Recovery of a wader bird of conservation concern (pied avocet, Recurvirostra avosetta) after wetland restoration: A 17-years study

doi:10.21203/rs.3.rs-3182513/v1

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Recovery of a wader bird of conservation concern (pied avocet, Recurvirostra avosetta) after wetland restoration: A 17-years study

https://doi.org/10.21203/rs.3.rs-3182513/v1

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Waders (Charadriiformes) are birds sensitive to change in water levels in wetlands. In this paper, we report a multi-year trend in abundance of adults, nesting pairs and chicks of a biogeographically isolated population of pied avocet (Recurvirostra avosetta L., Aves, Charadriiformes) localized in a salt-water wetland of central Italy where restoration interventions were carried out in 2009. Our hypothesis is that the actions aimed to regulate water levels have allowed the establishment of a stable local population of this rare species. We used a standardized transect methods to obtain values of abundance during the breeding periods (April-July) along the 2006–2022 time range. Comparing data before and after the interventions, we observed an increasing trend in the abundance following the water regulation interventions leading to the establishment of a stable population. The difference in abundance between before and after the restoration was also evident by controlling for rainfalls. When comparing the effects of wetland restoration with rainfall data, we observed as the former was the main predictor (multiple regression) in determining the abundance of pied avocets. The logistic GLM analysis indicates a threshold of 20 individuals comparing before and after the restoration suggesting as the interventions exceed the threshold for the establishment of a stable population. Pied avocet may be an indicator of restoration effort in salt wetlands, since this wader meets many of the typical criteria requested for a biological indicator.

Water-related birds

abundance

nesting period

rainfalls

habitat restoration

Italy.

Waders are water-related birds sensitive to change in water levels in wetlands, these last due to different natural or anthropogenic events (Tinarelli et al. 2005; Zacchei et al. 2011; Battisti et al. 2015; Franks et al. 2018). In particular, human-induced events can show both negative impacts (e.g., due to anthropogenic threats; Fanelli and Battisti 2014; Giovacchini et al. 2023) and positive effects (e.g., due to habitat restoration interventions: Eglington et al. 2008; Massarutto and de Carli 2014; Anderson and Rooney 2019; Battisti et al. 2023) on these sensitive birds. In this regard, it has been underlined that the conservation of these species should be based on long term ecological studies (Dowding and Murphy 2001).

The pied avocet (Recurvirostra avosetta L.) is a wader bird (Charadriiformes) of conservation concern (included in EU 79/409/Bird Directive; European Commission 1979) with a large, breeding distribution throughout the Western Palearctic (Cramp and Simmons 1983). This species shows a biogeographical interest on a Mediterranean scale. In fact, in this region the nesting populations are extremely localized mainly along the coastal areas (wetlands with sparsely vegetation and salt waters; López et al. 2010; Chokri and Selmi 2011).

Many field studies were carried out on Pied Avocet (Cadbury and Olney 1978; De Bie and Ziljstra 1979; Watier and Fournier 1980; De Bie and Ziljstra 1985; Casini 1986; Hill 1988; Girard and Yésou 1989; Hötker 1998, 2000, 2005; Hötker and Segebade 2000; Cuervo 2004; Lengyel 2006; Barati and Nouri 2009; Chokri and Selmi 2011; Boukrouma 2021). However, research on the effects of habitat restoration is still scanty, excluding someones related to specific conservation actions (e.g., islet creation: Chambon et al. 2019; tidal restoration: Van den Bergh et al. 2005; see also Goutner 1997).

Pied avocet is particularly sensitive to water levels during the nesting period (Goutner 1985). In brackish habitats, water levels are often maintained through artificial regulation of the waters in reservoirs (e.g., in active salt marshes; McKinley et al. 2020) or, in the case of natural environments, by meteo-climatic events (e.g., water rainfall; Xin et al. 2017) which, in spring-summer, can affect the nesting success (Nussbaumer et al. 2021).

In this work we reported data obtained along a multi-year trend of a biogeographically isolated population of pied avocet (the only one located on the Tyrrhenian coast of central Italy; Brichetti and Fracasso 2004). This population nests in a wetland, where a habitat restoring has been carried out in the first decade of the 2000s. Our hypothesis is that these interventions have allowed the establishment of a stable population of pied avocet during this long-time range (17 years). Therefore, we compared some population parameters (mean and maximum abundance of individuals, breeding pairs, and chicks) before and after the restoration interventions. We also tested the effects of the rainfalls on nesting pair density in the late spring-summer period (April-July), since rainfalls represent a natural factor affecting nesting success (Lengyel 2006). Finally, we compared both rainfalls and restoration to search for a main predictor in abundance of this wader of conservation concern and biogeographic interest.

