Feeding ecology of the early life-history stages of two dominant gobiid species in the headwaters of a warm-temperate estuary

Estuarine, Coastal and Shelf Science 109 (2012) 11e19

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Feeding ecology of the early life-history stages of two dominant gobiid species in the headwaters of a warm-temperate estuary Ryan J. Wasserman* Department of Zoology, Nelson Mandela Metropolitan University, P.O. Box 1600, Port Elizabeth 6000, South Africa

a r t i c l e i n f o

a b s t r a c t

Article history: Received 15 June 2011 Accepted 5 May 2012 Available online 11 May 2012

The diet and population structure of larval and early juvenile Glossogobius callidus and Redigobius dewaali (Gobiidae) were examined from the headwater region of the permanently open Great Fish Estuary along the south-east coast of southern Africa. Stomach contents of five selected size classes were sorted and identified to the lowest possible taxonomic level for each goby species. Using % Index of Relative Importance values, ontogenic shifts and dietary breadth were determined for each species as was dietary overlap between species. Numerically, both gobiid species showed similar temporal and spatial trends. Seasonal differences in catches were evident, although no numerical differences across sampled sites were found. A large degree of dietary overlap was found between the two species. The zooplanktonic diet showed a greater degree of ontogenic shift in R. dewaali than G. callidus, although similar trends were found for both. In both goby species, Calanoid sp. (Copepoda) generally decreased in importance across size classes, being the most important in the smallest size class whilst Corophium sp. (Amphipoda) increased in importance across size classes, being the least important at the smallest size classes. For both G. callidus and R. dewaali, Insecta contributed significantly to at least one of the five size classes. The larger size classes showed the least dietary overlap and the highest niche breadth. In addition, as is the case in many gobiids worldwide, the larger size classes of both sampled gobiid species consumed a broader prey size range. In conclusion, dietary overlap was largely similar between the young gobiids, suggesting that either food resources are not limiting, or niche separation is attributed to differences in foraging strategies. Ontogenic dietary shifts were however present for both gobiids with regard to prey items and prey size, suggesting a greater degree of foraging niche separation in adults of the species. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: estuary headwaters larval fish dietary shift mouth gape Glossogobius callidus Redigobius dewaali Insecta

1. Introduction Partitioned resources within ecological communities include those of space, time and food (Schoener, 1983; Ross, 1986). As communities are regularly comprised of phylogenetically related and ecologically similar species, resources are often partitioned on a delicate scale (Plattell and Potter, 2001; Gladfelter and Johnson, 2004) with similar species showing large resource utilisation overlap (Tokeshi, 1999; Malavasi et al., 2005). The determination of mechanisms facilitating the coexistence of these similar species is important for the understanding of community ecology, with implications for biodiversity conservation (Chave et al., 2002; Amarasekare et al., 2004). As such, the utilisation of

* Corresponding author. Present address: Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa. E-mail address: [email protected]. 0272-7714/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2012.05.003

food resources by two closely related, sympatric estuarine gobiid fishes was investigated in a warm-temperate, permanently open estuary. Globally, estuarine ecosystems act as nursery areas for both marine- and estuarine-spawned fish species (Blaber and Blaber, 1980; Warlen and Burke, 1990; Whitfield, 1999; Lazarri et al., 2003; Le Pape et al., 2003; Strydom et al., 2003; Chícharo et al., 2006). Consequently, estuaries play a vital role in the survival of early developmental stage fishes relying on these nursery habitats for favourable feeding conditions and shelter opportunities. International studies have recently shown that both marine- and estuarine-spawned fish species utilize low salinity and even freshwater environments in the headwater regions of these estuarine systems (Araujo et al., 1999; Faria et al., 2006; Hoeksema and Potter, 2006; Hindell, 2007; Rehage and Loftus, 2007; Morais et al., 2010; Wasserman and Strydom, 2011). Little information however, is available on the feeding ecology of the marine and estuarine fish species utilising these habitats, specifically in southern Africa.

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Dietary information on fish species utilising estuaries is essential for understanding their distribution patterns and life-history strategies (Blaber, 1997). Furthermore, such information reveals and highlights community level dynamics and gives support to the understanding of mechanisms facilitating the foraging niches of species. Globally, the gobiids represent a large fish family with many species represented in freshwater, estuarine and marine environments, most of which are benthic (Smith and Heemstra, 1995). In South Africa, larval fish studies have shown that gobiids often dominate planktonic fish catches along the east coast, in temperate (Strydom et al., 2003; Montoya-Maya and Strydom, 2009; Wasserman et al., 2010) and subtropical estuaries (Harris and Cyrus, 2000; Pattrick et al., 2007). Despite their diversity, estuarine gobies are usually dominated by a few species (Harris and Cyrus, 2000; Strydom et al., 2003; Montoya-Maya and Strydom, 2009; Wasserman et al., 2011a). While occurring in estuaries between northern Mozambique and the Cape region of South Africa, the estuary-spawned Glossogobius callidus and Redigobius dewaali are particularly prevalent in the Eastern Cape of South Africa. In this region, they often dominate gobiid representation, while generally occurring in higher numbers in the low salinity environments of the middle and upper reaches of these systems (Whitfield, 1998; Strydom et al., 2003). While G. callidus is thought to breed mostly during the spring months of October and November, R. dewaali is believed to breed in both spring and summer (September to February) (Skelton, 2001). Despite their numerical dominance within the upper reaches of many east coast southern African estuaries, feeding studies on these species are scant with limited information available on adult G. callidus (Vumazonke et al., 2008) and no known published information available on R. dewaali. The numerical dominance of these species suggests that they play a key ecological role within the upper reaches of estuaries (Strydom et al., 2003; Strydom and Neira, 2006). This prompted an investigation into the diet of the early life-history stages of G. callidus and R. dewaali in a freshwater dominated permanently open estuary along the south-eastern coastline of South Africa. The present study aims to describe the diet and resource partitioning of the early life-history stages of G. callidus and R. dewaali in the upper reaches of the Great Fish Estuary, where they largely dominate the ichthyofauna. My hypotheses were that in this system, where these species both occur in very large numbers:

