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TECHNIQUES FOR ESTIMATING THE AGE AND GROWTH OF MOLLUSCS: GASTROPODA.

INTRODUCTION

The Gastropoda represent the largest class belonging to the phylum Mollusca, containing an estimated 80,000 species (Bouchet et al. 2005). Although gastropod fisheries are smaller than global finfish and bivalve fisheries, gastropod populations support large fisheries around the world with estimated landings of over 165,000 t in 2016 (FAO 2017). These fisheries range from small-scale artisanal harvesting of species such as muricid gastropods (e.g., the banded and purple dye murex Hexaplex trunculus) (Vasconcelos et al. 2006) and the intertidal whelk Buccinanops globulosus (Avaca et al. 2015) to much larger scale fisheries of certain whelk species such as Buccinum undatum and Busycotypus (=Busycon) canaliculatus (Marine Management Organisation 2016, Fisher & Rudders 2017). Like any commercial species, questions of sustainability are frequently raised for gastropod fisheries, leaving fisheries scientists to ascertain the most appropriate way(s) to manage what are often difficult to monitor groups of species. The application of reliable age determination to a population of any species allows inferences to be made regarding key management metrics such as size at age, age at maturity, and other age- and length-based indicators (ICES 2016). In the case of the Gastropoda, there are several structures that can be used to estimate age, with differing methods and success rates between species. This review discusses the current methods that can be used for determining the age and growth rate of different gastropod species.

SHELLS

In a similar way to the Bivalvia, gastropods usually produce an external protective shell made from calcium carbonate; exceptions are seen in species of Opisthobranchia where the shell is reduced, internal, or absent (Fretter & Graham 1994). Unlike the paired shells of the Bivalvia, gastropods produce a single shell and were previously known as univalves for this reason. The evolutionary pathways of many gastropod species have led to planispiral shell coiling, although there are notable exceptions to this, such as the limpets. If shell growth is seasonal, then the shells of coiled gastropods are likely to contain a record of their ontogenetic growth history of life in the form of a series of serially deposited growth rings similar to those seen in members of the Bivalvia (Richardson 2001). The planispiral coiled nature of many gastropod shells make them difficult to section and analyze in a traditional way when compared with most of the bivalve shells.

Growth Rings and Lines

External Growth Rings

External surface growth rings (annuli) or checks and internal growth lines representing a gastropod's age occur because of changes in seasonal shell growth rates that cause a change in the appearance in the shell as a result of variations in the inorganic/organic content and the shell crystal structure. External ridges on the gastropod shell have been shown to represent annual growth cycles in certain species of marine and freshwater genera [e.g., Fissurella crassa (Bretos 1980), Monodonta lineata (Williamson & Kendall 1981) various littoral species (Lewis et al. 1982), and Clithon retropictus (Shigemiya & Kato 2001)]. External rings have been shown to reliably determine the age of several species of abalone such as Haliotis australis (Poore 1972), although in some Haliotis species either an annual periodicity was not evident or the putative annual lines were confused with other subannual growth checks [e.g., Haliotis lamellosa (Bolognari 1953), Haliotis tuberculata (Forster 1967), Haliotis mariae (Shepherd et al. 1995), and Haliotis iris (Naylor & Breen 2008, Naylor 2015)]. Visible external rings have also been shown to be unreliable in other species such as Gibbula cineraria (Schone et al. 2007). Schone et al. (2007) applied oxygen isotope sampling (a technique which will be explained in section 5) to several shells of G. cineraria; however, little similarity was seen between the annual isotope cycles (see section 5 for details) and visible external rings, suggesting that the rings were formed because of some other physiological or environmental factor(s). Santarelli and Gros (1986) also concluded that there was no record of visible external rings on the surface of shells of the commercially important whelk Buccinum undatum. For many gastropod species, if external annual surface growth rings were present, it is likely that repeated shell damage of B. undatum through contact with mobile fishing gear in heavily fished areas such as the Southern North Sea (Mensink et al. 2000) and unsuccessful predator attacks would obscure the rings and render them unusable for age estimations.

