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Hydrobiologia

, Volume 827, Issue 1, pp 293–307 | Cite as

Spatial structure of a multi-species guild: the dominant biofilm-grazing microgastropods of seagrass

  • R. S. K. Barnes
Primary Research Paper

Abstract

Although all-too-often ignored ecologically, gastropods < 5 mm in largest dimension may be dominant aquatic assemblage components. In Moreton Bay, Australia, for example, intertidal seagrass supports a guild of 24 such biofilm-grazing species at mean density one-third that of the whole macrobenthic seagrass assemblage. Detailed spatial patterns of the 14 guild members at one c. 1 ha locality were investigated via a 256-station lattice. Relative importance of the guild within the macrobenthic assemblage as a whole was spatially uniform but its abundance was significantly patchy at all spatial scales—a few stations supporting up to 170 times background levels of some species—and guild patchiness showed a relatively constant magnitude across those scales. Patches of individual species were independently distributed, showing no evidence of negative inter-specific interactions, the few significant spatial correlations between species being very weak and positive. Levels of syntopy (up to six species within a 0.0054 m2 area) did not differ from those expected under null models of independent assortment. Although diverse, overall guild abundance was low, appearing well below potential carrying capacity, and dominated by few species. Power–law relationships suggested temporal stability of these patterns. Possible causes of such guild structure are discussed.

Keywords

Competition Macrobenthos Marine Mollusc Patchiness 

Introduction

Very small gastropods (‘microgastropods’ < 5 mm in largest dimension) numerically dominate the soft sediments of many of the world’s aquatic systems (Sasaki, 2008; Strong et al., 2008; Barnes, 2010; Middelfart et al., 2016). One such microgastropod-dominated habitat is intertidal seagrass on clastic sands and muds, whether in the cool temperate zone (e.g. Blanchet et al., 2004; Barnes & Ellwood, 2011), the warm temperate zone (Barnes, 2017a), or into the subtropics (Barnes, 2017b); though not it would seem those on tropical calcareous coral sands (e.g. Klumpp & Kwak, 2005; Barnes, 2010). Like the majority of very small animals, however, microgastropods are poorly known and usually systematically problematic. In considerable measure, this is consequent on a taxonomy and a general understanding for a long time based solely on their shells, notwithstanding that (a) convergent evolution has often led markedly dissimilar animals to produce very similar shells (Fukuda & Ponder, 2003; Bichain et al., 2007; Criscione & Patti, 2010; Scuderi & Amati, 2012; etc.) and (b) shells of tiny species are often simple, unornamented and particularly convergent (Davis, 1979; Hershler & Ponder, 1998). Hence, in marked contrast to the attention usually given to the ecology of larger prosobranchs, with the exception of northern-hemisphere hydrobiid mud-snails (e.g. Araújo et al., 2015) marine microgastropods have in the past often been ‘ignored or grossly underestimated’ (Bouchet et al., 2002, p. 422; Albano et al., 2011; Golding, 2014) and when reported have often been misidentified (Barnes, 2017a).

In comparison to many other areas, however, the microgastropods of eastern Australia have received much recent attention at least in terms of their systematics and phylogeny (e.g. Ponder, 1984; Strong et al., 2011; Criscione & Ponder, 2013; Wilke et al., 2013; Golding, 2014; Criscione et al., 2016). Illustrated guides to several elements of the New South Wales microgastropod fauna are even available (Ponder et al., 2000; Beechey, 2017). Nevertheless, although laboratory and museum studies of anatomy and relationships have greatly extended our knowledge of these species, with the exception of those in coralline algal turfs (e.g. Olabarria & Chapman, 2001, 2002; Olabarria et al., 2002; Kelaher, 2003) still virtually nothing is known of them in life, beyond statements of habitat data such as ‘on seagrass in estuaries, sheltered bays and coastal lagoons in lower littoral and shallow sublittoral’ (Ponder et al., 2000). The < 2.5 mm truncatelloid Calopia imitata Ponder, 1999 exemplifies our failure to appreciate microgastropod importance. Although museums have been housing its material dating back over a century and it is now known to occur along the entire seaboard of eastern Australia, i.e. over at least 29° of latitude (Hallan et al., 2015), the species only became known scientifically in 1999 (Ponder, 1999). However, only in the last decade, it has become apparent that it is one of the most numerous and widespread animals through much of southern Moreton Bay, Queensland, occurring over large areas in densities of up to some 850 m−2 (Rachello-Dolmen et al., 2013a; Barnes, 2017b).

