Dietary Change in Seabirds on Guangjin Island, South China Sea

HOL0010.1177/0959683616660163The HoloceneWu et al. 660163research-article2016

Research paper

The Holocene 8–1 Dietary change in seabirds on Guangjin © The Author(s) 2016 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav Island, South China Sea, over the past 1200 DOI: 10.1177/0959683616660163 years inferred from stable isotope analysis hol.sagepub.com

Libin Wu,1 Xiaodong Liu,1 Pingqing Fu,2 Liqiang Xu,3 Daning Li4 and Yeling Li1

Abstract Quantifying variation in animals’ paleodiet from the fossil record is difficult as a continuous record of their remains is difficult to obtain. Here we assess dietary change in seabirds from Guangjin Island, Xisha Archipelago, South China Sea, by using stable nitrogen isotopes in seabird bones and prey remains collected from a coral sand ornithogenic sediment profile. δ15N of seabird bone collagen varied from 11.7‰ to 14.1‰ (averaging 12.8‰ ± 0.4‰), but that of fish bones and scales showed minor variations. Flying fish and squid are two favorite foods of tropical seabirds, and the average values of muscle δ15N in typical flying fish and squid samples were 9.2‰ and 10.2‰, respectively. Based on nitrogen isotope mass balance calculation, we conclude that flying fish accounts for 80% ± 40% of seabird diet averaged over the past 1200 years, but this prey accounted for only about 37% ± 30% during the ‘Little Ice Age’ (AD 1400–1850). Flying fish averaged up to 88% ± 2% during the ‘Medieval Warm Period’ (AD 850–1200), close to modern observed value of 89.6%. Thus, it appears that seabirds on Guangjin Island mainly preyed on flying fish during warm periods, and shift to squid during cooler periods. Our results suggest that recent global warming and human activities have likely caused a rapid decrease in tropical seabird population and dietary shift.

Keywords δ15N, bone collagen, climate change, fish muscle, paleodiet, Xisha Archipelago Received 20 November 2015; revised manuscript accepted 7 June 2016

Introduction Coral islands, composed of coral debris, are almost all inorganic Dietary change in seabirds can occur with local fishery failures when initially formed. Subsequent seabird activities transfer quan- (Montevecchi et al., 1988), restoration of piscivorous fish popula- tities of nutrient-rich guano to such barren islands (Allaway and tions (Hebert et al., 2008), and the relative availability of school- Ashford, 1984). The existence of nitrogen, phosphorus, and other ing prey (Gaston and Elliott, 2014). Erwin and Congdon (2007) essential elements allows vegetation to develop later. It is important found that when sea surface temperature (SST) declined, terns to focus on seabirds when investigating coral island ecosystems (Sterna fuscata) on the Great Barrier Reef will prey significantly because of their obvious core status in this process. Also, seabirds more on squid. Thus, dietary studies are crucial for understanding are very sensitive to environmental changes, and they have poten- seabird ecology. Traditional methods for studying a wild animal’s tial as monitors of environmental pollution and climate change diet include direct observation, stomach dissection analysis, and (Furness and Camphuysen, 1997; Grémillet and Charmantier, 2010). Furthermore, population size of seabirds, as well as their 1 dietary compositions and genomic structures, showed significant Institute of Polar Environment, School of Earth and Space Sciences, variances because of changes in climate, oceanic, and anthropo- University of Science and Technology of China, P.R. China 2LAPC, Institute of Atmospheric Physics, Chinese Academy of Sciences, genic processes (Emslie and Patterson, 2007; Lambert et al., 2002; P.R. China Nie et al., 2015). We have reported many studies on coral island 3School of Resources and Environmental Engineering, Hefei University ecosystems, especially on seabird population changes. For exam- of Technology, P.R. China ple, Xu et al. (2012) reconstructed the relative variation of seabird 4South China Sea Institute of Oceanology, Chinese Academy of populations by reflectance spectroscopy after applying a new Sciences, P.R. China method to identify the source material levels in coral sand ornithogenic sediments. Recently, Xu et al. (2014) considered the variation Corresponding author: of δ13C and δ15N on bird bone collagen was a response to a shift in Xiaodong Liu, Institute of Polar Environment, School of Earth and Space seabird diet and thus reconstructed a late-Holocene paleodietary Sciences, University of Science and Technology of China, Hefei, Anhui 230026, P.R. China. record from Ganquan Island, and squid probably contributed more Email: [email protected] to the diet of seabirds during 1200–200 BP. However, their data were only relative, not a quantitative analysis, because of the lack Liqiang Xu, School of Resources and Environmental Engineering, Hefei of modern isotopic data. Therefore, quantitatively assessing and University of Technology, Hefei, Anhui 230009, P.R. China. explaining the change of seabird diet is our main focus here. Email: [email protected]

