Plumage-Based Phylogenetic Analyses of the Merops Bee-Eaters

Ibis (2004), 146, 481–492

Blackwell Publishing,Plumage-based Ltd. phylogenetic analyses of the Merops bee-eaters

D. BRENT BURT* Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85712, USA

I review previous systematic work on the family Meropidae and present phylogenetic hypotheses derived from my analyses of colour, pattern and shape variation in 30 plumage regions among species and subspecies in this family. Consistent patterns are seen across shallow portions of the trees. Uncertainty remains concerning the placement of several deep branches within this group’s phylogeny. In particular, the phylogenetic placement of Meropogon forsteni and Merops breweri, M. ornatus, M. hirundineus and M. boehmi remains uncertain. The biogeographical patterns in the resultant trees are similar with either a Southeast Asian or African origin for the family, with most of the early diversiﬁcation occurring in Africa, and with multiple independent subsequent invasions of non-African areas.

The bee-eaters, family Meropidae, are a group of and further behavioural observations. The major areas 26 species of brightly coloured coraciiform birds. of disagreement between the conclusions of these They are distributed throughout the palaeotropics two researchers concern the placement of four forest and southern Eurasia (Fry 2001). Bee-eaters display species. Fry’s Merops gularis and M. muelleri are placed a great range of diversity in several ecological and in a separate genus (Meropiscus) in Boetticher’s clas- behavioural traits, including breeding systems, migratory sification. Fry’s Merops breweri and Meropogon forsteni habits, foraging behaviours and nest-site preferences are placed into the genus Nyctyornis in Boetticher’s (Fry 1969, 1984, Fry & Fry 1992, Burt 1996). These classification. Furthermore, Fry (1969) places the African traits could be subjects of productive comparative forest-dwelling M. breweri among African savanna studies. However, to make a valid comparative study Merops species whereas Boetticher places this species of any of these traits, we must first know the phylo- with Asian forest species. Fry later revised his views, genetic relationships within the group. agreeing that M. breweri’s closest relative may be The relationships among families in the Order Meropogon forsteni (Fry 1984, p. 203). Relationships Coraciiformes are uncertain because of early and rapid among bee-eater species from these previous systematic diversification of these lineages (Cracraft 1981, Sibley studies were based primarily on each author’s intuitive & Ahlquist 1990). Few systematic studies of the family feel for the characters considered. The analyses have been completed previously and no studies of reported here are the first to reconstruct the phylo- the family have utilized molecular data. Von Boetticher genetic relationships within the family using explicit, (1951) primarily used plumage colour and shape cladistic methods. characters to derive a classification for the family. Fry In this study, I reconstruct the evolutionary rela- (1969) used behavioural, biogeographical, ecological tionships among the species in the family Meropidae and plumage colour/shape characters to derive a using data on variation in plumage colour, pattern phenetic classification and tree. Fry (1984) later modi- and shape (see Appendix). Results are presented fied the placement of certain lineages using informa- from two maximum parsimony-based analyses with tion from geographical distributions of subspecies either species or subspecies as terminal taxa. I then examine the biogeographical distribution of each lineage to uncover potential patterns of geographical *Present address: Department of Biology, Stephen F. Austin State University, Box 13003 SFA Station, Nacogdoches, TX 75962- origin and dispersal. Finally, I compare the results of 3003, USA. my analyses with the previous phenetic studies of Email: [email protected] this group by Fry (1969, 1984).

