MARINE ECOLOGY PROGRESS SERIES Vol. 256: 271–286, 2003 Published July 17 Mar Ecol Prog Ser

Maritime mammals: terrestrial mammals as consumers in marine intertidal communities

James T. Carlton1,*, Janet Hodder2

1Maritime Studies Program, Williams College — Mystic Seaport, PO Box 6000, Mystic, Connecticut 06355, USA 2Oregon Institute of Marine Biology, University of Oregon, PO Box 5389, Charleston, Oregon 97420, USA

ABSTRACT: The phenomenon of terrestrial mammals as predators in marine intertidal communities, and thus as agents of energy transfer from sea to land, is poorly understood. We review here the evi- dence for terrestrial mammals intentionally entering the ocean shore at low tide in order to prey on living marine invertebrates, fish, algae, and seagrasses. We introduce the term ‘maritime mammals’, defined as coastal mammalian predators that utilize living intertidal energy resources and transfer these resources to the land. We document 135 records of among 45 of terrestrial mammals in 8 orders feeding in marine intertidal zones. Most predation events are by carnivores (59%, mostly by raccoon, mink, black bear, and Arctic fox), followed by rodents (20%) and artio- dactyls (14%). Maritime mammals occur on all continental coastlines of the world except Antarctica. Most records are from the Eastern North Pacific Ocean, with 21 species of maritime mammals. Twelve maritime mammal species occur in the Western North , and 8 maritime mam- mals are known for the Eastern South Pacific Ocean. These 3 regions account for 42% of the diver- sity of maritime mammals. A total of 228 different prey taxa are known to be consumed, representing 2 12 phyla of marine organisms; /3 of these taxa are bivalve and gastropod mollusks, , and fish. Introduced populations of 17 species of mammals have been recorded as maritime predators; 15 of these are recorded on islands where endemic mammals were absent or rare. Maritime mammals are widespread globally, with often repeated cases of predation being observed for the same species. We suggest that predation by maritime mammals is a rarely studied, rather than rare, phenomenon, and maritime mammals are thus a largely overlooked guild of intertidal predators. Quantitative field observations (using techniques such as infrared night vision, radiotelemetry, and stable isotope analysis) and experimental studies (using exclosures, or by taking advantage of the removal of insular introduced mammal populations) are required. The importance of intertidal resources in supplying energy to terrestrial populations of many species of mammals world wide may have been underappreciated.

KEY WORDS: Intertidal predators · Intertidal prey · Invasions · Mammal predation · Intertidal communities · Subsidies

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INTRODUCTION 1999). Energy-flow pathways between marine ecosys- tems include a variety of phenomena. A prominent The amount of energy transferred between trophic example is the transport of detritus from one ecosystem levels, and the mechanisms by which that energy to another. For example, drift algae and carcasses of flows, are major organizing phenomena and processes marine vertebrates are commonly washed ashore of community structure (Krebs 1993, Ricklefs & Miller and utilized by terrestrial consumers (Polis & Hurd 1999). In addition, the transfer of energy between 1996a,b). Coastal algae and seagrasses are exported to ecosystems is widely recognized as an important com- the open ocean and the deep sea (Wolff 1976, Zieman ponent of food webs (Polis et al. 1997, Stapp et al. et al. 1979, Graham et al. 2003). An equally common

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phenomenon is the utilization of prey in one habitat by an observation apparently not made since the 17th predators from another habitat: terrestrial carnivores century (Table 1). In some instances however, preda- prey upon sea turtle eggs buried in sandy beaches tion by maritime mammals may be enhanced by (Hirth 1987, National Research Council 1990), terres- human activities. Urbanization may lead to higher trial herbivores feed on intertidal salt marsh vegetation densities or new populations of native or introduced (Shanholtzer 1974), and deep sea and nekton predators. High densities of domestic close to vertically migrate to prey upon organisms in upper the shore may also lead to increased interactions with ocean strata (Vinogradov 1968). the marine environment; (3) The phenomenon may be Energy derived from such allochthonous detritus or highly localized: predation on marine organisms by prey can subsequently flow into yet other parts of an terrestrial mammals may occur only in certain local- adjacent ecosystem. Examples include bear feces com- ized regions, albeit being common at such sites posed of salmon contributing to energy flow in forests (Navarrete & Castilla 1993); (4) The phenomenon may (Willson et al. 1998), and seabird feces composed of be relatively common but unrecognized and underre- fish contributing to energy flow in other terrestrial bio- ported: predation on marine organisms by terrestrial mes (Heatwole 1971, Crawford & Shelton 1978). Other mammals may be common but largely underappreci- major between-ecosystem energy transfers involve ated or underdescribed, for at least 5 reasons. These long-distance migration of some species of insects, are, (i) it is rarely reported in easily accessible litera- fish, birds, mammals, and other organisms. All of these ture, (ii) incidental observations by marine ecologists cross-ecosystem energy flows may have important and others are over time increasingly less likely to be influences on the abundance, distribution and inter- published because of their nonquantitative or nonex- actions of prey, predator, and detritivore populations, perimental nature, (iii) it may be underrecorded, and thus the structuring of communities. being a primarily crepuscular or nocturnal low tide Within this context, the phenomenon of strictly ter- activity (Moore 2002), (iv) it falls at the interface of the restrial mammals as consumers, and thus as agents of disciplines of marine and terrestrial ecology and is energy transfer, in marine intertidal communities is thus rarely studied (Navarette & Castilla 1993), or poorly understood (Ricketts et al. 1952, Navarrete & (v) experimental studies on the importance of terres- Castilla 1993). While the flow of energy from the sea to trial mammals as intertidal predators are non-existent, the land has come under increased scrutiny (Pollis and thus it has been presumed to be insignificant both & Hurd 1996a,b, Stapp et al. 1999), the majority of in terms of an energy flow pathway and as an orga- reviews of marine littoral ecosystems make little or no nizing force in intertidal community structure. reference to terrestrial mammals as intertidal pre- We review here (and provide previously unpub- dators (Valiela 1995, Raffaelli & Hawkins 1996, Ny- lished data on) the phenomenon of terrestrial mam- bakken 2000, Levinton 2001), and few direct studies mal predation in coastal ecosystems worldwide. Our exist that focus on this phenomenon (Navarrete & focus is on the evidence for terrestrial mammals Castilla 1993, Conradt 2000). intentionally entering the ocean shore at low tide in This lack of recognition (and thus understanding) of order to consume living (not detrital) marine inverte- the phenomenon of terrestrial mammals as intertidal brates, fish, algae, and seagrasses. We call this con- consumers may arise from at least 4 situations: (1) The sumption predation. We introduce the term ‘maritime phenomenon may be naturally rare: predation on mammals’, defined as coastal mammalian predators marine organisms by terrestrial mammals may be rare that utilize living intertidal energy resources and both in time and space, and thus not a significant transfer these resources to the land. We exclude from mechanism of either interecosystem energy flow or of our review 3 phenomena which also bring terrestrial the structuring of intertidal communities; (2) The mammals into maritime arenas: (1) predation on phenomenon may be rarer now: in some regions, be- seabird and sea turtle eggs and hatchlings; (2) the cause of the extirpation by humans of both predator scavenging of carrion and detritus on beaches; and and prey from urbanized coastal zones, once more- (3) predation in salt marshes and mangroves. These 3 common predation events may now be infrequent or aspects are reviewed in part by Moore (2002). We no longer occur. Indeed, most coastal observation sta- have excluded in particular those reports of domestic tions (such as marine biological laboratories) are now animals (such as cows, horses, and pigs) feeding on in relatively urbanized areas. An example may be the intertidal algae where it is unclear if these herbivores observation of predation by bears on intertidal are feeding on attached living seaweed or on drift lobsters in Maine. John Josselyn, writing in 1674 of plant material. This noted, the consumption of sea- observations made in 1638 and in 1663, wrote that weed wrack is common enough in parts of Europe ‘The bear is a tyrant at a lobster and at low water will such that certain algae have been given common go down to the rocks after them with great diligence’, names such as pig weed, cow weed, and horse weed Carlton & Hodder: Terrestrial mammals as intertidal predators 273

