05 G 0.02 g wwt mÿ2) of P. peringueyi. Abundance was highest in the lower reach following recruitment of juveniles during the open phase (6.4 G 7.9 ind mÿ2) and biomass greatest in the lower reach at the end of the study (0.56 G 0.73 g wwt mÿ2). Palaemon peringueyi was restricted to the lower and middle reaches of the West Kleinemonde estuary. The lack of any strong correlations between the physico-chemical variables and shrimp abundance and biomass suggests that factors such as habitat type on a local scale, more specifically habitat structural complexity, and recruitment and emigration on a large scale may determine the distribution of P. peringueyi within the estuary. The presence of juvenile P. peringueyi in the estuary 3 months following mouth closure, suggests recruitment through marine overtopping events. The absence of juvenile P. peringueyi within the estuary for the remainder of the study suggests that recruitment through overtopping events is sporadic. The sex ratio did not differ from the expected 1:1 ratio (c2 Z 0.61, p O 0.05). Results of the study further demonstrated that females were significantly larger than the males ( p ! 0.05, mean over entire study: female Z 14.15 G 2.27 mm CL, male Z 13.47 G 1.66 mm CL), suggesting sexual dimorphism. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Palaemon peringueyi; temporarily open/closed estuary; breaching; overtopping; recruitment
1. Introduction The caridean shrimp Palaemon peringueyi (Macpherson, 1990) occurs along the southern African coastline from Walvis Bay on the west coast to Kosi Bay on the east coast (De Villiers et al., 1999). The shrimp has a marine adult phase and a juvenile phase that can either
* Corresponding author. E-mail address: [email protected] (A.T.F. Bernard). 0272-7714/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2004.10.011
be completed in an estuarine or marine environment through the use of inter tidal rock pools (Emmerson, 1985). Peaks in recruitment into permanently open estuaries occur during summer, with a secondary peak occurring in winter (Emmerson, 1986). Recruitment occurs when shrimps are between 6 and 10 mm in total length, with the emigration of adults occurring between 30 and 40 mm of length, which corresponds to a residence time of approx. 9 months (Emmerson, 1986; De Villiers et al., 1999). In permanently open estuaries, P. peringueyi occurs with greater densities
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within the beds of submerged macrophytes that dominate the lower and middle reaches of the systems (Emmerson, 1986; Lubke et al., 1988). The submerged macrophytes provide refuge for adults and juveniles by increasing the structural complexity of the habitat thus restricting predator access (Emmerson, 1986; Rozas and Odum, 1987; Knieb and Wagner, 1994; Walsh and Mitchell, 1998; Adams et al., 1999). Temporarily open/closed estuaries constitute c. 70% of all estuaries along the South African coastline (Whitfield, 1992). For the majority of the year these estuaries are separated from the sea by a sandbar that forms across the mouth. During flood events, or when the water level exceeds the height of the sandbar, the estuaries breach resulting in a dramatic decrease in the water level. During this phase, river conditions dominate throughout the system (Bennett and Branch, 1990; Whitfield, 1992; Perissinotto et al., 2000; Froneman, 2002). The open phase is usually short, depending on the volume of the freshwater flow, with long-shore sand movement in the surf zone, rebuilding the sandbar within weeks (Whitfield, 1992). The majority of temporarily open/closed estuaries along the southeast coast of South Africa are nonperched (i.e. height of the sandbar does not exceed the height of the mean spring tide) and are thus subjected to marine overtopping events during spring high tides or severe storms (Cooper, 2001). These overtopping events not only maintain relatively high salinities (Cooper, 2001; Froneman, 2002), but also create an ephemeral connection with the marine environment. Recent studies have shown that juvenile fish and invertebrate species utilize these events to recruit into temporarily open/ closed estuaries (Bell et al., 2001; Cowley et al., 2001; Vivier and Cyrus, 2001; Froneman, 2004; Kemp and Froneman, 2004). Although Palaemon peringueyi can be regarded as a conspicuous component of the macroinvertebrate community in temporarily open/closed estuaries (Froneman, 2004), there have been, to date, no studies on the population dynamics of this species in these systems. In contrast, a number of studies on the population dynamics of P. peringueyi have been undertaken in permanently open systems (Emmerson, 1983, 1985, 1986). The aim of this study is to gain insight into the population structure and recruitment dynamics of P. peringueyi in a temporarily open/closed estuary, situated along the southeast coastline of South Africa.
2. Materials and methods 2.1. Study site The West Kleinemonde estuary (33 33#S 27 02#E) is classified as a large temporarily open/closed system,
being navigable for approximately 6 km (Fig. 1). The estuary is relatively wide (30–200 m) and shallow (2–3 m in the main channel). The system is predominantly closed although breaching does occur following heavy rains. A more or less pronounced salinity gradient is present, with the upper reaches being characterized by low salinities (5–10). Due to the non-perched structure (see Cooper, 2001) of the sandbank that closes this system, overtopping occurs frequently and as a result the lower reaches are characterized by high salinities (25–30). Temperature variability exhibits a strong seasonal component ranging between 22 C and 29 C in summer and 12 C and 15 C in winter. 2.2. Physico-chemical environment Temperature, salinity and dissolved oxygen were measured bimonthly over an 11-month period (May 2003–March 2004) in the lower, middle and upper reaches of the West Kleinemonde estuary. Temperature ( C) and dissolved oxygen (mg O2Lÿ1) values were recorded using a YSI 550 oxygen meter, and salinity with a hand held refractometer (Atago S10). The physico-chemical variables were recorded in triplicate within each reach of the estuary. Non-parametric ANOVAs (Kruskal–Wallis, Statistica, version 6) were used to determine if the physico-chemical variables varied significantly between the reaches and the six samples. 2.3. Sampling method Sampling occurred bimonthly over an 11-month period (May 2003–March 2004), with three stations being occupied within the lower, middle and upper reaches of the estuary. Two sampling methods were employed to investigate the biomass, abundance, length frequency distribution, sex length relationships and sex ratio of Palaemon peringueyi. On the first four occasions, samples were collected using a 4 m seine net (mesh size 0.5 mm) pulled parallel to the shore over a distance of 5 m. The last two samples were collected using a dip net (mouth area Z 0.3 ! 0.3 m, mesh size Z 1.0 mm) pushed over a distance of 5 m parallel to the shore. To account for the differences in net size, shrimps were collected from five distances from the shore (0, 1, 2, 3, 4 m) for each replicate using the dip net. A comparison between the catch (ind mÿ2) of the two sampling methods was conducted within the lower reach of the Kariega estuary. A random block design was used focusing on vegetated (O70% submerged vegetation cover) and non-vegetated areas (!30% submerged vegetation cover). The results of the statistical analysis revealed no significant difference in catch per unit effort between the different methods in the vegetated areas (seine net: n Z 3, mean Z 58.8 G 29.3 ind mÿ2; dip
A.T.F. Bernard, P.W. Froneman / Estuarine, Coastal and Shelf Science 63 (2005) 73–81
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Fig. 1. Geographic location of the temporarily open/closed West Kleinemonde estuary on the southeastern seaboard of southern Africa. Positions of the sampling stations occupied in the lower, middle and upper reaches are indicated.
net: n Z 3, mean Z 46.2 G 14.7 ind mÿ2; Mann–Whitney U test p O 0.05) and the non-vegetated areas (seine net: n Z 3, mean Z 21.6 G 12.3 ind mÿ2; dip net: n Z 3, mean Z 42.4 G 35.1 ind mÿ2; Mann–Whitney U test p O 0.05). After collection, samples were fixed in a 5% buffered (hexamine) formalin solution for later analysis in the laboratory. When less than 100 individuals were caught the entire sample was analyzed, while 1/2 to 1/4 subsamples were analyzed when the samples contained greater than 100 shrimps. During each sampling trip visual estimates of submerged vegetation cover (%) and channel characteristics within the sampled areas were made.
carapace and the posterior tip of the telson), carapace length (CL, defined as the region from the anterior tip of the carapace to the dorsal midline of the posterior margin of the carapace), wet weight (wwt) and dry weight (dwt). The length measurements (mm) were made using electronic Vernier calipers. Dry weight was measured using a Sauter AR 100 microbalance after oven drying individuals at 80 C for 24 h. Regression relationships between selected measurements were calculated using the statistical analysis program Statistica (version 6).
