Sage Journals: Discover world-class research

Abstract

The Eurasian Spoonbill Platalea leucorodia is currently experiencing an increasing population trend in Western Europe and colonising areas in its breeding range. In this study we assessed the diet and trophic ecology of spoonbill chicks in Portuguese colonies (Ria Formosa and Tagus Estuary) occupied at different years during the population expansion in the country. We accomplished this by combining diet analysis with blood and feather stable isotopic analysis. Spoonbills from the Portuguese colonies relied mainly (but not exclusively) on crustaceans (Ria Formosa = 75%, Tagus Estuary = 72.5%) and fish (Ria Formosa = 17.11%, Tagus Estuary = 37.50%) to feed their chicks. Crustaceans seems to be the most important prey group. Nevertheless, chicks from Ria Formosa were fed with prey from a higher trophic level than chicks from Tagus Estuary. In both colonies chicks were fed with available in habitats near the colony, although in Tagus Estuary most prey originated from freshwater habitats. Diet of chicks remained constant through the development period and the proportions of crustaceans and fish consumed differed from other colonies elsewhere in Western Europe (Spain and the Netherlands). We conclude that in Portugal, spoonbills feed their chicks with prey commonly found in the vicinity of colonies. Prey originating from artificial habitats, particularly the invasive Louisiana crayfish Procambarus clarkii in the more recently occupied colony, were the most important items in the diet of chicks.

Keywords

population expansion trophic ecology saltpans

Introduction

Several waterbird species are increasing in numbers in Europe.¹ There are multiple potential drivers for the expansion of waterbirds, with the main factors suggested being the increment in legal protection of species and habitats.^2,3 Another likely contributor to this trend is the creation of artificial wetland habitats such as rice fields, saltpans and fishponds that can act as alternatives to natural habitats.⁴ These habitats are particularly relevant as foraging habitat, once they can provide high abundance of food resources during the breeding season.^5–8 Finally, the occurrence of exotic species that have the potential to become profitable food resources can also be regarded as a potential contributor to waterbird expansion. A remarkable example being the Louisiana Crayfish Procambarus clarkii that has become part of the diet of several European Ardeidae species.^9,10 The Eurasian Spoonbill Platalea leucorodia is a migratory waterbird, and the subspecies Platalea l. leucorodia breeds in Europe and winters across a wide latitudinal range, from south Europe to Senegal (Africa), using mostly coastal wetlands in both continents.¹¹ Spoonbills are one of these waterbird species that are increasing in numbers³ and (re)colonising areas across the breeding range.¹²

In Portugal, breeding spoonbills were absent until 1988, despite historical records of breeding pairs in the 17^th century.¹³ Portugal was always a key area for spoonbills during stopover and winter,¹⁴ and in 1988 the first returning breeding pairs were recorded in the area of Paúl do Boquilobo.¹⁵ Ria Formosa was the next site to be recolonised only five years later,¹⁴ and currently ten breeding colonies are known to exist in Portugal.¹⁶

The breeding ecology and dietary choices of Eurasian spoonbills is well documented, especially for populations from the traditional European colonies, in the Netherlands Wadden Sea and in Spain (e.g. 17–20). It is well known that the species forages in shallow waters, varying from saline to freshwater, mostly feeding on small fishes, crustaceans, amphibians, and other small invertebrates.^17,18,20 In contrast, information from other colonies remains extremely scarce, with only one more study available from Germany, but also referring to the Wadden Sea.²¹ In order to investigate potential drivers of the increasing numbers in Portugal, as well as the contribution of dietary sources in making recently colonised potentially sites attractive for the species, we aimed to unravel chick diet and trophic ecology in traditional and recently established colonies in the country. Specifically, we assessed chick diet in Ria Formosa, one of the first Portuguese colonies (occupied since 1993), and in Tagus Estuary, a more recently occupied location (established in 2013), characterized for being close to an extensive area of rice fields. The major aim was to assess the diet and trophic ecology of spoonbill chicks. Using traditional dietary methods, we (1) determine diet composition for chicks of both colonies and predict that in Tagus Estuary spoonbills would rely on the invasive Louisiana Crayfish that is abundant in the nearby rice fields. We then use stable isotope analysis on blood and feathers to (2) provide a more comprehensive assessment of the diet during the entire chick growth period and to determine the origin of prey (freshwater or saltwater) and the dietary niche width. We hypothesise that chicks from the Tagus Estuary would be fed with prey items from both saline and freshwater habitats (as adults are known to use the rice fields) and, therefore, should present a larger niche width than birds from Ria Formosa. Finally, we compare the diet of chicks in these two colonies to that of European colonies in Spain and the Netherlands (compiled from published sources) and explored possible changes in the diet of chicks along their development (using the stable isotope date) as this seems to be important in the Netherlands (at least in late born chicks).

