Increased Sexual Dimorphism in Dense Populations of Olive-Backed Sunbirds on Small Islands: Morphological Niche Contraction in Females but Not Males

Emu - Austral Ornithology

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Increased sexual dimorphism in dense populations of Olive-backed Sunbirds on small islands: morphological niche contraction in females but not males

Darren P. O’Connell, David J. Kelly, Seán B. A. Kelly, Síofra Sealy, Adi Karya, Kangkuso Analuddin & Nicola M. Marples

To cite this article: Darren P. O’Connell, David J. Kelly, Seán B. A. Kelly, Síofra Sealy, Adi Karya, Kangkuso Analuddin & Nicola M. Marples (2019): Increased sexual dimorphism in dense populations of Olive-backed Sunbirds on small islands: morphological niche contraction in females but not males, Emu - Austral Ornithology, DOI: 10.1080/01584197.2019.1588743 To link to this article: https://doi.org/10.1080/01584197.2019.1588743

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Increased sexual dimorphism in dense populations of Olive-backed Sunbirds on small islands: morphological niche contraction in females but not males Darren P. O’Connell a,b, David J. Kelly a, Seán B. A. Kelly a, Síofra Sealya, Adi Karyac, Kangkuso Analuddin c and Nicola M. Marples a aDepartment of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland; bSchool of Biology & Environment Science, University College Dublin, Dublin, Ireland; cDepartment of Biology and Biotechnology, Universitas Halu Oleo, Kendari, Indonesia

ABSTRACT ARTICLE HISTORY Competition takes place not only between species but also within them. Intersexual competition Received 2 November 2018 for resources may increase sexual dimorphism in body size to minimise ecological niche overlap. Accepted 24 February 2019 Change in the level of sexual dimorphism in a species is a common feature of island radiations. KEYWORDS This is often interpreted as ecological release from interspecific competitors absent from small Sexual dimorphism; island islands, allowing niche expansion by both sexes of a dimorphic species. The Olive-backed Sunbird biogeography; competition; (Cinnyris jugularis) is a widespread island-colonising species found throughout the Indo-West Indo-West Pacific; Pacific. Here we investigate sexual dimorphism in morphological niche of Olive-backed Sunbird morphological niche; density populations in South-east Sulawesi, Indonesia. We found decreased overlap in morphological compensation niche between females and males on the species-depauperate Wakatobi Islands, in comparison to mainland Sulawesi and its larger continental islands, indicating greater sexual dimorphism on the small islands. This change in sexual dimorphism was associated with a decrease in the morphological niche hypervolume of females, but no change in males. Therefore there was no indication of expansion of morphological niche space in the absence of mainland competitors. These morphological differences were associated with the significantly higher population density of Wakatobi Olive-backed Sunbirds. Therefore this increased sexual dimorphism may serve to alleviate intraspecific competition for resources.

Introduction competition (Selander 1966; Desrochers 1989). This promotes selection for an accentuation of the pre-existing size Competition was proposed by Darwin (1859)asaprimary difference between males and females, facilitating resource driver of diversification. Competition for resources takes partitioning between the sexes (Slatkin 1984;Shine1989; place not only between species but within them (Doebeli Bolnick and Doebeli 2003) and increasing the overall niche 2011;Meiriet al. 2014). Intraspecific competition is space occupied by a species (Butler et al. 2007). typically at its strongest in high-density populations Sexual dimorphism in a species can initially arise (Robinson-Wolrath and Owens 2003; Pafilis et al. 2009). through a number of different processes such as natural Strong intraspecific competition can drive increased inter- selection for resource partitioning (Dayan and Simberloff individual diversity in resource use within a species 1994), sexual selection (Gittleman and Van Valkenburgh (Svanbäck and Bolnick 2007; Sheppard et al. 2018). This 1997) and fecundity selection (selection for larger females increased inter-individual variation in resource use leads to with greater reproductive capacity) (Scharf and Meiri awidernicheforthepopulationasawhole(Scottet al. 2013;Meiriet al. 2014). Regardless of how sexual 2003; Svanbäck and Persson 2004; Svanbäck and Bolnick dimorphism arose originally, a change in selection pres- 2005;Bolnicket al. 2007). Sexually dimorphic species pre- sure can lead to differences in the degree of sexual sent a special case of within-species niche differentiation, dimorphism between populations of the same species but have often been overlooked in studies of niche evolu- (Butler et al. 2007). This phenomenon has been studied tion (Bolnick and Doebeli 2003;Butleret al. 2007). Males most intensely in Caribbean Anolis lizards, where it has and females in sexually dimorphic species tend to occupy been shown that Anolis species broadly show greater different but interlinked niches (Doebeli 2011). If a popula- sexual dimorphism when there are fewer congeneric tion of a sexually dimorphic species experiences strong competitors on small islands, and less sexual dimorphism intraspecific competition it can take the form of intersexual

