Bryconadenos, Weitzman & Menezes & Evers & Burns, 2005

Weitzman, Stanley H., Menezes, Naércio A., Evers, Hans-Georg & Burns, John R., 2005, Putative relationships among inseminating and externally fertilizing characids, with a description of a new genus and species of Brazilian inseminating fish bearing an anal-fin gland in males (Characiformes: Characidae), Neotropical Ichthyology 3 (3), pp. 329-360 : 334-338

Bryconadenos , new genus

Type species. Bryconadenos tanaothoros , new species by monotypy and original designation.

The list of characters below is followed by a discussion comparing the characters listed with those of similar or the same structure in certain other characid genera.

Etymology. The first part of the name Bryconadenos is from the characid generic name Brycon that is from Greek bryko to eat greedily. The word brycon is an often-used component of various generic names of small characids. The second part, adenos is from the Greek adenos meaning gland. Gender masculine.

Diagnosis. The following two characters are autapomorphic for Bryconadenos .

(1) Specimens of adult male, sexually active Bryconadenos have glandular club cells at the surface of the epidermis on the anterior part of the anal fin. These cells are organized into an organ whose cells apparently undergo holocrine secretion. Although certainly secretory, we suggest that this organ may be pheromonal in nature and associated with courtship activity. See Appendix 1 for histological details. Also, see the Discussion below for a review of the taxonomic distribution of the newly discovered club cells on the anal, pelvic, and caudal fins of male characids.

(2) There is a close articulation between the anterior and posterior facets of the basal portions of the anterior seven basal pterygiophores.

Distinguishing Characters. The remaining five characters, although useful for distinguishing Bryconadenos , are not unique to this genus.

(3) There is an increased development of the muscles involved in the movement of the anal-fin rays of males, in particular the erectors anales and the depressors anales in Bryconadenos compared to nearly all other species of the Characidae . This feature is also synapomorphy number 3 for the species of Attonitus, Vari & Ortega (2000: 120) . Although this feature is present in Bryconadenos , it is not as well-developed as in Attonitus .

(4) Specimens of adult sexually active males of Bryconadenos lack pelvic-fin hooks.

(5) A band of dark chromatophores is located on the ventrolateral portion of the body wall above the anal-fin base, a pigment pattern more developed in males of Bryconadenos than in females. This was listed as synapomorphy # 6 for species of Attonitus by Vari & Ortega (2000: 120).

(6) Body wall somewhat convex proximate to anal-fin base. This was listed as synapomorphy # 1 for species of Attonitus , by Vari & Ortega (2000: 120).

(7) Lateral-line pores surrounded by a ring of dark chromatophores or at least associated with dark chromatophores. This character is a synapomorphy uniting the single species of Bryconadenos with the three species of Attonitus . However, it is somewhat better developed in Bryconadenos , being strongly present for the entire lateral-line length whereas in Attonitus it tends to be faded or weaker posteriorly. This feature was not proposed by Vari & Ortega (2000) as a synapomorphy for the species of Attonitus .

Discussion: Certain features that distinguish Bryconadenos from most other characid genera are in part shared with a few other characid genera, especially those in Clade A of Malabarba & Weitzman (2003). Sometimes these shared features differ in detail, opening questions about their homology and they often occur in different combinations among those genera. Possible phylogenetic relationships based on a cladistic analysis using these features are unfortunately clouded by inadequate sampling of characters of not only the Clade A genera, but many characid nominal genera. Certain large Clade A genera such as Bryconamericus and Knodus that are putatively plesiomorphic for the inseminating Clade A genera are little known phylogenetically, for example see remarks by Silva (2004:55 & 59), and are therefore difficult to use with confidence, except in a very simplistic fashion, as outgroup taxa for inseminating Clade A groups. Currently the Clade A genera Knodus , with caudal fin squamation, and especially Bryconamericus , without caudal-fin squamation, lack the derived features that distinguish most other Clade A genera. At least a few species of Knodus are inseminating, indicating a possible relationships with at least some glandulocaudines, stevardiines, and other inseminating Clade A characids, but their primary sexual features, such as sperm cell structure, need further study to hypothesize a possible phylogeny of this genus and the relatively plesiomorphic genera of the Stevardiinae as those in the Diapomini.

