Pacific Science (1990), vol. 44, no. I: 88-93 © 1990 by University of Hawaii Press. All rights reserved

Use of the Exotic faya by Native and Exotic Birds in Hawai'i Volcanoes National Park 1

SUE A. WOODWARD,2 PETER M. VITOUSEK,2 KATHLEEN MATSON,2 FLINT HUGHES,2 KECIA BENVENUTO, 2 AND PAMELA A. MATSON 3

ABSTRACT: The exotic nitrogen-fixing tree Myrica faya is invading Hawai'i Volcanoes National Park (HA Va). Observations of avian use ofM.faya demon­ strated that although four species ofnative birds visited the , they rarely fed on the . Seven species ofexotic birds were seen visiting M.faya, and five of these were observed ingesting the . The most frequent visitor and consumer was the Japanese White-eye (Zosterops japonicus). Over one-third of the cap­ tured Z. japonicus produced fecal samples containing M. faya seeds, and those seeds were as viable as those picked from M. faya trees and beneath their canopies.

THE SYMBIOTIC nitrogen-fixing tree Myrica canopy of other trees and (Smathers fa ya Ait. () was introduced to and Gardner 1979). This pattern of establish­ Hawai'i from the or Azores ment reflects M.faya seed rain; from 2.5 to 4.8 late in the nineteenth century. Colonization of seeds per month have been captured in seed M.faya is favored by human disturbance, as is traps (1 m") under the native tree Metrosideros true of most exotic species in Hawai'i and polymorpha, while none was captured in the elsewhere (Allan 1936, Egler 1942, Orians open (Vitousek and Walker 1989). This pat­ 1986, Crawley 1987). However, M.faya also tern of seed rain is characteristic of in colonizes and dominates otherwise undis­ which seeds are dispersed by perching birds turbed primary successional sites and seasonal (Glyphis et al. 1981, McDonnell and Stiles submontane forests in Hawai'i Volcanoes Na­ 1983, McDonnell 1986). tional Park (HAVa) (Whiteaker and Gardner The fruit of M. faya is a fleshy drupe 1985). Within HAvo, M . faya is invading (Gardner 1985) believed to be bird-dispersed strongly nitrogen-deficient sites that previ­ in its native habitat. Smathers and Gardner ously lacked a symbiotic nitrogen-fixing . (1979) speculated that the exotic Japanese Colonization by M.faya significantly increases White-eye (Zost erops japonicus) is the major ecosystem-level inputs and biological avail­ agent of dispersal in HAva because of its ability of nitrogen (Vitousek et al. 1987, abundance and its broad diet, which includes Vitousek and Walker 1989); it therefore fruit, foliageinsects, and M .polymorphanectar. represents a more serious threat to native However, LaRosa et al. (1985) combined ex­ biota and natural successional patterns than periments on caged birds with 86 hr of obser­ invasions that do not alter ecosystem-level vation on avian use ofM.faya and concluded properties. that although Z.japonicus is a frequent visitor In HAVO , M.faya establishes primarily in to M .faya, it rarely consumes the fruit. They open-canopied areas in microsites under the suggested that the exotic House Finch (Car­ podacus mexicanus) and the native 'Oma'o (Myadestes obscurus)-are-more-important agents ofM.faya dispersal in HAva. 1 Manu script accepted I May 1989. We observed avian visits to M. faya, seed 2 Department of Biological Sciences, Stanford Univer­ sity, Stanford, California 94305. consumption, and presence and germination 3 Ecosystem Science and Technology Branch, NASA­ potential of seeds in the feces ofcaptured birds Ames Research Center, Moffett Field, California 94035. across a range of sites colonized by M. faya. 88 Use of Myricafaya by Native and Exotic Birds-WooDWARD ET AL. 89

