Sage Journals: Discover world-class research

Abstract

The island of Borneo suffers from one of the highest deforestation rates in the world, primarily due to agriculture, logging, and other human activities. This habitat loss may be partly mitigated by reforestation programs in degraded landscapes, especially anthropogenic grasslands that have little conservation or economic value. By monitoring native bird communities, we evaluated the success of two small (<20 ha) community reforestation projects in Gunung Palung National Park in Indonesian Borneo. Birds responded rapidly following reforestation, with species richness doubling over 7 years at one site, and increasing by 29% in just 3 years at the other. Final tallies (63–70 species per site) were comparable to those obtained in older secondary forests elsewhere in Borneo. Anthropogenic fire is the primary threat to reforestation success, but intensive fire prevention allows bird communities to recover from temporary setbacks. Absence of fire was thus the most important factor in recovery, and we detected no effect of replanted area on bird species richness. Our results suggest that by engaging local communities and ensuring long-term maintenance, even small reforestation sites in Borneo can provide immediate benefits for native biodiversity.

Keywords

biodiversity hotspots deforestation ecological succession fire restoration ecology species–area relationship

Introduction

The island of Borneo suffers from some of the world's highest deforestation rates (Damayanti & Prasetyo, 2015; Margono, Potapov, Turubanova, Stolle, & Hansen, 2014), imperiling its thousands of endemic species and ranking it among the world's biodiversity hotspots (Corlett, 2014; Myers, Mittermeier, Mittermeier, da Fonseca, & Kent, 2000). Over half the island's forests have been converted to other land uses, including oil palm plantations and croplands (Fitzherbert et al., 2008; Zamzani, Onda, Yoshino, & Masuda, 2009), and forest loss is rampant even within protected areas (Curran et al., 2004; Margono et al., 2014). The long-term survival of Borneo's biodiversity thus depends on reforestation as a supplement to the creation of protected areas (Chazdon, 2008; International Tropical Timber Organization [ITTO], 1990; Kettle et al., 2011; Normile, 2009).

Much of Borneo's land area is potentially available for reforestation. Following widespread forest clearing and subsequent wildfires, hundreds of thousands of square kilometers of the island have become dominated by alang-alang (Imperata cylindrica) grassland (Garrity et al., 1997; ITTO, 1990; Kuusipalo et al., 1995). These areas have little value for native species and are unused economically (Garrity et al., 1997; Kuusipalo et al., 1995; Ohta, 1990), but if protected from fire can revert to natural forest (Yassir, van der Kamp, & Buurman, 2010). They thereby offer substantial reforestation opportunities with few costs to local communities. Tropical reforestation projects, however, may not replicate natural conditions or may fail altogether (Chazdon, 2008; Wuethrich, 2007). Our knowledge of Bornean reforestation progress, and how it benefits native species, remains especially limited (Kettle et al., 2011).

Here, we evaluate two community reforestation projects in Gunung Palung National Park in Indonesian Borneo. The park is a 108,000-ha protected area in West Kalimantan, consisting mostly of lowland dipterocarp rainforest (∼3,000 mm annual precipitation). The buffer zones around the park have lost nearly all their forest cover, and at least 10% of the park itself has been deforested due to illegal logging and conversion to agriculture (Curran et al., 2004; Zamzani et al., 2009). Open lands continue to encroach into the park, aided by frequent wildfires. In partnership with the park administration, the conservation and human health NGO Yayasan Alam Sehat Lestari (ASRI) has worked with local communities to reforest two areas on the park border (Pohnan, Ompusunggu, & Webb, 2015). We evaluate the success of those efforts using bird communities as indicators of restoration progress. Borneo is home to over 400 bird species, many of which play vital roles in ecological processes like seed dispersal, and their diversity is a useful indicator of forest quality (Edwards, Ansell, Ahmad, Nilus, & Hamer, 2009; Lambert & Collar, 2002; Maas et al., 2016). Bird species respond predictably to disturbance and vegetation structure (Lack, 1933), and their species richness increases as degraded areas are restored to natural vegetation (Edwards et al., 2009; Pei et al., 2018). Moreover, the small size of the reforestation sites (<20 ha) allows us to investigate impacts at a scale relevant to the conservation capacity of local communities and nonprofit organizations. Our results highlight the conservation value of secondary rainforest (Chazdon et al., 2009; Takano et al., 2014) and suggest that even small reforestation projects can provide rapid benefits for Borneo's native biodiversity.

