Introduction
Tropical forests continue to be cleared for agriculture, resulting in high levels of biodiversity loss (Edwards et al., Reference Edwards, Socolar, Mills, Burivalova, Koh and Wilcove2019; Oakley & Bicknell, Reference Oakley and Bicknell2022). For example, more than 68 million ha of forest were converted during 2001–2015 to produce cattle, oil palm, soy, cocoa and coffee (Goldman et al., Reference Goldman, Weisse, Harris and Schneider2020). Public attention has focused on the land-use impacts of major agricultural commodities such as palm oil, but little attention has been paid to other oil crops such as coconut Cocos nucifera (Meijaard et al., Reference Meijaard, Abrams, Juffe-Bignoli, Voigt and Sheil2020).
Coconut is a perennial crop that contributes to the livelihoods of millions of people in tropical and subtropical countries, with the leading producers being Indonesia, the Philippines and India (FAOSTAT, 2020). Although the crop is generally grown at the smallholder scale, the cumulative area of coconut farming is large, amounting to > 12.3 million ha (FAOSTAT, 2020). A preliminary study based on global databases identified coconut as a crop with potentially significant impacts on wildlife because coconut palms are mainly grown on tropical islands and/or in coastal areas with high levels of species diversity and endemism (Meijaard et al., Reference Meijaard, Abrams, Juffe-Bignoli, Voigt and Sheil2020). Although the potential impacts of coconut farming are concerning, there are few biodiversity appraisals that compare the conservation value of coconut palm plantations to forests or other land uses (Henson, Reference Henson2005; Basheer & Aarif, Reference Basheer and Aarif2013; Dinanti et al., Reference Dinanti, Winarni and Supriatna2018).
Coconut plantations cover > 3.4 million ha across Indonesia (c. 6% of non-forested land), making it the third largest agricultural commodity in the country in terms of area covered (after oil palm Elaeis guineensis and rubber Hevea brasiliensis at 14.3 and 3.6 million ha, respectively; Badan Pusat Statistik, Reference Badan Pusat Statistik2022). Almost one-third of the area under cultivation is in the Wallacea region, a major centre of species endemism comprising the islands of Sulawesi, Nusa Tenggara and Maluku (Struebig et al., Reference Struebig, Aninta, Beger, Bani, Barus and Brace2022). Sulawesi in particular has a long history of coconut cultivation. By 2021, at least 763,135 ha of coconut farms were estimated to have been planted on the island (c. 8% of non-forested land), primarily by smallholders. Although deforestation rates have been much lower on Sulawesi than in other parts of Indonesia, there has been a surge in deforestation in recent years associated with the expansion of farming and mining (Voigt et al., Reference Voigt, Supriatna, Deere, Kastanya, Mitchell and Rosa2021). This deforestation is leading to the gradual loss of specialized and endemic wildlife species and their replacement by widely distributed generalists, as demonstrated by bird surveys across the Wallacea region (Mitchell et al., Reference Mitchell, Edwards, Martin, Deere, Voigt and Kastanya2022). Nevertheless, the conservation value of the agricultural matrix surrounding the forests of Wallacea remains poorly documented for oil crops such as coconut.
Areas of open, unshaded and/or homogeneous croplands tend to have impoverished wildlife communities and low biodiversity (Oakley & Bicknell, Reference Oakley and Bicknell2022). Similarly to other palms, the planting of coconut changes the floristic, structural and soil characteristics of the habitat available to wildlife (Young et al., Reference Young, Raab, McCauley, Briggs and Dirzo2010), leaving an open understorey and fewer opportunities for feeding and shelter (Dinanti et al., Reference Dinanti, Winarni and Supriatna2018). However, because coconuts are generally grown by smallholders in small plantations and gardens, the effects of this cultivation on biodiversity could be relatively benign compared to those of other crops that are grown at an industrial scale. For example, bird diversity is significantly lower in rubber plantations than in rubber agroforestry and forests in Sumatra (Beukema et al., Reference Beukema, Danielsen, Vincent, Hardiwinoto and van Andel2007), and in Kalimantan, indicator species associated with forests and mixed gardens were absent from nearby oil palm plantations (Simamora et al., Reference Simamora, Purbowo and Laumonier2021). Multiple studies have demonstrated that oil palm plantations support much lower levels of species diversity and abundance, even if forests are nearby (Aratrakorn et al., Reference Aratrakorn, Thunhikorn and Donald2006; Fitzherbert et al., Reference Fitzherbert, Struebig, Morel, Danielsen, Brühl, Donald and Phalan2008; Edwards et al., Reference Edwards, Hodgson, Hamer, Mitchell, Ahmad, Cornell and Wilcove2010).
