Foraging over Sargassum by Western North atlantic seabirds.
Abstract: Drifting reefs of Sargassum (a brown alga) are used by a variety of pelagic seabirds in the western Atlantic Ocean. We examined gut contents from 964 individuals of 39 seabird species collected 5 to 60 km off the coast of North Carolina for evidence of Sargassum use. Sargassum pieces or Sargassum-associated prey were found in nine of 10 Procellariiformes species and less frequently among Charadriiformes (12 of 25 species). No Sargassum-associated prey was found in Pelecaniformes examined, hut observational data indicated that Atlantic tropicbirds (Phaethon lepturus and P. aethereus) and Masked Boobies (Sula dactylatra) commonly foraged over Sargassum. Four species were considered Sargassum specialists, having frequencies of occurrence >25% and high volumes of Sargassum-associated prey: Audubon's Shearwater (Puffinus lherminieri), Royal Tern (Thalasseus maximus), Bridled Tern (Onychoprion anaethetus), and Red-necked Phalarope (Phalaropus lobatus). Seven species fed in Sargassum to a lesser extent, and nine species had ingested Sargassum pieces, but contained no Sargassum-associated prey. It is likely that other seabird species forage regularly over Sargassum, as our conclusions are based on relatively small sample sizes taken during random sampling in the open ocean. Our conservative analysis and extensive observational data indicate the Sargassum community is critical for feeding for some western North Atlantic seabirds. Degradation of Sargassum habitats by oil development, harvest, and/ or ocean acidification would undoubtedly have negative effects on fitness of these birds.
Article Type: Report
Subject: Foraging (Research)
Sea birds (Behavior)
Sea birds (Environmental aspects)
Plant-animal interactions (Environmental aspects)
Plant-animal interactions (Psychological aspects)
Authors: Moser, Mary L.
Lee, David S.
Pub Date: 03/01/2012
Publication: Name: The Wilson Journal of Ornithology Publisher: Wilson Ornithological Society Audience: Academic Format: Magazine/Journal Subject: Biological sciences Copyright: COPYRIGHT 2012 Wilson Ornithological Society ISSN: 1559-4491
Issue: Date: March, 2012 Source Volume: 124 Source Issue: 1
Topic: Event Code: 310 Science & research
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 285207243
Full Text: Consolidated reefs of floating pelagic brown algae of the genus Sargassum are important and recurring features of tropical and sub-tropical marine environments. Holopelagic S. natans and S. fluitans support a diverse and abundant fish and invertebrate fauna in the western Atlantic Ocean (Fine 1970, Settle 1993, Casazza and Ross 2008). Recent remote sensing data indicates Sargassum reefs originate in the northwestern Gulf of Mexico in June each year and are advected into the western Atlantic in early summer by the Loop Current, moving northward with the Gulf Stream (Gower and King 2011). The floating weed moves to the south and west in fall and winter, becoming less buoyant with age. The circulation of Sargassum is consistent among years and is driven by predictable currents and trade winds (Gower and King 2011).

Floating Sargassum can be extensive, yet ephemeral habitat for seabirds. Airborne imagery indicated that drift lines of the algae extend for continuous lengths of at least 5 km and primarily consist of 20-80 [m.sup.2] reefs of Sargassum (Marmorino et al. 2011). Satellite images indicate Sargassum slicks can be even larger, ranging from 100 to 1,000 m in width and up to hundreds of kilometers in length (Gower et al. 2006). However, consolidated drift lines of Sargassum off the coast of Florida start to disintegrate as wind speeds exceed 5 m/sec (Marmorino et al. 2011). The amount of pelagic Sargassum in the North Atlantic was estimated at 0.54 metric tons/ [km.sup.2] in the Gulf Stream and 0.02 metric tons/[km.sup.2] over the Continental Shelf, for a combined standing crop of >50,000 metric tons off the Carolinas (Howard and Menzies 1969). Gower and King (2011) estimated the wet weight of Sargassum in the Atlantic has regularly exceeded 1.8 million metric tons during the past decade and that even greater amounts can occur in the Gulf of Mexico. Thus, Sargassum reefs are important feeding stations and possible roosting sites for pelagic seabirds (Haney 1986).

