Rice Fields Used As Feeding Habitats for Waterfowl Throughout The

Rice Fields Used as Feeding Habitats for Waterfowl throughout the Growing Season Author(s): Candela Marco-Méndez, Patricia Prado, Luis Miguel Ferrero- Vicente, Carles Ibáñez and José Luis Sánchez-Lizaso Source: Waterbirds, 38(3):238-251. Published By: The Waterbird Society DOI: http://dx.doi.org/10.1675/063.038.0304 URL: http://www.bioone.org/doi/full/10.1675/063.038.0304

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Rice Fields Used as Feeding Habitats for Waterfowl throughout the Growing Season

Candela Marco-Méndez1,*, Patricia Prado2, Luis Miguel Ferrero-Vicente1, Carles Ibáñez2 and José Luis Sánchez-Lizaso1 1Department of Marine Science and Applied Biology, University of Alicante, Apartado Correos 99, 03080, Alicante, Spain

2IRTA Aquatic Ecosystems, Central Poble Nou km 5.5, Apartado Correos 200, 43540, Sant Carles de la Ràpita, Tarragona, Spain

*Corresponding author; E-mail: [email protected] Abstract.—The role of rice fields as feeding habitats for the two main waterfowl herbivores, Eurasian Coot (Fulica atra) and Mallard (Anas platyrhynchos), in the Ebro Delta, a Mediterranean wetland in northeastern Spain, was investigated. Exclusion cages and tethering experiments were deployed within a rice field at the beginning of the growing season (summer 2010) and before harvest (autumn 2010). In summer, waterfowl abundances were low, but cage experiments detected rice field damage by waterfowl grazing through a significant reduction in plant biomass (although consumption was undetectable using tethers). In autumn, waterfowl abundance increased and tethering experiments detected consumption of rice plants with developed seeds, whereas cage experiments did not show grazing effects. Gut content analyses indicate that Mallards are mainly granivorous, feeding mostly on seeds of spiral ditch grass (Ruppia cirrhosa) and rice (Oryza sativa), while Eurasian Coots are herbivorous, feeding mainly on macrophyte leaves. However, stable isotope analyses and mixing model results showed that in the long term both species seem to acquire most of their dietary needs from rice plants and sago pondweed (Potamogeton pectinatus). Dietary analyses confirm the importance of rice in both species’ diets but also suggest that waterfowl may undergo seasonal dietary variations. These are mostly influenced by changes in the availability of food resources in the area rather than by their nutritional quality. This study confirms the ecological importance of rice fields as a complementary feeding habitat for waterfowl during the growing season in Mediterranean areas. It also highlights the importance of including these habitats in wetland management for waterfowl conservation. Received 11 December 2014, accepted 27 April 2015. Key words.—Anas platyrhynchos, Eurasian Coot, Fulica atra, grazing experiments, Mallard, rice fields, stable isotopes. Waterbirds 38(3): 238-251, 2015

Wetlands are vital habitats for many Rice field systems, including irrigation ca- waterbird species, but human activities are nals, are used by a variety of waterbirds such greatly impacting them throughout the as waders, gulls, terns, ducks and herons, world through: 1) complete loss (e.g., drain- primarily as feeding habitats (Elphick and age for urbanization or dry cultivation); 2) Oring 1998; Bird et al. 2000). Damage to rice degradation in quality (e.g., contamination fields by birds can be caused by trampling, or alteration of hydrological regimes); or 3) which can disturb the grain or destroy seed- conversion of land to aquatic agriculture, lings, or by ingurgitation of rice seeds (Hoff- which changes the structure and function of mann and Johnson 1991). The majority of the habitat, but retains the area as wetland the studies concerning rice field damage by (Tourenq et al. 1999, 2000). In the latter situ- waterfowl have been conducted in North ation, rice (Oryza sativa) cultivation is by far and South America, Africa and Australia the most common, and 40% of the world’s (Stafford et al. 2006, 2010). In Europe, this population now depends on this food source topic has been studied primarily outside the (Fasola and Ruiz 1997). As a consequence, growing season (Tourenq et al. 2003; Ibañez in many regions natural wetlands have now et al. 2010), even though this is the period virtually disappeared, and rice fields have when rice fields become important feeding become the primary wetland habitat for win- and sheltering grounds for many species of tering (Tréca 1994; Elphick and Oring 1998) waterfowl (Pierluissi 2010). In Mediterra- or breeding (Acosta et al. 1996; Lane and Fi- nean areas, there is a lack of information on jioka 1998) waterbirds. habitat use (Tourenq et al. 2003), and many

238 Waterfowl Feeding on Rice Fields 239 studies have been solely focused on foraging pling time (Legagneux et al. 2007). Stable herons (Fasola et al. 1996). isotope analyses are another technique that Mediterranean wetlands, such as the can provide non-destructive and time-inte- Ebro Delta and those at the Albufera and grative information about the diet and often Doñana National Parks, are some of the provenance of food sources (Hobson and main wintering areas for waterfowl within Clark 1992a, 1992b, 1993; Inger and Bear- the Western Palearctic region (Sánchez- hop 2008). Since consumers feed on isotopi- Guzmán et al. 2007; Rendón et al. 2008). In cally distinct food items, their tissues reflect some of these wetlands, Mallard (Anas platy- the different stable isotopic compositions rhynchos) and Eurasian Coot (Fulica atra) are of their diets. This depends on the period the dominant species, especially in winter when the birds consumed the diet as well as (Martínez-Vilalta 1996; Mañosa et al. 2001). the turnover rates of the tissues (Legagneux Both species have been reported to feed et al. 2007), so it can be used to make infer- mainly on the submerged aquatic vegetation ences about diet and the type of habitats in of marshes and lagoons (Rodríguez-Villafra- which they live (Inger and Bearhop 2008). ñe et al. 2007; Marco-Méndez et al. 2015). The main objective of this study was to However, over the past few centuries these elucidate the importance of rice fields as al- Mediterranean wetlands have been reduced ternative feeding habitats for the two main to 10-20% of their original area (Fasola and waterfowl species (Mallard and Eurasian Ruiz 1997), which enhances the relative im- Coot) of the Ebro Delta during the growing portance of rice fields as an alternative feed- season. For this purpose we: 1) investigated ing habitat for waterfowl species (Fasola and seasonal abundances of both species within a Ruiz 1996). rice field; 2) quantified the seasonal grazing In Mediterranean countries, the rice impact of waterfowl on rice plant biomass cropping cycle begins in April when flooded and seeds using exclusion cage experiments; fields are sown (Longoni 2010). Rice reaches 3) quantified seasonal consumption of rice its maximum height in August and is usually plants using tethering experiments; and 4) then harvested in September or October, studied dietary contributions through gut after fields have been drained. In the Ebro content and stable isotope analyses. Addi- Delta, fields remain flooded until January in tionally, we investigated the role of nutrient a new agro-environmental initiative of the content in food selectivity. We hypothesized European Union to increase wintering areas that waterfowl use rice fields as alternative for migratory waterbirds. In those rice fields, feeding habitats, especially during the grow- waterfowl forage for the available food re- ing season when there is an increasing avail- sources: invertebrates, land plants and wa- ability of vegetative structure and food re- ter weeds, or rice seeds (Elphick and Oring sources. 1998; Manley et al. 2004).

