RESEARCH Ancient Termite Pollinator of Milkweed Flowers in Dominican Amber Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021 GEORGE O. POINAR, JR. hen we think of pollinators, bees are the first things considered separate families, rather than subfamilies included that come to mind. However, there are many other within the Apocynaceae. While the overlap in morphological Wless obvious pollinators in the insect world, many of structure of the pollinia in these groups can be similar, the which pollinate tropical flowers we never knew existed. When we manner by which they attach their pollinaria to the pollinator think of termites, the first thing that comes to mind is the terrible differs. While the orchids typically attach their pollinaria by a damage they can do to our homes. We never think of termites sticky pad (viscidium) (Dressler 1993; Poinar 2016a, 2016b), the as visiting flowers and especially not pollinating them, which milkweeds normally use a slender, more or less rigid structure makes the present discovery so interesting. Embedded in a piece called a corpusculum that is usually sutured along the outer of Dominican amber is a harvester termite (Isoptera: Termitidae) surface, but smooth on the inner surface, to attach their pol- with a pollinarium from an adjacent milkweed flower attached linia to insects (Swarupanandan et al. 1996)(Fig. 1). Milkweed to its head. Such an association is completely unknown today. pollinia and pollinaria vary in structure among different ascle- Currently, there are two major plant families that distribute piad lineages: pollinia of the common milkweed, Asclepias their pollen in little sacs called pollinia for attachment to insects: syriaca L., which are often found attached to the mouthparts orchids (Orchidoideae and Epidendroideae) and milkweeds of honeybees, are rather slender, while others such as the fossil (Asclepiadoideae). Also possessing pollinia are members of pollinia attached to the termite are more swollen. the Periplocoideae and Secamonoideae, if those lineages are The fossil termite adjacent to the milkweed flower in Domini- can amber carries pollinia that match those found in the stigmat- ic cavity of the flower, thus establishing termites as pollinators of ancient lineages of the Asclepiadoideae in the mid-Tertiary. The flower, which represents the first fossil milkweed flower, is described below, and ways in which the termite may have acquired the pollinia are discussed. Materials and Methods The fossil flower originated from amber mines in the northern mountain range (Cordillera Septentrional) of the Dominican Republic between Puerto Plata and Santiago. Amber from mines in this region was produced by Hymenaea protera Poinar (1991) (Fabaceae), and based on the recovered biota, the origi- nal habitat was characterized as a tropical moist forest (Poinar and Poinar 1999). Ages range from 20–15 mya based on Foraminifera (Itur- ralde-Vinent and MacPhee 1996) and 45–30 mya based on coccoliths (Cêpek in Schlee 1990). These are minimum dates, since most of the amber was secondarily deposited in turbid- itic sandstones of the Upper Eocene to Lower Miocene Mamey Group (Draper et al. 1994) and the length of time it took to re-deposit it is unknown. Observations and photographs were made with a Nikon SMZ- 10 R stereoscopic microscope and Nikon Optiphot compound Fig. 1. Extant pollinarium of Asclepias syriaca L. attached to the mouth- parts of a honeybee (Apis mellifera: Apidae: Hymenoptera). C = corpus- microscope with magnifications up to 800 X. Helicon Focus Pro culum, T = translator arm; P = pollinium. X64 was used to stack photos for better clarity and depth of field. 52 American Entomologist • Spring 2017 Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021 Fig. 2. Lateral view of holotype of Discoflorus neotropicus gen. & sp. n. in Dominican amber. C = hirsute basal portion of coronal column; L = tips of coronal scales; T = termite. Scale bar = 1.8 mm. Fig. 4. A. Gynostegium of Discoflorus neotropicus gen. & sp. n. in Domin- ican amber showing the ten-lobed stigmatic disk. Arrows show tips of three coronal scales. Scale bar = 0.6 mm. B. Diagrammatic drawing of Fig. 3. Bottom of holotype of Discoflorus neotropicus gen. & sp. n. the gynostegium of Discoflorus neotropicus gen. & sp. n. showing the in Dominican amber. C = calyx tube; Pe = peduncle, P = petal. Scale ten-lobed stigmatic disk (white), ten locules of the five anthers (black), bar = 1.2 mm. and tips of the ten corona scales (stippled). Description Diagnosis. Flower perfect, actinomorphic, with a five-lobed Family Apocynaceae short calyx with sepals united at base, a five-parted rotate corolla Subfamily Asclepiadoideae with five equal to subequal, separate petals, five fertile stamens with bilocular, broadly oblong anthers adherent to a ten-lobed Discoflorus