Couturier Et Al. 2012 Mobulid Review PDF

Journal of Fish Biology (2012) 80, 10751119 doi:10.1111/j.1095-8649.2012.03264.x, available online at wileyonlinelibrary.
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Biology, ecology and conservation of the Mobulidae

L. I. E. Couturier*, A. D. Marshall, F. R. A. Jaine , T. Kashiwagi*, S. J. Pierce, K. A. Townsend**, S. J. Weeks , M. B. Bennett* and A. J. Richardson
*School of Biomedical Sciences, The University of Queensland, St Lucia, Qld 4072, Australia, Climate Adaptation Flagship, CSIRO Marine and Atmospheric Research, Ecosciences Precinct, GPO Box 2583, Brisbane, Qld 4102, Australia, Marine Megafauna Association and ECOCEAN USA, Tofo Beach, Inhambane, Mozambique, Biophysical Oceanography Group, School of Geography, Planning and Environmental Management, The University of Queensland, St Lucia, Qld 4072, Australia, Molecular Fisheries Laboratory, Department of Employment, Economic Development and Innovation, P. O. Box 6097, Brisbane, Qld 4072, Australia, School of Biological Sciences, The University of Queensland, St Lucia, Qld 4072, Australia, Centre for Applications in Natural Resource Mathematics, School of Mathematics and Physics, The University of Queensland, St Lucia, Qld 4072, Australia and Environmental Decisions Group, School of Biological Sciences, The University of Queensland, Brisbane, Qld 4072, Australia
The Mobulidae are zooplanktivorous elasmobranchs comprising two recognized species of manta rays (Manta spp.) and nine recognized species of devil rays (Mobula spp.). They are found circumglobally in tropical, subtropical and temperate coastal waters. Although mobulids have been recorded for over 400 years, critical knowledge gaps still compromise the ability to assess the status of these species. On the basis of a review of 263 publications, a comparative synthesis of the biology and ecology of mobulids was conducted to examine their evolution, taxonomy, distribution, population trends, movements and aggregation, reproduction, growth and longevity, feeding, natural mortality and direct and indirect anthropogenic threats. There has been a marked increase in the number of published studies on mobulids since c. 1990, particularly for the genus Manta, although the genus Mobula remains poorly understood. Mobulid species have many common biological characteristics although their ecologies appear to be species-specic, and sometimes region-specic. Movement studies suggest that mobulids are highly mobile and have the potential to rapidly travel large distances. Fishing pressure is the major threat to many mobulid populations, with current levels of exploitation in target sheries unlikely to be sustainable. Advances in the elds of population genetics, acoustic and satellite tracking, and stable-isotope and fatty-acid analyses will provide new insights into the biology and ecology of these species. Future research should focus on the uncertain taxonomy of mobulid species, the degree of overlap between their large-scale movement and human activities such as sheries and pollution, and the need for management of inter-jurisdictional sheries in developing nations to ensure their long-term sustainability. Closer collaboration among researchers worldwide is necessary to ensure standardized sampling and modelling methodologies to underpin global population estimates and status. 2012 The Authors
Journal of Fish Biology 2012 The Fisheries Society of the British Isles
Key words: by-catch; distribution; elasmobranch; sheries; Manta; Mobula.
Author to whom correspondence should be addressed. Tel.: +61733467975; email: l.couturier@uq.edu.au
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2012 The Authors Journal of Fish Biology 2012 The Fisheries Society of the British Isles
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L. I. E. COUTURIER ET AL.
INTRODUCTION The Mobulidae, which comprises manta rays (Manta spp.) and devil rays (Mobula spp.), is a diverse family of planktivorous elasmobranchs occurring worldwide in tropical, subtropical and temperate waters. Represented by two genera and 11 recognized species, the family contains the largest rays, reaching over 7 m disc width (WD ) (Compagno & Last, 1999; Marshall et al., 2009). Although early historical accounts painted devil and manta rays as diabolical creatures and ferocious brutes, accusing them of stealing boats and deliberately killing divers (Gill, 1908; Saenz-Arroyo et al., 2006), it is now known that these rays are harmless to humans and feed mainly on zooplankton. The genus Manta was recently re-described and has at least two distinct species, the reef manta Manta alfredi (Krefft 1868) and the giant manta Manta birostris (Walbaum 1792), and a third putative species, Manta sp. cf birostris (Marshall et al., 2009). Manta individuals can reach a maximum size ranging between 5 and 7 m WD . The genus Mobula comprises nine recognized species that attain a WD from 1 to 5 m: the pygmy devil ray Mobula eregoodootenkee (Bleeker 1959), the Atlantic devil ray Mobula hypostoma (Bancroft 1831), the spinetail devil ray Mobula japanica (M ller & Henle 1841), the shortn devil ray Mobula kuhlii (M ller u u & Henle 1841), the giant devil ray Mobula mobular (Bonnaterre 1788), Munks devil ray Mobula munkiana Notarbartolo-di-Sciara 1987, the lesser Guinean devil ray Mobula rochebrunei (Vaillant 1979), the Chilean devil ray Mobula tarapacana (Philippi 1893) and the bentn devil ray Mobula thurstoni (Lloyd 1908). Although the existence of mobulids has been documented since at least the 17th century (Willughby & Ray, 1686), there is surprisingly little information available on their biology and ecology. Such baseline knowledge is now urgently needed as dramatic increases in shing pressure on most species threatens the stability of many regional sub-populations (Alava et al., 2002; Dewar, 2002; White et al., 2006a). Fisheries for mobulids are considered to be unsustainable because of large, directed catches coupled with the low fecundity and conservative life history of this group. Mobulids are landed in large numbers in targeted and by-catch sheries across the globe, and the demand for mobulid products in the Asian market is rising (Lack & Sant, 2008, 2009; FAO, 2009). Assessment of the current conservation status of mobulids is hampered by the paucity of information, resulting in a data-decient status for three Mobula species (M. hypostoma, M. kuhlii and M. tarapacana) on IUCN Red List for Threatened Species (Clark et al., 2006a; Bizzarro et al., 2007, 2008). Of those that have been assessed on the IUCN Red List, four species of Mobula are listed as near threatened (M. eregoodootenkee, M. japanica, M. munkiana and M. thurstoni ), one as vulnerable (M. rochebrunei ) and one as endangered (M. mobular) (Pierce & Bennett, 2003; Bizzarro et al., 2006; Clark et al., 2006b; Notarbartolo-diSciara et al., 2006; White et al., 2006b; Valenti & Kyne, 2007). Both Manta species were reassessed in 2011 and are listed as globally vulnerable on the IUCN Red List (Marshall et al., 2011a, b). The Mobulidae are highly mobile epipelagic rays that are challenging to observe and investigate in their extensive oceanic environment. Predicting the occurrence of these pelagic species is often difcult with eld observations spatially (e.g. one study area) and temporally (e.g. by dive time and during the day and night) restricted. There are relatively few locations around the world where mobulids are easily observed and approached [e.g. Gulf of California (Notarbartolo-di-Sciara, 1988); Hawaii (Deakos
2012 The Authors Journal of Fish Biology 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, 80, 10751119
B I O L O G Y A N D E C O L O G Y O F T H E M O BU L I DA E
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et al., 2011); Mozambique: (Marshall et al., 2011c); Maldives: Kitchen-Wheeler, 2010); eastern Australia (Couturier et al., 2011)]. Even at well-established aggregation sites, obtaining detailed biological information without restraining or killing individuals can be difcult because of the large size and fast swimming abilities of most mobulid species. Species identication of mobulids has proven problematic because of the close external resemblance of many species that has led to taxonomic ambiguities (e.g. M. munkiana and M. thurstoni, M. mobular and M. japanica, M. alfredi and M. birostris). The taxonomy of the family Mobulidae has a complicated history with several generic and species synonyms described in the literature. Historically, species descriptions have been limited, often based on a single museum specimen or no type specimen at all. Misidentication of Mobula spp. is common even in the current literature, where synonyms referring to several recognized species are used [e.g. Mohanraj et al. (2009), Raje & Zacharia (2009) and Borrell et al. (2011) refer to M. diabolus, which is a synonym of M. mobular and M. kuhlii ]. The recent revision of the genus Manta (Marshall et al., 2009) is particularly important for future studies and highlights the fact that past literature needs to be re-evaluated to clarify which species is referred to. Since c. 1990, there has been a marked increase in the number of published studies on the Mobulidae [Fig. 1(a)]. Most of these studies consist of notes on taxonomy, reports on the occurrence of species and reports on by-catch and sheries [Fig. 1(b)]. There are relatively few studies on the life history and ecology of the 11 species, leaving serious gaps in the knowledge needed to understand the important aspects of biology relevant to population dynamics and conservation requirements. This is particularly true for the genus Mobula, with only 28 published studies primarily focused on at least one of these species since 1980 [Fig. 1(c)]. In contrast, Manta spp. have received increasing scientic attention over the past decade [Fig. 1(c)]. Manta rays are iconic species, and there is growing interest in their ecotourism potential, especially in coastal communities and developing countries where they can generate signicant economic benets (Anderson et al., 2010). The predictable aggregative behaviour of these species has enabled the development of this industry, as Manta spp. can be relatively easy to nd and readily approached by scuba divers or by snorkellers at the surface. Partially as a result of the growing popular interest in these species, eld research has increased in the last decade at established aggregation sites (e.g. off Australia, Hawaii, Japan, Maldives and Mozambique). One important feature of Manta spp. is that all individuals bear a unique skin pigmentation pattern on their ventral surface that can be used to differentiate individuals using photographic identication (photo-ID) (Kitchen-Wheeler, 2010; Marshall et al., 2011c). Photo-ID has already provided high-quality information on Manta spp. ecology, population structure and behaviour at several locations around the world (Kashiwagi et al., 2010, 2011; Marshall & Bennett, 2010a, b; Couturier et al., 2011; Deakos et al., 2011; Marshall et al., 2011c). Although there is an increase in published studies on the genus Manta, knowledge of their biology and ecology still remains limited, with critical biological data missing on longevity, age at maturity, growth rates, diet, short and long-term movement patterns. The current fragmented information on the biology, ecology and threats to the Mobulidae in the published literature compromises an integrated understanding of this group and limits assessment of their global status and local and regional
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Number of published studies Number of published studies 10 11 12 10 20 30 40 50 60 70 80 90 9 0 0 2 4 6 8 8
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Fig. 1. Figure legend on next page.