2.4. Morphometric relationships
Total abundance and biomass of Palaemon peringueyi within the lower, middle and upper reaches of the estuary were calculated using the swept area method. The area sampled was calculated by multiplying the effective width of the trawl by the towing distance. To standardize the data, the number of individuals (for
One hundred shrimp ranging in size from 3.4 to 18.0 mm CL were used to determine the morphometric relationships. Measurements made included total length (TL, defined as the distance between anterior tip of the
2.5. Abundance and biomass
A.T.F. Bernard, P.W. Froneman / Estuarine, Coastal and Shelf Science 63 (2005) 73–81
Shrimps larger than 9 mm CL were measured and their sex determined by the presence or absence of an appendix masculina (A.M.) on the endopod of the second pleopod (Pakhomov et al., 2000). Below 9 mm, identification of the rami became impossible under the dissecting microscope (mag Z 10!) and thus all individuals smaller than 9 mm (CL) were considered to be juveniles. Following this, the male to female sex ratio was determined and a chi-squared test was used to determine if the observed ratios differed from the expected 1:1 ratio. 2.7. Length frequency analysis For the length frequency analysis the carapace length (CL) of the Palaemon peringueyi were measured using electronic Vernier calipers. The length frequency distributions were constructed using 0.5 mm intervals of carapace length. A two-way ANOVA and post hoc tests (Fishers LSD) were used to look at the interactive effects of time (month) and area (reach) on the mean size of the shrimp. To establish if there was any difference in the mean size of male and female shrimp each sample a t-test for independent samples by groups was used (Statistica, version 6).
3. Results 3.1. Environmental variables The upper reach of the estuary was characterized by steep banks, a narrow channel, and sparse submerged vegetation cover (cover ! 10% of the total surface area). The middle reach of the estuary was relatively shallow (depth ! 1 m), and was characterized by
Temperaure (°C)
2.6. Sex ratio
extensive submerged vegetation cover (cover O 70% of total surface area). The vegetation cover in the lower reach was patchy and thin (cover ! 20% of total surface area). A gradual increase in submerged vegetation cover was observed throughout the estuary during the study period. One week prior to the first sampling trip, the estuary breached which resulted in a dramatic decrease in the water level in the upper and middle reaches of the estuary. As a result, only the lower reach was sampled. During this period salinities were highly variable (6.5– 32), and low dissolved oxygen concentrations prevailed (5.5 G 0.7 mg O2Lÿ1). The temperature remained relatively warm and stable (18 G 1.4 C). The estuary remained open until mid June. Over the course of the study, temperature and dissolved oxygen displayed little spatial variability (Fig. 2). A distinct spatial pattern in salinity values was observed, with the lower reaches being characterized by higher salinities (mean Z 17.4 G 5.2) than the upper reaches (mean Z 13.9 G 3.4; Kruskal–Wallis ANOVA, p ! 0.05). Results from the statistical analysis indicated that the physico-chemical variables expressed strong seasonal variability (Kruskal–Wallis ANOVA, p ! 0.05 in all cases). Temperature expressed a summer (January 2004) maximum of c. 31 C and a spring (September 2003) minimum of c. 15 C. The lowest salinities were recorded in summer (January 2004),
35 30 25 20 15 10 5 0
Salinity
abundance) or the total wet weight of the individuals (for biomass) captured at a sampling station was divided by the area sampled. A mean abundance and biomass of the three stations occupied within each reach was then determined. Abundance results were expressed as individuals per m2 (ind mÿ2), and biomass in grams wet weight per m2 (g wwt mÿ2). Wet weight was measured using a Sauter AR100 microbalance. Two-way ANOVAs and post hoc tests (Fishers LSD; Statistica, version 6) were used to determine the interactive effects of time (month) and area (reach) on the abundance and biomass values of Palaemon peringueyi within the estuary. Spearman’s correlation analyses were used to determine the significance of the relationships between the physico-chemical variables and abundance and biomass.
35 30 25 20 15 10 5 0
Dissolved oxygen (mg O2 L-1)
76
A
B
12 10
18 May 2003 8 July 2003 5 Sep 2003 6 Nov 2003 23 Jan 2004 21 March 2004
C
8 6 4 2 0 Lower
Middle
Upper
Reach
Fig. 2. Trends in mean (GSD) temperature (A), salinity (B) and dissolved oxygen (C) recorded in the lower, middle and upper reaches of the West Kleinemonde estuary. Arrows indicate open phase.
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3.2. Morphometric relationships The results from the regression analysis showed a strong relationship between total length and carapace length (r2 Z 0.99, p ! 0.001), and dry weight and wet weight (r2 Z 0.99, p ! 0.001; Table 1). 3.3. Abundance and biomass In the first sample (May 2003) Palaemon peringueyi were very rare, with a total of 10 shrimps being caught in the lower reach. Throughout the study P. peringueyi were restricted to the lower and middle reaches of the estuary. An exception was recorded during winter (July 2003), with a single individual being recorded in the upper reach. Maximum abundances of Palaemon peringueyi were recorded within the lower reach during the July sampling trip (mean Z 6.4 G 7.9 ind mÿ2), while minimum abundances were recorded in the lower reach at the beginning of the study, May 2003 (mean Z 0.08 G 0.05 ind mÿ2; Fig. 3A). Results from the twoway ANOVA indicated that the between effects of time (month) and area (reach) on abundance of P. peringueyi were significant ( p ! 0.05). Post hoc analysis (Fishers LSD) showed that there was no significant difference between the abundance of P. peringueyi in the lower and middle reaches although both differed significantly from the upper reach values. Similarly, the abundance of P. peringueyi recorded during July 2003 was significantly greater than all the other samples collected. The maximum biomass values (mean Z 0.56 G 0.73 g mÿ2) were recorded in the lower reaches in March 2004, while the lowest were recorded during the open phase in May 2003 (mean Z 0.05 G 0.02 g mÿ2; Fig. 3B). Results Table 1 Standard linear relationships for carapace length and total length, and wet weight and dry weight in P. peringueyi n
2
r
Abundance (ind m-2)
ranging between 8 in the upper reaches and 15 in the lower reaches. This period coincided with the most marked horizontal gradient in salinity. For the remainder of the study the estuary was predominantly mesohaline (15–20). Dissolved oxygen peaked in winter (mean Z 8.13 G 0.53 mg O2Lÿ1), with the highest concentrations generally being found in the middle reaches. The lowest dissolved oxygen concentrations were recorded in summer (mean Z 4.97 G 0.27 mg O2Lÿ1).
16 14 12 10 8 6 4 2 0
Biomass (g wwt m-2)
A.T.F. Bernard, P.W. Froneman / Estuarine, Coastal and Shelf Science 63 (2005) 73–81
1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0
A
18 May 2003 8 July 2003 5 Sep 2003 6 Nov 2003 23 Jan 2004 21 March 2004
B
Lower
Middle
Upper
Reach
Fig. 3. Trends in mean (GSD) abundance (A, ind mÿ2) and biomass (B, g wwt mÿ2) of Palaemon peringueyi within the lower, middle and upper reaches of the West Kleinemonde estuary. Arrow indicates open phase.
from the two-way ANOVA showed that the between effects of time (month) and area (reach) on Palaemon peringueyi biomass were significant ( p ! 0.05). The post hoc analysis (Fishers LSD) showed that the mean total biomass value from the lower reach, 0.29 (G0.39) g wwt mÿ2, was significantly greater than the middle reach, 0.11 (G0.1) g wwt mÿ2, and the upper reach, 0.0009 (G0.0002) g wwt mÿ2 ( p ! 0.05), while temporal variation in biomass was not significant ( p O 0.05). Results for the Spearman’s correlation analysis showed that only salinity and biomass were significantly correlated, with the biomass of Palaemon peringueyi increasing with an increase in salinity (R Z 0.34, p ! 0.05). The remainder of the relationships between the physico-chemical variables and abundance and biomass were not significant. 3.4. Sex ratios There was no significant difference between the male to female ratios from the lower and middle reaches (t-test for independent samples, p ! 0.05). As a result the data were pooled. The mean male:female ratio (1.07 G 0.38:1), over the study period, did not differ from the expected 1:1 ratio (c2 Z 0.61, p O 0.05). 3.5. Size frequency analysis
p-Value Regression equation
Carapace length 100 0.99 !0.001 TLZ0:668C2:346!CL (CL)–total length (TL) Wet weight (wwt)–dry 100 0.99 !0.001 dwtZ0:00003C0:203!wwt weight (dwt)
The population size structure of Palaemon peringueyi within the estuary reflected the loss of cohort of large individuals when the estuary breached and the subsequent recruitment and growth of a cohort of juveniles to mature adults within the study period (Figs. 4–6).
