Drymon, J. Marcus

Feldheim, K.

Fournier, A. M.V.

Jefferson, A. E.

Kroetz, A. M.

Powers, Sean P.

Seubert, E. A.

English

University of South Alabama Institutional Repository

University of South Alabama JagWorks@USA University Faculty and Staff Publications 2019 Tiger Sharks Eat Songbirds: Scavenging a Windfall of Nutrients From the Sky J. Marcus Drymon K. Feldheim A. M.V. Fournier E. A. Seubert A. E. Jefferson See next page for additional authors Follow this and additional works at: https://jagworks.southalabama.edu/usa_faculty_staff_pubs  Part of the Aquaculture and Fisheries Commons, Behavior and Ethology Commons, Biology Commons, Marine Biology Commons, Ornithology Commons, Other Animal Sciences Commons, Other Ecology and Evolutionary Biology Commons, Population Biology Commons, and the Terrestrial and Aquatic Ecology Commons Authors J. Marcus Drymon, K. Feldheim, A. M.V. Fournier, E. A. Seubert, A. E. Jefferson, A. M. Kroetz, and Sean P. Powers Tiger sharks eat songbirds:scavenging a windfall of nutrientsfrom the skyJ. M. DRYMON ,1,2,7 K. FELDHEIM,3A. M. V. FOURNIER ,1,4 E. A. SEUBERT,1A. E. JEFFERSON,1,2 A. M. KROETZ5, AND S. P. POWERS6Manuscript received 4 February 2019; revised 20 March2019; accepted 29 March 2019. Corresponding Editor: JohnPastor.1Coastal Research and Extension Center, Mississippi StateUniversity, 1815 Popps Ferry Road, Biloxi, Mississippi 39532USA.2Mississippi-Alabama Sea Grant, 703 East Beach Drive,Ocean Springs, Mississippi 39564 USA.3Field Museum, Pritzker Laboratory for MolecularSystematics and Evolution, 1400 South Lake Shore Drive,Chicago, Illinois 60605 USA.4Forbes Biological Station-Bellrose Waterfowl ResearchCenter, Illinois Natural History Survey, Prairie ResearchInstitute, University of Illinois at Urbana-Champaign, Havana,Illinois 62644 USA.5National Marine Fisheries Service, Southeast FisheriesScience Center, 3500 Delwood Beach Road, Panama CityBeach, Florida 32408 USA.6Department of Marine Sciences, University of SouthAlabama, 5871USADrive North,Mobile, Alabama 36688USA.7 E-mail: marcus.drymon@msstate.eduCitation: Drymon, J. M., K. Feldheim, A. M. V.Fournier, E. A. Seubert, A. E. Jefferson, A. M. Kroetz,and S. P. Powers. 2019. Tiger sharks eat songbirds: scav-enging a windfall of nutrients from the sky. Ecology100(9):e02728. 10.1002/ecy.2728Key words: DNA barcoding; feeding ecology; food webs;Galeocerdo cuvier; passerines; trophic interaction; trophic sub-sidy.Tiger sharks (Galeocerdo cuvier) are notorious fortheir dietary breadth. As predators, tiger sharks activelyhunt prey including crustaceans, fishes, sea snakes, seaturtles, sea birds, and marine mammals (Castro 2010),but as facultative scavengers, they also supplement theirdiet by opportunistically scavenging items such as whalecarcasses (Clua et al. 2013). Surprisingly, tiger sharksconsume terrestrial birds as well. While isolated andanecdotal accounts date back to the 1960s, we know lit-tle about the pervasiveness of, and mechanism behind,this unique trophic interaction.In 2010, while conducting a long-term shark popula-tion monitoring survey along the Mississippi–Alabamacoast, we captured a small tiger shark that regurgitatedfeathers prior to being tagged and released. We collectedthe feathers for further inspection; subsequent visualidentification and DNA barcoding revealed that thefeathers belonged to a Brown Thrasher, Toxostomarufum. During monthly surveys from 2010 to 2018, weopportunistically examined stomach contents from 105tiger sharks for the presence of whole birds and birdremains (feathers, beaks, feet) using gut content analysisfrom dead sharks and gastric lavage from live sharks(Fig. 1).Tiger-shark–bird interactions were pervasive andoccurred each year from 2010 to 2018 with the exceptionof 2014; none of the tiger sharks caught that year wereexamined for bird remains. Most of the interactions tookplace in the fall (September, October, and November),although some interactions took place during the spring(April and May). Of the 105 sharks examined, 41 (39%)contained bird remains. We archived all bird remains forvisual identification and DNA barcoding. These tech-niques facilitated conclusive identification of 11 bird spe-cies in 13 interactions: eight passerine songbirds (BarnSwallow, Hirundo rustica; Eastern Kingbird, Tyrannustyrannus; House Wren, Troglodytes aedon; Common Yel-lowthroat, Geothlypis trichas; Marsh Wren, Cistothoruspalustris; Eastern Meadowlark, Strunella magna; SwampSparrow, Melospiza georgiana; and Brown Thrasher);two near passerine land birds (White-winged Dove,Zenaida asiatica and Yellow-bellied Sapsucker, Sphyrapi-cus varius); and one waterbird (American Coot, Fulicaamericana). Counter to our expectations, no marinebirds were found in tiger shark stomachs.To explore a potential mechanism underpinning thepervasiveness