J . Zool., Lond. (1992) 228, 625-640

The behavioural and morphological affinities of some vanelline plovers (Vanellinae: Charadriiformes: Aves)

DAVID WARD

Department of Zoology and Entomology, University of Natal, P.O. Box 375, Pietermaritzburg 3200, South Africa

(Accepted 2 September 1991)

(With 6 figures in the text)

The behavioural displays of six species of vanelline plover (Vanellus, Charadriidae, Charadrii- formes) in southern Africa and Israel were recorded in the field. Using those displays considered to be systematically useful, I compared the relationships between species using behavioural and morphological characters. In general, the relationships between species using behaviour and morphology were congruent. The placement of the blackwinged plover Vane//us melanopterus and lesser blackwinged plover V . lugubris in a superspecies (Snow, 1978) was not supported by either behavioural or morphological data. The superspecific status of the blacksmith plover V. armatus and spurwinged plover V. spinosus proposed by Snow (1978) was supported by both data sets examined here. The morphological data examined indicate that the two South American species, the Chilean lapwing V . chilensis and Andean lapwing V . resplendens, are more closely related to one another than to any other lapwing species, and are probably derived from the Old World blacksmith/spurwinged plover superspecies.

Contents

Introduction . . . . . . . . . . . . . . . . The study species . . . . . . . . . . . . . .

Methods . . . . . . . . . . . . . . . . . . Behavioural observations . . . . . . . . . . Morphology . . . . . . . . . . . . . . . .

Results . . . . . . . . . . . . . . . . . . Behaviour . . . . . . . . . . . . . . . . . Morphology . . . . . . . . . . . . . . . .

Discussion . . . . . . . . . . . . . . . . . . The status of the genus Vanellus . . . . . . . . Interspecific relationships . . . . . . . . . .

References . . . . . . . . . . . . . . . . . .

Page . . . . . . . . . . . . . . . 625 . . . . . . . . . . . . . . . 626 . . . . . . . . . . . . . . . 627 . . . . . . . . . . . . . . . 627 . . . . . . . . . . . . . . . 628 . . . . . . . . . . . . . . . 628 . . . . . . . . . . . . . . . 628 . . . . . . . . . . . . . . . 634 . . . . . . . . . . . . . . . 635 . . . . . . . . . . . . . . . 635 . . . . . . . . . . . . . . . 635 . . . . . . . . . . . . . . . 639

Introduction

The interspecific phylogenetic relationships of the family Charadriidae, and in particular members of the Vanellinae (vanelline plovers or lapwings), have been debated since the work of Seebohm (1888). Subsequent workers have proposed a number of classifications (Peters, 1934; Bock, 1958; Strauch, 1978) which have either split the species into a large number of genera

Present address: Dept. of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, B.C. V6T 124, Canada

625 0 1992 The Zoological Society of London

626 D. WARD

(Peters, 1934) or lumped them into a single genus (Bock, 1958), both classifications being considered equally unsatisfactory (Johnsgard, 198 1).

Vanelline plovers have an African centre of distribution (Bock, 1958); 14 of the 23 species are found there. All but five species are found on the southern continents (except Antarctica). None of the species occurs in North America. The other three subfamilies of the Charadriidae are the Charadriinae (‘sand’ plovers, 41 species), Pluvianinae (golden plovers, three species) and Hoploxypterinae (monotypic pied plover Hoploxypterus cayanus) (Johnsgard, 198 I). The Charadriinae and Pluvianinae have largely Holarctic distributions, while Hoploxypterus cayanus is found in northern South America.

Vanelline plovers are characteristic birds of the African waterside, although several species are found in short and burnt grass habitats (Snow, 1978). The vanelline plovers differ from other members of the Charadriidae by virtue of their generally larger size, long legs, and prominently marked black-and-white wings. Features of the vanelline plovers not found in other members of the family are facial wattles and wing spurs, although not all vanelline plovers possess these features. Jehl (1968) showed that only the downy young of vanelline plovers had a post-cranial black collar, while Strauch (1978) delineated the Vanellinae morphologically from the other subfamilies of the Charadriidae by the presence of a second cervical vertebral strut.

Bock (1958) was unable to detect differences between vanelline plover species on the basis of skeletal characters. He suggested that the most effective means of determining relationships between birds of the family Charadriidae would be by the use of biochemical and behavioural characters. However, molecular genetic characters have not proved particularly successful in determining the lower-order relationships of the Charadriidae (Sibley & Ahlquist, 1985; Baker & Strauch, 1986), albeit among a subset of these birds. For example, Sibley & Ahlquist (1985) were unable to separate at least two species of Vanellus (V. coronatus and V . cinereus) using DNA hybridization techniques, in spite of major plumage differences and great distances separating their distributions (sub-Saharan Africa and east Asia, respectively).

The use of behavioural characters for phylogenetic analysis has been disputed by Atz (l970), Parsons (1972), McClearn & DeFries (1973) and Dunford & Davis (1975), among others, on account of the structural and temporal plasticity of behaviour independent of phylogenetic change. However, behaviour is closely interrelated with other phenotypic characters (e.g. morphology and physiology) and is subject to the same evolutionary processes and constraints. Therefore, it should change in ways that reflect phylogenetic relationships (McLennan, Brooks & McPhail, 1988; Prum, 1990). As long as one uses behavioural characteristics which are not under strong natural selection, they are valid taxonomic characters (McLennan et al., 1988; Prum, 1990). Recently, several studies have indicated that behavioural studies, in conjunction with more conventional systematic techniques, may be most useful in phylogenetic analysis (e.g. Baker & Hockey, 1984; Miller, Gunn & Veprintsev, 1988; McLennan et al., 1988; Prum, 1990).

