Introduction

While evaluating arthropod biodiversity at the Leon Levy Native Plant Preserve (Fig. 1) (Eleuthera Island, the Bahamas) in thesummer of 2013, PAD collected several specimens of a large turquoise-faced katydid (Orthoptera: Tettigoniidae: Conocephalinae) from coppice forests within the park boundaries (Fig. 2). Males were singing at night with sustained chirping on various species of palm vegetation. These specimens were determined to be a new species close to Erechthis gundlachi Bolívar, 1888.

Erechthis gundlachi is known originally from Cuba (Bolívar 1888) and more recently the Dominican Republic of Hispaniola (Perez-Gelabert 2014). Yong (2015) gives its wider distribution on Cuba and includes effective photos of living coloration: pale strawbrownish yellow contrasting with the bay brown of a median body dorsal stripe. In studying a series of museum specimens of Erechthis, we then discovered a third species (grouped as E. gundlachi), this from the island of Hispaniola.

Erechthis is placed within the tribe Agraeciini. The unresolved taxonomy of ‘agraeciine’ conocephaloids was recently much improved by Chamorro-Rengifo et al. (2015). They reworked the polyphyletic genus Agraecia, creating a new sub tribe Agraeciina, that consists of 3 new genera: laratrox, Starkonsa, Yvelinula, along with Agraecia; the latter is left with just three species: Agraecia punctata Saint-Fargeau & Audinet-Serville, Agraecia dorsalis Karny and Agraecia agraecioides (Rehn 1911). From these agraeciines Erechthis is distinguished “in the shape of the fastigium verticis which is much longer than the scapus and has a pointed apex” (Chamorro-Rengifo et al. 2015). Gorochov (2015) created a new tribe, Cestrophorini, involving two other possibly related agraeciine genera, Cestrophorus and Acanthacara: these species share Erechthis' produced and acuminate fastigium verticis, but differ in other features (open eardrums, a shallow prothorax). Currently we are unsure which if any of these taxa makes a convincing ‘sister genus’ to Erechthis.

As Tettigoniidae Erechthiss spp.,belong to a family well-known for stridulation. Male katydids broadcast a calling song to attract females and to mediate rivalry (Gwynne 2001). We present an analysis of the calling signal of the Eleutheran species based upon field recordings of four individuals. Variability among Erechthis species in the structure of the median prong of the male subgenital plate and of the cerci is discussed in relation to their function during copulation. We also discuss the adaptive potential of the striking turquoise head color of the Eleutheran species, and propose dispersal scenarios for these three species in the Caribbean.

Methods

Field-Site: The Bahamas.—The Leon Levy Native Plant Preserve, hereafter LLNPP, is approximately 10 ha in area, reached off Banks Road outside Governor's Harbour, Eleuthera, the Bahamas (central coordinates of LLNPP: 25.188° N,-76.212°W). It is the only national park on Eleuthera and is operated by the Bahamas National Trust in conjunction with the Leon Levy Foundation. Vegetation at the LLNPP is predominantly Dry Broadleaf Evergreen Formation-Forest/ Shrubland (coppice),with the most common plants including poison wood (Metopium toxiferum), pigeon plum (Coccoloba diversifolia) and gum elemi (Bursera simaruba). The site is also characterized byseveral species of palm, such as buccaneer (Pseudophoenix sargentii), coconut (Cocos nucifera), sabal (Sabal palmetto), silver top (Coccothrinax argentata) and thatch (Thrinax morrisii). Man-made walking trails run throughout the coppice forests (Fig. 1) and it was from along these trails that the new ‘blue-faced’ Erechthis species was collected.