Studies to date have used observations of seabird behavior around Sargassum reefs to reach conclusions about why seabirds are attracted to this habitat (Haney 1985, 1986). We examined the gut contents of 39 species of pelagic seabirds for evidence of foraging over Sargassum. Percent frequency of occurrence, numerical abundance, and volume of Sargassum-associated prey were used to ascertain the relative extent of Sargassum foraging exhibited by the species sampled. These data were supported by extensive visual observation of marine birds feeding in pelagic habitats off the coast of North Carolina. Our objectives were to: (1) identify seabird species that rely most heavily on pelagic Sargassum for feeding, and (2) document prey items most frequently targeted by these birds.

METHODS

Gut content analysis from 964 individual seabirds of 39 species collected 5 to 60 km off the North Carolina coast was conducted as described in Moser and Lee (1992). In addition, visual observations of seabird foraging were made from a vessel during 231 day trips (averaging 1,201 seabird observations and 25.2 species/trip). Birds were collected during all seasons between 1975 and 1989, although fewer sampling and observation trips were made in winter. Observations and collections occurred over a wide geographic area in an attempt to census inshore coastal waters, the inner and outer Continental Shelf, and deeper waters over the Shelf's edge. Lee and Socii (1998) mapped the areas surveyed by month.

Documentation of Sargassum use was not the original focus of seabird collections or observations. The birds used in this study were collected opportunistically during their entire period of occurrence in North Carolina waters to obtain data on heavy metal accumulation, plastic ingestion, age and sex ratios, body temperature, parasite load, molt sequence, behavior, and ecology (e.g., Moser and Lee 1992, Lee 1995, Lee and Haney 1996). Foraging flocks quickly dispersed when approached by our survey boats and birds foraging over Sargassum were not targeted, nor were they particularly easier to collect. Sargassum is typically found in the vicinity of the outer Continental Shelf along the western wall of the Gulf Stream and, to a lesser extent, in wind rows within the Stream. Only 40% of the surveys were near the Shelf edge where Sargassum typically occurs, and the alga was frequently not in the immediate vicinity of our survey sites.

Contents from the stomach and gizzard of each bird were combined, and birds with empty upper digestive tracts were excluded from the analysis. Percent frequency of occurrence of Sargassum (leaves or bladders) and Sargassum-associated fauna was calculated for each seabird species (number of birds with prey 'A' divided by the total number of birds x 100). Sargassum associates were defined as those species (fish, crustaceans, and gastropods) that reside in Sargassum during the life history phase when ingested (following Dooley 1972, Settle 1993). Unidentifiable prey items were assumed not to be Sargassum associates, and the mean percent volume of Sargassum-associated prey in the digestive tract was used as a direct measure of the relative importance of Sargassum for foraging within species. Thus, our estimates of Sargassum use are conservative.

RESULTS

Gut contents of birds from three Orders, five families, 16 genera, and 39 species were analyzed. Twenty-one species (53.8%) had ingested Sargassum pieces or Sargassum-associated prey (Table 1). Birds were classified as Sargassum specialists (species that had >25% occurrence of Sargassum-associated prey), Sargassum users (those with up to 25% occurrence of Sargassum or associated prey), and Sargassum incidentals (species that contained only pieces of Sargassum and no associated prey). We regarded the presence of alga in digestive tracts as evidence of foraging associated with pelagic Sargassum. Its presence among gut contents that lacked any identifiable Sargassum-associated prey was probably a result of the bird's inability to rapidly digest the alga.

Evidence of Sargassum foraging was found in most Procellariiformes (9 of 10 species) and less frequently in Charadriiformes (12 of 25 species). It is possible that Sooty Tern (Onychoprion fuscatus) could be added to the species that use Sargassum, as four of 11 birds sampled contained flying fish (Exocoetidae). There was equivocal evidence from digestive tract analysis for Sargassum use by two of the four Pelecaniformes. Relatively few individuals of these species were collected. Our extensive visual observations of the pelagic members of this family indicated they forage over algal mats. Moreover, two of five White-tailed Tropicbirds (Phaethon lepturus) and two of three Red-billed Tropicbirds (P. aethereus) ingested flying fish.

