Birds of the Man and Biosphere Reserve of Luki , Bas-Congo province , Democratic Republic of Congo

1 University of Kinshasa, Unit of Animal Production and Health, Nature Conservation and Development, Department of Biology, Faculty of Science, P.O. Box 218 Kinshasa XI, Democratic Republic of Congo 2 University of Kansas, Biodiversity Institute and Department of Ecology and Evolutionary Biology, 1345 Jayhawk Blvd., Lawrence, KS, 66045, USA 3 American Museum of Natural History, Department of Ornithology, Central Park West at 79th St., New York, NY, 10024, USA 4 Current address: University of New Mexico, Department of Biology and Museum of Southwestern Biology, MSC03 2020, 1 University of New Mexico, Albuquerque, NM 87131, USA 5 Field Museum of Natural History, Science and Education, 1400 South Lake Shore Drive, Chicago, IL, 60605, USA 6 Université Officielle de Bukavu, Faculty of Science, Department of Biology, Bukavu, B.P. 570, Democratic Republic of the Congo * Corresponding author. E-mail: mjandersen@unm.edu


INTRODUCTION
The Democratic Republic of Congo (DRC), the largest country in Sub-Saharan Africa, holds a highly diverse avian fauna owing to its vast land area and variety of habitats present.A total of ~1100 bird species is known to occur in the country distributed among the moist lowland evergreen forests, semi-evergreen forests, and swamp-forests of the Congo Basin in the northern half of the country; savannas north and south of the these Congo Basin forests; grasslands and montane forests of the Albertine Rift highlands in the country's eastern region; and dry forests and miombo woodland on the Katanga plateau in the southeast (Demey and Louette 2001).A network of 29 protected areas consisting of 7 parks and 22 reserves has been established in the country but detailed ornithological work in these protected areas is largely absent (Inogwabini et al. 2005).Efforts have been made to describe the ecology of some species (Kisasa and Aloni 2011;Kisasa 2012aKisasa , 2012b) but more comprehensive monitoring and research programs are required to guide management strategies in these protected areas (Struhsaker et al. 2005).
The Man and Biosphere (MAB) Reserve of Luki (hereafter, Luki), established in 1979, encompasses 327 km 2 of lowland forest that forms part of the Mayombe forest patch near the DRC's Atlantic coast (Figure 1).Situated in the Luki River basin, the reserve has a rolling topography ranging between 100-500 m above sea level and consists of a variety of habitats, including mature and young secondary forest, gallery forest, wooded savanna, secondary bush, and cultivated area (Figure 2).The reserve receives an annual rainfall of 1,155-1,818 mm, mostly during the months of October to April (Pendje and Baya 1992;Mutambue 1996;Demey and Louette 2001).Detailed information on the birds of Luki is lacking, because no ornithological survey has been conducted in the area.Demey and Louette (2001) created a provisionary list of 136 biome-restricted species known from the Mayombe forest that they expected to be present at Luki.Based on this list, the Luki Forest Reserve Important Bird Area meets Birdlife International's A3 criteria for biome-restricted species, which states that, "the site is known or thought to hold a significant component of the group of species whose distributions are largely or wholly confined to one biome" (Birdlife International 2015).In this paper we open areas receiving more frequent visits.The weather was seasonably cool and dry during the study period with the exception of one period of light drizzle on 28 June 2012.We prepared 177 specimens of 50 species as dried study skins or preserved whole in 10% formaldehyde.We collected ~0.05 g of pectoral muscle tissue from document the first detailed field survey of birds from the MAB Reserve of Luki based on collected specimens, photographs, audio recordings, and direct observations.