Here we explore the conservation value of coconut palm plantations relative to forests and other farmland in Sulawesi. Specifically, we characterize patterns of biodiversity and community structure amongst forest sites, coconut palm plantations and mixed farmland, using birds as a focal taxon. Birds are useful indicators of anthropogenic disturbance as they can be surveyed relatively easily and tend to be sensitive to landscape changes (Schulze et al., Reference Schulze, Kessler, Pitopang, Shahabuddin, Veddeler and Muhlenberg2004; Gardner et al., Reference Gardner, Barlow, Araujo, Ávila-Pires, Bonaldo and Costa2008; Winarni & Jones, Reference Winarni and Jones2012). In Sulawesi, forest conversion to cacao agroforests has negatively affected endemic forest birds (Maas et al., Reference Maas, Putra, Waltert, Clough, Tscharntke and Schulze2009), and forest disturbance is an important predictor of occupancy of knobbed hornbills Rhyticeros cassidix (Winarni & Jones, Reference Winarni and Jones2012). We undertook standardized bird surveys in forests and farmland in the province of Gorontalo and compared species diversity and community structure between landscapes and habitats.
Study area
Gorontalo is located on the Minahasa peninsula of Sulawesi, and is one of the most forested provinces on the island, with more than 856,000 ha of forest cover (c. 71% of the province) from the coastal lowlands up to an altitude of 2,211 m (Potapov et al., Reference Potapov, Hansen, Pickens, Hernandez-Serna, Tyukavina and Turubanova2022). Key forest trees include rao Dracontomelon dao, nantu Palaquium obovatum and pangi Pangium edule (Macdonald et al., Reference Macdonald, Collins, Johnson, Clayton, Malhi and Fisher2011; Rahim, Reference Rahim2015), and these habitats support populations of iconic endemic vertebrates such as the knobbed hornbill, maleo Macrocephalon maleo, lowland anoa Bubalus depressicornis and Sulawesi babirusa Babyrousa celebensis. Although deforestation rates have been lower in Gorontalo than in other parts of Sulawesi, the province is projected to lose 32% of forest cover by the 2050s (Voigt et al., Reference Voigt, Supriatna, Deere, Kastanya, Mitchell and Rosa2021) because of encroachment from small-scale agriculture, namely from coconut, corn and oil palms. Approximately 9% of the province is used to cultivate coconut (Badan Pusat Statistik, Reference Badan Pusat Statistik2022). Similarly to other parts of Sulawesi, the landscape is highly heterogenous because of multiple crops being grown in the region (often in smallholder systems).
Methods
Bird surveys
We undertook bird surveys across forests and farmlands in three landscapes of Gorontalo: Nantu-Tamilo (around Saritani village), Hutamono-Tapaada (Rumbia and Dulangeya) and Bogani-Tinemba (around Lombongo and Tinemba; Fig. 1, Supplementary Table 1). The forest sites included two protected areas: Bogani Nani Wartabone National Park and Nantu Wildlife Reserve. The agricultural areas were dominated by coconut farms, corn fields and mixed farmland, with some smaller areas of oil palm plantations.
Fig. 1 Study sites in Gorontalo Province, Sulawesi, Indonesia. An overview of the spatial configuration of point count locations within each survey transect is shown in the inset.
