Evaluation of food competition and resource partitioning of recruiting fish with permanent residents in a seagrass habitat

ABSTRACT

Recruiting King George whiting Sillaginodes punctatus were studied to assess the potential for food competition with permanent resident fish species in a nursery habitat. Marine migrant post larval S. punctatus (<60 mm TL) consumed primarily harpacticoid copepods and had high (>0.6) diet overlap with permanent resident fish species Favonigobius leteralis and Stigmatopora nigra. Food electivity index indicated that S. punctatus juveniles preferred harpacticoid copepods and amphipods, while juvenile Heteroclinus adelaide and Gymnapistes marmoratus migrating to the nursery habitat targeted larger prey such as amphipods. Preference for larger prey by H. adelaide and G. marmoratus species coupled with differences in prey composition in the stomach was due to mouth size and feeding habits, resulting in different food preferences to S. punctatus. The whiting showed an ontogenetic shift in diet with early settlers (>60 mm TL) consuming less copepods and more amphipods, while previous year recruits (>120 mm TL) consumed polychaete worms. This study indicates that competition for food resources between the new recruiting S. punctatus juveniles and permanent resident juveniles is reduced through differences in temporal and spatial feeding behaviours, mouth morphology, and ontogenetic shift in prey consumption.

KEYWORDS:

• Competition
• resource partitioning
• King George whiting
• diet
• seagrass
• estuary

Introduction

Seagrass habitats in estuaries form a highly productive ecosystem and are important nursery sites for many fish species (Able, 2005; Akin and Winemiller 2006). In southern Australia, seagrass beds can hold 40 times more benthic invertebrates than surrounding bare sand habitats (Bologna and Heck 2002). However, these habitats face considerable stress from climate change and anthropogenic activities such as urban development, eutrophication, pollution and recreational use (Bologna and Heck 2002; Bintz et al. 2003; Oviatt 2004; Davies et al. 2010; Hemraj et al. 2017). Loss of seagrass beds impact both food availability for fish species associated with this habitat, and biodiversity in the coastal environment (Heck et al. 2003). Understanding environmental factors and their influence on fish distribution and abundance is important to effectively manage fisheries and protect aquatic resources (Moyle and Cech 2004; Dinh et al. 2015).

Competitive interactions between teleosts can play an important role in habitat selection, foraging behaviour, growth, and survival and exerts influence on successful recruiting of juvenile fish to spawning stock (Munday et al. 2001; Mookerji et al. 2004; Polivka 2005). Food competition among fish species is generally greatest during early life stages and declines as fish grow (Ross, 1986; Dinh et al. 2017). The increased competition for resources is due to the influx of marine migrants and marine stragglers competing with permanent residents before migrant fish grow and move away from nursery areas (Najjar et al. 2000). It is well accepted that the success of one species can displace or outcompete another species if they cannot successfully partition resources (McDonald et al. 2001; Marks et al. 2011; Hossain, Ye, et al. 2017). In an inshore or estuarine environment, the success of permanent residents has the potential to impact on the success of arriving migrants via direct competition, whereas conversely, the successful recruitment of a migrant may place pressure on resources for permanent residents. Loss of suitable habitat may exacerbate competition among species as marine migrants compete for resources with permanent residents (Hobday et al., 1999). In addition, low juvenile recruitment of a species caused by the overfishing of breeding stocks can allow for an increase in abundance of less targeted fish species that share a similar diet. This could result in less available habitats and food resources being available for migrating juveniles (Hobday et al., 1999).

The Barker Inlet is the largest estuary in South Australia lying within the Gulf St Vincent. It is an inverse estuary due to high evaporation and low freshwater inflow. The Barker Inlet serves as a nursery ground for both post larvae and juveniles of the commercially important King George whiting (Sillaginodes punctatus). This nursery system provides seagrass beds of Zostera sp. and Heterozostera sp. that are vital for the successful recruitment of S. punctatus post larvae (Jones 1984; Fowler et al. 2002). However, susceptibility to global warming and anthropogenic activities such as storm water runoff and treated effluent has resulted in considerable changes to habitat structured and distribution in this region (Petrusevics 1993; Hossain, Hemraj, et al. 2017). In South Australia, S. punctatus spawn in the deep offshore waters off Kangaroo Island where ocean currents transport larvae northwards into the shallow waters of Gulf St Vincent (Fowler et al. 2002). Throughout winter and spring, S. punctatus larvae recruit into the shallow seagrass beds in protected bays (Fowler and Short 1996). The juvenile fish develop in these nursery areas for 1–2 years where they primarily feed on copepods, amphipods and polychaete worms (Connolly 1995) before moving out into the open waters of the gulfs. At approximately three years of age, S. punctatus begin their migration back towards the spawning grounds (Fowler et al. 2002). The recruitment success of S. punctatus post larvae that settle into seagrass beds likely drives the population dynamics of adult fish (Myers and Cadigan 1993). Despite competition links to survival of early life stages, no study on S. punctatus has evaluated the potential for trophic interactions with other seagrass dwelling fishes, or how S. punctatus recruitment might be impacted by habitat loss and competition for resources.

