Bioacoustics of Brachyhypopomus

Description. Members of the genus exhibit relatively little variation in body and head shape, and are generally delimited by a combination of morphometric and meristic characters. For brevity, we describe here external characters common to all congeners rather than repeating these in each of the species descriptions and redescriptions presented below. Maximum known body size 461 mm TL (see redescription of B. brevirostris ). Body elongate and laterally compressed (body width as percentage of body depth 36.4- 82.1% and 18.9-51.7% at anal-fin origin and anal-fin middle respectively), reaching maximum width and depth in posterior region of body cavity and tapering gently posteriorly; short to very long caudal filament located posterior to the anal-fin terminus (4.2-54.5% TL; 7.4-83.1% LEA in intact specimens) – comprising mostly electrocytes, vertebral centra or a cartilaginous rod-like structure, and associated blood vessels and nerves ( Albert, 2001 ). Greatest body depth and width located in area of body cavity or slightly posterior to body cavity, lateral sides of body more or less straight in dorsal view posterior to abdominal cavity. Dorsal profile of body straight or nearly straight in lateral view. Single hypaxial electric organ (EO) extending just posterior to the urogenital orifice to the end (or near end) of the caudal filament; 1-6 bilateral horizontal (length way) columns of electrocytes along its length, 3-6 columns at anal-fin terminus, and 2-6 columns at a midpoint between anal-fin terminus and end of caudal filament. Paired subdermal accessory EO of unknown function in the opercular region are known from three species: B. bombilla , B. menezesi , and B. regani . Anal fin elongate (71.6-94.0% LEA) with origin located in anterior portion of body cavity, posterior to cleithrum of pectoral girdle; 143 to 293 rays (branched and unbranched combined). Each anal-fin ray connected via a ball-and-socket joint to a proximal anal-fin pterygiophore, and articulated in circular movements by the pinnalis analis muscles ( Ellis, 1913 ). Anal-fin pterygiophores shorter than hemal spines at midbody. Pectoral fin short to moderate (longest pectoral ray 3.2- 8.5% LEA), broad and distally rounded or pointed, with 10-21 rays (branched and unbranched combined). Dorsal, adipose, and pelvic fins, and pelvic girdle absent, in common with all gymnotiforms. Caudal fin absent in common with all Rhamphichthyoidea , Sternopygidae , and Gymnotidae -although see de Santana et al. (2013) for comments on the caudal skeleton of Electrophorus . Body cavity restricted to no more than 2.5 head-lengths posterior to occiput, with viscera rotated so that the anus and urogenital orifice are positioned below the operculum, near the isthmus. Anus and urogenital orifice in close juxtaposition. Urogenital papilla developed into elevated tube in breeding males and females. Transparent and thinwalled non-vascularized and non-physostomous swim bladder, comprising a smaller anterior chamber, and a larger posterior chamber ( Ellis, 1913: 189 , fig. 32). Body cavity short, with 15-26 precaudal vertebrae (including up to 3 transitional vertebrae). 1-3 slender displaced hemal spines embedded in hypaxial musculature posterior to body cavity, sometimes forked with bifurcated portions facing anteriorly. Scales cycloid, with irregular ovoid shape; smaller dorsally and ventrally and larger laterally, especially in posterior region of body; partially or completely covered with skin and distributed over all of post-cranial portion of body except fins (exceptions are the absence of scales along the middorsal region of anterior third of body and over the anal-fin pterygiophores in B. benjamini and B. provenzanoi ). 4-9 rows of lateral line scales above lateral line to dorsal midline at midbody. Anterior-most perforated lateral line scale located near vertical through pectoral-fin origin. Lateral line continuous in most species anterior to anal-fin terminus, but not continuing to end of caudal filament; usually terminating in the middle portion of the caudal filament. Dorsal branch of posterior lateral line nerve separate from recurrent ramus of anteroventral lateral line nerve ( Albert, 2001 : character 117 therein). No fleshy dorsal electroreceptive organ (as in the Apteronotidae ). Body variably pigmented with dark bands and mottled patterns of stellate chromatophores and subcutaneous pigment, but never translucent as in several sternopygid taxa, notably many Eigenmannia and Rhabdolichops species ( Crampton, 2007 ). Chromatophores contract at night resulting in a striking pale appearance of most Brachyhypopomus