The behavioural similarities of five species of southern African vanelline plovers were examined, as well as a Palaearctic-African lapwing, and related to morphological data collated by Strauch (1978). Strauch (1 978) examined the higher-order relationships of the order Charadriiformes (shorebirds) using the technique of character-compatibility analysis, but did not consider the relationships below the generic level.

The study species

The crowned plover Vunellus coronatus, blackwinged plover V . melunopterus and lesser

SYSTEMATICS OF VANELLINE PLOVERS 621

blackwinged plover V. lugubris are grassland birds and have been variously classified into the genera Stephanibyx (Peters, 1934) and Vanellus (Bock, 1958), although subgeneric status has also been proposed for these three species (Johnsgard, 1981; Maclean, 1985). Blackwinged and lesser blackwinged plovers are considered to constitute a superspecies by Snow (1978) and Johnsgard (198 1) on account of plumage similarities (white forehead patch, brown plumage with white bellies, absence of wing spurs, wattles and hind toe) and parapatric distributions (in east and south Africa). Wolters (1975) placed blackwinged and lesser blackwinged plovers on their own in the genus Titihoia. Crowned plovers are widespread in sub-Saharan Africa (except the forested zone) and are sympatric with both blackwinged and lesser blackwinged plovers.

The blacksmith plover V. armatus and spurwinged plover V. spinosus are sometimes placed in the genus Hoplopterus, along with the Indian spurwinged plover Vanellus duvaucelii (e.g. Peters, 1934; Johnsgard, 1981; Cramp & Simmons, 1983), while subgeneric status has also been proposed for this group (Snow, 1978). This grouping of waterside vanelline plovers is based on the bold black, white and grey plumage, wing (carpal) spurs, and ‘metallic’ call. Blacksmith and spurwinged plovers are largely parapatric, although there is an area of sympatry in Kenya (Snow, 1978). Wolters (1975) has placed the spurwinged and Indian spurwinged plovers in the genus Hoplopterus, with the blacksmith plover in the monotypic genus Anitibyx, on account of differences in morphological characters between these species.

The African wattled plover V. senegallus is a waterside bird and differs in plumage coloration and adornments from both of the above species groups. This species possesses wing spurs and yellow facial wattles, and is probably most closely related to the white-crowned plover V. albiceps (Snow, 1978).

Methods

Behavioural observations

The behaviour of crowned, blackwinged, lesser blackwinged, African wattled and blacksmith plovers was observed in the field a t Pietermaritzburg, South Africa (29” 3 0 S, 30” 30’ E) and in Zululand, South Africa (particularly a t Ndumu-26” 30’ S, 32” 45‘ E) over a period of 3 years. These behaviours were recorded in 51 breeding pairs ofcrowned plovers, 21 pairs of blackwinged plovers, 33 pairs of lesser blackwinged plovers, 16 pairs of blacksmith plovers and 1 1 pairs of wattled plovers. This involved over 400 observation hours on each of the first 3 species and a minimum of 150 hours’ observation of the latter 2 species. In addition, the reaction of all 5 species to playback of their own and the other 4 species’ vocalizations was noted. Behavioural observations of spurwinged plovers V. spinosus (27 breeding pairs, minimum of 100 hours’ observation) were made at Maagan Mikhail, Israel (September 1988, April-May 1989), but no playback experiments were performed.

Comparisons with those species whose behaviour has been described, namely the northern lapwing Vanellus vanellus (Dabelsteen, 1978; Cramp & Simmons, 1983) and the Chilean lapwing V. chilensis (Maclean, 1972) are also provided.

Members of the genus Vanellus are referred to either as lapwings or plovers, with no consistent pattern (cg. Hayman, Marchant & Prater, 1986). I use the common name of ‘vanelline plover’ for the Vanellinae rather than ‘lapwing’ because the former term is used in Africa (e.g. Maclean, 1985), which is the centre of distribution of these species (Bock, 1958) and most species are found there. Thus, common names for African and Eurasian Vanellus species used here will be ‘plover’. I retain the usage of ‘lapwing’ for species occurring in South America and Australia, following the precedent of Johnsgard, 1981 and Hayman et a/., 1986. The name northern lapwing for the type species Vanellus vanellus has also been retained because this name has become entrenched in the literature.

628 D. W A R D

Morphology

Qualitative morphological features of 5 skeletal specimens of African wattled plovers and blacksmith plovers were examined (see Table I1 for a list of characters used). Skeletons of 1 1 crowned plovers, 7 blackwinged plovers and 6 lesser blackwinged plovers were also examined. Specimens were either provided by natural history museums in South Africa (see Acknowledgments on p. 639) or collected by the author. Skeletal features were compared with descriptions provided by Strauch (1978) in his analysis of the relationships between members of the order Charadriiformes.

