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Managed marshes can be good alternatives to natural marshes as breeding habitats for birds
Ecological Engineering 139 (2019) 105584
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Managed marshes can be good alternatives to natural marshes as breeding habitats for birds Junyan Wanga, Qianyan Zhoua, Wei Wub, Wei Liangc, Qiang Mab, Zhijun Maa,
T
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a Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Coastal Ecosystems Research Station of the Yangtze River Estuary, and Shanghai Institute of Eco-Chongming (SIEC), Fudan University, Shanghai 200433, China b Management Office of Chongming Dongtan Nature Reserve, Chongming 202183, China c Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou 571158, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Acrocephalus orientalis Artificial wetlands Breeding success rate Marsh birds Nest predation Oriental reed warbler Wetland management
Loss of natural tidal marshes has caused rapid population declines for many bird species, raising the question about whether managed marshes can be used for bird conservation. Although many studies have indicated that managed marshes can provide a complementary habitat for birds, it is unclear how the breeding habitats provided by managed marshes compare with those provided by natural marshes. We compared habitat conditions (vegetation and food) and breeding performance of a common reed specialist, the Oriental reed warbler (Acrocephalus orientalis), in natural and managed artificial reed marshes (about 2 km × 5 km) at Chongming Dongtan, an estuarine wetland in China. We found that vegetation was denser and warbler food resources were greater in managed than in natural marshes. The density of breeding territories, nest density, clutch size, egg size, and fledgling number per nest were greater in managed than in natural marshes. Breeding failure was reduced in managed marshes because of a reduced risk of nest predation. However, the high nest position on the reeds in the managed marshes increased the risk of nest destruction by strong wind. The better breeding performance in managed than in natural marshes could be attributed to the following factors: the high and stable water level in the managed marshes increased reed growth and arthropod reproduction and decreased access by terrestrial predators; dense vegetation helped conceal nests from predators; and human activities in the managed marshes deterred nest predators. The results suggest that managed marshes can provide quality breeding habitat for the Oriental reed warbler and probably for other marsh birds and can therefore help compensate for the loss of natural marshes. The preference of the Oriental reed warbler for managed marshes largely depends on the suitable habitat conditions. The current study highlights the importance of maintaining a relatively high and stable water level.
1. Introduction Tidal marshes along the coasts provide important habitats for birds (Greenberg, 2006; Gedan et al., 2009). Yet tidal marshes have been seriously damaged over the past several decades by anthropogenic activities, such as reclamation and exploitation, and by sea level rise. As a consequence, many species of marsh birds have suffered dramatic population declines due to habitat loss (Takekawa et al., 2006; Wilson et al., 2007; Correll et al., 2016). On the other hand, the coastal area represented by artificial or managed marshes has increased worldwide (Ramsar Convention Secretariat, 2010). An important question is whether managed marshes are good alternatives to natural marshes. Many studies have compared bird communities in natural vs. managed marshes. The results have indicated that although managed
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marshes cannot replace all of the ecological functions of natural marshes, they can provide a complementary habitat for many birds and thus mitigate the negative effects of natural marsh loss (e.g., Melvin and Webb, 1998; Desrochers et al., 2008; Li et al. 2013). In comparing managed and natural marshes as habitats for birds, breeding habitat is particularly important for several reasons. First, the breeding period is critical in the annual cycle of birds, and reproductive output will obviously affect population maintenance (Bradbury et al., 2000). Second, birds have strict habitat requirements for breeding (Wilson et al., 2007). Documenting and comparing the demographic benefits of managed and natural marshes would provide critical information needed for bird conservation. It is unclear, however, how the breeding habitats provided by managed marshes compare with those provided by natural marshes.
Corresponding author. E-mail address: [email protected] (Z. Ma).
https://doi.org/10.1016/j.ecoleng.2019.105584 Received 7 December 2018; Received in revised form 12 August 2019; Accepted 24 August 2019 Available online 30 August 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.
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provide high and stable water levels that are suitable for the growth of reeds (Tanneberger et al., 2009), we hypothesized that reeds in managed marshes are higher and denser and contain more arthropod food resources for the warblers than reeds in natural marshes. Second, because marsh birds prefer nest sites with dense vegetation and abundant food (Batáry et al., 2004), we hypothesized that the warblers establish breeding territory earlier, and that nest density is higher in the managed than in the natural marshes. Our third hypothesis was that there is no significant difference in breeding performance of birds, in terms of clutch sizes, egg sizes, and body condition of fledglings, between managed and natural marshes. Finally, we hypothesized that the stable water level, dense vegetation, and frequent human activities in the managed marshes reduce nest predation (Ibáñez-Álamo et al., 2015) and thereby increase the breeding success rate.
Different environmental conditions between natural and managed marshes affect habitat use and breeding performance of marsh birds. Natural marshes along the coasts are strongly influenced by tidal rhythms, and these hydrological conditions greatly affect plant communities (Greenberg, 2006). In addition, natural marshes are often inconvenient for human activities, and thus are seldom directly affected by human disturbance (Greenberg, 2006; Gedan et al., 2009). Unlike natural marshes, managed marshes are generally enclosed by dams and are not affected by tidal rhythms. Hydrological conditions in managed marshes are controlled by managers, are relatively stable, and affect the plant communities that develop (Ma et al., 2010). In addition to being managed, managed marshes differ from natural marshes in that they often support some commercial production and tourism (Desrochers et al., 2008; Li et al., 2013). Vegetation characteristics and food resources are the key factors affecting habitat use of birds in breeding season. Marsh birds prefer to nest in densely vegetated areas, perhaps because such areas increase nest concealment (Batáry et al., 2004; Jedlikowski et al., 2015). In addition, dense vegetation usually contains high numbers of invertebrates, which are the main food for breeding marsh birds, and therefore supports high nest densities. Because both vegetation characteristics and invertebrate diversity are affected by hydrologic conditions (Manci and Rusch, 1988), the differences in vegetation characteristics and food resources between natural and managed marshes may strongly affect the habitat use and breeding performance of birds. Nest predation is an important cause of breeding failure in birds (Ibáñez-Álamo et al., 2015; Menezes and Marini, 2017). Nest predators in marshes include both terrestrial and aerial predators (Picman et al., 1993; Takekawa et al., 2006; Ibáñez-Álamo and Soler, 2010). Foraging by terrestrial predators is generally reduced by deep water (Picman et al., 1993; Jobin and Picman, 1997), and the detectability of nests is reduced by dense vegetation (Jobin and Picman, 1997). In addition, some nest predators are deterred by human activity (Dyrcz and Nagata, 2002; Ibáñez-Álamo and Soler, 2010). As a consequence, differences in hydrologic conditions, vegetation, and human activity could affect nest predation and finally the breeding success of marsh birds in managed and natural marshes. Given the widespread declines in marsh birds due to loss of natural habitats (Takekawa et al., 2006; Wilson et al., 2007; Correll et al., 2016), it is critical to understand how well managed marshes function as habitats for birds. A recent wetland restoration project at the Chongming Dongtan Ramsar site (CMDT, 121.9°E, 31.6°N) in the Yangtze Estuary, China, provides an opportunity for comparing natural and managed marshes as habitats for breeding birds. The large area of reed (Phragmites australis) marshes on the natural tideland wetlands at CMDT supports diverse marsh-breeding birds (Ma et al., 2011). To eradicate the alien invasive smooth cordgrass (Spartina alterniflora) that rapidly spread on the tideland, an ecological engineering project was implemented in 2010. The seawall constructed as part of this project enclosed tidal marshes dominated by smooth cordgrass. The aboveground parts of the smooth cordgrass were cut off during the growing season, and the underground parts were killed by flooding for > 2 months. Native reeds were subsequently planted, resulting in the creation of an managed marsh that provided resting, foraging, and breeding habitats for birds (Ma, 2017). The oriental reed warbler (Acrocephalus orientalis) is a common reed specialist in Eastern Asia. It constructs nests on reed stems and greatly depends on reed habitat in breeding season (Lei, 2010; Dyrcz and de Juana, 2018). The abundance of the Oriental reed warbler has declined because of the dramatic loss of natural marshes (Lei, 2010). Earlier studies indicated that Oriental reed warblers breed in both natural and managed reed marshes at CMDT (Wang, 2015), suggesting that managed marshes might mitigate the loss of natural marshes. Here, we compared habitat conditions and breeding performance of the Oriental reed warbler in the natural and managed marshes at CMDT. We tested four hypothesis. First, because managed marshes
2. Methods 2.1. Study sites The natural marsh at CMDT experiences regular inundation by tidewater. The tide is regular and semidiurnal, with two high and two low tides every day. All of the tidal flats are submerged by tidewater during the high tide of the spring tide and are exposed during the neap tide and the low tide of spring tide (Ma et al., 2011). The marsh vegetation is mainly composed of reeds in the high tide zone and bulrush (Scirpus spp.) in the middle tide zone. The height of the reeds submerged by the tidewater is generally < 50 cm. Birds can nest on the reeds but not on the bulrush, which is short (< 50 cm) and is completely submerged by tidewater during high tide. Thus, the reedbed is the main breeding habitat for marsh birds (Gan et al., 2009; Ma et al., 2011). During breeding season, human activity is rare in the natural marsh. The area with managed marshes is adjacent to the area with natural marshes at CMDT. They are enclosed by a seawall and thus are not affected by tides. Embankments divide the whole area into three different zones, each of which is ~1 to 2 km2 (Fig. S1). The area of reed and open water roughly accounts for half of the total area in each zone. The water level is generally lowered in early spring to promote reed germination. Following reed germination, the water level is raised and maintained at a certain depth to favor reed growth. In 2013, the water depth was ~30 cm during the breeding period of birds. In 2014, due to frequent rainfall, the water depth was ~60 cm during the breeding season. The managed marshes have boardwalks and public education infrastructure and are frequently visited by humans. Moreover, the administrative staff patrols the seawall and embankment every day. Both the natural and managed reed marshes support diverse birds. Over 20 species of marsh-breeding birds have been recorded at each of the two habitats (Gan et al., 2009; Ma et al., 2011; Wang, 2015). The Oriental reed warbler is the dominant bird species in both kinds of marshes. Individuals of this species arrive at CMDT from their nonbreeding grounds in late April and build nests exclusively in the reedbed (Ma et al., 2011). The reeds form a monoculture in both the natural and managed marshes. Because reeds were not harvested in the study region in year before the study, both old and new stems were present and intermixed in the reedbeds during the current study. 2.2. Vegetation surveys We conducted surveys using the same methods in the two breeding seasons of 2013 and 2014. To avoid edge effects, all surveyed sites were located > 10 m from the edge of vegetation. We randomly selected sampling sites (~10 ha per site) with continuous and uncut reeds vegetation in the managed marshes (one site in each zone) and also in the adjacent natural marshes (three in managed marshes and three in natural marshes, Fig. S1). At each site, five 0.5 m × 0.5 m plots were designated. In late April, when the Oriental reed warblers begin to 2
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survey day. The sequence used to survey plots was randomized each day to avoid a potential effect of survey time on the results.
