Prey type and prey size selection in a Eurasian oystercatcher population at the edge of its distribution range

Introduction

The study of prey and prey size selection helps us better understand ecological interactions between predator and prey, and their possible influence on the structuring of food webs and prey communities (Pokharel 2020Pokharel A. 2020. Prey Selection by Birds of Prey. Dissertations and Theses in Biological Sciences, 108. University of Nebraska (https://digitalcommons.unl.edu/bioscidiss/108?utm_source=digitalcommons.unl.edu%2Fbioscidiss%2F108&utm_medium=PDF&utm_campaign=PDFCoverPages)
). The decision of what and where to forage is guided theoretically by the strategy of optimizing energy acquisition by unit of time, as analysed by optimal foraging theory (Fargallo et al. 2020Fargallo J.A., Navarro-López J., Palma-Granados P., Nieto R.M. 2020. Foraging strategy of a carnivorous-insectivorous raptor species based on prey size, capturability and nutritional components. Sci. Rep. 10: 7583 http://doi.org/10.1038/s41598-020-64504-4.
, Strandmark 2024Strandmark S. D. 2024. Optimal Foraging of Three Predatory Fishes on Red Swamp Crayfish (Procambarus clarkii) (Master’s thesis, Michigan State University).
). However, fitness factors other than the balance between energy acquisition and costs may also play a role, as will be discussed below.

Oystercatchers are known to be quite plastic regarding prey type choice, consuming the most abundant prey at each coastal site (Tjørve and Tjørve 2010Tjørve C.M.C., Tjørve E. 2010. Food of Eurasian oystercatcher (Haematopus ostralegus) chicks raised in rocky shores in Southern Norway. Ornis Norvegica 33: 56-62. https://doi.org/10.15845/on.v33i0.146
). In fact, when they colonize inland territories far from the coast, their diet can shift to terrestrial prey (van de Pol et al. 2014van de Pol M., Atkinson P., Blew J., et al. 2014. A global assessment of the conservation status of the nominate subspecies of Eurasian Oystercatcher (Haematopus ostralegus ostralegus). Int. Wader Stud. 20: 47-61.
). Additionally, the selection of prey items by oystercatchers may also be influenced by parameters that determine the cost/benefit ratio, such as size, thickness of the valve, pulp content, presence of barnacles on the valves and seasonal differences in available sizes (Hilgerloh and Pfeifer 2002Hilgerloh G., Pfeifer D. 2002. Size selection and competition for mussels, Mytilus edulis, by oystercatchers, Haematopus ostralegus, herring gulls, Larus argentatus, and common eiders, Somateria mollissima. Ophelia 56: 43-53. https://doi.org/10.1080/00785236.2002.10409488.
, Rossignol et al. 2011Rossignol A., Buckingham S., Stephen L., Nagarajan R. 2011. Breaking down the mussel (Mytilus edulis) shell: which layers affect oystercatchers’ (Haematopus ostralegus) prey selection? J. Exp. Mar. Biol. Ecol. 405: 87-92. https://doi.org/10.1016/j.jembe.2011.05.021
). Many studies have approached prey size selection by the Eurasian oystercatcher (see e.g. Cayford and Goss-Custard 1990Cayford J., Goss-Custard J.D. 1990. Seasonal changes in the size selection of mussels, Mytilus edulis, by oystercatchers, Haematopus ostralegus: an optimality approach. Anim. Behav. 40: 609-624. https://doi.org/10.1016/S0003-3472(05)80691-8
, Zwarts et al. 1996Zwarts L., Cayford J.T., Hulscher l.B., Kersten M., Meire P., Triplet P. 1996. Prey size selection and intake rate. In: Goss-Custard, J.D. The Oystercatcher from individuals to populations, 30-55. Oxford University Press. Oxford.
), reporting a wide range of results depending on the physical and ecological characteristics of each study site. However, Hilgerloh and Pfeifer (2002)Hilgerloh G., Pfeifer D. 2002. Size selection and competition for mussels, Mytilus edulis, by oystercatchers, Haematopus ostralegus, herring gulls, Larus argentatus, and common eiders, Somateria mollissima. Ophelia 56: 43-53. https://doi.org/10.1080/00785236.2002.10409488.
suggested the existence of a preferred mussel size for oystercatchers, so that if the size class which seemingly optimizes the benefit/cost relationship is not available, oystercatchers would then try to forage on mussels as close in size to it as possible, if costs or time constraints are not too demanding.

