Promerops Cafer Research Articles

A demonstration of the value of recapture data for informing moult phenology models for avian species with imperfect moult data

The Underhill–Zucchini model has revolutionised the study of moult in the context of birds’ annual cycles, but, as for all statistical models, inferences are vulnerable to violations of model assumptions. In particular, the standard Underhill–Zucchini models for moult phenology are vulnerable to imperfect moult data arising, for example, from non-random sampling and/or the misclassification of non-moulting birds. Similarly, inference is challenging for species with dispersed moult periods (population-level moult extending beyond an annual cycle). Using ringing data from Cape Weavers Ploceus capensis and SAFRING data for Cape Sugarbirds Promerops cafer, we demonstrate how recent extensions to the Underhill–Zucchini framework can help the robust estimation of moult parameters in such situations, in particular when within-season recapture data is available.

Acute, Fatal, Presumptive Xylitol Toxicosis in Cape Sugarbirds ( Promerops cafer).

Twenty-nine wild Cape sugarbirds ( Promerops cafer) died acutely after ingestion of a homemade xylitol nectar solution from a bird feeder. The most aggressive feeders were first affected. Most birds showed clinical signs within 15 minutes of nectar ingestion, including incoordination, weakness, falling from perches, collapse, and death. A few birds showing clinical signs seemed to spontaneously recover and fly away. Full necropsy examinations done on 27 birds were hampered by freezing artifact and autolysis, but results indicated death was caused by the consequences of acute hypoglycemia. A presumptive diagnosis of xylitol toxicity was made based on the history, clinical signs, and absence of other obvious causes of death. This is potentially the first record of xylitol toxicity in wild birds.

Reproductive biology of three co-occurring, primarily small-mammal pollinated Protea species (Proteaceae)

This study investigated the role of vertebrates in the reproductive biology of a community of three co-occurring Protea species (Protea canaliculata, Protea sulphurea and Protea humiflora, Proteaceae) at Kraggashoek in the Western Cape, South Africa. Live-trapping, measures of facial and faecal pollen loads, and footage from remote cameras facing the inflorescences confirmed that all three are visited by small mammals and specialist nectarivorous birds. These plant species have bowl-shaped inflorescences that produce highly concentrated (34.1–42.9%) sucrose-rich nectar and a “yeasty” scent, typical traits of small-mammal pollinated plants. Camera footage indicated that 140 visits were made by eight small mammal species to an accumulative 19 inflorescences of the three Protea species. Small mammals thus made up 69% of total visits by all vertebrate species. Camera footage revealed that Micaelamys namaquensis visited flowers more frequently than any other vertebrate visitor (41% of total visitations by birds and mammals) but Elephantulus edwardii (10% of total visitations by birds and mammals) spent the longest time foraging on inflorescences (~28s per inflorescence). The ‘trap shy’ species, Graphiurus ocularis, was observed for the first time on camera, visiting Protea humiflora and Protea sulphurea inflorescences. Galerella pulverulenta (Cape gray mongoose) also visited inflorescences of P. canaliculata. The remaining 31% of total vertebrate visits, primarily to Protea humiflora, were by three species of specialist nectarivorous birds (the Cape sugarbird Promerops cafer, and the shorter-billed sunbirds, Anthobaphes violacea and Cinnyris chalybeus). Breeding system experiments with Protea sulphurea revealed that pollinators are needed for seed set, although exclusion of vertebrate pollinators only marginally lowered seed set of this partially self-incompatible species. These three Protea species had asynchronous flowering periods, supporting a wide range and relative abundance (overall live mammal trapping success rate of 22.7% nocturnal and 5.7% diurnal species) of vertebrate pollinators over a three month period in winter. That these Protea species co-occur suggests there is a community of vertebrate flower visitor species and primarily small mammal-pollinated plant species. The partitioning of nectar resources over a long period has conservation implications for both the plants and animals.

Birds Mediate a Fungus-Mite Mutualism.

