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Rev Biol (2011) 21:205–223 DOI 10.1007/s11160-010-9167-5

REVIEWS

The importance of and pipefishes in the diet of marine

D. Kleiber • L. K. Blight • I. R. Caldwell • A. C. J. Vincent

Received: 29 September 2009 / Accepted: 12 May 2010 / Published online: 1 June 2010 Ó Springer Science+Business Media B.V. 2010

Abstract A review of 135 accounts of on predators: these included taxa that do not frequent the seahorses and pipefishes identified 82 predator spe- demersal generally occupied by seahorses and cies, with nine of seahorses and 25 of pipefishes. Thus, seahorses and pipefishes may be pipefishes recorded as prey. These cryptic fishes moving in the open more than suspected, were generally depredated in low numbers. Where perhaps using floating mats of marine vegetation. If syngnathids formed a high proportion of predator so, this behaviour could act as a hitherto unknown diets, predation occurred on (1) a single abundant vector for syngnathid movement and dispersal. species during a population boom or large die-off, (2) Information on syngnathid abundance in predator concentrations of individuals utilising floating marine diet (measured as percent number, volume, or mass) vegetation, or (3) juveniles when abundant during the was available in 45 reviewed accounts; in 27% breeding season. Predation coinciding with high (n = 12) of these studies seahorses or pipefishes syngnathid densities suggests their predators are comprised C20% of predator diet (range 0.005– foraging opportunistically rather than targeting syng- 100%). Frequency of occurrence (percent stomachs, nathids as prey. Invertebrates, fishes, turtles, bill-loads, or regurgitations in which a prey waterbirds and marine mammals were all syngnathid item occurred) was provided in 39 accounts, with 15% (n = 6) of these recording a frequency of C20% (range 0.003–65%). D. Kleiber and L. K. Blight contributed equally to this work. Keywords Marine food webs Á Electronic supplementary material The online version of Predator–prey interactions Á Á this article (doi:10.1007/s11160-010-9167-5) contains Hippocampus Á Crypsis Á Dispersal supplementary material, which is available to authorized users.

D. Kleiber Á L. K. Blight Á I. R. Caldwell Á A. C. J. Vincent Introduction Project , Fisheries Centre, The University of British Columbia, 2202 Main Mall, Vancouver, BC V6T 1Z4, Canada Predation risk can shape individual behaviour and ecology as well as population level processes. L. K. Blight (&) According to the ‘‘life-dinner’’ principle (Dawkins Centre for Applied Conservation Research, and Krebs 1979), in the arms race between predator The University of British Columbia, 2424 Main Mall, Vancouver, BC V6T 1Z4, Canada and prey, adaptive pressure should be greater on the e-mail: [email protected] prey than on the predator. In marine ecosystems, 123 206 Rev Fish Biol Fisheries (2011) 21:205–223 predation pressure can affect: where individuals are corals, or ) and can change their colour to found (Walters and Martell 2004); select for predator adapt to changes in their environment. Species of avoidance behaviours such as schooling (Seghers seahorses, pipehorses, and seadragons that live 1974; Magurran 1990; Pitcher and Parrish 1993)or among seagrass or other flora often have filaments refuge use (Sih 1997; Krause et al. 2000); create that increase their resemblance to their habitat, while trade-offs with other behaviours such as mating those living amongst coral often have a textured body (Berglund 1993; Sih 1994) or feeding (Krause et al. surface. Although some species of pipefishes lack 2000; Plath and Schlupp 2008); and select for filaments, these nonetheless have an elongated body attributes to either evade detection (e.g., crypsis) or that allows them to mimic vertical features of the make prey less palatable or otherwise less attractive environments in which they live such as blades of (Endler 1986; Smith 1997). Knowing the predation seagrass, loose weeds, or sticks (Kuiter 2000, 2009). risk faced by a given species can help to elucidate the Overall, predator avoidance through crypsis is highly pressures that have shaped its behaviour, morphol- evolved in this family of fishes. ogy, and general biology. Although effective, crypsis is an imperfect defence The Syngnathidae (seahorses, pipefishes, pipehors- strategy and predation of cryptic species does occur. es and seadragons) are a cosmopolitan family of In the predator–prey arms race, predators may charismatic fishes that serve as flagship species for develop more effective search images (Gendron marine conservation, yet little is known about their 1986) or search rates (Guilford and Dawkins 1987) basic biology. Syngnathids are harvested in a global to find cryptic prey. Crypsis can also become less trade for use in traditional medicines and curios effective when shifts in habitat no longer favour a (Foster and Vincent 2004). The extent of syngnathid certain phenotype (e.g., changed frequency of dark vs. exploitation by is well documented, but little light substrates; Mallet 2004), or when there is a trade- is known about their ecological role and the forces off between predator avoidance and other life history that structure their populations (Martin-Smith and requirements (e.g., mating, feeding; Sih 1994; Walters Vincent 2005). Two syngnathid species are listed on and Martell 2004). For example, work by Berglund the International Union for the Conservation of (1993) on the mating behaviour of the pipefish Nature (IUCN) Red List as ‘‘Endangered’’, seven as typhle during the presence of a predator ‘‘Vulnerable’’, and two as ‘‘Near Threatened’’. How- suggests that adults may be at high risk of predation ever, the vast majority are assessed as ‘‘Data Defi- during mating. Conversely, remaining cryptic may cient’’, indicating the practical need for further restrict an ’s access to other resources. Sea- information about these species. The purposes of this horses and pipefishes use rapid (from dark to light review were to find out which predators eat this within seconds, and vice versa) colour change to cryptic group of fishes, and under which circum- attract mates yet at least some species limit such stances; to identify in more detail the role of displays when exposed to predation risk (Fuller and syngnathids in marine food webs; and to attempt to Berglund 1996). Seahorses have a prehensile tail, elucidate poorly known syngnathid life history traits allowing them to grasp vegetation and remain related to movement and behaviour. stationary; by limiting their movement and staying All Syngnathidae have physical characteristics that within small home ranges (Foster and Vincent 2004; allow them to hide from predators. Avoiding preda- Vincent et al. 2005), seahorses can ensure they remain tion by blending with surroundings is a well-studied camouflaged. However, with a simple grasping tail or strategy used by a wide range of organisms (e.g., an otherwise reduced caudal fin, seahorses, pipehors- Endler 1986). Such crypsis comes in two main forms: es, and seadragons primarily use their dorsal fin for (1) disguise (blending with the background) and (2) thrust and may be weaker swimmers than other fish. masquerade (the imitation of another object; Ruxton Thus, if they are caught outside their normal habitat or et al. 2004). Syngnathids are notable marine exam- their camouflage fails they are presumably vulnerable ples of cryptic fauna that rely on both colouration and to more rapidly-swimming predators. Developing an form to blend with their habitat (Foster and Vincent understanding of the circumstances under which 2004; Kuiter 2000, 2009). Most syngnathids are crypsis fails, then, may provide an indirect window coloured to blend into their marine (seagrass, on little-studied aspects of syngnathid life history. 123 Rev Fish Biol Fisheries (2011) 21:205–223 207