gen. n. stigmatic disk and a ten-scaled coronal tube forming a gynoste- Type species: Discoflorus neotropicus gen. n., sp. n. gium (Figs. 2-4). Locules of the five anthers positioned between Diagnosis: As for the type species (monotypic) every lobe of the stigmatic disk (Fig. 4). Tips of coronal scales are free, surround and barely surpass the peltate five-parted Discoflorus neotropicus gen. n., sp. n. (Figs. 2-9). stigma (Fig. 4). Pollinaria in stigmatic cavities were composed Etymology: The generic name is from the Latin “discora”= dif- of a corpusculum, translator arms and a fractured pollinium ferent and the Latin “floris” = blossom. Etymology—The spe- with some released pollen grains (Fig. 5). The slender corpus- cific epithet indicates the geographical location of the fossil. culum was sutured along the entire length of the outer surface. Type: Holotype in the Poinar amber collection maintained at Description. Flower perfect, small, with short calyx; sepals Oregon State University (Cat. No. Sd-9-46). united at base; corolla rotate, with five equal or subequal, sepa- Type locality: Amber mine (La Búcara) in the northern moun- rate petals with three reflexed and two upturned; stamens five, tain ranges (Cordillera Septentrional) of the Dominican anthers bilocular, broadly oblong, adherent with stigma head Republic (DD 19.4 by 70.4). and forming a gynostegium; corona composed of ten hirsute American Entomologist • Volume 63, Number 1 53 column at base, 2.0 mm; length calyx 0.6 mm; length calyx lobes, 0.3-0.4 mm; length petals, 3.1-3.3 mm; width petals at base, 0.9-1.3 mm; diameter of stigma head, 1.4 mm; length of anthers, 340 µm; length pollinium translator arm, 90 µm; length corpuscula, 90-120 µm; greatest dimension of pollinium on termite head, 223 µm; diameter of pollen grains, 18-22 µm. Associated termite. A pollinarium with four pollinia is attached to the head of a 5 mm worker forager termite (Ter- mitidae: Isoptera) adjacent to the flower (Fig. 6). The corpus- culum is attached to the labrum and four adjacent pollinia are resting on the post-clypeus (Figs. 7-10). Pollinia size and shape vary greatly in the Asclepiadoideae; however, features of the fossil pollinia fall within the range of those depicted in Swarupanandan et al. (1996). The size and shape of the cor- Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021 puscula and the diameter of the pollen grains in the flower head are similar to those on the termite, and the pollinaria on the termite are considered to have originated from Discoflorus neotropicus gen. & sp. n. While two intact pollinia are clearly Fig. 5. Detail of corpusculum (C), part of translator arm (T), and pollen visible on the post-clypeus of the termite (Figs. 6-8), the outer grains (P) from a ruptured pollinium in the stigmatic chamber of Disco- two are broken and reduced in size (Fig. 9). florus neotropicus gen. & sp. n. in Dominican amber. Scale bar = 95 µm. Remarks. Of the nine extant genera of asclepiads in Hispan- iola (Liogier 1994), Discoflorus neotropicus gen. & sp. n. most scales mostly united into a column that surrounds the filaments closely resembles members of the genus Metastelma R. Br., and gynoecium. Tips of coronal scales free, surrounding and in particular M. parviflorium (Sw.) Roem. & Schult. that has barely surpassing the peltate five-parted stigma. Stigma disk small flowers, a long-stipitate gynostegium and linear-spat- ten-lobed with locules of the five anthers positioned between ulate corona scales as long as the gynostegium. However, in every lobe. Ovary and style hidden from view. Metastelma, the corona has only five scales and the stigmatic Floral measurements. Length entire flower, 2.7 mm; length disk (gynostegium) is five-lobed, which is the normal condi- peduncle, 1.6 mm, length united portion of coronal column, tion in flowers of the Asclepiadoideae (Endress and Bruyns 1.8 mm; length free portion of coronal scales, 1.0 mm; width 2000; Endress 1994). In Discoflorus neotropicus gen. & sp. n., Fig. 6. Forager termite adjacent to the flower of Discoflorus neotropi- Fig. 7. Dorsal view of head of forager termite with two attached pol- cus gen. & sp. n. in Dominican amber. Arrow shows location of pollinia linia (P) of Discoflorus neotropicus gen. & sp. n. in Dominican amber. attached to termite head. Scale bar = 0.8 mm. Scale bar = 0.37 mm. 54 American Entomologist • Spring 2017 Downloaded from https://academic.oup.com/ae/article/63/1/52/3062818 by guest on 28 September 2021 Fig. 9. Detail of four pollinia (arrows) of Discoflorus neotropicus gen. & sp. n. attached to termite head in Dominican amber. The two inner pol- linia are entire, but the two outer pollinia are partial. Scale bar = 130 µm. Fig. 8. Frontal view of forager termite in Dominican amber with two attached entire pollinia (P) of Discoflorus neotropicus gen.