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Figure 1. (a) Map of South China Sea and Xisha Islands (Xisha Archipelago) location showing (b) Yongle Islands and sampling site GJ2 and (c) sampling site GJ2 on Guangjin Island. micro histological analysis of feces (Deloria-Sheffield et al., 2001; mass balance equation may be used to determine the proportion Luo et al., 2012). In recent years, stable isotope analysis had been of flying fish and squid, respectively, if tissues of the seabirds applied because of its superiority, especially for extinct or small and their prey can be recovered to determine their nitrogen isoto- animals (Davis et al., 2012; Fricke et al., 2011). For a consumer pic composition. feeding on two or more types of prey, the composition proportion Nitrogen isotope analyses can be applied to teeth (Sandberg of each prey in the total diet can be calculated by an isotope mass et al., 2014), feathers, bone (Chamberlain et al., 2005), and fish balance equation (Saito et al., 2001). The proportion of prey scales (Wainright et al., 1993). Inamura et al. (2012) and Rous- A (f) can be evaluated quantitatively by only one equation: sel et al. (2013) established positive relationships between fish δδXfpredator =−*+Xfprey A (1 )*δX prey B +∆ X , where X refers to 13C muscles and scales using δ13C and δ15N. Hammond and Savage 15 or N, and ΔX refers to estimated trophic enrichment of the carbon (2009) fed treatment estuarine fish Notolabrus celidotus with a or nitrogen signature, if the consumer only has two kinds of prey, 15N enriched bivalve diet (δ15N = 108.8‰) for up to 90 days which is the simplest case. and examined the integration of the dietary source signature in Stable nitrogen isotopic composition can be used to identify the scale margin, regenerated scale, and dorsal muscle tissues. the trophic level of organisms because of significant nitrogen Riverine fish scales were collected to analyze δ13C and δ15N isotope fractionation, which can cause an obvious increase in variations in the foodweb of two European rivers experiencing δ15N in organisms up the food chain, and this process usually different degrees of anthropogenic pressure; high δ13C values occurs when nitrogenous nutrients transmit from prey to predator in the Scorff River reflected anthropogenic N inputs to the (Hobson, 1999; Post, 2002; Schoeninger and DeNiro, 1984; riverine environment (Roussel et al., 2013). Here, both well- Wada et al., 1991). Wiley et al. (2013) reported that fisheries preserved ancient bone and scale samples have been recovered induced an evident decline in bird trophic level in the Hawaiian from the Xisha Archipelago. We use these tissues to reconstruct Islands over the past 100 years. However, human activities still long-term dietary changes in seabirds on Guangjin Island by seem to influence less the δ15N of fish compared with δ13C (Davis analyzing δ15N. Our results are applicable to understanding the et al., 2015; Gerdeaux and Perga, 2006). According to previous ecology of modern seabirds on this coral island ecosystem and research, the average δ15N value in tissues tends to increase about their future conservation. 3.4‰ with the enhancement of one trophic level (DeNiro and Epstein, 1981; Minagawa and Wada, 1984; Post, 2002), therefore we can estimate the trophic level (TL) of the consumer if we Study sites have known bulk organism δ15N of both consumer and producer The Xisha Archipelago is situated on the northwest of South 15 15 by the equation TLconsumer =N()δδconsumer −+N/producer 3.4 1, and China Sea (Figure 1a), and mainly consists of two parts: the west- nitrogen isotope mass balance equation can be expressed as ern Yongle Islands (Figure 1b) and the eastern Xuande Islands. 15 15 15 δδN*predator =+ffN(prey A 1)−+*Nδ prey B 3.4, if the con- The islands are located in the central tropics and have a typical sumer only has two kinds of prey A and B. However, the latter tropical marine climate, with a year-round high temperature and equation is seldom used independently to calculate diet because an annual average temperature that usually ranges from 26 to of the diversity of an animal’s food source. Fortunately, here we 27°C. The center area of some islands is covered by trees Pisonia encounter the simplest case; seabirds on tropical islands primar- grandis and Guettarda speciosa, and bordered by shrubs Scae- ily feed on predominantly two kinds of prey, that is, flying fish vola sericea. According to previous reports, more than 60 kinds of and squid (Cherel et al., 2008; Xu, 2015; Young et al., 2010), birds, among which Red-footed Booby (Sula sula), Great Frigate- which differ in trophic level. Therefore, the nitrogen isotope bird (Fregata minor), Great Crested Tern (Sterna bergii), and