establish their breeding territories, we measured reed stem number, stem height (for stems higher than 0.5 m), and stem diameter (at 1.0 m height, for the highest 10 stems). The reed vegetation was composed of dry stems that grew in the previous year and growing stems that newly spouted that year. We measured the growing and dry stems separately. Because reeds grow rapidly in late April, the vegetation surveys in managed and natural marshes were conducted on the same day in each year.
2.6. Nest surveys Nests were surveyed in early June when birds have finished nest construction. We used the same plots used for the territory surveys. Two or three investigators walked together, with 3 m between them, and searched for nests from one side to another side of each plot. The investigators walked along different routes to cover the entire plot. When a nest was found, it was numbered and its location was recorded using a hand-held Global Position System (GPS). The height of the nest from the ground was measured. The breeding period was determined based on the condition of nests, eggs, or nestlings (Lei, 2010; Wang 2015). After finding and recording a nest, the investigator bound together the reed stalks located ~2 m away from the nest to facilitate the finding of the nest in subsequent surveys.
2.3. Surveys for bird food resources We collected arthropods, the food for the Oriental reed warblers (Lei, 2010; Dyrcz and de Juana, 2018), using sweeping nets (35 cm diameter) in the same sites used for vegetation surveys (three sites per marsh type). We randomly selected five plots in each sample. Arthropods were collected by sweeping vegetation 50 times with an insect net in a radius of 1 m in each of five randomly selected plots (10 m2/ plot) per site. While sweeping the net, we hit the reed stems with the net frame to frighten the arthropods attached to the leaves or stems in order to enhance their collection. The captured arthropods were kept in plastic bottles containing 75% alcohol. Because arthropod activity is affected by time of day and weather, arthropods were collected around noon on clear days. Arthropod surveys were conducted twice each year: in early May, when birds establish their breeding territories (early breeding period), and in late June, after fledging (late breeding period). Arthropods were identified to order and counted.
2.7. Breeding monitoring An automatic time-lapse camera (DPS 63070, Primos, Flora, MS, USA) was placed on a tripod ~1 m from each nest to record nest activities. The camera photographed the nest every 5 s. The nests and the cameras were checked every 4–5 days until fledging occurred or breeding failed. Oriental reed warblers lay one egg every day (~3 to 6 eggs in total), and the incubation period is ~2 weeks (Lei, 2010; Dyrcz and de Juana, 2018). We estimated the date of egg laying (as the date when the first egg was laid) for each nest according to the camera records, number of eggs in the nests and the incubation period date. When eggs began to hatch, clutch size was recorded. We also measured the length (L) and breadth (B, maximum diameter) of each egg with a Vernier caliper (to the nearest 0.1 mm) in 2014. The nestling period is ~12 days (Lei, 2010; Wang, 2015). Because body mass and size are stable when nestlings are close to fledging, body mass and tarsus length of the nestlings were measured on the 10th or 11th day after hatching as indicators of fledgling body condition. Disturbance to the nests and nestlings was minimized during the surveys. We determined the causes of breeding failure based on the photographs taken by the cameras, the status of the nestlings, and the presence of predator traces, eggshell fragments, and nestling corpses. If a nestling disappeared from the nest after 9 days had passed since incubation and if the photographs did not indicate nestling mortality, we assumed that the nestling had fledged. Breeding was considered successful if a nest produced one or more fledglings.
2.4. Crab surveys Recent studies indicated that the mudflat crab Chiromantes neglectum is a nest predator of marsh-breeding birds. Crabs can climb up the reed stems and enter the nests to prey on eggs or nestlings (Yang et al., 2014; Li et al., 2015). We surveyed the mudflat crabs in natural and managed marshes at the peak breeding period in early June. The mudflat crabs generally remain on the ground during the day time. At dusk, they may climb on reed stems and enter the nests of birds (Xiong and Zhao, 2016). We designated five 10-m-long transects for crab surveys at each of the sites used for vegetation surveys. At 1 hr before sunset, investigators walked along the transects and recorded the number of crabs climbing on the reeds within 1 m of each side of the transect. To avoid an effect of human disturbance on crab activity, no other surveys was conducted on the day of crab surveys. Although this method certainly underestimated the total crab density in the area, we used the same method in both habitats, and only those crabs climbing on the reeds could be potential nest predators; this method therefore reasonably assessed the threat of crab predation in the two habitats.
2.8. Data analysis Linear mixed models (LMM) were used to detect the effects of habitat type (managed vs. natural marshes), year (2013 vs. 2014), and their interaction on the characteristics of habitats (height, diameter, and density of reeds), food for birds (density of total arthropods and the dipterans, the major food for the Oriental reed warbler, Lei, 2010; Wang, 2015), and the relative number of mudflat crabs. LMMs were also used to compare the density of bird territories between the two habitats. Habitat type, date of bird surveys, year, interactions of habitat type with year, and survey date were included in the model as fixed effects. Site serial number and plot serial number were included in LMMs as nested random factors. LMMs with site serial number and plot serial number as nested random factors were used to determine the effects of habitat type, year, and their interactions on the date on which the first egg was laid in a nest, clutch size, egg size (average of eggs in each nest), and fledgling number. Egg size in terms of egg volume (V) was estimated as V = 0.51 × L × B2 (Hoyt, 1979). Clutch size was included in the model when egg size between the two habitats was compared. LMMs were also used to detect the effects of habitat type, year, measurement date (days
2.5. Breeding territory surveys The Oriental reed warbler is generally monogamous. The males exhibit obvious territoriality involving frequent and loud singing from the upper parts of reed stems during the early breeding season (Lei, 2010, Wang, 2015). We estimated the numbers of territories by assessing the numbers of singing birds. Bird were surveyed at the same sites (three per marsh type) used for vegetation surveys. At each site, one plot with an area of 100 m × 50 m was designated. Two investigators, who were located at an elevated position ~10 m away from the plot, used 8× binoculars to determine the number of singing birds. The two investigator were ~30 to 50 m apart and therefore observed the plots from different angles. Four or five observation locations were used per plot per day, with one 3 min observation period per observation location. Territory surveys were conducted once every 2–3 days during days without rain beginning in mid-April, when birds arrived at CMDT. Territory surveys lasted 3–4 weeks until the singing decreased and birds began constructing nests. The surveys began after sunrise, ~4 h on each 3
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2013 and 2014, respectively, n = 3 for both) than in managed marshes (1.93 ± 0.31 and 0.60 ± 0.53 crabs per transect in 2013 and 2014, respectively, n = 3 for both) (F1, 48 = 68.95, P < 0.001). Moreover, crab density was significantly lower in 2014 than in 2013 (F1, 48 = 16.62, P < 0.001), and the decline between years was significantly greater in the managed than in the natural marshes (interaction between habitat type and year: F1, 48 = 11.08, P = 0.002).
after hatching), and nestling numbers in a brood on the body mass and tarsus length of birds. Two-way interactions were included in the models. Generalized linear mixed models (GLMM, with a binomial distribution and logit link function) were used to detect the effects of habitat type, year, and their interaction on the breeding success of birds and on the occurrence of nest predation. Chi-square tests were used to compare the breeding success rate and the occurrence of nest predation between the two habitats in the same year. A GLMM was also used to detect the relationship between the occurrence of nest overturn and nest height, with habitat type, year, and their interactions as fixed variables and with site serial number and plot serial number as nested random variables. All statistical analyses were performed using PASW Statistics 18.0.0 (SPSS Inc., Chicago, IL, USA). Results are presented as means ± SE.
3.4. Territory density, nest density, and nest height Territorial density increased in both habitats during the study period (F1, 8 = 306.08, P < 0.001), but was significantly higher in the managed than in the natural marshes (F1, 8 = 21.64, P < 0.001). Moreover, territorial density increased more rapidly in managed than in natural marshes (interaction of habitat type and date: F1, 8 = 30.52, P < 0.001). Similar trends were detected in the two years (F1, 8 = 0.1, P = 0.90) (Fig. 3). A total of 161 (89 in 2013 and 72 in 2014) nests were recorded in managed marshes and 92 (46 in 2013 and 46 in 2014) nests in natural marshes. Nest density was significantly greater in managed marshes (29.7 ± 4.7 and 24.3 ± 5.5 nests per ha in 2013 and 2014, respectively, n = 3 for both) than in natural marshes (15.3 ± 4.1 and 15.3 ± 3.2 nests per ha in 2013 and 2014, respectively, n = 3 for both) (F1, 8 = 33.0, P < 0.001). Nest density did not significantly differ between the two years (F1, 8 = 1.09, P = 0.33). Nests were significantly higher in managed marshes (143.7 ± 4.0 cm in 2013 and 159.0 ± 3.9 cm in 2014, n = 3 for both) than in natural marshes (120.9 ± 4.9 cm in 2013 and 119.9 ± 3.1 cm in 2014, n = 3 for both) (F1, 112 = 150.8, P < 0.001). Moreover, the nest height in managed marshes was significantly higher in 2014 than in 2013 (F1, 112 = 52.3, P = 0.01), but nest height in natural marshes did not significantly differ between the two years (F1, 112 = 0.07, P = 0.81).