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4. Discussion Compared to permanently open estuaries within the same geographic region, the temporarily open/closed
Percentage of total numbers caught
Open
Closed
100 80 60 40 20 0
03 003 004 003 v 2003 n 2004 l 20 ar 2 o ay 2 ep 2 a 8 Ju 6N 5S 18M 23 J 21 M Juvenile Female Date Male
Fig. 4. Percentage contribution of juveniles, females and males to the Palaemon peringueyi population in the West Kleinemonde estuary, in relation to mouth state. Note overtopping events occurred at least once on a monthly basis. Z open phase, Z closed phase.
Open
Carapace length (mm)
There was strong evidence for length based sexual dimorphism (Fig. 7), with the females being significantly larger ( p ! 0.05, 14.15 G 2.27 mm CL) than the males (13.47 G 1.66 mm CL) for all months except May and July 2003 when juveniles dominated the P. peringueyi community (t-test for independent samples by groups, p ! 0.05). As a result, the length frequency analysis was done separately for juveniles, females and males. Juveniles dominated the total catch during July and September 2003, contributing between 100 and 85% of the total catch, respectively (Fig. 4). In both the July and September 2003 samples, shrimp from the middle reaches were significantly larger (mean Z 5.12 G 1.24 and 8.18 G 0.54 mm CL, respectively) than those recorded in the lower reaches (mean Z 4.14 G 0.6 and 6.42 G 1.25 mm CL, respectively; one-way ANOVA, p ! 0.05 in both cases). Following this, juveniles contributed less than 5% of the total catch in November, and were not recorded in the January and March 2004 samples (Fig. 4). Length frequency analysis revealed that juvenile P. peringueyi were recorded in the estuary 3 months after mouth closure suggesting that some degree of recruitment had occurred through overtopping (Figs. 4, 6). The smallest individuals were recorded during July (min Z 2.96 mm CL, mean Z 4.45 G 0.98 mm CL), while the largest were recorded at the end of the study in March 2004 (female mean Z 15.5 G 1.33 mm CL, male mean Z 14.35 G 1.2 mm CL). Female and male P. peringueyi did not express spatial patterns in mean size within the estuary (one-way ANOVA, p ! 0.05 in all cases).
Closed
17 16 15 14 13 12 11 10 9 8 7 6 5 4 3 2 1 0
4 003 003 004 003 003 200 ly 2 ov 2 3 Jan 2 ep 2 arch 8 Ju 6N 5S 2 21 M
ay 2
18 M
Date
Juvenile Male Female
Fig. 5. Mean carapace length of juvenile, female and male Palaemon peringueyi within the West Kleinemonde estuary for the six samples. Note overtopping events occurred at least once on a monthly basis. Z open phase, Z closed phase.
West Kleinemonde estuary supports a much lower biomass of Palaemon peringueyi. For example, Emmerson (1986) reported that within the Zostra capensis beds of the permanently open Sundays and Swartkops river estuaries (eastern Cape) the annual biomass of P. peringueyi was 2.69 g dwt mÿ2 and 2.16 g dwt mÿ2, respectively. These values are considerably higher than the mean P. peringueyi biomass from the lower and middle reaches found over this study period (0.2 G 0.13 g wwt mÿ2, or 0.04 G 0.026 g dwt mÿ2 calculated using the wwt:dwt regression equation in Table 1). A factor that could contribute to the disparity in biomass observed is habitat type sampled. The present study focused on the majority of submerged habitat types, vegetated and non-vegetated, within the West Kleinemonde estuary, while Emmerson (1986) focused on the Z. capensis beds, that are known to contain higher densities of grass shrimp than the surrounding nonvegetated areas (Emmerson, 1986; Lubke et al., 1988; Walsh and Mitchell, 1998). Following this, the lower biomass could reflect restricted recruitment into temporarily open/closed estuaries, caused by the presence of the sandbar, compared to the permanently open estuaries where recruitment is uninhibited and only dependent on the presence of juvenile P. peringueyi in the surf-zone adjacent the estuary mouth. A number of studies have demonstrated that breaching events in temporarily open/closed estuaries result in a significant disturbance to estuarine biological communities culminating in the loss of plankton (Perissinotto et al., 2000; Kibirige and Perissinotto, 2003; Froneman, 2004), benthic invertebrates (De Decker, 1987) and fish biomass (Whitfield, 1998) to the marine environment. Emmerson (1986) found that flooding severely affected the biomass of Palaemon peringueyi within the permanently open Kromme river estuary. Thus, the virtual absence of shrimp during the open phase could be attributed to the flooding associated with the breaching of the West Kleinemonde estuary. The impact of the
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A.T.F. Bernard, P.W. Froneman / Estuarine, Coastal and Shelf Science 63 (2005) 73–81 Length at recruitment
Length at emigration
40 18 May 2003
30 20 10 0 160
8 Jul 2003
140 120 40 20 0 40
5 Sep 2003
Number of observations
30 20 10 0 40
6 Nov 2003
30 20 10 0 40
23 Jan 2004
30 20 10 0 40
21 Mar 2004
30 20
Juvenile
10
Female Male
2.5 3.0<=x < 3.5<=x 3.0 < 4.0<=x 3.5 < 4.5<=x 4.0 < 5.0<=x 4.5 < 5.5<=x 5.0 < 6.0<=x 5.5 < 6.5<=x 6.0 < 7.0<=x 6.5 < 7.5<=x 7.0 < 8.0<=x 7.5 < 8.5<=x 8.0 < 9. <=x 8.5 9.50<= <9.0 x 10 <= <9 . x .5 10 0<= <10 . x . 11 5<= <10 0 . x . 11 0<= <11 5 .5< x< .0 12 = 11 . x . 12 0<= <12 5 . x . 13 5<= <12 0 . x . 13 0<= <13 5 . x . 14 5<= <13 0 .0< x< .5 14 = 14 . x . 15 5<= <14 0 . x . 15 0<= <15 5 . x . 16 5<= <15 0 . x . 16 0<= <16 5 . x . 17 5<= <16 0 .0< x< .5 17 = 17 . x . 18 5<= <17 0 . x . 18 0<= <18 5 .5< x< .0 =x 18. <1 5 9.0
0
Length classes (CL) Fig. 6. Stacked length frequency histograms of juvenile, female and male Palaemon peringueyi within the West Kleinemonde estuary for the six samples. Lines represent approximate carapace length at recruitment (2.356 mm) and emigration (12.5 mm), calculated from TL estimates (Emmerson, 1986) using a CL:TL regression formula (Table 1). Note overtopping events occurred at least once on a monthly basis.
flooding is also reflected in the size structure of the P. peringueyi population with mature individuals disappearing from the estuary following the breaching event (Fig. 6). The tidal phase following mouth opening is usually associated with recruitment of estuarine dependent marine breeding organisms (Whitfield, 1998; Froneman, 2004). This agrees with the present findings, which showed P. peringueyi juveniles dominate the catches following the breaching event (Figs. 4, 6).
