Abstract
The relationship between mistletoes and their host trees constitutes one of the unique host–parasite interactions in ecosystems. Most West African studies have reported on the parasitic nature of the relationship between Tapinanthus dodoneifolius mistletoes and Parkia biglobosa trees. However, there is little on bird species’ use and subsequent dispersal of the mistletoe on P. biglobosa, and consequently, we investigated aspects of this relationship in the present study. We conducted our study in Amurum Forest Reserve, located in the central part of Nigeria, from May to September 2017. The study area consists of a mosaic of savanna, gallery forest, and rocky outcrops. Of the bird community in this area, the yellow-fronted Tinkerbird Pogoniulus chrysoconus had the highest number of visits to T. dodoneifolius fruits, while the Senegal Eremomela Eremomela pusilla spent the most time foraging on the fruits. Four sunbird species were recorded feeding on T. dodoneifolius flowers for nectar; all but the Copper Sunbird Cinnyris cupreus were observed opening the flowers of T. dodoneifolius. Other bird species were recorded foraging on insects on T. dodoneifolius, and some simply perching on twigs or pecking on mistletoe fruits. This was a mutualistic relationship between the respective bird species and the mistletoe. This indirectly benefitted the parasitised host by attracting potential pollinators, seed dispersers, and insectivores for the host, hence, improving the rate of visitation to the host. These patterns of visitation behaviours highlighted the ecological importance of T. dodoneifolius within the reserve, particularly in enhancing the survival of other taxa within the reserve. Findings from this study contribute to developing more-nuanced conservation strategies for mixed high savannah habitat types across the tropics.
Zusammenfassung
Vögel nutzen Tapinanthus dodoneifolius-Misteln, die an Johannisbrotbäumen Parkia biglobosa im Amurum-Waldreservat, Nigeria, parasitieren
Die Beziehung zwischen Misteln und ihren Wirtsbäumen ist eine der einzigartigen Wirt-Parasit-Interaktionen in Ökosystemen. Die meisten westafrikanischen Studien haben die parasitären Aspekte der Beziehung zwischen Tapinanthus dodoneifolius-Misteln und den Bäumen der Parkia biglobosa untersucht, aber nur wenige die Nutzung der Misteln durch Vögel und die daraus resultierende Verbreitung der Misteln. Deshalb haben wir uns in unserer Arbeit auf diesen Aspekt der Beziehung konzentriert. Wir führten unsere Untersuchung von Mai bis September 2017 im Amurum Wald-Reservat im zentralen Teil Nigerias durch. Das Untersuchungsgebiet besteht aus einem Mosaik aus Savanne, Galeriewald und felsigen Aufschlüssen. Von den Vögeln dort besuchte der Gelbstirn-Bartvogel Pogoniulus chrysoconus die Früchte der Misteln am häufigsten, während der Graukappeneremomela Eremomela pusilla die meiste Zeit mit dem Fressen der Früchte verbrachte. Vier Nektarvögel-Arten wurden bei der Nektaraufnahme an den Mistelblüten beobachtet, wobei alle außer dem Kupfernektarvogel Cinnyris cupreus dabei gesehen wurden, wie sie Blüten der T. dodoneifolius-Misteln öffneten. Andere Vogelarten wurden beim Verzehr von Insekten auf den Misteln beobachtet, während einige nur einfach auf Zweigen hockten oder auf Mistelfrüchten herumpickten. All dies war eine für beide nutzbringende Beziehung zwischen der Mistel und der jeweiligen Vogelart; dem parasitierten Wirt kam zugute, dass potenzielle Bestäuber, Samenverbreiter und Insektenfresser für ihn angelockt wurden und damit die Rate der Besuche beim Wirt erhöhte. Diese Muster des Besuchsverhaltens unterstreichen die ökologische Bedeutung von T. dodoneifolius innerhalb des Reservats, insbesondere durch die Erhöhung der Überlebenschancen anderer Taxa im Reservat. Die Ergebnisse dieser Studie tragen dazu bei, differenziertere Schutzstrategien für gemischte Hochsavannen-Habitattypen in den Tropen zu entwickeln.
