Artificial irrigation ponds and sea coast as foraging habitat for larids breeding in protected wetlands
Esther Sebastián-González A B E , Francisco Botella A , Otso Ovaskainen C , Antonio Delgado D and José Antonio Sánchez-Zapata A
+ Author Affiliations
- Author Affiliations
A Department of Applied Biology, Miguel Hernández University, Avenida de la Universidad s/n, E-03202, Elche, Spain.
B Departamento de Ecologia, Universidade de São Paulo (IB-USP), Rua do Matão 321, Cidade Universitária, CEP 05508-900 São Paulo, Brazil.
C Department of Biosciences, University of Helsinki, PO Box 65 (Viikinkaari 1), FI-00014 The University of Helsinki, Finland.
D Instituto Andaluz de Ciencias de la Tierra (CSIC-UGR), E-18100 Armilla, Granada, Spain.
E Corresponding author. Present address: Biology Department, University of Hawaii, 200 W. Kawili Street, Hilo, HI 96720, USA. Email: esebgo@gmail.com
Marine and Freshwater Research 66(9) 831-840 https://doi.org/10.1071/MF14145
Submitted: 20 February 2014 Accepted: 20 September 2014 Published: 19 March 2015
Abstract
Questions related to the preservation of foraging sites of breeding birds have received little attention, although they can be of major importance for population persistence. Here, we used stable isotopes and field observations to evaluate the relative importance of man-made irrigation ponds as foraging areas for a larid community of conservation concern. We also studied the habitat preferences of the bird species and determined whether pairs of species co-occurred or avoided each other while foraging. Six species used marine habitats preferentially, whereas three species preferred freshwater habitats, the latter being provided mainly by irrigation ponds. Larids foraged preferentially in large and vegetated ponds located close to the breeding areas, and avoided sandy areas at the coast. We propose that the European Union subsidies related to the creation and alteration of irrigation ponds should be linked to management strategies that maximise pond quality for waterbirds. A third of the species pairs examined showed strong support for the species co-occurring more often than expected by random. Our study showed that larids breeding in mixed colonies segregate spatially in their foraging niche between marine and freshwater environments. Both breeding and foraging habitats need to be addressed when analysing larid population dynamics and conservation strategies.
Additional keywords: agriculture, artificial habitat, attraction, co-occurrence, stable isotopes.
References
Abdennadher, A., Ramírez, F., Romdhane, M. S., Ruiz, X., Jover, L., and Sanpera, C. (2010). Biomonitoring of coastal areas in Tunisia: stable isotope and trace element analysis in the yellow-legged gull. Marine Pollution Bulletin 60, 440–447.| Biomonitoring of coastal areas in Tunisia: stable isotope and trace element analysis in the yellow-legged gull.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1ertr0%3D&md5=9fb7876f272d168de33e11b5fa3b5b28CAS | 19896145PubMed |
Abellán, P., Sánchez-Fernández, D., Millán, A., Botella, F., Sánchez-Zapata, J. A., and Giménez, A. (2006). Irrigation ponds as macroinvertebrate habitat in a semi-arid agricultural landscape (SE Spain). Journal of Arid Environments 67, 255–269.
| Irrigation ponds as macroinvertebrate habitat in a semi-arid agricultural landscape (SE Spain).Crossref | GoogleScholarGoogle Scholar |
Arizaga, J., Jover, L., Aldalur, A., Cuadrado, J. F., Herrero, A., and Sanpera, C. (2013). Trophic ecology of a resident yellow-legged gull (Larus michahellis) population in the Bay of Biscay. Marine Environmental Research 87–88, 19–25.
| Trophic ecology of a resident yellow-legged gull (Larus michahellis) population in the Bay of Biscay.Crossref | GoogleScholarGoogle Scholar | 23541603PubMed |
Becker, P. H., Frank, D., and Sudmann, S. R. (1993). Temporal and spatial pattern of common tern (Sterna hirundo) foraging in the Wadden Sea. Oecologia 93, 389–393.