Internal Growth Lines

For some gastropod species, especially those without coiled shells, internally formed growth lines may be deposited with an annual periodicity. These growth lines are observed by embedding a shell in resin and sectioning it through regions of interest, for example, the shell apex or shell margin, and etching, illuminating, or staining the lines with appropriate reagents (see Richardson 2001). Annually deposited growth lines have been demonstrated in shells of the common limpet Patella vulgata by Ambrose et al. (2016) who combined growth experiments with chemical analysis of the shells to confirm an annual growth line periodicity of visible lines in the nacreous layers of the shell (Fig. 1). Internal growth lines have been used to estimate age in the slipper limpet Crepidula fornicata (Guy et al. 2013). A similar technique is used to count growth rings in commercially important abalone species. In this instance, a hole is ground on the outer shell surface close to the apex of the shell to uncover the internal annually banded nacreous layers (Fig. 2; Munoz-lopez 1976). Since its initial publication, this method has been used many times (e.g., Prince et al. 1988, Shepherd et al. 1995, 2000, Naylor 2010, and others), although the reliability of this technique appears to be variable between species and locations (Shepherd & Triantafillos 1997, Shepherd & Turrubiates-Morales 1997).

Although the coiled nature of many gastropod shells prevents a complete reconstruction of shell growth along the full growth axis, Tojoa and Ohnob (1999) combined both vertical and horizontal sectioning of the shell columella to reconstruct the ontogenetic growth history and observe the growth patterns in Terebralia palustris. Columella sections revealed growth banding deposited with a tidal periodicity that supposedly enabled shell growth rates to be measured to subdaily resolution (Fig. 3). Tidally deposited bands have also been demonstrated in the shells of the marine pulmonate Siphonaria gigas from Costa Rica (Crisp et al. 1990) and the limpet Cellana toreuma from the rocky shores of Hong Kong (Richardson & Liu 1994). Sectioning the shell lip of another coiled gastropod, the netted whelk Nassarius (=Hinnia) reticulatus, revealed that the lip thickens with annual lines once the growth of the animal slows over time, allowing for accurate age determination (Barroso et al. 2005a). As such, the thickness of the lip has also been shown to be a reliable reflection of age (Chatzinikolau & Richardson 2008).

Using Shell Size to Estimate Age

In lieu of using surface growth rings or internal growth lines in shells to directly age individual gastropod specimens, individual age can often be estimated from measurements such as total shell length and lip thickness, provided that population growth rates have already been established. Population growth rates can be estimated using several methods for gastropod populations, such as size frequency analysis, length frequency distribution analysis (LFDA) (Richardson et al. 2005, Chatzinikolaou & Richardson 2008), mark-recapture experiments (MRE), and chemical analyses of the shell.

Size Frequency Analysis

Growth rate estimation using size frequency analysis is often the easiest to accomplish as minimal sampling effort is needed. Following the collection of multiple animals (usually 300-500) from a single population, a common size measurement is used to produce a size frequency histogram. The chosen measurement can be any nonsubjective measurement; for example, shell length, lip thickness, and shell weight were all used in an analysis of queen conch Lobatus (=Strombus) gigas populations (Baqueiro Cardenas & Aldana Aranda 2014). Plotted as a histogram, modal year classes can often be distinguished, particularly in the early year classes. An assumption of the method is that individual size classes (cohorts) are distinct, and this arises if there is low size class variability within year cohorts and year class strength is prominent and confined to a short settlement and recruitment period (Gayanilo et al. 2005, Fontoura-da-Silva et al. 2016). As growth and size increase, the distinctness of the older size (age) classes can be less obvious and frequently age classes merge together becoming indistinguishable from each other. Statistical separation of individual size classes can be achieved and average modal class size can be assigned using the method of Bhattacharya (Bhattacharya 1967). Size-at-age data obtained in this way are plotted to generate population growth curves. The calculated size at age may only be applicable to an individual population at the time of year when the study was undertaken. Where population length frequency distributions are generated monthly, LFDA has been used to determine shell growth rates (Richardson et al. 2005, Alsayegh 2015, Fontoura-da-Silva et al.