of tiger shark encounters with terrestrialbirds, we used data from eBird, the world’s largest biodi-versity-related citizen science project (data availableonline).8 We queried bird sightings data from the Missis-sippi–Alabama coast for our 11 species of terrestrialbirds during spring and fall migration (Able 1972), theperiods corresponding to the trophic interactions. Peaksin coastal bird sightings for the 11 species we identifiedshowed remarkable alignment with individual tiger-shark–bird interactions (Fig. 2A), suggesting that tigershark consumption of these terrestrial birds is tied topredictable annual migrations rather than episodicevents. In the spring, areas along coastal Mississippi andAlabama are the first stopover location for migratorybirds flying north; in the fall, these same areas are thefinal stopover for southward-migrating birds prior to8 https://ebird.orgArticle e02728; page 1The Scientific NaturalistEcology, 100(9), 2019, e02728© 2019 by the Ecological Society of America 19399170, 2019, 9, Downloaded from https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecy.2728 by University Of South Alabama, Wiley Online Library on [26/10/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons LicenseFIG. 1. Acquiring stomach contents from a live tiger shark (gastric lavage) and examples of avian remains recovered during thisstudy. (Tiger shark gastric lavage photo by David Hay Jones).FIG. 2. (A) Species-specific relative abundance (number of eBird sightings) from the coasts of Mississippi and Alabama for the11 species of birds conclusively identified in tiger shark stomachs. Distributions in orange are during the spring migration (March,April, and May) and distributions in purple are from the fall migration (August, September, October, November). Vertical lines ineach plot mark the date the tiger sharks from the tiger-shark–bird interaction were captured. Note that house wrens were consumedby tiger sharks in two separate years and thus shown with respect to two different bird distributions. Similarly, two Yellow-belliedSapsuckers were consumed, but during the same year. (B) Monthly relative abundance for tiger sharks (tiger sharks100hooks1h1) from a shark population monitoring survey (2010–2018) along the Mississippi/Alabama coast. Error bars representstandard error of the mean.Article e02728; page 2 THE SCIENTIFIC NATURALIST Ecology, Vol. 100, No. 9 19399170, 2019, 9, Downloaded from https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecy.2728 by University Of South Alabama, Wiley Online Library on [26/10/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons Licensecrossing the Gulf of Mexico. We predicted that tigershark/bird interactions would occur primarily during thespring, when fatigued northward-migrating birds strug-gle to reach the Mississippi–Alabama coast followingtheir long journey across the Gulf of Mexico. Surpris-ingly, 11 of the 13 interactions we documented tookplace in the fall, during the initial portion of the birds’southward migration. In coastal Alabama, departuredecisions for southward-migrating birds are influencedby a combination of factors including energetic condi-tion, weather, and date. Specifically, once migratorybirds accumulate ample fat reserves, they strategicallytime their fall departure to coincide with favorable (i.e.,southward) winds following cold fronts, which are moreprevalent in late fall (after 24 September; Deppe et al.2015). However, following departure, unforeseenweather events can result in mass mortality (thousandsof birds per event; Newton 2007). These inclementweather events force migratory birds to the surface ofthe water, where (unlike waterbirds) they are unable torest and resume flight. We suggest that these weatherevents, while lethal for the birds, provide unique scaveng-ing opportunities for tiger sharks.Tiger sharks are capable of aligning their movementsand/or altering their foraging strategy to coincide withseasonal peaks in resource availability. For example,individual tiger sharks travel thousands of kilometers toremote Hawaiian atolls specifically to prey on seasonallyabundant fledgling Albatross (Phoebastria spp.) duringsummer months (Meyer et al. 2010). Additionally, offthe coast of Australia, tiger sharks rely on scavengingabundant green turtle (Chelonia mydas) carcasses astheir principle feeding strategy during the nesting season(Hammerschlag et al. 2016). The events we observed dif-fer from those in Hawaii and Australia in two primaryways. While the above-mentioned seasonal peaks inAlbatross and green turtle are spatially concentrated,weather-impacted migratory birds are a spatially diffuseresource. Despite this, the frequency of tiger-shark–birdinteractions reflects the sheer magnitude of seasonalbird migrations across the Gulf of Mexico (in excess