Water-related bird assemblages in an urban pond ‘archipelago’: by M. P. Di Santo

Lakes and Reservoirs: Research and Management 2015 20: 33–41

Water-related bird assemblages in an urban pond ‘archipelago’: Winter patterns of bird species occurrence, abundance and richness Maria Paola Di Santo,1 Giuseppe M. Carpaneto2 and Corrado Battisti3* Xe mina - emozioni in natura Cultural and Environmental Association, 2Dipartimento di Biologia Ambientale, Universit a “Roma Tre”, and 3“Torre Flavia” LTER (Long Term Ecological Research) Station, Environmental Service, Province of Rome, Rome, Italy 1

Abstract This study reports on the patterns of species occurrence, abundance and richness of a wintering water-related bird assemblage in an ‘archipelago’ of 70 small artificial urban ponds (AUPs) embedded in a metropolitan landscape (Rome, central Italy). A total of 20 species in 26 AUPs were sampled. Only the largest AUPs (>0.1 ha) contained all these species, except for Gallinula chloropus. The highest total mean species abundance was observed in the largest ponds, with statistically significant differences evident among size classes. Two significant spatial thresholds in species abundance and richness were observed (between 0.01 and 0.1 ha; between 0.1 and 1 ha in size). The abundance of single species was correlated with their frequency of occurrence. Ponds in urban areas must be larger than 0.1 ha to host a rich winter assemblage of birds, with a further increase in richness noted with a surface area larger than 1 ha. The highest number of species was observed in the larger ponds (>1 ha). The species richness of each AUP is directly correlated to their size (log-transformed species–area relationship: log S = 3.515 + 0.497 log A; R2 = 0.76). Further research should be conducted to confirm these patterns and to implement information useful for planning and management of artificial ponds in urban areas for this purpose.

Key words abundance, frequency of occurrence, pond management, richness, species–area relationships.

INTRODUCTION Urban landscapes can host a unique biodiversity. Species assemblages in these remnant fragments and altered anthropogenic habitats (e.g. wooded parks, green areas, ponds) include many species of conservation concern, as well as many synanthropic, generalist or alien taxa (Beissinger & Osborne 1982; Rebele 1994; van Heezik et al. 2008). The artificial or semi-natural water bodies (fountains, ponds, small lakes) occurring in urban landscapes are suitable in many cases for hosting many vagrant or resident bird species (Tyser 1982). These habitats exhibit characteristics (food availability, artificial lighting, scarcity of predators, etc.) that may be attractive for some ‘urban exploiters’ (Marzluff 2001; Savard & Falls 2001; *Corresponding author. Email: c.battisti@provincia.roma.it Accepted for publication 28 December 2014.

Doi: 10.1111/lre.12086

McKinney 2002; Faeth et al. 2005; Chace & Walsh 2006). Several studies have demonstrated a key role played by natural or artificial ponds for water-related birds (e.g. waterfowls, waders) not only as wintering or breeding sites, but also as stopover areas during migration (Chovanec 1994). In heavily human-transformed landscapes, such as metropolitan areas, these ponds may represent a multifunctional resource of vital importance to the conservation of many species (Gledhill et al. 2004; Zacchei et al. 2011). The role of area in defining the number and abundance of species has been largely highlighted in both natural and anthropogenic wet habitats (Celada & Bogliani 1993; Benassi et al. 2007; Magurran & McGill 2011). As a general model, larger water bodies host a higher number of species and individuals, compared to smaller ponds. This is due to a higher availability of