We surveyed birds during October–November 2021 by conducting 10-min point counts during periods of peak bird activity (05.40–09.30) in clear weather. On each survey morning, a pair of observers (KY and ZZ/MAWG, or BI and BGA) surveyed a transect of nine points, which were arranged in three clusters of three points each. A distance of c. 1 km separated neighbouring clusters, and the points within a cluster were at least 200 m apart (the recommended distance for avian point counts to ensure spatial independence; Lees & Peres, Reference Lees and Peres2009; Supplementary Fig. 1). We surveyed six transects (two in each landscape), totalling 54 independent points, with four repeat visits to each point conducted on different days. Points were distributed across the three habitat types: forest (16 point count locations), palm (18 coconut farms, with one site also dominated by sugar palm Arenga pinnata) and mixed farmland (20 locations; Supplementary Table 1). We sought to survey multiple habitats within each transect (ideally oil palm, coconut palm plantations and mixed farmland in a single morning) and switched the order in which we sampled these points on repeat visits. We defined the configuration in advance of the survey using Google Earth imagery (Google, Mountain View, USA) to avoid location bias in the field.
For each point count, observers recorded the number and identity of individual birds that were identified based on their vocalizations or direct observations. We made audio recordings of most counts, and a second observer verified these (using recordings shared on xeno-canto if needed; Xeno-canto Foundation, Reference Xeno-canto Foundation2021) at a later date. We included birds observed in flight in these counts. We followed the taxonomy used by Eaton et al. (Reference Eaton, van Balen, Brickle and Rheindt2016) and BirdLife International (Reference BirdLife International2023) and classified species as endemic based on available checklists (Lepage & Warnier, Reference Lepage and Warnier2014).
Analysis
To compare species accumulation between landscapes and habitats, we constructed sample-based rarefaction curves based on the point count data using the package iNEXT in R 3.5.2 (Hsieh et al., Reference Hsieh, Ma and Chao2016; R Core Team, 2019). The rarefaction analyses used the Hill number framework to generate three measures of diversity: species richness (i.e. effective species numbers), Shannon index (i.e. the exponent of Shannon entropy, with high values representing a high level of uncertainty in species identity and thus high diversity) and Simpson index (i.e. the inverse of the Simpson concentration, with high values indicating greater evenness in the species abundance distribution and thus high diversity; Magurran, Reference Magurran2004). We extrapolated bird detections to a common upper sample size of 1,000 individuals for standardized comparisons, and we generated 84% confidence intervals for the curves. Comparisons of the curves are deemed statistically significant when these confidence intervals do not overlap, which is equivalent to a P-value of 0.05 (MacGregor-Fors & Payton, Reference MacGregor-Fors and Payton2013).
We used ordinations to explore variations in bird community compositions between landscapes and habitats. We first standardized the species-point data matrix by maximum values (a Wisconsin double standardization) to facilitate the detection of community patterns, before calculating pairwise Bray–Curtis dissimilarity coefficients between point-count inventories. We generated a non-metric multidimensional scaling ordination using the R package vegan (Oksanen et al., Reference Oksanen, Simpson, Blanchet, Kindt, Legendre, Minchin and O'Hara2022) to visualize patterns of bird community composition across forests, mixed farmland and palm plantations. We applied permutational multivariate analysis of variance to examine compositional differences amongst habitats using the ADONIS function in vegan. We also identified indicator species for each habitat type using the multi-level pattern analysis in the Indicspecies package in R (Dufrene & Legendre, Reference Dufrene and Legendre1997; Cáceres & Legendre, Reference Cáceres and Legendre2009). Species indicator values combine information on the relative abundance and relative frequency of occurrence of species in the defined habitats to narrow down a large number of species to a few species of interest that are the most characteristic species of the groups. We implemented the analysis predefining the three habitats as ‘groups’ and calculated indicator values with 999 permutations as a measure of statistical significance. Thus, the detections of species with significant indicator values are strongly associated with particular habitat types.
Results
We recorded 100 bird species during 162 visits to the 54 point-count localities (Supplementary Table 1). Of these, 62 species were observed in forests, 75 in coconut palm plantations and 75 in mixed farmland. Species accumulation curves for each habitat type approached an asymptote, indicating sufficient survey effort (Fig. 2). Although there were no significant differences in the numbers of bird species between forests, coconut palm plantations and mixed farmland, forests supported more even bird communities (i.e. species were present at similar abundances), as indicated by significantly higher Shannon and Simpson diversity (Fig. 3). Palm plantations supported intermediate levels of diversity compared to forests and mixed farmland. Forests also supported more endemic bird species and fewer non-endemics than palm plantations and mixed farmland (Fig. 3, Supplementary Fig. 1).