Species that had no Sargassum or identifiable Sargassum-associated prey in their digestive tracts included: Band-rumped Storm-Petrel (Oceanodroma castro, n = 12), White-tailed Tropicbird (n = 5), Red-billed Tropicbird (n = 3), Northern Gannet (Morus bassanus, n = 5), Double-crested Cormorant (Phalacrocorax auritus, n = 1), Parasitic Jaeger (Stercorarius parasiticus, n = 4), Great Skua (S. skua, n = 1), Great Black-backed Gull (Larus marinus, n = 1), Herring Gull (L argentatus, n = 2), Ring-billed Gull (L. delawarensis, n = 2), Arctic Tern (Sterna paradisaea, n = 2), Caspian Tern (Hydroprogne caspia, n = 2), Forster's Tern (S. forsteri, n = 3), Gull-billed Tern (Gelochelidon nilotica, n = 3), Least Tern (Sternula antillarum, n = 1), Sandwich Tern (Thalasseus sandvicensis, n = 8), Sooty Tern (n =- 11), and Brown Noddy (Anous stolidus, n = 2).

Four species of seabirds had frequencies of Sargassum-associated prey >25% and were considered Sargassum specialists (Table 1). The single Sabine's Gull (Xema sabini) sampled contained a seahorse (Hippocampus sp.), which is a Sargassum dweller. These gulls were observed following Sargassum drift lines during migration but, sample size did not support including this gull in the Sargassum specialists category. The four specialists contained almost exclusively Sargassum-associated prey, as evidenced by high volumes of identifiable prey items in their digestive tracts (Table 2). Sargassum users, birds that contained Sargassum prey less frequently (7 species), also contained high volumes of Sargassum-associated prey.

Most birds feeding in Sargassum contained small Sargassum-associated fishes (Table 2). The only exceptions were the two species of phalaropes, which had consumed Sargassum shrimp (Latreutes fucorum) and the Sargassum-associated gastropod, Litiopa melanostoma. This gastropod was also found in Cory's Shearwaters (Calonectris diomedea). Specialists fed on a minimum of seven Sargassum-associated fish species, and most measurable fish prey were <50 mm standard length (Table 2). However, Royal Terns (Thalasseus maximus) generally consumed slightly larger fish (range = 40105 mm) than the other birds we examined (range = 6-75 mm). Filefish (Monacanthus sp.) occurred with the highest frequency in Audubon's Sheari waters (Puffinus lherminieri), Bridled Terns (Onychoprion anaethetus), and Royal Terns, but numerical abundance of filefish was highest only in Audubon's Shearwaters and Royal Terns (Fig. 1A, C). The mean number of filefish per bird was five. Bridled Terns (Fig. 1B) had the highest number of tetradontids (mean number of puffers/bird = 6) and also consumed large numbers of ostraciids (mean number of trunkfish/bird = 4).

DISCUSSION

Gut content analysis identified four Sargassum specialists, while visual observations indicated that several additional species target this habitat for feeding. Audubon's Shearwater, Royal Tern, Bridled Tern, and Red-necked Phalarope (Phalaropus lobatus) contained relatively high levels of Sargassum-associated prey. The single Sabine's Gull examined contained a Sargassum-associated prey item and this species was observed to follow Sargassum drift lines. Visual observations indicated Bridled Terns regularly associated with Sargassum patches and tended to use the mats and associated flotsam as roosting sites (Duncan and Harvard 1980, Haney 1986). Our observational data also indicated that Masked Boobies (Sula dactylatra) and the two species of tropicbirds target Sargassum patches while feeding as also reported by Haney et al. (1999).

Diet analysis underestimated prey from Sargassum habitat and excluded some seabird species. For example, the digestive tracts of Bridled Terns in our study contained insects of terrestrial origin, which we did not consider to be Sargassum associates (5 consumed Lepidoptera, 6 ate Coleoptera, 2 ate Hymenoptera, and 6 contained unidentified insects). Haney et al. (1999) reported insects were the second most common food item in Bridled Terns. These insects may have been resting on Sargassum mats when ingested. We commonly observed both species of Atlantic tropicbirds feeding around Sargassum reefs. Flying fish were recovered from their digestive tracts, but this was not direct evidence of Sargassum use, as flying fish regularly occur where Sargassum is absent (Casazza and Ross 2008). We observed tropicbirds as they plunged near and sometimes under the Sargassum. The same was true of Masked Boobies, a species seen infrequently off the Carolinas but usually in association with Sargassum.