Surveys of the seagrass-associated macrobenthos in one limited area of Moreton Bay (summarised in Barnes, 2017b) have disclosed the occurrence of some 40 microgastropod species, and since their identities are now relatively well established (at least at the genus level), it has become possible to investigate what processes structure this abundant, species-rich and probably ecologically important guild, and by extension other such multi-species associations of presumed ecologically equivalent animals. Specific guild-related hypotheses that are tested here include: whether the component species are truly syntopic (in the sense of apparently coexisting within the same very small area) or are merely generally sympatric (in the sense of occurring in the same habitat type); whether their distribution and abundance patterns display evidence of inter-specific competition; whether spatial peaks and troughs in the abundance of different species tend to cancel each other out creating a guild of relatively uniform overall abundance; and whether the relative importance of the guild varies spatially.

In Moreton Bay, such seagrass-associated microgastropods fall into two distinct feeding categories: (i) ectoparasites of polychaetes and other molluscs, and (ii) grazers of biofilms (Beesley et al., 1998; Rachello-Dolmen et al., 2013b). Very little indeed is known of the biology of the first category, and hence the present study was restricted to the latter one, itself a diverse assemblage of members of six different prosobranch superfamilies. Because it largely consumes the seagrass itself (Rossini et al., 2014), Smaragdia souverbiana Montrouzier, 1863 was excluded, as were < 5 mm juveniles of sympatric larger macrogastropods such as Calthalotia, Monilea, Monetaria, Cerithium, Batillaria, Nassarius and Tritia that are known to be feeders on algae or ‘detritus’ or to scavenge when adult.

Materials and methods

Spatial distribution of the seagrass microgastropod guild was studied over a period of 10 weeks during the 2017 austral spring at a site at the southern end of the Rainbow Channel coast of North Stradbroke Island (a.k.a. Minjerribah) within the relatively pristine Eastern Banks region of the subtropical Moreton Bay Marine Park, Queensland (Dennison & Abal, 1999; Gibbes et al., 2014) (Fig. 1). The lower half of the intertidal zone of this coast supports meadows dominated by the dwarf-eelgrass Zostera (Zosterella) capricorni Ascherson, 1876 [Nanozostera capricorni in the recent revision of the Zosteraceae by Coyer et al., 2013] plus some Halophila ovalis (Brown, 1810) and Halodule uninervis (Forsskål, 1775) (Young & Kirkman, 1975; Abal et al., 1998). The precise site investigated, centred on 27°30′26″S,153°24′30″E in Deanbilla Bay, was a c. 125 × 200 m block of visually uniform seagrass bed occurring from some mean low-water neap tide level down to an unvegetated sand bar at low-water spring aligned parallel to the shoreline, the seagrass continuing sublittorally beyond the bar. As is typical in such conditions, the dwarf-eelgrass plants were of the small morphological forms characteristic of shallow periodically exposed areas (Young & Kirkman, 1975), many leaves being < 10 cm long. The substratum was basically fine- to medium-grained, well-rounded, silica sand, with sedimented silt, organic detritus and some coarser material.
Fig. 1

Location of the study, showing the general area of the Rainbow Channel coast investigated and the position of the specific Deanbilla Bay site

To represent the area without spatial bias, samples were arranged in a 16 × 16 square lattice with columns and rows a unit 5.75 m apart (c. 0.2″ of latitude and longitude), which, for ease of geospatial referencing, was oriented at c. 25° off alignment with the long axis of the shore. As most benthic seagrass macrofauna are known to be located within the top few cm of sediment [e.g. 98% in the top 5 mm in the study by Klumpp & Kwak (2005) at other sites in Queensland], individual samples were in the form of a core with a spatial grain of 0.0054 m2 and a depth of 100 mm. Collection and treatment of core samples followed the same procedure as in earlier studies of macrobenthic assemblages associated with dwarf-eelgrass beds both within the North Stradbroke intertidal (e.g. Barnes & Hamylton, 2015; Barnes, 2017b) and elsewhere (e.g. Barnes, 2013, 2016). Cores were collected just before tidal ebb when the areas of the bed concerned were still covered by some 2–5 cm of water, and were gently sieved through 710-µm mesh on site, this mesh size being a compromise between not retaining too much coarse material (particles > 500 µm being particularly abundant at Deanbilla Bay) and capturing a representative array of organisms the size of microgastropods. Retained material from each core (i) was placed in a large polythene bag of seawater within which all seagrass was shaken vigorously to dislodge all microgastropods and then discarded; (ii) was then re-sieved and transported immediately to a local laboratory, and (iii) was then placed in a 30 × 25 cm white tray on an A3 LED board in which living animals were located by visual examination using 3.5× magnifying spectacles. After identification and counting, all animals were returned alive to the seagrass. All organismal nomenclature is as listed in the World Register of Marine Species (www.marinespecies.org) in June 2018.