Mutualisms between ophiostomatoid fungi and arthropods have been well documented. These fungi commonly aid arthropod nutrition and, in turn, are transported to new niches by these arthropods. The inflorescences of Protea trees provide a niche for a unique assemblage of ophiostomatoid fungi. Here, mites feed on Sporothrix fungi and vector the spores to new niches. Protea-pollinating beetles transport the spore-carrying mites between Protea trees. However, many Protea species are primarily pollinated by birds that potentially play a central role in the Protea-Sporothrix-mite system. To investigate the role of birds in the movement of mites and/or fungal spores, mites were collected from Protea inflorescences and cape sugarbirds, screened for Sporothrix fungal spores and tested for their ability to feed and reproduce on the fungal associates. Two mite species where abundant in both Protea inflorescences and on cape sugarbirds and regularly carried Sporothrix fungal spores. One of these mite species readily fed and reproduced on its transported fungal partner. For dispersal, this mite (a Glycyphagus sp.) attached to a larger mite species (Proctolaelaps vandenbergi) which, in turn, were carried by the birds to new inflorescences. The results of this study provide compelling evidence for a new mite-fungus mutualism, new mite-mite commensalisms and the first evidence of birds transporting mites with Sporothrix fungal spores to colonise new Protea trees.

Mutualism between co-occurring plant species in South Africa's Mediterranean climate heathland is mediated by birds.

Interactions among plant species via pollinators vary from competitive to mutualistic and can influence the probability of stable coexistence of plant species. We aimed to determine the nature of the interaction via flower visitors between Leucospermum conocarpodendron and Mimetes fimbriifolius, two shrubs in the Proteaceae that share many ecological traits and coexist on the Cape Peninsula, South Africa. To assess the extent of pollinator sharing we analysed nectar properties and recorded the pollinator fauna, their behaviour and contribution to seed set. To test for competition via interspecific pollen transfer, we recorded the movement patterns of pollinators and quantified pollen loads. To determine the effect of co-flowering on visitation rates we recorded visits in stands that varied in the density of the two species. We found that the species produce similar rewards and share pollinating Cape Sugarbirds (Promerops cafer). Interspecific pollen transfer is avoided by placing pollen on different parts of the bird. Both species are visited by nectar-thieving Orange-breasted Sunbirds (Anthobaphes violacea). Insects and autonomous self-pollination contributed little to seed set. Pollinator visits increased with conspecific density in both species, and the slope of the increase was steepest in the presence of high densities of the co-occurring plant species. Nectar thief visits also increased with conspecific density in both species, but the slope declined with increasing density of the co-occurring species. Co-occurrence enhanced pollinator visits and alleviated nectar robbing in both plant species, consistent with mutualisms. Mutualism within a trophic level is unusual, but may help to explain the stable coexistence of ecologically similar species.

Urbanization, climate and ecological stress indicators in an endemic nectarivore, the Cape Sugarbird

Stress, as a temporary defense mechanism against specific stimuli, can place a bird in a state in which growth rates and resistance to diseases are diminished. The Cape Sugarbird Promerops cafer is an endemic specialist of the Cape Floristic Region (CFR) of South Africa that may be threatened by urbanization and climate change. Ecological stress due to urbanization and climate may result in disease and morphological abnormalities. We investigated the correlation between urbanization and climate and four ecological stress indicators (tarsal disease, fluctuating asymmetry, body condition and feather fault bars) in 1375 Cape Sugarbirds from 14 sites across the CFR. Sugarbirds at sites with warmer climates had a higher incidence of tarsal disease and fault bars. Birds closer to urban settlements had higher levels of fluctuating asymmetry and fault bars in feathers. There were no clear correlations among stress indicators. Cape Sugarbirds are subject to multiple stressors, and adequate monitoring of population health will require assessment of multiple rather than single stress responses.

A bird pollinator shows positive frequency dependence and constancy of species choice in natural plant communities.

