8 Plant-Animal Interactions — Update 2014 K. Greg Murray & Judith L. Bronstein Plant-pollinator Interactions pollination syndromes. He found that both birds The suites of morphological, phenological, and bats visited flowers of both plant species, and behavioral characteristics of plants and but that only bats effectively pollinated both. pollinators that comprise “pollination Hummingbirds effectively pollinated B. syndromes” remain useful for predicting the tenuiflora, but because the reproductive parts of players in pollination mutualisms. For example, B. cyclostigmata extend further from the red tubular flowers are likely to be visited by nectaries, birds can access nectar without hummingbirds, and short-tongued bees are more contacting the anthers and stigma. This work likely to visit flowers with a more open nicely demonstrates the need for caution in morphology that doesn’t restrict their access to assuming too much about the identity of nectar and pollen. However, the frequent pollinators merely on the basis of floral finding that floral visitors aren’t restricted just to morphology and timing of nectar secretion. those usually associated with a particular Muchhala suggests that these species of syndrome has increasingly led to criticism of the Burmeistera demonstrate generalization for utility of the syndrome idea itself (e.g., Ollerton pollination by both bats and hummingbirds. 2009, but see Rosas-Guerrero 2014), as has the Work at Monteverde since 2000 has added realization that many animals feed at flowers detailed information on the basic reproductive usually associated with different types of biology of local plants as well. {Cascante- pollinators. {Muchhala, 2003, Exploring the Marin, 2005, Reproductive biology of the boundary between pollination syndromes: bats epiphytic brorneliad Werauhia gladioliflora in a and hummingbirds as pollinators of Burmeistera premontane tropical forest}, for example, cyclostigmata and B-tenuiflora studied the flowering phenology and breeding (Campanulaceae)} work with Burmeistera system of the bat-pollinated bromeliad Werauhia tenuiflora and B. cyclostigmata at Monteverde (formerly Vriesia) gladiolifolia, and {Bush, demonstrates some of the ambiguity of 2009, Early autonomous selfing in the hummingbird-pollinated epiphyte Pitcairnia rates and appear to be more pollen-limited than brittoniana (Bromeliaceae)} elucidated the those at lower elevations (e.g., San Luis) or breeding system of the hummingbird-pollinated those further south in Costa Rica (i.e., Las bromeliad Pitcairnia brittoniana. Both species Cruces and Las Alturas; {Stone, 2008, Pollinator were capable of self-pollination, and both fruit- abundance and pollen limitation of a and seed set were equivalent in plants limited to solanaceous shrub at premontane and lower self-pollination as in those available to montane sites}. However, when {Stone, 2014, pollinators. Self-pollination is common among Transmission advantage favors selfing allele in epiphytes, which may suffer unpredictable experimental populations of self-incompatible visitation due to their isolation and limited floral Witheringia solanacea (Solanaceae)} created displays {Bush, 1995, Breeding systems of experimental gardens with both genotypes and epiphytes in a tropical montane wet forest}, but allowed them to be pollinated naturally, SC and Bush and Guilbeau found that pollen loads SI plants had roughly equivalent fruit- and seed deposited by hummingbirds were also sufficient set but less than 10% of SC seeds resulted from to ensure nearly full seed set in P. brittoniana. self-fertilization. They concluded that embryonic As they noted for P. brittoniana, it seems likely inbreeding depression was still substantial in SC that many epiphytes cross-pollinate when plants, but suggested that these genotypes will pollinators are available, but self-pollinate when continue to spread because the transmission they are scarce. advantage of selfing through male function Another contribution from Monteverde is effectively outweighs even severe inbreeding Judy Stone’s work with colleagues on depression. pollination ecology and breeding system evolution in Witheringia solanacea. Self- Plant-Frugivore Interactions compatibility has evolved independently many Much of the work on plant-frugivore times, but the conditions that favor it remain interactions in Monteverde since the book’s somewhat controversial because theory predicts publication has focused on the post-dispersal that they must outweigh the costs of self- fates of seeds. To a large degree this emphasis fertilization (primarily lowered fitness via the mirrors that in the field of plant-frugivore production of offspring with two copies of interactions in general. It is motivated by the deleterious