INTRODUCTIONTop

Estuaries are highly successful nursery areas worldwide in an otherwise competitive environment where refuge and food are premium (Whitfield 1999Whitfield A.K. 1999. Ichthyofaunal assemblages in estuaries: a South African case study. Rev. Fish. Biol. Fisher. 9: 151-186., Potter et al. 2015Potter I.C., Tweedley J.R., Elliott M., et al. 2015. The ways in which fish use estuaries: a refinement and expansion of the guild approach. Fish. Fish. 16: 230-239.). Since multiple species co-exist in estuarine nursery areas, this presents clear evidence of successful niche differentiation and some level of successful community co-existence. Co-existing species can differentiate niches through habitat partitioning for a multitude of reasons (Felley and Felley 1986Felley J.D., Felley S.M. 1986. Habitat partitioning of fishes in an urban, estuarine bayou. Estuaries 9: 208-218., Welsh and Perry 1998Welsh S.A., Perry S.A. 1998. Habitat partitioning in a community of darters in the Elk River, West Virginia. Env. Biol. Fish. 51: 411-419.) but this is seldom explored across a range of habitat types in estuarine ecosystems. This work examined a well-known estuarine fish nursery in warm temperate South Africa in order to further understand habitat partitioning among juvenile fishes. Early stage marine fishes recruit into estuarine nurseries typically in spring and summer to utilize the mosaic of available habitats in these systems (França et al. 2009França S., Costa M.J., Cabral H.N. 2009. Assessing habitat specific fish assemblages in estuaries along the Portuguese coast. Estuar. Coast. Shelf Sci. 83: 1-12.) during certain life stages (Strydom 2015Strydom N.A. 2015. Patterns in Larval Fish Diversity, Abundance, and Distribution in Temperate South African Estuaries. Estuar. Coast. 38: 268-284., Potter et al. 2015Potter I.C., Tweedley J.R., Elliott M., et al. 2015. The ways in which fish use estuaries: a refinement and expansion of the guild approach. Fish. Fish. 16: 230-239.). Specific habitat preferences within these systems remain an area of interest for fish conservation worldwide (Beck et al. 2001Beck M.W., Heck K.L., Able K.W., et al. 2001. The Identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: a better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51: 633-641., Able 2005Able K.W. 2005. A re-examination of fish estuarine dependence: evidence for connectivity between estuarine and ocean habitats. Estuar. Coast. Shelf Sci. 64: 5-17., Strydom 2015Strydom N.A. 2015. Patterns in Larval Fish Diversity, Abundance, and Distribution in Temperate South African Estuaries. Estuar. Coast. 38: 268-284.). Fishes are likely to select those habitats, or a combination of habitats, that meet their physico-chemical requirements as well as provide abundant food resources and protection from larger predatory fishes (Courrat et al. 2009Courrat A., Lobry J., Nicolas D., et al. 2009. Anthropogenic disturbance on nursery function of estuarine areas for marine species. Estuar. Coast. Shelf Sci. 81: 179-190., França et al. 2009França S., Costa M.J., Cabral H.N. 2009. Assessing habitat specific fish assemblages in estuaries along the Portuguese coast. Estuar. Coast. Shelf Sci. 83: 1-12., Sheppard et al. 2011Sheppard J.N., James N.C., Whitfield A.K., et al. 2011. What role do beds of submerged macrophytes play in structuring estuarine fish assemblages? Lessons from a warm-temperate South African estuary. Estuar. Coast. Shelf Sci. 95: 145-155.).

Much research has focussed on the value of refugia in estuaries, specifically mangroves (Nanjo et al. 2014Nanjo K., Kohno H., Nakamura Y., et al. 2014. Differences in fish assemblage structure between vegetated and unvegetated microhabitats in relation to food abundance patterns in a mangrove creek. Fisher. Sci. 80: 21-41.) and eelgrass and/or seagrass habitats in both South Africa (Whitfield et al. 1989Whitfield A.K., Beckley L.E., Bennet B., et al. 1989. Composition, species richness and similarity of ichthyofaunas in eelgrass Zostera capensis beds of southern Africa. S. Afri. J. Mar. Sci. 8: 251-259., Paterson and Whitfield 2000Paterson A., Whitfield A.K. 2000. Do shallow-water habitats function as refugia for juvenile fishes? Estuar. Coast. Shelf Sci. 51: 359-364., Strydom 2003Strydom N.A. 2003. An Assessment of Habitat Use by Larval Fishes in a Warm Temperate Estuarine Creek Using Light Traps. Estuaries. 26: 1310-1318.) and other estuarine zones around the world (França et al. 2009França S., Costa M.J., Cabral H.N. 2009. Assessing habitat specific fish assemblages in estuaries along the Portuguese coast. Estuar. Coast. Shelf Sci. 83: 1-12., Baillie et al. 2015Baillie C.J., Fear J.M., Fodrie F.J. 2015. Ecotone effects on seagrass and saltmarsh habitat use by juvenile nekton in a temperate estuary. Estuaries Coasts. 38: 1414-1430.). This work has also been supplemented with the inclusion of saltmarsh creeks as important refugia for juvenile fishes in estuaries (Le Quesne 2000Le Quesne W.J.F. 2000. Nekton utilisation of intertidal estuarine marshes in the Knysna Estuary. Trans. Roy. Soc. S. Afr. 55: 205-214., Paterson and Whitfield 2000Paterson A., Whitfield A.K. 2000. Do shallow-water habitats function as refugia for juvenile fishes? Estuar. Coast. Shelf Sci. 51: 359-364., Jin et al. 2007Jin B., Fu C., Zhong J., et al. 2007. Fish utilization of a salt marsh intertidal creek in the Yangtze River estuary, China. Estuar. Coast. Shelf Sci. 73: 844-852.). However, most studies involving habitat evaluation have only considered two habitats simultaneously (Weinstein and Brooks 1983Weinstein M.P., Brooks H.A. 1983. Comparative ecology of nekton residing in a tidal creek and adjacent seagrass meadow: community composition and structure. Mar. Ecol. Prog. Ser. 12: 15-27., Sogard and Able 1991Sogard S.M., Able K.W. 1991. A comparison of eelgrass, sea lettuce, macroalgae and marsh creeks as habitats for epibenthic fishes and decapods. Estuar. Coast. Shelf Sci. 33: 501-519., Paterson and Whitfield 2000Paterson A., Whitfield A.K. 2000. Do shallow-water habitats function as refugia for juvenile fishes? Estuar. Coast. Shelf Sci. 51: 359-364.), sometimes with conflicting results on the value of certain habitat types for different species. Moreover, there is a paucity of work involving multiple habitat comparisons, including other substrata such as sand and mud (Sogard and Able 1991Sogard S.M., Able K.W. 1991. A comparison of eelgrass, sea lettuce, macroalgae and marsh creeks as habitats for epibenthic fishes and decapods. Estuar. Coast. Shelf Sci. 33: 501-519., Baillie et al. 2015Baillie C.J., Fear J.M., Fodrie F.J. 2015. Ecotone effects on seagrass and saltmarsh habitat use by juvenile nekton in a temperate estuary. Estuaries Coasts. 38: 1414-1430.).