Methods

Reforestation Sites

We monitored bird communities at two reforestation sites within Gunung Palung National Park (Figure 1(a)). The first site (1°22′15′′S, 110°13′31′′E, elevation 27 m) is a 23-ha area near the village of Laman Satong that was clearcut in the 1990s (Figure 1(b)). It lies on the park border, surrounded by selectively logged forest within the park and a road and agricultural land outside. After clearcutting, repeated wildfires destroyed the soil seed bank and remaining woody vegetation. By 2009, it was dominated by alang-alang grass and bracken ferns (Pteridium aquilinum), fire-tolerant natives that colonize disturbed areas and slow forest succession (Kuusipalo et al., 1995; Yassir et al., 2010). The land was then targeted for reforestation by ASRI and the national park. Each year from 2009 to 2015, at the beginning of the wet season from November to December, 2 to 7.5 ha were planted with a mix of ∼30 native tree species at a density of 1,300 to 4,000 seedlings per hectare. Seeds and seedlings were collected from forests in the national park or from community-owned forests, or from local citizens in exchange for health care subsidies at ASRI's private clinic. Replanted areas were weeded 3 to 4 times per year until seedlings were tall enough to overtop competing grass and ferns, and firebreaks were constructed to protect the site from fire. Site preparation, planting, and maintenance were conducted by over 400 local employees and community members, sometimes through outreach events aimed at informing communities about forest loss (Pohnan et al., 2015). The replanted area reached a peak of 19.8 ha (out of the 23 ha available) before being burned by a wildfire in 2013, leaving only 0.9 unburned hectares that had been planted in 2009. Planting efforts continued, with intensified fire prevention, and by 2015, the replanted area had recovered to 8.2 ha.

Figure 1.

(a) Our reforestation sites were in Gunung Palung National Park in West Kalimantan, Indonesia. (b) Aerial view of Laman Satong in 2009 before planting and (c) the same for Sedahan Jaya in 2012.

The second site (1°13′7.26′′S, 110°2′2.00′′E, elevation 15 m), ∼27 km away from the first and near the village of Sedahan Jaya, is a 6.5-ha freshwater swamp and peat forest (Figure 1(c)). It is surrounded by a mixture of rice paddies, fallow farmland, slash-and-burn gardens dominated by bananas and fruit trees, and selectively logged forest within the park. The site was cleared by farmers in 2010 for conversion to rice paddies. Parts of it were burned and farmed for 1 year, but then abandoned and left fallow. The soil seed bank was still partly intact in some areas and natural secondary succession began immediately, driven primarily by fast-growing Macaranga species. Other areas remained dominated by bracken ferns. ASRI and the national park then targeted the site for reforestation as part of a dispersal corridor for Bornean orangutans (Pongo pygmaeus). In 2013, they planted the understory of all 6.5 ha using a mix of ∼20 species at a density of ∼1,000 seedlings per hectare, followed by targeted enrichment plantings in 2014. Labor and maintenance were conducted by several dozen local employees and community members.

Bird Surveys

We surveyed bird species at the Laman Satong site in 2011, 2012, 2013, 2014, and 2016. We also conducted a preliminary survey just before planting began in 2009. For the preliminary survey, we conducted point counts of 3 minutes each at 10 randomly selected locations in the reforestation area between 0510 and 0630. We identified and counted all birds seen or heard within a 40 × 40 meter square centered on the point, thereby covering four reforestation treatment plots (each of 20 × 20 m). We surveyed each point once per day for 10 days between 30 October and November 11, for a total of 100 point surveys, all conducted by the same individual. All 100 point counts were compiled to produce a species list for 2009. For subsequent surveys, we monitored the entire reforestation site for ∼8 hours per day for 5 days during the first half of November, between 0600 and 1800, noting any birds seen or heard within the property, and recording unidentified calls using a Sony hand recorder or PCM-D50 linear recorder. Recorded calls were later identified to species using audio references (Niklasson, 2013; Scharringa, 2005; selected recordings from the Cornell Lab of Ornithology). Field guides were used for visual identifications (Meyers, 2009; Phillips & Phillips, 2009; Shi, 2012).

We first surveyed the Sedahan Jaya site in early November 2013, seven months after completing planting, then again in 2014 and 2016, using the same methods as the later Laman Satong surveys.