CONTACT Darren P. O’Connell [email protected] Supplemental data for this article can be accessed here. © 2019 BirdLife Australia 2 D. P. O’CONNELL ET AL. when they have more congeneric competitors on large and fruit resources (Sodhi et al. 1997; Higgins et al. 2006; islands (Lister 1976a, 1976b;Butleret al. 2007). Greater Cheke and Mann 2018). Olive-backed Sunbirds live in sexual dimorphism in island lineages may allow males pairs, though they can be found foraging singly, in pairs, and females to better use non-overlapping regions of in small groups with conspecifics and in interspecific niche space (Schoener 1967; Temeles et al. 2000;Butler flocks with other small passerines (Cheke and Mann et al. 2007). A similar pattern of increased sexual 2018). During the breeding season each pair defends a dimorphism has been noted in the island populations of small territory around their nest, while foraging more a diverse range of taxa (Selander 1966;Meiriet al. 2014), widely in the landscape (Higgins et al. 2006), with several including woodpeckers (Selander 1966), finches pairs often attracted to high-value patchily distributed (Ebenman and Nilsson 1982), mustelids (Dayan and resources such as flowering trees (pers. obs.). Olive- Simberloff 1994) and pythons (Pearson et al. 2002). backed Sunbirds can breed at any time of the year, though The increased sexual dimorphism seen in island most breeding activity is concentrated around peak per- populations is thought to be associated with (1) fewer iods, varying by region (Cheke and Mann 2018). In interspecific competitors, allowing species which suc- Sulawesi this breeding peak is typically between ceed in island colonisation to increase in density and September and March, most highly concentrated diverge into niche space usually occupied by mainland in December–January. The Olive-backed Sunbird is a competitors and (2) greater intraspecific competition resident species throughout its range, typically making due to higher population densities, driving intersexual only small local movements (Cheke and Mann 2018). niche divergence (Selander 1966; MacArthur et al. Two Olive-backed Sunbird subspecies are found in 1972; Butler et al. 2007; Greenberg and Olsen 2010). South-east Sulawesi. The subspecies C. j. infrenatus is A recent meta-analysis by Meiri et al.(2014) of sexual found on mainland Sulawesi and its continental islands, dimorphism in lizards and carnivorous mammals while C. j. plateni is found on the Wakatobi Islands (Kelly found that the number of competitor species was not and Marples 2011;O’Connell et al. 2017; Cheke and linked to sexual dimorphism, calling into question Mann 2018). The two subspecies are similar, with some whether release from interspecific competition plays a minor plumage differences. Sulawesi C. j. infrenatus role in increased sexual dimorphism. Meiri et al.(2014) males have characteristic yellow supercilial and malar highlight the need for further research assessing the stripes, while Wakatobi C. j. plateni males lack these relative roles that interspecific and intraspecific com- features entirely, have generally darker upperparts, and petition may have in sexual dimorphism, particularly have a deeper yellow breast and abdomen which is reg- in island radiations. While increased sexual dimorph- ularly tinged with orange (Hartert 1903; Kelly and ism in individual traits has been noted in many species, Marples 2011;Kelly2014). Females from both popula- few studies have quantified dimorphism in multidi- tions look quite similar; however, Sulawesi C. j. infrenatus mensional morphological niche space, or directly females have strong yellow supercilial stripes which are related niche space to metrics of intraspecific competi- greatly reduced and duller in Wakatobi C. j. plateni tion such as population density (though see Butler et al. females. Both male and female C. j. plateni are slightly (2007) and Greenberg and Olsen (2010)). smallerinbodysizethanC. j. infrenatus individuals In the heart of the Wallacea region, the south-eastern (Kelly 2014). While recent research has suggested that peninsula of Sulawesi provides an excellent study system several Olive-backed Sunbird subspecies may represent to test how natural selection on small islands may affect genetically distinct species (Lohman et al. 2010;Eaton sexual dimorphism (Figure S1). There are continental et al. 2016), there is only minor separation in mitochon- islands (Buton, Muna and Kabaena) which were con- drial DNA between C. j. infrenatus and C. j. plateni (Kelly nected to Sulawesi at the time of the last glacial max- 2014), which falls below the level indicating a species-level imum, around 20 000 years ago (Voris 2000), and oceanic split (Hebert et al. 2004;Kerret al. 2007). islands (including the Wakatobi Islands) which have On the mainland and continental islands there are never been connected to the Sulawesi mainland seven ecologically similar, generalist small passerine spe- (Milsom and Ali 1999;NugrahaandHall2018). The cies which may compete directly or indirectly with the region is home to the Olive-backed Sunbird (Cinnyris Olive-backed Sunbird for resources; the Brown-throated jugularis), an extremely successful island coloniser, with Sunbird (Anthreptes malacensis), Black Sunbird a wide range stretching from Southeast Asia to north-east (Leptocoma aspasia), Crimson Sunbird (Aethopyga sipar- Australia (Cheke and Mann 2018). It shows distinct sex- aja), Lemon-bellied White-Eye (Zosterops chloris), Pale- ual dimorphism in plumage and body size, with males bellied White-Eye (Zosterops consobrinorum), Grey-sided larger than females. The Olive-backed Sunbird is a gen- Flowerpecker (Dicaeum celebicum) and Yellow-sided eralist forager, feeding on a variety of invertebrate, nectar Flowerpecker (Dicaeum aureolimbatum)(Eatonet al. EMU - AUSTRAL ORNITHOLOGY 3

