Patterns of seagrass macrobenthic biodiversity in the warm-temperate Knysna estuarine bay, Western Cape: a review

R. S. K. Barnes

doi:10.1007/s10452-021-09848-3

Patterns of seagrass macrobenthic biodiversity in the warm-temperate Knysna estuarine bay, Western Cape: a review

Barnes, R. S. K. 2021-03-11 00:00:00 Aquat Ecol (2021) 55:327–345 https://doi.org/10.1007/s10452-021-09848-3(0123456789().,-volV)(0123456789().,-volV) Patterns of seagrass macrobenthic biodiversity in the warm- temperate Knysna estuarine bay, Western Cape: a review R. S. K. Barnes Received: 3 December 2020 / Accepted: 24 February 2021 / Published online: 11 March 2021 The Author(s) 2021 Abstract Knysna estuarine bay in South Africa’s constant; further, one-third of species occur through- Garden Route National Park is that country’s most out. Intertidally, all but peripheral compartments are signiﬁcant estuarine system for biodiversity and low density and infaunally dominated, while some conservation value. One outstanding feature is support peripheral areas, and much of the subtidal, are higher of 40% of South Africa’s—and maybe 20% of the density and epifaunally dominated. Overall, seagrass world’s—remaining vulnerable and decreasing dwarf- macrobenthos appears maintained below carrying eelgrass, Zostera capensis, whose associated benthic capacity (e.g., by abundant juvenile ﬁsh) and of macrofauna has been studied since 2009. For these random species composition within a site. Two further invertebrates, Knysna comprises several signiﬁcantly characteristics are notable: Unusually, seagrass sup- different compartments: sandy mouth; well-ﬂushed ports fewer animals than adjacent unvegetated areas, marine embayment; poorly ﬂushed central sea-water probably because of lack of bioturbatory disturbance ’lagoon’; and two disjunct but faunistically similar in them, and the vegetation cover may ameliorate peripheral regions–marine backwater channels, and ambient habitat conditions. Unfortunately, continual low-salinity upper estuary. Although macrofauna heavy and effectively unpreventable exploitation for ranges from dilute brackish to fully marine, its bait occurs, and chlorophyte blooms have developed abundance, local patchiness, and over considerable because of high nutrient input. Knysna presents a stretches, species density remains remarkably microcosm of problems facing biodiverse and high- value habitats set within areas of high unemployment where subsistence ﬁshing provides the main source of Handling Editor: Te ´lesphore Sime-Ngando protein and seagrass provides the only source of bait. R. S. K. Barnes (&) Keywords Biodiversity Conservation Intertidal Department of Zoology and Entomology, Rhodes University, Eastern Cape, Makhanda 6140, Republic of Knysna Macrobenthos Seagrass South Africa e-mail: rsb1001@cam.ac.uk R. S. K. Barnes Knysna Basin Project Laboratory, Western Cape, Introduction Knysna 6571, Republic of South Africa The permanently open Knysna estuarine bay (34803 S, R. S. K. Barnes 23803 E) is a drowned river valley in South Africa’s Department of Zoology and Conservation Research Institute, University of Cambridge, Cambridge, UK 123 328 Aquat Ecol (2021) 55:327–345 Western Cape separated from the adjacent Indian (Hippocampus capensis), and it is one of the only two Ocean by a narrow gorge (300 m wide, 700 m long, localities that support the critically endangered sea- and 4 m deep at low tide) carved through the coastal grass false-limpet (Siphonaria compressa) and a quartzite ridge by the Knysna River during times of seagrass population of the dwarf cushion-star Parvu- lower sea level. The bay forms part of the open-access lastra exigua. Except in the immediate vicinity of the Garden Route National Park, and on a basket of mouth, Z. capensis, together with some mixed criteria, including its size, diversity of habitat, zonal Halophila ovalis, occurs virtually throughout the rarity, and biodiversity, is ranked South Africa’s most intertidal zone of the system as one continuous bed signiﬁcant estuarine system in terms of conservation (Maree 2000), and it also occurs subtidally though importance (Turpie and Clark 2007; van Niekerk et al. more patchily (Wasserman et al. 2020; Barnes and 2019). Known locally as the Knysna Lagoon, the Claassens 2020). Such meadows support well-devel- system has an area of some 10 km at low tide and 16 oped invertebrate macrofaunas that serve the vital km at high tide and receives the inﬂow of the Knysna functions of consuming epiphytic algal growths and River at its head and a large number of smaller streams providing the trophic link between microphytobenthic along its northern and eastern shores. Nevertheless, it production and that of the larger, more mobile nekton is marine-dominated, consequent on low average rates (Murphy et al. 2021). This article synthesizes the main of freshwater inﬂow and a very large tidal prism, ﬁndings of the disparate series of researches conducted 6 3 during spring tides equaling 19 9 10 m [the largest on these invertebrate faunal assemblages at Knysna of any South African estuary (Grindley 1985)], since 2009, re-analyzing the original data where causing semi-diurnal ﬂushing of its main channel. appropriate, with particular emphasis on patterns of The estuarine bay can be divided hydrologically into macrofaunal assemblage composition, abundance, three linear compartments, which vary in areal extent species richness, and patchiness along the bay’s main and precise geographical position with the tidal cycle axial transitional gradient, as well as along the and magnitude of river ﬂow: An outer marine bay gradient of shelter, located perpendicular to that axis tidally ﬂushed with cool water from the Indian Ocean across its eastern section. and with salinities usually [ 34; a middle, more isolated lagoonal water body also of high salinity (30–34) but with long residence times (c. 4 weeks); General methodology and an inner, stratiﬁed and well-ﬂushed estuarine region with low and variable salinity (0–30) as a result Patterns described in this review are based mainly on a of freshwater input from the Knysna River (Largier series of 23 sites positioned to represent the whole area et al. 2000). over which Zostera capensis is present intertidally This system is also one of the most thoroughly (Fig. 1), with additional comparison between the researched of any South African estuary with more macrofaunal eelgrass assemblages at some of those than 100 published articles (Russell et al. 2012; sites and the equivalent assemblages in immediately Whitﬁeld and Baliwe 2013), work there beginning in adjacent areas of bare sediment and/or in subtidal 1947 (Day et al. 1951) (see the summaries of Day seagrass. Sampling was conducted each year between 1967; Grindley 1985; Russell et al. 2012; and the 2009 and 2020 during the austral summer, the research articles in Hodgson and Allanson 2000). Among other being approved by SANParks and conducted in important features, Knysna supports 40% of South accordance with their scientiﬁc research regulations Africa’s dwarf-eelgrass, Zostera (Zosterella) capensis and requirements. A standard procedure was used, [or Nanozostera capensis in the recent revision of the involving series of core samples, each of 0.0027 m Zosteraceae of Coyer et al. (2013)] which may equate diameter prior to 2013 and of 0.0054 m diameter to 20% of its world area (Adams 2016; Wasserman thereafter and of 100 mm depth, taken from contin- et al. 2020). It also forms the only known African uous stretches of seagrass while still covered by [ 10 locality of the unusual marine valvatoidean gastropod cm of water. Cores were gently sieved (’puddled’) Cornirostra (GBIF 2020), as well as being the main through 710-lm mesh on site. This sampling proce- habitat of several other rare seagrass-associated dure collects the smaller and more numerous members species, including the endangered Knysna seahorse of the benthic and epibenthic macrofauna that 123 Aquat Ecol (2021) 55:327–345 329 Fig. 1 Knysna estuarine bay, showing location of the linear Steenbok Channels separating the two large bay islands from the chain of 17 sampling sites along its longitudinal axis and of the mainland. The approximate geographical extents of the faunally six sites a–f set within the backwaters of the Ashmead and distinct regions suggested in Fig. 2 are also indicated constitute the large majority of invertebrate biodiver- dimension are virtually unknown. Such animals were sity (Bouchet et al. 2002; Albano et al. 2011), though treated as morphospecies, an operationally appropriate not the meiofauna nor much scarcer megafauna nor procedure to detect spatial patterns of numbers of sessile animals attached to the seagrass leaves. species and their differential abundance (Dethier and In the laboratory, retained animals from each core Schoch 2006; Gerwing et al. 2020). were identiﬁed to species level wherever possible, All calculations were carried out in Microsoft Excel with all organismal nomenclature here being as listed for Mac 16.37 with the StatPlus:mac Pro 7.1.1 add-on in the World Register of Marine Species (www. or via PAST 3.24 (Hammer et al. 2019). Numbers of marinespecies.org), accessed November 2020, except each component zoobenthic species at each site were in respect of the currently genus-less microgastropods subjected to similarity analysis, and assemblage ’Assiminea’ capensis and ’A’. globulus (see Barnes metrics were derived and compared. Univariate met- 2017). It should be noted, however, that the speciﬁc rics assessed included: (i) overall faunal numbers per identity of several animals, especially among the unit area, (ii) observed numbers of species per unit Polychaeta, is questionable because of lack of recent sample, N [i.e., ’species density’ sensu (Gotelli and revision; those of South African taxa of Polycladida, Colwell 2001)], and (iii) patchiness in spatial abun- Oligochaeta, and Nemertini, and many members of dance of the macrofaunal assemblages as estimated by other groups less than 3 mm–4 mm in largest the ’index of patchiness’ (I ) of Lloyd (1967), with 123 330 Aquat Ecol (2021) 55:327–345 Fig. 2 nMDS plot based on Bray–Curtis similarities between backwaters and axial channel conditions in the marine section percentage species composition data at the 23 sites, showing the would appear to lie along the Steenbok Channel in that site D four groups of seagrass macrofaunal assemblage types, i.e., falls within one grouping and E in the other. Envelopes enclose those in: a the sandy mouth region; b the marine bay; c the sites with the stated levels of Bray–Curtis similarity, for which lagoon and lower estuary; and d the upper estuary and the the approximate geographical locations are shown in Fig. 1 marine-basin backwater channels. The boundary between statistically signiﬁcant departures from random being solely differential taxonomic composition and to determined by Monte Carlo simulation using 9999 permit comparison of curve slopes (Passy 2016), a iterations. Correlations were assessed using Spear- measure of equitability in individual species contri- man’s rank coefﬁcient S or the Pearson product- bution to the total (Whittaker 1972). Overlaps in moment coefﬁcient P as appropriate; number of quantitative assemblage composition between adja- species per site unit of 30 cores and per region unit of cent regions were measured by the Bray–Curtis 180 cores was determined by Mao tau rarefaction; similarity index. All multivariate analyses were based curves were ﬁtted using KaleidaGraph 4.5.4; and, on sample sizes of [ 250 animals, well