Analysis of the morphological relationships between species were performed with an unweighted pair- group method using arithmetic averaging (UPGMA). This method was employed with: (1) the city block (or Manhattan) metric; and (2) squared Euclidean distances, to determine the differences between species based on a correlation matrix. The correlation matrix was derived from the Pearson product-moment correlation coefficients between the variables of each species. A third technique, a weighted-pair cluster analysis (WPGMA) was also performed on these data. The last technique clusters pairs of species based on the correlation matrix and weights the species most recently admitted to a cluster equal with all previous members. The Euclidean distance measure was used to determine the difference between species in the WPGMA analysis.

The debate continues as to whether cladistic or phenetic methodology is more accurate in the determination of the phylogeny of an organism (e.g. Hennig, 1966; Sokal & Sneath, 1973; Wiley, 1981; Sokal, 1985; Mickevich & Platnick, 1989). I have decided to use an eclectic approach. I used clustering techniques conventionally used by pheneticists, with ‘cladistic’ characters, namely meristic (categorical, non- continuous) characters that are synapomorphic (shared derived characters). I believe that the techniques employed here are expedient to the desired aim, namely to assist in the development of an accurate phylogeny of the Vanellinae and to provide a framework for further analysis. I have used these techniques for the following reasons:

( I ) Like both pheneticists and cladists, I provide a matrix of coded characters to allow direct comparison using other techniques. The absence of such a matrix has been a major criticism of evolutionary systematics and conventional taxonomy because the data cannot be re-analysed using different techniques and according to other philosophies (e.g. Wiley, 1981).

(2) Phenetic clustering methods are considered to be more accurate than cladistics when few characters are used (Sokal, 1985). I have used several clustering algorithms and used only the congruencies among them to postulate relationships+ongruencies presumably indicate more rigorous support for a hypothesis (Mayr, 1973).

(3) I concur with Hennig (1966) that not all characters are useful to the systematist and that shared derived characters are most valuable. However, like Strauch (1984), I believe that homoplastic characters at a higher level of organization (e.g. family) may be useful phylogenetic characters at lower levels (e.g. genus or species).

Results

Behauiour

The following behavioural displays were noted and differences compared for the six vanelline plover species:

( I ) Post-copulatory wing-lifting display: three forms of this display were noted: (a) The male dismounts, stands behind the female and lifts both wings to a vertical position (African wattled plover-Fig. la). (b) The male stands alongside the female and each bird lifts the wing further from the other bird to a vertical position with the hand folded (crowned plover-Fig. 1 b). (c) In blackwinged plovers, the behaviour described above for crowned plovers is altered by the display

SYSTEMATICS OF VANELLINE PLOVERS 629

FIG. 1 . Post-copulatory wing-lifting display in (a) African wattled plovers, and (b) crowned plovers (modified from Maclean, 1972).

630 D. W A R D

FIG. 2. Nest-scrape display in blacksmith plover. This display is performed with the male positioned behind the female, and both birds performing the same display.

being formed while both birds run for about 1 m (Maclean, 1972). Lesser blackwinged, spurwinged and blacksmith plovers did not perform a post-copulatory wing-lifting display.

(2) Butterfly-flight display: used by male vanelline plovers to demonstrate territorial ownership and to attract females. This display involves flying above the territory in a circular path with exaggerated wingbeats, emphasizing the downstroke and making a short, quick upstroke (for a graphical presentation of this in V. vanelfus see Dabelsteen, 1978). This display occurred in crowned, blackwinged, blacksmith, spurwinged and African wattled plovers. Lesser blackwinged plovers performed a display using a circular flight-path but did not have a butterfly-flight pattern.

(3) Nest-scrape display: precedes copulation and involves one bird (male) lying down about 1 m behind the other (female), both birds’ chests touching the ground, and then following by kicking out backwards with their feet (Fig. 2). Only blacksmith and spurwinged plovers performed this display. This display has also been recorded in northern lapwings (Nethersole-Thompson, 1940, 1988).

(4) Double-wing flick agonistic display: when threatened or when threatening conspecifics, other bird species or predators, crowned, blackwinged, African wattled, blacksmith and spurwinged plovers lift both wings vertically to display the contrasting black-and-white coloration of the wings (Fig. 3). This display is most frequently displayed towards large mammalian herbivores approaching too close to a nest. This display is performed concurrently with a small jump ( 5 cm high), although in cases of extreme conspecific interaction a bird may jump over another bird while performing this display. Lesser blackwinged plover juveniles also performed this display when threatened, although adults rarely did. Only a slight jump occurred in lesser blackwinged plovers concurrent with this display. Lesser blackwinged plovers never performed this display in conspecific encounters.

( 5 ) Bobbing threat display: when threatened by terrestrial predators or other vanelline plovers, the initial reaction of all six lapwing species was to bob the entire body backwards while keeping the legs motionless. Lesser blackwinged plovers, however, frequently bobbed their heads up-and- down in a single, quick movement in the manner of members of the genus Charadrius (Simmons, 1953; Cramp & Simmons, 1983, pers. obs.). A low-intensity threat display performed by all six species which was frequently associated with the bobbing display was false-feeding or ground-

SYSTEMATICS OF VANELLINE PLOVERS 63 1

c

FIG. 3. Double-wing flick agonistic display in blackwinged plovers (modified from Maclean, 1972)

pecking (Maclean, 1972). The birds pretended to pick up items from the ground in this display. Maclean (1972) regards this as a threat display because the head-lowered position is used in many shorebird displays as threat.

(6) High-intensity conspecific threat display: the head was held low and the neck feathers ruffled as the bird (all six lapwing species) chased off intruders. Lesser blackwinged plovers also kicked out backwards with their feet. one foot at a time, brushing up loose soil.