that transitions between similarly coloured character METHODS states are easier than they are to other coloured character states (e.g. orange-red to red easier than Specimens and plumage characters either is to blue). Two data matrices were used in the study: one with Three basic levels of transition rules were used in species as terminal taxa and one with subspecies as construction of step matrices. It is assumed that each terminal taxa. Single specimens from each of the level represents an increasingly difficult transition nominate subspecies were first examined to docu- between colours. The easiest level of transition was ment the basic plumage character patterns of each that between green and green with blue tips, chestnut species. Multiple individuals of each sex from each and red chestnut, and between dark greenish-brown of the geographically defined subspecies (Fry 2001) and light greenish-brown. The next level of transition were then examined to document the extent of char- linked all greens together and these to greens mixed acter variation within and among taxa. with other colours. Also in this transition level were Thirty plumage regions were scored for colour, similar rules for blues, oranges and reds. The most pattern and shape using museum study skins and spirit difficult level of transition was that between more specimens (see Appendix). Data from spirit specimens distant colours. No attempt was made to construct were excluded when specific plumage colours had more detailed step matrices for relationships between evidently faded. Evidence of fading was derived by colours of more distant spectral affinity. Although comparison of plumage colours from study skins and complex, these step matrices are actually quite illustrations in Fry and Fry (1992). Detailed structural conservative while still utilizing much of the informa- components of feathers consistently associated with tion available in each multistate plumage character. carotenoid pigments suggest homology of these colours Character step matrices can be accessed in the data (Fry 1969). Plumage characters were retained only files at the TreeBASE website (www.treebase.org/ if they were invariant within subspecies in analyses. treebase. S 1021). Subspecies identified as distinct by Fry (2001) were An alternative method of extracting the same combined if they did not differ in plumage characters information is to break each multistate plumage (Nyctyornis athertoni athertoni = N. a. brevicaudata, character into multiple, individual characters. That Merops hirundineus hirundineus = M. h. furcatus, M. method was not used in this study because it would pusillus meridionalis = M. p. argutus, M. bullockoides artificially inflate the number of independent char- bullockoides = M. b. randorum, M. orientalis cyanophrys acters in each data matrix. That is, certain characters = M. o. muscatensis, M. o. viridissimus = M. o. flavoviridis, would contain character states that could not exist, M. superciliosus superciliosus = M. s. alternans). M. given any character state in certain other characters. nubicus and M. nubicoides are considered as distinct An example illustrates how this problem could occur. phylogenetic species owing to their disjunct breeding The step matrix for the forecrown colour has three distributions and plumage differences. Sexual dichro- basic transition classes. The first transition class matism is rare in bee-eaters, but in cases where it does represents slight changes among species with green in occur, the dichromatic characters were coded as the forehead. In some cases the basic green forehead polymorphic for that taxon. Data matrices can be is only slightly modified by the addition of faint accessed at the TreeBASE website (www.treebase.org/ blue tips and this slight difference is indicated by a treebase. S 1021). The subspecies data matrix and cost of only a single step. Other transitions from the character descriptions are documented in the basic green involve more complex changes such Appendix. as the addition of other colours (e.g. orange, brown) throughout the forehead region. These more complex changes result in an increased cost of two Character step matrices steps. Finally, some species have either a chestnut or Each plumage region typically has a large array of reddish-chestnut forehead, probably indicating that colours when examined across all geographically these species are closely related, and therefore transi- distinct subspecies. Each plumage region is repre- tions between these two colours cost only a single sented here as a single character with several colour step in the matrix. All other transitions are between or shape character states. Each multistate character colours of more distant spectral affinity and therefore is linked to character-specific step matrices to retain cost three steps. It is possible to represent these additional information. Character step matrices assume basic colour changes in the forehead as different