(Moore 2002). We also exclude the activities of RESULTS human (Homo sapiens) predators and foragers in this review. Biogeography and diversity of maritime mammals We further examine these data for evidence of the relative roles of introduced (non-indigenous) versus We document 135 records of predation among native predators, given the predominance of certain 45 species of terrestrial mammals in 8 orders (Tables 1 species of introduced mammals on islands and in & 2) feeding in marine intertidal zones. Eighty-seven coastal zones (King 1985). We also consider the role of percent of the mammalian predators are in 3 orders introduced prey species in maritime mammal diets. We (Carnivora 44%, Rodentia 27%, and Artiodactyla further consider hypotheses that address why terres- 16%). The remaining orders (marsupials [Didelphi- trial mammals would seek food resources in the inter- morphia and Dasyuromorphia], Primates, Lagomor- tidal zone, and the spatial or temporal circumstances pha, and Insectivora) are represented by far fewer spe- under which such predation may occur. We review cies. Most predation events are by Carnivora (59%, biases in the nature and quality of the data, and then mostly by raccoon, mink, black bear, and Arctic fox), 1 ask whether the phenomenon of maritime mammals is followed by Rodentia (20%, over /3 of which are the rare, highly localized, or perhaps common but largely Norway rat), and Artiodactyla (14%, over half of which unrecognized. are domestic pigs and mule deer). Finally, we discuss the evidence for, and research No living terrestrial mammal species are known to needs to determine, the potential ecological impor- specialize entirely on intertidal prey. Sheep, however, tance of this phenomenon relative to both landward on North Ronaldsay and Linga-Holme on the Orkney energy flow and to altering the diversity, abundance Islands in Scotland are known to live almost exclu- and distribution of intertidal prey species. sively on intertidal seaweeds (Hall 1975, Conradt 2000). We note the existence of the poorly known and now-extinct sea mink Mustela macrodon, last verifi- MATERIALS AND METHODS ably seen in 1880 (Carlton et al. 1999). This mink lived on the coastal zone from Canada to Connecticut, We searched the literature for reports of predation and was hunted to extinction for its fur. It appears to by terrestrial mammals on marine intertidal animals have been restricted to rocky shore habitats both on and plants and interviewed colleagues familiar with the mainland and on offshore islands, and may have intertidal shores. In some instances we admit reliable spent most of its time in the water (Manville 1966, reports of observations of mammals foraging and con- Campbell 1988). It may have preyed almost entirely suming organisms in the intertidal zone, although the on marine intertidal and shallow sublittoral prey, exact nature of the prey is not yet known. Most pub- although the only verified prey were intertidal fish lished observations occur as incidental remarks, and (Manville 1966). If the sea mink was a specialized we thus assume that we have missed reports. We maritime mammal, then the only such species has report our own field observations derived from west- become extinct. ern and eastern North America (Oregon, California, and Connecticut). For analysis of prey diversity, we scored individual Biogeographic patterns species where reported. For prey reported only at higher taxonomic levels (e.g. brachyurans, crusta- Maritime mammals occur on all continental coast- ceans, tide pool fish, bivalves, and so forth) we conser- lines of the world except Antarctica. Most records are vatively scored these as unique taxa only if the same from the Eastern North Pacific Ocean (Alaska to the type of organism in the same geographic region was Galapagos Islands) with 21 species of maritime mam- not already reported at the species level for that preda- mals known, of which 12 are unique (but not necessar- tor. For example, where the brachyuran Cancer is ily endemic) to this region (Beechey ground squirrel, reported as prey of mink in Washington, and brachyu- deer mouse, Keen’s mouse, muskrat, Townsend’s vole, rans as prey of mink in nearby British Columbia, we coyote, gray fox, red fox, grizzly bear, American pine scored these reported prey as only one species for both marten, mule deer, mountain goat). regions. However, if distinctly different geographic Twelve maritime mammal species are reported for regions were involved, we scored unidentified prey as the Western North Atlantic Ocean (Greenland to the different species. For example, where the brachyuran Caribbean, including the Gulf of Mexico), of which crab Ocypode is reported as prey of domestic dogs in 3are unique records (opossum, masked shrew, and Fiji, and brachyura as prey of dogs in Puerto Rico, we gray wolf). Eight maritime mammals are known for the scored these prey as 2 different species. Eastern South Pacific Ocean (the west coast of South 274 Mar Ecol Prog Ser 256: 271–286, 2003

Table 1. Terrestrial mammals feeding in the intertidal zone. Common and Latin mammal names follow Nowak (1999). Prey that are introduced in the localities are indicated by Latin names in bold. Abbreviations are as follows: Summary of prey taxa (∑P): A= no. of different species consumed, P = no. of different plant species consumed; native/introduced status of mammals: N = native, I = introduced; observations (if not shown, nature of observation is not given by author): B = material in burrows or dens, DO = direct observation of feeding, S = scat (feces), SI = based on stable isotopes, ST = stomach or digestive tract contents

