Introduction

The Phainoplea, Phainopepla nitens (Swainson), is a flycatcher (Aves: Passeriformes: Ptiliogonatidae) that inhabits arid woodlands and deserts of southwestern USA and Mexico (Chu & Walsberg, 1999).

The coccidia is a polyphyletic group of parasites, which are all obligate intracellular parasitic protists. Some species are homoxenous and are thought to be reasonably host-specific, while other species have complex heteroxenous life-cycles that involve a broad range of different host species (Tenter et al., 2002). To date, no coccidian species have been identified from any flycatcher in the Ptiliogonatidae. Here we describe a new species of Isospora from P. nitens.

Materials and methods

During a two-days trip to Joshua Tree National Park (33°41′42′′N, 115°48’7′′W; 33°43′26′′N, 115°48′51′′W; 33°44′51′′N, 115°49′36′′W; 34°1′49′′N, 116°8′49′′W; 34°1′45′′N, 116°9′3′′W), CA, USA, phainopepla birds (P. nitens) were observed and photographed. Birds were perched atop mesquite or palo verde trees, and fruiting shrubs. Birds were observed fruiting desert mistletoe (Phoradendron californicum) and swallowing berries whole. During photographic sessions at different locations, 5 adult male phainopepla left droppings that we collected. Each fresh faecal sample (with whole mistletoe berries) was placed into a separate 1.5 ml a plastic vial containing 2.5% (w/v) potassium dichromate solution (K2Cr2O7) at a ratio of 1:4 (v/v); each sample was studied under a light microscope (Duszynski & Wilber, 1997). Five days after, samples were placed into petri dishes and maintained at 20-26°C. Morphological observations, photomicrographs and measurements (n = 30) were taken according to Duszynski & Wilber (1997) and Berto et al. (2014a).

Results

Four of the 5 faecal samples examined (80%) contained oöcysts. Five days after collection of samples, more than 70% of the oöcysts were sporulated (under the conditions used in this study).


Isospora phainopepla n. sp.


Type-host: Phainopepla nitens (Swainson) (Aves: Passeriformes: Ptiliogonaditidae).

Type-locality: Joshua Tree National Park, CA, USA (33°41′42′′N, 115°48′7′′W; 33°43′26′′N, 115°48′51′′W; 33°44′51′′N, 115°49′36′′W; 34°1′49′′N, 116° 8′49′′W; 34°1′45′′N, 116°9′3′′W).

Type-material: Oöcysts in dichromate solution, phototypes and line drawings of sporulated oöcysts are deposited and available in the Repository (www.ibirds.org) of the Institute for Biodiversity Research, Development & Sustainability (iBIRDS). Photographs of the type-host specimens (symbiotypes) are deposited in the same collection. The repository number is ESV-27/2019. Photomicrographs of sporulated oöcysts are deposited and available in the Repository of iBIRDS (www.ibirds.org). The repository number is ESV-27/2019.

Prevalence: Oöcysts of this species were found in 4/5 (80%) of the fresh faecal samples examined.

Site of infection: Unknown. Oöcysts were recovered from fresh faecal droppings.

ZooBank registration: The Life Science Identifier (LSID) for Isospora phainopepla n. sp. is urn:lsid:zoobank.org:act:01DADE99-E625-4928-9043-8F0376D8D291.

Etymology: The specific epithet is derived from the genus name of the type-host.

Description (Figs. 1, 2)

Sporulated oöcyst

Fig. 1
figure 1

Photomicrographs of sporulated oöcysts and sporocysts of Isospora phainopepla. A, Two sporocysts with a polar granule between them (arrow). Both sporocysts residua (SR) and the elongate refractile bodies (RB) of the sporozoites are clearly visible; B, Two sporocysts facing the same direction with sub-Stieda bodies (SSB) clearly visible. C, A single sporocyst released from its oöcyst showing the refractile bodies (RB) of two of the four sporozoites. Scale-bars: 10 µm

Full size image

Oöcysts (n = 30) ellipsoid to ovoid, 30-35 × 22-29 (32.9 × 25.4), with smooth bi-layered wall (c.1.2 thick); length/width (L/W) ratio 1.2-1.35 (1.3). Micropyle absent; one polar granule present, rice-shaped (0.9 × 2.0) (Fig. 2).

Fig. 2
figure 2

Line drawing of a sporulated oöcyst of Isospora phainopepla collected from Phainopepla nitens. Scale-bar: 10 µm

Full size image

Sporocyst and sporozoites

Sporocyst (n = 30) bottle-shaped, 22-27 × 11-14 (23.9 × 12.0); length/width (L/W) ratio 1.97-2.02 (2.0). Stieda body present, half-moon shaped (0.75 thick); sub-Stieda body present, rounded, prominent, 2.0-2.4 high × 3.8-4.7 wide; para-Stieda body absent. Sporocyst residuum present, consisting of many spherules of different sizes (0.5-0.8). Sporozoites 4, vermiform, 3.4-3.6 × 16.8-18.1, with posterior refractile body (7.5 in length) and anterior refractile body (2.0 in diameter) (Figs. 1A–C, 2).

Discussion

Coccidian species have not been identified previously in any flycatcher species in Ptiliogonatidae of the Americas. Two Eimeria species (Soriano-Vargas et al., 2015, 2017; McAllister & Hnida, 2019), and a total of 17 Isospora species have been identified from birds of the order Passeriformes in North America (Berto et al., 2011, 2014b; Berto & Lopes, 2013; Salgado-Miranda et al., 2016; Luna-Castrejón et al., 2018).

Mean dimensions of sporulated oöcysts (32.9 × 25.4 µm) and sporocysts (23.9 × 12.0 µm) of I. phainopepla n. sp., appear to be larger than those in all species of Isospora identified from Passeriformes in the Americas (Berto et al., 2011; Berto & Lopes, 2013). To date, the larger sporulated oöcyst identified (32.1 × 28.9 µm) is for I. bocamontensis Pereira, Berto, Flausino, Lovato & Lopes, 2011, described from the yellow cardinal Gubernatrix cristata (Vieillot) in Brazil (Pereira et al., 2011), and the larger sporocyst identified (23.4 × 11.8 µm) is for I. sayacae Berto, Balthazar, Flausino & Lopes, 2009, decsribed from the sayaca tanager Thraupis sayaca (Linnaeus) in Brazil (Berto et al., 2009). It appears that I. phainopepla n. sp. is the largest Isospora species identified in passerines of the New World.

Four of five phainopepla faecal samples contained oöcysts of I. phainopepla. To establish a more accurate prevalence of the parasite in these natural populations, further studies with a higher number of bird and/or faecal samples are need. As small berries and flying insects are the main foods taken by phainopepla (Chu & Walsberg, 1999), there is a low possibility that isosporans observed in collected faeces samples were spuriuos parasites of the phainopepla we photographed and from which faeces were collected. Some of the southern populations of this bird species are located at a desert into the Reserva de la Biósfera Cuicatlán-Tehuacán, Puebla, Mexico (Howell & Webb, 1995). Phylogenetic analysis of isosporans from both phainopepla populations are needed (Ogedengbe et al., 2018).