Data Analysis

Because the 2009 preliminary survey at Laman Satong differed in methods (timed point counts vs. comprehensive surveys with audio recordings), we excluded it from year-to-year comparisons. We did, however, include it in the total species list. To better categorize the bird communities, for each species, we also determined its feeding guild (13 guilds adapted from Edwards et al., 2009; Lambert, 1992) and conservation status (International Union for Conservation of Nature [IUCN], 2017). Finally, we tested for relationships between species richness and reforested area and site age using ordinary least squares regression. Variables were tested for normality using the Shapiro–Wilk test. Analysis was done in R (R Core Team, 2012). This work complied with the laws of the countries in which it was performed.

Results

Bird species richness increased rapidly at both sites in response to reforestation. We recorded a total of 101 bird species, 81 from Laman Satong and 69 from Sedahan Jaya (Table 1). As anthropogenic grassland at Laman Satong was succeeded by native rainforest (Figure 2(a) and (b)), bird species richness increased by 94% from 2011 to 2016 (from 36 to 70 species, Figure 3(a)), despite the limited scale of reforestation (<8 ha planted per year and <20 ha maximum extent). Annual increases in species richness were initially high (67% from 2011 to 2012), then declined due to the 2013 fire (−47% from 2012 to 2013) before rising again (59% from 2013 to 2014, average of 17% per year from 2014 to 2016). At the less degraded Sedahan Jaya site, species richness increased by 29% over a 3-year period beginning shortly after planting (from 49 to 63 species, Figure 3(b)), as early successional Macaranga groves and bracken fern began to mature into more diverse rainforest. Annual increases ranged from 4% (2013–2014) to 11% per year (average from 2014 to 2016). Across both sites and excluding the decline due to fire at Laman Satong, species richness increased by an average of 27 (±23, n = 7)% per year.

Table 1.

Birds Observed at Two Reforestation Sites in Gunung Palung National Park, West Kalimantan, Indonesian Borneo.