In temperate South Africa, halophytic plant species such as seagrass (Zostera capensis) (Talbot and Bate 1987Talbot M.M.B., Bate G.C. 1987. The distribution and biomass of the seagrass Zostera capensis in a warm-temperate estuary. Bot. Mar. 30: 91-99.) and ricegrass (Spartina maritima) are widely distributed (Colloty et al. 2000Colloty B.M., Adams J.B., Bate G.C. 2000. The use of a botanical importance rating to assess changes in the flora of the Swartkops estuary over time. Water SA. 26: 171-180.) in the lower reaches of permanently open estuaries. Despite the known importance of these habitats, which support a high abundance and diversity of juvenile fishes due to their high productivity and structural complexity (Ter Morshuizen and Whitfield 1994Ter Morshuizen L., Whitfield A.K. 1994. The distribution of littoral fish associated with eelgrass Zostera capensis beds in the Kariega Estuary, a southern African system with a reversed salinity gradient. S. Afri. J. Mar. Sci. 14: 95-105., Martino and Able 2003Martino E.J., Able K.W. 2003. Fish assemblages across the marine to low salinity transition zone of a temperate estuary. Estuar. Coast. Shelf Sci. 56: 969-987., Sheppard et al. 2012Sheppard J., Whitfield A.K, Cowley P., et al. 2012. Effects of altered estuarine submerged macrophyte bed cover on the omnivorous Cape stumpnose Rhabdosargus holubi. J. Fish. Biol. 80: 705-712.), the value of vegetated areas relative to other adjacent habitat types on offer in estuarine nurseries leaves room for further enquiry.

Habitat use and preferences in young fishes utilizing estuarine nurseries is important for the elucidation of critical habitats for species and for conservation planning in estuaries worldwide (Beck et al. 2001Beck M.W., Heck K.L., Able K.W., et al. 2001. The Identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: a better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51: 633-641.). However, given conflicts in the literature, more information is needed to fully understand use patterns within estuarine nurseries.

The permanently open Swartkops Estuary on the warm temperate coast of South Africa provided an ideal study system for assessing habitat partitioning among juveniles fishes across a range of common habitat types that are typical in estuaries worldwide and could serve as nurseries. The ecology of Swartkops Estuary fish fauna is well studied, with research on adults (Marais and Baird 1980Marais J., Baird D. 1980. Seasonal abundance, distribution and catch per unit effort of fishes in the Swartkops estuary. S. Afr. J. Zool. 15: 66-71.), juveniles (Winter 1979Winter P.E.D. 1979. Studies on the distribution, seasonal abundance and diversity of the Swartkops Estuary ichthyofauna. MSc thesis. Univ. Port Elizabeth, 979., Beckley 1983Beckley L.E. 1983. The ichthyofauna associated with Zostera capensis (Setchell) in the Swartkops estuary, South Africa. S. Afri. J. Zool. 18: 15-24.) and larval stages (Strydom 2003Strydom N.A. 2003. An Assessment of Habitat Use by Larval Fishes in a Warm Temperate Estuarine Creek Using Light Traps. Estuaries. 26: 1310-1318., Strydom 2015Strydom N.A. 2015. Patterns in Larval Fish Diversity, Abundance, and Distribution in Temperate South African Estuaries. Estuar. Coast. 38: 268-284.) already undertaken.

The aim of this study was to assess the habitat partitioning in juvenile fishes in four abundant and well-defined habitat types, namely eelgrass/ricegrass vegetation stands, saltmarsh creeks, muddy substrata and sand substrata within the lower reaches of the estuary. It was hypothesized that species, particularly in the marine estuarine-dependent group that rely on estuaries as nurseries, will favour vegetated habitats, exhibiting a higher abundance and diversity of species, while lesser studied sand and mud substrata will show species-specific preferences (Connolly 1994Connolly R. 1994. A comparison of fish assemblages from seagrass and unvegetated areas of a southern Australian estuary. Mar. Freshwater. Res. 45: 1033-1044., Gray et al. 1996Gray C.A., McElligott D.J., Chick R.C. 1996. Intra- and Inter-estuary differences in assemblages of fishes associated with shallow seagrass and bare sand. Mar. Freshwater. Res. 47: 723-735.). It is also hypothesized that the physico-chemical conditions within each habitat type will be distinct and that fishes will be associated with specific environmental conditions, particularly warmer temperatures.