3. Results 3.1. Characteristics of reed vegetation The reed vegetation significantly differed between the natural and managed marshes (Table 1). For both growing and dry reeds, stems were higher and thicker in the managed marshes than in the natural marshes. Reed density did not significantly differ between the two habitats. Although reed characteristics differed in 2013 vs. 2014, the overall trends between the two habitats were consistent in both years (Fig. 1, Table 1). 3.2. Food for birds Arthropod density significantly differed between the two habitats (F1, 48 = 40.17, P = 0.003) and between the early and late breeding periods (F1, 48 = 29.64, P < 0.001) (Fig. 2A). In the early breeding period, arthropods were more abundant in managed than in natural marshes. In the late breeding period, arthropod abundance significantly decreased in managed marshes but did not in natural marshes (interaction between habitat type and period: F1, 48 = 44.47, P < 0.001). The arthropod density was similar in 2013 and 2014 (F1, 48 = 0.65, P = 0.42) (Fig. 2A). The density of dipterans, which accounted for 76.2% and 56.6% of the arthropod abundance in managed and natural marshes respectively, exhibited the same trends as the total arthropod density (Fig. 2B).
3.5. Egg laying date, clutch size, and egg size Eggs were laid significantly earlier in the managed marshes than in the natural marshes (F1, 103 = 10.28, P = 0.03) (Fig. 4a). The date on which eggs were laid did not significantly differ between the two years (F1, 103 = 1.50, P = 0.22) (Fig. 4a). The clutch size of the Oriental reed warblers ranges from 3 to 6 eggs. The clutch size was significantly higher in managed marshes than in natural marshes (F1, 130 = 11.46, P = 0.02). Clutch size did not significantly differ between 2013 and 2014 (F1, 130 = 1.80, P = 0.18, Fig. 4b). As clutch size increased, egg size decreased (F1, 42 = 26.52, P < 0.001). For a given clutch size, egg size was significantly greater in the managed marshes than in the natural marshes (F1, 42 = 5.02, P = 0.04) (Fig. 4c).
3.3. Density of mudflat crabs The relative density of mudflat crabs was significantly greater in natural marshes (22.67 ± 5.32 and 9.47 ± 1.14 crabs per transect in
3.6. Number and body condition of fledglings
Table 1 The effects of marsh type (natural vs. managed marsh), year (2013 vs. 2014), and their interaction on the height, diameter, and density of growing reeds and dry reeds. Linear mixed models (LMM) with site serial number and plot serial number as nested random variables were used for data analysis. Independent variable
Height F1,
48
Diameter
Density
P
F1,
P
F1,
48
48
Fledglings were significantly more abundant in managed than in natural marshes (F1, 69 = 6.67, P = 0.04), and fledgling numbers did not significantly differ between the two years (F1, 69 = 0.83, P = 0.37) (Fig. 4d). Neither fledgling body mass (F1, 63 = 0.23, P = 0.64, Fig. 4e) nor tarsus length (F1, 60 = 0.60, P = 0.44, Fig. 4f) significantly differed between the two habitats. As clutch size increased, fledgling body mass (F1, 63 = 38.8, P < 0.001) and tarsus length (F1, 60 = 4.84, P = 0.03) decreased. Fledgling body mass and tarsus length did not significantly differ between the two years (F1, 63 = 1.66, P = 0.20 for body mass; F1, 63 = 1.37, P = 0.25 for tarsus) or among measurement dates (F1, 63 = 0.07, P = 0.79 for body mass; F1, 60 = 0.39, P = 0.68 for tarsus).
P
Growing reeds Marsh type Year Marsh type × Year
46.38 132.72 1.495
0.002 < 0.001 0.23
11.60 20.18 2.59
0.03 < 0.001 0.11
1.70 1.91 6.05
0.26 0.17 0.02
Dry reeds Marsh type Year Marsh type × Year
19.94 3.75 0.34
0.01 0.06 0.56
35.91 16.52 8.19
0.004 < 0.001 0.006
3.82 82.99 2.63
0.12 < 0.001 0.11
3.7. Breeding failure and causes Among all 150 nests surveyed in both habitats and both years, the
Bold values indicate P < 0.05. 4
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Fig. 1. Plant height (A, B), diameter at breast height (C, D), and density (E, F) of growing reeds (A, C, E) and dry reeds (B, D, F) in managed marshes (white bars) and natural marshes (dark grey bars). Values are means ± SE (n = 3).
breeding failure rate was 56.0%, and more than half of the breeding failures (52.4%) were caused by nest predation (Fig. 5). The Siberian weasel (Mustela sibirica) and the Lesser coucal (Centropus bengalensis) were the main nest predators and were responsible for 38.6% and 29.5%, respectively, of the nest predation caused by known predators (Fig. S2). Breeding failure also resulted from the overturning of nests by strong wind (22.6%), nest abandonment by parents (19.0%), and nest parasitism by cuckoos (Cuculus spp., 6.0%) (Fig. 5). Mudflat crabs were more frequently recorded in the nests of birds in natural marshes (24.6% in 2013 and 22.0% in 2014) than in managed marshes (2.4% in 2013 and 2.0% in 2014) (χ2 = 9.60, P = 0.004 in 2013; χ2 = 14.48, P = 0.002 in 2014). Photographs indicated, however, that the presence of crabs in nests usually occurred after the nests had been preyed upon by other predators or had been abandoned by parents (as indicated by the absence of incubation activity for at least 1 day). There was only one record of nest predation by crabs shortly after the parents left the nest in natural marshes. In 25.0% of the cases of nest predation, the predators were unknown because the predation apparently occurred at night, when the cameras did not function (Fig. S2). The breeding success rate was significantly higher in managed marshes (50.0%, n = 42 in 2013 and 61.5%, n = 39 in 2014) than in natural marshes (25.8%, n = 31 in 2013 and 37.5%, n = 38 in 2014) (Wald chi-square = 8.82, P = 0.003) (Fig. 5). This was mainly due to the lower nest predation rate in managed marshes (25.0% in 2013 and 2.6% in 2014) than in natural marshes (41.9% in 2013 and 45.8% in 2014) (Wald chi-square = 11.01, P = 0.001) (Fig. 5). The nest predation rate in managed marshes was significantly lower in 2014 than in 2013 (χ2 = 7.99, P = 0.05), while the nest predation rate in natural marshes did not significantly differ between the two years (χ2 = 0.12,
Fig. 2. Density (number of individuals per m2) of Arthropods (A) and dipterans (B), the major food of the Oriental reed warbler, in the early and late breeding periods in managed marshes (white bars) and natural marshes (dark grey bars). Values are means + SE (n = 3). 5
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Fig. 5. Breeding success and failure rates, and causes of breeding failure for the Oriental reed warblers in managed and natural marshes in 2013 and 2014. The number above each column indicates the number of nests examined.
4. Discussion This study indicated that managed marshes provide better breeding habitat for the Oriental reed warbler than the natural marshes at CMDT. The birds established breeding territories in greater numbers in the managed than in natural marshes. In managed marshes relative to natural marshes, nest density was higher (241% higher in 2013 and 197% in 2014), clutch size was greater (123% greater in 2013 and 110% in 2014), breeding success rate was higher (194% higher in 2013 and 164% in 2014), and fledgling number per nest was higher (113% higher in both 2013 and 2014). As a consequence, the number of offspring produced per unit area was 5.3 times greater in 2013 and 3.6 times greater in 2014 in the managed marshes than in the natural marshes. This suggests that the managed marshes are critical for maintenance of the Oriental reed warbler populations. With managed hydrological conditions, managed marshes provided more suitable conditions for reed growth than natural marshes, which was consistent with our first hypothesis. Although reed density was similar in the two habitats, reeds were higher and stems were thicker in the managed than in the natural marshes, suggesting that the vegetation was denser in the managed marshes. The managed marshes
Fig. 3. Territorial density of Oriental reed warblers in managed marshes (dashed line) and natural marshes (solid line) in 2013 and 2014. Values are means ± SE (n = 3).
P = 0.34). The nests in managed marshes were more likely to be overturned than those in natural marshes (overturning caused 41.9% of the breeding failures in managed marshes and 11.3% in natural marshes, χ2 = 10.47, P = 0.005) (Fig. 5). Higher nests were more susceptible to being overturned than lower nests (heights of overturned and not overturned nests were 160.0 ± 16.1 and 134.3 ± 21.3 cm, respectively, Wald chi-square = 15.8, P < 0.001).