It is important to note breaching events likely pose the only mechanism by which estuarine organisms can migrate from the estuary to the marine environment in temporarily open/closed systems. As a result under conditions of prolonged mouth closure, the reproductive potential of those species with an obligate marine phase will be reduced. Emmerson (1986) suggested that Palaemon peringueyi emigrate from permanently open estuaries when 30–40 mm in total length, which corresponds to
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5 Sep 2003
6 Nov 2003
23 Jan 2004
21 March 2004
20 p>0.05
P<0.05
p<0.001
p<0.001
p<0.05
18 16 14 12 10 8 f
m
Sex
f
m
Sex
f
m
Sex
f
m
Sex
f
m
Sex
Fig. 7. Mean carapace length of female (F) and male (M) Palaemon peringueyi within West Kleinemonde estuary. Error bars denote 0.95% confidence interval, p values provided on graph.
a residence time of c. 9 months. Results from the length frequency analysis indicate that the majority of the P. peringueyi within the West Kleinemonde estuary obtained a length of between 30 and 40 mm (total length) within 7 months of the study (Fig. 6). Results of subsequent studies in the West Kleinemonde estuary indicate that the system remained closed for up to 15 months after the initial breaching event in May 2003. Marine overtopping events pose an alternative mechanism through which larvae and juveniles of estuarine dependent invertebrate and vertebrate species can recruit into temporarily open/closed estuaries (Whitfield, 1998; Bell et al., 2001; Cowley et al., 2001; Vivier and Cyrus, 2001; Froneman, 2004; Kemp and Froneman, 2004). A recent study conducted by Kemp and Froneman (2004) in the temporarily open/closed West Kleinemonde estuary found that post larvae (CL ! 2 mm) Palaemon peringueyi recruit into the estuary during overtopping events. During the present study period overtopping occurred on a monthly basis, although the intensity and duration of the events were highly variable (P. Cowley, pers comm). The presence of juvenile P. peringueyi in the estuary up to 3 months following mouth closure (Figs. 4, 6) provides further support for the findings of Kemp and Froneman (2004). Although recruitment of P. peringueyi into permanently open estuaries peaks during summer and winter months (Emmerson, 1986), the shrimp does demonstrate continuous recruitment (Emmerson, 1985). The virtual absence of juveniles from the last two samples, undertaken during the summer months, suggests that overtopping is not always associated with recruitment. These facts suggest that while overtopping can create an ephemeral means of recruitment, the establishment of a link to the marine environment following breaching represented the primary mechanism of recruitment for P. peringueyi into the West Kleinemonde estuary during the present study (Figs. 3, 6). A spatial pattern in the size distribution of juvenile Palaemon peringueyi can be seen in the July and September samples, with the middle reach having larger
individuals than the lower reach (Fig. 5). The observed pattern may reflect a re-colonization process, with the shrimps that have established themselves within the lower reaches, following recruitment, migrating up the estuary. The size distribution pattern was not observed following September, this could be a result of reduced recruitment as well as the maturation of the P. peringueyi population. The lack of any strong relationship between the physico-chemical variables and Palaemon peringueyi biomass and abundance during this investigation suggests the distribution could be related to habitat preference rather than physical constraints. The importance of submerged vegetation as a habitat for a variety of estuarine invertebrates is well documented (De Villiers et al., 1999). During the study submerged vegetation cover within the West Kleinemonde estuary was most extensive at the station occupied in the middle and lower reaches. It is possible that the observed pattern in P. peringueyi distribution, abundance and biomass during the study was associated with the presence of submerged macrophytes, which likely provide refuge against predators. The absence of P. peringueyi from the upper reach could thus be related to the sparse vegetation cover (!10% of the total surface area sampled). This distribution pattern is similar to what is seen in permanently open estuaries, where the density of P. peringueyi in the upper reach is considerably lower than the densities recorded in the middle and lower reaches (Emmerson, 1986; Lubke et al., 1988). Variations in size and growth rates between male and female shrimp has been described on a number of occasions (Alon and Stancyk, 1982; Oh et al., 1999). The present study presents evidence for length based sexual dimorphism in Palaemon peringueyi within the temporarily open/closed West Kleinemonde estuary (Fig. 7). Emmerson (1985) found that while male P. peringueyi (25 mm TL or 10.34 mm CL) attain sexual maturity at a shorter length than females (41 mm TL or 17 mm CL), there was no significant difference in the mean size of
A.T.F. Bernard, P.W. Froneman / Estuarine, Coastal and Shelf Science 63 (2005) 73–81
males and females sampled from tidal pools. Oh et al. (1999) found that female Crangon crangon grew faster and attained a larger size at age than the males. The significantly larger size of female P. peringueyi recorded during this study may reflect differences in male and female growth rates. Results of the study indicate that the breaching event was essential for the recruitment of Palaemon peringueyi into the temporarily open/closed West Kleinemonde estuary, and, possibly of more importance to the shrimp population within the estuary, breaching allows emigration to the marine environment where the sexually mature individuals can reproduce. While there is some evidence that frequent overtopping events may also be associated with the recruitment of P. peringueyi into the estuary, the low frequency of occurrence of juveniles in the system following these events suggest that it is not the principal method of recruitment. Future studies should begin to assess the growth and mortality of P. peringueyi within temporarily open/closed estuaries.
Acknowledgements Thanks are extended to B. Donavan, J. Kemp and L. Jackson for their assistance with the field sampling. Funding for this research was acquired from the Joint Research Council (JRC) of Rhodes University. Finally I would like to thank Prof. A.N. Hodgson for his advice during the early stages of this study.
References Adams, J., Bate, G., O’callagham, M., 1999. Primary producers. In: Allanson, B.R., Baird, D. (Eds.), Estuaries of South Africa. Cambridge University Press, Cambridge, United Kingdom, pp. 91– 198. Alon, N.C., Stancyk, S.E., 1982. Variation in the life-history patterns of the grass shrimp Palaemonetes pugio in two South Carolina estuarine systems. Marine Biology 68, 265–276. Bell, K.N.I., Cowley, P.D., Whitfield, A.K., 2001. Seasonality in frequency of marine access to an intermittently open estuary: implications for recruitment strategies. Estuarine, Coastal and Shelf Science 52, 327–337. Bennett, B.A., Branch, G.M., 1990. Relationships between production and consumption of prey species by resident fish in the Bot, a cool temperate South African estuary. Estuarine, Coastal and Shelf Science 31, 139–155. Cooper, J.A.G., 2001. Geomorphological variability among microtidal estuaries from the wave-dominated South African coast. Geomorphology 40, 99–122. Cowley, P., Whitfield, A.K., Bell, K.N.I., 2001. The surf zone ichthyoplankton adjacent to the mouth of a predominantly closed southern African estuary, with evidence of recruitment during marine overwash events. Estuarine, Coastal and Shelf Science 52, 1–10. De Decker, H.P., 1987. Breaching of the mouth of the Bot River estuary, South Africa: impact on its benthic macrofaunal
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communities. Transactions of the Royal Society of South Africa 46, 231–250. De Villiers, C., Hodgson, A.N., Forbes, A., 1999. Studies of estuarine macroinvertebrates. In: Allanson, B.R., Baird, D. (Eds.), Estuaries of South Africa. Cambridge University Press, Cambridge, United Kingdom, pp. 167–208. Emmerson, W.D., 1983. Tidal exchange of two decapod larvae, P. peringueyi pacificus (Caridea) and Upogebia Africana (Thalassinidae) between the Swartkops river estuary and adjacent coastal waters. South African Journal of Zoology 18, 326–330. Emmerson, W.D., 1985. Seasonal abundance, growth and production of Palaemon pacificus (Stimpson) in eastern cape tidal pools. South African Journal of Zoology 20, 221–231. Emmerson, W.D., 1986. The ecology of Palaemon pacificus (Stimpson) associated with Zostra capensis, Setchell. Transactions of the Royal Society of South Africa 46, 79–97. Froneman, P.W., 2002. Food web structure in three contrasting estuaries determined using stable isotope (13C). African Journal of Aquatic Science 27, 107–115. Froneman, P.W., 2004. Zooplankton community structure and biomass in a southern African temporarily open/closed estuary. Estuarine, Coastal and Shelf Science 60, 125–132. Kemp, J.O.G., Froneman, P.W., 2004. Recruitment of ichthyoplankton and macrozooplankton during overtopping events into a temporarily open/closed southern African estuary. Estuarine, Coastal and Shelf Science 61, 529–537. Kibirige, I., Perissinotto, R., 2003. The zooplankton community of the Mepanjati Estuary, a South African temporarily open/closed system. Estuarine, Coastal and Shelf Science 58, 724–741. Knieb, R.T., Wagner, S.L., 1994. Nekton use of vegetated marsh habitats at different stages of tidal inundation. Marine Ecological Progress Series 106, 227–238. Lubke, R.A., Gess, F.W., Bruton, M.N., 1988. A Field Guide to the Eastern Cape Coast. Grahamstown Center of the Wildlife Society of Southern Africa, Grahamstown, South Africa, 559 pp. Macpherson, E., 1990. The validation of Palaemon peringueyi (Stebbing 1915) from South African waters and its relationships with Palaemon pacificus (Stimpson 1860) (Decapoda, Palaemonidae). Journal of Natural History 24, 627–634. Oh, C.-W., Hartnoll, R.G., Nash, R.D.M., 1999. Population dynamics of the common shrimp, Crangon crangon (L.), in Port Erin Bay, Isle of Man, Irish Sea. ICES Journal of Marine Systems 56, 718–733. Pakhomov, E.A., Kuun, P., McQuaid, C.D., 2000. Biology of the bottom dwelling shrimp Nauticaris marionis Bate, 1888, at the sub-Antarctic Prince Edward Islands. Polar Biology 23, 522–530. Perissinotto, R., Walker, D.R., Webb, P., Wooldridge, T.H., Bally, R., 2000. Relationships between zoo- and phytoplankton in a warm temperate, semi-permanently closed estuary, South Africa. Estuarine, Coastal and Shelf Science 51, 1–11. Rozas, L.P., Odum, W.E., 1987. The role of submerged aquatic vegetation in influencing the abundance of nekton on contiguous tidal fresh-water marshes. Journal of Experimental Marine Biology and Ecology 114, 289–300. Vivier, L., Cyrus, D.P., 2001. Juvenile fish recruitment through wave overtopping into a closed subtropical estuary. African Journal of Aquatic Science 26, 109–113. Walsh, C.J., Mitchell, B.D., 1998. Factors associated with variations in abundance of epifaunal caridean shrimps between and within seagrass meadows. Marine and Freshwater Research 49, 769–777. Whitfield, A.K., 1992. A characterization of South African estuarine systems. South African Journal of Aquatic Sciences 18, 89–103. Whitfield, A.K., 1998. Biology and Ecology of Fishes in Southern African Estuaries. Ichthyological Monographs, vol. 2. J.L.B. Smith Institute of Ichthyology, 223 pp.
