Effects of Pollinator Loss on Endemic New Zealand Mistletoes (Loranthaceae)

499

Conservation Biology, Pages 499–508Volume 13, No. 3, June 1999

Effects of Pollinator Loss on Endemic New Zealand Mistletoes (Loranthaceae)

ALASTAIR W. ROBERTSON,*‡ DAVE KELLY,† JENNY J. LADLEY,† ANDASHLEY D. SPARROW†

*Ecology Department, Massey University, Private Bag 11222, Palmerston North, New Zealand†Plant and Microbial Sciences Department, University of Canterbury, Private Bag 4800, Christchurch,New Zealand

Abstract:

The endemic mistletoes

Peraxilla colensoi

and

P. tetrapetala

(Loranthaceae) have declined consider-ably in New Zealand since 1840, reputedly because of introduced herbivores but coincident with a major de-cline in native bird densities. We show that at two South Island sites (Craigieburn and Ohau) there are toofew bird pollinators visiting the flowers to allow full fruit set. We studied pollination rates in

P. colensoi

atWakefield and

P. tetrapetala

at Craigieburn over four flowering seasons and

P. tetrapetala

in one season atOhau. Supplemental hand pollination increased fruit production 1.25–5.3 times at Craigieburn and Ohaubut not at Wakefield. Excluding birds by covering mistletoes with mesh bags decreased fruit set significantlyat 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. Alack of pollen tubes in the style, not self-incompatibility or resource shortage, caused the low fruit productionin unmanipulated flowers at Craigieburn. Thus, at the two

P. tetrapetala

sites (Craigieburn and Ohau) fruitset 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 willrequire maintenance of native bird populations. Tuis and Bellbirds are important pollinators and dispersersof many other New Zealand plants, and the breakdown of such mutualistic relationships may have wide-spread consequences.

Efectos de la Pérdida de Polinizadores en Muérdagos (Loranthaceae) de Nueva Zelandia

Resumen:

Los muérdagos endémicos

Peraxilla colensoi

y

P. tetrapetala

(Loranthaceae) han declinado consid-erablemente en Nueva Zelandia desde 1840, supuestamente debido a la introducción de herbívoros, pero escoincidente con un mayor declive en las densidades de aves nativas. Mostramos que en tres sitios de la Isladel Sur (Wakefield, Craigieburn y Ohau) hay muy pocas aves polinizadoras visitando las flores como parapermitir el establecimiento de frutos. Estudiamos las tasas de polinización en

P. colensoi

en Wakefield y

P.tetrapetala

en Craigiebum a lo largo de cuatro estaciones de floresencia y

P. tetrapetala

en una estación enOhau. La suplantación de polinización manual incrementó la producción de frutos de 1.25 a 5.3 veces enCraigieburg y Ohau, pero no en Wakefield. La exclusión de aves mediante la cobertura de muérdagos conbolsas de malla disminuyó significativamente el establecimiento de frutos en Wakefield. Pero tuvo pocoefecto en Craigiebum y Ohau. Las aves

Anthornis melanura

y

Prosthemadra novaeseelandiae

visitaron floressignificativamente más frecuentemente en Wakefield que en Craigieburn. La carencia de tubos de polen en elestilo, la no autocompatibilidad o reducción de recursos causó la baja producción de frutos en flores no ma-nipuladas en Craigieburn. Por ello, en los dos sitios de

P. tetrapetala

(Craigieburn y Ohau) el establecimientode frutos estuvo crónicamente limitado por polen, mientras que

P. colensoi

no estuvo limitada por polen enWakefield. Datos de otros sitios con especies de

Peraxilla

también sugieren fallas en la polinización. Nuestroestudio sugiere que la conservación de especies de

Peraxilla

requerirá del mantenimiento de las poblaciones

‡

email [email protected] submitted November 24, 1997; revised manuscript accepted October 14, 1998.

500

Pollen Limitation of New Zealand Mistletoes Robertson et al.

Conservation BiologyVolume 13, No. 3, June 1999

de aves nativas.

Anthornis

y

Prosthemadra

son polinizadores importantes y dispersores de muchas otras plan-tas de Nueva Zelanda, el rompimiento de estas relaciones mutualistas puede tener consecuencias de amplia

distribución.

