Biodiversity and Conservation 8: 1707–1715, 1999. © 1999 Kluwer Academic Publishers. Printed in the Netherlands.
The Pacific Banyan in the Cook Islands: have its pollination and seed dispersal mutualisms been disrupted, and does it matter? S.G. COMPTON1,∗ and G. McCORMACK2 1 Ecology and Evolution Group, School of Biology, University of Leeds, Leeds LS2 9JT, UK; 2 Cook Islands Natural Heritage Project, P.O. Box 781, Rarotonga, Cook Islands; ∗ Author for
correspondence (fax: +44-113-2332835; e-mail:
[email protected].) Received 27 November 1998; accepted in revised form 30 April 1999
Abstract. Fig trees (Ficus spp., Moraceae) are pollinated by species-specific fig wasps and have seeds that are mainly dispersed by fruit bats and birds. Consequently, they should be strongly dependent on mutualisms with animals for their reproductive success. As elsewhere in the Pacific, extinctions of potential seed dispersers have occurred on the islands in the southern Cook Islands archipelago. The abundance of the Pacific Banyan, Ficus prolixa, was found to be unrelated to the extent of potential seed disperser extinctions on different islands. There was no evidence of recruitment on Rarotonga, which has the most diverse bird and bat assemblage, and healthy populations on Mangaia, where all the native avian frugivores are extinct. Despite its very small population sizes on some of the islands, the tree’s pollinators are still present, showing that this mutualism has not yet been disrupted. Habitat loss, rather than a loss of mutualists, appears to be the main problem facing this species. Key words: Ficus, mutualism, Pacific islands, pollination, seed dispersal
Introduction The linkage between biological diversity and ecosystem functioning is a question of major concern for both ecologists and conservation biologists. Species are increasingly being lost from ecological communities as a result of human activities, usually with undocumented consequences for the population dynamics of the remaining species. The deletion of species from communities is expected to be most significant when those communities are already species-poor, with little ecological redundancy and consequently a high proportion of keystone species (Cushman 1995). Experimental studies support this conclusion, with greater deterioration in ecosystem processes as diversity declines from moderate (less than ten species) to very low values, contrasting with relatively little impact of species depletion when initial species richness was higher (McGrady-Steed et al. 1997). The tropical forests found on Pacific islands are naturally depauperate in species relative to those of Asia or Australasia, due to their isolation and smaller size. This already low biodiversity has been reduced further by the activities of man, a
1708 process dating back a millenium or more, when Polynesian migrants first colonised the islands. Avian diversity, in particular, has declined dramatically on many islands, leaving only remnants of the original faunas. The broader ecological consequences of these losses can generally only be speculated upon, but in some cases it is possible to identify extant species which are likely to have been affected by the disappearance of species on which they are likely to have depended. Plants which rely on vertebrates for seed dispersal are perhaps the largest group of such species. Many plants in tropical forests produce fleshy fruits that are attractive to vertebrate seed dispersers. Specificity between these plants and their dispersers is usually low, with each plant species dispersed by a number of different vertebrates, each of which feed on fruits produced by a range of plant species. The reduced species richness on isolated islands nonetheless means that plant–disperser relationships are necessarily less diffuse than elsewhere. This is particularly so from the plants’ perspective, where anthropogenic extinctions may have dramatically reduced the diversity of potential dispersal agents. Fig trees (Ficus spp., Moraceae) are a diverse group of largely bird and bat dispersed shrubs and trees. Because they are often abundant and fruit throughout the year, they are considered to be keystone resources for frugivorous vertebrates in many tropical forests (Thornton et al. 1996). In contrast to the generally diffuse relationship between fig trees and their seed dispersers, fig trees have a highly specific relationship with their pollinators, with each species of fig tree generally pollinated by a single species of fig wasp (Hymenoptera: Agaonidae). Fig trees on islands can therefore only reproduce if the islands are also colonised by their particular species of fig wasp. Fig wasps have exceptional dispersal abilities (Thornton et al. 1996), but maintenance of local fig wasp populations poses more of a problem because extinctions are likely when the number of trees is below a critical population size. The Cook Islands are situated in the South Pacific to the east of Fiji. Their southern group comprise six major islands of volcanic or raised atoll origins (Table 1). Rarotonga, the largest island, comprises a central mountainous area still largely covered by forest and a relatively flat coastal strip where much of the native flora has been removed for agriculture and human settlement. Aitutaki is a smaller island, lacking the steep mountains of Rarotonga. Most of its native forest has been cleared. Mangaia differs geologically from Rarotonga and Aitutaki, with much of its surface formed by raised limestone (makatea). The Cook Islands have a native flora of about 180 species (G. McCormack, unpublished), many of which produce fleshy-fruits to facilitate dispersal by fruit-eating birds or bats. Fossil evidence indicates that there was probably a moderate-sized assemblage of such species before the arrival of man, comprising various ground doves, fruit doves, fruit pigeons and lorikeets and the fruit bat Pteropus tonganus, all of which were probably resident on all the islands in the group (Steadman and Kirch 1990; Steadman 1997). The arrival of the Polynesians had quite rapid impacts on these species (Steadman 1997) and only vestiges of this original frugivorous fauna
