OCCURRENCE THRESHOLDS OF AFRICAN ANT-FOLLOWING BIRDS INSIDE AN AGROFORESTRY MOSAIC

Master Thesis by Carolina Maria Ocampo Ariza Born in Bogotá, Colombia September 11th, 1991

Thesis submitted to the Faculty of Biology and Psychology in partial fulfillment of the requirements for the integrated bi-national degree

MASTER OF SCIENCE/ MASTER OF INTERNATIONAL NATURE CONSERVATION (M.SC. / M.I.N.C.)

From the Georg-August-Universität, Göttingen; Germany and Lincoln University, Christchurch; New Zealand

Göttingen, Germany. May 30th, 2017

Carolina María Ocampo-Ariza Beneficiaria Crédito-Beca Colfuturo, Promoción 2015

First Supervisor: PD Dr. Matthias Waltert Workgroup on Endangered Species, Georg-August-Universität Bürgerstr. 50, 37075, Göttingen, Germany

Second Supervisor: PD Dr. Holger Kreft Biodiversity, Macroecology, Conservation, Biogeography Faculty of Forest Sciences and Forest Ecology, Georg-August-Universität Büsgenweg 1, 37077, Göttingen, Germany

German Title: Schwellenwerte im Vorkommen von Ameisen-folgenden Vögeln in einem afrikanischen Agroforst-Mosaik

Day of Announcement: 01.12.2016 Day of Submission: 30.05.2017 Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 2

ACKNOWLEDGEMENTS

I would first like to thank Denis Kupsch who collected and provided the information used in this study and gave me useful feedback throughout the data analysis and writing process. His patience and support to master students have been vital for our study group to continue its research in the tropical forests of Cameroon. I sincerely thank him and ornithologist Francis Njie for their ornithological guidance and for making me fall in love with the avifauna of Korup National Park.

I would like to express my sincere gratitude to my supervisor PD Dr. Matthias Waltert for his help and encouragement in the development of this project. It has been a pleasure to work with a professor with such a wide knowledge and passion of the West-African fauna and their conservation; and even more being able to spend time together in the field. I am also sincerely thankful to my supervisor PD Dr. Holger Kreft, whose comments and constant feedback have helped me improve my skills in ecology, data analysis and even writing.

I would like to thank my friends and fellow MINCs Meagan Selvig, Torben Langer and Jakob Katzenberger, with whom I’ve shared amazing experiences and valuable discussions about diverse conservation issues. I thank my aunt Dr. Ma. Cristina Ocampo for always supporting me in the ups and downs of my studies abroad. Last but not least I would like to thank my parents and my partner César, whose support has been essential for me to stay sane, happy and motivated all throughout my master studies. Thank you for your infinite patience and love.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 3

ABSTRACT

Afrotropical ant-following birds are known to be vulnerable to forest loss and disturbance but occurrence thresholds for these insectivorous species regarding forest cover have never been estimated. I tested the effect of forest cover, landscape and land-use type on the encounter frequency and species richness of ant-following bird communities in Korup National Park and its surrounding area in the Southwest region of Cameroon. I used data of forest cover and of 1812 ant-following bird records obtained through 10-minute point counts at 48 one-km2 sites, across an area of 4,000 km2 that contained three landscapes: Korup National Park, adjacent unprotected agroforestry areas and industrial oil palm plantations. Twenty-six bird species known for their ant- following habits (including occasional and frequent swarm attendants) were detected and classified into ecological groups according to diet (true insectivores, omnivorous and carnivores), preferred foraging stratum and nesting site. Occurrence thresholds in regard to forest cover were calculated using Multiple Additive Regression Splines for the encounter frequency and species richness of the whole community, non-frugivorous species and each of the ecological groups, as well as individual species. Encounter frequency of ant-following birds differed significantly among landscapes and land-use type and the interaction of such factors, while only landscape had a significant effect on the species richness of the community. Species richness declined from ca. 18 spp. in fully forested areas to <=10 spp. in sites with <74% of forest cover. At ca. 80% of forest cover, encounter frequency was reduced to less than 50% compared to fully forested sites (from an average of 40 birds in fully forested areas to 20 birds). Encounter frequency in non-forested sites within oil palm plantations, was limited to only one bird per km2 and detection of only one spp. There was a steady decline of species richness of ca. 1 species with every 7.8% of forest cover lost. The most sensitive species were the fire-crested alethe (A. castanea), with an occurrence threshold estimated at ca. 74% of forest cover; the eastern bearded greenbul (C. chloronotus), the shining drongo (D. atripennis), and the white-tailed ant-thrush (N. poensis), with occurrence thresholds estimated at ca. 52% of forest cover. Species foraging and nesting in the understory were absent below 52 % and 25% of forest cover, respectively; while clear occurrence thresholds were identified for the species richness of ground foragers and ground-nesting species at 52 % and 72 % of forest cover, respectively. This study show that African ant-followers are very sensitive to forest loss from industrial oil palm development. Wildlife-friendly farming systems require substantial proportions of forest cover, probably above 75%, to avoid the loss of these species at the landscape level.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 4

CONTENTS

ACKNOWLEDGEMENTS ...... 3

ABSTRACT ...... 4

LIST OF FIGURES ...... 6

LIST OF TABLES ...... 7

LIST OF ABBREVIATIONS ...... 8

INTRODUCTION ...... 9

METHODS...... 11

1. Study area ...... 11

2. Sampling design ...... 13

3. Data collection ...... 13

4. Data analysis ...... 14

RESULTS...... 16

1. Description of the ant-following bird guild ...... 16

2. Effects of landscape and land-use type on species richness and encounter frequency of

ant-following birds ...... 17

3. Forest cover thresholds for ant-following birds inside a land-use mosaic ...... 18

4. Effect of forest cover change on ecological guilds from ant-following birds ...... 20

DISCUSSION ...... 25

1. Overall response to deforestation ...... 25

2. Differential response of non-frugivorous species and ecological guilds ...... 26

3. Implications for forest management and conservation in Southwest Cameroon ...... 28

CONCLUSIONS ...... 31

REFERENCES ...... 32

APPENDICES ...... 36

APPENDIX 1...... 36

APPENDIX 2...... 37

APPENDIX 3...... 39

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 5

LIST OF FIGURES

Figure 1. Map of the study area around the Korup National Park ...... 12

Figure 2. Mean value and error bars of encounter frequency and species richness of ant- following birds per study plot (1km2) inside the three landscapes found in the study area ...... 17

Figure 3. Encounter frequency and species richness per study site (1km2), in each of the land-use types and landscapes present in the study area ...... 18

Figure 4. Encounter frequency (A, C) and species richness (B, D) of ant-following birds (A, B) and non-frugivorous ant-followers (C, D) in study areas of 1km2 with different forest cover ..... 19

Figure 5. Encounter frequency of individual ant-following bird species in study areas of 1km2 with different proportions of forest cover ...... 21

Figure 6. Encounter frequency of ant-following bird groups with different ecological features in study areas of 1km2 with different percentages of forest ...... 22

Figure 7. Species richness of groups of ant-following birds with different ecological features in study areas of 1km2 with different percentages of forest ...... 23

Appendix 3. Occurrence thresholds for individual ant-following bird species based on percentage forest cover ...... 38

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 6

LIST OF TABLES

Table 1. Encounter frequency of each species found in the survey inside the three landscapes of the study area and differences among landscapes ...... 16

Table 2. Average percentage and standard error (SE) of land-use types found in each of the landscapes in the study area ...... 17

Appendix 1. Summarized table of bird encounter frequency, bird species richness and percentage cover of each land-use type inside each village sampled during the study ...... 36

Appendix 2. Ant-following bird species observed during the bird survey with total number of records in the whole sampling (total encounter frequency) and in each of the studied landscapes ...... 38

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 7

LIST OF ABBREVIATIONS

CEPF Critical Ecosystem Partnership Fund

EARTH Multivariate Additive Regression Splines

calculated through the EARTH for R Studio

Freq. Bird encounter frequency

GLM Generalized linear models

IPP Industrial palm plantations

KNP Korup National Park

K-W Kruskal-Wallis one-way analysis of variance

M-W Mann-Whitney U test

NPF Near-primary forest

OPP Industrial oil palm plantations

Rich. Bird species richness

SF Secondary forest

TP Traditional plantations

UA Unprotected agroforestry areas

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 8

INTRODUCTION

Among the African avifauna, ant-following birds are considered one of the most vulnerable groups to habitat loss and fragmentation (Peters et al., 2008; Waltert et al., 2005). Especially in areas of intensive agricultural use, specialized ant-followers are expected to disappear as a consequence of the impacts of disturbance on terrestrial arthropods (Peters et al., 2008). Species richness of ant- following birds in fragmented forests of East Africa has been linked to the abundance of Dorylus wilverthi and D. molestus ant swarms; whose activity varies according to forest structure and humidity (Peters et al., 2009; Peters & Okalo, 2009). Nevertheless, or knowledge of ant-following bird diversity and ecology in West African forests remains limited.

The tropical forests of Southwest Cameroon hold a significant proportion of the avifauna from the Guinean Gulf forests (Bobo et al., 2005), including many ant-following species (del Hoyo et al., 2016; Waltert et al., 2005). However, the habitats of the region are threatened by continuously growing agricultural activities, which include the establishment of industrialized oil palm plantations (Mbile et al., 2005). Even though the creation of protected areas is a priority of the National Plan for Environmental Management (MINEP & UNDP, 1996), many of the established areas are surrounded by transformed environments and hold large human settlements inside. This is the case of Korup National Park, which comprises an area of 126,000 ha, with five villages inside the park and 25 villages located at up to three kilometers from the park’s boundaries (CBFP, 2016; Mbile et al., 2005). Since its creation in 1986, efforts have been made to integrate conservation and development in the management of Korup National Park. The activities developed so far show that involvement of local communities and satisfaction of their basic needs is a key element for the successful achievement of conservation goals (Mbile et al., 2005; Schmidt- Soltau, 2002). Under a perspective of increasing human population and agricultural activities in the region, it becomes a priority to provide stakeholders with useful tools to conserve the biodiversity of the region.