characters (e.g. ‘basic green or not’, ‘green with other branch swapping in each analysis. The starting trees colour or not’, ‘chestnut or not’), but the characters are for branch swapping were derived by stepwise addi- not then independent. That is, if the forehead is chestnut, tion of taxa. The number of TBR islands represented it cannot be green. Although the independence of in the MPT set and the number of replicates in characters in most phylogenetic analyses is typically which they were found is reported to indicate the assumed and not tested, one should not knowingly thoroughness of searches (Maddison 1991). Permu- use non-independent characters (Farris 1983). tation tail probability test (PTP) results (using 1000 replicates), and consistency index (CI), retention index (RI), rescaled consistency index (RC) and homoplasy Plumage characters and bootstrap index (HI) values are given to indicate the strength analysis of structure and levels of homoplasy in both species The nature of the characters used in this study and subspecies data matrices. provides one significant analytical problem. Bootstrap Relationships among the families of the order analyses are reliable estimates of the information Coraciiformes are unclear because of long diver- content of data matrices and the relative probabili- gence times among the families (Cracraft 1981, ties of each node in resultant reconstructions rep- Sibley & Ahlquist 1990). The choice and utility of resenting those in the true phylogeny (Felsenstein outgroup taxa among these families are therefore 1988, Hillis & Bull 1993). Bootstrapping measures questionable. Instead, the trees were rooted between the variation present in the characters of a data matrix the two species of the probable basal genus Nyctyornis and how representative this subset of characters is and the remaining bee-eater lineages. Evidence for of the larger distribution of all possible characters. the basal placement of this genus is seen in the DNA– Multiple bootstrap pseudoreplicate matrices are DNA hybridization data of Sibley and Ahlquist (1990: created by sampling characters with replacement figure 359). Comparisons of the trees’ fit to biogeo- from the original data matrix. Use of this technique graphical patterns were examined by mapping assumes that characters are independent. In this geographical distributions on each phylogenetic study, a great deal of information is contained in each hypothesis using MacClade (version 4.0, Maddison of the large multistate characters (and its relevant & Maddison 2000). Breeding distributions were taken step matrix). The amount of information lost during from Fry (1984). the creation of each bootstrap replicate by leaving out any single, large, multistate character is therefore RESULTS much greater than that lost when using more con- ventional characters. Bootstrap analyses in this case Phylogenetic reconstructions result in overly conservative bootstrap consensus trees with very little resolution. This problem can The analysis using the subspecies matrix resulted in be corrected if each multistate plumage character is 2016 MPTs with 826 steps (PTP results: P = 0.001, broken into multiple characters. However, we then CI = 0.652, RI = 0.7465, RC = 0.487, HI = 0.338). have the problem of non-independence discussed This single TBR island of trees was found in 558 of above. Therefore, regardless of how characters are 1000 search replicates. The strict consensus tree coded in this study, use of the bootstrap technique from this MPT set is shown in Figure 1. The analysis is not appropriate. using the species matrix resulted in four MPTs with 816 steps (Fig. 2; PTP results: P = 0.001, CI = 0.603, RI = 0.491, RC = 0.296, HI = 0.344). Two trees each Phylogenetic analyses options were reconstructed in two TBR tree islands. These PAUP* (version 4.0b10, Swofford 2002) was used to islands were found in 147 and 389 of 1000 search carry out maximum parsimony phylogenetic analy- replicates. ses. I conducted heuristic searches because of the number of taxa in both the species and the subspe- Biogeographical patterns cies data matrices. All the most parsimonious trees (MPTs) were retained. To increase the chance that Biogeographical patterns are similar for trees from the most parsimonious solution would be found, analyses of both subspecies and species matrices 1000 random addition sequence searches were (Fig. 3). Trees show the origin of the family as either conducted with tree bisection and reconnection (TBR) Southeast Asia or Africa, with much of the early

Figure 1. The strict consensus tree of 2016 most parsimonious trees from the analysis of the subspecies data matrix. diversification of the family occurring in Africa. In all M. philippinus are also apparent in most of the resultant trees, Meropogon forsteni shows a pattern of invasion trees. Subspecies group into species clusters, if not of Indonesia from African ancestors. Several always clades, for all species except M. orientalis. additional invasions of non-African areas are seen in This species has six subspecies of which one, M. clades associated with basal branches in the genus orientalis ferrugeiceps, does not group with the other Merops. Figure 3(a) shows more uncertainty in subspecies in the species (Fig. 1). Finally, Meropogon biogeographical patterns due to two deep polytomies. forsteni is placed within the Merops clade in all trees. Assuming an African origin would show simultaneous Certain taxa, however, vary conspicuously in their diversification within Africa and invasion of non- placement among trees (i.e. M. apiaster, M. boehmi). African areas. However, it is also possible to show Comparing trees between analyses shows more un- early diversification in Asia with a later invasion of certainty over the placement of certain deep branches Africa in this tree. of the tree. The branching order of lineages in the Meropogon forsteni to M. albicollis clade is consistent. However, the branching order of lineages involving DISCUSSION M. hirundineus – M. ornatus, M. viridis – M. leschenaulti Several consistent patterns can be seen when trees and M. persicus – M. superciliosus – M. philippinus and from each analysis are examined. First, certain clades the problematic lineages M. apiaster and M. boehmi are consistent across the shallow portions of the trees is less consistent. (Meropogon forsteni – Merops breweri – M. muelleri – M. gularis, M. pusillus – M. variegatus – M. oreobates, Comparison with earlier systematic work M. malimbicus – M. nubicus – M. nubicoides, M. hirundineus – M. ornatus, M. viridis – M. leschenaulti). The only attempt to reconstruct explicit phylogenetic Furthermore, certain lineages consistently group together relationships within the family Meropidae prior to in sequential evolutionary patterns coming off the this study was that of Fry (1969). In that study, main backbone of the Merops clade (M. bulocki – M. a combination of morphological, biogeographical, bullockoides, M. revoilii – M. albicollis). The close rela- ecological and behavioural characters was used to derive tionships among M. persicus, M. superciliosus and a phenetic-based hypothesis of species relationships.