above the where not known, information on life style of minimum number recommended by Forcino et al. individual species was derived from that of close (2015). relatives in compendia such as Macdonald et al. (2010). Multivariate comparison of macrofaunal assem- Principal ﬁndings blage composition used hierarchical clustering anal- ysis of S Bray–Curtis similarity, ANOSIM, Patterns in assemblage composition ANCOVA, SIMPER, and ordination by non-metric multidimensional scaling (nMDS), with 9999 permu- In total, some 67,000 individual macrofauna, repre- tations. For such comparison, all data sets were senting 160 species, were examined in 2,100 core standardized for overall species density (by dividing samples from the Zostera beds during the study. These all ranks by the total number of species in the set) and ranged from typical freshwater/dilute-brackish species for sample size (by dividing each species total by the such as Afrochiltonia capensis, Corallana africana overall number of individuals in the set) to reﬂect and Melanoides tuberculata through to fully marine 123 Aquat Ecol (2021) 55:327–345 331 Fig. 3 Levels of Bray–Curtis similarity between the seagrass Fig. 2), and b along the axis of shelter perpendicular to ’A’ from macrofaunal assemblages of adjacent sites: a along the the main channel into the fringing backwaters of the marine longitudinal axis of the estuarine bay (arrows indicating points embayment of transition between adjacent faunal assemblage types shown in forms such as Gibbula cicer, Limaria tuberculata, essentially similar pattern to that derived earlier using Nebalia capensis and Parechinus angulosus. Ordina- non-standardized (but fourth-root transformed) abun- tion by nMDS of Bray–Curtis similarity data from the dance data (Barnes 2013a). These represented: (i) the 23 intertidal sites suggested that four signiﬁcantly sandy mouth region immediately adjacent to the true different faunal clusters occurred in the system mouth, (ii) the outer marine embayment, and (iii) the (ANOSIM R = 0.88; P \ 0.0001) (Figs. 1and 2), an lagoon plus lower-estuary divisions of the main axial 123 332 Aquat Ecol (2021) 55:327–345 Table 1 The more dominant members of the Knysna intertidal P = 0.62) (Fig. 4), further indicating similarity seagrass macrofauna present in all four signiﬁcantly different between the different local assemblages. Number of compartments of the system. These 21 species together com- species per sample did not vary across test areas of up prise 70% of the total macrofaunal individuals sampled to 1.5 ha at a given site, whether in the bay or in the GASTROPODA Capitella sp. lagoon (Table 3). The observation that the seagrass ’Assiminea’ capensis Orbinia angrapequensis macrofauna of the brackish upper estuary did not Nassarius kraussianus Cirriformia sp. differ from that in the fully saline, saltmarsh-enclosed Alaba pinnae Paradoneis lyra capensis backwater channels of the marine embayment is Turritella capensis PERACARIDA noteworthy and reinforces the earlier comments of BIVALVIA Exosphaeroma hylecoetes Day (1959) and Barnes (1989) that so-called estuarine Arcuatula capensis Melita zeylanica faunas may be as characteristic of sheltered areas of Salmacoma litoralis Grandidierella lutosa fully marine soft sediment as they are of regions OLIGOCHAETA Cymadusa ﬁlosa subject to low salinity. tubiﬁcid sp. BRACHYURA Major differences, however, did occur in the POLYCHAETA Danielella edwardsii relative importance of infauna versus epifauna. Except Simplisetia erythraeensis Hymenosoma orbiculare at the lagoonal site 9, where the small bioﬁlm-feeding cushion star Parvulastra exigua occurs in large Prionospio sexoculata OSTRACODA Caulleriella capensis ?Cylindroleberis sp. numbers, the intertidal zone of the whole axial channel apart from the upper estuary is dominated by infaunal species (Fig. 5a), principally by polychaetes. From sites 1 to 15, the infauna comprised 68% (SE 3.7) of channel, and (iv) the fringing backwater-creek system animals with no signiﬁcant trend in their relative of the smaller, saltmarsh-enclosed creeks and channels importance along the gradient (S = 0.31; P = 0.26) that separate the bay’s two large islands (each c. (Fig. 5B). In contrast, the shores of the upper estuary 82–84 ha) from the mainland, together with sites in the and the marine backwater channels were dominated by upper estuary. Separation of the backwaters/upper- epifaunal truncatelloid microgastropods, especially by estuary sites from those along the main axial channel ’Assiminea’ capensis and Hydrobia knysnaensis, epi- was the most marked, with a Bray–Curtis similarity fauna here comprising 64.4% of individuals. Only a between the two blocks of sites of only 20%, and the few subtidal Z. capensis sites have so far been mouth region was an outlier within the axial channel. examined, but such areas are also overwhelmingly The three points of change along the longitudinal axis dominated by an epifaunal microgastropod, here by of the bay, however, were not marked by sharp faunal the cerithioid Alaba pinnae, although the importance contrasts (Fig. 3). Indeed, SIMPER indicates that of this species and hence of the subtidal epifauna in most ([ 50%) of the differences are brought about by general decreases upstream so that epifauna and the relative abundances of just eight common and infauna contribute equally in the upper estuary widespread species, the gastropod molluscs Hydrobia (Fig. 5a). Thus in the bay region there is a transition knysnaensis and ’Assiminea’ capensis (dominant in at some LWS between a burrowing polychaete infauna region iv), Turritella and Alaba (dominant in i), and and a seagrass-leaf-associated gastropod epifauna, and Nassarius (dominant in iii), and the polychaetes although upstream sub- and intertidal faunas are Prionospio (dominant in iii), and Caulleriella and relatively similar, downstream in the bay they are Simplisetia (dominant in ii). Despite statistically markedly different (Fig. 6a). Few data are available to signiﬁcant regionalization, 32% of the species (repre- help explain the great downstream subtidal abundance senting [ 75% of the total individuals) occurred in all of the epifaunal Alaba (a mean density of four regions in more than token quantities (Table 1 -2 28,000 m ), although various studies have suggested lists the more numerous of these shared taxa, and that few ﬁsh consume signiﬁcant numbers of shelled Table 2 displays those characteristic of each region). gastropods, even relatively small ones (McCormick Patterns of relative species abundance within the four 1998; Reynolds et al. 2018), not least because of their regions did not differ (ANCOVA equality of means low nutritive value per unit intake (Vinson and Baker F = 0.17, P = 0.92; equality of slopes F = 0.59, 2008). It is known that in South Africa, mugilids will 123 Aquat Ecol (2021) 55:327–345 333 Table 2 Characteristic Species % Species % intertidal seagrass macrofauna (i.e., those Mouth sandﬂats Marine bay together comprising 75% of Alaba pinnae 21.4 Simplisetia erythraeensis 17.8 the faunal individuals) of Turritella capensis 13.5 Prionospio sexoculata 11.1 the four signiﬁcantly different faunal regions of Simplisetia erythraeensis 9.8 Caulleriella capensis 8.9 the Knysna estuarine bay ?Cylindroleberis sp 7.1 Exosphaeroma hylecoetes 4.5 Orbinia angrapequensis 4.3 Nassarius kraussianus 3.6 Paradoneis lyra capensis 3.6 Melita zeylanica 3.5 Pseudopolydora ?kempi 2.9 Hymenosoma orbiculare 3.4 Diogenes brevirostris 2.9 Danielella edwardsii 3.4 Caulleriella capensis 2.7 Cyathura estuaria 3.1 Nassarius kraussianus 2.6 Grandidierella lutosa 2.4 Paridotea ungulata 1.9 Cymadusa ﬁlosa 2.4 Grandidierella lutosa 1.8 Arcuatula capensis 2.3 Lagoon ? lower estuary tubiﬁcid sp. 2.1 Prionospio sexoculata 27.3 ?Cylindroleberis sp. 2.0 Nassarius kraussianus 15.6 Paramoera capensis 1.9 Arcuatula capensis 10.7 ’Assiminea’ capensis 1.6 Parvulastra exigua 6.0 Alaba pinnae 1.5 Simplisetia erythraeensis 5.3 Backwater channels ? upper estuary Salmacoma litoralis 5.2 ’Assiminea’ capensis 40.0 Cirriformia sp. 2.9 Hydrobia knysnaensis 27.3 Dosinia hepatica 2.7 Halmyrapseudes cooperi 4.1 Simplisetia erythraeensis 3.7 Hydrobia at the backwater site ’A’ in Fig. 1 (R take microgastropods (Whitﬁeld and Blaber 1978; s- Whitﬁeld 1988), but at Knysna mugilids do not = 0.78; P \ 0.00001). Such a parasite/host associa- characterize the dense sublittoral eelgrass beds tion is known from the western Atlantic (e.g., Hershler favored by Alaba (Pollard et al. 2017). Several and Davis 1980), but although the pyramidellid equivalent subtidal areas of seagrass in other conti- concerned is a widely distributed animal, it is other- nents are also dominated by species of Alaba, although wise not recorded from Africa (GBIF 2020). That Knysna is the only known such locality outside the exception apart, however, in a large sample (325 tropics (Barnes and Claassens 2020). These other cores) from the Kingﬁsher Creek seagrass (site 2 in areas are of relatively high salinity which may help to Fig. 1), for example, Barnes (2013b) recorded 75 account for the lesser importance of this gastropod in macrofaunal species at overall and mean densities of -2 and near the upper estuary. Why the same suite of 2581 and 34 m , respectively. Considering the 34 truncatelloid microgastropods dominates the other- relatively common species there that each attained a -2 wise contrasting habitats of the intertidal backwaters mean density of at least 10 m (and together and upper estuary is not known for certain, but their comprised 96% of the total individuals), all pairwise common shelter (see paragraph above) is likely to be correlations of species abundance were very weak to an important component. non-existent (sensu Moore et al. 2018), positives With one exception, no evidence of any strong averaging only P = 0.069 (± 0.060 SD) and nega- species interactions within any given site was forth- tives P = 0.047 (± 0.035 SD); and allowing for the coming. The exception was the positive correlation familywise errors inherent in such a large correlation between numbers of the ectoparasitic pyramidellid matrix (via Bonferroni correction), no negative corre- snail Sayella sp. and those of its probable host lations and only three positive ones were signiﬁcant at 123 334 Aquat Ecol (2021) 55:327–345 Fig. 4 Species abundance diagrams (Whittaker plots) for each of the four faunistically distinct assemblage types Table 3 Uniformity of number of intertidal species per sample index of spatial homogeneity (I ), with signiﬁcance of I tested a p at different scales across test areas of (A) 0.2 ha and (B) 1.5 ha by Monte Carlo simulation (data from Barnes, 2013b, 2016 and at Site 2 and (C) along a 350 m transect at site 9, as assessed by Barnes and Hendy, 2015a) Lloyd’s index of patchiness (I ) and the Azovsky et al. (2000) Unit sample size Lloyd’s I Azovsky et al.’s I Signiﬁcance of uniformity p a 0.0015 m 0.948 0.977 P = 0.1 0.0027 m 0.938 0.988 P = 0.03 0.0054 m 0.933 0.995 P = 0.004 0.0095 0.962 0.995 P = 0.009 0.0054 m 0.974 0.997 P = 0.005 0.0054 m 0.929 0.994 P = 0.01 a critical a of \ 0.05 (between the polychaetes older literature) from the majority of the system, Simplisetia and Caulleriella, Glycera and Cirriformia, faunal relationships between seagrass and bare sedi- and between the polychaete Prionospio and the ment at Knysna are not the classic one of seagrass gastropod Nassarius). Equivalently, although qualita- supporting the greater number of species and of tive co-occurrence patterns across the whole of the individuals