These 2017 data were analysed in terms of spatially referenced distributions, the occurrence of correlations between the abundance patterns of the various component species, and dispersion patterns across hierarchically nested spatial scales. Following Hurlburt (1990), spatial dispersion of abundance was assessed by Morisita’s original (1959, 1962) procedure, rather than by Smith-Gill’s (1975) standardised version. This is effectively identical to the Lloyd (1967) index advocated by Payne et al. (2005) and Rindorf & Lewy (2012). Statistically significant heterogeneity (patchiness) was tested by one-sided upper-tail χ2 (Morisita, 1962). In this respect, Hoel (1943) has demonstrated that tests of significance using the χ2 distribution can break down when mean values of a dataset are < 5 (Diggle, 1983, sets the lower limit at 4), as were the numbers of each individual species at the smallest areal scale reported here. There is little problem when the test distribution is Poisson, but it can be more severe when it is binomial, leading to a much greater chance of Type II errors in upper-tail tests. Hoel (1943, p. 162) concluded that therefore results from binomial distributions ‘must be handled carefully in such situations’. Granted the actual values of χ2 obtained here for datasets where m = <  4–5, however, such failures to detect significant cases of patchiness where they do exist were only the possible issue in respect of Tricolia (see below), and any such potential analytical problems disappeared at larger spatial scales of analysis. Correlation analyses used non-parametric Spearman’s ρ, and relative importance of individual species in the guild was assessed by the Barnes (2014) index of numerical importance that combines information on both their abundance and occupancy (= percentage frequency of occurrence). The null hypothesis of syntopic species density at any point not differing from that expected as a result of independent assortment (‘random placement’) was tested by the method of Barnes & Barnes (2014) using the Kolmogorov–Smirnov test.

Additional data on overall seagrass microgastropod abundance and biodiversity in the general Rainbow Channel area, collected each year over the period 2009–2016 during austral-spring sampling of seagrass macrofauna, were also extracted from the databases underlying the author’s earlier series of papers on seagrass spatial ecology (see Barnes, 2017b) and cumulative species lists and mean abundances were derived. These extended the total area under study to the landward interface with mangrove near mean sea level and to the equivalent interface with the bare sandflat referred to above, and over a distance along the shore of 7 km (Fig. 1).

Results

Overall 2009–2016 patterns of guild composition and abundance

Over the earlier period 2009–2016 as a whole, the biofilm-grazing microgastropod guild in the Rainbow Channel intertidal seagrass comprised a mean value of some 34% of the whole seagrass macrobenthic total of 2500 ind. m−2. Overall the guild was represented by a total of 24 species belonging to 13 different families (Table 1), although just one species, Calopia imitata, contributed 66% to guild numbers, having a density > 5.5 times that of its nearest rival and with an equivalent occupancy > 4 times greater, occurring right throughout the seagrass beds into their boundary zones with both adjacent bare sediment and with mangrove pneumatophores near mean sea level. Pseudoliotia (present in the form of three species) and Circulus were the next most abundant, but even together these four tornids achieved less than half the numbers and occupancy of Calopia (Table 1). The Calopia, Pseudoliotia and Circulus species together comprised 94% of total guild members. Ranking the species by their relative contribution to the assemblage’s total numerical importance produced a reasonable approximation to an exponential decline (R2 = 0.96) for all but the overwhelming dominant Calopia, so that several species had a very low expectation of being encountered (≤ 1 in 1000 core samples) (Fig. 2). The experience of Bouchet et al. (2002) suggests that others will not have been sampled at all. Some 35 + other gastropod species were also recorded in the seagrass with those under consideration here, including 14 in the same size range, i.e. Smaragdia, Cornirostra and the largely ectoparasitic pyramidelloids, murchisonelloids and Sticteulima.
Table 1

Overall density and occupancy of 22 species of biofilm-grazing microgastropod occurring within the intertidal seagrass beds from 27°27″57″S to 27°30′35″S along the Rainbow Channel coast of North Stradbroke Island, Moreton Bay [n.b. two further species—Stenothyra australis Hedley, 1901 (Stenothyridae) and Wakauraia fukudi Golding, 2014 (Iravadiidae)—occurred in the marginal zones of seagrass beds only where immediately adjacent to mangroves]

 

Density (m−2)

% Occupancy

Calopia imitata (Calopiidae)

631.7

73.9

Pseudoliotia speciosa (Angas, 1871) (Tornidae)