Family	Species	Common Name	Laman Satong						Sedahan Jaya			IUCN status	Feeding guild
Family	Species	Common Name	2009	2011	2012	2013	2014	2016	2013	2014	2016	IUCN status	Feeding guild
Ardeidae	Ardea alba	Great Egret	–	–	–	–	–	–	X	X	X	LC	P
	Ardea intermedia	Intermediate Egret	–	–	–	–	–	–	X	X	X	LC	P
	Butorides striata	Little Heron	–	–	–	–	–	–	–	X	X	LC	P
	Egretta garzetta	Little Egret	–	–	–	–	–	–	X	X	–	LC	P
	Ixobrychus cinnamomeus	Cinnamon Bittern	–	–	–	–	–	–	X	–	–	LC	P
Accipitridae	Accipiter gularis	Japanese Sparrowhawk	–	–	–	–	X	X	–	–	–	LC	R
	Ictinaetus malaiensis	Black Eagle	–	–	X	–	–	–	–	–	–	LC	R
	Pernis ptilorhynchus	Oriental Honey Buzzard	–	X	X	–	–	X	–	–	–	LC	R
	Spilornus cheela	Crested Serpent Eagle	–	–	X	–	–	X	–	–	X	LC	R
Rallidae	Amaurornis cinerea	White-browed Crake	–	–	X	–	–	–	–	X	X	LC	P
	Amaurornis phoenicurus	White-breasted Waterhen	–	X	X	–	–	X	X	X	X	LC	P
Columbidae	Chalcophaps indica	Common Emerald Dove	–	X	X	–	X	X	–	X	X	LC	TF
	Macropygia ruficeps	Little Cuckoo-dove	–	X	X	–	–	X	–	–	X	LC	ArF
	Spilopelia chinensis	Spotted Dove	–	–	X	–	X	X	X	–	X	LC	TF
	Treron curvirostra	Thick-billed Green Pigeon	–	–	X	–	–	X	–	–	–	LC	ArF
	Treron vernans	Pink-necked Green Pigeon	–	X	X	–	X	X	–	X	X	LC	ArF
Cuculidae	Cacomantis merulinus	Plaintive Cuckoo	X	X	X	X	X	X	X	X	X	LC	ArI
	Cacomantis sepulcralis	Rusty-breasted Cuckoo	–	–	–	–	X	X	X	X	X	LC	ArI
	Cacomantis sonneratii	Banded Bay Cuckoo	–	–	X	X	X	X	X	X	X	LC	ArI
	Centropus bengalensis	Lesser Coucal	–	–	–	–	X	X	X	X	X	LC	TI
	Centropus sinensis	Greater Coucal	–	X	X	X	X	X	X	X	X	LC	TI
	Cuculus micropterus	Indian Cuckoo	–	–	X	X	X	X	X	X	X	LC	ArI
	Phaenicophaeus curvirostris	Chestnut-breasted Malkoha	–	–	–	–	–	–	–	–	X	LC	ArI
	Surniculus lugubris	Square-tailed Drongo-cuckoo	–	–	–	–	–	X	X	X	X	LC	ArI
Strigidae	Otus rufescens	Reddish Scops Owl	–	–	–	X	X	X	–	–	–	NT	R
Caprimulgidae	Caprimulgus macrurus	Large-tailed Nightjar	–	X	X	–	–	X	–	–	–	LC	AeI
Hemiprocnidae	Hemiprocne longipennis	Grey-rumped Treeswift	–	–	–	–	X	X	–	X	X	LC	AeI
Apodidae	Aerodramus fuciphagus	Edible-nest Swiftlet	–	–	–	–	X	X	X	X	X	LC	AeI
	Aerodramus maxima	Black-nest Swiftlet	–	–	–	–	–	X	X	X	X	LC	AeI
	Aerodramus salangana	Mossy-nest Swiftlet	–	–	–	–	–	X	X	X	X	LC	AeI
	Apus nipalensis	House Swift	–	–	X	X	X	X	X	X	X	LC	AeI
	Collocalia esculenta	Glossy Swiftlet	–	X	X	X	X	X	X	X	X	LC	AeI
	Cypsiurus balasiensis	Asian Palm Swift	–	–	–	–	–	–	X	X	X	LC	AeI
Coraciidae	Eurystomus orientalis	Oriental Dollarbird	–	X	X	X	X	X	–	–	–	LC	SI
Alcedinidae	Alcedo meninting	Blue-eared Kingfisher	–	–	–	–	–	–	X	–	–	LC	P
	Halcyon coromanda	Ruddy Kingfisher	–	–	–	–	–	–	–	–	X	LC	P
	Pelargopsis capensis	Stork-billed Kingfisher	–	X	X	–	–	–	–	X	X	LC	P
	Todiramphus chloris	Collared Kingfisher	–	–	–	–	–	–	–	–	X	LC	P
Meropidae	Merops philippinus	Blue-tailed Bee-eater	–	–	–	–	–	–	–	–	X	LC	SI
	Merops viridis	Blue-throated Bee-eater	–	X	X	X	–	X	X	X	X	LC	SI
Bucerotidae	Aceros corrugatus	Wrinkled Hornbill	–	–	–	–	–	–	X	–	X	NT	ArF
	Anthracoceros albirostris	Oriental Pied Hornbill	–	–	X	–	X	X	X	X	X	LC	ArF
	Anthracoceros malayanus	Black Hornbill	–	–	–	–	–	–	X	X	X	NT	ArF
	Buceros rhinoceros	Rhinoceros Hornbill	–	–	X	X	X	X	X	X	X	NT	ArF
	Rhyticeros undulatus	Wreathed Hornbill	–	–	X	X	X	X	X	–	X	LC	ArF
Megalaimidae	Megalaima rafflesii	Red-crowned Barbet	–	X	X	X	X	X	–	–	–	NT	ArIF
	Psilopogon chrysopogon	Golden-whiskered Barbet	–	–	–	X	X	X	X	X	X	LC	ArF
	Psilopogon duvaucelii	Blue-eared Barbet	–	–	X	X	X	X	X	X	X	LC	ArF
	Psilopogon mystacophanos	Red-throated Barbet	–	X	X	X	X	X	–	–	–	NT	ArF
Picidae	Micropternus brachyurus	Rufous Woodpecker	–	–	–	–	–	–	–	X	X	LC	BSI
Falconidae	Microhierax fringillarius	Black-thighed Falconet	–	–	X	–	X	X	–	–	–	LC	SI
