Imperfect Replacement of Native Species by Non‐Native Species as Pollinators of Endemic Hawaiian Plants

Native plant species that have lost their mutualist partners may require non‐native pollinators or seed dispersers to maintain reproduction. When natives are highly specialized, however, it appears doubtful that introduced generalists will partner effectively with them. We used visitation observations and pollination treatments (experimental manipulations of pollen transfer) to examine relationships between the introduced, generalist Japanese White‐eye (Zosterops japonicus) and 3 endemic Hawaiian plant species (Clermontia parviflora, C. montis‐loa, and C. hawaiiensis). These plants are characterized by curved, tubular flowers, apparently adapted for pollination by curve‐billed Hawaiian honeycreepers. Z. japonicus were responsible for over 80% of visits to flowers of the small‐flowered C. parviflora and the midsize‐flowered C. montis‐loa. Z. japonicus‐visited flowers set significantly more seed than did bagged flowers. Z. japonicus also demonstrated the potential to act as an occasional Clermontia seed disperser, although ground‐based frugivory by non‐native mammals likely dominates seed dispersal. The large‐flowered C. hawaiiensis received no visitation by any birds during observations. Unmanipulated and bagged C. hawaiiensis flowers set similar numbers of seeds. Direct examination of Z. japonicus and Clermontia morphologies suggests a mismatch between Z. japonicus bill morphology and C. hawaiiensis flower morphology. In combination, our results suggest that Z. japonicus has established an effective pollination relationship with C. parviflora and C. montis‐loa and that the large flowers of C. hawaiiensis preclude effective visitation by Z. japonicus.

[1]  T. Hoffman Fifty Years of Invasion Ecology: The Legacy of Charles Elton , 2012 .

[2]  E. Zavaleta,et al.  Effects of Native and Non‐Native Vertebrate Mutualists on Plants , 2012, Conservation biology : the journal of the Society for Conservation Biology.

[3]  D. Wilcove,et al.  Invasive rats and recent colonist birds partially compensate for the loss of endemic New Zealand pollinators , 2012, Proceedings of the Royal Society B: Biological Sciences.

[4]  上田 恵介,et al.  小笠原諸島父島におけるメジロ Zosterops japonicus のハイビスカス花への盗蜜行動 , 2011 .

[5]  S. Harris,et al.  Resurrecting Extinct Interactions with Extant Substitutes , 2011, Current Biology.

[6]  R. Julliard,et al.  Worldwide decline of specialist species: toward a global functional homogenization? , 2011 .

[7]  A. Shiels Frugivory by introduced black rats (Rattus rattus) promotes dispersal of invasive plant seeds , 2011, Biological Invasions.

[8]  D. Kelly,et al.  Cascading Effects of Bird Functional Extinction Reduce Pollination and Plant Density , 2011, Science.

[9]  Clare E. Aslan Implications of newly-formed seed-dispersal mutualisms between birds and introduced plants in northern California, USA , 2011, Biological Invasions.

[10]  Judith L Bronstein,et al.  Mutualisms in a changing world: an evolutionary perspective. , 2010, Ecology letters.

[11]  D. Richardson,et al.  Mutualisms: Key Drivers of Invasions … Key Casualties of Invasions , 2010 .

[12]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[13]  A. Traveset,et al.  Conservation and restoration of plant–animal mutualisms on oceanic islands , 2010 .

[14]  R. Cann,et al.  Negative Effects of an Introduced Bird Species on Growth and Survival in a Native Bird Community , 2009, Current Biology.

[15]  C. Atkinson,et al.  Introduced Avian Diseases, Climate Change, and the Future of Hawaiian Honeycreepers , 2009, Journal of avian medicine and surgery.

[16]  James F. Smith,et al.  Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae) , 2009, Proceedings of the Royal Society B: Biological Sciences.

[17]  Fabian M Jaksic,et al.  Ecological efficiency and legitimacy in seed dispersal of an endemic shrub (Lithrea caustica) by the European rabbit (Oryctolagus cuniculus) in central Chile , 2008 .

[18]  Nigel,et al.  Tree recruitment in an empty forest. , 2008, Ecology.

[19]  A. Boyer Extinction patterns in the avifauna of the Hawaiian islands , 2008 .

[20]  J. Foster,et al.  Introduced Birds and the Fate of Hawaiian Rainforests , 2007, Conservation biology : the journal of the Society for Conservation Biology.