MATERIALS AND METHODSTop

Study area

The study area was located in the lower reaches of the Swartkops Estuary (33°52′S; 25°38′E), on the warm temperate coastline of South Africa (Fig. 1). The permanently open estuary is approximately 16 km in length with a tidal range of <1.5 metres (Beckley 1983Beckley L.E. 1983. The ichthyofauna associated with Zostera capensis (Setchell) in the Swartkops estuary, South Africa. S. Afri. J. Zool. 18: 15-24.). The area experiences bimodal rainfall with peaks in autumn and spring (Whitfield 1998Whitfield A.K. 1998. Biology and ecology of fishes in southern African estuaries. Ichthyological Monographs of the J.L.B Smith Institute of Ichthyology, No 2. 223 pp.). The lower reaches of the estuary are characterized by extensive mudflats, salt marshes and large stands of submerged aquatic vegetation dominated by halophytic eelgrass Zostera capensis and ricegrass Spartina maritima (Talbot and Bate 1987Talbot M.M.B., Bate G.C. 1987. The distribution and biomass of the seagrass Zostera capensis in a warm-temperate estuary. Bot. Mar. 30: 91-99., Colloty et al. 2000Colloty B.M., Adams J.B., Bate G.C. 2000. The use of a botanical importance rating to assess changes in the flora of the Swartkops estuary over time. Water SA. 26: 171-180.). The Tipper’s Creek arm of the lower estuary (Fig. 1) supports the highest percentage (59%) of this vegetation (Talbot and Bate 1987Talbot M.M.B., Bate G.C. 1987. The distribution and biomass of the seagrass Zostera capensis in a warm-temperate estuary. Bot. Mar. 30: 91-99.).

Field sampling and laboratory analysis

Juvenile fishes were sampled in the lower reaches of the Swartkops Estuary in consecutive months, twice per season for a period of one year, spanning a total of eight sampling trips between March 2013 and January 2014. Fishes were collected in four habitat types, and each habitat type was sampled in two separate locations in the lower estuary. Each sampling trip was conducted on an incoming tide during the day. Fishes were sampled using a 30×1.5 m seine net (mesh size=10 mm) at eight sites accessed by boat in the lower 3 km of the estuary. Two replicate sites were selected to represent four predetermined habitat types: sand flats (S), mud flats (M), vegetated areas (V) and shallow estuarine creeks (C) (Fig. 1). The sand and mud habitat types were selected based on a consistent substrate of either sand or mud, respectively, with no vegetation cover. Estuarine creek habitats were characterized by shallow, unvegetated drainage channels that were permanently supratidal and surrounded by an adjacent Sarcocornia spp. saltmarsh with a muddy substrate. The creek habitats differed from the mud habitats as they were not situated in the main channel but maintained tidal connectivity with the main channel. Vegetated habitats were selected in areas where there was consistent and dense coverage of submerged Zostera capensis and/or Spartina maritima ranging in cover from 90% to 100%. It was impossible to separate Spartina maritima and Zostera capensis vegetation as they co-occurred along the margins. Sampling of vegetated areas involved dragging a seine net directly through the vegetated areas. Sites were selected to ensure no overlap in habitat types and habitats were replicated to ensure that species occurrence patterns were persistent with habitat type, if applicable, and were treated as separate samples for analyses. Water sampling depth for fishes and physico-chemical variables at each site did not exceed 1.2 m on all sampling occasions. On each sampling occasion, temperature (°C), total dissolved solids (TDS), salinity, pH, turbidity (NTU) and conductivity (µS/cm) were measured at each site 20 cm below the water surface using a YSI multi-parameter meter (660 V).

A single seine net haul was conducted at each site on each occasion. The seine net was manually operated by two to four people in a semi-circle over the selected habitat area and pulled perpendicular to the shoreline. Each fish was identified to the lowest possible taxon (Van der Elst and Wallace 1976Van der Elst R., Wallace J. 1976. Identification of the juvenile mullet of the east coast of South Africa. J. Fish. Biol. 9: 371-374., Smith and Heemstra 1995Smith M.M., Heemstra P.C. 1995. Smiths’ Sea Fishes. Macmillan, Johannesburg. 1047 pp.) and was measured to the nearest 1.0 mm total length (TL) in the field. All catches were expressed as catch per unit effort (CPUE) referring to the number of fishes per seine haul. All fish were released except for individuals that could not be positively identified. These were fixed in 10% formalin for later laboratory identification and measurement. All positively identified fishes were categorized into estuary association categories based on guild according to Potter et al. (2015)Potter I.C., Tweedley J.R., Elliott M., et al. 2015. The ways in which fish use estuaries: a refinement and expansion of the guild approach. Fish. Fish. 16: 230-239.EF. The categories applicable to this study include, in the marine category, the marine straggler group, the marine estuarine-opportunist group and the marine estuarine-dependent group. Within the estuarine category, the relevant groups include the solely estuarine group, the estuarine and marine group and the estuarine migrant group. Finally, catadromous species and freshwater estuarine-opportunist species also feature (Potter et al. 2015Potter I.C., Tweedley J.R., Elliott M., et al. 2015. The ways in which fish use estuaries: a refinement and expansion of the guild approach. Fish. Fish. 16: 230-239.).

Statistical analyses

Descriptive and inferential statistics for both the physico-chemical and biological data were generated using the Statistica software package version 11, 2012. Data were assessed for normality using a visual normal probability plot and the Shapiro-Wilk test and homogeneity of variance was tested using Levene’s test following square root and log transformations. All biological and physico-chemical data did not conform to parametric assumptions and therefore only non-parametric tests were used. Multivariate and diversity analyses were done using the Primer statistical package version 6.1 (2001) (Clarke and Gorley 2001Clarke K., Gorley R. 2001. PRIMER v6. PRIMER-E Ltd. Plymouth, UK.).

Spatial and seasonal variability in temperature (°C), TDS, salinity, pH, turbidity (NTU) and conductivity (µS/cm) were assessed using a Kruskal-Wallis test by rank. A Kruskal-Wallis test was also used to test for differences in fish abundance among habitats and seasons. Species included in these analyses (dominant species) were identified as those that showed a total catch of more than 40 individuals throughout the study period in order to allow for a large enough sample size. Species showing significant habitat partitioning were explored for relationships with environmental variables also showing a significant difference between habitats using multiple linear regression. Shannon-Wiener diversity indices (H’) were compared among habitats and seasons using a non-parametric Kruskal-Wallis test.