2016). In particular, the Olive-backed Sunbird has been islands are relatively large; Sulawesi: 180 680 km2,Buton: noted as being subordinate in the foraging hierarchy to 4408 km2, Kabaena: 873 km2, with a maximum altitude of theBrown-throatedSunbirdandBlackSunbirdelsewhere 3455, 1190 and 1560 m respectively (UN System-wide in its range (Noske 1995; Coates and Bishop 1997). On Earthwatch 1998). Peninsular South-east Sulawesi, Buton the Wakatobi Islands there are only three such ecologi- and Kabaena are home to a diversity of habitats with cally similar passerine species present. The Lemon-bellied important remaining areas of forest and concentrations of White-Eye and Grey-sided Flowerpecker are present biodiversity, though they have suffered from significant throughout the Wakatobi Islands (Kelly and Marples recent deforestation (Wardill et al. 1998; Gillespie et al. 2010), with both Wakatobi populations being recently 2005;Martinet al. 2012, 2018a;O’Connell et al. 2017). proposed as new species, the 'Wakatobi White-eye' The Wakatobi Islands are limestone islands formed (Zosterops flavissimus) and 'Wakatobi Flowerpecker’ through uplift of fossil coral reefs (Clifton 2003;Nugraha (Dicaeum kuehni) respectively (Kelly et al. 2014; and Hall 2018), which have never been connected to main- O'Connell et al. in press). An unnamed white-eye species land Sulawesi (Milsom and Ali 1999). Sampling was carried (the ‘Wangi-wangi White-Eye’) is found only on the most out on the Wakatobi Islands Wangi-wangi, Oroho, northern Wakatobi Island (Wangi-wangi) (Eaton et al. Kaledupa, Hoga, Lintea Selatan, Tomia and Binongko 2016; O'Connell et al. in press). (Figure S1). They are small (Wangi-wangi: 155 km2, We hypothesised that (1) there would be greater sexual Oroho: 13 km2,Kaledupa:63km2,Hoga:3.5km2,Tomia: dimorphism in Olive-backed Sunbird populations on the 53 km2,LinteaSelatan:8.3km2 and Binongko: 99 km2) Wakatobi Islands than in the mainland system (mainland (Daft Logic 2018a), and low lying (Wangi-wangi: 274 m, Sulawesi and the continental islands), (2) greater sexual Kaledupa: 203 m, Tomia: 271 m, Binongko: 222 km, dimorphism would be accompanied by an expansion in Oroho, Hoga and Lintea Selatan: <20 m) (UN System- morphological niche volume in both sexes in the absence wide Earthwatch 1998;MilsomandAli1999;pers.obs.). of interspecific competitors, and (3) greater sexual Buton is only 27 km distant from Wangi-wangi, which dimorphism would be accompanied by higher population forms a northern Wakatobi group with Oroho, Kaledupa density in Olive-backed Sunbirds, likely increasing intras- and Hoga (Kelly et al. 2014). There is a 16 km gap from pecific competition. To investigate these hypotheses we Kaledupa to Tomia, which forms the southern Wakatobi had three associated research goals; to measure the over- group with Lintea Selatan and Binongko (Daft Logic lap in morphological niche between female and male 2018b). In comparison to the mainland system, the Olive-backed Sunbirds on each island to test for a differ- Wakatobi Islands are relatively dry and lacking in habitat ence in sexual dimorphism between the mainland system diversity (Kelly and Marples 2010;O’Connell et al. 2018). and the Wakatobi Islands (Hypothesis 1), ascertain any The Wakatobi Islands are largely covered in scrub and differences in morphological niche volumes for female or mixed farmland, with some patches of remaining forest male Olive-backed Sunbirds between the mainland sys- and mangrove fringes, with the small islets of Oroho and tem and the Wakatobi Islands (Hypothesis 2), and assess Lintea Selatan the least heavily developed (pers. obs.). the population density of Olive-backed Sunbirds across Mist-nets were used to trap birds for sampling. the study area (Hypothesis 3). Trapped birds were colour ringed for easy identification if re-trapped. Coates and Bishop (1997) and Eaton et al.(2016) were used for species identification and for Materials and methods the ageing and sexing of trapped birds. The morphological measurements wing length (maximum chord), Study site and sampling bill length (tip of bill to the base of the skull), and mass Sampling was carried out throughout South-east Sulawesi (grams) were taken (Svensson 1992; Redfern and Clark (Figure S1), on research expeditions undertaken between 2001). All measurements were taken by a single recor- 1999 and 2017 in the months of June–September der (N.M.M.). Only adult birds were included in mor- (just before the main breeding season for Olive-backed phological analyses. Birds in wing moult were excluded Sunbirds in Sulawesi), by N.M.M., D.J.K., A.K., S.B.A.K., from analyses. Mist-netting was carried out in habitats S.S. and D.O.C. Olive-backed Sunbirds were sampled on 10 used by Olive-backed Sunbirds, including a variety of islands throughout the region for this study. The mainland scrub, forest-edge, farmland and mangrove habitats. system consisted of the island of Sulawesi, and its nearby To establish Olive-backed Sunbird population den- continental islands Buton (6 km distant) and Kabaena sities where they were mist-netted, line-transects were (16 km distant), which were connected to Sulawesi at