Study area

The Diaccia Botrona wetland [42°47' N – 10° 55' E] is a coastal wetland of international importance (Ramsar Convention) included in the Municipalities of Grosseto and Castiglione della Pescaia (province of Grosseto, Tuscany, central Italy: size area: 800 ha). This wetland is a habitat remnant of the larger Lake Prile of the Roman Age, for a long time extended almost 120 km². Located on the edge of the final stretch of the Bruna River, it also appears to be within the homonymous Regional Reserve (1348 ha-wide; Special Protection Area “Padule Diaccia Botrona” - code IT51A0011, according to Directive 147/2009/EC) managed by the Tuscany Region Public Agency. The wetland, identified by the two sub-areas ‘Diaccia’ and ‘Botrona’, is separated from the coast by a sandy “tombolo” with a pine forest of Pinus pinea rich in herbaceous-shrub undergrowth.

From the vegetation point of view, ‘Diaccia Botrona’ is of one of the most important coastal lagoons of Tuscany including 327 plant species as, for example: Ranunculus trilobus Desf., Atriplex halimus L., Isatis tinctoria L., Scirpus litoralis Schrader and Aeluropus littoralis (Gouan) Parl. (Sforzi and Selvi 1999).

In recent decades, due to the worsening quality of the circulating waters, the rapid proliferation of aquatic vegetation and seasonal dryness which over time have further contributed to deteriorating its freshwater character, shows marked signs of ecological changes, such as to observe the turnover in the Phragmites australis (Cav.) Trin. ex Steud. Phytocoenoses, and the subsequent development of halophytic essences such as, for example, Salicornia perennis Mill. and Halimione portulacoides (L.) Aellen. Exception for the autumn-winter rainfall, the seabed in the two lockouts currently reaches a maximum depth of about 50–70 cm. The entire system, until the early 2000s, was characterized by incoming brackish water with the presence of internal areas without water ponds.

The Diaccia Botrona represents an area of considerable importance for wintering or breeding waterfowl and waders, with significant numbers or species such as, for example, greylag goose Anser anser, eurasian wigeon Mareca penelope, common crane Grus grus, pied avocet Recurvirostra avosetta, black-winged stilt Himantopus himantopus and common redshank Tringa totanus (Zenatello et al. 2014; Giovacchini and Stefanini 2015). Here, there is an important heronry where great egret Egretta alba in 2015 was nesting for the first year (Corsi and Giovacchini 1995; Giovacchini et al. 2017). In particular, the pied avocet is locally reported for the first time with two pairs in 2002 (Ceccolini and Cenerini, pers. com.), representing the only isolated population along the Tyrrhenian coast of Italy (being the colonies mainly concentrated on the Adriatic coast; Brichetti and Fracasso 2004).

In the study area, a habitat restoration project was launched in 2009, with the aim to manage the circulation of salt waters therefore providing suitable water levels for birds.

In the 2006–2022 period from 15 April to 30 July, a standardized sampling design has carried out (61 monthly censuses) focused on the pied avocet in the Diaccia Botrona wetland and in the immediately surrounding areas, walking along 21 overall transects into which the wetland is divided. Each survey was carried out with appropriate optical equipment, consisting of binoculars (7x42 e 8x30) and spotting scopes (Swarovski AT 80).

The protocol adopted intended the carrying out of the censuses in the afternoon when it is possible easily detect adults and chicks of this wader (Glutz von Blotzheim et al. 1977; Cramp and Simmons 1983; Goutner 1985; Hötker 1998). Each session engaged for 3–4 hours, starting at 04:30 p.m. Along each transect, the information collected was reported on field cards, without setting time limits (Crump and Scott 1994), and controlling for double counts (pseudoreplication; Wanless and Harris 1984; Fasola 1991; Battisti et al. 2014), The observation distance was always chosen to be large enough to minimize disturbance to pied avocet or other birds. As parameters of abundance, we recorded the number of adult individuals (n. ind.), the number of nesting pairs and the number of chicks (= non volant pulli).

Along the period 2006–2022, also monthly cumulative data on the rainfall regimes were collected in the breeding period (from April to July). Weather information have been taken from the nearby meteorological stations of ‘Casotto Pescatori’ and Grosseto Airport, in the municipality of Grosseto (www.sir.toscana.it; www.wunderground.com), 5–7 km away from study area.

