Little is known about the ecology of the Grey-headed Fish-Eagle (GHFE) (Ichthyophaga ichthyaetus) despite it being a formerly widespread species throughout Indo-Malaya (Ferguson-Lees and Christie 2001) in apparent decline (Samant et al. 1995, Grimmett et al. 1998) with a conservation status of globally near-threatened (IUCN 2008). Several researchers have suggested that causes of population decline (BirdLife International 2001, Baral and Inskipp 2004) may include deforestation, pesticides, and anthropogenic disturbance, but few of these are based on anything more than anecdotal evidence. If the apparent population decline is to be addressed through effective conservation planning, however, then it is essential that conservation decisions are based on a thorough understanding of the species' ecological requirements. Some of the first quantitative data on the GHFE, gathered at Tonle Sap Lake in Cambodia, have been reported earlier by Tingay et al. (2006). Here, we extend those findings with more detailed results, which may contribute to more informed conservation decisions in this regionally important aquatic ecosystem, the largest freshwater lake in Southeast Asia (Campbell et al. 2006).

We previously documented (Tingay et al. 2006) a high-density breeding population of GHFEs in the seasonally inundated swamp forest at Prek Toal. This population appears to be regionally significant, considering the reported declines in neighboring Thailand, Malaysia, Myanmar, Laos, and Vietnam (Wells 1999, Robson 2000, Fuchs et al. 2007). The breeding cycle of GHFE at Prek Toal begins when the floodwater begins to rise in September and ends when the floodwaters are fully receded in March (Tingay et al. 2006, S. Visal unpubl. data). This population is at least partly dependent on water snakes as prey and may be threatened by the unsustainable mass-harvesting of water snakes by the local human population (Tingay et al. 2006), because an estimated 6.9 million snakes are removed annually from the lake for human and captive-crocodile consumption, as well as for the medicinal wildlife trade in Southeast Asia (Brooks et al. 2007). GHFE at Prek Toal may also be threatened by the upstream construction of hydropower dams in China, Laos, Thailand, and Cambodia, which have the potential to alter drastically the Tonle Sap Lake flood cycle (Kummu and Sarkkula 2008).

In this report, we present analysis of features of nest-site selection by GHFE at Prek Toal. First we examine whether GHFE preferentially place nests in the tallest trees with an open canopy structure, as this will minimize the risk of nest-flooding and allow unencumbered parental access: studies of other tropical fish-eagle species have documented selection of such traits (Berkelman et al. 2002, Hollamby et al. 2006). Next, we consider whether GHFE preferentially nest closer to permanent water, because this should allow access to a more prolonged aquatic food supply, given that floodwaters recede in the latter part of the breeding cycle. We also test whether a known component of the diet, water snakes, are more abundant in permanent water than in temporary water when floodwaters are receding (typically, during the nestling-rearing phase). Finally, we examine whether GHFE nest site distribution is influenced by proximity to human habitation.

Methods

Study Area

The Tonle Sap Lake (12°25′ to 13°25′N; 103°25′ to 104°40′E; Fig. 1) covers 2500 km² in the dry season (January to May), expanding to 12 000 km² during the wet season (June to October; Rundel 2000; Fig. 1). The Tonle Sap River connects the Tonle Sap Lake to the Mekong River, making the lake a highly productive wetland ecosystem (Campbell et al. 2006) that supports one of the largest freshwater fisheries in the world (Hortle et al. 2004). The dominant floodplain habitat is described as freshwater swamp forest and is characterized by the seasonality of the flooding, as opposed to the permanent flooding of the classic swamp forest of Southeast Asia (Rundel 2000). This unique ecosystem forms a large vegetation belt 7–40 km wide surrounding the open water surface and is estimated to cover approximately 3600 km² (Rundel 2000). It is adapted to withstand seasonal water-level variation of up to 10 m and is of relatively simple floristic composition, comprising three main vegetation types: short-tree scrublands, gallery forest, and aquatic herbaceous vegetation. The short-tree scrublands cover approximately 80% of the floodplain and consist of dense, fairly homogenous stands of short trees and scrub 2–4 m in height. Typical species include Vitex holadenon, Acacia spiralis, and Corbretum trifoliatum. The gallery forest covers approximately 10% of the floodplain and is primarily found close to the shoreline and rivers, consisting of 7–15-m-tall trees dominated by Barringtonia acutangula and Diospyros cambodiana (Campbell et al. 2006). The Tonle Sap Lake contains three designated core protected areas: Prek Toal (21 342 ha), Boeng Chhma (14 560ha) and Stung Sen (6355 ha). The Prek Toal Core Area (13°07′N, 103°39′E), where our study was based, is situated at the northwestern end of Tonle Sap and is considered one of the most intact areas of freshwater swamp forest around the lake (Chan et al. 2004).

Figure 1

Location of the three Core Areas on Tonle Sap Lake, Cambodia, and the extent of the floodwater.