112.2

14.7

Pseudoliotia micans (Adams, 1850) (Tornidae)

99.9

18.4

Pseudoliotia axialis Laseron, 1958 (Tornidae)

28.1

5.1

Circulus cinguliferus (Adams, 1850) (Tornidae)

27.6

4.4

Tricolia fordiana (Pilsbry, 1888) (Phasianellidae)

18.0

8.2

Alaba difformis (Laseron, 1956) (Litiopidae)

15.4

7.3

Lucidestea nitens (Frauenfeld, 1867) (Rissoidae)

8.9

3.6

Elachisina sp (Elachisinidae)

3.0

1.4

?Cyclostremiscus sp (Tornidae)

2.2

1.8

Finella fabrica (Laseron, 1956) (Scaliolidae)

2.0

1.0

Voorwindia umbilicata Ponder, 1985 (Rissoidae)

1.8

1.0

Nozeba topaziaca (Hedley, 1908) (Iravadiidae)

1.5

0.7

Diffalaba opiniosa Iredale, 1936 (Litiopidae)

1.3

0.6

Cerithidium diplax (Watson, 1886) (Cerithiidae)

1.3

0.5

Iravadia goliath (Laseron, 1956) (Iravadiidae)

0.6

0.3

Scaliola ?bella Adams, 1960 (Scaliolidae)

0.6

0.2

Alvania novarensis Frauenfeld, 1867 (Rissoidae)

0.6

0.2

Diala semistriata (Philippi, 1849) (Dialidae)

0.2

0.1

Neripteron violaceum (Gmelin, 1791) (Neritidae)

0.2

0.1

Eatonina sp (Cingulopsidae)

0.2

0.1

Vitrinella sp (Tornidae)

0.2

0.1

The 14 species in bold were present at the Deanbilla Bay site in 2017

Fig. 2

The relationship between relative importances of the component species of the biofilm-grazing microgastropod guild in intertidal seagrass beds of the Rainbow Channel coast of North Stradbroke Island, Moreton Bay, Queensland

Detailed patterns in Deanbilla Bay in 2017

Fourteen members of this local species pool were present within the intensely sampled 0.85 ha study area at Deanbilla Bay in 2017 (Table 1), occurring at a mean density per core of 4.0 ± SE 0.3 (equivalent to 747 m−2) with a maximum of 43 core−1; 16% of samples contained no microgastropods at all (Fig. 3). The whole guild was distributed extremely patchily across all hierarchically nested spatial scales within the studied area (Table 2; Fig. 4a), four contrasting distribution patterns being apparent in the component species. (i) Six species occurred rarely (those of Lucidestea, Cerithidium, Iravadia, Finella, Scaliola and ?Cyclostremiscus), i.e. only as 1–4 individuals in total and as no more than a single individual in any one core. (ii) A further rare species, Elachisina, only occurred at five sites and at four of those as a single individual but at the other it was relatively abundant (five individuals). (iii) Tricolia was distributed thinly and randomly across the whole site (Fig. 4b) (χ2 = 292; df = 255; P = 0.055; see below), never occurring as more than two individuals per 0.0054 m−2 sample; Alaba (Fig. 4c) displayed an equivalent pattern but was significantly patchy (χ2 = 322; df = 255; P = 0.003). (iv) In contrast, as over the general area, species of Calopia, Pseudoliotia and Circulus were more abundant and they showed very patchy distributions (χ2 > 830; df = 255; P ≪ 0.0001), being extremely numerous in some samples (P. axialis Laseron, 1958) up to 8 ind core−1, P. micans (Adams, 1850) up to 14, Calopia up to 17, P. speciosa (Angas, 1871) up to 26 and Circulus up to 37) (Figs. 4d and 5a–d) (at other local sites, Calopia has attained maximum densities of 38 ind. core−1, equivalent to 7000 ind. m−2) but absent from others. Calopia was present at 70% of stations but no other species achieved an occupancy > 20%, the 13 other species averaging only 5%. Comparisons of the variances of their numbers per unit area indicate that P. speciosa, Calopia and Circulus were responsible for 77% of the overall patchiness in guild abundance, and together with P. micans and P. axialis for 86%.
Fig. 3

Range of overall abundance of the biofilm-grazing microgastropod guild per 0.0054 m2 sample at Deanbilla Bay

Table 2

Significant patchiness displayed by the whole biofilm-grazing microgastropod guild across hierarchically nested spatial scales (i.e. blocks of samples) within the 0.85 ha Deanbilla Bay sampling site (Morisita’s χ2 test)