The discussion below is arranged by character number as used for the list of Bryconadenos characters given above. Obviously this discussion is preliminary in nature, especially for those newly discovered features not previously known in characids.

(1) Only Bryconadenos appears to have club cells on the anterior part of the anal fin of sexually mature males organized into an organ, Figs. 1-2, 4 & 21 A & B, and that we suggest produces a pheromone used in courtship. This structure is absent in females, Fig. 3. A general survey of many species of stevardiines as well as Clade A and non-Clade A characids revealed that a wide variety of characids have club cells concentrated at the surface of the epidermis of parts of the anterior region of the anal fin of sexually mature males. These club cells are often associated with the bony hooks present on the anal-fin rays. Ordinarily in otophysans club cells are confined to the deeper skin layers of the epidermis in many parts of the body’s surface and function as alarm substance pheromone cells. Hyphessobrycon diancistrus Weitzman is a good example of a characid with club cells at the surface of the epidermis associated with anal-fin hooks of adult males. The white tissue masses associated with the two remarkably large anal-fin hooks of males in this species were previously thought to be a collection of mucus cells, but they remained histologically uninvestigated. The presence and distribution of skin surface club cells in the anal-fin and sometimes in the pelvic-fin, where they are often associated with fin-ray hooks in sexually mature males, remains to be investigated and recorded in detail in characid taxa. Menezes et al. (2003) recorded the presence of club cells at the surface of the pelvic-fin epidermis of Planaltina myersi Böhlke and especially P. glandipedis , both Clade A species currently placed in the Diapomini of the Stevardiinae . We recently discovered that the caudal-fin apparent pheromone cells of species of the glandulocaudine genera Lophiobrycon , Glandulocauda , and Mimagoniates , subfamily Glandulocaudinae , are actually club cells, not derived mucous cells as described for Corynopoma riisei , tribe Stevardiini , subfamily Stevardiinae , byAtkins & Fink (1979).

(2) Fig. 5 illustrates a close articulation between the basal anterior and posterior facets of the basal portions of the anterior seven basal anal-fin pterygiophores of an adult male Bryconadenos tanaothoros , a derived feature that includes more fin-ray bases in adult Bryconadenos males than in adult males of Attonitus , Fig. 6. Relatively long ligaments in most characids attach the posterior and anterior facets of these basal pterygiophores to each other. However, only relatively short ligaments attach the basal pterygiophores of the species of Attonitus . The first six anterior basal and the first six middle pterygiophores are fused to each other in Bryconadenos whereas in A. irisae at least, the first three anterior basal and the first three middle pterygiophores are solidly fused. Compare Figs. 5 & 6. The basal pterygiophores of Bryconadenos are not expanded in the sagittal plane as in the species of Attonitus .

(3) Compared to at least most other characids Bryconadenos has an increased development of the muscles involved in the movement of the anal-fin rays of males, in particular the erectors anales and the depressors anales. A similar but more developed modification is also present in the species of Attonitus as described by Vari & Ortega (2000). Bryconadenos as in the species of Attonitus has the soft connective tissues and ligaments associated with these muscles strongly developed compared to most characids (compare Figs. 5 & 6). Thus in these structures Bryconadenos apparently displays some of the features synapomorphic for the species of Attonitus , but with a more plesiomorphic condition in Bryconadenos .

