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Oil Gland and Oil Pores in Billfishes: in Search of a Function F

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Oil Gland and Oil Pores in Billfishes: in Search of a Function F © 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb224956. doi:10.1242/jeb.224956 RESEARCH ARTICLE Oil gland and oil pores in billfishes: in search of a function F. Dhellemmes1,2,*, M. J. Hansen1, S. D. Bouet1,2, J. J. Videler3, P. Domenici4, J. F. Steffensen5, T. Hildebrandt6,7, G. Fritsch6,P.Bach8,9, P. S. Sabarros8,9, A. Krüger1, R. H. J. M. Kurvers10 and J. Krause1,2 ABSTRACT billfishes’ (Istiophoridae and Xiphiidae) elongated rostra (Habegger Billfishes are well known for their distinctive elongated rostra, i.e. bills. et al., 2015). Speculations on the role of these morphological The functional significance of billfish rostra has been frequently structures are numerous, but detailed investigations are scarce discussed and the recent discovery of an oil gland (glandula because of the logistical complexity of open-ocean research. oleofera) at the base of the rostrum in swordfish, Xiphias gladius, In the case of billfishes, the rostrum has been shown to serve as a has added an interesting facet to this discussion regarding the potential weapon to stab or strike prey (Domenici et al., 2014; Shimose et al., co-evolution of gland and rostra. Here, we investigated the oil gland and 2007). Additionally, it was hypothesized to create turbulence in the oil pores (through which the oil is brought to the skin surface) of four boundary layer, reducing pressure drag because of a delay in flow billfish species – swordfish, Atlantic blue marlin (Makaira nigricans), separation (Aleyev, 1977; Kozlov, 1973; Videler, 1995). Drawing on Indo-Pacific sailfish (Istiophorus platypterus)andstripedmarlin(Kajikia the functional morphology approach, researchers have analysed the audax) – and provide detailed evidence for the presence of an oil gland morphology of the bill to gauge its function. Recently, Habegger et al. in the last three. All four species had a high density of oil pores on the (2015) reported the presence of a poorly calcified structure in front of forehead which is consistent with the hypothesis of hydrodynamic the eyes at the base of the rostrum on billfish specimens. This benefits of the oil. The extension of the pores onto the front half of the structure, first mentioned by Gudger (1940), was recently analysed in rostrum in sailfish and striped marlin, but not in swordfish or blue marlin, detail by Videler et al. (2016) in swordfish, Xiphias gladius.They suggests that the oil may have additional functions. One such function described it as an oil-producing gland (glandula oleofera) connected could be linked to the antibacterial and anti-inflammatory properties of via a capillary network (rete lubricans) to micro-pores on the forehead the oil. However, the available evidence on predatory rostrum use (and and the base of the rostrum. The presence of this gland, especially in hence the likelihood of tissue damage) is only partly consistent with the connection with the capillary network running into the rostrum, adds extension of pores on rostra across species. We conclude that the oil an interesting angle to the debate on bill functionality, particularly gland probably serves multiple, non-mutually exclusive functions. More regarding the potential co-evolution of gland and rostra. detailed information on rostrum use in blue marlin and swordfish is The prime function of the oil gland put forward by Videler et al. ’ needed to better link behavioural and morphological data with the aim (2016) is that it lubricates the fish s forehead, creating a hydrophobic ’ of accomplishing a full comparative analysis. layer on the skin. The authors analysed the oil s chemical composition and properties and studied the distribution and size of KEY WORDS: Comparative method, Functional morphology, the pores on the swordfish forehead. The oil was found to consist of Rostrum, Glandula oleofera, Rete lubricans, Fatty acids, Co-evolution fatty acids and to congeal at 8°C. The authors suggested that the oil stays fluid at the swordfish’s typical foraging depths thanks to a heat- INTRODUCTION producing muscle located behind the eyes (Videler et al., 2016). Low Pelagic predators possess an array of morphological adaptations dynamic pressure over the concave front part of the head has been thought to facilitate prey detection and/or capture. Examples of proposed as the oil’s passive excretion mechanism. The hydrophobic these adaptations include the hammerhead shark’s (Sphyrnidae) layer resulting from the oil lubrication, associated with micro- dorsoventrally flattened cephalofoil (McComb et al., 2009) and the protrusions on the skin, is thought to decrease frictional drag (Luo et al., 2015; Videler et al., 2016). Therefore, these findings placed functional explanations of the oil gland and capillary system in the 1Department of Biology and Ecology of Fishes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587 Berlin, Germany. context of a hydrodynamic benefit that reduces the metabolic costs of 2Faculty of Life Sciences, Humboldt-Universität zu Berlin, Invalidenstrasse 42, swimming (Videler et al., 2016). 