Introduction

The loss of mutualistic interactions is an insidious pro-cess that may go unnoticed but may have major conse-quences for the integrity of ecosystems (Janzen 1974).Few studies have investigated how the breakdown of mu-tualistic pollination relationships might contribute to thedecline of endangered plants (Bond 1994). Low fruit-to-flower ratios may indicate a chronic breakdown of theplant-pollinator relationship which results in pollen limi-tation—a shortage of compatible pollen on stigmas thatconstrains fruit production—and which may threaten thelong-term persistence of that population ( Jennersten1988). Alternatively, plants may produce low fruit cropsif (1) insufficient resources are available for the crop tomature (Willson & Price 1980; Lee & Bazzaz 1982; Quel-ler 1985); (2) plants employ a strategy that maximizessome other component of fitness (e.g., male fitness[Sutherland & Delph 1984]); or (3) plants maintain off-spring quality through the selective abortion of inferiorzygotes (Willson & Burley 1983).

Pollen supplementation experiments can discriminatebetween these alternatives (Bierzychudek 1981). Liberalamounts of compatible pollen are applied by hand to stig-mas, and seed set is compared to control flowers to deter-mine the degree of pollen limitation. Burd (1994) re-viewed 258 such studies and found that 62% showedsome pollen limitation, suggesting that, contrary to theo-retical predictions (Queller 1983; Sutherland & Delph1984), pollen limitation may be common in plants. Unfor-tunately, many studies in Burd’s review had methodologi-cal flaws that could lead to an overestimation of the im-portance of pollen limitation. Pollen supplementationstudies ideally should involve all flowers on a plant; other-wise, the influence of resource limitation may be maskedby the transfer of resources from flowers that receive less(or worse) pollen to the hand-pollinated flowers (Bawa &Webb 1984; Horvitz & Schemske 1988; Zimmerman &Pyke 1988). In addition, pollen supplementation may in-crease fruit set within a season but reduce future repro-ductive output (Chaplin & Walker 1982; Zimmerman &Aide 1989; Ackerman & Montalvo 1990) so that total life-time fitness does not necessarily increase ( Janzen et al.1980). A final consideration is that, unless plants are seed-limited, reducing fruit production may have no effect onpopulation size (Crawley 1990).

We tested the hypothesis that two New Zealand mistle-toes (

Peraxilla colensoi

and

P. tetrapetala

, Loranthaceae)are pollen-limited due to decreased bird visitation.

Perax-

illa colensoi

and

P. tetrapetala

are hemiparasitic, long-lived (50–100 years) mistletoes whose normal host treesare

Nothofagus

species (Fagaceae) (Powell & Norton1994; Norton et al. 1997). Both

Peraxilla

species have de-clined dramatically since 1840 (de Lange et al. 1997) andare now listed as “vulnerable” (Cameron et al. 1995). Thedecline is commonly attributed to habitat destruction andbrowsing by the introduced Australian brushtailed possum(

Trichosurus vulpecula

) (Ogle & Wilson 1985; Norton1991), but we suggest that reproductive failure caused bythe decline in mutualist bird populations (Diamond &Veitch 1981) may also be important (Ladley & Kelly1995

a

, 1995

b

, 1996; Kelly et al. 1996; Ladley et al. 1997).The large, tubular mistletoe flowers (

P. colensoi

petallength 43 mm,

P. tetrapetala

27 mm) contain copious di-lute nectar and are thus well adapted for bird pollination(Ladley et al. 1997). Moreover, buds require external forceto open (Ladley & Kelly 1995

a

), usually from two speciesof honeyeaters (Meliphagidae), Tuis (

Prosthemadera no-vaeseelandiae

), and Bellbirds (

Anthornis melanura

; Lad-ley et al. 1997), and occasionally from bees (Kelly et al.1996). If buds are not opened, the petals eventually ab-scise from the base while remaining fused at the top, pro-ducing a bottom-opened flower (diagram in Ladley & Kelly1995

a

). A national survey of populations of both mistle-toes revealed that many buds are not opened by birds orinsects, as shown by abundant bottom-opened flowers onthe ground below the plants (Ladley & Kelly 1995

b

).To test the pollen-limitation hypothesis, we performed

pollen supplementation studies at three sites over severalyears to determine if pollinator scarcity reduced seed pro-duction. We also estimated how much fruit would be set ifall pollinators were lost by examining self-compatibility andthe rate of autonomous self-pollination in both species.