Number of samples in unit block

Notional area represented (m2)

Numbers of sample blocks

χ 2

P

20 samples

33

256

1713

< 0.0001

22 samples

130

64

397

< 0.0001

24 samples

530

16

109

< 0.0001

26 samples

2115

4

13

0.005

Fig. 4

Choropleth diagrams of spatial variation in numbers per 0.0054 m2 sample of various microgastropods in a c. 1 ha intertidal seagrass bed at Deanbilla Bay, I: a the whole biofilm-grazing guild; b Tricolia fordiana; c Alaba difformis; and d Pseudoliotia axialis

Fig. 5

Choropleth diagrams of spatial variation in numbers per 0.0054 m2 sample of various microgastropods in a c. 1 ha intertidal seagrass bed at Deanbilla Bay, II: a Pseudoliotia micans; b Pseudoliotia speciosa; c Circulus cinguliferus (from Barnes & Laurie, 2018) and d Calopia imitata

The mean number of different microgastropod species present in unit 0.0054 m−2 sample was 1.5, with a range of 0–6. The frequency distribution of syntopic species density per sample did not depart from that be to be expected if all species were distributed independently granted their individual overall frequencies of occupancy (Kolmogorov–Smirnov P ≫ 0.2) (Fig. 6). Nevertheless, at the level of individual species pairs, correlation analysis between the numbers per given area of the more common and widespread species suggests that some very weak but nevertheless significant positive relationships did occur, although no negative ones such as might be induced by competitive interactions. Because the four tornid species appear to be very similar animals apart from their shell patterns, and because they and Calopia are the numerical dominants, possible relationships between the co-occurring densities of these species are of particular ecological interest. Weak but significant positive correlations occurred between the numbers of Pseudoliotia axialis and P. speciosa, as well as between those of both Calopia and P. speciosa with Circulus (ρ = + 0.13–+ 0.16; P = 0.035), and a somewhat stronger positive correlation was found between numbers of P. axialis and P. micans (ρ = 0.27; P < 0.0001).
Fig. 6

Range of number of syntopic guild species in individual 0.0054 m2 samples at Deanbilla Bay, both as those observed and as those expected from their overall frequencies of occupancy if distributed independently of each other

Power–law relationships between the 2017 means and variances of the numbers of individual species and of the whole guild across spatial scales fell on the same curves as those displayed by the same species in 2014 (as calculated from the data of Barnes & Hamylton, 2015) (Fig. 7). This suggests relative temporal stability of their patterns of dispersion. The relationship for Tricolia shows a value of Taylor’s power–law exponent β > 1 indicating that it becomes more patchy with increasing analytical area and that the random distribution suggested by Morisita’s χ2 at the smallest scale (i.e. χ2 = 292; df = 255; P = 0.055 above) may not be a Type II error. It is also clear from Fig. 7 that β is effectively unity in the case of Circulus. This demonstrates scale invariance of its patchy dispersion pattern (Barnes & Laurie, 2018). The value of β for the whole guild is also close to one, although overall the degree of patchiness of the microgastropod assemblage appears to show a slight decrease with spatial scale (β = 0.93) but whether this value of β significantly departs from unity cannot be determined.
Fig. 7

Power–law relationships in the Deanbilla Bay seagrass microgastropods [i.e. variance = α meanβ (Taylor, 1961)] in 2014 (circles) and 2017 (squares): a Whole biofilm-grazing guild; b Calopia imitata, Circulus cinguliferus and Tricolia fordiana

Numbers per unit area of the whole biofilm-grazing guild at Deanbilla Bay and especially those of Pseudoliotia speciosa (ρ = 0.41; P ≪ 0.00001) and Calopia (ρ = 0.69; P ≪ 0.00001) were significantly correlated with those of the total seagrass-associated macrofauna (ρ = 0.60; P ≪ 0.00001) (macrofaunal data of Barnes & Laurie, 2018), but not with those of the non-microgastropod species also present (ρ = < 0.05; P = 0.43). The guild comprised a relatively uniform 25.5% of the total faunal individuals in each sample (Standard Error 1.27), a somewhat lower percentage than generally was the case along that coast (see above), possibly in part because of a significant local reduction in the numbers of Calopia from 5.4 to 2.1 ind. core−1 in 2017 compared to Deanbilla Bay in 2011 (Mann–Whitney U; P = 0.007).

Therefore, with respect to the specific questions addressed by this study, in summary: levels of syntopy did not differ from those expected from random placement; species distributions showed no evidence of negative influence of any inter-specific competitive effects, the only significant correlations being weak and positive; and the guild comprised few common but many rare, thinly scattered species, its relative importance in the macrobenthic assemblage being spatially uniform but its abundance being significantly patchy across all spatial scales, with the patches of individual component species distributed independently.