Studies in diverse geographical locations have found that the species richness and abundance of bird communities change significantly in response to habitat loss, and that such variations are not always linear (e.g. ; Betts et al., 2007; Lindenmayer et al., 2005; Morante-Filio et al.,2015; Radford et al., 2005). This lack of linearity may respond to the presence of a critical threshold, which refers to an abrupt reduction in the probability of survival of the studied organisms as a result of quantitative or qualitative changes in their habitat (Andren, 1994; Fahrig, 2001; With & King, 1999). Identifying the presence of critical habitat thresholds for vulnerable species can help focus conservation and management efforts from various perspectives, such as sustainable resource management, establishment of targets for habitat preservation and restoration and the effective design of landscapes with a focus on biodiversity conservation (Brown et al., 1999; Huggett, 2005; Lindenmayer et al., 2005).

The presence and nature of a critical threshold is tightly related to the ecological requirements of a species (Edwards, Woodcock, et al., 2013; Ochoa‐Quintero et al., 2015). While some bird species may be negatively affected by habitat loss, others may benefit from both habitat change and the

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 9 disappearance of competitors (Ghazoul & Hellier, 2000; Morante-Filho et al., 2015). Therefore, the evaluation of critical thresholds for groups of species must take into account the diversity of ecological traits among them (Banks-Leite et al., 2014).

I used direct observations of ant-following bird species in Southwest Cameroon to evaluate the response of the community to deforestation across a full gradient of forest loss. The study covered an area of approximately 4,000km2 in three landscapes with contrasting forest covers and land-use types: Korup National Park, with large forested areas and some farms around villages; agroforestry areas, with a mosaic of farms inside a forest matrix; and industrial palm oil plantations, with an anthropogenic matrix and forest patches mainly on the edge. I aimed to identify occurrence thresholds based on forest cover for the whole ant-following bird community, for individual species and for guilds with different ecological features. I hypothesized that (H1) there would be non-linear negative responses of the ant-following bird community to forest loss and this would be reflected both on differences among landscapes and among land-use types; (H2) species with specialized ecological traits would be more vulnerable to deforestation than generalist ones and would, therefore, be absent in deforested areas. Based on my results I propose recommendations for the design of wildlife-friendly systems in the area.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 10

METHODS

1. Study area

The Guinean Gulf forest extends through eight countries from Guinea and Sierra Leone to the Sanaga River in North Cameroon. It is a humid zone mostly composed of evergreen rain forests, both in lowlands and montane areas (Maley, 2001). The Guinean Gulf tropical forests are considered a biodiversity hotspot by the Critical Ecosystem Partnership Fund (CEPF); they contain approximately 9,000 vascular plant species, 20 % of which are endemic, and around 2,048 vertebrate animal species (CEPF, 2000). The avifauna of this hotspot is composed by approximately 785 bird species, which include 68% of all the African passerine birds and a total of 78 endemic species (CEPF, 2000; Groombridge & Jenkins, 2000).

Data collection for this study was carried in the vicinity of Korup National Park (KNP), in Southwest Cameroon, from 4°57′N to 5°10′N and 8°44′E to 9°7′E and between 56 and 768m.a.s.l (Figure 1). The study area is located in the former Korup Project Area (KPA), which includes: (1) the Korup National Park (KNP); (2) adjacent agroforestry areas, located between KNP and the Rumpy Hills Wildlife Reserve and (3) industrial oil palm plantations from the company PAMOL. The area presents a pseudo-equatorial climate, characterized only by two climatic seasons, instead of the four typical seasons of equatorial regions: A dry season between December and February and a humid one between March and November (Chuyong et al., 2004; Rodewald et al., 1994). Total annual rainfall in the area is negatively correlated with latitude and ranges from just 1,500 mm to over 10,000 mm (Ministry of Plan and Regional Development, 1989; White, 1983). The mean annual temperature varies according to land cover. Cooler annual average temperatures of around 24.7°C are found in forest areas; while deforested zones are much warmer, with average temperatures up to 32.6 °C (Rodewald et al., 1994).

These special climatic conditions, its geographic location and a considerable portion of continuous forest make the region around KNP one of the most important areas for biodiversity conservation in Africa (Rodewald et al., 1994). The Korup Project Area is considered the oldest rainforest of the continent, with an approximate age of 60 million years (Ruitenbeek, 1992). Its avifauna represents around 53.4 % of the bird diversity found in the Guinean Gulf forests, including 12 endemic species of the montane areas of Southwest Cameroon and Nigeria and 7 endemic species of lowlands and montane forests of Cameroon (Bobo et al., 2005; Rodewald et al., 1994).

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 11

Figure 1. Map of the study area around the Korup National Park. Background colors indicate landscapes: Green: Korup National Park; yellow: Oil palm plantations; landscape matrix: Unprotected agroforestry areas, which include a mixture of native forests and small-scale farming. Note that each landscape may contain more than one land-use type. The dots indicate sampling points around each village: Yellow sampling points: Villages inside the Korup National Park; Purple sampling points: villages inside unprotected agroforestry areas; Green sampling points: villages inside Oil Palm Plantations. The KPA has a total population of approximately 4200 inhabitants (CBFP, 2016; Mbile et al., 2005). The livelihoods of these communities rely mainly on the extraction of resources from the forests: hunting, trapping, and collection of non-timber forest products; as well as agricultural practices mainly related to food and cocoa crops (Mbile et al., 2005). Additionally, part of the income for the region comes from the production of palm oil products either through small-scale farms, owned by local farmers, or industrial plantations, which belong to the public-owned

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 12 company PAMOL. PAMOL is the oldest oil palm company in Cameroon and it currently owns crops covering an area of 5,088ha in the Ndian Division (Nkongho et al., 2015; Pamol, 2016).

2. Sampling design

Sampling was developed by Denis Kupsch, Elleni Vendras, and ornithologist Francis Njie in three distinctive landscapes (Vendras, 2014): (1) Protected forests in Korup National Park (hereafter KNP); (2) Unprotected agroforestry regions (hereafter UA) in the KSZ, and (3) Industrial oil palm plantations (hereafter OPP) located in the Ndian State of Cameroon. Four villages per landscape (3 landscapes x 4 villages = 12 villages) were selected for this study and four study plots per village (12 villages x 4 study plots = 48 study plots) were located for sampling at a distance of 1.5km from the center of the village. Each study plot had an area of 1km2 and was composed by a total of nine sampling points.

3. Data collection

Data collection was performed during the dry season in two stages: Six of the villages were sampled between June and July of 2013 and the remaining half were sampled between May and June, 2014 (see Laudemann (2015) for details).

Bird diversity was sampled through ten-minute unlimited distance point counts (Ralph et al., 1995). Each sampling point was visited once either in the morning (between 6 and 11am) or in the afternoon (between 3 and 6pm) and all the bird species seen or heard were registered only once per sampling point, excluding flyovers (see Laudemann (2015) for details on methods). For the current study, I selected all bird species explicitly identified in the current literature as followers of Dorylus spp. ant swarms (del Hoyo et al., 2016; Peters et al., 2008; Waltert et al., 2005). I pooled the information collected at the sampling plots and considered the study plots as the minimum sampling units. Consequently, a species’ encounter frequency refers to the number of records found per km2, which can have a maximum value of nine per study plot (number of sampling points per study plot); 36 per village (9 sampling points x 4 study plots) and 144 per landscape (9 sampling points x 4 study plots x 4 villages per landscape). Bird species richness corresponds to the number of bird species registered in the same area.

The habitat of the sampling points was assessed through visual estimation of the percentage of over-storey and under-storey vegetation cover. Based on such information each sampling point was classified as: (1) Near-primary forest (NPF), understood as nearly undisturbed native rain forest; (2) Secondary forest (SF), understood as a regenerating forest with younger trees than those found in NPF; (3) Traditional plantations (TP), understood as smallholder croplands of cocoa, yam or other agricultural products; and (4) Industrial palm plantations, considered as large-scale plantations of Elaeis guineensis owned by companies, rather than by local farmers. Based on the habitat classification of each sampling point, I calculated the percentage of each habitat type inside the 48 study plots. Forest cover of each study plot was assessed by Denis Kupsch (Workgroup on Endangered Species Conservation, Georg-August-Universität Göttingen) through Landsat imagery and ground-truthing vegetation survey data in ESRI ArcGIS 10.3 (Laudemann, 2015;

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 13

Vendras, 2014). Classifications of the feeding guild, habit, foraging location and nesting location for the bird species found in the survey were made following del Hoyo et al. (2016); Fry et al. (2004) and Waltert et al. (2005).

4. Data analysis

Neither of the two response variables, species richness and frequency, presented a normal distribution (WSpecies richness=0.882, p=0.002; WEncounter frequency=0.951,p=0.043) and consequently non-parametric methods were selected for data analysis.

I tested whether bird frequency and species richness was different between landscapes through Kruskal-Wallis tests. Mann-Whitney U-Tests were carried as a post-hoc analysis to identify differences between pairs of landscapes and a Bonferroni correction was applied to account for multiple testing (Dytham, 2011). I followed this same methodology to test for differences in the encounter frequency of individual species among the three landscapes. Means are given with standard error if not mentioned otherwise. All statistical analyses were performed using the software R Studio (R Studio Team, 2015). I evaluated the impact of landscape and land-use type on encounter frequency and species richness of ant-following birds through generalized linear models including both predictive variables and their interaction (landscape*landuse).

