Doctoral Programme on Marine Ecosystem Health and Conservation
 PhD Subject Catalogue Fifth Edition - 2014
Arctic meltdown affects tropical seagrass meadows via migrant shorebird
PhD Code: MARES_14_03:
  • Host institute 1: P6 - Stichting Koninklijk Nederlands Instituut voor Zeeonderzoek (NIOZ)
  • Host institute 2: P8 - University of Gdansk
  • Host institute 3: P13 – University of Aveiro
Research fields:
  • T2 - Understanding biodiversity effects on the functioning of marine ecosystems
  • Włodzimierz Meissner
  • José Alves
  • Theunis Piersma
Contact Person and email: Jan van Gils -

Subject description
The top-down role of consumers in ecosystems has been recognized since long (1). By killing prey, predators relax the competition among surviving prey, thereby promoting per capita growth rate, fecundity and biodiversity (2, 3). Furthermore, predators induce trophic cascades by releasing herbivore pressure on plants (4, 5). New is the realization that consumers migrating seasonally between sites play such steering roles in what then may be seen as globally connected meta-ecosystems (6).
Human impact on higher-order consumers is tremendous due to habitat loss, overfishing, and climate change (7). While species extinctions are community-wide phenomena, it is often the highest trophic levels disappearing first (8), thereby inducing cascading effects throughout the food-web (9). With migrant consumers connecting ecosystems worldwide, there is the realistic but underappreciated threat that human impact on migrants in a disturbed ecosystem may reverberate to other, seemingly undisturbed, ecosystems.
Among anthropogenic impacts on organisms, climate change is considered to be very prominent (10). Although obviously a global problem, some parts of the world are changing faster than others. Notably the Arctic region is warming up at unprecedented rates (11, 12), a phenomenon called ‘Arctic amplification’. Several shorebirds are long-distance migrants breeding in the High Arctic and spending the rest of the year in coastal habitats (13). Most shorebird species are active predators, foraging on macro-benthos for the largest part of the year and on terrestrial invertebrates during the arctic summer, having potentially structuring roles in these ecosystems. Henceforth, migratory shorebirds may carry over effects of rapid climate change to regions that are climatologically more stable.
Taking the red knot (Calidris canutus canutus) as a model species, we propose to study how a phenotypic reduction in body size, induced by Arctic amplification, (A) alters the birds’ diet in the non-breeding season, (B) their survival chances, and (C) how this change may induce a regime shift in their tropical wintering grounds (Banc d’Arguin, Mauritania, West Africa, one of the world’s largest seagrass-based intertidal ecosystems). Smaller bodies are seen as a universal response to global warming (14), but the ecological consequences have yet to be studied, certainly for cases where a shrinking migrant connects a rapidly warming region of the world to a climatologically more stable region. 
Recent analyses have revealed the dramatic effect of timing of High-Arctic snow melt on the growth of red knot chicks. Juveniles intercepted in Poland during their first southward migration are smaller after an Arctic summer that commenced early, and this size-effect is most pronounced in the length of their bill (R2 = 0.50; P = 4e-4; N = 1,886 individuals caught between 1983-2013 (15)). Most likely this is due to a trophic mismatch, with the chick’s arthropod food supply peak advancing more rapidly than their own hatching date, a widespread phenomenon among migrating birds that lack cues of advanced springs (16) (this idea is supported by the fact that Normalized Difference Vegetation Index [NDVI], a proxy for arthropod abundance (17, 18), scales positively with juvenile body size; P = 2e-3 in the same dataset (15)). Once on their intertidal wintering grounds, knots use their bill to detect and retrieve buried mollusc prey (19-21). Stable-isotope analyses revealed that in Banc d’Arguin, shorter-billed knots have difficulties finding enough mollusc prey (22), most likely because many are out of reach. Birds that have been trapped twice in their life have shown us that small juveniles become small adults (e.g. correlation between juvenile and adult bill length: R2 = 0.90; P = 5e-15) (23). Henceforth, the foraging constraints induced by climatic conditions during neonatal development are lasting lifelong (i.e. a so-called silver spoon effect (24)).
However, being well-known for their phenotypic flexibility (25), shorter-billed knots have found a way out by consuming the shallowly buried rhizomes of seagrass (seagrass contribution to diet vs. bill length in 657 individuals caught between 2002-2013 (22): R2 = 0.76; P = 5e-4). In Banc d’Arguin, seagrass (mainly Zostera noltii) is a dominant ecosystem engineer that provides the foundation for much diversity among benthic invertebrates (26, 27). Over the past decade, knots have more than doubled their per capita grazing pressure on seagrass (22).
For a shorebird renowned for its specialized ability to detect (28) and process (29) mollusc prey, a diet of less nutritious seagrass is likely to incur survival costs. Indeed, preliminary stable-isotope analyses (22) suggest that, within our study area, most seagrass is consumed at the site (Baie d’Aouatif) where annual survival rates are lowest (30) (a similar result was recently found in another shorebird species, the black-tailed godwit – Limosa limosa islandica (31)). Also speed of spring migration might be affected by diet, as seagrass-consuming red knots, compared to shellfish-consuming conspecifics, seem to have a higher propensity of making an additional stopover in France when travelling from Mauritania to their High-Arctic breeding grounds (32) (under normal circumstances, French stopover sites are skipped in spring (33)).
