Strange Little Flies in the Big City: Exotic Flower-Breeding Drosophilidae (Diptera) in Urban Los Angeles

<div><p>Urban landscapes are commonly considered too mundane and corrupted to be biotically interesting. Recent insect surveys employing 29 Malaise traps throughout Los Angeles, California, however, have uncovered breeding populations of two unexpected species of one of the most studied and familiar groups of organisms, <i>Drosophila</i> “fruit” flies. Unlike most introduced species of drosophilids, which breed in fresh or decaying fruits, these are specialized flower-breeders. A common species in the survey was <i>Drosophila (Drosophila) gentica</i> Wheeler and Takada, previously collected only once, in El Salvador. It belongs to the <i>flavopilosa</i> species group, all species of which have been known until now from central Chile, Argentina and Uruguay, to Veracruz, Mexico and the Caribbean, breeding in flowers of <i>Cestrum</i> (“jessamine”) and <i>Sessea</i> (Solanaceae). The Los Angeles populations are probably breeding in a native and/or introduced <i>Cestrum</i>; in addition, populations in San Luis Obispo County were visiting ornamental <i>Cestrum</i>. <i>Drosophila gentica</i> occurs as far north as San Francisco, where it was found breeding in <i>Cestrum aurantiacum</i>. <i>D</i>. <i>gentica</i> is redescribed and figured in detail for diagnostic and identification purposes. Specimens from Jamaica previously identified as <i>D</i>. <i>gentica</i> are a distinct species but are not formally described in lieu of complete male specimens. Rare in the Malaise traps was <i>Drosophila (Sophophora) flavohirta</i> Malloch, a common species in Australia on the blossoms of native Myrtaceae, found on introduced <i>Eucalyptus</i> in South Africa and both <i>Eucalyptus</i> and <i>Syzygium</i> in Madagascar; adults feed on myrtaceous pollen and nectar, larvae breed in the flowers. It is also redescribed in detail, including its unusual egg. This is the first New World report of this species; DNA sequences confirm it is a morphologically highly aberrant member of the <i>D</i>. <i>melanogaster</i> species group. This study reveals how intensive field sampling can uncover remarkable biodiversity in even the most urbanized areas.</p></div

<i>Drosophila gentica</i> Wheeler and Takada collected in Los Angeles.

<p><b>A</b>: frontal view of head. B: Female, lateral view. <b>C</b>: Male, dorsal view of thorax; Unlabelled arrows point to enlarged acrostichals in front of <i>adc</i> setae. <b>D:</b> Male terminalia, lateral view, with aedeagus everted. <b>E</b>: Female terminalia, posterior view. <b>F:</b> Spermatheca. <b>G, H:</b> Drawings of female terminalia of <i>Drosophila gentica</i> specimens from El Salvador (H, right valve) and Los Angeles (G, complete terminalia). I: Male terminalia of LA specimen, posterior view. <b>J</b>: Aedeagus of LA specimen (male), lateral view. Abbreviations: <i>adc</i>, anterior dorsocentral seta; <i>dscl</i>, dorsal sclerite (of oviscapt), <i>ivel</i>, inner lobe of ventral epandrial lobe; <i>pdc</i>, posterior dorsocentral seta. For more details and comparisons see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0122575#pone.0122575.s009" target="_blank">S1 Text</a>.</p

Contexts for sampling flower-breeding <i>Drosophila</i> in Los Angeles and other areas in California.

<p><b>A.</b> Map of the Los Angeles area, showing major highways, each dot indicating the location of Malaise traps used in the BioSCAN project. Yellow dots are where <i>Drosophila gentica</i> specimens were captured; orange dots are where <i>D</i>. <i>flavohirta</i> specimens were captured; there is one site where both species were captured. Inset shows areas outside of Los Angeles where <i>D</i>. <i>gentica</i> was also found. Map: <b>B.</b> Malaise trap in backyard with two of the participants, one of them Eric Keller. Photo by Phyllis Sun. <b>C-E</b>. <b><i>Cestrum nocturnum</i> x <i>diurnum</i> hybrid</b> (“Orangel Peel”) in flower, May 2014, Los Osos, California. The shrub (C), was attracting hundreds of <i>Drosophila gentica</i> to its small tubular flowers (D, E). Photos by Brian Brown.</p

<i>Drosophila (Sophophora) flavohirta</i> Malloch.

<p><b>S</b>pecimens dried from ethanol using HMDS; <b>A-H</b> from California (Photos and drawings by D. Grimaldi), <b>I-J</b> from Stroud, Australia (Photos by S. McEvey). <b>A</b>. Lateral habitus, female. <b>B.</b> Frontal view of head, same. <b>C</b>. Female terminalia, lateral view. <b>D:</b> Spermathecal capsule, lateral view. <b>E:</b> Arista. <b>F</b>: Epandrium with cerci and surstyli, posterior view. <b>G</b>. Hypandrium, aedeagus, paraphyses and aedeagal apodeme, ventral view. <b>H</b>. Male protarsus, mesal view. <b>I</b>. Egg emerging from oviscapt. <b>J</b>. Anterior tip of egg, showing short, blunt pair of filaments. Abbreviations: <i>aed</i>, aedeagus; <i>aedap</i>, aedeagal apodeme; <i>hyp</i>, hypandrium; <i>ilp</i>, inner lobe of paraphysis; <i>olp</i>, outer lobe of paraphysis; <i>vel</i>, ventral epandrial lobe.</p

Images of <i>Apocephalus borealis</i> and honey bees.

<p>(A) Adult female <i>A. borealis</i>. (B) Female <i>A. borealis</i> ovipositing into the abdomen of a worker honey bee. (C) Two final instar larvae of <i>A. borealis</i> exiting a honey bee worker at the junction of the head and thorax (red arrows).</p

Distribution of phorid-infected honey bees sampled in this study (red).

<p>Inset shows the San Francisco Bay Area counties where we found phorid-parasitized honey bees. The routes of commercial hives tested are indicated (arrows), where dotted lines represent states the hives crossed before viral microarray testing and solid lines represent the route of hives during the period of microarray testing. Sites where <i>A. borealis</i> was previously known <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0029639#pone.0029639-Genersch1" target="_blank">[7]</a> are indicated by black dots.</p