per unit area (Hemminga and Duarte 2000; marine-inﬂuenced embayment at Knysna show deter- Pillay et al. 2011; Hyman et al. 2019, etc.). To date ministic structuring (Barnes and Elwood 2011), as studies have only concerned the outer marine embay- indeed might be expected granted the location of the ment, but there seagrass macrofauna at a given site is sampled sites in three distinct faunal regions (sandy more similar to those occurring in adjacent areas of mouth, marine bay, and backwater system), syntopic bare sediment than either habitat is to other areas of the species within a single one of those regions did not same type in the general region [Bray–Curtis faunal differ from random co-occurrences (Barnes and Bar- similarity between the two contiguous habitat types nes 2014b). being a mean 0.58, whereas within-habitat-type sim- In the absence of strong bioturbators such as ilarity averaged 0.26 for the seagrass and 0.25 for the Kraussillichirus kraussi (Callianassa kraussi in the bare sediment (ANOVA F = 5.05; P \ 0.05)] (see 1,14 123 Aquat Ecol (2021) 55:327–345 335 Human et al. (2016). In these circumstances, the former seagrass sites clustered together, as did the same areas when de-vegetated, although macrofaunal abundance was again signiﬁcantly lower in the former seagrass than it was in the replacement bare sediment (in a ratio of 0.62: 1) and again largely because of an increased number of polychaetes and decreased num- ber of crustaceans in the unvegetated sediment (Bar- nes 2019a). Knysna’s marine embayment forms a natural harbor, has been in the past a busy port (Grindley 1985), and today supports several marinas, and hence it is one of the centers of ship-borne alien immigrant species in South Africa (Grifﬁths et al. 2009). Alien species of Boccardia, Polydora, Dipolydora, Pseu- dopolydora, Diopatra, Capitella, Desdemona, Eric- thonius, Jassa, Monocorophium, Paracerceis, Elysia, Favorinus and Indothais all form part of its seagrass fauna, as do amphipods such as Cymadusa ﬁlosa, Melita zeylanica and Americorophium triaeonyx that are regarded by Robinson et al. (2005) and Mead et al. (2011) as being cryptogenic—to which could presum- ably be added Victoriopisa chilkensis. Relatively recently, these aliens have been joined by more northerly species spreading southward probably as a result of global warming. Smaragdia souverbiana, for example, is now a member of the subtidal seagrass fauna (Barnes and Claassens 2020). In the Knysna Fig. 5 Relative importance of infauna and epifauna in a the intertidal, Melanoides tuberculata has arrived and different intertidal and subtidal regions of the estuarine bay and joined Cerithidea decollata (Hodgson and Dickens b at each of the sites along the longitudinal axial channel 2012) and Austruca occidentalis (formerly Uca annulipes) (Peer et al. 2015), the latter two in the adjacent saltmarsh or at the seagrass/saltmarsh Fig. 6b). In general, seagrass beds supported lower, not higher, levels in half the metric comparisons in interface. which there was a signiﬁcant difference (Barnes and Barnes 2014a). Overall, faunal abundance was lower Patterns in assemblage metrics along the axial gradient in seagrass in the ratio of 0.64: 1, while species density was indeed higher, but only by 1.13 to 1, with in large As would be expected, the number of species at the 17 measure the higher numbers in the unvegetated sediments resulting from a quadrupled abundance of sites that were spaced along the system’s longitudinal axis decreased with distance upstream (S = -0.82; infaunal polychaetes, maybe because of the greater P \ 0.0001; Fig. 7a), but the form of the decrease in volume of available sedimentary habitat in the absence of eelgrass rootmass, although numbers of epifaunal species density suggests the occurrence of a step change within the general area of the lower estuary, crustaceans were 15 times less there (from a much smaller base). The same overall effect was not the with the downstream sites showing a considerable degree of uniformity of species density (Fig. 7b; case, however, in bare areas created by the death of seagrass following blanketing by the chlorophyte Table 4). The points in Fig. 7 are based on the whole available 12-year dataset, and hence, the location of blooms described by Allanson et al. (2016) and faunal and regional boundaries will have been blurred 123 336 Aquat Ecol (2021) 55:327–345 Fig. 6 nMDS plots based on Bray–Curtis similarities between channel (site 1) into the backwater Steenbok Channel and its percentage species composition data: a at four sites in the tributaries, showing similarity between macrofaunal assem- Knysna estuarine bay, one in each faunal compartment, showing blages in seagrass and in adjacent areas of bare sediment (from the similarity between macrofaunal assemblages of seagrass at data in Barnes and Barnes 2014a). Envelopes enclose sites at the LWS in the intertidal zone and in the adjacent subtidal area stated levels of Bray–Curtis similarity, and site codes are those (from data in Barnes and Claassens 2020), and b at three sites in given in Fig. 1, plus in (A) an additional site, ’X’, located the marine embayment forming a transect from the main between sites 1 and 2 Fig. 7 Change in number of seagrass macrofaunal species along the longitudinal axis of the estuarine bay a. Note in b the apparent break between sites 10 and 11, corresponding to the one in the same area shown by Barnes and Ellwood (2012) by temporal shifts, but an individual survey of also would be expected, the total fauna contained in macrofaunal animals along the axial channel in 2012 each is considerably in excess of that at any individual showed an almost identical (and sharper) feature site. (Barnes and Ellwood 2012) in the same general Assemblage abundance per unit area (S = -0.35; location. Comparison of data across different spatial P = 0.16; Fig. 8a) and patchiness in assemblage scales shows that decline upstream in number of abundance (S = -0.20; P = 0.45; Fig. 8b), however, species when assessed per site (Fig. 7) is greater than showed no signiﬁcant change with distance upstream; when assessed per region (Table 4): Clearly, the bay indeed, degree of patchiness along the axial gradient and lagoon ? lower-estuary regions are large and, as was signiﬁcantly unchanging (Barnes 2019b). Neither 123 Aquat Ecol (2021) 55:327–345 337 Table 4 Biodiversity metrics of the various intertidal faunal functional categories as per Macdonald et al. (2010) and regions of Knysna estuarine bay: Mao tau species density (N ), Barnes and Hendy (2015a)]. Each axial regional metric is with Chao 2 estimations; N and N species diversity; based on the common sample size of 180 9 0.0054 m cores, 1 2 equitability of species abundance (J); taxonomic diversity (D) yielding some 90% of the likely total species; backwaters * 2 and distinctness (D ); and N functional diversity (F ) [with metric based on 148 9 0.0054 m samples. Peak values in bold 2 d Mouth Bay Lagoon ? lower estuary Upper estuary Backwaters Mao tau N density 94 78 72 34 59 Chao 2 N 104 84 76 38 63 N diversity 21.3 23.5 14.8 9.8 5.5 N diversity 10.9 13.1 8.1 7.8 3.1 J equitability 0.68 0.73 0.61 0.65 0.42 D diversity 4.09 4.25 3.89 3.75 2.45 D distinctness 4.54 4.50 4.72 4.32 3.61 F diversity 7.56 8.38 5.13 4.77 1.64 was there any signiﬁcant relationship between number General discussion and conclusions of species per site and overall assemblage abundance The most striking feature of the Knysna intertidal there (S = 0.43; P = 0.08). However, signiﬁcant relationships have been found between how patchy seagrass-associated macrobenthos is its relative spatial uniformity. Macrofaunal abundance does not vary an individual species is and its occupancy and, to a lesser extent, its abundance: The more abundant and markedly along the longitudinal axis, neither does patchiness of macrofaunal density. Number of species widespread the species, the less its patchiness, both in subtidal and in intertidal seagrass (Barnes per unit area at a given site is a constant, while species 2019c, 2020), and both in interspeciﬁc comparisons density along whole sections of the gradient can be (Barnes 2020) and intraspeciﬁcally (Barnes, in prep.) relatively uniform, and its fauna appears to form a (Fig. 9). This suggests that the well-known macroe- single assemblage with only local variation in relative cological abundance-occupancy pattern (e.g., He and frequency of its dominant components. Even the Gaston 2003) can be extended into a patchiness- subtidal fauna does not differ qualitatively from the intertidal one, although there are marked quantitative abundance-occupancy one, at least in this habitat type. As can be seen in Fig. 9, the slopes of the power laws differences and overall it is much more abundant especially in the most marine-inﬂuenced regions relating logit occupancy to log patchiness in individual species are much more variable than those interspecif- where Alaba dominates (Barnes and Claassens 2020). Admittedly, being a marine-dominated system ically in the different faunal regions; thus, while the interspeciﬁc occupancy-patchiness slopes represent- with under normal circumstances relatively little ing different regions do not differ (ANCOVA F = 1.3, freshwater input (Day et al. 1951), for an estuarine P = 0.3), the equivalent intraspeciﬁc slopes are system salinity is relatively constant; however, occa- heterogeneous (ANCOVA F = 4.9, P \ 0.0001) with sional episodes of severe freshwater ﬂooding do occur once every 10–12 years or so, rendering most or all of a further six of the dominants (including the epifaunal Alaba and Cymadusa, and infaunal Caulleriella and the system temporarily fresh (see, e.g., Korringa 1956; Blake and Chimboza 2010). But, although sea water Salmacoma) not showing signiﬁcant occupancy- patchiness relationships at all. This also indicates that may penetrate far upstream and dominate most areas, there is much change along the Knysna axis in other disparate species together form assemblages with similar properties in the various regions. There were features of direct relevance to macrobenthos, as in no discernable trends in either metric upstream, transitional paralic systems in general (Tagliapietra although the upper estuary did display the largest et al. 2012;Perez-Ruzafa et al. 2019). Sediment value of both b and R . changes from clean sand at the mouth, to soft organic mud in the lagoonal and lower estuarine regions, and 123 338 Aquat Ecol (2021) 55:327–345 Fig. 8 Relative constancy of intertidal seagrass macrofaunal patchiness (data from Barnes 2019b). b(ii) illustrates spatial -2 assemblage metrics along the longitudinal axis of the estuarine variation in macrofaunal density 0.01 m across an area of site bay: a assemblage abundance, with an inset showing abun- 2 (from data in Barnes 2016) dances at the six backwater-channel sites; and b(i) assemblage to mud with admixed riverine gravel in the upper exposure (den Hartog 1970; Adams and Talbot 1992); estuary (Day et al. 1951); shelter changes both as the and so on. estuary narrows and on transition from axial channel Being located at 34S, Knysna lies within the into backwater creeks (Day 1967); and shore proﬁles narrow mid-latitude belt recently identiﬁed by Whalen change from extensive tidal ﬂats near the mouth to et al. (2020) as that displaying peak intensity of animal narrow steep slopes in the estuary supporting only food consumption and hence potential top-down linear strips of seagrass (Day 1967; Maree 2000). control of prey species. Like other South African Rates of water