Within a nursery, there is a dynamic use of prey resources from different age classes and species, leading to complex trophic interactions. The objective of this study was to use juvenile S. punctatus of various ages throughout their temporary residency as a representative species to assess the potential food competition between recruiting fish and permanent resident fish over the period of ontogenetic diet shift. This study tests the hypothesis that permanent resident fishes compete for food with new settlers. The results would provide insight into the understanding of possible exclusion of recruiting fish by permanent dwelling fishes in the same nursery ground within a seagrass habitat.

Materials and methods

Water quality parameters and fish collection

Monthly sampling for post larvae of Sillaginodes punctatus and other resident fish was undertaken for a period of six months between June and November 2007. The sampling area was at King’s Beach, located at the northern end of the Barker Inlet (Figure 1), which historically has provided the largest catches of juvenile S. punctatus (Jackson and Jones 1999). Sampling was conducted using a 5-m beach seine net with a 1-mm mesh. Three replicate hauls were conducted each month one hour either side of low tide between 1000 and 1200 h. For each haul, the net was towed perpendicular to the beach between two people over a patchy 20-m stretch of Zostera sp. and Heterozostera sp. seagrass beds where juvenile whiting were likely to reside. Net hauls were separated by 10–15 m. After completing each haul, the net was redirected towards the beach, pursed and lifted onto the beach. All fish were removed from the net and placed into a lethal dose of benzocaine prior to preservation in 10% buffered formalin. In order to compare diets of post larvae with larger-sized S. punctatus, a 60-m seine net with 2-m mesh wings and a bag mesh of 0.5 cm was deployed in January 2008 at the same location to capture early settlers (61-120 mm) and previous year recruits (>120 mm) for dietary comparisons. The sizes of S. punctatus used in this study were well below the size at maturity (30 cm) around 3 years old (Fowler et al. 2002). Temperature and salinity were measured in triplicate upon arrival at the study site in each month prior to fish and zooplankton sampling (Table 1).

Figure 1. Location of study site (King’s Beach, Barker Inlet) in relation to South Australian coastline (adapted from Cann et al. 2009).

Table 1. Monthly variations of water temperature, salinity and fish abundance with the same fishing effort (60 m trawling distance) at King’s Beach, Barker Inlet, South Australia.

Month	Temperature (°C)	Salinity (ppt)	Fish (n)
June July August September October November	11.7 11.1 12.2 20.8 17.9 20.4	38.0 38.5 38.8 38.8 40.0 40.5	155 28 168 51 176 244

Collection and treatment of pelagic and benthic food sources

Pelagic zooplankton samples were collected monthly by towing a plankton net (30-cm open diameter, 100-µm mesh) fitted with a flow meter over the seagrass where fish were collected. As the water level was different at each sampling month, the zooplankton net was towed just above the level of the seagrass on all occasions. Each tow covered a length of 60 m and was replicated three times. The zooplankton samples were then transferred to storage containers and preserved in 3–5% neutrally buffered formalin. An exact volume (2.5% of the total) was subsampled in triplicate after thoroughly mixing the sample and then pipetting each subsample into a Sedgewick-Rafter counting cell under a microscope at 40–100× magnification.

To collect sediment samples of benthic fauna (e.g. copepod, amphipod, decapod, polychaete, nematode and molluscan), two replicated core samples were taken monthly at each of the three net haul sites, yielding a total of six cores per month. To collect samples, a 10.5 cm diameter piece of PVC pipe with a 0.25-mm mesh covering the top was pushed 5 mm into the sediment. A steel plate was then forced under the pipe and the corer was inverted to capture the sediment as described in Jenkins and Hamer (2001). Most of the water was drained through the mesh and the sediment was placed into containers for processing in the laboratory. To facilitate sorting organisms from the sediment, all sediment samples were sieved through four mesh sizes: 2, 1, 0.5, 0.25 mm and the infauna and epifauna from each core were collected. Samples were placed into a counting wheel, which held 5–10 mL samples in a rotating circular trough. Infauna and epifauna were counted and identified on a dissecting microscope at 40× magnification. For the small mesh sizes where sediment remained, the samples were preserved in a formalin sucrose solution and stained with rose Bengal during counting and identification. Infauna and epifauna were taxonomically identified to the level of order.

Fish dietary analysis

In the laboratory, all fish captured in the net tows were identified and measured to the nearest millimetre using standard length (tip of the snout to caudal peduncle). Fish were dissected by removing the outer flesh and ribcage from one side of the fish and the stomach and intestine were excised. Only prey items within the oesophagus and stomach were analysed by removing the intestine from the posterior of the stomach with a scalpel. The stomachs were then placed in a drop of water and an incision was made so that the contents could be flushed out into the water. The water containing prey items was then drawn through a pipette and placed onto a Sedgewick counting chamber for identification and enumeration. The only exception to this was for pipefish which have no distinct stomach and consequently, the entire digestive tract was used. Depending on the total number of fish species collected, up to 20 stomachs of each species were analysed for diet comparison.