Methods

Study sites and sample collection

We selected two Portuguese breeding colonies (Figure 1) considering accessibility to the nests while minimizing the disturbance to breeding birds. The colony in Ria Formosa Natural Park (RF) (36° 59’N, 7° 55’W) represents the oldest colonies in Portugal (occupied since 1993). It is located inside a coastal protected area, separated from the Atlantic Ocean by a system of small barrier islands and sand banks, encompassing several habitats such as marshes, intertidal flats, fresh and brackish lagoons, saltpans, dune banks and agricultural fields. The colony in the Tagus Estuary Reserve (TE) (38°49’N, 8°59’N) represent recent colonised sites (established in 2013). The Tagus Estuary comprises a large diversity of habitats, including estuarine open waters, intertidal flats, alluvial agriculture fields, where the rice is one important culture, saltpans, salt marshes and reed beds. Both colonies are located within Special Protection Areas (SPA) for birds under the birds directive of the European Union (2009/147/EC) and are also inscribed in the Ramsar Convention. Both colonies have similar habitats in their surroundings, the difference being the presence of extensive rice fields around the Tagus estuary that are absent in the Ria Formosa.

Figure 1.

Location of the two spoonbill breeding colonies sampled in Portugal and colonised in different periods: a) Tagus Estuary (more recently occupied colony), with rice fields shaded in black and b) Ria Formosa (traditional colony), with saltpans shaded in black. Stars indicate the location of each colony at country (black) and wetland (whiter) scale. Data from Corine Land Cover 2018.

During the 2017 breeding season we visited the Ria Formosa colony twice (in May and late June) and the Tagus Estuary colony once (in early July), and again both colonies once in 2020 (in June). In 2017 we collected 150µl of blood from the brachial vein (TE= 11, RF=13) and the 5th primary feathers (cut at the base) of pre-fledging spoonbill chicks (TE=4, RF=28) from different nests in the colony. Blood and feathers were stored in eppendorfs (containing alcohol 70%) and plastic bags, respectively, until stable isotope analysis (see below). During these visits we also collected regurgitations and fresh faecal samples opportunistically, as spoonbill chicks usually regurgitate spontaneously when handled.¹⁹ Whilst the number of fresh faecal samples collected was larger in 2017 (TE=5, RF=5) than in 2020 (TE = 1, RF = 0), this was the opposite regarding regurgitations (2017: TE = 1, RF = 6; 2020: TE = 3, RF=11). In Ria Formosa we could also collect dry faecal samples from the nests (RF=11) in 2017. These dry faeces are usually deposited in nest cups and are clearly different than fresh faeces. All regurgitation and faeces samples were stored in plastic bags and frozen (at -20°C) until laboratorial analysis.

Diet

To reconstruct the diet of chicks we searched for prey items with a stereomicroscope (Wild Heerbrugg M3B) in regurgitations and faeces. When fish and crustaceans were found almost intact, they were identified to the lowest taxonomic level (using a stereomicroscope at 40x magnification). Prawns were identified based on the identification key proposed by González-Ortegón and Cuesta,²² and fish otoliths were identified following published sources.^23,24 Other smaller remains (often very small fragments) were grouped by colour: dark red parts were considered as belonging to Louisiana Crayfish (that has a red exoskeleton) and orange parts considered as remains of other crustaceans (shrimps, prawns or crabs). These small remains were only considered for frequency of occurrence. Small gastropods, bivalves and vegetal matter were not identified to lower taxa since they were possibly ingested accidentally. We calculated numerical frequency (number of estimated individual prey based on prey fragments) using only the regurgitation samples due to the low detectability of some prey on faeces samples^25,26 which could bias the results. Faecal samples were thus only used to estimate frequency of occurrence. Results present prey at family level, unless otherwise indicated.

Stable isotope analysis

We used stable isotope analysis of carbon (C) and nitrogen (N) to infer the dietary space of chicks during the entire chick development. Stable isotopic ratio of carbon (δ¹³C) and nitrogen (δ¹⁵N) present in consumer’s tissues are correlated to those of their diet items in a predictable way: δ¹⁵N increases approximately 3 to 5 parts per thousand (‰) between successive trophic levels ^27–29; while δ¹³C discriminates between freshwater and marine items, with lower values originating from freshwater habitats.^30–32 We sampled ca. 25 day-age chicks, and analysed the stable isotopes form: blood, to attain information concerning their entire growth period until that moment ^33,34; and of different parts of the primary feathers (base and tip) reflecting different periods within the initial 25 days of live,^35–37 that allow us to compare between earlier (tip) and later (base) phases of chick development. We did not analyse the middle part of the feather to ensure the necessary transition from early to late phase of chick growth.

