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Human facilitation of sap‐feeding birds in the Bijagós archipelago, West Africa

2019; Wiley; Volume: 162; Issue: 1 Linguagem: Inglês

10.1111/ibi.12790

1474-919X

Jorge S. Gutiérrez, Teresa Catry, José P. Granadeiro,

Wildlife Ecology and Conservation

IbisVolume 162, Issue 1 p. 250-254 ViewpointFree Access Human facilitation of sap-feeding birds in the Bijagós archipelago, West Africa Jorge S. Gutiérrez, Corresponding Author Jorge S. Gutiérrez jsgutierrez.bio@gmail.com orcid.org/0000-0001-8459-3162 Centro de Estudos do Ambiente e do Mar, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Lisboa, 1749-016 Portugal Corresponding author Email: jsgutierrez.bio@gmail.com Twitter: @_JSGutierrezSearch for more papers by this authorTeresa Catry, Teresa Catry orcid.org/0000-0003-4047-9995 Centro de Estudos do Ambiente e do Mar, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Lisboa, 1749-016 PortugalSearch for more papers by this authorJosé Pedro Granadeiro, José Pedro Granadeiro orcid.org/0000-0002-7207-3474 Centro de Estudos do Ambiente e do Mar, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Lisboa, 1749-016 PortugalSearch for more papers by this author Jorge S. Gutiérrez, Corresponding Author Jorge S. Gutiérrez jsgutierrez.bio@gmail.com orcid.org/0000-0001-8459-3162 Centro de Estudos do Ambiente e do Mar, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Lisboa, 1749-016 Portugal Corresponding author Email: jsgutierrez.bio@gmail.com Twitter: @_JSGutierrezSearch for more papers by this authorTeresa Catry, Teresa Catry orcid.org/0000-0003-4047-9995 Centro de Estudos do Ambiente e do Mar, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Lisboa, 1749-016 PortugalSearch for more papers by this authorJosé Pedro Granadeiro, José Pedro Granadeiro orcid.org/0000-0002-7207-3474 Centro de Estudos do Ambiente e do Mar, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Lisboa, 1749-016 PortugalSearch for more papers by this author First published: 08 November 2019 https://doi.org/10.1111/ibi.12790AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Background Few animal groups have evolved the ability to feed on phloem sap (Douglas 2006) yet some bird species (e.g. woodpeckers and hummingbirds) include this energy-rich food resource in their diets (Southwick & Southwick 1980, Sutherland et al. 1982, Núñez Montellano et al. 2013). The facilitation of sap-feeding birds by woodpeckers is widespread and well documented: several species of woodpeckers drill ‘sap wells’ into trees that provide abundant nourishment for themselves, but also for insects, mammals and other birds that otherwise would not be able to reach this food resource (Foster & Tate 1966, Sutherland et al. 1982, Ehrlich & Daily 1988, Daily et al. 1993, Blendinger 1999, Núñez Montellano et al. 2019, Winkler & Christie 2019a). However, very few cases are known where animal species other than woodpeckers enable other species to exploit sap. Notably, Chapman et al. (1999) reported observations of 16 species of birds foraging at sap-scars made by Yellow-bellied Gliders Petaurus australis. To our knowledge, there are only two published reports of sap-feeding by birds taking advantage of sap wells made by humans. Kilham (1964) first reported that Yellow-bellied Sapsuckers Sphyrapicus varius in New Hampshire, USA, targeted trees that had been injured by snow ploughs and undercutting of banks. By drilling holes in already wounded trees, sapsuckers may have induced a greater and more concentrated flow. More recently, Rasal (2015) reported observations of three bird species (Black Drongo Dicrurus macrocercus, Rose-ringed Parakeet Psittacula krameri and Common Myna Acridotheres tristis) opportunistically feeding on the sap of tapped wild Date Palm Phoenix sylvestris in India. Here we document the first cases of human facilitation of sap-feeding by three species of African forest birds that are unable to exploit this resource on their own. Case study Study area and species We recorded three bird species (Village Weaver Ploceus cucullatus Ploceidae, Common Bulbul Pycnonotus barbatus Pycnonotidae, and Mouse-brown Sunbird Anthreptes gabonicus Nectariniidae) regularly feeding on the sap flowing from holes made by local wine tappers in Oil-palm trees Elaies guineensis in the Bijagós archipelago, Guinea-Bissau (Fig. 1). Palm wine is deeply rooted in West African culture and traditions and is the most frequently consumed alcoholic beverage – mainly in non-Islamic regions where alcohol consumption is not religiously prohibited. In the Bijagós, wine tappers make an incision above the base of the inflorescence and insert a folded leaf ‘funnel’ in it to lead the sap into a container placed under the hole (Fig. 1). They then climb up the trees and collect the naturally fermented sap (or binho di palma as it is called locally) from the bottles in the early morning (06.00–08.00 h) and late afternoon (17.00–19.00 h), usually consuming it soon after collection (within 24 h). Figure 1Open in figure viewerPowerPoint (a) Local wine tapper harvesting wine from an Oil-palm tree Elaies guineensis on Orango island, Guinea-Bissau. (b) Village Weaver Ploceus cucullatus, (c) Common Bulbul Pycnonotus barbatus and (d) Mouse-brown Sunbird Anthreptes gabonicus