Population dynamics of the caridean shrimp Palaemon peringueyi in a temperate temporarily open/closed southern African estuary A.T.F. Bernard*, P.W. Froneman Coastal Research Group, Department of Zoology, Rhodes University, PO Box 94, Grahamstown 6140, South Africa Received 28 June 2004; accepted 22 October 2004
Abstract The population dynamics of the caridean shrimp Palaemon peringueyi were investigated bimonthly over an 11-month period (May 2003–March 2004) in the upper, middle and lower reaches of the temporarily open/closed West Kleinemonde estuary situated on the Eastern Cape coastline of South Africa. Temperature and dissolved oxygen displayed little spatial variability within the estuary ( p O 0.05), while a horizontal gradient in salinity was present ( p ! 0.05). Seasonal variability in the physico-chemical variables was marked ( p ! 0.05). The flood conditions associated with breaching of the estuary at the onset of the study coincided with the lowest abundance (0.08 G 0.05 ind mÿ2) and biomass values (0.05 G 0.02 g wwt mÿ2) of P. peringueyi. Abundance was highest in the lower reach following recruitment of juveniles during the open phase (6.4 G 7.9 ind mÿ2) and biomass greatest in the lower reach at the end of the study (0.56 G 0.73 g wwt mÿ2). Palaemon peringueyi was restricted to the lower and middle reaches of the West Kleinemonde estuary. The lack of any strong correlations between the physico-chemical variables and shrimp abundance and biomass suggests that factors such as habitat type on a local scale, more specifically habitat structural complexity, and recruitment and emigration on a large scale may determine the distribution of P. peringueyi within the estuary. The presence of juvenile P. peringueyi in the estuary 3 months following mouth closure, suggests recruitment through marine overtopping events. The absence of juvenile P. peringueyi within the estuary for the remainder of the study suggests that recruitment through overtopping events is sporadic. The sex ratio did not differ from the expected 1:1 ratio (c2 Z 0.61, p O 0.05). Results of the study further demonstrated that females were significantly larger than the males ( p ! 0.05, mean over entire study: female Z 14.15 G 2.27 mm CL, male Z 13.47 G 1.66 mm CL), suggesting sexual dimorphism. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Palaemon peringueyi; temporarily open/closed estuary; breaching; overtopping; recruitment
1. Introduction The caridean shrimp Palaemon peringueyi (Macpherson, 1990) occurs along the southern African coastline from Walvis Bay on the west coast to Kosi Bay on the east coast (De Villiers et al., 1999). The shrimp has a marine adult phase and a juvenile phase that can either
* Corresponding author. E-mail address: [email protected] (A.T.F. Bernard). 0272-7714/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2004.10.011
be completed in an estuarine or marine environment through the use of inter tidal rock pools (Emmerson, 1985). Peaks in recruitment into permanently open estuaries occur during summer, with a secondary peak occurring in winter (Emmerson, 1986). Recruitment occurs when shrimps are between 6 and 10 mm in total length, with the emigration of adults occurring between 30 and 40 mm of length, which corresponds to a residence time of approx. 9 months (Emmerson, 1986; De Villiers et al., 1999). In permanently open estuaries, P. peringueyi occurs with greater densities
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within the beds of submerged macrophytes that dominate the lower and middle reaches of the systems (Emmerson, 1986; Lubke et al., 1988). The submerged macrophytes provide refuge for adults and juveniles by increasing the structural complexity of the habitat thus restricting predator access (Emmerson, 1986; Rozas and Odum, 1987; Knieb and Wagner, 1994; Walsh and Mitchell, 1998; Adams et al., 1999). Temporarily open/closed estuaries constitute c. 70% of all estuaries along the South African coastline (Whitfield, 1992). For the majority of the year these estuaries are separated from the sea by a sandbar that forms across the mouth. During flood events, or when the water level exceeds the height of the sandbar, the estuaries breach resulting in a dramatic decrease in the water level. During this phase, river conditions dominate throughout the system (Bennett and Branch, 1990; Whitfield, 1992; Perissinotto et al., 2000; Froneman, 2002). The open phase is usually short, depending on the volume of the freshwater flow, with long-shore sand movement in the surf zone, rebuilding the sandbar within weeks (Whitfield, 1992). The majority of temporarily open/closed estuaries along the southeast coast of South Africa are nonperched (i.e. height of the sandbar does not exceed the height of the mean spring tide) and are thus subjected to marine overtopping events during spring high tides or severe storms (Cooper, 2001). These overtopping events not only maintain relatively high salinities (Cooper, 2001; Froneman, 2002), but also create an ephemeral connection with the marine environment. Recent studies have shown that juvenile fish and invertebrate species utilize these events to recruit into temporarily open/ closed estuaries (Bell et al., 2001; Cowley et al., 2001; Vivier and Cyrus, 2001; Froneman, 2004; Kemp and Froneman, 2004). Although Palaemon peringueyi can be regarded as a conspicuous component of the macroinvertebrate community in temporarily open/closed estuaries (Froneman, 2004), there have been, to date, no studies on the population dynamics of this species in these systems. In contrast, a number of studies on the population dynamics of P. peringueyi have been undertaken in permanently open systems (Emmerson, 1983, 1985, 1986). The aim of this study is to gain insight into the population structure and recruitment dynamics of P. peringueyi in a temporarily open/closed estuary, situated along the southeast coastline of South Africa.