the carried out in the vicinity of mist-netting sites, in the time of the last glacial maximum (Milsom and Ali 1999; same habitats. Transects were 1 km in length and only Robinson-Dean et al. 2002;NugrahaandHall2018). These Olive-backed Sunbirds up to 25 m either side of this 4 D. P. O’CONNELL ET AL. transect were recorded. A relatively tight boundary for the dispersion of trait values to be quantified for (25 m) on either side of the transect line was chosen female and male Olive-backed Sunbirds, along with to ensure both a minimum of false recordings due to how much the trait space of females and males over- identification errors (female Black and Brown-throated lap on each island. To calculate this hypervolume Sunbirds could be mistaken for Olive-backed Sunbirds we used dynamic range boxes implemented in the at moderate distances) and because the greater the Rpackage‘dynRB’ (Junker et al. 2016), which recording distance, the greater chance of failing to provided a non-parametric approach to quantify record individuals in the survey area. Therefore each n-dimensional hypervolumes. This method was transect surveyed an area of 5 ha. Transects were car- chosen as it employs a quantile-based approach ried out from 6:00 to 8:30 a.m., during the peak of bird that is very robust to outliers, which can be proble- activity. Each transect was surveyed only once. All matic when using other approaches to calculating Olive-backed Sunbirds seen or heard within the survey hypervolumes (Blonder 2018). For each group area were recorded. Male, female and unidentified sex assessed, ‘dynRB’ calculates the size of that group’s (recorded by call) Olive-backed Sunbirds were all n-dimensional hypervolume, and the proportion of added together to give a total count of Olive-backed that hypervolume that overlaps with each other group Sunbirds recorded for the survey area. D.O.C., S.B.A. is assessed. Hypervolumes and overlap values were K., D.J.K., S.S. and A.K. carried out the transects, bounded between 0 and 1. ensuring that at least two recorders participated in In brief, paraphrasing Kuppler et al.(2017), dynamic each transect at a recommended pace of 1–2 km/h range boxes work by calculating a number of m nested (Bibby et al. 2000). Line transects were chosen over standardised range boxes for each population under con- alternative methods for assessing population density sideration (female and male Olive-backed Sunbirds on such as point counts, as the foraging ranges of several each island). Each box contains a decreasing percentage Olive-backed Sunbird pairs can overlap, therefore mul- of values per dimension n =1,…, n,startingwiththe tiple pairs can visit the same area during a survey interval consisting of the 0-quantile (= minimum) and session (particularly if near high-value nectar the 1-quantile (= maximum) in every dimension and resources). This characteristic would make population shrinking in m steps to a degenerated interval containing AðÞα BðÞα estimation difficult for a stationary survey such as a only the medians. Letting Rn i and Rn i denote the point count, as a surveyor could not be certain whether ith range box corresponding to the nth dimension of the they were recording the same, or new, individuals. By first and the second population (A and B), respectively, surveying a greater area and moving while surveying, then their volume and the portion of the first in the α line transects are more likely to record only new indi- second and vice versa (for every i) are computed. viduals (Bibby et al. 2000). A GPS unit was used to Calculating the product of the resulting quantities finally measure the length and mark the locations of each yields what we will refer to as the morphological niche transect. volume (vol(A)) and morphological niche overlap (port (A, B)), which is the portion of the morphological niche of population B covered by the morphological niche of Quantification of overlap in morphological niche population A (i.e. how much the morphological niche of All statistical analyses were performed in R software female and male Olive-backed Sunbirds overlaps on each v. 3.5.1 (R Core Team 2018). To quantify the overlap island). For a full description of this approach see Junker in morphological niche, we utilised the concept of et al.(2016), Kuppler et al.(2017) and Blonder (2018). As n-dimensional hypervolumes (Hutchinson 1957). In each morphological trait was on a different scale, they this framework we defined the morphological niche were first re-scaled using the scale function in R (R Core as the three-dimensional hypervolume produced Team 2018). from the combination of the three morphological Using the dynamic range box method we calculated variables measured. Bill length, wing length and the morphological niche volume for female and male body mass provide only a limited assessment of over- Olive-backed Sunbirds on each island sampled. We uti- all morphological niche, but are three of the most lised the aggregation method ‘mean’ in ‘dynRB’ as this is commonly used morphological measurements in the most suitable for evaluating similarity between two avian biology (Svensson 1992; Redfern and Clark niches (Junker et al. 2016). The aggregation method 2001) and provide an important indication of diet ‘mean’ takes the arithmetic mean of the side lengths of (bill length) and body size (wing length and body each range box (rather than the product or geometric mass) (Grant 1965, 1968). Using a hypervolume mean). To investigate sexual dimorphism between female approach to calculating morphological niche allowed and male Olive-backed Sunbirds, the proportion of the EMU - AUSTRAL ORNITHOLOGY 5 morphological niche that overlapped between females (R Core Team 2018). QQ-plots of the residuals of each and males on each island was calculated. The proportion test were used to ensure that the assumption of a of morphological niche overlap provided a measure of normal distribution was not violated. sexual dimorphism in each population, i.e. less overlap in morphological niche indicated greater sexual dimorphism between female and male Olive-backed Sunbirds. A Results Welch two-sample t-test was carried out to test for a difference in the proportion of morphological niche Sexual dimorphism in morphological niche volume overlap between the mainland system and the Wakatobi A total of 246 Olive-backed Sunbirds (93 female, 153 ’ Islands populations. In addition, a Welch two-sample male) were trapped; 72 (27 female, 45 male) across the t-test was carried out to test for a difference in the total mainland system and 174 (66 female, 108 male) across morphological niche volume between the mainland sys- seven of the Wakatobi Islands (Figure S1; Table S1). ’ tem and the Wakatobi Islands populations, for both Olive-backed Sunbirds on the Wakatobi Islands were female and male Olive-backed Sunbirds. QQ-plots of more sexually dimorphic thaninthemainlandsystem,as the residuals of each test were used to ensure that the shown by there being significantly less overlap in morpho- assumption of a normal distribution was not violated. logical niche on the Wakatobi Islands than in the mainland The morphological niche overlap values were log trans- system (Welch t-test t = 2.8702, df = 5.7836, P <0.05) formed to conform to a normal distribution. (Figure 1; Figure S2; Table S2). The morphological niche volume of female Olive-backed Sunbirds was significantly Individual morphological traits smaller on the Wakatobi Islands than in the mainland system, indicating a narrower range of trait values in the To further assess morphological sexual dimorphism, Wakatobi population (Welch t-test t = 3.0359, df = 3.8873, bill length, wing length and body mass were investi- P < 0.05) (Figure 2). There was no difference in the gated individually. Two-way ANOVAs were carried morphological niche volume of male Olive-backed out for these three traits to test for any difference Sunbirds between the two areas (Welch t-test t = 1.0307, between the mainland system and Wakatobi Islands df = 7.7805, P = 0.3336). for both females and males, and to test for any inter- action between sex and zone. Testing for an interac- tion between sex and zone provided an assessment of Individual morphological traits whether there was a change in the level of sexual dimorphism in the trait being tested. Tukey honest Wing length was significantly longer in the mainland sys- significant difference (HSD) tests were used as a post temthanintheWakatobiIslands(ANOVA:F1, 242 =34.49, hoc to the ANOVAs. QQ-plots of the residuals of each P < 0.001) (Figure 3). In addition there was a change in the test were used to ensure that the assumption of a level of sexual dimorphism in wing length between the normal distribution was not violated. mainland system and Wakatobi Islands (ANOVA: F1, 242 =5.35,P < 0.05), caused by the larger decrease in wing length in Wakatobi Island females in comparison Population density to mainland females (Tukey HSD: mean diff. = −1.64, Differences in population density of Olive-backed Padj< 0.001), than was seen between Wakatobi Island Sunbirds between islands were tested by modelling males and mainland males (Tukey HSD: mean diff. = −0.75, transect counts of Olive-backed Sunbirds with a gen- Padj< 0.01) (Figure 3). Bill length was significantly longer eralised linear model (GLM) with Poisson errors. As a in the mainland system than in the Wakatobi Islands post hoc to the GLM, a Tukey HSD test was carried out (ANOVA: F1, 242 =35.63,P < 0.001) (Figure S3). using the ‘glht’ function in the R package ‘multcomp’ However, there was no change in sexual dimorphism (Hothorn et al. 2008). The Tukey HSD post hoc between the mainland system and Wakatobi Islands allowed for pairwise comparisons to be carried out (ANOVA: F1, 242 = 0.17, P = 0.68) as both females and between all islands, and this method corrects for multi- males showed a similar decrease (female – Tukey HSD: ple comparisons (Maxwell and Delaney 2018). Year, mean diff. = −0.67, Padj< 0.001; male – Tukey HSD: mean month and island area were included in the initial diff. = −0.58, Padj< 0.001). There was no significant model but dropped from the final model after model change in body mass between the mainland system and selection using AIC, R2 and standard plots of model fit Wakatobi Islands (Figure S4). 6 D. P. O’CONNELL ET AL.