For community analysis, abundance data were transformed by log(x+1) and grouped by both habitat type and season for the multivariate analyses. This transformation was used to reduce the contribution of highly abundant species. Abundance data were grouped into a similarity matrix using the Bray-Curtis similarity measure. A 3-D non-metric multidimensional scaling (nMDS) plot of abundance in each habitat type was generated. Species that were not frequently caught during the study period (caught on less than three occasions) and sites that showed zero catch during the study period were excluded from the nMDS so that clear community trends could be observed. A two-way crossed ANOSIM analysis was conducted to assess habitat and seasonal similarities in community composition and a two-way crossed SIMPER analysis by Bray-Curtis similarity was used to assess individual species contributions to the similarity attributes among these groups.

RESULTSTop

Environmental variability

Of the six physico-chemical parameters measured during the study, TDS (H=14.89; n=64; P<0.01), salinity (H=14.91; n=64; P<0.01) and conductivity (H=14.40; n=64; P<0.01) showed a significant difference between the four habitat types (df=3). Temperature, turbidity and pH showed no significant variation between habitats, but temperature and pH varied significantly between seasons (temperature H=42.64, n=64, P<0.01; pH H=49.38, n=64, P<0.01; df=3). As expected, the highest water temperatures occurred in summer (mean=25.32°C) and the lowest in winter (mean=14.34°C), with spring (mean=19.05°C) and autumn (mean=20.67°C) showing moderate temperatures. The ranges of environmental variables recorded in each habitat are shown in Table 1. During the summer sampling period, the highest temperatures were recorded in the shallow creek sites, but vegetated sites showed the highest temperatures in winter and spring. The lowest temperatures were generally recorded at the sand sites (Table 1). The range of temperatures recorded was fairly consistent among the different habitat types. TDS was variable among the different habitat types but consistent throughout the seasons and also showed a large range of values within specific habitat types, exceeding 20 TDS units in some cases, particularly in the creek habitats (Table 1). The highest salinity and conductivity values recorded were in the vegetated habitats, which maintained stable salinities throughout the seasons. The most variable salinities were recorded in the creek and sand habitats (Table 1). pH was fairly stable throughout the different habitat types (range not exceeding 1.0 unit), but changes >1 unit were observed between seasons, with the lowest average pH in the system recorded in spring and summer and the highest pH in the colder seasons (Table 1). Turbidity was highly variable throughout the habitat types and seasons but this variability was not significant.

Habitat occurrence

Species composition

A total of 11537 fishes were sampled belonging to 18 families and 35 species (Table 2). The dominant species caught were the solely estuarine Gilchristella aestuaria and estuarine and marine Atherina breviceps, which contributed 27.10% and 25.80%, respectively, to the total catch. The marine estuarine-dependent sparid, Rhabdosargus holubi, was the third most abundant species, contributing 11.50% to the total catch. Other families that contributed notably to the catch were the Mugilidae and Gobiidae, while all the remaining families contributed less (<1%) to the total catch. In terms of estuarine dependence, solely estuarine and estuarine and marine species dominated the catches, comprising 64.18%, followed by the marine estuarine-dependent species with 23.14%. Mugilidae individuals <30 mm TL, which could not be identified, contributed 6.70% of the total catch and probably belonged to the marine estuarine-opportunist category, as is typical for the most commonly occurring Mugilidae in warm temperate South African estuaries.

Temporal trends

Five of the dominant species showed a significant difference in catch among seasons (df=3) (Fig. 2). These were all marine species including Diplodus capensis (H=17.68; n=13; P<0.01), Liza dumerili (H=14.73; n=17; P<0.01), L. macrolepis (H=11.03; n=12; P<0.01), R. globiceps (H=20.51; n=16; P<0.01) and R. holubi (H=14.93; n=35; P<0.01). The highest catches were in winter (CPUE=280.62) and autumn (CPUE=218.38), followed by summer (CPUE=176.12) and spring (CPUE=45.81). The unusually high catches in winter were attributed exclusively to large catches of the solely estuarine and estuarine and marine G. aestuaria and A. breviceps, respectively. When these two species were excluded from the analyses, the winter season showed the lowest fish abundance. The largest contribution of marine species to total catch occurred in autumn and spring, whereas the estuarine species showed greater variability in abundance throughout the year (Fig. 2).

Diversity peaked in autumn (H’=1.17) and summer (H’=1.11), with lower diversity occurring in spring (H’=0.98) and winter (H’=0.96), but diversity did not vary significantly between seasons (P>0.05).

TLs of dominant species caught were compared between seasons. Seasonal variation in TL occurred in estuarine resident species, namely A. breviceps (H=44.48; n=313; P<0.01), Glossogobius callidus (H=14.88; n=357; P<0.01), Caffrogobius nudiceps (H=47.97; n=326; P<0.01), G. aestuaria (H=180.11; n=670; P<0.01), Psammogobius knysnaensis (H=24.78; n=321; P<0.01), and in marine estuarine migrant species, namely Heteromycteris capensis (H=45.84; n=131; P<0.01), Myxus capensis (H=38.30; n=258; P<0.01), R. holubi (H=33.06; n=721; P<0.01) and Solea turbynei (H=8.36; n=32; P< 0.05).

Spatial trends

The abundance of fishes was compared between four habitat types at the species level and 8 of the 15 dominant species showed a significant difference in abundance between the four habitat types. These included the solely estuarine Gilchristella aestuaria (H=9.54; n=64; P<0.05), three estuarine and marine species, Caffrogobius gilchristi (H=20.36; n=64; P<0.01), Caffrogobius nudiceps (H=15.98, n=64, P<0.01) and Glossogobius callidus (H=10.38, n=64, P<0.01), two marine estuarine opportunists, Diplodus capensis (H=11.64; n=13; P<0.01) and Heteromycteris capensis (H=21.73; n=21; P<0.01), the marine estuarine-dependent Rhabdosargus holubi (H=19.13; n=35; P<0.01) and finally the catadromous Myxus capensis (H=10.66; n=29; P<0.01).