Moore, 1998), a section now river dominated as a result of the unnaturally elevated freshwater inflow. 2.2. Field sampling This study was conducted in the historic ebb and flow region of the Great Fish Estuary. Early developmental stages of Glossogobius callidus and Redigobius dewaali were sampled using fine meshed fyke nets (Wasserman and Strydom, 2011), twice per season (autumn, winter, spring and summer) between March 2009 and January 2010. Sampling was conducted at five fixed sampling sites (Fig. 1), over the dark moon period at the same state of the lunar cycle for each sampling event. Fyke nets were set before sunset (around 16.00) and collected after sunrise (around 7.00) the following day with net collection following the sequence of net deployment. The tied cod end of the double-winged, 6-hooped, 1 mm mesh fyke nets were set using an anchor with the fyke net openings facing downstream. The two wings on either side of the opening were stabilized by 1.8 m long iron bars which were driven into the sediment. Two nets were set per site, one on each bank, close to shore yet low enough to avoid net exposure at low tide. Young G. callidus and R. dewaali (< 30 mm body length (BL)) were preserved on site in 10% buffered formaldehyde. Specimens > 30 mm BL were measured and released on site. Physico-chemical measurements were all taken during daylight hours at time of net deployment. Salinity (PSU) and temperature ( C) were measured at each site in the surface and bottom waters using a YSI 6600 multi-parameter probe. Water transparency measurements were also taken at all sites using a Secchi disc, with depth recordings (centimetres) being converted into an extinction coefficient (k) following Dawes (1981). 2.3. Laboratory analysis Sampled larval and early juvenile Glossogobius callidus and Redigobius dewaali were identified following Strydom and Neira (2006) and sorted into five size classes (size class 1 ¼ 6e10 mm, 2 ¼ 11e15 mm, 3 ¼ 16e20 mm, 4 ¼ 21e25 mm and 5 ¼ 26e30 mm body length). For both goby species, 10 individuals per size class were randomly selected from each sampled season for

1. There would be resource partitioning between the two gobiids 2. Ontogenic dietary shifts would be present in the early lifehistory stages. Elucidation of such issues will result in a better understanding of the nursery function estuarine headwaters offer as well as provide guild ecology information for the early life-history stages of the studied species. 2. Materials and methods 2.1. Study area The Great Fish Estuary is located within the Eastern Cape province of South Africa and has a catchment area of 29,284 km2 and a mean annual run-off of 526
106 m3 (Watling and Watling, 1983). Freshwater input into the estuary is augmented from the Orange River, via an inter-basin transfer scheme (Pech et al., 1995). As a result, the Great Fish Estuary has become a freshwaterdominated system (Reddering and Esterhuysen, 1982). Fishes were collected from the historic ebb and flow region (Lubke and de

Fig. 1. The geographic position of the Great Fish Estuary showing location of headwater region and sampling sites.

R.J. Wasserman / Estuarine, Coastal and Shelf Science 109 (2012) 11e19

dissection. Stomachs were dissected and the contents emptied into a 50 mm (long)
50 mm (wide)
1 mm (deep) tray, the bottom of which was marked with a 1 mm
1 mm grid. Contents were sorted, identified where possible, to the lowest taxon, and counted. In the cases where soft body parts were digested, counts were based on the number of heads present. Total length of whole prey items were measured wherever possible. An indirect volumetric assessment of the volume of each food category was obtained by flattening food items in the tray under a microscope slide and calculating the area of squash over the marked grid. Mouth gape and body length were compared for all dissected G. callidus and R. dewaali. For mouth gape measurements, maximum mouth gape width was ascertained by carefully opening the mouth of the gobiids with the aid of fine-tipped forceps and using a tapered needle to keep the mouth open at maximum gape. Measurements across the distance of the gape were then made, using an eyepiece micrometer. Similarly, the body lengths of all whole prey items were measured using an eyepiece micrometer. Where prey items were damaged with only parts of the body intact (e.g. heads or abdomen), body length measurements were not taken. Per sampled gobiid with measurable prey content in the stomach, the average, smallest and largest prey item body length measurements were compared against the body length of the fish.

2.4. Data analysis For the catch data, gobies sampled were expressed as catch per unit effort (CPUE) using the equation: CPUEi ¼ Ci/E, where for i (Glossogobius callidus or Redigobius dewaali), C is the total catch in number of fish and E is the effort expended to obtain Ci (effort ¼ overnight set). Per gobiid size class, prey abundance, frequency of occurrence and percentage volume were calculated for each taxon found in the diet. Prey abundance was expressed as the number of individuals as a percentage of all prey items (%N). The frequency of occurrence of prey was expressed as the number of stomachs containing a specific prey item as a proportion of all sampled stomachs (%F). The volume of each prey item consumed was expressed as a percentage of the total volume of stomach contents (%V). With these values, an index of relative importance (IRI) was calculated for each of the prey items using the formula (%N þ %V) x (%F) as described by Pinkas et al. (1971). Percentage (%) IRI was then calculated as the IRI value per prey group as a proportion of the sum of IRI values for all prey items. Significance levels of P < 0.05 were set for all statistical tests. A 2-way analysis of variance (ANOVA) was employed to test for differences among sites and seasons for CPUE and physicochemical data using the Statistica software package. The same software package was used to determine relationships between CPUE and physico-chemical variables via multiple linear regressions. Simple classification trees (Euclidean distance, single link) based on %IRI of prey were constructed in the PRIMER v6 software package to show diet similarities among size classes per species while the SIMPROF test was employed to assess if differences were significant. The same program and tests were used with numerical prey data to construct classification trees for illustration and analysis of the similarities among seasonal prey item consumption for both gobiid species. In addition, overall dietary overlap and dietary niche breadth as well as overlap and dietary breadth per size class were estimated for each goby species from %IRI values using the Rstatistical software package. Dietary diversity (Levins niche breadth) was calculated using the formulae:

