8 - 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 , and behavioral characteristics of 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 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 }, 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 , 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 {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 (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. 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 habitats like those in floor, suggesting that dispersers do move Monteverde {Gibson, 2013, Near-Complete epiphyte seeds to especially appropriate Extinction of Native Small Mammal Fauna 25 establishment sites more often than would be Years After Forest Fragmentation;Meserve, expected by chance. Seeds dispersed by birds 2011, Global climate change and small mammal (rather than by mammals or wind) dominated in populations in north-central Chile;Sheldon, both habitats and over all seasons, highlighting 2011, Climate change and community the importance of animal dispersers – especially disassembly: impacts of warming on tropical birds – in maintaining the ecological integrity of and temperate montane community structure}. the Monteverde forest. {Chinchilla, 2009, Seed predation by mammals {Wenny, 1999, Two-stage dispersal of in forest fragments in Monteverde`, Costa Rica} Guarea glabra and G-kunthiana (Meliaceae) in compared mammalian seed predator populations Monteverde`, Costa Rica} studied the effects of and seed removal rates in a large tract of primary (by birds and non-flying mammals) and continuous forest (including the MCFR) and in secondary (by scatter hoarding rodents, e.g., two nearby forest fragments of 350 and 20 ha. agoutis) dispersal on survival and germination in As expected, the fragments were missing some two species of Guarea. Seeds were moved up to of the larger species of seed predators (e.g., 65 m beyond parent tree crowns by primary peccaries and pacas), but experienced seed dispersers, but median distances were within 15 removal rates that were only marginally lower m for both G. glabra and G. kunthiana. than those in intact forest. Chinchilla attributed

much of the compensatory predation in the experiments were consistent with the fragments to the higher abundance of the comparisons between seed bank and annual seed specialist seed predator Heteromys rain densities outlined above: seeds of the same desmarestianus there, compared to intact forest, species with high seed bank : annual seed rain where it was uncommon. ratios also survived well in the field since 1993 Murray and Garcia-C. (2002) reported on a (Murray and Garcia-C 2002). {Veldman, 2007, long-term study of the roles played by seed Chemical defense and the persistence of pioneer dispersal and seed survival in facilitating plant seeds in the soil of a tropical cloud forest} coexistence of a large guild of pioneer plant investigated the chemical basis for the patterns species that depend upon a limited resource: of mortality among six of the pioneer species in space in recently formed treefall gaps. They Murray and Garcia-C’s (2002) study (P. found that the top 10 cm of Monteverde soils rivinoides, C. polyphlebia, G. poasana, U. elata, contains 3000 to 6500 viable but dormant B. frutescens, and Witheringia meiantha), and pioneer seeds per square meter - seeds that found that seed extracts from species that germinate rapidly in response to gap formation. survive for long periods in the soil were indeed And because species richness is high even on more toxic to and fungi in the very small spatial scales (ca. 20-25 species per laboratory. The responsible chemicals in B. 625 cm2 sample), both intra- and interspecific frutescens were identified as three related competition for space in recent treefall gaps is alkaloids, all of which were much more intense. Murray and Garcia-C’s work showed concentrated in seeds than in leaf tissue. P. that spatial heterogeneity of the soil “seed bank” rivinoides and G. poasana contain chemicals was extremely high, however, so that toxic to fungi as well, but they remain as yet competitively inferior pioneer species were unidentified (Veldman et al. 2007, K. G. likely sometimes to germinate in gaps without Murray, unpublished data). Chemical defense any superior competitors nearby. This of pioneer plant seeds is thus clearly important, phenomenon, termed “recruitment limitation,” and much work remains to be done. can facilitate coexistence by reducing the {Nadkarni, 2009, Canopy Seed Banks as intensity of competition on ecologically relevant Time Capsules of Biodiversity in Pasture- spatial scales. Part of the spatial patchiness in Remnant Tree Crowns} found that the soils and the seed bank resulted from patchiness in the epiphyte mats that accumulate in tree canopies seed rain, but site-to-site