Waterfowl diet or selectivity can be in- Methods fluenced by several factors, such as food availability (Petrie and Rogers 1996), high Study Area nutrient contents (McGlathery 1995; Prado The Ebro Delta is located in the Province of Tarra- et al. 2010), high protein and energy con- gona, Catalonia, in northeastern Spain. The area holds tents (Hughes 1980; Sedinger and Raveling a total breeding waterbird population of nearly 60,000 1984; Murphy and King 1987) or easier di- pairs, including gulls and terns (48%), ducks and coots (25%), waders (14%) and herons (13%). The ornitho- gestibility (Charalambidou and Santamaría logical importance of the Ebro Delta is also well-known 2002), the last especially affecting selectiv- during autumn and winter, when the area is visited by ity for seeds. Among methods for quantify- some 250,000 birds, including ducks and coots (50%), ing dietary contributions, stomach content gulls and terns (29%), waders (18%) and herons (3%) analysis is the most accurate, although it (Martínez-Vilalta 1996; Mañosa et al. 2001). The Ebro Delta is included on the Ramsar Convention list of wet- gives dietary information relative to a short lands of international importance and is considered an time period and requires an extended sam- Important Bird Area by BirdLife International (Viada 240 Waterbirds

1998). The area supports well-developed rice farming in summer 2010 (from mid-June to mid-July) when activity on which waterfowl conservation depends to rice was in the vegetative phase (seedlings with four a large extent. As a consequence of agricultural prac- to five leaves) and waterfowl abundance was expected tices, coastal lagoons and marshes have been reduced to be low, and in autumn 2010 (from mid-September to about 25%, while rice fields occupy about 65% of the to mid-October) when rice was in the ripening phase total delta area. Nowadays, the Ebro Delta Natural Park (maximum plant biomass and developed seeds) and and some neighboring wetlands and rice fields, which waterfowl abundance was expected to be high. total about 12,000 ha, are included in the Natura 2000 Network (Ibañez et al. 2010). Waterfowl Populations To carry out this study, we selected a 24-ha area made up of the rice field under study (surrounded by From previous surveys by Ebro Delta Natural Park other rice fields) and a flooded area we considered to and observations during 2008-2010 (A. Curcó, pers. com- be representative of the different habitats available for mun.), Mallards and Eurasian Coots were normally the waterfowl in the Ebro Delta (Fig. 1). The study area most abundant species in the area (summer: 50% and was 250 m away from the 418-ha Encanyissada lagoon, 23%, respectively; autumn: 45% and 55%, respectively). the largest in the Ebro Delta. The submerged vegeta- Mallards were also often the most abundant species in rice tion in the study area was dominated by spiral ditch fields (e.g., summer: 20%; autumn: 25%) despite a greater grass (Ruppia cirrhosa) in high salinity areas (12-27 variety of waterbird species in these fields. For these rea- ‰) and by sago pondweed (Potamogeton pectinatus) sons, as well as their reported grazing activity on the neigh- in low salinity areas (3-12‰) (Prado et al. 2013). Ex- boring lagoon (Marco-Méndez et al. 2015), we focused our periments were deployed within one of the rice fields survey efforts on Mallards and Eurasian Coots.

Figure 1. Map of the Encanyissada lagoon showing the location of the rice field used in this study (adapted from Prado et al. 2013). Waterfowl Feeding on Rice Fields 241