Animal pollinators mediate reproduction of many plant species. Foraging theory suggests that animal pollinators exhibit preferences for common plant species in natural communities (positive frequency-dependent foraging) and temporary single-species specialization (flower constancy) during foraging bouts. Positive frequency dependence may favor common plant species; flower constancy may enhance conspecific pollen transfer particularly in rare plant species. Previous experimental studies suggest that avian pollinators are unlikely to exhibit these behaviors. We studied foraging behavior of Cape Sugarbirds (Promerops cafer), the main avian pollinator of many Protea species, using focal-plant and focal-bird sampling, assisted by high-resolution maps of the spatiotemporal distribution of Protea individuals and their flowering status. We found that Sugarbird's visitation preference increased with species' relative floral abundance, and that individual Sugarbirds tended to visit single species in sequence. Flower constancy during foraging bouts was significantly higher than expected from random plant-animal encounters at the scale of pollinator movements. Positive frequency dependence may favor the reproduction of abundant plant species while flower constancy may be particularly important for rare plant species. This first simultaneous study of both behaviors in a natural plant-pollinator system shows that bird pollinators exhibit both types of behavior and, in this way, possibly influence plant community structure.

Responses of nectar‐feeding birds to floral resources at multiple spatial scales

The responses of animal pollinators to the spatially heterogeneous distribution of floral resources are important for plant reproduction, especially in species‐rich plant communities. We explore how responses of pollinators to floral resources varied across multiple spatial scales and studied the responses of two nectarivorous bird species (Cape sugarbird Promerops cafer, orange‐breasted sunbird Anthobaphes violacea) to resource distributions provided by communities of co‐flowering Protea species (Proteaceae) in South African fynbos. We used highly resolved maps of about 125 000 Protea plants at 27 sites and estimated the seasonal dynamics of standing crop of nectar sugar for each plant to describe the spatiotemporal distribution of floral resources. We recorded avian population sizes and the rates of bird visits to > 1300 focal plants to assess the responses of nectarivorous birds to floral resources at different spatial scales. The population sizes of the two bird species responded positively to the amount of sugar resources at the site scale. Within sites, the effects of floral resources on pollinator visits to plants varied across scales and depended on the resources provided by individual plants. At large scales (radii > 25 m around focal plants), high sugar density decreased per‐plant visitation rates, i.e. plants competed for animal pollinators. At small scales (radii < 5 m around focal plants), we observed either competition or facilitation for pollinators between plants, depending on the sugar amount offered by individual focal plants. In plants with copious sugar, per‐plant visitation rates increased with increasing local sugar density, but visitation rates decreased in plants with little sugar. Our study underlines the importance of scale‐dependent responses of pollinators to floral resources and reveals that pollinators’ responses depend on the interplay between individual floral resources and local resource neighbourhood.

Floral divergence in closely related Leucospermum tottum (Proteaceae) varieties pollinated by birds and long-proboscid flies

The Proteaceae are renowned for their floral diversity but surprisingly the role of pollinators in driving evolutionary divergence in this family has been underexplored. Here we focus on recently diverged taxa to gain insight into the processes that generate diversity by testing whether two varieties of Leucospermum tottum might have originated by pollinator mediated adaptive divergence. L. tottum var. tottum has pale salmon-coloured horizontally-oriented flowers, long nectar tubes, and small volumes of concentrated nectar. L. tottum var. glabrum has red and yellow vertically oriented flowers, short nectar tubes, and large volumes of dilute nectar. Despite the morphological divergence, the varieties are indistinguishable using eight molecular markers, indicating a very early stage of differentiation. Consistent with their morphologies, L. tottum var. tottum is pollinated by long-proboscid flies (Philoliche rostrata and Philoliche gulosa), Cape sugarbirds (Promerops cafer), and, to a lesser extent, by Orange-breasted sunbirds (Anthobaphes violacea), whereas, L. tottum var. glabrum is pollinated only by Orange-breasted sunbirds. A. violacea visits both varieties, but makes more frequent contact with pollen presenters when foraging on L. tottum var. glabrum. The exclusion of birds caused a steeper reduction in seed production in L. tottum var. glabrum than in L. tottum var. tottum, consistent with specialization for bird-pollination in this variety. Additionally, L. tottum var. glabrum exhibits autogamy, whereas L. tottum var. tottum does not. Floral divergence between the two L. tottum varieties corresponds with divergence in pollinator use.