exchange vary along the channel estuarine areas supporting dwarf-eelgrass (Whitﬁeld (Largier et al. 2000); characteristic density and shoot et al. 1989; Nel et al. 2018), it is a nursery area for length of the eelgrass change with shore height and many nektonic species (Whitﬁeld and Kok 1992), 123 Aquat Ecol (2021) 55:327–345 339 Knysna’s seagrass macrobenthos become more understandable. Three lines of evidence suggest that across the whole system seagrass macrofaunal abundance is below carrying capacity and not structured by density- dependent factors. First, the prevailing intertidal density along the longitudinal axis of some -2 2 4,000 m is very low compared to the [ 40,000 m animals occurring in similar intertidal dwarf-eelgrass beds in cool-temperate Europe (Blanchet et al. 2004; Barnes and Ellwood 2011; etc.) where predator rates are almost certainly lower on a fauna of similarly sized animals that are often members of the same families as represented at Knysna (Barnes and Hendy 2015b). Secondly, constancy of number of species per unit area, as demonstrated at the Kingﬁsher Creek site at Knysna (Barnes 2013b), is exactly what would be expected were the various species to be distributed independently of each other (granted their overall frequencies of occurrence) (Barnes and Barnes 2014b). Such independence of distribution is likely only if the whole assemblage is being maintained below the level at which species would otherwise interact. Thirdly, the large quantitative dataset of Barnes (2013b) from the same Kingﬁsher Creek site also showed that there were very few signiﬁcant correlations (0.5%) between the abundances of pairs Fig. 9 The power laws (y = ax ) describing signiﬁcant of species and all those were very weak. Moreover, as relationships between log Lloyd’s I patchiness and logit seen elsewhere, for example within Paciﬁc Canadian occupancy in the seagrass macrofauna of Knysna estuarine Zostera marina meadows (Stark et al. 2020), weak and bay, both a interspeciﬁcally in the different assemblage types and b intraspeciﬁcally in individual dominant species very weak positive relationships greatly out-numbered negative ones, further suggesting the lack of compet- itive interspeciﬁc interactions. In such overall circum- schools of juvenile ﬁsh being a common sight in its stances of low and unpredictable density of potential invertebrate prey species, predators could thus be seagrass beds. Indeed, seagrass beds have been regarded as one the most important types of coastal expected to have to forage optimally (Beseres and nursery (Whitﬁeld 2017; Lefcheck et al. 2019), both Feller 2007) and to graze down local prey stocks to because of the food they provide (Whitﬁeld 2017) and threshold levels before moving and repeating the as refuge from larger ﬁsh predators (Whitﬁeld 2020a). process elsewhere, and having reduced their food If, as is generally held to be the case in seagrass stocks to low levels over wide areas could themselves (Moksnes et al. 2008; Lewis and Anderson 2012; then experience food limitation (Saulnier et al. 2000). The actions of such predators roaming widely over the Duffey et al. 2015, etc.), the effect of this consump- tion, together with that exerted by adult ﬁsh (Pollard surface might also help explain the uniform levels of macrofaunal patchiness characterizing large areas et al. 2017) and predatory members of the invertebrate macrobenthos, is top-down control of the seagrass (Barnes and Hamylton 2019). A second process that could help account for the microphytobenthic-bioﬁlm consumers that dominate both epifauna and infauna, then many of features of observed features of the Knysna macrobenthic assem- blages, and particularly their relative uniformity along the longitudinal axis, is if the presence of the seagrass 123 340 Aquat Ecol (2021) 55:327–345 Fig. 10 Destructive effects of bait-collecting activities on by such mudprawn pushing; and c, the resultant plugs scattered intertidal seagrass habitat in the ’no-take bait sanctuary’ section over the seagrass surface; d, an area of seagrass destroyed by of the Knysna estuarine bay: a The hole and jettisoned plug trenching for bait worms (from Barnes and Claassens 2020) created by pushing for mudprawn; b, a substratum pock-marked ameliorates variation in the local ambient microcli- Claassens et al. (2020), and the two that might matic conditions, as a macro-algal cover has been particularly affect the seagrass and its inhabitants are shown to do (Scrosati 2017; Monteiro et al. 2017). uncontrolled bait harvesting by destructive means and Within the relatively uniform and stable conditions chlorophyte blooms. Bait harvesting by ’pushing’ for provided by the Z. capensis bed, species can penetrate mudprawns (Upogebia capensis) and trenching for upstream further than they might otherwise be able to worms (Marphysa, Polybrachiorhynchus and Areni- do (Barnes and Ellwood 2012). Seagrass beds and cola spp.) is rife in Knysna (Simon et al. 2019), even other structurally complex systems (Hyman et al. (and arguably especially) in the formally protected 2019) generally appear to support macrofaunal assem- bait-reserve area (Fig. 10) that also supports 79% of blages that display spatial and temporal stability of the estuarine bay’s seagrass-associated species. Unfor- abundance and composition, and high levels of tunately, there are immense logistic and social prob- resilience (Whanpetch et al. 2010; Blake et al. 2014; lems associated with preventing illegal and restricting Gartner et al. 2015), and this may have important legal bait harvesting in southern Africa, especially in knock-on effects on the whole local coastal food web areas of high unemployment where subsistence ﬁshing (Jankowska et al. 2019). provides the main or only source of protein (Bandeira Granted the current high loss rates of seagrass and Gell 2003; Napier et al. 2009) and the local throughout the world (Waycott et al. 2009; Short et al. intertidal provides the only source of bait (Barnes and 2011) and of Zostera capensis in southern Africa Claassens 2020). Subsistence harvesting at Knysna is (Adams 2016), an important question is the implica- worth some ZAR 1 9 10 (Turpie 2007). Its precise tion of the operation of such potential structuring effect on the seagrass macrofauna is unknown; factors at Knysna for the future of its important however, basically because the extent of harvesting seagrass system. Threats to the health of Knysna means that a like-with-like, harvested versus unhar- estuarine bay have recently been reviewed by vested, comparison is not possible: No area of 123 Aquat Ecol (2021) 55:327–345 341 intertidal seagrass remains un-pushed or un-pumped. ([ 30% of the saltmarsh has already gone, and 25% At other localities, however, it and the associated of that remaining is under threat). Thus far, at least, it trampling are known to have severe consequences has managed to fare better than many other South (e.g., Pillay et al. 2010; Garmendia et al. 2017; Short African estuarine systems (van Niekerk et al. 2013), et al. 2011; Adams 2016). Nevertheless, the inherent and it may yet continue to do so. resilience and spatial uniformity of the Knysna Acknowledgements I am most grateful to SANParks area seagrass beds referred to above, together with the fact ofﬁce, Knysna, and SANParks Scientiﬁc Services, Rondevlei, that they form one large interconnected system with for permission to conduct research on the Knysna system over dispersal possible between all sections, does offer the last decade or so; to Rhodes University Research Committee hope. for their support; to my collaborators at various times, sequentially Farnon Ellwood, Morvan Barnes, Ian Hendy and In respect of the second major threat, at the moment Louw Claassens, for their contribution to the study; to Brian the problems of eutrophication, to which Z. capensis is Allanson for his copious encouragement and support; and to an known to be sensitive (Mvungi and Pillay 2019), and anonymous reviewer for saving me from error. consequent algal blooms are only local, affecting mainly the backwater channels into which the munic- Author contributions RSKB conceived, designed, and executed this study and wrote the manuscript. No other person ipal sewage treatment plant discharges and in which is entitled to authorship. there is a legacy of organic matter retention (Human et al. 2020). Knysna’s large tidal prism proves Funding No funding was received for conducting this study. invaluable insofar as minimizing blooms in the main axial channel is concerned. But the local effect of the Data availability and material Datasets on which these analyses are based have been lodged in electronic format in the chlorophyte blanket is dramatic and destructive. Rondevlei Ofﬁce of SANParks Scientiﬁc Services (http:// Animal numbers may increase on its seasonal dieback, dataknp.sanparks.org/sanparks/metacat/Nerinak.23.11/ except in the very local areas of anoxia, although this sanparks) and are available on request. increase is almost entirely conﬁned to densities of the Compliance with ethical standards dominant polychaete groups (except, for some reason, cirratulids) (Barnes 2019a). Crustaceans do not Conﬂict of interest The author declares no conﬂict of interest. bounce back so readily, and as they provide the food for most ﬁsh in the nearby Swartvlei Estuary (Whit- Consent for publication The author consents to publication. ﬁeld 1988, 2020b) and presumably therefore do so at Ethical approval All applicable international, national, and/ Knysna, the ﬁsh populations may suffer the conse- or institutional guidelines for sampling, care, and experimental quences: There is some evidence that this is indeed the use of organisms for the study were followed, and all necessary case (Pollard et al. 2018). The chlorophyte problem is permissions and approvals were obtained in respect of the soluble (no pun intended) but at considerable cost (see original collections of the data. Human et al. 2020). The ﬁnancial reward, however, Open Access This article is licensed under a Creative Com- might also be large, not least because such blooms mons Attribution 4.0 International License, which permits use, impact on tourism (Boesch et al. 1996) and tourists sharing, adaptation, distribution and reproduction in any med- contribute some ZAR 1 9 10 per annum to the ium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Knysna economy (Turpie 2007). Commons licence, and indicate if changes were made. The Knysna is perhaps not a typical South African images or other third party material in this article are included in estuary in being permanently open (see van Niekerk the article’s Creative Commons licence, unless indicated et al. 2020), without a signiﬁcant presence of Kraus- otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your sillichirus, and with a subtidal dominated by the little- intended use is not permitted by statutory regulation or exceeds known Alaba pinnae, but nevertheless its fauna the permitted use, you will need to obtain permission directly generally appears to be the classic Cape estuarine from the copyright holder. To view a copy of this licence, visit one (Day 1981; de Villiers et al. 1999); indeed, it http://creativecommons.org/licenses/by/4.0/. supports [ 40% of South African estuarine biodiver- sity. 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Publisher: Springer Journals
Copyright: Copyright © The Author(s) 2021
ISSN: 1386-2588
eISSN: 1573-5125
DOI: 10.1007/s10452-021-09848-3
Publisher site: See Article on Publisher Site

Abstract