(7) Interspecific threat display: in cases of attack by terrestrial predators, all vanelline plovers except lesser blackwinged plovers spread their wings horizontally and lowered their heads as they approached the intruders (e.g. spurwinged plover-Fig. 4a). In the early stages of this display, the head was held up until the intruder approached too closely. Thereafter, the head was lowered. This display was followed by aerial mobbing. Lesser blackwinged plovers spread their wings horizontally but never lowered their heads while performing this display (Fig. 4b). They did not perform an aerial-mobbing display except when they had chicks less than about two weeks old. The low intensity form of this display involves false-brooding by one member of a pair in all six species examined. False-brooding occurs when a bird squats on the ground with the tail feathers slightly lifted, as if brooding eggs.

(8) Nest-and-chick-defence displays: during the first 20 days of incubation, crowned, blackwinged, African wattled, spurwinged and blacksmith plovers aerially mobbed intruders. After this period, aerial mobbing was performed in addition to a ‘broken-wing display’ (crowned

c

r---

FIG. 4. Interspecific threat display in (a) spurwinged plover, and (b) lesser blackwinged plover (modified from Maclean, 1972).

and blackwinged plovers only) which involved lying with the chest on the ground with wings horizontally outstretched so that the wings touched the ground (Fig. 5). The wings were flapped up and down, with the tips never lifting more than about 5 cm from the ground. All six species also crouched down and, with the wings held closed, vigorously flapped the wings close to the body. Lesser blackwinged plovers did not perform the ‘broken-wing display’ but did stand upright, with the head held erect, and flapped both wings forward in front of the body in a ‘clapping’ motion. Ths clapping motion was also seen in spurwinged plovers ‘upon alighting after aerial mobbing attacks (Cramp & Simmons, 1983).

A summary of interspecific differences in behaviour is shown in Table I.

SYSTEMATICS OF V A N E L L I N E PLOVERS 633

FIG. 5 . Broken-wing display in crowned plover (from a photograph by C . Urquhart).

TABLE I Differences in behaviour of crowned. blackwinged, lesser blackwinged. blacksmith, spurwinged and African wattled plovers. Species with the same number share the same state

of a characler

Species

Crowned plover Blackwinged plover Lesser blackwinged plover Blacksmith plover Spurwinged plover African wattled plover

Behaviour pattern

A B C D E F G

1 2 1 1 2 1 2 1 2 1 1 2 1 2 2 2 2 2 2 2 1 1 2 2 1 1 1 2 1 2 2 1 1 1 2 1 1 2 1 2 1 2

A=Presence (1) or absence (2) of a double wing-flick

B =Presence (1) or absence (2) of a post-copulatory

C =Presence (1) or absence (2) of post-copulatory

D = Presence (1) or absence (2) of an inverted U-note in

E =Presence (1) or absence (2) of a nest-scrape display. F =Presence (1) or absence (2) of a butterfly flight

G = Broken-wing display performed while standing

display.

display employing two fully-extended wings.

display employing one wing (with the hand folded).

territorial call.

display.

upright (1) or with belly on ground (2).

Crowned, blackwinged, African wattled and blacksmith plovers all responded to playback of one another’s calls by threat displays and displacement activities (such as feeding, copulation and false-brooding). These four species did not respond to lesser blackwinged plover calls. Lesser blackwinged plovers responded to playback of their own calls by threat displays and displacement activities mentioned above.

634 D . WARD

Morphology

In the cluster analyses of skeletal features, several characters used by Strauch (1978) were

(1) A maxillopalatine strut (strut C seam Strauch, 1978) was not included in the analysis because Strauch (1978) classified it incorrectly. Strauch (1978) recorded this strut as absent in lesser blackwinged plovers, yet it was present in all specimens of this species examined in this study. Thus, it is possible that this character was incorrectly coded for other species too.

(2) The number of supraoccipital foramina was excluded because this character was variable in all the species examined, being present in young specimens and absent in larger, older birds. These

omitted because they were found to be either incorrectly classified or variable within a species:

TABLE I 1 Differences in morphological characters among members of the genus Vanellus. Species with the same number share the same state of a

character

A B C D E F G H I J K

V. malabaricus V. melanopterus V . lugubris V. tricolor V . gregarius V . leucurus V. coronatus V. cinereus V. IL'CtUS

V. ranellus V. chilensis V . resplendens V . albiceps V. senegallus V. spinosus V. armatus V. duvaucelii V. miles V. macropterus V. indicus V. crassirostris

1 2 2 2 1 2 2 2 1 1 1 I 2 2 2 1 2 2 2 1 1 2 1 2 2 2 2 2 2 2 2 1 2 2 1 2 2 1 2 2 2 1 1 I 1 2 2 1 1 2 2 2 2 1 2 1 1 2 1 1 2 2 1 2 2 2 1 2 2 2 1 2 2 2 1 1 2 1 2 2 1 1 2 2 1 2 1 1 2 2 2 2 1 2 2 2 1 1 1 2 1 2 1 1 2 2 2 1 1 2 2 1 1 1 1 2 2 1 1 1 2 2 1 1 2 1 2 2 1 1 1 2 I 1 1 2 1 2 2 2 2 1 1 1 2 1 1 1 2 2 2 1 I l 1 2 1 2 1 2 2 I 1 1 2 1 2 1 2 1 2 2 1 1 1 2 2 2 1 2 1 2 2 1 1 1 2 2 2 1 1 1 2 1 2 1 1 1 1 2 1 1 1 2 1 2 1 1 1 1 2 1 1 1 2 I I l I 1 2 2 1 I l l 1 1 1 1 2