Percentage of prey occurrence in stomachs was calculated as the percent of a prey found in all stomachs of a particular species. Mouth gape for each fish was recorded by placing the fish under a microscope fitted with a digital camera (Moticam 2500), extending the mouth with a pair of forceps and taking a digital image. The Motic image program (Motic image plus 2.0) was then used to measure the mouth gape to the nearest 0.1 mm using a subsample of 10 fish per species.

Prey types identified in the fishes’ diets were used in calculating dietary characteristics. These prey types included copepods (cyclopoid, calanoid, harpacticoid porcelid harpacticoid, and nauplii), amphipods (gammarids and caprellids), tanaids, mysid shrimp, cumaceans, penaeid shrimp, polychaete worms, barnacle nauplii and plant material. Porcelid harpacticoids and caprellid amphipods were placed separately to other harpacticoids and gammarus amphipods using body morphology and structure (Karanovic 2008; Hayward and Ryland 2017).

Food preference

The Manly/Chesson index (Chesson 1983) was used to determine prey preference of the different fish species.${\alpha }_i=\frac{r_i/n_i}{{\sum }_{i=1}^m{r}_i/n_i},=1\dots ,m$where α_i is the preference for prey type i ranging from 0 to 1, n_i is the proportion of prey type i in the environment, r_i is the proportion of i in the fish stomach, and m is the number of prey types in the environment.

To obtain a better comparison, dietary preference was further calculated as an electivity index (ε):${\epsilon }_i=\frac{m{\alpha }_i-1}{(m-2){\alpha }_i+1},i=\dots ,m$where the α_i is the preference value and m is the number of prey types. The values (ε_i) range from −1 to +1, where −1 indicates the absence of prey in stomachs and therefore suggests prey avoidance. Conversely, positive values suggest active selection of prey types. Results of zero indicate that there is no or little selection and that feeding is at random.

Dietary overlap

Diet overlap was calculated using Schoener’s overlap index (Schoener 1970).$\alpha =1-0.5\left(\sum _{i=1}^n\left|Pij-Pik\right|\right)$The index determines overlap (α), where P_ij = the proportion of the _ith resource (prey category) used by species _j, and P_ik = the proportion of the _ith resource used by species k. Overlap index values range from 0 (no overlap) to 1.0 (complete overlap), Values 0–0.29 indicate low overlap, 0.3–0.59 indicate moderate, and ≥0.6 indicate high dietary overlap between the two fish species being compared (Langton 1982).

Feeding strategy

To determine if fish fed as specialists or generalists, Levins index (Krebs 1999) niche breadth was utilised:$\mathrm{B}={\left[\sum _{i=1}^n{\mathrm{P}}_i^2\right]}^{-1}$where P_i is the proportion of the _ith prey in the diet of a fish species and the n is the number of prey groups. The average percentage of prey numbers (n) was used as the proportion (n%). Low values (B) indicate specialists and high values indicate generalists (Fjosne and Gjosaeter 1996). A standardised measure of this niche breadth B_A is calculated as:$BA=\frac{B-1}{n-1}$

where the value of B_A ranged from 0 (specialist) to 1 (generalist).

Statistical analysis and calculation

Due to data availability, the abundance of selected fish species (i.e. S. punctatus <60 mm, Stigmatopora nigra, F. lateralis, Gymnapistes marmoratus, and Heteroclinus adelaide) and prey types (i.e. harpacticoid copepods and amphipods) were used in correlation analysis. Spearman’s rank correlation analyses were used to determine the relationship between prey abundance and fish abundance using SPSS (version 18, IBM Corporation).

Results

During the study period from a cold and wet season (June) to hot and dry season (November), water temperature varied from 11.1°C to 20.8°C. A small increase in salinity was recorded from 38 to 40.5 ppt during the sampling period (Table 1). There was no significant correlation between total number of fish collected and temperature or salinity (r = 0.43, P = 0.40; r = 0.57, p = 0.23, respectively).

In benthic samples, prey species were dominated by harpacticoid copepods followed by gammarid amphipods and errant polychaete worms (Table 2). Over the sampling period, total abundance of harpacticoid copepods peaked in July and was lowest in October (Table 2). In comparison, the maximal abundance of gammarid amphipod occurred in September, but its lowest abundance was found in November. Errant polychaete abundance showed two peak periods in June and August.

Table 2. The abundance of benthic infauna and epifauna (mean ± SD, n = 6 per month) included in a sediment core area (86.6 cm²) at King’s Beach, Barker Inlet, South Australia (2007).