Fig. 2 Rarefied species accumulation curves for bird communities in the forests, coconut palm plantations and mixed farmland of Gorontalo Province, Sulawesi, Indonesia (Fig. 1). We conducted analyses separately for (a) all species, (b) taxa endemic to Sulawesi and the surrounding islands and (c) non-endemic species. We extrapolated the curves (dashed lines) to 1,000 individuals to ensure a consistent sample size for each comparison. We set the confidence intervals (shaded areas) at 84%, which has been demonstrated to be equivalent to a P-value of 0.05 for significant differences (MacGregor-Fors & Payton, Reference MacGregor-Fors and Payton2013).
Fig. 3 Standardized comparisons (at 1,000 individuals) of richness, Shannon–Weiner diversity and Simpson diversity of bird species amongst forest, coconut palm plantations and mixed farmland sites in Gorontalo Province, Sulawesi, Indonesia. Analyses are shown for the whole bird community and for endemic and non-endemic species. Error bars represent 84% confidence intervals (for rationale, see MacGregor-Fors & Payton, Reference MacGregor-Fors and Payton2013).
The non-metric multidimensional scaling ordinations robustly reflected the variation in bird community structure amongst sites according to stress values (all < 0.157), and showed substantial overlap in community composition between forests, coconut palm plantations and mixed farmland. Nevertheless, permutational multivariate analysis of variance comparisons revealed subtle and significant differences between the bird communities across all three habitats (R 2 = 0.11, P < 0.001), as well as between individual locations within the same habitat type (R 2 = 0.06–0.11, P < 0.002). This pattern persisted when we repeated the analyses for endemic (R 2 = 0.10, P < 0.001) and non-endemic (R 2 = 0.10, P < 0.001) species. Notably, there was much more variation in the identity and abundance of non-endemic species between different forest sites than between agricultural sites; the latter tended to be much more homogeneous in their bird community compositions (Fig. 4).
Fig. 4 Non-metric multidimensional scaling (NMDS) ordinations showing variation in bird community structure across forest, coconut palm plantation and mixed farmland sites in Gorontalo Province, Sulawesi, Indonesia. We undertook ordinations separately for (a) all species, (b) endemic species only and (c) non-endemic species.
Indicator species analysis revealed eight species that were significantly associated with forest habitat, four with coconut palm plantations and five with mixed farmland (Table 1). Amongst the forest indicator species, six were endemic: the Sulawesi dwarf kingfisher Ceyx fallax, ashy woodpecker Dryocopus fulvus, Oberholser's fruit dove Ptilinopus gularis, Sulawesi babbler Pellorneum celebense, ornate lorikeet Saudareos ornata and pale-blue monarch Hypothymis puella. There were no endemics amongst the indicator species of palm plantations, and only one endemic was identified for mixed farmland (the grosbeak myna Scissirostrum dubium). A further two species were prominent in forests and coconut palm plantations (the Sulawesi cuckoo dove Macropygia albicapilla and white-eyed spangled drongo Dicrurus leucops), and three were indicators of mixed farmland and coconut palm plantations. No indicator species overlapped between forests and mixed farmland.
Table 1 Bird indicator species for forests, mixed farmland and coconut palm plantations in Sulawesi, Indonesia (Fig. 1), as well as indicator species for forest and coconut palm plantations, and those for mixed farmland and coconut palm plantations.
*P < 0.5, **P < 0.01, ***P < 0.001.