Some seabird species may not feed directly over Sargassum, but the alga is critical habitat for certain life stages of their fish prey. For example, flying fish can represent >50% of the total diet of the two tropicbirds collected off North Carolina (Lee et al. 1981, Lee and Irvin 1983) and flying fish are important prey in other parts of their range (Lee and Walsh-McGehee 1998). Flying fish use Sargassum for spawning and rearing, and Sargassum is essential habitat for these and other fish species (Casazza and Ross 2008). Thus, Sargassum contributes indirectly to the fitness of tropicbirds and other seabirds, notably Sooty Terns and Masked Boobies.

Sargassum specialists used a variety of foraging modes, including surface-seizing, plunging (aerial diving), pursuit plunging/diving, pattering, and dipping (following Ashmole 1971). We observed Audubon's Shearwater feeding near the surface, either by shallow diving (1-2 m), surface-seizing, or hydroplaning in and around Sargassum reefs. However, in the Bahamas, this shearwater feeds by pursuit diving during the nesting season with dives averaging 7.6 m (n = 136) to a maximum of 29 m (Mackin 2004). Phalaropes, which prey on aquatic invertebrates in shallow pools in the tundra by surface feeding (Haney 1985), use the same behavior when seizing snails and crustaceans from Sargassum mats. The spinning behavior associated with phalarope feeding in freshwater habitats (Obst et al. 1996) was not observed at sea. Sargassum-associated prey taken by small seabirds were rarely >50 mm, indicating these birds picked prey from within the alga, as opposed to diving beneath it where larger fish are typically found (Moser et al. 1998). An advantage of foraging in Sargassum reefs is that piscivorous predators drive prey up into the Sargassum mats, where it is more accessible to the smaller-bodied seabirds (Safina and Burger 1985, Haney 1986).

Prey types in digestive tracts provided additional information about seabird feeding. Both frequency of occurrence and numerical abundance of fish prey in Bridled Terns indicated they select relatively uncommon members of the Sargassum fish fauna: tetradontids (puffers), ostraciids (trunkfishes), stromateids (driftfish), and priacanthids (bigeyes) (Dooley 1972, Settle 1993). However, these fishes may occur at the periphery of Sargassum patches, where they are less frequently collected during Sargassum sampling with nets (Casazza and Ross 2008). In contrast, Royal Terns, Audubon's Shearwaters, and Red Phalaropes fed on prey that are dominant members of the Sargassum community: filefishes, jacks, and Sargassum shrimp (Fine 1970, Dooley 1972, Settle 1993, Casazza and Ross 2008). Haney (1986) found a significant relationship between bird body size and Sargassum patch size. We noted that large-bodied Royal Terns contained relatively large prey; but this was likely a function of their feeding mode (plunging) rather than Sargassum patch size.

Sargassum foraging was documented during all months of the year despite the Sargassum mat structure and attendant fish community changing seasonally and in response to weather (Moser et al. 1998, Casazza and Ross 2008, Gower and King 2011). Fine (1970) noted that faunal composition in Sargassum collected from the Gulf Stream and Sargasso Sea was similar, but that non-colonial macrofauna were more abundant in spring than in fall. This may affect the way seabirds use Sargassum habitat. Royal Terns commute daily from Outer Banks nesting colonies to forage in Sargassum mats along the edge of the outer continental shelf, a round trip of up to 160 km or more (DSL, unpubl, data). Common (Sterna hirundo) and Black (Chlidonias niger) terns, and Sabine's Gulls seasonally migrate north and south, and likely use rows of Sargassum along the western edge of the Gulf Stream and drift lines within the Stream to both orient and feed.

