Exceptional Species Diversity of Drosophilidae (Diptera) in a Neotropical Forest Author Grimaldi, David A. Author Richenbacher, Courtney text American Museum Novitates 2023 2023-05-10 2023 3997 1 28 https://bioone.org/journals/american-museum-novitates/volume-2023/issue-3997/3997.1/Exceptional-Species-Diversity-of-Drosophilidae-Diptera-in-a-Neotropical-Forest/10.1206/3997.1.full journal article 10.1206/3997.1 0003-0082 Drosophila SUBGENUS Drosophila (fig. 6): As expected, the number of Drosophila individuals was larger than for any other group in the study, some 659 specimens . Neotropical Drosophila are very diverse and very abundant at fallen fruits and flowers, on leaf litter and forest fungi. Although specimens were not databased as such, species groups represented in the samples include the annulimana , bromeliae , calloptera , canalinea , cardini , castanea , flavopilosa , guarani , mesophragmatica , onycophora , repleta , and tripunctata groups, as well as many ungrouped species. The most abundant species were captured by diverse methods. For example, the 20 most abundant ones were captured using an average of four to five sampling methods, the next 20 an average of 2.8 sampling methods. Seventy percent of the rarest species (< 4 specimens ) were captured only in Malaise traps. There were four very surprising results. First, species diversity is far greater than expected. With 141 species, Drosophila is 2.4× more diverse than the second-most diverse group at Zurquí, Zygothrica (see below). Many of the species were rare: 81 species (57%) are represented by five or fewer specimens. Possible explanations for such rare diversity are provided in the Discussion. Second, Malaise traps captured all but six of the 141 species, and nearly half (68 species) were collected exclusively in Malaise traps. Conversely, bait traps captured only 25 species (17%), as well as a small proportion of the individuals. It needs to be emphasized that only a small portion of the two most abundant D. ( Drosophila ) , sp. 1 and sp. 2, were mounted, so their total abundance is undercounted here (fig. 6). This is, nonetheless, a stark example of how many Drosophila species are missed by using just the standard collecting method of drosophilists, bait trapping. This explains the relatively low diversity of Drosophila in other surveys that used bait trapping exclusively (e.g., Monteiro et al., 2016 ; Duarte et al., 2018 ). Third, a significant number of species were captured at light traps (28, or 19%) and at emergence traps (19 species, or 13%) (nine species were captured at both). For species captured at lights there appeared to be a strong relationship between overall abundance of a species and the number at light: some of the more common species had larger proportions of individuals at light—a relationship that did not seem to pertain to the emergence-trap samples. Species in emergence traps were probably breeding in humus, on mycelia, or fallen, decaying fruits and flowers. Fourth, there were no specimens of the invasive Drosophila species that are so common worldwide, despite the Zurquí site being at the very edge of disturbed land and partially surrounded by pasture. Invasives found in abundance in Costa Rican lowlands include D. ( Sophophora ) melanogaster , simulans , malerkotliana , and suzukii , as well as D . ( Drosophila ) immigrans , hydei , and repleta . The wet, misty, cool weather at Zurquí probably limits the altitudinal dispersal of these species. SUBGENUS Sophophora (fig. 7): This group is taxonomically treated as a subgenus of the genus Drosophila , even though Sophophora and the nominal subgenus are not closely related based on both morphology ( Throckmorton, 1962 , 1975 ; Grimaldi, 1990a ) and genetics (e.g., Finet et al., 2021 ). Sophophora is a monophyletic group, as are the two species groups in it that are endemic to the neotropics (the willistoni and saltans groups). Species of Sophophora are classified into seven major species groups and several smaller ones. The center of diversity is the paleotropics, especially Southeast Asia and New Guinea , where hundreds of species in the melanogaster and montium species groups occur. Neotropical diversity is relatively modest, with three species groups (two of them endemic): willistoni group (neotropical only; 24 species total, 12 in Central America), saltans group (neotropical only, 23 species total, 10 in Central America), and the obscura group (a mostly Holarctic group of 45 species, five of them in Central America). All three groups have been intensively surveyed for studies in evolutionary biology (e.g., Lakovaara and Saura, 1982 ; Ehrman and Powell, 1982 ; Roman et al., 2022 ), so there appear to be few undescribed Neotropical species. The willistoni and saltans groups are sister groups; species in both groups breed in fallen, decaying fruits. Some species in the willistoni group can be very abundant at fruit falls in neotropical forests (e.g., Drosophila nebulosa ); saltans group flies are rarely abundant. No obscura group specimens were collected at Zurquí despite the appropriate elevation; these flies prefer the higher, cooler altitudes like Zurquí. Of a total of 27 species of Sophophora known for Central America 16 were found at Zurquí. Sophophora were extremely abundant at Zurquí (N = 551 specimens ), but this is due to two very abundant species (spp. 1 and 2: fig. 7), which comprised 72% of all Sophophora specimens. Again, it needs to be emphasized that only a small portion of these two species were mounted, so the abundances of these species are underestimates. The remaining 14 species ranged from 40 individuals to one (mean of 10 specimens each). Four species are in the saltans group. The abundance distribution of this group, as a result, has an extremely steep drop to the base of the tail (fig. 7). A very unexpected result was how few Sophophora specimens were captured in fruit-baited traps (only 4% of the individuals in three species), and how many