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management needs. This review collates the available information on the Mobulidae, both published and in the grey literature. It provides a comprehensive synthesis of all basic biological data known, the threats facing these animals and the new approaches available to help ll some of these knowledge gaps. It is hoped that this comparative synthesis will stimulate future research into these understudied species and, in so doing, contribute in the longer term to an improved prognosis for their conservation. BIOLOGY AND ECOLOGY
E VO L U T I O N
Fossil, morphological and molecular data show that the Mobulidae are one of the most derived groups of elasmobranchs (Compagno, 1977; Maisey, 1984; Nishida, 1990; Cappetta et al., 1993; Lovejoy, 1996; McEachran et al., 1996; Shirai, 1996; Dunn et al., 2003; de Carvalho et al., 2004; Gonz lez-Is is & Domnguez, 2004; a a Maisey et al., 2004; McEachran & Aschliman, 2004; Musick & Eliis, 2005; Naylor et al., 2005; Cicimurri & Knight, 2009; Claeson et al., 2010). No mobulid-like species has been found in the fossil record prior to the CretaceousTertiary boundary. Although extinct species of Mobula have a fossil record extending back to the Late Oligocene (236257 million years before present, b.p.) (Cicimurri & Knight, 2009), the earliest record of Manta is from the late early-Pliocene (c. 48 Mb.p.) (Snyder et al., 1983; Bourdon, 1999; Purdy et al., 2001; Cappetta & Stringer, 2002), although there have been some species that were erroneously referred to as Manta previously (Cappetta, 1970, 1987; Case, 1980; Bourdon, 1999). Further accounts on extinct genera can be found in the works of Herman (1979), Bourdon (1999), Cappetta & Stringer (2002) and Cicimurri & Knight (2009).
TA X O N O M I C H I S T O RY
The most recent, detailed taxonomic description of the recognized Mobula spp. can be found in the study of Notarbartolo-di-Sciara (1987b). While the genus Mobula currently comprises nine recognized species (Table I), at least 29 different species have been proposed previously (Notarbartolo-di-Sciara, 1987b; Pierce & Bennett, 2003; Froese & Pauly, 2010; Polack, 2011). The rst species to be identied, M. (Raia) mobular, was collected in the late 1700s from the Mediterranean Sea (Bonnaterre, 1788). Six species were described in the 1800s with type localities from around the globe: Jamaica, Japan, India, Malaysia, western Africa and Chile, and two in the 1900s from India and Mexico. Type material is limited, especially for the older species, and there are no holotypes to accompany the original descriptions of M. eregoodootenkee, M. kuhlii, M. mobular, M. tarapacana and M. thurstoni as
Fig. 1. Literature survey on mobulids: (a) all peer-reviewed literature, published technical shery reports and historical literature (pre-1950s, n = 263), (b) by research theme (ordered by frequency) and (c) by recent publications from the primary literature subdivided by genus Manta ( ) and Mobula ( ) (containing either Manta or Mobula in the title, n = 96). Literature was sought using ISI resource and Google Scholar using Mobulid*, Mobula, Manta, Mobulidae and devil ray as key words, and citations in key papers (Notarbartolo-di-Sciara, 1987a, b; Marshall et al., 2009).
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Table I. Biological and ecological information from both published and grey literature relevant to the conservation of mobulid species Mobula eregoodootenkee Mobula hypostoma Mobula japanica
Common name IUCN Status (year assessed)
Habitat
Gestation Longevity (years) Age at maturity (years) Maximum disc width (WD , mm) WD at maturity (mm) (M, male; F, female) 1 (>550) (Bigelow & Schroeder, 1953)
Atlantic devil ray Data decient (Bizzarro et al., 2008) Pelagic coastal and oceanic (Bizzarro et al., 2008) Unknown Unknown Unknown 1200 (Notarbartolo-di-Sciara, 1987b) M: 1140, F: 1110 (Bigelow & Schroeder, 1953)
Number of pups (WD at birth, mm)
Spinetail devil ray Near threatened (White et al., 2006b) Pelagic inshore and offshore (White et al., 2006b) Unknown Unknown Unknown 3100 (Notarbartolo-di-Sciara, 1987b) M: 2016, F: >2360 (Notarbartolo-di-Sciara, 1987b) 1 (900) (White et al., 2006a)
Diet
Pygmy devil ray Near threatened (Pierce & Bennett, 2003) Pelagic coastal (Pierce & Bennett, 2003) Unknown Unknown Unknown 1000 (Notarbartolo-di-Sciara, 1987b) <1000 (Notarbartolo-di-Sciara, 1987b) 1 (>241) (Notarbartolo-di-Sciara, 1987b) Unknown
Maximum movement recorded Unknown
Unknown
Mysid-like shrimps, striped salt-water minnow (Fundulus majalis) (Bigelow & Schroeder, 1953) Unknown Cape Lookout, North Carolina (U.S.A.): summer (Coles, 1916)
Known aggregations
Euphausiids (Nyctiphanes simplex ), other planktonic organisms (Notarbartolo-diSciara, 1988; Sampson et al., 2010) 50 km in 24 h (Freund et al., 2000) Gulf of California (summer, rare in winter) (Notarbartolodi-Sciara, 1988; Sampson et al., 2010)
Table I. Continued Mobula eregoodootenkee Unknown Unknown Unknown Unknown Mobula hypostoma Mobula japanica
Population size Population trend
Fisheries
Omani waters (Henderson & Reeve, 2011)
Unknown Possibly increasing (Bizzarro et al., 2008) Unknown
By-catch
Shark bather nets (Young, 2001)
Longline, nets (Bizzarro et al., 2008)
Conservation actions
Unknown
Unknown
Gulf of California (Notarbartolo-di-Sciara, 1987a; 1988; Sampson et al., 2010), eastern Indonesia (White & Dharmadi, 2007) European tuna purse seine shery (Amand et al., e 2010), drift gillnets (White et al., 2006a) Fishery ban in Mexico, Ecuador and Protected in New Zealand waters Mobula mobular
Mobula kuhlii
Common name IUCN Status (year assessed) Habitat
Gestation Longevity (years) Age at maturity Maximum WD (mm)
Giant devil sh Endangered (Notarbartolo-di-Sciara et al., 2006) Pelagic, offshore deep waters, shallow waters (Notarbartolo-di-Sciara et al., 2006) Unknown Unknown Unknown 5200 (Notarbartolo-di-Sciara, 1987b) Unknown
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WD at maturity (mm) (M, male; F, female)
Shortn devil ray Data decient (Bizzarro et al., 2007) Shelf pelagic near continental coastal areas (Bizzarro et al., 2007) Unknown Unknown Unknown 1000 (Notarbartolo-di-Sciara, 1987); 1197 (White et al., 2006a: M. cf. kuhlii ) M: 11501190, F: unknown (White et al., 2006a: M. cf. kuhlii )
Table I. Continued Mobula kuhlii Mobula mobular
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Number of pups (WD at birth, mm) Diet Unknown Unknown
1 (310) (Compagno & Last, 1999) Unknown
Maximum movement recorded Known aggregations
Population size
Uncommon (Compagno & Last, 1999)
Population trend Fisheries
1 (1660) (Notarbartolo-di-Sciara & Serena, 1988) Euphausiid (Meganychtiphanes norvegica), small shes (Celona, 2004; Notarbartolo-di-Sciara et al., 2006) 337 km in 120 days (Canese et al., 2011) Strait of Messina (Sicily): Late spring to autumn (Celona, 2004; Canese et al., 2011); southern Mediterranean coast in winter and northern Mediterranean coast in spring (Hemida et al., 2002, Braidii & Capap , 2001) e Unknown but in low density (Notarbartolo-di-Sciara et al., 2006) Decreasing (Notarbartolo-di-Sciara et al., 2006) North Africa (Hemida et al., 2002)
By-catch
Decreasing (Bizzarro et al., 2007) Eastern Indonesia (White & Dharmadi, 2007); Mozambique (A. Marshall, unpubl. obs.) South Africa: shark bather nets (Young, 2001); Indonesia: drift gillnets (White et al., 2006a)
Unknown
European tuna purse seine shery (Amand et al., 2010), e eastern tropical Atlantic Ocean: purse-seine shery (M nard et al., 2000), Sardinia: tuna traps (Storai et al., e 2011). High mortality from pelagic driftnet (illegal), longlines, purse seines and trawls (Bauchot, 1987; Cavanagh & Gibson, 2007) Protected under U.N. (Barcelona) Convention for the Protection Of The Mediterranean Sea Against Pollution 1976 Annexe II Mobula rochebrunei Lesser Guinean devil ray Vulnerable (Valenti & Kyne, 2007) Surface and close to the bottom (McEachran & S ret, e 1990)
Mobula munkiana
Munks devil ray Near threatened (Bizzarro et al., 2006) Shallow coastal waters (Bizzarro et al., 2006)
Table I. Continued Mobula munkiana Unknown Unknown Unknown 1330 (Notarbartolo-di-Sciara, 1987b) Unknown 1 (>350) (Notarbartolo-di-Sciara, 1987b) Small sh and plankton (Maigret & Ly, 1986) Unknown Senegal coast (Cadenat, 1958) Unknown Unknown Western Africa (Valenti & Kyne, 2007) Mobula rochebrunei
Gestation Longevity (years) Age at maturity (years) Maximum WD (mm) WD at maturity (mm) (M, male; F, female) Number of pups (WD at birth, mm)
Diet
Population size Population trend Fisheries
By-catch Conservation actions Mobula tarapacana
Unknown Unknown Unknown 1100 (Notarbartolo-di-Sciara, 1987b) M: 820 (Notarbartolo-di-Sciara, 1987b), F: 910 (Villavicencio-Garayzar, 1991) 1 (350360) (Notarbartolo-di-Sciara, 1987b; Villavicencio-Garayzar, 1991) Mysidium spp. (Notarbartolo-di-Sciara, 1988) Unknown Gulf of California: mainly winter (Notarbartolo-di-Sciara, 1988) Unknown Unknown Gulf of California (Notarbartolo-di-Sciara, 1987a, b; 1988; Bizzarro et al., 2009), Ecuador (A. Marshall, unpubl. obs.) Unknown Fishery ban in Mexico and Ecuador Gillnet (Valenti & Kyne, 2007) Unknown Mobula thurstoni Bentn devil ray Near threatened (Clark et al., 2006b) Shallow neritic waters (Clark et al., 2006b) Unknown Unknown
Gestation Longevity (years)
Chilean devil ray Data decient (Clark et al., 2006a) Oceanic and occasionally in coastal waters (Clark et al., 2006a) Unknown Unknown
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Table I. Continued Mobula tarapacana Unknown 3700 (Compagno & Last, 1999) M: 23402522, F: unknown (White et al., 2006a) 1 (>1052) (Notarbartolo-di-Sciara, 1987b) Various planktonic organisms, small sh (Notarbartolo-di-Sciara, 1988) Mobula thurstoni
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Age at maturity (years) Maximum WD (mm) WD at maturity (mm) (M, male; F, female) Number of pups (WD at birth, mm) Diet
Population size Population trend Fisheries
Unknown 1800 (Notarbartolo-di-Sciara, 1987b) M: >1500, F: 1538 (Notarbartolo-di-Sciara, 1987b; White et al., 2006a) 1 (650850) (Notarbartolo-di-Sciara, 1987b) Shift in diet according to season: Euphausiidae spp. (N. simplex ) in summer, Mysidium spp. (juvenile) in winter, other planktonic organisms (Notarbartolo-diSciara, 1988; Sampson et al., 2010) Unknown Gulf of California: present all year around (Notarbartolo-di-Sciara, 1988) Unknown Unknown Lamakera, Indonesia (Dewar, 2002); Gulf of California (Notarbartolo-di-Sciara, 1987a, b; Sampson et al., 2010), eastern Indonesia (White & Dharmadi, 2007); India (Pillai, 1998, Mohanraj et al., 2009) Indonesia (White et al., 2006a), south-eastern Brazil (Casas et al., 2006)
By-catch
Unknown Gulf of California: summer and autumn (Notarbartolo-di-Sciara, 1988) Unknown Unknown Lamakera, Indonesia (Dewar, 2002), eastern Indonesia (White & Dharmadi, 2007); Gulf of California (Notarbartolodi-Sciara, 1987a, b); Senegal (Marine Megafauna Association, pers. comm.) European tuna purse-seine shery (Amand et al., 2010), Indonesia (White e et al., 2006a); North-west Africa (Zeeberg et al., 2006) Fishery ban in Mexico, Ecuador Manta alfredi Reef manta Vulnerable (Marshall et al., 2011a)
Fishery ban in Mexico, Ecuador Manta birostris Giant manta Vulnerable (Marshall et al., 2011b)
Common name IUCN Status (year assessed)
Table I. Continued Manta alfredi Manta birostris
Habitat
Gestation Longevity (years) M: 36, F: unknown (Clark, 2010) 5000 (Marshall et al., 2009) M: 27003000, F: 37003900 (Marshall et al., 2009; Clark, 2010; Deakos, 2010b) 1 (13001500) (Marshall et al., 2009) Planktonic crustaceans (Whitley, 1936) >500 (Couturier et al., 2011)
Inshore, coastal areas (Marshall et al., 2009) 1213 months (Marshall & Bennett, 2010b) >31 (Clark, 2010)
Age at maturity (years) Maximum WD (mm)
WD at maturity (mm) (M, male; F, female) Number of pups (WD at birth, mm) Diet
Offshore, oceanic, productive coastlines (Marshall et al., 2009) Unknown >20 (A. Marshall, J. Holmerg, J. M. Brunnschweiler & S. J. Pierce, unpubl. data) Unknown >7000 to 9000 (Compagno & Last, 1999; Marshall et al., 2009) M: 3800, F: 4130 (White et al., 2006a) 1 (Beebe & Tee-Van, 1941; White et al., 2006a) Shrimp, crabs and small shes (Bigelow & Schroeder, 1953) >1000 (Rubin et al., 2008; Marshall et al., 2010) Gulf of California, Mexico; Ecuador; Mozambique; Sri Lanka; Indonesia (Marshall et al., 2009; Kashiwagi et al., 2011*) Minimum numbers in Kashiwagi et al. (2011)
Maximum movement recorded (km) Known aggregations
Population size
Population trend
Hawaii; Mozambique; Maldives; Ryukyu Island, Japan; Yap; Indonesia; eastern Australia, Western Australia (Marshall et al., 2009; Kashiwagi et al., 2011*) Total population in Mozambique: 802 individuals (Marshall et al., 2011c); maximum seasonal population in Hawaii: 230 individuals (Deakos et al., 2011), minimum numbers at other locations in Kitchen-Wheeler (2010); Couturier et al. (2011); Kashiwagi et al. (2011) Eastern Indonesia: decreasing (Dewar, 2002)
Unknown
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Table I. Continued Manta alfredi North Sulawesi, Indonesia (Anon, 1997); eastern Indonesia (Dewar, 2002), Mozambique (Marshall et al., 2011a) Manta birostris
Fisheries
By-catch