Fig. 4. Date of egg laying (A, the date on which first egg were laid in a nest), clutch size (B), egg volume (C), fledgling number per nest (D), fledgling body mass (E), and fledgling tarsus length (F) of Oriental reed warblers in managed marshes (white bars) and natural marshes (dark gray bars). Values are means + SE (n = 3). The number above each column indicates the total number of nests examined in each habitat. 6
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unknown, nocturnal animals. The percentage of Oriental reed warbler nests that were overturned by wind increased with nest height. This could be explained by the increase in instability with increasing height on the reed stem. The high water level in managed marshes caused the birds to build their nests at relatively high positions on the reed stems, such that the nests were vulnerable to strong winds. This suggests that although a high water level helps protect nests from terrestrial predators, a too high water level could reduce breeding success due to the effects of wind. The percentage of nest parasitism was similar in the natural and managed marshes. The probability that a nest is parasitized generally increases with nest visibility (Burhans, 1997; Moskát and Honza, 2000). Although nest concealment is greater in managed marshes than in natural marshes, infrastructure (e.g., houses and poles) in managed marshes might provide perches and thereby increase the occurrence of nest parasites (Moskát and Honza, 2000).
supported a high density of arthropods in the early breeding season, perhaps because the dense vegetation and stable water level benefits the development and growth of arthropods (Poulin et al., 2002). The decreased density of total arthropod and the dipteran during each breeding season in the managed marshes may have resulted from intensive consumption by breeding birds, which require abundant food for themselves and their nestlings. With relatively fewer breeding birds in natural marshes (Wang, 2015), the food requirement is lower than in managed marshes. It is also possible that the periodic tides might increase arthropod immigration to the natural marshes. We found that the Oriental reed warbler established more breeding territories and had higher nest densities in managed than in natural marshes, suggesting that the birds prefer managed marshes as nesting sites. This finding, which was consistent with our second hypothesis, could be related to the dense vegetation and abundant food in the managed marshes. Moreover, many marsh birds prefer nesting at sites with a stable water level because a stable water levels reduces the ability of terrestrial predators to access the nests (Picman et al., 1993; Graveland, 1998). Although the territorial density was always higher in the managed than in the natural marshes, it increased in both habitats during the survey period. This suggests that when making settlement decisions, birds may use various cues, such as vegetation, food, and social information, to evaluate the tradeoff between habitat quality and intraspecific competition (Forsman et al., 2008). Inconsistent with our third hypothesis, eggs were laid earlier and clutch size was larger in the managed than in the natural marshes. This might be explained by a superior body condition of birds that nested in the managed marshes and/or by the high habitat quality of the managed marshes (Riddington and Gosler, 1995; Lambrechts et al., 2004). The greater number of fledglings per nest in the managed marshes can be related to the larger clutch size in the managed marshes. In addition, the abundant food would support more nestlings and fledglings in the managed marshes. Although fledgling body condition did not significantly differ between the two habitats, the higher nest density, clutch size, and breeding success in the managed marshes than in the natural marshes indicate that the carrying capacity for breeding Oriental reed warblers was greater in the managed marshes than in the natural marshes. Consistent with our fourth hypothesis, the breeding success rate was higher and the predation rate was lower in managed than in natural marshes. The lower predation in managed marshes the could result from the high and stable water level, the dense vegetation, and the increase in human activity, all of which would reduce the ability of predators to detect and access nests (Dyrcz and Nagata, 2002; Batáry et al., 2004; Ibáñez-Álamo and Soler, 2010; Jedlikowski et al., 2015). Although natural marshes are submerged by tidewater during the high tide of the spring tide, they are accessible to terrestrial mammals during the neap tide and the low tide of the spring tide when the tideland is exposed. The nest predation rate was significantly lower in 2014 than in 2013 in the managed marshes, perhaps because the water level was higher in 2014. The mudflat crab prefers habitats that are exposed during low tide and submerged during high tide (Xiong and Zhao, 2016). With a high and stable water level, managed marshes may be unsuitable for the mudflat crab. Thus, the density of mudflat crabs was much lower in managed marshes than in natural marshes. Although several recent studies found that the mudflat crab was a major nest predator of marsh birds (Yang et al., 2014; Li et al., 2015), we detected only one case of a nest being preyed upon by crabs. Mudflat crabs are sensitive to disturbance when climbing on the reeds (Xiong and Zhao, 2016), and are easily knocked to the ground by adult birds that stay in the nests (Wang JY, field observation). Although nest predation by crabs is not uncommon (Menezes and Marini, 2017), the mudflat crab may not be an important predator of Oriental reed warbler nests and may mainly consume eggs in abandoned nests. On the other hand, much of the nest predation in the current study occurred at night and was conducted by
4.1. Implications for conservation This study increases our understanding of the roles of managed wetlands in providing habitats for birds. Although we focused on the habitat use and breeding performance of the Oriental reed warbler, the stable water level, dense vegetation, and abundant food in the managed marshes can also provide high-quality habitats for other marshbreeding birds (e.g., Jobin and Picman, 1997; Graveland, 1998; Poulin et al., 2002). The managed and natural marshes at CMDT contain similar bird species, but bird abundances are greater in the managed marshes (Wang, 2015), suggesting that managed marshes can be a good alternative to natural ones for breeding birds. Given the rapid loss of natural marshes and the wide distribution of managed marshes worldwide, managed marshes play important function in mitigating the negative effects of loss of natural ones. The preference of the Oriental reed warbler for managed marshes largely depends on the suitable habitat conditions resulting from hydrology adjustment and the impacts of such management on the vegetation. Therefore, effective management is the key to improving the quality of managed habitats (Ma et al., 2010). While it is important to protect the remaining natural marshes, it is also important to increase and correctly manage managed marshes as habitats for breeding birds. The current study highlights the importance of maintaining a relatively high and stable water level. This study was conducted at Chongming Dongtan with limited sample size, we propose further studies at larger scale to clarify the role of managed marshes in supporting habitat for breeding birds. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements We thank K Tan, Y Chen, HB Peng, WJ Xue, XS Feng, XL Wang, C Zhang, and X Jin for field assistance, and the Chongming Dongtan Nature Reserve for facilitating the fieldwork. Funding statement This work was financially supported by the National Key Research and Development Program of China (2018YFC1406402), the National Natural Science Foundation of China (31272334), and the Science and Technology Department of Shanghai (18DZ1205002). Ethics statement All the studies were conducted with the permission of the local 7
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management office and was strictly complied with the requirement of Chinese Wild Animal Protection Law.
Jedlikowski, J., Brzezinski, M., Chibowski, P., 2015. Habitat variables affecting nest predation rates at small ponds: a case study of the Little Crake Porzana parva and Water Rail Rallus aquaticus. Bird Study 62, 190–201. Jobin, B., Picman, J., 1997. Factors affecting predation on artificial nests in marshes. J. Wildl. Manage. 61, 792–800. Lambrechts, M.M., Caro, S.P., Charmantier, A., Gross, N., Galan, M.J., Perret, P., CartanSon, M., Dias, P.C., Blondel, J., Thomas, D.W., 2004. Habitat quality as a predictor of spatial variation in blue tit reproductive performance: a multi-plot analysis in a heterogeneous landscape. Oecologia 141, 555–561. Lei, F.M., 2010. Oriental reed warbler Acrocephalus orientalis. In: Cheng, T.H., Lu, T.C., Yang, L., Lei, F.M., Xian, Y.H. (Eds.), Fauna Sinaca, Aves Vol 12, Passeriformes, Muscicapidae III. Science Press, Beijing, pp. 87–90. Li, D.L., Chen, S.H., Lloyd, H., Zhu, S.Y., Shan, K., Zhang, Z.W., 2013. The importance of artificial habitats to migratory waterbirds within a natural/artificial wetland mosaic, Yellow River Delta, China. Bird Conserv. Int. 23, 184–198. Li, D.L., Sun, X.H., Lloyd, H., Que, P.J., Liu, Y., Wan, D.M., Zhang, Z.W., 2015. Reed parrotbill nest predation by tidal mudflat crabs: evidence for an ecological trap? Ecosphere 6, 20. Ma, Z.J., 2017. The importance of habitat conservation for species conservation. Bull. Biol. 52 (11), 6–8. Ma, Z.J., Cai, Y.T., Chen, J.K., Li, B., 2010. Managing wetland habitats for waterbirds: an international perspective. Wetlands 30, 15–27. Ma, Z.J., Gan, X.J., Cai, Y.T., Chen, J.K., Li, B., 2011. Effects of exotic Spartina alterniflora on the habitat patch associations of breeding saltmarsh birds at Chongming Dongtan in the Yangtze River estuary, China. Biol. Invas. 13, 1673–1686. Manci, K.M., Rusch, D.H., 1988. Indices to distribution and abundance of some inconspicuous waterbirds at Horicon marsh. J. Field Ornithol. 59, 67–75. Melvin, S.L., Webb Jr., J.W., 1998. Differences in the avian communities of natural and created Spartina alterniflora salt marshes. Wetlands 18, 59–69. Menezes, J.C.T., Marini, M.A., 2017. Predators of bird nests in the Neotropics: a review. J. Field Ornithol. 88, 99–114. Moskát, C., Honza, M., 2000. Effect of nest and nest site characteristics on the risk of cuckoo Cuculus canorus parasitism in the great reed warbler Acrocephalus arundinaceus. Ecography 23, 335–341. Picman, J., Milks, M.L., Leptich, M., 1993. Patterns of predation on passerine nests in marshes: effects of water depth and distance from edge. Auk 110, 89–94. Poulin, B., Lefebvre, G., Mauchamp, A., 2002. Habitat requirements of passerines and reedbed management in southern France. Biol. Conserv. 107, 315–325. Ramsar Convention Secretariat, 2010. Wetland inventory: a Ramsar framework for wetland inventory and ecological character description. Ramsar Handbooks for the Wise Use of Wetlands, 4th ed. Ramsar Convention Secretariat, Gland, Switzerland. Riddington, R., Gosler, A.G., 1995. Differences in reproductive success and parental qualities between habitats in the great tit Parus major. Ibis 137, 371–378. Takekawa, J.Y., Woo, I., Spautz, H., Nur, N., Grenier, J.L., Malamud-Roam, K., Nordby, J.C., Cohen, A.N., Malamud-Roam, F., De La Cruz, S.E.W., 2006. Environmental threats to tidal-marsh vertebrates of the San Francisco Bay estuary. In: Greenberg, R., Maldonado, J.E., Droege, S., McDonald, M.V. (Eds.), Terrestrial Vertebrates of Tidal Marshes: Ecology, Evolution and Conservation, pp. 176–197 Studies in Avian Biology. Tanneberger, F., Tegetmeyer, C., Dylawerski, M., Flade, M., Joosten, H., 2009. Commercially cut reed as a new and sustainable habitat for the globally threatened Aquatic Warbler. Biodivers. Conserv. 18, 1475–1489. Wang, J.Y., 2015. Comparison on the Community and Breeding Ecology of Saltmarsh Birds in Natural and Managed Marshes at Chongming Dongtan. Master Dissertation at Fudan University, Shanghai. Wilson, M.D., Watts, B.D., Brinker, D.F., 2007. Status review of Chesapeake Bay marsh lands and breeding marsh birds. Waterbirds 30, 122–137. Xiong, L.H., Zhao, X., 2016. Plant-climbing behavior of a mudflat crab Chiromantes neglectum at reed-dominated tidal marsh in Changjiang River Estuary. Chin. J. Zool. 51, 423–433. Yang, C.C., Møller, A.P., Ma, Z.J., Li, F., Liang, W., 2014. Intensive nest predation by crabs produces source–sink dynamics in hosts and parasites. J. Ornithol. 159, 219–223.