(4) Sexually active Bryconadenos males lack pelvic-fin hooks. There is much variation regarding the presence or absence of hooks on the pelvic fins of characid species, including the inseminating species of Clade A. Presumably the presence or absence of anal-fin hooks in males of these taxa is associated with variation in courtship activity. For example, all known species of Attonitus have numerous pelvic-fin hooks in adult sexually active males, but in the species of the nominal genus Bryconamericus and the apparently related species of the nominal genus Knodus , hooks are not consistently present among their respective species. However, because the phylogenetic relationships in these nominal genera essentially remain unstudied and uncertain and the possible presence versus absence of insemination in the species of these genera is nearly unknown, little can be interpreted from our incomplete survey of the species. The type species of Bryconamericus , Bryconamericus exodon Eigenmann (USNM 181813), so far as we could determine by histological examination, is a non-inseminating species, but does have pelvic-fin hooks in adult males as do adult males of Bryconamericus alpha Eigenmann (USNM 285343), and Bryconamericus iheringi (Boulenger) (USNM 285884). However, adult sexually active males of Bryconamericus deuterodontoides Eigenmann (USNM 349407) lack pelvic-fin hooks as do male specimens of Bryconamericus alfredae Eigenmann (ANSP 143357), and Bryconamericus stramineus Eigenmann (USNM 325698). The inseminating species of the non-Clade A Brittanichthys axelrodi Géry (USNM 198132, holotype) and presumably inseminating species Brittanichthys myersi Géry (USNM 198131, holotype) lack pelvic-fin hooks, but have highly derived autapomorphic caudal-fin structures bearing hooks that immediately distinguish this genus from any other characid genus (see also Malabarba & Weitzman, 1999: 425-426 and Géry 1965: fig. 6, and Burns & Weitzman, 2005). Note that histological examination of the caudal modifications in Brittanichthys axelrodi revealed no modified mucous cells or club cells. Most species of Creagrutus are known to have pelvic-fin hooks, including the two known to be inseminating, Creagrutus melasma Vari, Harold, & Taphorn (1994) and Creagrutus lepidus Vari et al. (1993) , see Vari & Harold (2001). Sexually active adult males of Hollandichthys multifasciatus (Eigenmann & Norris) (USNM 297983 & USNM 320271) have pelvic-fin hooks and are inseminating, but do not belong to Clade A.