Discussion
Community structure and composition amongst forests and agricultural habitats
Sulawesi is a rugged and geologically complex region, with much of the island being mountainous and only a small proportion of forest in the lowlands (Whitten et al., Reference Whitten, Henderson and Mustafa2002). In Gorontalo, pressures from logging, transmigration and estate crop plantation are high because of this limited extent of lowland forests (FWI/GFW, 2002; Supriatna et al., Reference Supriatna, Shekelle, Fuad, Winarni, Dwiyahreni and Farid2020). There have not been many studies conducted on the use of commodity plantations by birds in Indonesia and Southeast Asia more broadly. Bird surveys in the forests, rubber plantations and agroforest systems of jungle rubber, damar Shorea javanica and durian Durio zibethinus of Sumatra revealed higher species richness in the agroforest rubber tree systems than damar and durian systems, with the lowest diversity occurring in the durian areas (Thiollay, Reference Thiollay1995; Beukema et al., Reference Beukema, Danielsen, Vincent, Hardiwinoto and van Andel2007). The bird diversity in the forest-like conditions of jungle rubber sites tended to be most similar to that recorded in forest sites (Beukema et al., Reference Beukema, Danielsen, Vincent, Hardiwinoto and van Andel2007). Bird diversity is known to be significantly reduced in oil palm plantations, although this reduction is less severe in smallholder farms, especially those with higher yields (Razak et al., Reference Razak, Saadun, Azhar and Lindenmayer2020). In Sulawesi, bird taxa are able to persist in shade-grown cacao farms, including ornate lorikeets that are endemic to the island and crimson sunbirds Aethopyga siparaja (Siebert, Reference Siebert2002), two species confirmed as indicators of forest habitat in our study.
Our surveys in the northern region of Sulawesi demonstrate that overall bird diversity levels are similar between forests, mixed farmland and palm/coconut plantations, yet the agricultural habitats lacked many of the endemic species characteristic of forests and instead were dominated by generalist, non-endemic species. This pattern of biotic homogenization is being reported increasingly around the world (McKinney, Reference McKinney2006; Devictor et al., Reference Devictor, Julliard, Clavel, Jiguet, Lee and Couvet2008; Ibarra & Martin, Reference Ibarra and Martin2015; Kormann et al., Reference Kormann, Hadley, Tscharntke, Betts, Robinson and Scherber2018), including in Sulawesi (Maas et al., Reference Maas, Putra, Waltert, Clough, Tscharntke and Schulze2009). Across six Wallacean islands, conversion from forest to agricultural landscapes was associated with the replacement of more specialized, range-restricted species by a shared cohort of generalists and human commensals with wider global ranges (Mitchell et al., Reference Mitchell, Edwards, Martin, Deere, Voigt and Kastanya2022).
The modest differences in the bird communities were reflected in the differences in bird diversities between forests, mixed farmland and palm/coconut plantations. Forest sites supported the highest levels of bird diversity compared to sites in coconut plantations or mixed farmland. It has been suggested previously that agroforest is an environment in which small frugivores, foliage insectivores and nectarivores can thrive (Thiollay, Reference Thiollay1995). Our indicator species analyses for Gorontalo revealed that frugivores and insectivores tended to flourish in forests, whereas there were more aerial insectivores (barn swallow Hirundo rustica) and granivores (Eurasian tree sparrow Passer montanus) in mixed farmland. The coconut plantations may act as an intermediate habitat between forests and the much more open mixed farmland as smallholder coconut plantations are usually intercropped with other plants. This provides an intermediate vegetation structure that is more complex than mixed farmland (Kumar & Kunhamu, Reference Kumar and Kunhamu2022) and thus offers potential habitat features for nectarivores and insectivores. Similar species compositions were also indicated in the coconut farms in West Java, where the lesser coucal Centropus bengalensis was dominant (Dinanti et al., Reference Dinanti, Winarni and Supriatna2018). Recent research on oil palm plantations in Indonesia found no indicator bird species in these plantations (Simamora et al., Reference Simamora, Purbowo and Laumonier2021). Further studies comparing bird diversity in coconut vs oil palm plantations are needed to investigate whether this apparent lack of indicator species reflects any significant differences in the communities supported by these crops.