The role of syngnathids as potential prey has been Emphasis was placed on identifying measures of highlighted by a recent and dramatic population relative abundance of syngnathids in the diet. We increase in snake pipefish Entelurus aequoreus that made several ‘‘rationalized’’ assumptions to convert has occurred in the northeast Atlantic and qualitative terms where possible into quantitative since 2003 (Kirby et al. 2006; Harris et al. 2007a; metrics for comparative purposes. Specifically, Kloppmann and Ulleweit 2007). For example, Con- descriptions of stomachs being ‘‘full’’ and tinuous Recorder data from the NE Atlantic ‘‘crammed’’ with syngnathids were considered to showed more juvenile and larval E. aequoreus in the represent 100% occurrence by volume, first half of 2005 than in the entire period from 1958 while terms such as ‘‘numerous’’ and ‘‘on many to 1972 (Kirby et al. 2006). Though the E. aequoreus occasions’’ were taken to be 30% occurrence. This population increases have been linked to anomalous deliberately conservative latter estimation was used sea surface temperatures (Kirby et al. 2006), eruptive so as not to overinflate subjective descriptions. In two population events may be a general feature of instances, percent volume was estimated from pho- syngnathid population biology. There have been tographs of stomach contents included in these similar observations of dramatically increased inci- papers. As frequency of occurrence (FOO; percent dence of pipefishes as prey off the California coast of total stomachs—or, for marine , of regurgi- (Connell 2007; Horn et al. 2009), of sudden increases tations or bill-loads—containing a given prey item) in numbers of big-bellied seahorses Hippocampus overemphasises the importance of items occurring at abdominalis off (K. Martin-Smith, in litt.), low frequency in the diet of a population of animals and of increases in unidentified seahorses in New (Cullen et al. 1992), studies reporting FOO (or those Zealand waters (Seahorse2000 2007). Such periods of where FOO was inferred using the qualitative terms hyper-abundance could be expected to increase above) were compared separately to those providing encounter rates by predators of prey species that are percent abundance by mass, volume or total number usually protected from predation via cryptic mor- of prey items consumed. Though the use of percent phology and behaviour. number as a metric also has the potential to overem- phasise items occurring at low frequencies—e.g., if several small syngnathids were consumed with one Methods large prey item—this was not the case in the reviewed studies, where documented prey items were We conducted a search of peer-reviewed and other of similar sizes in the few studies presenting percent literature for records of predation on syngnathids. number. Thus, we combined the three measures of These included diet-related studies of , percent abundance in our descriptions. The data from marine mammals, reptiles, fishes, and , studies that provided both FOO and percent mass/ and observations of foraging or chick-feeding by volume were only used in the comparisons of the seabirds. We used materials recorded in ISI Web of latter category. Science and additional sources referenced in publi- All seahorse species were classified according to cations (in five languages) found therein, the online Lourie et al. (2004), and all pipefish species accord- databases FishBase (Froese and Pauly 2009) and ing to Kuiter (2009). CephBase (Wood and Day 2006), and such museum records as were identified in the literature search. We also consulted internationally via electronic expert Results mailing lists. Our goal was to obtain the broadest possible overview of predators of the Syngnathidae, With the inclusion of one unpublished account by this and we included studies that provided qualitative data paper’s authors, we identified 135 reports of preda- or which used only limited analyses, as well as tion on syngnathids by at least 82 predator species findings in unpublished and non-reviewed publica- from a range of taxa (Table 1). Four species of tions, referred to as grey literature. We achieved a marine invertebrates (cephalopods, arthropods, and comprehensive, although not exhaustive, account of cnidarians), 47 species of fishes (5 elasmobranchs, 42 available information. ), two marine turtles, 26 waterbirds, and three 123 208 Rev Fish Biol Fisheries (2011) 21:205–223