	June	July	August	September	October	November	Total
Amphipoda
Caprellid amphipod	0.2 ± 0.2	2.8 ± 2.8	4.3 ± 2.6	0	0.7 ± 0.3	0	13.9
Gammarid amphipod	18.5 ± 7.3	152.0 ± 25.8	61.5 ± 38.6	285.7 ± 64.8	79.5 ± 32.3	13.2 ± 2.8	982.0
Copepoda
Calanoid copepod	0	0	0	0	0	0	0
Cyclopoid copepod	12.8 ± 7.1	0	5.7 ± 4.4	0	0	0	30
Harpacticoid copepod	228.5 ± 42.4	1640.7 ± 148.2	880.5 ± 155.0	161.2 ± 56.5	62.8 ± 12.8	119.2 ± 10.5	3518.3
Porcelid harpacticoid	0	0	2.2 ± 2.2	0.3 ± 0.3	0.5 ± 0.5	0	6.0
Cumacea Cumacean	0	2.2 ± 2.2	2.7 ± 2.3	0	0	0	9.4
Decapoda Penaeid prawn	0.3 ± 0.2	0	0	0.2 ± 0.2	0	0.2 ± 0.2	1.1
Mysida Mysid shrimp	0	0	0	0	0.2 ± 0.2	0	0.4
Tanaidacea Tanaid	0	0	4.3 ± 2.2	0.2 ± 0.2	4.3 ± 2.3	0.2 ± 0.2	13.9
Mollusca Molluscan veliger	0	0	0	0	1.5 ± 1.0	0	2.5
Nematoda Nematode	109.3 ± 32.8	0	13.0 ± 8.6	3.5 ± 1.8	0.8 ± 0.7	5.7 ± 1.4	177.6
Polychaeta Errant polychaete	161.0 ± 48.6	73.0 ± 11.4	182.2 ± 48.9	134.2 ± 31.6	62.5 ± 34.8	9.5 ± 1.7	802.0
Sedentary polychaete	20.3 ± 6.7	18.7 ± 4.2	31.0 ± 17.2	5.5 ± 2.1	20.3 ± 5.8	34.5 ± 3.3	169.8
Total	551.0	2084.0	1669.4	590.8	323.8	202.6	5421.6

In pelagic samples, harpacticoid copepods and copepod nauplii were the most common pelagic prey available to fish living in the seagrass beds (Table 3). Cyclopoid copepods and polychaete larvae were the next abundant although polychaete larvae did not appear in the stomach contents of any fish species. Harpacticoid copepods and copepod nauplii recorded two peaks in abundance in September and November. Polychaete larvae showed two peaks with the first one in August and the second occurring in November. Mollusc veliger larvae were only found in October.

Table 3. Abundances of pelagic zooplankton (N m⁻³, mean ± SD) collected with a zooplankton trawl net at King’s Beach, Barker Inlet, South Australia (2007).

	June	July	August	September	October	November	Total
Amphipoda
Gammarid amphipod	0	3.6 ± 2.3	2.6 ± 2.6	47.2 ± 15.7	1.6 ± 1.6	0	55.0
Copepoda
Calanoid copepod	16.5 ± 7.2	25.7 ± 14.8	15.7 ± 6.8	293.6 ± 109.5	7.8 ± 1.5	332.9 ± 50.6	692.2
Copepod nauplii	203.6 ± 121.6	258.5 ± 28.1	733 ± 170.7	870.2 ± 299.0	237.5 ± 29.1	2131.0 ± 461.5	4433.8
Cyclopoid copepod	130.5 ± 91.6	92.8 ± 25.6	562.2 ± 164.7	256.9 ± 29.2	51.9 ± 16.6	1017 ± 112.1	2111.3
Harpacticoid copepod	597.6 ± 215. 7	476.4 ± 145.4	1425.9 ± 282.1	1986.6 ± 391.4	385.3 ± 55	3017 ± 207.1	7888.8
Mollusca
Molluscan veliger	0	0	0	0	196.6 ± 47.6	0	196.6
Polychaeta
Errant polychaete	0	10.5 ± 6.9	5.2 ± 5.2	10.5 ± 5.2	4.7 ± 2.7	5.2 ± 2.6	36.1
Polychaete larvae	80.2 ± 59.2	61.9 ± 19.1	783.7 ± 129.1	340.7 ± 51.7	23.6 ± 5.4	353.9 ± 136.4	1644.8
Total	1028.4	929.5	3528.3	3805.7	909.0	6857.7	17,058.6

There was a negative trend between total benthic prey density (Arthropoda, Annelida, Mollusca), and total fish population (r = 0.83, p = 0.04, n = 6), although comparisons for all individual fish with total benthic prey density had no significant correlations except A. microstoma (r = 0.98, p < 0.001). No significant correlations were recorded between fish species and total pelagic prey density (r = 0.25, p = 0.62, n = 6). No significant correlations were observed between benthic or pelagic prey density and water temperature or salinity (p > 0.21). There was a negative but non-significant correlation between benthic prey abundance and temperature (r= −0.54) and salinity (r= −0.57) while there was a positive correlation between pelagic prey and temperature (r= 0.60) and salinity (r= 0.40).