Discussion

It is clear that although microgastropod biodiversity was high within the limited area of seagrass under study, few genera, essentially only two (Calopia and Pseudoliotia), could be described as common and widespread members of the biofilm-grazing guild; most were rare both in terms of abundance and distribution. It is impossible to be certain of the status of Circulus because it is so patchy: although locally highly abundant, since 66% of its observed total numbers were located within 1% of the area sampled, missing one or more such concentrations would radically change overall estimates of its abundance. This pattern of distribution was not confined to 2017 in that in 2014, for example, 79% of Circulus individuals occurred in < 1% of samples (from the database of Barnes & Hamylton, 2015). The description above of Calopia and Pseudoliotia being ‘common’, however, is relative only to their sympatric taxa. Microgastropods, indeed the whole 200 + species of the Deanbilla Bay seagrass macrofaunal assemblage, are not numerous in the Rainbow Channel dwarf-eelgrass relative to those in equivalent intertidal dwarf-eelgrass beds that have been investigated in cooler latitudes. In the intertidal Z. capensis Setchell, 1933 beds of the warm-temperate Knysna estuarine bay in South Africa, for example, there are fewer microgastropod species (only three) but numbers can locally be  more than 30 times greater than on North Stradbroke (Barnes, 2017a), a trend that continues into cool-temperate Europe where the sole microgastropod species dominating intertidal Z. noltei Hornemann, 1832 around the shores of the North Sea can attain densities up to a further ten times higher still, whether in seagrass or on adjacent bare sediment (Barnes & Ellwood, 2011; Kraan et al., 2011). This trend runs counter to that of local seagrass productivity (Duarte & Chiscano, 1999) and presumably also to that of their biofilm food. The same trend for decreasing microgastropod diversity but increasing density across these sites also applies to the whole seagrass-associated assemblage of which they are part, the Rainbow Channel supporting the highest species diversity but lowest macrofaunal abundance.

Other evidence also suggests that the seagrass microgastropods are below carrying capacity on North Stradbroke, and such a state would go a long way to explaining the observed structure of the guild. Not only within the guild itself, but for the whole seagrass assemblage, species composition at any given point comprises a randomly assorted subset of those species present in the locally available pool, both because of the occurrence of spatially homogeneous species density across individual seagrass beds (Barnes, 2014) and also because of the absence of significant negative species co-occurrence patterns across spatial scales of < 150 m (Barnes & Ellwood, 2011). Such stochastic composition will only be found where no species is in a position to affect the distribution of any other (Barnes & Barnes, 2014), i.e. when populations are below carrying capacity and competitive interactions do not occur, even if niche overlap may be almost complete. No evidence from the detailed distributions of the Deanbilla Bay microgastropods suggests any effects of competition or interference; for example, apart from some of the hotspots there was no evidence of spatial separation of species. Nevertheless, the sampling system used was still relatively crude, enclosing all parts of the seagrass plant and the adjacent sediment within each sample. More microhabitat-specific sampling will be required to show the extent to which the species are likely to come into direct contact in nature and/or show different microhabitat preferences.

No data are available on the diets of the Rainbow Channel microgastropods and so it is not known whether these overlap, nor is there any convincing explanation available for the relatively huge densities of Calopia, of P. speciosa and P. micans, and of Circulus in a few small patches within the study region. These hot spots did not appear visually to differ from other parts of the bed at the time of sampling, and the abundant snails were not juveniles and their aggregations could not be an accident of recruitment (insofar as is known, all have planktotrophic larvae; Rachello-Dolmen et al., 2013b). Moelzner & Fink (2015) concluded that the freshwater grazing gastropod Lymnaea can home in on volatile organic chemicals (‘volatile infochemicals’) released by the grazing of conspecifics and can thereby aggregate on their localised food sources. Indeed, they suggest that this is ‘a possible mechanism to explain the frequently observed patchy distribution of grazers in ecosystems’ (Moelzner & Fink, 2015, p. 1). Heterogeneous resource availability is a very common cause of heterogeneous consumer distribution and abundance (Wiens, 1976), and it is conceivable that some microgastropod species have very specialist biofilm diets, and that their target food sources might be very localised. But whether minute snails could negotiate their way distances of tens of metres across seagrass beds following odour trails against the background of shifting water movements in the intertidal zone is another matter. Clearly, the microgastropods involved both move (in the present study, Elachisina quite rapidly relative to its size) and can be moved by current and tidal flows. Little else is certain, and rarely have the displacements achieved by small gastropods been measured (and never in seagrass beds); distances of some tens of centimetres a day are given by Chapman (1997) and Barnes (1998). These limited available observations hardly support any notion that tiny gastropods such as Circulus are able to home in on spatially rare resources from across broad expanses of seagrass bed. Unfortunately, it is not known whether these species-specific microgastropod hot spots persist through time, and if so for how long, nor is the extent to which biofilms of very specific type (from the viewpoint of a microgastropod) not only occur at all, but, if they do, whether they vary spatially and temporarily. Neither is there any available information on whether they exhibit breeding aggregations, as for example in the larger Strombus luhuanus Linnaeus, 1758 (Catterall & Poiner, 1983). These areas of ignorance are major barriers to our understanding.