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X B ¼ 1= P2i where Pi is the relative frequency of prey item i in the diet of predator P (Levins, 1968). As Pi is the denominator, the larger the B value the greater the dietary diversity. Pianka’s index (0 ¼ total separation, 1 ¼ total overlap) was used to determine trophic niche overlap between the two gobiids species using the equation:

Ojk ¼

X

X 1=2 X PijPik= P 2 ij P 2 ik

where Pi is defined as the frequency of occurrence of prey items i in the diet of species j and k (Pianka, 1973). The relationship between mouth gape and body length was investigated for both gobiid species via a non-linear, polynomial regression analysis using the GraphPad Prism 5 software package. Linear regressions using the same software package were employed to illustrate the relationship between gobiid body length and the total length of their undamaged prey items. 3. Results 3.1. Environmental variability Seasonal differences in the measured physical variables are summarised in Table 1 (Wasserman and Strydom, 2011). Of the measured physical parameters, temporal differences (n ¼ 80, df ¼ 3) were found for temperature (P < 0.001), salinity (P < 0.001) and turbidity (P < 0.05). While recorded temperature and turbidity values were higher during the summer and autumn periods, salinity was higher during autumn and winter sampling events. No significant spatial differences (n ¼ 80, df ¼ 4) were found for temperature, salinity nor turbidity (P > 0.05 in all cases). 3.2. Temporal and environmental trends in gobiid numbers Significant seasonal differences (n ¼ 80, df ¼ 3, P < 0.001), with much lower autumn and winter catches were found for both Glossogobius callidus and Redigobius dewaali. Gobiid numbers increased in the spring and even more so in the summer samples (Fig. 2). No significant differences (P > 0.05) were found across sites (n ¼ 80, df ¼ 4) for catches of either species, nor for sites within seasons (n ¼ 80, df ¼ 12). Per gobiid species however, the contribution of each size class to overall CPUE varied across seasons (Fig. 2). For Glossogobius callidus, the largest contribution of the smaller size class (size class 2) occurred during winter with very few of the intermediary size classes contributing. In spring and summer however, the G. callidus intermediary size classes 3 and 4 dominated catches. In contrast, the intermediary sized (size class 3 and 4) Redigobius dewaali dominated winter catches with the smaller size class (size class 2) contributing the least to overall winter numbers, while dominating spring and summer contributions. Both Glossogobius callidus and Redigobius dewaali numbers showed positive relationships with salinity (R ¼ 0.47, R ¼ 0.36 respectively) and temperature (R ¼ 0.40, R ¼ 0.33 respectively), and Table 1 Mean and standard deviation of physico-chemical parameters across seasons from the headwater reaches of the Great Fish Estuary (Wasserman and Strydom, 2011). Values for standard deviation presented in parentheses. Physical variables

Salinity (PSU) Temperature ( C) Turbidity (k)

Mean (Standard deviation) Autumn

Winter

Spring

Summer

0.7 (0.1) 21.6 (2.0) 0.27 (0.25)

0.7 (0.1) 14.0 (0.6) 0.09 (0.01)

0.7 (0.0) 19.6 (1.7) 0.07 (0.01)

0.9 (0.1) 24.7 (0.3) 0.07 (0.01)

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Fig. 2. Total numbers of Glossogobius callidus and Redigobius dewaali caught per season in the headwater reaches of the Great Fish Estuary, including percentage contribution of each size class.

negative relationships with turbidity (R ¼ 0.09, R ¼ 0.14 respectively). 3.3. Diet composition and ontogenic shift A total of 200 individuals per species (10 individuals
5 size classes
4 seasons) were selected for gut content analysis. Forty (20.0%) of the sampled Glossogobius callidus stomachs were empty, with the smaller size classes contributing most of the empty stomachs (Table 2). A greater number of Redigobius dewaali with empty stomachs (34.5%, 69 individuals) from all size classes were found. Glossogobius callidus stomachs contained 12 distinct prey items as well as unidentified invertebrate remains (Table 3). Calanoids (Copepoda) were the most important prey items in all 5 size classes (73.7, 72.1, 64.6, 89.4 and 41.4 %IRI respectively), but were markedly less importance in the largest fish size class. The Amphipoda (dominated by Corophium sp.) were comprised of 2 taxa and generally increased in importance as the gobiid size class increased (size class 1 ¼ 0.8 %IRI, size class 5 ¼ 31.3 % IRI). Insecta (6 taxa as well as unidentified remains), being the second most important component of the diet in size class 1 (6e10 mm BL, %IRI ¼ 9.7) did not rate high in importance for any other size classes (%IRI < 5). No significant dietary differences were found among the different size classes (SIMPROF test, P > 0.05), with classes 1, 2 and 4 being the most similar (Fig. 3). The diet composition of the largest size class was the most dissimilar when compared to the other size classes.

The stomach contents of Redigobius dewaali comprised more diverse prey than that recorded in Glossogobius callidus. A total of 15 distinct prey items were identified in the stomachs of R. dewaali as well as unidentified invertebrate remains (Table 3). The dominant taxa present in the stomachs of R. dewaali were however similar to those found in G. callidus. The Calanoid sp. (Copepoda) was identified as the most important component in the diet of the first four size classes of R. dewaali (60.0, 78.2, 90.8 and 82.9 %IRI respectively), increasing in importance from size classes 1 to 3, then decreasing through size classes 4 and 5. The Amphipod, Corophium sp. was absent from the smallest size class but demonstrated an increase in importance with an increase in fish size, contributing 44.6 % IRI to the largest size class. Unlike in G. callidus, the Insecta (particularly Simulidae) featured more consistently across size classes of R. dewaali, while being the dominant prey group in the largest size class (8 taxa, %IRI ¼ 18.2). Similar to G. callidus however, sand particles were found in the gut of the smallest size class R. dewaali (32.8 %IRI). No significant dietary differences were found among R. dewaali size classes (SIMPROF test, P > 0.05). Inter-sizeclass differences were however greater in R. dewaali than between G. callidus size classes, with the smallest and largest size classes showing increased dissimilarity (Fig. 3). No significant seasonal differences in prey items consumed were found for either of the gobiid species (SIMPROF test, P > 0.05). However, of the minor differences present, those of Redigobius dewaali were greater than those found for Glossogobius callidus (Fig. 4).