Deforestation leads to increased forest fragmentation and edge effects, changing the community structure of birds, and increases the distribution of common, introduced species (Leven & Corlett, Reference Leven and Corlett2004; Waltert et al., Reference Waltert, Mardiastuti and Muhlenberg2005; Maas et al., Reference Maas, Putra, Waltert, Clough, Tscharntke and Schulze2009; Sodhi et al., Reference Sodhi, Sekercioglu, Barlow and Robinson2011). The latter pattern is characteristic of biotic homogenization, in which native, specialized and endemic species are replaced by widely distributed, common, generalist species (Devictor et al., Reference Devictor, Julliard, Clavel, Jiguet, Lee and Couvet2008; Mitchell et al., Reference Mitchell, Edwards, Martin, Deere, Voigt and Kastanya2022). Sooty-headed bulbuls Pycnonotus aurigaster, Java sparrows Padda oryzivora and zebra doves Geopelia striata are becoming widely distributed in the Minahasa peninsula, from North Sulawesi to Bogani Nani Wartabone National Park in Gorontalo (Fitzsimons et al., Reference Fitzsimons, Thomas and Argeloo2011). Over 10 years of observations in Lore Lindu, Central Sulawesi, endemic birds decreased in abundance and were replaced by more generalist species (Maas et al., Reference Maas, Putra, Waltert, Clough, Tscharntke and Schulze2009). An earlier study in that region demonstrated clearer differences in the bird fauna between forest and agroforest habitats than we describe in Gorontalo (Waltert et al., Reference Waltert, Mardiastuti and Muhlenberg2004), implying that biotic homogenization is an ongoing process and could be at a more advanced stage in the farming systems in the north of Sulawesi. In our study we recorded the more generalist species such as sooty-headed bulbuls in all habitat types, including the forest, and we only recorded the zebra dove in mixed farmland and palm plantations. Birds such as sooty-headed bulbuls were amongst the first species to colonize Krakatau 25 years after its eruption, suggesting that they are pioneers that are able to utilize human-disturbed areas and secondary forests (Thornton et al., Reference Thornton, Zann and Stephenson1990; Corlett & Hau, Reference Corlett, Hau, Elliot, Kerby, Blakesley, Hardwick, Woods and Anusarnsunthorn2000; Winarni & Wijoyo, Reference Winarni and Wijoyo2014; Winarni et al., Reference Winarni, Nuruliawati and Afifah2019). Although these birds have been reported in South Sulawesi since the 1990s (MacKinnon & Phillipps, Reference MacKinnon and Phillipps1993; Coates et al., Reference Coates, Bishop and Gardner1997), their presence in the North Sulawesi and Gorontalo provinces is probably a result of caged birds having escaped there, rather than an expansion of the population from South Sulawesi (Fitzsimons et al., Reference Fitzsimons, Thomas and Argeloo2011).
Implications for endemic birds
There is a growing literature on the changes to ecological communities because of agriculture, including the replacement of native bird species with widely distributed, often invasive, taxa (Maas et al., Reference Maas, Putra, Waltert, Clough, Tscharntke and Schulze2009; Peh, Reference Peh2010; de Solar et al., Reference de Solar, Barlow, Ferreira, Berenguer, Lees and Thomson2015; Newbold et al., Reference Newbold, Hudson, Contu, Hill, Beck and Liu2018). Forests accommodate more endemic species, whereas non-endemic species thrive in palm plantations and mixed farmland. We recorded birds originally from Southeast Asia such as zebra doves and sooty-headed bulbuls in mixed farmland and palm plantations. The invasion of these species could have a significant effect on native species through competition, leading to their local extirpation. Invasive bird species could also become agricultural pests and carry diseases that harm native flora and fauna (Mack et al., Reference Mack, Simberloff, Lonsdale, Evans, Clout and Bazzaz2000; Sodhi et al., Reference Sodhi, Sekercioglu, Barlow and Robinson2011). We recorded the sooty-headed bulbul (an introduced Javan and Indochinese species) during our surveys, which has been suggested as a potential competitor to native, endemic birds in Wallacea (Peh, Reference Peh2010).
Coconut is cultivated and produced in all 34 provinces in Indonesia (Alouw & Wulandari, Reference Alouw and Wulandari2020). Over decades, this cultivation has expanded from lowland coastal areas to include some hilly areas (Sondakh & Kaligis, Reference Sondakh, Kaligis, Shelton and Stur1991). Intercropping with corn, rice, soybeans, groundnuts, cassavas or sweet potatoes occurs in coconut farming, which could support greater biodiversity (Godoy & Bennett, Reference Godoy and Bennett1991; Sondakh & Kaligis, Reference Sondakh, Kaligis, Shelton and Stur1991; McLaughlin & Mineau, Reference McLaughlin and Mineau1995; Manoppo & Yusron, Reference Manoppo and Yusron2021). Birds may be able to use palm trees for nesting and foraging in agricultural environments where native plants are lacking. Birds particularly utilize the crowns of live palm trees in the upper layer of the canopy for nesting, as well as dead trunks in the middle layer of the canopy (Basheer & Aarif, Reference Basheer and Aarif2013; Dinanti et al., Reference Dinanti, Winarni and Supriatna2018).