The Iberian Peninsula represents the southernmost limit of the distribution of Eurasian oystercatchers (Haematopus ostralegus) in the western Palearctic, along with the populations of the Greek and Turkish peninsulas. Populations located at the limit of their distribution range may have different vital rates and foraging ecology to those of populations located closer to the centre of the distribution range of the species, tending to be more vulnerable to environmental stochasticity due to their small size, and to local extinction due to a poor rescue effect when distance to population cores is great (Van Schmidt and Beissinger 2020Van Schmidt N.D., Beissinger S.R. 2020. The rescue effect and inference from isolation-extinction relationships. Ecol. Lett. 23: 598-606. https://publons.com/publon/10.1111/ele.13460
). Hence, the study of edge populations should be considered a conservation priority (see e.g. Martínez-Abraín et al. 2019AMartínez-Abraín A., Santidrián Tomillo P., Mouriño J., et al. 2019a. Delayed predator-prey collapses: the case of black-legged kittiwakes and Iberian sardines. Mar. Ecol. Prog. Ser. 631: 201-207. https://doi.org/10.3354/meps13164
, 2023Martínez-Abraín A., Santidrián Tomillo P., Mouriño J., et al. 2023. Predator-prey collapses at the edge of predator distribution: the case of clupeids and common guillemots (Uria aalge) in NW Iberia. Sci. Mar. 87: e053. https://doi.org/10.3989/scimar.05299.053
) despite the overall conservation status of the species, which in Europe is Near Threatened in the case of H. ostralegus (BirdLife International 2019BirdLife International. 2019. Haematopus ostralegus. The IUCN Red List of Threatened Species 2019 (https://www.iucnredlist.org/species/22693613/154998347). Last accessed October 2nd, 2024.
).

In the Iberian Peninsula, oystercatcher populations have experienced a decline in the northeast (Ebro Delta), showing a 4% annual decrease during the period 2001-2020. On the other hand, northwestern Iberian populations (Galicia) have progressively increased (Rías Baixas) or remained stable (Lugo coast) over the last few decades (Mouriño et al. 2021Mouriño J., Curcó A., Bermejo A., et al. 2021. Ostrero euroásiatico, Haemotopus ostralegus. In: López-Jiménez, N (ed.). Libro Rojo de las Aves de España, 125-136. SEO/BirdLife. Madrid.
). The oldest colonies in NW Spain are located in abrupt coastal islets where nesting oystercatchers have found an ecological refuge in the last few decades (Mouriño et al. 2021Mouriño J., Curcó A., Bermejo A., et al. 2021. Ostrero euroásiatico, Haemotopus ostralegus. In: López-Jiménez, N (ed.). Libro Rojo de las Aves de España, 125-136. SEO/BirdLife. Madrid.
). However, human rural flight during the last 60-70 years has allowed oystercatchers to colonize or recolonize small flat islets (Fig. 1). These sites are easily accessible by humans and remained unoccupied by gulls and oystercatchers until recently due to permanent human disturbance (see Martínez-Abraín et al. 2019bMartínez-Abraín A., Jiménez J., Oro D. (2019b). Pax Romana: “refuge abandonment” and expansion of fearless behaviours. Anim. Conserv. 22: 3-13. https://doi.org/10.1111/acv.12429
, 2021Martínez-Abraín A., Ferrer X., Jiménez J., et al. 2021. The selection of anthropogenic habitat by wildlife as an ecological consequence of rural exodus: empirical examples from Spain. Anim. Biodivers. Conserv. 44: 195-203. https://doi.org/10.32800/abc.2021.44.0195
). They constitute a suboptimal alternative to beaches and dunes, which are locally occupied by people and thus largely unavailable to wildlife, unlike the Ebro Delta colony in NE Spain where beaches and dunes are protected (Fig. 1). This forced nest site selection (anthropogenic forcing) is expected a priori to influence foraging behaviour due to factors unrelated to foraging preference or edge-of-distribution-related effects (ecological forcing), a fact that is often overlooked in studies of prey and prey size selection.