differences in density also accumulate seed banks, just as do soils on and species composition were also magnified by the forest floor. Moreover, they surveyed such survival probabilities in the soil that varied by seed banks in the canopies of remnant pasture species. trees to determine whether such seed banks Despite the fact that the life histories of most might augment other effects that render remnant pioneers include a soil seed bank, Murray and trees effective “regeneration foci.” They found Garcia-C. found a wide range in the ability of that these seed banks contained dense and seeds to survive for long periods in the soil. diverse assemblages of seeds, including many Some, like Phytolacca rivinoides, Bocconia woody species characteristic of primary forest, frutescens, and Guettarda poasana, maintain and concluded that pasture canopy seed banks soil seed banks with densities several orders of could function as “time capsules” of forest magnitude higher than the annual seed rain, biodiversity that could speed forest regeneration suggesting that seeds survive in Monteverde’s recovery on pastures. Nadkarni and Haber also soil for tens to hundreds of years. In contrast, compared the seed banks in remnant tree other species of pioneers, like Cecropia canopies with those in primary forest tree polyphlebia and Urera elata, maintain soil seed canopies and in soils from the forest floor. Seed banks with only a year’s worth of seed rain, densities and species richness in forest floor suggesting high mortality rates. Only Hampea soils, but those from pasture and primary forest appendiculata and Piper umbellatum among the tree canopies did not differ from one another 23 species studied in detail did not maintain a Earlier work on plant-frugivore interactions seed bank at all. Results of replicated field at Monteverde demonstrated that some of the

most important fruit-eating birds migrated of the Tilaran Mountains`, Costa Rica} studied altitudinally, and suggested that these the occurrence of Bare-necked Umbrella birds at movements were driven by seasonal patterns in different elevations in the Monteverde-Arenal- fruit availability at different elevations. Since San Ramon region of the Cordillera de Tilaran, the publication of Nadkarni and Wheelwright and found that their movements over an (2000), these patterns have been further elevation range from 400-1400 m correlated to investigated by Chaves-Campos et al. (2003), seasonal patterns in fruit availability. And as Chaves-Campos (2004), Powell and Bjork with Bellbirds, elevations used for breeding (2004), and Papes et al. (2012). {Powell, 2004, were fairly well-protected, while those used Habitat linkages and the conservation of tropical outside the breeding season were not. Like Biodiversity as indicated by seasonal migrations {Powell, 2004, Habitat linkages and the of three-wattled bellbirds} elucidated the conservation of tropical Biodiversity as migratory patterns of Three-wattled Bellbirds in indicated by seasonal migrations of three- detail using radiotelemetry, and found that birds wattled bellbirds}, Chaves-Campos concluded breeding on the Atlantic slope of the Cordillera that the inadequacy of protected lands used de Tilaran crossed over to highly fragmented during the non-breeding season constituted a forest on the Pacific slope just 5-15 km away significant threat to the species in the region. after the breeding season. In September and {Chaves-Campos, 2004, Elevational October, they migrate to the lowlands of movements of large frugivorous birds and northeastern Costa Rica and southeastern temporal variation in abundance of fruits along Nicaragua, and in November and December they an elevational gradient} studied changes in the migrate to southwestern Costa Rica, where they abundances of large fruit-eating birds between remain until returning in March to the Atlantic 400 and 1400 meters elevation in the Cordillera slope near Monteverde to breed. Powell and de Tilaran in relation to the availability of fruits, Bjork suggested that the birds are following the and found mixed evidence that the migratory availability of their primary food sources (fruits movements of these birds are driven in large part in the family Lauraceae) as the fruiting seasons by fruit availability. Although small sample of species in different parts of the bellbird’s sizes and high variation among replicates made range wax and wane, rather than following an statistical comparisons difficult, Chaves-Campos invariant migratory route. Whatever the reason, suggested that migratory movements of these the four areas used over the annual cycle were birds were driven by fruit availability in the non- separated by as much as 280 km, and much of breeding season, but not during the breeding the land in three of the four areas (lowlands of season. northeastern