Aquat Ecol (2021) 55:327–345 https://doi.org/10.1007/s10452-021-09848-3(0123456789().,-volV)(0123456789().,-volV) Patterns of seagrass macrobenthic biodiversity in the warm- temperate Knysna estuarine bay, Western Cape: a review R. S. K. Barnes Received: 3 December 2020 / Accepted: 24 February 2021 / Published online: 11 March 2021 The Author(s) 2021 Abstract Knysna estuarine bay in South Africa’s constant; further, one-third of species occur through- Garden Route National Park is that country’s most out. Intertidally, all but peripheral compartments are signiﬁcant estuarine system for biodiversity and low density and infaunally dominated, while some conservation value. One outstanding feature is support peripheral areas, and much of the subtidal, are higher of 40% of South Africa’s—and maybe 20% of the density and epifaunally dominated. Overall, seagrass world’s—remaining vulnerable and decreasing dwarf- macrobenthos appears maintained below carrying eelgrass, Zostera capensis, whose associated benthic capacity (e.g., by abundant juvenile ﬁsh) and of macrofauna has been studied since 2009. For these random species composition within a site. Two further invertebrates, Knysna comprises several signiﬁcantly characteristics are notable: Unusually, seagrass sup- different compartments: sandy mouth; well-ﬂushed ports fewer animals than adjacent unvegetated areas, marine embayment; poorly ﬂushed central sea-water probably because of lack of bioturbatory disturbance ’lagoon’; and two disjunct but faunistically similar in them, and the vegetation cover may ameliorate peripheral regions–marine backwater channels, and ambient habitat conditions. Unfortunately, continual low-salinity upper estuary. Although macrofauna heavy and effectively unpreventable exploitation for ranges from dilute brackish to fully marine, its bait occurs, and chlorophyte blooms have developed abundance, local patchiness, and over considerable because of high nutrient input. Knysna presents a stretches, species density remains remarkably microcosm of problems facing biodiverse and high- value habitats set within areas of high unemployment where subsistence ﬁshing provides the main source of Handling Editor: Te ´lesphore Sime-Ngando protein and seagrass provides the only source of bait. R. S. K. Barnes (&) Keywords Biodiversity Conservation Intertidal Department of Zoology and Entomology, Rhodes University, Eastern Cape, Makhanda 6140, Republic of Knysna Macrobenthos Seagrass South Africa e-mail: rsb1001@cam.ac.uk R. S. K. Barnes Knysna Basin Project Laboratory, Western Cape, Introduction Knysna 6571, Republic of South Africa The permanently open Knysna estuarine bay (34803 S, R. S. K. Barnes 23803 E) is a drowned river valley in South Africa’s Department of Zoology and Conservation Research Institute, University of Cambridge, Cambridge, UK 123 328 Aquat Ecol (2021) 55:327–345 Western Cape separated from the adjacent Indian (Hippocampus capensis), and it is one of the only two Ocean by a narrow gorge (300 m wide, 700 m long, localities that support the critically endangered sea- and 4 m deep at low tide) carved through the coastal grass false-limpet (Siphonaria compressa) and a quartzite ridge by the Knysna River during times of seagrass population of the dwarf cushion-star Parvu- lower sea level. The bay forms part of the open-access lastra exigua. Except in the immediate vicinity of the Garden Route National Park, and on a basket of mouth, Z. capensis, together with some mixed criteria, including its size, diversity of habitat, zonal Halophila ovalis, occurs virtually throughout the rarity, and biodiversity, is ranked South Africa’s most intertidal zone of the system as one continuous bed signiﬁcant estuarine system in terms of conservation (Maree 2000), and it also occurs subtidally though importance (Turpie and Clark 2007; van Niekerk et al. more patchily (Wasserman et al. 2020; Barnes and 2019). Known locally as the Knysna Lagoon, the Claassens 2020). Such meadows support well-devel- system has an area of some 10 km at low tide and 16 oped invertebrate macrofaunas that serve the vital km at high tide and receives the inﬂow of the Knysna functions of consuming epiphytic algal growths and River at its head and a large number of smaller streams providing the trophic link between microphytobenthic along its northern and eastern shores. Nevertheless, it production and that of the larger, more mobile nekton is marine-dominated, consequent on low average rates (Murphy et al. 2021). This article synthesizes the main of freshwater inﬂow and a very large tidal prism, ﬁndings of the disparate series of researches conducted 6 3 during spring tides equaling 19 9 10 m [the largest on these invertebrate faunal assemblages at Knysna of any South African estuary (Grindley 1985)], since 2009, re-analyzing the original data where causing semi-diurnal ﬂushing of its main channel. appropriate, with particular emphasis on patterns of The estuarine bay can be divided hydrologically into macrofaunal assemblage composition, abundance, three linear compartments, which vary in areal extent species richness, and patchiness along the bay’s main and precise geographical position with the tidal cycle axial transitional gradient, as well as along the and magnitude of river ﬂow: An outer marine bay gradient of shelter, located perpendicular to that axis tidally ﬂushed with cool water from the Indian Ocean across its eastern section. and with salinities usually [ 34; a middle, more isolated lagoonal water body also of high salinity (30–34) but with long residence times (c. 4 weeks); General methodology and an inner, stratiﬁed and well-ﬂushed estuarine region with low and variable salinity (0–30) as a result Patterns described in this review are based mainly on a of freshwater input from the Knysna River (Largier series of 23 sites positioned to represent the whole area et al. 2000). over which Zostera capensis is present intertidally This system is also one of the most thoroughly (Fig. 1), with additional comparison between the researched of any South African estuary with more macrofaunal eelgrass assemblages at some of those than 100 published articles (Russell et al. 2012; sites and the equivalent assemblages in immediately Whitﬁeld and Baliwe 2013), work there beginning in adjacent areas of bare sediment and/or in subtidal 1947 (Day et al. 1951) (see the summaries of Day seagrass. Sampling was conducted each year between 1967; Grindley 1985; Russell et al. 2012; and the 2009 and 2020 during the austral summer, the research articles in Hodgson and Allanson 2000). Among other being approved by SANParks and conducted in important features, Knysna supports 40% of South accordance with their scientiﬁc research regulations Africa’s dwarf-eelgrass, Zostera (Zosterella) capensis and requirements. A standard procedure was used, [or Nanozostera capensis in the recent revision of the involving series of core samples, each of 0.0027 m Zosteraceae of Coyer et al. (2013)] which may equate diameter prior to 2013 and of 0.0054 m diameter to 20% of its world area (Adams 2016; Wasserman thereafter and of 100 mm depth, taken from contin- et al. 2020). It also forms the only known African uous stretches of seagrass while still covered by [ 10 locality of the unusual marine valvatoidean gastropod cm of water. Cores were gently sieved (’puddled’) Cornirostra (GBIF 2020), as well as being the main through 710-lm mesh on site. This sampling proce- habitat of several other rare seagrass-associated dure collects the smaller and more numerous members species, including the endangered Knysna seahorse of the benthic and epibenthic macrofauna that 123 Aquat Ecol (2021) 55:327–345 329 Fig. 1 Knysna estuarine bay, showing location of the linear Steenbok Channels separating the two large bay islands from the chain of 17 sampling sites along its longitudinal axis and of the mainland. The approximate geographical extents of the faunally six sites a–f set within the backwaters of the Ashmead and distinct regions suggested in Fig. 2 are also indicated constitute the large majority of invertebrate biodiver- dimension are virtually unknown. Such animals were sity (Bouchet et al. 2002; Albano et al. 2011), though treated as morphospecies, an operationally appropriate not the meiofauna nor much scarcer megafauna nor procedure to detect spatial patterns of numbers of sessile animals attached to the seagrass leaves. species and their differential abundance (Dethier and In the laboratory, retained animals from each core Schoch 2006; Gerwing et al. 2020). were identiﬁed to species level wherever possible, All calculations were carried out in Microsoft Excel with all organismal nomenclature here being as listed for Mac 16.37 with the StatPlus:mac Pro 7.1.1 add-on in the World Register of Marine Species (www. or via PAST 3.24 (Hammer et al. 2019). Numbers of marinespecies.org), accessed November 2020, except each component zoobenthic species at each site were in respect of the currently genus-less microgastropods subjected to similarity analysis, and assemblage ’Assiminea’ capensis and ’A’. globulus (see Barnes metrics were derived and compared. Univariate met- 2017). It should be noted, however, that the speciﬁc rics assessed included: (i) overall faunal numbers per identity of several animals, especially among the unit area, (ii) observed numbers of species per unit Polychaeta, is questionable because of lack of recent sample, N [i.e., ’species density’ sensu (Gotelli and revision; those of South African taxa of Polycladida, Colwell 2001)], and (iii) patchiness in spatial abun- Oligochaeta, and Nemertini, and many members of dance of the macrofaunal assemblages as estimated by other groups less than 3 mm–4 mm in largest the ’index of patchiness’ (I ) of Lloyd (1967), with 123 330 Aquat Ecol (2021) 55:327–345 Fig. 2 nMDS plot based on Bray–Curtis similarities between backwaters and axial channel conditions in the marine section percentage species composition data at the 23 sites, showing the would appear to lie along the Steenbok Channel in that site D four groups of seagrass macrofaunal assemblage types, i.e., falls within one grouping and E in the other. Envelopes enclose those in: a the sandy mouth region; b the marine bay; c the sites with the stated levels of Bray–Curtis similarity, for which lagoon and lower estuary; and d the upper estuary and the the approximate geographical locations are shown in Fig. 1 marine-basin backwater channels. The boundary between statistically signiﬁcant departures from random being solely differential taxonomic composition and to determined by Monte Carlo simulation using 9999 permit comparison of curve slopes (Passy 2016), a iterations. Correlations were assessed using Spear- measure of equitability in individual species contri- man’s rank coefﬁcient S or the Pearson product- bution to the total (Whittaker 1972). Overlaps in moment coefﬁcient P as appropriate; number of quantitative assemblage composition between adja- species per site unit of 30 cores and per region unit of cent regions were measured by the Bray–Curtis 180 cores was determined by Mao tau rarefaction; similarity index. All multivariate analyses were based curves were ﬁtted using KaleidaGraph 4.5.4; and, on sample sizes of [ 250 animals, well above the where not known, information on life style of minimum number recommended by Forcino et al. individual species was derived from that of close (2015). relatives in compendia such as Macdonald et al. (2010). Multivariate comparison of macrofaunal assem- Principal ﬁndings blage composition used hierarchical clustering anal- ysis of