Mark-Recapture Experiments

Capture, MRE are used to estimate individual growth rates over time that can then be used to infer growth and age for the wider population. In practice, a selection of individual specimens is collected from a single population, for example, shell height (umbo-rim axis) measured, and each individual then marked; this often involves gluing an identifying label to each specimen. These individuals are then released back into the same population which is resampled at set time intervals (see Chatzinikolaou 2006, Chatzinikolaou & Richardson 2008). When a marked animal is recaptured, the size is once again measured, giving an estimation of growth over the period between sampling incidences. The cumulative increase in shell height (growth) over time can then be used to infer individual and wider population growth rates, which in turn can be extrapolated to estimate individual ages for newly sampled specimens. This technique has been successfully used to analyze growth rates in several gastropod species [e.g., Antarctic limpets Nacella (=concinna) polaris (Clarke et al. 2004) and Tegula viridula (Fontoura-da-Silva et al. 2016)] and has been especially effective in the monitoring of commercially important Lobatus (=Strombus) gigas populations where recapture rates of ~50% have been achieved (Peel & Aldana Aranda 2012). This has allowed quantification of growth parameters in wild populations over a period of 4 y (Baqueiro Cardenas & Aldana Aranda 2014). Field-based experimental marking approaches have an advantage over laboratory-based growth studies as the observed growth in the former is undoubtedly natural with individuals growing in their natural environment. Field growth studies often require substantial effort as multiple sampling periods are needed and recapture rates are frequently low. Alongside this, the very act of tagging animals may affect their growth rates and increase mortality (Walker et al. 2011). As an example of the pitfalls of MRE, Kideys (1996) studied a population of Buccinum undatum using MRE, tagging over 3,000 animals. Only 34 were recaptured over the course of the 3-y study and 50% of the recaptured animals exhibited no or negative growth. Mark-recapture experiments work best with low mobility species, unless the aim is to assess species spread, making them suitable for many crawling gastropod species. With the right conditions, tagging experiments can be extremely successful: Hancock (1963) tagged 10,038 B. undatum in July 1957 and 1958, of which 3,236 were recaptured during the period of study (up to July 1960) demonstrating very high recapture rates in the area of intensive commercial fishery. These data were successfully used for calculation of growth parameters.

Shell Lip Measurement

Other aspects of shell morphology and shell length can often be a good indicator of age or maturity. Once sexual maturation was reached in the commercially important queen conch Lobatus (=Strombus) gigas, the shell lip continued to grow and thicken after the length of the shell had stopped increasing (Appledorn 1988). Shell lip thickness has been used in several studies to estimate maturity in L. (=Strombus) gigas (e.g. Stoner & Schwarte 1994, Aradna & Frenkiel 2007, Stoner et al. 2012). Visual appraisal and measurement of shell thickness can be administered without damage to live animals, meaning this type of technique is both noninvasive and easy to implement, giving it an advantage over other maturity estimation techniques, provided its validity has previously been established. This is a crucial tool for managing important commercial species that are facing drastic population declines through overfishing (Stoner et al. 2012).

OPERCULA

A second structure that can be used to determine the age of gastropods is the operculum (plural opercula): a shield-like plate, often wholly organic, that the gastropod uses to close off its aperture and protect the soft body tissues inside the shell from predatory attacks and in intertidal species to prevent potential desiccation. Not all gastropods have an operculum (e.g., limpets and abalone), and their structures differ between the species which do have them (see Checa & Jimenez-Jimenez 1998). Different growth shapes occur, such as concentric and spiral, and some species have calcified opercula. A common operculum form used in age determination is the concentric opercula, for example, in the Neogastropoda (Checa & Jimenez-Jimenez 1998). Concentric opercula have been shown to contain two sets of growth line, with both ventral and dorsal surfaces revealing growth rings (Checa & Jimenez-Jimenez 1998) (see Fig. 4).

The dorsal surface growth rings (Fig. 4A) are formed as incremental layers of organic material and added to the edge of the operculum as the animal grows. With seasonal variations in growth, controlled by seawater temperature, the distance between the rings narrows as growth slows, giving the visual impression of a growth ring. Surface opercula growth rings have been used to age many gastropod species, including several commercially important species such as Busycotypus canaliculus (Fisher & Rudders 2017) and Buccinum undatum (Fig. 4A) (Santarelli & Gros 1986, Shelmerdine et al. 2007, Heude-Berthelin etal. 2011).