Blood samples were collected into an empty eppendorf tube and dried at 50°C during 48h leaving whole blood solid particles. From each 5^th primary feather we extracted two sections: one from the base of the feather (close to its calamus), reflecting the later chick development phase, and another from the tip, reflecting the earlier chick development phase. Feather sections were cleaned in 2:1 chloroform and methanol solution to remove surface impurities and lipids and dried at 60°C for 24 hours. Finally, nitrogen and carbon isotopic ratios were measured by continuous flow-isotope ratio mass spectrometry (CF-IMRS). Results were expressed in δ notation as result of the equation:

δ^{13} C o r δ^{15} N = [(R s a m p l e / R s t a n d a r d) - 1] \times 1000,

where R=¹³C/¹²C or ¹⁵N/¹⁴N and standards were the PeeDee Belemnite (PDB) in the case of δ¹³C, and atmospheric nitrogen (N₂) in the case of δ¹⁵N. Carbon and nitrogen measurements had an analytical precision of 0.2‰.

Data analysis

Feather isotopic results were corrected to account for different isotopic assimilations of the tissues using the procedure described in Cherel 2014,³⁴ thus enabling to compare those with the results of blood. We first compared δ¹³C and δ¹⁵N values of isotope samples from Ria Formosa with the ones from Tagus Estuary using one way analysis of variance (ANOVA) for Carbon and the Kruskal-Wallis test to compare values of Nitrogen (as this data was not parametric). Next, we compared (within colony) the values of δ¹³C and δ¹⁵N in the different tissues, using ANOVA in all cases except for Carbon in Ria Formosa and Nitrogen in Tagus Estuary were Kruskal-Wallis test was used. Significant differences between groups were investigated with post-hoc tests (Tukey test for ANOVA and Pairwise Wilcoxon tests for Kruskal-Wallis).

To assess the isotopic niches of spoonbill chicks from the different colonies and periods (i.e. sampled tissues), “SIBER”, Stable Isotope Bayesian Ellipses in R,³⁸ was used to calculate the area of standard ellipses (SEAc) corrected for unbalanced and small sample sizes.³⁹ In addition, we calculated the Bayesian estimates of the standard ellipses (SEA_B) to test for differences in size of niche widths.³⁹ All statistical analyses were performed in R environment.⁴⁰

Results

Diet

Samples from both regurgitations and faeces originating from Ria Formosa and Tagus Estuary were mostly composed by crustaceans (of order Decapoda) and fish (Table 1). Other prey items were gastropods, isopods, and insects. Crustaceans occurred in all samples from both colonies and years. Overall, all unidentified crustacean from regurgitations belonged to the order Decapoda and were mostly shrimps (91.67%) and were always most frequent in the regurgitations samples than fish. In Ria Formosa, the most frequent identified crustaceans (at species level) in 2017 was Carcinus maenas (50%) whereas in 2020 it was Palaemon elegans (62.96%) (Figure 2). Procambarus clarkii (the only identified species from the Cambaridae family), which was absent from Ria Formosa, was present in all dietary samples from Tagus Estuary. The only other crustacean identified in the Tagus was P. varians (Figure 2). The occurrence of fish in Ria Formosa samples was constant in both years (54.55%), yet the numerical frequency differed between 2017 (22.64%) and 2020 (14.14%). All regurgitations from the Tagus Estuary of 2020 included fish, whereas the single sample from 2017 was only composed by P. clarkii. The numerical frequency of fish was higher in regurgitations from Tagus Estuary (2020) than from Ria Formosa. In the Tagus, identified fish belonged to the Gobiidae and Poeciliidae families whereas in the Ria Formosa, the most frequent identified prey belonged to the Gobiidae family in both years (2017: 75%, 2020: 66.67%) (Figure 2). The families Atherinidae and Mugilidae were only identified in faeces samples, however, Atheneridae was the most frequent identified family of fish in faeces from Ria Formosa (69.23%). In these samples we were only able of identifying fish otoliths, as other prey items were very digested.

Table 1.

Percentage of occurrence of each prey item (at family level) in spoonbill chick regurgitations and faeces (N_RF = 33, N_TE = 10) and numerical frequency of prey items in regurgitations (N_RF = 152, N_TE = 48) from the Ria Formosa (RF) and the Tagus Estuary (TE). Category “Others” includes gastropods, isopods and insects.

