The filter pads and filtration mechanisms of the devil rays: Variation at macro and microscopic scales

Abstract

Three lineages of cartilaginous fishes have independently evolved filter feeding (Lamniformes: Megachasma and Cetorhinus, Orectolobiformes: Rhincodon, and Mobulidae: Manta and Mobula); and the structure of the branchial filters is different in each group. The filter in Rhincodon typus has been described; species within the Lamniformes have simple filamentous filters, but the anatomy and ultrastructure of the branchial filter in the mobulid rays varies and is of functional interest. In most fishes, branchial gill rakers are elongated structures located along the anterior ceratobranchial and/or epibranchial arches; however, mobulid gill rakers are highly modified, flattened, lobe-like structures located on the anterior and posterior epibranchial elements as well as the ceratobranchials. The ultrastructure of the filter lobes can be smooth or covered by a layer of microcilia, and some are denticulated along the dorsal and ventral lobe surface. Flow through the mobulid oropharyngeal cavity differs from other filter-feeding fishes in that water must rapidly deviate from the free stream direction. There is an abrupt 90° turn from the initial inflowing path to move through the laterally directed branchial filter pores, over the gill tissue, and out the ventrally located gill slits. The deviation in the flow must result in tangential shearing stress across the filter surface. This implies that mobulids can use cross-flow filtration in which this shearing force serves as a mechanism to resuspend food particles initially caught by sieving or another capture mode. These particles will be transported by the cross filter flow toward the esophagus. We propose that species with cilia on the rakers augment the shear mediated movement of particles along the filter with ciliary transport.

A dated molecular phylogeny of manta and devil rays (Mobulidae) based on mitogenome and nuclear sequences

“…Mobula contains nine currently recognized species: M. japanica (Müller and Henle, 1841), M. mobular (Bonnaterre, 1788), M. tarapacana (Philippi, 1892), M. thurstoni (Lloyd, 1908), M. kuhlii (Müller and Henle, 1841), M. eregoodootenkee (Bleeker, 1859), M. hypostoma (Bancroft, 1831), M. rochebrunei (Vaillant, 1879);and M. munkiana (Notarbartolo di Sciara, 1987). Morphologically, Manta is distinct from Mobula in exhibiting a terminal mouth, a broader head relative to maximum disc width (DW), and morphometrics of the spiracles (Compagno and Last, 1999;Notarbartolo di Sciara, 1987) and structure of filter plates (Paig-Tran et al, 2013). The two Manta species show differences in maximum DW (M. birostris and M. alfredi, 700 and 500 cm respectively), coloration patterns, dentition, denticle and spine morphology (Marshall et al, 2009).…”

“…The two Manta species show differences in maximum DW (M. birostris and M. alfredi, 700 and 500 cm respectively), coloration patterns, dentition, denticle and spine morphology (Marshall et al, 2009). Mobula species share a ventral placement of the mouth, and can be distinguished from each other by maximum DW, coloration, skin, presence or absence of a vestigial caudal spine, structure of filter plates (Paig-Tran et al, 2013), and morphometrics of pectoral fins, tails, cephalic lobes and spiracles (Notarbartolo di Sciara, 1987). M. birostris, M. alfredi, M. mobular, M. japanica and M. tarapacana are among the larger rays in the family, with maximum DWs of 700, 500, 520, 370 and 310 cm respectively (Couturier et al, 2012).…”

Phylogeny of the manta and devilrays (Chondrichthyes: mobulidae), with an updated taxonomic arrangement for the family

“…rochebrunei and M. mobular/M. japanica that suggest they may possibly be conspecifics (Notarbartolo di Sciara, 1987;Paig-Tran et al, 2013;Poortvliet et al, 2015;Henderson et al, 2016). Phylogenetic inferences based on morphology have either been more concerned with the phylogenetic placement of mobulids within Myliobatiformes rather than the relationships among mobulids, or have focused on the evolution of particular structures.…”

“…The remaining two clades comprise the smaller species M. kuhlii-M. eregoodootenkee-M. thurstoni and M. munkiana-M. rochebrunei-M. hypostoma. Despite this progress in characterizing mobulid diversity, mobulid taxonomy overall remains largely unresolved due to a very complicated nomenclatural history and the fact that phylogenetic inferences have been limited by gaps in taxonomic and/or genomic sampling. Notable long-standing uncertainties regarding mobulid taxonomy include the validity of the genus Manta (Herman et al, 2000;Adnet et al, 2012;Paig-Tran et al, 2013;Naylor et al, 2012b;Aschliman, 2014;Poortvliet et al, 2015), as well as distinguishing species boundaries from intraspecific geographical variants within multiple lineages of Mobula. Specifically, gross morphological and/or genetic similarities have been noted between species pairs M. kuhlii/M.…”

Paleogene origin of planktivory in the Batoidea

“…A transition such as this one would require robust protection of the gill filaments from abrasive sediments as well as some means of cross-flow filtration or a sieve-like gill apparatus to strain benthic meiofauna from the sediment. The former method, cross-flow filtration, has already been evidenced in mobulids, the immediate sister taxa to Rhinoptera (Paig-Tran et al, 2013;Paig-Tran and Summers, 2014). …”