Of these species, the commonly estuarine families, including the Gobiidae (>50.00%) and the Clupeidae (G. aestuaria) (78.00%), showed the highest proportions of catches in the creek sites, whereas the Sparidae (D. capensis) (83.00%) showed the highest proportion of catches in the vegetated sites (Fig. 3). Although the highest proportion of R. holubi was caught in the creek habitat (45.00%), the vegetated habitat also yielded a large proportion of the total catch (31.00%) of this species (Fig. 3). Overall, CPUE (including all species) was highest in the creek sites (CPUE=331.38) followed by the sand sites (CPUE=144.56) with the lowest CPUE occurring in the vegetated (CPUE=139.31) and mud sites (CPUE=105.94). However, the largest contributor to catch in the sand sites, A. breviceps, was caught in high numbers on a single sampling occasion. If this species is excluded from calculations, the average CPUE for sand habitats is reduced (CPUE=45.88), making it the site with the lowest CPUE. Despite differences in species catch among habitats and the variability of salinity, TDS and conductivity between habitats, no significant relationships were observed between partitioning species and the environmental variables measured in these habitats in the lower estuary.

Species diversity (H’) was highest in the mud (H’=1.24) and vegetated (H’=1.02) habitats, followed by the sand (H’=0.79) and creek (H’=0.44) habitats. These differences were, however, not significantly different among the four habitat types (P>0.05).

Of the dominant species caught, A. breviceps (H=42.91; n=313; P<0.01), C. gilchristi (H=11.22; n=357, P<0.01), C. nudiceps (H=20.68; n=326, P<0.01), G. aestuaria (H=182.02; n=670; P<0.01), Heteromycteris capensis (H=10.06; n=131; P<0.05), L. dumerilli (H=32.40; n=88; P<0.01), M. capensis (H=9.75; n=258; P<0.01), P. knysnaensis (H=10.41; n=321; P<0.01), R. globiceps (H=57.87; n=317; P<0.01) and R. holubi (H=76.76 n=721; P<0.01) showed a significant difference in TL among the four habitat types. The largest R. holubi (mean TL=50.08) and L. dumerilli (mean TL=191.37) individuals were caught in the vegetated habitats and the smallest in the sand habitats (mean TL=26.00 and 30.77, respectively), whereas R. globiceps were largest in the creek habitats and smallest in the mud habitats (mean TL=43.39 and 32.83, respectively) (Table 2). Diplodus capensis, G. callidus, L. macrolepis and S. turbynei were dominant species in the community in the lower reaches and showed no significant differences in TL between the four habitat types sampled.

Fish community trends

A two-way crossed ANOSIM also revealed a significant difference between seasonal groups (Global R=0.21; significance level (SL)=0.10%, averaged across habitat). Pairwise tests showed that the seasons that differed significantly included autumn and spring (R statistic=0.26; SL=1.60%), autumn and summer (R statistic=0.28; SL=0.70%), winter and summer (R statistic=0.36; SL=0.10%) and spring and summer (R statistic=0.31; SL=0.20%) combinations. Comparisons between autumn and winter and winter and spring showed no significant differences. SIMPER analysis showed that the summer season differed significantly from the other seasons due to high catches of the marine estuarine-dependent Sparidae Rhabdosargus holubi (26.66%) and marine estuarine opportunists Diplodus capensis (21.87%) and Rhabdosargus globiceps (15.46%) (Table 3). The winter and spring seasons were characterized by higher catches of estuarine resident Gobiidae species compared with other seasons (Table 3).

A two-way crossed ANOSIM revealed that there was a significant difference between habitat groups (Global R=0.27; significance=0.10%, averaged across season). Pairwise tests comparing habitats showed that the habitats that differed the most were the creek and sand habitats (R statistic=0.39; SL=0.10%), the sand and vegetated habitats (R statistic=0.53; SL=0.10%) and the mud and vegetated habitats (R statistic=0.27; SL=0.40%). The comparison of creek and mud habitats as well as mud and sand habitats showed no significant differences. Abundance data in a 3-D nMDS analysis showed a distinct grouping of sites by habitat based on similarities in species abundance (Fig. 4). Although habitat groupings based on dissimilarity are not distinct, there is subtle grouping of sand, creek and vegetated habitats with mud habitats tending to fall in between these groups.

SIMPER analysis of habitat types showed that sand habitats were characterized by sand-associated species such as Psammogobius knysnaensis (37.41%) and Heteromycteris capensis (31.34%), whereas these species did not contribute significantly to catches in the other habitats (Table 3). The mud habitats showed high catches of the estuarine resident Gobiidae as well as Rhabdosargus holubi (23.71%) (Table 3). However, the highest catches of marine Sparidae were in the vegetated habitats separating this habitat type from the others in terms of species catch composition (Table 3). The creek habitats differed from other habitats in the high abundance of the estuarine species Gilchristella aestuaria (18.90%), in addition to the moderate abundance of some marine Sparidae (Table 3). Other predatory piscivorous fishes were found only in the creek habitats in low numbers.