Here we analyse for the first time whether the expanding breeding populations of Eurasian oystercatcher from NW Spain show a preference for any prey type or prey size (for chick feeding) on three small flat islets in which the species has nested syntopically with yellow-legged gulls (Larus michahellis) during the last few decades. Based on current knowledge, our a priori expectations were that oystercatchers would show high foraging plasticity, with no selection of prey type but a tendency to select larger, more profitable prey sizes.

Material and methods

Field data collection

 ⌅

To study prey consumption, prey availability and prey size, Areoso, Pedregoso and Farallóns were each sampled once, on 17 July 2020, 16 July 2021 and 2 July 2022, respectively. All samplings were carried out at low tide to be able to determine prey availability in adjacent foraging grounds. The samplings were performed during the month of July, taking into account the local breeding calendar of the species and the need to avoid overlapping with the most vulnerable period of its reproduction (egg incubation in May). We took advantage of the fact that piles of discarded shells were generated at high-tide spots after molluscs were eaten most likely for chick feeding, so remains were found concentrated on small patches of bare rock (approximately 4×4 m in our case; Fig. 2). This probably happens because chicks were hidden in high-tide-safe sheltered points, and this fortuitously led to the formation of the dense piles of discarded shells close to them as a by-product when adults bring food onshore to feed the chicks. The mussels were opened in half in a vertical plane by the oystercatchers, and hence the valves were complete. Limpets were not found broken either, but just as whole shells detached from the rock. We first searched for piles of discarded shells on each islet. Mussel valves were assumed to come from independent individual mussels regardless of whether they were left or right valves. This may have introduced some unknown degree of bias in favour of mussels on the islet where mussels were relatively common (Areoso), although it is certainly not relevant because no positive selection of mussels was detected (see Results section). Prey availability was sampled in foraging areas adjacent to breeding areas because previous observations (A. Bermejo, J. Mouriño, X. Silvar, own unpublished information) indicated that breeding oystercatchers forage in the vicinity of breeding colonies during low tide on the study islets. This finding is consistent with the short foraging excursions reported by Tjørve and Tjørve (2010)Tjørve C.M.C., Tjørve E. 2010. Food of Eurasian oystercatcher (Haematopus ostralegus) chicks raised in rocky shores in Southern Norway. Ornis Norvegica 33: 56-62. https://doi.org/10.15845/on.v33i0.146
, although this is not the case for all populations (Leopold et al. 1996Leopold M.F., Van Elk J.F., Van Heezik Y.M. 1996. Central place foraging in oystercatchers Haematopus ostralegus: Can parents that transport mussels Mytillus edulis to their young profit from size selection? Ardea 84: 311-325.
). The study of consumed prey was performed by launching a wire square (40×40 cm) blindly two to three times on top of the discarded shell piles. We counted the number of shells of each prey type found within the squares. We measured the width and length of the prey found within the squares using a Mitutoyo digital caliper, to the nearest 0.01 mm. We also measured the length and width of prey items found in our samplings of prey availability. To study prey availability, we launched the wire square overhead on the foraging grounds at low tide. The square was launched backwards by different observers to avoid launching biases such as aiming unconsciously for areas with larger-size prey (i.e. sampling was randomized). A total of 12 launches were performed in Areoso, 10 launches in Farallóns and 4 launches in Pedregoso. The number of launches performed was smaller on Pedregoso than on the other two islets because an initial visual inspection of the area showed an overall scarcity of mussels. Additionally, the sampling of prey availability was stopped in the fourth launch because there was a large number of limpets within the limits of the wire square, providing a large enough sample size to determine mean limpet size. Increasing the number of square launches would have not changed the proportion of mussels. However, we must acknowledge some unknown degree of bias in the determination of limpet length if limpet size is not independent within quadrats.

Fig. 2.  A, discarded shell pile on Farallóns islet. B, discarded shell pile on Pedregoso islet (note the digital caliper in the lower left corner for scale, blue arrow). C, sampling of available prey in foraging grounds at low tide on Pedrogoso islet. D, oystercatcher pair at high tide in foraging grounds (image credits: Xan Silvar).