−0.75

−0.50

−0.25

0.00 Sulawesi Wakatobi OBSB Morphological Niche Overlap ±OBSB Morphological Niche SE Zone

Figure 1. Bar plot showing the mean (± SE) proportion of morphological niche overlap between female and male Olive-backed Sunbirds (OBSB) on Sulawesi and the continental islands, and on the Wakatobi Islands. Note: values plotted are log10 transformed and on a negative scale, so a larger volume (Wakatobi) indicates less morphological niche overlap.

0.8

0.6

zone

0.4 SUL WAK

0.2 OBSB Niche Volume ± SE Volume OBSB Niche

0.0

Female Male Sex

Figure 2. Bar plot showing the mean morphological niche volume (± SE) of female and male Olive-backed Sunbirds (OBSB). Zone abbreviations: SUL – Sulawesi mainland and continental islands, WAK – Wakatobi Islands.

Transect results than in the mainland system (Tukey HSD: P <0.001 for all comparisons) (Table S4). Within the Wakatobi A total of 114 transects were carried out; 67 across the Islands, Olive-backed Sunbirds had a significantly three continental islands and 47 across five of the higher density on Tomia than Kaledupa (Tukey Wakatobi Islands (Wangi-wangi, Kaledupa, Hoga, HSD: estimate ± SE = 0.30908 ± 0.09678, P <0.05), Tomia and Binongko) (Table S3). There was a signifi- but there were no other significant differences. cant difference in the density of the Olive-backed Within the mainland system, Kabaena had a signifi- Sunbird populations between islands (Poisson GLM: cantly higher density of Olive-backed Sunbirds than pseudo R2 =0.77,Z = 50.277, P <0.001)(Figure 4; 7106 Sulawesi (Tukey HSD: estimate ± SE = 0.60044 Table S3). The Olive-backed Sunbird had a signifi- ± 0.1698, P <0.01)orButon(TukeyHSD: cantly higher density on all of the Wakatobi Islands EMU - AUSTRAL ORNITHOLOGY 7

Sex Female Male Mainland Wakatobi

51 Wing Length (mm)

SUL BUT KAB WAN ORO KAL HOG TOM LIN BIN Island

Figure 3. Wing length of Olive-backed Sunbirds on each island in the mainland system and Wakatobi Islands. Island abbreviations: SUL – Sulawesi mainland, BUT – Buton, KAB – Kabaena, WAN – Wangi-wangi, ORO – Oroho, KAL – Kaledupa, HOG – Hoga, TOM – Tomia, LIN – Lintea Selatan and BIN – Binongko.