Character coding for Table TI:

A =Seven (1) or eight (2) caudal vertebrae, omitting the pygostyle. B =Twelve (1) or 13 (2) cervical vertebrae, omitting those with

C =Presence (1) or absence (2) of a wing spur. D = Presence (1) or absence (2) of a hallux. E =Presence ( I ) o r absence (2) of hypotarsal canal 4. F =Presence ( I ) or absence (2) of hypotarsal canal 5. G = Presence (1) or absence (2) of hypotarsal canal 6. H =Presence (1) or absence (2) of a red iris. 1 = Black-lipped ( I ) or white (2) secondary feathers. J =Tail with a black band in it (1) or wholly white (2). K =Presence ( I ) or absence (2) of wattles.

unfused cervical ribs.

SYSTEMATICS OF VANELLINE PLOVERS 635

foramina are presumed to ossify with age. The shape of the posteromedial edge of the ilium was also excluded from the analysis because it was found to be variable within all the species examined.

The following features were used in the morphological analysis: (1) the number of caudal vertebrae, omitting the pygostyle; (2) the number of cervical vertebrae, omitting those with unfused cervical ribs; (3) presence or absence of a wing spur; (4) presence or absence of a hallux; (5-7) presence or absence of canals in the hypotarsus for tendon numbers 4, 5 and 6 (sensu Strauch, 1978); (8) presence or absence of a red iris; (9) black-tipped or white secondary feathers; (10) tail white or with a black band in it; and (1 1) presence or absence of wattles.

A further 60 skeletal characters were examined, which were the other characters used by Strauch (1978). These characters were invariable among the Vanellus species examined and were therefore not included in the analysis. All characters for species not examined in this study were assumed to be correctly coded by Strauch ( 1 978), with the exception of the incorrectly-coded or variable characters mentioned above. The presence of red eye-colour, the two plumage features and wattles were included in the analysis because they are considered to be synapomorphic (shared derived characters), and are not present in other members of the Charadriidae. All other plumage characters examined were found to be symplesiomorphies and thus excluded from the analysis. The differences between the skeletal features of the species studied are shown in Table 11. Phenograms of the morphological similarities among species are shown in Fig. 6a-c.

The syringeal morphology of crowned, blackwinged, lesser blackwinged, African wattled and blacksmith plovers was examined in another study (Brown & Ward, 1990). Some interspecific differences were found in the degree of ossification of the syrinx, but these appeared to be correlated with size of the species, larger species having more ossified syringes. The variation in syringeal morphology among species of Charadriiformes is considerable and of great systematic value (Brown & Ward, 1990). Thus, examination of syringes of other vanelline plover species may prove systematically useful.

Discussion

The status of’ the genus Vanellus

Several authors (e.g. Wolters, 1975; Snow, 1978; Johnsgard, 1981; Cramp & Simmons, 1983) have expressed disagreement at the lumping of all vanelline plovers into the single genus Vanellus by Bock (1958). Mickevich & Parenti (1980) re-analysed Strauch’s (1978) data using the parsimony method of cladistics and suggested (in contrast to Strauch) that Vanellus may be a paraphyletic group. The data presented here indicate that there are very few morphological differences among species in this taxon. Among the species examined, behavioural differences are few. It is unlikely that Vanellus is paraphyletic because all species possess q second cervical strut (Strauch, 1978) and post-cranial black ring in the downy young (Jehl, 1968). These characters constitute synapomorphies (Wiley, 198 1). Behaviourally, all VaneLlus species for which behaviours have been described show the double-wing flick agonistic display. This display is not recorded in other species in the Charadrii (Cramp & Simmons, 1983) and has probably evolved in association with the bold black-and-white pattern in the wings that is absent in the rest of the taxon.

In terspec(fic relationships

The phenograms of morphological characters, as well as the interspecific behavioural

636 D. WARD

(b) v spinosus 7 V armatus

V duvaucelii V chilensis

V resplendens

A zza?zerus

V tricolor V. tectus

V malabaricus

V. albiceps 5 7 L Z:iz:us

V miles

- V macropterus V indicus

V lugubris

V leucurus

V gregarius i! crassirostris

V vanellus

, _-_ 25 20 15 10 5 0

Rescaled distance

I

v spinosus v armatus

V. duvaucelii

V chilensis

V resplendens

I! vanellus - V. melanopterus 7 v: coronatus c', ,? V. tricolor

-- 25

V albiceps

V macropterus

V miles

V indicus

v cinereus ~ V. lugubris

V crassirostris

V gregarius

V leucurus

20 15 10 5 0 Rescaled distance

V malabaricus V tricolor

V tectus V melanopierus

V coronatus

V albiceps V cinereus

V senegallus

V miles

V macropterus

V indicus

V leucurus

V vanellus

v chilensis V resplendens

v sprnosus v armatus

V duvaucelii V crassirostris

V lugubrrs

.- I ___I-- v gregarius

-

. ..--A -0.26 0-18 062 1-05

Distance

FIG. 6. Phenograms showing similarities among morphological characters of Vanellus species. (a) Phenogram derived by unweighted-pair group mean cluster analysis (UPGMA) using the city-block distance measure on a correlation matrix. (b) Phenogram derived by UPGMA using the squared Euclidean distance measure on a correlation matrix. (c) Phenogram derived by weighted-pair cluster analysis (WPGMA) using the Euclidean distance measure on a correlation matrix.