During each study season (summer and autumn (e.g., growth and/or decomposition). Control repli- 2010), 4 days were randomly selected for visual surveys. cates consisted of identical numbers of rice plants (n Each morning (around 09:00 hr), individuals were = 20) placed in the rice field with a protective mesh counted (using binoculars) by the same person from a (1-cm2 mesh size) to prevent consumption during fixed point. The abundance of Mallards and Eurasian the study period. After that period, all replicates were Coots counted in the study area was expressed as den- collected and reweighed for variations in wet weight sity (ind·ha-1). To elucidate the relative importance of (WW) as a proxy of leaf loss by consumption (g WW·d- this habitat for each waterfowl species, the percentage 1). Therefore, we calculated the weight of plants eaten of individual Mallards and Eurasian Coots was estimat- by waterfowl (with apparent bites) as the difference ed using the lagoon and the rice field in summer and between initial and final wet weight of tissue exposed autumn 2010. We estimated total abundances using sea- to herbivores, using biomass variation in control teth- sonal abundances in the rice field and those recorded ers to correct consumption estimates. In autumn, we in the lagoon in a simultaneous survey (Marco-Méndez also counted the number of seeds lost after 30 days (nº et al. 2015) carried out during the same study period. seeds·shoot-1·d-1). Exclusion Cage Experiment Gut Contents To evaluate the effects of waterfowl grazing on rice To support patterns from exclusion and tethering fields, six bird exclusion cages and six open control cag- experiments, individuals of both waterbird species were es (1.5 m2) were deployed randomly within a rice field. collected in the study area for gut contents (n = 10 in- The top and sides of exclusion cages were made of rigid dividuals per species) and stable isotope analyses (n = 5 plastic netting (1 cm2 mesh size) attached to four poles individuals per species). For legal reasons, individuals (1.5 m long, 1 cm diameter) driven into the sediment, could only be collected during the hunting season (Oc- preventing the entrance of birds. tober-February), mainly during the first 2 months, so Exclusion and open control cages were deployed gut contents reflect the available food consumed during for a 30-day period in summer and autumn 2010. In our autumn experiments (from mid-September to mid- summer (from mid-June to mid-July), rice plants con- October, which includes the end of the harvest season) sisted of four to eight small leaves (seedlings), whereas and winter (after harvest). To integrate longer tempo- in autumn (from mid-September to mid-October) ral variability into resource acquisition, we also used plants were much larger and had developed seeds. Af- stable isotope analyses. Studies suggest that animals can ter a 30-day period, one rice plant sample was collected retain information about previous feeding locations for within each control and exclusion cage using a 16-cm periods that depend upon the elemental turnover rates diameter PVC core (n = 12 samples per season). After for the tissue of interest (Tieszen et al. 1983; Tieszen each sampling event, plants were kept within labeled and Boutton 1989; Hobson and Clark 1992a). There- plastic bags and transported to the laboratory where fore, in our study muscle tissue may reflect waterfowl they were washed to remove attached sediments. All diet/habitat several weeks before individuals were col- samples were dried at 60 °C to a constant dry weight lected (Tieszen et al. 1983; Hobson and Clark 1992a). (DW), and the following variables were measured: to- This means that if individuals were hunted in October tal biomass (g DW·m-2), shoot density (number [n°] of (most individuals, except two Eurasian Coots that were shoots·m-2) and also seed biomass (g DW of seeds·m-2) collected in late autumn-early winter), they will likely and density (n° seeds·m-2) in the harvest season (au- reflect items consumed in late summer-early autumn. tumn). Differences in those variables between control Individuals were processed in the laboratory. After and exclusion cages were used to quantify the impact of extraction, muscle was reserved for isotopic analyses, grazing on the rice field. and guts were stored in 70% alcohol until analyzed (Mouronval et al. 2007). The content of each gut was Tethering Experiments analyzed under a microscope and sorted into the differ- Tethering experiments were conducted simultane- ent food items found: leaf and stem fragments of spiral ously with the deployment of exclusion cages during ditch grass and sago pondweed and their seeds, rice the two study seasons to quantify consumption rates seeds (no rice plant fragments were found), algae and of rice plants through waterfowl herbivory. In each unidentifiable material. Each item was dried at 60 °C, season, tethering lines consisted of replicates with to a constant weight. The importance of each food item similar amounts of rice plants collected from the field was expressed as a percentage of total weight within the and weighed in the laboratory (g wet weight; n = 20). gut. Replicates were plants with leaves (seedlings) in sum- Stable Isotope and Nutrient Content Analyses mer and plants with ripe seeds in autumn, as for cage experiments. Plants were attached to pins using cable Samples of submerged macrophytes, rice plants and ties and randomly deployed within the rice field for 30 seeds seasonally available in the lagoon and the studied days. Tethers were separated from each other by ap- rice field were randomly collected for stable isotope and proximately 1.5 m, and each picket was considered an nutrient content analyses. Samples of spiral ditch grass independent sample (Prado et al. 2007). Controls for leaves (SD-L), sago pondweed leaves (SP-L), rice plants tethering experiments were carried out simultaneously (Rice), spiral ditch grass seeds (SD-S), sago pondweed to correct changes in plant mass unrelated to herbivory seeds (SP-S), rice seeds (Rice-S) and the muscle of Mal- 242 Waterbirds lards and Eurasian Coots (n = 5 samples for each food When assumptions could not be met by transformation, item and each consumer) previously dried to a constant the significance level was set at 0.01 to reduce the possi- weight (60 °C, 24 hr) were ground to fine powder for bility of a Type I error (Underwood 1997). The Student stable isotope (δ15N and δ13C ‰) and nutrient content Newman-Keuls post-hoc test (Zar 1984) was then used (C:N molar ratio) analyses. Analyses were carried out to investigate the presence of significant groupings. All with an EA-IRMS (Thermo Finnigan) analyzer in con- ANOVAs and the post-hoc test were carried out using tinuous flow configuration. The average difference in GMAV 5 software (Underwood et al. 2002). isotopic composition between the sample and refer- Significant patterns of variation in gut contents be- ence material (δ sample-standard, expressed as ‰) is deter- tween Mallards and Eurasian Coots were identified with mined by the equation: n-MDS ordination (Bray-Curtis similarity index) and the analysis of similarity (ANOSIM). Finally, percent- [(R – R )/R ] × 1,000 = δ ages of similarity were given using SIMPER analyses to sample standard standard sample-standard identify which dietary items primarily accounted for ob- 13 12 15 14 served differences in the stomach contents of Mallards where Rsample is C/ C or N/ N in the sample, Rstandard 13 12 15 14 and Eurasian Coots, using PRIMER-E software package is C/ C or N/ N in the working reference (CaCO3 from Vienna Pee Dee belemnite and atmospheric ni- (Clarke and Warwick 2001). trogen is the standard for δ13C and δ15N measurements, respectively), calibrated against an internal standard (Atropine, IAEA and/or UGS). The analytical precision Results of the methods used was 0.15‰. Statistical Analyses Waterfowl Population We used a one-way analysis of variance (ANOVA) No significant differences between sea- with two levels (summer, autumn) to separately inves- sons were detected in either Mallard (F1 = tigate seasonal variations in Mallard and Eurasian Coot -3.340; P = 0.117) or Eurasian Coot abun- abundance. Differences in biomass and shoot density dances (F = 2.9; P = 0.140). However, the between treatments were investigated separately for 1 each season (summer and autumn) using a one way- populations of both species, especially Mal- ANOVA with two levels (control, exclusion). These tests lards, tended to increase from summer to were carried out using GMAV5 software (Underwood et autumn (Fig. 2A). The total number of in- al. 2002). Rice seeds were present only in autumn, and dividuals counted in the study area in sum- differences in rice seed biomass and density between mer was 235 (84% Mallards; 16% Eurasian control and exclusion cages were assessed with a Mann Whitney test for independent samples (due to lack of Coots) and in autumn 492 (86% Mallards; normality and homoscedasticity in the data). We used 14% Eurasian Coots). Considering the to- the same test to analyze seasonal differences in rice con- tal individuals counted in the lagoon and sumption from tethers. These tests were carried out us- the rice field area, Mallards showed higher ing SPSS (SPSS, Inc. 2009). percentages in the rice field (summer: 57%; Differences in stable isotope composition (δ15N and δ13C) and nutrient contents (C:N molar ratio) between autumn: 38%) while Eurasian Coots had food items were investigated with a one-way ANOVA higher percentages in the lagoon (summer: with six levels using GMAV5 software (Underwood et 23%; autumn: 47%) (Fig. 2B). al. 2002). IsoSource (Phillips and Gregg 2003) isotope mixing models were used to identify the contributions of each food source to Mallard and Eurasian Coot diets. Exclusion Cages and Tethering Experiments The input parameters for the model were the isotopic values for the consumers, the trophic resources (mea- In summer, rice plant biomass was signifi- sured in this study) and the overall rate of fractionation. cantly higher in exclusion cages (206.01 ± The model was run using fractionation values (3.2 ‰ 36.39 g DW·m-2) than in control cages (96.21 for δ15N and 1.45 ‰ for δ13C) from other studies on -2 ± 10.32 g DW·m ; F1 = 8.73, P = 0.014; Fig. waterfowl with similar herbivorous diets (Hobson and 3A). In autumn, significantly higher values Bairlein 2003; Evans Ogden et al. 2004; Inger et al. 2006). Since no differences in the isotopic signals were found were recorded for control cages (695.01 ± -2 between seeds and plant tissue, for Mallards we ran the 108.18 g DW·m ) than for exclusion cages model using the average of seed and plant tissue in 15N -2 δ (312.13 ± 31.37 g DW·m , F1 = 13.85, P = and δ13C values of rice, spiral ditch grass and sago pond- 0.004; Fig. 3A). For rice shoot density, sum- weed, and for Eurasian Coots the isotopic values of each mer values in control and exclusion cages plant species’ tissues (Phillips and Gregg 2003). For all ANOVAs, assumptions of normality and did not differ significantly (136.26 ± 8.10 -2 -2 homogeneity of variance were assessed with the Kol- shoots·m and 137.29 ± 7.22 shoots·m , re- mogorov-Smirnov and Cochran’s C tests, respectively. spectively; F1 = 0.01, P = 0.927), whereas Waterfowl Feeding on Rice Fields 243 grass and sago pondweed, algae and unidentifiable material, together constituting the remaining 32%. Eurasian Coot guts con- tained only leaf fragments of sago pondweed (90%) and spiral ditch grass (10%). n-MDS ordination of the items found in the gut contents showed different groupings for Mallard and Eurasian Coot samples. ANOSIM results confirmed that these two groupings were significantly different (Glob- al R = 0.424, P = 0.002). The average similarity among Mallards was only 21%, whereas for Eurasian Coots the value was 78%. The average dissimilarity between Mallards and Eurasian Coots was 95%, mostly due to differences in the presence of sago pondweed leaf fragments (45%) (Table 1).

