Clupeiformes

Arratia, Gloria, 2018, Otomorphs (= otocephalans or ostarioclupeomorphs) revisited, Neotropical Ichthyology 16 (3), pp. 1-24 : 6-9

Alepocephali.

Alepocephaliforms ( Fig. 4b ) are characterized by the presence of parietal bones [of traditional terminology] separated by the supraoccipital; branchiostegal cartilages; one postcleithrum; epipleural bones extending forward to about abdominal vertebra 3; opercle reduced dorsally and by several absent structures such as posttemporal fossa; gas bladder; adipose fin; and urodermal bone ( Johnson, Patterson, 1996). Although general descriptions of some alepocephaliform structures, such as the skull roof bones, crumeral organs, and caudal skeletons, were published by Greenwood, Rosen (1971), new information on the posterior part of the skull roof, including extrascapulars and the ontogenetic transformation of vertebral structures and caudal skeleton, are provided below.

In comparison to clupeiforms and ostariophysans, the Alepocephali comprise a small group of 137 species, 32 genera, three families and one order, all living in marine waters ( Nelson et al., 2016). Most species of the assemblage inhabit meso- to bathypelagic environments ( Nelson et al., 2016).

Early taxonomic studies associated alepocephaliforms with clupeiforms (e.g., Berg, 1937, 1958; Gosline, 1960) and other primitive teleosts on the basis of common similarities, the traditional approach of the time. However, this can be misleading without completely understanding the order Clupeiformes as defined by Berg, which included not only the suborders Clupeoidei and Alepocephaloidei, but also several other clades, such as †Lycopteroidei, Chanoidei, Phractolaemoidei, and Salmonoidei. During the last 50 years, alepocephaliforms have been traditionally included within the Euteleostei, closer to the salmoniforms ( Greenwood et al., 1966; Markle, 1976) or specifically within the Argentinoidei ( Greenwood, Rosen, 1971; Lauder, Liem, 1983; Begle, 1992; Johnson, Patterson, 1996; Diogo, 2008; Wiley, Johnson, 2010).

The inclusion of alepocephalids within the argentinoids is based on the presence of a crumenal organ, the descended position of the distal part of the two to four epineurals, and caudal median cartilages supporting the lowermost ray of the upper caudal lobe ( Johnson, Patterson, 1996). Although those features are present in alepocephalids and argentinoids, under the new taxonomic interpretations given by molecular studies, they need further revisions. For instance:

1. A crumenal organ is a specialization of alepocephaliforms and argentinoids. It is a posterior branchial structure that was referred to as an epibranchial organ until Greenwood, Rosen (1971) named it “crumenal organ”. The main distinction between the crumenal organ and the epibranchial organ is the presence of a distinct accessory cartilage that may have arisen by segmentation from the posterior articular surface of ceratobranchial 5 in alepocephalids and argentinoids ( Nelson, 1967; Greenwood, Rosen, 1971) and in Denticeps ( de Pinna, Di Dario, 2010) . Thus, the finding of this accessory cartilage in Denticeps opened the necessity for extensive comparative studies in various teleosts.

2. The third feature proposed as shared by argentinoids and alepocephalids, the caudal median cartilages supporting the lowermost ray of the upper caudal lobe ( Johnson, Patterson, 1996) is controversial due to its variability. The caudal medial cartilages (mc) are commonly associated with the middle principal caudal rays (PR) in argentinoids (mc versus PR10 and 11) and not with the lowermost ray of the upper caudal lobe. The condition as shown in Fig. 7 for Argentina is also found in alepocephalids (see below, the section on Analysis of characters), salmonids ( Fujita, 1990; Arratia, Schultze, 1992), and other euteleosts ( Fujita, 1990).

3. The caudal skeleton is a complex structure in need of further investigation in alepocephaliforms (see below, Analysis of characters) and in argentinoids. Unlike most other euteleosts (and also in alepocephaliforms), argentinoids have one vertebral centrum bearing the parhypural and hypurals 1 and 2, a centrum that was interpreted as formed by preural centrum 1 plus ural centrum 1 [of the diural terminology] by Patterson (1970:figs. 38, 40] in Argentina sialis and preural centrum 1 plus ural centrum 1 plus uroneural 1 in Bathylagus antarcticus . However, it is unknown how many vertebral centra form this centrum that I interpret, in a preliminary way, as compound (CC in Fig. 7 ), but noting that its origin and composition is still unknown (currently under study by GA based on its ontogenetic series). A similar structure has been interpreted as a compound centrum in adult engraulids, e.g., Engraulis and Coilia , where the centrum includes preural centrum 1 plus ural centra 2 and 3+4 [of the polyural terminology] ( Schultze, Arratia, 2013:figs. 18, 19A-D), and in ostariophysans (e.g., Monod, 1968; Lundberg, Baskin, 1969; Fink, Fink, 1981; Schultze, Arratia, 1989, 2013; Fujita, 1990). However, it is unknown whether the structure interpreted as a compound centrum in ostariophysans forms the same way in different ostariophysan subgroups (see Schultze, Arratia, 2013; Wiley et al., 2015). The fossil ostariophysan † Tischlingerichthys also has a long vertebral centrum bearing the parhypural and hypurals 1 and 2 ( Arratia, 1997:fig. 67). Consequently, argentinoids differ from many other euteleost clades, and also from alepocephaliforms, in the presence of a possible compound vertebral centrum that articulates with the parhypural and hypurals 1 and 2, ventrally.