Papua New Guinea (C. Rose, pers. comm.); Philippines (Dolar, 2004); KwaZulu-Natal, South Africa (Young, 2001), eastern Australia (Sumpton et al., 2011)
Manta protected zones in the Maldives, Yap and Hawaii
Indonesia (White et al., 2006a), India (Pillai, 1998; Mohanraj et al., 2009), Sri Lanka (P. Hilton, pers. comm.); Tanzania (Bianchi, 1985; Jiddawi & Stanley, 1999; A. Marshall, unpubl. obs.); Peru (M. Harding, pers. comm.); Ghana (Essumang, 2010) Atlantic Ocean (Amand et al., 2010); KwaZulu-Natal, e South Africa (Young, 2001); West Thailand (A. Marshall, unpubl. obs.); Ecuador and Peru (M. Harding, pers. comm.); South Brazil (Zerbini & Kotas, 1998); Georgia and east Florida (Trent et al., 1997; Carlson & Lee, 2000); central-western Pacic (Coan et al., 2000) Legally protected in Hawaii, Mexico, Ecuador, New Zealand, Philippines [see Fig. (4)]
*General comments on abundance at 20 localities can be found in Kashiwagi et al. (2011) but the number of photographic records provided in the Appendix is not equivalent to population size estimates.
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some were not collected and some have been lost (Polack, 2011). This lack of original material and the on-going uncertainties about species ranges and identities, such as possible confusion of M. mobular with M. japanica, can only be resolved through contemporary collection of both morphological examinations and genetic samples. The genus Manta has a long and confused taxonomic history. Over 10 generic and 25 specic synonyms have been used to describe manta rays since Walbaums (1792) rst description (some authors ascribe the original species designation to Donndorffs (1798) description of Walbaums species). Difculties associated with transporting and preserving large specimens have resulted in a paucity of preserved specimens, and type material is absent for almost all of the species described since 1792. The genus currently includes two recognized species, with the possible existence of a third putative species Manta sp. cf. birostris, proposed to be endemic to the western Atlantic Ocean and Caribbean Sea (Marshall et al., 2009). The failure to differentiate the two Manta spp. prior to 2009 has resulted in confusion concerning almost all the biological information available (Homma et al., 1999; Dewar et al., 2008).
DISTRIBUTION
Mobulids occur in tropical and temperate seas between 40 N and 40 S, although the majority of species have a tropical to subtropical distribution (Fig. 2). These rays have an apparent preference for water temperatures of 2026 C (Dewar et al., 2008; Clark, 2010; Canese et al., 2011; Marshall et al., 2011c). Mobula spp. are regarded as pelagic or epipelagic species of coastal waters, and may be encountered in both shallow-inshore environments and deeper offshore waters (Bizzarro et al., 2007; Cort s & Blum, 2008; Scacco et al., 2009; Canese et al., 2011). Manta alfredi, M. e birostris, Mobula japanica, M. tarapacana and M. thurstoni have worldwide distributions, with each species reported from the Pacic, Atlantic and Indian Oceans (Clark et al., 2006a, b; White et al., 2006b; Marshall et al., 2009, 2011a, b; Kashiwagi et al., 2011) [Fig. 2(a), (b)]. The only observation of M. tarapacana from the western Atlantic Ocean is based on an aerial survey off Venezuela (Notarbartolo-di-Sciara & Hillyer, 1989), and conrmation of this species occurrence in the Caribbean Sea is required. Mobula eregoodootenkee and M. kuhlii are both restricted to the Indo-West Pacic Ocean (Pierce & Bennett, 2003; Bizzarro et al., 2007) [Fig. 2(c)]. Mobula eregoodootenkee has a contiguous distribution from coastal regions of southern Africa to northern Australia, Papua New Guinea and the Philippines (Pierce & Bennett, 2003). In contrast, records for M. kuhlii are patchy over a similar range (Bizzarro et al., 2007), possibly as a result of misidentications or insufcient sampling [Fig. 2(a)]. White et al. (2006a) refer to specimens from Cilacap, Java, Indonesia, as M. cf. kuhlii, suggesting that there is uncertainty about the species identity in this region. The record from the Philippines is for a single individual from Iloilo City Fish Port (Compagno et al., 2005). Further investigation of the distribution of M. kuhlii is needed. Mobula hypostoma is a widely distributed species endemic to coastal and shelf waters of the western Atlantic Ocean, from North Carolina, U.S.A., through much of the Gulf of Mexico, Greater and Lesser Antilles, to northern Argentina in the south (McEachran et al., 2002; Bizzarro et al., 2008) [Fig. 2(c)]. Mobula munkiana is endemic to tropical coastal and oceanic waters in the eastern Pacic Ocean, extending to the waters of Cocos, Malpelo and Galapagos Islands (Bizzarro et al., 2006;
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Smithsonian Tropical Research Institute, 2011) [Fig. 2(c)]. Mobula rochebrunei is a pelagic species found primarily along the central and south-eastern Atlantic coast of Africa (Cadenat, 1958; Maigret & Ly, 1986; McEachran & S ret, 1990), although e there are isolated records of the species from coastal waters off Paran State, Brazil a (Valenti & Kyne, 2007) [Fig. 2(c)]. Further verication of this species in the western Atlantic Ocean is required. Mobula mobular is an offshore, epipelagic species that occasionally frequents shallow coastal waters. Some authors consider this species to be endemic to the Mediterranean Sea (Notarbartolo-di-Sciara & Bianchi, 1998), whereas others suggest that its range extends to waters of the eastern Atlantic Ocean (Scacco et al., 2009). Reports of this species encompass Ireland in the north, Senegal in the south and remote offshore islands including the Azores, Canary Islands, Cape Verde Islands and Madeira (Santos et al., 1997; Wirtz et al., 2008) [Fig. 2(c)]. The species has even been suggested to occur in waters off Cuba, the U.S.A. and India (Froese & Pauly, 2010; Zacharia & Kandan, 2010). Many of these records need to be veried as they are unconrmed and misidentication cannot be excluded because of the close morphological resemblance with M. japanica (Notarbartolo-di-Sciara, 1987b Notarbartolo-di-Sciara et al., 2006). Further taxonomic description of both M. mobular and M. japanica is likely to aid eld workers, particularly as the separation of both species is only based on the observation of one specimen of M. mobular (Panceri & De Sanctis, 1869; Notarbartolo-di-Sciara, 1987b). An author survey of Mobula images taken by recreational divers and accessible on the internet indicates that this species occurs at many sites in the Mediterranean Sea (e.g. Crete, Corsica and Sardinia) for which there are no formal scientic records.
P O P U L AT I O N T R E N D S
The current status of each mobulid species is unclear, as research into population trends is only in its infancy. Understanding the status of these wide-ranging species across their entire distributions remains a challenge. Estimates of the world global catch of mobulids have increased from c. 900 t in 2000 to >3300 t in 2007 (FAO, 2009; Lack & Sant, 2009). Despite the increasing catches worldwide, dramatic declines in mobulid catches have been documented in some areas (e.g. Philippines: Alava et al., 2002), suggesting serial depletions through over-shing. There are no solid quantitative data to determine long-term population trends with the exception of M. hypostoma in the Atlantic Ocean region, which is thought to be increasing based on trawl surveys conducted since 1989 (Bizzarro et al., 2008). The use of photo-ID methodology has enabled minimum estimates of M. alfredi populations at several locations around the world (Kashiwagi et al., 2011). Current local population sizes of M. alfredi in Hawaii indicate that up to 230 are resident to the island of Maui within one sampling period of c. 3 months (Deakos et al., 2011). In Mozambique, the annual population estimates of M. alfredi vary between 149 and 454, with a total population estimate of 890 (Marshall et al., 2011c) (Table I). Although all current estimates of population size are for M. alfredi, minimum numbers of individuals identied at aggregation sites exist for M. birostris (Kashiwagi et al., 2011). Without signicant natural markings on which to base photo-ID studies, efforts to quantify numbers of Mobula spp. are effectively limited to sheries data, aerials surveys and studies that employ conventional tags. Such approaches have yet to produce reliable population estimates for these species.
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(a)
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Fig. 2. Figure legend on next page.
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M O V E M E N T S A N D A G G R E G AT I O N S
Movement patterns and swimming capacities of most mobulid species are poorly understood. All mobulids are believed to undertake relatively large-scale movements, travelling from one productive area to another, and some species aggregate at specic locations (Notarbartolo-di-Sciara, 1988; Celona, 2004; Couturier et al., 2011). While members of each species may be seen alone, or with a few other individuals, most species have been observed travelling and feeding in schools. Schools may contain a few to hundreds of individuals and aggregate seasonally in large numbers at different locations throughout their ranges (Table I). Predictable aggregations of mobulids are mainly associated with local productivity and food availability (Notarbartolodi-Sciara, 1988; Celona, 2004; Sleeman et al., 2007; Dewar et al., 2008; Marshall, 2009; Anderson et al., 2011; Couturier et al., 2011; Marshall et al., 2011c). The aggregative behaviour of Mobula spp. remains largely understudied, with most information on potential aggregation drawn from sheries data in which some species are caught more frequently during particular seasons (e.g. Gulf of California: Notarbartolo-di-Sciara, 1987a; Mumbai: Raje & Zacharia, 2009). The seasonal occurrence of M. munkiana in winter in the Gulf of California and M. japanica and M. tarapacana in summer appears to be linked to the seasonal abundance of different types of zooplanktonic prey (Notarbartolo-di-Sciara, 1988). Mobula thurstoni is the only species known to occur all year around at this location (Notarbartolo-di-Sciara, 1988). Smaller individuals are mostly caught during winter suggesting temporal size segregation of this species in the Gulf of California (Notarbartolo-di-Sciara, 1988). Mobula mobular seasonally aggregates between late spring and summer in the Messina Strait, central Mediterranean Sea (Celona, 2004; Canese et al., 2011). There are also suggestions that the species undertakes seasonal northsouth migrations within the Mediterranean Sea in relation to water temperature or productivity (Hemida et al., 2002; Celona, 2004; Scacco et al., 2009). The limited information available on the movement of Mobula spp. includes one published study of M. mobular (Canese et al., 2011) and one conference abstract on M. japanica (Freund et al., 2000). Satellite tag data for three M. mobular individuals in the Messina Strait, central Mediterranean Sea, have shown that they spent >80% of their time within the upper 50 m of the water column and dived to 700 m depth (Canese et al., 2011). One tagged individual travelled 278 km in 60 days, while the two others travelled 298 and 337 km in 120 days (Canese et al., 2011). Using acoustic telemetry techniques in the southern Gulf of California, M. japanica has been
Fig. 2. Distributions of mobulid species. (a) Distributions of the two known species of manta rays, Manta alfredi ( ) and Manta birostris ( ). This gure incorporates data from Kashiwagi et al. (2011) and the new IUCN Red List assessment for these species (Marshall et al., 2011a, b). In some regions, both species occur close to one another and are colour-coded accordingly ( ) [Kashiwagi et al. (2011) provides further detail about sympatric and allopatric occurrence]. (b) Distribution of wide-ranging species of Mobula: Mobula japanica ( ), Mobula tarapacana ( ) and Mobula thurstoni ( ); adapted and modied from Clark et al. (2006a, b) and White et al. (2006b). (c) Distribution of regionally endemic species of Mobula: Mobula eregoodootenkee ( ), Mobula hypostoma ( ), Mobula kuhlii ( ), Mobula mobular ( ), Mobula munkiana ( ) and Mobula rochebrunei ( ); adapted and modied from Pierce & Bennett (2003), Bizzarro et al. (2006, 2007, 2008), Notarbartolo-di-Sciara et al. (2006) and Valenti & Kyne (2007). Question marks indicate some uncertainty about the identity of M. mobular in the North Atlantic Ocean, and M. kuhlii off Java, Indonesia.