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Sooty Tern (Sterna fuscata) are important species, have been Analytical methods found to inhabit in the Xisha Archipelago (Cao et al., 2007; We employed both 210Pb (Appleby, 2008) and radiocarbon (accel- Exploration Group of Xisha Islands of Institute of Soil Science of erator mass spectrometer (AMS) 14C) dating to establish the chro- Chinese Academy of Sciences (CAS), 1977). However, at present nology of the profile GJ2. Following the method of Xu et al. most of islands have no bird occupations, except for Dongdao (2010), radioactive measurements of 210Pb and 137Cs were con- Island of the Xuande Islands, where there are still many seabirds, ducted using HPGE gamma spectrometry (AMETEK, GWL- predominantly the Red-footed Booby (Cao, 2005). DSPEC-PLUS). The subsamples in the upper profile were ground Guangjin Island (16°27′N, 111°42′E), named in memory of to a 120 mesh size and then dried to a constant weight at 105°C. the ‘Guangjin’ ship that cruised here in the late Qing Dynasty, is The bulk sediments (5–10 g) were then packed into standard a small coral island on Chenhang reef, and a spit connects counting geometries for gamma analysis. Excess 210Pb activities between Guangjin and Chenhang Islands. The Guangjin Island were determined by total 210Pb activity subtracting the supported 2 has an area of about 0.06 km and ~4.2 m high elevation relative activity, which is in equilibrium with the 226Ra in the sediments, to the present sea level. This island is surrounded by a relatively and all the measurement data were obtained from Gamma Vision high coral sand barrier, leading to the appearance of low-lying software. At the same time, several bird and fish bone samples terrain in its middle part. When the tide is low, most of Guangjin were sent to the University of Georgia for AMS 14C analysis. The Island is exposed and beach rocks around the island protect it AMS 14C dates were then calibrated into calendar years before from erosion. Guangjin Island is covered with thriving vegeta- present, using the INTCAL98 dataset (Stuiver et al., 1998) and tion, and typical plant communities display circular-zonary the CALIB 4.3 program (Stuiver and Reimer, 1993). We choose growth patterns around this small islet. Its interior is mainly −25 ± 20 year as ΔR and assume organic carbon were all marine- covered by trees such as Guettarda speciosa and Pisonia gran- derived because tropical seabirds mainly feed on pelagic fish dis, and bordered by shrubs such as Scaevola sericea, Messer- (Weimerskirch et al., 2008). schmidia argentea, and Morinda citrifolia. Unfortunately, we Bird and fish bones were also sent to the University of Georgia did not observe any seabirds on Guangjin Island during field for collagen stable isotope δ13C and δ15N analyses. The bone was trips. However, a large number of guano pellets, eggshells, and cleaned using an ultrasonic bath. After cleaning, the dried bone bird bones were observed in the widely distributed ornithogenic was gently crushed to small fragments. The chemically cleaned sediment layers, and this discovery could provide strong evi- sample was then reacted under vacuum with 1 N HCl to dissolve dence of past seabird activities there. the bone mineral and release carbon dioxide from bioapatite. The residue was filtered, rinsed with deionized water, and under Methods slightly acid condition (pH = 3) heated at 80°C for 6 h to dissolve collagen and to leave humic substances in the precipitate. The Sample collection collagen solution was then filtered to isolate pure collagen and Our sample sediment profile GJ2 (Figure 1c) was captured from dried. The dried collagen was combusted at 575°C in evacuated/ Guangjin Island to a depth of 86 cm, and a total of 53 bulk sam- sealed Pyrex ampoule in the present CuO. The sample δ13C and ples were taken at an interval of every 1–2 cm. A coarse fraction δ15N were measured using a stable isotope ratio mass spectrome- of sediment samples from an adjacent duplicate pit (about 1 m × ter MAT 251 and expressed