under artificial illumination; even those that are very darkly pigmented during the day. Ampullary electroreceptors in rosettes, with highest density on snout and around mouth. Schreckstoff club cells and observable fright response absent ( Fink & Fink, 1981 : character 117 therein). Head widest in opercular region and deepest in occipital region. Eye small to relatively large in size (5.9-20.6% HL), laterally positioned on dorsal half of head, visible in dorsal view, and completely covered by thin translucent epidermis (orbital margin not free). Mouth small and terminal or slightly to moderately sub-terminal; closed lips meet ventral to a horizontal through ventral margin of eye. 3-7 small, needle-like premaxillary teeth present in all examined small juveniles (< 50 mm TL) but absent in adults except in B. bennetti and B. walteri ( Sullivan et al. , 2013 ) . Dentary edentate in adults, although small conical dentary teeth present in all examined small juveniles (< 50 mm TL). Maxilla edentate. Premaxillary and maxillary portions of upper jaw gently convex anteriorly, joining to form a slight concave angle or moderate to acute sigmoidal profile to upper jaw. Anterior and posterior nares present; both either ellipsoid or circular in shape. Anterior nares located at upper lip. Posterior nares located near eye (1.1-10.4% HL from anterior margin of orbit). Dorsal and ventral profile of head from almost straight to strongly convex. Snout short (18.7-32.6% HL) and rounded. Cephalic lateral line canals and pores complete in adults, with pores conspicuous ( de Santana & Crampton, 2011: 1104 , fig. 2) – with the following two exceptions: i. The antorbital is absent in B. bennetti and B. walteri ; ii. The branch of the infraorbital canal over the frontal is absent in B. alberti , B. arrayae , B. belindae , B. hamiltoni , and B. verdii . Branchial opening restricted to a short vertical aperture at posterior margin of opercle, branchial membranes joined at isthmus. 25-63 gill filaments on first arch. Sexual dimorphism of cranial morphology absent in all species in contrast to its presence in many apteronotid taxa ( Albert & Crampton, 2009 ; de Santana & Vari, 2010 ; Fernandes et al. , 2002 ) and in the sternopygid genus Archolaemus ( Vari et al. , 2012 ) . Functional biology and ecology. Specializations associated with the Electrogenic and Electrosensory system : As with other Gymnotiformes , Brachyhypopomus species exhibit a suite of morphological specializations associated with active electroreception and nocturnal activity. The eyes are reduced in size and retinal projections to the brain are much reduced ( Lázár et al. , 1987 ). A culteriform (knife-shaped) body plan facilitates maximum dipole separation of the fish as a dipole source (and therefore maximizes field strength per unit body mass, Stoddard et al. , 1999 ), and optimizes use of the body surface as a relatively rigid electroreceptive array. Locomotion by undulation of the elongated anal-fin permits backwards-forwards electroreceptive rostral probing (‘scan swimming’ sensu Julian et al. , 2003 ) ( Albert & Crampton, 2005 ; Lannoo & Lannoo, 1993 ; Lissmann, 1961 ; Nanjappa et al. , 2000 ; Stoddard et al. , 1999 ) (in addition to anal-fin locomotion, Brachyhypopomus also swim in rapid bursts by anguilliform movement of the body when startled, Ellis, 1913 ). Body rigidity is augmented by ossified intermuscular bones ( Schlesinger, 1910 ). Most of the post-cranial body and caudal filament is specialized for electrogenesis, with the body cavity confined to an area extending no more than 2.5 head-lengths posterior to the occiput ( Ellis, 1913: 189 , fig. 32). Electric Organs: The hypaxial electric organ (EO) comprises myogenic electrocytes (derived from muscle cells). Studies of B. gauderio demonstrate that the EO develops from the ventral hypaxial musculature in larvae, and is retained through development ( Franchina, 1997 ). Initially the EO comprises cylindrical, overlapping stalk-less electrocytes, but these later shorten along the rostrocaudal axis, separate into vertically aligned “rows”, and form stalklike caudal projections onto which the spinal electromotor neurons terminate ( Bass, 1986: 16 , fig. 1; Franchina, 1997: 115-117 , figs. 7-10). EODs are first generated six days after hatching, at 7 mm TL in B. gauderio ( Franchina, 1997 ) , and at 6-8 mm in B. beebei ( Westby, 1988 ) . Beyond the late larval stage (TL> 37 mm ), the EO of B. gauderio extends parallel to the body axis along the entire ventrolateral margin, from near the gill isthmus to the tip of the caudal filament (although in some species the distal portions of the caudal