Table 2 Number of stomachs of Glossogobius callidus and Redigobius dewaali sampled from each season per size class (BL ¼ body length), including number of empty stomachs in samples. Values for R. dewaali presented in parentheses. Size class (mm BL)

Glossogobius callidus (Redigobius dewaali) Autumn

6e10 11e15 16e20 21e25 26e30

Winter

Spring

Summer

Sampled

Empty

Sampled

Empty

Sampled

Empty

Sampled

Empty

10 10 10 10 10

1 2 0 0 0

10 10 10 10 10

4 1 3 3 6

10 10 10 10 10

7 4 0 0 0

10 10 10 10 10

4 5 0 0 0

(10) (10) (10) (10) (10)

(4) (2) (0) (0) (0)

(10) (10) (10) (10) (10)

(3) (2) (1) (0) (1)

(10) (10) (10) (10) (10)

(9) (7) (4) (9) (9)

(10) (10) (10) (10) (10)

(6) (7) (3) (2) (0)

R.J. Wasserman / Estuarine, Coastal and Shelf Science 109 (2012) 11e19

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Table 3 Diet and ontogenic dietary change of Glossogobius callidus and Redigobius dewaali (R. dewaali data presented in parentheses). %N ¼ number of samples containing prey type, % IRI ¼ Index of relative importance, as a proportion of the total IRI of all species sampled. Taxa

Glossogobius callidus (Redigobius dewaali) 6e10 mm BL

Amphipoda Amphipod sp. Corophium sp Arachnida Acari sp. Maxillopoda Calanoid sp. Copepod sp. 1 Malacostraca Tanaidacea sp. Megalopa Crustacea remains Insecta Ceratopogonidae Simulidae Ephemoptera sp Zygoptera sp. Corixidae Trichoptera sp. 1 Trichoptera sp. 2 Trichoptera sp. 3 Trichoptera sp. 4 Insect remains Teleostei G. callidus Fish remains Unidentified Plant material Unidentified eggs Detritus Sand particles Unidentified Material

11e15 mm BL

16e20 mm BL

21e25 mm BL

26e30 mm BL

%N

%IRI

%N

%IRI

%N

%IRI

%N

%IRI

%N

%IRI

0.0 2.6 (0.0)

0.0 0.8 (0.0)

0.0 5.0 (9.3)

0.0 2.5 (7.5)

0.0 17.4 (4.9)

0.0 24.1 (2.8)

2.4 (0.0) 7.1 (10.5)

0.2 (0.0) 3.3 (12.3)

4.4 (0.0) 6.9 (13.6)

5.2 (0.0) 26.1 (44.6)

0.0

0.0

0.0 (3.7)

0.0 (0.2)

0.0

0.0

0.0

0.0

0.0

0.0

59.0 (54.2) 10.3 (0.0)

73.7 (60.0) 6.8 (0.0)

42.5 (50.0) 20.0 (11.1)

72.1 (78.2) 4.0 (1.7)

63.0 (64.8) 2.2 (9.0)

64.6 (90.8) 0.3 (1.5)

74.6 (79.0) 0.0 (1.3)

89.4 (82.9) 0.0 (0.8)

77.0 (71.5) 0.5 (2.0)

41.4 (31.1) 0.3 (0.1)

0.0 0.0 0.0

0.0 0.0 0.0

0.0 0.0 2.5 (0.0)

0.0 0.0 0.2 (0.0)

0.0 0.0 (1.6) 1.1 (0.0)

0.0 0.0 (0.4) 0.3 (0.0)

0.0 0.0 5.6 (1.3)

0.0 0.0 2.7 (0.04)

0.0 (0.6) 0.0 (1.4) 0.0 (2.3)

0.0 (0.3) 0.0 (2.6) 0.0 (0.5)

0.0 0.0 (4.2) 0.0 0.0 2.6 (0.0) 2.6 (0.0) 0.0 0.0 0.0 12.8 (0.0)

0.0 0.0 (0.8) 0.0 0.0 0.3 (0.0) 0.2 (0.0) 0.0 0.0 0.0 9.2 (0.0)

0.0 5.0 (7.4) 2.5 (3.7) 0.0 0.0 0.0 0.0 (1.9) 2.5 (1.9) 0.0 2.5 (3.7)

0.0 1.9 (6.3) 0.4 (0.2) 0.0 0.0 0.0 0 (0.3) 0.4 (0.1) 0.0 0.7 (1.9)

0.0 2.2 (3.3) 0.0 (2.5) 0.0 (1.6) 0.0 0.0 1.1 (0.0) 0.0 (0.8) (0.0) 1.1 (0.8)

0.0 0.8 (0.6) 0.0 (0.8) 0.0 (0.3) 0.0 0.0 0.03 (0.0) 0.0 (0.1) 0.0 0.3 (0.1)

0.0 0.8 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.8

0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1

0.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.03 (0.0) 0.0 (11.2) 0.0 (0.3) 0.0 (0.4) 0.0 (1.6) 0.0 0.0 (1.8) 0.0 (2.8) 0.0 (0.1) 0.0

0.0 0.0

0.0 0.0

0.0 0.0

0.0 0.0

0.0 0.0

0.0 0.0

0.0 0.8 (0.0)

0.0 0.1 (0.0)

1.5 (0.0) 0.0

0.04 (0.0) 0.0

0.0 0.0 0.0 0.0 10.3 (29.2)

0.0 0.0 0.0 0.0 (32.8) 9.0 (6.3)

0.0 0.0 2.5 (3.7) 0.0 15.0 (3.7)

0.0 0.0 0.7 (2.0) 0.0 17.0 (1.5)

0.0 0.0 1.1 1.1 9.8

0.0 (0.1) 0.0 (0.3) 0.2 (1.0) 0.04 (0.0) 9.5 (1.2)

0.8 (0.0) 0.0 0.0 (1.7) 0.0 7.1 (1.7)