Table 1 Predators of the syngnathidae Predator Prey syngnathida Maximum % preyb Locationc References FOO % (n) % (v) % (m)

Mollusca Cephalapoda Common Octopus vulgaris Hippocampus Ria Formosa, PT Caldwell, unpubl. data guttulatus Cuttlefish Sepia officinalis Syngnathid sp. 1.5 1.3 Ria de Vigo, ES Castro and Guerra (1990) Syngnathus sp. 1.0 0.9 Syngnathus typhle 0.3 0.2 Syngnathus sp. 0.01 Morbihan Bay, FR Blanc et al. (1998) Syngnathus sp. 8.0 Atlantic, FR Pinczon du Sel et al. (2000) Arthropoda Malacostraca sp. Pipefish sp. Gullmarsfjord, 58 Vincent et al. (1995) 15N1128E,SEd Cnidaria Anthozoa Sea anemone sp. S. typhle Gullmarsfjord, 58 Vincent et al. (1995) 15N1128E,SE Chordata sp. Hippocampus sp. AU Whitley and Allan (1958) Skate sp. Hippocampus sp. NZ Whitley and Allan (1958) Horn shark Heterodontus S. auliscus 1.1 0.7 0.2 Laguna San Ignacio, Segura-Zarzosa francisci MX et al. (1997) Mako shark Isurus oxyrinchus H. erectus 0.2 0.1 \0.1 N.W. Atlantic Stillwell and Kohler (1982) Blue shark Prionace glauca S. californiensis 0.7 \0.1 0.9 Monterey Bay, CA, US Harvey (1989) Pelagic Pteroplatytrygon Hippocampus sp. 25.0 N.W. Atlantic, 38 35 N Bigelow and (Dasyatis) violacea 68 14 W Schroeder (1962) Hippocampus sp. Atlantic Wilson and Beckett (1970) Thornback ray Raja clavata Hippocampus sp. 0.48 0.44 S.E. , TR Saglam and Bascinar (2008) Syngnathus sp. 0.12 0.45

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Table 1 continued Predator Prey syngnathida Maximum % preyb Locationc References FOO % (n) % (v) % (m)

Osteichthyes Bullhead sp. Cottidae S. typhle Scandinavia Fries et al. (1895) Black porgy Acanthopagrus S. acus Tolo Harbour, HK Wu (1984) schlegeli Yellow-eyed Aldrichetta forsteri nigra Western Port, AU Edgar and Shaw (1995) Lancetfish Alepisaurus sp. H. erectus N.W. Atlantic, 40 US National Museum 27N6615W (USNM) Cat. No. 223085 (1957) Caspian marine shad S. abaster S.E. Caspian Sea Vetchanin (1984) braschnikowi Striped anglerfish Antennarius H. abdominalis AU Kuiter (2000) striatus H. breviceps Slender-spined catfish Arius platypogon S. californiensis 5.38 1.02 0.79 San Ignacio , MX Cruz et al. (2000) Eastern Australian trutta 34.5 Western Port, AU Robertson (1982) carinirostris Western Australian salmon A. truttacea S. nigra Western Port, AU Edgar and Shaw (1995) Syngnathid sp. Port Phillip Bay, AU Hindell et al. (2000a) Syngnathid sp. 5.0 Port Phillip Bay, AU Hindell et al. (2000b) Syngnathid sp. 0.1 Port Phillip Bay, AU Hindell et al. (2002) S. argus 7.2 Port Phillip Bay, AU Hindell (2006) Trevally sp. H. kuda Honolulu, HI, US Academy of Natural Sciences Philadelphia (ANSP) Cat. No. 87726 (1917) Bar jack C. ruber Syngnathus sp. Gulf of Batabano, CU Popova and S’erra (1983) brachycephalus Black seabass Centropristis Hippocampus sp. 0.3 N.W. Atlantic Bowman et al. (2000) striata S. fuscus 0.5 Chelidonichthys S. acus 1.11 0.18 1.19 Cape Coast, ZA Meyer and Smale (1991) capensis

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Table 1 continued Predator Prey syngnathida Maximum % preyb Locationc References FOO % (n) % (v) % (m)