zone

SUL WAK 10 OBSB mean count ± SE

SUL BUT KAB WAN KAL HOG TOM BIN Island

Figure 4. Bar plot showing the mean transect count (± SE) of Olive-backed Sunbirds (OBSB) across the study area. Zone abbreviations: SUL – Sulawesi mainland and continental islands, WAK – Wakatobi Islands. Island abbreviations: SUL – Sulawesi mainland, BUT – Buton, KAB – Kabaena, WAN – Wangi-wangi, KAL – Kaledupa, HOG – Hoga, TOM – Tomia and BIN – Binongko. estimate ± SE = 0.98083 ± 0.21909, P < 0.001). Buton results showed increased sexual dimorphism in popula- and Sulawesi did not differ (Table S4). tions on small islands, demonstrated by a decrease in intersexual morphological niche overlap in populations on the small Wakatobi Islands, in comparison to the main- Discussion land system (Figure 1;FigureS2;TableS2),supporting This study assessed sexual dimorphism in an island-colo- Hypothesis 1. In addition, we found that Olive-backed nising passerine bird, to assess whether it followed the Sunbirds were found in significantly higher density on expectation of increased sexual dimorphism in small island the Wakatobi Islands (Figure 4), supporting Hypothesis populations and what might be driving this. This was the 3. However, we did not find any evidence for an expansion first assessment of this pattern in the Nectariniidae. Our of morphological niche in the absence of several mainland 8 D. P. O’CONNELL ET AL. interspecific competitors; rather, we found a decrease in Olive-backed Sunbird showed a decrease in morphological themorphologicalnichevolumeforfemaleOlive-backed niche volume (Figure 2).ThemaleOlive-backedSunbirdis Sunbirds, and no change for males (Figure 2). When heavier and is therefore likely to be the dominant forager individual traits were assessed it was found that there was (Francis et al. 2018), so in a population with increased a change in sexual dimorphism of wing length, an impor- intraspecific competition the female is likely to experience tant body size variable, with females decreasing in wing stronger selection to avoid intersexual competition (Peters length more than males on the Wakatobi Islands (Figure and Grubb 1983; Desrochers 1989). The foraging ecology 3). Therefore Hypothesis 2 was not supported. Assessing of the Olive-backed Sunbird may mean that females these results together, we provide no indication of a direct experience more resource competition with males than a effect of interspecific competition on sexual dimorphism, species with a stricter territory boundary. The Olive- but evidence that intersexual competition promotes mor- backed Sunbird is not strictly territorial in terms of its phological niche divergence in high-density populations. foraging territory; small groups of Olive-backed Sunbirds The Olive-backed Sunbird populations assessed fol- will sometimes forage together and several pairs may be lowed the expected pattern of increased sexual dimorphism drawn to valuable resources such as flowering trees (pers. in populations on small islands (Selander 1966;Butleret al. obs.; Cheke and Mann 2018).Thelargerdecreaseinwing 2007)(Figure 1). This was associated with significantly length seen in female Olive-backed Sunbirds on the higher density in the Wakatobi Island Olive-backed Wakatobi Islands (Figure 3), in comparison to males, Sunbird populations (Figure 4). While there were some may reflect a decrease in body size due to selection for differences in density between islands within the mainland avoidance of direct competition with males. In a similar system and Wakatobi Islands (Figure 4;TableS4),the case, Dayan and Simberloff (1994)foundthatanincrease strongest pattern was a consistently higher density on all in sexual dimorphism in mustelids on a smaller, more of the small oceanic Wakatobi Islands than on any of the species-depauperate island was due to a morphological larger continental islands. Increased population density in niche shift in females, not males. As in this study, male island-colonist populations, on species-depauperate mustelids were the larger sex on both islands, and this islands, is known as density compensation (MacArthur sexual dimorphism was exaggerated on a smaller island et al. 1972). This phenomenon has been noted in a wide by females showing reduced body size. range of taxa, and has been associated with reduced species The lack of any expansion of morphological niche richness on islands, potentially leading to less interspecific volume may indicate that the Olive-backed Sunbird’s competition for resources and lower predation pressure morphological niche was not being limited by interspeci- (Nilsson 1977;George1987; McGrady-Steed and Morin fic competitors on the Sulawesi mainland. While the 2000; Rodda and Dean-Bradley 2002; Buckley and Jetz increased density of Olive-backed Sunbird populations 2007; Longino and Colwell 2011). The greater access to on the Wakatobi Islands indicated it probably has access resources provided by freedom from interspecific competi- to more resources than on the mainland (Grant 1966), tion can allow successful colonists of species-depauperate resource partitioning with the additional competitors on islands to reach far higher densities than they do in main- the mainland may have been temporal or spatial rather land systems (Whittaker and Fernández-Palacios 2007). than morphological (Schoener 1974; Albrecht and Gotelli Intraspecific competition is at its most intense in these 2001; Robertson et al. 2014). Additionally it is possible high-density populations (Robinson-Wolrath and Owens that resources are more limiting on the Wakatobi Islands, 2003;Pafiliset al. 2009), and can drive selection for diver- preventing morphological niche expansion. When inves- sificationwithinapopulation(Bolnick2004; Svanbäck and tigating whether Leaf-Warblers in species-depauperate Bolnick 2007), such as increased sexual dimorphism areas of the Himalayas experienced character release, (Greenberg and Olsen 2010; Greenberg and Danner 2013). Ghosh-Harihar and Price (2014) actually found that Unexpectedly, we found no expansion in morphologi- they showed niche contraction, likely due to less diversity calnichevolumeforeitherfemaleormaleOlive-backed of prey in the species-depauperate areas. The Wakatobi Sunbirds on the Wakatobi Islands, in conditions with Islands exhibit little habitat diversity (Kelly and Marples reduced interspecific competition. An expansion in mor- 2010;O’Connell et al. 2018) and may lack the resource phological niche in response to reduced interspecific com- base for morphological niche expansion. The change in petition on islands has been inferred as a major factor bill length of the Wakatobi Olive-backed Sunbird popula- driving greater sexual dimorphism in insular populations tion does suggest a change in foraging ecology and may (Selander 1966;Butleret al. 2007; Greenberg and Olsen reflect an adaptation to a different resource base on the 2010). However, no change was found in male Olive- Wakatobi Islands (Figure S3). These results must be inter- backed Sunbird morphological niche volume between the preted with caution as only three morphological traits Wakatobi and the mainland system, while the female were used in our assessment of morphological niche. EMU - AUSTRAL ORNITHOLOGY 9