Order/Species/∑P N/I Location/(observations) Prey Source

Didelphimorphia Virginia opossum N USA: Gulf of Mexico Brachyura (Uca pugilator) Rathbun (1918) (Didelphis virginiana) A:1 N USA: Gulf of Mexico ‘Living among jetty rocks and feeding Britton & Morton (1989) upon the sessile mid-littoral jetty fauna’ Dasyuromorphia Tasmanian devil N Australia: Tasmania Amphipoda (Talitridae) Moore (2002) (Sarcophilus harrisii) A:1 Insectivora Lesser white-toothed shrew N UK: Scilly Islands Amphipoda (probably Talitridae) Churchfield (1990) (Crocidura suaveolens) A:1 ‘As well as other small invertebrates’ Masked shrew N Canada: Nova Scotia Amphipoda (‘Littoral’, possibly Tali- Stewart et al. (1989) (Sorex cinereus) A:2 Bon Portage Isl. (ST) tridae); Diptera (kelp flies, Coelopidae) Primates Chacma baboon N South Africa ‘Marine shellfish and ’ Avery & Siegfried (1980) (Papio ursinus) A:7 N South Africa Amphipoda (Talitridae) Brown & McLachlan (1990) N South Africa: Bivalvia (‘black ’: Choromytilus Hall (1962) Cape of Good meridionalis); (‘periwinkles’, Hope (DO, S) ’limpets’); Amphipoda (Talorchestia sp.); Isopoda (‘rock lice’, possibly Ligia); Brachyura (Cyclograpsus punctatus; Plagusia chabrus) Lagomorpha Domestic rabbit (Oryctolagus I South Africa: Schaapen Algae (Ulva) G. Branch (pers. comm.); cuniculus) P:1 Isl., Saldanha Bay (DO) Moore (2002) Rodentia Beechey ground squirrel N USA: California: Monterey Foraging in intertidal zone: J. T. Carlton (pers. obs.) (Spermophilus beecheyi) P:1 Bay: Pacific Grove (DO) prey not known N USA: California: Eelgrass Roest (1993) Morro Bay (DO) (Zostera marina) Deer mouse (Peromyscus N USA: California: Amphipoda (Talitridae, Megalorchestia?); Osborne & Sheppe (1971) maniculatus) A:3 Humboldt County (ST) Diptera Coleoptera, (Staphylinidae) N Mexico: Baja California ‘Intertidal invertebrates’ Stapp (1999) Keen’s mouse N Canada: British Columbia: ‘Intertidal organisms’ Drever et al. (2000) (Peromyscus keeni) Triangle Isl. (SI) Andean rat (Chroeomys N Chile: Punta Metri (ST) Bivalvia (Mytilidae); Gastropoda; Martinez et al. (1986) olivaceus) A:3, P:1 Anomura (Petrolisthes sp.); algae House mouse I Chile: Las Cruces (ST) Gastropoda; Brachyura; Navarrete & Castilla (1993) (Mus musculus) A:2, P:1 Rhodophyta Mouse (unidentified) N?/I? USA: Oregon: Gastropoda Frank (1965) A:1 Coos Bay (DO) (limpet, Lottia digitalis) Towsend’s vole N Canada: British Columbia: ‘Intertidal organisms’ Drever et al. (2000) (Microtus townsendii cowani) Triangle Isl. (SI) Muskrat (Ondatra zibethicus) N USA: Washington: Bivalvia Martinez et al. (1986) A:1 Puget Sound (mussels, Mytilus) False water rat (Xeromys N Australia: Victoria: Brachyura (Carcinus maenas) G. Parry (pers. comm.) myoides) A:1 Queenscliff, Swan Bay (DO) House (black) rat (Rattus I Midway Atoll (DO) Brachyura (Uca sp.) N. Seto (pers. comm.) rattus) A:16 I Chile: Punta Metri (ST) Bivalvia (Mytilidae); Gastropoda Martinez et al. (1986) I Chile: Punta Kilian: Bivalvia (Perumytilus purpuratus); Zamorano (1986) Mehuin (S) Gastropoda (Concholepas concholepas, Fissurella picta, F. nigra, Siphonaria lessoni, parasitica); Polyplaco- phora (Chiton latus, C. granosus); Bra- chyura (Acanthocyclus gayi, A. hassleri, Carlton & Hodder: Terrestrial mammals as intertidal predators 275

Table 1 (continued)

Order/Species/∑P N/I Location/(observations) Prey Source

Pisoides edwardsi, Homalaspis plana); (Petro- listhes violaceus); Anomura Fish (Sicyases sanguineus, Calliclinus geniguttatus) Rat (Norway? Black?) N Europe: Denmark? Gastropoda (limpet ) Thorson (1971) Norway rat I Italy: Po River valley Bivalvia (Cerastoderma lamarcki, Ensis sp., Parisi & Gandolfi (1974) (Rattus norvegicus) Mactra corallina, Mytilus galloprovincialis, A:66, P:1 Scrobicularia plana); Gastropoda (Haminoea sp.); Brachyura (Carcinus aestuarii) I UK: Isle of Man (D) ‘Occasionally seen Thompson et al. (2000) foraging on the shore’ I USA: Bivalvia; Gastropoda Menge & Sutherland (1987) Massachusetts (including Nucella lamellosa) IUSA: Atlantic coast ‘Forage at low tide on invertebrates’; Amos (1966) (Brachyura, Ocypodidae) ‘ghost crabs’ I USA: Pacific coast Brachyura ( crassipes) Garth & Abbott (1980) I Canada: Queen Charlotte Bivalvia; Gastropoda; Crustacea: Drever & Harestad (1998) Islands Amphipoda, ; Fish I Chile: Las Cruces Bivalvia (Perumytilus purpuratus, Brachidontes Navarrete & Castilla (1993) (B, S) granulata, Mesodesma donacium, Tagelus dombeii); (Gastropoda Fissurella crassa, F. axima, F. costata, F. limbata, Collisella spp., Scurria scurra, S. parasitica, niger, Tegula atra, Diloma nigerrima, Littorina peru- viana, Siphonaria lessoni, Concholepas concho- lepas, Trimusculus peruvianus); Polyplacophora (Chiton granosus, C. spp.); Cirripedia (Austro- megabalanus psittacus); Brachyura (Allopetro- isthes punctatus, Leptograpsus variegatus, Acanthocyclus gayi, A. hassleri, Paraxanthus barbiger; Homalaspis plana, Taliepus dentatus); Anomura (Petrolisthes violaceus, P. tuberculatus, P. granulosus, P. laevigatus, Pachycheles grossi- manus); Asteroidea (Heliaster helianthus); Echi- noidea (Loxechinus albus); Fish (Aphos porosus, Sicyases sanguineus) I Chile: Punta Metri (ST) Bivalvia (Mytilidae); Gastropoda; Martinez et al. (1986) Anomura (Petrolisthes sp.); algae I Chile: Las Cruces (ST) Polychaeta; Gastropoda; Navarrete & Castilla (1993) Brachyura; Rhodophyta I New Zealand: Polychaeta Bivalvia (mussels, Xenostrobus Moors (1985) Noises Isl. (S, ST) pulex); Gastropoda (Onchidella sp., cf. O. nigricans; Cellana spp., Nerita atramentosa; Eatoniella sp. Lepsiella scobina, Diloma sp.); Cirripedia (Chamaesipho columna); Brachyura (Pinnotheres novaezelandiae); I New Zealand: Ike Isl. (B) Gastropoda ( smaragdus, Thais Moors (1985) orbita); Brachyura (Leptograpsus variegatus); Polynesian rat I Midway Atoll Brachyura N. Seto (pers. comm.) (Rattus exulans) A:1 (DO) (Uca sp.) Pygmy rice rat (Oligo- N Chile: Punta Metri (ST) Gastropoda; algae Martinez et al. (1986) ryzomys longicau- datus) A:1, P:1 Carnivora Raccoon dog (Nycte- N Russia: Pacific coast Brachyura; Echinoidea Novikov (1956) reutes procyonoides) A:2 Coyote (Canis latrans) N Mexico: Baja California Bivalvia (‘clams’) fish (‘puffer fish’) Crawford (1953) A:7, P:2 Santa Maria Bay (DO) N Mexico: Baja California: Polychaeta (‘tube worms’); Gastropoda Rose & Polis (1998) Gulf of California (S) (‘snails’); Isopoda (Ligia, Tylos); Brachyura (Ocypodidae); Chlorophyta; Phaeophyta

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Table 1 (continued)

Order/Species/∑P N/I Location/(observations) Prey Source

N Mexico: Baja California ‘A consistent intertidal feeder’ Ricketts et al. (1952) Gray wolf A:1 (Canis lupus) N USA: Gulf of Mexico Brachyura (Uca pugilator) Rathbun (1918)

