Vol. 21: 261–265, 2014 AQUATIC BIOLOGY Published online October 29 doi: 10.3354/ab00599 Aquat Biol

OPENPEN ACCESSCCESS NOTE Distribution of ampullary pores on three catshark species (Apristurus spp.) suggest a vertical-ambush predatory behaviour

D. M. Moore*, I. D. McCarthy

School of Ocean Sciences, College of Natural Sciences, Bangor University, Menai Bridge, Anglesey LL59 5AB, UK

ABSTRACT: Apristurus is a genus of typically small sharks that inhabit deep waters around the globe. Relatively little is known about the feeding behaviour of these species. Here, the electro - sensory biology of 3 species, A. aphyodes, A. melanoasper and A. microps, was investigated. Intra-specific variation in ampullary pore abundance was high in all species, highlighting the need for studies to examine multiple individuals. Abundance and distribution of ampullary pores on the head indicate that all 3 species are vertical ambush predators.

KEY WORDS: Apristurus aphyodes · A. melanoasper · A. microps · Rockall Trough · Ampullae of Lorenzini

INTRODUCTION will attempt to examine intra-specific variation in ampullary pore counts and furthermore elucidate the Electroreception in elasmobranchs is thought to fa- reliability of single individual representations. cilitate various types of behaviour, including social in- The majority of studies on elasmobranch electro - teraction (Sisneros et al. 1998) and navigation (Paulin reception to date have focussed on coastal or upper 1995, Montgomery & Walker 2001). However, by far pelagic species, and few on species from deep water the most important use of electroreception in elasmo- environments, owing to limited accessibility. How- branchs is believed to be predator/prey detection ever, there is a growing need to better understand (Kalmijn 1971, Raschi et al. 2001). The distribution of the ecology of deeper-dwelling species such as Apris- ampullary pores in elasmobranchs has been studied turus spp., which are under increasing pressure from in numerous species (Fishelson & Baranes 1998, Kaji- both targeted and non-targeted fishing. The genus ura 2001, Atkinson & Battaro 2006), and there is an Apristurus Garman, 1913 comprises 36 recognised increasing interest in mapping ampullary pore distri- species, which are poorly understood. We suggest bution as a tool to infer behaviour and ecology (Fishel- that the ecology of Apristurus spp. may be inferred son & Baranes 1998, Kajiura 2001, Atkinson & Bottaro from ampullary pore distribution, by comparison 2006, Kempster & Collin 2011a,b). Some published with species in which their ecology is better studied. works of this field adopt a traditional meristical ap- At least 5 species of Apristurus are found in the proach, whereby ampullary pores are counted and Rockall Trough, Northeast Atlantic, an area under in - mapped from a single individual and taken as typical tense fishing pressure from Europe (Neat et al. 2008): for the species (Kempster & Collin 2011a,b), particu- A. aphyodes Nakaya & Stehmann, 1998; A. lau rus - larly in large or rarely sighted shark species. As most sonii (Synonym A. maderensis) Saemundsson, 1922; studies take data from multiple individuals, this study A. manis Springer, 1979; A. melanoasper Iglé si as,

© The authors 2014. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 262 Aquat Biol 21: 261–265, 2014

