Cages Mitigate Predation on Eggs of Threatened Shorebirds: A Manipulative-Control Study

Abstract

Beach-nesting birds (plovers; Aves; Charadridae) are impacted by many natural and human-induced threats (e.g., people trampling, dogs, and natural predators). In this regard, the use of anti-predator cages on their nests is effective in order to mitigate some of these pressures (i.e., predation). To evaluate the efficacy of anti-predator cages and the causes of nest failure in a breeding site of two species (Charadrius alexandrinus and C. dubius), we carried out a control-experimental design, comparing false nests (n = 69) in cages (experiment; n = 30) with false nests without cages (control; n = 39). We carried out the study in three seasonal periods (May, June, and July), controlling predations after three periods (three, six, and nine days) since positioning, recording the frequency of eggs still present and evidencing any predation event. The percentage of residual eggs was significantly higher in experimental nests when compared to control nests in all recording periods. Considering 59 predation events on false nests, the most important predators were: in experimental nests (n = 21) the fox, Vulpes vulpes (47.6%), and in control nests (n = 38), the hooded crow, Corvus cornix (50%). Our data suggest that the use of anti-predator cages significantly limits predation on eggs and therefore is likely to increase the hatching success in these ground-nesting birds independently in the seasonal period. However, also in the presence of a cage, the fox is a relevant egg predator.

1. Introduction

Ground-nesting birds are impacted by many natural and human-induced threats [1,2,3]. This plethora of threats is evident in birds nesting on coastal beaches (plovers; Aves; Charadridae) [4,5]. In coastal beaches, in addition to mechanical cleaning and accidental trampling, natural or human-related predators have been identified as the main factor in the low hatching success of plovers. However, few manipulative experiments have attempted to address this issue. In this regard, protection measures greatly increased hatching success [6].

In central Italy, two species of birds nest on the ground along the coast: the Kentish plover (Charadrius alexandrinus) and the Little Ringed Plover (Charadrius dubius), both of them being in rapid decline throughout Europe [7,8,9]). Both species nest on ephemeral environments of European conservation concern (shifting embryonic dunes) and are exposed in the breeding period to several threats, mainly linked to the pressures originated from the use of beaches by people (i.e., mechanical cleaning of the beaches, trampling, and domestic dogs; [10,11]) and by other natural events, especially predation, with crows, gulls, and foxes being the main predators [7,10,11,12]). The use of anti-predator cages has proved to be an effective action in order to minimize the risks of predation for these ground-nesting species [6,13,14,15].

In this note, we tested the effect of cages in reducing predation risks on false nests located on a coastal beach of Tyrrhenian Italy where these two bird species are known to naturally breed. To test the effectiveness of cages on false nests, we used an experimental-control design, that is we compared false nests with cages versus false nests without cages.

2. Materials and Methods

2.1. Study Area

The study area (Torre Flavia wetland—Natural Monument) is located on the Tyrrhenian coast (Ladispoli; province of Rome; Central Italy; 41.57′ N; 12.02′ E). For its conservation value, this wetland and surrounding beaches are designated as a ‘‘Special Protection Area’’ (code IT6030020; 147/2009/CE ‘Birds’ Directive).

The wetland (43 ha in size) is a remnant of a larger ecosystem that was drained and transformed in the last century [16]. Along the coastline, the area is characterized by several typical coastal habitats of European conservation concern, mainly corresponding to the Habitat 2110 (Embryonic shifting dunes), characterized by the dominance of Thinopyrum junceum and Anthemis maritima [17], details in [18].

In this area, two species of plovers locally breed, the Kentish plover (Charadrius alexandrinus) with one to two pairs (2021: one nesting event), and the Little-ringed Plover (C. dubius) with two to three pairs (2021: five nesting events). The Torre Flavia coastline is an important breeding site for both of the species at the regional level [8]. These species build their nests with their eggs hatching in May–June, and flighting taking place in June–July.

The protected area is currently managed by a Public Agency (Città Metropolitana di Roma Capitale) which periodically carries out a set of conservation actions aimed to protect these targets and mitigate some specific anthropogenic threats (e.g., dogs, trampling [19]). Since 2017, some pilot interventions have been carried out in order to protect the dunes, delimiting these habitats with poles, ropes, and signals, limiting people trampling and communicating the value of the dunal ecosystems to the visitors.

2.2. Experimental Design and Data Analyses

To evaluate the efficacy of anti-predator cages in limiting the predation on the nests, we defined a control-experimental design comparing the rate of predation in false nests placed in cages (experiment) with false nests placed without cages (control; Figure 1). We used the number (and relative frequency) of remnant nests, checking also for the number (and frequency) of predated eggs. A total of 90 eggs were placed in 30 false nests with cages (experiment) and 117 eggs in 39 false nests without cages (control), with each one spaced at least 25 m apart. In each false nest (both in the experiment and in the control), three quail (Coturnix coturnix) eggs were placed. Quail eggs were used due to their large availability in commerce and for their similar shape, color, and size when compared to plover eggs.

The cages used were built specifically for this study and consisted of a metal mesh composed of a grid of 76.2 × 63.5 mm units and equipped with a roof created with the same mesh (for construction details: [20]). False nests (with and without cages) were placed randomly along the Torre Flavia beach (total length: about 1000 m). With our study sites (embryonic shifting dunes) being relatively homogeneous in their fine-grained pattern (vegetation: alo-psammophilous plants; substrate: sand), we assumed that any environmental differences would not have influenced our data. We placed false nests in three different sub-seasonal sessions: 20 May (I session), 1 June (II session), and 2 July 2021 (III session).