In spite of a possible reduction in the total population size of red knots due to High-Arctic climate change, the increase in the per capita grazing pressure on seagrass in Banc d’Arguin is possibly not sustainable. Grazing above-ground seagrass material is usually not affecting seagrass biomass, as leaves show a high degree of compensatory regrowth (34). However, below-ground grazing is known to be detrimental (35), as rhizomes and roots (i) regenerate at a much slower rate, and (ii) form the physical structure of seagrass beds. Due to erosion, even non-grazed patches of seagrass will disappear when surrounded by patches that are grazed below ground (35). Such continued grazing pressures by an altered shorebird phenotype will impair the system’s resilience, possibly pushing the system to a tipping point where seagrass-dominated mudflats teeming with life transform into species-poor bare flats.
Our objective is to study how effects of High-Arctic climate change may be carried over to the knots’ tropical wintering grounds in Banc d’Arguin. More specifically, we will address the following questions:
(A) How is diet in Banc d’Arguin affected by body size?
This will be studied by collecting stable-isotope samples from individual red knots (i.e. by taking a few droplets of blood from their wing vein (36); for which we have approval from the Ethics Committee) and relating this to age, sex and biometrics. More mechanistically, we will carry out functional response experiments with captive birds of variable size and manipulate burrowing depth of bivalve prey in seagrass patches. Over the years, running such type of experiments with captive red knots in Banc d’Arguin (20, 37, 38) has rendered much mechanistic insights in the actual foraging constraints. After the experiments, usually lasting 3-5 weeks, the birds will be released. 
(B) How is survival rate affected by body size and diet?
Since 2002 we have been individually marking the red knot population in Banc d’Arguin by catching annually about 200 birds and giving each bird a unique combination of colour bands. Resighting the marked birds in the field enables us to estimate annual and seasonal survival rate (19, 30, 39). Normally, birds are caught and banded halfway their wintering season, i.e. in November/December. In this PhD project we will catch the birds during and just after their southward migration, by catching birds in Poland (mid August – mid September) and in Banc d’Arguin (September), as we have indications that most mortality among the smallest juveniles takes place in the first half of winter (23). The usual NIOZ resighting expeditions to Banc d’Arguin in November/December will then provide us with the estimates of who survived and who didn’t, which will then be related to diet and body dimensions (such as bill length) as determined earlier in August/September.
(C) What are the top-down effects of seagrass grazing?
Recent theory suggests that the spatial patterning of disturbed (bare) and undisturbed (seagrass-covered) patches might be used as an early-warning signal for a system approaching a tipping point (40, 41). Being highly relevant for the science of conservation ecology, this idea requires rigorous testing in natural systems (42). Our system with natural and experimentally controlled grazing pressure provides an ideal test case. Below-ground grazing pressure by red knots will be controlled for by using exclosures (21) and using captive red knots in enclosures (43, 44). In these plots, grazing pressure and subsequent regrowth will be measured at the level of individual ramets using rhizome and leaf marking techniques (45). Additionally, the response of benthic invertebrates living in these plots will be monitored.
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Expected outcomes
This work will reveal “invisible interactions” that exist between Arctic and tropical food webs, with migrant shorebirds as the connecting agents, and climate change as the “large-scale experimental treatment”. We expect the outcomes of this study to be published in high-ranking journals as body size shrinkage due to climate change is topical, the idea of migrants connecting worlds is novel (1), and seagrass meadows are considered important but globally threatened ecosystems (e.g. note attention for our seagrass-paper in Science (2)).
Besides these immediate scientific outcomes, we expect our research to generate societal spin-offs. For example, our work will improve the understanding of the functioning of one of the world’s largest intertidal seagrass-based ecosystems, the Banc d’Arguin. The people living in Banc d’Arguin, the Imraguen, make their living by fishing traditionally using non-motorized sailboats. Henceforth, their culture, wealth and safety depend critically on the existence of seagrass beds “at their doorstep”. There are strong links between NIOZ and Parc National du Banc d’Arguin (PNBA), the organization managing Banc d’Arguin. Thanks to our work in the past (e.g. the main applicant’s NWO-VIDI project), PNBA is fully aware of the keystone role of seagrass in their park and is striving to protect it. 
Lobbied by Dutch scientists from NIOZ and the University of Groningen, a new research station will be built in Banc d’Arguin, scheduled for 2015. This building will not only host scientists working in Banc d’Arguin, it will also serve as an education center for West-African conservationists and students. The knowledge gained in the proposed project will contribute significantly to this training program. 
Finally, our work will be beneficial to the science-based conservation (3) of birds. Twice a year, millions of migrant birds pass through Europe between their Arctic breeding grounds and their tropical wintering grounds in Africa. This sets European responsibilities to protect these ‘partly European’ globetrotters, which obviously requires knowledge. We know that most mortality in our study population of red knots takes place during winter in Banc d’Arguin, while mortality is almost negligible during summer (4). The proposed work tests the idea that some of the mortality during winter is actually the result of a carry-over effect brought about by High-Arctic climate change. Our work could thereby contribute to the growing awareness that global climate change may actually induce species loss (5). For example, the red knot has now been shortlisted under the US Endangered Species Act, as the first avian species threatened by climate change (6). Note that the proposed work will align closely with other conservation-ecological research projects from involved partners, notably Metawad (NIOZ/Univ. Groningen) and Global Flyway Network (Univ. Groningen/NIOZ). 
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  • 4. J. Leyrer et al., Mortality within the annual cycle: seasonal survival patterns in Afro-Siberian red knots. J. Ornithol. 154, 933 (2013). 
  • 5. A. E. Cahill et al., How does climate change cause extinction? Proc. R. Soc. B 280, 20121890 (January 7, 2013, 2013). 
  • 6. K. Worth, Master of long-distance aviation loses ground. Sci. Am. 310, in press (2014).

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