Nakaya & Stehmann, 2004, and A. microps Gilchrist, 1922. Three of these species (selected due to avail- ability of useable sample numbers) shall be the focus herein. A. aphyodes lives in depths of 1014 to 1800 m, from 49° 1.9’ N to 60° 49.7’ N (Nakaya & Stehmann 1998). It preys upon crustaceans, cephalo pods and small teleost fishes (Duffy & Huveneers 2004). It is classed as Data Deficient on the IUCN Red List of Threat- ened Species. A. melanoasper inhabits waters from 512 to at least 1520 m depth and is distributed across the North Atlantic between 39° 17’ N and 61° 06’ N (Iglé sias et al. 2002). It is classed as Data Deficient on the IUCN Red List and there are currently no studies on its diet. A. microps inhabits waters between 700 and 1200 m depth in both the North and South Atlantic Fig. 1. Use of a fibre optic cold light source to highlight Ocean. It feeds on small teleost fishes, crustaceas and electrosensory pores in Apristurus microps cephalopods (Compagno et al. 1989) and is classed as Least Concern on the IUCN Red List. All 3 species are regularly caught as by-catch in RESULTS the deep-water fisheries of the Rockall Trough region (F. C. Neat, pers. comm.), but there are no detailed All 3 Apristurus species showed similarity in assessments. their pore grouping distribution pattern (Fig. 2). Most pores were grouped around the anterior snout region of the head, with only 12.1 ± 1.4%, MATERIALS AND METHODS 9.0 ± 0.7% and 11.3 ± 1.5% (mean ± SD) of pores being positioned posterior to the eye in A. aphyo- Specimens of Apristurus spp. were collected dur- des, A. melanoasper and A. microps, respectively. ing a Marine Scotland Science deep-water trawl sur- There was large intra-specific variation from the vey of the Rockall Trough area during September mean total pore count for all species. Variation 2009 (see Moore et al. 2013). A maximum equal-sex from the mean was found to be highest in A. aphy- and -length stratified subsample was taken, con - odes at up to 20.6% (177 pores). Intra-specific sisting of 20 A. aphyodes (10m and 10f), 10 A. variation in mean total pore count was 18.5% and melanoasper (5m and 5f) and 18 A. microps (9m and 13.0% for A. melanoasper and A. microps respec- 9f). Heads of specimens were removed by a single tively. All 3 species displayed variation in pore dorsoventral cut just posterior of the 5th gill slit, as aperture dia meter. all ampullary pores were found anterior of this Total pore counts in A. aphyodes ranged from 761 point upon visual inspection. Heads were frozen for to 1037. Female A. aphyodes had significantly more transportation. pores than males with a mean (±SD) pore count of After defrosting in a warm water bath, heads were 898 and 822, respectively (Table 1; Kruskal-Wallis examined using a Schott KL 1500 fibre optic cold test, H20 = 7.41, p = 0.007). There was no significant light source (Fig. 1). Digital images were taken using difference in total length (TL) between the sexes a Ricoh Caplio R6 7.2 megapixel camera and then (ANOVA, F(1,18) = 0.60, p = 0.448). Both males and subsequently used for drawing of pore maps using females displayed significantly higher pore counts Paint v6.1. Pores were counted in situ by direct visual and pore density on the dorsal surface than on the inspection with counted pores marked in ink to limit ventral surface (Table 1; ANOVA, m F(1,19) = 91.97, observer error. Pore density estimations were estab- p < 0.001, f F(1,19) = 108.19, p < 0.001). There was no lished following Raschi (1986), utilising ImageJ pic- significant relationship between pore count and TL 2 ture analysis software. (GLM, r = 0.91, F(1,15) = 1.75, p = 0.357). Data were tested for normality (Anderson-Darling) Total pore counts in A. melanoasper ranged from and homoscedasticity (Hartlets) to ensure that as - 1355 to 1781. There was no significant difference sumptions made by statistical tests were met. between males and females (ANOVA, F(1,9) = 0.03, Moore & McCarthy: Apristurus spp. ampullary pore distribution 263

Fig. 2. Comparison of ampullary pore regions between Apristurus aphyodes, A. melanoasper and A. microps showing dorsal and ventral perspectives. Representations are not to scale p = 0.869). The difference in TL between sexes was sity (Table 1) on the ventral surface than on the dor- significant (Kruskal-Wallis test, H10 = 5.77, p = 0.016). sal surface, and the highest pore densities of the 3 There were no significant differences between dorsal species. and ventral pore counts (ANOVA, m F(1,9) = 1.41, p = Total pore counts in A. microps ranged from 820 to 0.269, f F(1,9) = 1.34, p = 0.281), nor between pore 1035, with no significant difference between males 2 count and TL (GLM, r = 0.07, F(1,9) = 0.52, p = 0.496). and females (ANOVA, F(1,18) = 0.21, p = 0.653). There A. me lanoasper displayed a higher mean pore den- was no significant difference in TL between the