After each session, the false nests (with and without the protective cage) were monitored through three periodical recording checks (the first after three days from positioning, the second after six days, and the third after nine days) with the aim of obtaining the number of remnant nests and eggs (i.e., not still predated).

The data were processed both as a whole and separately for each sampling session and each recording period (after three, six, and nine days). Furthermore, during each recording we checked for any sign of predation, associating it to the specific predator when possible. We considered an ‘event of predation’ to be any predatory event on a false nest independently from the number of eggs removed. For the assignment of the species of predator, we referred to the tracks or to camera images (Apeman H70), classifying them according to [21].

The contingency table χ² test was used to compare the frequency values [22]. All statistical analyses were performed using the Past 4.1 software for Windows [23], with alpha set at 5%.

3. Results

In any seasonal session, we observed a significant decrease in the number of remnant nests both in experiments (χ² = 42.054) and controls (χ² = 103.81, d.f. = 3, p < 0.001). A similar pattern emerged when considering the number of remnant eggs (experiments: χ² = 62.581; controls: χ² = 69.649, d.f. = 3, p < 0.001;

Table 1. Number and relative frequency (fr) of remnant nests and eggs in experiments (with cage) and controls (without cage) during the recording sessions (three, six, and nine days) in the three sub-seasonal sessions (May, June, and July).

	Recording Sessions
	Experiment (with Cage)
			3 Days		6 Days		9 Days
	nests	eggs	nests (fr)	eggs (fr)	nests (fr)	eggs (fr)	nests (fr)	eggs (fr)
May	10	30	9 (0.9)	27 (0.9)	7 (0.7)	21 (0.7)	4 (0.4)	12 (0.4)
June	10	30	8 (0.8)	24 (0.8)	4 (0.4)	12 (0.4)	4 (0.4)	12 (0.4)
July	10	30	10 (1)	30 (1)	4 (0.4)	12 (0.4)	2	6 (0.2)
tot	30	90	27 (0.9)	81 (0.9)	15 (0.5)	45 (0.5)	10 (0.33)	30 (0.33)
	Control (without Cage)
May	13	39	3 (0.23)	8 (0.21)	0 (0)	0 (0)	0 (0)	0 (0)
June	13	39	5 (0.38)	15 (0.38)	1 (0.08)	3 (0.08)	1 (0.08)	3 (0.08)
July	13	39	7 (0.54)	21 (0.54)	1 (0.08)	3 (0.08)	0 (0)	0 (0)
tot	39	117	15 (0.38)	44 (0.38)	2 (0.05)	6 (0.05)	1 (0.025)	3 (0.08)

).

However, the number of remnant nests was significantly lower in controls when compared to experiments in any recording session (after 3 days: χ² = 18.91; 6: χ² = 18.388; χ² = 11.98), analogous to the number of remnant eggs (after 3 days: χ² = 58.38; 6: χ² = 55.163; 9: χ² = 35.94; d.f. = 3, p < 0.001; Table 1; Figure 2). We did not observe seasonal differences in trends among seasons (χ² test, p > 0.05).

Overall, we recorded 59 events of nest predation. In experimental nests (n = 21 events), the most frequently recorded predator was the fox, Vulpes vulpes (n = 10; 47.6%; Figure 3); in control nests (n = 38 events), the most frequently recorded predator was the hooded crow, Corvus cornix (n = 19; 50%).

When comparing single predation events, there was a significantly higher frequency of predation by foxes in control nests (χ² = 21.8, p < 0.001).

4. Discussion

Our data show that the use of anti-predator cages greatly limits predation on eggs and, therefore, is likely to increase hatching success in these ground-nesting birds. This evidence was independent from the seasonal breeding period.

Specifically, by analyzing all positioning events, the percentage of eggs occurring after the three recording periods was significantly higher in the experimental nests (with cage: 33.3% of residual eggs) when compared to the control nests (without cages: less than 3%).

Foxes and hooded crows were the main predators. However, cages are selective for different predators: when the cage (experimental nests) was present, the predation by foxes was significantly higher. This phenomenon was probably due to the ability of this generalist mammal to adapt its behavior and overcome the cage system by digging deep under the cage and feeding on the eggs (Figure 3) [24]. Furthermore, this canid was apparently able to associate the presence of the cage with the presence of eggs [24]. Thus, the cage constitutes a clue for the presence of food that is easily identified by this predator [25]. Further effort should be devoted to developing cages that are designed to impede the predation by foxes. In addition, a limited number of hooded crows overcame the grid of these cages. This fact should be particularly considered in suburban areas where these birds occur at high density. In this regard, further creative solutions should be developed with the aim of improving the control of predation and, at the same time, allowing the movements of plovers.

The observed percentage of predation on experimental nests could be overestimated. Indeed, differently from false nests, in the presence of true nests, adults of these birds perform behavioral displays to distract the predators, thus preventing the predation of the eggs [25,26,27]. Moreover, we assumed for our experiments that the habitat type was locally homogeneous (embryonic shifting dunes with alo-psammophilous vegetation and sandy substrate): therefore, we carried out a random (not stratified) sampling design. Nevertheless, there is a potential for fine-grained internal heterogeneity to influence our data.

Despite these caveats, and in the light of the strong pressure of predation on plovers along the beaches, e.g., [6,7], we strongly suggest that anti-predator cages should be used to protect plover eggs. However, the decision on where the various cages should be located must be context-declined considering the type, size, and species density of local predators.

Further efforts should be aimed at developing specific measures to prevent the entry of other predators (e.g., rats) while favoring the entry of the hatching adults, for example by using creative techniques used in conservation project management [28,29].