13 Pollination, Seed Predation, and Seed Dispersal I. Types and Patterns of Pollination A. Pollinator Functional Groups B. Measurement of Pollination C. Spatial and Temporal Patterns of Pollination II. Effects of Pollination III. Types and Patterns of Seed Predation and Dispersal A. Seed Predator and Disperser Functional Groups B. Measurement of Seed Production and Dispersal C. Spatial and Temporal Patterns of Seed Predation and Dispersal IV. Effects of Seed Predation and Dispersal V. Summary INSECTS AFFECT PLANT REPRODUCTION AND ASSOCIATED PROCESSES in a variety of ways. Direct and indirect effects of herbivores on plant produc- tion and allocation of resources to reproduction were described in Chapter 12. Pollination, seed predation, and seed dispersal are major processes by which insects (and other animals) affect plant reproduction and distribution. Pollina- tors control fertilization and reproductive rates for many plant species, especially in the tropics. In fact, some plant species depend on pollinators for successful reproduction and may disappear if their pollinators become rare or extinct (Powell and Powell 1987, Steffan-Dewenter and Tscharntke 1999). Seed preda- tors consume seeds and thereby reduce plant reproductive efficiency but often move seeds to new locations and thereby contribute to plant dispersal. Many plant species depend on seed dispersers for successful movement of seeds to new habitats and may be vulnerable to disappearance of their dispersers (O’Dowd and Hay 1980, Schupp 1988, Witmer 1991). Pollinators and seed predators play important roles in seed production, seedling recruitment, and plant demography. Insects are the major agents of pollination, seed predation, or seed dis- persal in many ecosystems (Bawa 1990, Degen and Roubik 2004, Sallabanks and Courtney 1992). For example, Momose et al. (1998b) noted that for 270 plant species in a lowland dipterocarp forest in Sarawak, Malaysia, social bees were the primary pollinators for 44%, beetles for 24%, solitary bees for 19%, and birds 383 013-P088772.qxd 1/24/06 11:03 AM Page 383 and bats for 6%. Pollination and seed dispersal are among the most intricate mutualisms between animals and plants and have been studied widely from the perspective of co-evolution. Nevertheless, few studies have evaluated the effects of pollinators,seed predators,and seed dispersers on ecosystem processes,despite their importance to seedling recruitment and vegetation dynamics. Different functional groups of pollinators and seed-feeders affect seedling recruitment and vegetation dynamics in different ways. I. TYPES AND PATTERNS OF POLLINATION Plants exhibit a diversity of reproductive mechanisms. Many reproduce vegeta- tively, but this mechanism is limited largely to local reproduction. Genetic het- erozygosity and colonization ability are increased by outcrossing.Although many plant species are capable of self-fertilization, a large percentage (a vast majority in some ecosystems) are self-incompatible, and many are dioecious (e.g., 20–30% of tropical tree species), with male and female floral structures separated among individual plants to preclude inbreeding (Bawa 1990, Momose et al. 1998a). Mechanisms for transporting pollen between individuals becomes increasingly critical for reproduction with increasing separation of male and female structures and increasing isolation of individual plants (Ghazoul and McLeish 2001, Regal 1982, Steffen-Dewenter and Tscharntke 1999). Several mechanisms move pollen among flowering individuals. Pollen can be transferred between plants through abiotic and biotic mechanisms (Regal 1982). Pollen is transported abiotically by wind. Biotic transport involves insects (Fig. 13.1), birds, and bats. Insects are the major pollinators for a vast majority of plant species in the tropics (Bawa 1990), but the proportion of wind-pollinated plants increases toward the poles, reaching 80–100% at northernmost latitudes (Regal 1982). These mechanisms provide varying degrees of fertilization efficiency, depending on ecosystem conditions. A. Pollinator Functional Groups Functional groups of pollinators may be more or less restricted to groups of plants based on floral or habitat characteristics (Bawa 1990). A large number of pollinators are generalists with respect to plant species. This functional group includes many beetles, flies, thrips, etc. that forage on any floral resources avail- able. Specialist pollinators often exploit particular floral characteristics that may exclude other pollinators. For example, nocturnally flowering plants with large flowers attract primarily bats, whereas plants with small flowers attract primarily moths.Long,bright-red flowers attract birds but are