Collection and study of specimens.—Searches on Eleuthera were made over two successive years (2013 –2014) during the summer months (June, July). We collected specimens at night (between 20:00 – 1:00 h) with temperatures ranging from 25 – 30°C. We located singing males by tracking their song by ear to the source and capturing individuals by hand or with a sweep net. Just one female was located. All the males, except one, were found on various species of palm (i.e., buccaneer, coconut, sabal, silver top and thatch), at heights of 2 – 3 m above the ground. The exceptional male, still on site, was collected from a banana tree located in a fruit orchard (Fig. 1, Edible History Garden). The single female was discovered on the ground along the Tower Loop Trail. Locations where individuals were collected are indicated in Fig. 1. We euthanized specimens by placing them in a freezer for several hours, then preserved them in 70% isopropyl alcohol.

Fig. 1.

Map of The Leon Levy Native Plant Preserve. Asterisks on walking trails mark where Erechthis levyi specimens were collected. Star indicates holotype collecting location (Welcome Center). Entire park site spans 10 ha in area. Inset: Enlarged view of walking trails in the Edible History Garden. One male was collected here on a banana tree.

Five of the 6 specimens of E. gundlachi hail from the Philadelphia Academy of Sciences (ANSP), several determined to this species by M. Hebard in 1926. The remaining specimen, a female, also determined by Hebard, is from the University of Michigan Museum of Zoology (UMMZ). Male holotype and female allotype specimens of E. levyi, along with 4 paratypes are deposited in ANSP, with the other 4 paratypes deposited in UMMZ. All specimens of E. ayiti are returned to ANSP.

Specimens were studied and compared using a stereomicroscope (Nikon SMZ1000) fitted with a camera (DSFi1). Some photos were z-stacked using Helicon Focus (6.5.1 Pro). For scanning electron microscopy we employed a NeoScope (JCM 5000, Jeol).

Measurements (mm) and graphite drawings were made using a calibrated microscope (software: Nikon Elements), or in the case of body length, we used digital calipers (Fowler, Sylvac). Landmarks for measures were: body length: tip of fastigium verticis to tegmina extremity; pronotum length: disc in dorsal view midline distance cephalic margin to caudal; mesofurcal pits separation: distance in ventral view between furcal pit centres; metafemur length: distance from anterior coxotrochanteral articulation distad to femorotibial joint, excluding genicular lobes; ovipositor length: from ovipositor extremity to clasper sockets of female's subgenital plate, i.e., where the cercal teeth of the male engage during mating.

Making acoustic recordings.—For the Eleutheran species, we were able to make field recordings of the mate attraction songs of four males on a single night in June 2013. Two males were caught immediately after recording, the other two escaped. We used a Sony Zoom Q3 digital audio recorder (48 kHz sampling rate) with a frequency response up to 24 kHz, saving recordings as stereo MP3 files. Upon locating each singing male we directed the microphone toward the dorsal surface of its thorax from a distance of 1 – 3 m, avoiding obstructions (e.g., tree branches or leaves). The gain level on the recorder was adjusted for each male to avoid overload distortion. Recordings varied in length from 6 –48s (mean = 20 s, N = 4 males).

Song analysis.—We analyzed temporal and spectral features using Audacity 2.0.2 ( http://audacity.sourceforge.net/). Spectral measurements employed the ‘Spectrum’ function (FFT size = 8192 Hz, Hamming window), and we used a frequency cut-off of -20 dB relative to the highest amplitude frequency in the song, as frequencies below this threshold are unlikely to have biological relevance (Ewing 1989). For each male, we measured 10 consecutive chirps from the middle portion of a male's recording. We report descriptive statistics of song parameters as the mean ± standard error (SE).

Results

Fig. 2.

A. Habitus of Erechthis levyi male. B. Dorsal aspect of pronotum and fastigium verticis of head showing length relative to antennal scape and bay/castaneous dorsomedian stripe. C. Female ovipositor right lateral aspect showing tegmina body overreach. D. Turquoise frons and frontal fastigium with prominent ocellus between antennal scrobes. E. Protibia tympanal slits. For color version, see Plate I.

Fig. 3.