Authors’ contributions ZJM and JYW conceived the ideas and designed methodology; JYW, QYZ, and WW collected the data; JYW and ZJM analysed the data; JYW and ZJM led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecoleng.2019.105584. References Batáry, P., Winkler, H., Báldi, A., 2004. Experiments with artificial nests on predation in reed habitats? J. Ornithol. 145, 59–63. Bradbury, R.B., Kyrkos, A., Morris, A.J., Clark, S.C., Perkins, A.J., Wilson, J.D., 2000. Habitat associations and breeding success of yellowhammers on lowland farmland. J. Appl. Ecol. 37, 789–805. Burhans, D.E., 1997. Habitat and microhabitat features associated with cowbird parasitism in two forest edge cowbird hosts. Condor 99, 866–872. Correll, M.D., Wiest, W.A., Hodgman, T.P., Shriver, W.G., Elphick, C.S., McGill, B.J., O'Brien, K.M., Olsen, B.J., 2016. Predictors of specialist avifaunal decline in coastal marshes. Conserv. Biol. 31, 172–182. Desrochers, D.W., Keagy, J.C., Cristol, D.A., 2008. Created versus natural wetlands: avian communities in Virginia salt marshes. Ecoscience 15, 36–42. Dyrcz, A., Nagata, H., 2002. Breeding ecology of the Eastern Great Reed Warbler Acrocephalus arundinaceus orientalis at Lake Kasumigaura, central Japan. Bird Study 49, 166–171. Dyrcz, A., de Juana, E., 2018. Oriental Reed-warbler (Acrocephalus orientalis). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A., de Juana, E. (Eds.), Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona https://www.hbw.com/node/ 58805. Forsman, J.T., Hjernquist, M.B., Taipale, J., Gustafsson, L., 2008. Competitor density cues for habitat quality facilitating habitat selection and investment decisions. Behav. Ecol. 19, 539–545. Gan, X.J., Cai, Y.T., Choi, C.Y., Ma, Z.J., Chen, J.K., Li, B., 2009. Potential impacts of invasive Spartina alterniflora on spring bird communities at Chongming Dongtan, a Chinese wetland of international importance. Estuar. Coast. Shelf Sci. 83, 211–218. Gedan, K.B., Silliman, B.R., Bertness, M.D., 2009. Centuries of human-driven change in salt marsh ecosystems. Ann. Rev. Mar. Sci. 1, 117–141. Greenberg, R., 2006. Tidal marshes: Home for the few and the highly selected. In: Greenberg, R., Maldonado, J.E., Droege, S., McDonald, M.V. (Eds.), Terrestrial Vertebrates of Tidal Marshes: Ecology, Evolution and Conservation, pp. 2–9 Studies in Avian Biology. Graveland, J., 1998. Reed die-back, water level management and the decline of the great reed warbler Acrocephalus arundinaceus in the Netherlands. Ardea 86, 187–201. Hoyt, D.F., 1979. Practical methods of estimating volume and fresh egg weight of bird eggs. Auk 96, 73–77. Ibáñez-Álamo, J.D., Magrath, R.D., Oteyza, J.C., Chalfoun, A.D., Haff, T.M., Schmidt, K.A., Thomson, R.L., Martin, T.E., 2015. Nest predation research: recent findings and future perspectives. J. Ornithol. 156 (S1), 247–262. Ibáñez-Álamo, J.D., Soler, M., 2010. Investigator activities reduce nest predation in Blackbirds Turdus merula. J. Avian Biol. 48, 208–212.
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Managed marshes can be good alternatives to natural marshes as breeding habitats for birds Junyan Wanga, Qianyan Zhoua, Wei Wub, Wei Liangc, Qiang Mab, Zhijun Maa,
T
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a Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Coastal Ecosystems Research Station of the Yangtze River Estuary, and Shanghai Institute of Eco-Chongming (SIEC), Fudan University, Shanghai 200433, China b Management Office of Chongming Dongtan Nature Reserve, Chongming 202183, China c Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou 571158, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Acrocephalus orientalis Artificial wetlands Breeding success rate Marsh birds Nest predation Oriental reed warbler Wetland management
Loss of natural tidal marshes has caused rapid population declines for many bird species, raising the question about whether managed marshes can be used for bird conservation. Although many studies have indicated that managed marshes can provide a complementary habitat for birds, it is unclear how the breeding habitats provided by managed marshes compare with those provided by natural marshes. We compared habitat conditions (vegetation and food) and breeding performance of a common reed specialist, the Oriental reed warbler (Acrocephalus orientalis), in natural and managed artificial reed marshes (about 2 km × 5 km) at Chongming Dongtan, an estuarine wetland in China. We found that vegetation was denser and warbler food resources were greater in managed than in natural marshes. The density of breeding territories, nest density, clutch size, egg size, and fledgling number per nest were greater in managed than in natural marshes. Breeding failure was reduced in managed marshes because of a reduced risk of nest predation. However, the high nest position on the reeds in the managed marshes increased the risk of nest destruction by strong wind. The better breeding performance in managed than in natural marshes could be attributed to the following factors: the high and stable water level in the managed marshes increased reed growth and arthropod reproduction and decreased access by terrestrial predators; dense vegetation helped conceal nests from predators; and human activities in the managed marshes deterred nest predators. The results suggest that managed marshes can provide quality breeding habitat for the Oriental reed warbler and probably for other marsh birds and can therefore help compensate for the loss of natural marshes. The preference of the Oriental reed warbler for managed marshes largely depends on the suitable habitat conditions. The current study highlights the importance of maintaining a relatively high and stable water level.
1. Introduction Tidal marshes along the coasts provide important habitats for birds (Greenberg, 2006; Gedan et al., 2009). Yet tidal marshes have been seriously damaged over the past several decades by anthropogenic activities, such as reclamation and exploitation, and by sea level rise. As a consequence, many species of marsh birds have suffered dramatic population declines due to habitat loss (Takekawa et al., 2006; Wilson et al., 2007; Correll et al., 2016). On the other hand, the coastal area represented by artificial or managed marshes has increased worldwide (Ramsar Convention Secretariat, 2010). An important question is whether managed marshes are good alternatives to natural marshes. Many studies have compared bird communities in natural vs. managed marshes. The results have indicated that although managed
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marshes cannot replace all of the ecological functions of natural marshes, they can provide a complementary habitat for many birds and thus mitigate the negative effects of natural marsh loss (e.g., Melvin and Webb, 1998; Desrochers et al., 2008; Li et al. 2013). In comparing managed and natural marshes as habitats for birds, breeding habitat is particularly important for several reasons. First, the breeding period is critical in the annual cycle of birds, and reproductive output will obviously affect population maintenance (Bradbury et al., 2000). Second, birds have strict habitat requirements for breeding (Wilson et al., 2007). Documenting and comparing the demographic benefits of managed and natural marshes would provide critical information needed for bird conservation. It is unclear, however, how the breeding habitats provided by managed marshes compare with those provided by natural marshes.
Corresponding author. E-mail address: [email protected] (Z. Ma).
https://doi.org/10.1016/j.ecoleng.2019.105584 Received 7 December 2018; Received in revised form 12 August 2019; Accepted 24 August 2019 Available online 30 August 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.
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provide high and stable water levels that are suitable for the growth of reeds (Tanneberger et al., 2009), we hypothesized that reeds in managed marshes are higher and denser and contain more arthropod food resources for the warblers than reeds in natural marshes. Second, because marsh birds prefer nest sites with dense vegetation and abundant food (Batáry et al., 2004), we hypothesized that the warblers establish breeding territory earlier, and that nest density is higher in the managed than in the natural marshes. Our third hypothesis was that there is no significant difference in breeding performance of birds, in terms of clutch sizes, egg sizes, and body condition of fledglings, between managed and natural marshes. Finally, we hypothesized that the stable water level, dense vegetation, and frequent human activities in the managed marshes reduce nest predation (Ibáñez-Álamo et al., 2015) and thereby increase the breeding success rate.