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shown to move relatively fast, travelling up to 50 km in 24 h with swim speeds of up to 83 km h1 (Freund et al., 2000). Tagged animals spent most of their time at relatively shallow depths, with occasional deeper excursions to 445 m (Freund et al., 2000). Manta spp. tend to form predictable aggregations. Aggregations and movements in both M. alfredi and M. birostris species are associated with seasonal food availability, current circulation patterns, seawater temperature, mating behaviour and cleaningstation visits (Sleeman et al., 2007; Dewar et al., 2008; Luiz et al., 2009; Anderson et al., 2011; Couturier et al., 2011). Over the past few years, movements and swimming behaviour of Manta spp. have been documented at several locations (Dewar et al., 2008; Kashiwagi et al., 2008; Couturier et al., 2011; Deakos et al., 2011; A. Marshall, J. Holmerg, J. M. Brunnschweiler & S. J. Pierce, unpubl. data). Manta spp. are regularly present around shallow-reef cleaning stations and coastal feeding grounds during daylight hours and potentially move to deeper and offshore waters at night (Dewar et al., 2008; Marshall et al., 2009; Clark, 2010; Anderson et al., 2011). Long-term sighting records of M. alfredi at established aggregation sites suggest that this species is more resident than M. birostris, preferring inshore tropical waters and exhibiting relatively small home ranges and movements (Homma et al., 1999; Dewar et al., 2008; Kitchen-Wheeler, 2008; Anderson et al., 2011; Couturier et al., 2011; Deakos et al., 2011; Marshall et al., 2011c). Using acoustic telemetry, van Duinkerken (2010) found that M. alfredi can travel up to 70 km in a day and photoID studies have shown that this species undertakes seasonal migrations of up to 500 km between known aggregation sites (Homma et al., 1999; Kashiwagi et al., 2010; Kitchen-Wheeler, 2010; Anderson et al., 2011; Couturier et al., 2011). In the Hawaiian Islands, M. alfredi appears not to travel between Maui and Hawaii Islands, only 49 km apart, despite intensive monitoring between 2005 and 2009 in both places (Clark, 2010; Deakos et al., 2011). Movements of M. alfredi may be restricted here by bathymetric features or regional circulation patterns (Deakos et al., 2011). Manta birostris is a larger, more oceanic and probably more migratory species than M. alfredi, with individuals regularly sighted around offshore islands, oceanic seamounts and submarine ridge systems (Yano et al., 1999; Rubin, 2002; Marshall et al., 2009; Kashiwagi et al., 2010, 2011). In addition, rare or seasonal sightings of M. birostris at locations such as northern New Zealand (Duffy & Abbott, 2003), southern Brazil (Luiz et al., 2009), the Azores and the Similan Islands (A. Marshall, pers. obs.), and the eastern coast of the U.S.A. (Bigelow & Schroeder, 1953) suggest that this species undergoes extensive migrations. Preliminary pop-off satellite tag studies have recorded broad-scale movements of >1000 km (Rubin et al., 2008; A. Marshall, J. Holmerg, J. M. Brunnschweiler & S. J. Pierce, unpubl. data). Together with international photo-ID projects, these data have so far revealed little interchange between regional populations, and whether M. birostris crosses ocean basins is still unknown.
R E P RO D U C T I O N
The Mobulidae, as all chondrichthyans, employ internal fertilization to reproduce (Wourms, 1977; Carrier et al., 2004; Pratt et al., 2005). Data on the time for claspers to extend past the pelvic ns, together with observation of mating behaviour, suggest
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that male M. alfredi mature at 36 years in Hawaii (Clark, 2010). Field observations in Mozambique and Japan indicate a complex mating process for both Manta species, which involves a ritualized sequence of chasing, biting, copulating, post-copulation holding and separation (Yano et al., 1999; Marshall & Bennett, 2010b). Mating behaviour in the wild has rarely been observed and so far has only been documented for M. alfredi and M. birostris (Yano et al., 1999; Marshall & Bennett, 2010b). Mobulids are aplacental viviparous (Gill, 1908; Wourms, 1977; Dulvy & Reynolds, 1997). Embryos develop in the uterus, where they initially feed on the yolk and are then nourished with protein and lipid-rich histotroph or uterine milk, secreted by uterine villi (Wourms, 1977; Dulvy & Reynolds, 1997; Compagno & Last, 1999). The gestation period of most species is unknown, but the reproductive cycle is likely to last for c. 1 year, with occasional resting period of 2 years between pregnancies (Notarbartolo-di-Sciara, 1988; Marshall & Bennett, 2010b). Marshall & Bennett (2010b) reported a gestation period in M. alfredi of c. 1 year in the wild. Similar gestation periods were observed under captivity in the Churaumi Aquarium, Okinawa, Japan, where a captive M. alfredi gave birth four times, after 366374 days of gestation (Okinawa Churaumi Aquarium, 2010). All mobulid species normally give birth to a single pup, but may produce twins on rare occasions (Gill, 1908; Coles, 1913; Notarbartolo-di-Sciara, 1987b; Marshall & Bennett, 2010b). Data on size at birth and size at maturity for each species are summarized in Table I.
AG E , G ROW T H A N D L O N G E V I T Y
Mobulids are widely presumed to be long lived and slow growing, in keeping with their relatively large sizes and low reproductive rates (White et al., 2006a; Deakos et al., 2011). This hypothesis remains largely untested. As yet, there have been no published studies on the ageing and growth of Mobula spp. or Manta spp. despite their prevalence in sheries. This dearth of information may be partially explained by the apparent difculty in ageing these species. The conventional ageing technique applicable to most elasmobranch species is to section vertebral centra in the thoracic region (Cailliet et al., 2006). Generally, growth-band pairs are visible to a greater or lesser degree within centra obtained from the anterior vertebrae of sharks (Goldman, 2004) and posterior vertebrae of batoids (White et al., 2001; Pierce & Bennett, 2010). It appears that at least some mobulid species have a highly derived vertebral structure that makes it difcult to use this technique (Cuevas-Zimbr n, 2007). Dissections o of M. alfredi (S. Pierce, unpubl. obs.) and M. birostris (A. Marshall, unpubl. obs.) suggest that Manta species do not have obvious calcied centra. Mobula japanica specimens from Mexico have been successfully aged based on band-pair counts from caudal vertebrae with the maximum number of 14 band pairs found in a female of o o 2300 mm WD (Cuevas-Zimbr n, 2007; Cuevas-Zimbr n et al., 2008). Unlike many elasmobranch species, for which maximum age is modelled from growth curves, long-term diver visits to some areas where Manta spp. are commonly sighted provide eld observations of minimum longevity. Photo-ID surveys of M. alfredi off Japan and Hawaii indicate that this species can live for at least 30 years (Ito, 1987; 2000; Kashiwagi et al., 2008; Clark, 2010; Marshall et al., 2011a) while individuals of M. birostris have been re-sighted using photo-ID up to 20 years after their initial identication (Marshall et al., 2011b). These observations place both Manta species amongst the longest-lived batoids (Smith et al., 2007;
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Pierce & Bennett, 2010) and, as the age at rst identication of these animals was unknown, actual longevity is likely to be exceptional within this group.
FEEDING Behaviour and strategies
Despite regular observations of feeding activities, the feeding behaviour and strategies of mobulids have only been cursorily described. As in all planktivorous elasmobranchs, mobulids possess gills modied into complex rigid sieving plates for ltering plankton (Bigelow & Schroeder, 1953; Cort s et al., 2008). Descriptions e of these branchial sieve plates can be found in Bigelow & Schroeder (1953) for M. birostris and M. hypostoma. When feeding, mobulids are generally observed to swim forward with an open mouth creating a passive water ow through the gill-raker apparatus, a behaviour referred to as ram lter feeding (Sanderson & Wassersug, 1990; 1993; Cort s et al., 2008). Cephalic lobes are used to guide water into the e mouth, where food particles then get sieved by the gill rakers before the water exits the oropharyngeal cavity through the gill slits (Coles, 1916; Paig-Tran et al., 2011). Anecdotal reports on feeding behaviour of Manta spp. reveal varying foraging strategies between locations, most likely related to prey density and foraging efciency (Coles, 1916; Deakos, 2010a). For example, hundreds of M. alfredi have been reported to aggregate in the Maldives where they perform chain feeding, following each other in a circling movement from surface to bottom creating a cyclonic motion (Law, 2010). Observations of feeding behaviour in localized looping motion and bottom skimming were also made at several Manta spp. aggregation sites, highlighting the adaptive responses of these animals according to prey distribution in the water column (Deakos, 2010a; Osada, 2010).
Diet
Stomach content analyses indicate that mobulids feed on zooplankton and small shes (Whitley, 1936; Bigelow & Schroeder, 1953; Notarbartolo-di-Sciara, 1988; Celona, 2004). Those studies highlight that several mobulid species appear to target high abundances of zooplankton found seasonally at certain locations (Notarbartolodi-Sciara, 1988; Celona, 2004; Sampson et al., 2010). Aggregations of several Mobula species in the Gulf of California coincide with the peak abundance of the euphausiid Nyctiphanes simplex (Hansen 1912), and this prey item dominates the stomach contents of several Mobula spp. caught in that region (Notarbartolo-diSciara, 1988). Mobula munkiana is the only species in this location that is present only during winter, feeding exclusively on mysids, Mysidium spp., the most abundant planktonic prey available at this time of the year (Notarbartolo-di-Sciara, 1988). Similarly, M. mobular feeds in areas where the euphausiid Meganychtiphanes norvegica is in high density, and stomach content analysis conrmed M. norvegica as the dominant prey item (Celona, 2004). Mobula thurstoni stomach contents in the Gulf of California were dominated by either mysid shrimps or euphausiids, although the two types of prey were never found together in the same stomach (Notarbartolo-diSciara, 1988). Mobula thurstoni mainly feed on N. simplex during summer, when it is most abundant, and on Mysidium spp. during winter. These observations suggest that M. thurstoni is able to adapt and shift diet, according to the dominant food available in a particular location.
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Results from stomach content analyses corroborate stable isotope analyses that indicate that Mobula species mainly feed on zooplankton (Sampson et al., 2010; Borrell et al., 2011). These two stable isotope studies are to be interpreted with caution as calculations involving the trophic enrichment factor could be inappropriate (Hussey et al., 2010). Isotopic values in tissues of M. japanica and M. thurstoni are relatively stable, indicating a consistent diet across individuals (Sampson et al., 2010). Borrell et al. (2011) found that Mobula species caught in sheries off Vervaval, north-west India, had stable-isotope signatures consistent with those expected for zooplankton feeders. It is not possible to determine which Mobula spp. is referred to in that study as the species name, M. diabolus, is a synonym used to designate several Mobula species (Notarbartolo-di-Sciara, 1987b). Data on the diet and trophic position of species can contribute to improve ecological understanding and can help support conservation management plans for areas where the temporal and spatial abundance and distribution of prey are understood.
N AT U R A L M O RTA L I T Y
Natural predation on the Mobulidae appears to be low and opportunistic with sharks probably the most common cause. Non-fatal shark-inicted injuries are regularly observed on manta rays (Homma et al., 1999; Marshall & Bennett, 2010a; Deakos et al., 2011) and occasionally on mobulids (A. Marshall, unpubl. obs.). The frequency of shark attacks on M. alfredi individuals appears to differ among locations, with 76% of the identied population in Mozambique bearing a shark-inicted injury (Marshall & Bennett, 2010a), compared with 24% off Maui, Hawaii (Deakos et al., 2011). Attackers of M. alfredi are thought to be primarily larger sharks such as grey reef sharks Carcharhinus amblyrhynchos (Bleeker 1856), silvertip sharks Carcharhinus albimarginatus (R ppell 1837), bull sharks Carcharhinus leucas (M ller u u & Henle 1839), tiger sharks Galeocerdo cuvier (P ron & LeSueur 1822) and great e white sharks Carcharodon carcharias (L. 1758) (Marshall & Bennett, 2010a). Galeocerdo cuvier and C. amblyrhynchos have been observed attacking and feeding on Manta spp. (Ebert, 2003; Marshall & Bennett, 2010a; Deakos et al., 2011). The rate of delayed mortality induced by shark attacks is unknown, but physical injuries and the redirection of energy into wound healing may affect reproduction in M. alfredi (Marshall & Bennett, 2010a). In addition, remains of unidentied mobulids have been found in the stomach contents of C. leucas (Cliff & Dudley, 1991). Killer whales Orcinus orca are also known to occasionally feed on mobulids (Fertl et al., 1996; Homma et al., 1999; Visser & Bonoccorso, 2003).
THREATS Mobulids are affected by numerous human activities including directed shing, incidental capture as by-catch, entanglement in marine debris and boat strikes. Mobulids are easy to target in sheries because of their large size, aggregative behaviour, predictable habitat use and lack of human avoidance. Mobulid products are valuable items in international trade markets. Their gill rakers are particularly sought after and are used in Asian medicinal products (Zhongguo yao yong dong wu zhi xie zuo zu bian zhu, 1983; Shen et al., 2003; Rajapackiam et al., 2007a).