sexes (ANOVA, F(1,18) = 0.70, Table 1. Total pore count (mean ± SD) and mean total length (TL) for Apristurus aphyodes, p = 0.415). Both males and A. melanoasper and A. microps by sex females displayed signifi- cantly higher pore counts and Species Sex Pore number Pore density pore density on the dorsal sur- TL Mean ±SD Dorsal ±SD Ventral ±SD Dorsal Ventral face than on the ventral sur- (cm) (pores/cm2) face (ANOVA, m F(1,19) = f Apristurus M 44.8 822 70 495 49 326 25 10.35 6.65 204.99, p < 0.001, F(1,17) = aphyodes F 46.9 898 81 559 62 339 26 11.69 6.91 302.08, p < 0.001). There was Apristurus M 60.2 1496 165 716 83 780 86 13.90 14.58 no significant relationship melanoasper F 45.2 1511 121 732 44 779 80 14.21 14.56 between pore count and TL Apristurus M 56.0 910 69 585 54 325 21 10.91 5.66 2 microps F 52.1 923 56 596 41 327 22 11.12 5.69 (GLM, r = 0.01, F(1,18) = 0.01, p = 0.914). 264 Aquat Biol 21: 261–265, 2014

DISCUSSION snout and head within all study species. However this can be countered by the sub-terminal position of the All species of Apristurus displayed similar charac- mouth in all 3 target species which would only be con- teristics in their ampullary pore distribution pattern, current with targeting prey from above; a strategy including bi-lateral symmetry and concurrency with made more likely in A. melano asper by its higher pore previously generated pore maps for other species count being on the ventral surface. The labial pores in within this genus (Cornett 2006). The dorsal surface A. microps may suggest some in-sediment feeding displayed distinct longitudinally arranged central and would therefore suggest that the increased mean and peripheral pore regions to the anterior of the eye, pore number on the dorsal surface is more for detec- a crescent region above the eye and two smaller re - tion of predators than prey. The mean pore densities gions posterior to the eye. Similarities in ventral sur- in all 3 target species (Table 1) match the relationship face distribution included a double line of pores run- displayed by the mean pore number; density however ning longitudinally posterior of the mouth, a roughly provides a much better indication of electrorecep - triangular pore assemblage anterior of the nares and tion resolution (Raschi 1986). Following this, both A. a longitudinal region in the mesial zone of the snout. aphyodes and A. microps have greater electrorecep- This distribution pattern was also found in A. brun- tion resolution on the dorsal surface, whereas it is on ne us (Cornett 2006) and is likely common to the the ventral surface that A. melanoasper exhibits the whole genus. Only A. microps had pores in the labial greater electroreception resolution. area. Total pore counts for Apristurus spp. were Mauchline & Gordon (1983) outline stomach con- high, compared to other scyliorhinids (Kaji ura 2010). tents for unidentified Apristurus spp. as being mainly Maximum pore density was typically in the pore as - composed of decapod crustaceans with an ontoge- semblages below the eyes, although in A. mela no - netic shift in diet to include more cephalopods and asper pore density in this region was also equalled by crustaceans with increasing total length. In addition, that of the mesial snout assemblages. Ebert et al. (1996) also showed a mixed diet of tele - Only A. aphyodes showed sexual dimorphism in osts and crustaceans for Apristurus spp., but in the total pore count, females having significantly higher South Atlantic. Such a varied diet over the sharks’ numbers of ampullary pores. However, Fishelson & lifetimes is likely to suggest that Apristurus spp. are Baranes (1998) also found the highest number of opportunistic generalist feeders and the conflicting pores on female individuals of another carcharhini- sensory/morphological evidence supports this. Such form, the Oman shark Iago omanensis, which sug- a feeding strategy is also very agreeable in a deep- gests sexual dimorphism in total pore counts could be water environment where feeding opportunities are interesting area of future research. Neither A. aphy- likely intermittent. odes nor A. microps showed significant differences in There was no significant relationship between total TL be tween sexes and it is likely the positive result length and pore count in any species, suggesting for A. melanoasper is due to low sample size. With Apristurus spp. individuals are born with a set num- this in mind it is likely that intra-specific variation in ber of electrosensory pores which remain active total pore number is not linked to sexual dimorphism throughout their lives, as found in other shark spe- and is more likely of genetic origin. cies (Kajiura 2001, Raschi & Gerry 2003, Cornett The higher pore counts on dorsal surfaces than ven- 2006, Mello 2009). However, the increase in TL with tral surfaces in A. aphyodes and A. microps are not age necessarily results in a decrease in pore density concurrent with findings for other deep water habitat as pore number remains constant. High pore densi- species such as Galeus melastomus or Etmo pterus ties are correlated with less mobile prey (like epifau- spinax where ventral pores were more numerous nal and infaunal crustaceans) whereas lower pore (Atkinson & Bottaro 2006). Both G. melasto mus and E. densities are correlated with more mobile prey (like spinax hunt fast-moving pelagic prey (Wurtz & Vacchi cephalopods and teleosts), due to a reduction in res- 1981) and a higher ventral pore number may suggest olution as pore density decreases (with age-related that these species hunt by ambushing prey found be- growth), leaving the animal less able to detect immo- low them in the water column. The higher dorsal pore bile prey items (Jordan 2008, Bedore et al. 2014). It is number in A. aphyodes and A. microps suggests a therefore likely that the ontogenetic diet shift as more benthic existence; this higher dorsal pore num- described by Mauchline & Gordon (1983) is driven by ber may facilitate detection of passing prey or preda- both a reduced ability to detect more immobile prey tors above. This suggestion of vertical am bush is fur- and an increase in mouth gape size that allows it to ther reinforced by the de pressed morphology of the target larger prey items. Moore & McCarthy: Apristurus spp. ampullary pore distribution 265