Tub gurnard C. lucernus S. abaster 0.04 \0.01 \0.01 Tagus , PT Costa (1988) Dolphinfish H. fisheri HI, USA USNM Cat. No. 126534 hippurus (1901) H. erectus 0.02 Atlantic Gibbs and Collette (1959) S. phlegon 1.3 0.59 , Massutı´ et al. (1998) Majorca Hippocampus sp. 75.0 Unspecified Sharpe (1998) Crested weedfish Cristiceps Syngnathid sp. Port Phillip Bay, AU Hindell et al. (2000a) australis European sea bass Dicentrarchus S. abaster 0.29 9.15 0.46 Tagus Estuary, PT Costa (1988) labrax Spottail porgy Diplodus Hippocampus sp. ZA Whitley and Allan (1958) holbrookii Honeycomb rockcod Epinephelus 0.01 Pacific Ocean, Society Randall and Brock (1960) merra flavofasciatus Kawakawa Euthynnus grayi Basilan , Sulu Herald (1949) affinis Archipelago Eutrigla S. typhle Unspecified de Gee and Kikkert (1993) gurnardus Entelurus aequoreus 100 N.E. Atlantic Harris et al. (2007a) morhua S. typhle Scandinavia Fries et al. (1895) S. typhle W. Sweden Berglund (1993) E. aequoreus 100 North Sea van Damme and Couperus (2008) Ling Genypterus Hippocampus sp. NZ Whitley and Allan (1958) blacodes Blue rock whiting Haletta U. carinirostris Western Port, AU Edgar and Shaw (1995) semifasciata phillipi Sea-perch Helicolenus Hippocampus sp. NZ Whitley and Allan (1958) sp. Skipjack Katsuwonus H. kuda Kaena Point, HI, US ANSP Cat. No. 79700 pelamis (No date)

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Table 1 continued Predator Prey syngnathida Maximum % preyb Locationc References FOO % (n) % (v) % (m)

Striped trumpeter lineata Hippocampus sp. NZ Whitley and Allan (1958) Melanogrammus E. aequoreus 100 N.E. Atlantic Harris et al. (2007a) aeglefinus Striped bass Morone saxatilis S. fuscus 0.4 Hudson River Estuary, Dew (1988) NY, US toadfish Opsanus tau S. fuscus NJ, US Roelke and Sogard (1993) Blue cod colias Hippocampus sp. NZ Whitley and Allan (1958) Chilean chilensis 0.4 0.2 0.1 Talcahuano, CL, Gonza´lez and Oyarzu´n blainvilleanus 36 41 S 73 06 W (2003) Flathead Platycephalus sp. H. breviceps AU Kuiter (2000) Bartail flathead P. indicus S. acus Tolo Harbour, HK Wu (1984) Grassy flathead P. laevigatus Pipefish sp. Corner Inlet, AU Klumpp and Nichols (1983) Western Port, AU Edgar and Shaw semistriatus (1995) U. carinirostris V. phillipi King flathead P. speculator U. carinirostris 0.3 \0.1 \0.1 Wilson Inlet, AU, Humphries et al. 117 25 E 34 50 S (1992) Pollack E. aequoreus 100 Scandinavia Fries et al. (1895) Bluefish Pomatomus saltatrix H. erectus 0.6 0.2 W. Atlantic Buckel et al. (1999) S. fuscus 1.9 0.6 Red cod Pseudophycis bachus Hippocampus sp. NZ Whitley and Allan (1958) Pikeperch Sander lucioperca S. abaster 3.2 5.2 N. Caspian Sea Stolyarov (1985) Atlantic scombrus E. aequoreus W. IE, 51 23 N van Damme and 11 27 W Couperus (2008)

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Table 1 continued Predator Prey syngnathida Maximum % preyb Locationc References FOO % (n) % (v) % (m)

Sheatfish Silurus glanis S. abaster 3.9 2.8 N. Caspian Sea Stolyarov (1985) Tuna Thunnus sp. Hippocampus sp. N.W. Atlantic, 38 USNM unregistered 39N6570W (No date) H. erectus NJ, US, 39 17 N 71 USNM Cat. No. 49 W 223090 (No date) H. kuda Honolulu, HI, US ANSP Cat. No. 89313 (1924) Yellowfin tuna T. albacares Hippocampus sp. N.W. Hawaiian Islands, US Herald (1949) H. erectus N.W. Atlantic, 35 USNM Cat. No. 00N7000W 223083, (1960) Hippocampus sp. 1.9 E. Pacific Alverson (1963) Hippocampus sp. 5.9 Gulf of Guinea Sund and Richards (1967) 10.0 Indian Ocean Kornilova (1980) bicoarctatus Atlantic bluefin tuna T. thynnus Syngnathid sp. 2.0 Atlantic Gulf Stream Matthews et al. (1977) Hippocampus sp. 6.0 H. erectus 5.0 S. phlegon Ligurian Sea Orsi Relini et al. (1999) Reptilia Loggerhead sea turtle Caretta E. aequoreus 30.0 Azores region Pouchet and de caretta Guerne (1940) Hippocampus sp. 50.0 Nova Scotia, CA Bleakney (1967) H. erectus 70.0 W. Atlantic Burke et al. (1993) H. hippocampus 0.02 W. Mediterranean Tomas et al. (2001) Kemp’s ridley sea turtle Lepidochelys H. erectus 20.0 W. Atlantic Burke et al. (1993) kempii Aves Razorbill Alca torda Pipefish sp. St Kilda Island, UK Money (2005) E. aequoreus 2.6 Fair Isle, UK Shaw et al. (2005) Heron sp. Ardeidae S. argus Western Port, AU 38 Howard and Koehn 28 S 145 18 E (1985) Little blue heron Egretta Syngnathus sp. 2.7 0.7 Tampa Bay, FL, US Kent (1986) caerulea Snowy egret E. thula Syngnathus sp. 1.1 0.4 Tampa Bay, FL, US Kent (1986) 123 Rev Fish Biol Fisheries (2011) 21:205–223 213