Figure 2. Four most parsimonious trees from the analysis of the species data matrix.

Fry’s hypothesis is represented by a figure of a ‘cross- subspecies analysis also suggests that M. v. lafresnayii section through the top of a phylogenetic tree’ (Fry might represent a distinct lineage just above M. oreobates 1969: p. 587) reproduced in Figure 4. and at the base of the M. variegatus – M. pusillus clade. Comparisons between trees in this study with Previous researchers have debated this possibility Fry’s species groups and superspecies show areas of because of the relative colorations and sizes of agreement and conflict. Each tree in this study shows individuals in these lineages (reviewed in Fry 1969). Fry a sister species relationship between M. philippinus also placed M. boehmi and M. orientalis in a species and M. superciliosus. Fry includes M. ornatus with group. This arrangement is not supported by this each of these species in a species group. This study study; however, neither is there any strong support does not support a close relationship between M. ornatus for the placement of M. boehmi between any specific and M. philippinus or M. superciliosus. In fact, each branches in this study. The close relationships between tree in this study supports a sister species relationship several other species in this study show additional between M. ornatus and M. hirundineus. Fry places general consistencies with Fry’s hypothesis: N. amictus M. hirundineus in a species group with M. pusillus – N. athertoni, M. gularis – M. muelleri, M. bulocki – and the superspecies M. variegatus and M. oreobates. M. bullockoides, M. revoilii – M. albicollis, M. malimbicus This study supports a strong relationship among the – M. nubicus – M. nubicoides, M. viridis – M. leschenaulti latter three species; however, each tree shows a sister – M. apiaster. relationship between M. variegatus and M. pusillus, The basal relationship of Meropogon forsteni to the not between M. variegatus and M. oreobates. The Merops bee-eaters in Fry’s hypothesis is quite different

Figure 3. Reconstructions of biogeographical patterns. (a) Strict consensus tree from subspecies analysis. (b) Representative species tree. Biogeographical patterns are similar for each of the four species trees. from the pattern seen in this study. The placement primarily African Merops seems to be more intuitive of the Indonesian Meropogon forsteni well within an and would further suggest an Asian origin for the African clade in my reconstructions seems biogeo- family. Furthermore, differing rib numbers and graphically improbable. Branching of this species structure are reported for this species, setting it apart between the Asian/Indonesian Nyctyornis and the from both Merops and Nyctyornis (Fry 1969, 1984).

I thank Hilary Fry and Stephen Emlen for addressing basic bee-eater questions early in this study. Judie Bronstein, Priscilla Coulter, David Maddison, Wayne Maddison, Nancy Moran and Dan Papaj provided constructive com- ments on early drafts of the manuscript. Hilary Fry, David Parkin and an anonymous reviewer provided helpful com- ments on the submitted manuscript. The University of Kansas Museum of Natural History, the U.S. National Museum of Natural History and the Natural History Museum (Tring) graciously allowed access to their collec- tions. Financial support was provided by the University of Arizona Department of Ecology and Evolutionary Biology, the Silliman Memorial Fund, the Research Training Group in the Analysis of Biological Diversiﬁcation, and the U.S. National Science Foundation (Dissertation Improve- ment Award) and the Stephen F. Austin State Univer- sity College of Science and Mathematics and Department of Biology.