M. P. Di Santo et al.

niches and resources (Wiens 1976, 1989). The species abundance and richness of birds in natural wetlands is directly related to the area as a proxy of the environmental heterogeneity (Brown & Dinsmore 1986; Acuna et al. 1994; Hoyer & Canfield 1994; Suter 1994; Froneman et al. 2001; Newbold & Eadie 2004). In particular, large-area sites are preferred by water-related birds, being used as roosts, trophic and refuge sites, especially in winter (Tuite et al. 1984). Nevertheless, the effect of area on the abundance of birds in urban ponds has not been extensively studied (Tyser 1982, 1983; Hoyer & Canfield 1994; Suter 1994; Naugle et al. 1999; Froneman et al. 2001; Hattori & Mae 2001; Riffell et al. 2001; Guadagnin & Maltchik 2007; Pearce et al. 2007; Guadagnin et al. 2009), especially in the Mediterranean area (Benassi et al. 2009). The present study analyses the structure of wintering bird assemblages occurring in a large number of small water bodies located in the metropolitan area of Rome, to assess the patterns of the occurrence, abundance and richness of species. It is hypothesized that: (i) the number of wintering species increases with increasing size, following the species–area relationship applied to mainland fragment archipelagos (MacArthur & Wilson 1963; Diamond 1975; Connor & McCoy 2001; see review in Watling & Donnelly 2006 and Magurran & McGill 2011); (ii) there are size thresholds of these water bodies wherein mean species richness and abundance significantly increase; and (iii) consistent with the relationship between the distribution and abundance applied to wet ecosystems (Paracuellos & Teller ıa 2004; Paracuellos 2006), the most widely diffused species (i.e. higher frequency of occurrence) also are the more abundant. To this end, the results of this study may be useful for pond management and planning in large urbanized landscapes.

MATERIALS AND METHODS Study area The metropolitan area of Rome (lat. 41°550 31.487″, long. 12°270 10.930″; central Italy) covers approximately 129 000 ha and hosts almost 3 million inhabitants, with an average density of 21.9 inhabitants ha 1. The area examined in this study is represented by the core area of Rome (about 36 000 ha), encircled by the Grande Raccordo Anulare, a beltway surrounding the city. The altitude ranges from 15 to 20 m (SW districts) up to 139 m (Monte Mario) above sea level. According to Blasi (1994), the phytoclimate of Rome is characteristic of the transitional Mediterranean region.

Selection of anthropogenic urban ponds An inventory of anthropogenic urban ponds (hereafter referred to as AUPs) in the Rome metropolitan area (central Italy; about 360 km2) was carried out, including lakes, fountains and small ponds, ultimately leading to identification of 70 sites, all being artificial (i.e. anthropogenic). Within a radius of 1 km, all the AUPs were embedded in an urbanized and homogeneous landscape matrix. It was assumed, therefore, that the landscape matrix was comparable among sites. The area of the AUP (A), comprising both the water surface and a buffer belt of about 5 m along the perimeter, was recorded for each site, as a dependent variable in this study. The surface area measurements (ha) were taken using the regional technical map (1:2000; Regione Lazio). For the smaller AUPs, field measurements were taken, using a rolling semi-rigid metre. The field measurements were compared to the cartographic data obtained from the technical regional map.

Water-related bird sampling Bird sampling was conducted from 7 November 2009 to 18 February 2010 (n = 85 days, for a total of 400 h of field work). Each AUP was visited eight times during this period (see Paillisson et al. 2002; Traut & Hostetler 2004; Paracuellos 2006). To counter a possible bias attributable to a time-of-day sampling effect (i.e. morning vs. afternoon), each site was visited four times in the morning (from 0700 to 1100 a.m.) and four times in the afternoon (from 0100 to 0500 p.m.). Days characterized by fog, heavy rain and/or strong winds (conditions that hamper the detectability of species) were avoided to increase the sampling accuracy (Bibby et al. 2000). The method of standardized circular transect (Sutherland 2006) was applied to obtain quantitative data on birds. This method consists of walking the perimeter of a pond at a constant velocity (1.5 km h 1), directly recording each wintering water bird belonging to a set of selected species (Table 1), thereby obtaining a value of abundance for each species. As smaller AUPs are easily exposed to disturbance attributable to the presence of the observer, the observer walked slowly in these sites, starting to count birds before their taxonomic identification from a distance of at least 100 m, during the approaching way. A Pentax (Pentax-Ricoh imaging corporation, Tokio, Japan) 10 9 50 binocular was used for bird identification and counts. Given the small size of the AUPs, attention was given to the movements of single birds to minimize the bias attributable to pseudoreplication. Although alien and/or domesticated forms of water-related birds also were observed