\~aO ( .5 'v " Kilauea HAW~" Caldera VOLCANOES! NATIONAY · PARK .j

HP

\t20.00'

~~~I~O==Ec:"S.p,.---",!",;; NATIONAL PARK KilaueaCaldera-l-l_.-' ~••oo 155"00' _-"'-__

FIGURE 1. Location s of the study sites in Hawai'i Volcanoes National Park .

Our goals were to determine the relative im­ (19°20' N, 155°15' W) in HAVO (Figure 1). portance of frugivory by native versus exotic Two ofthese (VB and LB) were in areas with birds in the six sites, and to determine their an intermittent overstory of M. polymorpha relative effectiveness in dispersing seeds ofM. that had survived 1-2 m of cinderfall from a faya in two of those sites. 1959 eruption ofKilauea Iki Crater (Smathers and Mueller-Dombois 1974). The LB site has a large population ofM.faya (now ca. 1100 in­ dividuals per ha), butMJaya colonization is MATERIALS AND METHODS much less advanced in the VB site (ca. 100 in­ Study Sites dividuals per ha). Two sites (HP and AH) were set up in seasonal submontane forest south Six sites were selected in and near the sum­ of the upper east rift of Kilauea (Mueller­ mit area and upper east rift ofKilauea Volcano Dombois et al. 1981), which is characterized 90 PACIFIC SCIENCE,Volume 44,January 1990 by a sparse overstory of M . polymorpha with greenhouse along with control groups of M. an understory of M. faya and exotic grasses. faya seeds collected from trees. Another site (TH) was selected in closed­ canopy montane rainforest that dates from an explosiveeruption of Kilauea in 1790. A sparse RESULTS AND DISCUSSION M. faya population (40 individuals per ha) persists in the understory ofthis site; they can Visitation Rates reach the canopy following treefall or stand­ levelcanopy dieback (Mueller-Dombois 1987). Avian activity in M. faya was observed for Finally, the sixth site (GC) was established in a total of 986.5 tree-hours (504.5 total hours) a residential subdivision near HAYO; M.faya in the six sites. A total of 1965 visits by 11 is now the dominant tree in vacant house lots species of birds (4 native , 7 exotic) was re­ that were bulldozed and then abandoned. corded. The largest number ofvisits per hour occurred in the morning, while the lowest visi­ tation rate was at midday. No variation in visits as a function of weather was observed. Methods There was significant variation in visits per Observations of bird use of M. faya were tree-hour depending on sex of the M. faya conducted from July to December 1987, a pe­ observed; pistillate and bisexual trees were riod spanning M . faya's peak fruiting season preferred over staminate trees by a factor of 2 (Whiteaker and Gardner 1987). Each obser­ ca. 2: 1 (P < .001, X ). Ofthe total visits to M . vation lasted for! hr and included one to faya, 80% were by Zijaponicus, which was the four M .faya trees. The location, sex, fruiting most important visitor in each site (Table 1). phenology, and growth form ofeach tree were The two other exotic species seen frequently recorded. Observers chose a concealed loca­ were C. mexicanus (House Finch) and Cardi­ tion (6 to 20 m away) from which to observe; nalis cardinalis (Northern Cardinal). Both every tree watched during a !-hr observation were observed most often at the GC site, the period was counted as ! tree-hour. Observa­ most disturbed of the study areas. The most tions were conducted in all weather conditions frequent native bird was Himatione sanguinea and throughout the day. ('Apapane). Though restricted principally to We recorded the species of each bird visit­ the VB, LB, and TH sites, H . sanguinea had ing a tree, the duration it stayed , and its activi­ an overall visitation rate second only to that ties while in the tree. From September to Dec­ of Z. japonicus. In the TH site, the native M. ember, we also recorded the number of fruits obscurus ('Oma'o) was also seen frequently. observed to be removed from the tree. How­ ever, because birds were often hidden by fo­ Seed Ingestion liage within the tree, this number is an under­ estimate of all seeds