Table 1 continued Predator Prey syngnathida Maximum % preyb Locationc References FOO % (n) % (v) % (m)

Tricolored heron E. tricolor Syngnathus sp. 5.2 0.4 Tampa Bay, FL, US Kent (1986) Fairy Eudyptula minor Hippocampus sp. 0.006 Phillip Island, AU Montague and Cullen (1988) Syngnathid sp. 0.003 H. abdominalis 2.0 Tasmania, AU Gales and Pemberton (1990) Pipefish sp. 0.6 H. breviceps 7.0 Phillip and Rabbit Cullen et al. (1992) Islands, AU H. whitei H. abdominalis Syngnathus sp. 3.0 H. abdominalis AU Kuiter (2000) H. breviceps Hippocampus sp. 10.0 Phillip Island, AU Chiaradia et al. (2003) L. norae \1 Oamaru, NZ Fraser and Lalas (2004) Pipefish sp. Atlantic puffin Fratercula arctica Pipefish sp. St Kilda Island, UK Money (2005) Northern fulmar Fulmarus glacialis E. aequoreus Rockall Trough, N.E. Wakefield (2005) Atlantic Common loon Gavia immer Syngnathus sp. North America Mcintyre and Barr (1997) Mew gull Larus canus S. rostellatus 30.0 Castricum, N. NL Reijnders and Keijl (1997) Lesser black-backed gull L. fuscus E. aequoreus Rockall Trough, N.E. Wakefield (2005) Atlantic Great black-backed gull L. marinus E. aequoreus N.E. Atlantic Harris et al. (2007b) Black-headed gull L. ridibundus E. aequoreus Rockall Trough, N.E. Wakefield (2005) Atlantic Northern gannet Morus bassanus E. aequoreus Rockall Trough, N.E. Wakefield (2005) Atlantic E. aequoreus N.E. Atlantic Harris et al. (2007b)

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Table 1 continued Predator Prey syngnathida Maximum % preyb Locationc References FOO % (n) % (v) % (m)

Yellow-crowned night heron Nyctanassa violacea Syngnathus sp. 0.005 NY & NJ, US Riegner (1982) Bridled Onychoprion Pipefish sp. 0.02 NC, USA Haney et al. (1999) anaethetus European shag Phalacrocorax aristotelis S. acus 1.1 S.W. Scotland, UK Lumsden and Haddow (1946) E. aequoreus 9.0 Isle of May, UK Harris et al. (2007b) Greater shearwater Puffinus gravis E. aequoreus Rockall Trough, Wakefield (2005) N.E. Atlantic Black-legged kittiwake Rissa tridactyla S. rostellatus 0.6 Helgoland, North Vauk and Jokele (1975) Sea, DE Syngnathus sp. 1.3 Pipefish sp. St Kilda Island, UK Money (2005) E. aequoreus Isle of May, UK Newell (2006) E. aequoreus N.E. Atlantic Kloppmann et al. (2007) E. aequoreus 46.0 Isle of May, UK Harris et al. (2007b) Black skimmer Rynchops niger S. folleti 5.3 2.9 Punta Rasa, AR Favero et al. (2001) Common eider Somateria E. aequoreus N.E. Atlantic Harris et al. (2007b) mollissima Tern sp. Sternidae H. trimaculatus Ashmore Reef, AU Northern Territory Museum (NTM) Cat. No. S. 12060-001 (No date) Roseate tern Sterna dougallii Pipefish sp. Falkner Island, CN, Richards and Schew (1989) US Arctic tern S. paradisaea Syngnathus sp. 3.4 Wadden Sea Frick and Becker (1995) Syngnathus sp. New England, US Hatch (2002) Pipefish sp. Røst, NO Anker-Nilssen and Aarvak (2006) Common tern S. hirundo S. fuscus Island, MA, US, Nisbet (1983) 41 40 N 70 43 W S. rostellatus 1.5 North Sea Becker et al. (1987) S. fuscus 10.0 Cedar Beach, NY, US Safina et al. (1990) Syngnathus sp. 11.9 Wadden Sea Frick and Becker (1995) S. rostellatus NL Frieswijk (1999)

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Table 1 continued Predator Prey syngnathida Maximum % preyb Locationc References FOO % (n) % (v) % (m)

