Introduction
Biological trait-based approaches are increasingly being adopted as a tool by which to explore changes in ecosystem functioning (Bremner et al., Reference Bremner, Frid and Rogers2003a, Reference Bremner, Rogers and Frid2003b; Degen et al., Reference Degen, Aune, Bluhm, Cassidy, Kedra, Kraan, Vandepitte, Wlodarska-Kowalczuk, Zhulay, Albano, Bremner, Grebmeier, Link, Morata, Nordström, Shojaei, Sutton and Zuschin2018). Morphological, life history and behavioural traits can be used to investigate ecosystem functions and properties such as energy and nutrient cycling, production, resilience and heterogeneity (Degen et al., Reference Degen, Aune, Bluhm, Cassidy, Kedra, Kraan, Vandepitte, Wlodarska-Kowalczuk, Zhulay, Albano, Bremner, Grebmeier, Link, Morata, Nordström, Shojaei, Sutton and Zuschin2018). However, extensive gaps still exist in our knowledge of the natural history of species even for well-documented faunas such as the marine benthos of the UK (Tyler et al., Reference Tyler, Somerfield, Vanden Berghe, Bremner, Jackson, Langmead, Palomares and Webb2012), and it is often necessary to resort to the application of generalized relationships, such as that between body size and age (e.g. Marine Ecological Surveys Limited, 2007) or reproductive mode (Strathmann & Strathmann, Reference Strathmann and Strathmann1982), even though in specific cases these may be misleading. Echinocyamus pusillus (O.F. Müller, 1776) is one such example.
Echinocyamus pusillus is a very small sea urchin with an oval, flattened body typically only 1 cm in length (Picton & Morrow, Reference Picton and Morrow2016), although reported to reach a maximum of 15 mm (Hayward & Ryland, Reference Hayward and Ryland1990). It is common all around the British Isles and is found from the extremely low intertidal to sublittoral depths of more than 200 m (Southward & Campbell, Reference Southward and Campbell2006). It has a preference for medium to coarse-grained sand (median grain size >200 μm) and reaches maximum densities in sediments with a median grain size of 500‒550 μm, preferring sediments with a low mud content (maximum 10%) (Degraer et al., Reference Degraer, Wittoeck, Appeltans, Cooreman, Deprez, Hillewaert, Hostens, Mees, Vanden Berghe and Vincx2006). Being a very small species in very coarse sediments, its occurrence may be under-recorded due to its inconspicuousness and the methodological problems of its extraction from the sediment. The test is completely covered with fine short spines and is coloured grey to greenish, becoming completely green when injured (Southward & Campbell, Reference Southward and Campbell2006). The calcite test has extraordinary structural strength and skeletal integrity within the echinoids, due to the absence of supportive collagenous fibres between single plates and an internal buttress system (Grun & Nebelsick, Reference Grun and Nebelsick2018). This provides the species with exceptional resilience to physical abrasion in coarse sediments that are often unstable and mobile. Since the coarse sands and gravels which E. pusillus inhabits are often the target for aggregate dredging by the construction industry, the species resilience to physical abrasion is likely to be crucial to its continued persistence in these areas (Marine Ecological Surveys Limited, 2007).The high preservation potential of the tests is also responsible for their frequent occurrence in both recent and fossil (Pliocene) death assemblages.
Despite its small size, E. pusillus has a planktotrophic larval phase in its life history. It has separate sexes and fertilization takes place externally. The breeding season is in the summer months and the echinoplutei are found in the plankton from summer to autumn (Southward & Campbell, Reference Southward and Campbell2006).
Echinocyamus pusillus is a deposit-feeder, its gut content including sediment, remains of plants and bottom material (detritus), and infauna, especially foraminiferans, and E. pusillus itself is eaten by fish, especially by dab and haddock (Mortensen, Reference Mortensen1927; de Ridder & Lawrence, Reference de Ridder, Lawrence, Jangoux and Lawrence1982; Eleftheriou & Basford, Reference Eleftheriou and Basford1989; Schückel et al., Reference Schückel, Ehrich, Kröncke and Reiss2010). Haddock show a strong preferential prey selection for E. pusillus in the North Sea, which may be effective as a grinding element in their stomach, enhancing digestion due to its hard calcareous shell and compensating for the low nutritional value of their benthic prey (Schückel et al., Reference Schückel, Ehrich, Kröncke and Reiss2010).