as δ13C with respect to PDB, with an 1 m square) with the depth of almost 100 cm was separated at the error of less than 0.1‰, and δ15N with respect to atmospheric air intervals of 1 cm using a 10-mesh stainless steel sieve in situ, and nitrogen with an error of less than 0.2‰. In this study, only δ15N this allowed us to obtain sufficient seabird and fish sub-fossils was used to do analysis for paleodietary reconstruction. such as guano pellets, eggshells, and bones for analysis in the The treatment method of flying fish and squid muscle samples laboratory. Further details and description of sampling were is based on Logan and Lutcavage (2008) and Inamura et al. reported by Xu et al. (2011). During sampling, we observed and (2012). After defrosting the fish and squid samples, dorsal mus- recorded in detail the color, rough grain-size, and material com- cles without skin were then removed with a forceps and knife. position of the sediments. According to observations both in the The muscle was ground into a 20 mesh size using a mortar and field and laboratory, the dominant source material of the bulk pestle after freeze-drying and then each 0.2-g sample was placed sediment is coral sand and the sediment structure is very simple into a 10 mL (1:1) chloroform/methanol solution to extract and because of the weak pedogenesis. The change of lithologic char- remove lipids for more than 12 h. Lipid extraction was performed acters from top to bottom in the profile is as following: the top twice for each sample. After that, the remaining samples were sediment layer contains mostly black fine humus, mixed with dried at approximately 60°C. Ancient and modern fish scales abundant dead leaves and plant roots, a few guano pellets and were treated with 1.2 N HCl for 2 min to remove carbonate and air bones, and then a large number of well-preserved guano pellets dried. The pretreated method before isotope measurement fol- and bones appeared in the middle layer; the bottom layer was pri- lowed that of Estep and Vigg (1985) and Sinnatamby et al. (2007). marily composed of more medium or coarse coral sands and For the isotopic analysis, the well-treated samples and standards fewer organic matter. In the laboratory, we obtained bird bones, were fully combusted and the gases CO2, N2, N2O, and NO were fish bones and scales, guano pellets, and eggshells from the whole separated by a ‘purge and trap’ adsorption column and then sent profile to do chemical analysis. to IRMS MAT 253. Like δ15N in the samples of bird and fish col- For comparison, more than 60 modern squid (Loligo chinensis) lagen, stable isotope composition of muscle and scale samples with different mass were collected by fishermen from Xisha Archi- was expressed in δ notation as the deviation from standards in 15 pelago, and these squid muscle samples can be considered to repre- parts per thousand (‰), δ N =−[(RRsample /)standard 1]×1000, 15 14 sent the typical species depredated by seabirds in the study area where R is the ratio N/ N, and the Rstandard value is based on (Cao, 2005). Here we selected some of these squid for stable isoto- atmospheric air nitrogen. Analytical precision (the standard devi- pic and ecological analyses. At the same time, to well establish the ation) for δ15N is less than ±0.2‰. nitrogen isotope (δ15N) correlation between fish scales and muscles Near infrared (wavelengths 380 to 2500 nm) reflectance spec- in the flying fish (Exocoetus volitans), 25 of these fish were col- troscopy can be used to identify source materials and properties in lected from the study area by fishermen and within the Eastern soils and sediments (Kleinebecker et al., 2013; Summers et al., equatorial waters of the Indian Ocean (5°S–8°N, 85°E–89°E) using 2011). Here, we analyzed the spectral properties of the bulk sedi- a small dredger in 2014. The size and weight of all the analyzed fish ment samples. Following the method of Xu et al. (2012), after samples are almost in the range of seabird food. being dried to a constant weight at a temperature of 105°C, the