Stable Isotope Analyses δ15N and δ13C signatures revealed signifi- Figure 2. (A) Abundances (mean ± SE) of Mallard (Anas cant differences among food items (one-way platyrhynchos) and Eurasian Coot (Fulica atra) in the ANOVA, P < 0.001; Table 2). The highest survey location (individuals·ha-1) and (B) percentages of δ15N signatures were found in sago pond- each species present in the survey location (RIC) and in weed vegetative tissues and seeds and spiral the neighboring lagoon (LAG) during the study period. ditch grass vegetative tissues, and the lowest NS = not significant. in spiral ditch grass seeds and in rice fragments and seeds. For δ13C signatures, rice significantly greater rice shoot density was fragments and seeds showed the highest val- observed in control cages compared to ex- -2 ues, whereas the lowest were found in spiral clusion cages (346.67 ± 28.26 shoots·m vs. ditch grass and sago pondweed vegetative tis- 170.53 ± 11.23 shoots·m-2, respectively; F = 1 sues and their seeds (Fig. 4A). 38.02, P < 0.001; Fig. 3B) in autumn. Analy- Results from the IsoSource model in- ses of exclusion cage data did not show sig- dicated that the diets of Mallards and Eur- nificant differences for seed biomass Z( = - asian Coots mostly consisted of rice plants 1.922, P = 0.055), whereas seed density was and sago pondweed with a low contribution significantly higher in control cages than in of spiral ditch grass (Mallards: rice = 62%, exclusion cages (Z = - 2.082, P = 0.037; Figs. sago pondweed = 38%, spiral ditch grass = 3C and 3D). In the tethering experiments, 0%; Eurasian Coots: rice = 61%, sago pond- rice plant consumption in autumn was weed = 36% and spiral ditch grass = 2%, at significantly higher than in summer Z( = - the percentile 50%). These results point to 2.612, P = 0.009). Consumption recorded -1 rice plants as the main food for both con- in autumn was 0.067 ± 0.071 g WW·d , with sumers with a non-negligible contribution of 0.37 ± 0.14 seeds lost per tethered shoot sago pondweed. and day.

Gut Contents Analyses Nutrient Contents in Waterfowl and Food Resources Gut contents of Mallards consisted of rice seeds (29%) and spiral ditch grass seeds C:N molar ratios were significantly differ- (39%) and, to a lesser extent, sago pond- ent between food items (one-way ANOVA, weed seeds, leaf fragments of spiral ditch P < 0.001; Table 2). The highest C:N molar 244 Waterbirds

Figure 3. Exclusion cage experiments: (A) Rice biomass (g DW·m-2); (B) Rice density (shoots·m-2); (C) Rice seed biomass (g DW Seeds·m-2); and (D) Rice seed density·m-2. Mean ± SE. Statistically significant differences are: * P < 0.05, *** P < 0.001. NS = not significant. ratios were found in sago pondweed seeds species were present in the rice field dur- and rice plants, and the lowest in rice seeds, ing the entire study period, Mallards were spiral ditch grass seeds and the leaves of spi- the most abundant (summer: 84%; autumn: ral ditch grass and sago pondweed (Fig. 4B). 86%), while Eurasian Coots seemed to be more present in the neighboring lagoon (summer: 72%; autumn: 86%). In this study, Discussion more intense grazing activity in the rice field was not related to population increases, as Our results confirm that waterfowl feed commonly reported (Perrow et al. 1997; on rice fields, either on seedlings or seeds Mitchell and Perrow 1998), but our results according to their availability, during the suggest that resident populations of water- growing season in Mediterranean wetlands fowl use rice field habitats throughout the such as the Ebro Delta. This can lead to a entire growing season. significant reduction in rice plant biomass, In summer, waterfowl abundance seems as we detected in summer. Isotope and gut to be lower but cage experiments detected content analyses confirm the importance of rice damage through their grazing, leading rice in both species’ diets, but also suggest to a significant reduction in plant biomass. that waterfowl may undergo seasonal dietary In contrast, consumption was undetectable variations, mostly influenced by changes in by tethers, which we think could be due to the availability of food resources in the area the low number of waterfowl encountering rather than by their nutritional quality. tethers. This possibly resulted from their Mallard and Eurasian Coot abundances high mobility in the area and/or the high recorded in our study appear to increase abundance of other resources in the neigh- from summer to autumn, following patterns boring lagoon (Menéndez and Sánchez previously reported (Martínez-Vilalta, 1996; 1998; Menéndez and Comín 2000). In fact, Marco-Méndez et al. 2015). Although both we know from the other simultaneous study Waterfowl Feeding on Rice Fields 245