Fish species composition

Throughout the study, 13 fish families were sampled from the seagrass beds (Table 4). The family of greatest abundance was Gobiidae (62%), with Favonigobius lateralis, accounting for 57% of all fish caught. The second most common family was Syngnathidae, with three species providing 15% of the total catch, of which Stigmatopora nigra was the most common at 14%. Both F. lateralis and S. nigra were the only species observed in all months and were the main permanent residents in this system. The greatest influx of fish to the region occurred in October and November with the third (Clinidae, Heteroclinus adelaide 8.4%), fourth (Sillaginidae S. punctatus 4.1%) and fifth (Scorpaenidae Gymnapistes marmoratus 2%) most abundant families recruiting throughout this period (Table 4).

Table 4. Monthly catch summary of fish species collected at King’s Beach, Barker Inlet, South Australia from June to November 2007.

Species	June	July	August	September	October	November	Total
Atherinidae
Atherinosoma microstoma	4	0	2	2	12	19	39
Clinidae
Heteroclinus adelaide (adult)	1	0	0	0	0	0	1
Heteroclinus adelaide (juvenile)	0	0	3	4	17	44	68
Engraulididae
Sprattus novaehollandiae	0	0	0	0	0	4	4
Gobiidae
Arenigobius bifrenatus	1	0	1	1	2	8	13
Bathygobius kreffti	0	0	0	0	0	9	9
Favonigobius lateralis	140	15	77	28	108	101	469
Gobiopterus semivestitus	1	0	1	0	1	0	3
Unidentified	0	0	0	0	4	13	17
Monacanthidae
Meuschenia freycineti	1	1	1	0	0	0	3
Mugilidae
Aldrichetta forsteri	0	0	5	0	0	0	5
Odacidae
Neoodax balteatus	1	1	1	0	0	0	3
Pleuronectidae
Rhombosolea tapirina	0	1	1	0	0	0	2
Scorpaenidae
Gymnapistes marmoratus (adult)	0	0	1	0	0	0	1
Gymnapistes marmoratus (juvenile)	0	0	0	0	1	15	16
Sillaginidae
Sillaginodes punctatus	3	3	0	10	15	3	34
Syngnathidae
Stigmatopora nigra	3	4	73	6	11	18	115
Vanacampus vercoi	0	0	0	0	3	5	8
Kaupus costatus	0	0	0	0	2	0	2
Terapontidae
Pelates octolineatus	0	3	1	0	0	0	4
Tetraodontidae
Contusus brevicaudus	0	0	1	0	1	0	1
Tetractenos glaber	0	0	0	0	0	5	5
Total	155	28	168	51	176	244	822

Diet composition

Diet varied between S. punctatus of different size classes with the 20–60 mm class consuming primarily harpacticoid copepods (86%) and small gammarus amphipods (9%, Figure 2). Despite the low quantity of gammarus amphipods consumed, this prey item was consumed regularly with 80% of S. punctatus stomachs making it a very important food source (Table 5). The remainder of the diet consisted of calanoid and cyclopoid copepods, and the occasional worm or crustacean (mysid shrimp). The S. punctatus in the 61–120 mm class consumed primarily amphipods (84%) with worms and other crustaceans making up the remainder at low frequencies (Table 5). Stomachs of the largest S. punctatus size class (>120 mm) contained only polychaete worms (Figure 2). The stomachs of F. lateralis contained a large proportion of harpacticoid copepods (88%) with a small percentage of the diets made up of amphipods (10%) and polychaete worms (2%, Figure 2). Amphipods were a frequently consumed prey item being present in 40% of stomachs (Table 5). The juvenile G. marmoratus and H. adelaide had similar diets which consisted mostly of crustaceans including amphipods (83%), tanaids, penaeid and mysid shrimp (<10%). A small percentage of their diets consisted of worms (<2% in both species) and copepods (7% in G. marmoratus and 11% in H. adelaide, Figure 2), but only occurred in a few of the stomachs (Table 5). The S. nigra primarily consumed copepods (59% cyclopoids, 35% harpacticoids, and 4% calanoids) with some incidents of small crustacean nauplii (0.7%, Figure 2) although the frequency of most prey items consumed was greater than 50% suggesting broad feeding habits (Table 5). The P. octolineatus contained a mix of copepods (15%) and amphipods (9%) but stomach contents mainly consisted of plant material (73%, Figure 2). The A. microstoma diets also consisted of a mix of calanoid, cyclopoid and harpacticoid copepods (93%) which were the most frequently consumed item (Table 5).

Figure 2. Individual prey types (%N) in the diet of the most common fish species captured in a seagrass bed in the Barker inlet from June 2007 to January 2008. *Other crustaceans include cumacean, tanaids and penaeid prawns grouped together.

Table 5. The occurrence (%) of each prey in the stomach of fishes collected at King’s Beach, Barker Inlet, South Australia from June 2007 to January 2008.