largely unattractive to insects (S. Johnson and Bond 1994). Such flowers often are narrow to hinder entry by bees and other insect pollinators (Heinrich 1979) but may nonetheless be polli- nated by some insects (Roubik 1989). Pollen feeders feed primary on pollen (e.g., beetles and thrips) and are likely to transport pollen acquired during feeding, whereas others are primarily nectar-feeders (e.g., beetles, butterflies, moths, and flies) and transport pollen more coincidentally. In fact, many nectar feeders avoid 384 13. POLLINATION, SEED PREDATION, AND SEED DISPERSAL 013-P088772.qxd 1/24/06 11:03 AM Page 384 I. TYPES AND PATTERNS OF POLLINATION 385 FIG. 13.1 Examples of pollinators. A: Honey bee, Apis mellifera, Louisiana, United States. B: Scarab beetle, Fushan Experimental Forest, Taiwan. 013-P088772.qxd 1/24/06 11:03 AM Page 385 386 13. POLLINATION, SEED PREDATION, AND SEED DISPERSAL the reproductive organs, often by perforating the base of the flower to reach the nectar (Dedej and Delaplane 2004) or, in the case of ants, may reduce pollen via- bility (Peakall et al. 1987). Bees, especially Apis spp., primarily feed on pollen and nectar. Functional groupings also reflect attraction to floral odors. For example, dung-, fungus-, and carrion-feeding flies and beetles are the primary pollinators of plants that emit dung or carrion odors (Appanah 1990, Norman and Clayton 1986, Norman et al. 1992). Ants frequently exploit floral resources but have little importance as pollina- tors. Peakall et al. (1987) suggested that antibiotic secretions produced by most ants, to inhibit infection by entomophagous fungi in a subterranean habitat, also inhibit germination of pollen. Ants lacking these secretions are known to func- tion as pollinators. Pollinator functional groups also have been distinguished on the basis of habitat preferences, such as vegetation stratum (Fig. 13.2). Appanah (1990) dis- tinguished four groups of plant-pollinator associations in a tropical lowland dipterocarp forest in Malaysia. The forest floor stratum was characterized by low visibility and limited airflow. Floral rewards were small, reflecting low produc- tivity of light-limited plants and low energy requirements of associated pollina- tors, and flowering times were extended, increasing the probability of pollination by infrequent visitors. The plant-pollinator association of this stratum was dom- inated largely by nonselective, low-energetic beetles, midges, and other flies. These pollinators were attracted over short distances by strong olfactory cues, 50 40 30 20 10 Basement Canopy Upper Emergent layer Centris fusci- ventris Epicharis albofasciata Eulaema polychroma Euglossa hemichlora Lower 0 FIG. 13.2 Vertical stratification of pollinator species in a tropical rainforest. The two bee species above pollinate flowers in the upper canopy and the two species below pollinate flowers in the subcanopy. From Perry (1984) © George V. Kelvin/Scientific American. 013-P088772.qxd 1/24/06 11:03 AM Page 386 often resembling dung or carrion, which have limited effective range.The under- story stratum shared many of the environmental features of the forest floor.Plants in this stratum also offered limited visual cues and floral rewards and were pol- linated by nonspecific trapliners (i.e., species that revisit particular plants along an established circuit; e.g., trigonid bees, solitary wasps,and butterflies).The over- story stratum generally was characterized by brightly colored flowers, held above the canopy to attract pollinators over a wide area, and brief, highly synchronized flowering within plant species. Dominant pollinators were Apis dorsata and trapliners such as carpenter bees, birds, and bats. Dipterocarps in the genera Shorea, Hopea, and Dipterocarpus formed a separate association based on tiny flowers with limited nectar rewards and nocturnal flowering. Thrips and other tiny, flower-feeding insects were the primary pollinators. By contrast, Sakai et al. (1999) observed that beetles (chrysomelids and curculionids), rather than thrips, were the primary pollinators of these tree species in Sarawak. Finally, some plant species representing various canopy positions were cauliflorous (i.e., they produced flowers along the trunk or main branches).These flowers usually were large, or small and clumped; pale colored; odiferous; and produced during a brief, highly synchronized period. Pollinators included under- story and overstory insects,birds,and bats. Momose et al. (1998b) noted that long- distance pollinators tended to be less common in Malaysian forests than in Neotropical forests. Roubik (1993) experimentally manipulated availability of floral resources from different canopy strata in