0.05 (0.0) 0.0 0.0 (1.9) 0.0 4.1 (1.2)

0.0 0.5 0.5 1.0 7.4

0.0 0.1 (0.0) 0.1 (1.7) 0.1 (0.0) 26.6 (0.8)

3.4. Niche breadth and dietary overlap

(0.8) (3.3) (3.3) (0.0) (3.3)

(0.4) (2.2) (0.9) (0.4)

(0.4)

(0.03) (0.9) (0.02) (0.02)

(0.01)

(0.0) (2.8) (0.8) (0.6) (0.3) (2.5) (0.6) (0.3)

(0.0) (0.3) (0.0) (0.6)

For both Glossogobius callidus and Redigobius dewaali, dietary (Levins) niche breadth was greatest in size class 5, the largest size class (Fig. 5-a). The maximum difference in niche breadth between the two species was found at size class 3. The diets of the two goby

species were largely similar (Fig. 5-b). Inter-specific dietary overlap was, however, slightly reduced at the smallest and largest size classes, a result of the increased variety of prey items consumed by these sizes. Conversely, inter-specific dietary overlap between the two gobiids at size classes 2, 3 and 4 as well as overall species dietary overlap was near entire.

Fig. 3. Dendrogram showing dietary similarities (%IRI) among the early life-history size classes of a.) Glossogobius callidus and b.) Redigobius dewaali, sampled from the headwaters of the warm-temperate Great Fish Estuary, South Africa.

Fig. 4. Dendrogram showing prey item (N) similarities among seasonal catches of a.) Glossogobius callidus and b.) Redigobius dewaali, sampled from the headwaters of the warm-temperate Great Fish Estuary, South Africa.

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3.5. Prey size-predator size relationships Body length (mm) to mouth gape length relationships were similar for Glossogobius callidus and Redigobius dewaali (Fig. 6), facilitating predation on larger prey items by bigger fish as a result of increased mouth gape size. Indeed, G. callidus showed a general increase in the size of prey consumed as body length and mouth gape increased. However, despite the similar body length-mouth gape relationships, the data suggests that the larger sized R. dewaali are more generalist feeders, consuming both larger and smaller prey items than G. callidus of similar sizes. 4. Discussion 4.1. Spatial and temporal patterns In their early life-history survey, Wasserman and Strydom (2011) showed that young Glossogobius callidus and Redigobius dewaali consistently dominated fish catches. They caught a total of 31,764 fishes, with less than 5% constituting species other than G. callidus (43.4%) and R. dewaali (51.8%). Although statistical differences in salinity across seasons were found, they were in fact, minute. From an ecological perspective, such a narrow range in salinity among seasons would be insignificant, an example of an incident where mathematical differences have little ecological bearing, following the argument of Johnson (1999). The physical homogeneity across sampled sites of the headwater region of the

Great Fish Estuary was reflected in the absence of any significant spatial patterns in the gobiid catches. Despite the lack of difference in catches across sites, seasonal differences in catches were evident for both goby species. In accord with studies by Strydom and Neira (2006) conducted in warm-temperate estuaries along the southeast coastline of southern Africa, the numbers of young G. callidus and R. dewaali showed positive relationships with temperature. The catches of both goby species were greatest in summer, with the smaller size classes dominating numerically. R. dewaali caught in spring and summer were generally smaller in body length than those of G. callidus. This is potentially explained by the findings of Strydom and Neira (2006), who showed that R. dewaali is less developed at birth than G. callidus. They also suggested that the two species are separated both temporal and spatially with regard to spawning. Another possible explanation is that there may be a difference in growth rates between the two species. Such differences would contribute to niche differentiation between the two species, potentially facilitating their sympatry. 4.2. Diet composition It is essential to consider the limitations associated with dietary indexes commonly used in feeding studies (Wallace, 1981; Cortéz, 1997). In this regard the use of %IRI values in ecological interpretation of trophic niche breath and dietary overlap have been identified as particularly useful for intra- and inter-specific dietary comparisons (Cortéz, 1997, 1998). Both Glossogobius callidus and Redigobius dewaali fed on a wide range of invertebrate prey items, the most dominant of which peaked in summer, along with the gobiid numbers. The largely zooplankton-based diet of the early life-history G. callidus and R. dewaali is typical of young estuarine and marine fish species (Baldo and Drake, 2002; Gning et al., 2008; Rodriques and Vieira, 2010). The calanoid copepods, a prevalent group in the diet of both goby species numerically dominate zooplankton counts in the upper reaches of estuaries of the region, including the Great Fish Estuary (Wooldridge, 2010). Similarly, the amphipod, Corophium sp., occurs in high densities in the benthic habitats (Wooldridge and Deyzel, 2009) and within the zooplankton (Wooldridge, 2010) of the upper reaches of temperate South African estuaries. The numerical dominance of these two prey items in the diets of the gobiids during this investigation is thus not unexpected and reflects their high availability. Insects were found to be important dietary components for both goby species, although their contributions were somewhat staggered, being important to G. callidus at the smallest size class and to R. dewaali at the largest sampled size class. Sutherland (2010) found insects to be an important component of the diet of selected estuarine species in the freshwater dominated upper reaches of the Sundays River, South Africa. Similarly, in a study on a Swedish Fjord, Corophium and chironomid species dominated the diet of two closely-related benthic gobiid species (Magnhagen and Wiederholm, 1982). Plant material, however, contributed minimally to the diet in both goby species, while sand particles featured in the diet of the smallest R. dewaali size class. Many estuarine fish species consume sand and mud particles in order to access attached organic material (Blaber, 1997). Sand particle ingestion by R. dewaali could, however, be accidental, merely highlighting the benthic foraging nature of these young fish. 4.3. Ontogenic shift

Fig. 5. a.) Levins niche breadth and b.) Pianka’s dietary overlap statistics for the gobiids sampled from the headwaters of the Great Fish Estuary. a-Niche breadth illustrated for each size class (1e5) of Glossogobius callidus and Redigobius dewaali, including overall niche breadth for each species. b- Overall dietary overlap between the two gobiid species, including overlap per size class. 0 ¼ total separation, 1 ¼ total overlap.