MATERIALS AND METHODS
We assembled a detailed list of birds at the MAB Reserve of Luki based on a collection of specimens, audio recordings, and direct observations made from 23-30 June 2012, and from 12-16 July 2013.We were based at the office and residence of the World Wide Fund for Nature at Luki (05.62150° S, 013.09819°E, 300 m above sea level).We consulted Sinclair and Ryan (2010) and Borrow and Demey (2001) for species identification and the Birds of Africa series (Fry et al. 1982(Fry et al. -2004) ) for status and distribution information.In this paper, we follow the taxonomy of Clements et al. (2012).
To collect specimens we used 34 12 m × 2.5 m mist nets that we installed in primary forest, forest edge, grassland, and garden habitat in 11 different locations in the reserve's core and buffer zones (Table 1; Figure 1).We carried out 164.5 net-days of netting effort (nets were open from approximately 06:00-17:00 h during the day).We visited nets 3-5 times each day, with nets in    (accession nos. 120773-120774, 120781-120803, 120868-120881, 120900-120902, 120923-120934, 120939, 120941-120942, 120945-120953, 120991-121050), and specimens from the 2013 survey are deposited at the Field Museum of Natural History, Chicago, Ilinois, USA.MJA conducted daily bird observations for a total of 31.75 hours during the 2012 survey work.All observations are freely available on-line through eBird (http://ebird.org).MJA recorded bird vocalizations from 27 species using a Nagra ARES-BB+ with a Sennheiser ME62 omnidirectional microphone mounted in a Telinga Universal parabolic reflector.All recordings are archived in the Macaulay Library at the Cornell Laboratory of Ornithology, Ithaca, New York, U.S.A and are available on-line at (http://macaulaylibrary.org).

RESULTS AND DISCUSSION
We recorded 136 species belonging to 96 genera, distributed among 37 families and eight orders (Table 2; Figures 3-8).Most species recorded were expected to occur in Luki (Demey and Louette 2001).As expected for the month of June, we did not encounter any boreal migrants.Knowledge about intra-African bird migration in the area is poor so we avoid speculating whether our records include intra-African migrants.
We obtained new southernmost records for four species based on known distribution information from the Birds of Africa, Volumes 1-7 (Fry et al. 1982(Fry et al. -2004) ) and Pedersen (2010).These range extensions include sightings of the following species: Aquila africana (Cassin, 1865); Columba iriditorques Cassin, 1856; Platysteira tonsa (Bates, 1911); and Malimbus erythrogaster Reichenow, 1893.Aquila africana and C. iriditorques were presumed to occur at Luki (Demey and Louette 2001), but no records existed prior to our work.Aquila africana is widespread and C. iriditorques is known from Gabon and the Congo Basin, but not from Bas-Congo province; thus, their presence at Luki is unsurprising.Platysteira tonsa and M. erythrogaster have not previously been recorded south of Gabon or northeastern DRC, and they were not previously suspected to occur at Luki (Demey and Louette 2001).
Evidence of breeding, observed in a total of 23 species, is summarized in Table 2.We observed juvenile birds of 19 species, indicating that late June marks the tail end of at least one breeding season at Luki.This timeframe coincides with the end of the October-April rainy season (Demey and Louette 2001), during which we suspect much breeding occurs.We noted this both with net-captured juvenile birds (age identified by plumage or the presence of bursa of Fabricius) and through observation of family groups in the forest.However, we also noted enlarged gonads in two species [Pogoniulis subsulphureus (Fraser, 1843) and Campethera caroli (Malherbe, 1852)], birds performing mating displays (Smithornis rufolateralis G.R. Gray, 1864), and an active breeding colony of Gymnobucco calvus (Lafresnaye, 1841), indicating that some species breed in the area in June.
Of the 136 species identified in our survey, only Psittacus erithacus Linnaeus, 1758, which occurs in the forests of Central Africa, is considered globally threatened due to heavy trapping for the pet trade ("Vulnerable," Birdlife International 2013).Cossypha heinrichi A. Smith, 1840 ("Vulnerable") is the only other threatened species that may be present (Fry et al. 1997), but we did not detect it.Three raptor species, Polemaetus bellicosus (Daudin, 1800; "Vulnerable"), Terathopius ecaudatus (Daudin, 1800; "Near-threatened"), and Stephanoaetus coronatus (Linnaeus, 1766; "Nearthreatened"), and the flycatcher Muscicapa tessmanni (Reichenow, 1907; "Data deficient"), were not recorded, but they may also be present at Luki (Brown 1982;Erard et al. 2002).On a local scale, Luki's avifauna is threatened by deforestation and trapping, issues that need to be addressed by all concerned stakeholders.This work represents a preliminary list of the avifauna of the Luki reserve.Coincidentally, our full list of 136 species is precisely the number of biome-restricted species predicted to occur at Luki by Demey and Louette (2001).However, we believe that our study likely overlooked some resident species because we covered only a small area of the reserve and our survey's duration was brief.Further surveys are recommended throughout the reserve, especially focused in the interior of the larger core Zone A (Figure 1).We advise additional surveys should be done at various times of year to maximize observations of boreal and intra-African migrant species, as well as to further document seasonal life history strategies of birds such as breeding, molt, and migration.Although incomplete, this list serves as a baseline with which to compare future bird surveys in the reserve.