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Table 1. AMS 14C dating results of the GJ2 profile on Guangjin Island using bird bones or fish bones recovered from the sediments.

Laboratory no. Sample no. Depth in core (cm) Material Conventional 14C age (BP) Cal. BP (2σ)

16785 GJ2-11 11 Fish bone 630 ± 25 289 (361–259) 16787 GJ2-31 31 Bird bone 730 ± 25 417 (466–309) 16788 GJ2-43 43 Bird bone 1110 ± 25 670 (729–640) 16789 GJ2-51 51 Bird bone 1260 ± 30 829 (912–716) 16790 GJ2-61 61 Fish bone 1250 ± 25 818 (903–734) 16791 GJ2-71 71 Fish bone 1340 ± 25 915 (960–867) 16792 GJ2-80 80 Bird bone 1450 ± 25 1008 (1087–942) 16793 GJ2-91 91 Fish bone 1480 ± 25 1050 (1137–965) 16794 GJ2-100 100 Fish bone 1420 ± 25 970 (1054–922)

AMS: accelerator mass spectrometer.

Figure 2. Chronology of profile GJ2. 210Pb and 226Ra activity versus depth (a), excess 210Pb activity versus depth (b), and Bayesian age-depth model of the profile GJ2 by both 210Pb and 14C dates (c). sub-sample powder was packed into a measuring cell and the dif- applied this dating model for the 210Pb age calculation here. Com- fuse reflectance spectrum of each sample was then acquired on a bined with AMS 14C ages (Figure 2c), sedimentary age varying UV-VIS-NIR recording spectrophotometer by scanning from 380 with depth was calculated using a Bayesian model (Blaauw and to 2500 nm, at the intervals of 1 nm. To calculate relative abun- Christen, 2011; Ramsey, 2009), and the software Bacon 2.2 was dance of source materials, the spectra of three end-members operated in R language. (plant humus, guano, and coral sand) were also investigated. The spectral signal of bulk sediments is a mixture of spectrum of each end-member with a different characteristic spectrum, and thus δ15N of ancient bone collagen and scales spectral mixing modeling can be applied to calculate the percent- C/N of some bone collagen and scale samples was tested. age of guano in the sediments. Although we have not tested all the samples, we can find all the C/N values of the bone collagen samples was within the range Results and discussion 2.9–3.6, indicating adequate preservation for accurate results (DeNiro, 1985), and C/N values of ancient and modern fish scale Chronology of GJ2 samples are nearly equal (2.89 ± 0.05 for ancient samples and Calibrated ages (AD) from both AMS 14C and 210Pb dating pro- 2.87 ± 0.05 for modern samples). In other words, all the samples vide chronology for profile GJ2 (Table 1, Figure 2). 210Pb and we determined were well preserved after deposition. 226Ra activity concentrations versus depth are plotted in Figure Figure 3a illustrates the changes of δ15N values in the bird and 2a. The 210Pb/226Ra equilibrium was reached at 9 cm of the profile fish bone collagen samples and fish scales versus age. The results and the excess 210Pb activities declined exponentially with depth indicate that the bird bone collagen δ15N varies largely versus age, (Figure 2b). Since an exponential pattern is acceptable for the with the relatively low and high δ15N values clearly observed dur- Constant Initial Concentration (CIC) model (Robbins, 1978), we ing the ‘Medieval Warm Period’ (MWP, AD 850–1200) and ‘Little

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Figure 3. (a) Changes of δ15N values in the bird bone collagen, fish bone collagen, and fish scales versus age; and (b) comparison of bird bone collagen δ15N with the proportion of guano in the ornithogenic sediments and age.

