Selbyana 33(1): 1–15. 2019. EATING OUT OR DINING IN: INSECT-PLANT INTERACTIONS AMONG SEVERAL SPECIES OF PIPER IN THE RIO ABAJO FOREST PRESERVE, PUERTO RICO 1 2 3 CHRISTA WISNIEWSKI , ALLAN J. BORNSTEIN *, DIANE L. WOOD 1Burns & McDonnell Engineering Company, Inc, 9400 Ward Parkway, Kansas City, MO 64114, USA 2Department of Biology, Southeast Missouri State University, One University Plaza, Cape Girardeau, MO 63701, USA; E-mail: [email protected] 3Department of Biology, Southeast Missouri State University, One University Plaza, Cape Girardeau, MO 63701, USA Abstract Pollination activity was investigated for Piper glabrescens, Piper hispidum, Piper jacquemontianum, and Piper umbellatum, common species in the Rio Abajo Forest Preserve in Puerto Rico. During observation periods, the main floral visitors were syrphid and drosophilid flies, which suggests they play a prominent role as potential pollen vectors for these four species. In addition, two ant species (Linepithema iniquum and Wasmannia auropunctata) were observed to nest in the stems of three Piper species (Piper abajoense, Piper aduncum, and Piper umbellatum). In the case of Piper umbellatum, this interaction is the first documentation of an ant-plant association in Piper section Pothomorphe. Key words: Piperaceae, Pollination, Syrphidae, Ant-plant interaction, Formicidae * Corresponding Author Wisniewski et al.: Insect-plant interactions of Piper 2 the Atlantic forest of Brazil (Vargas-Rojas Introduction and Vieira 2017). Multiple studies have addressed From a morphological perspective, insect-plant interactions involving Neo- individual flowers of Piper L. are small tropical pipers (genus Piper L., family and lack the perianth parts (or nectar) that Piperaceae), including herbivory (e.g., traditionally function to attract insects. Marquis 1990, 1991; Dyer et al. 2003, Therefore, insects visit Piper flowers to 2004, 2010; Letourneau 2004), pollination gather pollen, undoubtedly attracted by (e.g., Semple 1974; Fleming 1985; de the usually white to yellowish flowers Figueiredo and Sazima 2000, 2004; clustered together in large numbers to Kikuchi et al. 2007; Vargas-Rojas and produce elongate, spike-like inflores- Vieira 2017), and ant habitation (e.g., cences. With rare exception, Neotropical Risch et al. 1977; Letourneau 1998; species of Piper have bisexual flowers, Fischer et al. 2002; Tepe et al. 2004, which may explain their ability to self- 2007a, 2007b, 2009, 2014). pollinate, but those species studied in With respect to pollination biology, detail display some degree of dichogamy, available research suggests that insects, either protandry or protogyny (Martin and wind, and selfing play a role for Gregory 1962; de Figueiredo and Sazima Neotropical Piper. For example, Semple 2000; Kikuchi et al. 2007; Valentin-Silva (1974) found that several bee species of et al. 2015; Vargas-Rojas and Vieira the genus Trigona (Jurine) and some 2017), which presumably limits selfing to beetles were pollinators of various Piper some extent. spp. in Costa Rica. Similarly, Fleming Holldobler and Wilson (1990) (1985) discovered that Trigona bees, indicate that the predominant evidence for along with syrphid flies, were the main myrmecophily is the presence of plant pollinators in his study of five Piper structures that serve as domatia, but not species in Costa Rica. During his study of all ant affiliations are necessarily P. arieianum C. DC. in Costa Rica, symbiotic due to the opportunistic nature Marquis (1988) observed pollinators that of ants. A total of 11 Piper species from included 15 species of Diptera and Central and South America are known to Hymenoptera. For some pipers in harbor nesting ants (Burger 1972; Risch et southeastern Brazil, de Figueiredo and al. 1977; Tepe et al. 2004, 2009, 2014). Sazima (2000) observed that hoverflies Several ant species have been noted to and bees were common visitors and inhabit Piper spp. (Risch et al. 1977; therefore likely pollinators, but concluded Holldobler and Wilson 1990; Tepe et al. that wind was also a factor. In their study 2004, 2014; Muñoz et al. 2012), but of Piper dilatatum L.C. Rich. on Barro Pheidole (Westwood) appears to be the Colorado Island, Panama, Kikuchi et al. predominant genus, with Pheidole (2007) also determined that syrphids, bicornis (Forel) the principal species halictids, and stingless bees (e.g., Trigona (Letourneau 2004). Many of the nesting spp.) were the most likely pollinators, and ants establish colonies in petiolar cavities, that their activity, especially the bee stems, or both (Burger 1972; Risch et al. species, leads to significant levels of 1977; Letourneau 2004; Tepe et al. 2004, geitonogamy. Various bees [e.g., Apis 2009, 2014). In Piper cenocladum C. DC., mellifera (L.) and Melipona (Illiger) spp.] P. fimbriulatum C. DC., and P. and syrphids [especially Ocyptamus sagittifolium C. DC., Pheidole spp. (Macquart) spp.] were common visitors initially established nests in the petiolar based on a study of P. caldense C. DC. in cavities and, as the colony increased in SELBYANA Volume 33(1) 2019 Wisniewski et al.: Insect-plant interactions of Piper 3 size, entered and excavated the stem at the Materials and Methods base of the petiolar cavity (Risch et al. Study Site 1977). Obviously, Pheidole spp., as well This study was conducted in the Río as other ant species, are benefiting from Abajo Forest Reserve in Puerto Rico, nesting sites provided by various Piper located south of Arecibo, in the karst species. Additionally, several Piper spp. region. The reserve was established in are known to provide nutrients in the form 1935 on land that had previously been of single-celled food (pearl) bodies (Risch deforested (Acevedo-Rodriguez and et al. 1977; Fischer et al. 2002), which Axelrod 1999). The main ecosystems that occur, depending on the species, either on have been re-established in the reserve are the inner surface of the petiolar sheath tropical and subtropical forests (Acevedo- (Risch et al. 1977) or on the surface of the Rodriguez and Axelrod 1999). stem cavity (Tepe et al. 2009). There are 11 known Piper species in The occurrence of ants in young this area, including P. abajoense Bornst, Piper stems is facilitated by the general P. aduncum L., P. amalago L., P. lack of woodiness, with only the blattarum Spreng., P. glabrescens (Miq.) outermost, peripheral ring of vascular C. DC., P. hispidum Sw., P. jacque- bundles producing any noticeable montianum Kunth, P. marginatum Jacq., secondary tissues (Tepe et al. 2007a). This P. peltatum L., P. swartzianum (Miq.) C. means that a significant portion of the DC., and P. umbellatum L. As currently young stems consists of soft, circumscribed, most of these species are parenchymatous tissue, including the pith widely distributed in the Neotropics, region excavated for occupancy. Although except for the endemic P. abajoense there are some medullary vascular bundles (Puerto Rico), P. blattarum (Puerto Rico), in the pith, as well as a sclerenchymatous and P. swartzianum (Dominican Republic ring that separates the pith from the cortex + Puerto Rico). Although these 11 species (Tepe et al. 2007a), these features do not co-occur in the area, and previous appear to significantly deter insect collection labels indicate that many of activity. In addition, myrmecophytic them should be in flower simultaneously species of Piper studied anatomically at various times throughout the year, the have fewer raphides (needle-shaped pollination study was limited to those crystals) and starch grains in the pith species in flowering condition and present region (Tepe et al. 2007a), further in sufficient abundance during the time of facilitating excavation activity. the study; these species were P. To date, all of the studies concerning glabrescens, P. hispidum, P. jacque- Neotropical Piper pollination and ant montianum, and P. umbellatum. interactions have involved mainland Sampling Protocol species. However, insect (and plant) The first field season occurred from species often have limited distributions, so 5–10 January 2013, and prior to the first it is important to examine possible inter- full field day the best methods, times, and actions in different regions of the world. locations for examining species of Piper Therefore, the intent of this study was to and collecting potential pollinators were observe insect visitors to the inflores- determined. A second field season cences of Piper, and to document any ants occurred from 1–5 June 2013 to see if nesting in the stems of available Piper different pollinators might be active at species to compare the Puerto Rican insect that time. During both observation -Piper interactions with those of the periods, the time of day for peak insect mainland species. SELBYANA Volume 33(1) 2019 Wisniewski et al.: Insect-plant interactions of Piper 4 activity was determined to be from 10 insect visitors because field identification a.m. to 3 p.m. Collecting was conducted for many taxa to the level of genus or during these times to ensure that species is difficult. Additionally, some representative insect visitors were insects were purposely not collected in sufficiently documented. order to observe their basic behavior (e.g., how they moved along a given During the January collection period, inflorescence). P. glabrescens and P. umbellatum were in flower and abundant; a total of ca. 60 Plants were also visually inspected hours of collecting/observing occurred for for the presence of ants nesting in the the former species and ca. 30 hours for the