Table 1. SIMPER (Clarke and Warwick 2001) analysis showing the contribution of food items to dissimilarity (Jac- card Index) between Mallard (Anas platyrhynchos) and Eurasian Coot (Fulica atra) stomach contents. Spiral ditch grass leaves (SD-L); spiral ditch grass seeds (SD-S); sago pondweed leaves (SP-L); rice seeds (Rice-S). The cut off for low contributions is 90%. Similarity is given as SD (standard deviation). Mallard (average similarity: 20.53 ) Species Average Abundance Average Similarity Similarity/SD Contribution (%) Cumulation (%) SD-S 39.10 12.79 0.39 62.31 62.31 Rice-S 29.38 6.53 0.28 31.81 94.12

Eurasian Coot (average similarity: 77.78) Species Average Abundance Average Similarity Similarity/SD Contribution (%) Cumulation (%) SP-L 88.89 77.78 1.84 100 100

Mallard and Eurasian Coot (average dissimilarity = 94.64 ) Mallard Eurasian Coot Average Average Species Abundance Abundance Average Dissimilarity Dissimilarity/SD Contribution (%) Cumulation (%) SP-L 4.84 88.89 42.56 2.71 44.97 44.97 SD-S 39.10 0 19.55 0.81 20.66 65.63 Rice-S 29.38 0 14.69 0.67 15.52 81.15 SD-L 9.54 11.11 9.27 0.59 9.79 90.95

(Marco-Méndez et al. 2015) that waterfowl terfowl grazing by growing more (Howe and were also visiting the lagoon in summer and Westley 1988; Prado et al. 2011), but this can- grazing actively on spiral ditch grass, prob- not be assessed from the data in this study. ably influenced by the higher abundance The grazing detected by the tethering ex- of its flowers. This together with waterfowl periment appears to be consistent with the abundance data suggests that in summer greater waterfowl abundance, rice biomass both species were probably feeding actively and seeds in autumn, while both ‘shading’ in both habitats. Therefore, this grazing on effects and plant compensatory mechanisms the rice field seems plausible despite teth- are likely to have interfered in cage experi- ering experiments not detecting such con- ment results. Hence, despite these possible sumption. ‘masking effects’ our results suggest that wa- In autumn, although waterfowl abun- terfowl did feed on the rice field over the dance tends to increase, cage experiments entire study period, causing a notable reduc- did not detect the effects of waterfowl graz- tion in rice plant biomass in summer and ing on the rice field either in plant or seed rice seeds in autumn. biomass. However, tethering experiments Gut content analyses showed differences did show grazing with an emphasis on seed between waterfowl species diets, identifying consumption. Here, the lower biomass of the Mallard as primarily a granivorous spe- rice plants and seeds inside exclusion cages cies and the Eurasian Coot as primarily an vs. control cages suggests that grazing effects herbivore species. Among the range of food were possibly masked by a ‘shading effect.’ items found in gut contents, rice seeds and We hypothesize that the 1.5-cm2 netting spiral ditch grass seeds were the most impor- mesh used could have created light-limiting tant food resource for Mallards, while sago conditions during the time duration of the pondweed and spiral ditch grass fragments experiment, thus reducing growth and seed were the most important for Eurasian Coots, production in the rice plants (Bello et al. confirming their reported dietary prefer- 1995; Schou et al. 1998). Alternatively, rice ences (Rodríguez-Villafrañe et al. 2007; Staf- plants may also have compensated for wa- ford et al. 2010). These results are in con- 246 Waterbirds cordance with the local abundance of spiral *** sago ditch grass and sago pondweed in the Ebro Delta lagoons (Prado et al. 2011), show- P- value 0.000 ing that waterfowl were also feeding there at the time of collection (autumn-winter). seeds (SD-S);

F In particular, Potamogeton and spiral ditch 17.62 grass seeds (commonly available in autumn-

NT winter; Green et al. 2002; Rodríguez-Pérez C:N and Green 2006) and flowers (in summer;

MS Marco-Méndez et al. 2015) are known to be 13.208 232.737

spiral ditch grass subjected to high seasonal herbivory by waterfowl, with an important impact on plant SP-S = RI > Rice-S SD-S SD-L=P

5 communities (Rodríguez-Pérez and Green df 24 2006; Marco-Méndez et al. 2015). Regarding rice seeds, the fact that individuals were collected during the hunting season (autumn- *** winter) means that individuals could obtain P- value

0.000 them directly from the ripe plants or from grain not collected during harvest (Stafford et al. 2006). It is also known that hunters

F intentionally spill commercial rice grains

1670.849 (without the husk) to attract waterfowl. How- C 13 NT

δ ever, in our study we only detected this type of rice (clearly different from locally avail- MS 0.118 able rice still in the husk) in one individual, 197.245 which was discarded for dietary analyses. (Rice-S). Differences between groups were investigated with the Student Newman-Keuls were between groups (Rice-S). Differences We think that the high presence of seeds in 5

df Mallard guts seems consistent with the seed 24 SD-L = SP-L= SG-S > Rice-S Rice consumption detected by tethers in autumn and with Mallard abundance, indicating the rice fields are important feeding habitats for *** this species (Stafford et al. 2006, 2010). The P -value 0.000 importance of submerged macrophytes in the Eurasian Coot’s diet also concurs with

rice plant (Rice); seeds their greater presence in the lagoon and F with previous studies (Rodriguez-Villafañe 311.542

N et al. 2007; Marco-Méndez et al. 2015). How- 15 NT δ ever, the lack of rice plant tissue and seeds in

seeds (SP-S); their guts contrasts strikingly with their con- MS

0.179 sistent presence in the rice field during the 55.846

C signatures and nutrient contents (C:N ratios) between food items: spiral ditch grass leaves (SD-L); C signatures entire growing season. This could be due 13 to the seasonal restrictions in the collection 5 df 24