Results

Discussion

Based on our results, we cannot conclude the existence of clear positive or negative selection of one prey type over another. Although the values of the Savage index pointed to some preference for foraging on mussels over limpets, the null selection hypothesis was only statistically rejected for limpets on Pedregoso (negative selection). These results coincided with what was expected a priori, because previous studies found that oystercatchers choose the prey types that are most abundant within breeding territories (e.g. Tjørve and Tjørve 2010Tjørve C.M.C., Tjørve E. 2010. Food of Eurasian oystercatcher (Haematopus ostralegus) chicks raised in rocky shores in Southern Norway. Ornis Norvegica 33: 56-62. https://doi.org/10.15845/on.v33i0.146
). On Farallóns, we were unable to study prey selection because mussels were not available in the colony or present in shell piles. All consumed prey were limpets. Since shells remain in the shell piles for a long time, it is unlikely that the absence of valves in the foraging ground means that oystercatchers had already consumed all mussels available and that our results have validity only for a short time window. Additionally, we recorded the presence of periwinkles (Littorina sp.) on Farallóns (in seven out of the ten squares sampled in the foraging grounds), but this mollusc was not found in shell piles, suggesting a negative selection of this species, which would be consistent with the findings reported by Tjørve and Tjørve (2010)Tjørve C.M.C., Tjørve E. 2010. Food of Eurasian oystercatcher (Haematopus ostralegus) chicks raised in rocky shores in Southern Norway. Ornis Norvegica 33: 56-62. https://doi.org/10.15845/on.v33i0.146
in Norway. However, this species was not included in our study because it was not present in shell piles or sampling squares on Areoso and Pedregoso that were sampled prior to Farallóns.

In summary, the results of our study showed heterogeneity among sites in prey type, supporting the idea that oystercatchers may act as facultative specialists, foraging on the most common prey at each site without showing a clear preference for one prey type or another. Only the negative selection of limpets on Pedregoso suggested that oystercatchers may forage on limpets in a lower proportion than expected by its abundance in the local environment. This foraging plasticity has applied conservation consequences because it is easier for facultative specialists to expand and colonize new sites, as this is actually happening with this species in Atlantic Iberia.

Regarding prey size selection, our analyses detected selection for larger sizes in most cases: mussels and limpets on Areoso and limpets on Farallóns, consistently with the findings of most studies on prey size selection by the Eurasian oystercatcher (Drinnan 1958Drinnan R. E., 1958. The winter feeding of the oystercatcher (Haematopus ostralegus) on the edible mussel (Mytilus edulis) in the Conway Estuary, North Wales. Fishery Invest. Lond. (Ser. 2) 22: 1-15.
, Ens et al. 1992Ens B.J., Kersten M., Brenninkmeijer A., et al. 1992. Territory quality, parental effort and reproductive success of oystercatchers (Haematopus ostralegus). Journal of Animal Ecology 61: 703-715. https://doi.org/10.2307/5625
). However, Leopold et al. (1996)Leopold M.F., Van Elk J.F., Van Heezik Y.M. 1996. Central place foraging in oystercatchers Haematopus ostralegus: Can parents that transport mussels Mytillus edulis to their young profit from size selection? Ardea 84: 311-325.
found that selection for the most profitable prey could increase chick predation risk, because adults had to remain longer away from colonies and, hence, they did not select for large prey size unless they had to travel long distances. Our study oystercatchers nested associated with yellow-legged gulls (265 and 88 gull pairs on Pedregoso and Areoso, respectively, in 2022; Dirección Xeral de Patrimonio Natural 2024Dirección Xeral de Patrimonio Natural. Xunta de Galicia. 2024. Censo e seguimento da poboación reprodutora de distintas especies de aves mariñas durante o ano 2022 en Galicia. Dirección Xeral de Patrimonio Natural. Vicepresidencia segunda e Consellería de Medio Ambiente, Territorio e Vivenda. Xunta de Galicia.
) and great black-backed gulls (Larus marinus) (1 and 4 pairs on Pedregoso and Areoso, respectively, in 2023; J. Mouriño own unpublished data), all of them facultative oystercatcher predators (Tjørve and Tjørve 2010Tjørve C.M.C., Tjørve E. 2010. Food of Eurasian oystercatcher (Haematopus ostralegus) chicks raised in rocky shores in Southern Norway. Ornis Norvegica 33: 56-62. https://doi.org/10.15845/on.v33i0.146
). Nevertheless, we found that oystercatchers selected for larger prey to feed chicks, meaning that their foraging grounds had to be close to nesting sites (i.e. in exposed rocks at low tide around nesting areas, as previously observed by us), and thus that they were away from the proximity of chicks for short time periods. Moreover, our field observations of birds foraging in the Coelleira, Ansarón and Gaveira de Viveiro colonies (X.M. unpublished) support the need to minimize the risk of chick predation because the two adults of each nesting pair do not forage at the same time, but one of them remains in the vicinity of chicks until the second brings food for the chicks.