2. Materials and methods 2.1. Study site The West Kleinemonde estuary (33 33#S 27 02#E) is classified as a large temporarily open/closed system,
being navigable for approximately 6 km (Fig. 1). The estuary is relatively wide (30–200 m) and shallow (2–3 m in the main channel). The system is predominantly closed although breaching does occur following heavy rains. A more or less pronounced salinity gradient is present, with the upper reaches being characterized by low salinities (5–10). Due to the non-perched structure (see Cooper, 2001) of the sandbank that closes this system, overtopping occurs frequently and as a result the lower reaches are characterized by high salinities (25–30). Temperature variability exhibits a strong seasonal component ranging between 22 C and 29 C in summer and 12 C and 15 C in winter. 2.2. Physico-chemical environment Temperature, salinity and dissolved oxygen were measured bimonthly over an 11-month period (May 2003–March 2004) in the lower, middle and upper reaches of the West Kleinemonde estuary. Temperature ( C) and dissolved oxygen (mg O2Lÿ1) values were recorded using a YSI 550 oxygen meter, and salinity with a hand held refractometer (Atago S10). The physico-chemical variables were recorded in triplicate within each reach of the estuary. Non-parametric ANOVAs (Kruskal–Wallis, Statistica, version 6) were used to determine if the physico-chemical variables varied significantly between the reaches and the six samples. 2.3. Sampling method Sampling occurred bimonthly over an 11-month period (May 2003–March 2004), with three stations being occupied within the lower, middle and upper reaches of the estuary. Two sampling methods were employed to investigate the biomass, abundance, length frequency distribution, sex length relationships and sex ratio of Palaemon peringueyi. On the first four occasions, samples were collected using a 4 m seine net (mesh size 0.5 mm) pulled parallel to the shore over a distance of 5 m. The last two samples were collected using a dip net (mouth area Z 0.3 ! 0.3 m, mesh size Z 1.0 mm) pushed over a distance of 5 m parallel to the shore. To account for the differences in net size, shrimps were collected from five distances from the shore (0, 1, 2, 3, 4 m) for each replicate using the dip net. A comparison between the catch (ind mÿ2) of the two sampling methods was conducted within the lower reach of the Kariega estuary. A random block design was used focusing on vegetated (O70% submerged vegetation cover) and non-vegetated areas (!30% submerged vegetation cover). The results of the statistical analysis revealed no significant difference in catch per unit effort between the different methods in the vegetated areas (seine net: n Z 3, mean Z 58.8 G 29.3 ind mÿ2; dip
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Fig. 1. Geographic location of the temporarily open/closed West Kleinemonde estuary on the southeastern seaboard of southern Africa. Positions of the sampling stations occupied in the lower, middle and upper reaches are indicated.
net: n Z 3, mean Z 46.2 G 14.7 ind mÿ2; Mann–Whitney U test p O 0.05) and the non-vegetated areas (seine net: n Z 3, mean Z 21.6 G 12.3 ind mÿ2; dip net: n Z 3, mean Z 42.4 G 35.1 ind mÿ2; Mann–Whitney U test p O 0.05). After collection, samples were fixed in a 5% buffered (hexamine) formalin solution for later analysis in the laboratory. When less than 100 individuals were caught the entire sample was analyzed, while 1/2 to 1/4 subsamples were analyzed when the samples contained greater than 100 shrimps. During each sampling trip visual estimates of submerged vegetation cover (%) and channel characteristics within the sampled areas were made.
carapace and the posterior tip of the telson), carapace length (CL, defined as the region from the anterior tip of the carapace to the dorsal midline of the posterior margin of the carapace), wet weight (wwt) and dry weight (dwt). The length measurements (mm) were made using electronic Vernier calipers. Dry weight was measured using a Sauter AR 100 microbalance after oven drying individuals at 80 C for 24 h. Regression relationships between selected measurements were calculated using the statistical analysis program Statistica (version 6).
2.4. Morphometric relationships
Total abundance and biomass of Palaemon peringueyi within the lower, middle and upper reaches of the estuary were calculated using the swept area method. The area sampled was calculated by multiplying the effective width of the trawl by the towing distance. To standardize the data, the number of individuals (for
One hundred shrimp ranging in size from 3.4 to 18.0 mm CL were used to determine the morphometric relationships. Measurements made included total length (TL, defined as the distance between anterior tip of the
2.5. Abundance and biomass
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Shrimps larger than 9 mm CL were measured and their sex determined by the presence or absence of an appendix masculina (A.M.) on the endopod of the second pleopod (Pakhomov et al., 2000). Below 9 mm, identification of the rami became impossible under the dissecting microscope (mag Z 10!) and thus all individuals smaller than 9 mm (CL) were considered to be juveniles. Following this, the male to female sex ratio was determined and a chi-squared test was used to determine if the observed ratios differed from the expected 1:1 ratio. 2.7. Length frequency analysis For the length frequency analysis the carapace length (CL) of the Palaemon peringueyi were measured using electronic Vernier calipers. The length frequency distributions were constructed using 0.5 mm intervals of carapace length. A two-way ANOVA and post hoc tests (Fishers LSD) were used to look at the interactive effects of time (month) and area (reach) on the mean size of the shrimp. To establish if there was any difference in the mean size of male and female shrimp each sample a t-test for independent samples by groups was used (Statistica, version 6).
3. Results 3.1. Environmental variables The upper reach of the estuary was characterized by steep banks, a narrow channel, and sparse submerged vegetation cover (cover ! 10% of the total surface area). The middle reach of the estuary was relatively shallow (depth ! 1 m), and was characterized by
Temperaure (°C)
2.6. Sex ratio
extensive submerged vegetation cover (cover O 70% of total surface area). The vegetation cover in the lower reach was patchy and thin (cover ! 20% of total surface area). A gradual increase in submerged vegetation cover was observed throughout the estuary during the study period. One week prior to the first sampling trip, the estuary breached which resulted in a dramatic decrease in the water level in the upper and middle reaches of the estuary. As a result, only the lower reach was sampled. During this period salinities were highly variable (6.5– 32), and low dissolved oxygen concentrations prevailed (5.5 G 0.7 mg O2Lÿ1). The temperature remained relatively warm and stable (18 G 1.4 C). The estuary remained open until mid June. Over the course of the study, temperature and dissolved oxygen displayed little spatial variability (Fig. 2). A distinct spatial pattern in salinity values was observed, with the lower reaches being characterized by higher salinities (mean Z 17.4 G 5.2) than the upper reaches (mean Z 13.9 G 3.4; Kruskal–Wallis ANOVA, p ! 0.05). Results from the statistical analysis indicated that the physico-chemical variables expressed strong seasonal variability (Kruskal–Wallis ANOVA, p ! 0.05 in all cases). Temperature expressed a summer (January 2004) maximum of c. 31 C and a spring (September 2003) minimum of c. 15 C. The lowest salinities were recorded in summer (January 2004),
35 30 25 20 15 10 5 0
Salinity
abundance) or the total wet weight of the individuals (for biomass) captured at a sampling station was divided by the area sampled. A mean abundance and biomass of the three stations occupied within each reach was then determined. Abundance results were expressed as individuals per m2 (ind mÿ2), and biomass in grams wet weight per m2 (g wwt mÿ2). Wet weight was measured using a Sauter AR100 microbalance. Two-way ANOVAs and post hoc tests (Fishers LSD; Statistica, version 6) were used to determine the interactive effects of time (month) and area (reach) on the abundance and biomass values of Palaemon peringueyi within the estuary. Spearman’s correlation analyses were used to determine the significance of the relationships between the physico-chemical variables and abundance and biomass.
35 30 25 20 15 10 5 0
Dissolved oxygen (mg O2 L-1)
76
A
B
12 10
18 May 2003 8 July 2003 5 Sep 2003 6 Nov 2003 23 Jan 2004 21 March 2004
C
8 6 4 2 0 Lower
Middle
Upper
Reach
Fig. 2. Trends in mean (GSD) temperature (A), salinity (B) and dissolved oxygen (C) recorded in the lower, middle and upper reaches of the West Kleinemonde estuary. Arrows indicate open phase.