SP-S > SD-L = SP-L SD-S Rice-S Rice of individuals for analysis (some Eurasian N and δ sago pondweed

15 Coots were hunted in November) and that guts may reflect a post-harvest scenario; as a

(SP-L); consequence of decreasing food availability in the rice field (despite residual uncollect- ed seeds), Eurasian Coots probably moved to the lagoon for feeding. Stable isotope analyses and mixed model results showed that in the long term both = predicted probability or proportion; *** denotes statistically significant P < 0.001; NT = no probability P = predicted MS = mean square; of freedom; post-hoc test (SNK) (Zar 1984). Df = degrees transformation. Source of Variation pondweed leaves SNK Table 2. Differences in δ 2. Differences Table Residual Transformation Food item Waterfowl Feeding on Rice Fields 247

Figure 4. (A) δ15N and δ13C signatures and (B) C:N ratios in the muscle of Mallard and Eurasian Coot and in the different food items. Mean ± SE.

Eurasian Coots and Mallards seem to ac- content analyses for Mallards, showing that quire most of their dietary needs from rice individuals were intensively feeding in the plants and sago pondweed (seeds or plant short or long term in the rice field during tissue according to their seasonal availabil- the growing season. However, gut content ity). These results seem to match with gut analyses of Eurasian Coots pointed to a diet 248 Waterbirds based on macrophytes, while mixed model portant reduction of natural wetlands) rice results also showed an important long-term fields act as a complimentary feeding habi- contribution of rice plants to their diet. This tat for waterfowl during the growing season. apparent discrepancy between gut and sta- Hence, this use of such croplands by water- ble isotope analyses is likely to be related to fowl could help mitigate the loss of natural temporal changes in the diet. In fact, while habitats in other areas progressively domi- gut contents can only reflect waterfowl diet nated by agriculture. For this reason, in- at the moment of collection (autumn-win- creasing collaboration between researchers, ter), waterfowl muscle tissue can retain in- farmers and agronomists is needed to bet- formation of previous feeding locations for ter understand how appropriate field and periods of several weeks before individuals crop management can increase the conser- were collected (Tieszen et al. 1983; Hobson vation value of farmland for birds, without and Clark 1992a). Therefore, stable isotope compromising its economic viability. Future analyses suggest that Eurasian Coots were research could include the availability and feeding in rice fields during the growing value of wildfowl foods other than rice in the season (at least at the end of the season), fields, importance of field edges and water while gut contents seem to be reflecting a delivery infrastructure, effects of rice farm- post-harvest scenario where Eurasian Coots ing on population dynamics and a clearer feed mainly in the lagoon. In fact, changes analysis of how socio-economic factors influ- in diet and foraging behavior have been pre- ence the ecology and conservation of wet- viously reported in both species (Guillemain land birds using rice fields. et al. 2002; Dessborn et al. 2011). These al- low them to face seasonal changes in abun- Acknowledgments dance or availability of food within the wetland (Rodríguez-Pérez and Green 2006) This study was carried out under a collaboration and respond to the differential nutritional agreement between IRTA Aquatic Ecosystems and the University of Alicante, and we are grateful for their requirements of wintering seasons (higher scientific and technical support. We are also grateful consumption of carbohydrate-rich seeds) to Toni Curcó (Parc natural del Delta de l´Ebre), Ig- or breeding seasons (increased protein-rich nasi Ripoll (Riet Vell reserve/SEO BirdLife) and the food; Baldassarre and Bolen 1994; Hohman Restaurant L’Estany (Casa de Fusta) for sharing their et al. 1996). In addition, studies also suggest data with us and providing advice and experimental location without which this study could not have been that herbivores maximize the consumption possible. Individuals used for dietary analyses were of food items with higher nutritional, pro- provided by the Restaurant L’Estany (Casa de Fusta) tein and energy contents (Hughes 1980). following the legal framework established for the Thus, high nutritional contents could influ- hunting of these species. The experiment was autho- ence higher consumption of macrophytes by rized by the authorities of the environmental department of Generalitat de Cataluña responsible for the Eurasian Coots. Similarly, seed selectivity of Ebro Delta Park management. We specially thank Ken waterfowl may be related to other factors not Heck whose advice has been crucial during the writing measured here, such as high protein and/ of the manuscript, and Julie Smith and Guido Jones or energy contents (Hughes 1980; Sedinger for the English revision. and Raveling 1984; Murphy and King 1987) or by the ease with which they can be digest- Literature Cited ed (Charalambidou and Santamaría, 2002). Ultimately, our results suggest that waterfowl Acosta, M., L. Mugica, C. Mancina and X. Ruiz. 1996. Resource partitioning between Glossy and White feed complimentarily on rice fields during Ibises in a rice field system in south central Cuba. the growing season; this is mostly influenced Colonial Waterbirds 19: 65-72. by seasonal changes in the availability of Baldassarre, G. A. and E. G. Bolen. 1984. Field-feeding food resources in the area rather than by ecology of waterfowl wintering on the Southern their nutritional quality. High Plains of Texas. Journal of Wildlife Manage- ment 48: 63-71. Our results confirm that in Mediterra- Bello, I. A., M. D. Owen and H. M. Hatterman-Valenti. nean regions (where there has been an im- 1995. Effect of shade on velvetleaf (Abutilon theo- Waterfowl Feeding on Rice Fields 249