and southwestern Costa Rica, and Most recently, {Papeş, 2012, - Vegetation middle elevations on the Pacific slope of Costa dynamics and avian seasonal migration: clues Rica near Monteverde) is highly fragmented and from remotely sensed vegetation indices and poorly protected. Powell and Bjork concluded ecological niche modelling} investigated the that the bellbird population (and hence the possibility of explaining bellbird movements on in which they perform important seed the basis of remote sensing data that could serve dispersal services) are thus vulnerable, despite as a proxy for forest canopy characteristics. adequate protection of the forests used during They generated ecological niche models based the breeding season. In part as a result of their on several remotely sensed vegetation indices work, the Costa Rican government and several that reflect seasonal changes in canopy structure private-sector organizations are cooperating to and productivity, but these did not explain create the Bellbird Biological Corridor, which seasonal bellbird movements in the Monteverde will protect a migratory corridor on the Pacific region reliably. Rather, these models suggested slope by promoting habitat restoration and that much of the Atlantic slope is suitable for protection, largely on privately held lands. breeding, but that factors other than vegetation Similarly, {Chaves-Campos, 2003, seasonality, e.g., lower rates of nest predation at Altitudinal movements and conservation of bare- middle elevations, may attract bellbirds to necked Umbrellabird Cephalopterus glabricollis middle elevations for breeding.

Animal-mediated seed dispersal and cattle pasture trees at Monteverde was demonstrated pasture regeneration directly by {Sheldon, 2013, The use of pasture Since Groom’s (2000) study of woody plant trees by birds in a tropical montane landscape in regeneration in abandoned pastures, much of the Monteverde`, Costa Rica}, who documented work on seed dispersal at Monteverde has over 900 visits by 52 species in 20 different concerned the role that such dispersal by animals families to just one common pasture tree species plays in pasture regeneration. Cattle production ( glandulosum). They also found that the now occupies over 27% of rural land area in size of the tree, its degree of isolation from other Latin America ({Murgueitio, 2011, Native trees trees, and the size of its epiphyte load increased and shrubs for the productive rehabilitation of bird visitation. Surprisingly, Murray et al. (2008) tropical cattle ranching lands}, yet the ultimate found that wind-dispersed remnant trees were fate of most pasture lands is abandonment or just as effective as recruitment foci for animal- conversion to some other use, often via dispersed colonists as were trees that themselves regeneration to forest. Much of the work on produced fleshy fruits sought by animals, pasture regeneration concerns the physical and presumably because seed dispersers are also biological barriers that limit the rate and attracted to the elevated perch sites, cover, and constrain the trajectory of regeneration (e.g., perhaps insect food resources that such trees {Holl, 2000, Tropical Montane Forest provide. Restoration in Costa Rica: Overcoming Barriers Murray and colleagues also tracked the to Dispersal and Establishment}, and since progress of regeneration to determine how the limited seed availability is one of the more spatial and compositional patterns of regrowth obvious factors, many have concentratd on the that were initiated by seed dispersers changed roles that seed dispersing animals play in over time. As has been found elsewhere (e.g., transporting seeds from surrounding forest into {Schlawin, 2008, 'Nucleating’ succession in pastures. recovering neotropical wet forests: The legacy {Murray, 2008, The roles of disperser of remnant trees}, the concentration of pasture behavior and physical habitat structure in colonists beneath remnant trees formed regeneration of post-agricultural fields} reported “recruitment foci” or “nucleation sites” for on a long-term study of regeneration in two forest plant species. Subsequent censuses of the pastures near the MCFP, and found that nearly same and similar plots 14 and 30 years post- all early colonization by woody plants with abandonment showed that the initial strong animal-dispersed seeds was beneath the crowns effect of remnant trees on the density and of bordering trees and “forest remnant” trees that species richness of regeneration became weaker were left standing in the pasture when it was over time – by 30 years post-abandonment, both created. In contrast, wind-dispersed species density and species richness of pasture colonists colonized areas without overhanging vegetation was just as high in parts of the original pasture just as frequently as areas