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Interannual variation in resource abundance has become more unpredictable, and food shortages have increasingly occurred in the recent decades. However, compared to seasonal fluctuations in resource abundance, the influences of interannual variation in resource abundance on the dietary niches of consumers remain poorly understood. Poyang Lake, China, is a very important wintering ground for the globally endangered Siberian Crane (Leucogeranus leucogeranus), White-naped Crane (Grus vipio), and Hooded Crane (G. monacha), as well as the non-endangered Eurasian Crane (G. grus). Tubers of Vallisneria spp., the dominant submerged macrophytes at Poyang Lake, is an important food for cranes. Nevertheless, submerged macrophytes have experienced serious degradation recently. In this study, we used metabarcoding technology to explore the consequences of Vallisneria tuber collapse on the diet compositions, breadths, and overlaps of the four crane species based on fecal samples collected in winter 2017 (a year with tuber collapse) and winter 2018 (a year with high tuber abundance).

Compared to previous studies, our study elucidates crane diets in an unprecedented level of detail. Vallisneria tubers was confirmed as an important food source of cranes. Surprisingly, the grassland plant Polygonum criopolitanum was also found to be an important food source in the feces of cranes. Agricultural fields were important foraging sites for Siberian Cranes, White-naped Cranes, and Hooded Cranes, providing foods that allowed them to survive in winters with natural food shortages. However, the three crane species preferred natural wetlands to agricultural fields when the abundance of natural foods was high. The abundance of Vallisneria tubers, and probably P. criopolitanum, greatly influenced the dietary compositions, breadths and overlap of cranes. During periods of preferred resource shortage, White-naped Cranes and Hooded Cranes widened their dietary niches, while Siberian Cranes maintained a stable niche width. The dietary niche overlap among crane species increased substantially under conditions of plentiful preferred food resources.

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Our study emphasizes the superior quality of natural wetlands compared to agricultural fields as foraging habitats for cranes. To provide safer and better foraging areas for cranes, it is urgent to restore the submerged plants at Poyang Lake. While high dietary niche overlap is often interpreted as intense interspecific competition, our study highlights the importance of taking food abundance into account.

Optimal foraging theory is often used to predict the foraging decisions of animals [20, 21]. According to the theory, when resources are abundant, species should consume the most profitable food items with high nutrition and accessibility while ignoring less profitable foods. When preferred food items become depleted, species add less profitable foods to their diet [22, 23]. Great Knots (C. tenuirostris), for example, changed their diet composition and prey selection to include prey items that were physically more difficult to digest after a severe decline in food abundance and quality [24]. Optimal foraging theory predicts a reduction in dietary niche breadth during seasons of high food abundance and an increasing trend during seasons of low food abundance. This pattern of niche width variation has been observed across a range of taxa, including birds [12, 25], mammals [26, 27], fish [28, 29], and invertebrates [30, 31]. The theory also predicts an increase in dietary niche overlap between species when resources are abundant [7, 32, 33]. The increased overlap may be related to the reduced competitive interaction between species due to great resource availability. For example, there was an absence of dietary niche partitioning among shorebird species at Delaware Bay, USA, when the density of their primary prey Horseshoe Crab eggs was high [34]. Extensive degree of dietary niche overlap has also been revealed among seabird species breeding on the Argentinean Patagonian coast with superabundance of pelagic fish [35].

Understanding how dietary niche changes for any species as fluctuations in food abundance occurs is useful for designating management strategies to preserve biodiversity and ecosystem services [32, 36]. However, most research is focused on the influences of seasonal variation in food abundance on dietary niches [10, 11, 32, 37]. Due to global climate change and increased human disturbance, interannual variation in resource abundance has increased in frequency and intensity, promulgating food scarcity at higher rates in recent decades [38,39,40]. For example, floods that negatively affect submerged plant growth and even lead to mass death of plants have become more frequent at Poyang Lake, China [41,42,43], which may threaten the survival of birds that feed on them [38, 44, 45]. Seasonal variation in food abundance occurs regularly. Animals have evolved strategies to cope with the predictable environmental variation [46]. Interannual variation in food abundance occurs less frequently, although its frequency and intensity have recently increased [38,39,40]. Without sufficient evolutionary time, animals may not adapt well to the interannual variation; thus, it may pose a challenge for many taxa [19, 47, 48].