tropical forests in Panama. Results indicated that the apparent fidelity of pollinator species to particular canopy strata reflected pollinator preferences for particular floral resources. Most pollinator species were attracted to their preferred floral resources regardless of their location in the canopy. B. Measurement of Pollination Pollination efficiency reflects the probability that pollen reaches a conspecific flower. A number of factors influence the efficiency of pollen transport between conspecific reproductive structures. The mechanism of pollen transport, proxim- ity of conspecific plants, pollinator attraction to floral structures, adaptations for carrying pollen, fidelity, and thermodynamic constraints determine the prob- ability that a flower will receive conspecific pollen. Several methods have been used to measure pollinator activity and pollina- tion efficiency. Observations of the type and frequency of floral visitors can provide a measure of pollinator activity (Aizen and Feinsinger 1994, Ghazoul and McLeish 2001, Sakai et al. 1999, Steffan-Dewenter and Tscharntke 1999, Steffan- Dewenter et al. 2001). Interception traps also can be used to collect insects visiting flowers (S. Johnson et al. 2004). The number of fertilized seeds per flower provides a measure of pollination for self-incompatible species (Steffan- Dewenter et al. 2001, S. Johnson et al. 2004). Kohn and Casper (1992) used electrophoresis to identify seeds containing alleles that did not occur in neigh- boring plants. G. White et al. (2002) used DNA (deoxyribonucleic acid) marker I. TYPES AND PATTERNS OF POLLINATION 387 013-P088772.qxd 1/24/06 11:03 AM Page 387 techniques to measure pollen transfer among trees, Swietenia humilis, in isolated fragments of tropical forest in Honduras. Wind pollination is highly inefficient.The probability of successful pollen trans- fer by wind decreases as the cube of distance between plants (Moldenke 1976). However, plant investment in individual pollen grains is negligible so large numbers can be produced, increasing the cumulative probability that some will land on conspecific reproductive structures.Directed transport of pollen by animal pollinators increases efficiency to the extent that the pollinator visits a conspecific flower before the pollen is lost or contaminated with pollen from other plant species. Hence, animal-pollinated plant species may invest energy and nutrients in adaptations to improve the fidelity of the pollinator.These adaptations include nectar rewards to attract pollinators, floral and aromatic advertisements; floral structures that restrict the diversity of pollinators visiting the flowers,synchronized flowering among conspecific individuals, and divergence in time of flowering among plant species to reduce pollen contamination (Heinrich 1979). Nectar rewards must be sufficient to compensate the pollinator for the forag- ing effort. For example, a greater nectar return is necessary to attract bees during cooler periods, when energy allocation to thermoregulation is high compared to warmer periods (Heinrich 1979). Heinrich (1979) noted that pollinator fidelity reflects offsetting adaptations. Plants invest the minimum amount of energy nec- essary to reward pollinators, but pollinators quickly learn to concentrate on flowers offering the greatest rewards. Individual plants in aggregations could attract bees and be pollinated even if they produced no nectar, provided that their neighbors produced nectar.The nonproducers should be able to invest more energy in growth and seed production. However, if these “cheaters” became too common, pollinators would switch to competing plant species that offered greater food rewards (Feinsinger 1983). A. Lewis (1993) suggested that floral character- istics may reflect advantages accruing to the plant when pollinators must make a substantial investment in learning to handle a flower, thereby becoming facul- tative specialists. Plant investment in attractants and rewards for pollinators rep- resents an evolutionary tradeoff between growth and reproduction (Heinrich 1979) and may affect the ability of light- or resource-limited species to attract pollinators.Bawa (1990) reviewed studies that demonstrated long-distance pollen flow and outcrossing for tropical canopy trees but a high degree of inbreeding for many tropical herbs and shrubs. Effects of pollination on plant seedling recruitment and ecosystem processes have been measured less frequently. Effects on seed production can be measured as the number of seeds produced when pollinators have access or are excluded from flowers (S. Johnson et al. 2004, Norman and Clayton 1986, Norman et al. 1992, Steffan-Dewenter and Tscharntke 