I modeled occurrence thresholds of ant-following birds in areas with different forest cover percentage through Multivariate Additive Regression Splines (hereafter EARTH) (Friedman, 1991), with the package Earth for R Studio (Milborrow, 2011). Analyses were done for all species combined and for the community excluding primarily frugivorous species (n= 5 spp.), most which are very common in the area and very rare attendants to ant swarms (del Hoyo et al., 2016). The models were run including a generalized linear model (GLM) option and a Poisson distribution. Each model was run twice, using either the pruning method “backward” or “cross validation”. The best model selected was that with a highest GR2 value. GR2 is understood as the model’s estimates of generalization performance; in other words, it serves as an indicator of the predictability of the model (Milborrow, 2016). The best model was plotted and the presence of a threshold was identified based on the position of possible breakpoints in the curve. An occurrence threshold is defined here as the point at which there is a clear decrease in the probability of survival of the species or community evaluated (Andren, 1994; Fahrig, 2001; With & King, 1999). In a graph with forest cover loss in the x axis, this will be depicted by the presence of a breakpoint after which the slope of the curve increases and, therefore, the response variable (encounter frequency or bird species richness) decreases with forest loss or gain at a faster rate.

I decided not to consider the presence of a threshold in cases in which the slope of the curve equaled zero after a breakpoint and indicated a linear decrease in the response variable before it (see Figure 4C for an example). In all such cases, the breakpoint pointed to the percentage forest cover at which the study subject could be predicted to be absent (go extinct) in the study area. I interpret these cases to indicate a linear negative response of the study subject to deforestation, since the slope at any point before the extinction of the subject indicates a decrease in its probability of survival. Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 14

I also ran separate threshold models for groups of non-frugivorous bird species with different (a) foraging locations; (b) nesting locations and (c) feeding guilds. Occurrence thresholds were also modeled for individual species. Foraging and nesting locations were ordinal categories: (1) floor

(nforaging= 11 spp.; nnesting= 4 spp.), (2) understory (nforaging= 8 spp.; nnesting= 18 spp.) and (3) all locations (nforaging= 2 spp.; nnesting= 0 spp.). Feeding guilds were: Insectivorous (n= 7 spp.); carnivorous (n= 4spp.), considered as insectivorous with occasional consumption of other animals and omnivorous (n=10spp.), considered as non-specialized insectivorous.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 15

RESULTS

1. Description of the ant-following bird guild

1806 records of 26 ant-following bird species were collected in the study area (Table 1). The most abundant species in the entire survey was the little greenbul (Andropadus virens), while the species with the lowest encounter frequency overall was the red-tailed ant thrush (Neocossyphus rufus) (Table 1).The encounter frequency of 18 ant-following bird species was significantly lower in plots located inside the OPP landscape than in either KNP or UA. Conversely, encounter frequency of the little greenbul (A. virens) and the common bulbul P. barbatus was significantly higher in OPP than in either KNP or UA. For five ant-following bird species, encounter frequency was significantly higher inside KNP than in UA areas, while for the remaining 13 species there were no significant differences between KNP and UA (Table 1).

Table 1.Encounter frequency of each species found in the survey inside the three landscapes of the study area and differences among landscapes through Kruskal-Wallis tests (K-W) (p= 0.05) and Mann-Whitney U tests (M-W) (p= 0.016 after Bonferroni correction). Taxonomic classification follows del Hoyo et al. (2016).Underlined species have a frugivorous diet. ND= No significant differences; * =0.05≥p≥0.01; **= 0.01>p≥0.001; ***= p≤0.001.

Total K-W M-W M-W M-W Family Species encounter KNP UA OPP (Chi2, KNP/UA KNP/OPP UA/OPP frequency sig.) (W, sig.) (W,sig.) (W, sig.) Lophoceros camurus 17 6 11 0 ND ND *** *** Bucerotidae Horizocerus albocristatus 8 5 3 0 ND ND ND ND Alcedinidae Halcyon badia 13 4 8 1 * ND ND ** Pycnonotus barbatus 124 4 8 112 ND ND *** *** Andropadus latirostris 283 135 127 21 ND ND *** *** Andropadus virens 354 98 118 138 ND ND *** ** Baeopogon indicator 28 12 15 1 ND ND ** ** Pycnonotidae Thescelocichla leucopleura 4 0 2 2 ND ND ND ND Phyllastrephus icterinus 33 18 13 2 ND ND ** ND Bleda syndactylus 92 58 34 0 ND ND *** *** Bleda notatus 85 58 26 1 * *** *** *** Criniger chloronotus 83 50 33 0 ND ND *** *** Criniger calurus 110 54 53 3 ND ND *** *** Stizorhina fraseri 41 23 17 1 ND ND *** *** Neocossyphus poensis 73 46 26 1 ND *** *** ND Neocossyphus rufus 2 1 1 0 ND ND ND ND

Turdus pelios 25 0 0 25 ND ND *** *** Turdidae Chamaetylas poliocephala 31 16 15 0 ND ND *** ***

Alethe castanea 79 42 33 4 ** ND *** *** Stiphrornis erythrothorax 117 67 43 7 * ND *** *** Shepphardia cyornithopsis 3 2 1 0 ND ND ND ND Muscicapidae Muscicapa sethsmithi 17 10 7 0 ND ND ** ** Illadopsis cleaveri 7 1 6 0 ND ND ND ND Timaliidae Illadopsis rufipennis 81 42 39 0 ND ND *** *** Illadopsis fulvescens 27 14 13 0 *** *** *** *** Dicruridae Dicrurus atripennis 69 33 35 1 ND ND *** ***

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 16

2. Effects of landscape and land-use type on species richness and encounter frequency of ant-following birds

24 bird species were found in KNP and 25 in UA, with an average of 14.87±0.55 and 15.19±0.73 bird species/km2, respectively. In contrast, only 16 species were found in the OPP landscape, with an average of 4.25±0.55 species/km2. Ant-following bird encounter frequency and species richness were not significantly different in KNP than in UA (WFreq. = 175, p= 0.079; WRich= 118.5, p= 0.73).

There were significantly less birds and species inside OPP than in either KNP (WFreq. = 255, p<0.001, WRich= 256, p<0.001) or UA (WFreq. = 3, p<0.001, WRich= 0.5, p<0.001) (Figure 2). There was an average of 12.18±0.64 non-frugivorous ant-following bird species per village in KNP, 12.31±0.70 bird species per village in UA and only 1.75±0.45 bird species per village in OPP. The differences in bird encounter frequency and species richness were not significant between KNP and UA for non-frugivorous ant-followers (WFreq. = 178 p= 0.061; WRich= 126, p= 0.954). There were significantly less non-frugivorous birds and bird species inside OPP than in either KNP (W= 256, p<0.001) or UA (W= 0, p<0.001) (Figure 2).

Figure 2. Mean value and error bars of encounter frequency and species richness of ant-following birds per study plot (1km2) inside the three landscapes found in the study area. KNP: Korup National Park; UA: Unprotected agroforestry; OPP: Industrial oil palm plantations. Black indicates values for the whole ant-following bird community, while gray indicates values excluding frugivorous species (see Methods). Different letters on top of means indicate a significant difference among landscapes (Mann-Whitney U test with Bonferroni correction, p<0.05). The dominant land-use type was different in each of the three landscapes found in the study area. Near-primary forest had the largest cover in KNP, while inside the UA landscape primary and secondary forest had similar percent cover (W=141.5, p=0.622). Palm plantations covered the largest area of the OPP landscape (Table 2).

Table 2. Average percentage and standard error (SE) of land-use types found in each of the landscapes in the study area. Values were calculated based on the total amount of land-use types in each village.

Near- Industrial Secondary Traditional Landscape primaryforest palm plantations forest (SF) plantations (TP) (NPF) (IPP) Korup National Park 73±7.85 17.31±5.65 9.68±4.67 0 Unprotected agroforestry 45.75±9.50 37.06±7.77 22.06±5.33 0 Oil Palm Plantation 2.75±1.64 6.25±3.48 6.87±2.91 84.12±6.18

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 17

There was a significant effect of landscape, land-use type and their interaction on the encounter 2 2 frequency of ant-following birds (Chi landscape = 19.37, p<0.001; Chi landuse= 16.85, p< 0.001; 2 2 Chi landscape*landuse= 13.18, p= 0.004) and non-frugivorous ant-following birds (Chi landscape = 56.34, 2 2 p<0.001; Chi landuse= 31.53, p<0.001; Chi landscape*landuse= 29.17, p<0.001). Conversely, only landscape had a significant effect on the species richness of both the whole ant-following bird 2 2 2 community (Chi landscape = 14.15, p<0.001; Chi landuse= 3.73, p<0.291; Chi landscape*landuse= 4.38, 2 2 p=0.22) and the non-frugivorous species (Chi landscape = 19.87, p<0.001; Chi landuse= 5.33, p=0.149; 2 Chi landscape*landuse= 4.29, p= 0.231) (Figure 3).

Figure 3. Encounter frequency and species richness per study site (1km2), in each of the land-use types and landscapes present in the study area. Land-use types: NPF= near-primary forest; SF= secondary forest; TP= traditional plantations; IPP= industrial palm plantations. Landscapes: KNP= Korup National Park; UA= Unprotected agroforestry; OPP= Industrial oil palm plantations. Black indicates values for the whole ant-following bird community; while blue indicates values excluding frugivorous species (see methods). There is a significant effect of the interaction between landscape and land-use type on the encounter frequency of both bird groups.

3. Forest cover thresholds for ant-following birds inside a land-use mosaic

There was a positive association between forest cover and encounter frequency of all ant-following birds (GR2=0.65, R2= 0.70), as well as of non-frugivorous species (GR2=0.67, R2= 0.69). No encounter frequency threshold was identified for the ant-following bird community. A breakpoint

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 18 was identified in the graph at 52% of forest cover. Above the breakpoint, the encounter frequency of ant-following birds declined linearly from an average of 53.5±2.59 bird records/km2 in fully forested areas to 30.85 bird records/km2 in areas with 52% of forest cover. Above the breakpoint, encounter frequency decreased at a rate of 4.35bird records/km2per 10% of forest loss. Below the breakpoint, the decline rate decreased to 2.57bird records/km2 per 10% of forest loss. In areas with no forest cover, encounter frequency of ant-following birds was 17±1 bird records/km2.