Dwarf Kingfisher
One observed in primary forest.White-crested Hornbill Uncommon.Several seen foraging at the periphery of mixed-species flocks in forest.

Tockus camurus Cassin, 1857
Red-billed Dwarf Hornbill Fairly common.Seen most days in groups of 1-6 individuals.Always associated with mixed-species foraging flocks.
Tockus fasciatus (Shaw, 1812) African Pied Hornbill Common.Seen daily in forest edge at camp and throughout forest, especially in secondary, mayombe-like forest.Usually seen in large groups of 10-22 individuals, but some small groups (3-7) seen, as well.

Verreaux, 1851
Yellow-billed Barbet Fairly common.Heard often, but rarely seen throughout forest.
Gymnobucco calvus § (Lafresnaye, 1841) Naked-faced Barbet Fairly common in forest edge near camp.One breeding colony observed with upwards of 14 individuals.MJA observed one individual Gymnobucco that showed characters inconsistent with G. calvus.It was associating with the G. calvus colony and appeared dark-billed with erect feather tufts at the maxilla (calvus is pale-billed and lacks dense feather tufts above the bill), but the face pattern was not well seen, nor was overall plumage color noted.The two dark-billed Gymnobucco species (G.sladeni Ogilvie-Grant, 1907 andG. bonapartei, Hartlaub, 1854) are not known from the study region, but both are known to occur in G. calvus breeding colonies (Short and Horne 1988a).Given the uncertainty of this sighting, we remain cautious about interpreting this as anything but an unidentified Gymnobucco.
Pogoniulus scolopaceus (Bonaparte, 1850) Speckled Tinkerbird Fairly common, seen most days in small numbers (1-3).One individual with red irides collected.African Piculet Uncommon.Upwards of two birds noted in stream-edge vegetation along the transition between primary and mayombe-like forest.

Gabon Woodpecker
One bird observed in primary forest.

Dendropicos xantholophus Hargitt, 1883
Golden-crowned Woodpecker Uncommon.Singles seen three times.Observed foraging in the understory at forest edge, associated with mixed-species flocks.

Dendropicos elliotii (Cassin, 1863)
Elliot's Woodpecker One bird observed at edge of primary forest, associated with mixed-species flock.

Psittacus erithacus Linnaeus, 1758
Gray Parrot Fairly common.Upwards of three pairs were observed daily flying over camp heading to a presumed roosting site.

Order pAssEriFOrmEs Family Eurylaimidae
Smithornis rufolateralis* † § G.R. Gray, 1864 Rufous-sided Broadbill Fairly common.Several males observed giving display sallies in primary forest.Platysteira tonsa (Bates, 1911) White-spotted Wattle-eye One pair seen once foraging with mixed-species flock in understory of primary forest edge by MJA.The birds were easily distinguished and immediately recognizable from P. castanea based on the small, but distinct, white post-ocular spot and the female's white malar.They were observed within 0.5 km of camp.P. tonsa has a disjunct distribution in the Lower Guinea Forest and northeastern DR Congo with an isolated population in the Congo Basin at Salonga National Park.Erard and Fry (1997) suggest it is probably more widespread, especially in the Congo Basin.

Batis minor Erlanger, 1901
Black-headed Batis One bird observed in gardens near the camp clearing.

Family malaconotidae
Dryoscopus senegalensis (Hartlaub, 1857) Red-eyed Puffback Uncommon.Singles observed twice, and one pair observed once in secondary forest and edge.

Family campephagidae
Campephaga petiti Oustalet, 1884 Petit's Cuckooshrike Four birds (two males, two females) seen once in a mixed-species canopy flock at primary forest edge near camp clearing.

Campephaga quiscalina Finsch, 1869
Purple-throated Cuckooshrike Singles seen twice in mixed-species canopy flocks at primary forest edge near camp clearing.

Cyanograucalus azureus (Cassin, 1852)
Blue Cuckooshrike Two individuals seen in canopy at transition between primary forest and secondary, mayombe-like forest.Loosely associated with mixedspecies canopy flock.

Family Oriolidae
Oriolus brachyrhynchus Swainson, 1837 Western Black-headed Oriole Common.Seen daily in numbers ranging from 1-8 individuals.Usually associated with mixed-species flocks.

Oriolus nigripennis J. Verreaux & E. Verreaux, 1855
Black-winged Oriole One individual seen in a mixed-species flock at forest edge near the camp clearing.