Ice Age’ (LIA, AD 1400–1850), respectively. Figure 3b shows the historical relationship between the bird bone collagen δ15N and seabird population size on Guangjin Island, which can be indicated by the change of guano proportion in the bulk sediments (Liu et al., 2011; Xu et al., 2012). The result indicates that the δ15N values in the seabird bones positively correlated with the historical change of seabird populations. There are two possible reasons accounting for this result: the environmental background δ15N value was higher in the LIA than the MWP, or seabirds were feeding at a higher trophic level during LIA since δ15N is usually used to represent trophic level of diet. However, the δ15N values in the fish collagen samples and scales were not high in the LIA. The averaging δ15N of fish bones was 6.3‰ ± 0.4‰ and 6.4‰ ± 1.1‰ in the period of AD 850–1200 and 1400–1850, respectively, and the correlation coefficient between bird and fish collagen δ15N is Figure 4. Relationship between flying fish scale and muscle δ15N. just 0.373 (n = 15, p > 0.1). Thus, we suggest that the changes in bird bone collagen δ15N were not the result of changes in the environmental background δ15N or nitrogen isotope composition in the time, and so the respective proportion of dietary composition can flying fish. Therefore, we hypothesize that the principal cause for be inferred based on the isotope mass balance equation mentioned the appearance of relatively high δ15N values during the LIA is a previously (Saito et al., 2001) dietary shift to a higher trophic level, which was likely because of 15 15 15 the change of diet composition discussed below. δδN=S ff*NA +(1)− *Nδ B +3.4 (1) According to the modern survey data in the Xisha Archipelago, 15 15 15 at present the Red-footed booby (Sula sula) has the largest popula- where δ NS is seabird bone collagen δ N, δ NA is flying fish 15 15 15 tion on Dongdao Island where it is well protected now. Like many muscle δ N, δ NB represents squid muscle δ N, and f is the pro- other kinds of tropic seabirds here, including Great Frigatebird portion of flying fish preyed upon by the seabirds. Here, we chose (Fregata minor), Great Crested Tern (Sterna bergii), and Sooty the optimal solution for the value of f when f is greater than 1 or 15 Tern (Sterna fuscata), this booby feeds mainly on flying fish and smaller than 0, so f ∈ [0, 1]. Since δ NS had been measured squid, averaging 89.6% and 10.4% in biomass in their diet, respec- directly, to determine f in the next step we need to know values for 15 15 tively (Cao, 2005; Yin et al., 2008). Considering the fact that the δ NA and δ NB. tropical seabirds on the Xisha Archipelago have a similar dietary composition and mainly prey on flying fish and squid (Cao, 2005; 15 Cherel et al., 2008), we combine multiple species under the single Flying fish and squid muscle δ N category of ‘seabird’ that occupied Guangjin Island as a whole to Neither flying fish nor squid have produced ancient muscle sam- analyze their dietary change. In general, squid is positioned at a ples. Fortunately, there are sufficient fish bones and scales, relatively high trophic level compared with flying fish (Bugoni assumed to be flying fish; those are well preserved in the ornitho- et al., 2010). Based on the change of δ15N values in the seabird genic sediments. Thus, we can establish the mathematical rela- bones, we inferred that the seabirds on Guangjin Island might prey tionship of δ15N between the fish muscle and bone or scale, and 15 on more squid during the LIA than during the MWP. In the follow- then we can reasonably infer the δ NA in the flying fish muscle. ing section, we quantitatively reconstruct the proportional change Considering the difficulty and high cost to determine bone colla- of flying fish and squid in the dietary composition of the ancient gen δ15N, here we attempted to establish a relationship between seabirds. fish scale and muscle δ15N using 25 flying fish. Figure 4 shows We assumed that the dietary components of seabirds (S) are the model yx=1.473×− 0.692, where x and y mean scale and predominantly composed of flying fish (A) and squid (B) all the muscle δ15N, respectively. The average of ancient fish scale δ15N