Bird assemblages in urban ponds

Table 1. Water-related bird species selected for sampling in 70 artificial urban ponds (AUPs) in Rome metropolitan area (central Italy) Family Ardeidae

Scientific name Egretta alba (Linnaeus, 1758)

The frequency of occurrence for each species was calculated as the ratio between the number of AUP occupied and the total number of AUP (n = 70). A species–area relationship was finally obtained, based on the equation (MacArthur & Wilson 1963): Log S ¼ c þ zlog A;

ð1Þ

Ardea cinerea (Linnaeus, 1758) Bubulcus ibis (Linnaeus, 1758) Egretta garzetta (Linnaeus, 1766) Anatidae

Anas crecca (Linnaeus, 1758) Anas strepera (Linnaeus, 1758) Anas platyrhynchos (Linnaeus, 1758) Aythya fuligula (Linnaeus, 1758) Anser anser (Linnaeus, 1758) Anser fabalis (Baillon, 1834)

Rallidae

Fulica atra (Linnaeus, 1758) Gallinula chloropus (Linnaeus, 1758)

Podicipedidae

Podiceps cristatus (Linnaeus, 1758) Tachybaptus ruficollis (Pallas, 1764)

Phalacrocoracidae

Phalacrocorax carbo (Linnaeus, 1758)

Scolopacidae

Gallinago gallinago (Linnaeus, 1758)

Alcedinidae

Alcedo atthis (Linnaeus, 1758)

Accipitridae

Circus aeruginosus (Linnaeus, 1758)

Laridae

Chroicocephalus ridibundus (Linnaeus, 1766) Larus michahellis (Naumann, 1840)

in the AUPs, only the data on autochthonous wild species were reported in this study (see Table 1 checklist).

Data analysis To analyse the patterns of occurrence, abundance and richness of wintering water-related birds species depending on size, the 70 sampled AUPs were divided into five size classes, including AUP1 (range of 0–0.001 ha; mean area of 0.0003 0.0002 ha; n = 3), AUP2 (range of >0.001–0.01 ha; mean area of 0.0053 0.0027 ha; n = 13), AUP3 (range of >0.01–0.1 ha; mean area of 0.037 0.024 ha; n = 31), AUP4 (range of >0.1–1 ha; mean area of 0.28 0.27 ha; n = 15) and AUP5 (>1 ha; mean area of 4.10 3.65 ha; n = 8). The data collected for each AUP were processed to obtain the values of the following parameters: (i) occurrence of single species, (ii) abundance of each waterrelated bird species, (iii) total abundance of all species (as a sum of the abundances for all the species occurring in each AUP) and (iv) species richness (S). The mean abundance, the total mean abundance and the species richness (Smean) were obtained for each AUP size class.

where S = species richness of each AUP, and A = size. The Kruskal–Wallis test and Mann–Whitney nonparametric U-test were performed to verify the significance of the differences among mean values of abundance, total abundance and species richness. A two-tailed Spearman rank correlation test was performed to correlate the abundance of single species for their frequency of occurrence in the AUP archipelago (relationship abundance vs. occurrence), and a v2 test was utilized to test the difference between the frequency of occurrences in the five size classes. The software PASW Statistics 18 (SPSS Inc. 2009, Chicago, IL, USA) was used, with the alpha value set to 0.05.

RESULTS Patterns of occurrence Birds were recorded only in 26 AUPs (37.1% of the total number of AUPs). The difference between the frequency of species occurrences among the AUP size classes was statistically significant (v2 = 9.75; P < 0.01; Table 2). Almost all species were found only in the larger AUPs (>0.1 ha), except for Gallinula chloropus, which was the only species sampled in all the AUP size classes (Table 3). The most widely spread species were Gallinula chloropus, Phalacrocorax carbo, Chroicocephalus ridibundus and Anas platyrhynchos (Table 3). All the species are wintering. Of the species, three species (Gallinula chloropus, Anas platyrhynchos and Alcedo atthis) also are breeders.

