Does sediment composition sort kinorhynch communities? An ecomorphological approach through geometric morphometrics

Ecomorphology studies the relationship between organisms’ morphology and environment features. To better understand whether the shape of the body and the appendages involved in the movement

is correlated to sediment composition in meiofaunal organisms, we study the evolved morphological adaptations to environment in selected taxa of the phylum Kinorhyncha: the allomalorhagid

families Dracoderidae and Pycnophyidae, and the cyclorhagid genus Echinoderes. The selected taxa include the most diverse groups of Kinorhyncha worldwide, representing the 75.5% of the total

phylum diversity. Widened, plump bodies and lateral terminal spines may be adaptive for species living in coarse, more heterogeneous sediments, as they could maintain a more powerful

musculature to actively displace the sediment grains applying a greater force. Conversely, slender, vermiform bodies and lateral terminal spines would represent an adaptation of species

inhabiting fine, more homogeneous sediments where there would not be much need to exert a high force to displace the sediment particles, and a more vermiform shape would even favour the

burrowing of the animal through the smaller interstices. The studied kinorhynch taxa would also be adapted to the higher velocity of the sea-water and the intense erosion and transportation

of heterogeneous sediments by possessing more robust bodies, avoiding getting laid off substratum under these conditions. These findings provide evolutionary evidence that body shape in the

studied kinorhynch groups is adapted to environment.

Morphological adaptations are frequently a response of ecological pressures and changes in environmental variables1,2. Ecomorphology can be defined as the study of the relationship between

organisms’ morphology and ecological features3,4. Indeed, environmental heterogeneity is one of the main promoters of morphological variation in animals that inhabit changeable habitats5,6.

In the context of marine ecosystems, meiobenthic habitats possess complex, dynamic interactions that are intricately combined and influenced by numerous abiotic factors7. The structure of

the sediment is one of the main meiobenthic abiotic parameters, performing a leading role in meiobenthic ecology since its features influence the degree of accessibility of meiofaunal

organisms8,9.

Soft sediments are composed of inorganic particles, organic matter and pore water, so meiobenthic organisms are strongly affected by their variations10. As for instance, the grain size of

the sediment inhabited by the organisms determines the relative availability of interstitial spaces and subsequently influences the abundance and composition of the meiofaunal communities11.

Morphological and size adaptations of meiofauna to grain size have been evidenced in different groups. Meiofauna can be divided in several categories regarding the different way of movement

through the sediment particles: interstitial forms, burrowers, epibenthic organisms and hyperbenthic taxa. Interstitial meiofauna moves among sedimentary grains without displacing them,

whereas burrowing meiofauna actively displace the particles, usually with body structures acting as spades and moved by muscles10. Most interstitial taxa (e.g. tardigrades, some harpacticoid

copepods and nematodes, a few ostracods such as Xestoleberididae, and most gastrotrichs and annelids) are stouter and plumper in finer sediments where they need to dig through the sediment

particles or live as sediment dwellers near the surface, whereas slender, vermiform species tend to inhabit in coarser sediments where they can move more easily through the interstitial

space12,13,14,15. However, some exceptions to this can be found, as certain interstitial taxa (e.g. the gastrotrich genus Musellifer Hummon, 1969, or even some kinorhynchs such as the genera

Cateria Gerlach, 1956 and Franciscideres Dal Zotto et al., 2013, or some species of Cephalorhyncha Adrianov in Adrianov and Malakhov, 1999) live in fine sediments and are rather slender and

vermiform. Burrowing meiofauna (e.g. loriciferans, most kinorhynchs and ostracods, and some annelids, harpacticoid copepods and nematodes), that moves by active displacement of the

sediment, is more frequent in finer sediments, and relationships between grain size and body shape are much more uncharted16,17,18. Other categories of meiofaunal organisms must also be

mentioned, such as the epibenthic forms (e.g. gastropods, some foraminiferans such as the Symbiodinium Freudenthal, 1962 group), which live on top of other meiofaunal organisms or algae, or

the hyperbenthic taxa (most copepods, nauplii, some annelids, nematodes and bivalves) that are able to swim through the water column, having both a more reduced relationship with sediment

features7,14.

On the other hand, the influence of organic matter on meiofaunal communities has been widely studied from a trophic point of view as it is fundamental for the productivity of meiobenthic

communities19, but its possible role in the organism shapes still remains unexplored. The carbon-to-nitrogen ratio (C/N) is a good measure of the quality of detritus whose accumulation over

sediment usually changes the physical properties of the latter, acting as a cementing agent20. Moreover, the C/N ratio also gives information on the state of the decomposition processes, as

it depends on several factors including sedimentary features, rate of microbial degradation, column water productivity and terrestrial inputs21,22. Finally, the hydrogen ion concentration

(pH) is also of relevance in meiobenthic ecology as it can induce morphological deformations and act as limiting factor for many organisms8,23.

In this regard, kinorhynchs are an ideal model to study morphology-sediment relationships since this phylum is mainly composed of burrowing meiofaunal species that inhabit a wide variety of

oceanic soft sediments24,25. The main aim of the present paper is to determine whether and how sediment features (grain size, content of organic matter and pH) affect body shape and size of

kinorhynchs, through a geometric morphometrics approach using selected kinorhynch taxa: the allomalorhagid families Dracoderidae (2.3% of the total phylum diversity) and Pycnophyidae (31% of

the total phylum diversity), and the cyclorhagid genus Echinoderes Claparède, 1863 (42.2% of the total phylum diversity). Likewise, we test if shape and size of two kinds of cuticular

appendages are also affected by sediment: lateral terminal spines (LTS) and primary spinoscalids. Primary spinoscalids are used by kinorhynchs to actively move through the sediment24,25,

whereas the LTS, of still unclear function, are in constant contact with the sediment, being very conspicuous and large in most of the groups and thus forced to move through the sediment

particles.

Most of the analysed sediment samples (n = 16) consisted in sand, with an average size of 49.44–327.8 μm. Seven samples were defined as mud, with an average size of 9.5–27.52 μm, and only

two were dominated by gravel, with an average size of 56.96–1353.9 μm. Values of sorting (σ) were generally low (mean of σ = 4.085), and hence most of the sediment samples were poorly

sorted, with the sediment spread over a large range of size classes (i.e. more heterogeneity). However, some samples had high values of sorting and were well sorted (σ up to 16.54), with

most of the sediment confined to a few size classes. Values of skewness (Sk) indicated a general trend to the asymmetry in the spread of the particle sizes towards low diameters (mean of Sk 

= −0.243), meaning that the samples contain more categories of particles with sizes under the average value (i.e. more categories of finer particles). Nevertheless, some samples had positive

values of Sk with more categories of coarser particles above the average size. Finally, values of kurtosis (K) revealed that most of the samples are leptokurtic, with a low concentration of

the particles relative to the average size (mean of K = 1.704). Some samples were determined as platykurtic (K 2 mm diameter, sand as particles from 2 mm to 63 μm, and silt (i.e. mud) as

particles from 63 μm to 4 μm51. Particles defined as clay (