The ventral growth rings, also known as adventitious layers (Fig. 4B), form in a different way from the surface rings, appearing to form over time to strengthen the organic operculum. The adventitious layers have been used to determine the age of several gastropod species [e.g., Hexaplex trunculus (Vasconcelos et al. 2012), Buccianops globulosus (Navarte 2006, Avaca et al. 2013, Bokenhans et al. 2013), Buccinum isaotakii (llano et al. 2004), Neptunea arthritica (Miranda et al. 2008), and Neptunea antiqua (Richardson et al. 2005)] and are often much easier to read than the surface rings. Despite their widespread use as an age determination tool, it has been suggested that for many species, these rings do not represent annual cycles and are instead formed as a function of growth, to strengthen the operculum as the animal grows (Hollyman 2017). Vasconcelos et al. (2012) compared the ages derived from both the surface and the adventitious growth rings in H. trunculus and concluded that the adventitious layers likely overestimate the age. Similar findings were reported by Hollyman (2017) for seven different Buccinum undatum populations.

Issues with the use of opercula have largely focused on the clarity and readability of surface rings. The use of opercula to age the whelk Buccinum undatum was validated by Santarelli and Gros (1985) and has been used by several studies since. Kideys (1996) and Lawler (2013) both discarded almost 50% of their specimens because of poor opercula readability. It is likely that such a high proportion of sample discard resulted in some form of unintentional sample bias.

STATOLITHS

The final structure that can be used to age many gastropod species is the statolith. Statoliths are small (<0.5 mm) paired calcium carbonate structures found within the nervous system (Fig. 5), and in gastropods, they generally have a roughly spherical morphology containing prominent growth rings and comprise aragonite (Hollyman et al. 2017b). Galante Oliveira et al. (2014) also found a minor trace of calcite within the statoliths of Nassarius (=Hinnia) reticulatus. A statolith is contained within a sac called a statocyst and aids the animal in gravity perception as it moves within the statocyst (Chase 2002). Statoliths can be extracted using two main approaches: dissolving of body tissues in a substance such as sodium hydroxide (e.g., Richardson et al. 2005) or direct dissection and removal (e.g., Chatzinikolau & Richardson 2007, Hollyman et al. 2017b). Once removed from the animal, they are mounted on a microscope slide (in a thermoplastic resin such as Crystalbond 509) where they are either visualized whole provided that transmitted light can easily pass through the specimen (e.g., Galante-Oliveira et al. 2013 - multiple species, Hollyman et al. 2017b - Buccinum undatum) or they are ground and polished to the central plane (using fine grinding papers) to expose the growth rings (e.g., Chatzinikolaou & Richardson 2007 - Neptunea antiqua, Fisher & Rudders 2017 - Busycotypus canaliculatus). Several issues have been identified with the clarity of statoliths. First, they can be crystalized like fish otoliths and cephalopod statoliths (Bettencourt & Guerra 2000, Coffin 2009; Fig. 6A) and can also be deformed (Fig. 6B); in many of these cases, the growth rings are still visible. They can also be opaque (Fig. 6B); this is possibly because of sample preservation (Hollyman 2017). Opaque statoliths are more frequently observed in animals that have started to decompose through poor storage following collection and/or subsequent inadequate sample preservation, for example, freezing quickly after live collection (personal observation). Perhaps most importantly, for species which have elliptical shaped statoliths (i.e., not perfectly spherical), correct orientation is necessary for clear visualization of the growth rings (Fig. 6D; Chatzinikolau & Richardson 2007, Hollyman et al. 2017b). The clarity and readability of statoliths are often far higher than those of opercula (Fisher 2015, Hollyman 2017).

As statoliths calcify continuously throughout the life of the animal (like their shells), they can contain ontogenetic growth histories in the form of growth rings, as the rates of growth change throughout the life of the animal. These rings have been demonstrated to represent events such as larval settlement in species with planktonic larval stages, for example, Nassarius reticulatus (Barroso et al. 2005b, Chatzinikolaou & Richardson 2007), and hatching rings in direct developing species, for example, Buccinum undatum (Hollyman et al. 2017b). More important than rings denoting early life history, annual growth rings have been demonstrated in a variety of species [B. undatum (Hollyman et al. 2017b), N. reticulum (Barroso et al. 2005b), Polinices pulchellus (Richardson et al. 2005), Neptunea antiqua (Richardson et al. 2007), and Busycotypus canaliculars (Fisher & Rudders 2017)].