	Ria Formosa						Tagus Estuary
	% Occurrence			Numerical frequency			% Occurrence			Numerical frequency
	2017	2020	Total	2017	2020	Total	2017	2020	Total	2017	2020	Total
N	22	11	33	53	99	152	6	4	10	10	38	48
Fish	54.55	54.55	54.55	22.64	14.14	17.11	0.00	75.00	30.00	0.00	47.37	37.50
Atherinidae	22.73	0.00	15.15	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00
Mugilidae	4.55	0.00	3.03	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00
Sparidae	9.09	9.09	12.12	3.77	3.77	2.63	0.00	0.00	0.00	0.00	0.00	0.00
Batrachoididae	4.55	0.00	3.03	1.89	0.00	0.66	0.00	0.00	0.00	0.00	0.00	0.00
Gobidae	40.91	27.27	36.36	16.98	4.04	8.55	0.00	25.00	10.00	0.00	13.16	10.42
Poeciliidae	0.00	0.00	0.00	0.00	0.00	0.00	0.00	25.00	10.00	0.00	10.53	8.33
Unidentified	13.64	36.36	21.21	0.00	8.08	5.26	0.00	75.00	30.00	0.00	23.68	18.75
Crustacean	100.00	100.00	100.00	60.38	82.83	75.00	100.00	100.00	100.00	100.00	52.63	62.50
Crangonidae	9.09	0.00	6.06	7.55	0.00	2.63	0.00	0.00	0.00	0.00	0.00	0.00
Palaemonidae	81.81	100.00	87.87	11.32	49.49	36.18	0.00	75.00	30.00	0.00	44.74	35.42
Portunidae	9.09	18.18	18.18	11.32	5.05	7.24	0.00	0.00	0.00	0.00	0.00	0.00
Cambaridae	0.00	0.00	0.00	0.00	0.00	0.00	100.00	100.00	100.00	100.00	7.89	27.08
Unidentified	100.00	100.00	100.00	37.74	28.28	31.58	0.00	0.00	0.00	0.00	26.32	20.83
Others	13.64	18.18	15.15	16.98	3.03	7.89	0.00	25.00	10.00	0.00	0.00	0.00

Figure 2.

Detailed composition of the frequency of identified crustacean species (a) and fish families (b) in spoonbill chicks regurgitations from both colonies and years. Ria Formosa is identified in light grey, and Tagus Estuary in dark grey. 2017 is presented in a plain colour, and 2020 in a diagonal striped pattern. In 2017, in the Tagus Estuary, we did not find any fish remains in the regurgitation samples.

Stable isotope analysis

Stable isotope ratios from chicks (Table 2) differed between colonies. δ13C was higher in Ria Formosa (mean = -14.98 ± 0.13) than in Tagus Estuary (mean = -24.22 ± 0.31) (F_1,86 = 1016, p < 0.001). And δ15N was also higher slightly in Ria Formosa (mean = 13.44 ± 0.11) than in Tagus Estuary (mean = 12.79 ± 0.31) (H(1) = 5.85, p=0.016).

Table 2.

Stable isotope ratio values for δ¹³C and δ¹⁵N (mean ± SD) from blood and feathers from spoonbill chicks of Ria Formosa and Tagus Estuary. N is the number of each tissue samples analysed.

Tissue	Ria Formosa			Tagus
Tissue	N	δ¹³C	δ¹⁵N	N	δ¹³C	δ¹⁵N
Blood	13	−14.46 ± 0.62	13.2 ± 0.62	11	−23.65 ± 1.42	12.43 ± 1.43
Feather base	28	−15.22 ± 1.10	13.66 ± 0.99	4	−25.27 ± 0.37	12.87 ± 1.10
Feather tip	28	−14.98 ± 1.09	13.33 ± 0.83	4	−24.77 ± 1.06	13.71 ± 1.02

When comparing tissues within colonies we found no differences between δ15N of tissues from Ria Formosa (F_2,63 = 1.62, p= 0.21) and the Tagus Estuary (H(2) = 4.07, p=0.13). But for δ13C, whilst we found no differences for Tagus Estuary (F_2,16= 3.08, p = 0.07), those were present in Ria Formosa (H(2) = 7.41, p = 0.02), with Kruskal-Wallis test identifying differences only between feather base and blood (feather base/blood p = 0.02, feather tip/blood p = 0.12, feather tip/feather base p = 1).

Niche width estimated as SEA_C was wider in the Tagus (Figure 3). Indeed, SEA_B size of blood was significantly larger in the Tagus than in Ria Formosa (p=0). Regarding niche width of feathers there was no difference between the tip and the base in Tagus (p = 0.09) or in Ria Formosa (p = 0.25).

Figure 3.

Isotopic niches of spoonbill chicks in Ria Formosa (circles) and Tagus Estuary (triangles) based on Jackson et al. (2011) applied to Stable isotopic ratios in blood (black) and feather tip (earlier stage – light grey) and base (later stage – dark grey) sections. The area of the standard ellipses (SEAc) is represented.