S Bray–Curtis similarity, ANOSIM, Patterns in assemblage composition ANCOVA, SIMPER, and ordination by non-metric multidimensional scaling (nMDS), with 9999 permu- In total, some 67,000 individual macrofauna, repre- tations. For such comparison, all data sets were senting 160 species, were examined in 2,100 core standardized for overall species density (by dividing samples from the Zostera beds during the study. These all ranks by the total number of species in the set) and ranged from typical freshwater/dilute-brackish species for sample size (by dividing each species total by the such as Afrochiltonia capensis, Corallana africana overall number of individuals in the set) to reﬂect and Melanoides tuberculata through to fully marine 123 Aquat Ecol (2021) 55:327–345 331 Fig. 3 Levels of Bray–Curtis similarity between the seagrass Fig. 2), and b along the axis of shelter perpendicular to ’A’ from macrofaunal assemblages of adjacent sites: a along the the main channel into the fringing backwaters of the marine longitudinal axis of the estuarine bay (arrows indicating points embayment of transition between adjacent faunal assemblage types shown in forms such as Gibbula cicer, Limaria tuberculata, essentially similar pattern to that derived earlier using Nebalia capensis and Parechinus angulosus. Ordina- non-standardized (but fourth-root transformed) abun- tion by nMDS of Bray–Curtis similarity data from the dance data (Barnes 2013a). These represented: (i) the 23 intertidal sites suggested that four signiﬁcantly sandy mouth region immediately adjacent to the true different faunal clusters occurred in the system mouth, (ii) the outer marine embayment, and (iii) the (ANOSIM R = 0.88; P \ 0.0001) (Figs. 1and 2), an lagoon plus lower-estuary divisions of the main axial 123 332 Aquat Ecol (2021) 55:327–345 Table 1 The more dominant members of the Knysna intertidal P = 0.62) (Fig. 4), further indicating similarity seagrass macrofauna present in all four signiﬁcantly different between the different local assemblages. Number of compartments of the system. These 21 species together com- species per sample did not vary across test areas of up prise 70% of the total macrofaunal individuals sampled to 1.5 ha at a given site, whether in the bay or in the GASTROPODA Capitella sp. lagoon (Table 3). The observation that the seagrass ’Assiminea’ capensis Orbinia angrapequensis macrofauna of the brackish upper estuary did not Nassarius kraussianus Cirriformia sp. differ from that in the fully saline, saltmarsh-enclosed Alaba pinnae Paradoneis lyra capensis backwater channels of the marine embayment is Turritella capensis PERACARIDA noteworthy and reinforces the earlier comments of BIVALVIA Exosphaeroma hylecoetes Day (1959) and Barnes (1989) that so-called estuarine Arcuatula capensis Melita zeylanica faunas may be as characteristic of sheltered areas of Salmacoma litoralis Grandidierella lutosa fully marine soft sediment as they are of regions OLIGOCHAETA Cymadusa ﬁlosa subject to low salinity. tubiﬁcid sp. BRACHYURA Major differences, however, did occur in the POLYCHAETA Danielella edwardsii relative importance of infauna versus epifauna. Except Simplisetia erythraeensis Hymenosoma orbiculare at the lagoonal site 9, where the small bioﬁlm-feeding cushion star Parvulastra exigua occurs in large Prionospio sexoculata OSTRACODA Caulleriella capensis ?Cylindroleberis sp. numbers, the intertidal zone of the whole axial channel apart from the upper estuary is dominated by infaunal species (Fig. 5a), principally by polychaetes. From sites 1 to 15, the infauna comprised 68% (SE 3.7) of channel, and (iv) the fringing backwater-creek system animals with no signiﬁcant trend in their relative of the smaller, saltmarsh-enclosed creeks and channels importance along the gradient (S = 0.31; P = 0.26) that separate the bay’s two large islands (each c. (Fig. 5B). In contrast, the shores of the upper estuary 82–84 ha) from the mainland, together with sites in the and the marine backwater channels were dominated by upper estuary. Separation of the backwaters/upper- epifaunal truncatelloid microgastropods, especially by estuary sites from those along the main axial channel ’Assiminea’ capensis and Hydrobia knysnaensis, epi- was the most marked, with a Bray–Curtis similarity fauna here comprising 64.4% of individuals. Only a between the two blocks of sites of only 20%, and the few subtidal Z. capensis sites have so far been mouth region was an outlier within the axial channel. examined, but such areas are also overwhelmingly The three points of change along the longitudinal axis dominated by an epifaunal microgastropod, here by of the bay, however, were not marked by sharp faunal the cerithioid Alaba pinnae, although the importance contrasts (Fig. 3). Indeed, SIMPER indicates that of this species and hence of the subtidal epifauna in most ([ 50%) of the differences are brought about by general decreases upstream so that epifauna and the relative abundances of just eight common and infauna contribute equally in the upper estuary widespread species, the gastropod molluscs Hydrobia (Fig. 5a). Thus in the bay region there is a transition knysnaensis and ’Assiminea’ capensis (dominant in at some LWS between a burrowing polychaete infauna region iv), Turritella and Alaba (dominant in i), and and a seagrass-leaf-associated gastropod epifauna, and Nassarius (dominant in iii), and the polychaetes although upstream sub- and intertidal faunas are Prionospio (dominant in iii), and Caulleriella and relatively similar, downstream in the bay they are Simplisetia (dominant in ii). Despite statistically markedly different (Fig. 6a). Few data are available to signiﬁcant regionalization, 32% of the species (repre- help explain the great downstream subtidal abundance senting [ 75% of the total individuals) occurred in all of the epifaunal Alaba (a mean density of four regions in more than token quantities (Table 1 -2 28,000 m ), although various studies have suggested lists the more numerous of these shared taxa, and that few ﬁsh consume signiﬁcant numbers of shelled Table 2 displays those characteristic of each region). gastropods, even relatively small ones (McCormick Patterns of relative species abundance within the four 1998; Reynolds et al. 2018), not least because of their regions did not differ (ANCOVA equality of means low nutritive value per unit intake (Vinson and Baker F = 0.17, P = 0.92; equality of slopes F = 0.59, 2008). It is known that in South Africa, mugilids will 123 Aquat Ecol (2021) 55:327–345 333 Table 2 Characteristic Species % Species % intertidal seagrass macrofauna (i.e., those Mouth sandﬂats Marine bay together comprising 75% of Alaba pinnae 21.4 Simplisetia erythraeensis 17.8 the faunal individuals) of Turritella capensis 13.5 Prionospio sexoculata 11.1 the four signiﬁcantly different faunal regions of Simplisetia erythraeensis 9.8 Caulleriella capensis 8.9 the Knysna estuarine bay ?Cylindroleberis sp 7.1 Exosphaeroma hylecoetes 4.5 Orbinia angrapequensis 4.3 Nassarius kraussianus 3.6 Paradoneis lyra capensis 3.6 Melita zeylanica 3.5 Pseudopolydora ?kempi 2.9 Hymenosoma orbiculare 3.4 Diogenes brevirostris 2.9 Danielella edwardsii 3.4 Caulleriella capensis 2.7 Cyathura estuaria 3.1 Nassarius kraussianus 2.6 Grandidierella lutosa 2.4 Paridotea ungulata 1.9 Cymadusa ﬁlosa 2.4 Grandidierella lutosa 1.8 Arcuatula capensis 2.3 Lagoon ? lower estuary tubiﬁcid sp. 2.1 Prionospio sexoculata 27.3 ?Cylindroleberis sp. 2.0 Nassarius kraussianus 15.6 Paramoera capensis 1.9 Arcuatula capensis 10.7 ’Assiminea’ capensis 1.6 Parvulastra exigua 6.0 Alaba pinnae 1.5 Simplisetia erythraeensis 5.3 Backwater channels ? upper estuary Salmacoma litoralis 5.2 ’Assiminea’ capensis 40.0 Cirriformia sp. 2.9 Hydrobia knysnaensis 27.3 Dosinia hepatica 2.7 Halmyrapseudes cooperi 4.1 Simplisetia erythraeensis 3.7 Hydrobia at the backwater site ’A’ in Fig. 1 (R take microgastropods (Whitﬁeld and Blaber 1978; s- Whitﬁeld 1988), but at Knysna mugilids do not = 0.78; P \ 0.00001). Such a parasite/host associa- characterize the dense sublittoral eelgrass beds tion is known from the western Atlantic (e.g., Hershler favored by Alaba (Pollard et al. 2017). Several and Davis 1980), but although the pyramidellid equivalent subtidal areas of seagrass in other conti- concerned is a widely distributed animal, it is other- nents are also dominated by species of Alaba, although wise not recorded from Africa (GBIF 2020). That Knysna is the only known such locality outside the exception apart, however, in a large sample (325 tropics (Barnes and Claassens 2020). These other cores) from the Kingﬁsher Creek seagrass (site 2 in areas are of relatively high salinity which may help to Fig. 1), for example, Barnes (2013b) recorded 75 account for the lesser importance of this gastropod in macrofaunal species at overall and mean densities of -2 and near the upper estuary. Why the same suite of 2581 and 34 m , respectively. Considering the 34 truncatelloid microgastropods dominates the other- relatively common species there that each attained a -2 wise contrasting habitats of the intertidal backwaters mean density of at least 10 m (and together and upper estuary is not known for certain, but their comprised 96% of the total individuals), all pairwise common shelter (see paragraph above) is likely to be correlations of species abundance were very weak to an important component. non-existent (sensu Moore et al. 2018), positives With one exception, no evidence of any strong averaging only P = 0.069 (± 0.060 SD) and nega- species interactions within any given site was forth- tives P = 0.047 (± 0.035 SD); and allowing for the coming. The exception was the positive correlation familywise errors inherent in such a large correlation between numbers of the ectoparasitic pyramidellid matrix (via Bonferroni correction), no negative corre- snail Sayella sp. and those of its probable host lations and only three positive ones were signiﬁcant at 123 334 Aquat Ecol (2021) 55:327–345 Fig. 4 Species abundance diagrams (Whittaker plots) for each of the four faunistically distinct assemblage types Table 3 Uniformity of number of intertidal species per sample index of spatial homogeneity (I ), with signiﬁcance of I tested a p at different scales across test areas of (A) 0.2 ha and (B) 1.5 ha by Monte Carlo simulation (data from Barnes, 2013b, 2016 and at Site 2 and (C) along a 350 m transect at site 9, as assessed by Barnes and Hendy, 2015a) Lloyd’s index of patchiness (I ) and the Azovsky et al. (2000) Unit sample size Lloyd’s I Azovsky et al.’s I Signiﬁcance of uniformity p a 0.0015 m 0.948 0.977 P = 0.1 0.0027 m 0.938 0.988 P = 0.03 0.0054 m 0.933 0.995 P = 0.004 0.0095 0.962 0.995 P = 0.009 0.0054 m 0.974 0.997 P = 0.005 0.0054 m 0.929 0.994 P = 0.01 a critical a of \ 0.05 (between the polychaetes older literature) from the majority of the system, Simplisetia and Caulleriella, Glycera and Cirriformia, faunal relationships between seagrass and bare sedi- and between the polychaete Prionospio and the ment at Knysna are not the classic one of seagrass gastropod Nassarius). Equivalently, although qualita- supporting the greater number of species and of tive co-occurrence patterns across the whole of the individuals per unit area (Hemminga and Duarte 2000; marine-inﬂuenced embayment at Knysna show deter- Pillay et al. 2011; Hyman et al. 2019, etc.). To date ministic structuring (Barnes and Elwood 2011), as studies have only concerned the outer marine embay- indeed might be expected granted the location of the ment, but there seagrass macrofauna at a given