SYSTEMATICS OF VANELLINE PLOVERS 631

differences, indicate that blackwinged and crowned plovers are more similar to one another than to any other Vanellus species. In addition, lesser blackwinged plovers are not as similar to blackwinged plovers as general plumage characters would appear to suggest. On the basis of this analysis, I suggest that blackwinged and lesser blackwinged plovers do not constitute a superspecies as has been suggested by Snow (1978) and Johnsgard (1981). Rather, the analyses conducted here indicate that crowned and blackwinged plovers constitute a superspecies group. The black ring around the crown of adult crowned plovers is the major plumage difference between these latter two species. This is the feature that has led some systematists (e.g. Wolters, 1975; Snow, 1978) to place crowned and blackwinged plovers in separate generalsubgenera. This feature may be neotenic in crowned plovers because the downy young of all Vanellus species are characterized by the presence of a black post-cranial ring (Jehl, 1968).

The lack of stereotyping of certain ‘typical’ Vanellus behaviour patterns in the lesser blackwinged plover (bob and double-wing flick), and the absence of the butterfly-flight display, are puzzling. This species did not respond to playback of the calls of the other four South African species examined, while all other species responded to heterospecific calls. This last-mentioned difference may be due to the absence of a call note appearing as an ‘inverted U-shaped’ note in sonograms (Ward & Maclean, 1988; Ward, 1989). The absence of these stereotyped behaviours and vocalizations in the lesser blackwinged plover may be related to the cryptic nature of this small bird. The larger species of Vanellus have evolved elaborate display postures, in contrast with the more subtle, less visible displays of Charadrius species (Maclean, 1972). The lesser blackwinged plover lives mostly in open woodlands where it relies on crypsis to avoid detection (Ward, 1987; Ward & Maclean, 1989). This species appears to have secondarily lost the elaborate Vanellus displays to aid crypsis. These behavioural features were probably secondarily lost because some species of Charadrius possess some of these characters, particularly the butterfly flight (e.g. kentish plover C . alexandrinus and ringed plover C . hiaticula (Simmons, 1953. 1955)). The similarity of plumage of blackwinged and lesser blackwinged plovers may be the result of lack of change from an ancestral plumage. This ancestral plumage is displayed in members of the genus Charadrius (e.g. whitefronted plover C . marginatus and kentish plover C . alexandrinus), a group from which Vanellus is probably derived (Bock, 1958; Jehl, 1968; Strauch, 1978).

The close phylogenetic relationship between blacksmith and spurwinged plovers is indicated by the congruence of the behavioural characteristics and phenograms. This relationship is further indicated by the similarity of the ‘metallic’ vocalizations of these two species (for sonograms see Cramp & Simmons, 1983; Maclean, 1985). Maclean (1972) suggested that the wing-raising displays of crowned and blackwinged plovers have been largely suppressed in the blacksmith plover and the vocalizations correspondingly elaborated to become an accompaniment to the post-copulatory run. This observation was supported in this study of blacksmith plovers and was also found to be true of the spurwinged plover.

Additionally, morphological evidence presented here indicates that the Indian spurwinged plover V. duvaucelii appears to be most closely related to the blacksmith and spurwinged plovers, as postulated by earlier workers (Snow, 1978; Johnsgard, 1981).

Additional species groups suggested by the morphological analyses are:

(1) The two South American species, Chilean lapwing V. chilensis and Andean lapwing V. resplendens. It appears that the South American species, which are allopatric (occur on opposite sides of the Andes mountains), represent a single invasion of South America by the vanelline plovers. This is supported by data on DNA hybridization (Sibley & Ahlquist, 1985). All three phenograms indicate that these two species constitute a sister group to the blacksmith-

638 D. W A R D

spurwinged-Indian spurwinged plover group. All five of these species possess carpal spurs, predominantly black-and-white plumage, and red eyes and lack wattles. However, the Chilean lapwing does possess several displays that differ from those of the blacksmith and spurwinged plovers. These displays are:

(a) conspecific defensive threat displaydonsists merely of showing the bright red wing spurs by removing the wrists from their pectoral ‘pockets’ (Maclean, 1972). The wing spurs of blacksmith and spurwinged plovers are black and less conspicuous than those of the Chilean lapwing, which may explain the absence of this display in the two Old World species.

(b) advertising wing display-two birds run together with wings opened vertically (Maclean, 1972). This differs from the post-copulatory wing-lifting display of crowned and blackwinged plovers because the wing is fully opened and the context is not post-copulation. An advertising wing display is absent in the blacksmith and spurwinged plovers.

(c) partial wing-lifting display-one wing is held open, the other closed with the wing spur exposed, and the body tilted forward as if the bird were feeding. Maclean (1972) considers this display to be a combination of ground-pecking (false-feeding-a head-down aggressive threat), advertising (wing-raising) display and the exposed-wrist element of the upright (defensive) threat posture (display (a) above). This display has been recorded in crowned and blackwinged plovers (Ward, 1989), although the context was submissive (indicating defeat in conspecific threat displays).