Pisttaculidae	Loriculus galgulus	Blue-crowned Hanging Parrot	–	X	X	–	–	–	–	–	–	LC	ArF
	Psittacula longicauda	Long-tailed Parakeet	–	X	X	–	–	–	X	–	–	NT	ArF
	Psittinus cyanurus	Blue-rumped Parrot	–	–	X	–	–	–	–	–	–	NT	ArF
Eurylaimidae	Calyptomena viridis	Green Broadbill	–	–	–	–	–	–	X	X	X	NT	ArF
	Eurylaimus javanicus	Banded Broadbill	–	–	–	–	–	–	X	X	X	NT	SGI
	Eurylaimus ochromalus	Black-and-yellow Broadbill	–	–	–	X	X	X	X	X	X	NT	SGI
Pittidae	Erythropitta granatina	Garnet Pitta	–	–	–	–	–	–	X	X	X	NT	TI
	Hydrornis baudii	Blue-headed Pitta	–	–	–	–	–	–	X	X	X	VU	TI
	Pitta sordida	Hooded Pitta	–	X	X	–	–	–	–	–	–	LC	TI
Tephrodornithidae	Hemipus hirundinaceus	Black-winged Flycatcher-shrike	–	–	X	–	X	X	–	–	–	LC	SI
Artamidae	Artamus leucorynchus	White-breasted Woodswallow	X	X	X	–	–	–	X	–	–	LC	AeI
Campephagidae	Pericrocotus speciosus	Scarlet Minivet	–	–	–	–	–	–	X	–	X	LC	ArI
Laniidae	Lanius cristatus	Brown Shrike	–	–	–	–	–	X	–	–	–	LC	SGI
	Lanius schach	Long-tailed Shrike	X	–	–	–	–	–	–	–	–	LC	SGI
Dicruridae	Dicrurus paradiseus	Greater Racket-tailed Drongo	–	X	X	X	X	X	–	X	X	LC	SGI
Rhipiduridae	Rhipidura javanica	Malaysian Pied Fantail	–	–	X	X	X	X	–	X	X	LC	SI
	Rhipidura perlata	Spotted Fantail	–	–	X	–	–	X	–	–	–	LC	SI
Corvidae	Corvus enca	Slender-billed Crow	–	X	X	X	X	X	X	X	X	LC	ArI
	Platylophus galericulatus	Crested Jay	–	–	X	–	–	X	–	X	X	NT	ArI
Stenostiridae	Culicicapa ceylonensis	Grey-headed Canary-flycatcher	–	–	–	–	–	X	–	–	–	LC	SI
Pycnonotidae	Alophoixus bres	Grey-cheeked Bulbul	–	X	X	–	X	X	–	–	X	LC	ArIF
	Alophoixus phaeocephalus	Yellow-bellied Bulbul	–	X	X	X	X	X	X	X	X	LC	ArIF
	Pycnonotus atriceps	Black-headed Bulbul	–	–	–	–	–	X	–	X	–	LC	ArIF
	Pycnonotus brunneus	Asian Red-eyed Bulbul	–	X	X	X	X	X	–	–	–	LC	ArIF
	Pycnonotus goiavier	Yellow-vented Bulbul	X	X	X	X	X	X	X	X	X	LC	ArIF
	Pycnonotus plumosis	Olive-winged Bulbul	–	–	X	–	X	X	X	–	X	LC	ArIF
Hirundinidae	Hirundo rustica	Barn Swallow	–	–	–	–	–	–	–	X	X	LC	AeI
	Hirundo tahitica	Pacific Swallow	–	X	X	X	X	X	X	X	X	LC	AeI
Cisticolidae	Orthotomus ruficeps	Ashy Tailorbird	–	X	X	X	X	X	–	–	–	LC	ArI
	Orthotomus sericeus	Rufous-tailed Tailorbird	–	X	X	X	X	X	X	X	X	LC	ArI
	Prinia flaviventris	Yellow-bellied Prinia	X	X	X	X	X	X	X	X	X	LC	ArI
Timaliidae	Macronous bornensis	Bold-striped Tit-babbler	X	X	X	–	X	X	–	–	–	LC	ArI
	Stachyris maculata	Chestnut-rumped Babbler	–	–	X	X	X	X	–	–	–	NT	ArI
Pellorneidae	Pellorneum capistratum	Black-capped Babbler	–	–	–	–	–	X	–	–	–	LC	TI
Irenidae	Irena puella	Asian Fairy-bluebird	–	X	X	–	X	X	–	X	X	LC	ArF
Sturnidae	Gracula religiosa	Common Hill Myna	–	X	X	X	X	X	X	X	X	LC	ArF
Muscicapidae	Copsychus saularis	Oriental Magpie-robin	–	–	–	–	X	–	–	–	–	LC	SI
	Cyornis umbratilis	Grey-chested Jungle Flycatcher	–	X	X	–	–	X	–	–	–	NT	SI
Chloropseidae	Chloropsis cochinchinensis	Blue-winged Leafbird	–	–	X	–	X	X	–	–	–	NT	NIF
	Chloropsis sonnerati	Greater Green Leafbird	–	X	–	–	X	X	–	–	–	VU	NIF
Dicaeidae	Dicaeum chrysorrheum	Yellow-vented Flowerpecker	–	–	X	–	–	X	–	–	–	LC	NIF
	Dicaeum cruentatum	Scarlet-backed Flowerpecker	–	–	X	–	–	X	–	–	–	LC	NIF
	Dicaeum trigonostigma	Orange-bellied Flowerpecker	–	–	X	X	X	X	X	X	X	LC	NIF
Nectariniidae	Aethopyga siparaja	Crimson Sunbird	–	–	–	–	X	X	–	–	–	LC	NI
	Anthreptes malacensis	Brown-throated Sunbird	–	X	X	X	X	X	X	–	X	LC	NI
	Anthreptes simplex	Plain Sunbird	–	–	–	–	–	X	–	–	–	LC	NIF
	Arachnothera longirostra	Little Spiderhunter	–	–	X	X	X	X	X	X	X	LC	NI
Estrildidae	Lonchura atricapilla	Chestnut Munia	X	X	X	–	–	X	X	–	X	LC	TF
	Lonchura fuscans	Dusky Munia	X	X	X	X	X	X	X	X	X	LC	TF
	Lonchura leucogastra	White-bellied Munia	–	–	–	–	X	–	–	–	–	LC	TF
Total			8	36	60	32	51	70	49	51	63