site is sampled sites in three distinct faunal regions (sandy more similar to those occurring in adjacent areas of mouth, marine bay, and backwater system), syntopic bare sediment than either habitat is to other areas of the species within a single one of those regions did not same type in the general region [Bray–Curtis faunal differ from random co-occurrences (Barnes and Bar- similarity between the two contiguous habitat types nes 2014b). being a mean 0.58, whereas within-habitat-type sim- In the absence of strong bioturbators such as ilarity averaged 0.26 for the seagrass and 0.25 for the Kraussillichirus kraussi (Callianassa kraussi in the bare sediment (ANOVA F = 5.05; P \ 0.05)] (see 1,14 123 Aquat Ecol (2021) 55:327–345 335 Human et al. (2016). In these circumstances, the former seagrass sites clustered together, as did the same areas when de-vegetated, although macrofaunal abundance was again signiﬁcantly lower in the former seagrass than it was in the replacement bare sediment (in a ratio of 0.62: 1) and again largely because of an increased number of polychaetes and decreased num- ber of crustaceans in the unvegetated sediment (Bar- nes 2019a). Knysna’s marine embayment forms a natural harbor, has been in the past a busy port (Grindley 1985), and today supports several marinas, and hence it is one of the centers of ship-borne alien immigrant species in South Africa (Grifﬁths et al. 2009). Alien species of Boccardia, Polydora, Dipolydora, Pseu- dopolydora, Diopatra, Capitella, Desdemona, Eric- thonius, Jassa, Monocorophium, Paracerceis, Elysia, Favorinus and Indothais all form part of its seagrass fauna, as do amphipods such as Cymadusa ﬁlosa, Melita zeylanica and Americorophium triaeonyx that are regarded by Robinson et al. (2005) and Mead et al. (2011) as being cryptogenic—to which could presum- ably be added Victoriopisa chilkensis. Relatively recently, these aliens have been joined by more northerly species spreading southward probably as a result of global warming. Smaragdia souverbiana, for example, is now a member of the subtidal seagrass fauna (Barnes and Claassens 2020). In the Knysna Fig. 5 Relative importance of infauna and epifauna in a the intertidal, Melanoides tuberculata has arrived and different intertidal and subtidal regions of the estuarine bay and joined Cerithidea decollata (Hodgson and Dickens b at each of the sites along the longitudinal axial channel 2012) and Austruca occidentalis (formerly Uca annulipes) (Peer et al. 2015), the latter two in the adjacent saltmarsh or at the seagrass/saltmarsh Fig. 6b). In general, seagrass beds supported lower, not higher, levels in half the metric comparisons in interface. which there was a signiﬁcant difference (Barnes and Barnes 2014a). Overall, faunal abundance was lower Patterns in assemblage metrics along the axial gradient in seagrass in the ratio of 0.64: 1, while species density was indeed higher, but only by 1.13 to 1, with in large As would be expected, the number of species at the 17 measure the higher numbers in the unvegetated sediments resulting from a quadrupled abundance of sites that were spaced along the system’s longitudinal axis decreased with distance upstream (S = -0.82; infaunal polychaetes, maybe because of the greater P \ 0.0001; Fig. 7a), but the form of the decrease in volume of available sedimentary habitat in the absence of eelgrass rootmass, although numbers of epifaunal species density suggests the occurrence of a step change within the general area of the lower estuary, crustaceans were 15 times less there (from a much smaller base). The same overall effect was not the with the downstream sites showing a considerable degree of uniformity of species density (Fig. 7b; case, however, in bare areas created by the death of seagrass following blanketing by the chlorophyte Table 4). The points in Fig. 7 are based on the whole available 12-year dataset, and hence, the location of blooms described by Allanson et al. (2016) and faunal and regional boundaries will have been blurred 123 336 Aquat Ecol (2021) 55:327–345 Fig. 6 nMDS plots based on Bray–Curtis similarities between channel (site 1) into the backwater Steenbok Channel and its percentage species composition data: a at four sites in the tributaries, showing similarity between macrofaunal assem- Knysna estuarine bay, one in each faunal compartment, showing blages in seagrass and in adjacent areas of bare sediment (from the similarity between macrofaunal assemblages of seagrass at data in Barnes and Barnes 2014a). Envelopes enclose sites at the LWS in the intertidal zone and in the adjacent subtidal area stated levels of Bray–Curtis similarity, and site codes are those (from data in Barnes and Claassens 2020), and b at three sites in given in Fig. 1, plus in (A) an additional site, ’X’, located the marine embayment forming a transect from the main between sites 1 and 2 Fig. 7 Change in number of seagrass macrofaunal species along the longitudinal axis of the estuarine bay a. Note in b the apparent break between sites 10 and 11, corresponding to the one in the same area shown by Barnes and Ellwood (2012) by temporal shifts, but an individual survey of also would be expected, the total fauna contained in macrofaunal animals along the axial channel in 2012 each is considerably in excess of that at any individual showed an almost identical (and sharper) feature site. (Barnes and Ellwood 2012) in the same general Assemblage abundance per unit area (S = -0.35; location. Comparison of data across different spatial P = 0.16; Fig. 8a) and patchiness in assemblage scales shows that decline upstream in number of abundance (S = -0.20; P = 0.45; Fig. 8b), however, species when assessed per site (Fig. 7) is greater than showed no signiﬁcant change with distance upstream; when assessed per region (Table 4): Clearly, the bay indeed, degree of patchiness along the axial gradient and lagoon ? lower-estuary regions are large and, as was signiﬁcantly unchanging (Barnes 2019b). Neither 123 Aquat Ecol (2021) 55:327–345 337 Table 4 Biodiversity metrics of the various intertidal faunal functional categories as per Macdonald et al. (2010) and regions of Knysna estuarine bay: Mao tau species density (N ), Barnes and Hendy (2015a)]. Each axial regional metric is with Chao 2 estimations; N and N species diversity; based on the common sample size of 180 9 0.0054 m cores, 1 2 equitability of species abundance (J); taxonomic diversity (D) yielding some 90% of the likely total species; backwaters * 2 and distinctness (D ); and N functional diversity (F ) [with metric based on 148 9 0.0054 m samples. Peak values in bold 2 d Mouth Bay Lagoon ? lower estuary Upper estuary Backwaters Mao tau N density 94 78 72 34 59 Chao 2 N 104 84 76 38 63 N diversity 21.3 23.5 14.8 9.8 5.5 N diversity 10.9 13.1 8.1 7.8 3.1 J equitability 0.68 0.73 0.61 0.65 0.42 D diversity 4.09 4.25 3.89 3.75 2.45 D distinctness 4.54 4.50 4.72 4.32 3.61 F diversity 7.56 8.38 5.13 4.77 1.64 was there any signiﬁcant relationship between number General discussion and conclusions of species per site and overall assemblage abundance The most striking feature of the Knysna intertidal there (S = 0.43; P = 0.08). However, signiﬁcant relationships have been found between how patchy seagrass-associated macrobenthos is its relative spatial uniformity. Macrofaunal abundance does not vary an individual species is and its occupancy and, to a lesser extent, its abundance: The more abundant and markedly along the longitudinal axis, neither does patchiness of macrofaunal density. Number of species widespread the species, the less its patchiness, both in subtidal and in intertidal seagrass (Barnes per unit area at a given site is a constant, while species 2019c, 2020), and both in interspeciﬁc comparisons density along whole sections of the gradient can be (Barnes 2020) and intraspeciﬁcally (Barnes, in prep.) relatively uniform, and its fauna appears to form a (Fig. 9). This suggests that the well-known macroe- single assemblage with only local variation in relative cological abundance-occupancy pattern (e.g., He and frequency of its dominant components. Even the Gaston 2003) can be extended into a patchiness- subtidal fauna does not differ qualitatively from the intertidal one, although there are marked quantitative abundance-occupancy one, at least in this habitat type. As can be seen in Fig. 9, the slopes of the power laws differences and overall it is much more abundant especially in the most marine-inﬂuenced regions relating logit occupancy to log patchiness in individual species are much more variable than those interspecif- where Alaba dominates (Barnes and Claassens 2020). Admittedly, being a marine-dominated system ically in the different faunal regions; thus, while the interspeciﬁc occupancy-patchiness slopes represent- with under normal circumstances relatively little ing different regions do not differ (ANCOVA F = 1.3, freshwater input (Day et al. 1951), for an estuarine P = 0.3), the equivalent intraspeciﬁc slopes are system salinity is relatively constant; however, occa- heterogeneous (ANCOVA F = 4.9, P \ 0.0001) with sional episodes of severe freshwater ﬂooding do occur once every 10–12 years or so, rendering most or all of a further six of the dominants (including the epifaunal Alaba and Cymadusa, and infaunal Caulleriella and the system temporarily fresh (see, e.g., Korringa 1956; Blake and Chimboza 2010). But, although sea water Salmacoma) not showing signiﬁcant occupancy- patchiness relationships at all. This also indicates that may penetrate far upstream and dominate most areas, there is much change along the Knysna axis in other disparate species together form assemblages with similar properties in the various regions. There were features of direct relevance to macrobenthos, as in no discernable trends in either metric upstream, transitional paralic systems in general (Tagliapietra although the upper estuary did display the largest et al. 2012;Perez-Ruzafa et al. 2019). Sediment value of both b and R . changes from clean sand at the mouth, to soft organic mud in the lagoonal and lower estuarine regions, and 123 338 Aquat Ecol (2021) 55:327–345 Fig. 8 Relative constancy of intertidal seagrass macrofaunal patchiness (data from Barnes 2019b). b(ii) illustrates spatial -2 assemblage metrics along the longitudinal axis of the estuarine variation in macrofaunal density 0.01 m across an area of site bay: a assemblage abundance, with an inset showing abun- 2 (from data in Barnes 2016) dances at the six backwater-channel sites; and b(i) assemblage to mud with admixed riverine gravel in the upper exposure (den Hartog 1970; Adams and Talbot 1992); estuary (Day et al. 1951); shelter changes both as the and so on. estuary narrows and on transition from axial channel Being located at 34S, Knysna lies within the into backwater creeks (Day 1967); and shore proﬁles narrow mid-latitude belt recently identiﬁed by Whalen change from extensive tidal ﬂats near the mouth to et al. (2020) as that displaying peak intensity of animal narrow steep slopes in the estuary supporting only food consumption and hence potential top-down linear strips of seagrass (Day 1967; Maree 2000). control of prey species. Like other South African Rates of water exchange vary along the channel estuarine areas supporting dwarf-eelgrass (Whitﬁeld (Largier et al. 2000); characteristic density and shoot et al. 1989; Nel et al. 2018), it is a nursery area for length of the eelgrass change with shore height and many nektonic species (Whitﬁeld and Kok 1992), 123 Aquat Ecol (2021) 55:327–345 339 Knysna’s seagrass