Study Sites and Methods

We studied

Peraxilla colensoi

at Wakefield (lat 41

8

23

9

S,long 173

8

02

9

E), Nelson province (northern South Is-land), in three isolated, 0.5-ha silver beech (

Nothofagusmenziesii)

stands surrounded by pasture. We studied

P. tetrapetala

at Craigieburn (lat 43

8

09

9

S, long 171

8

43

9

E),Canterbury (central South Island), in continuous, puremountain beech (

Nothofagus solandri

var.

cliffortio-ides)

forest and at Ohau (lat 44

8

14

9

S, long 169

8

49

9

E),Canterbury, in an 8-ha remnant stand of mountainbeech. Mistletoes were common at all three sites.


Robertson et al. Pollen Limitation of New Zealand Mistletoes

501

Self-Compatibility

Self-compatibility has been reported in both

Peraxilla

species (Ladley & Kelly 1995

a

). We tested for self com-patibility in five randomly selected

P. colensoi

plants atWakefield and six

P. tetrapetala

plants at Craigieburn inthe summers of 1992–1993. On each plant, approxi-mately 20 buds were placed inside fine mesh cotton bagsto exclude pollinators. When the buds ripened, the bagswere removed, and the buds were opened by hand andeither randomly self-pollinated or cross-pollinated withpollen from a nearby plant. Fruit set could be assessed vi-sually once the fruits developed, because each flower hasa single ovule that develops into a pseudoberry.

In 1994–1995, we tested 12 Craigieburn

P. tetrapetala

plants with

,

200 flowers for cryptic self-incompatibilityat the whole-flower level (the preferential developmentof outcrossed rather than selfed fruits when resources areconstrained [Bateman 1956; Becerra & Lloyd 1992]). Notall flowers on

P. tetrapetala

can be pollinated becausethe caterpillar

Zelleria maculata

(Yponomeutidae) de-stroys the internal structures of some unripe buds(Patrick & Dugdale 1997). As buds ripened, every flowernot infested with

Zelleria

(about 89% of buds that sea-son) was hand-pollinated either with self-pollen fromthree flowers on the same plant or cross-pollinated witha standard cocktail of pollen from six other donor plants.We conducted 263 self- and 272 cross-pollinations. Werecorded the resulting fruit set and harvested the ripefruits. These whole-plant hand-pollinations also testedwhether enhanced fruit set with hand-pollination wasdue to redirection of resources within a plant or tohigher total-plant fruit set.

To determine whether selfed seeds suffered from in-breeding depression, we compared the performance ofthe selfed and outcrossed fruits in germination and seed-ling survival tests. In April 1995, we removed the pericarpsfrom 34 self and 38 outcross fruits, placed them on dampfilter paper in petri dishes, and recorded the rates of germi-nation. In addition, we planted 68 self and 55 outcrossseeds on branches on three mountain beech trees on theCanterbury University campus in July 1995. Germinationand survival were monitored monthly until April 1997.

Pollination Experiments

To determine whether pollen limited fruit set in thesespecies, we performed additional experiments at Wake-field (

P. colensoi

) and Craigieburn (

P. tetrapetala

). Onthe same plants receiving hand-pollinations, additionalbuds were chosen in 1992–1993, 1995–1996, and 1996–1997 and either placed in mesh bags to exclude all polli-nators or left as controls to establish natural rates of pol-lination. Fruit set was monitored as above. The sameprocedure was used in 1994–1995, except that thehand-pollinations to test self-compatibility used all avail-

able flowers on the Craigieburn plants, so the additionalbuds were chosen on different plants. In 1996–1997, wecarried out these pollination manipulations on

P. tetra-petala

at Ohau.In 1995–1996, we examined styles from some buds in

each treatment group for pollen tubes. Unmanipulatedbuds were checked daily to determine when they openednaturally, and “bagged” buds were checked for ripeness.One to nine days after opening (hand-pollinated or natu-rally opened flowers) or ripening (bagged-unopenedbuds), the style was excised and preserved in a 3:1 mix-ture of 70% ethanol and 45% glacial acetic acid. Pollentubes were counted by the aniline blue fluorescencemethod (Martin 1959). The preserved styles were rinsedtwice in distilled water, softened with 8N NaOH for 12hours, rinsed five times, and stained overnight in 0.1%aniline blue in 0.1 M K

3

PO

4

. The styles were mountedand squashed, and the pollen tubes at the base of thestyle were counted on an epifluoresence microscope un-der UV light.