Discussion

Diet

Spoonbills from Ria Formosa feed their chicks mostly with crustaceans of the genus Palaemon, which are present in the lagoons and saltpans in the vicinity of the colony, likely making this an easy and predictable prey. In fact, many other birds, such as Calidris alpina and Sterna albifrons, also feed on these prawns in Ria Formosa.^41,42 Nevertheless, and probably due to the small biomass of these crustaceans,⁴³ spoonbills also provided their chicks with fish, that are of higher energetic value.^20,44 The most consumed fish families, Atherinidae and Gobbidae are common in Ria Formosa^45,46 suggesting that these may also be a relatively easy to catch prey due to their availability.

On the Tagus Estuary the general chick dietary pattern was similar, with high occurrence of crustaceans. The main difference was the presence of the Louisiana Crayfish in all samples, which is known to be very common in the rice fields nearby the colony.⁴⁷ This result is in accordance with the reported diet from other waterbird species in southern Europe that also consume this invasive species.^9,10,48 To the best of our knowledge, only two other studies confirmed the ingestion of this crayfish by spoonbills, both in South-West Spain: in Odiel Estuary and in Guadalquivir marshes.^10,18 The widespread consumption of this previously absent prey may be advantageous, as some waterbird species like the Eurasian Bittern Botaurus stellaris and the Grey Heron Ardea cinerea, show positive population trends as the consumption of this prey increased.^10,49 However, for other species, such as the Glossy Ibis Plegadis falcinellus in Doñana (South Spain), the consumption of this crayfish alone cannot underline the reported population increase, as this has not been described as an important prey in is diet,⁵⁰ although this may not be the case in more recent years and at other wetlands where the species has been frequently observed consuming this crayfish (pers. obs). Other seemingly important prey in Tagus Estuary are fish of the families Gobidae and Poeciliidae, and the shrimp Palaemon varians. Both prey types are very common in Tagus Estuary, especially the family Gobidae^51,52 and P. varians, is present both in intertidal mudflats and in saltpans.^52–54

Stable isotope analysis

Trophic niche of earlier and late chick development phase (assessed by sampling different parts of feathers) revealed no differences on both colonies, implying a similar diet of the chicks since feathers start to be developed. However, blood δ¹⁵N in Ria Formosa differed from feather base. We did not expect this result but it may be possible that spoonbills chicks in Ria Formosa changed their diet only few days before sampling collection and the quicker turn over of blood⁵⁵ reflected that. The small difference in δ¹⁵N values between colonies may corroborate the differences found in dietary analysis. Ria Formosa highest δ¹⁵N indicates that spoonbills chicks from there are fed with prey of a higher trophic level than chicks from Tagus Estuary.^27–29 Indeed, the higher occurrence of the Louisiana crayfish may result in lower δ¹⁵N values in Tagus Estuary, as this crustacean occupies a lower trophic level than fish. Regarding the differences in δ13C values between colonies suggest that spoonbills feed their chick from prey items obtained in the vicinity of the colonies. This is because higher values of δ13C indicate marine prey, which will occur around the saltmarsh island in Ria Formosa. i.e. around their colony, whereas the signature of freshwater prey is indicated by lower δ13C values,^30,32,56 suggesting that spoonbills in the Tagus Estuary depend less on the intertidal areas that also surround their colony, but more so on the vast rice-fields present in the vicinity of the colony. However, this pattern is less clear in the dietary analysis, where P. varians were common, suggesting that prey from more saline habitats is also taken. In accordance, the difference in sizes of niche width between colonies suggest indeed a more diverse diet in the Tagus Estuary colony^57,58 that was not detected based on the diet samples alone. This is likely a limitation of such analysis particularly when sample sizes are relatively small. In fact, the use of regurgitations to infer diet is always limited, representing a snapshot of the diet as it only includes items consumed on that day. It is also further constrained by different digestive rates of prey, which leads to the impossibility of identifying some prey items and the total absence of others.^25,59 Regarding faeces samples, this disadvantage is even larger because only hard parts are preserved.^25,59 The analysis of dry faeces constitutes another uncertainty of this study because they can remain in the nests for several years. This means that the dry faeces that we collected in Ria Formosa can originate from previous seasons, which may justify the presence of two families of fish (Atherinidae and Mugilidae) in only this type of samples. In order to further understand diet variation a larger number of samples should be collected and analysed, combined with isotopic SIAR mixing models^20,60,61 to estimate the percentage of each prey type.