Domestic dog I Puerto Rico Brachyura (‘crabs’) Crosby (1972) (Canis famliaris) A:5 I USA: Maine: Cirripedia (Semibalanus balanoides) J. T. Carlton (pers. obs.) Vineyard Haven (DO) I Fiji: Yanuca Isl. (DO) Brachyura (Ocypodidae, Ocypode sp.) L. Eldredge & J. T. Carlton (pers. obs.) I Kiribati: Canton Fish (mullet) Degener & Gillaspy (1955) Atoll (DO) P. Jokiel (pers. comm.) I Peru: Atacama coast ‘shellfish’ Crosby (1972) Black-backed jackal N Namibia (DO) Fish (Mugil cephalus) Nel & Loutit (1986) (Canis mesomelas) A:2 N Namibia: Cape Bivalvia (‘brown ’) Hiscocks & Perrin (1987) Cross Seal Reserve (S) Arctic fox (Alopex N Iceland (S) ; Crustacea; Insecta (Diptera, Hersteinsson & MacDonald lagopus) A:29, P: 2 ‘kelp flies’); algae (‘seaweed’) (1996) N Iceland Fish (Cyclopterus lumpus) Braestrup (1941) NGreenland Porifera; Polychaeta (‘worms’); Bivalvia Braestrup (1941) (Mytilus edulis, Mya arenaria, M. tyrun- cata); Gastropda (including ‘sea slugs’); Brachyura (Hyas areneus, Chionoecetes opilio) Asteroidea; Echinoidea; Holo- thuroidea; Ascidiacea; Fish (Pholis gunellu, Lumpenus fabricus Mallotus villosus, Gadus saidua) NGreenland (DO) Fish (Pholis fasciatus, Cyclopterus Nielsen (1991) lumpus, Myoxocepalus sp. ‘and others’) NGreenland (ST) ‘Fish, shellfish and seaweed’ Kapel (1999) N Russia: Arctic island ‘Marine invertebrates important in Lavrov (1932), Fox (1975) summer diet’ N Russia: Commander Porifera; Polychaeta (‘worms’); Mollusca; Novikov (1956) Islands ‘crustaceans’; Echinoidea; Holothuroidea; Ascidiacea I USA: Alaska: Porifera; Cirripedia; Amphipoda; West (1987) Aleutian Islands Brachyura; Holothuroidea; Nizki/Alaid Islands (ST) Phaeophyta (kelp) I USA: Alaska: Bivalvia (mussels,clams); Gastropoda; West (1987) Aleutian Islands: Cirripedia; Amphipoda; Isopoda; Kagalaska Isl. (S) Brachyura; Echinoidea; Holothuroidea; Phaeophyta (kelp) I USA: Alaska: Polychaeta (Nereis); Bivalvia (clams, Murie (1959) Aleutian Islands (S) mussels); Gastropoda; Amphipoda; Cirripedia (Pollicipes polymerus); Isopoda; Echinoidea Gray fox (Urocyon N Mexico: Baja California Gastropoda; Brachyura Rose & Polis (1998) cinereoargenteus) A: 3 Gulf of California (DO) (‘crabs’); Holothuroidea Patagonian fox (Pseu- I Falkland Islands Gastropoda (limpets); Brachyura (‘crabs’); Strange (1983) dalopex griseus) A:3 fish (dogfish, Harpagifer hispinis) Peruvian desert fox N Peru: ocean Brachyura (‘crabs’) Huey (1969) (Dusicyon sechurae) A:1 beaches adjacent to Sechura Desert (S) Red fox I USA: Washington: Foraging in intertidal: Holmes (1992), (Vulpes vulpes) San Juan Isl. (DO) prey not known M. Herko (pers. comm.) Red or gray fox N/I Pacific American coast: Amphipoda (‘Traskorchestia Ricketts et al. (1986) ‘islands to the far north’ and other amphipods’) Brown hyena N Namibia: Brachyura Stuart & Shaughnessy(1984) (Parahyaena brunnea) A:1 Sandwich Harbor (S) Striped hyena N Kenya Brachyura (open coast sand beach species) National Geographic (Hyaena hyaena) A:1 Society (1998) Carlton & Hodder: Terrestrial mammals as intertidal predators 277

Table 1 (continued)

Order/Species/∑P N/I Location/(observations) Prey Source

American black bear N USA Maine Canada: Astacura (lobster, Homarus americanus) Josselyn (1674) (Ursus americanus) British Columbia: Cirripedia (Balanus glandula); Brachyura (in Conkling 1999) A:6, P:1 Clayoquot Sound (DO) (‘shore crabs’ []); Asteroidea Oldershaw (1995) N Canada: Queen Amphipoda (Talitridae, Traskorchestia Ellis & Wilson (1981) Charlotte Islands (DO) traskiana); Brachyura (Hemigrapsus nudus) N Canada: Rolling large cobbles and D. Padilla (pers. comm.) Vancouver Isl.: Bamfield eating (Cirripedia) N Canada: Photograph of black bear flipping rocks Ramsay (1985) Vancouver Isl. in search of crabs (Brachyura) N Canada: Queen Charlotte Scraping barnacles off E. A. Mills (pers. comm.) Islands Princess Royal Isl. (DO) intertidal rocks N USA: Alaska: southern Phaeophyta (Fucus gardneri) O’Clair & O’Clair (1998) N USA: Alaska: Katmai Bivalvia (mussel, Mytilus californianus)T. Klinger (pers. comm.) National Park Shelikof Strait N USA: Alaska: Foraging in mussel beds: prey not known C. Hewitt (pers. comm.) Prince William Sound N USA: Alaska: Tracy Video of bears scraping barnacles off N. Folsom (pers. comm.) Arm (South of Juneau) and intertidal rocks; scat consists of Glacier Bay National Park remains (DO, S) Grizzly (brown) bear N USA: Alaska: Kenai Bivalvia M. Matthews (pers. comm.) (Ursus arctos) A:3 Peninsula: Kachemak (Saxidomus giganteus) Bay, Ishmaloff Isl. (DO) N USA: Alaska: Katmai Bivalvia (Siliqua patula) E. A. Mills (pers. comm.) National Park Shelikof Strait (DO) N USA: Alaska: Katmai Foraging in intertidal: prey not known T. Klinger (pers. comm.) National Park Shelikof Strait N USA: Alaska: Glacier Video of bears foraging in intertidal N. Folsom (pers. comm.) Bay National Park zone by flipping rocks, searching (DO) for and consuming crabs Raccoon N USA: Connecticut: New Bivalvia (Geukensia Daiber (1982) (Procyon lotor) A:35 London: Bluff Point (DO) demissa, Mya arenaria) J. T. Carlton (pers. obs.) N USA: Gulf of Mexico Brachyura (Uca pugilator) Rathbun (1918) N Pacific coast of America: ‘Foraging in the mussel beds’; ‘visits Ricketts et al. (1986) Puget Sound to Baja the shore at low tide feeding principally California on crabs’ [Brachyura] I Canada: Queen Bivalvia (mussels); Gastropoda (‘snail’ and Hartman (1990, 1993) Charlotte Islands (S) ‘limpet’); Cirripedia (Pollicipes polymerus); Amphipoda; Isopoda; Brachyura (Hemi- grapsus nudus); Echinoidea (‘sea urchin’) I Canada: Queen Foraging for small fish in intertidal zone E. A. Mills (pers. comm.) Charlotte Islands I Canada: Vancouver Brachyura (Hemigrapsus) D. Padilla (pers. comm.) Isl.: Bamfield (S) NWashington Bivalvia (Mytilus trossulus); Brachyura (Hemi- Dalquest (1948) grapsus, nudus, H. oregonensis Cancer pro- ductus); Anomura (Petrolisthes eriomerus); N USA: Pacific coast Amphipoda (Talitridae, Megalorchestia Barnard et al.(1980) californiana) N USA: California: Mendocino Bivalvia (‘clams’); Brachyura (‘crabs’); Warrick & Wilcox (1981) Co.: Big River Fish N USA: California: Bodega Cirripedia (Pollicipes polymerus); Amphipoda J. T. Carlton (pers. obs.) Bay: Bodega Head (S) (Talitridae, Megalorchestia); Brachyura (Pachygrapsus crassipes) N USA: California: Bodega Brachyura (Carcinus maenas) J. T. Carlton (pers. obs.) Bay: Bodega Harbor (S) N USA: California: Pt. Reyes (S) Anomura (Emerita analoga) A. Cohen (pers. comm.)