The objective of this study is to establish some of the major life history traits relating to the function of this species, in particular its lifespan or time taken to reach maximum size, which can be established by cohort growth analysis.
Materials and methods
Quantitative samples of Echinocyamus pusillus were collected at six offshore sites licensed for aggregate extraction in the southern North Sea and eastern English Channel (Figure 1, Table 1) in May and June 2005 as part of a broader research programme investigating the ability of benthic communities to recover from aggregate extraction (Marine Ecological Surveys Limited, 2007). The bottom sediments comprised coarse mixtures of sand and gravel, occasionally with a small mud component, and water depths ranged from 18‒49 m (Table 1). Ten 0.1 m2 Hamon grab samples of sediment were taken randomly within each site, sieved over a 0.5 mm mesh sieve, gently eluted to remove excess fine sediment and preserved in formalin for further separation and analysis in the laboratory. Test-length measurements to the nearest 0.1 mm were made under a binocular microscope using an eyepiece graticule calibrated with a stage micrometer. Size-frequency analysis requires a reasonably large number of specimens, and all specimens from all 10 samples taken from a particular area have been combined to establish the size-frequency distribution. Areas where less than 20 specimens were recorded, across the 10 samples, have been excluded from this analysis.
Map of SE England showing locations of the six sampling areas. Inset: photograph of a living specimen of Echinocyamus pusillus.
Sediment composition in sampling areas as Folk classification categories (Folk, Reference Folk1954), with sampling date in 2005 and water depth (m)
Number of grab samples comprising each sediment type in parentheses.
Several computer packages such as ELEFAN, SLCA, MULTIFAN and MULTIFAN-CL are available to identify modes in size-frequency distributions (see Van der Meer et al., Reference Van der Meer, Brey, Heip, Herman, Moens, van Oevelen and Eleftheriou2013 and references therein) but these are based on the assumption that the sizes in each age class are normally distributed, which is intuitively invalid. If recruitment occurs over a period of time and the recruits then begin to grow and suffer mortality then we would expect a right-skewed size distribution for that cohort (i.e. with the mode to the left of the distribution). In practice, if cohorts are clear they can be identified by eye without the need for computationally cumbersome techniques, and this approach has been adopted here. A further problem arises when attempting to estimate the number of year classes in the population in that the local recruitment of many benthic species is erratic (see e.g. Buchanan & Warwick, Reference Buchanan and Warwick1974) and in some years may be particularly strong while in others it may be weak or there may be a complete recruitment failure.
Results
Figure 2 shows that, for all areas combined, there are clearly five cohorts present, giving a maximum age of five years. The smallest cohort, with a modal length of 1.5 mm, can be assumed to be almost one year old, since samples were collected in May/June and spawning and planktonic larval development takes place in the summer‒autumn (Southward & Campbell, Reference Southward and Campbell2006). The maximum length attained is just 7.3 mm, at Area 461. Clearly, the five cohorts are not all well represented in all areas and interpretation of the data from one area alone could be quite misleading. In Area 461 there appears to be a single cohort of large animals which would suggest an annual species with a rapid growth rate. Size-frequency data from Areas 452 and 460 would be interpreted as having 2 cohorts (but these are not of equal size in the two areas), with a lifespan of two years. Areas 458 and 483 would be interpreted as having three cohorts, with a lifespan of three years, whilst data from Area 430 are more difficult to interpret but suggest a lifespan of at least two years.
Size-frequency histograms of Echinocyamus pusillus test length in the six individual areas and in all areas combined.