were collected in Malaise traps (60% of the individuals in all species), as well as in emergence traps (11% of individuals belonging to seven species), and by sweeping (19%, six species). The finding of seven species in emergence traps is entirely unexpected, since the widespread view is that species of Sophophora breed in decaying fruits, not leaf litter or humus. MYCOPHAGOUS GENERA (fig. 8): The data from Zurquí have been combined in the histogram for five genera: Hirtodrosophila (176 world species, 28 Neotropical, 12 at Zurquí), Mycodrosophila (132 world, 12 Neotropical, one at Zurquí), Paraliodrosophila (five species, all Neotropical, two at Zurquí), Paramycodrosophila (16 world species, four Neotropical, six at Zurquí), and an undescribed genus, “X,” which is being described in a separate paper (Grimaldi et al, in prep.). These form a well-defined monophyletic group ( Grimaldi, 1990 a , 1990b; Finet et al., 2021 ), which feed, mate, and breed in macrofungi ( Grimaldi, 1987 ; Valer et al., 2016 ; Policha et al., 2019 ; Santa-Brígida et al., 2019 ). The Zurquí sample is rather modest ( 147 specimens , belonging to 26 species total). Zygothrica is also in this group of genera ( Grimaldi, 1990a ), but it is treated separately because it was so abundant and diverse at Zurquí. FIG. 7. Species abundances by various collecting methods of Drosophila , subgenus Sophophora . Abundances for species 1 and 2 were much higher since this graph includes only specimens that were mounted from the bait traps, not all specimens. Sampling these flies at Zurquí involved most of the techniques employed: Malaise traps (20 of the 26 species), hand collecting (eight species), flight-intercept traps (eight species), emergence traps (seven species), and light traps (three species). Malaise traps did not capture a substantial majority of specimens; in fact, six of the 26 species were captured only by other means. We are inclined to believe that adults of these mycophagous species do not disperse far and may settle around a site of fungus for much of their brief lives. Collecting by hand yielded most of the specimens, and these were comprised largely (43% of individuals) of Paraliodrosophila spp. 1 and 2. The flies collected by hand were caught on Auricularia (Auriculariaceae) , Ganoderma (Polyporaceae) , and an undetermined genus of polypore. The undescribed genus “X” is known to feed on, and probably breed in, particular genera of ascomycetes, based on extensive observations elsewhere. The Zurquí data reinforce our impression that thorough sampling of these genera requires collecting them on their hosts. Hirtodrosophila has what appears to be the largest numbers of undescribed Neotropical species in this group of genera after Zygothrica . Zygothrica (fig. 9). This is a circumtropical genus currently of 125 described species, only 10 of which are Old World, all others being Neotropical. A total of 58 species were collected at Zurquí, making this the second-most diverse genus there after the subgenus Drosophila (Drosophila) . Species of Zygothrica are morphologically and ecologically very diverse, as well as speciose. The revisions by Grimaldi (1987 , 1990b ) cover only part of the genus; large sections still need work. Species are small to large bodied, many with striking patterns: wing spots and other markings, notal and frontal stripes, and bands, spots or other patterns on the abdomen. There can be striking sexual dimorphism in head shape (e.g., the dispar group), or coloration (e.g., the aldrichi group). Adult Zygothrica are usually found in large aggregations on forest mushrooms, where they graze, court and mate. Some species breed in the mushrooms ( Grimaldi, 1987 ; Valer et al., 2016 ; Policha et al., 2019 ); other species (even ones congregating at fungi) breed in flowers ( Grimaldi, 1987 ; Santa-Brígida et al., 2019 ; dos Santos and Vilela, 2005 ; Vaz et al., 2014 ). The attraction of Zygothrica to mushrooms is exploited by some pleurothalidiine orchids such as the genus Dracula , which lure the flies to the orchid’s labellum, which looks and smells like a small mushroom ( Endara et al., 2010 ; Policha et al., 2016 , 2019 ). Females of some Zygothrica species have impressively long, piercing oviscapts that are used for inserting eggs into flowers (fig. 9: spp. 12, 13, 23). While a long, piercing oviscapt is always associated with drosophilid species that breed in flowers ( Brncic, 1983 ; Grimaldi 1990a ), there are many anthophagous species with the typical, short oviscapt (such as the Drosophila bromeliae group [ Grimaldi, 2016 ]). At Zurquí, at least 10 (17%) of the 58 species have a long, piercing oviscapt, but since some species are known only by males, and some with a typical oviscapt are probably also flower breeders, we conservatively estimate about 30% of the Zurquí Zygothrica are anthophagous. The species-abundance curve for Zurquí Zygothrica is strongly concave, with just four of the 58 species (spp. 1, 4, 13, 19) comprising 50% of all individuals. Equally striking is the very long tail of rare species: 46 of the 58 species are known by just five or fewer specimens, suggestive of immense diversity. Indeed, there are probably hundreds of new species, especially in montane neotropical forests, but it will require long-term sampling to find them. Exceptional diversity of Zygothrica is also suggested by a dramatic separation of species that occur in lowland rainforests and those in montane forests. At Zurquí, there were no specimens in the Zygothrica aldrichi and dispar groups, which dominate in lowlands ( Grimaldi, 1987 ). Malaise traps were very effective at sampling Zygothrica at Zurquí: 84% of the individuals and all but nine of the species. Flight intercept traps sampled just 9% of the individuals and 19 of the species (five of the species uniquely: spp. 56, 59, 60, 61, 62). One specimen each in three species was obtained using emergence traps; these may have been breeding on mycelia or depleted fungal sporocarps.