1709 Table 1. The southern Cook Islands and their frugivorous vertebrate faunas. Rarotonga Mangaia
Aitutaki
Atiu
Mitiaro
Mauke
Size (km2 ) Nearest island (km) Geology
67 204 Volcanic
Max. elevation (m) F. prolixa abundance Obligate frugivores Fruit bat (Pteropus tonganus) Pacific fruit pigeon Cook Islands fruit dove Facultative frugivores Rarotonga starling Indian mynah∗ Blue lorikeet∗ Total obligate frugivores Total potential frugivores
652 Rare
52 204 Volcanic & Limestone 169 Very common
18 102 Mixed atoll & Volcanic 124 Rare
27 50 Volcanic & Limestone 72 Common
22 50 Volcanic & Limestone 15 Uncommon
18 59 Volcanic & Limestone 29 Common
√
√
×
×
×
×
√ √
√
√
×
×
× √
× √
2
√ √
× ×
× ×
√ √
× √
× 3
× 1
× √ √
5
2
0
× 2
× × × 1
2
3
1
× 1
∗ Introduced species.
exist today (Table 1). Fossil evidence inevitably underestimates the true number of extinctions, but Pimm et al. (1995) estimated that around 455 of the bird species of S.E. Polynesia may have been lost. In addition to the native species, alien Indian mynahs have been introduced to the major islands, where they have become the most abundant frugivorous species. The Pacific Banyan or Ava (F. prolixa) is the only species of fig tree which is believed to have certainly reached the Cook Islands without human assistance. The Dye Fig or Mati (F. tinctoria) is also present, but it is known to have been used as a fire tree (Corner 1963), and may have been introduced. F. prolixa is found on all the major southern Cook Islands. These islands possess different-sized remnants of their original seed disperser assemblages, with at one extreme the Mangaian fauna retaining no native frugivorous birds, and an uncommon fruit bat, whereas that of Rarotonga, the largest island, is relatively rich, with the fruit bat, a fruit dove, a fruit pigeon and a starling (Table 1). Dating of bones from a site in Mangaia suggests that extinctions were already taking place at least 1000 years ago (Steadman 1997). How have F. prolixa populations responded to the losses of their seed dispersers, which have occurred to varying extents on the different islands? If disperser richness per se is significant, then islands such as Mangaia would be expected to support few F. prolixa (and other fleshy-fruited trees), while they should be relatively abundant on Rarotonga. Abundance estimates for the flora of the islands have been assembled by the Cook Islands Natural Heritage Project over a period of several years. They
1710 indicate a very different story (Table 1), with F. prolixa particularly common on some of the most disperser-depauperate islands, and uncommon on Rarotonga. This pattern of abundance appears paradoxical if seed dispersal is of major importance to the plants: how can F. prolixa flourish on islands with so few species of dispersers, and why is it doing so badly on some islands which have greater numbers of potential dispersal agents? Seed dispersal by vertebrates is of course only one of the factors influencing the reproductive success of a plant, and this paper examines various (non-mutually exclusive) hypotheses to account for the rarity of F. prolixa on the islands of Rarotonga and Aitutaki and its abundance on Mangaia. These include a breakdown in pollination (pollinator populations may have gone locally extinct as tree numbers declined), spatial displacement between the trees and potential dispersal agents (dispersal agents may be present on an island, but do not occur in the same areas as the trees) and the loss of suitable habitats. Natural history F. prolixa is regarded as a coastal species, and is found throughout most of Polynesia (Corner 1963). On the Cook Islands, F. prolixa is largely restricted to the lowlands as only a single specimen has been recorded from the montane interior of Rarotonga. It can grow as a strangler fig (a hemi-epiphyte that germinates from seeds deposited on other trees), or as a free-standing tree developing from seeds deposited on the ground. In forest situations F. prolixa can reach 20 m or more, with extensive aerial roots, hence its name as the Pacific Banyan. F. prolixa produces small petiolate figs (reaching about 10 mm in diameter) in the leaf axils, which turn red when mature. The form of the figs suggests that birds are the likely seed dispersal vectors of this species (it is a favoured food of the Red-bellied Fruit Dove, Ptilinopus greyii in Vanuatu; Bregulla 1992), although fruit bats will also feed on similar figs produced by other species (Compton and Shilton, unpublished observations). It is monoecious, with individual figs producing both seeds and the fig wasps which disperse its pollen. The pollinator of F. prolixa is recorded as Platyscapa innumerabilis (Wiebes 1994). Methods Studies of the status of fig trees on three islands (Rarotonga, Mangaia and Aitutaki) with contrasting numbers of potential dispersers and F. prolixa abundance were carried out over a two week period in July 1998. Trees on Rarotonga and Aitutaki that had been detected previously by the Cook Islands Heritage Project were examined, together with some additional trees that were located by surveying apparently suitable habitats. The general health and growth form of the fig trees were noted, and if figs
1711 were present their developmental stages and whether they had been pollinated were determined.
