Failure of evolutionary convergence in 'nectarivorous' birds between Australia (Meliphagidae) and southern Africa (Nectariniidae)

@kokhuitan @lukedowney @tonyrebelo @jeremygilmore @ludwig_muller @ptexis @vynbos @baldcoot

INTRODUCTION

Australia and southern Africa are ecologically comparable.

Both landmasses possess a range of climates, from mediterranean (https://en.wikipedia.org/wiki/Mediterranean_climate) and adjacent arid to summer-rainfall tropical (https://en.wikipedia.org/wiki/Climate_of_Australia#:~:text=The%20largest%20part%20of%20Australia,varying%20between%20grasslands%20and%20desert. and https://en.wikipedia.org/wiki/Climate_of_South_Africa).

Furthermore, in both cases the substrates tend to be nutrient-poor, owing to profound weathering on a largely flat topography (https://pubmed.ncbi.nlm.nih.gov/17624961/ and https://www.researchgate.net/publication/6213166_Ecology_of_Australia_The_effects_of_nutrient-poor_soils_and_intense_fires and https://www.jstor.org/stable/2845371).

In both Australia and southern Africa, there are many and various plants pollinated mainly by birds (https://www.tandfonline.com/doi/pdf/10.1080/0028825X.1979.10432566#:~:text=The%20genera%20most%20frequently%20visited,insects%20as%20well%20as%20birds. and https://www.tandfonline.com/doi/abs/10.1080/0028825X.1979.10432566 and https://mdahlem.net/birds/plant/pollen.php and https://science.uct.ac.za/fitzpatrick/research-understanding-biodiversity-evolutionary-and-behavioural-ecology/bird-pollination-cape-floristic-region and https://naturesvalleytrust.co.za/wp-content/uploads/2023/07/Whitehead-K.-2018.pdf and https://www.sciencedirect.com/science/article/abs/pii/S0367253006000259 and https://www.jstor.org/stable/43234070).

On both landmasses, the flowers/inflorescences in question tend to be bright-hued, bearing copious nectar deep within a structure that makes it adaptive for nectarivorous passerine birds to have long, curved beaks.

In general, the norm in meliphagids is relatively large-bodied and short-beaked, whereas the norm in nectariniids is small-bodied and long-beaked. However, the variation is potentially sufficient for close counterparts to have evolved on the two separate landmasses.

AIMS

It is widely believed that certain Meliphagidae (https://en.wikipedia.org/wiki/Honeyeater) in Australia and certain Nectariniidae (https://en.wikipedia.org/wiki/Sunbird) in southern Africa show evolutionary convergence (https://en.wikipedia.org/wiki/Convergent_evolution), as part of an adaptive syndrome of mutualism with ornithophilous plants (https://en.wikipedia.org/wiki/Ornithophily).

The aim of this Post is to test evolutionary convergence in the case of meliphagids in Australia vs nectariniids in southern Africa.

NON-CONVERGENCES EMERGING FROM MY INTERCONTINENTAL COMPARISON OF MELIPHAGIDS WITH NECTARINIIDS

The following scrutiny undermines the 'textbook' interpretation.

Meliphagids have undergone an extreme evolutionary radiation in the 'island continent', Australia. However, it is the differences between meliphagids and nectariniids - according to my findings - that emerge as more significant than the similarities.

This failure of evolutionary convergence is partly in line with the observation that meliphagids generally differ from nectariniids in having relatively large bodies and relatively short beaks. However, the biological disparities are manifold, and most remain even iin the closest intercontinental counterparts.

The main intercontinental disparities are as follows.

Firstly, the tongues are remarkably different.

In meliphagids, the tongue is fairly simple except for its brush-like tip (https://www.merriam-webster.com/dictionary/fimbriated and https://www.perplexity.ai/search/does-the-morphology-of-the-ton-dWPr2lh8Qi.prkVX4Uv7Jg and https://www.perplexity.ai/search/can-the-tongue-of-any-nectarin-M7OaIr9IR86NcZp.ZVFZjA).

By contrast, in nectariniids the tongue is odd even among nectarivorous birds (https://www.biorxiv.org/content/10.1101/2024.05.14.594085v1.full.pdf). This is because it operates by means of suction, as opposed to either capillarity, or pressure exerted by the closure of the beak.

In other words, the tongue of nectariniids serves as a drinking straw (https://en.wikipedia.org/wiki/Drinking_straw), the main complication being the distal bifurcation of the straw.