macrobenthos become more understandable. Three lines of evidence suggest that across the whole system seagrass macrofaunal abundance is below carrying capacity and not structured by density- dependent factors. First, the prevailing intertidal density along the longitudinal axis of some -2 2 4,000 m is very low compared to the [ 40,000 m animals occurring in similar intertidal dwarf-eelgrass beds in cool-temperate Europe (Blanchet et al. 2004; Barnes and Ellwood 2011; etc.) where predator rates are almost certainly lower on a fauna of similarly sized animals that are often members of the same families as represented at Knysna (Barnes and Hendy 2015b). Secondly, constancy of number of species per unit area, as demonstrated at the Kingﬁsher Creek site at Knysna (Barnes 2013b), is exactly what would be expected were the various species to be distributed independently of each other (granted their overall frequencies of occurrence) (Barnes and Barnes 2014b). Such independence of distribution is likely only if the whole assemblage is being maintained below the level at which species would otherwise interact. Thirdly, the large quantitative dataset of Barnes (2013b) from the same Kingﬁsher Creek site also showed that there were very few signiﬁcant correlations (0.5%) between the abundances of pairs Fig. 9 The power laws (y = ax ) describing signiﬁcant of species and all those were very weak. Moreover, as relationships between log Lloyd’s I patchiness and logit seen elsewhere, for example within Paciﬁc Canadian occupancy in the seagrass macrofauna of Knysna estuarine Zostera marina meadows (Stark et al. 2020), weak and bay, both a interspeciﬁcally in the different assemblage types and b intraspeciﬁcally in individual dominant species very weak positive relationships greatly out-numbered negative ones, further suggesting the lack of compet- itive interspeciﬁc interactions. In such overall circum- schools of juvenile ﬁsh being a common sight in its stances of low and unpredictable density of potential invertebrate prey species, predators could thus be seagrass beds. Indeed, seagrass beds have been regarded as one the most important types of coastal expected to have to forage optimally (Beseres and nursery (Whitﬁeld 2017; Lefcheck et al. 2019), both Feller 2007) and to graze down local prey stocks to because of the food they provide (Whitﬁeld 2017) and threshold levels before moving and repeating the as refuge from larger ﬁsh predators (Whitﬁeld 2020a). process elsewhere, and having reduced their food If, as is generally held to be the case in seagrass stocks to low levels over wide areas could themselves (Moksnes et al. 2008; Lewis and Anderson 2012; then experience food limitation (Saulnier et al. 2000). The actions of such predators roaming widely over the Duffey et al. 2015, etc.), the effect of this consump- tion, together with that exerted by adult ﬁsh (Pollard surface might also help explain the uniform levels of macrofaunal patchiness characterizing large areas et al. 2017) and predatory members of the invertebrate macrobenthos, is top-down control of the seagrass (Barnes and Hamylton 2019). A second process that could help account for the microphytobenthic-bioﬁlm consumers that dominate both epifauna and infauna, then many of features of observed features of the Knysna macrobenthic assem- blages, and particularly their relative uniformity along the longitudinal axis, is if the presence of the seagrass 123 340 Aquat Ecol (2021) 55:327–345 Fig. 10 Destructive effects of bait-collecting activities on by such mudprawn pushing; and c, the resultant plugs scattered intertidal seagrass habitat in the ’no-take bait sanctuary’ section over the seagrass surface; d, an area of seagrass destroyed by of the Knysna estuarine bay: a The hole and jettisoned plug trenching for bait worms (from Barnes and Claassens 2020) created by pushing for mudprawn; b, a substratum pock-marked ameliorates variation in the local ambient microcli- Claassens et al. (2020), and the two that might matic conditions, as a macro-algal cover has been particularly affect the seagrass and its inhabitants are shown to do (Scrosati 2017; Monteiro et al. 2017). uncontrolled bait harvesting by destructive means and Within the relatively uniform and stable conditions chlorophyte blooms. Bait harvesting by ’pushing’ for provided by the Z. capensis bed, species can penetrate mudprawns (Upogebia capensis) and trenching for upstream further than they might otherwise be able to worms (Marphysa, Polybrachiorhynchus and Areni- do (Barnes and Ellwood 2012). Seagrass beds and cola spp.) is rife in Knysna (Simon et al. 2019), even other structurally complex systems (Hyman et al. (and arguably especially) in the formally protected 2019) generally appear to support macrofaunal assem- bait-reserve area (Fig. 10) that also supports 79% of blages that display spatial and temporal stability of the estuarine bay’s seagrass-associated species. Unfor- abundance and composition, and high levels of tunately, there are immense logistic and social prob- resilience (Whanpetch et al. 2010; Blake et al. 2014; lems associated with preventing illegal and restricting Gartner et al. 2015), and this may have important legal bait harvesting in southern Africa, especially in knock-on effects on the whole local coastal food web areas of high unemployment where subsistence ﬁshing (Jankowska et al. 2019). provides the main or only source of protein (Bandeira Granted the current high loss rates of seagrass and Gell 2003; Napier et al. 2009) and the local throughout the world (Waycott et al. 2009; Short et al. intertidal provides the only source of bait (Barnes and 2011) and of Zostera capensis in southern Africa Claassens 2020). Subsistence harvesting at Knysna is (Adams 2016), an important question is the implica- worth some ZAR 1 9 10 (Turpie 2007). Its precise tion of the operation of such potential structuring effect on the seagrass macrofauna is unknown; factors at Knysna for the future of its important however, basically because the extent of harvesting seagrass system. Threats to the health of Knysna means that a like-with-like, harvested versus unhar- estuarine bay have recently been reviewed by vested, comparison is not possible: No area of 123 Aquat Ecol (2021) 55:327–345 341 intertidal seagrass remains un-pushed or un-pumped. ([ 30% of the saltmarsh has already gone, and 25% At other localities, however, it and the associated of that remaining is under threat). Thus far, at least, it trampling are known to have severe consequences has managed to fare better than many other South (e.g., Pillay et al. 2010; Garmendia et al. 2017; Short African estuarine systems (van Niekerk et al. 2013), et al. 2011; Adams 2016). Nevertheless, the inherent and it may yet continue to do so. resilience and spatial uniformity of the Knysna Acknowledgements I am most grateful to SANParks area seagrass beds referred to above, together with the fact ofﬁce, Knysna, and SANParks Scientiﬁc Services, Rondevlei, that they form one large interconnected system with for permission to conduct research on the Knysna system over dispersal possible between all sections, does offer the last decade or so; to Rhodes University Research Committee hope. for their support; to my collaborators at various times, sequentially Farnon Ellwood, Morvan Barnes, Ian Hendy and In respect of the second major threat, at the moment Louw Claassens, for their contribution to the study; to Brian the problems of eutrophication, to which Z. capensis is Allanson for his copious encouragement and support; and to an known to be sensitive (Mvungi and Pillay 2019), and anonymous reviewer for saving me from error. consequent algal blooms are only local, affecting mainly the backwater channels into which the munic- Author contributions RSKB conceived, designed, and executed this study and wrote the manuscript. No other person ipal sewage treatment plant discharges and in which is entitled to authorship. there is a legacy of organic matter retention (Human et al. 2020). Knysna’s large tidal prism proves Funding No funding was received for conducting this study. invaluable insofar as minimizing blooms in the main axial channel is concerned. But the local effect of the Data availability and material Datasets on which these analyses are based have been lodged in electronic format in the chlorophyte blanket is dramatic and destructive. Rondevlei Ofﬁce of SANParks Scientiﬁc Services (http:// Animal numbers may increase on its seasonal dieback, dataknp.sanparks.org/sanparks/metacat/Nerinak.23.11/ except in the very local areas of anoxia, although this sanparks) and are available on request. increase is almost entirely conﬁned to densities of the Compliance with ethical standards dominant polychaete groups (except, for some reason, cirratulids) (Barnes 2019a). Crustaceans do not Conﬂict of interest The author declares no conﬂict of interest. bounce back so readily, and as they provide the food for most ﬁsh in the nearby Swartvlei Estuary (Whit- Consent for publication The author consents to publication. ﬁeld 1988, 2020b) and presumably therefore do so at Ethical approval All applicable international, national, and/ Knysna, the ﬁsh populations may suffer the conse- or institutional guidelines for sampling, care, and experimental quences: There is some evidence that this is indeed the use of organisms for the study were followed, and all necessary case (Pollard et al. 2018). The chlorophyte problem is permissions and approvals were obtained in respect of the soluble (no pun intended) but at considerable cost (see original collections of the data. Human et al. 2020). The ﬁnancial reward, however, Open Access This article is licensed under a Creative Com- might also be large, not least because such blooms mons Attribution 4.0 International License, which permits use, impact on tourism (Boesch et al. 1996) and tourists sharing, adaptation, distribution and reproduction in any med- contribute some ZAR 1 9 10 per annum to the ium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Knysna economy (Turpie 2007). Commons licence, and indicate if changes were made. The Knysna is perhaps not a typical South African images or other third party material in this article are included in estuary in being permanently open (see van Niekerk the article’s Creative Commons licence, unless indicated et al. 2020), without a signiﬁcant presence of Kraus- otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your sillichirus, and with a subtidal dominated by the little- intended use is not permitted by statutory regulation or exceeds known Alaba pinnae, but nevertheless its fauna the permitted use, you will need to obtain permission directly generally appears to be the classic Cape estuarine from the copyright holder. To view a copy of this licence, visit one (Day 1981; de Villiers et al. 1999); indeed, it http://creativecommons.org/licenses/by/4.0/. supports [ 40% of South African estuarine biodiver- sity. 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Patterns of seagrass macrobenthic biodiversity in the warm-temperate Knysna estuarine bay, Western Cape: a review

Patterns of seagrass macrobenthic biodiversity in the warm-temperate Knysna estuarine bay, Western Cape: a review

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Patterns of seagrass macrobenthic biodiversity in the warm-temperate Knysna estuarine bay, Western Cape: a review

Patterns of seagrass macrobenthic biodiversity in the warm-temperate Knysna estuarine bay, Western Cape: a review

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