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3.2. Morphometric relationships The results from the regression analysis showed a strong relationship between total length and carapace length (r2 Z 0.99, p ! 0.001), and dry weight and wet weight (r2 Z 0.99, p ! 0.001; Table 1). 3.3. Abundance and biomass In the first sample (May 2003) Palaemon peringueyi were very rare, with a total of 10 shrimps being caught in the lower reach. Throughout the study P. peringueyi were restricted to the lower and middle reaches of the estuary. An exception was recorded during winter (July 2003), with a single individual being recorded in the upper reach. Maximum abundances of Palaemon peringueyi were recorded within the lower reach during the July sampling trip (mean Z 6.4 G 7.9 ind mÿ2), while minimum abundances were recorded in the lower reach at the beginning of the study, May 2003 (mean Z 0.08 G 0.05 ind mÿ2; Fig. 3A). Results from the twoway ANOVA indicated that the between effects of time (month) and area (reach) on abundance of P. peringueyi were significant ( p ! 0.05). Post hoc analysis (Fishers LSD) showed that there was no significant difference between the abundance of P. peringueyi in the lower and middle reaches although both differed significantly from the upper reach values. Similarly, the abundance of P. peringueyi recorded during July 2003 was significantly greater than all the other samples collected. The maximum biomass values (mean Z 0.56 G 0.73 g mÿ2) were recorded in the lower reaches in March 2004, while the lowest were recorded during the open phase in May 2003 (mean Z 0.05 G 0.02 g mÿ2; Fig. 3B). Results Table 1 Standard linear relationships for carapace length and total length, and wet weight and dry weight in P. peringueyi n
2
r
Abundance (ind m-2)
ranging between 8 in the upper reaches and 15 in the lower reaches. This period coincided with the most marked horizontal gradient in salinity. For the remainder of the study the estuary was predominantly mesohaline (15–20). Dissolved oxygen peaked in winter (mean Z 8.13 G 0.53 mg O2Lÿ1), with the highest concentrations generally being found in the middle reaches. The lowest dissolved oxygen concentrations were recorded in summer (mean Z 4.97 G 0.27 mg O2Lÿ1).
16 14 12 10 8 6 4 2 0
Biomass (g wwt m-2)
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1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0
A
18 May 2003 8 July 2003 5 Sep 2003 6 Nov 2003 23 Jan 2004 21 March 2004
B
Lower
Middle
Upper
Reach
Fig. 3. Trends in mean (GSD) abundance (A, ind mÿ2) and biomass (B, g wwt mÿ2) of Palaemon peringueyi within the lower, middle and upper reaches of the West Kleinemonde estuary. Arrow indicates open phase.
from the two-way ANOVA showed that the between effects of time (month) and area (reach) on Palaemon peringueyi biomass were significant ( p ! 0.05). The post hoc analysis (Fishers LSD) showed that the mean total biomass value from the lower reach, 0.29 (G0.39) g wwt mÿ2, was significantly greater than the middle reach, 0.11 (G0.1) g wwt mÿ2, and the upper reach, 0.0009 (G0.0002) g wwt mÿ2 ( p ! 0.05), while temporal variation in biomass was not significant ( p O 0.05). Results for the Spearman’s correlation analysis showed that only salinity and biomass were significantly correlated, with the biomass of Palaemon peringueyi increasing with an increase in salinity (R Z 0.34, p ! 0.05). The remainder of the relationships between the physico-chemical variables and abundance and biomass were not significant. 3.4. Sex ratios There was no significant difference between the male to female ratios from the lower and middle reaches (t-test for independent samples, p ! 0.05). As a result the data were pooled. The mean male:female ratio (1.07 G 0.38:1), over the study period, did not differ from the expected 1:1 ratio (c2 Z 0.61, p O 0.05). 3.5. Size frequency analysis
p-Value Regression equation
Carapace length 100 0.99 !0.001 TLZ0:668C2:346!CL (CL)–total length (TL) Wet weight (wwt)–dry 100 0.99 !0.001 dwtZ0:00003C0:203!wwt weight (dwt)
The population size structure of Palaemon peringueyi within the estuary reflected the loss of cohort of large individuals when the estuary breached and the subsequent recruitment and growth of a cohort of juveniles to mature adults within the study period (Figs. 4–6).
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4. Discussion Compared to permanently open estuaries within the same geographic region, the temporarily open/closed
Percentage of total numbers caught
Open
Closed
100 80 60 40 20 0
03 003 004 003 v 2003 n 2004 l 20 ar 2 o ay 2 ep 2 a 8 Ju 6N 5S 18M 23 J 21 M Juvenile Female Date Male
Fig. 4. Percentage contribution of juveniles, females and males to the Palaemon peringueyi population in the West Kleinemonde estuary, in relation to mouth state. Note overtopping events occurred at least once on a monthly basis. Z open phase, Z closed phase.
Open
Carapace length (mm)
There was strong evidence for length based sexual dimorphism (Fig. 7), with the females being significantly larger ( p ! 0.05, 14.15 G 2.27 mm CL) than the males (13.47 G 1.66 mm CL) for all months except May and July 2003 when juveniles dominated the P. peringueyi community (t-test for independent samples by groups, p ! 0.05). As a result, the length frequency analysis was done separately for juveniles, females and males. Juveniles dominated the total catch during July and September 2003, contributing between 100 and 85% of the total catch, respectively (Fig. 4). In both the July and September 2003 samples, shrimp from the middle reaches were significantly larger (mean Z 5.12 G 1.24 and 8.18 G 0.54 mm CL, respectively) than those recorded in the lower reaches (mean Z 4.14 G 0.6 and 6.42 G 1.25 mm CL, respectively; one-way ANOVA, p ! 0.05 in both cases). Following this, juveniles contributed less than 5% of the total catch in November, and were not recorded in the January and March 2004 samples (Fig. 4). Length frequency analysis revealed that juvenile P. peringueyi were recorded in the estuary 3 months after mouth closure suggesting that some degree of recruitment had occurred through overtopping (Figs. 4, 6). The smallest individuals were recorded during July (min Z 2.96 mm CL, mean Z 4.45 G 0.98 mm CL), while the largest were recorded at the end of the study in March 2004 (female mean Z 15.5 G 1.33 mm CL, male mean Z 14.35 G 1.2 mm CL). Female and male P. peringueyi did not express spatial patterns in mean size within the estuary (one-way ANOVA, p ! 0.05 in all cases).
Closed
17 16 15 14 13 12 11 10 9 8 7 6 5 4 3 2 1 0
4 003 003 004 003 003 200 ly 2 ov 2 3 Jan 2 ep 2 arch 8 Ju 6N 5S 2 21 M
ay 2
18 M
Date
Juvenile Male Female
Fig. 5. Mean carapace length of juvenile, female and male Palaemon peringueyi within the West Kleinemonde estuary for the six samples. Note overtopping events occurred at least once on a monthly basis. Z open phase, Z closed phase.