4. The most anterior uroneural or modified uroneural or stegural with an antero-dorsal membranous outgrowth is interpreted as a euteleostean synapomorphy, but its absence in argentinoids is considered to be secondary by parsimony optimization ( Wiley, Johnson, 2010). The element interpreted as the most anterior uroneural in argentinoids and alepocephaliforms is different in both groups. The most anterior uroneural has a complex structure in argentinoids. It was identified as uroneural 1 by Patterson (1970:fig. 37), Greenwood, Rosen (1971:figs. 12, 14), and Fujita (1990:figs. 56-59). According to my studies, the first and enlarged uroneural bearing an expanded membranous outgrowth is an autogenous element lying on the dorsal surface of the compound centrum in juvenile and sub-adult specimens of Argentina sialis and has an overall resemblance to the stegural of salmonids (see Arratia, Schultze, 1992; Grünbaum, Cloutier, 2010) and other euteleosts. However, the antero-lateral base of this element fuses to the dorso-lateral surface of the centrum in larger specimens, resembling a pleurostyle ( Fig. 7a, b ). Consequently, this element differs from the euteleostean stegural (that is always an autogenous element; Arratia, Schultze, 1992; Grünbaum, Cloutier, 2010), but it also differs from the pleurostyle present in ostariophysans and clupeiforms, except for Denticeps (for information on the pleurostyle see below, section on Analysis of characters). Thus, I term this element a “pseudopleurostyle” to note its different formation than that of the pleurostyle and stegural. Summarizing, there are disagreements concerning the interpretations of alepocephaliforms as argentinoids and also of alepocephaliforms as salmoniforms based on morphological characters.

These older interpretations based on morphological evidence (e.g., Greenwood et al., 1966; Greenwood, Rosen, 1971; Markle, 1976; Lauder, Liem, 1983; Begle, 1992; Johnson, Patterson, 1996; Diogo, 2008; Wiley, Johnson, 2010) have been challenged by molecular evidence, which supports the inclusion of the alepocephaliforms within the Otomorpha (see Fig. 2b, c ), specifically as sister to the Ostariophysi (Betancur-R et al., 2017). Lavoué et al. (2008), in turn, found the Alepocephaliformes - Ostariophysi affinity more likely than the Alepocephaliformes - Clupeiformes one, but no definitive conclusion was proposed.

In comparison to the clupeiforms and ostariophysans, the alepocephaliform fossil record is young (Cenozoic) and sparse. It is represented by † Carpathichthys polonicus (see Fig. 8 ) from the Miocene-Oligocene, about 30 to 23 Ma, of Carpathians (Jerzmanska, 1979) and alepocephaliform otoliths of the Mediterranean Basin, Quaternary of Italy ( Girone, 2003; Girone et al., 2006).

Figures

Fig. 4. Diagrammatic representation of different otomorph groups such as: a. clupeiformes; b. alepocephaliforms; c. gonorynchiforms; d. cypriniforms; e. characiforms; f. siluriforms; g. gymnotiforms.

Fig. 7. Caudal skeleton of Argentina sialis (SIO 66-4) in lateral view. a. photograph of specimen of 144.2 mm standard length; photograph courtesy of C. Quezada-Romegialli; b. interpretative drawing. Note that the posterior hemi-lepidotrichia of principal ray 10 is displaced. The color orange is used to denote a modified uroneural named pseudopleurostyle herein. CC = compound vertebral centrum; E = epural; H1,3,6 = hypurals 1,3,6; hsPU2 = haemal spine of preural centrum 2; naPU1 = neural arch of preural centrum 1; PR1 = 10,11,19 = principal caudal ray 1,10,11,19; PU3 = preural centrum 3; ‘UD’ = ten- don-bone urodermal; UN = uroneural.

Fig. 2. Hypotheses of Otomorpha relationships according to molecular and morphological evidence (a) and only molecular evidence (b and c). a. after Lé et al., 1993; Lecointre, 1993; Lecointre, Nelson, 1996; Arratia 1996, 1997, 1999, 2010; Wiley, Johnson, 2010; b. after Lavoué et al., 2005, Lavoué et al., 2008; Poulsen et al., 2009; c. after Near et al., 2012; Betancur-R. et al., 2013; Betancur-R. et al., 2017.

Fig. 8. Fossil otomorph in lateral view: a. Carpathichthys polonicus Jerzmanska, 1979; Miocene-Oligocene, Polish Carpathians, Europe (ZPALWr a/2004, holotype). b. Carpathichthys sp. from the same locality and age (ZPALWr N/6116). Photo- graphs courtesy of Małgorzata Bieńkowska-Wasiluk.