| Temporal and spatial pattern of common tern (Sterna hirundo) foraging in the Wadden Sea.Crossref | GoogleScholarGoogle Scholar |
Bicknell, A. W. J., Oro, D., Camphuysen, K. C. J., and Votier, S. C. (2013). Potential consequences of discard reform for seabird communities. Journal of Applied Ecology 50, 649–658.
| Potential consequences of discard reform for seabird communities.Crossref | GoogleScholarGoogle Scholar |
Blázquez, M., Sánchez-Zapata, J. A., Botella, F., Carrete, M., and Eguía, S. (2009). Spatio-temporal segregation of facultative scavengers at ungulate carcasses. Acta Oecologica 35, 645–650.
| Spatio-temporal segregation of facultative scavengers at ungulate carcasses.Crossref | GoogleScholarGoogle Scholar |
Carrete, M., and Donázar, J. A. (2005). Application of central-place foraging theory shows the importance of Mediterranean dehesas for the conservation of cinereous vulture, Aegypius monachus. Biological Conservation 126, 582–590.
| Application of central-place foraging theory shows the importance of Mediterranean dehesas for the conservation of cinereous vulture, Aegypius monachus.Crossref | GoogleScholarGoogle Scholar |
Chamberlain, D. E., Fuller, R. J., Bunce, R. G. H., Duckworth, J. C., and Shrubb, M. (2000). Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. Journal of Applied Ecology 37, 771–788.
| Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales.Crossref | GoogleScholarGoogle Scholar |
Chase, J. M., and Leibold, M. A. (2003). ‘Ecological Niches: Linking Classical and Contemporary Approaches.’ (University of Chicago Press: Chicago, IL.)
Chesson, P. (2000). General theory of competitive coexistence in spatially-varying environments. Theoretical Population Biology 58, 211–237.
| General theory of competitive coexistence in spatially-varying environments.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7hvVCquw%3D%3D&md5=28217461d68d269af512e5375267281cCAS | 11120650PubMed |
Christel, I., Navarro, J., del Castillo, M., Cama, A., and Ferrer, X. (2012). Foraging movements of Audouin’s gull (Larus audouinii) in the Ebro Delta, NW Mediterranean: a preliminary satellite tracking study. Estuarine, Coastal and Shelf Science 96, 257–261.
| Foraging movements of Audouin’s gull (Larus audouinii) in the Ebro Delta, NW Mediterranean: a preliminary satellite tracking study.Crossref | GoogleScholarGoogle Scholar |
Cotin, J., García-Tarrasón, M., Sanpera, C., Jover, L., and Ruiz, X. (2011). Sea, freshwater or saltpans? Foraging ecology of terns to assess mercury inputs in a wetland landscape: the Ebro Delta. Estuarine, Coastal and Shelf Science 92, 188–194.
| Sea, freshwater or saltpans? Foraging ecology of terns to assess mercury inputs in a wetland landscape: the Ebro Delta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsF2jtbk%3D&md5=d51488e8633fc505aa7453539635ca7bCAS |
Cramp, S. (1998). ‘The Complete Birds of the Western Palearctic.’ (Oxford University Press: London.)
Cushman, S. A. (2006). Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biological Conservation 128, 231–240.
| Effects of habitat loss and fragmentation on amphibians: a review and prospectus.Crossref | GoogleScholarGoogle Scholar |
Diamond, J. M. (1975). Assembly of species communities. In ‘Ecology and Evolution of Communities’. (Eds M. L. Cody and J. M. Diamond.) pp. 352–444. (Harvard University Press: Cambridge, MA.)
Donald, P. F., Green, R. E., and Heath, M. F. (2001). Agricultural intensification and the collapse of Europe’s farmland bird populations. Proceedings. Biological Sciences 268, 25–29.
| Agricultural intensification and the collapse of Europe’s farmland bird populations.Crossref | GoogleScholarGoogle Scholar |
Duhem, C., Roche, P., Vidal, E., and Tatoni, T. (2008). Effects of anthropogenic food resources on yellow legged gull colony size on Mediterranean islands. Population Ecology 50, 91–100.
