Reductions in bird numbers could hamper ecosystem services such as pollination, but experimental proof is lacking. We show that functional extinction of bird pollinators has reduced pollination, seed production, and plant density in the shrub Rhabdothamnus solandri (Gesneriaceae) on the North Island ("mainland") of New Zealand but not on three nearby island bird sanctuaries where birds remain abundant. Pollen limitation of fruit set is strong [pollen limitation index (PLI) = 0.69] and significant on the mainland but small (PLI = 0.15) and nonsignificant on islands. Seed production per flower on the mainland is reduced 84%. Mainland sites have similar adult densities, but 55% fewer juvenile plants per adult, than island sites. Seed addition experiments near adult R. solandri plants on the mainland found strong seed limitation 5 years after sowing for R. solandri but not for two other co-occurring woody species. This demonstrates a terrestrial trophic cascade.
Summary 1.Many studies have examined the effects of frugivores on the germination of seeds of fleshy fruited plants. However, three key issues are rarely addressed: the need to measure germination of seeds in intact fruits; the effect of germination conditions on results; and the distinction between dead vs dormant seeds. 2. A literature review including 51 plant species from 28 families found that the oftenmeasured scarification effect (germination of bird-defecated vs hand-cleaned seeds) is significantly smaller than the rarely-measured deinhibition effect (germination of handcleaned seeds vs those in intact fruits). 3. Both the literature review and new experimental data show that germination conditions affect germination. In particular, seeds in intact fruits have much lower germination percentages in Petri dishes than in the field. Poor germination from intact fruits in Petri dishes may be an artefact. 4. A field experiment with three New Zealand species showed variable effects of nonremoval of the fruit pericarp. The retention of the pericarp had no effect on germination in Nestegis cunninghamii ; increased the proportion of seeds entering dormancy in Melicytus lanceolatus ; and greatly increased seed mortality in Pennantia corymbosa . 5. Germination experiments must be designed carefully to evaluate accurately the risks for plants of frugivory mutualism failures.
Environmental changes threaten plant-pollinator mutualisms and their critical ecosystem service. Drivers such as land use, invasions and climate change can affect pollinator diversity or species encounter rates. However, nitrogen deposition, climate warming and CO(2) enrichment could interact to disrupt this crucial mutualism by altering plant chemistry in ways that alter floral attractiveness or even nutritional rewards for pollinators. Using a pumpkin model system, we show that these drivers non-additively affect flower morphology, phenology, flower sex ratios and nectar chemistry (sugar and amino acids), thereby altering the attractiveness of nectar to bumble bee pollinators and reducing worker longevity. Alarmingly, bees were attracted to, and consumed more, nectar from a treatment that reduced their survival by 22%. Thus, three of the five major drivers of global environmental change have previously unknown interactive effects on plant-pollinator mutualisms that could not be predicted from studies of individual drivers in isolation.
The endemic mistletoes Peraxilla colensoi and P. tetrapetala (Loranthaceae) have declined considerably in New Zealand since 1840, reputedly because of introduced herbivores but coincident with a major decline in native bird densities. We show that at two South Island sites ( Craigieburn and Ohau) there are too few bird pollinators visiting the flowers to allow full fruit set. We studied pollination rates in P. colensoi at Wakefield and P. tetrapetala at Craigieburn over four flowering seasons and P. tetrapetala in one season at Ohau. Supplemental hand pollination increased fruit production 1.25–5.3 times at Craigieburn and Ohau but not at Wakefield. Excluding birds by covering mistletoes with mesh bags decreased fruit set significantly at Wakefield but had little effect at Craigieburn and Ohau. Bellbirds (Anthornis melanura) and Tuis ( Prosthemadera novaeseelandiae) visited flowers significantly more often at Wakefield than at Craigieburn. A lack of pollen tubes in the style, not self‐incompatibility or resource shortage, caused the low fruit production in unmanipulated flowers at Craigieburn. Thus, at the two P. tetrapetala sites (Craigieburn and Ohau) fruit set was chronically pollen limited, whereas P. colensoi at Wakefield was not pollen‐limited. Data from other Peraxilla sites also suggest pollination failure. Our study suggests that the conservation of Peraxilla species will require maintenance of native bird populations. Tuis and Bellbirds are important pollinators and dispersers of many other New Zealand plants, and the breakdown of such mutualistic relationships may have widespread consequences.
We tested the relative frequency of pollen limitation and dispersal limitation for two birdpollinated and bird-dispersed New Zealand mistletoes, Peraxilla tetrapetala and Alepis flavida, at a South Island site where the bellbird (Anthornis melanura) is the sole pollinator and disperser. There was no evidence of dispersal limitation for P. tetrapetala over four seasons or A. flavida over two seasons. Few ripe fruits were present on plants at any one time (usually <5%), and more than 90% of the fruit crop was removed. A. flavida was not pollen limited, but P. tetrapetala was significantly pollen limited in 6 of 10 years. The presence of pollen limitation but not dispersal limitation, despite both services depending on the same bird, is influenced by the much faster rates of flower ripening per day compared with fruit ripening (15-54 times faster in P. tetrapetala). In New Zealand, pollination failure probably threatens at least as many plant species as dispersal failure. In theory, dispersal should threaten fewer plant species, because dispersal usually involves more animal species, makes smaller quantitative demands on the dispersers (fewer fruits B02086; ripening per day, and fruits can wait longer for attention), and may be less obligate for at least some reproduction to occur.
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