Although both gobiid species considered remained in the same foraging guild, they did demonstrate a degree of ontogenic shift in their early life history, a feature not uncommon in young fish dietary studies (Baldo and Drake, 2002; Gning et al., 2008). Size class

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a

b

Fig. 6. a.) Mouth gape and b.) minimum, mean and maximum prey length relationships with Glossogobius callidus and Redigobius dewaali body length.

dietary differences were generally greater in Redigobius dewaali than Glossogobius callidus, highlighting a greater degree of ontogenic dietary shift in the former species. In addition, young R. dewaali seem to consume prey items of a broader size class range. This suggests that R. dewaali is perhaps a more generalist feeder than G. callidus at these early life-history stages. 4.4. Dietary overlap, niche breadth and partitioning According to Nikolskii (1969), when comparing between similar species, young fish generally have more analogous diets than those of their adult counterparts. In the present study, the diets of the young gobiids were largely similar with regard to composition, as has been found for many sympatric, closely related juvenile fish species (Delbeek and Williams, 1987; Darnaude et al., 2001; Rodriques and Vieira, 2010). It is highly likely that this is not the case for adults of the species. Indeed, for both Redigobius dewaali and Glossogobius callidus, the largest sampled size classes had the greatest niche breadth while the dietary overlap between the species was lowest, revealing a more defined foraging separation between the two species at this size. These larger sized gobies have the ability to select for a greater range of prey items, a result of increased mouth gape width. The increase in mouth gape and body size was accompanied by an increase in the maximum prey size consumed. In his study on the goby Lepidogobius lepidus, sampled from a coastal bay in California, U.S.A., Grossman (1980) showed that older fish forage increasingly on larger prey items, but still feed on the smaller items. He suggested that this facilitates superiority of older fish within intraspecific competition. In addition, the ability to select prey items of a more varied size range should increase prey species availability, potentially driving dietary niche breadth and reducing the degree of dietary overlap between species. The lowest dietary overlap between the largest sampled size classes of G. callidus and R. dewaali could be an indication of the commencement of foraging niche separation between adults of the species. Unfortunately, at present, limited information is available on the adult feeding of these two gobiids, making comparisons between juveniles and adults of the species

impossible. An additional complication in this particular interspecies comparison lies in the sexual polymorphic nature of R. dewaali, with regard to mouth gape size. Males of the species have a considerably wider mouth gape than that of the females (Kok and Blaber, 1977). This suggests that there is a degree of niche separation between sexes within the species and possibly explains the slightly lower R2 found for the regression analysis between BL and mouth gape when compared to G. callidus. Unfortunately, despite the effort, sex could not be determined for the fishes dissected, as sexual organs were poorly developed in these young fish. The most frequently used resources are those of food and space (Krebs, 1989). Stable coexistence of species competing for the same resources is possible if inter-specific competition can be reduced through niche-partitioning mechanisms (Gilbert et al., 2008). The early life-history stage Glossogobius callidus and Redigobius dewaali appear to be consuming the same prey items and using similar habitats. The spatial partitioning between these gobiids could be facilitated through differences in micro-habitat utilisation, as has been found between closely related gobiids in a Northern Hemisphere Fjord (Magnhagen and Wiederholm, 1982). Similarly, temporal feeding (such as day versus night foraging), morphological or behaviour differences could reduce the inter-specific competition between the two species such as in the case of certain closely related juvenile sympatric flatfish (Darnaude et al., 2001). Another possible explanation for the coexistence of these two closely related species may be the abundant food availability. According to Borza et al. (2009), high levels of dietary overlap between species evolve in the absence of competition, should there be no limitation of shared resources. Since the dominant prey groups are often the most abundant invertebrate taxa in these sections of temperate, South African estuaries (Wooldridge and Deyzel, 2009; Wooldridge, 2010), lack of food resource limitation was likely a major contributor to the high dietary overlap between the young fishes in this study. As published information on the feeding of Glossogobius callidus and Redigobius dewaali is scant, future research assessing the diet of adults of the species should be considered. Freshwater habitats at