Discussion
In the present study size-frequency distributions have only been established for a single point in time and so the annual nature of the size modes is equivocal. However, cohort growth analysis has been widely used in field programmes directed towards the estimation of annual production of marine benthic macrofaunal species in UK waters (Buchanan & Warwick, Reference Buchanan and Warwick1974; Warwick & Price, Reference Warwick and Price1975; Warwick et al., Reference Warwick, George and Davies1978; Price & Warwick, Reference Price and Warwick1980; Warwick & George, Reference Warwick, George, Collins, Banner, Tyler, Wakefield and James1980; George & Warwick, Reference George and Warwick1985). Such studies typically result in a time series of size-frequency distributions, from which the demographic parameters of recruitment, growth rates and mortality rates can be derived (Crisp, Reference Crisp, Holme and McIntyre1984; Van der Meer et al., Reference Van der Meer, Brey, Heip, Herman, Moens, van Oevelen and Eleftheriou2013). A time series of size-frequency distributions is used to follow the progression of size-modes over time so that it is possible to determine whether the size modes are annual or not, since it is conceivable that modes could result from a series of discrete spawnings over time periods shorter than a year, or annual modes might be missing due to recruitment failure. Thus, if a species is only present in one or two areas, the data must be interpreted with caution since the size modes may not represent successive years. However, in all the studies of benthic species cited above these size modes have proved to be annual, and therefore this is assumed to be the case for Echinocyamus pusillus.
This analysis is predicated on the assumption that the settlement timing and post-settlement growth rates are similar in all areas. The composition of each size cohort in the combined graph comprises individuals from more than one area (except for the oldest). The first cohort comprises individuals from all areas except 461, being particularly strong in area 483. The second cohort also comprises individuals from all areas except 461, being particularly strong in area 452. The third cohort comprises individuals from all areas, the fourth from areas 452, 460 and 461 only and the fifth from area 461 only. The most logical scenario is therefore that the overall pattern results from varying recruitment success in different areas with roughly the same settlement time and growth rate in each. A possible alternative explanation of the combined distribution might be that there are fewer year classes than five but settling at very different times and growing at very different rates in individual areas. The two areas of highest urchin abundance, 483 and 452, each provide a clear indication of only two cohorts and would lead to the conclusion of a two-year lifespan, but if this were the case it would imply very different settlement times and/or growth rates in the two areas, which are only some 150 km apart in the same sea area and have a very similar sediment type. This would also contradict data from the other areas, where more than two cohorts were typically observed. Furthermore, while there are small differences among areas in the size range of individuals within each year class, if these differences had been larger they would have blurred the clear separation of classes.
The combined size distribution charts suggest that E. pusillus is very slow growing in the studied areas, taking five years to reach the small maximum size of 7.3 mm. The somewhat larger size elsewhere may either mean that it grows faster in these areas or lives longer. Although this species is reported to attain a greater size of 15 mm (Hayward & Ryland, Reference Hayward and Ryland1990), there is no primary citation to support this value, although it is also attributed to Degraer et al. (Reference Degraer, Wittoeck, Appeltans, Cooreman, Deprez, Hillewaert, Hostens, Mees, Vanden Berghe and Vincx2006) by WoRMS Editorial Board (2019). One of us (BP) has counted many thousands of individuals of this species throughout the UK, and never encountered specimens this large, and the 10 mm of Picton & Morrow (Reference Picton and Morrow2016) is probably more realistic. The slow growth rate may be due in part to the low organic content of the coarse sediments that it inhabits, and also to its feeding behaviour which is potentially expensive energetically. The feeding mechanism is atypical for clypeasteroids because the coarse sediment particles are too large relative to the body size to be ingested whole. Sediment particles with attached food material are selected and transported by the suckered podia to the mouth, where particles are held in place and slowly rotated by the free margin of the peristomial membrane, while the teeth strip away diatoms and organic debris (Telford et al., Reference Telford, Harold and Mooi1983). This mode of feeding is thus akin to that of many meiobenthic taxa that feed by scraping the biotic films from sediment particles, e.g. many nematodes (Wieser, Reference Wieser1953) and harpacticoid copepods (Marcott, Reference Marcott1977).