Different environmental conditions between natural and managed marshes affect habitat use and breeding performance of marsh birds. Natural marshes along the coasts are strongly influenced by tidal rhythms, and these hydrological conditions greatly affect plant communities (Greenberg, 2006). In addition, natural marshes are often inconvenient for human activities, and thus are seldom directly affected by human disturbance (Greenberg, 2006; Gedan et al., 2009). Unlike natural marshes, managed marshes are generally enclosed by dams and are not affected by tidal rhythms. Hydrological conditions in managed marshes are controlled by managers, are relatively stable, and affect the plant communities that develop (Ma et al., 2010). In addition to being managed, managed marshes differ from natural marshes in that they often support some commercial production and tourism (Desrochers et al., 2008; Li et al., 2013). Vegetation characteristics and food resources are the key factors affecting habitat use of birds in breeding season. Marsh birds prefer to nest in densely vegetated areas, perhaps because such areas increase nest concealment (Batáry et al., 2004; Jedlikowski et al., 2015). In addition, dense vegetation usually contains high numbers of invertebrates, which are the main food for breeding marsh birds, and therefore supports high nest densities. Because both vegetation characteristics and invertebrate diversity are affected by hydrologic conditions (Manci and Rusch, 1988), the differences in vegetation characteristics and food resources between natural and managed marshes may strongly affect the habitat use and breeding performance of birds. Nest predation is an important cause of breeding failure in birds (Ibáñez-Álamo et al., 2015; Menezes and Marini, 2017). Nest predators in marshes include both terrestrial and aerial predators (Picman et al., 1993; Takekawa et al., 2006; Ibáñez-Álamo and Soler, 2010). Foraging by terrestrial predators is generally reduced by deep water (Picman et al., 1993; Jobin and Picman, 1997), and the detectability of nests is reduced by dense vegetation (Jobin and Picman, 1997). In addition, some nest predators are deterred by human activity (Dyrcz and Nagata, 2002; Ibáñez-Álamo and Soler, 2010). As a consequence, differences in hydrologic conditions, vegetation, and human activity could affect nest predation and finally the breeding success of marsh birds in managed and natural marshes. Given the widespread declines in marsh birds due to loss of natural habitats (Takekawa et al., 2006; Wilson et al., 2007; Correll et al., 2016), it is critical to understand how well managed marshes function as habitats for birds. A recent wetland restoration project at the Chongming Dongtan Ramsar site (CMDT, 121.9°E, 31.6°N) in the Yangtze Estuary, China, provides an opportunity for comparing natural and managed marshes as habitats for breeding birds. The large area of reed (Phragmites australis) marshes on the natural tideland wetlands at CMDT supports diverse marsh-breeding birds (Ma et al., 2011). To eradicate the alien invasive smooth cordgrass (Spartina alterniflora) that rapidly spread on the tideland, an ecological engineering project was implemented in 2010. The seawall constructed as part of this project enclosed tidal marshes dominated by smooth cordgrass. The aboveground parts of the smooth cordgrass were cut off during the growing season, and the underground parts were killed by flooding for > 2 months. Native reeds were subsequently planted, resulting in the creation of an managed marsh that provided resting, foraging, and breeding habitats for birds (Ma, 2017). The oriental reed warbler (Acrocephalus orientalis) is a common reed specialist in Eastern Asia. It constructs nests on reed stems and greatly depends on reed habitat in breeding season (Lei, 2010; Dyrcz and de Juana, 2018). The abundance of the Oriental reed warbler has declined because of the dramatic loss of natural marshes (Lei, 2010). Earlier studies indicated that Oriental reed warblers breed in both natural and managed reed marshes at CMDT (Wang, 2015), suggesting that managed marshes might mitigate the loss of natural marshes. Here, we compared habitat conditions and breeding performance of the Oriental reed warbler in the natural and managed marshes at CMDT. We tested four hypothesis. First, because managed marshes
2. Methods 2.1. Study sites The natural marsh at CMDT experiences regular inundation by tidewater. The tide is regular and semidiurnal, with two high and two low tides every day. All of the tidal flats are submerged by tidewater during the high tide of the spring tide and are exposed during the neap tide and the low tide of spring tide (Ma et al., 2011). The marsh vegetation is mainly composed of reeds in the high tide zone and bulrush (Scirpus spp.) in the middle tide zone. The height of the reeds submerged by the tidewater is generally < 50 cm. Birds can nest on the reeds but not on the bulrush, which is short (< 50 cm) and is completely submerged by tidewater during high tide. Thus, the reedbed is the main breeding habitat for marsh birds (Gan et al., 2009; Ma et al., 2011). During breeding season, human activity is rare in the natural marsh. The area with managed marshes is adjacent to the area with natural marshes at CMDT. They are enclosed by a seawall and thus are not affected by tides. Embankments divide the whole area into three different zones, each of which is ~1 to 2 km2 (Fig. S1). The area of reed and open water roughly accounts for half of the total area in each zone. The water level is generally lowered in early spring to promote reed germination. Following reed germination, the water level is raised and maintained at a certain depth to favor reed growth. In 2013, the water depth was ~30 cm during the breeding period of birds. In 2014, due to frequent rainfall, the water depth was ~60 cm during the breeding season. The managed marshes have boardwalks and public education infrastructure and are frequently visited by humans. Moreover, the administrative staff patrols the seawall and embankment every day. Both the natural and managed reed marshes support diverse birds. Over 20 species of marsh-breeding birds have been recorded at each of the two habitats (Gan et al., 2009; Ma et al., 2011; Wang, 2015). The Oriental reed warbler is the dominant bird species in both kinds of marshes. Individuals of this species arrive at CMDT from their nonbreeding grounds in late April and build nests exclusively in the reedbed (Ma et al., 2011). The reeds form a monoculture in both the natural and managed marshes. Because reeds were not harvested in the study region in year before the study, both old and new stems were present and intermixed in the reedbeds during the current study. 2.2. Vegetation surveys We conducted surveys using the same methods in the two breeding seasons of 2013 and 2014. To avoid edge effects, all surveyed sites were located > 10 m from the edge of vegetation. We randomly selected sampling sites (~10 ha per site) with continuous and uncut reeds vegetation in the managed marshes (one site in each zone) and also in the adjacent natural marshes (three in managed marshes and three in natural marshes, Fig. S1). At each site, five 0.5 m × 0.5 m plots were designated. In late April, when the Oriental reed warblers begin to 2
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survey day. The sequence used to survey plots was randomized each day to avoid a potential effect of survey time on the results.
establish their breeding territories, we measured reed stem number, stem height (for stems higher than 0.5 m), and stem diameter (at 1.0 m height, for the highest 10 stems). The reed vegetation was composed of dry stems that grew in the previous year and growing stems that newly spouted that year. We measured the growing and dry stems separately. Because reeds grow rapidly in late April, the vegetation surveys in managed and natural marshes were conducted on the same day in each year.
2.6. Nest surveys Nests were surveyed in early June when birds have finished nest construction. We used the same plots used for the territory surveys. Two or three investigators walked together, with 3 m between them, and searched for nests from one side to another side of each plot. The investigators walked along different routes to cover the entire plot. When a nest was found, it was numbered and its location was recorded using a hand-held Global Position System (GPS). The height of the nest from the ground was measured. The breeding period was determined based on the condition of nests, eggs, or nestlings (Lei, 2010; Wang 2015). After finding and recording a nest, the investigator bound together the reed stalks located ~2 m away from the nest to facilitate the finding of the nest in subsequent surveys.
2.3. Surveys for bird food resources We collected arthropods, the food for the Oriental reed warblers (Lei, 2010; Dyrcz and de Juana, 2018), using sweeping nets (35 cm diameter) in the same sites used for vegetation surveys (three sites per marsh type). We randomly selected five plots in each sample. Arthropods were collected by sweeping vegetation 50 times with an insect net in a radius of 1 m in each of five randomly selected plots (10 m2/ plot) per site. While sweeping the net, we hit the reed stems with the net frame to frighten the arthropods attached to the leaves or stems in order to enhance their collection. The captured arthropods were kept in plastic bottles containing 75% alcohol. Because arthropod activity is affected by time of day and weather, arthropods were collected around noon on clear days. Arthropod surveys were conducted twice each year: in early May, when birds establish their breeding territories (early breeding period), and in late June, after fledging (late breeding period). Arthropods were identified to order and counted.
2.7. Breeding monitoring An automatic time-lapse camera (DPS 63070, Primos, Flora, MS, USA) was placed on a tripod ~1 m from each nest to record nest activities. The camera photographed the nest every 5 s. The nests and the cameras were checked every 4–5 days until fledging occurred or breeding failed. Oriental reed warblers lay one egg every day (~3 to 6 eggs in total), and the incubation period is ~2 weeks (Lei, 2010; Dyrcz and de Juana, 2018). We estimated the date of egg laying (as the date when the first egg was laid) for each nest according to the camera records, number of eggs in the nests and the incubation period date. When eggs began to hatch, clutch size was recorded. We also measured the length (L) and breadth (B, maximum diameter) of each egg with a Vernier caliper (to the nearest 0.1 mm) in 2014. The nestling period is ~12 days (Lei, 2010; Wang, 2015). Because body mass and size are stable when nestlings are close to fledging, body mass and tarsus length of the nestlings were measured on the 10th or 11th day after hatching as indicators of fledgling body condition. Disturbance to the nests and nestlings was minimized during the surveys. We determined the causes of breeding failure based on the photographs taken by the cameras, the status of the nestlings, and the presence of predator traces, eggshell fragments, and nestling corpses. If a nestling disappeared from the nest after 9 days had passed since incubation and if the photographs did not indicate nestling mortality, we assumed that the nestling had fledged. Breeding was considered successful if a nest produced one or more fledglings.
2.4. Crab surveys Recent studies indicated that the mudflat crab Chiromantes neglectum is a nest predator of marsh-breeding birds. Crabs can climb up the reed stems and enter the nests to prey on eggs or nestlings (Yang et al., 2014; Li et al., 2015). We surveyed the mudflat crabs in natural and managed marshes at the peak breeding period in early June. The mudflat crabs generally remain on the ground during the day time. At dusk, they may climb on reed stems and enter the nests of birds (Xiong and Zhao, 2016). We designated five 10-m-long transects for crab surveys at each of the sites used for vegetation surveys. At 1 hr before sunset, investigators walked along the transects and recorded the number of crabs climbing on the reeds within 1 m of each side of the transect. To avoid an effect of human disturbance on crab activity, no other surveys was conducted on the day of crab surveys. Although this method certainly underestimated the total crab density in the area, we used the same method in both habitats, and only those crabs climbing on the reeds could be potential nest predators; this method therefore reasonably assessed the threat of crab predation in the two habitats.