Validation of the annual periodicity of the statolith growth rings has been achieved in several ways. Barroso et al. (2005b) combined size frequency histograms (derived from shell length measurements) with the number of growth rings in the statolith of each animal to confirm an annual periodicity. Annual cycles in strontium were later found to correspond to each growth ring, further confirming an annual periodicity (Galante-Oliveira et al. 2015). Marginal increment analysis has also been used to track annual statolith ring formation in a single population on a monthly basis over an annual cycle (e.g., Richardson et al. 2005, AlSayegh 2015). Where high variability is found within the growth rates of a species, different methods of annual growth line validation must be sought. For the commercially important whelk Buccinum undatum, Hollyman et al. (2017b) reared juvenile specimens from egg cases for a period of 3 y to validate the periodicity of growth ring formation. This, coupled with high-resolution trace element analysis across the statolith using secondary ion mass spectrometry (SIMS), revealed clear cycles of magnesium and sodium that were coincident with the visible statolith growth rings, regardless of the size or sex of the whelk (Hollyman et al. 2017a). Several issues should be considered when attempting to use statoliths in gastropod age estimation. The processes involved in statolith preparation can be time consuming when compared with other age estimation methods (such as those involving the opercula). The necessity of the grinding process will depend on the size and clarity of statoliths on a species-by-species basis. Figure 7 highlights how grinding may make interannual disturbance rings more visible in B. undatum whelk statoliths, confusing the interpretation of the annual rings.

It is also important to understand the life history of gastropods; the larval development strategy (i.e., free-swimming versus direct development) should be known as well as an estimate of when statolith growth might slow enough during the annual cycle for a growth ring to form. Without an estimate of this information, the interpretation of the growth rings will be difficult; the same principle applies to the use of most types of age-registering structures.

The use of statoliths for age determination of commercially important species is a growing field of research. Validation and methods of use for statoliths in the commercially important whelk Buccinum undatum have recently been published (Hollyman et al. 2017b). Recent work on the channelled whelk (Busycotypus canaliculatus) has highlighted success with the use of statoliths for determining age, suggesting they are preferable to opercula as tools for determining the age of this species as opercula can underestimate the true age of this whelk (Fisher & Rudders 2017).

CHEMICAL ANALYSES

Just as the shells, opercula, and statoliths contain life history information in the form of growth lines and rings, mollusc carbonate structures act as repositories of environmental information contained in the form of isotope ratios and trace element concentrations within the calcium carbonate matrix. The oxygen isotope ratio within biogenic calcium carbonate of mollusc shells can reflect the seawater temperature at the time of formation because of the relationship between seawater isotope ratios with which calcification is often in equilibrium, and seawater temperature which has a strong thermodynamic control over oxygen isotope incorporation (Epstein et al. 1953, Leng & Lewis 2016). Once formed, the isotope ratio at the time of calcification is locked within the carbonate structure. This ratio can then be calculated at a later date through the use of techniques such as isotope ratio mass spectrometry. Multiple high-resolution samples from a single individual allow the reconstruction of historical annual seawater temperature cycles, which can in turn be used to infer the age of an individual. High-resolution sampling of the outer shell layer is achieved by drilling consecutive samples of calcium carbonate along the growth axis of the whorled spiral shell (see Fig. 8). Powder samples of shell material are collected by manually drilling trenches into the outer surface of a shell using a small (often <1 mm depending on the resolution required) drilling burr and collecting the powder in sample vials. By sampling the complete growth axis of a spiralled shell at a set resolution, the full growth history of an individual animal can be reconstructed by using oxygen isotope sampling or another analogous technique.

This approach has been successfully applied to determine the age of several gastropod species such as Conus ermenius (Sosdian et al. 2006, Gentry et al. 2008), Gibbula cineraria (Schone et al. 2007), Olivancillaria deshayesiana (Arrighetti et al. 2012), European abalone (Haliotis tuberculata, Roussel et al. 2011), Rapana venosa (Kosyan & Antipushina 2011), and Buccinum undatum (Hollyman et al. 2017a). This methodology has also been used for fossilized samples of Neptunea angulate from the late Pliocene and early Pleistocene (Owen 2016). By determining the number of oxygen isotope cycles contained within the growth axis of a shell, a definitive age can be assigned to a number of individuals, and these data can be used to construct a size-at-age key for the population.