beneath remnant trees. that had lacked overhanging tree crowns as in Concentration of early colonists beneath areas beneath remnant trees. The reason, of remnant trees or planted “tree islands” has been course, was that as the pasture colonists grew found in many other studies as well (e.g., and formed expanding islands of regenerating {Sandor, 2014, Remnant Trees Affect Species forest centered on the original remnant trees, the Composition but Not Structure of Tropical colonists themselves served as perch sites for Second-Growth Forest} and references cited animals carrying seeds and the land area without therein; {Zahawi, 2006, Tropical forest overhanging tree crowns decreased to zero. restoration: Tree islands as recruitment foci in The work of {Harvey, 2000, degraded lands of Honduras} – a pattern that COLONIZATION OF AGRICULTURAL results in part from the attraction of forest birds WINDBREAKS BY FOREST TREES: to habitats with greater structural complexity EFFECTS OF CONNECTIVITY AND and in part to the tendency of birds to defecate REMNANT TREES;Harvey, 2000, and regurgitate seeds while perched rather than WINDBREAKS ENHANCE SEED in flight. The attraction of birds to isolated DISPERSAL INTO AGRICULTURAL

LANDSCAPES IN MONTEVERDE`, COSTA diverse assemblages of seeds, including many RICA} in planted windbreaks between active woody species characteristic of primary forest pastures in the Monteverde region also and concluded that pasture canopy seed banks demonstrates the importance of animal seed could function as “time capsules” of forest dispersers in forest regeneration in agricultural biodiversity that could speed forest regeneration landscapes. As was the case for remnant trees, on abandoned pastures. the seed rain of woody species beneath Clearly, both remnant trees and windbreaks windbreaks was orders of magnitude more dense facilitate forest regeneration in agricultural and far more diverse than in pasture just 5 landscapes at Monteverde and elsewhere, largely meters away (Harvey 2000a). Bird-dispersed because of the interaction of their physical species predominated, but pastures received structure with the behavior of dispersers – almost as many bat-dispersed seeds as especially birds. These patterns highlight both windbreaks, perhaps because bats defecate in the importance of maintaining healthy disperser flight as well as when perched. Harvey (2000b) populations as well as managing landscape also studied colonization of windbreaks and features such as pasture size and composition, so adjacent pastures by surveying seedlings of as to maintain the interactions that facilitate forest plants recruited into them, and in many forest regeneration. ways her findings parallel those of Harvey (2000a): forest plants readily recruited into Fig biology windbreaks, especially those forest plants Figs remain a subject of fascination to dispersed by birds. Moreover, both density and biologists, especially those who work in the diversity of colonists was significantly higher in tropics. Our understanding of figs’ complex windbreaks connected to adjacent forest patches interactions with other species has been than in those not so connected. reviewed most recently by Herre et al. 2008, but Neither Harvey (2000a,b), Murray et al. new information continues to accumulate at a (2008), nor Sheldon and Nadkarni (2013b) rapid pace. Yet, in spite of growing worldwide found any correlation between seed input, recruit interest in figs, no publications have appeared density or bird visitation with distance to the over the past fifteen years describing research nearest forest edge, perhaps because the pastures carried out at Monteverde. pertusa, which typical of the region are relatively small – rarely has attracted the great majority of attention in more than a few hundreds of meters across. Monteverde, has been studied a little more Neither did {Aide, 1996, Forest recovery in elsewhere in Costa Rica as well as in Mexico abandoned cattle pastures along an elevational and Brazil, mostly in the context of its flowering gradient in northeastern Puerto Rico}) in Puerto phenology and seed dispersal. Ficus yoponensis Rico, where pastures are also relatively small. remains a species of great interest to researchers In regions like Amazonia, however, where at Barro Colorado, Panama, where it is pastures can be kilometers across, distance consumed heavily by bats that act as highly effects may be common. {DaSilva, 1996, Plant effective seed dispersers (Heer et al. 2010). succession`, landscape management`, and the Ficus tuerckheimii, F. crassiuscula, and F. ecology of frugivorous birds in abandoned velutina remain little-studied from the Amazonian pastures}), for example, found that pollination and seed dispersal perspective. even tanagers that frequent the forest/pasture It is particularly unfortunate that