1999, Steffan-Dewenter et al. 2001). Pol- linator effects on ecosystem processes should reflect their direct influence on plant reproduction and indirect influence on vegetation dynamics. C. Spatial and Temporal Patterns of Pollination Pollination by insects is more prevalent in some types of ecosystems than in others. Pollination by animals is more common in angiosperm-dominated eco- 388 13. POLLINATION, SEED PREDATION, AND SEED DISPERSAL 013-P088772.qxd 1/24/06 11:03 AM Page 388 systems than in gymnosperm-dominated ecosystems, but pollination by wind is energetically efficient for dominant species in grasslands and temperate forests. The regularity with which conspecific plants occur in close proximity to each other largely determines their pollination mechanism. Long-lived species that dominate relatively simple ecosystems (i.e., grasslands and temperate forests) are pollinated primarily by wind. These plant species do not require efficient polli- nation or frequent reproduction to ensure population survival. Energetically inexpensive transport of pollen by wind provides sufficient pollination (and suc- cessful reproduction) so that energy need not be diverted to production of expen- sive nectar rewards and floral displays to advertise availability. Directed transport of pollen by animals is critical to reproduction of plant species that are short-lived, are sparsely distributed, or occur in habitats with restricted airflow (Appanah 1990, Moldenke 1979, Regal 1982, Somanathan et al. 2004). In contrast to long-lived plants, short-lived plants have limited opportuni- ties for future reproduction and, therefore, tend to depend on more efficient pol- lination to ensure seed production. Sparsely distributed plants and plants in areas of limited airflow cannot rely on inefficient transport of pollen by wind between distant or inaccessible individuals. Such species include early successional plants dominating ephemeral communities, widely spaced plants in harsh environments (e.g., deserts), scattered forbs in grasslands, subdominant trees, shrubs and herbs in temperate forests, and all (or most) plant species in tropical forests (S. Johnson et al. 2004, Momose et al. 1998b, Regal 1982). Regal (1982) reported that fewer than 6% of desert shrub species are wind pollinated. All of the 270 plant species in a lowland diperocarp forest in Sarawak, Malaysia,were animal pollinated,90% by insects (Momose et al. 1998b). Insects and other animal pollinators can transport pollen over considerable distances. Kohn and Casper (1992) documented gene flow among bee-pollinated buffalo gourds, Cucurbita foetidissima, over distances up to 0.7 km in New Mexico, United States. Somanathan et al. (2004) reported that carpenter bees, Xylocopa tenuiscapa, pollinated a Neotropical tree, Heterophragma quadriloculare, isolated from pollen sources by as much as 330 m, permitting reproduction by spatially isolated trees. G. White et al. (2002) identified sources of pollen reaching isolated Swietenia humilis trees and forest fragments in Honduras. A substantial proportion of pollen (25%) was transported over dis- tances of >1.5 km, to more than 4.5 km between fragments. By contrast, a Neotropical shrub, Lasiosiphon eriocephalus, pollinated by a weakly flying nitidulid beetle, may be particularly vulnerable to isolation or fragmentation (Somanathan et al. 2004). Roubik (1989) reviewed studies that distinguished seasonal patterns of polli- nator activity. Primary pollinators usually were most active during periods of peak flowering. Heithaus (1979) reported that megachilid and anthophorid bees were most active during the dry season in Costa Rica, halictid bees during both wet and dry seasons, and andrenid and colletid bees during the wet season or during both seasons. Social pollinators (e.g., apid bees) require a sequence of floral resources throughout the year to support long-lived colonies and visit a succession of flowering plant species, whereas more ephemeral, solitary species I. TYPES AND PATTERNS OF POLLINATION 389 013-P088772.qxd 1/24/06 11:03 AM Page 389 with short life spans can be relatively more specialized on seasonal floral resources (S. Corbet 1997, Roubik 1989). II. EFFECTS OF POLLINATION Pollination contributes to genetic recombination and survival of plant species in heterogeneous environments. Many plants can reproduce vegetatively or by self-fertilization, but these mechanisms are not conducive to long-distance colonization or genetic recombination. Species survival and adaptation to chang- ing environmental conditions requires outcrossing and environmental selection among diverse genotypes. Some long-lived perennials may endure adverse condi- tions and persist by vegetative