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the heads of estuaries are often extensively utilised by young marine- and estuarine-spawned fish species, and as such, dietary and body condition comparisons between individuals caught in low salinity and high salinity habitats could be assessed to determine the importance of the respective environments to the species. The freshwater environment, above the ebb and flow of the studied estuary seems to be important for G. callidus and R. dewaali as both species are found in exceptionally high numbers in this part of the estuary. In the present study, insects made up an important component of the diet of the studied fish species at various stages of development. As aquatic insects are primarily freshwater associated, these low salinity estuarine environments where insects occur are potentially advantageous to young estuarine fish, offering increased foraging opportunities. The increased abundance of aquatic insects and their larvae in spring and summer (Baptista et al., 2001; Dallas, 2004) is likely to contribute to the facilitation of the young gobiid aggregation in these habitats. The utilisation of these habitats by young estuarine fish is therefore important and access to estuary headwater environments by small and young fish should be maintained. Both freshwater flow restriction to estuaries and the presence of in-stream barriers in the upper reaches of estuaries, have the potential to exclude estuarine Ichthyological communities from low salinity habitats (Wasserman et al., 2011a). This, and the threat by introduced piscivorous freshwater fishes to the estuarine ichthyological community utilising low salinity habitats (Wasserman et al., 2011b) needs to be considered for the sound management of estuarine habitats. Acknowledgements This work is based on financial support from the National Research Foundation, South Africa. Thanks are extended to N.A. Strydom for additional funding and T.H. Wooldridge for assistance in prey identification and manuscript revision. Gratitude is also expressed to G.I.H. Kerley, P.W. Froneman, Tim Vink, Tanja van de Ven and Craig Tambling for advice on the manuscript. References Amarasekare, P., Hoopes, M.F., Mouquet, N., Holyoak, M., 2004. Mechanisms of coexistence in competitive metacommunities. The American Naturalist 164, 310e326. Araujo, F.G., Bailey, R.G., Williams, W.P., 1999. Spatial and temporal variations in fish populations in the upper Thames estuary. Journal of Fish Biology 55, 836e853. Baldo, F., Drake, P., 2002. A multivariate approach to the feeding habits of small fishes in the Guadalquiver estuary. Journal of Fish Biology 61, 21e32. Blaber, S.J.M., 1997. Fish and Fisheries of Tropical Estuaries. Chapman and Hall, London, p. 367. Blaber, S.J.M., Blaber, T.G., 1980. Factors affecting the distribution of juvenile estuarine and inshore fish. Journal of Fish Biology 17, 143e162. Baptista, D.F., Buss, D.F., Dorvillé, L.F.M., Nessimian, J.L., 2001. Diversity and habitat preference of aquatic insects along the longitudinal gradient of the Macaé River Basin, Rio De Janeiro, Brazil. Revista Brasileira Biologia 61, 249e258. Borza, P., Eros, T., Oertel, N., 2009. Food resource partitioning between two invasive gobiid species (Pisces, Gobiidae) in the littoral zone of the River Danube, Hungary. International Review of Hydrobiology 94, 609e621. Chave, J., Muller-Landau, H.C., Levin, S.A., 2002. Comparing classic community models: theoretical consequences for patterns of diversity. The American Naturalist 159, 1e23. Chícharo, A.M., Chícharo, L., Morais, P., 2006. Inter-annual differences of ichthyofauna structure of the Guadiana estuary and adjacent coastal area (SE Portugal/ SW Spain): before and after Alqueva dam construction. Estuarine, Coastal and Shelf Science 70, 39e51. Cortéz, E., 1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 726e738. Cortéz, E., 1998. Methods of studying fish feeding: reply1. Canadian Journal of Fisheries and Aquatic Sciences 55, 2708. Dallas, H.F., 2004. Seasonal variability of macroinvertebrate assemblages in two regions of South Africa: implications for aquatic bioassessment. African Journal of Aquatic Science 29, 173e184.

Darnaude, A.M., Harmelin-Vivien, M.L., Salen-Picard, C., 2001. Food partitioning among flatfish (Pisces: Pleuronectiformes) juveniles in a Mediterranean coastal shallow sandy area. Journal of the Marine Biological Association of the United Kingdom 81, 119e127. Dawes, C.J., 1981. Marine Botany. John Wiley and Sons, New York, pp. 306e309. Delbeek, J.C., Williams, D.D., 1987. Food resource partitioning between sympatric populations of brackishwater sticklebacks. Journal of Animal Ecology 56, 949e967. Faria, A., Morais, P., Chícharo, M.A., 2006. Ichthyoplankton dynamics in the Guadiana estuary and adjacent coastal area, South-East Portugal. Estuarine, Coastal and Shelf Science 70, 85e97. Gilbert, B., Srivastava, D.S., Kirby, K.R., 2008. Niche partitioning at multiple scales facilitates coexistence among mosquito larvae. Oikos 117, 944e950. Gladfelter, W.B., Johnson, W., 2004. Feeding niche separation in a guild of tropical Reef fishes (Holocentridae). Ecology 64, 552e563. Gning, N., Vidy, G., Thiaw, O.T., 2008. Feeding ecology and ontogenic diet shifts of juvenile fish species in an inverse estuary: the Sine-Saloum, Senegal. Estuarine, Coastal and Shelf Science 76, 395e403. Grossman, G.D., 1980. Ecological aspects of ontogenetic shifts in prey size utilisation in the bay goby (Pisces: Gobiidae). Oecologia 47, 233e238. Harris, S.A., Cyrus, D.P., 2000. Comparison of larval fish assemblages in three large estuarine systems, KwaZulu-Natal, South Africa. Marine Biology 137, 527e541. Hindell, J.S., 2007. Determining patterns of use by black bream Acanthopagrus butcheri (Munro, 1949) of re-established habitat in a south-eastern Australian estuary. Journal of Fish Biology 71, 1331e1346. Hoeksema, S.D., Potter, I.C., 2006. Diel, seasonal, regional and annual variations in the characteristics of the ichthyofauna of the upper reaches of a large Australian microtidal estuary. Estuarine, Coastal and Shelf Science 67, 503e520. Johnson, D.H., 1999. The insignificance of statistical significance testing. The Journal of Wildlife Management 63, 763e772. Kok, H.M., Blaber, S.J.M., 1977. A new freshwater goby (Teleostei: Gobiidae) from the Pongola floodplain, Zululand, South Africa. Zoologica Africana 12, 163e168. Krebs, C.J., 1989. Ecological Methodology. Harper & Row, New York, p. 652. Lazarri, M.A., Sherman, S., Kanwit, J.K., 2003. Nursery use of shallow habitats by epibenthic fishes in Maine nearshore waters. Estuarine, Coastal and Shelf Science 56, 73e83. Le Pape, O., Holley, J., Guérault, D., Désaunay, Y., 2003. Quality of coastal and estuarine essential fish habitats: estimations based on the size of juvenile common sole (Solea solea L.). Estuarine, Coastal and Shelf Science 58, 1e11. Levins, R., 1968. Evolution in Changing Environments. Princeton University Press, Princeton, NJ, p. 120. Lubke, R.A., de Moore, F.C., 1998. Field Guide to the Eastern and Southern Cape Coasts. University of Cape Town Press, p. 559. Magnhagen, C., Wiederholm, A.-M., 1982. Habitat and food preferences of Pomatoschistus minutes and P. microps (Gobiidae) when alone and together: an experimental study. Oikos 39, 152e156. Malavasi, S., Franco, A., Fiorin, R., Franzoi, P., Torricelli, P., Mainardi, D., 2005. The shallow water gobiid assemblage of the Venice Lagoon: abundance, seasonal variation and habitat partitioning. Journal of Fish Biology 67, 146e165. Montoya-Maya, P.H., Strydom, N.A., 2009. Description of larval fish composition, abundance and distribution in nine south and west coast estuaries of South Africa. African Zoology 44, 75e92. Morais, P., Babaluk, J., Correia, A.T., Chícharo, M.A., Campbell, J.L., Chícharo, L., 2010. Diversity of anchovy migration patterns in an European temperate estuary and in its adjacent coastal area: implications for fishery management. Journal of Sea Research 64, 295e303. Nikolskii, G.V., 1969. Theory of Fish Population Dynamics as the Biological Background for Rational Exploitation and Management of Fishery Resources. Oliver & Boyd Ltd, Edinburgh, p. 323. Pattrick, P., Strydom, N.A., Wooldridge, T.H., 2007. Composition, abundance, distribution and seasonality of larval fishes in the Mngazi Estuary, South Africa. African Journal of Aquatic Science 32, 113e123. Pech, G.A., Mccourt, B., Kemper, N.P., 1995. Orange River Development Project, Replanning Study. Environmental Overview of the Eastern Cape Rivers. Department of Water Affairs and Forestry, Cape Town, South Africa. Ninham Shand Incorporated Report No. 2357. Pianka, E.R., 1973. The structure of lizard communities. Annual Review of Ecological Systems 4, 53e74. Pinkas, L., Oliphant, M.S., Iverson, I.L.K., 1971. Food habits of albacore, bluefin tuna and bonita in Californian waters. California Fish and Game 152, 1e105. Plattell, M.E., Potter, I.C., 2001. Partitioning of food resources amongst 18 abundant benthic carnivorous fish species in marine waters on the lower coast of Australia. Journal of Experimental Marine Biology and Ecology 261, 31e54. Reddering, J.S.V., Esterhuysen, K., 1982. Fluvial Dominated Sedimentation in the Great Fish Estuary. ROSIE Report 4. University of Port Elizabeth, Port Elizabeth, South Africa. Rehage, J.S., Loftus, W.F., 2007. Seasonal fish community variation in headwater mangrove creeks in the southwestern everglades: an examination of their role as dry-down refuges. Bulletin of Marine Science 80, 625e645. Rodriques, F.L., Vieira, J.P., 2010. Feeding strategy of Menticirrhus americanus and Menticirrhus littoralis (Perciformes: Sciaenidae) juveniles in a sandy beach surf zone of Southern Brazil. Zoologia 27, 873e880.