Intra-specific variation in total pore count was high Kajiura SM (2010) Sensory adaptations to the environment: (>10%) for all target species, as found in other electroreceptors as a case study. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives. II. Bio- studies (Jordan 2008, Bedore et al. 2014), but is un- diversity, adaptive physiology and conservation. CRC likely due to observer error owing to the marking Press, Boca Raton, p 393–433 methodology employed. Future research should aim Kalmijn AJ (1971) The electric sense of sharks and rays. to understand to what extent, if any, such variation J Exp Biol 55: 371−383 Kempster RM, Collin SP (2011a) Electrosensory pore distri- has on electrosensory capability. In addition, identi- bution and feeding in the megamouth shark Mega - fying the species’ prey would assist in understanding chasma pelagios (Lamniformes: Megachasmidae). Aquat the significance of pore distribution patterns in these Biol 11: 225−228, doi: 10.3354/ab00311 deep-water elasmobranch species. Kempster RM, Collin SP (2011b) Electrosensory pore distri- bution and feeding in the basking shark Cetorhinus maximus (Lamniformes: Cetorhinidae). Aquat Biol 12: Acknowledgements. The Marine Scotland Science deep- 33−36, doi:10.3354/ab00328 water trawl survey (Cruise 1209S) was funded by the Scot- Mauchline J, Gordon JDM (1983) Diets of the sharks and tish Government (Grant MF0763). Thanks go to Francis chimaeroids of the Rockall Trough, North Eastern Neat (Marine Scotland) and the skipper and crew of the Atlantic Ocean. Mar Biol 75: 269−278 FRV ‘Scotia’ for assistance in obtaining samples. Additional Mello W (2009) The electrosensorial pore system of the thanks go to E. G. Cunningham and M. Kurr as well as 3 cephalofoil in the four most common species of hammer- anonymous referees for constructive comments that have head shark from the southwestern Atlantic. C R Biol 332: improved this manuscript. 404−412 Montgomery J, Walker M (2001) Orientation and navigation LITERATURE CITED in elasmobranchs: which way forward? Environ Biol Fishes 60: 109−116 Atkinson CJL, Bottaro W (2006) Ampullary pore distribution Moore DM, Neat FC, McCarthy ID (2013) Population bio- of Galeus melastomus and Etmopterus spinax: possible logy and ageing of the deep water sharks Galeus melas- relations with predatory lifestyle and habitat. J Mar Biol tomus, Centroselachus crepidater and Apristurus aphyo- Assoc UK 86: 447−448 des from the Rockall Trough, north-east Atlantic. J Mar Bedore CN, Harris LL, Kajiura SM (2014) Behavioral Biol Assoc UK 93:1941−1950 responses of batoid elasmobranchs to prey-simulating Nakaya K, Stehmann M (1998) A new species of deep-water electric fields are correlated to peripheral sensory