Family corvidae Corvus albus Statius Müller, 1776
Pied Crow One individual seen flying over clearing at camp.

Family Hirundinidae
Cecropis abyssinica* Guérin-Méneville, 1843 Lesser Striped-Swallow Common.Flock of about 50 birds seen daily in clearing at camp.Birds roosted in buildings and they likely nest here, as well, but we did not observe evidence of breeding.

Macrosphenus flavicans* § Cassin, 1859
Yellow Longbill Uncommon in scrubby vegetation at forest edge and clearings.Bursa present in one specimen.

Family cettiidae
Erythrocercus mccallii (Cassin, 1855) Chestnut-capped Flycatcher Fairly common.Seen often in garden in clearing near camp and in secondary, mayombe-like forest, often with mixed-species flocks.

Family cisticolidae
Apalis rufogularis (Fraser, 1843) Buff-throated Apalis Uncommon.Seen twice (a singleton and pair, respectively) associating with mixed-species flocks in the canopy of primary forest.

Figure 1 .
Figure 1.Map of the Man and Biosphere Reserve of Luki showing survey sites and its location in the Democratic Republic of Congo.
Liyandja et al. | Birds of the Man and Biosphere Reserve of Luki, Democratic Republic of Congo Megabyas flammulatus J. Verreaux & E. Verreaux, 1855 African Shrike-flycatcher One individual observed in mayombe-like forest.

Table 1 .
Geographical coordinates of netting locations at the Man andBiosphere Reserve of Luki.
* Locality of the 2013 survey.All other localities are from the 2012 survey.
Liyandja et al. | Birds of the Man and Biosphere Reserve of Luki, Democratic Republic of Congoeach specimen for molecular studies.We noted detailed information on each specimen, including collecting date and locality information, weight, sex, type and measurement of gonads, coloration of soft parts (iris, bill, mouth lining, tarsus, and feet), skull ossification, presence and measurement of bursa of Fabricius, stomach and crop contents, molt condition, and fat condition.

Table 2 .
List of species recorded from the Man and Biosphere Reserve of Luki with notes indicating relative abundance, evidence of breeding, and other noteworthy natural history observations.Relative abundance criteria are as follows: common, observed numerous instances daily (usually >3 individuals); fairly common, observed almost daily; uncommon, observed regularly, but only once every 2-3 days.Birds seen fewer than once every 2-3 days were deemed rare or difficult to detect and are noted as the total number of birds seen during the survey.* Indicates species for which voucher specimens were collected.† Indicates species for which audio recordings were made.§ Indicates species for which evidence of breeding was observed either through mating displays or the presence of juveniles or enlarged gonads.Eagle Two birds were observed once soaring over camp; one adult, one juvenile.The birds were very vocal during the ten-minute observation.Groups of 2-4 seen twice foraging over camp with Apus affinis and Cypsiurus parvus.
Continued Liyandja et al. | Birds of the Man and Biosphere Reserve of Luki, Democratic Republic of Congo The most common tinkerbird.Very vocal throughout forest.Maximum of five seen/heard daily.One specimen with testes enlarged.Indicator sp. was observed in garden clearings around camp, but it was not identified satisfactorily.It had streaked flanks with a dark malar, but small Indicator spp.are difficult to identify in the field based on plumage characters alone, and no vocalizations were noted to aid in identification.At least two species are possible at Luki based on distribution maps (I.exilis and I. conirostris; Short and Horne 1988b), but further survey work is needed to determine which species occurs at Luki.

Table 2 .
Continued.Continued Liyandja et al. | Birds of the Man and Biosphere Reserve of Luki, Democratic Republic of Congo Seen twice (one and two individuals, respectively) in mixed-species foraging flocks in canopy at forest edge.Singles seen three times in mixed-species foraging flocks in canopy at forest edge. in scrubby vegetation at forest edge near camp, otherwise not recorded on bird surveys.Bursa present in one specimen.

Table 2 .
Continued.Continued Liyandja et al. | Birds of the Man and Biosphere Reserve of Luki, Democratic Republic of Congo Seen most days in family groups (n=4 individuals) foraging in canopy associated with mixed-species flocks.Adults of this species are sexually monomorphic and distinct from juveniles, which are overall lemon-yellow below and gray above.One individual white-eye seen twice in a fruiting vine tangle at forest edge near camp.Photographed by MJA.The photos depict a bright yellow bird that lacks the dusky green flanks and back of Z. senegalensis and the distinct yellow lores, of Z. stenocricotus.