[FIGURE 1 OMITTED]

Reduction in the Sargassum community would have negative effects on a number of western North Atlantic seabirds, based on digestive tract analysis and at-sea observations, including five tropical species considered to be of conservation concern (Schreiber 2000). Observations of Bermuda Petrels (Pterodroma cahow) and Roseate Terns (Sterna dougallii) indicated these Endangered Species also use Sargassum to forage. Sargassum use by seabirds in the Pacific and Indian oceans is unknown, but it is likely that many of the same species and their ecological counterparts exploit Sargassum reefs in those oceans as well. Commercial harvest threatens to reduce the standing crop of Sargassum in the western North Atlantic (Settle 1997), and there are possible negative impacts to Sargassum from oil and gas exploration on the outer Continental Shelf off the coast of North Carolina (Lee 1999). Seabird surveys in the Gulf of Mexico shortly after the Deepwater Horizon oil spill (April 2010) indicated Sargassum habitat was damaged by this event (J. C. Haney and DSL, unpubl, data). Global climate change and attendant ocean acidification may also affect Sargassum (Porzio et al. 2011). Significant reduction in the amount or quality of Sargassum habitat could reduce seabird abundance, influence marine distribution, alter seasonal movements, and/or jeopardize the birds' physiological condition.

ACKNOWLEDGMENTS

We thank S. W. Ross for help with fish identification and for reviewing an early version of this manuscript. H. J. Porter aided in gastropod identification. J. M. Butzerin, T. P. Good, J. C. Haney, W. A. Mackin, R. L. Pitman, and an anonymous reviewer provided helpful reviews of this manuscript. Funding for this study was provided in part by the National Marine Fisheries Service, U.S. Fish and Wildlife Service, U.S. Army Corps of Engineers, and U.S. Department of the Navy.

Received 22 March 2011. Accepted 7 October 2011.

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MARY L. MOSER (1, 2, 4) AND DAVID S. LEE (3)

(1) Zoology Department, North Carolina State University, Raleigh, NC 27695, USA.

(2) Current address: Northwest Fisheries Science Center, National Marine Fisheries Service, 2725 Montlake Boulevard East, Seattle, WA 98112, USA.

(3) The Tortoise Reserve, P. O. Box 7082, White Lake, NC 28336, USA.

(4) Corresponding author; e-mail: mary.moser@noaa.gov
TABLE 1. Frequency of occurrence (%) of Sargassum and
Sargassum-associated prey in western North Atlantic seabirds. Species
having >25% occurrence of Sargassum-associated prey were considered
Sargassum specialists; those with <25% associated prey were classified
as Sargassum users, and species that contained only pieces of
Sargassum were Sargassum incidentals. Mean percent volume of fish prey
is in parenthesis. Primary season of occurrence of seabirds off North
Carolina from Lee (1986, 1995).

                                                         Sargassum

                           Primary season
Species                    of occurrence       n       Prey   Pieces

Sargassum specialists
  Audubon's Shearwater     late Apr-Nov        100      59.0    15.0
  Puffinus lherminieri
  Red-necked Phalarope     mid Apr-early        37      62.2    16.2
  Phalaropus lobatus       Jun; mid Jul-Oct
  Royal Tern Thalasseus    mid Mar-late Oct     20      40.0       0
  maximus
  Bridled Tern             mid May-mid Oct      58      31.0       0
  Onychoprion anaethetus   Mar-May; Sep-Oct      1     100.0       0
  Sabine's Gull Xema
  sabini

Sargassum users
  Great Shearwater         mid Mar-mid Nov      50      48.0    44.0
  Puffinus gravis
  Cory's Shearwater        mid May-mid Nov     136      30.1    26.0
  Calonectris diomedea
  Manx Shearwater          mid Oct-mid Jun      13      23.1    15.4
  Puffinus puffinus
  Red Phalarope            mid Oct-Apr          92      10.9     1.1
  Phalaropus fulicarius
  Laughing Gull            year round           11      54.5    54.5
  Leucophaeus atricilla
  Bonaparte's Gull         Sep-Mar              31      16.1     6.4
  Chroicocephalus
  philidelphia
  Common Tern Sterna       Apr-Sep             43       18.6     7.0
  hirundo