For comparison, limited data are available on growth rates of two larger heart urchins from offshore sediments in this area. Echinocardium cordatum (Pennant, 1777) in the southern part of the North Sea off the Dutch coast has been shown, by an analysis of annual growth rings on the ventral plate, enigmatically to grow fastest in sediments with the lowest organic content (Duineveld & Jenness, Reference Duineveld and Jenness1984). It reaches a maximum length of 43 mm at more southern sites and 33 mm further north, but a longevity of 10 years is the same in all areas. On the other hand, Brissopsis lyrifera (Forbes, 1841) in the finer offshore sediment off the Northumberland coast has a lifespan of four years, reaching a maximum size of 60 mm. The four-year-old individuals breed in November‒December and do not survive to breed a second time (Buchanan, Reference Buchanan1967; Buchanan & Warwick, Reference Buchanan and Warwick1974). The feeding mode of this species is more typical of irregular echinoids, the fine organic sediment being ingested whole.
The results of this study indicate that E. pusillus has an unusual combination of functional traits. Planktotrophic larval development is prevalent in larger-bodied macrobenthic species (no meiobenthic species have planktonic larvae) and is unusual in a species of this size. According to the body sizes recorded in the WoRMS database (WoRMS Editorial Board, 2019), E. pusillus has the smallest body size (length) of all the 37 infaunal genera with planktotrophic larval development listed as occurring in offshore sand and gravel sediments in 20 areas around the UK (Marine Ecological Surveys Limited, 2007). For such a small species, it also has an unusually long lifespan.
On the basis of functional trait analysis it has been concluded that E. pusillus is robust with respect to its potential recoverability from anthropogenic disturbance caused by offshore aggregate extraction (Marine Ecological Surveys Limited, 2007). This will obviously also apply to disturbance by benthic fishing. Although recovery from aggregate extraction has been found to require much longer periods than from benthic fishing (Foden et al., Reference Foden, Rogers and Jones2010), the latter activity takes place over very much wider areas both in UK waters and globally, and the sediments in which E. pusillus lives are particularly vulnerable to scallop dredging (Kaiser et al., Reference Kaiser, Clarke, Hinz, Austen, Somerfield and Karakassis2006). In a study of the effects of fishery exclusion on the benthos in the areas of offshore wind farms in the Belgian part of the North Sea, E. pusillus showed increases in abundance in the no-fishery areas, supporting its potential for recovery from trawling activities (Coates et al., Reference Coates, Kapasakali, Vincx and Vanaverbeke2016). Echinocyamus pusillus has been assigned to AMBI ecological group I, species very sensitive to organic enrichment and disturbance (Borja et al., Reference Borja, Franco and Perez2000), but AMBI has been shown to be a poor indicator for detecting the physical impacts of aggregate extraction, there being no increased abundance of opportunistic species as a result of the extractions, and is similarly not useful in other naturally stressed communities (Muxika et al., Reference Muxika, Borja and Bonne2005).
Of the traits relevant to the resilience and recoverability from physical disturbance, size, fecundity, lifespan, age at maturity, larval development mode and adult mobility have been considered the most important (Marine Ecological Surveys Limited, 2007). Fecundity and age at maturity for E. pusillus remain unknown and so it is not possible to predict mortality in the plankton or immediately after settlement. However, the numbers of specimens in the successive year classes found in the study area imply an increasing mortality rate with increasing size, presumably mainly as a result of predation by demersal fish, with none surviving beyond their fifth year.
To complete our knowledge of the demographics of this species, more data clearly need to be gathered. A time series of sampling at one or more locations, perhaps also exploring the possibility of analysing test skeletal features for ageing, would substantiate (or otherwise) the annual nature of the cohorts described in the present study. Analysis of the age at reproductive maturity, fecundity and frequency of spawning, concurrently with sampling of larvae in the plankton would substantially enhance our understanding of the functioning of this important and enigmatic species in the benthic ecosystem and its relevance as an indicator of ecological condition.
Acknowledgements
Richard Warwick acknowledges his Sir Walter Murdoch Distinguished Collaborator award and Adjunct Professorship at Murdoch University and his Honorary Research Fellowship at the Plymouth Marine Laboratory. Bryony acknowledges the work of staff at MESL to extract and preserve E. pusillus from grab samples collected as part of project MEPF 04/02. Bryony also acknowledges the support provided by the aggregate extraction licence holders who allowed and facilitated safe access to their active extraction sites.
Financial support
This work was supported by the UK Department for Environment Food & Rural Affairs (Defra) Aggregate Levy Sustainability Fund, Marine Environment Protection Fund Research Grant No. MEPF 04/02.