Urbanization Drives a Reduction in Functional Diversity in a Guild of Nectar-feeding Birds

Urbanization is a widespread and rapidly growing threat to biodiversity, therefore we need a predictive understanding of its effects on species and ecosystem processes. In this paper we study the impact of urbanization on a guild of nectar-feeding birds in a biodiversity hotspot at the Cape of Africa. The guild of four bird species provides important ecosystem services by pollinating 320 plant species in the Cape Floral Region. Functional diversity within the guild is related to differences in bill length. The long-billed Malachite Sunbird (Nectarinia famosa) plays an irreplaceable role as the exclusive pollinator of plant species with long nectar tubes. We analyzed the composition of the guild in suburban gardens of Cape Town along a gradient of increasing distance from the nearest natural habitat. Urbanization reduces the functional diversity of the nectarivore guild. Malachite Sunbirds did not penetrate more than 1 km into the city, whereas only the short-billed Southern Double-collared Sunbirds (Cinnyris chalybea) occurred throughout the urbanization gradient. The lack of data precludes conclusions regarding the detailed responses of Orange-breasted Sunbirds (Anthobaphes violacea) and Sugarbirds (Promerops cafer), however their absence across the entire gradient is suggestive of high sensitivity. The functional diversity of this guild of pollinators can potentially be restored, but the pros and cons of this conservation action need to be considered.

Fynbos Fires May Contribute to the Maintenance of High Genetic Diversity in Orange-Breasted Sunbirds (Anthobaphes violacea)

The maintenance of genetic diversity in populations is one of the key concerns in wildlife management. Levels of genetic diversity are partly determined by the evolutionary history of a population and partly by environmental factors which affect population size, gene flow and mating systems. In this study, we used microsatellite DNA markers to assess the level of genetic diversity in a population of orange-breasted sunbirds (Anthobaphes violacea), an endemic nectarivore in the fynbos biome at Jonkershoek Nature Reserve, South Africa. We found high levels of genetic diversity in this population, with an average of 19 alleles per locus, and both expected and observed heterozygosities of 0.84. The level of genetic diversity found in this species is comparable to that of Cape sugarbirds (Promerops cafer), a fellow fynbos endemic, but higher than that reported for other species of nectarivorous birds not affected by frequent habitat fires. We suggest that the destruction of flowering plants by fires, forcing birds to disperse, may have contributed to the maintenance of high levels of genetic diversity through encouraging outbreeding in orange-breasted sunbirds and Cape sugarbirds. We also discuss the implications of our findings for management of these species.

Farming with native bees (Apis mellifera subsp. capensis Esch.) has varied effects on nectar‐feeding bird communities in South African fynbos vegetation

AbstractOutside their natural range, honeybees (Apis mellifera) are known to have detrimental effects on indigenous pollinators through exploitative or interference competition, but little is known about the effect of honeybee farming in areas where honeybees occur naturally. In the Cape Floristic Region of South Africa, where honeybees are indigenous, managed hives potentially elevate the abundance of honeybees far above natural levels, but impacts on other floral resource‐dependent species have not been studied. Here we use experimental manipulation of honeybee density to test whether honeybee farming affects nectar‐feeding birds. We selected the common sugarbush (Protea repens), utilized by both birds and bees, and analysed the time (before/after) by treatment (control/experiment) interaction to explore changes in bee abundance, nectar availability and bird abundance at three sites. Hive addition increased honeybee abundance in inflorescences of P. repens above expected levels. Despite experimental increase in honeybee numbers, there is no reduction in nectar sugar availability relative to the control areas. Where honeybee density was highest, sugarbird (Promerops cafer) numbers declined relative to expected, but sunbirds (Nectarinidae) were not affected at any of the sites. We conclude that stocking rates of more than one honey bee per P. repens inflorescence have detrimental effects on bird abundance due to interference, rather than resource competition.