	S. punctatus 20–60 mm	S. punctatus 61–120 mm	S. punctatus >120 mm	F. lateralis	H. adelaide	G. marmoratus	S. nigra	A. microstoma	P. octolineatus
Fish sample size (n)	20	20	11	20	20	20	20	20	20
Amphipoda
Gammarid amphipod	80	76	0	40	100	75	55	50	0
Caprellid amphipod	0	0	0	0	5	0	0	5	5
Copepoda
Cyclopoid copepod	25	0	0	10	10	10	65	15	15
Calanoid copepod	15	0	0	0	0	5	60	5	0
Harpacticoid copepod	80	14	0	90	0	5	80	80	30
Porcelid harpacticoid	20	0	0	0	40	0	15	5	0
Copepod nauplii	5	0	0	0	0	0	0	15	0
Cirripedia
Barnacle nauplii	0	0	0	0	0	0	5	10	0
Cumacea
Cumacean	0	0	0	0	5	0	0	5	0
Decapoda
Penaeid prawn	0	5	0	0	10	10	0	5	0
Mysida
Mysid shrimp	5	0	0	0	10	5	0	5	0
Tanaidacea
Tanaid	0	0	0	0	5	0	0	0	0
Polychaeta
Polychaete worm	15	38	90	10	0	5	0	10	0
Plant material	0	0	0	0	0	0	0	0	80

Niche breadth, prey preference and diet overlap

According to the preference index, S. punctatus less than 60 mm and F. lateralis shared similar feeding behaviour showing active preference for harpacticoid copepods (ε_i = 0.5) and neutral selection for amphipods (ε_i = 0.05, −0.24, respectively). Food preference of both G. marmoratus and H. adelaide was positive for amphipods (ε_i > 0.5). With the exception of S. nigra, all fish species showed active avoidance of calanoid and cyclopoid copepods. All fish species exhibited selection against polychaete worms and large crustaceans (with the exception of S. punctatus >120 mm TL). G. marmoratus and H. adelaide were the only two fish species that selected against harpacticoid copepods (Table 6). Niche breadth was quite low for all species with the highest value observed in S. nigra (B_A = 0.09, Table 6). The G. marmoratus and H. adelaide with their similar diets had a slightly lower niche breadth (B_A = 0.04) while S. punctatus >120 mm showed no dietary breadth consuming only one prey type (Table 6). Juvenile S. punctatus (<60 mm) had high dietary overlap (α ≥ 0.6) with F. lateralis and S. nigra while moderate (α = 0.3–0.59) overlap was observed with P. octolineatus (Table 7). Whiting <60 mm exhibited low (α < 0.029) overlap with H. adelaide, G. marmoratus, A. microstoma and also with the larger size of S. punctatus (61–120 mm) and high dietary overlap with H. adelaide and G. marmoratus, moderate overlap with A. microstoma and low overlap with all other species and S. punctatus size classes. The S. punctatus >120 mm had very little overlap with other species or other size classes of S. punctatus (Table 7).

Table 6. The range of fish length and mouth gape, mean stomach fullness rank and electivity index of fish caught between June 2007 and January 2008.

Fish species	Length (mm)	Mouth gape (mm)	Stomach fullness	Niche breadth				Electivity (εi)
					Cal	Cyc	Harp	Nau	Amp	Cru	Wor
Atherinidae
Atherinosoma microstoma	31–62	1.5–4.3	7 ± 1.8	0.02	−0.78	−0.90	0	−0.85	−0.04	−0.89	−0.86
Clinidae
Heteroclinus adelaide	23–46	1.8–4.5	7 ± 1.2	0.04	−1.00	−1.00	−0.69	−1.00	0.77	−0.51	−1.00
Gobiidae
Favonigobius lateralis	27–45	2.0–3.9	4 ± 3.0	0.02	−1.00	−0.91	0.54	−1.00	−0.24	−1.00	−0.9
Scorpaenidae
Gymnapistes marmoratus	18–26	2.5–4.4	4 ± 2.6	0.04	−0.87	−0.85	−0.97	−1.00	0.52	−0.35	−0.98
Sillaginidae
Sillaginodes punctata (20-60 mm)	17–45	0.8–2.8	5 ± 2.4	0.03	−0.72	−0.75	0.50	−1.00	0.05	−0.9	−0.76
S. punctata (61-120 mm)	84–112	3.0–6.0	5 ± 2.2	0.03	−1.00	-1.00	−0.89	−1.00	0.57	−1.00	−0.34
S. punctata (>120 mm)	177–203	6.0–9.0	7 ± 1.8	0.00	−1.00	−1.00	−1.00	−1.00	−1.00	−1.00	1.00
Syngnathidae
Stigmatopora nigra	67–100	0.7–1.1	6 ± 3.5	0.09	−0.22	0.17	0.03	−0.97	−0.78	−1.00	−1.00

Notes: Stomach fullness ranged from 0 (empty) to 10 (full). Niche breadth index values range from 0 (specialist) to 1 (generalist) in feeding. The food electivity (εi) ranges from −1 (avoidance) to + 1 (positive selection). Cal: calanoid, Cyc: cyclopoid, Har: harpacticoid, Nau: Nauplii, Amp: amphipod, Cru: other crustaceans, Wor: polychaete worms.