taken. Consumption of M.faya seeds was limited Between 10 October and 24 November, almost entirely to exotic birds . One native mist-nets were maintained in the VB and LB species (M. obscurus) was observed ingest­ sites to obtain fecal samples from birds. The ing two seeds throughout the 6-month study, mist-nets were 6 to 12 m long and 2.5 m high; and none of the other natives now present in the mesh size was 38 mm. Nets were situated the sites (with the possible exception of either against a row of M . faya and M . poly­ Hemignathus virens) would be expected to morpha trees or within a corridor between consume fruit. Z. japonicus was the most fre- trees-Mist-netting was carried outfor a total . quent consumer ofM.jayaseeds and was seen of2l2.5 net-hours in VB and 146.4 net-hours ingesting fruit at all sites (Table 2). Z.japonicus in LB. Captured birds were held in a muslin was also observed carrying the intact fruit in bag for 30 min to obtain a fecal sample . Seeds its bill, and on one occasion an individual was found in the fecal samples were planted in a seen bringing fruit to a nest. Use ofMyricafaya by Native and Exotic Birds-WOODWARD ET AL. 91

TABLE I AVIAN VISITS TOM .faya (IN NUMBER OFVISITS PER TREE-HOUROFOBSERVATION)

DB LB HP AH TH GC

Total number of tree-hours 126 276 173 133.5 76 202 Exotic birds Zo sterops japonicus 1.79 1.89 1.45 2.16 0.66 1.66 Carpodacus mexicanus 0 0.01 0.01 0.01 0 0.28 Cardinalis cardinalis 0.03 0.02 0 0.01 0 0.15 Lophura leucomelana 0.05 0.05 0 0 0 0 A cridotheres tristis 0 0 0 0 0 0.03 Garrulax canorus 0.01 0.01 0 0 0 0 Lonchura pun ctulata 0 0 0 0 0 0.02 Exotic bird total 1.88 1.98 1.46 2.18 0.66 2.14 Native birds Himatione sanguinea 0.14 0.21 0 0.02 0.17 0 Chasiempos sandwichensis 0 0.02 0 0 0 0 Hemignathus virens 0.02 0 0.02 0.04 0 0 Myadestes obscurus 0.01 0 0.01 0 0.12 0 Native bird total 0.17 0.23 0.03 0.06 0.39 0 Combined total 2.05 2.21 1.49 2.24 1.05 2.14

TABLE 2 AVIAN CONSUMPTION OFM .faya (IN NUMBEROF FRUITS INGESTED PERTREE-HOUR OFOBSERVATION)

DB LB HP AH TH GC

Total number of tree-hours 126 276 173 133.5 76 202 Exotic birds Zosterops japonicus 0.16 0.09 0.05 0.05 0.21 0.09 Carpodacus mexicanus 0 0 0 0 0 2.7 Cardinalis cardinalis 0 0 0 0 0 0.10 Acridotheres tristis 0 0 0 0 0 0.01 Native birds Myadestes obscurus 0.01 0 0 0 0.03 0

Feeding by exotics other than Z. japonicus were observed ingesting seeds from M.faya in was noted during regular observations only at both the DB and LB sites. the GC site, where C. mexicanus was observed to consume large numbers of fruit on two Mist-netting Results occasions. Though we could not determine whether the finches were crushing the seeds or Fifty-six birds of five species, only one of swallowing them intact, ingestion by C. mexi- which was native, were captured with mist-nets canus could be substantial. In 202 hr ofobser- in the DB and LB sites (Table 3). Eighty-four vation at this human-disturbed site, 546 seeds percent ofthe birds caught were Z.japonicus; were taken by C. mexicanus, while only 42 this species accounted for 86% of the visita­ were ingested by.Z s-japonious. G.- cardinalis --t ion in these sites. OnlyZ-japonicuspassed-M. and Acridotheres tristis (Common Myna) were faya seeds or fruit. Of the 47 Z. japonicus also observed ingesting a few M.faya fruits at netted, 17 (36%) passed one to six M. faya this site. Outside our regular observation peri- seeds, and an additional 5 (11%) yielded M . ods, Kalij Pheasants (Lophura leucomelana) faya fruit pulp only. 92 PACIFIC SCIENCE, Volume44, January 1990

TABLE 3

BIRDS CAPTURED BY MIST-NETTING IN THE VB AND LB SITES (COMBINED)

SPECIES NO. CAPTU RED % WI TH M .faya IN FECES

Zoslerops jap onicus 47 47 Himatione sanguinea 4 o Cardinalis cardinalis I o Carpodacus mexicanus 2 o Leiothrix lutea 2 o

