Meiofaunal organisms are tremendously dependent of sediment and therefore reveal the effect of sediment structure and composition on morphology as crucial to better understand animals-habitat interactions. For our group of study, the allomalorhagid families Dracoderidae and Pycnophyidae and the cyclorhagid genus Echinoderes (phylum Kinorhyncha), we found relationships between body and LTS shape with some of the analysed sediment variables. Additionally, the phylogeny contributed to the variation in shape of kinorhynchs as well.
Body shape adaptations of meiofauna to grain size have been mainly explored in interstitial taxa. Sediments with coarser size of particles usually host slender, more vermiform species as they have to move through tight interstitial spaces, whereas finer sediments are inhabited by stouter species whose body enables them to penetrate more easily through the particles, acquiring a movement similar to that of burrowers12,13,14,15. However, relationships between body shape and sediment composition still remains unexplored for burrowing meiofauna. Kinorhynchs, as meiofaunal burrowers mainly, use the introvert scalids to move through the sediment17,25,27.
We found statistically significant influence of average size, skewness and kurtosis of sedimentary particles over body shape of the analysed kinorhynch taxa. The analyses showed that kinorhynch species inhabiting coarser sediments with a high variety of different particles’ sizes tended to be stouter and plumper compared to those inhabiting finer, more homogeneous sediments, whose bodies were slender and more vermiform. These results seem to go, at first sight, against those above mentioned for the interstitial meiofauna. However, the analysed kinorhynch taxa are representatives of the burrowing meiofauna that move actively through the sediment displacing the grains with the introvert scalids24,25. In this context, a more robust and plumper body may suppose an adaptive advantage for the species that live in coarser sediments, allowing to maintain a more powerful musculature to displace the sediment particles by generating a greater force. Indeed, for the interstitial taxa that act to some extent as burrowers in finer sediments, plump and robust bodies suppose an adaptation for this active movement through the sediment, as previously explained. In parallel, the possession of a slender, vermiform body in species inhabiting finer sediments would also be adaptive, since it would not be necessary to apply much force to move the finer sediment particles, and this body morphology would even facilitate the burrowing through the smallest interstices by simple movements of the body combined with that of the introvert scalids. Indeed, fine-grained sediments of moderate to high water content show the phenomenon of thixotropy, where a small force against the sediment is enough to allow sediment displacement10. It remains to be seen if other kinorhynch taxa not included in the present study (e.g. Franciscideridae, Kentrorhagata, Xenosomata) agree with the results herein obtained for Dracoderidae, Pycnophyidae and Echinoderes, or if they contrarily exhibit different patterns of body morphological adaptations to sediment.
Heterogeneity of grain sizes, very different from those of the average (kurtosis), also seems to favour the presence of more robust, plump species. These sediments correspond to gravel and gravelly sand, reflecting the presence of many different categories of coarser sizes. This result seems to also support the previously proposed hypothesis. Heterogeneity of inorganic particles dominated by coarse sediments also reflects a heterogeneity of sedimentary processes, with variable and strong depositional currents10,27,28,29. In these areas of high current velocity, with intense erosion and transportation, meiofaunal organisms must be capable of rapid reburial, favouring the presence of stout and plump burrowing species in coarser sediments.
Regarding the phylogenetic component of the models, body shape differences among classes and families are strongly influenced by genetics. In this context, some kinorhynch taxa with slender and more vermiform bodies, such as the allomalorhagid genera Franciscideres Dal Zotto et al., 2013 and Gracilideres Yamasaki, 2019, or the cyclorhagid genera Cateria Gerlach, 1956, Triodontoderes Sørensen and Rho, 2009 and Zelinkaderes Higgins, 1990 have been found inhabiting relatively coarse sediments, except Triodontoderes lagahoo Cepeda et al., 2019 and Zelinkaderes floridensis Higgins, 1990. This could be due to the existence of different adaptation patterns in the remaining kinorhynch taxa not included in the present study. Although the allomalorhagid families Dracoderidae and Pycnophyidae plus the cyclorhagid genus Echinoderes constitute an extensive part of the total phylum diversity (75.5%), still another great part of kinorhynch morphological diversity is not included herein., which could possess different morphological adaptations to sediment.
It has been also hypothesized that slender, vermiform kinorhynchs tend to inhabit coarser sediments as an adaptation to the interstitial environment30. However, this hypothesis is mostly based in the presence of a thin and flexible cuticle that would make the animal more bendable when moving through the sediment particles, rather than in the shape of the body. Thus, it is likely that a combination of morphological features, including body shape and flexibility of the cuticle, among others, are responsible from defining the adaptive process of kinorhynchs to the different types of substrata.