The behaviour of the Andean lapwing has not yet been studied. The presence of the above three displays in the Andean lapwing will provide additional support for the hypothesis of a single invasion of South America by Vanellus.

Wolters (1975) suggested that the long-toed plover V. crassirostris is most closely related to the blacksmith and spurwinged plovers. The external morphological features common to the blacksmith and spurwinged plovers and the two South American species (see above) are also possessed by the long-toed plover. However, the relationship of the latter species with the former five is not supported by the phenograms. The behavioural displays of the long-toed plover remain to be described.

(2) The African black-headed plover V. tectus, Indian yellow-wattled plover V. malabaricus and the Australian masked lapwing V. miles. The morphological data do not support a single invasion of Australia by the vanelline plovers because the two Australian species, the masked lapwing and banded lapwing I/. tricolor, do not cluster together in any algorithm used. The black- headed plover and spot-breasted plover V. melanocephalus (not examined here) are placed in the genus Lobivanellus by Wolters (1975), although the affinities of each are obscure (Snow, 1978). Both the black-headed and spot-breasted plovers possess a small wattle and the plumage is predominantly brown, white and black, although the black-headed plover possesses a small knob on the carpal joint which may prove homologous with a carpal (wing) spur. The spot-breasted plover is endemic to Ethiopia where it inhabits high-altitude grasslands, mainly above 3000 m (Snow, 1978). It is sympatric with the black-headed plover but effectively allopatric (i.e. allotopic) on account of altitude and habitat separation. Thus, these two latter species may prove to be more closely related to one another than the black-headed plover is to the Indian yellow-wattled plover and the banded lapwing.

Two surprising features of the data were:

(1 ) the lack of phenetic similarity of the African wattled plover V. senegallus and the white-

SYSTEMATICS O F VANELLINE PLOVERS 639

crowned plover V. albiceps. two African waterside species with yellow legs, facial wattles, wing spurs and similar plumage coloration. These similarities led Wolters (1975) to place these two species in the genus Xiphidiopterus. Other workers (e.g. Peters, 1934; McLachlan & Liversidge, 1957) have usually retained the genus Xiphidiopterus for the white-crowned plover, and placed the African wattled plover in the monotypic genus Afribyx. Snow (1978) considered these two genera closest to one another in the Vanellinae, although he suggested that detailed studies of behaviour will be necessary to distinguish the relationships of these two species. The behaviour of the white- crowned plover has yet to be described.

(2) the lack of similarity among the Eurasian species, the northern lapwing V. vanellus, white- tailed plover V. leucurus and sociable plover V. gregarius, especially in view of the morphological and plumage similarities of the latter two species (absence of wing spur, presence of hind toe, black eye stripe and grey plumage). The presence of the nest-scrape display in the northern lapwing, blacksmith and spurwinged plovers may indicate that these species are closely related, although this is not supported by the phenograms based on morphological similarities.

This analysis must remain tentative until the behaviours of the other Vanellus species have been adequately described, in order to broaden the basis of selection of behavioural characters for systematic analysis. By demonstrating which characters have been used, this systematic analysis can be re-examined by other workers using other techniques and by supplementing these characters with others. Ultimately, a more rigorous analysis can then be performed which will more accurately reflect the phylogeny of the genus Vanellus.

I thank Gordon Maclean for his advice and stimulating arguments. Tamar Cassidy of the Transvaal Museum, Pretoria, Roy Earle of the National Museum, Bloemfontein and John Mendelsohn of the Durban Natural History Museum kindly lent me many of the specimens used in this study. David Johnson of the Natal Parks, Game and Fish Preservation Board provided permits to work in areas under his jurisdiction. I thank Gordon Maclean, Joe Strauch and Yael Lubin for comments on an earlier draft of this manuscript, the CSIR and the Frank M. Chapman fund of the American Museum of Natural History for financial support, and Fiona Lawes for typing much of this manuscript.

REFERENCES

Atz, J. W. (1970). The application of the idea of homology to behavior. In Development and evolution of behavior: 53-74. Aronson, L. R., Tobach, E., Lehrman, D. S . & Rosenblatt, J. S. (Eds). San Francisco: W. H. Freeman & Co.

Baker, A. J. & Hockey, P. A. R. (1984). Behavioral and vocal affinities of the African Black Oystercatcher (Haematopus moquini). Wilson Bull. 9 6 656-671.

Baker, A. J. & Strauch, J. G. (1986). Genetic variation and differentiation in shorebirds. In Genetic structure of avian populations: 1639-1645. Proc. h t . O m . Congr. No. 19. Barrowclough, G. F. & Baker, A. J. (Eds). Ottawa: University of Ottawa Press.

Bock, W. J. (1958). A generic review of the plovers (Charadriinae, Aves). Bull. Mus. comp. Zool. Haru. 118: 27-97. Brown, C . &Ward, D. (1990). The morphology of the syrinx in the order Charadriiformes (Aves): possible phylogenetic

Cramp, S. & Simmons, K . E. L. (1983). Birds of the western Palearctic 3. Oxford: Oxford University Press. Dabelsteen, T. (1978). An analysis of the song-flight of the lapwing (Vanellus vanellus L.) with respect to causation,

Dunford, C. & Davis, R. (1975). Cliff chipmunk vocalizations and their relevance to the taxonomy of coastal sonoran

Hayman, P., Marchant, J. & Prater, T (1986). Shorebirds: An identiJication guide to the waders of the world. London:

Hennig, W. (1966). Phylogenetic systematics. Urbana, Illinois: University of Illinois Press.

implications. Bonn. zool. Beifr. 41: 95-107.

evolution and adaptations to signal function. Behaviour 66: 136-178.

chipmunks. J . Mammal. 56: 207-212.