Feeding guilds: AeI = aerial insectivore; ArF = arboreal frugivore; ArI = arboreal gleaning insectivore; ArIF = arboreal gleaning insectivore/frugivore; BSI = bark-searching insectivore; NI = nectarivore/insectivore; NIF = nectarivore/insectivore/frugivore; P = piscivore; R = raptor; SGI = sallying gleaning insectivore; SI = sallying insectivore; TF = terrestrial frugivore; TI = terrestrial insectivore.

Figure 2.

Vegetation recovery at Laman Satong. (a) Before planting, the site was dominated by fire-tolerant grasses and ferns that impeded forest succession. (b) After several years of planting and fire prevention, unburnt areas were covered in young secondary forest.

Figure 3.

Bird species richness increased following reforestation efforts at (a) Laman Satong and (b) Sedahan Jaya. Open circles and dotted line show species richness. Solid circles and line show the area planted with native seedlings over the preceding year, and bars show cumulative reforested area at the time of the bird surveys. The 2013 dip in (a) is from a wildfire that burned most of the site.

The fire in 2013 at Laman Satong interrupted recovery and resulted in the disappearance of nearly half the observed bird species. The bird community recovered quickly, however, as unburnt forest continued to mature, surviving trees regrew, and new areas were planted. Just 3 years after the fire, species richness had surpassed its prefire peak in 2012 by 17% (70 vs. 60 species). Bird species richness initially tracked reforested area but then continued to rise despite lower planting rates and reforested area in postfire years. There was thus no relationship between species richness and reforested area (p = .42, r² = .22, n = 5) or site age (p = .24, r² = .42, n = 5), even when combining surveys from both sites (reforested area p = .33, r² = .16, n = 8; site age p = .28, r² = .19, n = 8). Recovery was instead a function of fire incidence and the resulting successional stage of the site.

Discussion

Reforestation can provide rapid benefits to native bird communities in Borneo. Our reforestation sites saw rises in bird species richness of up to 94% within a few years, with average annual increases of 27% in nonfire years. Final species richness estimates were comparable to those in 20-year-old secondary forests elsewhere in Borneo (Edwards et al., 2009), despite our sites being three orders of magnitude smaller (<20 vs. >10,000 ha). The rise in species richness is accompanied by other indicators of restoration success. Older trees at the sites regularly flower and produce fruits, and seedlings now germinate naturally from seeds dispersed by birds or primates. Feeding guild composition of the most recent surveys approached that of forest or mixed forest/agricultural bird communities at other tropical sites, with a predominance of insectivores and frugivores (Maas et al., 2016). Finally, in addition to birds, several mammals have been photographed at the sites, including orangutans at Sedahan Jaya. These positive responses were maintained despite temporary setbacks from a fire at one site, thanks to the protection of unburnt patches, regrowth of surviving trees, intensified fire prevention, and regular planting. Degraded and unused landscapes in Borneo can thus be restored to habitat for many native species, provided they receive appropriate long-term maintenance and protection from fire.

