Chewing Lice (Phthiraptera) Infesting Breeding Suliformes (Aves: Aequornithes) of the Arabian Peninsula

ABSTRACT Despite the large diversity of the migratory and resident avifauna of the Arabian Peninsula, relatively few species have been sampled for chewing lice. In this study, three breeding species of Suliformes, Phalacrocorax nigrogularis Ogilvie-Grant & Forbes, Sula dactylatra Lesson and Sula leucogaster (Boddaert) were examined for chewing lice. Four species of chewing lice were identified, two from the suborder Amblycera (Eidmanniella albescens (Piaget, 1880) and Eidmanniella nancyae Ryan & Price, 1969) and two from the suborder Ischnocera (Pectinopygus socotranus Timmermann, 1964 and Pectinopygus sulae (Rudow, 1869)). Diagnostic characters, examined and other known hosts, an identification key, and images of hosts and chewing lice are provided.


INTRODUCTION
The chewing lice of the Kingdom of Saudi Arabia (KSA) have recently received attention after a decade of neglect (El-Ahmed et al. 2012;Al-Ahmed et al. 2014;Nasser et al. 2015), but these efforts should be viewed as preliminary, considering the notable diversity of these ectoparasitic insects of the region. With more than 4 000 species worldwide, the chewing lice form one of the most diverse orders of parasitic Hexapoda (Price et al. 2003). Most of these species infest birds, but taxa are known from mammals (Price et al. 2003). From an ecological point of view, the chewing lice that infest marine birds is an important and interesting group of lice. Throughout the Middle East, little is known about the ectoparasites of sea birds, including those of Suliformes (Negm et al. 2013).
The order Suliformes is a recently designated order of birds introduced by the International Ornithologists' Union (Gill & Donsker 2014). In the past the Pelecaniformes were considered a monophyletic group (Olson 1985). Recent molecular studies have indicated that the Pelecaniformes are polyphyletic and should be divided into different orders, one of which is the new Suliformes (Boles & Christidis 2008 The Brown booby is a widely distributed sea bird, known from pantropical open oceans and warm seas (Anonymous 2012). Throughout the study region, the Brown booby breeds on remote rocky islands of the Red Sea (PERSGA 2003). The Masked booby occurs throughout the subtropics and tropics. In the Arabian Peninsula, there are three main breeding populations of this species, which use the Indian Ocean sandy beaches of the isolated islands of Oman and Yemen (Porter & Aspinall 2013). Outside the breeding seasons, the Brown and Masked boobies are "nomadic" and are considered true marine birds, spending months on the open water (Welty & Baptista 1990). Boobies are spectacular divers and feed mainly on small fish and squid (Alderton 2008).
The Socotra cormorant is the only species of Phalacrocoracidae that breeds in the Arabian Peninsula and is endemic to the region. It is considered a vulnerable endangered species by the IUCN. After the Gulf War in 1991, populations of this bird suffered large losses due to unprecedented oil spills (Evans et al. 1993). After the end of the war, major conservation efforts were directed at the Socotra cormorant in Bahrain, Kuwait, Qatar and the KSA, the results of which allowed populations to recover (Anonymous 2005).
There are two genera of chewing lice infesting birds of the order Suliformes, Eidmanniella (Amblycera) and Pectinopygus (Ischnocera) (Price et al. 2003). Several researchers have discussed the host/parasitic relationships of these genera (Kellogg & Kuwana 1902;Thompson 1940aThompson , 1940bThompson , 1946Thompson , 1947Thompson , 1948aThompson , 1948bRyan & Price 1969), but there is little data for these genera of the Arabian Peninsula. The objective of this paper is to review the known information of these two genera in this region, and to provide a taxonomic review of the lice collected from Suliformes in the Arabian Peninsula.