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Table 1 (continued)

Order/Species/∑P N/I Location/(observations) Prey Source

N USA: California: Brachyura (Pachygrapsus crassipes) T. Grosholz (pers. comm.) Bolinas Lagoon (S) N USA: California: Santa Cruz (S) Brachyura (Pachygrapsus crassipes) R. Everett (pers. comm.) N USA: Oregon: Bivalvia (Mya arenaria Macoma nasuta, Davidson (1990) Coos Bay (S, DO) Cryptomya californica); Brachyura (Cancer magister); Anomura (Neotrypaea californiensis, Upogebia pugettensis) N USA: Oregon: Echinoidea (Strongylocentrotus purpuratus) J. Hodder & J. T. Carlton Cape Blanco (DO) (pers. obs.) N USA: Washington: Polychaeta (Nereis); Bivalvia, Mytilidae Tyson (1950) Willapa Bay (ST) (presumably Mytilus), Ostreidae (Ostrea); Anomura (Emerita analoga), additional crabs reported as Ocypodidae, but this family does not occur in Washington; Caridea (Crangon nigricauda); Echiura (Urechis caupo); Fish (Clevelandia ios, Leptocottus armatus) N USA: Washington: Bivalvia (Venerupis philippinarum)V. Galluci (pers. comm.) San Juan Isl. (DO) American mink I Iceland: Grindavik (S) Amphipoda; Isopoda (Ligia oceanica, Idotea Skirmisson (1979) (Mustela vison) spp.), Brachyura (Carcinus maenas), Fish (Myxo- A:47 cephalus scorpius, Pholis gunnelus, Ciliata mustela, Cyclopterus humpus, Gasterosteus aculeatus, Pollachius virens, Sebastes sp.) I UK: Scotland: Ross Peninsula Isopoda (Ligia oceanica?); Brachyura (Carcinus Dunstone & Birks (1987) maenas, other crabs); Fish (Anguilla anguilla, Salmo sp., Gasterosteus aculeatus, Lipophyrs pholis, Pholis gunnelus, Ciliata mustela, Taurulus bubalis, Gobius sp., Spinachia vulgaris, flatfish) I : Baiona Brachyura (Pachygrapsus marmoratus, Necora Delibes et al. (2003) puber, Carcinus maenas, ); Fish (Coryphoblennius galerita, Lipophrys pholis, Gaidropsarus sp., Gobius cobitis) NUSA: Atlantic coast Forage at low tide on invertebrates Amos (1966) N USA: Maine (DO) Brachyura (Carcinus maenas) D. Jacobs (pers. comm.) N USA: Connecticut: Noank (DO) Foraging in intertidal zone: prey not known D. A. Carlton (pers. comm.) N Canada: British Columbia (DO) Brachyura (‘crab’) Echinoidea; ‘shellfish’ Carefoot (1977) N Canada: British Columbia Brachyura Garth & Abbot (1980) N USA: Alaska (southern) Bivalvia (‘clams’), Brachyura (‘crabs’), O’Clair & O’Clair (1998) ‘other crustaceans’; fish (‘tidepool’) N USA: Washington: Bivalvia (Veneroida, 2 spp.); Gastropoda (Lottidae, Perry (1998) San Juan Isl. (DO, S) Littorinidae, Trochidae); Mysidacea; Amphipoda; Isopoda; Caridea (Hippolytidae); Brachyura (Cancer; Majidae); Fish (Agonidae, Clupeidae, Cottidae, Cyclopteridae, Gadidae, Pholididae, Pleuronectiformes, Zoarcidae, Scorpaenidae, Stichaeidae) N USA: Oregon: Fish: sculpin in intertidal mussel beds J. Jansen (pers. comm.) Cape Arago (DO) American pine N USA: Alaska (southern) Marine crustaceans O’Clair & O’Clair (1998) marten (Martes americana) A:1 Old world badger N Ireland: Fenit Is County Amphipoda (Talitridae) Isopoda J. Davenport (pers. comm.) (Meles meles) A:2 Kerry (DO & S) Sleeman et al. (2001) Striped skunk N USA: Atlantic coast Forage at low tide on invertebrates; ‘ghost Amos (1966) (Mephitis mephitis) crabs’ (Brachyura: Ocypodidae) A:2 N USA: Washington: Puget Sound Brachyura (Hemigrapsus nudus) Dalquest (1948) Skunk (unidentified) N USA: Gulf of Mexico Brachyura (Uca pugilator) Rathbun (1918) Domestic cat I USA: Gulf of Mexico Brachyura (Uca pugilator) Rathbun (1918) (Felis catus) A:5 Carlton & Hodder: Terrestrial mammals as intertidal predators 279

Table 1 (continued)

Order/Species/∑P N/I Location/(observations) Prey Source

I USA: Gulf of Mexico ‘Living among jetty rocks and feeding upon the Britton & Morton (1989) sessile mid-littoral jetty fauna’ I Seychelles: Brachyura (Grapsus tenicrustatus); Fish Seabrook (1990) Aldabra Atoll (S, ST) I Galapagos Islands Brachyura (Sally Lightfoot Crabs, Lever (1994) Grapsus grapsus); Isopoda Artiodactyla Domestic pig (Sus I USA: Rhode Isl.: Bivalvia (Mya arenaria or Mercenaria mer- Miantonomo (1642) scrofa) A:6; P:1 Narragansett Bay (DO) cenaria; oysters, Crassostrea virginica) (in Cronon 1983) I USA: Oregon: Coos Bay Bivalvia (Mya arenaria) Peterson & Powers (1952) I New Zealand: Auckland Phaeophyta (Durvillea antarctica) Chimera et al. (1995) Islands (S of feral pigs) ITokelau Islands: Fakaofo Cephalopoda (‘octopi’); Fish (‘eels’) Hyman (1999) I Peru (DO) Anomura (Emerita) J. P. Myers (pers. comm.) Red deer (Cervus N UK: Isle of Rum (DO) Phaeophyta (Pelvetia caniculata, Fucus serratus, Conradt (2000) elaphus) P:6 F. spiralis, F. vesiculosus; Laminaria spp.) Rhodophyta (Porphyra sp.) Mule (black-tailed) I Canada: Queen Chlorophyta (Ulva), Phaeophyta T. Gaston (pers. comm.), deer (Odocoileus Charlotte Islands (DO) (Nereocystis), and other algae J. P. Myers (pers. comm.), hemionus) P:4 E. A. Mills (pers. comm.) N USA: Alaska: Tsongas Algae D. Cline (pers. comm.) National Forest (DO) N USA: Alaska (southern) Phaeophyta (Alaria marginata) O’Clair & O’Clair (1998) N USA: Washington: Rhodophyta (intertidal) M. Herko (pers. comm.) San Juan Isl. Chlorophyta (Ulva) D. Padilla (pers. comm.) N USA: California: Chlorophyta? (Ulva?) J. T. Carlton (pers. obs.) Bodega Bay: Bodega Harbor (DO) Reindeer (Rangifer I South Georgia (ST) Seaweed Leader-Williams (1988) tarandus) P:1 Domestic goat I USA: Washington: Chlorophyta (Ulva sp.) D. Padilla (pers. comm.) (Capra hircus) Wadda Isl. (near Neah P:3 Bay) (DO of feral goats) I New Zealand: Auckland Phaeophyta (Macrocystis sp., Durvillea Chimera et al. (1995) Isl. (ST of feral goats) antarctica) Striped skunk N USA: Atlantic coast Forage at low tide on algae Amos (1966) Mountain goat N USA: Alaska: Tracy Arm (Fucus) in winter months N. Folsom (pers. comm.) (Oreamnos (South of Juneau) and Gla- americanus) P:1 cier Bay National Park (DO) Domestic sheep I Iceland (DO) Rhodophyta (Rhodymenia); Levring(1977) (Ovis aries) P:4 Phaeophyta (Alaria) I UK: Channel Islands: Phaeophyta (kelp) Jarvis (1998) Lihou (DO) I UK: Orkney Isl. Phaeophyta: (Laminariales; Fucus) Hall (1975) I USA: Maine islands (DO) Rhodophyta P. Conkling (pers. comm.)