Flowering Rates of Experimental and Control Plants

In 1995–1996, the treatment plants of

P. tetrapetala

atCraigieburn used for the cryptic self-incompatibility testin 1994–1995 were used to measure the resource cost ofproducing a large fruit crop. Each year we measured thetotal bud production and volume (height

3

north-southwidth

3

east-west width) of each plant and then calcu-lated flower density per cubic meter of foliage. A com-parison of flowering densities on control and treatmentplants could show whether higher fruit set from hand-pollinations lowered flowering density the next seasoncompared with control plants. We summed actual fruitproduction on the treatment plants in the 1994–1995and 1995–1996 seasons to compare with fruit produc-tion predicted without pollen supplementation, assum-ing the control-plant level of fruit set in 1994–1995 andexpected 1995–1996 flower densities and average fruitset (based on 1994–1995 flowering density and 1995–1996 control-plant fruit set, respectively).

Bird Visitation Rates

The rate at which birds and insects visited flowers wasestimated from

.

175 hours of videotapes. Unattendedcameras were fixed for periods of 2–3 hours between0900 and 1800 hours, filming plants of different sizes,heights above the ground, and aspects. Plants that werefilmed had to be clearly visible from one side so were of-ten different from the pollination-treatment plants. Justafter filming, flowers and buds within the field of viewwere counted (or for large plants estimated by subsam-pling). We later screened videos to count and identifybird visitors. It was not usually possible to count howmany flowers a bird visited, so we recorded how long

502

Pollen Limitation of New Zealand Mistletoes Robertson et al.


the bird fed on the plant. Total foraging time was di-vided by the number of available buds and flowers andconverted to a per-hour rate for analysis.

Data Analysis

Fruit set is a binary parameter in which the number ofsuccesses and failures are scored for each plant andtreatment combination. Thus, fruit set was analyzed bymeans of a generalized linear model with a binomial er-ror distribution and logit link function using S-PLUS ver-sion 3.3 (MathSoft, Inc. 1995). Where the treatmentswere all performed on the same plant, the data weretreated as a randomized block design with the plants asblocks. Only buds that were not infested with

Zelleria

were included in the analyses. In the 1992–1993 and1994–1995 seasons, the number of buds in the unmanip-ulated treatment that were infested had to be estimatedfrom the averages on several other plants in the popula-tion where infestation rates had been measured. In sub-sequent seasons, the infested buds were identified in alltreatments and excluded from the analyses.

Each style collected for pollen tubes was classified aspollinated if it had

$

3 pollen tubes at the base of thestyle, because not every pollen tube is capable of fertiliz-ing the single ovule. We also tested defining pollinationas

$

1 pollen tubes, but the two analyses were highlycorrelated, so we present only the former analysis. Thedata were analyzed as a logistic analysis of covariance,with plant and pollination treatment as factors and dayssince ripe as a variate.

Results

Self-Compatibility

Both species were fully self-compatible. Fruit set follow-ing self- and cross-pollination did not differ significantlyin 1992–1993 for either species (Table 1). We found no

evidence for cryptic self-incompatibility (i.e., no selec-tive abortion of selfed fruit) when whole

P. tetrapetala

plants were pollinated in 1994–1995 (Table 1). Therewas also no evidence of inbreeding depression: neithergermination rates nor seedling survivorship over 2 yearswere lower for selfed seeds (Table 1).

Pollination Experiments

Pollination treatment affected fruit set significantly, but inopposite ways for the two species. At Wakefield

P. colen-soi

was never pollen-limited, and fruit set with naturalpollinator activity was approximately 50% (Fig. 1). Hand-pollination never increased this significantly, whereasexcluding birds with mesh bags always reduced fruit setdramatically. The pollen-tube accumulation data con-firmed that natural pollination was adequate (Fig. 2). Bythe time flowers began to abscise (9 days after ripening),78% of naturally opened flowers had three or more pol-len tubes at the base of the style, compared to only 25%of styles in unopened buds.