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This market has resulted in directed sheries for nearly all mobulid species. Artisanal sheries also target both genera for food and local products (White et al., 2006a; Essumang, 2009, 2010; Marshall et al., 2011c). Mobulids are also incidental by-catch in both large-scale sheries and small netting programmes such as sharkcontrol bather-protection nets (Paterson, 1990; Krogh & Reid, 1996; Young, 2001; Sumpton et al., 2011). As a result of sustained pressure from directed shing and by-catch, certain sub-populations have rapidly declined including in India, Indonesia, Mexico, the Philippines and Mozambique (Anon, 1997; Alava et al., 2002; Mohanraj et al., 2009; Marshall et al., 2011a, b). Particularly threatening to mobulid populations is the tendency for sheries to target individuals in critical habitats or aggregation sites, where they can be caught quickly in large numbers. On the basis of seasonal abundance at aggregation sites and the size of sheries catches, regional populations appear to be relatively small, and localized declines are unlikely to be signicantly mitigated by immigration and reproduction. This situation is exacerbated by the conservative life history of these rays, which constrains their ability to recover from a depleted state.
DIRECTED FISHERIES Fishing methods
Mobulids are currently killed or captured by a variety of methods including harpooning, netting and trawling. Gillnet sheries are the most common and efcient method, with each haul taking large numbers of individuals (Alava et al., 2002). Target sheries for M. thurstoni in Kerala State, south-west India, can capture up to 65 mobulids per gillnet per haul, extrapolating to thousands of shes caught annually (K. Bineesh, pers. comm.). Gillnets are widely used in most areas where large numbers of mobulids are landed, including Indonesia (White et al., 2006a; White & Dharmadi, 2007), the Gulf of California (Bizzarro et al., 2009), India (Rajapackiam et al., 2007a; CMFRI, 2009), western Africa (Essumang, 2010) and eastern Africa (A. Marshall & S. Pierce, unpubl. obs.). In some regions, mobulids are directly shed in large trap nets set in major migratory channels such as in the Tangkoko Nature Reserve in the Manado region of North Sulawesi, Indonesia (Anon, 1997). Some artisanal sheries still employ more traditional techniques to capture mobulids such as harpoons, hand spears, gaff hooks and hook and lines (Alava et al., 2002). Harpooning is commonly used to catch both species of Manta as well as M. kuhlii in southern Mozambique for local consumption (A. Marshall, unpubl. obs.). In northeast India, seasonal organized harpoon sheries for Mobula spp. occur in Andhra Pradesh State and the Indian Union Territory of Lakshadweep, north of the Maldives (Pillai, 1998). Although the technique does not appear to be widely applied, the capture of mobulids by trawlers has been reported in both the Kerala region, India (Nair, 2003), and Tanzania (Bianchi, 1985; Jiddawi & Stanley, 1999).
Targeted species
All mobulids are sought after and targeted, generally captured using non-discriminatory methods such as gillnets. Any mobulid species present within a shing area tend to be exploited. In Indonesia, for example, mobulid landings included all species known to occur in the area (i.e. M. japanica, M. tarapacana, M. kuhlii, M. thurstoni, M. alfredi and M. birostris) (Dewar, 2002; White &
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Dharmadi, 2007). Similarly in the Gulf of California, 94% of the number of elasmobranchs caught consisted of the four Mobula species present in the area, M. thurstoni, M. japanica, M. tarapacana and M. munkiana (Notarbartolo-di-Sciara, 1987b).
Value and use
Despite these intense sheries, mobulid meat is not highly valued for consumption. It is often sold at relatively low prices or used as shark bait. Only the branchial laments are highly prized and are sent to Asia (Booda, 1984; Dewar, 2002; Rubin, 2002; White et al., 2006a; Rajapackiam et al., 2007a; Mohanraj et al., 2009). For example, mobulids in Chennai, south-east India, are sold on the seashore. Gill rakers are then removed washed and dried before being sold for comparatively high prices to traders for export to Hong Kong, Singapore, Thailand, Malaysia and China (Rajapackiam et al., 2007a; Mohanraj et al., 2009). In Sri Lanka, the trade for mobulid gill rakers has become more lucrative than the shark-n trade (Hilton, 2008).
Reported catches
Although a few studies have focused on quantifying the catch of mobulids in particular regions (e.g. eastern Indonesia, the Philippines and India), such reports remain scarce. The few studies that have been conducted project considerable numbers, with >1000 rays caught per year in some areas (Alava et al., 2002; Dewar, 2002; White et al., 2006a). Species of Mobula and Manta are caught in large numbers in Indian waters, raising concerns for the sustainability of the local targeted shing practices (Fig. 3). The annual catch of elasmobranchs in India is currently estimated at c. 70 000 t year1 (Banerjee et al., 2008), representing 10% of the world annual catch (FAO, 2009; Lack & Sant, 2009). Surveys revealed that between 2001 and 2006, 5% of the elasmobranch biomass caught along the Chennai coast were Mobula spp. (Mohanraj et al., 2009). Over 340 t of Mobula spp. can be caught at a single landing station in one shing season, as was recorded at Nagapattinam from January to March 2009 (CMFRI, 2009). Substantial landings can also occur in a single day. For example, c. 33 t of rays were landed in one day in July 2009 at the Tuticorin shery harbour, with Mobula spp. (referred to as M. mobular but probably M. japanica) constituting 11% of the catch (Zacharia & Kandan, 2010). Thousands of mobulids are caught annually in Indonesian waters leading to several hundred tonnes of mobulid products. Catch of mobulids by targeted sheries along eastern Indonesia was estimated to be 4110 individuals annually, equivalent to a biomass of 544 t and representing 38% of the total batoid shery biomass (White et al., 2006a; White & Dharmadi, 2007). On a smaller scale, a report of the shery around Alor Island, south-east Indonesia, revealed that the recent demand for mobulid products in the Asian market has led to increased shing effort on the shes through improvement of shing techniques and the equipment used (Dewar, 2002). Annual catch in this region is estimated to be 1500 individuals (range 10502400 Manta spp.) (Dewar, 2002). Additionally, a study of the catch composition in North Sulawesi, Indonesia, between March 1996 and February 1997 reported 1424 Manta spp. caught within that year. While this practice was temporarily banned, it re-started illegally in late 1997 and shing effort has moved to new unmonitored locations (Anon, 1997). Similar landings have been reported from other locations, such as the
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Fig. 3. Distribution map of recent and current sheries and by-catch locations of mobulids. All directed and trade-driven sheries on mobulids: 1 Mexico, La Paz (Booda, 1984; Notarbartolo-di-Sciara, 1987a; Rubin, 2002; Bizzarro et al., 2009; Erisman et al., 2010; Sampson et al., 2010; Cartamil et al., 2011), 2 Ecuador (M. Harding, pers. comm.), 3 Peru (M. Harding, pers. comm.), 4 Mediterranean Sea, coast of Algeria (Hemida et al., 2002), 5 Senegal (Cadenat, 1958; Marine Megafauna Association, pers. comm.), 6 Ghana (Essumang, 2009; 2010), 7 Mozambique (A. Marshall, unpubl. obs.), 8 Tanzania (Bianchi, 1985; Jiddawi & Stanley, 1999), 9 India, Veraval region (Sivaprakasam, 1964; Kunjipalu & Boopendranath, 1981; Said Koya et al., 1993; Pillai, 1998; Borrell et al., 2011), 10 India, Mumbai region (Rane, 2002; Raje & Zacharia, 2009), 11 India, Karwar (Pillai, 1998), 12 India, Union Territory of Lakshadweep (Said Koya et al., 1993; Pillai, 1998), 13 India, Kerala region, Vizhinjam (Pillai, 1998; Nair, 2003; Bineesh, pers comm.), 14 India, Gulf of Mannar and Tuticorin (Rajapackiam et al., 1990; Rajapackiam & Balasubramanian, 1994; Pillai, 1998; Abdussamad et al., 2006; Arumugam & Balasubramanian, 2006; Zacharia & Kandan, 2010), 15 India, Nagapattinam (CMFRI, 2009), 16 India, Pondicherry (Pillai, 1998), 17 India, Chennai (Said Koya et al., 1993; Pillai, 1998; Rajapackiam et al., 2007a, b; CMFRI, 2009; Mohanraj et al., 2009; Kizhakudan et al., 2010), 18 Sri Lanka, Marissa (P. Hilton, pers. comm.), 19 Thailand, north-west coast (Compagno & Last, 1999), 20 Indonesia, Java (Barnes, 2005; White et al., 2006a; White & Dharmadi, 2007), 21 Indonesia, Bali (White et al., 2006a; White & Dharmadi, 2007), 22 Indonesia, East Lombok (White et al., 2006a; White & Dharmadi, 2007), 23 Indonesia, Alor Island (Dewar, 2002), 24 Indonesia, North Sulawesi (Anon, 1997), 25 Philippines, Bohol Sea (Dolar, 1994; Alava et al., 2002). All locations where mobulids have been reported in by-catch sheries: 1 Mexico, Gulf of California (Sampson et al., 2010), 2 Mexico, Gulf of Tehuantepec (Sarmiento-Nafate et al., 2007), 3 east Pacic Ocean, Isla de la Plata, Ecuador (M. Harding, pers. comm.), 4 south-eastern Brazil (Zerbini & Kotas, 1998; Amorim et al., 2002; Casas et al., 2006), 5 western Atlantic Ocean, south-eastern U.S. (Trent et al., 1997; Carlson & Lee, 2000; Beerkircher et al., 2002, 2009; Baremore et al., 2007; Schwartz, 2011), 6 Mediterranean Sea (Bradaii & Capap , 2001; Celona, 2004; Akyol et al., 2005; Scacco et al., e 2009; Akyol & Ceyhan, 2011; Storai et al., 2011), 7 European sheries off Mauritania (Zeeberg et al., 2006), 8 European purse-seine tuna shery (Rey & Munozchapuli, 1992; M nard et al., 2000; Amand` e e et al., 2010), 9 South African coast, Natal (Dudley & Cliff, 1993; Dudley & Gribble, 1999; Young, 2001), 10 Mozambique (Olsen et al., 2009; A. Marshall & S. Pierce, unpubl. obs.), 11 west Indian Ocean (Romanov, 2002), 12 Gulf of Aden (Bonl & Abdallah, 2004), 13 The Gulf (Henderson & Reeve, 2011; Moore, 2011), 14 west coast of Thailand and Myanmar (A. Marshall, unpubl. obs.), 15 eastern Indonesia (Dharmadi et al., 2008; Blaber et al., 2009), 16 Philippines (Dolar, 1994; P. Hilton, pers. comm.), 17 Papua New Guinea (C. Rose, pers. comm.), 18 eastern Australia (Paterson, 1990; Krogh & Reid, 1996; Harry et al., 2011; Sumpton et al., 2011), 19 northern New Zealand (Paulin et al., 1982), 20 central-western Pacic tropical purse-seine shery (Coan et al., 2000), 21 Chinese Pacic longline shery (Dai & Zhu, 2008). , The by-catch area for the corresponding shery number.
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Pamilacan Island in the Philippines where up to 1000 mobulids, particularly Manta spp. and a few species of the genus Mobula, are harvested each year by directed sheries (Alava et al., 2002).
Status of current sheries
Although targeted mobulid capture has been banned in a few areas, many direct sheries remain (Fig. 3). Targeted sheries are prevalent at many locations around India, particularly along the coast of Chennai, Tuticorin, Mumbai and Veraval, within the Union Territory of Lakshadweep and in the Andhra Pradesh and Kerala regions (Sivaprakasam, 1964; Said Koya et al., 1993; Rajapackiam & Balasubramanian, 1994; Pillai, 1998; Nair, 2003; Rajapackiam et al., 2007a, b; CMFRI, 2009; Mohanraj et al., 2009; Zacharia & Kandan, 2010). Some of these sheries are highly organized and efcient, such as a new shery formed along the Chennai coast that uses mechanized gillnets, following the high demand for mobulid products (Pillai, 1998; Rajapackiam et al., 2007a). After years of exploitation, mobulid catches have begun to decline in most shed regions suggesting serial depletions. Although shing effort has been increasing, annual landing of rays (including Mobula spp.) has been declining in several areas of India, including in the Kerala region (Nair, 2003) and along the Chennai (Mohanraj et al., 2009) and Tuticorin coasts (Zacharia & Kandan, 2010). Fisheries surveys in Mumbai waters revealed that shes were landed at a rate of 065 kg h1 in 1990, but only 024 kg h1 in 2004 (Raje & Zacharia, 2009). A dramatic reduction in mobulid capture was also reported in eastern Indonesia (Dewar, 2002; White et al., 2006a). Barnes (2005) reported that manta rays were historically shed by indigenous villagers in this region, with up to 360 animals caught in one year, but the shes became gradually scarcer until the catch rate reached zero.
Management and regulations
In response to the decline in mobulid catches, some regions have banned directed sheries, established marine protected areas and enacted protection legislation for some species (Fig. 4). The enforcement of those bans remains uncertain in many regions and illegal capture of mobulids still occurs and remains unreported (Anon, 1997, Alava et al., 2002, Bizzarro et al., 2009, Smith et al., 2009; Erisman et al., 2010). Moreover, many of the current management and interjurisdictional regulations for the Manta genus need to be reassessed, as most were put into place prior to the re-description of the two species. Consequently, M. birostris is the only Manta species mentioned and legally protected by some of this legislation (Fig. 4) and M. alfredi remains unprotected although this species more commonly occurs in tropical and subtropical coastal areas and thus is widely exposed to sheries. In regions where bans have successfully been enforced, such as in the Maldives, sheries have been replaced with equally or more lucrative tourism industries (Anderson et al., 2010).