Fluctuating asymmetry (i.e. departures from perfect bilateral symmetry) usually occurs due to the incapacity of the organisms to contain disorders from environment or endogenous conditions during its development, leading to a lesser reproductive success and survival rate31. According to our results, body asymmetry of analysed kinorhynchs is affected by pH, reflecting the largest deviations from the bilateral pattern of the sternal plates under values of pH below 7.0 (acidic) and above 8.5 (strongly alkaline) as well (see Supplementary Information). In marine sediments, pH between 7.5–8.5 is well-buffered against pH oscillations, but lower or higher values, combined with other stress factors (e.g. high temperatures, extreme salinity, etcetera) may be detrimental for meiofauna7. Indeed, previous studies have shown that meiofauna experiences episodes of high mortality after exposure to recurrent pH changes32,33,34,35.
On the other hand, animals with exoskeletons containing chitin, such as crustaceans and molluscs, suffer a significant loss of chitin under acidic pH values36,37. Kinorhynchs also possess an external cuticle with a chitinous basal layer25, and deformations in body morphology could be induced under acidic conditions. As for the possible effect of alkaline pH, it is likely that too alkaline (>8.5) values are not able by themselves to cause deviations from the bilateral symmetry of kinorhynchs. However, combined with other environmental factors such as episodes of increasing temperature and salinity, alkaline pH could induce deformations of kinorhynch sternal plates, leading to asymmetrical patterns.
The lack of genetic basis of the observed asymmetry in kinorhynchs is in accordance with the aforementioned idea about deviations from the bilateral symmetry, as these deviations usually lead to low rates of fitness and biological success in animals.
LTS are elongate, basally articulated, distally pointed cuticular appendages present in lateroventral position on segment 11 of most kinorhynch species25. The function of these spines still remains unknown, but they are the most conspicuous cuticular structures as they tend to be the largest ones compared to other appendages, projecting well beyond the end of the trunk. Another conspicuous cuticular appendage is the midterminal spine, present in some kinorhynch taxa such as the cyclorhagid orders Kentrorhagata and Xenosomata, or the allomalorhagid families Franciscideridae and Neocentrophyidae. In any case, LTS are forced to move through the sediment interstices accompanying the general movement of the animal.
According to our results, species with more shortened and widened LTS seem to occur in sediments with a wide range of different coarse particles (i.e. dominated by coarse sediments), whilst species with slender and more narrowed LTS tend to inhabit in substrata with a wide range of different fine particles (i.e. dominated by fine sediments). These results are similar to those obtained for kinorhynchs’ body shape. More robust and widened LTS could allow kinorhynchs of the analysed taxa better moving through the sediment particles in coarser sediments, actively moving and displacing the grains by exerting a greater force. In fact, LTS are the only cuticular appendages of Kinorhyncha (together with the midterminal spines) that are linked to internal muscles, meaning that the animals are able to move them38,39,40. Additionally, coarser sediments are usually a result of strong currents, so the presence of more robust, widened LTS could allow kinorhynchs clinging more tightly to the sediment particles under episodes of high hydrodynamics. It is important to note that the obtained results for the LTS adaptive shape are not necessarily applicable to kinorhynch taxa bearing an also conspicuous midterminal spine, which have not been included in the present study. Most of these kinorhynchs with a midterminal spine, also linked to internal muscles, inhabit fine sediments (Neuhaus, 2013), and a possible morphological adaptation to sediment of this cuticular appendage remains to be explored.
Moreover, species with shortened and widened LTS were mostly found in sediments with more content in organic nitrogen and more likely of marine origin, whereas species with slender and narrowed LTS were mainly found in sediments with more content in organic carbon and a significant input of terrestrial organic matter. The different proportions of carbon and nitrogen influence the abundance and composition of the micro and meiobenthos communities, influencing in the possible food sources for kinorhynchs and the complex biological interactions between the different taxa, and this could lead to the observed differences in LTS shape, rather than carbon and nitrogen affecting the physical properties of the sediment8.
Finally, a relationship between LTS’ size and three sediment variables (sorting, skewness and kurtosis) was found. Thus, larger LTS are related to sediments with many different size categories (heterogeneous) and a certain dominance of finer categories, while species with smaller LTS inhabit more homogeneous sediments with a certain dominance of coarser categories. Heterogeneous grain size distributions in marine sediments is usually linked to dynamic, intensely eroded areas, as mentioned above, or influenced by processes of bioturbation41. Additionally, heterogeneous sediments possess a more efficient grain packing than homogeneous sediments of similar size42. Sediment packing influences the amount of water that can be stored in sediment and its ease of circulation, the degree to which dissolved materials can be hosted and the strength of the sediment under shearing load43. In this context, the presence of larger LTS in such heterogeneous sediments, with more dynamism of sea-water circulation and bioturbation processes together with a larger amount of organic matter and other dissolved materials that may hinder movements, could facilitate the displacement of the animal through the interstices and furthermore favour its anchoring to the sediment particles if needed.
None of the sediment variables showed a significant influence on the primary spinoscalids shape. This result is striking taking into account that scalids are the main kinorhynch appendages used for displacement25 and consequently they should be influenced by sediment structure and composition. However, this could be explained by the lower sample size of primary spinoscalids’ micrographs (n = 22) compared to that of body shape (n = 127) and LTS (n = 99).
Source: Ecology - nature.com