Cranes are among the most threatened families of birds [49]. Poyang Lake, which is located on the southern bank of the Yangtze River, China, is an important wintering ground for cranes in East Asia (Fig. 1). It supports approximately 98% of the estimated global population of IUCN Critically Endangered Siberian Crane (Leucogeranus leucogeranus), approximately 18% of the estimated global population of Vulnerable White-naped Crane (Grus vipio), approximately 3% of the estimated global population of Vulnerable Hooded Crane, and approximately half of the Chinese population of Eurasian Crane (G. grus) [50,51,52]. With the degradation of lakes in the middle and lower Yangtze River floodplain, Poyang Lake is playing an increasingly important role in crane protection, especially for the Siberian Crane [53, 54]. It has been suggested that other than Poyang Lake, there are no alternative wintering sites for Siberian Cranes remaining in the Yangtze River floodplain [49].

Tubers of Vallisneria spp., the dominant submerged macrophytes at Poyang Lake, is an important food source for cranes [38, 55, 56]. However, submerged macrophytes have degraded seriously in recent decades [57,58,59,60]. They were widely distributed throughout Poyang Lake in previous years, but were restricted to small areas in 2012 [58]. The Vallisneria tuber density and biomass at three sublakes (Dahuchi, Shahu and Meixihu) of Poyang Lake declined greatly in the winters from 1999 to 2017 [57, 60]. The frequency and range of Vallisneria tuber collapse have also increased because of frequently occurring summer flood and autumn drought, extensive aquaculture, declining water quality, and other factors [38, 57, 60].

Tuber collapse has led to dietary and foraging habitat shifts of cranes. For example, the tuber collapses in the winters of 2015 and 2016 drove thousands of Siberian Cranes, for the first time, to switch from foraging in shallow waters they typically used to paddy fields and lotus ponds [57, 61]. Their main foods changed from Vallisneria tubers to rice (Oryza sativa) seeds and lotus (Nelumbo nucifera) rhizomes [62]. Many White-naped Cranes, Hooded Cranes and Eurasian Cranes also moved from natural wetlands to forage in paddy fields [63, 64]. Diet shifts may influence the dietary niche width and overlap between crane species and subsequently the competition level and fitness of cranes. Given the highly endangered status of cranes and the importance of Poyang Lake in crane protection, it is important to understand the consequences of Vallisneria tuber collapse on diets and competition levels among crane species so that effective protection measures can be implemented.

The Siberian Crane is regarded as the most aquatic of all cranes, using wetlands for nesting, feeding and roosting [49, 88]. The high dependence of the species on aquatic habitats was suggested to make it vulnerable to impacts of habitat degradation and to lead its classification as Critically Endangered [49]. At Poyang Lake, Siberian Cranes traditionally fed on tubers of Vallisneria, the dominant submerged macrophytes, in shallow waters and mudflats [89, 90]. In winter 2010, due to a flood-induced Vallisneria tuber collapse, they were observed foraging for P. limprichtii taproots and T. edulis bulbs in grasslands for the first time [38, 44]. In the winters from 2015 to 2017, the diets of Siberian Cranes changed again, with thousands of cranes feeding on rice seeds and lotus rhizomes in agricultural habitats [61, 62, 64].

Similar to Siberian Cranes, a diet shift was also observed in White-naped Cranes. Historically, White-naped Cranes only fed on submerged plants in shallow waters and mudflats of Poyang Lake [91]. Then, driven by the decline of submerged plants, they primarily fed at grasslands and mudflats [87, 91], consuming Vallisneria tuber, T. edulis, P. limprichtii, and Ranunculus polii [55, 87]. Our results indicate that, in addition to T. edulis and P. limprichtii that had previously been reported, the proportions of P. criopolitanum and Carex were also high in the feces. Hooded Cranes were suggested to mainly feed on the grassland plant P. limprichtii through direct observation [86]. Our study indicates that the grassland plants P. criopolitanum and Carex also occupied high proportions in the feces. The dominant food items in the feces of White-naped Cranes and Hooded Cranes varied greatly between the two winters. The variation in dietary composition indicated that the diversity and composition of the grassland plant community might have changed greatly between the two winters. The dietary niche overlap between White-naped Cranes and Hooded Cranes was the highest among the four crane species, aligning with their level of habitat niche overlap, which was also the highest among the species [92]. The high dietary and habitat niche overlaps suggest high competition potential between the two crane species. 006ab0faaa