ANÁLISIS DEL PRODUCTO

4.4.2.1 Classification of Ammonia species

The integrated taxonomic framework presented in Chapter 3 was employed to classify specimens of Ammonia. On the basis of morphological characters exhibited by Ammonia

specimens, two species of Ammonia, genotypes S5a and S6 were identified in this study. This highlights that the current taxonomic practice of recognising a single species of Ammonia in this area has potentially underestimated species diversity in this region.

However, new molecular analysis conducted in the NW Scottish shelf seas has discovered the presence of three co-existing genotypes of Ammonia S4, S5a and S6 at both Dunstaffnage and also in Loch Sunart (Bird et al., in prep.). The absence of Ammonia genotype S4 in this study is interesting and could indicate that the ecological (microhabitat) requirements of Ammonia

genotype S4 are not met at this site locality. Bird et al. (in prep.) hypothesised that the occurrence of Ammonia genotype S4 may be controlled by water depth, as this genotype is abundant in intertidal areas but is rare in sub-tidal localities. For example, only a single specimen of Ammonia genotype S4 was identified at Dunstaffnage and Loch Sunart. The absence of

Ammonia genotype S4 at this site could therefore be attributed to the sampling depth of 32m, which may be beyond the depth limit of this species. Further investigation is needed to clarify the ecological preferences (including depth partitioning) of these Ammonia species.

In practice it was sometimes difficult to classify juvenile specimens of Ammonia (<100 µm) using the key diagnostic morphological features identified in Chapter 3. This illustrates one of the major caveats of the integrated taxonomic framework presented in Chapter 3, as there is currently a paucity of knowledge of the morphological variability of Ammonia species at a population level.

4.4.2.2 Partitioning of Ammonia species

Currently there are a dearth of investigations which evaluate the influence of environmental controls on Ammonia abundance. Previously, temperature (Bradshaw 1957, 1961), salinity (Bradshaw 1957, 1961; Pascal et al., 2008), oxygen availability (Moodley and Hess, 1992; Martins et al., 2015) and the availability of organic matter (Martins et al., 2015) have been identified as important environmental controls on Ammonia abundance. However, these investigations predominantly classified specimens of Ammonia into broad morphospecies concepts including

Ammonia beccarii and Ammonia tepida. As a consequence, the validity of previously identified

Ammonia species-specific responses to environmental conditions are brought into question, as the broad morphospecies concepts previously recognised may represent an amalgamation of genetically distinct species.

This study reveals the presence of two species of Ammonia which co-exist in all the samples, whilst also exhibiting some subtle temporal partitioning (Figures 4.6, 4.7 and 4.8). However, the results revealed that no causal relationship between absolute abundance and temperature or salinity was identified. Alternatively, the partitioning exhibited between the two Ammonia

species could be attributed to other abiotic and biotic factors that were not quantified in this study. For example, Ammonia genotype S6 exhibits a similar temporal pattern to N. turgida,

albeit at a lower population density with a minor lag in response (Figures 4.6 and 4.7). The difference in response rates could be attributed to the species-specific reproduction cycles. Guffaston and Nordberg (2001) identified that thinner shelled taxa (like N. turgida) can rapidly

reproduce and grow to adulthood within less than a month, whilst taxa that possess thicker tests (e.g. Ammonia) lag behind because their reproduction cycles are longer. Furthermore, it could be hypothesised that abundance of Ammonia genotype S6 is controlled by the same environmental conditions as N. turgida such as food availability (Goineau et al., 2012). In contrast, the peak abundance of Ammonia genotype S5a coincides with the lowest relative abundance of N. turgida (Figure 4.5). Thus it could be asserted that Ammonia S5a is responsive to decreased competition and may be tolerant to low levels of phytodetritus or that it can survive on a range of food sources.