phrasti) growth, seed production, and dormancy. via borin): implications for delineating dietary and Weed Technology 9: 452-455. migratory associations in wild passerines. Canadian Bird, J. A., G. S. Pettygrove and J. M. Eadie. 2000. The Journal of Zoology 81: 1630-1635. impact of waterfowl foraging on the decomposition Hoffmann, L. and A. R. Johnson. 1991. Extent and con- of rice straw: mutual benefits for rice growers and trol of flamingo damage to rice crops in the Camar- waterfowl. Journal of Applied Ecology 37: 728-741. gue (Rhône delta, southern France). Pages 119-127 Charalambidou, I. and L. Santamaría. 2002. Waterbirds in Reunión Técnica Sobre la Situación y Problemáti- as endozoochorous dispersers of aquatic organisms: ca del Flamenco Rosa (Phoenicopterus ruber roseus) en a review of experimental evidence. Acta Oecologia el Mediterráneo Occidental y África Noroccidental 23: 165-176. (M. R. Pintos Martin, S. Pietro Ojeda, M. Rendon Clarke, K. R. and R. M. Warwick. 2001. Change in ma- Martos and A. R. Johnson, Eds.). Agencia de Medio rine communities: an approach to statistical analysis Ambiente, Sevilla, Spain. and interpretation, vol. 2. PRIMER-E, 2nd ed., Plym- Hohman, W. L., T. M. Stark and J. L. Moore. 1996. Food outh Marine Laboratory, Plymouth, England, U.K. availability and feeding preferences of breeding Ful- Dessborn, L., A. Brochet, J. Elmberg, P. Legagneux, vous Whistling-ducks in Louisiana rice fields. Wilson M. Gauthier-Clerc and M. Guillemain. 2011. Geo- Bulletin 108: 137-150. graphical and temporal patterns in the diet of pin- Howe, H. F. and L. C. Westley. 1988. Ecological relation- tail Anas acuta, wigeon Anas penelope, mallard Anas ships of plants and animals. Oxford University Press, platyrhynchos and teal Anas crecca in the Western Pa- New York, New York. learctic. European Journal of Wildlife Research 57: Hughes, K.Y. 1980. Optimal foraging theory in the ma- 1119- 1129 rine context. Oceanography and Marine Biology Elphick, C. S. and L. W. Oring. 1998. Winter manage- Annual Review 18: 423-481. ment of Californian rice fields for waterbirds. Jour- Ibáñez, C., A. Curcó, X. Riera, I. Ripoll and C. Sánchez. nal of Applied Ecology 35: 95-108. 2010. Influence on birds of rice field management Evans Ogden, L. J., K. A. Hobson and D. B. Lank. 2004. practices during the growing season: a review and Blood isotopic (δ13C and δ15N) turnover and diet— an experiment. Waterbirds 33: 167-180. tissue fractionation factors in captive Dunlin (Calid- Inger, R. and S. Bearhop. 2008. Applications of stable ris alpina pacifica). Auk 121: 170-177. isotope analyses to avian ecology. Ibis 150: 447-461. Fasola, M. and X. Ruiz. 1996. The value of rice fields Inger, R., G. D. Ruxton, J. Newton, K. Colhoun, K. as substitutes for natural wetlands for waterbirds in Mackie, J. A. Robinson and S. Bearhop. 2006. Us- the Mediterranean region. Colonial Waterbirds 19: ing daily ration models and stable isotope analysis to 122-128. predict biomass depletion by herbivores. Journal of Fasola, M. and X. Ruiz. 1997. Rice farming and water- Applied Ecology 43: 1022-1030. birds: integrated management in an artificial Lane, S. J. and M. Fujioka. 1998. The impact of changes landscape. Pages 210-235 in Farming and Birds in in irrigation practices on the distribution of forag- Europe: the Common Agricultural Policy and its ing egrets and herons (Ardeidae) in the rice fields Implications for Bird Conservation (D. J. Pain and of central Japan. Biological Conservation 83: 221- M. W. Pienkowski, Eds.). Academic Press, London, 230. England, U.K. Legagneux, P., M. Duhart and V. Schricke. 2007. Seeds Fasola, M., L. Canova and N. Saino. 1996. Rice fields consumed by waterfowl in winter: a review of meth- support a large portion of herons breeding in the ods and a new web-based photographic atlas for seed Mediterranean region. Colonial Waterbirds 19: 129- identification. Journal of Ornithology 148: 537-541. 134. Longoni, V. 2010. Rice fields and waterbirds in the Med- Green, A. J., J. Figuerola and M. I. Sánchez. 2002. Im- iterranean region and the Middle East. Waterbirds plications of waterbird ecology for the dispersal of 33: 83-96. aquatic organisms. Acta Oecologica 23: 177-189. Manley, S. W., R. M. Kaminski, K. J. Reinecke and P. D. Guillemain, M., G. Martin and H. Fritz. 2002. Feeding Gerard. 2004. Waterbird foods in winter-managed methods, visual fields and vigilance in dabbling rice fields in Mississippi. Journal of Wildlife Manage- ducks (Anatidae). Functional Ecology 16: 522-529. ment 68: 74-83. Hobson, K. A. and R. G. Clark. 1992a. Assessing avian Mañosa, S., R. Mateo and R. Guitart. 2001. A review of diets using stable isotopes. 1. Turnover of C-13 in the effects of agricultural and industrial contamina- tissues. Condor 94: 181-188. tion on the Ebro Delta biota and wildlife. Environ- Hobson, K. A. and R. G. Clark. 1992b. Assessing avian mental Monitoring and Assessment 71: 187-205. diets using stable isotopes. 2. Factors influencing Marco-Méndez, C., P. Prado, L. M. Ferrero-Vicente, C. diet-tissue fractionation. Condor 94: 189-197. Ibáñez, and J. L. Sánchez-Lizaso. 2015. Seasonal effects Hobson, K. A. and R. G. Clark. 1993. Turnover of 13 C of waterfowl grazing on submerged macrophytes: the in cellular and plasma fractions of blood: implica- role of flowers. Aquatic Botany 120: 275-282. tions for nondestructive sampling in avian dietary Martínez-Vilalta, A. 1996. The rice fields of the Ebro studies. Auk 110: 638-641. Delta. Pages 173-186 in Management of Mediterra- Hobson, K. A. and F. Bairlein. 2003. Isotopic discrimina- nean Wetlands (C. Morillo and J. L. González, Eds.). tion and turnover in captive Garden Warblers (Syl- Ministerio de Medio Ambiente, Madrid, Spain. 250 Waterbirds