No encounter frequency threshold was identified in this study for non-frugivorous ant-following bird species. The encounter frequency of non-frugivorous ant-followers was significantly lower than that of all ant-following species in fully forested areas (Mann-Whitney U=16, p= 0.02). The encounter frequency of non-frugivorous ant-followers declined linearly from an average of 39±3.01 bird records/km2 in fully forested areas to 2.10 bird records/km2 in areas with ≤24% of forest cover (Figure 4C). 4.44 less individuals were recorded per km2with every 10% of forest loss.

There was also a strong positive association between forest cover and species richness of the whole ant-following bird community (GR2=0.85, R2= 0.88) and non-frugivorous ant-followers (GR2=0.87, R2= 0.88). A species richness threshold was identified at 74 % of forest cover for the ant-following bird community. Above this threshold one ant-following bird species disappeared with every 11.5% of forest loss/ km2. Species richness decreased from an average of 17.75± 0.85 spp./ km2 in fully forested areas to 14 spp. in areas with 74 % of forest cover. Below the threshold of 74 % forest cover, species loss increased to a rate of 1 spp. per 6.6 % of forest loss. Areas with no forest cover held an average of 2.71 ± 0.18 ant-following bird species (Figure 4B). No threshold of forest cover was identified for the decrease in species richness of non-frugivorous ant-followers. Species richness of non-frugivorous ant-followers decreased from an average of 15.5 ±0.86 spp./ km2 in fully forested areas to an average of0.57 ±0.2 spp./ km2 in areas with no forest cover. There was a steady rate of decline of one spp./km2 with every 7.8% of forest lost.

Figure 4. Encounter frequency (A, C) and species richness (B, D) of ant-following birds (A, B) and non- frugivorous ant-followers (C, D) in study areas of 1km2 with different forest cover. Tendency line is the product of a multivariate additive regression spline. Red dotted line indicates a change in the slope of the curve and, therefore, a potential threshold. Dots represent values for each study plot inside the three landscapes: KNP= Korup National Park; OPP= Industrial oil palm plantations and UA= Unprotected Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 19 agroforestry areas and in the four land-use types: NPF= Near-primary forest; SF= Secondary forest; TP= Traditional plantations; IPP= Industrial palm plantations. Nine species were rejected from the individual threshold analyses (see methods, Appendix 3). The encounter frequency of 15 out of the 17 remaining ant-following species was positively related to forest cover; while the encounter frequency of the common bulbul (P. barbatus) and the little greenbul (A. virens) increased with forest loss (Figure 5 C, H). For the little greenbul, an occurrence threshold was identified at 15% of forest cover. In areas with higher forest cover, the encounter frequency of the bird declines linearly at a rate of 0.27 birds/km2 with every 10% increase in forest cover (Figure 5H). While the encounter frequency of the common bulbul decreased linearly at a rate of 1.05 birds/km2 with every 10% increase in forest cover and no birds were predicted to be present in areas with ≥76% of forest. No common bulbul was recorded in fully forested areas (Figure 5C).

No occurrence thresholds were identified for thirteen ant-following bird species. In five cases (B. indicator, S. fraseri, C. calurus, P. icterinus, and S. erythrothorax), there was a linear decline in encounter frequency with forest loss and the species were absent in areas with no forest (Figure 5 M-Q). For three other species (C. chloronotus, D. atripennis and N. poensis), encounter frequency declined linearly with forest loss in areas with ≥52% of forest cover and were predicted to be absent in areas with less forest cover (Figure 5D-F). The encounter frequency of both bristlebill species (B. notatus and B. syndactylus), as well as of the black-capped illadopsis (I. cleaveri), the pale-breasted illadopsis (Illadopsis rufipennis) and the brown-chested alethe (Chamaetylas poliocephala) declined linearly in areas with ≥24% of forest cover and the species were absent in areas with less forest cover (Figure 5G, I-L).

My results show an occurrence threshold for the fire-crested alethe (A. castanea) at 74% of forest cover. Above the threshold, encounter frequency of this species declined at a rate of 0.72 bird records/km2 with every 10% of forest lost; while below the threshold the rate decreased to 0.20 bird records/km2 with every 10% of forest lost. No fire-crested alethe was recorded in areas with no forest (Figure 5A). For the frugivorous yellow- whiskered greenbul (A. latirostris) an occurrence threshold was found at 52% of forest cover. Above the threshold the encounter frequency of the species remained stable at 8.08 bird records/km2; while below the threshold encounter frequency decreased at a rate of 1.57 bird records/km2 with every 10% of forest lost(Figure 5B).

4. Effect of forest cover change on ecological guilds from ant-following birds

There was a positive relation between forest cover and encounter frequency of all feeding guilds of non-frugivorous ant-following birds. No threshold was found for any of the feeding guilds evaluated in this study, all of them declined linearly with forest loss. The encounter frequency of insectivorous ant-followers declined at a rate of 1.36 bird records/km2 with every 10% of forest lost in areas with forest cover rates between 100 % and 24% and the guild was absent in areas with ≤24% of forest cover (Figure 6A). Carnivorous ant-followers declined at a rate of 0.52 bird records/km2 with every 10% of forest lost, in areas with between 100 % and 15% of forest cover.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 20

The guild was absent in areas with ≤15% of forest cover (Figure 6B). The encounter frequency of omnivorous ant-followers declined in areas with between 100 % and 24 % of forest cover at a rate of 2.51 bird records/km2 with every 10% of forest lost. An encounter frequency of 1.5 omnivorous ant-following bird records was predicted in areas with ≤ 24 % of forest cover (Figure 6C).

Figure 5. Encounter frequency of individual ant-following bird species in study areas of 1km2 with different proportions of forest cover. Tendency line is the product of a multivariate additive regression spline. Red dotted line indicates a change in the slope of the curve and, therefore, a potential threshold. Dots represent encounter frequency of the species in each of the study plots across the three landscapes: KNP= Korup National Park; OPP= Industrial oil palm plantations and UA= Unprotected agroforestry areas and in the

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 21 four land-use types: NPF= Near-primary forest; SF= Secondary forest; TP= Traditional plantations; IPP= Industrial palm plantations. Species richness of all feeding guilds declined linearly with forest cover loss. One omnivorous ant- following bird species disappeared with every 12.7% of forest cover lost and 1 bird spp./km2 were predicted to be detected in areas with ≤15% of forest cover (Figure 7C). One of the four carnivorous ant-following bird species registered in this survey was predicted to disappear with every 44% of forest loss and only 0.04 bird spp. /km2 were predicted to be detected in areas with no forest (Figure 7C). Insectivorous species declined at a rate of 1 spp./ 14.3 % of forest lost. No insectivorous species were predicted to be present in areas fully deforested areas.

Figure 6. Encounter frequency of ant-following bird groups with different ecological features in study areas of 1km2 with different percentages of forest. Insectivorous are all species with a diet exclusively composed by insects; other carnivorous are species with a diet composed by insects and other animals; omnivorous are species with a diet composed by animal prey, as well as occasional plant material, such as fruit and seeds. Foraging guilds indicate the vegetation stratus at which bird species forage, all strata foragers forage indistinctively on the ground, in the understory and in the tall canopy. Nesting guilds indicate the vegetation stratus at which species build their nests. Tendency line is the product of a multivariate additive regression spline. Red dotted line indicates a change in the slope of the curve and, therefore, a potential threshold. Dots represent encounter frequency (bird records/km2) for each study plot inside the three landscapes: KNP= Korup National Park; OPP= Industrial oil palm plantations; UA= Unprotected agroforestry areas and in the four land-use types: NPF= Near-primary forest; SF= Secondary forest; TP= Traditional plantations; IPP= Industrial palm plantations. There was a positive relation between both the encounter frequency and species richness of all foraging guilds and forest cover. No occurrence threshold was found for either ground or understory foragers. The breakpoint identified at 74 % of forest cover indicates a decrease in the slope of the curve. The encounter frequency of ground foragers declined at a rate of 3.01 bird Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 22 records/km2 with every 10% of forest lost; while below the rate declines to 1.03 bird records/km2 with every 10% of forest lost (Figure 6F). However, a species richness threshold was found for ground foragers at 52% of forest cover. Above the threshold, species richness decreased at a rate of 1 spp./km2 with every 24.68% of forest lost; while below the threshold, the rate increased to 1 spp./km2 with every 11.98% of forest lost (Figure 7D). Areas without forest cover held an encounter frequency 0.88 bird records, belonging to 0.54 spp. of ground foragers per km2.

The encounter frequency and species richness of understory foragers declined linearly with forest loss. In areas with forest cover between 100% and 24%, encounter frequency decreased at a rate of 1.76 bird records/km2 with every 10% of forest lost and species richness decreased at a rate of 1 spp./km2 with every 14.29% of forest lost. In areas with <24% of forest cover, encounter frequency and species richness of understory foragers were 0.1 bird records/km2, belonging to 0.26 bird species (Figure 6E, Figure 7E). Encounter frequency and species richness of the two bird species foraging at all strata decreased linearly at a rate of 0.15 bird records/km2 with every 10% of forest lost and 1 bird spp./km2 with every 22.06% of forest lost. The guild was absent in areas with no forest.