| Effects of anthropogenic food resources on yellow legged gull colony size on Mediterranean islands.Crossref | GoogleScholarGoogle Scholar |
Dunn, E. K. (1973). Changes in fishing ability of terns associated with wind speed and sea surface conditions. Nature 244, 520–521.
| Changes in fishing ability of terns associated with wind speed and sea surface conditions.Crossref | GoogleScholarGoogle Scholar |
Fasola, M., and Bogliani, G. (1990). Foraging ranges of an assemblage of Mediterranean seabirds. Colonial Waterbirds 13, 72–74.
| Foraging ranges of an assemblage of Mediterranean seabirds.Crossref | GoogleScholarGoogle Scholar |
Fasola, M., Bogliani, G., Saino, N., and Canova, L. (1989). Foraging, feeding and time-activity niches of eight species of breeding seabirds in the coastal wetlands of the Adriatic Sea. Bollettino di Zoologia 56, 61–72.
| Foraging, feeding and time-activity niches of eight species of breeding seabirds in the coastal wetlands of the Adriatic Sea.Crossref | GoogleScholarGoogle Scholar |
Field, I. C., Bradshaw, C. J. A., Burton, H. R., Sumner, M. D., and Hindell, M. A. (2005). Resource partitioning through oceanic segregation of foraging juvenile southern elephant seals Mirounga leonine. Oecologia 142, 127–135.
| Resource partitioning through oceanic segregation of foraging juvenile southern elephant seals Mirounga leonine.Crossref | GoogleScholarGoogle Scholar | 15365810PubMed |
Forbes, L. S., and Kaiser, G. W. (1994). Habitat choice in breeding seabirds: when to cross the information barrier. Oikos 70, 377–384.
| Habitat choice in breeding seabirds: when to cross the information barrier.Crossref | GoogleScholarGoogle Scholar |
Fred, M. S., O'Hara, R. B., and Brommer, J. E. (2006). Consequences of the spatial configuration of resources for the distribution and dynamics of the endangered Parnassius apollo butterfly. Biological Conservation 130, 183–192.
| Consequences of the spatial configuration of resources for the distribution and dynamics of the endangered Parnassius apollo butterfly.Crossref | GoogleScholarGoogle Scholar |
Furness, R. W., Edwards, A. E., and Oro, D. (2007). Influences of fisheries management practices and scavenging of seabirds on the availability of discards to benthic scavengers. Marine Ecology Progress Series 350, 235–244.
| Influences of fisheries management practices and scavenging of seabirds on the availability of discards to benthic scavengers.Crossref | GoogleScholarGoogle Scholar |
García-Charton, J. A., Pérez-Ruzafa, Á., Sánchez-Jerez, P., Bayle-Sempere, J. T., Reñones, O., and Moreno, D. (2004). Multi-scale spatial heterogeneity, habitat structure, and the effect of marine reserves on western Mediterranean rocky reef fish assemblages. Marine Biology 144, 161–182.
| Multi-scale spatial heterogeneity, habitat structure, and the effect of marine reserves on western Mediterranean rocky reef fish assemblages.Crossref | GoogleScholarGoogle Scholar |
Gilroy, J. J., and Sutherland, W. J. (2007). Beyond ecological traps: perceptual errors and undervalued resources. Trends in Ecology & Evolution 22, 351–356.
| Beyond ecological traps: perceptual errors and undervalued resources.Crossref | GoogleScholarGoogle Scholar |
Goodale, E., Beauchamp, G., Magrath, R. D., Nieh, J. C., and Ruxton, G. D. (2010). Interspecific information transfer influences animal community structure. Trends in Ecology & Evolution 25, 354–361.
| Interspecific information transfer influences animal community structure.Crossref | GoogleScholarGoogle Scholar |
Hobson, K. (2006). Using stable isotopes to quantitatively track endogenous and exogenous nutrient allocations to eggs of birds that travel to breed. Ardea 94, 359–369.