B Y- C AT C H
Mobulids are caught as by-catch in purse-seine and trawl sheries as well as netting programmes throughout their distributions (Fig. 3). The most threatened mobulid
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4 1 2 5 3 6 9 7 8
Fig. 4. Distribution map of current shing bans, management regulations and specic species protection for mobulids: 1 Hawaii, June 2009: introduction of criminal penalties and administrative nes for knowingly killing or capturing Manta spp. within state waters, House Bill 366 signed into law as Act 092; 2 Mexico, May 2007: the Mexican ofcial standard rules that regulate the shark and ray sheries in Mexican waters, Pesca responsable de tiburones y rayas. Especicaciones para su Aprovechamiento, 2005. Norma Ocial Mexicana Nom029-Pesc-2006, NOM 029 provides specic protection for Manta birostris, Mobula japanica, Mobula thurstoni, Mobula munkiana, Mobula hypostoma and Mobula tarapacana in Mexican waters; 3 Ecuador, August 2010: ban on shing, taking, keeping incidental catch for M. birostris, M. japanica, M. thurstoni, M. munkiana and M. tarapacana, La subsecretara de recursos pesqueros considerando. Acuerdo 093; 4 Mediterranean, 1995: Mobula mobular protected under U.N. (Barcelona) Convention for the Protection Of The Mediterranean Sea Against Pollution Annexe II; 5 Republic of Maldives, June 1995: export ban on ray products (preventing commercial sheries). Regulation No A-23/95; January 1996: export of ray skins prohibited Regulation No A-26/95 (of 15.7.95); June 2009: marine park areas created at two sites recognized as critical habitat for Manta alfredi ; 6 Western Australia, Manta spp. protected from any shing (Fisheries Act) and disturbance and harassment (Environment and Conservation Act) within marine parks only; 7 Philippines, March 1998: ban on the taking or catching, selling, purchasing and possessing, transporting and exporting of whale sharks (Rhincodon typus) and M. birostris. Fisheries Administrative Order 193 (implanted in 1998 then lifted in 1999 before being reestablished in 2002. Mobula spp. are not protected under this ban); 8 Yap, Micronesia, 2008: protected area for Manta spp. and their habitat [includes 16 main islands and 145 islets representing 21 349 km2 (8243 square miles)]. Manta Ray Sanctuary and Protection Act of 2008. Bill No 7-69,D1. Yap State Law No. 7-36 (note: not yet added to the Yap State Code, new Chapter 12 of title 18 of the Yap State Code to be created see law 7-36 in Seventh State Legislature); 9 New Zealand, 2010: M. birostris and M. japanica fully protected within New Zealand waters. Wildlife Act 1953, Schedule 7A.
ray, M. mobular, is subject to a high mortality rate as a result of incidental capture (Notarbartolo-di-Sciara et al., 2006). This ray is frequently caught as a by-catch in the Mediterranean Sea and eastern Atlantic Ocean (although this may be M. japanica) and is likely to be at unsustainable levels (Cadenat, 1958; M nard et al., 2000; e Bradaii & Capap , 2001; Celona, 2004; Akyol et al., 2005; Notarbartolo-di-Sciara e et al., 2006; Scacco et al., 2009; Amand` et al., 2010; Storai et al., 2011). e Tuna purse-seine sheries are one of the main contributors to mobulid by-catch with several species regularly caught in relatively large numbers. In the western
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Indian Ocean, between 53 and 112 t of mobulids are caught each year in these sheries (Romanov, 2002). It appears that the largest species of mobulids (Manta spp., M. mobular, M. tarapacana and M. japanica) are being caught by these offshore sheries. Globally distributed species such as Manta spp. and M. japanica are regularly caught in most oceans, including the eastern Atlantic Ocean (Amand` e et al., 2010), central-western Pacic Ocean (Coan et al., 2000), western Indian Ocean (Romanov, 2002), off Papua New Guinea (C. Rose, pers. comm.) and northern New Zealand (Paulin et al., 1982). Gillnet sheries also contribute to regular non-target landing of mobulid species at many locations. Reports of mobulid by-catch in these net sheries have been identied from the Philippines (Dolar, 1994), Indonesia (White et al., 2006a) and off the south-eastern U.S.A. (Trent et al., 1997; Carlson & Lee, 2000; Baremore et al., 2007) (Fig. 3). Industrial trawlers are also likely to have a considerable effect on mobulid species with up to 620 manta rays caught per year by trawlers operating off the north-west African coast (Zeeberg et al., 2006). This report indicates the catch to be M. birostris, but a photograph purporting to be a Manta sp. is actually a Mobula, most likely M. tarapacana, and further consideration of the raw data by the authors suggests that all catches were Mobula specimens. Mobulid species are also occasionally caught in longline sheries in the Atlantic Ocean (Rey & Munozchapuli, 1992; Trent et al., 1997; Carlson & Lee, 2000; Beerkircher et al., 2002, 2009; Baremore et al., 2007; Schwartz, 2011). Mobulids are regularly recorded as incidental catches in shark-control nets off both Australian and South African coasts (Paterson, 1990; Dudley & Cliff, 1993; Krogh & Reid, 1996; Dudley & Gribble, 1999; Young, 2001; Sumpton et al., 2011). Young (2001) reported that the KwaZulu-Natal shark-control nets caught 1191 manta (Manta spp.) and 440 devil rays (Mobula spp.) between 1981 and 2000, with up to three individuals caught per day. Mobulids constituted 12% of the total catch by number from these nets between 1981 and 1990, with a mean annual catch of 66 individuals and an average mortality rate of 33%. Of the 440 Mobula caught, 19 were identied as M. kuhlii, four as M. japanica and one as M. eregoodootenkee, leaving over 94% of the catch unidentied to species (Young, 2001). Similarly in Queensland, Australia, Sumpton et al. (2011) found that 93 mobulids from both genera were caught between 1992 and 2008 in shark-control nets, with a mortality rate of 41% for Manta spp. and 89% for Mobula spp. Although incidental catch and by-catch might not represent a major threat to mobulid populations, it is an additional stressor on top of the targeted sheries and other anthropogenic activities.
O T H E R T H R E AT S
Cryptic threats such as mooring-line entanglement and boat strikes can also wound mobulids, decrease tness and contribute to mortality (Marshall & Bennett, 2010a; Deakos et al., 2011). Many other threats have the potential to harm mobulids at a global scale such as habitat degradation, climate change, pollution, ingestion of microplastics and irresponsible tourism practices. Unmanaged, rapidly growing tourism (including in-water interactions and recreational boating trafc) is likely to affect Manta spp. use of and visit rates to critical cleaning and feeding habitats (Anderson et al., 2010; Osada, 2010; Deakos et al., 2011).
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Marine debris harms and kills a large number of marine animals through entanglement and ingestion (Laist, 1987; Hiruki et al., 1993; Cliff et al., 2002; Derraik, 2002; Page et al., 2004; Chaloupka et al., 2008; Boerger et al., 2010). Mobulids can become entangled, especially Manta spp., which are regularly observed hooked by lost shing lines (Marshall & Bennett, 2010a; Deakos et al., 2011). In Maui, Hawaii, 10% of the M. alfredi population has amputated or non-functioning cephalic ns, most likely caused from entanglement in monolament shing line (Deakos et al., 2011). Such debris may also greatly affect the tness and survival of marine species, especially since many are already affected by other threats such as shing (Cliff et al., 2002; Derraik, 2002). Ingestion of plastic debris by sea turtles, seabirds, sharks and shes has been well documented (Laist, 1987; Derraik, 2002), and can cause gastrointestinal blockages, ulcerations, internal perforation, malnutrition and death (Fry et al., 1987; Baird & Hooker, 2000; Mascarenhas et al., 2004; Boerger et al., 2010). Filter feeders, such as mobulids, may be repeatedly exposed to ingestion of microplastic debris mixed within their natural food source. For example, microplastic debris sampled in the North Pacic Ocean central gyre has a similar particle size distribution as zooplankton and the mass of debris can outweigh by about six times that of plankton (Moore et al., 2001). Planktivorous animals such as basking sharks Cetorhinus maximus (Gunnerus 1765) and baleen whales have been observed feeding in areas where marine debris was reported, and are at high risk of plastic ingestion (Choy & Adams, 1995; Gregory, 2009). Additionally, traces of heavy metals such as platinum, mercury and arsenic, known to be highly detrimental to human health, were found in high concentrations in tissues of mobulids off the Ghanaian coast (Essumang, 2009; 2010). Effects of these metals on mobulids are unknown. It has been suggested that mobulids have low vulnerability to climate change compared with other sharks and rays, as they do not appear to have high habitat specicity or rigidity to adaptation (Chin et al., 2010). As zooplanktivores, however, they are likely to be inuenced by the change in the abundance, phenology and distribution of their planktonic food as the global oceans warm (Hays et al., 2005). Further, the local and regional oceanographic conditions that cause seasonal zooplankton hotspots targeted by mobulids could alter under climate change (Richardson, 2008) and potentially inuence migration pathways and timing.
USING ADVANCED TECHNOLOGY TO STIMULATE MOBULID RESEARCH The mobility, vast pelagic habit and taxonomic uncertainties surrounding mobulids are major impediments to the gathering of information on the biology and ecology of this group. The collection of biological, behavioural, ecological and physiological information on these species has traditionally been limited to studies of individuals in inshore and surface waters, during the day, and to dead specimens for anatomical work. With the recent demand for more information on these species and rapid advances in technology, innovative techniques now allow researchers to examine new aspects of mobulid habitat use, seasonality, abundance and migrations, with a more comprehensive insight into their world.
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P O P U L AT I O N DY N A M I C S , H A B I TAT U S E A N D M O V E M E N T S Photographic identication
Photo-ID is a cost-effective and non-invasive approach in wide use for the longterm study of animal populations and individual behaviours. This technique is effective for individual identication of species that bear markings or scarring patterns that remain consistent through time. With the advent of inexpensive digital cameras equipped with underwater housings, this technology has become standard gear for recreational divers. With thousands of divers in the oceans at any one time, it is possible to gather information on vulnerable species such as mobulids quickly and inexpensively. Photographic research is often supported by eco-tourism operators and the dive community and thus increases environmental education and awareness (Couturier et al., 2011). Photo-ID has been used to examine various aspects of the biology and ecology of elasmobranchs (Castro & Rosa, 2005; Domeier & NasbyLycas, 2007; Bansemer & Bennett, 2008; Dudgeon et al., 2008) and recently, various aspects of M. alfredi and M. birostris. For manta rays, long-term photo-ID surveys with appropriate sampling design can allow for the estimation of local population sizes (Deakos et al., 2011; Marshall et al., 2011c), the examination of visitation patterns to specic sites (Luiz et al., 2009; Kitchen-Wheeler, 2010; OShea et al., 2010), the detection of movements between aggregation sites (Homma et al., 1999; Kashiwagi et al., 2010; Couturier et al., 2011) and population reproductive variables such as gestation period, sex ratio and male maturity (Clark, 2010; Marshall & Bennett, 2010b). Paired-laser photogrammetry is a technique that can be combined with photo-ID to provide data on the structure of a population. This technique uses photographs to indirectly make measurements of an object or, in this case, animals morphometrics. Two parallel laser pointers mounted to a camera, project two beams of light onto a targeted animal, creating a scale bar that can be used to extrapolate an estimated size of the individual (Deakos, 2010b; Rohner et al., 2011). When paired-laser photogrammetry and photo-ID are used together, they provide valuable data on the size structure of a population and could in the future enable the estimation of size at maturity (e.g. size of elasmobranch v. pregnancy or claspers development) and growth rate of a species (over multiple year surveys) (Deakos, 2010b; Marshall & Bennett, 2010b; Marshall et al., 2011c). Most photo-ID databases are limited to a particular aggregation area, and thus cannot be used to answer questions associated with the large-scale movements of Manta spp. To assess movements across ocean basins, regional or global databases are needed. A good example is the ECOCEAN global whale shark Rhincodon typus Smith 1828 database (www.whaleshark.org; Arzoumanian et al., 2005; Holmberg et al., 2009), which has >35 000 photos of 3226 individuals. A similar ECOCEAN global database for Manta spp. (www.mantamatcher.org) has just been launched. Increasing use of such databases in the future will facilitate studies of regional population size and exchange among Manta spp. aggregation sites, as has been investigated in R. typus (Brooks et al., 2010).