America), of which 4 are unique (Andean rat, house Africa: chacma baboon, rabbit, blackbacked jackal, mouse, Pygmy rice rat, Peruvian desert fox). Together and brown hyena. these 3 regions account for 42% of the diversity of mar- For many other areas of the world, there are rela- itime mammals recorded here. tively few records, which we suggest below is due to The Eastern North Atlantic Ocean (Europe and Ice- underreporting. No records are in hand from South- land) has 7 records (3 unique: white shrew, badger, red east Asia, and there are few reports from the Western deer). There are 5 records from New Zealand and Aus- South Atlantic Ocean (the east coast of South America) tralia, of which 2 are unique (Tasmanian devil and and the (where, however, the in- false water rat). Four unique records come from South tertidal zone is minimal to non-existent). 280 Mar Ecol Prog Ser 256: 271–286, 2003

Table 2. Terrestrial mammals feeding in the intertidal zone: In only one instance is there a record (from Oregon) summary of ordinal and species diversity of an introduced mammal (pigs) preying upon intro- duced prey (the Atlantic clam Mya arenaria). Order No. of mammal species

Didelphimorphia 1 Dasyuromorphia 1 DISCUSSION Insectivora 2 Primates 1 Biogeography and diversity of maritime Lagomorpha 1 mammals: biases Rodentia 12 Carnivora 20 Artiodactyla 7 Data biases and limitations obviously attend this Total orders: 8 Total species: 45 global review of maritime mammals. The most over- whelming bias is a geographic one. Striking examples are now-cosmopolitan species such as the house mouse Mus musculus (which is likely a predator in Predator-prey diversity many regions of the world, but for which there is but one report in the Eastern South Pacific Ocean, Chile), Of those prey identifiable to the level of phylum or and the domestic rabbit Oryctolagus cuniculus (for lower (as opposed to prey only identified as ‘intertidal which only South African intertidal records are avail- organisms’), 228 different prey taxa are known to be able, but which likely invades the intertidal zone in consumed, representing 12 phyla of marine organisms many areas of the world). We suggest that the lack of (8 animal phyla, 3 protistan phyla [algae], and 1 plant reports of terrestrial mammal predation in intertidal phylum) (Table 3). Two-thirds of these taxa (67%, or 153 taxa) are bivalve and gastropod mollusks, crabs, and fish (we discuss below potential biases that have Table 3. Number of prey species consumed by maritime mammals entered into these taxa being recorded as dominant prey items). No. of No. of maritime Globally, no fewer than 26 maritime mammal species prey mammal predators prey on intertidal crabs, 15 mammals prey on algae, species consuming prey type 13 on bivalves, 12 on gastropods, and 11 on fish (Table 3). Eight maritime mammals consume only Porifera 2 1 Annelida plant or algal prey (mule deer, red deer, reindeer, goat, Polychaeta 5 4 mountain goat, sheep, rabbit, and the Beechey ground Echiura 1 1 squirrel); 28 maritime mammal species consume only Mollusca animal prey, and only 7 mammals are known to con- Bivalvia 30 13 sume both animal and plant prey (grass mouse, house Gastropoda 40 12 mouse, Norway rat, rice rat, coyote, Arctic fox, and Polyplacophora 4 2 Cephalopoda 1 1 black bear) (Table 1). The prey of 2 species (Keen’s mouse and Townsend’s vole) is as yet unknown. Crustacea Cirripedia 5 5 Mysidacea 1 2 Amphipoda 7 12 Non-indigenous predators and non-indigenous prey Isopoda 8 6 Caridea 2 2 Brachyura/Anomura 42 26 Introduced populations of 17 species of mammals Astacura 1 1 have been recorded as maritime predators (Table 1). Insecta 3 3 Fifteen of these species are recorded on islands where Echinodermata endemic mammals were absent or rare, making pre- Asteroidea 3 3 dation by introduced mammals perhaps more obvious. Echinoidea 4 5 In turn, 4 maritime mammals utilize, in part, non-na- Holothuroidea 3 2 tive prey. The false water rat in Australia, the raccoon in Urochordata Ascidiacea 2 1 California, and the mink in Maine all prey on intro- Fish 41 11 duced populations of the European shore crab Carcinus Algae 22 15 maenas. On the Pacific coast, raccoons prey upon the Seagrass 1 1 introduced Atlantic clam Mya arenaria and the intro- Total: 228 duced Japanese clam Venerupis philippinarum. Carlton & Hodder: Terrestrial mammals as intertidal predators 281