Hobson, K. A., Sirois, J., and Gloutney, M. L. (2000). Tracing nutrient allocation to reproduction with stable isotopes: a preliminary investigation using colonial waterbirds of Great Slave Lake. The Auk 117, 760–774.
| Tracing nutrient allocation to reproduction with stable isotopes: a preliminary investigation using colonial waterbirds of Great Slave Lake.Crossref | GoogleScholarGoogle Scholar |
Hole, D. G., Perkins, A. J., Wilson, J. D., Alexander, I. H., Grice, P. V., and Evans, A. D. (2005). Does organic farming benefit biodiversity? Biological Conservation 122, 113–130.
| Does organic farming benefit biodiversity?Crossref | GoogleScholarGoogle Scholar |
Inger, R., and Bearhop, S. (2008). Applications of stable isotope analyses to avian ecology. The Ibis 150, 447–461.
| Applications of stable isotope analyses to avian ecology.Crossref | GoogleScholarGoogle Scholar |
Johnson, B. J., Fogel, M. L., and Miller, G. H. (1998). Stable isotopes in modern ostrich eggshell: a calibration for paleoenvironmental applications in semi-arid regions of southern Africa. Geochimica et Cosmochimica Acta 62, 2451–2461.
| Stable isotopes in modern ostrich eggshell: a calibration for paleoenvironmental applications in semi-arid regions of southern Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtFehsbY%3D&md5=2fd0b255e58d9ddfb7d5b4a612689bb2CAS |
Kelt, D. A., Meserve, P. L., Nabors, L. K., Forister, M. L., and Gutiérrez, J. R. (2004). Foraging ecology of small mammals in semiarid Chile: the interplay of biotic and abiotic effects. Ecology 85, 383–397.
| Foraging ecology of small mammals in semiarid Chile: the interplay of biotic and abiotic effects.Crossref | GoogleScholarGoogle Scholar |
Kong, F., Yin, H., Nakagoshi, N., and Zong, Y. (2010). Urban green space network development for biodiversity conservation: identification based on graph theory and gravity modeling. Landscape and Urban Planning 95, 16–27.
| Urban green space network development for biodiversity conservation: identification based on graph theory and gravity modeling.Crossref | GoogleScholarGoogle Scholar |
Luz, B., and Kolodny, Y. (1985). Oxygen isotope variations in phosphate of biogenic apatites. IV. Mammal teeth and bones. Earth and Planetary Science Letters 75, 29–36.
| Oxygen isotope variations in phosphate of biogenic apatites. IV. Mammal teeth and bones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlsFyjsrw%3D&md5=7c50cb24b04f12460f43fa519f704aa9CAS |
Ma, Z., Li, B., Zhao, B., Ping, K., Tang, S., and Chen, J. (2004). Are artificial wetlands good alternatives to natural wetlands for waterbirds? A case study on Chongming Island, China. Biodiversity and Conservation 13, 333–350.
| Are artificial wetlands good alternatives to natural wetlands for waterbirds? A case study on Chongming Island, China.Crossref | GoogleScholarGoogle Scholar |
Maerz, J. C., Blossey, B., and Nuzzo, V. (2005). Green frogs show reduced foraging success in habitats invaded by Japanese knotweed. Biodiversity and Conservation 14, 2901–2911.
| Green frogs show reduced foraging success in habitats invaded by Japanese knotweed.Crossref | GoogleScholarGoogle Scholar |
Mañosa, S., Oro, D., and Ruiz, X. (2004). Activity patterns and foraging behaviour of Audouin’s gulls in the Ebro Delta, NW Mediterranean. Scientia Marina 68, 605–614.
Martínez-Abraín, A., Maestre, R., and Oro, D. (2002). Demersal trawling waste as a food source for western Mediterranean seabirds during the summer. ICES Journal of Marine Science 59, 529–537.
| Demersal trawling waste as a food source for western Mediterranean seabirds during the summer.Crossref | GoogleScholarGoogle Scholar |
Meléndez-Pastor, I., Navarro-Pedreño, J., Gómez, I., and Koch, M. (2010). Detecting drought induced environmental changes in a Mediterranean wetland by remote sensing. Applied Geography 30, 254–262.