In contrast,

Peraxilla tetrapetala

at Craigieburn wasconsistently pollen-limited. Fruit production from unma-nipulated buds was consistently low (16–45%; Fig. 1),and excluding all pollinators did not usually reduce fruitset significantly. Conversely, hand-pollinations increasedfruit production to 50–85%, and this difference was sig-nificant in three of the four seasons. Moreover, despitewide between-season fluctuations in flower production,fruit production was remarkably constant (Fig. 3), aswould be expected if the resident pollinators could onlypollinate a low, constant density of flowers. Pollen-tubeaccumulation in 1995–1996 also demonstrated pollenlimitation (Fig. 2). No unopened buds and only 11% ofnaturally opened flowers had accumulated

$

3 pollentubes by the fourth day, whereas 73% of hand-pollinatedflowers had

$

3 tubes by the time they abscised (6 daysafter ripening).

Fruit set in

P. tetrapetala

at Ohau in 1996–1997 wasalso pollen-limited. Hand-pollinated flowers had high fruit

Table 1. Self-compatibility in

Peraxilla colensoi

and

P. tetrapetala

a

and checks for cryptic self-incompatibility and inbreeding depression in

P. tetrapetala

.

b

Self-pollinated (%) Cross-pollinated (%) Significance test

c

Species

P. colensoi

(

n

5

5) 49.9 51.2

t

5

0.428, nsP. tetrapetala (n 5 6) 38.6 53.8 t 5 0.844, ns

Stage testedfruit set 86.1 82.4 t 5 1.00, nsgermination, in petri dishes 100.0 100.0 identical meansgermination, on branches 94.1 89.1 x2 5 1.03, df 5 1, nssurvival to 3 April 1996 (9 mos.) 34.4 49.0 x2 5 1.02, df 5 1, nssurvival to 23 April 1997 (22 mos.) 19.1 16.4 x2 5 0.05, df 5 1, ns

aFruit set (%) on a sample of hand-pollinated flowers on large plants, 1992 and 1993. Significance tests are a posteriori to the logistic ANOVAsusing LSD comparisons.bBased on 12 small plants where half of all flowers were hand cross-pollinated and the rest were self-pollinated, Craigieburn 1994 and 1995.cns, not Significant


Robertson et al. Pollen Limitation of New Zealand Mistletoes 503

set, whereas unmanipulated controls and unopened budsset few fruits (Fig. 1).

Flowering Rates of Experimental and Control Plants

Our results suggest that plants incur a measurable costby maturing a large fruit crop. The high fruit set of theCraigieburn P. tetrapetala plants tested for cryptic self-incompatibility in 1994–1995 (82% fruit set, versus 16%for unmanipulated plants) allowed us to test the effectsof resource limitation on future reproduction and sur-vival. Both treatment and control plants showed a highlysignificant negative slope, indicating that a high flower

density in 1994–1995 is followed by a reduced densityin 1995–1996 (control plants, n 5 44, b 5 20.40, R2 50.467, p , 0.001; treatment plants, n 5 12, b 5 20.67,R2 5 0.821, p , 0.001) (Fig. 4). Plants with high flower-ing densities in 1994–1995 usually had low densities thefollowing season, and vice versa.

But overall plant reproduction was limited by pollina-tion, rather than by resources. Plants that received sup-

Figure 2. Pollen-tube accumulation in Peraxilla species in the 1995–1996 season. The mean proportion of buds of known age since ripening with three or more pollen tubes at the base of the style is shown, along with the fitted values (shown connected by a spline) from a logistic analysis of covariance. Symbols indi-cate treatment applied: circle, dotted line, hand-polli-nated buds; diamond, solid line, buds naturally opened by flower visitors; and square, dashed line, pol-linator-excluded buds. Details of the analysis can be found at our website: http://www.pams.canter-bury.ac.uz/105pol.htm

Figure 3. Flower and fruit production per volume of mistletoe foliage (6SE) of P. tetrapetala at the Craigie-burn site over three seasons. Based on totals from per-manently marked control plants (n 5 19, 59, and 73 plants in 1994–1995, 1995–1996, and 1996–1997, re-spectively).