Results Totals of nine and four individuals of F. prolixa were examined on Rarotonga and Aitutaki respectively. These represented almost all the known individuals on these islands. In addition, observations were made of numerous free-standing individuals on Mangaia, where the tree is more common, and where individuals of varying ages were present in the makatea. In contrast, general scouting for F. prolixa on Rarotonga and Aitutaki failed to detect any recent recruitment of young individuals. These results agreed with those based on more general surveys carried out by the Cook Islands Heritage Project (Table 1). The trees on Rarotonga and Aitutaki were almost all mature, ‘self-strangling’ individuals with numerous roots descending down the sides of the main trunk. Often these roots had established new trunks, allowing the trees to spread vegetatively. One huge individual had over 20 such inter-connected trunks, with a road running between some of them. The age of these trees made it uncertain whether or not they had started out as stranglers of other trees, or were always free-standing individuals. Only one relatively young F. prolixa was detected, growing as a strangler of Bischofia javonica (Euphorbiaceae). This host tree is common in the ‘slope forest’ which covers the lower sections of the mountainous interior of Rarotonga (McCormack and Kunzle 1995). One F. prolixa was itself being swamped by overgrowing vegetation, caused by an alien vine Entada phaseoloides which is widespread on the island (McCormack and Kunzle 1995). The trees were mainly situated in highly modified suburban or agricultural locations, which are the dominant habitats across Aitutaki and lowland Rarotonga. This is in contrast to the situation on Mangaia, where much of the makatea is relatively undisturbed, and supports a largely native vegetation, including F. prolixa. All the trees with figs at a suitable stage of development had been pollinated (Table 2). Non-pollinating fig wasps (a Sycoscapter species (Hymenoptera: Agaonidae), probably a parasitoid of the pollinator) were found in the figs of only one tree, from Rarotonga. Over half the trees on Rarotonga and Aitutaki had figs on them. This is a high proportion for a monoecious Ficus species, and was a consequence of the vegetative spread of many of the trees, with different sections apparently fruiting independently. The trees also produced relatively small crops for the size of their crowns, which might also be expected to allow them to produce crops more frequently. Two large F. tinctoria on Rarotonga were also examined. They were located near the Avatiu Stream road, south of Avarua. As neither had any figs on them, the status of their pollinator (Liporrhopalum gibbosae) on the island remains unknown.
Rarotonga
Island
Avana Stream road
Ara Tapu
Ara Metua
Ara Metua
Ara Metua
Ara Metua
Matavera Stream road
2
3
4
5
6
7
General location
1
Tree no.
423 1 E 7653 6 N 422 4 E 7653 1 N
423 3 E 7653 2 N 422 3 E 7654 6 N
424 2 E 7650 3 N 424 0 E 7651 7 N
424 0 E 7650 9 N
Coordinates
Mixed agricultural
Suburban
Mixed agricultural
Suburban
Stream-side
Mixed agricultural
Mixed agricultural
Habitat
Tree with some descending roots Young strangler
Multiple trunked tree
Large tree
Large selfstrangling Large tree
Large selfstrangling
Description
Absent
Absent
About 1000 Pre-inter- and postfloral figs
Absent
About 400 Interfloral figs
About 600 Interfloral and aborted figs