F. boundary rarely travel more than 150 meters into tuerckheimii has not attracted more attention, pasture. because it offers one of the clearest exceptions Nadkarni and Haber (2009) elucidated to a major piece of conventional wisdom about another way in which remnant pasture trees may figs: that every one of the >750 fig species has a act as effective regeneration foci and thereby unique pollinator. As Ramirez (1970) first facilitate forest regeneration on abandoned showed and several unpublished undergraduate pastures: via the seed banks that accumulate in course projects in Monteverde have followed up soils and epiphyte mats in the canopies of on, F. tuerckheimii has two pollinators (not “no” remnant pasture trees. They found dense and as the original text of this chapter erroneously

states), often cohabiting a single fig appear regularly (e.g., Herre et al. 2008, Jandér . They are easily distinguished by et al. 2012). color: Pegoscapus carlosi is black and P. mariae Work has accelerated in recent years yellow. New molecular data that allow fig wasps documenting seed dispersal and the dominant that appear identical to the human eye to be role fig fruits play in the diets of tropical discriminated have made it clear that F. vertebrates. A comprehensive review of fig tuerckheimii may not be that unusual in hosting consumers worldwide is now available multiple pollinators (Marussich and Machado (Shanahan et al. 2001), as is a detailed 2007). Conversely, certain pairs of fig species investigation of how fig fruit characteristics are now known to share a single pollinator (Moe have evolved in suites or “syndromes” et al. 2011). Overturning a related assumption - (Lomascolo et al. 2010). Intriguing geographical that figs and fig wasps must usually speciate differences within individual fig species together, given that there are hundreds of mostly continue to appear and still remain to be one-to-one interactions - reconstruction of explored. For example, new work finds F. evolutionary relationships using molecular data pertusa seeds to be abundant in bat droppings in reveals a much messier picture (Machado et al. Brazil (Teixiera et al. 2009), suggesting a 2005, Lopez-Vaamonde et al. 2009). However, primary role for bats as seed dispersers there. how speciation occurs and how associations This is consistent with observations from between particular pairs of fig and pollinator Panama, but distinctly different from species arise remain unresolved (Cook et al. Monteverde, where bats reject the red-ripe fruits. 2010). Ecologists increasingly identify figs as The most surprising change in our ecological keystone resources for fruit consumers. The understanding of the fig pollination mutualism is health of fig populations worldwide is, however, that developing fig wasps do not, as was threatened by habitat loss, habitat fragmentation, believed for over a century, consume fig seeds. and selective harvest for wood (e.g., Felton et al. Rather, before laying an egg, a female 2013). Furthermore, invasive frugivores deplete deposits a secretion that transforms an ovule into fruits essential to the well-being of native a gall; her offspring feeds upon sterile tissue vertebrates, while at the same time failing to (Jousselin and Kjellberg 2001, Martinson et al. disperse fig seeds in a germinable condition 2013). This leads to the obvious question of why (Staddon et al. 2010). There is a pressing need to these wasps transfer pollen at all, given that their treat figs as key targets for tropical conservation. offspring don’t eat seeds! There is some They may also hold promising roles for forest evidence that in seedless figs, wasp larvae restoration. develop very poorly (Jousselin et al. 2003). These and earlier studies at Monteverde Thus, regardless of their diet, active pollination highlight both the complexity of the interactions by the mother does appear to increase the among mutualists and their role in the success of her offspring. Even though fig wasp maintenance of whole ecological communities. larvae don’t consume seeds, each one still As important, they demonstrate how important it develops within an ovule that would otherwise is to base conservation planning on sound produce a seed. It remains unresolved why fig knowledge about the natural history of the wasps don’t lay eggs in every ovule, which organisms involved. Going forward, we hope would appear to benefit fig wasps in the short that biologists will continue to be drawn to run but which could lead to the demise of fig Monteverde both for the opportunity to reproduction and the extinction of both partners understand the natural world better and to satisfy in the long run. New ideas for how this uneasy their own need to preserve a particularly worthy relationship can persist over evolutionary time corner of it.

Literature Cited