Figure 1. Fruit set in Peraxilla colen-soi at Wakefield over four seasons (a) and P. tetrapetala at Craigieburn over four seasons and at Lake Ohau in 1996–1997 (b). Symbols indicate treatment applied: circle, hand-polli-nated buds; triangle, unmanipu-lated buds (control); and square, pol-linator-excluded buds. Within a season at one site, shared letters indi-cate means that are not significantly different according to generalized linear models with binomial error distributions and logit link functions.Details of the analysis can be found at our website: http://www.pams. canterbury.ac.uz/105pol.htm

504 Pollen Limitation of New Zealand Mistletoes Robertson et al.


plemental pollen (and set more fruit) in 1994–1995 didshow a significantly steeper decline in flower density inthe following year than did control plants (t 5 14.83, df 552, p , 0.001). Our results, however, do not supportthe hypothesis that the steeper decline in plants that arewell pollinated means that the gains in higher fruit set inone season are negated by reduced reproduction the fol-

lowing season. All 12 plants that received supplementalpollen on all flowers in 1994–1995 matured more fruitsthan average that year (Table 2). In the following year,flowering density was somewhat lower on the treatmentplants than on similar control plants, but this did nottranslate to a consistently lower fruit density. Five plantsset fewer fruit in 1995–1996 than expected based on

Figure 4. Cost of flowering in treat-ment and control groups of P. tetra-petala at Craigieburn. Relationship be-tween flowering density in 1994–1995 and the proportion of flowering effort of the two seasons combined that occurred in the 1995–1996 season. A score of y 5 0.5 would indicate ex-actly even flowering effort in the two seasons.

Table 2. Fruit production summed over the seasons of 1994-1995 and 1995-1996 for 12 plants of Peraxilla tetrapetala used in the self-compatibility trials at Craigieburn.*

Plant code Fruits in 1994-1995Difference

from predicted Fruits in 1995-1996Difference

from predicted Overall difference

k1 30 124.5 4 10.2 124.7k4 90 170.1 2 29.9 160.2k10 47 136.6 116 173.0 1109.6k19 58 141.1 12 19.8 150.8k22 11 19.3 69 161.6 170.9k24 19 113.4 23 16.1 119.5k27 63 147.4 6 23.0 144.4k28 35 129.0 0 22.1 127.0k30 20 115.9 7 0.0 115.9k32 10 17.0 0 23.5 13.5k36 33 126.5 17 18.4 135.0k38 20 14.4 6 216.7 212.2

Total 436 1325.2 256.0 1123.9 1449.1

*These plants had all their flowers hand-pollinated in 1994–1995 and thus had very high fruit set in that season (Table 1). Observed fruits perplant are shown for the two seasons separately, along with deviation from the predicted fruit number for both years, assuming the average pop-ulation fruit set from unmanipulated buds for each season and flower densities for the 1995–1996 season as predicted from the relationshipfor unmanipulated plants estimated in Fig. 3. There was no evidence that average flower and fruit production in 1995–1996 was reduced as aresult of the high fruit set in 1994–1995.



their 1994–1995 flowering density (assuming no hand-pollination the previous season), but six plants set morefruit than expected. Overall in 1995–1996, 120 morefruits were produced than expected, which gives no evi-dence for delayed resource limitation of fruit set. Overboth seasons combined, plants that received supplemen-tal pollen produced 692 fruits, 2.85 times the expectedtotal of 243. There was no indication of higher mortalitybecause all 12 plants survived the next 2 years.

Bird Visitation Rates

Flowers were visited by birds more often at Wakefieldthan at Craigieburn (Table 3). Bird visitations were 12times more common at Wakefield than at Craigieburn in1994–1995 and 21 times more common in 1995–1996. In1996–1997, we added the Ohau site but filmed fewerplants at the other sites than in previous years. AlthoughWakefield had higher visitation rates than Craigieburn andOhau, the differences were smaller and nonsignificant.

Discussion

Pollen-Limited Fruit Production

Our data show that in all five data sets from Craigieburnand Ohau, fruit production of Peraxilla tetrapetala waspollen-limited, associated with low bird visitation rates.There was so little natural pollination at Craigieburn,that excluding all pollinators from flowers did not signif-icantly reduce fruit production in three of the four sea-sons. Over three seasons at Craigieburn, fruit produc-tion per volume of mistletoe was constant, despite awidely fluctuating flowering density, suggesting thatfruit production is determined by the number of avail-able pollinators rather than the number of flowers. Incontrast, birds visited P. colensoi at Wakefield fre-quently and fruit production was never pollen-limited.