To further complicate phylogenetic implications of the features in the genera discussed here, inseminating and non-inseminating species occur in Knodus as it is currently defined.Adult males of K. meridae Eigenmann (USNM 121469), the type species of the genus which is apparently non-inseminating and has pelvic-fin hooks in sexually active adult males.Also, adult sexually active male K. septentrionalis Géry (USNM 361168) lack pelvic-fin hooks, but sexually active males of K. savenensis Géry (USNM 196088, holotype) and Knodus breviceps (IUM 17249), both apparently non-inseminating species, bear pelvic-fin hooks. One inseminating species currently assigned to Knodus (USNM 362386), has adult sexually active males with pelvic-fin hooks, while another inseminating species that may tentatively be considered a species of Knodus , K. pectinatus (Vari & Siebert) (USNM 303441, paratypes) is without pelvic-fin hooks in adult sexually active males. Finally adult sexually active males of at least two undescribed species of Monotocheirodon (MUSM 6756 & MUSM 11082) and sexually active males of M. pearsoni Eigenmann (CAS 59792, paratypes), all inseminating and perhaps related to inseminating Knodus species because of some sperm cell similarities that need further study, have derived pelvic-fin hooks that are unique to this genus so far as known. So far the presence or absence of club cells in association with the pelvic fins of these species remains unrecorded. An undescribed species referred to Monotocheirodon by Collette (1977: 238) and Zanata & Akama (2004:51) and described as having breeding tubercles is currently considered by us to belong to an undescribed species of Othonocheirodus . The specimens examined by Collette (1977) and referred to by Zanata & Akama (2004) are sexually mature adult males from ANSP 144106, Ecuador, Provence Zamora Chinchipe, backwaters of the río Zamora, tributary to the río Santiago, tributary to the río Marañon, 12 km northeast of the town of Zamora. (5) Dark band of chromatophores along the ventral portion of body wall in the region of the anal-fin base. Vari & Ortega (2000:118) used this feature as a synapomorphy for the three species of Attonitus . We found this character in Bryconadenos , Figs. 3, 4, 7 & 8 of a male and female, to be similar to its occurrence in Attonitus . We tentatively agree with Vari & Ortega regarding the use of this feature as a possible synapomorphy for the obviously closely related species of Attonitus . However, we find this character problematic for use as a synapomorphy uniting Bryconadenos with Attonitus . A black pigment line along the anal-fin base of many characins is relatively common although often weakly developed. As in the species of Attonitus , this pigment feature is more weakly developed in females than males and it apparently is not equally developed among the species of Attonitus . This pattern of distribution of this pigment is widespread among characids and primarily occurs on the lateral surface of the articular bases of the anal-fin rays. Many non-Clade A characids such as some or a few species of Brycon , Astyanax , Moenkhausia , Hemigrammus , Paracheirodon , and Bryconops have this pigment pattern modestly developed. It seems likely that black pigment along the anal-fin base in the Characidae may have evolved independently or been lost independently many times. The intensity or full adult development of this pigment pattern varies much in preserved specimens of characids and this raises at least several categories of problems regarding its use in phylogenetic reconstruction. First, in specimens in collections intensity of dark pigment preservation initially depends on the method of fixation and the behavioral condition of the specimens when fixed in the field. Also dark pigment pattern intensity of specimens when caught can depend on local ecological factors such as clarity of the water and darkness or lightness of the substrate. Further, the possibility of fading during time spent in a collection and exposure to daylight or artificial light must be considered. These factors make it difficult to evaluate what may have been the natural intensity of a dark pigment in preserved fishes. However, in keeping literally hundreds of species of Neotropical characids alive for over sixty years, the senior author has noted much variation in the intensity of this and other dark color patterns in characids, depending on the species and genera as well as on the behavorial state of a particular species. Thus, although intensity of dark color patterns may certainly be a phylogenetically meaningful data source, they may be difficult to use. Nevertheless in some characids this pigment pattern has become considerably derived. For example, in the three miniature species of the cheirodontine genus Spintherobolus ( Weitzman & Malabarba, 1999: figs. 15, 29-37) this pigment has become especially dark and presumably extended onto several of the posterior rays of the anal fin. This basal anal-fin pigment pattern is also dark and well-developed in some Clade A characids, but not so derived as in Spintherobolus . For example, see the stevardiine Ptychocharax rhyacophila Weitzman et al. (1994:40-47 , figs. 1-2) where it is strongly developed. Also, the non-glandulocaudine Clade A characid Caiapobrycon tucurui Malabarba & Vari (2000:319 , figs 2 and 3) has this pattern well-developed, but less so in the female. Because the Clade A cladogram of Malabarba & Weitzman (2003: 87, fig. 11) indicates that these two Clade A genera are not closely related to Attonitus or Bryconadenos and because a few dark chromatophores occur on the ray bases of many Clade A characids we believe it is best to use this character as a synapomorphy when it is distinctly derived as for example in the non-Clade A characid genus Spintherobolus .

(6) Convexity of body wall proximate to the anal-fin base. This feature was thoroughly discussed by Vari & Ortega (2000: 115-116) who found no outgroup characiforms that have a similar feature and that could be considered closely related to Attonitus . The only Clade A characid we found to have this characters is Bryconadenos which has this character much less developed than in the species of Attonitus , but may be indicative of a relationship. phores or at least associated with dark chromatophores. As noted above this character was not utilized by Vari & Ortega (2000), but we found no Clade A or other characids with this feature.

Note: The following three characters used as synapomorphies for the species of Attonitus by Vari & Ortega (2000: 120) are absent in the type species of Bryconadenos . These remain synapomorphies for the species of Attonitus . (1) Expansion of the anterior basal pterygiophores and realignment of the distal portion of the basal pterygiophores into a gentle arch in mature males. (2) Disparity in the relative size of the inner and outer premaxillary tooth rows, with a posterior curvature of the distal portions of the teeth on the inner tooth row and anterior curvature of the distal portions of the teeth in the outer tooth row. (3) An anteroventral curvature of the anterior portion of the dentary with a consequent anterodorsal orientation of the anterior dentary teeth and a distinct concavity of the ventral profile of the anterior portion of the dentary.