First steps toward suctorial feeding in millipedes: Comparative morphology of the head of the Platydesmida (Diplopoda: Colobognatha)

Abstract

Although most millipedes (Diplopoda) show a biting–chewing feeding mode, representatives of the so‐called Colobognatha (Platydesmida, Polyzoniida, Siphonocryptida, Siphonophorida), with their more or less reduced mouthparts, are assumed to have evolved a suctorial feeding mode, which enables them to exploit food sources like algal film and fungi hyphae. The Platydesmida are viewed as the key taxon for the understanding of mouthpart adaptations in Colobognatha, as their mouthpart elements still closely resemble those of biting–chewing millipedes. Studies of the skeletomuscular system of the Platydesmida are rare, impeding further understanding of the mouthpart evolution in millipedes. To overcome this impediment in the understanding of millipede evolution, we study the internal morphology of the head in specimens from four genera of Platydesmida: Brachycybe lecontii, Dolistenus spp., Gosodesmus claremontus, and Pseudodesmus spp. Although all Platydesmida show similarly structured skeletal elements and accompanying musculature, they are distinct from all other Diplopoda. Their head lacks eyes and organs of Tömösváry, and is pyriform and posteriorly bulging, overlapping the collum. The narrow mandibles are hidden underneath the broad genae. A previously described gnathochilarial postmentum is absent. Muscle attachment sites, such as the transverse mandibular tendon and the median septum, are reduced. The strong modifications of the head capsule, mandibles, and musculature limit the movability of the mandible for biting–chewing motions based on simulations of possible gape angles. Platydesmida likely show a scraping and slurping feeding mode, which is facilitated by the comparably well‐developed pharyngeal dilator muscles. We suggest that the Platydesmida show an intermediate state between the biting–chewing millipedes and the other suctorially feeding Colobognatha.

Feeding habits and multifunctional classification of soil‐associated consumers from protists to vertebrates

“…The ecology of Diplopoda species (including their trophic position) is not closely associated with their phylogeny; only Colobognatha are considered fluid feeders, likely by sucking on fungal hyphae or algae films (Read & Enghoff, 2009; Moritz et al ., 2021). In specific cases, feeding is linked to the species' life history and spatial preferences such as in Polyxenidae which feed on algae/lichen films and crusts, but life history is not known for most species (Alexander, 2012; Semenyuk & Tiunov, 2019).…”

A previously unknown feeding mode in millipedes and the convergence of fluid feeding across arthropods

“…The morphology of the head of nine species representing all six higher taxa (families) of the Polyzoniida, Siphonocryptida, and Siphonophorida was studied (table S1). For comparisons to the Platydesmida, already available μCT data ( 21 , 22 ) were used. All μCT data, segmentations, and digitalized histological data are deposited on Zenodo (https://doi.org/10.5281/zenodo.5215894).…”

“…Although Colobognatha have been observed on fungi or probing rotting plant material (3), the actual food intake and their internal morphology have not been documented to date. On the basis of the arrangement of muscles and skeletal elements, compared to bitingchewing millipedes and Platydesmida, with mandibles that move in a transverse plane (13,22,(51)(52)(53), the most likely movement of the mandibles in the studied millipedes is a protrusion-retraction through the minute functional mouth opening, similar to the protrusion movement of insect maxillae (30,54). Therefore, the mandibles can only be used to penetrate surfaces or to loosen particles by scraping or piercing instead of chewing.…”

“…1D), which constitute 2% of the extant millipede diversity ( 20 ). Except for Platydesmida, which show the classic transverse moving mouthpart configuration without a sucking pump and rather feed by “slurping” ( 21 , 22 ), the head morphology of the other lineages has not been studied. Here, we study the head morphology of representatives of all families within the remaining three colobognathan lineages (table S1).…”

Hábitat, agregaciones y desarrollo postembrionario del milpiés Hirudicryptus canariensis (Loksa, 1967) en el bosque de laurisilva de Tenerife (Diplopoda: Siphonocryptida)

“…The Colobognatha comprise the four taxa Platydesmida, Siphonophorida, Polyzoniida and Siphonocryptida (Blanke & Wesener, 2014), and are probably one of the least studied and most neglected millipede groups with regard to their taxonomy (Brewer et al, 2012;Read & Enghoff, 2018), biology and morphology (Manton, 1961;Hoffman, 1980;Read & Enghoff, 2009;Shorter et al, 2018). They share highly derived mouthparts, which are siphon-like in some groups (Manton, 1961) and used to feed on liquid food (Moritz et al, 2021(Moritz et al, , 2022. Colobognatha might feed on fungi, algae, or bacterially degraded substances (Lewis, 1984;Dunger, 1993;Macias et al, 2019).…”