communities in many areas of the world — even those defined as food not directly or intentionally obtained well studied by marine ecologists — is not due to the alive by the predator. Secondary prey may be derived rarity of the phenomenon. Rather, we hypothesize from 4 sources: (1) Scavenging: consumers may eat that many observations around the world have simply regurgitated food or food dropped by other predators. not been reported, or remain recorded in obscure Black-backed jackals in Namibia feed on regurgi- places. tated fish dropped by cormorants (Avery et al. 1987) When there are reports, it is also clear that there are and also appear to feed on mussels Perna perna biases in the nature and quality of the data. Research dropped by gulls (Nel & Loutit 1986). The presence of biases or limited geographic data contribute strongly fish in the stomachs of Norway rats on the Queen to any sense of those mammals with the highest diver- Charlotte Islands may be the result of the rats eating sity of prey. Thus, while Norway rats appear to con- prey brought inland by bald eagles and other scav- sume more prey (66 taxa) than any other mammal, engers (Drever & Harestad 1998). (2) Kleptopara- these data are derived largely from only 3 locations sitism: Avery et al. (1987) speculate that the black- (Chile, Italy, and New Zealand). Similarly, data indi- backed jackals noted by Nel & Loutit (1986) may cating that house rats eat 16 different taxa are derived have actively stolen the clams from the gulls, rather almost entirely from Chile. Perhaps more realistic is than picking up remnants. Black-backed jackals are the prey diversity of raccoons (35 taxa), representing known to rob gulls of the clam Donax serrata, freshly observations along much of the Pacific coast of North dropped by gulls on hard surfaces such as rocks and America, and the prey diversity of mink (47 taxa), rep- roads (Hiscocks & Perrin 1987). (3) Consumption of resenting data from both the Pacific and Atlantic epibiota or endobiota (organisms living on or in the Oceans. target prey organism): Norway rats eating the inter- Furthermore, observations have largely been in the tidal black mussel Xenostrobus also consume the daytime — when hunting activity is likely to be at its mussel’s endocommensal pea crab Pinnotheres, as lowest for these crepuscular and nocturnal predators. well as organisms living on the mussel’s shell, such as Most observations are largely incidental to other stud- the barnacle Chamaesipho and the tiny gastropod ies, and these in turn are seasonally biased (much Eatoniella (Moors 1985). (4) Consumption of the intertidal work and observations being in the summer). prey’s stomach contents: mink in Scotland were There are 5 sources for prey data. These are: found to have amphipods in their stomach, but these (1) direct observation of prey consumption where the may have been derived, in turn, from the stomachs of identity of the prey is known; (2) direct observation ingested fish prey (Dunstone & Birks 1987). Mink in of predator foraging and live prey handling, without Spain were similarly found to have small mollusks in actual observation of specific prey ingested; (3) study their feces, but these appear to be the prey of the of stomach contents; (4) study of scat (fecal) material; intertidal fish upon which the mink had fed (Delibes and (5) analysis of the contents of middens, burrows, et al. 2003). and dens. Challenges and complexities are associated with each of these approaches, but particularly with the Why would terrestrial mammals utilize the intertidal indirect observations in the last 3 data sources. In the zone as an energy resource? absence of direct observation (Sources 1 and 2) it may not be possible to determine if prey were consumed There are at least 3 alternative scenarios — over a alive or scavenged. For example, black-backed jackal spectrum of spatial and temporal conditions — as to middens in Namibia contain fish and crabs, but it is not why terrestrial mammals would intentionally seek out possible to determine whether these organisms were and utilize resources in the intertidal zone. taken alive or scavenged dead (Avery et al. 1987). Rel- (1) Facultative omnivory: some mammal species may ative to scat contents, a comparison of scats and direct simply be opportunistic . Indeed, many re- observations of predation by black-backed jackals cords of single observations of predator episodes for revealed considerable differences: scats included in- many of the mammals shown in Table 1 may simply be vertebrate prey, whereas direct observations did not facultative omnivory. (2) Perennial trophic subsidies: (Hiscocks & Perrin 1987). Similarly, it is not possible to mammals that live in perennially impoverished near- determine via stomach contents whether ruminants coastal ecosystems may seek out the adjacent and are feeding on live attached algae or on drift algae potentially more productive marine ecosystem for washed ashore. food. In the arid deserts adjacent to the Gulf of Califor- The potential role of the consumption of secondar- nia, coyotes Canis latrans feed on a variety of marine ily derived food is a further challenge when using organisms, including sea turtles, marine mammals, indirect observations. Secondarily derived food is fish, birds, invertebrates, and algae (Rose & Polis 282 Mar Ecol Prog Ser 256: 271–286, 2003

1998). Dogs on impoverished Canton Atoll (Kiribati) tial to influence the abundance and distribution of learned to herd fish into shallow water (Degener & predator species)? Gillaspy 1955). (3) Seasonal trophic subsidies: mam- The lack of experimental data (discussed below as a mals that live in seasonally or periodically impover- future key direction in maritime mammal research) ished near-coastal ecosystems may also seek out inhibits any extensive conclusions on the role maritime adjacent productive marine resources. Numerous ex- mammals may play in regulating community structure. amples are available. Deer in Alaska come down to the We note that predators need not necessarily be abun- shore in winter to feed on intertidal algae (D. Cline dant to affect an impact on prey distribution and abun- pers. comm.; O’Clair & O’Clair 1998). Marine inverte- dance, as Frank (1982) has demonstrated relative to brate use increases in the winter in Arctic fox diets on oystercatcher predation on intertidal limpets, and as St. Lawrence Island in the Bering Sea (Fay & Stephen- Estes et al. (1998) have shown relative to killer whale son 1989). On islands off Baja California, the deer predation on sea otters. Wooton (1992) has suggested mouse Peromyscus maniculatus is a granivore in wet that raccoons preying on sea urchins (Strongylocentro- years, but feeds extensively on intertidal organisms in tus spp.) on the mainland coast of Washington ‘may dry years, as revealed by stable isotope analysis (Stapp have an impact upon sea urchins comparable to birds’. et al. 1999, Stapp 2002). On a British Columbia island, At these Washington sites gulls, black oystercatchers, Keen’s mice Peromyscus keeni appear to expand their and crows had important impacts on the abundance diet to marine invertebrates before seabird eggs and distribution of sea urchins in low intertidal com- become available, which is work also based on stable munities, effects which then cascaded down to indi- isotope analysis (Drever et al. 2000). Feral rabbits in rectly affecting both the abundance and diversity of South Africa are believed to feed on marine algae to macroalgae (Wooton 1992). survive dry summers (Moore 2002). The increase in The potentially most important impact of Norway rat fish predation in winter by mink in Scotland may be predation in the Chilean intertidal is on the size and the result of decreased availability of their rabbit prey abundance of keyhole limpets (Navarrete & Castilla (Dunstone & Birks 1987). Red fox, presumably in the 1993). Rats fed on the smaller and less abundant size state of Washington, foraged intertidally in the spring classes of 2 species of these limpets — potentially and summer (May to July), but then decreased inter- removing nearly 20% of the small limpets annually in tidal predation in August when terrestrial food (black- the region studied. Keyhole limpets (like sea urchins) berries) became available (Holmes 1992). Avery & may in turn control the abundance of algae (Navarrete Siegfried (1980) implied that a seasonal effect may also & Castilla 1993), and thus rat predation on limpets regulate, in part, Chacma baboon intertidal predation could have an important indirect impact on algal distri- in South Africa, noting that the baboons ‘are known bution and biomass. Mink in Spain (at a population to capture and consume marine shellfish and crus- density of 4 mink km–1) are estimated to consume taceans, especially when the protein content of their 3700 blennies and 1850 crabs km–1 of shoreline in normal terrestrial plant food is low’. The numerous August; a single mink may consume 110 to 147 g of fish reports (Table 1) of bears feeding intertidally in Alaska (26 to 35 ind.) and 65 to 139 g of crabs (10 to 22 ind.) and British Columbia may further reflect annual or (Delibes et al. 2003). In turn, there may be critical cas- periodic depression of their terrestrial food resources. cading impacts of the predator-mediated removal of Alternatively, it may be noted that for some preda- this number of fish and decapods on the blennies’ and tors, food hoarding may alleviate the need to forage crabs’ prey. intertidally. Red and Arctic foxes thus store prey, Where predation intensity by terrestrial mammals on particularly seabird carcasses, in the winter (Fay & the shore is consistent and high, maritime mammals Stephenson 1989, Sklepkovych & Montevecchi 1996), may further be able to set the upper intertidal limit of but storage of marine invertebrates as winter food certain prey. Sheep, deer, and goats feeding on upper resources has not yet been reported. shore algae may be important in this regard, and exclusion experiments are called for. Island algal populations that have sustained decades or centuries What are the ecological and evolutionary of feeding pressure by sheep (Moore 2002) would be of consequences of maritime mammal predation? particular interest in this regard. Data are in hand, however, on the importance of What evidence is there that terrestrial mammal pre- landward flow of energy from the sea to the land (Polis dation (1) influences the diversity, abundance or distri- & Hurd 1996a,b, Polis et al. 1997, Anderson & Polis bution of prey species (and thus has the potential to 1998, Huxel & McCann 1998, Rose & Polis 1998). Rose impact community structure), and (2) is important in & Polis (1998) demonstrated that in the arid deserts of the landward flow of energy (and thus has the poten- Baja California, coyote Canis latrans abundance along Carlton & Hodder: Terrestrial mammals as intertidal predators 283