While rapid recovery of the bird community is heartening, it is worth noting that our sites contained fewer than the >200 species expected from intact primary rainforest (Edwards et al., 2009; Lambert & Collar, 2002), and not all the birds were forest specialists. We detected only two Borneo endemics (blue-headed Pitta Hydrornis baudii and the abundant generalist Dusky Munia Lonchura fuscans, compared to > 50 endemics across the island, Phillips & Phillips, 2009), and only two species of conservation concern (blue-headed Pitta and Greater Green Leafbird Chloropsis sonnerati, both listed as vulnerable). The sites also benefited from being in a nationally protected area and from bordering primary forest that served as a source of dispersing migrants. Our results may not hold for sites that are located far from natural forest remnants or are not strictly protected, or for threatened or endemic birds. Likewise, our failure to detect area effects on species richness may be an artifact of small size, lack of isolation, or presence of fire at our sites. Area effects may be more apparent at regional or landscape scales (Pei et al., 2018), in more isolated sites (Stratford & Stouffer, 2015), or in areas less impacted by fire. We thus emphasize the importance of protecting Borneo's remnant primary forests and suggest that reforestation is best viewed as a valuable supplement to the creation of protected areas.

Footnotes

Acknowledgments

We thank the Republic of Indonesia and local communities for allowing us to work in Gunung Palung National Park. T. Bishop at the Cornell Lab of Ornithology provided access to audio files and other resources for bird identification. E. Besozzi, M. Dantzler-Kyer, and one anonymous reviewer provided helpful comments that improved the manuscript.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This project was conducted as part of a reforestation program by Yayasan Alam Sehat Lestari (ASRI), with financial assistance from Health In Harmony, the Arcus Foundation, Disney Conservation Fund, Ford Foundation, USAID, U.S. Fish and Wildlife Service, and WWF.

References

Chazdon

R. L.

(2008) Beyond deforestation: Restoring forests and ecosystem services on degraded lands. Science 320: 1458–1460.

Chazdon, R. L., Peres, C. A., Dent, D., Sheil, D., Lugo, A. E., Lamb, D., … Miller, S. E. (2009). The potential for species conservation in tropical secondary forests. Conservation Biology, 23, 1406–1417.

Corlett

R. T.

(2014) The ecology of tropical East Asia, 2nd ed. Oxford, England: Oxford University Press.

Curran

L. M.

Trigg

S. N.

McDonald

A. K.

Astiani

Hardiono

Y. M.

Siregar

Kasischke

(2004) Lowland forest loss in protected areas of Indonesian Borneo. Science 303: 1000–1003.

Damayanti, E. K., & Prasetyo, L. B. (2015, September 7–11). Driver, pressure, state, impact, and response in the forest transition of Indonesian Borneo. Paper presented at the XIV World Forestry Congress, Durban, South Africa.

Edwards

D. P.

Ansell

F. A.

Ahmad

A. H.

Nilus

Hamer

K. C.

(2009) The value of rehabilitating logged rainforest for birds. Conservation Biology 23: 1628–1633.

Fitzherbert

E. M.

Struebig

M. J.

Morel

Danielsen

Brühl

C. A.

Donald

P. F.

Phalan

(2008) How will oil palm expansion affect biodiversity?. Trends in Ecology and Evolution 23: 538–545.

Garrity

D. P.

Soekardi

van Noordwijk

de la Cruz

Pathak

P. S.

Gunasena

H. P. M.

Majid

N. M.

(1997) The Imperata grasslands of tropical Asia: Area, distribution, and typology. Agroforestry Systems 36: 3–29.

International Tropical Timber Organization. (1990, May 16–23). Rehabilitation of logged-over forests in Asia/Pacific region. Paper presented at the Permanent Committee on Reforestation and Forest Management, Sixth Session, Denpasar, Bali.

10.

International Union for Conservation of Nature. (2017). The IUCN red list of threatened species. Retrieved from http://www.iucnredlist.org.

11.

Kettle

C. J.

Ghazoul

Ashton

Cannon

C. H.

Chong

Diway

Burslem

D. F. R. P.

(2011) Seeing the fruit for the trees in Borneo. Conservation Letters 4: 184–191.