Male terminalia of the three Erechthis species, compared from right lateroposterior aspect. Median subgenital plate prong and cerci of distinct shape. A. E. ayiti. B. E.gundlachi. C. E. levyi. Sclerotized titillators, an inner part of the insect's phallomeres, happen to be visible in the cleared specimen of E. ayiti just basad of the prong. For color version, see Plate I.

Fig. 4.

Scanning electron micrographs compare highly diagnostic prong tips. A. Erechthis ayiti. B. Erechthis gundlachi. C. Erechthis levyi.

Table 1.

Species diagnosis (males).

Table 2.

Average measurements (mm) for various body structures for each Erechthis species. Numbers in parentheses indicate the sample size contributing to each average.

Table 3.

Descriptive statistics of E. levyi. song parameters. Male #2 had 5 pulse trains in some of its chirps. For each male, pulse train (PT) and interval (I) values represent the mean measured from 10 consecutive chirps. Also provided is the mean ± standard error (SE) for all four males. Units are in milliseconds.

Fig. 5.

Cercal protuberances (‘teeth’) compared for the three Erechthis species. A. E. ayiti. B. E. gundlachi. C. E. levyi. Teeth prominent in levyi, reduced in ayiti; ventral tooth absent in E. gundlachi (mt, mesad-directed tooth; dt, dorsal tooth; vt, ventral tooth; eppt, epiproct; cere, cercus; pr, prong).

Discussion

For the Bahamas E. levyi. represents the first record of a new katydid species discovered in these islands. The Bahamian entomofauna is in general poorly known (Elliot 2003); the taxonomy of only a few groups has been studied in detail [e.g., ants (Morrison 1998); beetles (Browne et al. 1993, Turnbow & Thomas 2008); butterflies (Miller et al. 1992); cicadas (Sandborn 2001); grasshoppers (Smith et al. 2003) and termites (Scheffrahn et al. 2006)]. Bahamian katydids have been completely overlooked, and as Perez-Gelabert (2014) first noted for the katydids of Hispaniola, this is surprising, since most katydids are large and conspicuous in their habitat, especially per their audible acoustic behavior. Although E. levyi. has so far been described from specimens collected only on Eleuthera, we expect it to have a wider distribution in the Bahamas, particularly on islands with the same coppice forest habitat as that found at the LLNPP.

The form of terminalia among males readily distinguishes the three Erechthis species. Such structural specificity in geniatlic structures is commonplace in insects and usually explained in terms of sexual selection. For example, a recent comparative study of phallus diversity among katydids suggests certain specific structures (e.g., titillators and other modified ventral sclerites) may function to ensure female mating via cryptic choice (Chamorro-Rengifo & Lopes-Andrade 2014, Vahed 2015, Wulff et al. 2015). Many katydid genitalic structures must also be under natural selection, e.g., for correctly positioning the spermatophore for transfer (Heller & Liu 2015). In some katydids, modified cerci are used to grip females tightly during copulation (Wulff & Lehmann 2016).

Competition between the stored sperm of rivals can arise by cryptic intrasexual selection (Gwynne 2001). Could the evolutionary basis of the prong of Erechthis be as an adaptation to promote removal of a rival's sperm? This structure with its downcurving terminal spine is positioned to penetrate the female's genital chamber during coupling. Another tettigoniid offers an example where a midline subgenital plate appendage serves in sperm removal. In males of the phaneropterine Metaplastes ornatus there is a subgenital plate median projection involving downcurving terminal spurs (von Helversen & von Heiversen 1991). When a male mounts a female, prior to transferring his sperm, he inserts his subgenital plate projection into the female's genital chamber. As the projection is withdrawn, the spurs catch upon the chamber walls turning it “practically inside out”. There is also evidence that this inserted structure can stimulate (rival) sperm release by simulating the presence of an egg (von Helversen & von Helversen 1991). This intriguing hypothesis about prong function is well worth exploring with Erechthis; future studies examining live specimens in copula should shed light on the evolution and functional significance of these specialized reproductive structures.