Data analysis

The raw data in abundance (expressed in n. individuals, n. ind.) obtained for pied avocet in each session have been transformed in (i) averaged and median monthly abundance values (and standard deviation, s.d.), also obtaining the maximum values per year (max abb). Similarly, the averaged monthly values of rainfall (and s.d., in mm) were obtained. To check for significant variations between median values both for n. ind. of pied avocet and for rainfall, the Kruskall-Wallis test (among all years) and the Mann Whitney U test (between paired years) were used. Mean values of rainfall and mean abundance were correlated using the non-parametric Spearman rank correlation test (Dytham, 2011).

We performed a One-way ANCOVA (Analysis of Covariance) test for equality of means for several univariate groups, adjusted for covariance with another variable. In this case, we used the state of before and after restoration as the grouping variable and mean rainfalls in the April-July as a covariate. The ANOVA-like summary table contains sum-of-squares for the adjusted means (between-groups effect) and adjusted error (within-groups), together with an F test for the adjusted means. F test for the equality of regression slopes (as assumed by the ANCOVA) is also given (Hammer et al. 2001).

Using multiple regression, we compared the role of the two variables ‘rest’ (restoration) and ‘rain’ (rainfalls) to select the main predictor among them, using abundance as dependent variable. Finally, we performed a Generalized Linear Model, for a single explanatory variable (restoration, ‘rest’ vs. abundance, ‘abb’). Statistical analyses were done using the software PAST 4.01 (Hammer et al. 2001) with a significance level of p ≤ 0.05.

From 2006 to 2022 breeding periods (April-July) 4814 individuals, 271 nesting pairs and 182 chicks were recorded (Table 1; Supplementary materials 1). The multi-year rainfall trend compared to median and maximum abundances of individuals, nesting pairs and chicks is shown in Fig. 1.

Table 1

Rainfall regime (mean values, in mm) and number of pied avocets recorded (max abb: max number individuals/year; mean abb: mean number of individuals or pairs, and standard deviation: s.d.; pairs: number of nesting pairs and number of chicks). Dotted line indicate the year of restoration (2009).
	rainfalls	pied avocet
year	mean (sd)	max abb	mean abb (sd)	pairs	chicks
2006	11.825 (16.18)	66	30 (34.99)	5	0
2007	11.2 (12.44)	4	1 (2)	0	0
2008	46 (33.75)	17	6.5 (8.19)	0	0
2009	15.1 (12.52)	28	11.25 (11.93)	5	0
2010	18.75 (21.71)	50	22.75 (20.58)	4	4
2011	6.6 (4.73)	54	32 (25.5)	10	8
2012	30.4 (37.28)	84	50.5 (35.82)	21	7
2013	26.5 (35.14)	91	44.75 (46.39)	21	35
2014	58.1 (25.79)	244	127.25 (96.96)	13	38
2015	34.8 (34.55)	180	114.75 (55.54)	28	26
2016	15.95 (11.12)	127	85 (36.18)	5	0
2017	7.8 (6.33)	70	39.25 (36.18)	19	6
2018	56.7 (63.05)	270	151.5 (88.44)	17	18
2019	58.5 (43.20)	316	160.25 (109.33)	25	15
2020	22.1 (19.22)	160	109.5 (43.62)	16	14
2021	23.45 (11.77)	280	140.5 (93.88)	65	5
2022	21.95 (19.52)	114	76.5 (28.16)	17	6

The rainfalls (April-July) do not differ significantly between years (H = 17.91, p = 0.328; Kruskal-Wallis test for equal medians), while a significant variation of the median abundance has been observed in the 2006–2022 time range (H = 42.53, p < 0.001; Kruskal-Wallis test for equal medians; Fig. 1). In both cases, no differences were observed between paired years (U Mann Whitney test; p > 0.05).

The mean values both of abundance and rainfalls resulted significantly correlated (r_s = 0.638, p = 0.005; Spearman Ordinary Least Squares Regression: ‘rain’-‘abb’ slope: 0.656; intercept: 52.84, t = 2.328; p = 0.02; 95% bootstrapped confidence intervals; N = 1999; Fig. 2).

As the maximum values of abundance increases, the number of nesting pairs (r = 0.752, p < 0.001) and chicks (r = 0.644, p < .001) also significantly increases. Nesting pairs and chicks were significantly correlated among them (r = 0.646, p < 0.001, Spearman rank correlation test).

The ANCOVA using the state of before and after restoration as the grouping variable and the mean rainfalls in April-July period as a covariate showed that there is a highly significant difference between before and after the restoration when controlling for rainfalls (F = 12.32, p = 0.0014; Homogeneity (equality) of slopes: F = 6.463; p = 0.0164).