Figure 7. Species richness of groups of ant-following birds with different ecological features in study areas of 1km2 with different percentages of forest. Insectivorous are all species with a diet exclusively composed by insects; other carnivorous are species with a diet composed by insects and other animals; omnivorous are species with a diet composed by animal prey, as well as occasional plant material, such as fruit and seeds. Foraging guilds indicate the vegetation stratus at which bird species forage, all strata foragers forage indistinctively on the ground, in the understory and in the tall canopy. Nesting guilds indicate the vegetation stratus at which species build their nests. Tendency line is the product of a multivariate additive regression spline. Red dotted line indicates a change in the slope of the curve and, therefore, a potential Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 23 threshold. Dots represent values for each study plot inside the three landscapes: KNP= Korup National Park; OPP= Industrial oil palm plantations; UA= Unprotected agroforestry areas and in the four land- use types: NPF= Near-primary forest; SF= Secondary forest; TP= Traditional plantations; IPP= Industrial palm plantations. Encounter frequency and species richness of both nesting guilds were positively related with forest cover. Occurrence thresholds were found for ground-nesting ant-followers. My results indicate an encounter frequency threshold for this guild at 86% of forest cover. Below this threshold, the encounter frequency of the guild declines linearly at a rate of 0.56 bird records/km2 with every 10% of forest lost. A species richness threshold was also identified at 74% of forest cover; below which 1spp. disappeared with every 44.34% of forest lost. The model predicted the complete disappearance of the guild in areas with no forest (Figure 6G, Figure 7G). An encounter frequency threshold for understory foragers was identified at 52% of forest cover. The encounter frequency of the guild declined above the threshold at a rate of 4.75 bird records/km2 with every 10% of forest lost and at a rate of 1.47 bird records/km2 with every 10% of forest lost in areas with <52% of forest cover (Figure 6H). No species richness threshold was identified for understory-nesting species, which declined linearly at a rate of 1spp./km2 with every 9.16% of forest lost (Figure 7H). 1.02 bird records belonging to 0.46 spp. were found in areas with no forest.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 24

DISCUSSION

1. Overall response to deforestation

This study showed that ant-following bird communities in Korup National Park and the surrounding area exhibit non-linear negative responses to deforestation (H1). Species richness and encounter frequency of ant-followers is lower in landscapes with reduced forest cover, such as industrial oil palm plantations. Ground-specialist bird species are particularly sensitive to forest loss and decline rapidly in areas with medium and high levels of deforestation. My results suggest that large portions of forest are necessary to conserve this bird community in the area.

The results of this study are congruent with previous evidence of the negative impacts of deforestation on tropical bird communities. Forest loss is known to cause a decrease in the biodiversity of tropical bird communities (Sodhi et al., 2004) and to alter their composition and integrity (Kofron & Chapman, 1995; Martensen et al., 2012; Morante-Filho et al., 2015; Waltert et al., 2005). My results show that deforested areas covered with oil palm plantations inside the study area held a maximum of 46% of the total species richness of ant-following birds present in the region (12 out of 26 potential species) and significantly lower encounter frequency than either forests or agroforestry areas. Oil palm plantations in this study area are still submerged in a forest matrix, which increases the probability of occasional encounters of transient bird species, whose resources are mostly found inside the forest. Studies performed in Malaysian oil palm plantations indicate that the vicinity to forests can significantly increase the diversity and abundance of selected insect taxa inside the plantations (Lucey & Hill, 2012), which may provide additional feeding resources for ant-following bird species with forest preferences. Therefore, the resident avifauna community in the OPP landscape can be expected to be even smaller than the amount I report here.

The results of my study indicate a non-linear response for the encounter frequency of ant-following birds in the area of Korup National Park. While the rate of decrease in encounter frequency in response to deforestation shifts at 52 % of forest cover, the decrease rate below the threshold is lower. I interpret the fast decline in encounter frequency of ant-following birds at all degrees to forest loss as an indication of the vulnerability of ant-following bird communities to deforestation, even in largely forested areas. Such a high vulnerability is confirmed by the species richness threshold identified for the community at 74 % of forest cover. Species richness declines steeply in areas with less than 74% of forest cover, nevertheless it still declines linearly with forest loss above the threshold. To my knowledge, this is the first time that a threshold of such magnitude has been reported for a bird community. It is up to 60% higher than the thresholds calculated for bird communities in temperate regions, such as Canada (Betts et al., 2007), Australia (Radford et al., 2005) or the United States (Donnelly & Marzluff, 2004). It is also higher than the results of studies on tropical bird communities, which reported thresholds of around 43% of forest cover for understory birds of Amazonian forests (Ochoa‐Quintero et al., 2015) and even around 50% for neo-tropical bird and mammal communities in Atlantic forests of Brazil (Morante-Filho et al., 2015). Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 25

The elevated threshold reported in this study confirms the high sensitivity of West-African ant- following birds to forest loss and land-use change. Flocks of neo-tropical ant-following birds are known to decrease in size in response to forest loss and fragmentation (Kumar & O'Donnell, 2007). More local extinctions, in particular of specialized ant-following species, and reduced occupancy are reported with decreasing area of forest fragments (Ferraz et al., 2007; Harper, 1989). Similar results have been reported for Africa, where there is a negative effect of land-use change and decreased area of forest fragments on the species richness of ant-following birds in Congo-Guinean forests of Southwest Cameroon (Waltert et al., 2005) and Kenya (Peters et al., 2008).

2. Differential response of non-frugivorous species and ecological guilds

The thresholds identified in this study for the ant-following bird community disappeared once the frugivorous species were removed from the analysis. The remaining species exhibited a linear decline both on species richness and bird encounter frequency in function of species loss. Notably, the decline rate of non-frugivorous birds (4.44 bird records per 10 % of forest lost) was very similar to the steepest decline rate found for the whole community in terms of bird encounter frequency (4.35 bird records per 10 % of forest lost above the identified threshold) and also species richness (one ant-following bird spp. per 6.6 % of forest lost and one non-frugivorous spp. per 7.8 % of forest lost). Thus, it is relevant to highlight that the lack of a threshold does not indicate a lower sensitivity to the predictor variable evaluated (Swift & Hannon, 2010). On one side, it is possible that no threshold responses exist for certain ecosystems or to certain variables; on the other side, the absence of a threshold can be rather related to the diversity of habitat requirements of the species that have been grouped in the analysis (Lindenmayer et al., 2005). Ferraz et al. (2007) found that two species of ant-following birds responded contrastingly to habitat loss and connectivity in forests of the Amazon: while the white-chinned woodpecker responded negatively to the isolation of forest patches but not to patch area; the common black-throated ant shrike was very sensitive to area, but not to the isolation of forest patches. This highlights the value of testing the differential response of species inside the ant-following bird community, based on diverse ecological traits among them.

My results indicate that the lack of a common response to deforestation by ant-following birds is related to the ecological diversity found inside the community. Ground foragers displayed a non- linear response to forest loss. Below 52 % of forest cover, the species richness of ground foragers declined faster with forest loss than that of understory foragers. Ground nesting species also displayed a non-linear response to forest loss. Only up to three species were registered simultaneously in a study area and given the low number of species displaying such a trait in the community (n= 5 spp.), one half of the community was expected to be extinct in areas with less than approximately 40 % of forest cover (Figure 7). The high sensitivity of ground-dwelling ant- followers to deforestation has been related to the loss of forest structure and the protection provided by it. Terrestrial ant-following bird species disappeared with forest fragmentation but were able to recolonize patches with strong secondary growth of native trees (Stouffer & Bierregaard, 1995). The absence of many ground specialist bird species in deforested areas of my study may also be

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 26 related to the lack of secondary growth and vegetation complexity inside oil palm plantations and, consequently, increased exposition to predators and other threats during foraging and nesting.

Divergent responses to deforestation were also observed between feeding guilds. Even though all feeding guilds responded negatively to deforestation (Figure 6 A-C); omnivorous species had a higher species richness and encounter frequency in fully deforested areas than insectivorous or carnivorous ant-following birds (Figure 7 A-C). Forest specialists were always absent from areas with no forest cover and their encounter frequency decreased with forest loss. Moreover, an occurrence threshold was identified for ground foragers at 52 % of forest cover and for ground nesting species at 74 %. Studies of bird communities in tropical forests of Colombia (Kattan et al., 1994) highlighted that ground insectivorous bird species require larger forest areas than other understory species to survive in fragmented forests. Likewise, Waltert et al. (2005) relate the absence of ground insectivorous birds in deforested anthropogenic areas of Cameroon to the alteration in prey availability as a result of continuous disturbances. It is likely that the absence of ground-nesting species in deforested areas replaced by oil palm plantations is also related to the negative effect of continuous disturbances on reproductive success; both by direct human intervention to the nests or increased exposure to predators.

My results evidence that species with specialist ecological traits are more sensitive to deforestation than generalist occasional ant-followers (H2). Previous studies indicate that the integrity of tropical bird communities in forest cover gradients is affected by the disappearance and replacement of biome-restricted species (Banks-Leite et al., 2014; Kofron & Chapman, 1995). The vulnerability of such species to deforestation has been related to their low mobility and inability to cross habitat gaps (Martensen et al., 2012). Likewise, biome-restricted habits are usually associated to narrow niche widths and, therefore, dependence on very specific resources (Edwards, Woodcock, et al., 2013). 70 % of all forest-specialist species reported in this study are also diet specialists, which indicates a narrow niche breadth, at least respecting diet. Three forest specialist species disappear in areas with <52 % of forest cover and two more in areas with <25 % of forest cover. Among them, the white-tailed ant thrush (N. poensis) and the red tailed bristlebill (B. syndactylus) are additionally insectivorous specialized ant-followers (Peters et al., 2008) (Appendix 2). These species have been previously reported to be sensitive to forest loss and fragmentation and inhabit preferentially large forest patches (Peters et al., 2008). In the present study, the absence of these two specialized ant-followers in areas with medium to high deforestation rates seems to be compensated by the increase in the encounter frequency of opportunistic ant-following species. The encounter frequency of three bird species, the common bulbul, the little greenbul and the African thrush, increased with deforestation. All these species have wide habitat preferences, including various types of forests as well as human-intervened areas and have broad diets, composed of fruits and several groups of arthropods (Collar, 2017; Fishpool & Tobias, 2017b, 2017c). Therefore, the replacement of specialized ant-following birds in deforested areas may to be related to the ability of generalist species to persist in a different biome and switch their diets as necessary (Willis, 1979).

