JOURNAL OF MORPHOLOGY 000:000–000 (2012) Structural Adaptations for Ram Ventilation: Gill Fusions in Scombrids and Billfishes Nicholas C. Wegner,1,2* Chugey A. Sepulveda,3 Scott A. Aalbers,3 and Jeffrey B. Graham1 1Center for Marine Biotechnology and Biomedicine, Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093 2Fisheries Resource Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, California 92037 3Pfleger Institute of Environmental Research, Oceanside, California 92054 ABSTRACT For ram-gill ventilators such as tunas and mized, both respiratory and swimming efficiency mackerels (family Scombridae) and billfishes (families are increased (Freadman, 1979, 1981; Steffensen, Istiophoridae, Xiphiidae), fusions binding the gill lamellae 1985). However, at the relatively high swimming and filaments prevent gill deformation by a fast and con- speeds attained by scombrids and billfishes, ram tinuous ventilatory stream. This study examines the gills ventilation poses two challenges. First, the ram- from 28 scombrid and seven billfish species in order to determine how factors such as body size, swimming ventilatory current must be slowed to create opti- speed, and the degree of dependence upon ram ventilation mal flow conditions for efficient gas exchange at influence the site of occurrence and type of fusions. In the the respiratory lamellae (Brown and Muir, 1970; family Scombridae there is a progressive increase in the Stevens and Lightfoot, 1986; Wegner et al., 2012). reliance on ram ventilation that correlates with the elabo- Second, the gills must be reinforced in order to ration of gill fusions. This ranges from mackerels (tribe maintain normal orientation with respect to a Scombrini), which only utilize ram ventilation at fast high-pressure branchial stream, the force of which cruising speeds and lack gill fusions, to tunas (tribe Thun- increases with swimming speed (Muir and Ken- nini) of the genus Thunnus, which are obligate ram venti- dall, 1968; Brown and Muir, 1970). Recent work by lators and have two distinct fusion types (one binding the Wegner et al. (2010) showed that the morphomet- gill lamellae and a second connecting the gill filaments). The billfishes appear to have independently evolved gill rics of scombrid and billfish gills (e.g., shape, size, fusions that rival those of tunas in terms of structural and number of gill lamellae) increase branchial re- complexity. Examination of a wide range of body sizes for sistance and help slow ram-ventilatory flow. To some scombrids and billfishes shows that gill fusions increase the overall rigidity of the branchial sieve, begin to develop at lengths as small as 2.0 cm fork length. some scombrids and billfishes have structural sup- In addition to securing the spatial configuration of the gill ports in the form of gill fusions (Muir and Kendall, sieve, gill fusions also appear to increase branchial resist- 1968; Muir, 1969; Johnson, 1986; Wegner et al., ance to slow the high-speed current produced by ram ven- 2006). tilation to distribute flow evenly and optimally to the re- In most teleost fishes, the gill filaments are not spiratory exchange surfaces. J. Morphol. 000:000–000, interconnected and extend independently from the 2012. Ó 2012 Wiley Periodicals, Inc. gill arch, with lamellae extending freely from the KEY WORDS: tuna; mackerel; marlin; swordfish; gill filament; gill lamellae Contract grant sponsor: National Science Foundation; Contract grant number: IOS-0817774; Contract grant sponsors: The Tuna Industry Endowment Fund at Scripps Institution of Oceanography, the Pfleger Institute of Environmental Research, the George T. Pfleger Foundation, the Moore Family Foundation, the Nadine A. INTRODUCTION and Edward M. Carson Scholarship awarded by the Achievement Tunas, bonitos, and mackerels (family Rewards for College Scientists (ARCS), Los Angeles Chapter (N.C.W.), a National Research Council Associateship (N.C.W.), and Scombridae) and billfishes (families Istiophoridae, the Kennel-Haymet Student Lecture Award (N.C.W.). Xiphiidae) are continuous swimmers and breathe using ram ventilation, the mechanism through *Correspondence to: Nicholas C. Wegner, National Marine Fish- which forward swimming provides the force eries Service, Southwest Fisheries Science Center, 8901 La Jolla required to drive water into the mouth and Shores Dr., La Jolla, CA 92037. E-mail: [email protected] through the branchial chamber (Brown and Muir, 1970; Stevens, 1972; Roberts, 1975, 1978; Stevens Received 4 April 2012; Revised 21 July 2012; Accepted 23 August 2012 and Lightfoot, 1986; Wegner et al., 2012). Ram ventilation transfers the energetic cost of active Published online in gill ventilation to the swimming musculature, and