DISCUSSIONTop

Distinct species suites were recognized across all four habitat types typifying the lower reaches nursery area within the Swartkops Estuary. The importance of submerged aquatic vegetation for young fishes in the Swartkops Estuary supports previous findings on habitat use at the species level within eelgrass beds (Orth et al. 1984Orth R.J., Heck K.L., van Montfrans J. 1984. Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7: 339-350., Sheppard et al. 2011Sheppard J.N., James N.C., Whitfield A.K., et al. 2011. What role do beds of submerged macrophytes play in structuring estuarine fish assemblages? Lessons from a warm-temperate South African estuary. Estuar. Coast. Shelf Sci. 95: 145-155.) in studies comparing seagrasses and adjacent unvegetated areas (Beckley 1983Beckley L.E. 1983. The ichthyofauna associated with Zostera capensis (Setchell) in the Swartkops estuary, South Africa. S. Afri. J. Zool. 18: 15-24., Connolly 1994Connolly R. 1994. A comparison of fish assemblages from seagrass and unvegetated areas of a southern Australian estuary. Mar. Freshwater. Res. 45: 1033-1044., Jenkins and Wheatley 1998Jenkins G.P., Wheatley M.J. 1998. The influence of habitat structure on nearshore fish assemblages in a southern Australian embayment: Comparison of shallow seagrass, reef-algal and unvegetated sand habitats, with emphasis on their importance to recruitment. J. Exp. Mar. Biol. Ecol. 221: 147-172.) as well as in studies comparing multiple habitat types in nursery areas (Sogard and Able 1991Sogard S.M., Able K.W. 1991. A comparison of eelgrass, sea lettuce, macroalgae and marsh creeks as habitats for epibenthic fishes and decapods. Estuar. Coast. Shelf Sci. 33: 501-519., Guidetti 2000Guidetti P. 2000. Differences among fish assemblages associated with nearshore Posidonia oceanica seagrass beds, rocky–algal reefs and unvegetated sand habitats in the Adriatic Sea. Estuar. Coast. Shelf Sci. 50: 515-529., França et al. 2009França S., Costa M.J., Cabral H.N. 2009. Assessing habitat specific fish assemblages in estuaries along the Portuguese coast. Estuar. Coast. Shelf Sci. 83: 1-12.). However, in the present study, shallow-water creeks yielded the highest catches, supporting findings in a Northern Hemisphere study (Sogard and Able 1991Sogard S.M., Able K.W. 1991. A comparison of eelgrass, sea lettuce, macroalgae and marsh creeks as habitats for epibenthic fishes and decapods. Estuar. Coast. Shelf Sci. 33: 501-519.) and contrary to findings in the Kariega Estuary situated 130 km to the east of the study system (Paterson and Whitfield 2000Paterson A., Whitfield A.K. 2000. Do shallow-water habitats function as refugia for juvenile fishes? Estuar. Coast. Shelf Sci. 51: 359-364.), where vegetated areas showed higher fish abundance and more selective species occurrence among habitats.

Use of vegetated habitats by fish has been attributed to a number of driving forces, including the protective function as a result of structural complexity as well as their provision of food for growing larvae and juveniles (Orth et al. 1984Orth R.J., Heck K.L., van Montfrans J. 1984. Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7: 339-350., Paterson and Whitfield 2000Paterson A., Whitfield A.K. 2000. Do shallow-water habitats function as refugia for juvenile fishes? Estuar. Coast. Shelf Sci. 51: 359-364., Nanjo et al. 2014Nanjo K., Kohno H., Nakamura Y., et al. 2014. Differences in fish assemblage structure between vegetated and unvegetated microhabitats in relation to food abundance patterns in a mangrove creek. Fisher. Sci. 80: 21-41.). This would suggest that the more structurally complex vegetated areas should support more fishes, but in this study shallow, warm creeks were also important use area for numerous species. All habitats sampled showed unique species suites as well as a level of plasticity within species in terms of occurrence across habitats. Use of habitats was also found to vary seasonally within the estuary, coinciding with peak juvenile fish recruitment into estuaries during warmer spring and summer months.

Temporal trends

Seasonal use of temperate estuaries where abundance of juveniles increases in spring and peaks in summer, with numbers declining in autumn, after which abundance and diversity declines markedly as the water temperature cools, is a worldwide phenomenon coupled to recruitment from the ocean and productivity maxima within the estuary, typically linked to rainfall patterns and therefore food availability (Whitfield 1999Whitfield A.K. 1999. Ichthyofaunal assemblages in estuaries: a South African case study. Rev. Fish. Biol. Fisher. 9: 151-186., Ramos et al. 2006Ramos S., Cowen R.K., Ré P., et al. 2006. Temporal and spatial distributions of larval fish assemblages in the Lima estuary (Portugal). Estuar. Coast. Shelf Sci. 66: 303-314., Strydom 2015Strydom N.A. 2015. Patterns in Larval Fish Diversity, Abundance, and Distribution in Temperate South African Estuaries. Estuar. Coast. 38: 268-284.). This phenomenon was particularly evident for juveniles of marine spawned Mugilidae, Soleidae and Sparidae utilizing the estuary as a nursery. Schooling adults of resident pelagic Atherinidae and Clupeidae species within the estuary, however, compounded catches in the winter months in the Swartkops. Atherina breviceps breeds in spring and summer in the estuary and juveniles can be found in high abundances in autumn and winter (Neira et al. 1988Neira F., Beckley L.E., Whitfield A. 1988. Larval development of the Cape silverside, Atherina breviceps Cuv. and Val., 1835 (Teleostei, Atherinidae) from southern Africa. S. Afr. J. Zool. 23: 176-183., Whitfield 1998Whitfield A.K. 1998. Biology and ecology of fishes in southern African estuaries. Ichthyological Monographs of the J.L.B Smith Institute of Ichthyology, No 2. 223 pp.). Using the guild approach as described by Potter el al. (2015)Potter I.C., Tweedley J.R., Elliott M., et al. 2015. The ways in which fish use estuaries: a refinement and expansion of the guild approach. Fish. Fish. 16: 230-239. to categorize fish prior to analysis allows better elucidation of use patterns without the compounding effects of resident species on seasonal catches of marine recruits.