10115 Berlin, Germany. 3Groningen & Leiden University, Zuidlaarderweg 57, In this study, we investigated and compared the presence and Noordlaren, The Netherlands. 4IAS-CNR, Istituto per lo studio degli impatti Antropici e Sostenibilitàin ambiente marino, Consiglio Nazionale delle Ricerche, LocalitàSa characteristics of the oil gland of four billfish species: the Atlantic blue Mardini, 09170, Torregrande, Oristano, Italy. 5Marine Biological Section, University marlin (Makaira nigricans Lacepedè 1802), striped marlin [Kajikia of Copenhagen, Strandpromenaden 5, DK-3000 Helsingør, Denmark. 6Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315 Berlin, audax (Philippi 1887)], Indo-Pacific sailfish [Istiophorus platypterus Germany. 7Freie Universität Berlin, 14195 Berlin, Germany. 8MARBEC, Université (Shaw 1792)] and swordfish (Xiphias gladius Linnaeus 1758). First, de Montpellier, CNRS, Ifremer, IRD, 34203 Sete,̀ France. 9Institut de Recherche we used computed tomography (CT) scans to image the region in pour le Développement, Ob7, 34203 Sete,̀ France. 10Centre for Adaptive Rationality, Max Planck Institute for Human Development, Lentzeallee 94, 14195 which the oil gland was found in swordfish to identify similar structures Berlin, Germany. in the other billfish species. Second, we took oil samples from all species and determined the fatty acid composition of the oil. Third, we *Author for correspondence ([email protected]) measured the pore distribution along the bill to quantify potential F.D., 0000-0002-2043-4653; M.J.H., 0000-0003-3026-312X; J.J.V., 0000-0003- species differences in pore extension along the rostrum, and quantified 1226-9528; P.D., 0000-0003-3182-2579; J.F.S., 0000-0002-4477-8039; T.H., 0000- pore density and size. We discuss our results, considering what is 0001-8685-4733; P.B., 0000-0003-0804-8466; R.H.J.M.K., 0000-0002-3460-0392; J.K., 0000-0002-1289-2857 known about behavioural differences between the billfish species. If hydrodynamic benefits are indeed the main function of the oil Received 11 March 2020; Accepted 6 August 2020 gland, then we would predict that, in all four species, oil pores Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb224956. doi:10.1242/jeb.224956 would be primarily present on the forehead and base of the bill, as Pore distribution, density and size these regions face the greatest frictional drag in billfish (Aleyev, In all four species, oil pores as described by Videler et al. (2016) 1977). However, if the oil gland also relates to other functions such were found, but only on the dorsal surface. Therefore, we focused on as predatory rostrum use, then we would expect to find among- the dorsal side for our study. We examined the pore distribution on species differences in the extension of the pores along the rostrum. the bill by measuring the dorsal extension of the pores. We used a Sailfish are known to use their rostrum frequently in prey capture microscope (Leica Wild MZ, lens: Planapo 1.0×) to measure how (Domenici et al., 2014; Hansen et al., 2020). Striped marlin also use far towards the bill-tip the dorsal pores were present. To standardize their rostrum for prey capture, although less frequently than sailfish the extent of the pores across individuals (and species), we (Hansen et al., 2020). Blue marlin (Shimose et al., 2007) and measured, for each individual, the distance from the anterior eye swordfish (Stillwell and Kohler, 1985) are thought to rely less on edge to the maximum dorsal pore extension point and divided this their bill for prey capture, though this evidence is circumstantial as it by the total rostrum length (RL). The RL was measured as the is inferred from stomach content analyses rather than direct distance from the anterior eye edge to the rostrum tip. This approach observation. The rostra of billfish are subject to exceptionally thus provides a measure that quantifies how far the pores extend high biomechanical stress and show signs of tissue damage (Atkins relative to the total length of the rostrum. et al., 2014; Kurvers et al., 2017). Given the antibacterial properties Pore density (number of pores per cm2) was sampled at six of some of the fatty acids found in swordfish oil (i.e. oleic and equidistant dorsal locations starting at the eye edge and ending at the palmitic acid; Yff et al., 2002; Le et al., 2010; Videler et al., 2016), bill tip (Fig. 1). At each sampling point, the size (mm) of the four one potential function in connection with the rostrum’s use as a pores closest to the centre of the area was measured. Assessments of weapon could also be tissue repair. If the oil is linked to tissue repair, pore density and size were conducted using a Mitutoyo microscope we hypothesize that the oil pores would be more abundant on the (Vision Measuring Machine, Quickscope) and its image processing rostrum and would extend further towards the rostrum tip in sailfish software (QSPAK).
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