REFERENCES

Figure 4. (a) Diagram of a cross-section of the top of a von Boetticher, H. 1951. La systématique des guêpiers. Oiseau phylogenetic tree. Circles describe distance relationships with Rev. Fr. Ornithol. 5: 194–199. respect to Merops pusillus (6). Bottom to top of figure represents Burt, D.B. 1996. Phylogenetic and ecological aspects of coop- general advancement of characters from plesiomorphic states. erative breeding in the bee-eaters (Aves: Meropidae). PhD Dashed-line circles represent species groups. Dotted-line dissertation, University of Arizona, Tucson. circles represent superspecies. Shaded areas equal forest, Cracraft, J. 1981. Toward a phylogenetic classification of unshaded equals savanna. Black dots = Nyctyornis amictus the recent birds of the world (Class Aves). Auk 98: 681–714. and N. athertoni; hatched dot = Meropogon forsteni; numbers = Farris, J.S. 1983. The logical basis of phylogenetic analysis. Merops: (1) gularis, (2) muelleri, (3) bullockoides, (4) bulocki, (5) In Platnick, N.I. & Funk, V.A. (eds) Advances in Cladistics. hirundineus, (6) pusillus, (7) variegatus, (8) oreobates, (9) Proceedings of the Second Meeting of the Willi Hennig breweri, (10) revoilii, (11) malimbicus, (12) nubicus, (13) Society, Vol. 2: 7–36. New York: Columbia University Press. albicollis, (14) boehmi, (15) orientalis, (16) ornatus, (17) Felsenstein, J. 1988. Phylogenies from molecular sequences: superciliosus, (18) philippinus, (19) viridis, (20) leschenaulti, inference and reliability. Ann. Rev. Genet. 22: 521–565. (21) apiaster. Reproduced from Fry (1969). Fry, C.H. 1969. The evolution and systematics of bee-eaters (Meropidae). Ibis 111: 557–592. Fry, C.H. 1984. The Bee-Eaters. Calton, Staffordshire: Poyser. Fry, C.H. 2001. Family Meropidae (Bee-eaters). In del Hoyo, J., Elliott, A. & Sargatal, J. (eds) Handbook of the Birds of the World, Vol. 6: 286–341. Barcelona: Lynx Edicions. Fry (1969) suggests M. breweri is most closely Fry, C.H. & Fry, K. 1992. Kingfishers, Bee-Eaters and Rollers. related to his M. pusillus species group. In this study, A Handbook. Princeton: Princeton University Press. the forest-dwelling M. breweri is consistently associ- Hillis, D.M. & Bull, J.J. 1993. An empirical test of bootstrapping ated in some manner with other forest species: as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42: 182–192. M. muelleri, M. gularis and Meropogon forsteni. As Maddison, D.R. 1991. The discovery and importance of multiple mentioned in the introduction, Fry (1984: p. 203) islands of most-parsimonious trees. Syst. Zool. 40: 315–328. revised his views, stating that M. breweri’s closest Maddison, D.R. & Maddison, W.P. 2000. Macclade 4: Analysis of relative may be Meropogon forsteni. This sister-group Phylogeny and Character Evolution, Version 4.0. Sunderland, relationship is supported in part by this study MA: Sinauer Associates. Sibley, C.G. & Ahlquist, J.E. 1990. Phylogeny and Classification (several of the trees used to form Fig. 1, two trees in of Birds: a Study in Molecular Evolution. New Haven, CT: Fig. 2). Yale University Press. Additional phylogenetic data, particularly sequence Swofford, D.L. 2002. PAUP*. Phylogenetic Analysis Using data, are needed to test the phylogenetic hypotheses Parsimony (*and Other Methods), Version 4.0b10. Sunderland, presented here. These data could be especially import- MA: Sinauer Associates. ant for a better understanding of the phylogenetic Received 5 June 2003; revision accepted 6 February 2004. placement of Meropogon forsteni, M. breweri, M. First published online early on 25 May 2004; ornatus, M. hirundineus and M. boehmi. doi: 10.1111/j.1474-919x.2004.00289.x