Elegant tern Thalasseus S. auliscus 41.0 S. CA, US Connell (2007) elegans S. californiensis S. exilis S. leptorhynchus C. arctus Pipefish sp. 65.0 S. CA, US Horn et al. (2009) Sandwich tern T. sandvicensis Syngnathus sp. Wadden Sea Stienen et al. (2000) Common murre Uria aalge S. rostellatus North Sea Ouwehand et al. (2004) Pipefish sp. St Kilda Island, UK Money (2005) Pipefish sp. 1.5 Fair Isle, UK Shaw et al. (2005) Pipefish sp. 48.0 39.0 Helgoland, Sonntag and Hu¨ppop (2005) North Sea, DE Mammalia Common Delphinus E. aequoreus 100 S.W. IE, 49 van Damme and Couperus delphis 23 N 1117 W (2008) Black Sea dolphin D. delphis S. schmidti Black Sea Gordina et al. (1991) ponticus European otter Lutra lutra Pipefish sp. 3.3 Aran Islands, IE Kingston et al. (1999) a Full names of syngnathids are found in Table 2. b Quantities of syngnathids given in frequency of occurrence (FOO), percent number (n), volume (v), and mass (m); italicized numbers are estimates. c Country abbreviations follow the International Organization for Standardization 3166 alpha-2 standards, and US State abbreviations follow the US postal service codes. d Locations provided in Table 1 reflect the level of detail given in individual studies (see References) marine mammals were represented (Table 1; Fig. 1). colonies, from necropsies of salvaged birds and Ninety-five percent of the predator species were museum fish specimens, and from stomach content and of those 51% were fishes, studies. There was great variety in reported detail, followed by waterbirds (waders and seabirds; 32%; with some studies providing FOO, others providing Fig. 1). Unpublished expert communications yielded percent stomach contents by mass, volume or total one additional species of syngnathid (Bargibant’s number of prey items and others simply supplying a seahorse ), and ten new list of ingested prey. Some accounts identified prey predators (see Supporting Online Material), but these items to species, while others specified syngnathid are not further discussed here. Nor did we pursue prey only to type (‘‘seahorse’’ or ‘‘pipefish’’). Despite anecdotes of (Sternidae) using pipefishes as these limitations, at least 34 syngnathids (nine species non-comestible courtship display items. of seahorses and 25 of pipefishes) were documented In published studies, syngnathid predation was as prey (Table 2). No accounts were found describing identified from direct observations of predation predation of pipehorses or seadragons. As stomach events in diet or other studies, from observations of content studies often identify prey remains to a foraging adult seabirds and of chick feedings (regur- general category (e.g., ‘‘fish’’), this number is gitations or bill-load deliveries of whole fish) at their undoubtedly a low estimate of the diversity of 123 216 Rev Fish Biol Fisheries (2011) 21:205–223

Fig. 1 Frequency of syngnathid predators by taxonomic grouping syngnathids consumed as prey. All of the depredated cases, however, it was suggested qualitatively that the species of syngnathids are described as being demer- prey syngnathid was consumed frequently overall. sal except for Schmidt’s pipefish S. schmidti, which is For example the great pipefish S. acus was considered pelagic (Froese and Pauly 2009). However, some of ‘‘common’’ prey of black porgy Acanthopagrus these species have been found in association with schlegeli (Wu 1984), and S. schmidti ‘‘is a mainstay floating in pelagic waters, and E. aequoreus in the diet of the Black Sea dolphin [Delphinus is suspected of having both pelagic and demersal delphis ponticus] in the summer and fall’’ (Gordina tendencies (van Damme and Couperus 2008). Among et al. 1991). the predators, nine species of fish and 14 species of Accounts of predation on E. aequoreus predomi- seabird (28% of all identified predators, and 54% of nated. Of the 82 species identified as syngnathid all identified birds) were surface feeders and/or predators, the syngnathid prey of 13% of these pelagic in habit. (n = 11) was exclusively E. aequoreus during Fractional abundance (percent mass, volume or unusually large peaks in that species’ populations number) of syngnathids in the diet was provided in 39 (e.g., Pouchet and de Guerne 1940; Harris et al. accounts and estimated in 6 accounts (range 0.005– 2007a). Similarly, of the 100 accounts where syng- 100%), and FOO was measured in 38 accounts and nathid prey was identified to species, 20% (n = 20) estimated in one account (range 0.003–65%; were accounts of predation on E. aequoreus. For the Table 1). Of the studies reporting fractional abun- avian predators, the proportion of accounts recording dance, 27% (n = 12) reported that syngnathids E. aequoreus as prey was 26% (13 of 50 studies). comprised C20% of a predator’s diet, and syngnath- Moreover, in 7 of the 18 studies where syngnathids ids were found in C20% of sampled individuals in comprised C20% of the diet, E. aequoreus was the 15% (n = 6) of studies providing FOO. prey species. Half of all studies encountered (n = 68) included no measure or indication of relative abundance. Some of these described an observation of a predation Discussion event, and others provided observations of a single stomach sample. Many authors of these latter studies The apparently opportunistic nature of syngnathid reported only that a low number of syngnathid predation events suggests that the predator avoidance specimens was found in predator stomachs, or that strategies of these cryptic and bony fish may be syngnathids were observed as regurgitations or effective. Researchers used a variety of metrics to deliveries by avian predators to their young. In some describe amount of prey items in a predator’s diet,

123 Rev Fish Biol Fisheries (2011) 21:205–223 217

Table 2 Syngnathid Syngnathid species Number of species documented as prey times identified