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Data are available from the authors on request.
References
Adesina SK, Illoh HC, Johnny II, Jacobs IE (2013) African mistletoes (Loranthaceae); Ethnopharmacology, chemistry and medicinal values: An update. Afr J Tradit Complement Altern Med 10:61–170
Aizen MA (2003) Influences of animal pollination and seed dispersal on winter flowering in a temperate mistletoe. Ecology 84:2613–2627
Aliero BL, Samaila A (2000) The occurrence of parasitic mistletoe (Tapinanthus spp.) on Parkia biglobosa (Jacq.) Benth (African Locust Bean Tree) in Yauri Local Government Area, Kebbi State. Nig J Basic Appl Sci 9:5–10
Amico GC, Sasal Y, Vidal-Russell R, Aizen MA, Morales JM (2017) Consequences of disperser behaviour for seedling establishment of a mistletoe species. Austral Ecol 42:900–907
Amusa O, Adesoye A, Ogunkanmi A, Omoche O, Olowe O, Akinyosoye S, Omodele T (2014) Genetic diversity of Parkia biglobosa from different agroecological zones of Nigeria using RAPD Markers. Int J Biodiv 2014:1–6
Aukema JE, Martinez del Rio C (2002) Mistletoes as parasites and seed-dispersing birds as disease vectors: Current understanding, challenges, and opportunities. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution, and conservation. Wallingford, UK, CABI International, pp 99–110
Ayuba I (2000) A survey of occurrence, distribution and effects of African mistletoe (Tapinanthus spp.) on Parkia biglobosa (Jacq) and Butryospermum paradoxum (Gaertn. F.) Hepper in Yauri Local Government Area of Kebbi State. Doctoral and M. Sc. Dissertation, Usman Danfodo University Sokoto, Sokoto State, Nigeria.
Balogun WG, Adebayo IA, Yusuf U, Seeni A (2018) A review of the phytochemistry and medicinal activities of the popular African food additive: Parkia biglobosa seed. Oriental Pharm Exp Med 18:271–279
Barea LP (2008) Nest-site selection by the painted honeyeater Grantiella picta), a mistletoe specialist. Emu 108:213–220
Barea LP, Watson DM (2007) Temporal variation in food resources determines onset of breeding in an Australian mistletoe specialist. Emu 107:203–209
Barlow BA (1983) Biogeography of Loranthaceae and Viscaceae. In: Calder M, Bernhardt P (eds) The Biology of Mistletoe. Academic Press, Sydney, pp 19–46
Barlow BA (1987) Mistletoes Biologist 34:261–269
Borrow N, Demey R (2004) Field guide to the birds of Western Africa. London: Christopher Helm. pp 510
Bowen ME, McAlpine CA, House APN, Smith GC (2009) Agricultural landscape modification increases the abundance of an important food resource: mistletoes, birds and brigalow. Biol Conserv 142:122–133
Braimoh B, Iwajomo S, Wilson M, Chaskda A, Ajang A, Cresswell W (2018) Managing human disturbance: factors influencing flight-initiation distance of birds in a West African nature reserve. Ostrich 89:59–69
Brandt MJ, Cresswell W (2008) Breeding behaviour, home range and habitat selection of rock Firefinches Lagonosticta sanguinodorsalis in the wet and dry season in central Nigeria. Ibis 150:495–507
De BÂ, Francisco J, Lo L (2002) Mistletoe infection of trees located at fragmented forest edges in the cloud forests of Central Veracruz, Mexico. Forest Ecol Manage 164:293–302
Calder M (1983) Mistletoes in focus. In: Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sydney, Australia, pp 1–18
Candia AB, Medel R, Fonturbel FE (2014) Indirect positive effects of a parasitic plant on host pollination and seed dispersal. Oikos 123:1371–1376
Caraballo-Ortiz MA, González-Castro A, Yang S, dePamphilis CW, Carlo TA (2017) Dissecting the contributions of dispersal and host properties to the local abundance of a tropical mistletoe. J Ecol 105:1657–1667