Spatial trends

There was clear evidence of partitioning among juvenile fishes within the four habitat types common to the lower reaches of the Swartkops Estuary. Eight species showed significantly higher abundance in particular types of habitat and included species of both estuarine and marine origin. The highest catches throughout the study period occurred at shallow creek sites, as is supported by habitat use observations in an Atlantic estuary (Sogard and Able 1991Sogard S.M., Able K.W. 1991. A comparison of eelgrass, sea lettuce, macroalgae and marsh creeks as habitats for epibenthic fishes and decapods. Estuar. Coast. Shelf Sci. 33: 501-519.) but has not yet been described locally. The shoaling estuarine resident Gilchristella aestuaria often occurred in high numbers in creeks. It has been suggested that species also select habitats based on the degree of protection afforded by either the habitat directly (vegetation) or the behaviour of the species to avoid predation (Weinstein and Brooks 1983Weinstein M.P., Brooks H.A. 1983. Comparative ecology of nekton residing in a tidal creek and adjacent seagrass meadow: community composition and structure. Mar. Ecol. Prog. Ser. 12: 15-27., Orth et al. 1984Orth R.J., Heck K.L., van Montfrans J. 1984. Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7: 339-350.). In the case of resident G. aestuaria, this species is able to limit predation by shoaling in shallow creeks (Paterson and Whitfield 2000Paterson A., Whitfield A.K. 2000. Do shallow-water habitats function as refugia for juvenile fishes? Estuar. Coast. Shelf Sci. 51: 359-364.). However, creeks were also important areas for other species, evidenced by the high species diversity and the larger size range within species in creek habitats, particularly in the resident Gobiidae and the marine estuarine-dependent Sparidae and Mugilidae. The mixed community within creeks is contrary to findings by Paterson and Whitfield (2000)Paterson A., Whitfield A.K. 2000. Do shallow-water habitats function as refugia for juvenile fishes? Estuar. Coast. Shelf Sci. 51: 359-364., who found saltmarsh creeks dominated by taxa mainly of marine origin as well as to findings by Sogard and Able (1991)Sogard S.M., Able K.W. 1991. A comparison of eelgrass, sea lettuce, macroalgae and marsh creeks as habitats for epibenthic fishes and decapods. Estuar. Coast. Shelf Sci. 33: 501-519. and Weinstein and Brooks (1983)Weinstein M.P., Brooks H.A. 1983. Comparative ecology of nekton residing in a tidal creek and adjacent seagrass meadow: community composition and structure. Mar. Ecol. Prog. Ser. 12: 15-27., who both found that although density of fish in creeks was high, catches were dominated by only a few species and that these habitats showed a lower diversity of species when compared with vegetated sites.

Zostera capensis and Spartina maritima rich vegetated habitats also supported high abundances of juveniles, although the abundance was species-specific. All estuary guilds (Potter et al. 2015Potter I.C., Tweedley J.R., Elliott M., et al. 2015. The ways in which fish use estuaries: a refinement and expansion of the guild approach. Fish. Fish. 16: 230-239.) were recorded in vegetated areas, and these habitats appear to be very important for juvenile marine species, especially the marine estuarine-dependent sparid Rhabdosargus holubi and the marine estuarine opportunist Diplodus capensis, a finding also supported by Paterson and Whitfield (2000)Paterson A., Whitfield A.K. 2000. Do shallow-water habitats function as refugia for juvenile fishes? Estuar. Coast. Shelf Sci. 51: 359-364. in the nearby Kariega Estuary. Aside from the solely estuarine resident species, these Sparidae contributed the most to catches in these areas containing submerged vegetation, which was also reported by Beckley (1983)Beckley L.E. 1983. The ichthyofauna associated with Zostera capensis (Setchell) in the Swartkops estuary, South Africa. S. Afri. J. Zool. 18: 15-24.. However, vegetated habitats are seemingly less important for other marine estuarine opportunist species such as the sparid Rhabdosargus globiceps, which tends to occur more often in creek habitats.

Mud habitats also showed a higher diversity of juvenile fish species. In contrast to creek and vegetated habitats, sand habitats appeared to support the lowest abundance (excluding the large catch of shoaling marine and estuarine Atherina breviceps on a single occasion) and diversity of species. Sand habitats are the most uniform in terms of complexity and typically only support specialist sand species, namely the sand goby Psammogobius knysnaensis and the Soleidae. Based on these characteristics, vegetated and mud habitats tend to fall in between these extremes. This was evident in the study by Hanekom and Baird (1984)Hanekom N., Baird D. 1984. Fish community structures in Zostera and non-Zostera regions of the Kromme Estuary, St Francis Bay. S. Afr. J. Zool. 19: 295-301. in the Kromme Estuary, in which they compared Zostera beds with adjacent non-Zostera areas of muddy substrate. They found no significant differences in fish community. These habitats often share species composition and it could be that fish move between the two for feeding and refuge. Diet studies on species utilizing both habitat types will provide much insight into microhabitat use and habitat partitioning.

Habitat partitioning with ontogeny showed that species use of habitats varied depending on their estuary association category. The solely estuarine and estuarine migrants, such as the Gobiidae, Atherinidae (namely A. breviceps) and Clupeidae (namely G. aestuaria), were frequently sampled in all habitats in both juvenile and adult stages, suggesting less segregation based on size. Mugilidae, many of which are dependent on estuaries as juveniles, were also commonly caught in all habitats in sizes ranging from recently transformed juveniles to older juvenile stages, with some adults also recorded in catches.

In contrast, the marine estuarine-opportunist and dependent Sparidae species occurred mostly as small juveniles: no adults were caught (>190 mm TL) across habitats and larger specimens were mostly associated with vegetated and creek habitats. The average size of D. capensis is less than the average size of R. holubi and R. globiceps. This suggests that the marine estuarine-opportunist D. capensis may utilize estuarine nurseries for a shorter period of time during their juvenile phase when compared with the other two estuarine-dependent sparid species co-occurring in the nursery area due to their reliance on estuaries. This probably also contributes to the success of sharing habitats as diet and gape size will vary. Diplodus capensis is not wholly dependent on estuaries, often moving into tide pools and gullies in the ocean at larger sizes (Strydom et al. 2014Strydom N.A., Booth A.J., McLachlan A. 2014. Occurrence of larval fishes in a rocky shore-associated nursery area in temperate South Africa, with emphasis on temperature-related growth in dominant Sparidae. Afr. J. Mar. Sci. 36: 125-135.), whereas R. holubi has a fully dependent estuarine phase in its early life history. Sparidae typically also show ontogenetic shifts in habitat that are critical to survival as these species recruit into estuaries as postflexion larvae (Strydom 2015Strydom N.A. 2015. Patterns in Larval Fish Diversity, Abundance, and Distribution in Temperate South African Estuaries. Estuar. Coast. 38: 268-284.). Smaller-sized individuals were recorded in the open water areas at sand and mud sites. Strydom (2003)Strydom N.A. 2003. An Assessment of Habitat Use by Larval Fishes in a Warm Temperate Estuarine Creek Using Light Traps. Estuaries. 26: 1310-1318. proposed that the high numbers of recruiting postflexion Sparidae in open water areas as opposed to Zostera beds was a predation avoidance mechanism as transparent larvae are less visible in open water than against the darker background of the Zostera beds, which are already rich with juvenile predators. Upon completion of settlement, the Sparidae move into vegetated and creek habitats, where they occur mostly as larger juveniles, as was observed in this study. Open shallow water over sand and muddy substrata therefore becomes a transient habitat during ontogeny for marine species recruiting as larvae into estuaries (Strydom 2003Strydom N.A. 2003. An Assessment of Habitat Use by Larval Fishes in a Warm Temperate Estuarine Creek Using Light Traps. Estuaries. 26: 1310-1318.), after which they filter into vegetated or creek areas as juveniles, thereby utilizing multiple habitats throughout their early development following an ocean-estuarine habitat continuum (Able 2005Able K.W. 2005. A re-examination of fish estuarine dependence: evidence for connectivity between estuarine and ocean habitats. Estuar. Coast. Shelf Sci. 64: 5-17., Baillie et al. 2015Baillie C.J., Fear J.M., Fodrie F.J. 2015. Ecotone effects on seagrass and saltmarsh habitat use by juvenile nekton in a temperate estuary. Estuaries Coasts. 38: 1414-1430., Strydom 2015Strydom N.A. 2015. Patterns in Larval Fish Diversity, Abundance, and Distribution in Temperate South African Estuaries. Estuar. Coast. 38: 268-284.).