The expansion of coconut farmland is likely to lead to negative consequences for biodiversity across tropical and subtropical regions because much of the area left for cultivation is on small islands that support disproportionately large numbers of endemic species. For example, the newly described Wangi-wangi white-eye Zosterops paruhbesar is restricted to a single island of 155 km2 where coconut farming is extensive (Irham et al., Reference Irham, Prawiradilaga, Menner, Connell, Kelly and Analuddin2022). Although we recorded one endemic bird (the grosbeak myna) as being associated with mixed farmland, many endemic birds are highly or moderately dependent on forests (Buchanan et al., Reference Buchanan, Butchart, Dutson, Pilgrim, Steininger, Bishop and Mayaux2008). Forests remain important habitats for endemic Sulawesi birds, particularly forest dwellers such as the Sulawesi dwarf kingfisher and ashy woodpecker (Coates et al., Reference Coates, Bishop and Gardner1997). Therefore, the continuing expansion of croplands in Gorontalo is worthy of attention.
The decline of endemic species in Sulawesi is unlikely to be driven by agricultural expansion alone. For biodiversity monitoring on Buton Island, Southeast Sulawesi, the knobbed hornbill is used as an indicator of anthropogenic disturbance because of its sensitivity to human-induced habitat alteration. Although these birds are able to utilize different habitats, their presence or absence is explained by habitat disturbance and forest condition, because they require large trees for nesting and figs as a food resource (Kinnaird & O'Brien, Reference Kinnaird and O'Brien2007; Winarni, Reference Winarni2009; Winarni & Jones, Reference Winarni and Jones2012). In our study knobbed hornbills were rarely recorded within the forests, mixed farmland or palm plantations, suggesting that the nearby forests may have experienced some degradation. Forest degradation and fragmentation are generally linked with agricultural expansion in Wallacea (Voigt et al., Reference Voigt, Supriatna, Deere, Kastanya, Mitchell and Rosa2021), and exploring which incentives drive the trajectories of forest conversion in these systems should be a research priority in this region. The designation of additional protected areas alone may not be adequate to protect some endemic species, because protected area status does not necessarily reduce forest loss (Curran et al., Reference Curran, Trigg, McDonald, Astiani, Hardiono and Siregar2004; Hassan et al., Reference Hassan, Scholes and Ash2005). Safeguarding the endemic avifauna of Sulawesi is likely to require additional legislative enforcement of forest protections as well as a shift towards policies and management strategies that reduce the environmental impacts of agricultural activities.
Acknowledgements
We thank the Head of Bogani Nani Wartabone National Park and the Head of Balai Konservasi Sumber Daya Alam (BKSDA) Gorontalo of the Indonesian Ministry of Environment and Forestry for granting us access to survey the protected areas; the landowners who granted access to their land for the bird surveys; and the anonymous reviewers for their critiques. This study was funded under the Wallacea Programme of the Newton Fund via the Indonesian Ministry for Research, Technology and Higher Education (Ristekdikti, NKB-2892/UN2.RST/HKP, 05.00/2020 and 1/E1/KP.PTNBH/2019) for JS, and the UK Natural Environment Research Council (NERC, NE/S007067/1) for MJS. We dedicate this article to the late Tony Whitten, who inspired many Indonesian researchers to study the biodiversity of Sulawesi.
Author contributions
Study design: NLW, SLM, ZZ, JS, MJS; fieldwork: NLW, BGA, KY, BI, MAWG; data analysis: NLW, SLM, NJD, MJS; writing: NLW, SLM, JS, MJS.
Conflicts of interest
None.
Ethical standards
This research abided by the Oryx guidelines on ethical standards and followed ethical research standards in Indonesia, including appropriate field protocols and research permissions. Bird surveys were based on field observations, without collection or handling of specimens, and were conducted with permission from the landowners.
Open access