A similar approach has been used by determining cycles of trace element concentrations within the shells as a proxy for seawater temperature. For mollusc carbonates, Mg and Sr have been identified as potential proxies for seawater temperature at the time of calcification [e.g., Conus ermenius (Sosdian et al. 2006), Crassostrea virginica, and Magallana gigas (Durham et al. 2017)]. The reliability of these proxies varies between species and populations. This is because of the influence of physiological processes on trace element incorporation, commonly known as vital effects. Accounting for potential vital effects, trace element proxies have been successfully used to assign age in several gastropod species, for example, Mg in Neptunea antiqua (Richardson et al. 2007) and Sr in the cone shell C. ermenius (Sosdian et al. 2006, Gentry et al. 2008). Sosdian et al. (2006) combined both trace element and stable isotope analyses to age C. ermenius shells and identified an ontogenetic increase in Sr incorporation, although the annual cycles were still clearly visible allowing them to assign ages to each specimen (Fig. 9).

The use of analytical chemistry to evaluate the seasonal variation in elements and directly age individuals is accurate (within the accuracy of measurement of the analytical machine), but these methods are often costly. Instead, these techniques can be used to assign ages to individual animals as a means of validation of the ages found on other age-registering structures such as opercula and statoliths. Richardson et al. (2007) analyzed Mg variation in the shells of Neptunea antiqua and compared the numbers of annual cycles with the ages determined from the opercula and statoliths. This is similar to methods used by Hollyman et al. (2017b) and Santarelli and Gros (1986) to validate growth rings in the statoliths and opercula (respectively) of Buccinum undatum using oxygen isotope ratios ([[delta].sup.18]0). Trace element analysis of statoliths has also been undertaken in recent years; Galante-Oliveira et al. (2015) revealed annual cycles of Sr corresponding to visible annual growth lines within Nassarius reticulatus statoliths using laser ablation inductively coupled plasma mass spectrometry. Hollyman et al. (2017a) performed similar analyses at a higher resolution using secondary ion mass spectrometry on the statoliths of laboratory-reared B. undatum of known age and provenance, and demonstrated one and two Mg and Na cycles in statoliths of 1- and 2-y-old whelks, respectively. These cycles corresponded to the visible statolith growth lines in laboratory-reared juvenile and wild-caught adult specimens. Even though the use of statolith microstructures is potentially more time consuming than the use of opercula, for example, the literature pool relating to statoliths presents compelling arguments for their preferential use for many species because of their accuracy and reliability.

SUMMARY

This review presented an overview of the available techniques of age and growth rate determination for gastropod molluscs. There are many different options depending on the type of gastropod and the potential age-registering structures available. Whereas the use of internal and external growth lines is feasible for age determination in many species (especially those without coiled shells), the use of structures such as opercula and statoliths are far more reliable in others. The use of nonlethal techniques such as mark-recapture, length frequency analysis, and shell lip thickness to monitor growth and estimate age and maturity (respectively) is an excellent alternative for species facing concerns over sustainability, although they may not be as accurate as a reliable age-registering structure. The use of age and growth rate estimates in fisheries management plays a key role in analytical stock assessment, making the need for reliable age estimation tools critical for certain commercially important species. These techniques are not all suitable for all species and care should be taken to ensure that appropriate tools are being applied to answer necessary questions for the species in question.

ACKNOWLEDGMENTS

The authors would like to thank Mauricio Orostica (Bangor University) for his permission to reproduce Figure 1; Reyn Naylor (NIWA) for his permission to reproduce Figure 2; Elsevier for their permission to reproduce Figure 3 from Tojoa and Ohnob (1999); and John Wiley & Sons for their permission to reproduce Figure 9 from Sosdian et al. (2006).

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PHIL R. HOLLYMAN, (1*) VLADIMIR V. LAPTIKHOVSKY (2) AND CHRISTOPHER A. RICHARDSON (1)

(1) School of Ocean Sciences, College of Natural Sciences, Bangor University, Menai Bridge, Anglesey LL59 SAB, UK; (2) Centre for Environment, Fisheries and Aquaculture Science (CEFAS), Pakefield Road, Lowestoft, Suffolk NR33 OHT, UK

(*) Corresponding author. E-mail: p.hollyman@bangor.ac.uk

DOI: 10.2983/035.037.0408
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