Patterns of abundance The highest total mean abundance was observed in the larger size class (AUP5; Table 2). The differences between the total mean abundances were statistically significant (H = 37.767; P < 0.01; Kruskal–Wallis test). Two thresholds in total mean abundance were observed, between AUP3 and AUP4 size classes (Z = 2.042; P < 0.05) and between AUP4 and AUP5 size classes (Z = 3.624; P < 0.01). At the level of single species, and considering all the AUPs, the most abundant species observed were Gallinula chloropus, Anas platyrhynchos, Larus michahellis and Chroicocephalus ridibundus (Table 4). Gallinula chloropus, the only species occurring in all the size classes, exhibited increased abundance in the larger AUPs, with

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Table 2. Assemblage structure of water-related wintering birds in 70 AUPs (anthropogenic urban ponds)

Size class

AUP1

AUP2

AUP3

AUP4

AUP5

0–0.001

0.001–0.01

0.01–0.1

0.1–1

nocc (%)

1 (33.3)

13 5 (38.5)

31 6 (19.4)

6 (40)

8 (100)

Smean (SD)

0.33 (0.58)

0.15 (0.38)

0.06 (0.25)

1.33 (3.48)

7.38 (3.78)

Total mean abundance (SD)

0.04 (0.07)

0.03 (0.07)

0.01 (0.03)

5.38 (18.52)

52.25 (53.29)

Explanation: size class (range, in ha); n, number of AUPs; nocc (%), number and percentage of AUPs occupied by at least one species; S, species richness; Smean (SD), mean species richness and standard deviation. Table 3. Frequency of occurrence of the 20 water-related wintering bird species for each artificial urban pond (AUP) size class

Range (ha)

AUP1

AUP2

AUP3

AUP4

AUP5

0–0.001

0.001–0.01

0.01–0.1

0.1–1

Podiceps cristatus

—

0.13

Tachybaptus ruficollis

—

0.07

0.25

Phalacrocorax carbo

—

0.13

0.88

Egretta alba

—

0.25

Ardea cinerea

—

0.07

0.63

Bubulcus ibis

—

0.07

—

Egretta garzetta

—

0.13

0.5

Anas crecca

—

0.07

0.25

Anas strepera

—

0.13

Anas platyrhynchos

—

0.13

0.75

Aythya fuligula

—

0.13

Anser anser

—

0.13

Anser fabalis

—

0.13

Circus aeruginosus

—

0.13

Fulica atra

—

0.07

0.63

Gallinula chloropus

0.33

0.15

0.06

0.13

0.63

Gallinago gallinago

—

0.07

0.13

Alcedo atthis

—

0.13

0.38

Chroicocephalus ridibundus

—

0.2

0.75

Larus michahellis

—

0.07

0.63

significant differences among size classes (H = 16.882; P = 0.002; Kruskal–Wallis test). Comparing the mean abundance between the larger size classes (AUP3, AUP4, AUP5), a significant increase was observed for Phalacrocorax carbo (ZAUP3–AUP4 = 2.056 and ZAUP4–AUP5 = 3.594; both P < 0.01), Anas platyrhynchos (ZAUP3–AUP4 = 2.056, P < 0.05 and ZAUP4–AUP5 = 3.036, P < 0.01) and Chroicocephalus ridibundus (ZAUP–AUP4 = 2.546 and ZAUP4–AUP5 = 2.566; all P < 0.05, Mann–Whitney U-test). A significant difference also was observed between mean abundance in the two larger areas (AUP4 vs AUP5)

for Ardea cinerea (Z = 2.594; P < 0.01), Fulica atra (Z = 2.757; P < 0.01), Gallinula chloropus (Z = 2.337; P < 0.05) and Larus michahellis (Z = 2.757; P < 0.01; Mann–Whitney U-test). The abundance of single species was significant and directly correlated to their frequency of occurrence (rs = 0.830; P < 0.01; Spearman rank correlation test, 2 tail).