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15 15 Figure 5. Average δ N values in flying fish muscle (δ NA), squid 15 15 muscle (δ NB), ancient bird bone collagen samples (δ NS), and prey 15 15 15 δ NP (δ NP = δ NS – 3.4). Figure 6. Proportion f (%) change of flying fish in the diets of seabirds related to the SST anomaly (°C) in MWP, LIA (this study), and the present time (Cao, 2005; Yin et al., 2008). The data for the was 6.7‰ ± 0.7‰ (n = 27), and using the above mathematical SST anomaly are redrawn from Wei et al. (2004) and Yan et al. (2014, model we inferred that the average of ancient fish muscle samples 2015). 15 δ NA was 9.2‰ ± 1.0‰. SST: sea surface temperature. Ancient squid remains are hard to identify, so we chose modern representative samples to replace them. Squid collected from the Xisha sea area were weighed and measured for their length As shown in Figure 6, the respective proportions (f) of flying fish (DML, dorsal mantle length, Field et al., 2007); 15 of them with in the diets of seabirds are 88% ± 2%, 37% ± 30%, and 89.6% different mass were analyzed for muscle δ15N. There is a strong (Cao, 2005; Yin et al., 2008) in MWP, LIA, and the present time, correlation between squid mass and length and from this fact we corresponding to the warmer, cooler, and warm climate periods, can estimate the mass and DML of squid we have measured that respectively. Therefore, we can conclude that the relatively warm are evenly distributed from 40 to 250 g and 8 to 18 cm, respec- climate was favorable for the seabirds to prey upon flying fish in tively. The average squid mass was 110.6 ± 59.6 g and the average the Xisha region. 15 muscle δ NB was 10.2‰ ± 0.4‰. Indeed, with current global warming, the present Xisha sea region has been warming, and the modern ecological data from field observations and statistical analysis in the Xisha Archipelago Quantitative dietary change of seabirds during the have shown that the flying fish is the main dietary component of past 1200 years seabirds inhabiting Dongdao Island. Thus, it is reasonable to infer As discussed above, the data we need to determine paleodietary that the seabirds occupying this island during the warmer MWP changes in seabirds from the Guangjin Island are available. The should predominantly prey upon flying fish. However, when the 15 flying fish muscle mean δ NA is 9.2‰ ± 1.0‰, and the squid climate became cooler in the LIA, the feeding behavior of seabirds 15 muscle mean δ NB is 10.2‰ ± 0.4‰, and thus it is apparent that in the Xisha Archipelago might have exhibited a large change as the squid has relatively high δ15N. For the ancient bird bone sam- the squid became their main dietary source. Up to now, the exact ples retrieved from the GJ2 ornithogenic sediments, their average cause for the large dietary shift from flying fish to squid with the collagen δ15N is 12.8‰ ± 0.4‰, and by subtracting 3.4‰, it is cooling climate remains a challenge for us. The possible explana- 9.4‰ ± 0.4‰, which falls between the end-member values of two tion is that the seabird population reached a peak during the LIA, prey mentioned above (Figure 5). and the flying fish might have been insufficient for so many sea- According to the isotope mixing model, we used the end- birds as prey, and this might have led to the change of feeding member values mentioned above in formula (1) and obtained the behavior in the tropical seabirds. Human activities have the same 15 following formula: δ NS =*ff9.2+(1− )*10.2+3.4. Thus, the effect from global warming in terms of causing seabird population proportion (f) of flying fish in the dietary composition of ancient declines. In modern times, although the population of both flying 15 seabirds can be calculated as following: f =−(13.6 δ N)S /1.0. fish and squid decreased as a consequence of human activities Over the past 1200 years, the mean proportion of flying fish that (Cao, 2005; Myers and Worm, 2003), seabird populations seabirds preyed upon was 80% ± 40%, indicative of a large vary- decreased more significantly, and this may also cause a dietary ing range. As illustrated in Figure 6, the proportion of flying fish shift. In addition, since flying fish is also an important food source in the diet of seabirds displayed considerable change in the cli- for epipelagic ferocious fish (Wei and Chen, 1982), modern devel- mate periods of the LIA, MWP, and modern warming period. oped fisheries have caused a decline in the population of tunas, Therefore, it can be inferred that the paleodietary composition of dolphin fish, sailfish, and others, resulting in more flying fish seabirds has experienced considerable fluctuation during the past available for seabirds, and this may lead to a dietary shift by sea- 1200 years, possibly related to climate change in the study area. birds. As a result, the proportion of flying fish in the dietary com- During the past 1200 years, the time stages of AD 850–1200 position increases more rapidly now, which manifests in the fact and 1400–1850 are generally considered to be part of the MWP that the present SST is still far from that during the MWP, but f (Liang, 2008) and LIA (McGowan et al., 2013), respectively, and almost approaches the same value. That is to say, both global the temperature during the MWP was higher than in the LIA. warming and human activities accounting for global change is Indeed, some results have shown that the Xisha region experi- reflected in tropical seabird diets in the Xisha Archipelago. enced a relatively low temperature during the LIA compared with the MWP and modern period. If the SST anomaly in Xisha Archi- pelago in AD 1990–2000 (present time) was 0 ± 0.37°C based on Conclusion instrumental data, it was 0.89 ± 0.65°C in AD 990 ± 40 based on The predominant prey items of tropical seabirds in the Xisha Tridacna gigas studies and −1.08 ± 0.36°C in AD 1405 ± 51 Archipelago are assumed to be flying fish and squid, and histori- based on coral studies (Wei et al., 2004; Yan et al., 2014, 2015). cally their diets did not remain stable as the proportion of these