Carlo TA, Aukema JE (2005) Female-directed dispersal and facilitation between a tropical mistletoe and a dioecious host. Ecology 86:3245–3251
Chaskda AA (2005) Implications of Avian Foraging on the Reproductive Ecology of the Mistletoe. MSc Dissertation, AP Leventis Ornithological Research Institute, University of Jos, Nigeria
Chaskda AA, Fandip B (2017) Anthropogenic footprints in the Amurum Forest Reserve and the Jos Wildlife Park, Jos Plateau State, Nigeria. J Res Forest Wildl Environ 9:96–104
Chaskda AA, Mwansat GS (2006) Implications of avian foraging on the reproductive ecology of the mistletoe, Tapinanthus globiferus (Loranthaceae). J Ornith 147:147–147
Cooney SJ, Watson DM (2005) Diamond Firetails (Stagonopleura guttata) preferentially nest in mistletoe. Emu 105:317–322
Cooney SJN (2004) Why do birds nest in mistletoe? An experimental investigation. B. Applied Science. PhD thesis, Charles Stuart University, Albury, Australia
Corlett RT (2017) Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: an update. Global Ecol Conserv 11:1–22
Currie HA, Perry CC (2007) Silica in plants: Biological, biochemical and chemical studies. Ann Bot 100:1383–1389
Daru BH, Yessoufou K, Nuttman C, Abalaka J (2015) A preliminary study of bird use of fig ficus species in Amurum Forest Reserve, Nigeria. Malimbus 37:1–15
Dawang N, Abdulhameed A, Ezra G (2015) Phytodiversity of three habitat types in Amurum Forest: an important Bird Area in Jos, Nigeria. Afr J Nat Sci 13:1119–1104
Dean WRJ, Midgley JJ, Stock WD (1994) The distribution of mistletoes in South Africa: patterns of species richness and host choice. J Biogeogr 21:503–510
Dobbertin M, Rigling A (2006) Pine mistletoe (Viscum album ssp. austriacum) contributes to Scots pine (Pinus sylvestris) mortality in the Rhone valley of Switzerland. Forest Path 36:309–322
Edagbo DE, Ajiboye T, Borokin T, Ighere D, Alowonle A, Clement M (2012a) The influence of African mistletoe (Tapinanthus bangwensis) on the conversation status of Citrus sinesis in moor plantation. Int J Curr Agric Sci 4:484–487
Edagbo DE, Ighere DA, Clement M (2012b) The influence of African mistletoe (Tapinanthus bangwensis) on the conservation status and productivity of Irvingia gabonensis in Moor Plantation Area of Ibadan. Greener J Agric Sci 3:743–747
Ezealor AU (2002) Critical Sites for Conservation in Nigeria. Lagos, Nigerian Conservation Foundation, p 110
Fadini RF, Mellado A, Ghizoni LP (2014) A host creates an enemy-free space for mistletoes by reducing seed predation caused by a woodboring beetle: a hypothesis. Biotropica 46:260–263
Fontúrbel FE, Bruford MW, Salazar DA, Cortés-Miranda J, Vega-Retter C (2019) The hidden costs of living in a transformed habitat: ecological and evolutionary consequences in a tripartite mutualistic system with a keystone mistletoe. Sci Total Environ 651:2740–2748
Fontúrbel FE, Lara A, Lobos D, Little C (2018) The cascade impacts of climate change could threaten key ecological interactions. Ecosphere 9:e02485
Fontúrbel FE, Salazar DA, Medel R (2017) Why mistletoes are more aggregated in disturbed forests? The role of differential host mortality. Forest Ecol Manage 394:13–19
Gairola S, Bhatt A, Govender Y, Baijnath H, Procheş Ş, Ramdhani S (2013) Incidence and intensity of tree infestation by the mistletoe Erianthemum dregei (Eckl. and Zeyh.) V. Tieghem in Durban. South Africa Urban Forest Urban Green 12:315–322
Gbadamosi AE (2005) Genetic variation in Enantia chlorantha (oliv). A medicinal plant. J Food Agric Environ 3:153–156