MATERIAL AND METHODS
As part of the survey on chewing lice parasitising wild birds of the KSA, we examined three species of Suliformes that are typically difficult to capture. A sick adult Brown booby was caught by hand at Jazan Tourism Marina, KSA (16°54'7"N 42°32'28"E); juvenile Masked boobies were captured on nests on Al-Hallaniyah Island, Oman (17°29'59"N 56°4'51"E); and an adult Socotra cormorant was captured near Karan Island, KSA (27°43'5"N 49°49'31"E) using a mist net deployed over a partially sunk boat near the coast of the island, on which the birds had several times been observed resting (Fig. 1). The feathers and skin scales of these birds were examined visually for chewing lice, and clean forceps and a fine-toothed comb (teeth spaced 0.2-0.3mm apart) were used to collect individual lice.
Handling of the birds followed strict guidelines and was authorised by the National Commission for Wildlife Conservation and Development (NCWCD) (Abuzinada 1993). The birds were examined for lice and released unharmed at their capture location. Unfortunately, the sick Brown booby died during the visual inspection. All lice were preserved in 95 % ethyl alcohol. Specimens were then mounted on slides using Pauri's medium (Smart et al. 1965). The lice were identified using Kellogg and Kuwana (1902), Bienko (1964), Ryan and Price (1969) and Price et al. (2003).
The slides were examined under a Nikon Eclipse 80i microscope and photographed using a Panasonic Lumix FT2 14 mp camera. All photographic images were produced using a Canon Sx40 Hs and the map was produced using DIVA-GIS. Measurements were taken in cellSens Dimension 1.6 (Olympus Corporation, Center Valley, Pennsylvania) from digital photos. All measurements are given in millimetres. Abbreviations used for measurements: HL = head length along midline; HW = postantennal head width; HI = head index; TL = thoracic length; AL = abdominal length at midline; Total L = total length. All lice specimens were deposited in the King Saud University Museum of Arthropods, King Saud University, Riyadh.  Head semilunar, wider than long with faint preocular slit; hypopharyngeal sclerite well developed; antennae with characteristic club-shaped third and fourth segments with a constricted base attached in part with second antennal segment; temple expanded outward with four long setae; gula oblong with two small setae. Thorax with characteristic pointed median process on the prothorax; margin of prothorax with numerous short setae (14-18); legs long, nearly equal in length, concolorous, and third femur with sparse ventral setal brush. Abdomen elongated oval in shape, ventral brush not clearly apparent on segments III-V, last tergite with characteristic short blunt spiniform setae across the posterior margin, which separates this species from other Eidmanniella spp.; male genitalia weakly chitinised.    Head conical in shape with few lateral setae, frontal part slightly expanded; antenna sexually dimorphic, in male elbowed in shape, in female filiform, first antennal segment of male slightly longer than all the other segments combined, all antennal segments of female equal in size, brown, temporal margin flatly convex. Thorax trapezoidal in shape with very short fore legs and very long mid and hind legs, the hind legs are the longest; metathorax with irregular margins with three long setae on posterior lateral margin. Abdomen elongated, female abdomen with grainy texture, tergal and sternal plates with two short central setae; 9 th segment of female deeply angularly emarginated with numerous setae; male genitalia asymmetrical.  Head conical in shape with numerous setae, especially around the hyaline margin, frontal part slightly expanded; first antennal segment of male as long as all the other segments combined, the first antennal segment of female largest and the 5 th antennal segment brown; temporal margin flatly convex. Thorax trapezoidal, fore legs very short, mid and hind legs very long, equal in length; metathorax with irregular margins with five long setae on posterior lateral margin. Abdomen elongated with highly chitinised margins in both sexes, all segments with complete dark brown bands, tergal plates with two short central setae; each sternum with four short setae, 9 th segment of female deeply angularly emarginated with numerous setae; male genitalia asymmetrical with sharp pointed end.

DISCUSSION
Little is known about the ectoparasites of the large number of marine birds of the Arabian Peninsula (Negm et al. 2013;Nasser et al. 2015). The Suliformes, which form one of the most important components of marine ecosystems, especially for tropical seas, include the interesting endemic Socotra cormorant (Causey & Padula 2013). The order also contains many birds that have conservational value, such as the vulnerable Socotra cormorant (Jennings 2010). There are three genera of chewing lice known to infest birds of the order Suliformes: Eidmanniella Kéler, 1938 and Piagetiella Neumann, 1906 of the suborder Amblycera, and Pectinopygus Mjöberg, 1910 of the suborder Ischnocera (Price et al. 2003). Several researchers have revised the information on chewing lice of these genera (Kellogg & Kuwana 1902;Bedford 1931;Thompson 1940aThompson , 1940bThompson , 1946Thompson , 1947Thompson , 1948aThompson , 1948bTimmermann 1964Timmermann , 1967Ryan & Price 1969).
For the Arabian Peninsula no data is available for chewing lice infesting Suliformes except for the materials that were collected from Aden and used in the original description of E. nancyae Ryan &Price, 1969 andP. socotranus Timmermann, 1964. So, from a taxonomic point of view, the four species of lice that have been collected and reported here are new records for Saudi and Oman parasitic fauna. The high-definition photos presented form the only available photos for these species to date.
One of most interesting phenomena that appears clearly in Suliformes/lice interaction is the characteristic parasite/host distribution. Chewing lice show a high degree of host specificity for different species of cormorants, but not for the boobies. Each species of the genus Pectinopygus parasitises a unique species of cormorant while Pectinopygus sulae is known from three species of boobies (Price et al. 2003). On the other hand, species such as Eidmanniella albescens has been recorded from five species of boobies (Price et al. 2003). No doubt such relationships are related to overlapping distributions of the boobies, whereas cormorant species are allopatric. Further research is needed on this interesting group of birds, particularly using geographical information systems (GIS) to study the relationship between parasite specificity and distribution of hosts, in order to better understand their role in marine ecosystems.