Further research, incorporating a larger number of mor- morphological niche in order to avoid direct competition phological traits, and assessing feeding and competitive with males. The sunbirds of the Indo-West Pacific pro- behaviour in these Olive-backed Sunbird populations, vide an ideal group for further study into sexual dimorph- and the resource availability on different islands, would ism in island radiations, and the relative effect of give great insight into these results. intraspecific and interspecific competition on morpholo- Another avenue of research that may shed light on gical niche. A wider assessment of sexual dimorphism in these results would be to investigate the effect of preda- sunbird radiations may yield great insight into this pro- tion pressure on our study populations. Predators can cess. Gaining a greater understanding of how competition both depress population and alter the foraging ecology of may drive adaptation provides further insight into how species (George 1987; Laundré et al. 2014), therefore biodiversity is generated and maintained. predation pressure will likely affect both population size and morphological niche. Two notable predators of small passerine birds present on the mainland, the Vinous- Acknowledgements breasted Sparrowhawk (Accipiter rhodogaster)and We thank Kementerian Riset Teknologi Dan Pendidikan Dwarf Sparrowhawk (A. nanus), are absent from the Tinggi (RISTEKDIKTI) for providing the necessary permits Wakatobi Islands (Eaton et al. 2016), as is the Little and approvals for this study; permit numbers: 0143/SlP/FRP/ Bronze-Cuckoo (Chalcites minutillus), a known brood SM/Vll/2010, 278/SlP/FRP/SM/Vll/2012, 279/SIP/FRP/SM/ VIII/2012, 174/SIP/FRP/E5/Dit.KI/V/2016, 159/SIP/FRP/E5/ parasite of Olive-backed Sunbird nests (Cheke and Fit.KIVII/2017 and 160/SIP/FRP/E5/Fit.KIVII/2017. Also, we Mann 2018;Payneet al. 2018). This may contribute to would like to thank all of the research assistants who con- the higher density of the Olive-backed Sunbird on the tributed across many field seasons. Wakatobi. A lack of avian predators may also have allowed for the decreased wing length (particularly in females) seen in the Wakatobi Islands’ populations Author contributions (Figure 3), as loss of dispersal ability in island populations D.J.K., N.M.M., K.A., D.O.C. and A.K. conceived this study. has been associated with decreased predation pressure D.J.K., N.M.M., D.O.C., S.B.A.K., S.S. and A.K. carried out (Wright et al. 2016). However, more study is required, fieldwork. D.O.C. carried out the analyses and led the writ- ing. All authors contributed to revising and improving the as the distribution of these species is poorly known in the manuscript. region (Eaton et al. 2016; Martin et al. 2018b), and little is known about potential non-avian predators, particularly on the Wakatobi Islands. Funding This study highlighted the morphological shifts in an This research was supported by an Irish Research Council island radiation of a sexually dimorphic small passerine. PhD fellowship awarded to D.O.C; Irish Research Council Our results provide evidence of density compensation in [13046]. Operation Wallacea provided logistical support for small island populations of the Olive-backed Sunbird and the Indonesian fieldwork. an association between population density and increased sexual dimorphism. Intersexual competition may there- ORCID fore be the key driver in this process. We found no evidence of a direct effect of interspecific competition, Darren P. O’Connell http://orcid.org/0000-0001-9331- but more research is needed to understand the relation- 8189 ship between species richness and sexual dimorphism. David J. Kelly http://orcid.org/0000-0002-5880-4162 Seán B. A. Kelly http://orcid.org/0000-0002-3078-8404 While we found no direct effect of interspecific competi- Kangkuso Analuddin http://orcid.org/0000-0003-0258- tion, it may be that the true effect of reduced species 9376 richness is an indirect one. No expansion in morpholo- Nicola M. Marples http://orcid.org/0000-0003-4693-2607 gical niche was found on the Wakatobi Islands, but the higher population densities found on the Wakatobi References Islands suggest that certain resources are abundant. Less interspecific competition may therefore allow access to a Albrecht, M., and Gotelli, N. J. (2001). Spatial and temporal narrow but abundant band of resources (i.e. common niche partitioning in grassland ants. Oecologia 126, 134– flowering plants which all sunbirds would exploit), lead- 141. doi:10.1007/s004420000 ‘ ing to higher population densities. In these circumstances Bibby, C. J., Burgess, N., and Hill, D. (2000). Bird Census Techniques,’ 2nd edn. (Academic Press: London). greater intraspecific, and in particular intersexual, com- Blonder, B. (2018). Hypervolume concepts in niche- and petition may have promoted selection in female Olive- trait-based ecology. Ecography 41, 1441–1455. backed Sunbirds to become more specialised in their doi:10.1111/ecog.03187 10 D. 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