12.

Kuusipalo

Ådjers

Jafarsidik

Otsamo

Tuomela

Vuokko

(1995) Restoration of natural vegetation in degraded Imperata cylindrica grassland: Understorey development in forest plantations. Journal of Vegetation Science 6: 205–210.

13.

Lack

D. L.

(1933) Habitat selection in birds. With special reference to the effects of afforestation on the Breckland avifauna. Journal of Animal Ecology 2: 239–262.

14.

Lambert

F. R.

(1992) The consequences of selective logging for Bornean lowland forest birds. Philosophical Transactions of the Royal Society B 335: 443–457.

15.

Lambert

F. R.

Collar

N. J.

(2002) The future for Sundaic lowland forest birds: Long-term effects of commercial logging and fragmentation. Forktail 18: 127–146.

16.

Maas

Karp

D. S.

Bumrungsri

Darras

Gonthier

Huang

J. C.-C.

Williams-Guillén

(2016) Bird and bat predation services in tropical forests and agroforestry landscapes. Biological Reviews 91: 1081–1101.

17.

Margono

B. A.

Potapov

P. V.

Turubanova

Stolle

Hansen

M. C.

(2014) Primary forest cover loss in Indonesia over 2000–2012. Nature Climate Change 4: 730–735.

18.

Meyers

(2009) Birds of Borneo: Brunei, Sabah, Sarawak, and Kalimantan, Princeton, NJ: Princeton University Press.

19.

Myers

Mittermeier

R. A.

Mittermeier

C. G.

da Fonseca

G. A. B.

Kent

(2000) Biodiversity hotspots for conservation priorities. Nature 403: 853–858.

20.

Niklasson, M. A. (2013). Aves Vox, iOS application. Retrieved from http://avesvoxapp.com/.

21.

Normile

(2009) Restoring a ‘Biological Desert’ on Borneo. Science 325: 557.

22.

Ohta

(1990) Influence of deforestation on the soils of the Pantabangan Area, Central Luzon, the Philippines. Soil Science and Plant Nutrition 36: 561–573.

23.

Pei

Wang

Jin

Jia

Chen

Qie

Zhang

(2018) Long-term afforestation efforts increase bird species diversity in Beijing, China. Urban forestry & Urban Greening 29: 88–95.

24.

Phillips

(2009) Phillipps' field guide to the Birds of Borneo: Sabah, Sarawak, Brunei and Kalimantan, Oxford, England: Beaufoy.

25.

Pohnan

Ompusunggu

Webb

(2015) Does tree planting change minds? Assessing the use of community participation in reforestation to address illegal logging in West Kalimantan. Tropical Conservation Science 8: 45–57.

26.

R Core Team (2012) R: A language and environment for statistical computing, Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org.

27.

Scharringa

(2005) Birds of tropical Asia 3: Sounds and sights [CD-ROM], Westernieland, The Netherlands: Birds Songs International.

28.

Shi

W. T.

(2012) A Naturalist's guide to the Birds of Borneo: Sabah, Sarawak, Brunei and Kalimantan, Oxford, England: Beaufoy.

29.

Stratford

J. A.

Stouffer

P. C.

(2015) Forest fragmentation alters microhabitat availability for neotropical terrestrial insectivorous birds. Biological Conservation 188: 109–115.

30.

Takano

K. T.

Nakagawa

Itioka

Kishimoto-Yamada

Yamashita

Tanaka

H. O.

Sakai

(2014) The extent of biodiversity recovery during reforestation after swidden cultivation and the impacts of land-use changes on the biodiversity of a tropical rainforest region in Borneo. In: Sakai

Umetsu

(eds) Social-ecological systems in transition, global environmental studies, Tokyo, Japan: Springer Japan, pp. 27–49.

31.

Wuethrich

(2007) Reconstructing Brazil's Atlantic rainforest. Science 315: 1070–1072.

32.

Yassir

van der Kamp

Buurman

(2010) Secondary succession after fire in Imperata grasslands of East Kalimantan, Indonesia. Agriculture, Ecosystems and Environment 137: 172–182.

33.

Zamzani

Onda

Yoshino

Masuda

(2009) Deforestation and agricultural expansion processes in Gunung Palung National Park, West Kalimantan, Indonesia. Jurnal Manajemen Hutan Tropika 15: 24–31.