Table 7. Dietary overlap of King George whiting (Sillaginodes punctatus) at three size classes with other commonly occurring fishes in Barker inlet from June 2007 to January 2008.

	S. punctatus (20–60 mm)	S. punctatus (61–120 mm)	S. punctatus (>120 mm)
Atherinidae
Atherinosoma microstoma	0.075	0.489	0.003
Clinidae
Heteroclinus adelaide	0.1	0.870	0.001
Gobiidae
Favonigobius lateralis	0.965	0.095	0.013
Scorpaenidae
Gymnapistes marmoratus	0.17	0.885	0.031
Sillaginidae
S. punctatus (20–60 mm)	–	0.1	0.019
S. punctatus (61–120 mm)	0.235	–	0.115
S. punctatus (>120 mm)	0.019	0.115	–
Syngnathidae
Stigmatopora nigra	0.928	0.055	0
Terapontidae
Pelates octolineatus	0.4	0.13	0

Notes: Values 0–0.29 indicate low; 0.3–0.59 moderate; and ≥0.6 high dietary overlap. The values (>0.6) are bolded to show the trend of high dietary overlap.

Discussion

Fish species composition in Barker Inlet is similar to that reported in other studies of seagrass areas in temperate Australia (Crinall and Hindell 2004; Smith, Jenkins, et al. 2008). In the Barker Inlet habitat, fish abundance was relatively low compared to previous studies in the same area (Fowler and Short 1996; Jackson and Jones 1999). Habitat quality is often related to habitat selection, fish growth and survival (Nemerson and Able 2004). The seagrass beds at the sample site were covered by a thick coating of sediment which probably devalued the habitat quality and may have been responsible for the overall low fish abundance and low recruitment of S. punctatus into this historically productive nursery.

In a 10-year study, Jackson and Jones (1999) provided a thorough historical analysis of fish assemblages in the Port River and specifically at King’s Beach where this study was conducted. King’s Beach previously had a large population of S. punctatus and was the most abundant species at this location, approximately 2.8 times higher than the next most abundant family (Mugilidae). In this study, S. punctatus was ranked fifth behind Gobiidae, Syngnathidae, Clinidae and Atherinidae. Fish assemblages appear to have changed considerably between the two studies especially in regard to the number of S. punctatus.

The timing of benthic settlement can be important where resources are limited because exploitative competition may lead to individuals depleting a food supply before the arrival of a competitor (Ward et al. 2006). Differences in recruitment timing can also be important by increasing niche separation between species (Golani, 1994). In this study, we found that S. punctatus were recruiting to the seagrass beds in small numbers from June to November. The arrival of juveniles of H. adelaide, G. marmoratus and F. lateralis occurred later in the sampling period from August to November generally peaking in abundance in November. The data of dietary composition in the stomach suggest that S. punctatus arriving to the seagrass earlier in the year may be advantageous to recruitment success as competition for resources is primarily with permanent residents and not the increased number of conspecifics and migrants arriving later in the year in the seagrass nursery ground.

Post larval fish in the 20–60 mm size class often consume copepod and amphipod prey items (Livingston 1982; Whitfield 1985; Schlacher and Wooldridge 1996). While there are similarities in the size of fish species, mouth morphology appears to be important in separating diet selection as is seen in other species occupying the same habitat (Hyndes et al. 1997; Linke et al. 2001). Fish species within the study site were of similar body size. S. punctatus and F. lateralis had a small mouth gape and selected for small prey such as copepods compared to H. adelaide and G. marmoratus which had relatively larger mouth gapes and actively selected for the larger amphipod prey. This morphological characteristic separated the diet of post larval S. punctatus <60 mm from other species and potentially reducing food competition.

The F. lateralis shared a diet consisting mainly of harpacticoid copepods with S. punctatus <60 mm, as indicated by the high overlap index close to 1 (i.e. complete diet overlap). Smith, Hindell, et al. (2008) observed that most fish favoured the seaward side of the seagrass, whereas gobies Nesogobius sp. favoured the shoreward side of seagrass beds, suggesting spatial segregation with other seagrass-associated species. In this study, S. punctatus were located primarily over seagrass beds whereas the gobies, F. lateralis, could easily be observed being captured in the net on the shoreward side of the seagrass beds in shallower water. Therefore, despite the high food overlap, it is likely that these species are spatially separated to some extent. The macroalgae, Ulva australis, is often present at King’s Beach (Jackson and Jones 1999) and we found that F. lateralis often used this weed as shelter on the sand between the shore and the seagrass beds, whereas most other fish species were located in the seagrass beds. The difference in habitat selection along with preference for the most abundant prey species (harpacticoid copepods) may diminish food competition between recruiting S. punctatus <60 mm and permanent resident F. lateralis despite the high overlap recorded (Cabral et al. 2007). The increased shelter of Ulva australis for F. lateralis may explain the high abundance of this species despite the poor state of the seagrass beds. The preference for Ulva australis by F. lateralis may become advantageous allowing them to thrive in a sub-optimal seagrass habitat. Given the similarity in diets between F. lateralis and S. punctatus, loss of seagrass beds will likely reduce the habitat separation as S. punctatus seek other forms of shelter potentially contributing to an increase in competition for food resources. Generally, there are positive relationships observed between seagrass biomass and abundance of prey items such as harpacticoids and amphipods (Bologna and Heck 2002; Murphy et al. 2010). Loss of shelter may result in a loss of amphipods and force H. adelaide and G. marmoratus to exploit a less favoured prey items increasing the competition between seagrass associated fish.