2.8. Data analysis Linear mixed models (LMM) were used to detect the effects of habitat type (managed vs. natural marshes), year (2013 vs. 2014), and their interaction on the characteristics of habitats (height, diameter, and density of reeds), food for birds (density of total arthropods and the dipterans, the major food for the Oriental reed warbler, Lei, 2010; Wang, 2015), and the relative number of mudflat crabs. LMMs were also used to compare the density of bird territories between the two habitats. Habitat type, date of bird surveys, year, interactions of habitat type with year, and survey date were included in the model as fixed effects. Site serial number and plot serial number were included in LMMs as nested random factors. LMMs with site serial number and plot serial number as nested random factors were used to determine the effects of habitat type, year, and their interactions on the date on which the first egg was laid in a nest, clutch size, egg size (average of eggs in each nest), and fledgling number. Egg size in terms of egg volume (V) was estimated as V = 0.51 × L × B2 (Hoyt, 1979). Clutch size was included in the model when egg size between the two habitats was compared. LMMs were also used to detect the effects of habitat type, year, measurement date (days
2.5. Breeding territory surveys The Oriental reed warbler is generally monogamous. The males exhibit obvious territoriality involving frequent and loud singing from the upper parts of reed stems during the early breeding season (Lei, 2010, Wang, 2015). We estimated the numbers of territories by assessing the numbers of singing birds. Bird were surveyed at the same sites (three per marsh type) used for vegetation surveys. At each site, one plot with an area of 100 m × 50 m was designated. Two investigators, who were located at an elevated position ~10 m away from the plot, used 8× binoculars to determine the number of singing birds. The two investigator were ~30 to 50 m apart and therefore observed the plots from different angles. Four or five observation locations were used per plot per day, with one 3 min observation period per observation location. Territory surveys were conducted once every 2–3 days during days without rain beginning in mid-April, when birds arrived at CMDT. Territory surveys lasted 3–4 weeks until the singing decreased and birds began constructing nests. The surveys began after sunrise, ~4 h on each 3
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2013 and 2014, respectively, n = 3 for both) than in managed marshes (1.93 ± 0.31 and 0.60 ± 0.53 crabs per transect in 2013 and 2014, respectively, n = 3 for both) (F1, 48 = 68.95, P < 0.001). Moreover, crab density was significantly lower in 2014 than in 2013 (F1, 48 = 16.62, P < 0.001), and the decline between years was significantly greater in the managed than in the natural marshes (interaction between habitat type and year: F1, 48 = 11.08, P = 0.002).
after hatching), and nestling numbers in a brood on the body mass and tarsus length of birds. Two-way interactions were included in the models. Generalized linear mixed models (GLMM, with a binomial distribution and logit link function) were used to detect the effects of habitat type, year, and their interaction on the breeding success of birds and on the occurrence of nest predation. Chi-square tests were used to compare the breeding success rate and the occurrence of nest predation between the two habitats in the same year. A GLMM was also used to detect the relationship between the occurrence of nest overturn and nest height, with habitat type, year, and their interactions as fixed variables and with site serial number and plot serial number as nested random variables. All statistical analyses were performed using PASW Statistics 18.0.0 (SPSS Inc., Chicago, IL, USA). Results are presented as means ± SE.
3.4. Territory density, nest density, and nest height Territorial density increased in both habitats during the study period (F1, 8 = 306.08, P < 0.001), but was significantly higher in the managed than in the natural marshes (F1, 8 = 21.64, P < 0.001). Moreover, territorial density increased more rapidly in managed than in natural marshes (interaction of habitat type and date: F1, 8 = 30.52, P < 0.001). Similar trends were detected in the two years (F1, 8 = 0.1, P = 0.90) (Fig. 3). A total of 161 (89 in 2013 and 72 in 2014) nests were recorded in managed marshes and 92 (46 in 2013 and 46 in 2014) nests in natural marshes. Nest density was significantly greater in managed marshes (29.7 ± 4.7 and 24.3 ± 5.5 nests per ha in 2013 and 2014, respectively, n = 3 for both) than in natural marshes (15.3 ± 4.1 and 15.3 ± 3.2 nests per ha in 2013 and 2014, respectively, n = 3 for both) (F1, 8 = 33.0, P < 0.001). Nest density did not significantly differ between the two years (F1, 8 = 1.09, P = 0.33). Nests were significantly higher in managed marshes (143.7 ± 4.0 cm in 2013 and 159.0 ± 3.9 cm in 2014, n = 3 for both) than in natural marshes (120.9 ± 4.9 cm in 2013 and 119.9 ± 3.1 cm in 2014, n = 3 for both) (F1, 112 = 150.8, P < 0.001). Moreover, the nest height in managed marshes was significantly higher in 2014 than in 2013 (F1, 112 = 52.3, P = 0.01), but nest height in natural marshes did not significantly differ between the two years (F1, 112 = 0.07, P = 0.81).
3. Results 3.1. Characteristics of reed vegetation The reed vegetation significantly differed between the natural and managed marshes (Table 1). For both growing and dry reeds, stems were higher and thicker in the managed marshes than in the natural marshes. Reed density did not significantly differ between the two habitats. Although reed characteristics differed in 2013 vs. 2014, the overall trends between the two habitats were consistent in both years (Fig. 1, Table 1). 3.2. Food for birds Arthropod density significantly differed between the two habitats (F1, 48 = 40.17, P = 0.003) and between the early and late breeding periods (F1, 48 = 29.64, P < 0.001) (Fig. 2A). In the early breeding period, arthropods were more abundant in managed than in natural marshes. In the late breeding period, arthropod abundance significantly decreased in managed marshes but did not in natural marshes (interaction between habitat type and period: F1, 48 = 44.47, P < 0.001). The arthropod density was similar in 2013 and 2014 (F1, 48 = 0.65, P = 0.42) (Fig. 2A). The density of dipterans, which accounted for 76.2% and 56.6% of the arthropod abundance in managed and natural marshes respectively, exhibited the same trends as the total arthropod density (Fig. 2B).
3.5. Egg laying date, clutch size, and egg size Eggs were laid significantly earlier in the managed marshes than in the natural marshes (F1, 103 = 10.28, P = 0.03) (Fig. 4a). The date on which eggs were laid did not significantly differ between the two years (F1, 103 = 1.50, P = 0.22) (Fig. 4a). The clutch size of the Oriental reed warblers ranges from 3 to 6 eggs. The clutch size was significantly higher in managed marshes than in natural marshes (F1, 130 = 11.46, P = 0.02). Clutch size did not significantly differ between 2013 and 2014 (F1, 130 = 1.80, P = 0.18, Fig. 4b). As clutch size increased, egg size decreased (F1, 42 = 26.52, P < 0.001). For a given clutch size, egg size was significantly greater in the managed marshes than in the natural marshes (F1, 42 = 5.02, P = 0.04) (Fig. 4c).
3.3. Density of mudflat crabs The relative density of mudflat crabs was significantly greater in natural marshes (22.67 ± 5.32 and 9.47 ± 1.14 crabs per transect in
3.6. Number and body condition of fledglings
Table 1 The effects of marsh type (natural vs. managed marsh), year (2013 vs. 2014), and their interaction on the height, diameter, and density of growing reeds and dry reeds. Linear mixed models (LMM) with site serial number and plot serial number as nested random variables were used for data analysis. Independent variable
Height F1,
48
Diameter
Density
P
F1,
P
F1,
48
48
Fledglings were significantly more abundant in managed than in natural marshes (F1, 69 = 6.67, P = 0.04), and fledgling numbers did not significantly differ between the two years (F1, 69 = 0.83, P = 0.37) (Fig. 4d). Neither fledgling body mass (F1, 63 = 0.23, P = 0.64, Fig. 4e) nor tarsus length (F1, 60 = 0.60, P = 0.44, Fig. 4f) significantly differed between the two habitats. As clutch size increased, fledgling body mass (F1, 63 = 38.8, P < 0.001) and tarsus length (F1, 60 = 4.84, P = 0.03) decreased. Fledgling body mass and tarsus length did not significantly differ between the two years (F1, 63 = 1.66, P = 0.20 for body mass; F1, 63 = 1.37, P = 0.25 for tarsus) or among measurement dates (F1, 63 = 0.07, P = 0.79 for body mass; F1, 60 = 0.39, P = 0.68 for tarsus).
P
Growing reeds Marsh type Year Marsh type × Year
46.38 132.72 1.495
0.002 < 0.001 0.23
11.60 20.18 2.59
0.03 < 0.001 0.11
1.70 1.91 6.05
0.26 0.17 0.02
Dry reeds Marsh type Year Marsh type × Year
19.94 3.75 0.34
0.01 0.06 0.56
35.91 16.52 8.19
0.004 < 0.001 0.006
3.82 82.99 2.63
0.12 < 0.001 0.11
3.7. Breeding failure and causes Among all 150 nests surveyed in both habitats and both years, the
Bold values indicate P < 0.05. 4
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Fig. 1. Plant height (A, B), diameter at breast height (C, D), and density (E, F) of growing reeds (A, C, E) and dry reeds (B, D, F) in managed marshes (white bars) and natural marshes (dark grey bars). Values are means ± SE (n = 3).