West Kleinemonde estuary supports a much lower biomass of Palaemon peringueyi. For example, Emmerson (1986) reported that within the Zostra capensis beds of the permanently open Sundays and Swartkops river estuaries (eastern Cape) the annual biomass of P. peringueyi was 2.69 g dwt mÿ2 and 2.16 g dwt mÿ2, respectively. These values are considerably higher than the mean P. peringueyi biomass from the lower and middle reaches found over this study period (0.2 G 0.13 g wwt mÿ2, or 0.04 G 0.026 g dwt mÿ2 calculated using the wwt:dwt regression equation in Table 1). A factor that could contribute to the disparity in biomass observed is habitat type sampled. The present study focused on the majority of submerged habitat types, vegetated and non-vegetated, within the West Kleinemonde estuary, while Emmerson (1986) focused on the Z. capensis beds, that are known to contain higher densities of grass shrimp than the surrounding nonvegetated areas (Emmerson, 1986; Lubke et al., 1988; Walsh and Mitchell, 1998). Following this, the lower biomass could reflect restricted recruitment into temporarily open/closed estuaries, caused by the presence of the sandbar, compared to the permanently open estuaries where recruitment is uninhibited and only dependent on the presence of juvenile P. peringueyi in the surf-zone adjacent the estuary mouth. A number of studies have demonstrated that breaching events in temporarily open/closed estuaries result in a significant disturbance to estuarine biological communities culminating in the loss of plankton (Perissinotto et al., 2000; Kibirige and Perissinotto, 2003; Froneman, 2004), benthic invertebrates (De Decker, 1987) and fish biomass (Whitfield, 1998) to the marine environment. Emmerson (1986) found that flooding severely affected the biomass of Palaemon peringueyi within the permanently open Kromme river estuary. Thus, the virtual absence of shrimp during the open phase could be attributed to the flooding associated with the breaching of the West Kleinemonde estuary. The impact of the
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A.T.F. Bernard, P.W. Froneman / Estuarine, Coastal and Shelf Science 63 (2005) 73–81 Length at recruitment
Length at emigration
40 18 May 2003
30 20 10 0 160
8 Jul 2003
140 120 40 20 0 40
5 Sep 2003
Number of observations
30 20 10 0 40
6 Nov 2003
30 20 10 0 40
23 Jan 2004
30 20 10 0 40
21 Mar 2004
30 20
Juvenile
10
Female Male
2.5 3.0<=x < 3.5<=x 3.0 < 4.0<=x 3.5 < 4.5<=x 4.0 < 5.0<=x 4.5 < 5.5<=x 5.0 < 6.0<=x 5.5 < 6.5<=x 6.0 < 7.0<=x 6.5 < 7.5<=x 7.0 < 8.0<=x 7.5 < 8.5<=x 8.0 < 9. <=x 8.5 9.50<= <9.0 x 10 <= <9 . x .5 10 0<= <10 . x . 11 5<= <10 0 . x . 11 0<= <11 5 .5< x< .0 12 = 11 . x . 12 0<= <12 5 . x . 13 5<= <12 0 . x . 13 0<= <13 5 . x . 14 5<= <13 0 .0< x< .5 14 = 14 . x . 15 5<= <14 0 . x . 15 0<= <15 5 . x . 16 5<= <15 0 . x . 16 0<= <16 5 . x . 17 5<= <16 0 .0< x< .5 17 = 17 . x . 18 5<= <17 0 . x . 18 0<= <18 5 .5< x< .0 =x 18. <1 5 9.0
0
Length classes (CL) Fig. 6. Stacked length frequency histograms of juvenile, female and male Palaemon peringueyi within the West Kleinemonde estuary for the six samples. Lines represent approximate carapace length at recruitment (2.356 mm) and emigration (12.5 mm), calculated from TL estimates (Emmerson, 1986) using a CL:TL regression formula (Table 1). Note overtopping events occurred at least once on a monthly basis.
flooding is also reflected in the size structure of the P. peringueyi population with mature individuals disappearing from the estuary following the breaching event (Fig. 6). The tidal phase following mouth opening is usually associated with recruitment of estuarine dependent marine breeding organisms (Whitfield, 1998; Froneman, 2004). This agrees with the present findings, which showed P. peringueyi juveniles dominate the catches following the breaching event (Figs. 4, 6).
It is important to note breaching events likely pose the only mechanism by which estuarine organisms can migrate from the estuary to the marine environment in temporarily open/closed systems. As a result under conditions of prolonged mouth closure, the reproductive potential of those species with an obligate marine phase will be reduced. Emmerson (1986) suggested that Palaemon peringueyi emigrate from permanently open estuaries when 30–40 mm in total length, which corresponds to
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A.T.F. Bernard, P.W. Froneman / Estuarine, Coastal and Shelf Science 63 (2005) 73–81 18 May 2003
5 Sep 2003
6 Nov 2003
23 Jan 2004
21 March 2004
20 p>0.05
P<0.05
p<0.001
p<0.001
p<0.05
18 16 14 12 10 8 f
m
Sex
f
m
Sex
f
m
Sex
f
m
Sex
f
m
Sex
Fig. 7. Mean carapace length of female (F) and male (M) Palaemon peringueyi within West Kleinemonde estuary. Error bars denote 0.95% confidence interval, p values provided on graph.
a residence time of c. 9 months. Results from the length frequency analysis indicate that the majority of the P. peringueyi within the West Kleinemonde estuary obtained a length of between 30 and 40 mm (total length) within 7 months of the study (Fig. 6). Results of subsequent studies in the West Kleinemonde estuary indicate that the system remained closed for up to 15 months after the initial breaching event in May 2003. Marine overtopping events pose an alternative mechanism through which larvae and juveniles of estuarine dependent invertebrate and vertebrate species can recruit into temporarily open/closed estuaries (Whitfield, 1998; Bell et al., 2001; Cowley et al., 2001; Vivier and Cyrus, 2001; Froneman, 2004; Kemp and Froneman, 2004). A recent study conducted by Kemp and Froneman (2004) in the temporarily open/closed West Kleinemonde estuary found that post larvae (CL ! 2 mm) Palaemon peringueyi recruit into the estuary during overtopping events. During the present study period overtopping occurred on a monthly basis, although the intensity and duration of the events were highly variable (P. Cowley, pers comm). The presence of juvenile P. peringueyi in the estuary up to 3 months following mouth closure (Figs. 4, 6) provides further support for the findings of Kemp and Froneman (2004). Although recruitment of P. peringueyi into permanently open estuaries peaks during summer and winter months (Emmerson, 1986), the shrimp does demonstrate continuous recruitment (Emmerson, 1985). The virtual absence of juveniles from the last two samples, undertaken during the summer months, suggests that overtopping is not always associated with recruitment. These facts suggest that while overtopping can create an ephemeral means of recruitment, the establishment of a link to the marine environment following breaching represented the primary mechanism of recruitment for P. peringueyi into the West Kleinemonde estuary during the present study (Figs. 3, 6). A spatial pattern in the size distribution of juvenile Palaemon peringueyi can be seen in the July and September samples, with the middle reach having larger
individuals than the lower reach (Fig. 5). The observed pattern may reflect a re-colonization process, with the shrimps that have established themselves within the lower reaches, following recruitment, migrating up the estuary. The size distribution pattern was not observed following September, this could be a result of reduced recruitment as well as the maturation of the P. peringueyi population. The lack of any strong relationship between the physico-chemical variables and Palaemon peringueyi biomass and abundance during this investigation suggests the distribution could be related to habitat preference rather than physical constraints. The importance of submerged vegetation as a habitat for a variety of estuarine invertebrates is well documented (De Villiers et al., 1999). During the study submerged vegetation cover within the West Kleinemonde estuary was most extensive at the station occupied in the middle and lower reaches. It is possible that the observed pattern in P. peringueyi distribution, abundance and biomass during the study was associated with the presence of submerged macrophytes, which likely provide refuge against predators. The absence of P. peringueyi from the upper reach could thus be related to the sparse vegetation cover (!10% of the total surface area sampled). This distribution pattern is similar to what is seen in permanently open estuaries, where the density of P. peringueyi in the upper reach is considerably lower than the densities recorded in the middle and lower reaches (Emmerson, 1986; Lubke et al., 1988). Variations in size and growth rates between male and female shrimp has been described on a number of occasions (Alon and Stancyk, 1982; Oh et al., 1999). The present study presents evidence for length based sexual dimorphism in Palaemon peringueyi within the temporarily open/closed West Kleinemonde estuary (Fig. 7). Emmerson (1985) found that while male P. peringueyi (25 mm TL or 10.34 mm CL) attain sexual maturity at a shorter length than females (41 mm TL or 17 mm CL), there was no significant difference in the mean size of
A.T.F. Bernard, P.W. Froneman / Estuarine, Coastal and Shelf Science 63 (2005) 73–81
males and females sampled from tidal pools. Oh et al. (1999) found that female Crangon crangon grew faster and attained a larger size at age than the males. The significantly larger size of female P. peringueyi recorded during this study may reflect differences in male and female growth rates. Results of the study indicate that the breaching event was essential for the recruitment of Palaemon peringueyi into the temporarily open/closed West Kleinemonde estuary, and, possibly of more importance to the shrimp population within the estuary, breaching allows emigration to the marine environment where the sexually mature individuals can reproduce. While there is some evidence that frequent overtopping events may also be associated with the recruitment of P. peringueyi into the estuary, the low frequency of occurrence of juveniles in the system following these events suggest that it is not the principal method of recruitment. Future studies should begin to assess the growth and mortality of P. peringueyi within temporarily open/closed estuaries.
Acknowledgements Thanks are extended to B. Donavan, J. Kemp and L. Jackson for their assistance with the field sampling. Funding for this research was acquired from the Joint Research Council (JRC) of Rhodes University. Finally I would like to thank Prof. A.N. Hodgson for his advice during the early stages of this study.
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