The stomachs of S. nigra usually contain small amphipods and harpacticoid copepods (Howard and Koehn 1985). The S. nigra exhibited neutral selection for all families of copepods suggesting a diverse and generalised feeding habit. These data agree with Howard and Koehn (1985) who observed that S. nigra feed on pelagic or epibenthic prey on the eelgrass. In contrast, the lack of pelagic prey in the diets of S. punctatus suggests that its feeding area is close to the benthic region, although in shallow environments such as the Barker Inlet study site, feeding on pelagic prey items can be done without much change to the fish’s position in the water column. Mobility is a factor that can potentially reduce competition within an ecosystem (Gibson and Ezzi 1987). The S. punctatus are not confined to seagrass beds often feeding over bare sand (Jenkins and Wheatley 1998), providing evidence that feeding interactions may also be avoided between recruiting S. punctatus and resident S. nigra via spatial differentiation.

Ontogenetic changes in the diet of S. punctatus also aided in dietary separation. The S. punctatus >60 mm consumed a greater proportion of amphipods and fewer copepods. In contrast, S. punctatus >120 mm had a diet consisting almost entirely of polychaete worms which were not consumed in large amounts by any other species or S. punctatus of different sizes. Changes in ontogenetic food preference are important in creating greater niche partitioning and reducing competition (Schellekens et al. 2010). The relatively large mouth gape of juvenile H. adelaide and G. marmoratus indicates that they target larger prey than newly settled S. punctatus and this would make them more competitive with early recruited than newly settled S. punctatus. The ontogenetic shift away from small prey items as S. punctatus grow also limits the time spend competing for food with small permanent resident species.

Resource partitioning of fish can also be enhanced by temporal differences in the period of peak feeding (Piet and Guruge 1997). In this study, the stomach contents of both G. marmoratus and H. adelaide were almost fully digested. Scorpaenids feed at both day and night (Hobson 1974), while weedfish Cristiceps australis move to areas of higher food abundance at night (Smith, Hindell, et al. 2008). In our study, sampling was conducted in the late morning, therefore the highly digested food in the stomachs of G. marmoratus and H. adelaide were probably ingested during the night. Juvenile S. punctatus are reported to only feed during the day (Connolly 1995), therefore competition with G. marmoratus or H. adelaide might be reduced through feeding at different times.

The low abundance of different prey species may contribute to a high degree of dietary overlap between fish species (Moyle and Cech 2004). In this study, niche breadth was low due to the relatively small amount of prey items available at high concentrations. Benthic prey was dominated by harpacticoid copepods and amphipods with only very small amounts of other prey items being recorded. The lack of prey items is reflected in the niche breadth index, suggesting that most of these fish species feed as specialists.

Potential competitors rarely reach the population densities that exceed resource supplies (Moyle and Cech 2004). Despite the significant correlation observed between total fish population and prey benthic prey density, predation on harpacticoid copepods is not thought to be the principal cause of variations in seasonal abundance of copepod prey (Gee 1989). Likewise, predation on meiofauna, in general, does not significantly reduce prey density due to the rapid reproductive rates of meiofauna (Coull 1999). Therefore, it is unlikely that this nursery is resource limited in terms of food, despite the observed correlation between fish and benthic prey density and overlap being observed between a few fish species. The overall low numbers of fish and the abundance of harpacticoid copepods and amphipods suggest that there should be an adequate supply of food in the system and that competitive exclusion by depletion of food resources is not at a level likely to have significant influence on post larval recruitment or permanent resident populations.

In conclusion, S. punctatus of different size classes show distinct ontogenetic shifts in diet preference reducing the period of competition for food between age classes of S. punctatus, and small permanent resident fish. This study supports the hypothesis that species living in close proximity show dietary overlap and food competition, but the main prey types targeted by all fish are abundant and competition for scarce resources is unlikely to affect the recruitment success of recruiting fish in this system. Competition is also currently reduced by differences in mouth morphology between species and by discrepancy in temporal and spatial uses of prey items, allowing a number of species to coexist without reducing resources to a limiting level. However, loss of seagrass habitats is likely to exacerbate the competitive interactions of fish within this nursery through decreased prey abundance and reduced spatial segregation.

Acknowledgements

Gratitude is extended to Anthony Fowler, Liang Song and Sophie Leterme, for their contribution to site selection, field sampling and discussion on this project. Animal ethics approval was obtained through Flinders University approval number E318.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This study was part of a PhD project funded by Flinders University and the Playford Memorial Trust.