| Detecting drought induced environmental changes in a Mediterranean wetland by remote sensing.Crossref | GoogleScholarGoogle Scholar |
Mönkkönen, M., and Forsman, J. T. (2002). Heterospecific attraction among forest birds: a review. Ornithological Science 1, 41–51.
| Heterospecific attraction among forest birds: a review.Crossref | GoogleScholarGoogle Scholar |
Moreno, R., Jover, L., Munilla, I., Velando, A., and Sanpera, C. (2010). A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain. Marine Biology 157, 545–553.
| A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain.Crossref | GoogleScholarGoogle Scholar |
Navarro, J., Forero, M. G., González-Solís, J., Igual, J. M., Bécares, J., and Hobson, K. A. (2009). Foraging segregation between two closely related shearwaters breeding in sympatry. Biology Letters 5, 545–548.
| Foraging segregation between two closely related shearwaters breeding in sympatry.Crossref | GoogleScholarGoogle Scholar | 19364709PubMed |
Navarro, J., Oro, D., Bertolero, A., Genovart, M., Delgado, A., and Forero, M. G. (2010). Age and sexual differences in the exploitation of two anthropogenic food resources for an opportunistic seabird. Marine Biology 157, 2453–2459.
| Age and sexual differences in the exploitation of two anthropogenic food resources for an opportunistic seabird.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Krsb3P&md5=d688466485369495dc4d14dcce52270cCAS |
Oro, D., and Ruiz, X. (1997). Exploitation of trawler discards by breeding seabirds in the north-western Mediterranean: differences between the Ebro Delta and the Balearic Islands. ICES Journal of Marine Science 54, 695–707.
| Exploitation of trawler discards by breeding seabirds in the north-western Mediterranean: differences between the Ebro Delta and the Balearic Islands.Crossref | GoogleScholarGoogle Scholar |
Oro, D., Cam, E., Pradel, R., and Martínez-Abraín, A. (2004). Influence of food availability on demography and local population dynamics in a long-lived seabird. Proceedings. Biological Sciences 271, 387–396.
| Influence of food availability on demography and local population dynamics in a long-lived seabird.Crossref | GoogleScholarGoogle Scholar |
Oro, D., Genovart, M., Tavecchia, G., Fowler, M. S., and Martínez-Abraín, A. (2013). Ecological and evolutionary implications of food subsidies from humans. Ecology Letters 16, 1501–1514.
| Ecological and evolutionary implications of food subsidies from humans.Crossref | GoogleScholarGoogle Scholar | 24134225PubMed |
Ostrand, W. D., Drew, G. S., Suryan, R. M., and McDonald, L. L. (1998). Evaluation of radio-tracking and strip transect method for determining foraging ranges of black-legged kittiwakes. The Condor 100, 709–718.
| Evaluation of radio-tracking and strip transect method for determining foraging ranges of black-legged kittiwakes.Crossref | GoogleScholarGoogle Scholar |
Ovaskainen, O., Hottola, J., and Siitonen, J. (2010). Modelling species co-occurrence by multivariate logistic regression generates new hypotheses on fungal interactions. Ecology 91, 2514–2521.
| Modelling species co-occurrence by multivariate logistic regression generates new hypotheses on fungal interactions.Crossref | GoogleScholarGoogle Scholar | 20957941PubMed |
Pedrocchi, V., Oro, D., González-Solís, J., Ruiz, X., and Jover, L. (2002). Divergences in diet between the two largest breeding colonies of Audouin’s gulls: the effect of fishery activities. Scientia Marina 66, 313–320.
Peery, M. Z., Beissinger, S. R., Newman, S. H., Burkett, E. B., and Williams, T. D. (2004). Applying the declining population paradigm: diagnosing causes of low reproductive success in marbled murrelets. Conservation Biology 18, 1088–1098.
| Applying the declining population paradigm: diagnosing causes of low reproductive success in marbled murrelets.Crossref | GoogleScholarGoogle Scholar |
Ramírez, F., Navarro, J., Afán, I., Hobson, K. A., Delgado, A., and Forero, M. G. (2012). Adapting to a changing world: unraveling the role of man-made habitats as alternative feeding areas for slender-billed gull (Chroicocephalus genei). PLoS ONE 7, e47551.