filament are sometimes free of electrocytes, especially in breeding males; see descriptions and redescriptions herein). The adult EO of Brachyhypopomus comprises 3-6 bilateral longitudinal (horizontal) columns of cylindrical or box-shaped electrocytes bound by connective sheaths ( Bass, 1986 ; Bennett, 1961 ; 1971a ; Franchina, 1997 ; Hopkins et al. , 1990 ; Stoddard et al. , 1999 ). An opercular accessory electric organ distinct from the main hypaxial EO was first reported by Sullivan (1997) for B. regani (listed as B. electropomus ), and has also been discussed by Crampton & Albert (2006) and Carvalho (2013) . Caputi (1999) and Caputi et al. (1998) review how the synchronized activity of electrocytes in the EO of B. gauderio – combined with the filtering properties of the skin and tissue of the fish, and the load of the surrounding water – determine in ensemble the spatiotemporally complex “near field” discharge that sums to the head-to-tail recorded EOD recorded in the far field. Impedance matching: Impedance matching of electric organ anatomy to narrow ranges of conductivity has been noted in several species ( Crampton, 1998a ; Hopkins, 1999 ). Brachyhypopomus bullocki and B. brevirostris , which are restricted to low conductivity systems (<30 µScm-1 ) exhibit a predominantly serial arrangement of electrocytes in the caudal portion of the organ (longer caudal filaments comprising relatively few horizontal bilateral columns of electrocytes). In contrast, B. bennetti , B. diazi , and B. occidentalis (and also B. palenque , see description herein), which are restricted to high conductivity systems (>60 µScm-1 ), exhibit a parallel arrangement of electrocytes (short caudal filaments with more electrocyte columns). The possibility that conductivity may serve as a barrier to the dispersal of some species, and consequently play a role in reproductive isolation, has been suggested by Crampton (1998a ; 2011 ) and Hopkins (1999) . Electric Organ Discharges: Crampton & Albert (2006) reviewed the diversity of head-to-tail recorded EODs in Brachyhypopomus . Of 18 species for which EOD data have been presented, 12 generate biphasic or nearly biphasic EODs with durations varying from ca . 0.5-5 ms. One species, B. bennetti , generates a monophasic EOD. Five species generate relatively short (0.5 - 1.5 ms), more complex triphasic or tetraphasic EODs ( Crampton & Albert, 2006 ). Monophasic larval EODs have been documented in B. beebei , B. brevirostris , B. gauderio , and B. occidentalis , and this is presumed to be the case in other congeners, as in all other gymnotiforms ( Crampton & Albert, 2006 ). The EOD pulse rate of Brachyhypopomus varies from ca . 2 to 110 Hz, and typically increases from a lower resting day-time rate to a higher nocturnal active rate ( Crampton & Albert, 2006 ). Assad et al. (1999) , and Stoddard et al. (1999) map heterogeneity of the near-field recorded EOD of B. beebei , B. gauderio , and B. walteri . There is a rich and rapidly growing literature on the behavior, neuroethology, physiology, energetics, and hormonal basis of EOD generation and EOD plasticity in Brachyhypopomus – focused primarily on the model species B. gauderio , which is reviewed in part by Assad et al . (1999 , 1998), Stoddard (2006) , Gavassa et al. (2013) , Markham (2013) , Silva et al. (2013) , and Salazar et al. (2013) . Electroreceptors: In common with all other gymnotiforms, Brachyhypopomus possess a cutaneous array of ampullary and tuberous electroreceptors. Ampullary electroreceptors are tuned to low frequencies and facilitate passive electroreception of weak, lowfrequency bioelectric fields. Tuberous electroreceptors are typically tuned to higher frequencies and facilitate both the active electrolocation of objects, and the passive detection of electric fields from other fish – an important component of electrocommunication ( Hopkins, 2005 ; Hopkins et al. , 1997 ). The morphology of ampullary and tuberous electroreceptors in Brachyhypopomus , their distribution over the body surface, and their directional sensitivity are among the best known of all gymnotiforms, having been described by Bullock et al. (1961) , Hagiwara et al. (1962) , Szamier & Wachtel (1970) , Bennett (1971b) , Szabo (1974) , Yager & Hopkins (1993) , and McKibben et al . (1993) . Tuberous electroreceptor frequency responses in the genus, showing a correspondence of electroreceptor tuning with peak frequency characteristics of the EOD, are described by Bastian (1976 ; 1977 ) and Hopkins & Heiligenberg (1978) . Groove-like depigmented epidermal canals leading to tuberous electroreceptors, and which therefore may play a role in active