Griebel A, Watson D, Pendall E (2017) Mistletoe, friend and foe: synthesizing ecosystem implications of mistletoe infection. Environ Res Lett 12:115012
Hatcher MJ, Dick JT, Dunn AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Front Ecol Environ 10:186–194
Henríquez-Velásquez C, Henríquez JM, Aravena JC (2012) Damage caused by mistletoe Misodendrum punctulatum Banks Ex Dc. on architecture and radial growth of Nothofagus pumilio (Poepp. et Endl.) Krasser forests of southern Chile. Austral Ecol 37:816–824
Ibrahim MA, Koorbanally NA, Islam MS (2013) In vitro anti-oxidative activities of the various parts of Parkia biglobosa and GC-MS analysis of extracts with high activity. Afr J Tradit Complement Altern Med 10:283–291
Ibrahim MI (2002) Renewable Natural Resources (Rnr) Draft Action Plans for Laminga Community Forest (Amurum). Nigeria Conservation Foundation, pp 2–5
Ijarotimi OS, Keshinro OO (2012) Protein quality, haematological properties and nutritional status of albino rats fed complementary foods with fermented popcorn, African locust bean, and Bambara groundnut flour blends. Nutr Res Prac 6:381–388
Jordano P (2000) Seeds: the ecology of regeneration in plant communities. In: Ferner M (ed) Fruits and frugivory. CABI Publishing, Wallingford, pp 125–166
Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecol Lett 6:69–81
Kerckhove V (2011) Frugivores and seed dispersal (1985–2010); the ‘seeds’ dispersed, established and matured. Acta Oecol 37:517–520
Kitamura S (2011) Frugivory and seed dispersal by hornbills (Bucerotidae) in tropical forests. Acta Oecol 37:531–541
Knutson DM (1979) How parasitic seed plants induce disease in other plants. In: Horsfall JG, Cowling EB (eds) Plant disease, an advanced treatise. Academic Press, San Diego, pp 293–312
Koenig WD, Knops JM, Carmen WJ, Pesendorfer MB, Dickinson JL (2018) Effects of mistletoe (Phoradendron villosum) on California oaks. Biol Lett 14:20180240
Kolb TE, Fettig CJ, Ayres MP, Bentz BJ, Hicke JA, Mathiasen R, Stewart JE, Weed AS (2016) Observed and anticipated impacts of drought on forest insects and diseases in the United States. For Ecol Manage 380:321–334
Kossom ZY (2015) Prevalence and distribution of mistletoe on host plant species in Amurum Forest Reserve. MSc Dissertation, AP Leventis Ornithological Research Institute, Department of Zoology, University of Jos, Nigeria
Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley
Kwon-Ndung EH, Ismaila A (2009) Prospects of host resistance in improved and domesticated species of Parkia biglobosa to African mistletoes (Tapinanthus spp.) in Central Nigeria. J Environ Agric Food Chem 8:382–388
Lara C, Pérez G, Ornelas JF (2009) Provenance, guts, and fate: field and experimental evidence in a host-mistletoe-bird system. Ecoscience 16:399–407
López de Buen LL, Ornelas JF (2002) Host compatibility of the cloud forest mistletoe Psittacanthus schiedeanus (Loranthaceae) in Central Veracruz, Mexico. Am J Bot 89:95–102
Mathiasen RL, Hawksworth FG, Edminster CB (1990) Effects of dwarf mistletoe on growth and mortality of douglas-fir in the Southwest Great Basin. Naturalist 50:173–179
Mathiasen RL, Nickrent DL, Shaw DC, Watson DM (2008) Mistletoes: Pathology, systematics, ecology, and management. Plant Dis 92:988–1006
Mellado A, Hobby A, Lázaro-González A, Watson DM (2019) Hemiparasites drive heterogeneity in litter arthropods: Implications for woodland insectivorous birds. Aust Ecol 44:777–785
Mellado A, Zamora R (2016) Spatial heterogeneity of a parasitic plant drives the seed-dispersal pattern of a zoochorous plant community in a generalist dispersal system. Func Ecol 30:459–467