Croom Helm.

640 D. WARD

Jehl, J. R., Jr (1968). Relationships in the Charadrii (shorebirds): a taxonomic study based on the color patterns of the

Johnsgard, P. A. (1981). Theplovers, sandpipers andsnipes of the world. Lincoln, Nebraska: University of Nebraska Press. Maclean, G. L. (1972). Problems of display postures in the Charadrii (Aves: Charadriiformes). Zool. afr. 7: 57-74. Maclean, G. L. (1985). Roberrs’ birds of southern Africa. Cape Town: John Voelcker Bird Book Fund. Mayr, E. (1973). The principles of systematic zoology. Cambridge, Mass.: Belknap Press. McClearn, G. E. & DeFries, J. C. (1973). Introduction to behavioralgenetics. San Francisco: W. H. Freeman & Co. McLachlan, G. R. & Liversidge, R. (1957). Roberts’birds of southern Africa. Cape Town: John Voelcker Bird Book Fund. McLennan, D. A., Brooks, D. R. & McPhail, J. D. (1988). The benefits of communication between comparative ethology

Mickevich, M. F. & Parenti, L. R. (1980). Review: The phylogeny of the Charadriiformes (Aves): A new estimate using the

Mickevich, M. F. & Platnick, N. 1. (1989). On the information content of classifications. Cladistics 5: 33-48. Miller, E. H., Gunn, W. W. H. & Veprintsev, B. N. (1988). Breeding vocalizations of Baird‘s sandpiper Calidris bairdiiand

Nethersole-Thompson, D. (1940). Threat and injury-feigning display of Lapwing. Br. Birds 34: 138-139. Nethersole-Thompson, D. (1988). Waders; their haunts, watchers and breeding habits. Clapton, Staffordshire: T. & A. D.

Parsons, P. A. (1972). Genetic determination of behaviour (mice and men). In Genetics, environment and behauiour: 75-103.

Peters, J. L. (1934). Check-list of the birds of the world 2. Cambridge, Mass.: Harvard University Press. Prum, R. 0. (1990). Phylogenetic analysis of the evolution of display behavior in the Neotropical manakins (Aves:

Pipridae). Ethology 84: 202-23 1. Seebohm, H. (1888). The geographical distribution of the family Charadridiidae, or the plovers, sandpipers, snipes, and their

allies. London: Henry Sotheran. Sibley, C. G. & Ahlquist, J. E. (1985). The relationships of some groups of African birds based on comparisons of the

genetic material, DNA. In Proc. int. Symp. Afr. Vertebr., Bonn: 115-161. Huttiger, R. (Ed.). Bonn: Museum Alexander Koenig.

Simmons, K. E. L. (1953). Some aspects of the aggressive behaviour of three closely-related plovers (Charadrius). Ibis 95: 115-127.

Simmons, K. E. L. (1955). The nature of predator reactions of waders towards humans; with special reference to the role of the aggressive-, escape-, and brooding-drives. Behaviour 8: 130-1 73.

Snow, D. W. (1978). An atlas of speciation in African non-passerine birds. Publns Br. Mus. nut. Hist. No. 787. Sokal, R. R. (1985). The continuing search for order. Am. Nut. 126 729-749. Sokal, R. R. & Sneath, P. H. (1973). Numerical taxonomy. San Francisco: W. H. Freeman. Strauch, J. G., Jr (1978). The phylogeny of the Charadriiformes (Aves): a new estimate using the method of character

Strauch, J. G., Jr (1984). Use of homoplastic characters in compatibility analysis. Syst. Zool. 3 3 167-177. Ward, D. (1987). The biology and systematic relationships of Crowned, Blackwinged and Lesser Blackwinged Plovers.

Ward, D. (1989). Behaviour associated with breeding of crowned, blackwinged and lesser blackwinged plovers. Ostrich 60:

Ward, D. & Maclean, G. L. (1988). Coexistence of crowned and blackwinged plovers. Oecologia 77: 400-406. Ward, D. & Maclean, G. L. (1989). Habitat selection ofcrowned, blackwinged and lesser blackwinged plovers. Ostrich 60:

Wiley, E. 0. (1981). Phylogenetics. The theory andpractice of phylogenetic systematics. New York: John Wiley & Sons. Wolters, H. (1975-1982). Die Vogelarten der Erde. Berlin: Verlag Paul Parey.

downy young. Mem. S. Diego SOC. nut. Hist. No. 3. 1-54.

and phylogenetic systematics: a case study using gasterosteid fishes. Can. J. Zool. 66: 2177-2190.

method of character compatibility analysis. Syst. Zool. 2 9 108-1 13.

related species, with remarks on phylogeny and adaptation. Ornis scand. 1 9 257-267.

Poyser.

Ehrmann, L., Omenn, S. & Caspari, E. (Eds). New York: Academic Press.

compatibility analysis. Trans. zoo/. SOC. Lond. 34: 263-345.

Unpubl. PhD dissertation, University of Natal, South Africa.

141 -1 50.

49-54.