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 27

The three species whose encounter frequency increased with deforestation in this study have very plastic feeding and habitat preferences, which provides them an advantage to inhabit disturbed ecosystems. A study comparing bird diversity in undisturbed forests and deforested areas of Liberia found that the common bulbul (P. barbatus) inhabited exclusively deforested regions (Kofron & Chapman, 1995); while other studies highlight its broad dietary plasticity, which may even include the consumption of small vertebrates, nectar and even beewax (Fishpool & Tobias, 2017a; Horne & Short, 1990). Similarly, Kofron and Chapman (1995) affirmed that the little greenbul (A. virens) was probably preadapted to inhabit anthropogenic deforested areas. This was later proved by other authors who evidenced the adaptation of the species’ vocalizations to human disturbed environments (Slabbekoorn et al., 2002) and the special morphological and genetic features of populations inhabiting ecotones (Smith et al., 1997). However, given their occasional ant-following behavior, their presence cannot be regarded as an indicator of a functional ant- following bird community.

The replacement of specialized ant-followers by generalist bird species with occasional attendance to army ant swarms is thought to have profound effects on the establishment and stability of ant- following bird flocks. Specialized ant-followers are known to engage in specific behaviors that allow other birds to adequately locate and follow ant swarms (Willis & Oniki, 1978). Therefore, they are regarded as nuclear species whose absence may strongly impact the ability of other bird species to locate ant swarms and create mixed flocks (Maldonado-Coelho & Marini, 2004; Peters et al., 2008). Swarms of army ants and the animals that follow them are also known to control the population size of abundant insects and thus increase the diversity of insect communities (Franks & Bossert, 1983). Consequently, the absence of strong ant-following bird flocks in tropical forests may also impact insect communities and pest abundance in deforested areas.

3. Implications for forest management and conservation in Southwest Cameroon

The results reported in this study provide a first baseline about the deforestation limits that can be tolerated by highly sensitive bird species in tropical rain forests of West Africa and around the Korup National Park. The use of forest cover as the only variable to predict the occurrence of species has been validated by studies comparing the relevance of habitat configuration and quantity. The amount of habitat, in terms of percentage cover or the area of habitat patches seems to be the primary driver of species’ occurrence, rather than other landscape features, such as habitat connectivity or the shape of habitat patches (Fahrig, 2003). Moreover, forest cover is a useful predictor variable that may indirectly comprise and represent other limiting factors for the distribution of ant-following birds. The availability and foraging behavior of army ants, for example, seems to be strongly affected by humidity conditions of the area (Willis, 1986). Consequently, they are thought to remain inactive in open areas during the day if conditions are too dry (Peters & Okalo, 2009), which in turn may reduce the probability of occurrence of ant- following bird species. The use of forest cover as a predictor of ant-following bird occurrence, may therefore encompass other relevant variables such as food availability.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 28

My study indicates that the diversity of non-frugivorous ant-following birds declines linearly in response to forest loss. Nevertheless, the most sensitive guilds of the community do present a non- linear response to deforestation. Ground foragers and ground nesting species require large forested areas to persist in the landscape. Based on these results, it is recommended to maintain more than 83% of forest cover at the landscape level in order to prevent the disappearance of the most sensitive ecological role inside the ant-following bird community, the ground-nesting species.

The results of this study are also congruent with previous evidence of the negative effects of large industrial plantations on ornithological diversity in the tropics (Aratrakorn et al., 2006; Cajas- Castillo et al., 2015; Edwards, Edwards, et al., 2013; Koh & Wilcove, 2008). The species richness and encounter frequency of ant-following birds was significantly lower in industrial oil palm plantations, than in any other land use. Similarly, studies on ant-following bird flocks in tropical forests of Panama indicate that the percentage attendance of obligate ant-following species decreases around 50% in coffee plantations adjacent to forests and some even disappear in distanced plantations (Roberts et al., 2000). Likewise, oil palm and rubber plantations in Thailand presented a significantly less rich bird community than forest areas, with a clear replacement of rare and endangered species by widely dispersed ones (Aratrakorn et al., 2006). This evidence should therefore be used to design strategies for agricultural management in Southwest Cameroon, which seek to avoid large biodiversity losses.

Conversely to the negative effects of industrial plantations on ant-following bird communities, my results indicate no significant differences in species richness or encounter frequency between forests and agroforestry areas. Therefore, smallholder agricultural practices seem to have no significant negative effect on this bird community, probably because of the maintenance of a native forest matrix. With a perspective of farming practices heavily increasing in Southwest Cameroon it will be relevant to maintain wildlife-friendly agricultural practices which spare enough forest area to prevent the negative effects seen in large oil palm plantations.

Similar initiatives have been successfully created in Latin America for shade coffee plantations inside tropical forests (Rappole & King, 2003). Shade coffee plantations offer a high vegetation complexity, usually lost in large plantations, since they retain high canopy cover as well as understory plants (Perfecto et al., 1996). This key difference from industrial monocultures results in very similar animal communities from those found in native forests of the region (Mas & Dietsch, 2004; Perfecto et al., 2003; Perfecto et al., 1996; Roberts et al., 2000). In order to promote such agricultural practices and ensure sustainable coffee production, many conservation organizations, such as Conservation International, the Smithsonian Migratory Bird Service and the Rainforest Alliance, developed certification schemes for shade-grown coffee. Under sufficient regulations, such schemes seem to be successful in maintaining native biodiversity in agricultural areas and benefiting from the ecosystem services derived from it; if they include mechanisms to avoid excessive deforestation (Perfecto et al., 2003; Tejeda-Cruz et al., 2010). It seems likely that the development of sale strategies which favor the commercialization of products grown in agroforestry schemes in Southwest Cameroon may relent the ever-growing entrance of industrial plantations in the region.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 29

My study also provides indirect evidence of the inability of certain ant-following species, such as the white-tailed ant thrush or the red-tailed bristle bill, to cross habitat gaps. Such species are entirely absent in oil palm plantations, despite the fact that plantations are surrounded by native forest. The expansion of agricultural and urban areas threatens the maintenance of connected forest networks and may thus restrict the dispersion of many ant-following bird populations. Forest fragments inside large oil palm plantations have proved to be unable to effectively retain viable bird populations in Borneo (Edwards et al., 2010). Consequently, functional conservation of ant- following bird species in the area around Korup National Park should aim to preserve large forest areas and ensure the connectivity of such areas in the agricultural land.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 30

CONCLUSIONS

This study provided the first quantitative measurements of the vulnerability of the ant-following bird community to deforestation in the Guinean Gulf tropical rainforests. There was evidence of a non-linear response of non-frugivorous ant-following birds to deforestation in Southwest Cameroon (H1), indicated by an occurrence threshold at 74% of forest cover. Below such threshold the species richness of the community decreased steeply. My results evidenced diverse responses among the different ecological guilds of ant-following birds. Omnivorous ant-following birds were the only feeding guild remaining in entirely deforested areas; while the species richness of ground foraging and nesting species displayed a threshold at 52% and 74% of forest cover, respectively. Deforestation led to the replacement of specialized ant-following birds with generalist bird species with opportunistic attendance to army ant swarms (H2). Such a change in the ant-following bird community can be expected to have profound effects on the creation of ant-following bird flocks and the insect predation services provided by them.

The results of this study highlight the relevance of taking into account niche flexibility when evaluating the response of animal communities. Classifying birds into static ecological guilds might make it difficult to identify the most vulnerable species to forest loss and the traits that makes them weak (Edwards, Woodcock, et al., 2013). By re-classifying the ant-following bird species found in my study area into specific feeding, foraging and nesting guilds, I obtained new insights into the diversity of responses to deforestation. However, untangling the reasons why African ant-followers are especially sensitive to forest loss requires more detailed knowledge on their ecological and demographic features. Threshold levels will vary according to variables such as population size, variability among populations and the species’ vagility (Swift & Hannon, 2010). Additionally, as seen in this study, the possibility to test such thresholds with common methods like point counts is highly dependent on the probability of encounter of each species. While this study provides a baseline for evaluating the presence of ant-following bird species in diverse land-uses, structured monitoring strategies and more detailed ecological studies are required to understand and measure the use of resources and vulnerability of this bird community in West-African rainforests.

Overall, the conservation of ant-following bird species in South-West Cameroon requires the maintenance of areas with more than 83% of forest cover. The creation of large industrial plantations threatens the survival of most ant-following bird species and results in the disappearance of specialized ant-followers, which are key for the identification of army ant swarms and therefore for the assemblage of ant-following bird communities. The absence of many ant- following bird species from industrial oil palm plantations is also an indicator of their inability to cross large forest gaps and, therefore, should be taken as a warning of the possible effects of forest loss and fragmentation in the region. Agroforestry systems are, therefore, valuable systems for sustainable food production and avifauna conservation in Cameroon.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 31