The hypothesised ecological preference of Ammonia genotype S6 for high organic matter is supported by prior investigations which identified that Ammonia falsobeccarii is prevalent in high abundance in organically enriched sediments (Fontainer et al., 2002; Pucci et al., 2009; Schweizer et al., 2011). Ammonia genotype S6 was previously ascribed to the species concept

Ammonia falsobeccarii by Schweizer et al. (2011). This species concept of Ammonia falsobeccarii

is one of the few taxa within the Ammonia genus which has been consistently classified throughout time, and its morphospecies concept holds up against new lines of taxonomic evidence (Schweizer et al., 2011; Bird et al., in prep). As illustrated in Chapter 3, Ammonia

genotype S6 exhibits the diagnostic feature of discrete secondary dorsal openings which was originally identified as a key diagnostic feature in the type description of A. falsobeccarii

(originally Pseudoeponides falsobeccarii Rouvillois, 1974). Therefore, it could be considered that the previously identified ecological preferences of this taxon previously are robust. In contrast, little is known about the ecological preferences of Ammonia genotype S5a, owing to the historical taxonomic and nomenclatural confusion and the absence of a consistently recognised discrete diagnostic test identified diagnostic test features (as discussed in greater depth in Chapter 3).

4.4.2.3 Recognition of reproductive phases of Ammonia

Foraminiferal growth is often rapid and episodic in nature, with foraminiferal species frequently exhibiting clear seasonality in growth and reproduction (Murray, 1991; Lee et al., 1991). During foraminiferal calcification (growth), a layer of calcite is directly precipitated on both the inside and outside of the test from the ambient seawater (Bé et al., 1979; Debenay et al., 2000). As such, foraminifera have significant utility as biogeochemical recorders of seawater conditions (James and Austin, 2008). For example, the test provides a record of the δ18_{O of the seawater,}

water temperature and salinity at the time of calcification (Allison and Austin, 2003; Cage and Austin, 2008; Pearson, 2012). It is crucial to be able to identify phases of growth and reproduction in Ammonia in order to both refine our understanding of foraminiferal biology and to improve our understanding of the stable isotopic composition of extant and fossil foraminifera for palaeoenvironmental interpretations (as discussed in detail In Section 4.4.3). Presently, there is a dearth in the understanding of Ammonia reproduction. Previous population dynamic studies have identified that Ammonia beccarii continuously reproduces throughout the year (Haake, 1967; Basson and Murray, 1995). Venec-Peyre (1983) by contrast, suggested that

A. beccarii undergoes four distinctive phases of reproduction. Species of Ammonia in the NW Scottish shelf seas (classified under A. batavus or A. beccarii) have previously been found to exhibit seasonal phases in growth and reproduction. For example, individuals of Ammonia from stratified localities were found to grow (calcify) in late summer (Austin and Scourse, 1997; Scourse et al., 2004), whilst specimens from mixed localities grow (calcify) during spring or early summer (Scourse et al., 2004; Cage and Austin, 2008). However, all the studies outlined above use broad morphospecies concepts of Ammonia. As a consequence, our current understanding of Ammonia biology and reproductive stages may not be reliable, as current understanding may represent the calcification and reproduction behaviours of a mix of genetically distinct species. By taking into account previously unrecognised cryptic diversity, this study presents one of the most accurate pictures of the population dynamics of Ammonia species yet undertaken. The results reveal the presence of co-existing populations of different size classes throughout the year for both Ammonia genotypes S5a and S6. This indicates that both species exhibit continuous reproduction over the period of investigation (Figure 4.9) and supports the findings of previous investigations into the population dynamics of Ammonia (Haake, 1967; Basson and Murray, 1983). The results also reveal potential phases of increased reproduction for both

respective peak absolute abundances. Therefore, it could be hypothesised that these species maintain a background population throughout the year and only exhibit significant growth (calcification) during favourable environmental conditions.

This study could be strengthened by sampling the site at a higher temporal resolution in order to further elucidate the phases of increased reproduction for the two species. This is crucial, as it has been previously identified that monthly sampling may not always successfully capture recruitment (Murray, 1983). In addition, specimens of Ammonia can take as little as 20 days to reach full maturity during growth (Bradshaw, 1957, 1961). Further investigation is needed to elucidate the growth, life cycles and reproductive behaviours of these species. In addition, extensive environmental surveys, and culturing investigations will be essential in helping to elucidate the biological behaviours and ecological preferences of these species.