Drivers of spatial and temporal trends

Surprisingly, temperature was not found to be an important driver of habitat use. This is likely because all habitats were shallow and located in the lower reaches of the estuary, so they were subject to similar tidal and solar radiation effects and therefore had similar temperatures. Despite there being no significant difference in temperature among habitat types, the highest temperatures were recorded in creek and vegetated habitats, which also yielded the highest catches. As the Sparidae contributed substantially to catches in these two habitats, it is likely that this is a reflection of the temperature sensitivity in growth for these species (Strydom et al. 2014Strydom N.A., Booth A.J., McLachlan A. 2014. Occurrence of larval fishes in a rocky shore-associated nursery area in temperate South Africa, with emphasis on temperature-related growth in dominant Sparidae. Afr. J. Mar. Sci. 36: 125-135.) and these species also select these habitats based on subtly higher temperatures. The value of generally warmer estuarine nursery areas compared with the neighbouring ocean must be emphasized in species with temperature-dependent growth. These conditions are generally more suitable for the faster growth of larvae and juveniles using shallow-water nurseries such as estuaries and shallow embayments, thereby enhancing chances of survival (Strydom et al 2014Strydom N.A., Booth A.J., McLachlan A. 2014. Occurrence of larval fishes in a rocky shore-associated nursery area in temperate South Africa, with emphasis on temperature-related growth in dominant Sparidae. Afr. J. Mar. Sci. 36: 125-135., Baillie et al. 2015Baillie C.J., Fear J.M., Fodrie F.J. 2015. Ecotone effects on seagrass and saltmarsh habitat use by juvenile nekton in a temperate estuary. Estuaries Coasts. 38: 1414-1430.). Temperature most probably plays a more significant seasonal role rather than being a contributor to habitat occurrence on a fine scale, as in this study, which focuses on the lower estuary within the nursery area. Higher turbidity in creek sites, subject to tidal drainage of the salt marsh, may also provide additional protective isolation for young fishes from visual predators, lending to the value of creeks along with vegetated areas for refuge, but this value is not statistically measureable on such fine scales. Since environmental variables such as salinity, conductivity and TDS, which were significantly different among habitats, also showed no clear trends in structuring fishes in these areas, it is highly likely that other factors such as behaviour, linked to predator avoidance and coupled with feeding, are significant drivers of use in these habitats. Behaviour and feeding need to be considered in future studies focussed on fine-scale habitat partitioning.

CONCLUSIONTop

Although vegetated habitats have received worldwide attention and therefore show value in terms of their nursery role in estuaries, this work provides evidence for the importance of multiple habitat types among and within species and with ontogeny in temperate estuarine nurseries. Coupled with vegetated areas, shallow-water estuarine creeks also play an important role in the nursery function of estuaries in temperate South Africa given the high density of juvenile fishes concentrating in these areas. The value of an estuarine nursery is therefore likely to increase with increased submerged aquatic vegetation and shallow-water creek availability, essentially increasing refuge opportunities, assuming food availability is optimal. Large-scale and small scale environmental variability in estuaries probably shift in priority on a temporal and spatial scale in nursery areas. Temperature and olfactory cues provide the critical drivers of recruitment of larvae and juveniles into estuaries but upon arrival, a suite of factors probably underpin the success of the nursery, including habitat availability, physico-chemical factors, food availability and fish behaviour relative to competitors and predators. The ubiquity of various sizes across the four habitats in certain fish groups suggests greater habitat plasticity than was previously thought. This is seen in both resident and marine migrant fishes and therefore less partitioning exists among species than was previously hypothesized. This explains the conflicting findings of habitat use in previous studies, especially those using vegetated areas as a variable. Many studies have failed to identify plasticity in habitat use (Sogard and Able 1991Sogard S.M., Able K.W. 1991. A comparison of eelgrass, sea lettuce, macroalgae and marsh creeks as habitats for epibenthic fishes and decapods. Estuar. Coast. Shelf Sci. 33: 501-519., this study) because, most often, only two habitat types were compared at a time and with little separation of fishes into guilds prior to analysis to remove confounding effects from different use groups. Multiple habitat comparisons are required in future studies coupled with diet and ontogenetic shifts to fully understand how and whether nursery habitat use is as plastic as it appears to be among some species, particular estuary specialists. The subject is bound to remain complex and multidimensional as species may be partitioning habitats on finer scales than those currently being measured and these are as yet unexplored. Resilience appears to be a hallmark characteristic of fishes regularly using estuaries as nursery areas and success may well be embedded in behavioural and feeding plasticity rather than specialization.

ACKNOWLEDGEMENTSTop

Gratitude is expressed to the National Research Foundation for financial and bursary support (Grant number 79733, held by N.A. Strydom). Thank you to the many field and laboratory assistants for their invaluable support and input, especially C. Muller and P. Pattrick. Handling of fishes conformed to approval by the Ethics Committee of the Nelson Mandela Metropolitan University.

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