R.J. Wasserman / Estuarine, Coastal and Shelf Science 109 (2012) 11e19 Ross, S.T., 1986. Resource partitioning in fish assemblages: a review of field studies. Copeia, 352e388. Schoener, T.W., 1983. Field experiments on interspecific competition. The American Naturalist 122, 240e285. Skelton, P., 2001. Freshwater Fishes of Southern Africa. Struik Publishers, Cape Town. Strydom, N.A., Neira, F.J., 2006. Description and ecology of larvae of Glossogobius callidus and Redigobius dewaali (Gobiidae) from temperate South African estuaries. African Zoology 41, 240e251. Strydom, N.A., Whitfield, A.K., Wooldridge, T.H., 2003. The role of estuarine type in characterizing early stage fish assemblages in warm temperature estuaries, South Africa. African Zoology 38, 29e43. Sutherland, K., 2010. Larval fish diet, feeding guilds and zooplankton prey selection in the Sundays Estuary, South Africa. M.Sc. thesis, Nelson Mandela Metropolitan University, p. 131. Smith, M.M., Heemstra, P.C., 1995. Smiths’ Sea Fishes. Macmillan, Johannesburg, South Africa, p. 1047. Tokeshi, M., 1999. Species Coexistence: Ecological and Evolutionary Perspectives. Blackwell Science, Oxford. Vumazonke, L.U., Mainoane, T.S., Bushula, T., Pakhomov, E.A., 2008. A preliminary investigation of winter daily intake by four small teleost fish species from the Igoda Estuary, Eastern Cape, South Africa. African Journal of Aquatic Science 33, 83e86. Wallace, R.K., 1981. An assessment of diet-overlap indexes. Translations of American Fish Society 110, 72e76. Warlen, S.M., Burke, J.S., 1990. Immigration of larvae of fall/winter spawning marine fishes into a North Carolina estuary. Estuaries 13, 453e461.

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Wasserman, R.J., Strydom, N.A., Wooldridge, T.H., 2010. Larval fish dynamics in the NxaxoeNgqusi Estuary Complex in the warm temperate-subtropical transition zone of South Africa. African Zoology 45, 63e77. Wasserman, R.J., Strydom, N.A., 2011. The importance of estuary head waters as nursery areas for young estuary- and marine-spawned fishes in temperate South Africa. Estuarine, Coastal and Shelf Science 94, 56e67. Wasserman, R.J., Weyl, O.L.F., Strydom, N.A., 2011a. The effects of instream barriers on the distribution of migratory marine-spawned fishes in the lower reaches of the Sundays River, South Africa. Water SA 37, 495e504. Wasserman, R.J., Strydom, N.A., Weyl, O.L.F., 2011b. The diet of largemouth bass, Micropterus salmoides (Centrarchidae), an invasive alien in the lower reaches of an Eastern Cape river, South Africa. African Zoology 46, 378e386. Watling, R.J., Watling, H.R., 1983. Metal surveys in South African estuaries. VII. Bushmans, Kariega, Kowie and Great Fish Rivers. Water SA 9, 66e70. Whitfield, A.K., 1998. Biology and Ecology of Fishes in South African Estuaries. Ichthyological Monographs of the J.L.B. Smith Institute of Ichthyology, p. 223. Whitfield, A.K., 1999. Ichthyofaunal assemblages in estuaries: a South African case study. Reviews in Fish Biology and Fisheries 9, 151e186. Wooldridge, T.H., 2010. Characterisation of the mesozooplankton community in response to contrasting estuarine salinity gradients in the Eastern Cape, South Africa. African Journal of Aquatic Science 35, 173e184. Wooldridge, T.H., Deyzel, S.H.P., 2009. The subtidal macrozoobenthos of the riverdominated Great Berg Estuary. Transactions of the Royal Society of South Africa 64, 204e218.