Additionally, we also detected selection for small size of limpets on Pedregoso but were unable to show selection for size of mussels there. The selection for smaller limpets could be due to lack of independence of the limpets measured, as a large number of them came from the same quadrat (for example, individuals could be affected by density dependence or be closely related to each other). Alternatively, this result could also be a consequence of adult oystercatchers foraging farther from colonies than usual, trying to minimize the time spent away from chicks. The lack of selection for mussels could simply be an artefact caused by low sample size (n=17 mussels consumed and n=8 available). Selection for smaller prey has only been previously found in studies in which the Eurasian oystercatcher’s target prey was the common cockle (Cerastoderma edulis). However, the closely related African black oystercatcher (H. moquini) showed lack of discrimination of clam (Donax serra) size; there was temporal segregation of small and large clams but, even when large clams were abundant they took both small and large clams (Ward 1991Ward D. 1991. The size selection of clams by African black oystercatchers and kelp gulls. Ecology 72: 513-522. https://doi.org/10.2307/2937192
). Moreover, if oystercatchers forage mainly on mussels from the upper limit of their size class distribution, they could also influence the composition of mussel size classes available in the long run, so only smaller size classes would be available (i.e. self-trophic downgrading regarding prey size occurred; Hamilton 2000Hamilton D.J. 2000. Direct and indirect effects of predation by common eiders and abiotic disturbance in an intertidal community. Ecol. Monogr. 70: 21-43. https://doi.org/10.1890/0012-9615(2000)070[0021:DAIEOP]2.0.CO;2
). A similar effect is known to be caused by the anthropogenic preference for large prey in hunting and fishing (Soga and Gaston 2018Soga M., Gasto, K.J. 2018. Shifting baseline syndrome: causes, consequences, and implications. Front. Ecol. Environ. 16: 222-230. https://doi.org/10.1002/fee.1794
). Prey of different sizes present different profitability for the predator, depending on the time required for prey handling and the meat content. As stated in the introduction, Hilgerloh and Pfeifer (2002)Hilgerloh G., Pfeifer D. 2002. Size selection and competition for mussels, Mytilus edulis, by oystercatchers, Haematopus ostralegus, herring gulls, Larus argentatus, and common eiders, Somateria mollissima. Ophelia 56: 43-53. https://doi.org/10.1080/00785236.2002.10409488.
suggested that oystercatchers had an optimal median mussel size of 51 mm, and that when the mussels available were smaller than the ideal size, they selected the largest ones available. Interestingly, in our study the overall median length of consumed mussels was 46.86 mm (48.14±7.85; arithmetic mean±SD), close to 51.

As the study oystercatcher population is currently growing, with new colonies being established every year, further studies should be carried out in the future to confirm or amend these preliminary findings. Likely human influence on mussel availability due to collection of juvenile mussels for industrial mussel growth should also be explored within the framework of future plans for the conservation of this expanding oystercatcher population. This problem would be less important if oystercatchers could have access to protected mainland beaches and dune fields in the future for nesting and forage on different prey types (e.g. soft prey from sandy substrates).

Funding sources

This study was linked to project ED431B 2024/23, by which the Xunta de Galicia funded our research group (GIBE).

Authorship contribution statement

Nicolás Ron Arroyo: data curation; formal analysis; writing-original draft. Jorge Mouriño: investigation; data curation. Xan Silvar: investigation. Andrés Bermejo: investigation. Alejandro Martínez-Abraín: conceptualization; methodology; supervision; writing-reviewing and editing.

References