| Adapting to a changing world: unraveling the role of man-made habitats as alternative feeding areas for slender-billed gull (Chroicocephalus genei).Crossref | GoogleScholarGoogle Scholar | 23094062PubMed |
Robertson, B. A., and Hutto, R. L. (2006). A framework for understanding ecological traps and an evaluation of existing evidence. Ecology 87, 1075–1085.
| A framework for understanding ecological traps and an evaluation of existing evidence.Crossref | GoogleScholarGoogle Scholar | 16761584PubMed |
Sánchez-Zapata, J. A., Anadón, J. D., Carrete, M., Giménez, A., Navarro, J., Villacorta, C., and Botella, F. (2005). Breeding waterbirds in relation to artificial pond attributes: implications for the design of irrigation facilities. Biodiversity and Conservation 14, 1627–1639.
| Breeding waterbirds in relation to artificial pond attributes: implications for the design of irrigation facilities.Crossref | GoogleScholarGoogle Scholar |
Schaffner, F. C., and Swart, P. K. (1991). Influence of diet and environmental water on the carbon and oxygen isotopic signatures of seabird eggshell carbonate. Marketing Science 48, 23–38.
Sebastián-González, E., Sánchez-Zapata, J. A., and Botella, F. (2010a). Agricultural ponds as alternative habitat for waterbirds: spatial and temporal patterns of abundance and management strategies. European Journal of Wildlife Research 56, 11–20.
| Agricultural ponds as alternative habitat for waterbirds: spatial and temporal patterns of abundance and management strategies.Crossref | GoogleScholarGoogle Scholar |
Sebastián-González, E., Sánchez-Zapata, J. A., Botella, F., and Ovaskainen, O. (2010b). Testing the heterospecific attraction hypothesis with time-series data on species co-occurrence. Proceedings. Biological Sciences 277, 2983–2990.
| Testing the heterospecific attraction hypothesis with time-series data on species co-occurrence.Crossref | GoogleScholarGoogle Scholar |
Sebastián-González, E., Navarro, J., Sánchez-Zapata, J. A., Botella, F., and Delgado, A. (2012). Water quality and avian inputs as sources of isotopic variability in aquatic macrophytes and macroinvertebrates. Journal of Limnology 71, 191–199.
| Water quality and avian inputs as sources of isotopic variability in aquatic macrophytes and macroinvertebrates.Crossref | GoogleScholarGoogle Scholar |
Tablado, Z., Tella, J. L., Sánchez-Zapata, J. A., and Hiraldo, F. (2010). An invasion-conservation paradox: long-term positive effects of an American crayfish on a European community of predators. Conservation Biology 24, 1230–1238.
| An invasion-conservation paradox: long-term positive effects of an American crayfish on a European community of predators.Crossref | GoogleScholarGoogle Scholar | 20337679PubMed |
Tanhua, T., Hainbucher, D., Cardin, V., Álvarez, M., Civitarese, G., McNichol, A. P., and Key, R. M. (2013). Repeat hydrography in the Mediterranean Sea, data from the Meteor cruise 84/3 in 2011. Earth System Science Data 5, 289–294.
| Repeat hydrography in the Mediterranean Sea, data from the Meteor cruise 84/3 in 2011.Crossref | GoogleScholarGoogle Scholar |
Thomas, C. D., Cameron, A., Green, R. E., Bakkenes, M., Beaumont, L. J., Collingham, Y. C., Erasmus, B. F. N., Siqueira, M. F. D., Grainger, A., and Hannah, L. (2004). Extinction risk from climate change. Nature 427, 145–148.
| Extinction risk from climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFOgtQ%3D%3D&md5=451812231202219a758d55d745a75bcfCAS | 14712274PubMed |
Virkkala, R., Luoto, M., and Rainio, K. (2004). Effects of landscape composition on farmland and red-listed birds in boreal agricultural-forest mosaics. Ecography 27, 273–284.
| Effects of landscape composition on farmland and red-listed birds in boreal agricultural-forest mosaics.Crossref | GoogleScholarGoogle Scholar |