Surveys

We conducted our study over three years: 3–13 December 2005; 30 November–7 December 2006; 1 October–31 December 2007 (Fig. 2). We defined an occupied GHFE site according to previously described criteria (Rabarisoa et al. 1997), which included any sign of use such as the presence of green leaf nest-lining material, eggs or nestlings, or incubating or brooding adults. In 2005 we conducted a systematic survey via boat-based north–south transects 1 km apart, between 4.5 km and 8 km in length, in which we recorded all occupied and unoccupied nest sites (Tingay et al. 2006). In subsequent years, the study area was expanded (Fig. 2), including areas we searched for previously unrecorded sites and all previously identified nest sites (and their vicinity), with retention of the original criteria of nest-site occupation. The location of all occupied and unoccupied nest sites was recorded by handheld Geographical Positioning System (GPS) accurate to <10 m resolution.

Figure 2

The flooded swamp forest study site at Prek Toal, illustrating survey areas in 2005 and 2006/2007, with Prek Toal village highlighted in black.

In each year, whenever possible, we recorded the stage of breeding according to the two major phases of the breeding cycle: pre-hatching ( = late breeders) and post-hatching ( = early breeders). We based this on direct observations into the nests (eggs or nestlings) where possible, or, where access was limited, by indirect inference from observations, including adult posture on the nest (i.e., bird sitting low in the nest equals incubation; bird sitting high in the nest equals brooding nestlings). The validity of this inference was tested during a subsequent breeding season (2009), when predictions based on adult posture (n  =  42) were verified by climbing to each nest to inspect the contents. Predictions were correct in all but one nest, where we had predicted nestlings but the eggs were just in the early stage of hatching (R. Tingay unpublish. data).

Results

In the binomial GLM examining tree features associated with presence or absence of a nest, both crown density and tree height were significantly associated with the presence of a nest, negatively and positively, respectively (Table 1). Hence, GHFE nests were more likely to be found in relatively tall trees with an open crown structure. In 2006, 28 nests (82%) were in Ptol trees (Diospyros cambodiana), and three nests (9%) each were in Chrakeng (Mallotus anisopodus) or Taor (Terminalia cambodiana) trees. All nests in 2006 were orientated away from the south/southeast.

Table 1

Results of binomial GLM investigating the relationship between presence and absence of a GHFE nest site (response variable) with tree height and crown density as explanatory terms; df  =  63.

The distribution of distances from nests to permanent water differed significantly from that expected based on the “availability” of all points within the study area, both in 2005 (Kolmogorov-Smirnov Z  =  4.39, P < 0.001) and in 2006 (Kolmogorov-Smirnov Z  =  5.16, P < 0.001; Fig. 3). This was largely due to nest sites being closer to permanent water than expected (Fig. 3). A secondary peak in nest site distribution in 2005 at 1.3–1.4 km from water was potentially an artifact resulting from our inability to discriminate all permanent water using the available digital maps and the more restrictive 2005 study area (lower 50 percentile), but may still have influenced the test for 2005. Censoring 2005 data to 1 km removed this possible influence on the test and illustrated that observed and expected distributions still differed significantly (Kolmogorov-Smirnov Z  =  5.65, P < 0.001), confirming that fish-eagles were more likely to nest close to permanent water.

Figure 3

Distribution of distances to permanent water for occupied GHFE nest sites and all points within the study area (as estimated by an overlay of a 50-×-50-m grid in the GIS) for (a) 2005 and (b) 2006.

Median values of distance to permanent water for “early” and “late” breeders were, respectively, 0.32 km (n  =  6) and 0.32 km (n  =  7) in 2005 and 0.28 km (n  =  9) and 0.34 km (n  =  8) in 2006. There was no significant difference between ‘early’ and ‘late’ breeders according to distance to permanent water, either in 2005 (Mann-Whitney U  =  21, P  =  1.00) or 2006 (Mann-Whitney U  =  33, P  =  0.81). This suggested, although sample sizes were limited, that birds that started breeding earlier were not more likely to breed closer to permanent water.

In our initial saturated Poisson GLM neither explanatory variable (distance to permanent water and distance to Prek Toal) nor their interaction was significant, so we dropped the interaction term in a second model, which then revealed distance to Prek Toal as a significant positive term (Table 2). Our subsequent and best model (as judged by AIC) dropped distance to permanent water and retained only distance to Prek Toal, as a significant positive term (i.e., nest-occupancy was lower closer to the village; (Table 2, Fig. 4).

Figure 4

Index of GHFE territory occupation (0  =  not occupied in any year, 1  =  occupied in one or two years, 2  =  occupied in all three years) in the 2005 study area as a function of distance of the territory to the village of Prek Toal.

Table 2

Results of Poisson GLMs (log link function) investigating potential relationships between an index of GHFE territory occupancy (response variable) and distance to permanent water and distance to Prek Toal village (both variables square-root-transformed) as explanatory terms. Respectively, df  =  13, 14, and 15 for the three models.