Secondly, plumage and colouration differ according to the following syndrome:

• no meliphagid has iridescent plumage; by contrast, most nectariniids possess iridescent feathers, at least in males in breeding plumage;
• meliphagids tend to be less sexually dimorphic than nectariniids;
• males of meliphagids differ from those of nectariniids in lacking breeding plumage in a seasonal sense (https://www.perplexity.ai/search/in-nectariniidae-do-adult-male-rxXZ85P0T62TD9WeS6wEgA); and
• meliphagids lack the pectoral tufts (which are conspicuously bright-hued) possessed by many nectariniids (https://www.perplexity.ai/search/does-any-meliphagid-possess-pe-xLw1BDwASGGbtUQe5_JhhA).

Thirdly, most meliphagids do not build a 'dome' nest. By contrast, all nectariniids build nests protected and hidden by a roof.

CLOSEST INTERCONTINENTAL COUNTERPARTS

(My values for body length and body mass refer to adult females.)

In all the following cases:

• the tongue of meliphagids is brush-like, whereas that of nectariniids is tubular,
• the nest of meliphagids is open at the top, whereas that of nectariniids is sealed at the top, and
• there are no records of the consumption of sugary exudates other than floral nectar.

The meliphagid Sugomel nigrum (https://www.inaturalist.org/taxa/367631-Sugomel-nigrum, body length 11 cm, body mass 9.5 g) is fairly closely matched with the nectariniid Cinnyris fuscus (https://www.inaturalist.org/taxa/145189-Cinnyris-fuscus and https://thebdi.org/2024/06/04/dusky-sunbird-cinnyris-fuscus/, body length 10 cm, body mass ?8 g).

In both cases,

• the plumage of males achieves conspicuousness by means of darkness, not hue or iridescence,
• the colouration differs between the sexes,
• the habitat is the semi-arid interior of the landmass, where the vegetation is sparse, and
• the populations tend to be nomadic.

The similarity in colouration is greatest when males of the nectariniid are in non-breeding plumage (https://www.inaturalist.org/posts/98889-failure-of-evolutionary-convergence-in-nectarivorous-birds-between-australia-meliphagidae-and-southern-africa-nectariniidae#activity_comment_68c95b95-0846-4b9d-85ab-c2631edd7749).

However, the following differences remain:

• the meliphagid remains larger-bodied than the nectariniid, with a proportionately smaller head and shorter beak,
• the meliphagid qualifies, in males, as pied/piebald (https://www.merriam-webster.com/dictionary/piebald), which is not quite emulated by C. fuscus (https://www.inaturalist.org/observations/229807463), let alone any other nectariniid,
• the meliphagid has frequently been recorded eating ash (https://www.researchgate.net/publication/289010983_Some_notes_on_the_Black_Honeyeater_Sugomel_niger_in_Western_Australia_with_special_reference_to_feeding_on_ash), which as far as I know has never been recorded in any nectariniid,
• the nectariniid remains categorically more iridescent (https://www.inaturalist.org/observations/47327328 and https://www.inaturalist.org/observations/152404812 and https://www.inaturalist.org/observations/122277798 and https://www.inaturalist.org/observations/103055723 and https://www.inaturalist.org/observations/74663407 and https://www.inaturalist.org/observations/47327356 and https://www.inaturalist.org/observations/27908216 and https://www.inaturalist.org/observations/156621773) than any meliphagid, and
• males of the nectariniid - even in non-breeding plumage - retain bright-hued pectoral tufts (https://www.inaturalist.org/observations/17509372 and https://www.inaturalist.org/observations/16648040 and https://www.inaturalist.org/observations/6591102), absent from meliphagids.

Sugomel nigrum is associated mainly with Myoporaceae (https://www.inaturalist.org/observations?subview=map&taxon_id=136365&view=species). The nectariniid is instead associated mainly with Asphodelaceae (https://www.inaturalist.org/observations?place_id=113055&subview=map&taxon_id=71400&view=species and https://www.naturepl.com/stock-photo-dusky-sunbird-cinnyris-fuscus-feeding-on-the-nectar-of-quiver-tree-nature-image01596050.html and https://www.inaturalist.org/observations/224213747 and https://www.inaturalist.org/observations/55666885).