the shore is 2.4 to 13.7 times higher than adjacent zone (Bonesi et al. 2000). Conradt (2000) found that inland areas, densities achieved (as noted above) by adult sons and daughters of red deer on the Isle of consumption of marine organisms. Scat mass was more Rum, Scotland, adopted their mother’s extent of feed- than double at coastal locations compared to inland ing on seaweed and thus learned to use the seaweed study sites, and nearly half of all items in coastal scats habitat early in life, suggesting the potential for were from the ocean. West (1987) found that Arctic fox specialization within the species. populations on the Aleutian Islands ‘appear to be buffered from starvation by the abundance and renew- able nature of coastal marine resources’. Stewart et al. Conclusion: Is terrestrial mammal predation in the (1989) suggested that the high densities and extended intertidal a rare phenomenon, a highly localized breeding season of masked shrews Sorex cinereus on a phenomenon, or common but overlooked Nova Scotia island were sustained by abundant littoral (and thus rarely studied)? prey, particularly amphipods and kelp flies. Thus in certain biomes — impoverished coastal land systems We posed at the beginning of this review 3 scenarios and islands, for example — the utilization of shore that could account for the lack of recognition and energy by predators may be critical in permitting the attention paid to the phenomenon of terrestrial mam- success of species in regions that would not otherwise mals visiting the shore: (1) Predation on marine organ- support large or viable populations of these mammals. isms by terrestrial mammals may be rare everywhere. The significance of introduced predators, or of intro- Our data suggest that this is not the case: maritime duced prey, in maritime mammal ecology largely re- mammals appear to be widespread globally, with often mains to be explored. Introduced mammals on islands repeated cases of predation being observed by the which previously had no mammals have added a new same mammal species; (2) Predation on marine organ- guild of intertidal predators to such regions. In certain isms by terrestrial mammals may occur only in certain regions introduced mammal populations that prey on localized regions, albeit perhaps common at such sites. the shore may have been enhanced by their general Our data suggest that this is also not the case, although proximity to urban areas. Agricultural practices may as we have discussed earlier, because of those pro- sustain relatively large populations of introduced do- cesses that could draw mammals to the shore, there mestic grazing animals (such as pigs, sheep, and goats) may be areas where this phenomenon is relatively in rural areas adjacent to intertidal shores. In general, more important, even if globally ubiquitous; (3) Preda- one largely unrecognized aspect of mammalian inva- tion on marine organisms by terrestrial mammals is sions may be their impact on marine intertidal commu- relatively common but largely underreported and nities. Such impact may have long preceded the arrival overlooked. We suggest that this conclusion — that of the first ecologists. For example Rattus exulans was predation by maritime mammals is a rarely studied brought to New Zealand ca. 1000 yr ago by Maoris and phenomenon rather than a rare phenomenon — bears R. norvegicus ca. 400 yr ago by Europeans (Moors careful consideration, based on the abundance of 1985), and thus may have been intertidal predators in observations across a wide variety of taxa (Table 1). these regions for centuries. In many areas of the world, What is now required, however, to determine the populations of marine animals preyed on by introduced importance of maritime mammal predation are 2 cate- mammals may have undergone modifications well be- gories of data: (1) quantitative observations on preda- fore any scientific studies were launched. tion, and (2) experimental studies. Field observations Ecological and evolutionary consequences of mari- and data collection could and should be facilitated by time mammal predation may include the potential for the use of modern technologies, including advanced intraspecific specialization. Individual Norway rats infrared night vision technology, radiotelemetry of preying in the Chilean intertidal zone show some individuals (Birks & Dunstone 1985, Millspaugh & degree of specialization (Navarrete & Castilla 1993). Marzluff 2001, Moore 2002), and the use of stable iso- Rats in Italy dig and dive for mollusks at low tide, sug- topes for trophic web analysis (Angerbjorn et al. 1994, gesting individual specialization has occurred here as Stapp et al. 1999, Drever et al. 2000, Stapp 2002). well (Parisi & Gandolfi 1974). Coastal mink diets in Experimental studies on maritime mammals (noted by Scotland may vary individually (perhaps partly as Navarrete & Castilla 1993 as an important challenge) mediated by individual home range), as well as by could be conducted by the use of large exclosures, or in gender (larger male mink prey more heavily on areas where the removal of introduced mammals is rabbits, whereas smaller females prey more heavily on proposed, such as on islands (Wood et al. 2002). Partic- fish and crustaceans) (Dunstone & Birks 1987). Mink in ularly worthy of experimental work would be maritime Spain use core (critical) areas within a home range, mammal populations for which some quantitative prey and in coastal regions such areas include the intertidal data already exist, such as the Norway rat populations 284 Mar Ecol Prog Ser 256: 271–286, 2003

in Chile and Arctic fox populations on certain Aleutian immigrations, fluctuations in numbers based mainly on Islands. Raccoon populations would also appear to be trading statistics. Medd Gronl 131:1–101 particularly amenable for experimental manipulative Britton JC, Morton B (1989) Shore ecology of the Gulf of Mexico. University of Texas Press, Austin studies. Locating comparable communities with and Brown AC, McLachlan A (1990) Ecology of sandy shores. without maritime mammal predators may provide Elsevier, Amsterdam further insight, such as nearshore islands without Campbell RR (1988) Status of the sea mink, Mustela raccoons facing a mainland with raccoons acting as macrodon, in Canada. Can Field Nat 102:304–306 Carefoot T (1977) Pacific seashores, a guide to intertidal eco- known maritime mammals. Lacking experimental logy. University of Washington Press, Seattle evidence, the scale of interactions — whether strong, Carlton JT, Geller JB, Reaka-Kudla ML, Norse EA (1999) weak, or insignificant — cannot be adequately assess- Historical extinctions in the sea. Annu Rev Ecol Syst 30: ed (Menge & Sutherland 1987). 515–538 We conclude by expanding upon the conclusions of Chimera C, Coleman MC, Parkes JP (1995) Diet of feral goats and feral pigs on Auckland Island, New Zealand. NZ J Stapp et al. (1999): the importance of intertidal re- Ecol 19:203–207 sources in supplying energy to terrestrial populations Churchfield S (1990) The natural history of shrews. of many species of mammals world wide may have Christopher Helm, London been underappreciated. Maritime mammals have Conkling PW (1999) Islands in time. A natural history and cul- tural history of the islands of the Gulf of Maine. Island been a largely overlooked guild of intertidal predators. 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Editorial responsibility: Otto Kinne (Editor), Submitted: January 13, 2003; Accepted: April 3, 2003 Oldendorf/Luhe, Germany Proofs received from author(s): June 18, 2003