Female Cape sugarbirds (Promerops cafer) modify egg investment both for extra‐pair mates and for male tail length

The differential allocation hypothesis predicts that females should invest more in reproduction when paired with attractive males. We measured egg volume in Cape sugarbirds (Promerops cafer), a sexually dimorphic passerine, in relation to paternity of the offspring and in response to an experimental tail length treatment. We manipulated tail length, after pair formation, but before egg laying: males had their tails either shortened or left unmanipulated. Our manipulation was designed to affect female allocation in a particular breeding attempt rather than long-term mate choice: males with shortened tails would appear to be signalling at a lower level than they should given their quality. We found that egg volume was smaller in the nests of males with experimentally shortened tails but larger when the offspring were the result of extra-pair matings. Both these findings are consistent with the differential allocation hypothesis. We suggest that tail length may be used by females as a cue for mate quality, eliciting reduced female investment when breeding with social mates; and with males with shortened tails.

Long tails matter in sugarbirds—positively for extrapair but negatively for within-pair fertilization success

Extrapair mating is known to occur in many animals and potentially has a significant influence on reproductive success. Female extrapair mate choice may explain the occurrence of exaggerated ornaments in socially monogamous species, but the influence of ornamentation on extrapair mating success has rarely been investigated experimentally. Cape sugarbirds (Promerops cafer) are socially monogamous, almost always lay 2 egg clutches and have long-term pair bonds often lasting several seasons. However, they also display sexually dimorphic extravagant ornamentation in the form of a long, graduated tail and have one of the highest rates (65% of young) of extrapair paternity recorded in birds. We provide a test of the hypothesis that the ornamented tail is used in mate choice for extrapair partners by conducting an experiment in which tail length was manipulated after social mating but before copulation. This experiment therefore allowed females to respond to the manipulation of male tail length when making a choice of copulation partner but not social mate. We show that the tail length of male sugarbirds has a significant effect on the success of males in gaining extrapair paternity, with long-tailed males obtaining significantly more extrapair young than shorttailed males. However, males with short tails sire a significantly greater proportion of the nestlings in their own nests than longtailed individuals. This result suggests that males may adopt alternative strategies dependent on their ornamentation. Key words: extrapair mating, mate choice, Pomerops cafer, sexual selection, sugarbird, tail ornamentation. [Behav Ecol]

Morphological characteristics of Cape sugarbirds (Promerops cafer) from Helderberg Nature Reserve

Cape sugarbirds (Promerops cafer) are the largest nectarivores in the Western Cape and feed almost exclusively on protea nectar and associated arthropods. Helderberg Nature Reserve, Western Cape, South Africa, has a large diversity of Protea and supports breeding sugarbirds. As part of a larger study, we captured sugarbirds using mist-nets during the breeding and non-breeding season at several sites in the Helderberg Nature Reserve, Western Cape, South Africa, from 1996 to 2000. From these data (n =283 males, 272 females), we found that in both sexes, individuals with longer tails have longer wings. Males were significantly larger in mass, culmen, head, tarsus, wing and tail length than females. Males with larger mass were larger in all morphometric measurements than those with smaller mass. Mate choice and territory defence may be based on wing and tail ornament displays of male sugarbirds, thus larger males with larger ornaments could benefit through greater breeding success than smaller males.

Patterns of morphological variation in two sexually dimorphic bird species with different tail shapes

Many studies have focused on tail ornamentation in birds, but not all tail shapes have been studied in depth. Graduated and pin tails have received less attention than forked tails, despite being more likely, in terms of aerodynamic theory, to be honest signals. We report morphological variation in live specimens of two sexually dimorphic passerines from the same site with different tail shapes: graduated (Cape sugarbird Promerops cafer) and pin (orange-breasted sunbird Antobaphes violacea). Coefficients of variation (CVs) were calculated for all morphological traits, both non-ornamental (range 1.91–5.72) and ornamental (range 5.83–21.71). Males and females did not differ in CV for any non-ornamental trait. Ornamental traits in males of both species were significantly more variable than all non-ornamental traits. Cape sugarbird ornamental traits were significantly more variable than those of orange-breasted sunbirds. The high levels of variation in graduated tails relative to pintails suggest that these traits have been driven mainly by sexual selection. In contrast, both constraining natural and multiple ornament selection could be responsible for the relatively low levels of variation in pintails. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 437–443.