Sargassum incidentals
  Sooty Shearwater         late May-early        5      40.0    40.0
  Pufnus griseus           Jun
  Black-capped Petrel      year round           55      16.4    16.4
  Pterodroma hasitata
  Leach's Storm-Petrel     mid May-early         8      12.5    12.5
  Oceanodroma leucorhoa    Jun; mid
                           Sep-early Nov
  Wilson's Storm-Petrel    mid Apr-early       122       3.3     3.3
  Oceanites oceanicus      Sep
  Northern Fulmar          late Oct-Apr         32       3.1     3.1
  Fulmarus glacialis
  Long-tailed Jaeger       mid Sep-mid          13      15.3    15.3
  Stercorarius             Oct; May
  longicaudus
  Pomarine Jaeger S.       late Mar-Jun;        33      15.1    15.1
  pomarinus                late Oct-early
                           Nov
  Black Tern Chlidonias    late Apr-early        6      16.7    16.7
  niger                    May; mid
                           Jul-mid Sep
  Black-legged Kittiwake   early Nov-Mar        30      20.0    20.0
  Rissa tridactyla

Species                    Fish            Crustacean   Gastropod

Sargassum specialists
  Audubon's Shearwater      48.0 (89.2)         0            0
  Puffinus lherminieri
  Red-necked Phalarope         0                0         45.9
  Phalaropus lobatus
  Royal Tern Thalasseus     40.0 (91.0)         0            0
  maximus
  Bridled Tern              31.0 (79.0)         0            0
  Onychoprion anaethetus   100.0 (100.0)        0            0
  Sabine's Gull Xema
  sabini

Sargassum users
  Great Shearwater           2.0 (100.0)        0          2.0
  Puffinus gravis
  Cory's Shearwater          0.7 (50.0)         0          2.9
  Calonectris diomedea
  Manx Shearwater            7.7 (100.0)        0            0
  Puffinus puffinus
  Red Phalarope                0              7.6          2.2
  Phalaropus fulicarius
  Laughing Gull             18.2 (100.0)     18.2            0
  Leucophaeus atricilla
  Bonaparte's Gull           9.7 (98.3)         0            0
  Chroicocephalus
  philidelphia
  Common Tern Sterna        11.6 (80.0)         0            0
  hirundo

Sargassum incidentals
  Sooty Shearwater
  Pufnus griseus
  Black-capped Petrel
  Pterodroma hasitata
  Leach's Storm-Petrel
  Oceanodroma leucorhoa

  Wilson's Storm-Petrel
  Oceanites oceanicus
  Northern Fulmar
  Fulmarus glacialis
  Long-tailed Jaeger
  Stercorarius
  longicaudus
  Pomarine Jaeger S.
  pomarinus

  Black Tern Chlidonias
  niger

  Black-legged Kittiwake
  Rissa tridactyla

TABLE 2. Frequency of occurrence (%) and size range
(standard length in mm) of individual fish taxa ingested by
three Sargassum specialists: Audubon's Shearwater (n = 48),
Bridled Terns (n = 16), and Royal Terns (n = 8).

                            Frequency of occurrence (%) and size range
                                            (mm)

                            Audubon's
                            Shearwater     Bridled Tern   Royal Tern

Exocoetidae (flying fish)    6.2 (40-60)    6.2 (30)         0
Syngnathidae (pipefish)        0            6.2 (23)         0
Priacanthus sp. (bigeye)     4.2 (15)      12.5 (20)         0
Heteropriacanthus            2.1 (45)         0              0
cruentatus (glasseye)
Caranx sp. (jack)           14.6 (45-50)      0           12.5 (70)
C. hippos (crevalle jack)    2.1 (25)         0              0
Decapterus sp. (scad)        4.2            6.2              0
Trachurus lathami            2.1 (75)         0              0
(rough scad)
Stromateidae (butterfish)    4.2 (15)      12.5 (30-40)   12.5
Psenes sp. (driftfish)         0              0           12.5 (70-105)
Balistidae (triggerfish)     8.3 (15-20)   25.0 (20)         0
Aluterus sp. (filefish)     12.5 (40)         0           12.5 (40)
Monacanthus sp.             68.8 (15-50)   31.2 (10-22)   62.5 (40)
(filefish)
Monacanthus ciliatus         2.1 (25)         0              0
(fringed filefish)
Stephanolepis hispidus       2.1 (30-52)      0           12.5 (45)
(planehead filefish)
Lactophrys sp.                 0           12.5 (6-10)       0
(trunkfish)
Chilomycterus sp.              0              0           12.5
(burrfish)
Sphoeroides sp. (puffer)     2.1 (7-12)    18.7 (10-20)      0
S. maculatus                   0            6.2 (10-12)      0
(northern puffer)
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