Mutualism between Senita Cacti and Senita Moths

During the 1995 and 1996 field studies in the Sonoran Desert, Dr. Ted Fleming (University of Miami) and I discovered the third known pollinating seed-consuming mutualism involving active pollination. This mutualism between senita cacti and senita moths parallels, both ecologically and evolutionarily, the other two classic coevolved mutualisms of yucca/yucca moth and fig/fig wasp interactions. Other pollinating seed-eating interactions are known to occur, including globeflowers/flies, Lithophragma/Greya moth, Silene/Hadena moth, and Glochidion/Epicephala moth interactions, but only senita, yucca, and fig systems are known to involve the evolution of active pollination. The obligate pollinating seed-consuming mutualism between senita cacti and senita moths is a mutualism that entails both benefits and costs to both the plant and pollinator. Senita cacti benefit from pollination, but incur costs due to larval fruit consumption. Senita moths benefit from fruit food resources, but incur costs to larval survival from fruit abortions.

Both senita cacti and senita moths are endemic and geographically restricted to the Sonoran Desert of North America. They are distributed throughout Baja California and Sonora in Mexico, but only occur in Organ Pipe Cactus National Monument in Arizona within the United States. There are two species of senita, Pachycereus schottii and P. gatesii (formerly Lophocereus schottii and L. gatesii), with only one locale of P. gatesii at the southern tip of Baja California.

Senita is a long-lived (>75 years) columnar cactus that produces many 2-4 m stems radiating from its base. Once plants reach reproductive maturity, they typically flower every year. Ribs along stems bear many areoles (spine bearing reproductive pads) that can produce one or more whitish-pink flowers per night. Senita can produce upwards of 3,000 flowers during its flowering seasons from April-August. Flowers open and anthers dehisce at sunset, they close within 12 hours, and are pollinated only while open. Senita cacti are entirely self-incompatible, obligate outcrossers. Hermaphroditic flowers have an inferior ovary containing one pistil, many ovules, and hundreds of anthers. Only 50% of flowers produce any nectar at all, with an average 0.5 ml in nectar producing flowers. Pollinated flowers that set fruit usually produce mature fruit within 30 days, and contain on average 180 seeds per fruit.

The senita moth, Upiga virescens, is a small moth with forewings 8-10 mm in length. It is in the subfamily Glaphyriinae and is the only species in its genus. Until recently, the only report of U. virescens was its species account. All life stages of U. virescens are associated only with senita cacti. Larval growth consistently conforms to Dyar's rule, but unlike other Lepidoptera, only three larval instars have been identified. Adult moths mate on spines, female moths oviposit in flowers, larvae consume immature fruit, and pupation occurs in cactus stems.

Senita moths can commonly been seen mating on spines of senita cacti. Both male and female moths visit flowers for nectar, though most often flowers contain little to no nectar. Unlike male moths, however, female moths have a fairly elaborate and consistent set of behaviors and activities they exhibit during flower visitation. Immediately following sunset, female moths actively collect pollen from flowers using their pollen brush, a presumably morphological adaptation consisting of elongated scales on the ventral side of only female abdomens. The pollen brush facilitates the collection, adhesion, and transport of pollen grains (pg in adjacent picture) among flowers. After collecting pollen, moths depart that flower and presumably fly to another plant, as senita cacti are entirely self-incompatible.

Upon arriving at a flower that has not already been oviposited, as female moths avoid such flowers, female moths first exhibit a presumably adaptive behavior which has become known as active pollination among yucca moths and fig wasps. For senita moths, this first behavior of flower visitation consists of climbing onto the flower's stigma in a head-down position and actively rubbing her abdomen onto the lobed stigma, thereby transferring pollen grains from her abdomenal pollen brush to the stigma. In doing so, senita moths actively pollinate flowers, rather than passively pollinating them by incidentally bumping into stigmas and transferring pollen while obtaining a food resource (nectar, pollen), as is the case with almost all pollinators. While senita moths, yucca moths, and fig wasps each have their own unique active pollination behaviors, these insects are the only three groups of animals known in nature to exhibit active pollination behavior.

Following active pollination, female moths then oviposit a single egg on the flower she has just pollinated. In most cases, eggs are laid on the tips of flower petals, but they can also occur among anthers and within corolla tubes. By actively pollinating flowers, senita moths facilitate the survival of their offspring by increasing the likelihood of fruit set, as eggs and larvae in aborting flowers and fruit die. Before departing a flower, female moths actively collect pollen. In some cases, female moths attempt to nectar, either for a few minutes or for over an hour.

Within a few hours to 2-3 days after being laid, eggs hatch and larvae move down wilting corolla tubes toward the fruit's developing ovary. Larvae then bore into the fruit, consume developing ovules, and exit the base of the fruit and bore into the cactus stem where pupation occurs. This entire process, from oviposition to pupation, can be as short as one month. Not all eggs laid in flowers produce new adult moths, however, as many eggs and larvae die due to fruit abortions resulting from resource-limited fruit set in senita cacti.

Senita moths are typically abundant enough that their pollination does not limit seed or fruit production. While senita cacti rely almost entirely upon senita moths for reproduction, a few diurnal co-pollinators (halictid bees) do occur, but only very rarely do they make significant contributions to fruit set and plant reproduction.