Seahorsesa Big-belly seahorse Hippocampus abdominalis 4 Short-headed seahorse Hippocampus breviceps 4 Hippocampus erectus 9 Fisher’s seahorse Hippocampus fisheri 1 Large-snouted seahorse Hippocampus guttulatus 1 Short-snouted seahorse Hippocampus hippocampus 1 Yellow seahorse 3 Three-spot seahorse Hippocampus trimaculatus 1 White’s seahorse Hippocampus whitei 1 Pipefishesb Yellow-banded pipefish Corythoichthys flavofasciatus 1 Snub-nose pipefish 1 American crested pipefish Cosmocampus brachycephalus 1 Snake pipefish Entelurus aequoreus 20 Mud pipefish 1 American deep-bodied pipefish Leptonotus blainvilleanus 1 long-snout pipefish Leptonotus norae 1 Half-banded pipefish Mitotichthys semistriatus 1 Spotted pipefish 2 Wide-bodied pipefish 2 Europe’s short-snout pipefish Syngnathus abaster 5 Great pipefish Syngnathus acus 4 Barred pipefish Syngnathus auliscus 2 pipefish Syngnathus californiensis 3 Barcheek pipefish Syngnathus exilis 1 Follett’s pipefish Syngnathus folletti 1 Dusky pipefish Syngnathus fuscus 6 Bay pipefish Syngnathus leptorhynchus 1 Spiked pipefish Syngnathus phlegon 2 Lesser pipefish Syngnathus rostellatus 5 Schmidt’s pipefish Syngnathus schmidti 1 Deep-snouted pipefish Syngnathus typhle 6 a Common names from Bend stick pipefish Trachyrhamphus bicoarctatus 1 Lourie et al. (2004) Hairy pipefish 4 b Common names from Port Phillip pipefish 2 Kuiter (2009)

making inter-study comparisons problematic. None- place of scales, all syngnathids have a layer of theless, the information presented here suggests that stretched over a series of bony plates (i.e., scutes), predation of seahorses and pipefishes is generally rare which makes these fishes difficult to swallow and in time and/or space. As well as being cryptic, digest (Harris et al. 2007b; Kloppmann et al. 2007). syngnathids have a set of morphological adaptations In certain species that were found as prey, such as to deter predation: bony scutes and spines. In the H. guttulatus and H. breviceps, the edges of some