McGlathery, K. J. 1995. Nutrient and grazing influences Doñana, south-west Spain. Biological Conservation on a subtropical seagrass community. Marine Ecol- 141: 1371-1388. ogy Progress Series 122: 239-252. Rodríguez-Pérez, H. and A. J. Green. 2006. Water- Menéndez, M. and A. Sanchez. 1998. Seasonal varia- bird impacts on widgeon grass Ruppia maritima in tions in P-I responses of Chara hispida L. and Pota- a Mediterranean wetland: comparing bird groups mogeton pectinatus L. from stream Mediterranean and seasonal effects. Oikos 112: 525-534. ponds. Aquatic Botany 61: 1-15. Rodríguez-Villafañe, C., E. Bécares and M. Fernán- Menéndez, M. and F. Comín. 2000. Spring and sum- dez-Aláez. 2007. Waterfowl grazing effects on sub- mer proliferation of floating macroalgae in a Medi- merged macrophytes in a shallow Mediterranean terranean coastal lagoon (Tancada lagoon, Ebro lake. Aquatic Botany 86: 25-29. Delta, NE Spain). Estuarine Coastal and Shelf Sci- Sánchez-Guzmán, J. M., R. Morán, J. A. Masero, C. ence 51: 215-226. Corbacho, E. Costillo, A. Villegas and F. Santiago- Mitchell, S. F. and M. R. Perrow. 1998. Interactions be- Quesada. 2007. Identifying new buffer areas for tween grazing birds and macrophytes. Pages 175- conserving waterbirds in the Mediterranean basin: 196 in The Structuring Role of Submerged Macro- the importance of the rice fields in Extremadura, phytes in Lakes (E. Jeppesen, M. A. Søndergaard, Spain. Biodiversity and Conservation 16: 3333- M. O. Søndergaard and K. Christoffersen, Eds.). 3344. Springer-Verlag, New York, New York. Schou, J. B., D. L. Jeffers and J. G. Streeter. 1978. Ef- Mouronval, J. B., M. Guillemain, A. Canny and F. Po- fects of reflectors, black boards, or shades applied irier. 2007. Diet of non-breeding wildfowl Anatidae at different stages of plant development on yield of and Eurasian Coot Fulica atra on the Perthois grav- soybeans. Crop Science 18: 29-34. el pits, northeast France. Wildfowl 57: 68-97. Sedinger, J. S. and D. G. Raveling. 1984. Dietary selec- Murphy, M. E. and J. R. King. 1987. Dietary discrimina- tivity in relation to availability and quality of food tion by molting white-crowned sparrows given diets for goslings of cackling geese. Auk 101: 295-306. differing only in sulfur amino acid concentration. SPSS, Inc. 2009. Advanced statistics v. 18. SPSS, Inc., Physiological Zoology 60: 279-289. Chicago, Illinois. Perrow, M. R., J. H. Schutten, J. R. Howes, T. Holzer, Stafford, J. D., R. M. Kaminski and K. J. Reinecke. F. J. Madgwick and A. J. Jowitt. 1997. Interactions 2010. Avian foods, foraging and habitat conserva- between coot (Fulica atra) and submerged macro- tion in world rice fields. Waterbirds 33: 133-150. phytes: the role of birds in the restoration process. Stafford, J. D., R. M. Kaminski, K. J. Reinecke and S. Hydrobiologia 342/343: 241-255. W. Manley. 2006. Waste rice for waterfowl in the Petrie, S. and K. Rogers. 1996. Foods consumed by Mississippi Alluvial Valley. Journal of Wildlife Man- breeding white-faced whistling ducks (Dendrocygna agement 70: 61-69. viduata) on the Nyl river floodplain, South Africa. Tieszen, L. L. and T. Boutton. 1989. Applications of Gibier Faune Sauvage 13: 755-771. stable isotopic ratios in terrestrial ecosystems. Phillips, D. L. and J. W. Gregg. 2003. Source partition- Pages 167-195 in Stable Isotopes in Ecological Re- ing using stable isotopes: coping with too many search (P. W. Rundel, J. R. Ehleringer and K. A. sources. Oecologia 136: 261-269. Nagy, Eds.). Springer-Verlag, New York, New York. Pierluissi, S. 2010. Breeding waterbirds in rice fields: a Tieszen, L. L., Boutton, T. W., Tesdahl, K. G. and global review. Waterbirds 33: 123-132. Slade, N. A. 1983. Fractionation and turnover of Prado, P., N. Caiola and C. Ibáñez. 2013. Spatio- stable carbon isotopes in animal tissues: implica- temporal patterns of submerged macrophytes in tions for δ13C analysis of diet. Oecologia 57: 32-37. three hydrologically altered Mediterranean coastal Tourenq, C., N. Sadoul, N. Beck, F. Mesléard and J. L. lagoons. Estuarine Coastal and Shelf Science 36: Martin. 2003. Effects of cropping practices on the 414-429. use of rice fields by waterbirds in the Camargue, Prado, P., T. Alcoverro and J. Romero. 2010. Influ- France. Agriculture Ecosystems and Environments ence of nutrients in the feeding ecology of seagrass 95: 543-549. Posidonia oceanica (L.) consumers: a stable isotopes Tourenq, C., R. E. Bennetts, N. Sadoul, F. Mesleard, Y. approach. Marine Biology 157: 715-724. Kayser and H. Hafner. 2000. Long-term population Prado, P., F. Tomas, T. Alcoverro and J. Romero. 2007. and colony patterns of four species of tree-nesting Extensive direct measurements of Posidonia oceani- herons in the Camargue, South France. Waterbirds ca defoliation confirm the importance of herbivory 23: 236-245. in temperate seagrass meadows. Marine Ecology Tourenq, C., S. Aulagnier, F. Mesléard, L. Durieux, A. Progress Series 340: 63-71. Johnson, G. Gonzalez and S. Lek. 1999. Use of arti- Prado, P., C. J. Collier, J. Romero and T. Alcoverro. ficial neural networks for predicting rice crop dam- 2011. Distinctive types of leaf tissue damage influ- age by greater flamingos in the Camargue, France. ence nutrient supply to growing tissues within sea- Ecological Modeling 120: 349-358. grass shoots. Marine Biology 158: 1473-1482. Tréca, B. 1994. The diet of ruffs and black-tailed god- Rendón, M. A., A. J. Green, E. Aguilera and P. Al- wits in Senegal. Ostrich 65: 256-263. maraz. 2008. Status, distribution and long-term Underwood, A. J. 1997. Experiments in ecology: their changes in the waterbird community wintering in logical design and interpretation using analysis of Waterfowl Feeding on Rice Fields 251

variance. Cambridge University Press, Cambridge, Marine Ecology Laboratories, University of Sydney, U.K. Sydney, Australia. Underwood, A. J., M. G. Chapman and S. A. Richards. Viada, C. 1998. Áreas importantes para las aves en Es- 2002. GMAV-5 for Windows. An analysis of vari- paña, 2nd ed. Sociedad Española de Ornitología/ ance programme. Unpublished report, Centre for BirdLife, Madrid, Spain. (In Spanish). Research on Ecological Impacts of Coastal Cities, Zar, J. H. 1984. Biostatistical analysis, 2nd. ed. Prentice Hall, Inc., Englewood Cliffs, New Jersey.