APPENDIX

Subspecies data matrix

Character number

Subspecies 12345678910

Nyctyornis amictus 0016500000 Nyctyornis athertoni 0410004104 Meropogon forsteni 2227611200 Merops breweri 3338722200 Merops muelleri muelleri 044D4723201 Merops muelleri mentalis 04E1723201 Merops gularis gularis 0331722203 Merops gularis australis B33 5722203 Merops hirundineus hirundineus 5510330210 Merops hirundineus chrysolaimus 0511330210 Merops hirundineus heuglini 5510330210 Merops pusillus pusillus 4155854214 Merops pusillus meridionalis 4153854214 Merops pusillus cyanostictus 0151854214 Merops pusillus ocularis 4153854214 Merops variegatus variegatus 4155944214 Merops variegatus loringi 4151944214 Merops variegatus bangweoloensis 4155944214 Merops variegatus lafresnayii 0151944214 Merops oreobates B15 1944214 Merops bulocki bulocki 41505046 5 21 4 Merops bulocki frenatus 0151175214 Merops bullockoides 6661285214 Merops revoilii 7AA124A214 Merops albicollis 6772246214 Merops boehmi 9889194214 Merops orientalis orientalis CCF 01A6214 Merops orientalis viridissimus 5510400210 Merops orientalis cleopatra 5510400214 Merops orientalis cyanophrys 04111A0214 Merops orientalis beludschicus CCF 01A6214 Merops orientalis ferrugeiceps 98801A7211 Merops persicus persicus D45 43B4214 Merops persicus chrysocercus D41 43B0210 Merops superciliosus superciliosus 6BB22CB216 Merops philippinus ADG119C216 Merops ornatus 41001D5A214 Merops viridis viridis EEHA1AD217 Merops viridis americanus 98891A7211 Merops leschenaulti leschenaulti 9889857211 Merops leschenaulti quinticolor 9889857321 Merops leschenaulti andamanensis 9889857331 Merops apiaster 61 1 8 43E7211 Merops malimbicus 899B288215 Merops nubicus FFCCBF9212 Merops nubicoides FFCCA6E218

Subspecies data matrix continued

Character number

Subspecies 11 12 13 14 15 16 17 18 19 20

Nyctyornis amictus 000 0000000 Nyctyornis athertoni 133 0210141 Meropogon forsteni 000 0222022 Merops breweri 100 0222033 Merops muelleri muelleri 215 2043253 Merops muelleri mentalis 275 6?4?353 Merops gularis gularis 362 2043450 Merops gularis australis 362 2?4?450 Merops hirundineus hirundineus 062 1256164 Merops hirundineus chrysolaimus 021 4?5?164 Merops hirundineus heuglini 021 4?5?164 Merops pusillus pusillus 133 0163164 Merops pusillus meridionalis 133 0263164 Merops pusillus cyanostictus 133 0?6?164 Merops pusillus ocularis 133 0?6?164 Merops variegatus variegatus 133 0263164 Merops variegatus loringi 133 0?6?164 Merops variegatus bangweoloensis 133 0?6?164 Merops variegatus lafresnayii 133 0?6?164 Merops oreobates 133 0063164 Merops bulocki bulocki 133 0176150 Merops bulocki frenatus 133 0?7?150 Merops bullockoides 131 7276170 Merops revoilii 162 7185175 Merops albicollis 132 8091575 Merops boehmi 133 8291117 Merops orientalis orientalis 133 92911468 Merops orientalis viridissimus 000 9?9?199 Merops orientalis cleopatra 133 9?9?199 Merops orientalis cyanophrys 133 9?9?141 Merops orientalis beludschicus 133 9?9?146 Merops orientalis ferrugeiceps 133 9?9?186 Merops persicus persicus 133 9185167 Merops persicus chrysocercus 000 918?167 Merops superciliosus superciliosus 133 01856A7 Merops philippinus 72248181667 Merops ornatus 122 A274164 Merops viridis viridis 122 3171148 Merops viridis americanus 122 3?7?186 Merops leschenaulti leschenaulti 02207171064 Merops leschenaulti quinticolor 022 3?7?064 Merops leschenaulti andamanensis 02204?7?064 Merops apiaster 443 71858764 Merops malimbicus 554 5275970 Merops nubicus 622 B235 AB A Merops nubicoides 822 B235 A50