Mutlu S, Ilhan V, Turkoglu HI (2016) Mistletoe (Viscum album) infestation in the Scots pine stimulates drought-dependent oxidative damage in summer. Tree Physiol 36:479–489
Napier KR, Mather SH, McWhorter TJ, Fleming PA (2014) Do bird species richness and community structure vary with mistletoe flowering and fruiting in Western Australia? Emu 114:13–22
Ndagurwa HG, Nyawo E, Muvengwi J (2016) Use of mistletoes by the grey go-away-bird (Corythaixoides concolor, Musophagidae) in a semi-arid savannah, south-west Zimbabwe. Afr J Ecol 54:336–341
Norton DA, Ladley JJ, Sparrow AD (2002) Host provenance effects on germination and establishment of two New Zealand mistletoes (Loranthaceae). Func Ecol 16:657–663
Okubamichael DY, Griffiths ME, Ward D (2011) Host specificity, nutrient and water dynamics of the mistletoe Viscum rotundifolium and its potential host species in the Kalahari of South Africa. J Arid Environ 75:898–902
Olesen JM, Jordano P (2002) Geographic patterns in plant/pollinator mutualistic networks. Ecology 83:2416–2424
Ornelas JF, Licona-Vera Y, Ortiz-Rodriguez AE (2018) Contrasting responses of generalized/specialized mistletoe-host interactions under climate change. Ecoscience 25:223–234
Overfield D, Riches C, Samoah AM, Sarkodie O, Baah F (1998) A farming system analysis of the mistletoe problem in Ghanian Cocoa. Cocoa Grower’s Bulletin 51:42–50
Parkouda C, Nielsen DS, Azokpota P, Ouoba IL, Amoa-Awua WK, Thorsen L, Jakobsen M (2009) The microbiology of alkaline-fermentation of indigenous seeds used as food condiments in Africa and Asia. Crit Rev Microbiol 35:139–156
Pennings SC, Callaway RM (2002) Parasitic plants: parallels and contrasts with herbivores. Oecologia (Berl) 131:479–489
Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751
Quantum GIS Development Team (2016) QGIS geographic information system. Open Source Geospatial Foundation, Beaverton
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rawsthorne J, Watson DM, Roshier DA (2012) The restricted seed rain of a mistletoe specialist. J Avian Biol 43:9–14
Roxburgh L, Nicolson SW (2005) Patterns of host use in two African mistletoes: The importance of mistletoe-host compatibility and avian disperser behaviour. Func Ecol 19:865–873
Sangüesa-Barreda G, Linares JC, Camarero JJ (2012) Mistletoe effects on Scots pine decline following drought events: insights from within-tree spatial patterns, growth and carbohydrates. Tree Physiol 32:585–598
Sayad E, Boshkar E, Gholami S (2017) Different role of host and habitat features in determining spatial distribution of mistletoe infection. For Ecol Manage 384:323–330
Shaw DC, Watson DM, Mathiasen RL (2004) Comparison of dwarf mistletoes (Arceuthobium spp., Viscaceae) in the western United States with mistletoes (Amyema spp., Loranthaceae) in Australia—ecological analogs and reciprocal models for ecosystem management. Austr J Bot 52:481–498
Tella JL, Hiraldo F, Pacífico E, Díaz-Luque JA, Dénes FV, Fontoura FM, Blanco G (2020) Conserving the diversity of ecological interactions: the role of two threatened macaw species as legitimate dispersers of “megafaunal” fruits. Diversity 12:45
Tennakoon KU, Pate JS, Stewart GR (1997) Haustorium related uptake and metabolism of host xylem solutes by the root hemiparasitic shrub Santalum acuminatum (R. Br.) A. DC. (Santalaceae). Ann Bot (Lond) 80:257–264
Těšitel J (2016) Functional biology of parasitic plants: a review. Plant Ecol Evol 149:5–20
Tiffney BH (2004) Vertebrate dispersal of seed plants through time. Ann Rev Ecol Evol Sys 35:1–29