Patterns of richness and species–area relationships In the archipelago of 70 AUPs in this study, a total of 20 water-related bird species were observed (Table 1). The

Bird assemblages in urban ponds

Table 4. Mean abundance (and standard deviation) of the 20 water-related wintering bird species for each AUP size class AUP1

AUP2

AUP3

AUP4

AUP5

0–0.001

0.001–0.01

0.01–0.1

0.1–1

Podiceps cristatus

—

0.02 (0.05)

Tachybaptus ruficollis

—

0.09 (0.36)

0.50 (1.32)

Phalacrocorax carbo

—

0.04 (0.11)

1.27 (1.46)

Egretta alba

—

0.10 (0.18)

Ardea cinerea

—

0.23 (0.87)

0.27 (0.40)

Bubulcus ibis

—

0.03 (0.10)

—

Egretta garzetta

—

0.08 (0.26)

0.52 (0.85)

Anas crecca

—

0.02 (0.06)

0.39 (0.81)

Anas strepera

—

0.64 (1.81)

Anas platyrhynchos

—

2.28 (8.71)

29.66 (43.75)

Aythya fuligula

—

0.06 (0.18)

Anser anser

—

0.13 (0.35)

Anser fabalis

—

0.13 (0.35)

Circus aeruginosus

—

0.05 (0.13)

Fulica atra

—

0.08 (0.32)

2.21 (4.11)

Gallinula chloropus

0.04 (0.08)

0.03 (0.08)

0.01 (0.03)

0.83 (2.31)

4.33 (5.26)

Gallinago gallinago

—

0.33 (1.29)

0.13 (0.35)

Alcedo atthis

—

0.07 (0.23)

0.35 (0.65)

Chroicocephalus ridibundus

—

1.12 (3.70)

7.31 (8.75)

Larus michahellis

—

0.19 (0.74)

4.24 (7.73)

Range (ha)

higher number of species (19) was in the larger size class (AUP5 > 1 ha; Tables 2 and 3). Differences in the Smean values among the five size classes were statistically significant (H = 36.748; P < 0.01; Kruskal–Wallis test). A significant threshold in the Smean values occurred between the size classes AUP3–AUP4 (Z = 1.963; P < 0.01) and AUP4–AUP5 (Z = 3.387; P < 0.01; Mann– Whitney U-test). A direct and significant correlation between area and number of wintering water-related bird species was observed (rs = 0.463; P < 0.01; n = 70; log-transformed species–area relationship: log S = 3.515 + 0.497 log A; R2 = 0.76). Considering only the 26 AUPs in which birds were sampled, a stronger correlation was obtained (rs = 0.722; P < 0.01; n = 26; species–area relationship: log S = 4.747 + 0.345 log A; R2 = 0.75). The z coefficient (i.e. the slope of the regression line between species and area) was 0.497, considering all the AUPs. The slope was 0.345 for considering only the AUPs with at least one bird species.

DISCUSSION The creation of artificial wetlands can help reduce the negative impacts associated with the loss of natural wetlands because they can provide stopover refuges for

migratory birds and wintering areas (Kloskowski et al. 2009). Furthermore, artificial habitats can be more suitable for some water-related bird species, compared to natural wetlands, because of some favourable factors. These include a lack of predators, no hunting zones and minimization of some disturbances (Turnbull & Baldassarre 1987; Langley et al. 1998; Traut & Hostetler 2004; Kloskowski et al. 2009). Among the features that increase the importance of these habitats for wintering birds, the area (and the related habitat heterogeneity) was the most important predictor of the occurrence, abundance and richness of bird species. In the AUP archipelago in the present study, two thresholds in size (0.1 and 1 ha) were obtained, whereby the species richness of bird assemblages increased significantly, as demonstrated with previous studies (e.g. Pearce et al. 2007). A first important result of the present study, therefore, is that anthropogenic ponds and urban lakes should be larger than 0.1 ha in size in order to be able to host a rich assemblage, with a further increase in richness noted where their surface area was >1 ha. Benassi and Battisti (2011) reported higher thresholds in size (at 1 and 10 ha), which worked to increase the frequency of occurrence of water-related birds in small natural wetlands of central Italy.