Subspecies data matrix continued

Character number

Subspecies 21 22 23 24 25 26 27 28 29 30 31

Nyctyornis amictus 000 A00000101 Nyctyornis athertoni 0A1 1100 00102 Meropogon forsteni 022 22111101 Merops breweri 133 B9111113 Merops muelleri muelleri 024 46022223 Merops muelleri mentalis 024 46122223 Merops gularis gularis 049 C8033333 Merops gularis australis 0B9 C803 3333 Merops hirundineus hirundineus 277 53211113 Merops hirundineus chrysolaimus 277 53211113 Merops hirundineus heuglini 277 53211113 Merops pusillus pusillus 355 B4300013 Merops pusillus meridionalis 955 B4300013 Merops pusillus cyanostictus A55 B430 0013 Merops pusillus ocularis 955 B4300013 Merops variegatus variegatus 555 64300003 Merops variegatus loringi 555 64300003 Merops variegatus bangweoloensis B55 6430 0003 Merops variegatus lafresnayii C53 B430 0003 Merops oreobates A33 B900 0013 Merops bulocki bulocki 086 35011113 Merops bulocki frenatus 086 35011113 Merops bullockoides 086 35000013 Merops revoilii 086 33000013 Merops albicollis 66A 73100413 Merops boehmi 070 03100013 Merops orientalis orientalis DCC 5B1 0 001 2 Merops orientalis viridissimus D70 DA10 0013 Merops orientalis cleopatra DCC 5B1 0 001 4 Merops orientalis cyanophrys 6CC 5310 0014 Merops orientalis beludschicus DCC 5B1 0 00124 Merops orientalis ferrugeiceps DC5 5B1 0 00102 Merops persicus persicus 0CC DA10 00124 Merops persicus chrysocercus 0CC DA10 0013 Merops superciliosus superciliosus 07C DA15 5613 Merops philippinus 07C D31445101 Merops ornatus 870583100016 Merops viridis viridis 0CC 5310 00101 Merops viridis americanus 0CC 5310 0010 Merops leschenaulti leschenaulti 4D1 8C01 11102 Merops leschenaulti quinticolor 7D1 8301 1111 Merops leschenaulti andamanensis 4D1 8C01 1110 Merops apiaster 717 53116272023 Merops malimbicus 098 97167843 Merops nubicus 09B 93178953 Merops nubicoides 09B 93178953

12. Rump: 0. green, 1. chestnut-light blue, 2. blue, Characters and character state 3. green, blue tips, 4. yellow-green, 5. grey, slight 1. Forehead: 0. light blue, 1. yellow and white, red, 6. light blue, 7. blue-purple. 2. deep blue-purple, 3. black, 4. green with blue 13. Upper tail coverts: 0. green, 1. blue, 2. light blue, tips, 5. green, 6. white, 7. pied, 8. grey, 9. chestnut, 3. green, blue tips, 4. greyish red, 5. deep purple. a. light blue and green, b. little light blue, c. 14. First rectrix, dorsal: 0. green, 1. light blue, white green with orange, d. white and light blue, e. red tip, 2. dark blue to black, 3. blue, 4. blue-green, chestnut, f. greenish blue. white tip, 5. reddish black, 6. purple, 7. blue- 2. Forecrown: 0. lilac, 1. green with blue tips, green, 8. blue-green, black tip, 9. green, black 2. deep purple, 3. black, 4. light blue, 5. green, tip, 10. blue, black tip, 11. red to black tip. 6. white, 7. dark brown, 8. chestnut, 9. grey, 15. First rectrix rachis, dorsal: 0. black, 1. brown, a. pied, b. dark greenish-brown, c. green with 2. dark brown. orange, d. light greenish brown, e. red chestnut, 16. Outer rectrix, ventral: 0. proximal yellow, distal f. greenish blue. black, 1. yellow, 2. orange-brown to brown m 3. Hindcrown: 0. orange and green, 1. green, 2. deep to L, 3. darker light brown, 4. black, 5. brown, purple and brown, 3. black, 4. light blue, 5. white tips, 6 p to d, orange-brown, black, white?, green with blue tips, 6. orange, 7. dark brown, 8. 7. brown, 8. light brown, 9. light brown, dark tip. chestnut, 9. grey, a. pied, b. dark greenish- 17. Outer rectrix rachis, ventral: 0. yellow, 1. off- brown, c. greenish-blue, d. blue, e. purple, f. green white, 2. orange-brown, 3. tan to black distally, with orange, g. light greenish brown, h. red 4. off-white to brown distally, 5. tan, 6. brown. chestnut. 18. Scapulars: 0. green, 1. green with blue, 2. chest- 4. Supercilium: 0. green, 1. light blue, 2. white, nut, 3. chestnut-orange, 4. black, 5. green with 3. small blue, 4. white and blue, 5. very little orange, 6. greenish brown, 7. yellow-orange, blue, 6. green and lilac, 7. deep purple, 8. black, 8. yellow-orange with green, 9. grey, slight red, 9. chestnut, a. red chestnut, b. grey, c. greenish- a. red. blue. 19. Chin: 0. blue then red, 1. chestnut, 2. black 5. Infracilium: 0. green, 1. light blue, 2. white, 3. light then purple, 3. black, 4. blue, 5. red, 6. yellow, blue and white, 4. very little blue, 5. green and 7. white, 8. bluish-green, 9. green, a. yellow and red, 6. deep purple, 7. black, 8. yellow, 9. white white, b. greenish blue. and yellow, a. red, b. greenish blue. 20. Throat: 0. red, 1. blue, green sides, 2. deep purple, 6. Cheek: 0. green, 1. deep purple, 2. black, 3. 3. black, 4. yellow, 5. white, 6. bluish-green, white and blue, 4. white, 5. yellow, 6. red, 7. red 7. chestnut, 8. blue, 9. green, a. greenish blue. and blue, 8. red and white, 9. blue and chestnut, 21. Gorget: 0. none, 1. chestnut, 2. light blue, dark a. blue, b. blue and green, c. white, yellow and blue, 3. light blue, black, chestnut, 4. chestnut, chestnut, d. yellow and blue, e. white and yellow, black, 5. white, light blue, dark blue, chestnut, f. greenish blue. 6. light blue, black, light blue, 7. black, 8. chestnut, 7. Nape: 0. green, 1. dark brown, 2. black, 3. deep black, blue, 9. white, light blue, black, chestnut, purple, 4. green with blue, 5. orange, 6. orange- a. light blue, dark blue, black, chestnut, b. white, green, 7. chestnut, 8. grey, 9. red, a. green with light blue, dark blue-black, chestnut, c. light blue over orange, b. dark greenish brown, c. light blue, dark blue, chestnut, d. green-blue, black, greenish-brown, d. red chestnut, e. orange red. green-blue. 8. Lore: 0. lilac and red, 1. green, 2. black, 3. black 22. Breast: 0. red, green sides, 1. greenish-blue, 2. and chestnut. deep purple, 3. yellow-orange, 4. black and 9. Eyestripe: 0. none, 1. black, 2. chestnut, 3. black iridescent blue, 5. orange-yellow-green, 6. light and chestnut. green, 7. green, 8. orange-brown, 9. red, a. blue, 10. Mantle: 0. green, 1. chestnut, 2. red, 3. black, green sides, b. black and iridescent blue with red, 4. green, blue tips, 5. grey, 6. light greenish-brown, c. green with blue, d. yellowish green. 7. red chestnut, 8. orange red. 23. Flank: 0. green, 1. green and yellow, 2. brown- 11. Back: 0. green, 1. green, blue tips, 2. chestnut, grey, 3. yellow-orange, 4. blue, 5. orange-yellow- 3. black, 4. yellow and chestnut, 5. grey, slight green, 6. orange-brown, 7. greenish-blue, 8. red, red, 6. red, 7. light greenish-brown, 8. orange 9. iridescent blue and black, a. light green, red. b. orange-red, c. green with blue.