Mate attraction songs in katydids are used to facilitate pair formation. The temporal pattern of the song of E. levyi, in comparison to that of many other tettigoniids, has a high duty cycle and lacks stereotypy: the number of pulses per train and their amplitude varies within and among males (although with only four males we acknowledge the need to increase our sample size to better characterize variability in signal parameters). Greater inconsistency in song features could be the result of isolation from congenerics on Eleuthera: here males are experiencing less selection for stereotyped signal cues functioning in discrimination of related species (Gerhardt & Huber 2002). It will be worthwhile to obtain song recordings for E. gundlachi and E. ayiti for comparison with E. levyi, in order to determine similarities and differences in song structure, and whether males of sympatric species are exhibiting divergence in song features compared with conspecific males from isolated (allopatric) populations.

Fig. 6.

Mate attraction signal of a male E. levyi. A. Waveform showing pattern of 9 chirps. B. Expanded view of the fourth chirp, showing finer structure of five pulse trains. Each pulse train is composed of a series of 4 – 5 pulses produced in rapid succession. PT - Pulse train, I - Interval. C. Expanded view of the fourth pulse train from panel B, showing finer structure of 5 pulses. (D) Frequency spectrum. The signal has two frequency bands, a lower peak that ranges between 6.5 – 8.5 kHz, and a higher band from 11 7ndash; 24 kHz.

In contrast to the flexible escapement files of crickets (Montealegre-Z et al. 2009), many katydid files, as here with E. levyi, are thickened to resist longitudinal bending under scraper shear forces. The file of E. levyi (Fig. 7) has ∼80 broad file teeth, buttressed atop a stiffened transverse vein. Pulse is used here to describe song elements as continuous wave trains: the number of such trains (pulses) in a chirp (∼20) seems wildly inconsistent with the number of teeth in E. levyi's file. But given that each pulse/wave train of E. levyi varies greatly in amplitude, often becoming more intense later in the pulse (see Fig. 6C), multiple tooth contacts likely contribute to each pulse. Multiple tooth contribution to a sustained wave train is shown to be the case with another conocephaline katydid, Panacanthus pallicornis (Montealegre-Z & Mason 2005). The basis of this in P. pallicornis is a changing scraper velocity: in the file's mid-region velocity becomes appropriate for producing “successive tooth impacts…at an interval that matches the natural vibration frequency of the tegmina”. Scraper velocity can be altered by thoracic muscle activity but can also occur through elastic resonant stridulation (Morris 2008, Patek et al. 2011) when the springiness of scraper-associated cuticle enables very high velocity tooth contacts leading to ultrasonics.

Fig. 7.

Drawing of the stridulatory file of E. levyi. The file is located on the ventral surface of the left forewing and is composed of approximately 80 teeth. Numbers are included to better facilitate tooth count.

The frequency response limitation of our recording system leaves open the possibility of ultrasonic carrier frequencies beyond 24 kHz in the spectrum of E. levyi. The roll-off in energy beyond 23 kHz (Fig. 6D) maybe due to equipment rather than the insect. The song carrier is nevertheless a band spectrum rather than harmonically related peaks; it is the kind of spectrum made by a non-resonant generator mechanism, i.e., rates of scraper-file-tooth contact fall far below carrier frequencies (Elsner & Popov 1978). The spectral frequencies of E. levyi, with energy at 7 kHz and from 11 to 24 kHz, are likely the result of exciting radiating tegminal speculae into action, these then vibrating at their inherent resonance frequencies (Montealegre-Z et al. 2006, Morris et al. 2016).