The meliphagid Acanthorhynchus superciliosus (https://www.inaturalist.org/taxa/12237-Acanthorhynchus-superciliosus, female length 14 cm, body mass 9 g) is somewhat similar to the nectariniid Anthobaphes violacea (https://www.inaturalist.org/taxa/145130-Anthobaphes-violacea, female length 12 cm, body mass ?7-8 g).

In both cases,

• the colouration differs between the sexes,
• the beak is proportionately fairly long,
• there is a particular coevolutionary (mutualistic) association with extremely diverse floras (e.g. Proteaceae) in sclerophyllous, fire-prone vegetation (https://en.wikipedia.org/wiki/Kwongan and https://en.wikipedia.org/wiki/Fynbos) on nutrient-poor, sandy substrates under mediterranean climates, and
• clutch-size, normally two in the relevant meliphagids and nectariniids alike, is often only one in both A. supercilious and A. violacea.

However, differences remains in

• body size, with the meliphagid somewhat the larger (additionally verified by the fact that egg sizes differ, viz. 18 X 13 mm in the meliphagid, vs 16.5 X 12.4 mm in the nectariniid),
• aerial acrobatics, with the meliphagid the more powerful and rapid flier, and
• colouration, with conspicuously pale-tipped tail (in flight) only in the Australian species, and iridescence only in the southern African species.

Myzomela sanguinolenta (https://www.inaturalist.org/taxa/12443-Myzomela-sanguinolenta, body length 10 cm, body mass 8 g) is fairly similar to Hedydipna collaris (https://www.inaturalist.org/taxa/145122-Hedydipna-collaris, body length 10 cm, body mass 8 g).

The meliphagid actually exceeds the nectariniid in sexually dimorphism in colouration.

Furthermore, both spp.

• are equally small-bodied, with M. sanguinolenta being the smallest-bodied and brightest-hued (in the case of males, which qualify as glossy albeit not iridescent) of all meliphagids (other than Ephthianura),
• have short beaks,
• are insectivorous as much as nectarivorous,
• depend on dense forests, and
• reach nearly to the southern extreme of the mainland, where rain falls year-round.

However,

• females of the meliphagid (https://www.graemechapman.com.au/library/viewphotos.php?c=268&pg=2) are duller-hued than those of the nectariniid (which are yellow and green, https://ebird.org/species/colsun2/TZ#:~:text=The%20male%20has%20a%20green,hover%20to%20catch%20insect%20prey.),
• the meliphagid, unlike the nectariniid, is nomadic and associated mainly with flowering Myrtaceae,
• the meliphagid forages conspicuously, whereas the nectariniid forages unobtrusively, and
• the size of the clutch may differ, with only the nectariniid likely to lay as many as three eggs per breeding-attempt.

The intercontinental difference in the nests - in size as well as shape - is illustrated in:

• M. sanguinolenta https://www.birdsinbackyards.net/species/Myzomela-sanguinolenta, vs
• H. collaris https://upload.wikimedia.org/wikipedia/commons/9/94/Collared_Sunbird_%28Hedydipna_collaris%29_female_on_nest_..._%2830429792623%29.jpg.

The meliphagid Myzomela obscura (https://www.inaturalist.org/taxa/12376-Myzomela-obscura and https://search.informit.org/doi/abs/10.3316/informit.658559031573707, body length 13 cm, body mass ? g) is a counterpart for the nectarinid Cyanomitra olivacea (https://www.inaturalist.org/taxa/145136-Cyanomitra-olivacea, body length 13 cm, body mass 9 g).

Both forms

• lack sexual dimorphism in colouration,
• lack iridescence, even in males while breeding,
• are remarkably dull-coloured, and
• occur in wildfire-free, dense forest on the northeastern coastal strips of the landmasses.

However,

• the beak of the meliphagid (https://www.inaturalist.org/observations/191065425 and https://www.inaturalist.org/observations/217817820 and https://www.inaturalist.org/observations/215657135 and https://www.inaturalist.org/observations/199062178 and https://www.inaturalist.org/observations/101925662) is shorter than that of the nectariniid (https://www.inaturalist.org/observations/107888671 and https://www.inaturalist.org/observations/65335377),
• the diet of the meliphagid is more generalised than that of the nectariniid,
• the tongue of the meliphagid is particularly different from that of the nectariniid, because its tip has a particularly complex brush-like structure, and
• the meliphagid lacks the bright-hued pectoral tufts retained by both sexes of the nectariniid (https://www.inaturalist.org/observations/7734503 and https://www.inaturalist.org/observations/91081303 and https://www.inaturalist.org/observations/226685593 and https://www.inaturalist.org/observations/193779256).