Downloaded from hol.sagepub.com at CORNELL UNIV on July 30, 2016 Wu et al. 7 prey varied considerably during the past 1200 years. In the MWP, DeNiro MJ (1985) Postmortem preservation and alteration of in seabirds mostly preyed upon flying fish, similar to today, and con- vivo bone collagen isotope ratios in relation to palaeodietary sistent with warmer climatic conditions and smaller seabird popu- reconstruction. Nature 317: 806–809. lations. In contrast, the seabirds mainly preyed on squid and the DeNiro MJ and Epstein S (1981) Influence of diet on the distribu- proportion of flying fish decreased during the LIA corresponding tion of nitrogen isotopes in animals. Geochimica et Cosmo- to cooler climatic conditions and larger seabird populations. Thus, chimica Acta 45: 341–351. the shift in seabird diet might be attributed to their population Emslie SD and Patterson WP (2007) Abrupt recent shift in δ13C change. Both global warming and human activities caused mod- and δ15N values in Adélie penguin eggshell in Antarctica. Pro- ern seabird dietary changes close to those in the MWP about 1000 ceedings of the National Academy of Sciences of the United years ago. Unfortunately, the probable reason for this change was States of America 104: 11666–11669. not an increase in flying fish populations, but a rapid decline in Erwin CA and Congdon BC (2007) Day-to-day variation in sea- seabird populations. surface temperature reduces sooty tern Sterna fuscata foraging success on the Great Barrier Reef, Australia. Marine Acknowledgements Ecology Progress Series 331: 255–266. The authors are especially grateful to Professor Steven D Emslie Estep MLF and Vigg S (1985) Stable carbon and nitrogen isotope for his improvement in the manuscript and contributions to tracers of trophic dynamics in natural populations and fisher- improving the English. 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