REFERENCES

Andren, H. (1994). Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos, 355-366. Aratrakorn, S., Thunhikorn, S., & Donald, P. F. (2006). Changes in bird communities following conversion of lowland forest to oil palm and rubber plantations in southern Thailand. Bird Conservation International, 16(01), 71-82. Banks-Leite, C., Pardini, R., Tambosi, L. R., Pearse, W. D., Bueno, A. A., Bruscagin, R. T., Condez, T. H., Dixo, M., Igari, A. T., & Martensen, A. C. (2014). Using ecological thresholds to evaluate the costs and benefits of set-asides in a biodiversity hotspot. Science, 345(6200), 1041-1045. Betts, M. G., Forbes, G. J., & Diamond, A. W. (2007). Thresholds in songbird occurrence in relation to landscape structure. Conservation Biology, 21(4), 1046-1058. Bobo, K., Waltert, M., Fichtler, M., & Muehlenberg, M. (2005). New bird records for the Korup project area, Southwest Cameroon. Malimbus, 27(1), 13-18. Brown, J. R., Herrick, J., & Price, D. (1999). Managing low-output agroecosystems sustainably: the importance of ecological thresholds. Canadian Journal of Forest Research, 29(7), 1112-1119. doi:10.1139/x99-052 Cajas-Castillo, J. O., Cóbar-Carranza, A. J., Ávila-Santa, R. C., Cruz, C. K.-C., & Quiñónez- Guzmán, J. M. (2015). DIVERSIDAD DE AVES DE SOTOBOSQUE EN BOSQUES TROPICALES, ÁREAS DE REGENERACIÓN NATURAL Y CULTIVOS DE PALMA AFRICANA EN HUMEDALES DEL LAGO DE IZABAL, GUATEMALA. Ornitología Neotropical, 26, 1-12. CBFP, C. B. F. P. (2016). The Management and Business Plans of the Korup National Park, Cameroon goes under review. Retrieved 06.11, 2016,from http://pfbc- cbfp.org/news_en/items/korup-park.html. CEPF, C. E. P. F. (2000). Upper Guinean Forest Ecosystem of the Guinean Forests of West Africa Biodiversity Hotspot. Ecosystem Profile. Retrieved 30.10, 2016,from http://www.cepf.net/Documents/final.guineanforests.upperguineanforest.ep.pdf. Chuyong, G. B., Condit, R., Kenfack, D., Losos, E. C., Moses, S. N., Songwe, N. C., & Thomas, D. W. (2004). Korup forest dynamics plot, Cameroon. Tropical forest diversity and dynamism, 506-516. Collar, N., & J. del Hoyo, A. Elliott, J. Sargatal, D. A. Christie & E. de Juana. (2017). African thrush (Turdus pelios) [Handbook of the Birds of the World Alive]. Barcelona: Lynx Ediciones. del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A., & de Juana, E. (Eds.). (2016). Handbook of the Birds of the World Alive: Lynx Edicions, Barcelona. Retrieved from http://www.hbw.com/ Donnelly, R., & Marzluff, J. M. (2004). Importance of reserve size and landscape context to urban bird conservation. Conservation Biology, 18(3), 733-745. Dytham, C. (2011). Choosing and using statistics: a biologist's guide: John Wiley & Sons. Edwards, D. P., Hodgson, J. A., Hamer, K. C., Mitchell, S. L., Ahmad, A. H., Cornell, S. J., & Wilcove, D. S. (2010). Wildlife-friendly oil palm plantations fail to protect biodiversity effectively. Conservation Letters, 3(4), 236-242. doi:10.1111/j.1755-263X.2010.00107.x Edwards, D. P., Woodcock, P., Newton, R. J., Edwards, F. A., Andrews, D. J., Docherty, T. D., Mitchell, S. L., Ota, T., Benedick, S., & Bottrell, S. H. (2013). Trophic flexibility and the persistence of understory birds in intensively logged rainforest. Conservation biology, 27(5), 1079-1086. Edwards, F. A., Edwards, D. P., Hamer, K. C., & Davies, R. G. (2013). Impacts of logging and conversion of rainforest to oil palm on the functional diversity of birds in Sundaland. Ibis, 155(2), 313-326. doi:10.1111/ibi.12027 Fahrig, L. (2001). How much habitat is enough? Biological conservation, 100(1), 65-74. Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual review of ecology, evolution, and systematics, 34(1), 487-515. Ferraz, G., Nichols, J. D., Hines, J. E., Stouffer, P. C., Bierregaard, R. O., & Lovejoy, T. E. (2007). A large-scale deforestation experiment: effects of patch area and isolation on Amazon birds. science, 315(5809), 238-241. Fishpool, L., & Tobias, J., & J. del Hoyo, A. Elliott, J. Sargatal, D. A. Christie & E. de Juana. (2017a). Common bulbul (Pycnonotus barbatus) [Handbook of the Birds of the World Alive]. Barcelona: Lynx Ediciones.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 32

Fishpool, L., & Tobias, J., & J. del Hoyo, A. Elliott, J. Sargatal, D. A. Christie & E. de Juana. (2017b). Honeyguide greenbul (Baeopogon indicator) [Handbook of the Birds of the World Alive]. Barcelona: Lynx Ediciones. Fishpool, L., & Tobias, J., & J. del Hoyo, A. Elliott, J. Sargatal, D. A. Christie & E. de Juana. (2017c). Little Greenbul (Andropadus virens) [Handbook of the Birds of the World Alive]. Barcelona: Lynx Ediciones. Franks, N., & Bossert, W. (1983). influence of swarm raiding army ants on the patchiness and diversity of a tropical leaf litter ant community. Special publications series of the British Ecological Society. Friedman, J. H. (1991). Multivariate adaptive regression splines. The annals of statistics, 1-67. Fry, C., Keith, S., & Urban, E. (2004). The birds of Africa, vol. 7. Christopher Helm, London. Ghazoul, J., & Hellier, A. (2000). Setting critical limits to ecological indicators of sustainable tropical forestry. The International Forestry Review, 2(4), 243-253. Groombridge, B., & Jenkins, M. D. (2000). Global biodiversity: Earth's living resources in the 21st century: World Conservation Press. Harper, L. H. (1989). The persistence of ant-following birds in small Amazonian forest fragments. Acta Amazonica, 19, 249-263. Horne, J. F., & Short, L. L. (1990). Wax-eating by African common bulbuls. The Wilson Bulletin, 339-341. Huggett, A. J. (2005). The concept and utility of ‘ecological thresholds’ in biodiversity conservation. Biological conservation, 124(3), 301-310. Kattan, G. H., Alvarez‐López, H., & Giraldo, M. (1994). Forest fragmentation and bird extinctions: San Antonio eighty years later. Conservation Biology, 8(1), 138-146. Kofron, C., & Chapman, A. (1995). Deforestation and bird species composition in Liberia, West Africa. Tropical Zoology, 8(2), 239-256. Koh, L. P., & Wilcove, D. S. (2008). Is oil palm agriculture really destroying tropical biodiversity? Conservation Letters, 1(2), 60-64. doi:10.1111/j.1755-263X.2008.00011.x Kumar, A., & O'Donnell, S. (2007). Fragmentation and elevation effects on bird–army ant interactions in neotropical montane forest of Costa Rica. Journal of Tropical Ecology, 23(05), 581-590. Laudemann, C. (2015). The influence of habitat modification on bird communities with focus on biogeographical aspects in and around Korup National Park, Southwest Cameroon. Georg-August Universität, Göttingen, Germany. Lindenmayer, D., Fischer, J., & Cunningham, R. (2005). Native vegetation cover thresholds associated with species responses. Biological Conservation, 124(3), 311-316. Lucey, J. M., & Hill, J. K. (2012). Spillover of Insects from Rain Forest into Adjacent Oil Palm Plantations. Biotropica, 44(3), 368-377. doi:10.1111/j.1744-7429.2011.00824.x Maldonado-Coelho, M., & Marini, M. Â. (2004). Mixed-species bird flocks from Brazilian Atlantic forest: the effects of forest fragmentation and seasonality on their size, richness and stability. Biological Conservation, 116(1), 19-26. Maley, J. (2001). The impact of arid phases on the African rain forest through geological history. African rain forest ecology and conservation, 68-87. Martensen, A. C., Ribeiro, M. C., Banks‐Leite, C., Prado, P. I., & Metzger, J. P. (2012). Associations of forest cover, fragment area, and connectivity with neotropical understory bird species richness and abundance. Conservation Biology, 26(6), 1100-1111. Mas, A. H., & Dietsch, T. V. (2004). Linking shade coffee certification to biodiversity conservation: butterflies and birds in Chiapas, Mexico. Ecological Applications, 14(3), 642-654. Mbile, P., Vabi, M., Meboka, M., Okon, D., Arrey-Mbo, J., Nkongho, F., & Ebong, E. (2005). Linking management and livelihood in environmental conservation: case of the Korup National Park Cameroon. Journal of Environmental Management, 76(1), 1-13. Milborrow, S. (2011). Earth. R Package. Multivariate Adaptive Regression Splines. Derived from mda:mars by T. Hastie and R. Tibshirani Milborrow, S. (2016). Notes on the earth package. Plan National de Gestion de l'Environnement au Cameroun 1996. Ministry of Plan and Regional Development. (1989). Plan for developing the Korup National Park and its support zone. With support from World Wide Fund for Nature Commission of the European Communities and Overseas Development Natural Resources Institute: Republic of Cameroon, The Korup Project. Morante-Filho, J. C., Faria, D., Mariano-Neto, E., & Rhodes, J. (2015). Birds in anthropogenic landscapes: the responses of ecological groups to forest loss in the Brazilian Atlantic Forest. PloS one, 10(6), e0128923. Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 33