Excluding the overwhelmingly dominant position of Calopia, the ranked species importance curve of the remaining microgastropods in the Rainbow Channel fauna is basically similar to those characterising both Motomura’s (1932) geometric series and Tokeshi’s (1990) random-assortment models of assemblage construction. The geometric-series model is usually taken to apply to cases of pre-emptive niche apportionment through intense competition, but as above there is nothing to support the operation of strict competitively induced niche partitioning within seagrass assemblages and much to suggest that it is not so. In contrast, the Tokeshi model is essentially dynamic and stochastic. Under this model (and see Hubbell, 1997), species carve out their niches independently of each other and species abundances are also unrelated; in the model’s original formulation this is because of inhabiting a variable environment (temporarily and/or spatially) and/or of lack of sufficient time to establish competitive responses before balances of advantage change. But other mechanisms may also reduce populations of species below the level at which they would compete, one of which is top-down control of abundance, including by the sympatric crabs, mantis shrimps, amphipods, cephalopods, macrogastropods, opisthobranchs, polychaetes, nemertines and other infauna, as well as the juvenile prawns, crabs and fish that use the seagrass systems of Moreton Bay as nursery areas (Dall et al., 1991; Ebrahim et al., 2014; and see Lewis & Anderson, 2012; Bertelli & Unsworth, 2014; Whitfield, 2017; and Nowicki et al., 2018).

There seems little doubt that the small epibenthic to immediately subsurface invertebrates of seagrass beds and equivalent habitats are the key link between microphytobenthos and juvenile nekton (Sardá et al., 1998; Whitfield, 2017), nor indeed that microgastropods may numerically be the most important component of those invertebrate assemblages. Whether it then follows that it is therefore the microgastropods that are the key link is more controversial. It is known that many are taken by small sympatric invertebrate predators (e.g. McArthur, 1998; Dupuy et al., 2010), but unfortunately knowledge of consumption of microgastropods by nekton and larger benthos is limited and contradictory. On the one hand, a number of studies have shown that few nektonic consumers take a significant number of adult microgastropods (e.g. Edgar & Shaw, 1995; McCormick, 1998) or indeed of gastropods in general (Reynolds et al., 2018); and that in any event microgastropods are low in nutritive value (Vinson & Baker, 2008). A previous work, however, has indicated that, for example, the guts of algal and detritus-feeding fish can contain ‘numerous’ microgastropods (Debenay et al., 2011), and that they may constitute a major part of the diet of fish such as Mugil cephalus Linnaeus, 1758 (Bekova et al., 2013) and Clinus spatulatus Bennett, 1983 (Bennett & Branch, 1990). In any event, by far the greatest mortality faced by microgastropods on the sea bed occurs not at the adult stage but immediately post-settlement. Bachelet & Yacine-Kassab (1987) and Bachelet (1990), for example, recorded that only 1% of settling juvenile Peringia ulvae (Pennant, 1777) and other macrobenthic species remained after 3–5 months; yet in the southern North Sea most Peringia only become adult in the sense of being able to reproduce if they can survive a further 5 months of benthic life (Barnes, 1990). Many microcarnivorous consumers are known to feed on minute benthic animals at or near the meiofaunal size of settling larval stages of microgastropods (Gosselin & Qian, 1997). Some of these are specialist feeders, taking mainly crustaceans for preference, especially from the size of small amphipods down to harpacticoids (e.g. Coull et al., 1995). Others, however, including both epibenthically feeding fish and decapods may feed in a size- and substratum-specific fashion taking all available small near-surface material and causing significant mortality to most juvenile macrobenthos, including microgastropods, not only via direct predation but also through disturbance (Kneib, 1985), as early caging studies around the North Sea and North Atlantic showed in respect of Peringia and Ecrobia (Reise, 1978, 2012; Wiltse et al., 1984). Whatever the agents responsible, however, something certainly removes the large majority of the young microgastropods from the substratum relatively soon after settlement.