Wiley Online Library (wileyonlinelibrary.com) because mouth and opercular motions are mini- DOI: 10.1002/jmor.20082 Ó 2012 WILEY PERIODICALS, INC. 2 N.C. WEGNER ET AL. Fig. 1. Basic gill morphology and fusion structure described for tunas and billfishes. (A) First gill arch taken from the left side of the branchial chamber of a scombrid showing the gill filaments emanating from the arch. (B–E) Magnified views of black box in A showing the leading (water-entry) edges of three adjacent gill filaments (each containing two rows of gill lamellae) with different fusion types: (B) No gill fusions, (C) Interlamellar fusions, (D) Complete lamellar fusions, and (E) Filament fusions (with complete lamellar fusions extending underneath). Water flow direction in B-E is into the page. IF, interlamellar fusion; F, filament; FF filament fusions; L, lamellae; LF, complete lamellar fusion. gill filaments (Fig. 1A,B). The gill fusions of scom- (Istiophorus, Kajikia, and Xiphias; Muir and Ken- brids and billfishes connect these normally inde- dall, 1968; Johnson, 1986). In the tuna genus, pendent structures to form lamellar fusions (Fig. Thunnus, filament fusions are formed by the 1C–E) and filament fusions (Fig. 1E). Lamellar expansion of the mucosal filament epithelium fusions, which bind the gill lamellae near their (Muir and Kendall, 1968). In contrast, wahoo and leading (water-entry) edge and thus secure the billfish filament fusions are formed by bony epithe- spatial integrity of the interlamellar channels lial toothplates, which on the trailing edges of the (5lamellar pores), can be further categorized into filaments cover cartilaginous connections of the fil- two forms. Interlamellar fusions (Fig. 1C) bind ad- ament rods (Johnson, 1986). jacent lamellae on the same filament and have The diversity of gill fusion type and structure been described for wahoo, Acanthocybium solandri can be expected to reflect interspecific differences (a non-tuna scombrid), and striped marlin, Kajikia in reliance upon, or specialization for, ram ventila- audax (Wegner et al., 2006). Complete lamellar tion. Although all scombrids and billfishes use fusions (Fig. 1D) connect the lamellae on one fila- ram ventilation, basic information about the occur- ment to the closely positioned and opposing lamel- rence of fusions and their structure is not avail- lae of the adjacent filament, thus providing sup- able for many species, and there are few data port to both the gill lamellae and filaments (Muir addressing how fusion structure may change with and Kendall, 1968; Muir, 1969; Wegner et al., body size or the range of swimming speeds 2006). Complete lamellar fusions have been employed by these fishes. Because the family reported in several tuna species and in the striped Scombridae demonstrates a progression in adapta- marlin, where, in some areas of the gills, the inter- tions for fast, continuous swimming (from least lamellar fusions of adjacent filaments join together derived mackerels to most derived tunas) and an (i.e., the striped marlin has both complete lamellar associated increase in reliance on ram ventilation, and interlamellar fusions; Wegner et al., 2006). determination of gill fusion type and pattern along Filament fusions (Fig. 1E) bridge the interfila- this gradient can provide insight into the struc- ment space in a lattice-like pattern, binding adja- tural requirements of ram ventilation. This com- cent filaments on the same gill hemibranch (Muir parative study thus examines the gills of 28 scom- and Kendall, 1968; Johnson, 1986; Davie, 1990). brid and seven billfish species in order to deter- These fusions, which form on the trailing (water- mine how factors such as body size, swimming exit) and often leading (water-entry) edges of the speed, and the degree of dependence upon ram filaments, have been documented in tunas of the ventilation correlate with the site of occurrence genus Thunnus, the wahoo, and some billfishes and elaboration of fusions. Journal of Morphology GILL FUSIONS FOR RAM VENTILATION 3 TABLE 1. Scombrids and billfishes examined in relation to gill fusion type Species Common n total Fork length Mass Lamellar Filament Collection name name (collected) (cm) (kg) fusion fusion location Thunnus alalunga Albacore 4 (2) 39.0–82.0 1.0–11.3 LF ME 1 Thunnus albacares Yellowfin tuna 25 (19) 29.0–182.0 0.38–94.0 LF ME 1,2,3 Thunnus atlanticus Blackfin tuna 11 (5) 45.5–52.0 1.6–2.4 LF ME 4 Thunnus obesus Bigeye tuna 6 (5) 40.0–136.0 1.5–46.0 LF ME 3,5 Thunnus orientalis Pacific bluefin tuna 5 (5) 86.0–120.0 12.2–32.3 LF ME 2 Thunnus tonggol Longtail tuna 9 (2) 38.5–85.5 0.83–9.6 LF ME 6 Katsuwonus pelamis Skipjack tuna 14 (8) 30.4–77.0 0.48–9.6 LF -- 1,2,3 Euthynnus affinis