Finally:
Cinnyris frenatus (https://www.inaturalist.org/taxa/1504995-Cinnyris-frenatus, body length 10 cm, body mass ?8 g) of tropical northeasternmost Australia is extremely similar to Cinnyris venustus (https://www.inaturalist.org/taxa/145188-Cinnyris-venustus, body length 10 cm, body mass 7 g) of northeasternmost southern Africa.

Both spp. are equatorial to tropical. The colouration is similar, including the sexual difference. (Is the Australian species the less sexually dimorphic in colouration?)

This, the closest intercontinental matching of all in the present context, does not represent much evolutionary convergence. This is because

• the intercontinental counterparts belong to a single, exceptionally widespread and speciose (total 63 spp.) genus, and
• the main convergence is in body size within the genus (relative to e.g. Cinnyris coccinigastrus, which may have double this body mass, based on body length of 14 cm).

INTERCONTINENTAL SIMILARITY IN LACK OF LERP AND HONEYDEW IN DIETS

Meliphagids tend to eat honeydew/lerp/manna/extrafloral nectar as well as floral nectar (https://www.publish.csiro.au/mu/pdf/mu9800213#:~:text=Manna%2C%20honeydew%20and%20lerp%20have,of%20these%20resources%20and%20nectar. and https://www.tandfonline.com/doi/abs/10.1080/01584197.1980.11799277).

By contrast, nectariniids have not been recorded eating these alternative sugary exudates. The only exception of which I am aware is the ostensible eating of the sap of Elaeis guineensis (https://en.wikipedia.org/wiki/Elaeis_guineensis) by Cinnyris coccinigastrus (https://www.inaturalist.org/taxa/145182-Cinnyris-coccinigastrus), which may be anthropogenic.

I have not found any records of the eating of lerp/manna/extrafloral nectar in the meliphagids examined in this Post. This, as far as it goes, supports the notion of evolutionary convergence.

PHYLOGENETIC CONSTRAINTS?

The intercontinental differences pointed out here cannot be explained by means of phylogenetic constraints and the geographical isolation of Australia. This is because meliphagids show much adaptive versatility in relevant ways, including

• iridescence,
• form of the tongue, and
• form of the nest.

Iridescence is known in at least one species of meliphagid (https://en.wikipedia.org/wiki/T%C5%AB%C4%AB and https://www.inaturalist.org/taxa/12580-Prosthemadera-novaeseelandiae). Therefore, the failure of all the members of this family examined in this Post to develop iridescence is unlikely to be an accident of evolutionary history. It is instead likely to be adaptive in some poorly-understood way.

By a similar token, a brush-tipped, not tubular, tongue is known in at least one species of nectariniid (https://sora.unm.edu/sites/default/files/journals/condor/v073n04/p0485-p0486.pdf https://www.inaturalist.org/taxa/979744-Kurochkinegramma-hypogrammicum).

One species of meliphagid (https://www.inaturalist.org/taxa/12364-Ramsayornis-modestus), does actually build a nest similar to that of nectariniids (https://www.perplexity.ai/search/does-the-brown-backed-honeyeat-Owk0Fg1ySme.S4UJwWfsEA). This is particularly significant because the other species in the same genus builds a cup-shaped nest, typical of meliphagids.

Again: the failure of all the members of this family examined in this Post to build dome nests is unlikely to be an accident of evolutionary history. It is instead likely to be adaptive, and the relative paucity of certain predators on the 'island continent' is a possible factor.

Also relevant to the question of phylogenetic constraints is the fact that nectariniids have in fact reached Australia. Indeed, several genera of nectariniids may have reached what is now the Australian mainland, when there was a board land-bridge to what is now New Guinea. The failure of this avian family to undergo evolutionary radiation in Australia indicates ecological unsuitability rather than an accident of history.

Further investigation is warranted of the possible difference between meliphagids and nectariniids in predation on relatively large and venomous spiders. My impression from the literature is that nectariniids are the family more resembling 'arachnophages', in the sense that they use their long beaks not only to probe flowers, but also to kill spiders safely (https://www.inaturalist.org/posts/98889-failure-of-evolutionary-convergence-in-nectarivorous-birds-between-australia-meliphagidae-and-southern-africa-nectariniidae#activity_comment_0590a394-7178-4d76-bec2-11bc68b0e569).

Posted on September 17, 2024 11:18 PM by milewski