There was no significant difference in the mean length of snakes caught at sites 1 and 2 (t  =  0.73, df  =  107, P  =  0.468). The number of snakes and the total length of all snakes caught at site 1 was significantly greater than at site 2 (paired samples tests: t  =  10.08, df  =  3, P  =  0.002; t  =  8.89, df  =  3, P  =  0.003, respectively), indicating that snakes were more abundant in the permanent water site than in the temporarily flooded water site. The species composition of snakes, however, did not appear to differ between the permanent and temporarily flooded sampling sites (Table 3).

Table 3

Snakes captured using gill nets and proportional contribution to total catch per site in permanent water (Site 1, n  =  81) and temporary water (Site 2, n  =  28) at Prek Toal Core Area, Tonle Sap Lake.

Discussion

We found that GHFEs at Prek Toal selected relatively tall trees with an open crown structure as nest sites. Although GHFE preferred nesting closer to permanent water than expected, there was apparently no difference in timing of breeding according to distance to permanent water. Water snakes were significantly more abundant at a site in permanent water than in a temporarily flooded site (although see below for discussion on study limitations). We also found that human habitation had a negative effect on GHFE nest-site occupancy.

Grey-headed Fish-Eagle selection of relatively tall nest trees with an open crown structure is consistent with results from other fish-eagle species (Andrew and Mosher 1982, Shiraki 1994, Berkelman et al. 2002, Hollamby et al. 2006). This preference likely reflects ease of access, in addition to maximizing increased visibility for territorial defense. Due to our study's limitations we could not map tree characteristics at a landscape scale, but subjectively, our strong impression was that features of trees selected by GHFE for nest sites did not vary by distance to permanent water. This impression was confirmed by scrutiny of aerial photographs of the study area (R. Tingay unpubl. data). Our opinion, therefore, is that GHFE were not more likely to nest near permanent water due to nest-site availability. We suggest, based on our documentation of differences in water-snake abundance between permanent and temporarily flooded sites, consistent with the results of Karns et al. (2000), that GHFE prefer nesting close to permanent water because food abundance is greater here. Further research on GHFE diet, however, is required to test our suggestion rigorously. Tingay et al. (2006) documented water snakes as GHFE prey items, but their importance and potential seasonal availability is currently unknown; thus, our limited study may not account for seasonal variation in water snake abundance or GHFE prey preferences. Similarly, we have also recorded fish as GHFE prey (R. Tingay unpubl. data), and, based on studies elsewhere (Junk et al. 1989), we would predict fish abundance to be greater in permanent water, but research on fish ecology at the Tonle Sap is still in its infancy and currently is confined to the main lake (Campbell et al. 2006).

If GHFE prefer to breed closer to permanent water due to proximity to an abundant prey source, then any advantage accrued apparently did not translate into an earlier start to breeding. As all birds seem to commence breeding in early September when the flood waters are rising (toward the end of the rainy season), then when floodwaters are at their peak (October/November) most nests should contain nestlings or have eggs nearing hatch; peak food demands would therefore coincide with potential peak food abundance. However, the factors influencing breeding seasons in tropical fish-eagles are poorly understood. Our study season precluded documentation of reproductive success of birds by proximity to permanent or temporarily flooded habitats, and practically it would be difficult to access temporarily flooded areas at the end of the breeding season once waters have receded. Nevertheless, we speculate that differences in breeding success, due to enhanced prey availability, may explain the propensity for GHFE to nest near permanent water; further research on reproductive rate is required.

We can offer no single causal explanation for why GHFE avoided the proximity of human habitation, as several are possible and our results offered no means of discrimination. Potential explanatory candidates would include direct (albeit potentially unintentional) disturbance of nesting attempts through increased human activity close to Prek Toal village or indirect impacts through depletion of GHFE food supplies, given the intense human exploitation of potential GHFE prey (Campbell et al. 2006, Brooks et al. 2007).

If GHFE at Prek Toal already face potential difficulties from intense harvesting of their prey (Campbell et al. 2006, Brooks et al. 2007), then additional pressures from the change to the lake's hydrological regime induced by the construction of upstream hydropower dams (Kummu and Sarkkula 2008) may add to these problems. We have highlighted gaps in knowledge of GHFE biology at Prek Toal, and recommend research efforts to fill these gaps. We also recommend extending the research to other areas of the swamp forest surrounding Tonle Sap Lake. It is known that GHFE breed in the Boeng Chhma Core Area (Fig. 1; S. Visal unpubl. data), but the distribution and status of GHFE there, and in other areas of the swamp forest, is currently undocumented. Given the regional significance of the Prek Toal GHFE population, and the variety of potential threats to this population's stability (Tingay et al. 2006), our information on GHFE nesting ecology can be used to facilitate a rapid assessment throughout the Tonle Sap Lake swamp forest. In conjunction with filling these knowledge gaps, in light of the potential future changes to this unique ecosystem, we also recommend long-term monitoring of the high-density GHFE population at Prek Toal, as large raptors are excellent bioindicators of the health of ecosystems (Sergio et al. 2005, 2006).