Morphological characteristics of Cape sugarbirds (Promerops cafer) from Helderberg Nature Reserve

Cape sugarbirds (Promerops cafer) are the largest nectarivores in the Western Cape and feed almost exclusively on protea nectar and associated arthropods. Helderberg Nature Reserve, Western Cape, South Africa, has a large diversity of Protea and supports breeding sugarbirds. As part of a larger study, we captured sugarbirds using mist-nets during the breeding and non-breeding season at several sites in the Helderberg Nature Reserve, Western Cape, South Africa, from 1996 to 2000. From these data (n =283 males, 272 females), we found that in both sexes, individuals with longer tails have longer wings. Males were significantly larger in mass, culmen, head, tarsus, wing and tail length than females. Males with larger mass were larger in all morphometric measurements than those with smaller mass. Mate choice and territory defence may be based on wing and tail ornament displays of male sugarbirds, thus larger males with larger ornaments could benefit through greater breeding success than smaller males.

Apparent survival rates of Cape Sugarbirds Promerops cafer at a breeding and a non-breeding site

Reliable estimates of survival rates of southern African bird species are still rare. Yet precise information on life history traits of birds from this southern Mediterranean-type climate would help in evaluating the generality of global patterns of avian life history. We estimated annual survival of Cape Sugarbirds Promerops cafer at a breeding site and a non-breeding site, using capture-mark-recapture methods. Consistent between the two sites, annual survival was 0.54 for females and 0.64 for males, with an average of 0.62 at the breeding site. These estimates are close to estimates for more tropical African species, but at the upper range of estimates for northern-temperate passerines. With their small clutches, Cape Sugarbirds thus have a life history that is more similar to tropical passerines than to northern-temperate passerines. We found a high proportion of transient individuals at the non-breeding site, but not at the breeding site. This suggests that Cape Sugarbirds employ two strategies to cope with the spatially variable food supply during the non-breeding season. About half of the individuals appear to visit the same set of sites every year, whereas the others are more opportunistic and tend to visit different sites in different years.

Isolation of highly polymorphic autosomal microsatellite loci and a sex‐linked locus from sugarbirds

AbstractWe describe the isolation of six tetranucleotide microsatellites from the Cape sugarbird (Promerops cafer) using an enrichment protocol. All loci were highly variable with number of alleles ranging from nine to 26 and values of observed heterozygosity ranging from 0.534 to 0.931. All loci were in Hardy–Weinberg equilibrium with the exception of Pro66 and Pro86. Further analysis of Pro86 indicated it was Z‐linked. All loci amplified and were variable in the congeneric Gurneys sugarbird (Promerops gurneyi). These loci will be used in mating system and phylogeographic studies of Cape sugarbirds in South Africa.

Do sugarbirds feed on arthropods inside or outside Protea inflorescences?

The nectar of Protea inflorescences attracts sugarbirds (Promeropidae) as well as a large diversity of arthropods. In addition to feeding on nectar, sugarbirds feed on arthropods; but do sugarbirds feed on the arthropods within Protea inflorescences? Through the use of arthropod collections from within Protea inflorescences and diet sampling data from previous studies together with arthropod samples collected during the current study, we investigated whether sugarbirds fed on arthropods found inside Protea inflorescences or whether most arthropods taken were flying arthropods, seldom found in Protea inflorescences. Cape (Promerops cafer) and Gurney's (Promerops gurneyi) Sugarbirds showed a strong preference for flying insects, tourist or visitor species to Protea inflorescences, particularly Scarabaeidae and Apidae. Cape Sugarbirds showed a preference for Diptera and Gurney's Sugarbirds showed a preference for Heteroptera. Small arthropods found within Protea inflorescences, for example ants, may be eaten accidentally while the sugarbirds are feeding on nectar. The results of this study support the hypothesis that sugarbirds feed on arthropods by hawking rather than obtaining them from within Protea inflorescences.