Udobi CE, Onaolapo JA, Agunu A (2010) Antibacterial potentials of the methanolic extract and aqueous fraction of the stem bark of the African locust bean (Parkia biglobosa). Euro J Sci Res 43:590–597
Van Ommeren RJ, Whitham TG (2002) Changes in interactions between juniper and mistletoe mediated by shared avian frugivores: Parasitism to potential mutualism. Oecologia 130:281–288
Wala ZJ (2009) Effect of weather and nectar concentration on the foraging behaviour of four sunbird (Nectariniidae) species in the Amurum Forest Reserve. MSc thesis, University of Jos, Nigeria
Watson DM (2001) Mistletoe-a keystone resources in forests and woodlands worldwide. Ann Rev Ecol Syst 32:219–249
Watson DM (2002) Effects of mistletoe on diversity: a case-study from southern New South Wales. Emu 102:275–281
Watson DM (2004) Mistletoes: a unique constituent of canopies worldwide. In: Lowman MD, Rinker HB (eds) Forest canopies, 2nd edn. Academic Press, San Diego, pp 212–223
Watson DM (2009) Parasitic plants as facilitators: more dryad than Dracula? J Ecol 97:1151–1159
Watson DM (2015) Disproportionate declines in ground-foraging insectivorous birds after mistletoe removal. PLoS ONE 10:e0142992
Watson DM (2016) Fleshing out facilitation—reframing interaction networks beyond top-down versus bottom-up. New Phytol 211:803–808
Watson DM, Herring M (2012) Mistletoe as a keystone resource: an experimental test. Proc Royal Soc B 279:3853–3860
Watson DM, Milner KV, Leigh A (2017) Novel application of species richness estimators to predict the host range of parasites. Int J Parasit 47:31–39
Watson DM, Rawsthorne J (2013) Mistletoe specialist frugivores: latterday ‘Johnny Appleseeds’ or self-serving market gardeners? Oecologia 172:925–932
Way DA (2011) Parasitic plants and forests: a climate change perspective. Tree Physiol 31:1–2
Wenny DG, Sekercioglu C, Cordeiro NJ, Rogers HS, Kelly D (2016) Seed dispersal by fruit-eating birds. In: Sekercioglu CH, Wenny DG, Whelan CJ (eds) Why birds matter: Avian ecological function and ecosystem services. University of Chicago Press, Chicago, pp 107–145
Weston KA, Chapman HM, Kelly D, Moltchanova EV (2012) Dependence on sunbird pollination for fruit set in three West African montane mistletoe species. J Trop Ecol 28:205–213
Yessoufou K, van der Bank M, Abalaka J, Daru BH (2012) Fig-frugivore interactions follow a constrained Brownian motion model of evolution in an Important Bird Area, West Africa. Isr J Ecol Evol 58:39–51
Yule KM, Bronstein JL (2018) Reproductive ecology of a parasitic plant differs by host species: vector interactions and the maintenance of host races. Oecologia 186:471–482
Zuria I, Castellanos I, Gates JE (2014) The influence of mistletoes on birds in an agricultural landscape of central Mexico. Acta Oecol 61:51–56
Acknowledgements
We are grateful to the A.P. Leventis Ornithological Research Institute, Jos (NI), for study permission, sponsorship, and overall support. Thanks to Arin Izang for assistance with fieldwork. CTD thanks the National Research Foundation (ZA, Grant 98404) and the University of KwaZulu-Natal (ZA) for support. We thank the reviewers for their constructive comments that improved the manuscript.
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Raji, I.A., Chaskda, A.A., Manu, S.A. et al. Bird species use of Tapinanthus dodoneifolius mistletoes parasitising African locust bean trees Parkia biglobosa in Amurum Forest Reserve, Nigeria. J Ornithol 162, 1129–1140 (2021). https://doi.org/10.1007/s10336-021-01890-0
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DOI: https://doi.org/10.1007/s10336-021-01890-0