Whole-plant pollinations show that our results are notan artifact of resource shifts to a small number of well-pollinated flowers, a possible confounding factor in many

other pollen-limitation experiments (Bawa & Webb 1984;Horvitz & Schemske 1988; Zimmerman & Pyke 1988).Nor are the results confused by self-incompatibility(Seavey & Bawa 1986; Wiens et al. 1987), because self-pollen was as effective as cross-pollen. Immediate gains infruit production from pollen supplementation were notnegated by subsequent reductions in fecundity or survi-vorship. Instead, bird visitation rates were insufficient topollinate all the flowers, and we predict that fruit setwould increase if birds were more common.

Pollen limitation in Peraxilla mistletoes may be wide-spread on mainland New Zealand. Low fruit productionis not restricted to P. tetrapetala at Craigieburn andOhau: several other populations of both species alsoshow low fruit production (D. Kelly et al., unpublisheddata). At these sites, many flowers are not visited by pol-linators and fall from the plant bottom-opened (Ladley &Kelly 1995b).

Conservation Implications of Pollen Limitation

Although many studies show apparent pollen limitationin plants (Burd 1994), few address the consequences forthe conservation of species. Steiner and Whitehead(1996) showed that the South African shrub Ixianthesretzioides sets little seed in populations lacking a co-evolved oil-collecting bee. In fragmented landscapes,plants in small populations may receive fewer pollinatorvisits than those in larger patches (Lamont & Klink-hamer 1993; Aizen & Feinsinger 1994).

Whether pollinator loss affects population persistencedepends on three factors. First, some plants may havecompensation mechanisms (Bond 1994), such as asex-ual reproduction, self-pollination, or alternative pollina-tors. For Peraxilla, however, there is little compensa-tion. Asexual reproduction cannot spread mistletoesfrom old host trees to new ones. Self-pollination pro-duces less than one-fifth as many fruits as adequate polli-nation by birds. At some sites, native bees open buds ofPeraxilla tetrapetala, but fruit set is still below half theamount set with abundant pollination, and the bees donot regularly open Peraxilla colensoi buds (Kelly et al.

Table 3. Bird (Tui and Bellbird) visitation rates to Peraxilla spp. flowers (fl) as determined from videotapes.*

Year

Craigieburn P. tetrapetala Lake Ohau P. tetrapetala Wakefield P. colensoi

Within-seasondifferences

Birdvisitation(seconds/fl/hour) n

Videotapehours


Videotapehours


Videotapehours Statistic p

1994-1995 0.011 10 24.2 — — 0 0.132 8 32.9 t 5 2.63 ,0.051995-1996 0.005 9 33.7 — — 0 0.106 7 28.2 t 5 2.63 ,0.051996-1997 0.015 4 12.2 0.013 8 35.4 0.024 3 9.2 F 5 0.02 ns

*The duration of bird visits is expressed as seconds spent visiting flowers per flower per hour and is the mean of plant averages, n 5 number ofplants filmed. Two-sample t tests and an analysis of variance were used within seasons on data transformed by taking log (i 1 0.001) to testthe significance of between-site differences; ns, not significant.



1996). Introduced birds such as Chaffinches (Fringillacoelebs) are also poor alternative pollinators becausethey visit and open few flowers (Ladley et al. 1997).

Second, a larger fruit crop may have no population-level effect if fruit dispersal limits seedling establishment.Peraxilla species have obligate dispersal relationshipswith the same birds that pollinate their flowers becausetheir seeds must pass through the gut of a bird to havetheir pericarps removed before they can germinate (Ladley& Kelly 1996). Recruitment might be more limited by dis-persal than pollination if dispersal requires more birds,but several factors suggest this is probably not true forPeraxilla. Pollination has to occur over a much shorterperiod (2–3 weeks) than dispersal (spread over 2–6months), suggesting that fewer birds would be adequatefor dispersal. Although the P. tetrapetala fruit crop wasincompletely dispersed in 1992–1993 at Craigieburn(Ladley & Kelly 1996), it appears this was because fruitdid not ripen properly that year. In subsequent seasonswe recorded high rates of dispersal (D. Kelly et al., un-published data) at sites where there were low rates ofpollination.

