Variable and complex food web structures revealed by exploring missing trophic links between birds and biofilm.
Food webs are comprised of a network of trophic interactions and are essential to elucidating ecosystem processes and functions. However, the presence of unknown, but critical networks hampers understanding of complex and dynamic food webs in nature. Here, we empirically demonstrate a missing link, both critical and variable, by revealing that direct predator-prey relationships between shorebirds and biofilm are widespread and mediated by multiple ecological and evolutionary determinants. Food source mixing models and energy budget estimates indicate that the strength of the missing linkage is dependent on predator traits (body mass and foraging action rate) and the environment that determines food density. Morphological analyses, showing that smaller bodied species possess more developed feeding apparatus to consume biofilm, suggest that the linkage is also phylogenetically dependent and affords a compelling re-interpretation of niche differentiation. We contend that exploring missing links is a necessity for revealing true network structure and dynamics.
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Tomohiro
T
Kuwae
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Eiichi
E
Miyoshi
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Shinya
S
Hosokawa
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Kazuhiko
K
Ichimi
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Jun
J
Hosoya
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Tatsuya
T
Amano
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Toshifumi
T
Moriya
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Michio
M
Kondoh
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Ronald C
RC
Ydenberg
Coastal and Estuarine Environment Research Group, Port and Airport Research Institute, 3-1-1, Nagase, Yokosuka 239-0826, JapanSeto Inland Sea Regional Research Center, Kagawa University, 4511-15, Kamano, Aji, Takamatsu 761-0130, JapanJapanese Bird Banding Association, 115, Konoyama, Abiko 270-1145, JapanConservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UKJapan Bird Research Association, 1-29-9, Sumiyoshi-cho, Fuchu 183-0034, JapanDepartment of Environmental Solution Technology, Ryukoku University, 1-5, Yokotani, Seta Oe-cho, Otsu 520-2194, JapanPRESTO, Japanese Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, JapanCentre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, CanadaPacific Wildlife Research Centre, Environment Canada, 5421 Robertson Road, Delta, British Columbia, V4K 3N2, Canada.
Robert W
RW
Elner
D000818:Animals; D001502:Beak / Q000033:anatomy & histology; D018441:Biofilms; D049628:Body Size; D046091:Charadriiformes / Q000145:classification / Q000502:physiology*; D004032:Diet; D004734:Energy Metabolism; D005247:Feeding Behavior; D020387:Food Chain; D007554:Isotopes / Q000737:chemistry; D008954:Models, Biological; D010802:Phylogeny; D011235:Predatory Behavior; D014059:Tongue / Q000033:anatomy & histology / Q000648:ultrastructure
D007554:Isotopes