reproduction until conditions favor out- crossing and seedling recruitment. Such windows of opportunity are unpre- dictable, requiring annual investment in flower and seed production (Archer and Pyke 1991). Pollinator-facilitated reproduction is a key factor maintaining populations of ephemeral or sparsely distributed plant species. Obligate outcrossing plant species that depend on insect or vertebrate pollinators for pollination are vul- nerable to loss of these mutualists. Maintenance of rare plant species or restora- tion of declining species depends to a large extent on protection or enhancement of associated pollinators (Archer and Pyke 1991, S. Corbet 1997). Norman and Clayton (1986) and Norman et al. (1992) found that pawpaws, Asimina spp., in Florida, United States, depended on beetle and fly pollinators attracted to yeasty floral odors. Self-pollinated flowers occasionally produced fruits, but only seeds from cross-pollinated flowers germinated. Differential pollination and reproductive success among plant species affect vegetation dynamics. Plant species that maximize pollination efficiency and in- crease outcrossing via animal pollinators are able to persist as scattered individ- uals. However, pollination efficiency by insects is strongly affected by plant spacing. Momose et al. (1998a) found that pollination by thrips and consequent fruit and seed development of a small (<8m height) tree species, Popowia piso- carpa, in Sarawak declined dramatically when distances between trees exceeded 5m.Changes in pollinator abundances and pollination efficiency affect plant population dynamics and persistence in communities. Environmental changes that increase the distance between conspecific plants may threaten their survival, as shown in the following examples. Steffan-Dewenter and Tscharntke (1999) examined the effects of plant isola- tion on pollination and seed production in replicate grasslands surrounded by intensively managed farmland. They established small experimental patches of two grassland species, Sinapsis arvensis and Raphanus sativus, at increasing dis- tances from the grassland boundaries and found that the number and diversity of bees visiting flowers, and seed production, declined with increasing isolation (Fig. 13.3). Number of seeds per plant was reduced by 50% at 260 m from the nearest grassland for R. sativus and at 1000 m for S. arvensis. Changes in pollinator abundance, such as those resulting from ecosystem fragmentation, can affect plant reproduction and gene flow (Bawa 1990, Didham 390 13. POLLINATION, SEED PREDATION, AND SEED DISPERSAL 013-P088772.qxd 1/24/06 11:03 AM Page 390 et al. 1996). Powell and Powell (1987) compared attraction of male euglossine bees to floral chemical baits in forest fragments in Brazil.Abundance and species composition did not differ among sites prior to fragmentation. However, after fragmentation, visitation rates for most species were correlated to fragment size, and the bee species trapped in clearings differed from the species trapped in forests (Fig. 13.4). Powell and Powell (1987) concluded that the reduced abun- dance and activity of particular pollinators in fragmented forests threatened the viability of their orchid hosts. Aizen and Feinsinger (1994) compared polli- nator visitation among replicated blocks containing continuous forest and large (>2.2 ha) and small (<1 ha) fragments in subtropical dry forest in northwestern Argentina. The diversity and visitation frequency of native pollinators decreased significantly, and the visitation frequency of exotic honey bees, Apis mellifera, increased significantly with decreasing fragment size (Fig. 13.5). Fragments sup- ported fewer bee species than did continuous forests.Although honey bees from the surrounding agricultural matrix replaced most of the lost visitation by native pollinators, some plant species could be threatened by loss or reduced specificity of pollinators. Pollination also contributes to production of fruits and seeds that support associated food webs. Many animal species depend on fruit and seed production, at least seasonally (see later in this chapter). Hence, pollination of fruiting plants has consequences not only for plant reproduction but also for the survival of frugivores and seed predators (Bawa 1990). Pollinators can affect ecosystem energy and nutrient fluxes. Roubik (1989) calculated the effects of social bees on energy and nitrogen budgets of tropical forests in Central America. He estimated that 600 colonies km -2 har- vested 1.4 ¥ 10 7 kJ year -1 and disposed of an equivalent energy value represented by dead bees scattered on the ground within a few dozen meters of each nest. This value exceeded estimates of