There would appear to be little requirement to adopt differing feeding niches or microhabitat partitioning if these Moreton Bay microgastropods (and other benthos) are always maintained well below carrying capacity. Escape from being the food of others would seem to be much more of a prime requirement for successful survival. In this respect, not all the Deanbilla Bay microgastropods may be equal: Pseudoliotia species, for example, possess relatively large, strong shells bearing anti-predator knobs, whorls or ridges, dependent on species, whereas the shells of Calopia, Lucidestea, Elachisina and many others are very thin, simple and without structures or shapes that could serve as anti-predator devices (Vermeij, 1987, 2015). Such morphologically ‘unprotected’ species may potentially possess anti-predator or other behaviour patterns but this is an unknown since no behavioural studies have ever been undertaken.

Calopia and the rissooids are certainly almost identical in size, shell form and general appearance. Yet one is (relatively) abundant and the others are rare to very rare, and, further, this system seems stable. Over the 10 years of the present study, overall microgastropod numbers have fluctuated between some 620 and 1150 m−2 [considerably less than the fluctuations known to occur in some northern-hemisphere hydrobiids (Barnes, 1991)], whilst the rank order of importance within this guild has remained unchanged: Calopia has always been the most numerous, Pseudoliotia next most abundant, and so on, with Lucidestea, Elachisina, etc. always at very low density. The abundance pattern of individual species across spatial scales also changed relatively little between 2014 and 2017. For some species such as Iravadia goliath and Cerithidium diplax, their areas of maximum abundance are known to be elsewhere, in the adjacent mangrove (Barnes, 2017c) and sublittoral (Rachello-Dolmen et al., 2013a), respectively, so those in the seagrass can be regarded as stragglers. Others, like Elachisina and Circulus, are presumably genuinely rare in that they are not listed in the checklist of Moreton Bay gastropods (Healy et al., 2010), do not appear in Rachello-Dolmen & Ponder’s (2013) list of microgastropods of the region, nor are they shown as occurring there in the Atlas of Living Australia (www.ala.org.au).1 No information at all is available to suggest how or why Calopia can maintain 3000 times the density and 700 times the occupancy of more characteristically seagrass animals such as Diala, for example, but then this type of conundrum is by no means confined to microgastropods (Kunin & Gaston, 1993; Lennon et al., 2004). Miloslavich et al. (2013) in a recent study of the distribution patterns of rocky-shore gastropod assemblages regarded knowledge of processes that shape patterns of biodiversity of species assemblages as critical for understanding assemblage stability and resilience, and the effects on them of global change, but it appears that the nature of such processes in the present case will remain unknown until much more attention is paid to the detailed ecology of these species and until data on their microhabitat preferences, precise food sources and predator-avoidance strategies become available. As will be evident from the above, still very little is known of these tiny animals in life. However, they may yet prove crucial to the nursery function of the Moreton Bay and other equivalent seagrass beds for commercially significant prawn and fish species.

Footnotes

  1. 1.

    The Atlas does list a Circulus, ‘Circulus (Lodderia) lodderae (Petterd, 1884)’ [= Beechey’s (2017) ‘Circulus lodderae’] as occurring near the mouth of Moreton Bay, but Lodderia (and hence its type species L. lodderae) is considered by WoRMS and MolluscaBase (www.molluscabase.org) not to belong to the Tornidae at all, let alone be a Circulus, but to belong to the trochoidean family Skeneidae.

Notes

Acknowledgements

I am most grateful to the Quandamooka Yoolooburrabee Aboriginal Corporation, the Quandamooka Aboriginal Land and Sea Management Agency, and the Queensland Parks and Wildlife Service for permission to conduct research within the native title area of the Quandamooka People and within a Habitat Protection Zone of the Moreton Bay Marine Park, under permit QS2014/CVL588. I also warmly thank Ian Tibbetts and all the staff of the Moreton Bay Research Station for their help and support, and Morvan Barnes and Brian McCabe for computational advice. The work was made possible by the MBRS Distinguished Researcher Award from the UQ Centre for Marine Science, for which I am very grateful.

Funding

The project received no external funding.

Compliance with ethical standards

Conflict of interest

The author declares no conflicts of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed, and all necessary permits were obtained.

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Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.School of Biological Sciences and Centre for Marine ScienceUniversity of QueenslandBrisbaneAustralia
  2. 2.Biodiversity ProgramQueensland MuseumBrisbaneAustralia

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