Comparison with European traditional colonies

We found that in Portuguese colonies spoonbills appear to consume more crustaceans than fish, contrary to what has been described for traditional Dutch and Spanish colonies, where spoonbills heavily rely on small fish.^18,20 Also, in Germany, Enners 2020,²¹ found a diet similar to the traditional colonies with an higher consumption of fish over crustaceans. The results of stable isotopic analysis were in accordance with this because the values of δ15N from chicks of Portuguese colonies were overall lower than values found in studies from Dutch and German spoonbill chicks.^20,21,37 However, Veen 2012,⁶² found that in Mauritania, the diet of the subspecies Platalea leucorodia balsaci varied between years, with a varying dominance of fish or crustaceans in the diet. Still, we only have two years of data for Ria Formosa (the first sampling year for Tagus Estuary was very incomplete) and the proportion of crustacean was in both years higher than fish.

In addition, the fact that in Portugal the diet of chicks is almost constant during the entire chick development period contrasts with what was reported for the Dutch colonies, where a shift from freshwater to marine diet in the middle of chick rearing season occurs.³⁷ This suggests that rather than being a species-specific pattern, diet switching may be related to prey availability in the vicinity of colonies.

Our results are, however, in accordance with the results from studies in other colonies in the sense that, even considered as a specialist waterbird, the diet of spoonbills seems to be driven by food availability^21,37,62 and by feeding in the surrounding of the colonies.²⁰ In the Tagus Estuary, the rice field seems to constitute an important freshwater foraging habitat where spoonbills can feed on Louisiana crayfish and small fish. In Ria Formosa, P. varians, seems to be a very important prey, that can be easily accessed in the intertidal lagoons or in saltpans in the vicinity of the breeding colony.

Conclusions

Our study reveals differences in dietary and tropic ecology of spoonbills chicks on recently established and traditional colonies. Furthermore, the reliance on prey available in artificial habitats, such as saltpans, where prawns are abundant, or rice fields where new prey as the Louisiana Crayfish is present, may be important in the establishment of new spoonbill breeding colonies across its range. However long-term diet studies are necessary in order to further investigate such possibility.

Footnotes

Acknowledgements

We are grateful to Ria Formosa’s warders Silvério and Capela and to Pedro Rodrigues, for the help with the field work in the colonies, to Afonso Rocha for his help in Tagus colony and collection of samples, to the wardens of RNET (Reserva Natural do Estuário do Tejo), and to Vitor Encarnação for the information about Portuguese colonies, and to all the volunteers that helped with the fieldwork. Permits for bird sampling issued by the national authority for wild bird handling & ringing ICNF were granted to JAA (119/2017) and PMA (191/2020).

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Fundação para a Ciência e a Tecnologia, I.P. (FCT/MCTES), though national funds to [MSR (SFRH/BD/145942/2019), MARE (strategic project UIDB/04292/2020), Associate Laboratory ARNET (LA/P/0069/2020), and to CESAM (UIDP/50017/2020 + UIDB/50017/2020 + LA/P/0094/2020)].

ORCID iDs

Manuela S Rodrigues

Jose A Alves

Data Availability Statement

The sets used and/or analysed during the current study are available from the corresponding author on reasonable request.

References

Wetlands International . Waterbird Population Estimates. wpe.wetlands.org, 2016.

Donald

Sanderson

Burfield

, et al. International conservation policy delivers benefits for birds in Europe. Science 2007; 317: 810–813.

Wetlands International . Waterbird Population Estimates. Summary Report. Wageningen, The Netherlands. 2012.

Rodrigues

Araújo

Silva

, et al. Habitat selection and ontogeny of habitat use by juvenile Eurasian Spoonbill Platalea leucorodia revealed by GPS tracking. Bird Conserv Int 2023; 33: e31.

Fasola

Ruiz

. The Value of Rice Fields as Substitutes for Natural Wetlands for Waterbirds in the Mediterranean Region. Colon Warterbirds 1996; 19: 122–128. DOI: 10.2307/1521955.

Elphick

. Functional Equivalency between Rice Fields and Seminatural Wetland Habitats. Conserv Biol 2000; 14: 181–191. DOI: 10.1046/j.1523-1739.2000.98314.x.

Tucakov

. Changes of breeding numbers and habitat of Eurasian Spoonbill Platalea leucorodia in Vojvodina (N Serbia). Acrocephalus 2004; 25: 71–78.

Rendón

Green

Aguilera

, et al. Status, distribution and long-term changes in the waterbird community wintering in Doñana, south–west Spain. Biol Conserv 2008; 141: 1371–1388.

Correia

. Seasonal and interspecific evaluation of predation by mammals and birds on the introduced red swamp crayfish Procambarus clarkii (Crustacea, Cambaridae) in a freshwater marsh (Portugal). J Zool 2001; 255: 533–541.

10.

Tablado

Tella

Sánchez-Zapata

, et al. The Paradox of the Long-Term Positive Effects of a North American Crayfish on a European Community of Predators. Conserv Biol 2010; 24: 1230–1238. DOI: 10.1111/j.1523-1739.2010.01483.x.