electroreception are known from all members of the genus. Sullivan (1997) noted for B. diazi and B. occidentalis that “Microscopic examination and histological sections of these canals show them to be narrow tubes overlying one or more scales with an external pore anteriorly and a tuberous electroreceptor at the posterior end (J. Sullivan and C. Hopkins unpubl.).” The epidermal canals of Brachyhypopomus vary in abundance between species (see species descriptions and redescriptions herein) but are mostly located in the posterior half of the body – where they are restricted to nearby and either side of the lateral line, either side of the dorsal midline, and approximately midway between the lateral line and dorsal midline. In B. diazi the epidermal canals cover a larger area of the body than in congeners, including much of the dorsal and ventral flank of the anterior half of the body. Groove-like epidermal canals are also observable in all other hypopomid genera sensu Maldonado-Ocampo (2014) , including Akawaio , Hypopomus , Procerusternarchus , and (in considerably lower densities), in Microsternarchus and Racenisia . Auditory sensory apparatus: In addition to providing buoyancy, the swim bladder of Brachyhypopomus is involved in the ostariophysan hearing system, which involves a connection from the anterior chamber of the swim bladder to the stato-acoustic organ of the inner ear via the Weberian ossicles encased by the first four vertebrae. A pseudotympanum, a window-like thinning of the hypaxial muscles lateral to the anterior portion of the swim bladder is present, and comprises three distinct hiatuses in the obliquus inferioris and obliquus superioris muscles ( Dutra et al. , 2015 ). The pseudotympanum may enhance sound detection by acting as a window through which sound waves reach the anterior chamber of the swim bladder ( Dutra et al. , 2015 ). Adaptations to hypoxia : The influence of dissolved oxygen on the distributions of Brachyhypopomus is discussed by Crampton (1998b ; 2011 ; 2008 ) and Crampton & Albert (2006) . Species that occur in seasonally or perennially dysoxic habitats such as whitewater floodplains and terra firme swamps are adapted to survive protracted periods of hypoxia (<1 mgl-1 ) or complete anoxia, while those that occur in permanently normoxic habitats, such as terra firme streams, are not ( Crampton, 1998a ,b). Some species are able to tolerate hypoxia by undertaking aerial gill respiration – either by periodically aspirating air bubbles into their gill chambers, or by opening their mouths at the surface meniscus to expose the gill lamellae to air ( Crampton, 1998b ; Hopkins, 1991 ). Carter & Beadle (1931) reported an expanded gill chamber, unusually long gill lamellae, and greatly expanded secondary folds of the gill lamellae in B. “brevirostris ” (probably B. gauderio ) from the Paraguayan Chaco , and also concluded that the air bladder and gill chamber epithelium play no significant role in air breathing. Crampton et al. (2008) reported that species endemic to seasonally anoxic whitewater floodplain habitats exhibit significantly larger gills than species endemic to permanently normoxic terra firme stream systems. Many species of Brachyhypopomus also exhibit a reduction of activity and EOD pulse rate in response to declining oxygen levels ( Crampton, 1998b ). Regeneration: Brachyhypopomus species , as in other Rhamphichthyoidea and Sternopygidae , are able to regenerate the entire post-coelomic portion of the body following damage from predators, with the vertebrae replaced by a rigid cartilaginous rod ( Albert, 2001 ; Albert & Crampton, 2005 ; Ellis, 1913 ; Sullivan et al. , 2013 ). The proportion of individuals with caudal filament damage in natural populations has been estimated for three species: B. brevirostris – 8% ( Ellis, 1913 ); B. draco – 6.7%, with 22.1% exhibiting regeneration from earlier damage ( Cognato et al. , 2007 ); B. occidentalis – varying among populations from 12% to 46% ( Dunlap et al. , 2016 ). Hopkins et al. (1990) and Sullivan et al. (2013) documented how damage to portions of the body posterior to the body cavity can influence the EOD waveform. Reproductive anatomy: In B. gauderio , the males develop a paired, lobular testis of the unrestricted spermatogonial category, and females develop a paired saccular cystovary. In both sexes the gonads are positioned ventrally, and expand posteriorly until they reach the posterior wall of the abdominal wall ( Quintana et al. , 2004 ). Gonadal morphology appears to be similar in other species. França et al. (2007) and Giora & Burns (2011) describe the ultrastructure of spermatozoa in Brachyhypopomus .