Nkongho, R. N., Ndjogui, T. E., & Levang, P. (2015). History of partnership between agro- industries and oil palm smallholders in Cameroon. Oilseeds and Fats, Crops and Lipids, 22(3). Ochoa‐Quintero, J. M., Gardner, T. A., Rosa, I., Barros Ferraz, S. F., & Sutherland, W. J. (2015). Thresholds of species loss in Amazonian deforestation frontier landscapes. Conservation Biology, 29(2), 440-451. Pamol, P. (2016). Our Business: Plantations and Planted Hectares Overview. Retrieved 06.11, 2016,from http://www.pamolplantationsplc.cm/html/our_business.html. Perfecto, I., Mas, A., Dietsch, T., & Vandermeer, J. (2003). Conservation of biodiversity in coffee agroecosystems: a tri-taxa comparison in southern Mexico. Biodiversity & Conservation, 12(6), 1239-1252. Perfecto, I., Rice, R. A., Greenberg, R., & Van der Voort, M. E. (1996). Shade coffee: a disappearing refuge for biodiversity. BioScience, 46(8), 598-608. Peters, M. K., Fischer, G., Schaab, G., & Kraemer, M. (2009). Species compensation maintains abundance and raid rates of African swarm-raiding army ants in rainforest fragments. Biological Conservation, 142(3), 668-675. doi:10.1016/j.biocon.2008.11.021 Peters, M. K., Likare, S., & Kraemer, M. (2008). Effects of habitat fragmentation and degradation on flocks of African ant-following birds. Ecological Applications, 18(4), 847-858. Peters, M. K., & Okalo, B. (2009). Severe declines of ant-following birds in African rainforest fragments are facilitated by a subtle change in army ant communities. Biological Conservation, 142(10), 2050-2058. doi:10.1016/j.biocon.2009.03.035 R Studio Team, R. (2015). RStudio: Integrated Development for R. RStudio, Inc. Boston, MA Radford, J. Q., Bennett, A. F., & Cheers, G. J. (2005). Landscape-level thresholds of habitat cover for woodland-dependent birds. Biological conservation, 124(3), 317-337. Ralph, C. J., Droege, S., & Sauer, J. R. (1995). Managing and Monitoring Birds Using Point Counts: Standards and Applications. In C. J. Ralph, J. R. Sauer & S. Droege (Eds.), Monitoring bird populations by point counts (pp. 181). Berkeley, California, USA.: Pacific South-West Research Station. Rappole, J. H., & King, D. I. (2003). Coffee and conservation. Conservation Biology, 17(1), 334- 336. Roberts, D. L., Cooper, R. J., & Petit, L. J. (2000). FLOCK CHARACTERISTICS OF ANT‐ FOLLOWING BIRDS IN PREMONTANE MOIST FOREST AND COFFEE AGROECOSYSTEMS. Ecological Applications, 10(5), 1414-1425. Rodewald, P. G., Dejaifve, P.-A., & Green, A. A. (1994). The birds of Korup National Park and Korup Project Area, Southwest Province, Cameroon. Bird Conservation International, 4(01), 1-68. Ruitenbeek, H. J. (1992). The rainforest supply price: a tool for evaluating rainforest conservation expenditures. Ecological Economics, 6(1), 57-78. Schmidt-Soltau, K. (2002). Conservation initiatives and local responses around Korup National Park (Cameroon) Symposium conducted at the meeting of the Annual Conference of the Association for Anthropology in Southern Africa, Rhodes University, Grahamstown (South Africa) Slabbekoorn, H., Smith, T. B., & Dunn, P. (2002). Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals. Evolution, 56(9), 1849-1858. Smith, T. B., Wayne, R. K., Girman, D. J., & Bruford, M. W. (1997). A role for ecotones in generating rainforest biodiversity. Science, 276(5320), 1855-1857. Sodhi, N. S., Liow, L., & Bazzaz, F. (2004). Avian extinctions from tropical and subtropical forests. Annu. Rev. Ecol. Evol. Syst., 35, 323-345. Stouffer, P. C., & Bierregaard, R. O. (1995). Use of Amazonian forest fragments by understory insectivorous birds. Ecology, 76(8), 2429-2445. Swift, T. L., & Hannon, S. J. (2010). Critical thresholds associated with habitat loss: a review of the concepts, evidence, and applications. Biological reviews, 85(1), 35-53. Tejeda-Cruz, C., Silva-Rivera, E., Barton, J., & Sutherland, W. (2010). Why shade coffee does not guarantee biodiversity conservation. Ecology and Society, 15(1). Vendras, E. (2014). Along a Gradient from Forest to Oil Palm Plantation: Influence of Habitat Modification on Plant and Bird Diversity in an Agroforestry Landscape in Southwest Cameroon (Master Thesis). Georg-August Universität, Göttingen, Göttingen, Germany.

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 34

Waltert, M., Bobo, K. S., Sainge, N. M., Fermon, H., & Mühlenberg, M. (2005). From forest to farmland: habitat effects on Afrotropical forest bird diversity. Ecological Applications, 15(4), 1351-1366. White, F. (1983). The vegetation of Africa. Paris, France: UNESCO. Willis, E. (1986). West African thrushes as safari ant followers. Le Gerfaut, 76(2), 95-108. Willis, E. O. (1979). The composition of avian communities in remanescent woodlots in southern Brazil: Departamento de Zoologia. Willis, E. O., & Oniki, Y. (1978). Birds and army ants. Annual Review of Ecology and Systematics, 9, 243-263. With, K. A., & King, A. W. (1999). Extinction Thresholds for Species in Fractal Landscapes. Umbrales de Extinción para Especies en Paisajes Fraccionados. Conservation Biology, 13(2), 314-326. doi:10.1046/j.1523-1739.1999.013002314.x

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 35

APPENDICES

Appendix 1.Summarized table of bird encounter frequency, bird species richness and percentage cover of each land-use type inside each village sampled during the study.Data from habitat percentages correspond to averages from the four plots located around each village. Bird encounter frequency and bird species richness indicate the total values for each village.

Near- Industrial primary Traditional palm Bird forest Forest plantations plantations encounter Bird Species Landscape Village percentage percentage percentage percentage frequency richness Bera 89.00 100.00 0 0.00 146 15 Korup National Erat 41.75 83.50 16.50 0.00 126 14 Park 166 14 Esukutan 83.50 97.25 2.75 0.00 Ikenge 77.75 80.50 19.50 0.00 95 15

Ekundukundu 80.50 83.50 16.50 0.00 132 15 Unprotected Fabe 50.00 80.75 19.25 0.00 108 16 agroforestry 77 15 Lipenja 8.25 75.25 24.75 0.00 Mokango/ Massaka 44.25 91.75 8.25 0.00 89 17

Center A 0.00 0.00 5.50 94.50 0 0 Oil Palm Ikassa Camp 8.25 33.25 11.00 55.75 18 8 Plantation 2 2 Makeke Camp 0.00 0.00 11.00 89.00 Mana Camp 2.75 2.75 0 97.25 1 1

Carolina María Ocampo-Ariza Beneficiaria Crédito-Beca Colfuturo, Promoción 2015

Appendix 2.Ant-following bird species observed during the bird survey with total number of records in the whole sampling (Total encounter frequency) and in each of the studied landscapes: KNP= Korup National Park; UA= Unprotected Agroforestry areas; OPP= Industrial oil palm plantations. Feeding guilds indicate dietary preferences: I= Insectivorous, diet entirely composed by insects; C= Other carnivorous, diet composed by insects, mollusks and other animal groups; F= frugivorous, diet mostly composed by fruit and seeds, with secondary consumption of insects; O= Omnivorous, diet composed by insects, with secondary consumption of plant material, such as fruits and seeds. Foraging location indicate the preferred vegetation stratus for foraging activities: 1=Ground; 2=Understory; 3= Foraging activity in all vegetation strata. Nesting location refers to the vegetation stratus selected for nest building: 1=Ground; 2=Understory. Forest specialist indicates whether the species has been found only in forest habitats (1) or in forests, as well as other habitats, such as savannahs, plantations and even anthropogenic areas (2). See del Hoyo (2016) for a detailed description of all ecological features.

Order Common name Feeding Foraging Nesting Forest Family Species guild location location specialist Lophoceros camurus Dwarf hornbill O 2 2 1 Bucerotiformes Western long-tailed 1 Bucerotidae Horizocerus albocristatus 3 2 hornbill O Coraciiformes Chocolate-backed 1 Alcedinidae Halcyon badia 2 2 kingfisher C Passeriformes Pycnonotus barbatus Common bulbul F 2 2 2 Yellow-whiskered 2 Andropadus latirostris 2 1 greenbul F Andropadus virens Little greenbul F 2 1 2 Baeopogon indicator Honeyguide bulbul F 2 2 2 Thescelocichla leucopleura Swamp palm bulbul F 2 2 2 Pycnonotidae Phyllastrephus icterinus Icterine bulbul O 1 2 1 Bleda syndactylus Red-tailed bristlebill O 2 2 2 Bleda notatus Lesser bristlebill O 1 2 2 Eastern bearded 1 Criniger chloronotus 1 2 greenbul O Criniger calurus Red-tailed greenbul O 1 2 2

Carolina María Ocampo-Ariza Beneficiaria Crédito-Beca Colfuturo, Promoción 2015

Appendix 2. Continuation

Passeriformes Rufous 2 Stizorhina fraseri 3 2 flycatcher thrush O White-tailed ant 2 Neocossyphus poensis 1 2 thrush O Red-tailed ant 1 Neocossyphus rufus 1 2 thrush I Turdidae Turdus pelios African thrush O 1 2 Brown-chested 1 Chamaetylas poliocephala 1 2 alethe C Fire-crested 2 Alethe castanea 1 2 alethe C Stiphrornis erythrothorax Forest robin I 1 2 2 Shepphardia cyornithopsis Lowland alakat I 1 2 2 Yellow-footed 1 Muscicapidae Muscicapa sethsmithi 2 2 flycatcher I Black-capped 1 Illadopsis cleaveri 1 2 illadopsis C Timaliidae Pale-breasted 1 Illadopsis rufipennis 1 2 illadopsis I Illadopsis fulvescens Brown illadopsis O 2 1 1 Dicruridae Dicrurus atripennis Shining drongo I 2 2 1

Carolina Ocampo-Ariza Beneficiaria Colfuturo, Prom 2015 38

Appendix 3.Occurrence thresholds for individual ant-following bird species based on percentage forest cover. All species here depicted were rejected from the main analyses, since the number of sampling points in which they occurred was inferior to the bottom boundary of the confidence interval for the whole group of species sampled in the study Tendency line is the product of a multivariate additive regression spline. Red dotted line indicates a change in the slope of the curve and, therefore, a potential threshold. Dots represent values for each study plot inside the three landscapes: KNP= Korup National Park; OPP= Industrial oil palm plantations; UA= Unprotected agroforestry areas and in the four land-use types: NPF= Near-primary forest; SF= Secondary forest; TP= Traditional plantations; IPP= Industrial palm plantations.

Carolina María Ocampo-Ariza Beneficiaria Crédito-Beca Colfuturo, Promoción 2015