breeding failure rate was 56.0%, and more than half of the breeding failures (52.4%) were caused by nest predation (Fig. 5). The Siberian weasel (Mustela sibirica) and the Lesser coucal (Centropus bengalensis) were the main nest predators and were responsible for 38.6% and 29.5%, respectively, of the nest predation caused by known predators (Fig. S2). Breeding failure also resulted from the overturning of nests by strong wind (22.6%), nest abandonment by parents (19.0%), and nest parasitism by cuckoos (Cuculus spp., 6.0%) (Fig. 5). Mudflat crabs were more frequently recorded in the nests of birds in natural marshes (24.6% in 2013 and 22.0% in 2014) than in managed marshes (2.4% in 2013 and 2.0% in 2014) (χ2 = 9.60, P = 0.004 in 2013; χ2 = 14.48, P = 0.002 in 2014). Photographs indicated, however, that the presence of crabs in nests usually occurred after the nests had been preyed upon by other predators or had been abandoned by parents (as indicated by the absence of incubation activity for at least 1 day). There was only one record of nest predation by crabs shortly after the parents left the nest in natural marshes. In 25.0% of the cases of nest predation, the predators were unknown because the predation apparently occurred at night, when the cameras did not function (Fig. S2). The breeding success rate was significantly higher in managed marshes (50.0%, n = 42 in 2013 and 61.5%, n = 39 in 2014) than in natural marshes (25.8%, n = 31 in 2013 and 37.5%, n = 38 in 2014) (Wald chi-square = 8.82, P = 0.003) (Fig. 5). This was mainly due to the lower nest predation rate in managed marshes (25.0% in 2013 and 2.6% in 2014) than in natural marshes (41.9% in 2013 and 45.8% in 2014) (Wald chi-square = 11.01, P = 0.001) (Fig. 5). The nest predation rate in managed marshes was significantly lower in 2014 than in 2013 (χ2 = 7.99, P = 0.05), while the nest predation rate in natural marshes did not significantly differ between the two years (χ2 = 0.12,
Fig. 2. Density (number of individuals per m2) of Arthropods (A) and dipterans (B), the major food of the Oriental reed warbler, in the early and late breeding periods in managed marshes (white bars) and natural marshes (dark grey bars). Values are means + SE (n = 3). 5
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Fig. 5. Breeding success and failure rates, and causes of breeding failure for the Oriental reed warblers in managed and natural marshes in 2013 and 2014. The number above each column indicates the number of nests examined.
4. Discussion This study indicated that managed marshes provide better breeding habitat for the Oriental reed warbler than the natural marshes at CMDT. The birds established breeding territories in greater numbers in the managed than in natural marshes. In managed marshes relative to natural marshes, nest density was higher (241% higher in 2013 and 197% in 2014), clutch size was greater (123% greater in 2013 and 110% in 2014), breeding success rate was higher (194% higher in 2013 and 164% in 2014), and fledgling number per nest was higher (113% higher in both 2013 and 2014). As a consequence, the number of offspring produced per unit area was 5.3 times greater in 2013 and 3.6 times greater in 2014 in the managed marshes than in the natural marshes. This suggests that the managed marshes are critical for maintenance of the Oriental reed warbler populations. With managed hydrological conditions, managed marshes provided more suitable conditions for reed growth than natural marshes, which was consistent with our first hypothesis. Although reed density was similar in the two habitats, reeds were higher and stems were thicker in the managed than in the natural marshes, suggesting that the vegetation was denser in the managed marshes. The managed marshes
Fig. 3. Territorial density of Oriental reed warblers in managed marshes (dashed line) and natural marshes (solid line) in 2013 and 2014. Values are means ± SE (n = 3).
P = 0.34). The nests in managed marshes were more likely to be overturned than those in natural marshes (overturning caused 41.9% of the breeding failures in managed marshes and 11.3% in natural marshes, χ2 = 10.47, P = 0.005) (Fig. 5). Higher nests were more susceptible to being overturned than lower nests (heights of overturned and not overturned nests were 160.0 ± 16.1 and 134.3 ± 21.3 cm, respectively, Wald chi-square = 15.8, P < 0.001).
Fig. 4. Date of egg laying (A, the date on which first egg were laid in a nest), clutch size (B), egg volume (C), fledgling number per nest (D), fledgling body mass (E), and fledgling tarsus length (F) of Oriental reed warblers in managed marshes (white bars) and natural marshes (dark gray bars). Values are means + SE (n = 3). The number above each column indicates the total number of nests examined in each habitat. 6
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unknown, nocturnal animals. The percentage of Oriental reed warbler nests that were overturned by wind increased with nest height. This could be explained by the increase in instability with increasing height on the reed stem. The high water level in managed marshes caused the birds to build their nests at relatively high positions on the reed stems, such that the nests were vulnerable to strong winds. This suggests that although a high water level helps protect nests from terrestrial predators, a too high water level could reduce breeding success due to the effects of wind. The percentage of nest parasitism was similar in the natural and managed marshes. The probability that a nest is parasitized generally increases with nest visibility (Burhans, 1997; Moskát and Honza, 2000). Although nest concealment is greater in managed marshes than in natural marshes, infrastructure (e.g., houses and poles) in managed marshes might provide perches and thereby increase the occurrence of nest parasites (Moskát and Honza, 2000).
supported a high density of arthropods in the early breeding season, perhaps because the dense vegetation and stable water level benefits the development and growth of arthropods (Poulin et al., 2002). The decreased density of total arthropod and the dipteran during each breeding season in the managed marshes may have resulted from intensive consumption by breeding birds, which require abundant food for themselves and their nestlings. With relatively fewer breeding birds in natural marshes (Wang, 2015), the food requirement is lower than in managed marshes. It is also possible that the periodic tides might increase arthropod immigration to the natural marshes. We found that the Oriental reed warbler established more breeding territories and had higher nest densities in managed than in natural marshes, suggesting that the birds prefer managed marshes as nesting sites. This finding, which was consistent with our second hypothesis, could be related to the dense vegetation and abundant food in the managed marshes. Moreover, many marsh birds prefer nesting at sites with a stable water level because a stable water levels reduces the ability of terrestrial predators to access the nests (Picman et al., 1993; Graveland, 1998). Although the territorial density was always higher in the managed than in the natural marshes, it increased in both habitats during the survey period. This suggests that when making settlement decisions, birds may use various cues, such as vegetation, food, and social information, to evaluate the tradeoff between habitat quality and intraspecific competition (Forsman et al., 2008). Inconsistent with our third hypothesis, eggs were laid earlier and clutch size was larger in the managed than in the natural marshes. This might be explained by a superior body condition of birds that nested in the managed marshes and/or by the high habitat quality of the managed marshes (Riddington and Gosler, 1995; Lambrechts et al., 2004). The greater number of fledglings per nest in the managed marshes can be related to the larger clutch size in the managed marshes. In addition, the abundant food would support more nestlings and fledglings in the managed marshes. Although fledgling body condition did not significantly differ between the two habitats, the higher nest density, clutch size, and breeding success in the managed marshes than in the natural marshes indicate that the carrying capacity for breeding Oriental reed warblers was greater in the managed marshes than in the natural marshes. Consistent with our fourth hypothesis, the breeding success rate was higher and the predation rate was lower in managed than in natural marshes. The lower predation in managed marshes the could result from the high and stable water level, the dense vegetation, and the increase in human activity, all of which would reduce the ability of predators to detect and access nests (Dyrcz and Nagata, 2002; Batáry et al., 2004; Ibáñez-Álamo and Soler, 2010; Jedlikowski et al., 2015). Although natural marshes are submerged by tidewater during the high tide of the spring tide, they are accessible to terrestrial mammals during the neap tide and the low tide of the spring tide when the tideland is exposed. The nest predation rate was significantly lower in 2014 than in 2013 in the managed marshes, perhaps because the water level was higher in 2014. The mudflat crab prefers habitats that are exposed during low tide and submerged during high tide (Xiong and Zhao, 2016). With a high and stable water level, managed marshes may be unsuitable for the mudflat crab. Thus, the density of mudflat crabs was much lower in managed marshes than in natural marshes. Although several recent studies found that the mudflat crab was a major nest predator of marsh birds (Yang et al., 2014; Li et al., 2015), we detected only one case of a nest being preyed upon by crabs. Mudflat crabs are sensitive to disturbance when climbing on the reeds (Xiong and Zhao, 2016), and are easily knocked to the ground by adult birds that stay in the nests (Wang JY, field observation). Although nest predation by crabs is not uncommon (Menezes and Marini, 2017), the mudflat crab may not be an important predator of Oriental reed warbler nests and may mainly consume eggs in abandoned nests. On the other hand, much of the nest predation in the current study occurred at night and was conducted by
4.1. Implications for conservation This study increases our understanding of the roles of managed wetlands in providing habitats for birds. Although we focused on the habitat use and breeding performance of the Oriental reed warbler, the stable water level, dense vegetation, and abundant food in the managed marshes can also provide high-quality habitats for other marshbreeding birds (e.g., Jobin and Picman, 1997; Graveland, 1998; Poulin et al., 2002). The managed and natural marshes at CMDT contain similar bird species, but bird abundances are greater in the managed marshes (Wang, 2015), suggesting that managed marshes can be a good alternative to natural ones for breeding birds. Given the rapid loss of natural marshes and the wide distribution of managed marshes worldwide, managed marshes play important function in mitigating the negative effects of loss of natural ones. The preference of the Oriental reed warbler for managed marshes largely depends on the suitable habitat conditions resulting from hydrology adjustment and the impacts of such management on the vegetation. Therefore, effective management is the key to improving the quality of managed habitats (Ma et al., 2010). While it is important to protect the remaining natural marshes, it is also important to increase and correctly manage managed marshes as habitats for breeding birds. The current study highlights the importance of maintaining a relatively high and stable water level. This study was conducted at Chongming Dongtan with limited sample size, we propose further studies at larger scale to clarify the role of managed marshes in supporting habitat for breeding birds. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements We thank K Tan, Y Chen, HB Peng, WJ Xue, XS Feng, XL Wang, C Zhang, and X Jin for field assistance, and the Chongming Dongtan Nature Reserve for facilitating the fieldwork. Funding statement This work was financially supported by the National Key Research and Development Program of China (2018YFC1406402), the National Natural Science Foundation of China (31272334), and the Science and Technology Department of Shanghai (18DZ1205002). Ethics statement All the studies were conducted with the permission of the local 7
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