[21]  P. Hart,et al.  Distribution and abundance of forest birds in low-altitude habitat on Hawai'i Island: evidence for range expansion of native species , 2006, Bird Conservation International.

[22]  A. Traveset,et al.  Disruption of a Plant‐Lizard Seed Dispersal System and Its Ecological Effects on a Threatened Endemic Plant in the Balearic Islands , 2005 .

[23]  Jonathan P. Price,et al.  SPECIATION IN HAWAIIAN ANGIOSPERM LINEAGES: CAUSE, CONSEQUENCE, AND MODE , 2004, Evolution; international journal of organic evolution.

[24]  K. Gaston,et al.  Avian Extinction and Mammalian Introductions on Oceanic Islands , 2004, Science.

[25]  R. Camp,et al.  Evidence of change in a low-elevation forest bird community of Hawai'i since 1979 , 2003 .

[26]  S. Barrett,et al.  PERSPECTIVE: PURGING THE GENETIC LOAD: A REVIEW OF THE EXPERIMENTAL EVIDENCE , 2002, Evolution; international journal of organic evolution.

[27]  K. McConkey,et al.  Potential disruptions to seed dispersal mutualisms in Tonga, Western Polynesia , 2002 .

[28]  A. Young,et al.  Low outcrossing rates and shift in pollinators in New Zealand pohutukawa (Metrosideros excelsa; Myrtaceae). , 2000, American journal of botany.

[29]  Ian J. Renne,et al.  Seed Dispersal of the Chinese Tallow Tree (Sapium sebiferum (L.) Roxb.) by Birds in Coastal South Carolina , 2000 .

[30]  S. Barrett,et al.  A comparative analysis of pollen limitation in flowering plants , 2000 .

[31]  T. Work,et al.  Survival and Physiologic Response of Common Amakihi and Japanese White-Eyes During Simulated Translocation , 1999 .

[32]  S. Pimm Lessons from a kill , 1996, Biodiversity & Conservation.

[33]  W. L. Wagner,et al.  Biogeographical and Ecological Correlates of Dioecy in the Hawaiian Flora , 1995 .

[34]  Daniel Simberloff,et al.  Patterns of Extinction in the Introduced Hawaiian Avifauna: A Reexamination of the Role of Competition , 1991, The American Naturalist.

[35]  C. E. Freeman,et al.  Ornithophily among the Hawaiian Lobelioideae (Campanulaceae): evidence from floral nectar sugar compositions , 1986 .

[36]  P. Cox Extinction of the Hawaiian avifauna resulted in a change of pollinators for the ieie, Freycinetia arborea. , 1983 .

[37]  F. Carpenter,et al.  Plant‐Pollinator Interactions in Hawaii: Pollination Energetics of Metrosideros Collina (Myrtaceae) , 1976 .

[38]  H. T. Spieth Hawaiian Honeycreeper, Vestiaria coccinea (Forster), Feeding on Lobeliad Flowers, Clermontia arborescens (Mann) Hillebr , 1966, The American Naturalist.

[39]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[40]  A. Shiels,et al.  Large-scale rodent control reduces pre- and post-dispersal seed predation of the endangered Hawaiian lobeliad, Cyanea superba subsp. superba (Campanulaceae) , 2012, Biological Invasions.

[41]  R. Cann,et al.  Incipient extinction of a major population of the Hawaii akepa owing to introduced species. , 2008 .

[42]  C. Daehler,et al.  Documenting floral visitors to rare Hawaiian plants using automated video recordings , 2006 .

[43]  W. L. Wagner,et al.  Hawaiian Vascular Plants at Risk: 1999 , 1999 .

[44]  J. Lord Pollination and seed dispersal in Freycinetia baueriana, a dioecious liane that has lost its bat pollinator , 1991 .

[45]  T. Lammers Systematics of Clermontia (Campanulaceae, Lobelioideae) , 1991 .

[46]  P. Vitousek,et al.  Use of the exotic tree Myrica faya by native and exotic birds in Hawai'i Volcanoes National Park. , 1990 .

[47]  S. Weller,et al.  Japanese White-eye, an Introduced Passerine, Visits the Flowers of Clermontia arborescens, an Endemic Hawaiian Lobelioid , 1987 .

[48]  J. Thomason,et al.  Bite Club : Comparative Bite Force in Big Biting Mammals and the Prediction of Predatory Behaviour in Fossil Taxa Author ( s ) : , 2008 .