The turquoise face and vertex coloration of E. levyi (Fig. 2D) is a striking feature set against its tan-brown body (Fig. 2A). Erechthis gundlachi and (presumably) E. ayiti lack this feature, but share the same tan-brown body coloration (see live specimen photos in both Perez-Gelabert 2014, Yong 2015). Head color is unlikely to play a role in mating behaviour since both sexes share the feature (Andersson 1994). Rather, it suggests an anti-predator adaptation. Many neotropical katydid species utilize a wide assortment of strategies to protect themselves from predators, including various types of contrasting coloration and patterns that act to camouflage the body against background vegetation (see review: Nickle & Castner 1995). We have yet to encounter E. levyi during the day, despite our intensive searches for it on the various palm trees where males are typically found singing at night. Because of the insect's robust size, predators are most likely to be birds, snakes, lizards, tree frogs and larger spiders (e.g., huntsman and tarantulas), with birds, snakes and lizards being the most commonly observed diurnally-active predators (PAD, pers. obs.). As with most nocturnal katydids, individuals normally retreat to refugia during the day, but where this might be for E. levyi remains a mystery. One location could be bromeliad plants, which are extremely abundant throughout the forests at this site. Bromeliads are home to a wide assortment of insects that use them as daytime refugia (Frank & Lounibos 2009). The blue-green coloration of bromeliad leaves is similar to the turquoise face of E. levyi, and therefore one scenario could be that individuals hide “face up” within the tight rosette of leaves which cluster at the base of the plant, thus concealing the body within one of the many deep cups that form at the base of the rosette, while leaving the head exposed to blend in with the surrounding vegetation. Similar hiding behaviours occur in other katydid species (e.g., Cocconotus, Teleutias, and Vestria) which use the curled leaves of Heliconia (family: Heliconiaceae) plants to conceal themselves during the day (Nickle & Castner 1995). Searches of bromeliads are planned to determine where E. levyi might be hiding during the day, which may offer some clues as to the adaptive basis of its turquoise colored face.

Vicariance and dispersal are both implicated as the two major forces shaping Caribbean biogeography (Page & Lydeard 1994). The Bahamas, as part of The Greater Antilles (which includes the major islands of Cuba, Hispaniola, Jamaica and Puerto Rico), has experienced vi cariant events through repeated cycles of submergence and emergence over the past 3 million years. During the Pleistocene when sea levels were up to 200 m lower, the Great Bahama Bank, made up of present-day Bimini, Andros, New Providence, Eleuthera, the Exumas, Long and Cat Island, was within 15 km of Cuba at its closest point, which likely resulted in the natural movement of many species between these two landmasses (Holzapfel & Harrell 1968, Pregill & Olson 1981, Carew & Mylroie 1997). Cycles of rising sea levels would have resulted in range fragmentation for many species as landmasses became smaller and more separated from one another by ocean, with some populations going extinct while others experienced divergence (Gillespie & Roderick 2002, Glor et al. 2005, Oneal et al. 2010). In addition to vicariance, dispersal, whether from over-water means or rafting, has also been important in moving organisms around the Caribbean, and thus promoting divergence of populations between islands (Holzapfel & Harrell 1968, Censky et al. 1998, Glor et al. 2005, Scharer & Epler 2007). Cuba represents a centre of origin for many taxa distributed throughout The Greater Antilles, including ants (Morrison 1998), crickets (Oneal et al. 2010), lizards (Glor et al. 2005) and termites (Scheffrahn et al. 2006). Recent extensive sampling for E. gundlachi on Cuba (Yong 2015), and Hispaniola (Perez-Gelabert 2014), did not uncover specimens of E. levyi, which suggests the latter species may be confined to the Bahamas, making it the first endemic katydid known from these islands. If Cuba indeed represents the ancestral source location, then perhaps dispersal of populations during the Pleistocene when landmasses were closer, followed by vicariance as sea levels rose, isolated populations throughout the region, with E. gundlachi eventually arising in Cuba and Hispaniola, E. ayiti in Hispaniola, and E. levyi in the Bahamas. Continued sampling of these islands, coupled with phylogeographic analysis of all three species, will be crucial to help us better understand the evolutionary history of this genus and determine its present day distribution throughout The Greater Antilles.