123 218 Rev Fish Biol Fisheries (2011) 21:205–223 scutes are even elongated into spines (Lourie et al. were some surprising exceptions. Syngnathids are 2004). When crypsis fails, the low breakability, generally found in shallow, coastal areas where they digestibility and caloric value of these fishes (Harris can blend in with the seagrass, mangroves, or coral et al. 2007b; Kloppmann et al. 2007) may addition- habitats their cryptic morphology mimics (Kuiter ally encourage predators to reject seahorses and 2000, 2009). All the syngnathids identified here as pipefishes in favour of more palatable alternatives. prey are demersal except for the pelagic S. schmidti Predation thus may not be a primary factor driving (Froese and Pauly 2009). The majority of the ocean- the population dynamics of syngnathids. dwelling (i.e., non-avian) syngnathid predators doc- The number of instances where predation coin- umented in this review are either demersal, bentho- cides with high densities of syngnathids suggests that pelagic, or neritic-pelagic, with foraging ranges that many of their predators are opportunistic feeders likely include the demersal zone. However, nine acting on an abundant food source, rather than identified predators were either pelagic or bathype- specialized syngnathid predators. In general, high lagic and would not normally be found near the levels of predation occurred when predators con- where syngnathids are known to occur sumed a single species of syngnathid during a (Froese and Pauly 2009): blue shark Prionace population explosion (e.g., Harris et al. 2007a), glauca, mako shark Isurus oxyrinchus, pelagic during a large die off (Pouchet and de Guerne stingray Pteroplatytrygon (Dasyatis) violacea, blue- 1940), when they were found in high numbers fish Pomatomus saltatrix, Caspian marine shad floating in drifting marine vegetation (Sharpe 1998), Alosa braschnikowi, pikeperch Sander lucioperca, or when juveniles were numerous during the breeding Katsuwonus pelamis, yellowfin tuna season (Cullen et al. 1992; Blanc et al. 1998). Hairy Neothunnus macropterus, and lancetfish Alepisaurus pipefish Urocampus carinirostris, which is naturally sp. abundant in Australian seagrass habitat (Martin- Predation by such pelagic fishes suggests that Smith 2008), comprised 34.5% of the diet of Eastern syngnathids may be found in the open ocean more Australian salmon (Robertson 1982). regularly than previously thought. In one account of This suggests that crypsis is not necessarily effective predation by P. violacea, stomach contents included when prey populations reach a certain density both seahorses and weed Sargassum sp. (Kendrick and Hyndes 2003). Generally, however, (Wilson and Beckett 1970). While predators may syngnathids are thought to occur at low densities have ingested sargassum-associated prey in a demer- (Foster and Vincent 2004), which may in part account sal zone, it seems more likely that the seahorses were for being a minor component of most reported diets. attached to floating sargassum in pelagic waters: such Even when syngnathids are not abundant, they rafting of seahorses and pipefishes associated with may still be eaten by generalist predators. Most of the floating plant material has been reported in the predators identified here are considered to be oppor- and North Sea (Sharpe 1998; tunistic and/or generalist feeders, suggesting that Vandendriessche et al. 2007). Stomach contents of syngnathids were not specifically targeted as prey. dolphinfish Coryphaena hippurus found to be feeding Certainly, most piscivorous fishes occurring in shal- on seahorses have also included sargassum (Sharpe low seagrass habitat, where syngnathids are com- 1998), and C. hippurus is known to be attracted to monly found, are generalists (Edgar and Shaw 1995). floating debris (Froese and Pauly 2009). This asso- An assumption that young syngnathids are at greater ciation with may also explain the four risk of predation (Kuiter 2000) could not be corrob- accounts of seahorse predation by the tuna orated with available records. Most accounts did not N. macropterus in the tropical Pacific (Alverson specify the age of the prey species, though some were 1963), Northwest Atlantic (USNM 1960), the Gulf of stated to be adults. Guinea (Sund and Richards 1967), and near the Hawaiian Islands (Herald 1949). By associating with Habitat overlap of predators floating marine flora, syngnathids could maintain their crypsis in the open ocean, where they would Although the inferred habitats of syngnathids over- otherwise be obvious to pelagic predators. Given this lapped with those of most of their predators, there apparent periodic use of open ocean habitat, it is 123 Rev Fish Biol Fisheries (2011) 21:205–223 219 possible that rafting could be an important vector for Summary population dispersal. In general, predation of syngnathids seems to be rare Avian predators in time and space, perhaps reflecting the generally low abundance of these fishes. It also apparently This review documented an apparently high number tends to be opportunistic, with predators not specif- (26 species) of avian predators, although the fre- ically targeting their cryptic prey. Rather than quency of avian predation may partially reflect the suggesting that syngnathids are vulnerable at partic- prevalence and long-term nature of colonial bird ular life stages or sizes, the results of this review studies. More than half of the bird species identified indicate that seahorses and pipefishes are frequently were terns, gulls, gannets and tubenoses, all of which taken when they are abundant, and/or engaging in forage by seizing prey at or relatively near the water’s ‘‘risky’’ behaviour such as rafting. Syngnathid pre- surface. Like some fishes, they are also attracted to dators also seem to be encountering their prey outside floating marine debris (e.g., Vandendriessche et al. demersal habitats. Seahorses and pipefishes could be 2007). Other marine bird taxa listed here (, moving in the open ocean more than suspected, , cormorants or shags, sea ducks) pursue their perhaps attaching themselves to floating mats of plant prey underwater, either benthically or in the mid- material to maintain crypsis. If this is the case, such , while herons and egrets forage in behaviour may well act as an important vector for shallow water by stalking their prey from above. population movement and dispersal. Thus, while many avian predators forage in the Given the opportunistic and generalist habits of the marine demersal zone where syngnathids are com- predators identified here, this review found no monly found, the predominance of surface-feeding or indication that syngnathids can be considered an near surface-feeding birds again suggests that syng- important prey species in marine food webs. Indeed, nathid prey is often encountered outside demersal the inclusion of pipefish in the diet of many marine habitat. birds has coincided with lower than average breeding Almost 26% of the avian predation accounts were success or outright breeding failure at their colonies. of E. aequoreus, which may be at least partially Episodic predation on high densities of syngnathids pelagic during population booms (van Damme and by other taxa might indicate an absence of preferred Couperus 2008). In most cases, E. aequoreus was the prey, or it may conversely suggest that syngnathids only known syngnathid prey for the bird species in represent an important alternative prey source for question (e.g., as with the common guillemot Uria non-avian predators. There thus may be merit in aalge Sonntag and Hu¨ppop 2005), and/or the only further study of the importance of syngnathids as record of syngnathid predation was during a popula- food, especially given the poor quality of existing tion boom of E. aequoreus. The low caloric value of information. Syngnathid fishes comprise significant syngnathids (Harris et al. 2007b; Kloppmann et al. components of some seagrass ecosystems, and are 2007) suggests that marine birds may only feed on also present in many other coastal habitats. Future seahorses and pipefishes when preferred prey is studies observing or tracking syngnathid populations unavailable (Harris et al. 2007a). Seabirds generally could clarify whether or under what circumstances breed most successfully when feeding offspring on predation plays a role in regulating their populations. high-lipid prey, e.g., sandeels Ammodytes spp., and As the list of syngnathid predators compiled here is years where low-lipid prey predominates tend to undoubtedly incomplete, future studies will likely coincide with poor reproductive success or outright also reveal additional predators of these fishes. colony failures (e.g., Wanless et al. 2005; Hedd et al. 2006). Indeed, accounts of seabird chicks choking on Acknowledgments We thank the Seabird-L listserve E. aequoreus (Harris 2006) or starving in nests members who responded to Mike Harris’s original request for information on snake pipefish in seabird diets, to Mike surrounded by dead pipefish (Newell 2006) suggests Harris himself for sharing offline responses, and to those who that for some predators, syngnathids may actually be replied to our request for information via the Project Seahorse a detrimental food source rather than just a low-value syngnathid listserve. Conversations with Mike Harris, Sarah one. Wanless and Keith Martin-Smith also provided insight into the 123 220 Rev Fish Biol Fisheries (2011) 21:205–223

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