11.

Overdijk

Smart

Navedo

. An overview of Eurasian Spoonbill situation. In: JG

(ed) Proceedings of the Eurosite VII Spoonbill Workshop. 2013, pp.13–14.

12.

Overdijk

. The remarkable recovery of the North Atlantic Spoonbill breeding population. In: Navedo

(ed) Proceedings of the Eurosite VII Spoonbill Workshop. 2013, pp.9–12.

13.

Tait

. The birds of Portugal. London: Witherby, 1924, p.260.

14.

Farinha

Trindade

. Contribuição para o Inventário e Caracterização de Zonas Húmidas em Portugal Continental. Publicação MEDWET/Instituto da Conservação da Natureza, 1994.

15.

Pereira

. Garcas e afins na Reserva Natural do Boquilobo. Livro de de Resumos 1° Encontro Ornitológico do Paul da Tornada. Caldas da Rainha, 1989, pp.15–24.

16.

Encarnação

. Monitoring waterbird colonies. ICNB, Lisbon: CEMPA, 2014.

17.

Hancock

Kushlan

Kahl

. Storks, ibises and spoonbills of the world. London: Academic Press, 1992, p.385.

18.

Aguilera

Dispersal and migration in Eurasian spoonbills Platalea leucorodia. Ardea 1997; 85: 193-202.

19.

Lok

. Spoonbills as a model system: a demographic cost-benefit analysis of differential migration. PhD Thesis, University of Groningen, Groningen, The Netherlands, 2013.

20.

Jouta

De Goeij

Lok

, et al. Unexpected dietary preferences of Eurasian Spoonbills in the Dutch Wadden Sea: spoonbills mainly feed on small fish not shrimp. J Ornithol 2018: 1-11.

21.

Enners

Guse

Schwemmer

, et al. Foraging ecology and diet of Eurasian spoonbills (Platalea leucorodia) in the German Wadden Sea. Estuar Coast Shelf Sci 2020; 233: 106539.

22.

González-Ortegón

Cuesta

. An illustrated key to species of Palaemon and Palaemonetes (Crustacea: Decapoda: Caridea) from European waters, including the alien species Palaemon macrodactylus. J Mar Biol Assoc UK 2006; 86: 93–102.

23.

Assis

. Guia para a identificação de algumas famílias de peixes ósseos de Portugal continental, através da morfologia dos seus otólitos sagitta. 2004, p.190.

24.

Tuset

Lombarte

Assis

. Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Sci Mar 2008; 72: 7–198.

25.

Barrett

Camphuysen

Anker-Nilssen

, et al. Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 2007; 64: 1675–1691.

26.

Aguilera

Ramo

Court

CDL

. Food and feeding sites of the Eurasian spoonbill (Platalea leucorodia) in southwestern Spain. Colon Warterbirds 1996: 159–166.

27.

Schoeninger

DeNiro

. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim Cosmochim Ac 1984; 48: 625–639.

28.

Hobson

Welch

. Determination of trophic relationships within a high Arctic marine food web using δ ¹³ C and δ ¹⁵ N analysis. Mar Ecol Prog Ser 1992; 84: 9–18.

29.

Post

. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002; 83: 703–718.

30.

Craig

. The geochemistry of the stable carbon isotopes. Geochim Cosmochim Ac 1953; 3: 53–92.

31.

Fry

Scalan

Parker

. ¹³C/¹²C ratios in marine food webs of the Torres Strait, Queensland. Mar Freshw Res 1983; 34: 707–715.

32.

Fry

. Conservative mixing of stable isotopes across estuarine salinity gradients: a conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries Coast 2002; 25: 264–271.

33.

Hobson

. Using stable isotopes to trace long-distance dispersal in birds and other taxa. Diversity and Distributions 2005; 11: 157–164. DOI: 10.1111/j.1366-9516.2005.00149.x.

34.

Cherel

Jaquemet

Maglio

, et al. Differences in δ¹³C and δ¹⁵N values between feathers and blood of seabird chicks: implications for non-invasive isotopic investigations. Mar Biol 2014; 161: 229–237.

35.

Mizutani

Fukuda

Kabaya

, et al. Carbon isotope ratio of feathers reveals feeding behavior of cormorants. The Auk 1990; 107: 400–403.

36.

Thompson

Furness

. Stable-isotope ratios of carbon and nitrogen in feathers indicate seasonal dietary shifts in northern fulmars. The Auk 1995; 112: 493–498.

37.

El-Hacen

E-HM

Piersma

Jouta

, et al. Seasonal variation in the diet of Spoonbill chicks in the Wadden Sea: a stable isotopes approach. J Ornithol 2014; 155: 611–619. journal article. DOI: 10.1007/s10336-014-1043-y.