Multiple regression comparing the role of the two variables ‘rest’ and ‘rain’ (using abundance as dependent variable) showed as the first variable (‘rest’, restoration) was the main predictor (‘rest’: 63.072%, t = 3.205, p = 0.006; ‘rain’: 1.63%; t = 3.326, p = 0.005; ANOVA: F = 13.454, p = 0.0005). Generalized linear model (Binomial distribution, logit link) showed a clear pattern with a threshold in abundance at 20 individuals (before-after restoration; Log likelihood: -2.64; G: 13.265; p = 0.00027; Fig. 3).

Considering a long period of time (17 years), an increasing trend in the abundance of adult individuals and nesting pairs of pied avocet has been observed, following the water regulation interventions in the Diaccia Botrona wetland. Until the early 2000s, this species was locally represented by a few breeding pairs, the only ones along the peninsular Tyrrhenian Italy (Brichetti and Fracasso 2018). Since 2009, coinciding the local restoration actions, an increase in individuals, nesting pairs and chicks was observed which has led to the establishment of an apparently stable population over the following two decades.

However, in this long-time range (17 years), we have also witnessed fluctuations in rainfalls. Abundance of this species in nesting period is correlated to a large number of environmental parameters (Casini 1986; Hötker and Sebegade 2000). Indeed, in the chick-rearing phase, habitat, and seasonal variables as well as weather, may affect the breeding success (Lengyel 2006). For example, fledging success was higher in the wet years than in the dry year (Lengyel 2006). In our case we recorded a significant correlation of the abundance of pied avocet with the rainfalls. However, the difference between before and after restoration is also evident by controlling for rainfalls (ANCOVA analysis), with restoration appearing the main predictor (multiple regression) in determining the abundance of Pied Avocets, when compared with rainfalls.

In waders, as abundance increases, feedbacks and cascade effects can occur (Lengyel 2006). Indeed, herding behavior in colonial nesting appeared to be essential for Pied Avocets because it provided several anti-predatory benefits. For example, nesting success is higher in large colonies, with a “mass effect” once populations have reached relatively high abundances (i.e., > 15 pairs; see Lengyel 2006). The logistic GLM analysis indicates a threshold of 20 individuals comparing before and after the restoration and it can be suggested that these interventions have triggered a demographic increase such as to exceed the threshold for the establishment of a stable population. In this regard, the local project of wetland restoration may be considered a pulse process (i.e., a short-term process causing sudden changes in species abundance; Underwood 1989; Glasby and Underwood 1996), having a positive impact on the demographic increase (and possible eshtabliment) of a new biogeographically isolated subpopulation of Pied Avocet.

Once confirmed, these data could also suggest a response of Pied Avocet to habitat restoration (see López et al. 2010, for salt environments). In this regard, we think that this species could represent a good indicator (sensu Heink and Kowarik 2010), since this bird meets many of the typical criteria requested for a biological indicator (Noss 1990), i.e.: (i) Pied Avocet has a stable zoological systematic and taxonomy; (ii) it is a relatively widespread, and medium-sized species, relatively easy both to detect and sample with a minimum field (and economic) effort; (iii) it is sensitive to a specific process (in our case, habitat restoration): therefore, the species could represent a surrogate to indicate positive impact induced by management actions. Moreover: (iv) it is universally applicable and spatially comparable: this largely diffused species show a similar ecology and behaviour inside their geographical range (Cramp and Simmons 1983); (vi) interpretation and communication of results of monitorinng may be easily carried out through simple uni-variate metrics as, for example, the abundance of adults, nesting pairs and number of chicks; finally; (vii) Pied Avocet is a charismatic species (for example, is an icon for Italian ornithologist: https://ciso-coi.it/avocetta/), therefore, allowing a large communication addressed to a large number of people.

Acknowledgments

Wetland restoration actions have been carried out with the Acts n.805/2003, n. 3780/2005 and n.2369/2007, of the Grosseto Provincial Administration (Tuscany, Italy), Protected areas and Biodiversity Department. We wish to thank the rangers and practitioners working in the Diaccia Botrona natural reserve for the support during this long-term field study.

Author contributions P.G. developed the project, P.G., C.M., and P.S. carried out the field study, C.B. analyzed the data-sets, L.M. provided for a supervision. All authors reviewed the manuscript.

Funding No funding was received for conducting this study.

Data availability The datasets generated during and/or analysed during the current study are available when requested.

Competing interests The authors declare no competing interests.

Confict of interest The authors declare they have no fnancial interests.

Ethical approval The study did not involve human participants or research on animals, so ethics approval was not required.

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Abstract

Figures

Introduction

Study area

Materials and methods

Data analysis

Results

Discussion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1