of2 billion birds per season; Horton et al. 2019). In addi-tion, this seasonal pulse of nutrients benefits a particularportion of the tiger shark population. Our findingsdemonstrate that the timing of the fall migration formany North American birds coincides with annualpeaks in the relative abundance of neonate (i.e., new-born) tiger sharks in the north-central Gulf of Mexico(Fig. 2B). Of the 41 accounts of birds in tiger sharkstomachs, nearly one-half (46%) involved consumptionby neonates. At birth, neonate tiger sharks are a fraction(<20%) of their mature size (Branstetter 1990), and theylikely have very low predatory efficiency (Driggers et al.2008). For these neonates, scavenging on easily accessi-ble and seasonally predictable pulses of terrestrial birdsmay be a way to optimize foraging success before adulthunting strategies are learned. Spanish Imperial Eagles,Aquila adalberti also use scavenging as an efficientmeans of acquiring food during the first year of life(Margalida et al. 2017).Marine and terrestrial food webs are complex andcoupled systems (Polis and Strong 1996), often subsi-dized by internal (autochthonous origin) or external (al-lochthonous origin) resources (Nowlin et al. 2008). Forexample, seabirds indirectly (through guano) anddirectly (through carrion) transfer energy between mar-ine and terrestrial systems, inciting numerical responsesacross a range of species from arthropods (Polis andHurd 1996) to carnivorous mammals (Rose and Polis1998). Similarly, our findings suggest a predictable trans-fer of avian-derived nutrients, yet the direction of energyexchange is reversed (i.e., terrestrial to marine). Becausethese birds are disproportionately consumed by neo-nates, the nutrients they contain may influence thedynamics of tiger shark populations. Unlike many sharkspecies, tiger sharks do not use discrete areas as nurs-eries; rather, female tiger sharks may select areas of highlocalized primary productivity for parturition of theiryoung (Driggers et al. 2008). For these facultative scav-engers, a windfall of nutrients from the sky may explainthe elevated occurrence of neonate tiger sharks in thenorthern Gulf of Mexico.ACKNOWLEDGMENTSSpecial thanks to Neil Hammerschlag and Frank Moore fortheir insights into the spatial ecology of, and interactionsbetween, tiger sharks and migratory birds.LITERATURE CITEDAble, K. 1972. Fall migration in coastal Louisiana and the evo-lution of migration patterns in the Gulf region. WilsonBulletin 84:231–242.Branstetter, S. 1990. Early life history implications of selectedcarcharhinoid and lamnoid sharks of the northwest Atlantic.Pages 17–28 in H. L. Pratt, S. H. Gruber, and T. Taniuchi,editors. Elasmobranchs as living resources: advances in thebiology, ecology, systematics, and the status of the fisheries.NOAA Technical Report NMFS 90. U.S. Department ofCommerce, Washington, D.C., USA.Castro, J. I. 2010. The sharks of North America. Oxford Univer-sity Press, New York, NY, USA.Clua, E., C. Chauvet, T. Read, J. M. Werry, and S. Lee. 2013.Behavioural patterns of a tiger shark (Galeocerdo cuvier) feed-ing aggregation at a blue whale carcass in Prony Bay, NewCaledonia. Marine and Freshwater Behaviour and Physiology46:1–20.Deppe, J. L., et al. 2015. Fat, weather, and date affect migratorysongbirds’ departure decisions, routes, and time it takes tocross the Gulf of Mexico. Proceedings of the National Acad-emy of Sciences USA 112:E6331–E6338.Driggers III, W. B., G. W. Ingram Jr., M. A. Grace, C. T. Gled-hill, T. A. Henwood, C. N. Horton, and C. M. Jones. 2008.Pupping areas and mortality rates of young tiger sharks Gale-ocerdo cuvier in the western North Atlantic Ocean. AquaticBiology 2:161–170.August 2019 THE SCIENTIFIC NATURALIST Article e02728; page 3 19399170, 2019, 9, Downloaded from https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecy.2728 by University Of South Alabama, Wiley Online Library on [26/10/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons LicenseHammerschlag, N., I. Bell, R. Fitzpatrick, A. J. Gallagher, L.A. Hawkes, M. G. Meekan, J. D. Stevens, M. Thums, M. J.Witt, and A. Barnett. 2016. Behavioral evidence suggests fac-ultative scavenging by a marine apex predator during a foodpulse. Behavioral Ecology and Sociobiology 70:1777–1788.Horton, K. G., B. M. Van Doren, F. A. La Sorte, E. B. Cohen,H. L. Clipp, J. J. Buler, D. Fink, J. F. Kelly, and A. Farns-worth. 2019. Holding steady: little change in the intensity ortiming of bird migration over the Gulf of Mexico. 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Tiger Sharks Eat Songbirds: Scavenging a Windfall of Nutrients From the Sky

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Tiger Sharks Eat Songbirds: Scavenging a Windfall of Nutrients From the Sky

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