Finally, we need to establish whether populations areseed-limited (Calvo 1993; Bond 1994; Ågren 1996). Ifdensity-dependent seedling deaths are common, re-duced fruit set may not affect recruitment. Crawley(1990) concluded that plant populations were more fre-quently limited by microsite availability than by seed lim-itation. More recently, Eriksson and Ehrlén (1992) foundsome evidence of seed limitation in 9 of 14 species, andAckerman et al. (1996) enhanced seedling recruitmentof the epiphytic orchid Tolumnia variegata in PuertoRico by supplemental pollination of flowers. Therefore,the possibility of plant populations being seed-limitedmust be seriously considered.

Seed limitation in Peraxilla cannot be ruled out fromthe available data. Peraxilla seeds are usually widelyspaced after dispersal. Ladley and Kelly (1996) reported amean of 1.77 Peraxilla colensoi seeds per bird droppingcontaining this species, and we rarely see droppings adja-cent to one another. This suggests that density-dependentseedling mortality is unlikely to be strong. Because mistle-toes establish on the outer branches of host trees, theycan germinate in strong light environments without de-pending on gap creation and hence are not likely to be gap-(microsite-) limited. Therefore, Peraxilla species seemmore likely than many plant species to be seed-limited. Theideal way to resolve this question is by sowing additionalseed, but Peraxilla species are long-lived, which makesexperimentation problematic.

Hence, pollen limitation in Peraxilla species couldwell affect their population sizes. At many sites, fruitproduction per plant has probably been more thanhalved. As a result, some population declines may bedriven by recruitment rather than herbivory (Ogle &Wilson 1985). Historical evidence shows that pollination

failure in the central North Island coincided with a ma-jor decline in P. tetrapetala numbers. Field (1884:288–289) wrote of P. tetrapetala (as Loranthus fieldii) nearRaetihi that it “forms large bushes in the tops of trees,and the blossoms are so abundant as to almost hide thefoliage. . . . fully 10% of the large trees have one or moreLoranthus growing on them. . . . When cutting aline. . . . for the Wanganui–Taupo road, in Septemberand October 1882, my men felled many scores of treeson which the plant was growing.” In this area P. tetra-petala is now restricted to a few populations, each of ahandful of plants (de Lange et al 1997). Crucially, Field(1884) reported that the P. tetrapetala flowers “openvery peculiarly. A small proportion (certainly less than atenth) open from the apex downwards,” whereas therest open from the bottom. The bottom-opened flowershave not been visited by a pollinator (Ladley & Kelly1995a), and thus we can infer that in the central NorthIsland in 1882, over 90% of P. tetrapetala flowers werenot pollinated.

Pollination failure coincided with a major decline inmistletoe numbers during the period when bird densitiesalso declined on the mainland. Buller (1877, 1888) re-ported that Bellbirds virtually disappeared from the NorthIsland between 1860 and 1870, and Tuis were also se-verely depleted. A similar decline happened approxi-mately 30 years later in the South Island (Oliver 1955). Inboth islands the decline coincided with the spread of shiprats (Rattus rattus; Atkinson 1973). Although both spe-cies have recovered to some extent on both the main is-lands, high-density populations are now normally foundin areas where they are protected from predators, such asoffshore islands (Diamond & Veitch 1981).

Clearly, effective conservation of Peraxilla species willrequire maintenance of their bird mutualists. Tuis andBellbirds are also important pollinators and seed dispers-ers for many other New Zealand forest plants (Clout &Hay 1989; Castro & Robertson 1997), so the pollinationdifficulties seen in Peraxilla may extend to some ofthese other species, most of which have not been wellstudied. Many of the plants used by birds are long-livedwoody perennials. With relatively long lives and recentloss of mutualist birds, a lack of regenerative capacitymay take many years to become apparent. The presentforest composition may already be suffering subtle dam-age from weakened mutalisms, adding to the already dev-astating changes produced by introduced herbivores.

Acknowledgments

We thank B. and D. Ladley for accommodation; the Bash-ford family and the Department of Conservation for per-mission to work on their land; the Public Good ScienceFund for financial support; and L. Sessions, M. Willson,



and two anonymous referees for helpful comments onan earlier draft of the manuscript.

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Effects of Pollinator Loss on Endemic New Zealand Mistletoes (Loranthaceae)

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