mor- catshark, Apristurus aphyodes n. sp., from the eastern phology and ecology. Zoology 117: 95−103 North Atlantic (Chondrichthyes: Carchariniformes: Scylio - Compagno LJV, Ebert DA, Smale MJ (1989) Guide to rhinidae). Arch Fish Mar Res 46: 77−90 the sharks and rays of southern Africa. New Holland, Neat F, Burns F, Drewery J (2008) The deepwater ecosystem London of the continental shelf slope and seamounts of the Rock- Cornett AD (2006) Ecomorphology of shark electroreceptors. all Trough: a report on the ecology and biodiversity MS thesis, Florida Atlantic University, Boca Raton, FL based on FRS scientific surveys. Fish Res Serv Int Rep Duffy C, Huveneers C (2004) Apristurus aphyodes. IUCN 02/08 Red List of Threatened Species.Version 2010.4. www. Paulin MG (1995) Electroreception and the compass sense of iucnredlist.org (accessed 26 January 2013) sharks. J Theor Biol 174: 325−339 Ebert DA, Cowley PD, Compagno LJV (1996) A preliminary Raschi W (1986) A morphological analysis of the Ampullae of investigation of the feeding ecology of catsharks (Scylio- Lorenzini in selected skates (Pisces, Rajoidei). J Morphol rhinidae) off the west coast of southern Africa. S Afr J 189: 225−247 Mar Sci 17:233−240 Raschi WG, Gerry S (2003) Adaptations in the elasmo- Fishelson L, Baranes A (1998) Distribution, morphology, and branch electroreceptive system. In: Val AL, Kapoor cytology of ampullae of Lorenzini in the Oman shark, BG (eds) Fish adaptations. Science Publishers, Plymouth, Iago omanensis (Triakidae), from the Gulf of Aqaba, Red p 233−258 Sea. Anat Rec 251:417−430 Raschi W, Aadlond C, Keithar ED (2001) A morphological Iglésias SP, Du Buit MH, Nakaya K (2002) Egg capsules of and functional analysis of the ampullae of Lorenzini in deep-sea catsharks from eastern North Atlantic, with selected galeoid sharks. In: Kapoor BG, Hara TJ (eds) first description of the capsule of Galeus murinus and Sensory biology of jawed fishes. Science Publishers, Apristurus aphyodes. Cybium 26: 59−63 Plymouth, p 297−316 Jordan LK (2008) Comparative morphology of stingray Sisneros JA, Tricas TC, Luer CA (1998) Response properties lateral line canal and electrosensory systems. J Morphol and biological function of the skate electrosensory sys- 269: 1325−1339 tem during ontogeny. J Comp Physiol A 183: 87−99 Kajiura SM (2001) Head morphology and electrosensory Wurtz M, Vacchi M (1981) Ricerca di cicli nittemerali pore distribution of carcharhinid and sphyrnid sharks. nell’alimentazione di selaci batiali. Quad Lab Tecnol Environ Biol Fishes 61: 125−133 Pesca 3(Suppl 1): 155−164

Editorial responsibility: Christine Paetzold, Submitted: November 25, 2013; Accepted: August 29, 2014 Oldendorf/Luhe, Germany Proofs received from author(s): October 9, 2014