The avian species observed in artificial lakes are usually sedentary, omnivorous birds, with a high eco-ethological plasticity that enables them to live in urban environments, and tolerate different levels of human disturbance (Alberti et al. 2003; Sorace & Gustin 2008). Nevertheless, even the most generalist species cannot live in very small ponds, mainly because of the lack of food resources and refuges, and high competition or edge effects (Sousa 1984). The value of the z coefficient for the species/area relationship (i.e. the angular coefficient of the regression line between species and area) represents important information reflecting the degree of isolation of an archipelago for a specific target (MacArthur & Wilson 1963; Abbott 1983). The observed values in the present study were within the known range for ecological islands (0.17–0.72; Watling & Donnelly 2006), highlighting the effect of area on these bird assemblages inhabiting a small patchy water system included in an urbanized landscape. Nevertheless, for assemblages with a low number of species (e.g. <20), as in this case, the species/area relationship could be altered from qualitative differences among species belonging to different area-sensitive guilds (Robinson et al. 1992). At the level of a single species, Gallinula chloropus, Anas platyrhynchos, Larus michahellis and Chroicocephalus ridibundus were the most abundant species at the study sites. These species also were the most widespread species observed in the artificial water bodies in the study area. They are considered generalists, with a high degree of tolerance to human disturbance (Tuite et al. 1984; Allen & O’Connor 2000). Anas platyrhynchos exploits different urban environments as feeding sites and resting places during migration or as winter refuges (e.g. during the hunting season). This species may be present in large numbers in urban environments, even in combination with its domestic forms (Heusmann 1981, 1983; Figley & VanDruff 1982; Heusmann & Burrell 1984). The species with high population density exhibited the highest incidence rate (or percentage of occurrence) in the AUP archipelago. A greater species abundance generally corresponds to a greater number of occupied sites (i.e. direct correlation between abundance and distribution; Paracuellos & Teller ıa 2004; Paracuellos 2006). Evidence for an areal sensitivity was obtained for most water-related bird species in the study area. Indeed, all the sampled species occurred in AUPs larger than 0.1 ha. Thus, this size also may be considered an important ecological and spatial threshold at the species level, at least for water birds in urban ponds. Only Gallinula chloropus was observed at all study sites. This generalist rail often is found in altered, artificial and agricultural habitats, and in urban wetlands, including small ponds (Bannor & Kiviat 2002).

M. P. Di Santo et al.

Considering the concern of biotic homogenization of urban landscapes (McKinney 2006; Olden & Rooney 2006; Devictor et al. 2007; Cassey et al. 2008; Lambdon & Hulme 2008; Lougheed et al. 2008; Sorace & Gustin 2008), it was concluded that urban ponds larger than 0.1– 1 ha in area may increase the local diversity of waterrelated birds, even if limited to generalist taxa. A goal of the present study was to define the species–area relationship for wintering species in an urban pond archipelago, focusing on searching for size thresholds. Thus, variables at the landscape or patch (i.e. pond) scale that may further affect this relationship were not taken in to account. The present study considered the pond ‘area’ as the main predictor to determine our patterns, as widely recognized in other studies (Lomolino & Weiser 2001; Ding et al. 2006; Benassi et al. 2007). It is believed that the present study is the first to report wintering bird patterns for a large pond archipelago of an urbanized landscape. Nevertheless, as habitat patchiness at different scales may drive the species–area relationship (Wiens 1997; Nichols et al. 1998; Tews et al. 2004), further research on this topic might also take into account the role of intrapatch heterogeneity and other coarse- or fine-grained patch or landscape parameters that may directly affect observed patterns in the occurrence, richness and abundance of the studied species.

ACKNOWLEDGEMENTS We thank all the people who facilitated the realization of this study. A special thanks is given to Marianna Di Santo and Domenico Doleatto for their precious support during sampling, to Adriano Mazziotta for statistical support and to Dr. PhD Alessandro Zocchi for his help in English translation.

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