feeding on the sap flowing from holes made by wine tappers. Distribution ranges of (e) Village Weaver, (f) Common Bulbul and (g) Mouse-brown Sunbird. Areas shaded green correspond to the species shapefiles downloaded from the IUCN RedList (http://www.iucnredlist.org/, accessed in April 2019). The grey diamond depicts the Bijagós Archipelago. Countries in which palm-wine tapping (from various species of palm trees) is common are indicated with black stripes (sources: Dowson 1953, Amoa-Awua et al. 2007, Ogbulie et al. 2007, Noll 2008, Carrere 2010, Bisi-Johnson et al. 2011, Babitseng & Teketay 2013). [Colour figure can be viewed at wileyonlinelibrary.com] During the dry season, from January to April 2019, we made almost daily observations (totalling approximately 180 h) of birds feeding on the sap of four tapped Oil-palm trees located at two different locations (about 400 m away from each other) on Orango island. Two trees were located in a forest with a small human settlement, and the other two were in the nearby savanna close to the forest edge. Birds of the three species visited the sap holes and perched on the wooden sticks that tappers use to nail the leaf funnels to the sap holes. They seemed to be familiar with the location and productivity of the sap holes, as they typically arrived directly at active holes and proceeded to forage at the most productive hole – based on the amount of sap in the containers. Common Bulbuls were the most common visitors to the sap holes and their visits were, on average, longer (103 ± 15 s, n = 17 timed visits, mean ± se) than those of Village Weavers (64 ± 7 s, n = 10) or Mouse-brown Sunbirds (45 ± 5 s, n = 6). There is no previous evidence of sap feeding in any of these three bird species; however, they belong to families with diets based on fruits and nectar and also high efficiency in assimilation of sucrose (the major sugar component of sap) (Lotz & Schondube 2006). Both the Village Weaver and the Common Bulbul have a diverse diet that includes the epicarp of the Oil-palm nut (Craig & de Juana 2019, Fishpool & Tobias 2019), whereas the Mouse-brown Sunbird mainly hunts insects (Cheke & Mann 2019). In addition, the Grey Woodpecker Mesopicos goertae – another common resident of the Bijagós – does not rely on sap but primarily on arthropods (Winkler & Christie 2019b), meaning that they cannot enable other birds to gain access to sap. Although our observations cover only the dry season in one locality, these human–bird associations may apply to a much broader geographical area (see Fig. 1 for the geographical ranges of bird species and wine tapping in Africa) and possibly to other species as well (see Rasal 2015 for similar human–bird associations in Asia). For instance, frugivorous and nectarivorous birds closely associated with villages in the forested zone of Central-West Africa (e.g. Swamp Palm Bulbul Thescelocichla leucopleura, Yellow-chinned Sunbird Anthreptes rectirostris and Collared Sunbird Hedydipna collaris) and India (e.g. Baya Weaver Ploceus philippinus and Purple-rumped Sunbird Leptocoma zeylonica) could potentially feed on sap. Inter- and intraspecific agonistic interactions We observed both inter- and intraspecific agonistic interactions at sap holes (i.e. displacements involving chasing, fighting or a combination of both), which suggests the existence of interference competition. During agonistic interspecific interactions (n = 10) the larger Common Bulbul (29–49.5 g) and Village Weaver (33–46 g) always displaced the smaller Mouse-brown Sunbird (8–13 g). These observations agree with those of studies reporting hierarchical organization among facultatively sap-feeding heterospecifics (Blendinger 1999, Chapman et al. 1999, Núñez Montellano et al. 2013). On six occasions, weavers aggressively defended their sap holes from conspecifics. Sugar and ethanol content of palm sap Sap may contain a significant amount of sugars, mainly sucrose (Taiz & Zeiger 2002). As a result of natural fermentation, sap feeding may also entail ethanol ingestion by birds. We measured the sucrose content (Brix %; i.e. g sucrose in 100 g of solution) and approximate ethanol content (% alcohol by volume, %ABV) of palm sap using refractometer readings (HHTEC RHW-25; ± 0.2% Brix and ± 0.2% ABV) from two Oil-palm trees visited by birds. It is important to note that this instrument gives accurate measures of sugar concentration in the unfermented sap (and the alcohol content of the resulting wine), as once it starts fermenting any reading will be inaccurate due to the fact that alcohol has a higher refractive index than water. Hence, we collected sap from sap wells used by birds instead of from containers containing the fermenting sap (Fig. 1), which was inaccessible for birds. For each sample, two drops of palm sap were collected in situ at the morning harvest, and every 2 h thereafter, until the evening harvest. The sap averaged 12.96% Brix (range = 11.5–14.5%, n = 12) and 6.65% ABV (range = 5.6–7.6%, n = 12). The level of sucrose in the sap decreased throughout the day (linear model with BRIX % as response and time as covariate: F1,10 = 11.9, P = 0.006) as it converts to ethanol as a result of fermentation. In the wild, frugivorous and nectarivorous birds often eat fermenting fruits and nectar, and thus may consume