Sixty seeds collected from Z.japonicus feces LITERATURE CITED were planted to ascertain germination poten­ tial, along with 72 control seeds picked from ALLAN, H. H. 1936. Indigene versus alien in and under M.faya trees . After 10 months, 21 the New Zealand plant world. Ecology 17: 187-193. Z. japonicus-passed seeds and 27 of the con­ trol seeds had germinated. This difference was CRAWLEY, M. J. 1987. What makes a com­ 2 munity invasible? Pages 429-453 in A. J. not significant (P > .05, X ) . Gray, M. J. Crawley, and P. J. Edwards, eds. Colonization, succession and stability. Blackwell Scientific Publications, Oxford. CONCLUSIONS EGLER, F. E. 1942. Indigene versus alien in the development of arid Hawaiian vegetation. Our results indicate that Z. japonicus is the Ecology 23 : 14-23. primary dispersal agent for the seeds of M. GARDNER, D. E. 1985. Observations on some faya in natural areas ofHAva.It is the most unusual flowering characteristics ofMyrica frequent visitor, and Z. japonicus collected in faya. Newsl. Hawaii. Bot. Soc. 24: 14-17. the field passed viable M . faya seeds. Other GLYPHIS, J. P., S. J. MILTON, and W. R. exotic birds (particularly C. mexicanus) may SIEGFRIED. 1981. Dispersal ofAcacia cyclops be important in more modified habitats. These by birds. Oecologia (Berlin) 48: 138-141. results contrast with LaRosa et al.'s (1985) LARoSA, A. M., C. W. SMITH, and D . E. conclusion that "white-eyes [2. japonicus] GARDNER. 1985. Role of alien and native rarely ingest the seeds," but support Smathers birds in the dissemination of fire tree (My­ and Gardner's (1979) suggestion of a corre­ rica faya Ait.-Myricaceae) and associated lation between the foraging patterns of Z. plants in Hawaii. Pac . Sci. 39: 372-378. japonicus and the M. faya invasion. McDoNNELL, M . J. 1986. Old field vegetation height and the dispersal pattern ofbird dis­ seminated woody plants. Bull. Torrey Bot. ACKNOWLEDGMENTS Club II3: 6-11. McDoNNELL, M. J., and E. W. STILES. 1983. We thank the Research Experience for The structural complexity ofold field vege- Undergraduates Program for a supplement to tation and the recruitment ofbird-dispersed NSF Grant 84-15821. In addition, the follow- plant species. Oecologia (Berlin) 56: 109- ing people shared advice , equipment, and sup- 116. port: Nancy Howard, Sheila Conant, James MUELLER-DoMBOIS, D . 1987. Forestdynamics Jaco bivJackJeffrey, Jeff-Kelly,-AnneMarie -- --in-Hawaii -T rends-Ecol.Evoi.-2-: 216~220. LaRosa, Eric Macklin, Sandra Pletschet, MUELLER-DoMBOIS, D ., K. W. BRIDGES, and Maile Stemmerman, Clifford Smith, Charles H. L. CARSON, eds. 1981. Island ecosys- Stone, Charles van Riper, and the Research tems: Biological organization in selected and Resources Management Departments of Hawaiian communities. Hutchinson Ross, Hawai'i Volcanoes National Park. Stroudsburg, Pennsylvania. Use of Myrica faya by Native and Exotic Birds-WooDWARD ET AL. 93

ORIANS, G. H. 1986. Site characteristics favor­ VITOUSEK, P. M., L. R. WALKER, D. MUELLER­ ing invasions. Pages 133-148 in H. A. DOMBOIS, and P. A. MATSON. 1987. Biologi­ Mooney and J. Drake, eds. Ecology ofbio­ cal invasion by Myricafaya alters ecosystem logical invasions of North America and development in Hawaii. Science 238: 802­ Hawaii. Springer-Verlag, New York. 804. SMATHERS, G. A., and D. E. GARDNER. 1979. WHITEAKER, L. D. , and D . E. GARDNER. 1985. Stand analysis of an invading firetree The distribution of Myricafaya Ait. in the (Myrica faya Aiton) population, Hawaii. state of Hawaii. Technical Report no. 55. Pac. Sci. 33 :239-255. Cooperative National Park Resources SMATHERS, G . A., and D. MUELLER-DoMBOIS. Study Unit, University ofHawaii at Manoa, 1974. Invasion and recovery of vegetation National Park Service. after a volcanic eruption in Hawaii. Nat. --- . 1987. The phenology and stand struc­ Park Servo Sci. Monogr. no . 5. ture ofMyricafaya Ait. in Hawaii. Techni­ VITOUSEK, P. M., and L. R. WALKER. 1989. cal Report no. 62. Cooperative National Biological invasion by Myricafaya in Ha­ Park Resources Study Unit, University of waii: Plant demography, nitrogen fixation, Hawaii at Manoa, National Park Service. and ecosystem effects. Ecol. Mongr. 59: 247-265.