Acoustic telemetry
Acoustic telemetry involves the use of acoustic receivers to record the presence of an animal equipped with an acoustic transmitter within the detection range of the
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receiver. It has become an increasingly popular tool to monitor the occurrence patterns, home ranges, ne-scale movements and habitat use of various aquatic species, including elasmobranchs (Klimley et al., 1988; Heupel et al., 2004; Huveneers et al., 2006; Vaudo & Lowe, 2006). There are two main types of acoustic telemetry: (1) the passive monitoring of the occurrence of a tagged animal within an area via an automated array of acoustic receivers (Heupel et al., 2006) and (2) the active or manual tracking of movements of a tagged animal using a directional hydrophone and acoustic receiver (Cartamil et al., 2003). To date, these techniques have only been used in a few studies investigating mobulids. Passive acoustic telemetry has a great potential for investigating site delity patterns, seasonal occurrence and habitat use at particular monitored locations of mobulids (Dewar et al., 2008; Marshall, 2009; van Duinkerken, 2010). In addition, seasonal movements among sites by tagged individuals can be identied when several locations are being monitored simultaneously (Dewar et al., 2008). Active acoustic telemetry can provide information over a short period of time on the ne-scale movements of animals, including horizontal distance travelled, vertical movement in the water column and swimming speed of the tracked individual (Freund et al., 2000).
Satellite telemetry
Recent advances in the elds of wildlife tracking, remote sensing, geographic information systems and ecological modelling now allow researchers to monitor remotely the position and environmental conditions of free-ranging animals as they move undisturbed. In recent years, satellite-tracking technology has permitted observations of some previously undescribed aspects of the lives of large marine vertebrates, including predatory shes, marine birds, marine mammals and sea turtles (Weimerskirch et al., 2002; Block et al., 2011). To date, only one published study has investigated movements and behaviour of a Mobula species using satellite telemetry (Canese et al., 2011), and some preliminary results have been presented at conferences for Mobula spp. (Freund et al., 2000) and Manta spp. (Rubin et al., 2008; Jaine et al., 2011; F. R. A. Jaine, L. I. E. Couturier, S. J. Weeks, A. J. Richardson, K. A. Townsend & M. B. Bennett, unpubl. data; A. Marshall, J. Holmerg, J. M. Brunnschweiler & S. J. Pierce, unpubl. data). These studies have highlighted the potential for satellite telemetry to provide data on the migratory routes and distances travelled by individuals in a denite period of time. Satellite tags can also record information on the swimming behaviour and dive prole of tagged rays (Freund et al., 2000; et al., 2010; Canese et al., 2011; Jaine et al., 2011; F. R. A. Jaine, L. I. E. Couturier, S. J. Weeks, A. J. Richardson, K. A. Townsend & M. B. Bennett, unpubl. data).
P O P U L AT I O N S T R U C T U R E Genetics
Molecular analysis has become a standard tool to investigate populations of elasmobranchs (Heist, 2004a; Portnoy, 2010). An advantage of genetic approaches is that only a small tissue sample collected from living or deceased animals contains genomic information that can be investigated for genetic relationships at the individual, population, species and higher taxonomic levels (Heist, 2004a). Genetic methods will be used increasingly in the future to analyse population structure and
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connectivity, aiding sheries management and conservation decisions (Heist, 2004b; Ovenden et al., 2009, 2010). Although there are several population genetics studies on the Mobulidae commenced or underway (Poortvliet et al., 2011), there are currently no published studies.
Age and growth
Age and growth data are fundamental to future analyses of the sustainability of mobulid sheries and parameterization of demographic models. If the unique vertebral structure of some species precludes obtaining age and growth data from shed specimens, as preliminary observations suggest, long-term photographic sightresight studies should focus on this topic. Coupling the deployment of portable in-water measurement systems, such as camera-mounted parallel lasers (Deakos, 2010b), with studies of population ecology (Marshall et al., 2011c) to obtain growth rate and survivorship data are effective, if currently labour-intensive, means of estimating these parameters from eld observations. The lack of eld studies on Mobula spp. and the apparent lack of individually identiable features in these species mean that continuing efforts should be made to obtain vertebral structure data from shed specimens.
FEEDING ECOLOGY
Most published data on the diet of mobulids are based on stomach-content analysis and have a number of limitations. It is often difcult or unethical to obtain stomachs from animals threatened or protected in many countries. This means that often only a few stomachs are available for analysis, often from individuals washed up dead on the shore. Even in countries where they are the target of directed sheries, it can be difcult to obtain samples because of distrust in researchers. Once stomachs have been collected, their contents will only represent recent feeding, and individual prey items are often difcult to identify because of digestion, with hard body parts often all that remain. Ideally, stomach contents are needed from different periods, locations, size classes and both sexes to describe adequately the diet of a species. Fatty-acid and stable-isotope signatures are two indirect methods used to investigate the diet preference and trophic position of marine predators and have considerable potential in elucidating more light on the diet of mobulids, if correctly applied. Both methods have the advantage of only requiring a relatively small amount of tissue collected in the eld without killing the shes. Importantly, because these techniques allow the collection of samples from more individuals, they can detect potential shifts in the diet of a species and can contribute to understanding the dynamics behind animal movements (Kelly, 1999; MacNeil et al., 2005; Budge et al., 2006; Iverson, 2009).
Stable isotopes
Ratios of stable isotopes of nitrogen (15 N:14 N or 15 N) and carbon (13 C:12 C or C) in a consumers tissues are related to its assimilated food and are an index of its trophic position in the ecosystem. 15 N and, to a lesser extent, 13 C, show a predictable stepwise enrichment with each increasing trophic level (Hobson, 1999; Kelly, 1999; Dahl et al., 2003; Herman et al., 2005; Perga et al., 2006). This technique indicated that the trophic level of three mobulid species was between 34 and
13
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36 (second level consumer) (Sampson et al., 2010; Borrell et al., 2011). Values of 13 C provide information on the origin of the carbon entering the food web, whether it is from marine, freshwater or terrestrial origin (Fry & Sherr, 1984) or garnered from benthic or pelagic feeding (Dahl et al., 2003). For example, based on their known diet, the origin of 13 C values of Mobula spp. was extrapolated to be from the pelagic and epipelagic environment (Borrell et al., 2011).
Fatty acids
Diets of a number of predators have been examined using fatty-acid analysis, including species of marine mammal (Herman et al., 2005), seabird (Dahl et al., 2003) and elasmobranch (Semeniuk et al., 2007). Fatty acids are the principal constituents of most lipid molecules and degrade little when ingested. In the higher predator, fatty acids are generally assimilated intact and are mostly either used directly as an energy supply or are stored in adipose tissues (Iverson et al., 2004; Iverson, 2009). Hence, fatty-acid composition from prey will most likely directly inuence the fatty-acid composition of the stored fat of its consumer (Iverson et al., 2004; Budge et al., 2006; Iverson, 2009). Comparison of fatty-acid signatures of a range of potential prey species with its likely predators may provide dietary information beyond that revealed by gut-content analysis alone, such as shifts in diet and prey specialization. This method has not yet been applied to mobulid ray species, but could reveal new insights into possible prey specialization.
CONCLUSIONS Although the diverse Mobulidae family appears to be a successful group in their broad distribution and relative abundance, rising human pressures are a major threat to most of these species. Collectively, catch reports suggest that a large number of mobulids are being removed from the marine environment. Of particular concern is that most catch by directed sheries in many parts of the world remains unreported and unregulated. Reproductive adaptations of mobulids place these species amongst the least fecund elasmobranchs. This, combined with slow growth and an apparent low natural predation, suggests that mobulids are not likely to be able to cope with high shing mortality. Movement and aggregation studies suggest that mobulids are highly mobile and have the potential to travel large distances in relatively short periods of time. Further studies are needed to develop a more complete picture of the movements of mobulid species to evaluate the exposure to and overlap with human activities such as sheries and pollution. Knowing the location of migration routes and aggregation sites can provide useful information for their protection through the establishment of marine-protected areas (Game et al., 2009, 2010; Hobday et al., 2011). Although protected areas have typically been xed in time and space and prevented most sheries exploitation, migratory species that use particular aggregation sites could benet from protection that would restrict harmful shing practices at the time of year that mobulids visit. More work is needed to understand the reasons behind mobulid aggregations to underpin effective conservation and management models. Fundamental questions still exist regarding the taxonomy and basic species-specic biological variables such as reproduction and habitat requirements. Mobulids have
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many common biological characteristics, although many aspects of their ecology appear to be region and species-specic. Standardized techniques such as acoustic and satellite telemetry and stable-isotope and fatty-acid analyses can be applied to all species and will provide new insight into the differences in the biology of these species. Aggregations of mobulids provide opportunities for researchers to access many individuals for tagging programmes, genetic studies, intraspecic behavioural interactions and non-invasive dietary analyses. Scientic collaboration is crucial in order to generate estimates of global population status, and to standardize methodologies required for data input in ecosystem models. Implementation of sheries management is critical along with the concomitant need for management strategies capable of sustaining the Mobulidae into the future. To ensure their long-term sustainability, these slow-growing species demand greater scientic involvement in sheries and conservation management.
The authors thank P. Bassett, K. Hogg, H. Mitchell, K. Stephens and C. Bustamante for their precious help with the creation of maps and sheries information. The authors are also grateful to P. Kyne, C. Rohner, M. Mauffrey and A. Gutteridge for their useful comments and advice, to P. Nichols for his guidance on fatty acids work and to K. K. Binesh, P. McCann, C. Rose, M. Harding, G. Kodja, S. Yaha, I. Semesi, N. Michivo, C. Anderson, P. Hilton and N. Iddawi for advice and information supplied. A.D.M. and S.J.P.s work on this review was supported by Save Our Seas Foundation, one anonymous donor, Ocean Revolution and Casa Barry Lodge, Mozambique. Support for this work which includes Project Manta, a research programme based at the University of Queensland, was provided by ARC Linkage Grant (LP110100712), ARC Future Fellowship (FT099172), Sea World Research and Rescue Foundation Inc., EarthWatch Australia, Brother Pty Ltd, Lady Elliot Island Eco-Resort, Manta Lodge and Scuba Centre, Project AWARE.
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Journal of Fish Biology (2012) 80, 10751119 doi:10.1111/j.1095-8649.2012.03264.x, available online at wileyonlinelibrary.