38.

Jackson

Parnell

Jackson

. Package ‘SIBER’. 2020.

39.

Jackson

Inger

Parnell

, et al. Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. J Anim Ecol 2011; 80: 595–602.

40.

R Core Team . R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2016. 2019.

41.

Rufino

Araujo

Pina

, et al. The use of salinas by waders in the Algarve, South Portugal. Wader Study Group Bulletin 1984; 42: 41–42.

42.

Paiva

Ramos

Machado

, et al. Importance of marine prey to growth of estuarine tern chicks: evidence from an energetic balance model. Ardea 2006; 94: 241–255.

43.

Paiva

Ramos

Catry

, et al. Influence of environmental factors and energetic value of food on Little Tern Sterna albifrons chick growth and food delivery. Bird Study 2006; 53: 1–11.

44.

van Wetten

Wintermans

. The food ecology of the Spoonbill Platalea leucorodia. Verslagen en Technische Gegevens 1986; 49: 1–59.

45.

Erzini

Bentes

Coelho

, et al. Recruitment of sea breams (Sparidae) and other commercially important species in the Algarve (Southern Portugal). Commission of the European Communities DG XIV/C/I-Final Report 2002.

46.

Ribeiro

Monteiro

, et al. Long-term changes in fish communities of the Ria Formosa coastal lagoon (southern Portugal) based on two studies made 20 years apart. Estuar Coast Shelf Sci 2008; 76: 57–68.

47.

Correia

. Food choice by the introduced crayfish Procambarus clarkii. In: Annales Zoologici Fennici 2003, pp.517-528. JSTOR.

48.

Champagnon

Kayser

Petit

, et al. The settlement of Glossy Ibis in France. Stork, Ibis and Spoonbill (SIS) Conservation 2019; 2019.

49.

Poulin

Lefebvre

Crivelli

. The invasive red swamp crayfish as a predictor of Eurasian bittern density in the Camargue, France. J Zool 2007; 273: 98–105. DOI: 10.1111/j.1469-7998.2007.00304.x.

50.

Macías

Green

Sánchez

. The diet of the Glossy Ibis during the breeding season in Doñana, southwest Spain. Waterbirds 2004; 27: 234–239.

51.

Salgado

Costa

Cabral

, et al. Comparison of the fish assemblages in tidal salt marsh creeks and in adjoining mudflat areas in the Tejo estuary (Portugal). Cah Biol Mar 2004; 45: 213–224.

52.

Salgado

Cabral

Costa

, et al. Nekton use of salt marsh creeks in the upper Tejo estuary. Estuaries 2004; 27: 818–825.

53.

Rocha

Ramos

Paredes

, et al. Coastal saltpans as foraging grounds for migrating shorebirds: an experimentally drained fish pond in Portugal. Hydrobiologia 2017; 790: 141–155.

54.

Pinto

MdCV

. Optimização do cultivo de camarinha Palaemonetes varians. PhD Thesis, Universidade de Aveiro, 2010.

55.

Bearhop

Waldron

Votier

, et al. Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 2002; 75: 451–458.

56.

Fry

Sherr

. δ ¹³ C measurements as indicators of carbon flow in marine and freshwater ecosystems. Stable isotopes in ecological research. Springer, 1989, pp.196–229.

57.

Bearhop

Adams

Waldron

, et al. Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 2004; 73: 1007–1012.

58.

Newsome

Martinez del Rio

Bearhop

, et al. A niche for isotopic ecology. Front Ecol Environ 2007; 5: 429–436.

59.

Jordan

. Dietary analysis for mammals and birds: a review of field techniques and animal‐management applications. International Zoo Yearbook 2005; 39: 108–116.

60.

Inger

Ruxton

Newton

, et al. Temporal and intrapopulation variation in prey choice of wintering geese determined by stable isotope analysis. J Anim Ecol 2006; 75: 1190–1200.

61.

Parnell

Inger

Bearhop

, et al. Source partitioning using stable isotopes: coping with too much variation. PloS One 2010; 5: e9672.

62.

Veen

Overdijk

Veen

. The Diet of an Endemic Subspecies of the Eurasian Spoonbill Platalea leucorodia balsaci, Breeding at the Banc d'Arguin, Mauritania. Ardea 2012; 100: 123–130.

Exploring the variation in spoonbill chick diet and trophic niches between traditional and recently colonised sites in Portugal

Abstract

Keywords

Introduction

Methods

Study sites and sample collection

Diet

Stable isotope analysis

Data analysis

Results

Diet

Stable isotope analysis

Discussion

Diet

Stable isotope analysis

Comparison with European traditional colonies

Conclusions

Footnotes

Acknowledgements

Declaration of conflicting interests

Funding

ORCID iDs

Data Availability Statement

References