alleles). Most investigations of the understanding that the evolutionary evolution of self-compatibility rely on consequences of seed dispersal for plants comparisons of different but closely related (including coevolution with frugivores) are species, but {Stone, 2006, Variation in the self- mediated by the effects of dispersal on seed fate incompatibility response within and among and plant demography. Some of Wenny’s work populations of the tropical shrub Witheringia on dispersal of large-seeded species also deals solanacea (Solanaceae)} found populations of explicitly with dispersal per se, however. W. solanacea with both self-incompatible (SI) Wenny (1999) showed that seeds of and self-compatible (SC) genotypes at Beilschmiedia pendula, one of the largest seeds Monteverde and Varablanca. SI genotypes of dispersed by birds at Monteverde, are rarely W. solanacea suffered nearly complete deposited more than 10 m beyond the crowns of embryonic lethality when experimentally self- fruiting trees, but that seeds dispersed even short pollinated ({Stone, 2010, Embryonic inbreeding distances from the parent suffer less predation depression varies among populations and by (from rodents and beetle larvae) than those mating system in Witheringia solanacea deposited directly beneath the crown. His work (Solanaceae)}, but SC genotypes did not, and demonstrates that dispersal is indeed beneficial Stone et al. concluded that deleterious alleles for B. pendula, and that the effect occurs on had already been largely purged from the SC quite a small spatial scale. In contrast, seeds of genotypes. Such purging is most likely to occur Ocotea endresiana suffered nearly complete when plants are severely pollen-limited, and W. removal by predators regardless of dispersal solanacea populations near the MCFP did distance from the parent tree {Wenny, 2000, indeed have lower pollinator (bee) visitation Seed dispersal of a high quality fruit by specialized frugivores: High quality dispersal?}. Although secondary dispersers increased median Most birds moved seeds less than 25 m, but distances only slightly, they did have a profound male Three-wattled Bellbirds (Procnias effect on seed fate by burying seeds 1-3 cm deep tricarunculata) often deposited them beneath in the soil. Buried seeds were far more likely to courtship display perches, many of which survive than those that remained on the soil overhang treefall gaps. Wenny’s experiments surface, which were killed mostly by rodents failed to show any difference in gap vs. and insects (G. glabra) or by Collared Peccaries understory seed removal rates, but seedlings in (G. kunthiana). Wenny’s work on seed fate at gaps grew more rapidly and suffered less Monteverde also included comparisons among mortality from pathogenic fungi than did those ten additional species with different seed sizes, in understory. Thus, male Bellbirds provide a and although highly variable within size good example of directed dispersal (sensu Howe categories, seed survival tended to be higher for and Smallwood 1982), and may be the largest seeds. Because these seeds continued disproportionately important for recruitment of to suffer rodent attack after germination, O. endresiana. Determining the strength of the however, the relationship between seed size and effect relative to that of other dispersers will seedling recruitment was complex. {Wenny, require more detailed study, however. 2005, Post-dispersal seed fate of some cloud Another example of directed dispersal at forest tree species in Costa Rica} estimated that Monteverde is provided by {Sheldon, 2013, five species of small rodents were responsible Spatial and Temporal Variation of Seed Rain in for about 70% of seed predation. Insect the Canopy and on the Ground of a Tropical infestation was also common in some species, Cloud Forest} study, which compared the “seed but mostly occurred before dispersal. Secondary rain” deposited on the forest floor with that movement of seeds (by rodents) for short deposited in the forest canopy in part of the distances was common, but only Guarea was MCFP. Their study employed seed traps, with commonly cached and often buried; most seed those in the canopy estimating seeds that are movement thus resulted in predation. deposited and that accumulate in epiphyte mats Given the importance of mammalian seed and the soil associated with them. Despite broad predators as mediators of plant population overlap, the species composition of the seed rain dynamics, how forest fragmentation and was statistically distinct in each habitat: epiphyte distributional changes driven by climate change seeds dominated in the canopy, while those of will affect mammal populations is of great large trees were most common on the forest importance in montane