Biology, ecology and conservation of the Mobulidae

Key words: by-catch; distribution; elasmobranch; sheries; Manta; Mobula.

Author to whom correspondence should be addressed. Tel.: +61733467975; email: l.couturier@uq.edu.au

Number of published studies Number of published studies 10 11 12 10 20 30 40 50 60 70 80 90 9 0 0 2 4 6 8 8

Number of published studies (year1)

Fig. 1. Figure legend on next page.

Common name IUCN Status (year assessed)

Number of pups (WD at birth, mm)

Maximum movement recorded Unknown

Population size Population trend

Omani waters (Henderson & Reeve, 2011)

Unknown Possibly increasing (Bizzarro et al., 2008) Unknown

Shark bather nets (Young, 2001)

Longline, nets (Bizzarro et al., 2008)

Common name IUCN Status (year assessed) Habitat

Gestation Longevity (years) Age at maturity Maximum WD (mm)

WD at maturity (mm) (M, male; F, female)

Table I. Continued Mobula kuhlii Mobula mobular

Number of pups (WD at birth, mm) Diet Unknown Unknown

1 (310) (Compagno & Last, 1999) Unknown

Maximum movement recorded Known aggregations

Uncommon (Compagno & Last, 1999)

Population trend Fisheries

Common name IUCN Status (year assessed) Habitat

Maximum movement recorded Known aggregations

Population size Population trend Fisheries

By-catch Conservation actions Mobula tarapacana

Common name IUCN Status (year assessed) Habitat

Gestation Longevity (years)

Maximum movement recorded Known aggregations

Population size Population trend Fisheries

Common name IUCN Status (year assessed)

Table I. Continued Manta alfredi Manta birostris

Age at maturity (years) Maximum WD (mm)

Maximum movement recorded (km) Known aggregations

Manta protected zones in the Maldives, Yap and Hawaii

Fig. 2. Figure legend on next page.

P O P U L AT I O N DY N A M I C S , H A B I TAT U S E A N D M O V E M E N T S Photographic identication

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