levels of ethanol that could induce inebriation (Eriksson & Nummi 1982, Fitzgerald et al. 1990, Kinde et al. 2012). Previous work has shown that the effects of ethanol consumption can be negligible for some facultative or occasional nectarivores/frugivores (Mazeh et al. 2008, Zungu & Downs 2017). In addition, there is experimental evidence that Yellow-vented Bulbuls Pycnonotus xanthopygos decrease food intake when food ethanol concentration is relatively high, suggesting that birds may use behavioural mechanisms to avoid intoxication (Mazeh et al. 2008). We have no indications that sap feeding influenced birds’ behaviour or flying ability (see Dennis (1987) and unpublished observations reported in Eriksson and Nummi (1982)). An experimental trial to provide birds with access to fermenting and non-fermenting palm sap is needed to test whether increasing sap ethanol concentration could influence behaviour. Another case of cultural transmission in wild birds? The birds in our study site were not individually marked; however, we are certain that several different individuals fed on the sap of tapped Oil-palm trees (some birds were simultaneously observed at different sap wells, on either the same or different trees). This raises the question of whether cultural transmission (i.e. social learning) plays a role in the spread of this foraging innovation, as seems to be the case for wild, sap-feeding Chimpanzees Pan troglodytes from Guinea (Hockings et al. 2015). Cultural transmission also exists among non-primate animals, including birds. In the early 20th century, British tits (Great Tits Parus major and Blue Tits Cyanistes caeruleus) learned to open milk bottles to drink the layer of cream beneath the caps (Fisher & Hinde 1949); this is one of the most widely cited cases of cultural transmission in animals (Lefebvre 1995, Aplin et al. 2013, 2015). The bird species studied here, particularly the Village Weaver, are highly social and live in proximity to conspecifics. Thus, sap-feeding may potentially spread among them. Social-learning experiments (Aplin et al. 2015) in which wild-caught birds seeded with trained demonstrators need to solve a novel puzzle to access a resource could help answer this question. Moreover, spatial analyses (e.g. spatial auto- and cross-correlation analyses, see Saracco et al. 2004) could help our understanding of whether birds rely on one another to find ephemeral and patchily distributed palm wine trees. Indeed, social facilitation can be particularly important for tropical frugivorous and nectarivorous birds because the distribution of fruit patches is often especially heterogeneous in space and time (Saracco et al. 2004). Alternatively, this behavioural innovation may arise independently at different sites as a consequence of the presence of similar opportunities. Given the taxonomic diversity and geographical distribution of birds exhibiting this behaviour (at least six resident species belonging to six different families from two continents; this study and Rasal 2015), it seems likely that ecological pressure paired with opportunism could have led to this foraging innovation. In this context, one might expect birds to consume more sap during the dry season, when the supply of water and food resources such as arthropods and fleshy fruits is low. For instance, White-fronted Woodpeckers Melanerpes cactorum from semi-arid forests drill holes throughout the year, but sap consumption by this and other bird species is much greater during the dry season (Blendinger 1999, Núñez Montellano et al. 2013, 2019). Conclusions We show that birds from three African forest species regularly drink palm sap by taking advantage of a human-made activity, representing a rare case of facilitation where humans indirectly provide food to birds that are not morphologically adapted to drill wells in plants to feed on sap flows. Agonistic interactions suggest the existence of interference competition among and within sap-feeding species. Moreover, our data suggest that birds may consume ethanol as a by-product of sap fermentation. Many questions remain unanswered, such as whether sap-feeding arises via cultural transmission and/or as a consequence of ecological pressure(s). The Bijagós archipelago is an exceptional theatre in which to investigate human facilitation of sap-feeding birds, as it is composed of more than 80 islands and islets representing naturally fragmented landscapes, where the occurrence of human-assisted sap-feeding might be studied with relative ease. Understanding this human–plant–bird interaction requires new observations from this and other palm-growing regions of the world. We thank wine tappers Agostinho João Openor and Alexandre Dias Correia (‘Tchando’) for making our observations possible and collecting sap for the refractometer measures. We gratefully acknowledge the support of the Instituto da Biodiversidade e das Áreas Protegidas of Guinea-Bissau. Fieldwork was part of the projects ‘Waders of the Bijagós’ (MAVA Foundation) and ‘MigraWebs’ (PTDC/BIA-ECO/28205/2017, FCT). Thanks are due for the financial support to CESAM (UID/AMB/50017/2019) to FCT/MCTES through national funds. 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Volume162, Issue1January 2020Pages 250-254 FiguresReferencesRelatedInformation