energy fixed annually by primary pro- ducers, indicating that the energetics of flowering are greatly underestimated II. EFFECTS OF POLLINATION 391 Mustard (Sinapis arvensis) Mustard (Sinapis arvensis) Distance from nearest grassland (m) Distance from nearest grassland (m) 12 10 8 6 4 2 0 60 50 40 30 20 10 0 0 Wild bees per 15 min Seeds per plant (x100) 1000 400 900 1600 1600900400100 FIG. 13.3 Relationship between the plant distance from the nearest chalk grassland and abundance of pollinating bees per 15 minutes (left) and number of seeds per plant (right).The regression lines are significant at P < 0.003. From Steffan- Dewenter and Tscharntke (1999) with permission from Elsevier. Please see extended permission list pg 572. 013-P088772.qxd 1/24/06 11:03 AM Page 391 (Roubik 1989). The 600 colonies also distributed about 1800 kg trash (pupal exuviae and feces) ha -1 year -1 . At 4% nitrogen content, this represents a flux of 72 kg ha -1 year -1 or about 1% of above-ground nitrogen in biomass. Pollinator effects on community structure also should affect ecosystem processes. These effects warrant further study. 392 13. POLLINATION, SEED PREDATION, AND SEED DISPERSAL Euglossa chalybeata Euglossa stilbonata Euglossa crassipunctata Euglossa iopyrrha Euglossa prasina & E. augaspis Eulaema meriana & E. bombiformis Eulaema mocsaryi Exaerete frontalis Eufriesea laniventris & E. xantha Number of bees hr –1 10 8 6 4 2 0 Intact forest 100 ha fragment 10 ha fragment 1 ha fragment Cleared FIG. 13.4 Rates of visitation by male euglossine bees at chemical baits in intact forest, forest fragments of varying size (100 ha, 10 ha, and 1 ha), and recently deforested (500 ha). Modified from Powell and Powell (1987) with permission from the Association for Tropical Biology. FIG. 13.5 Rates of visitation by all pollinating insects, exotic honey bees (Apis mellifera) alone, and native pollinators alone on flowers of two plant species by treatment (continuous forest, and large [2.2 ha] and small [1 ha] fragments) and by time of day in Argentina. Vertical lines represent standard errors; bars under the same letter do not differ at P < 0.05. From Aizen and Feinsinger (1994) with permission from the Ecological Society of America. 013-P088772.qxd 1/24/06 11:03 AM Page 392 [...]... groups can be subdivided on the basis of predispersal or postdispersal seed predation, seed size, etc Predispersal frugivores and seed predators feed on the concentrated fruits and seeds developing on the parent plant, whereas postdispersal frugivores and seed predators must locate scattered fruits and seeds that have fallen to the ground Rodents and birds usually exploit larger seeds than do insects, and... been used to measure seed predation and dispersal Predispersal seed predation can be measured by marking fruits or seeds on the plant and observing their fate, using a life table approach (see Chapter 5) Mature fruits and seeds can be collected for emergence of seed predators (SteffanDewenter et al 2001) or dissected or radiographed for identity and number of internal seed predators or evidence of... survival and growth rates (height and diameter) of seedlings from insect- damaged seeds Ehrlén (1996) reported a significant positive correlation between the change in population growth rate and the reproductive value of seeds, as reduced by seed predation, indicating that survival of seeds and seedlings is the most important aspect of seed predator effects on plant population growth Postdispersal seed predators... excluded, this small-seeded composite became numerically dominant and reduced species diversity Many plant species have become dependent on animal mutualists for seed dispersal Seed and seedling survival for some species depends on distance from parent plants, under which seed predation may be concentrated (O’Dowd and Hay 1980, Schupp 1988) As found by Powell and Powell (1987) and SteffanDewenter and... discolor by ants, to nests averaging only 2.3 m from the nearest plant, reduced seed predation by desert rodents from 25–43% of seeds in dishes under parent plants to . replace small-seeded plant IV. EFFECTS OF SEED PREDATION AND DISPERSAL 401 01 3- P088772.qxd 1/24/06 11:03 AM Page 401 402 13. POLLINATION, SEED PREDATION, AND SEED DISPERSAL TABLE 13. 1 Effects. seeds and can significantly reduce populations of predispersal seed predators (Coe and Coe 1987, Herrera 1989). Sallabanks and Courtney 396 13. POLLINATION, SEED PREDATION, AND SEED DISPERSAL 0 20 40 60 80 100 0 20 40 60 80 100 120 140 160 1989. number of seeds per cone Year Seed damage or yield (%) Total seed per cone Seeds damaged by insects Seed yield FIG. 13. 6 Relationship between total seed produced, seed loss to insects, and seed yield