24. Belly: 0. green, 1. green and yellow, 2. brown- 28. Lesser coverts: 0. green, blue tips, 1. green, grey, 3. buff, 4. blue, 5. greenish-blue, 6. yellow- 2. chestnut, 3. black, 4. light greenish-brown, green, 7. greenish-white, 8. light green-blue, 5. dark greenish-brown, 6. green with chestnut, 9. red, a. light green, b. orange-yellow-green, 7. grey, 8. red. c. iridescent blue, d. green with blue. 29. Median and greater coverts: 0. green, blue 25. Undertail coverts and vent: 0. light green, 1. yellow, tips, 1. green, 2. chestnut, 3. black, 4. green 2. burnt orange, green tips, 3. light blue, 4. buff, with orange, 5. light greenish-brown, 6. dark 5. blue-purple, 6. blue, 7. reddish-grey, 8. iridescent greenish-brown, 7. green with chestnut, 8. grey, blue, 9. orange, green tips, a. green with blue, 9. red. b. greenish blue, c. light green-blue. 30. Tertials: 0. green, 1. green, blue tips, 2. chestnut, 26. Tail shape: 0. square, 1. streamer, 2. forked, 3. black, 4. grey, 5. red, blue tips. 3. slight fork. 31. Distribution: 0. Southeast Asia, 1. Indonesia, 27. Marginal coverts: 0. green, blue tips, 1. green, 2. India, 3. Africa, 4. Middle East, 5. Eurasia, 2. chestnut, 3. black, 4. light greenish-brown, 6. Australasia. 5. dark greenish-brown, 6. grey, 7. red.