(Insecta: Phthiraptera: Philopteridae) Infesting Breeding Terns in the Arabian Peninsula, with Notes on Their Phylogeny and Ecology

Home , Kerguelen tern, Lari, Saemundssonia

Author's personal copy

Parasitol Res (2015) 114:2587–2597 DOI 10.1007/s00436-015-4463-6

ORIGINAL PAPER

New records of species of Saemundssonia (Insecta: Phthiraptera: Philopteridae) infesting breeding terns in the Arabian Peninsula, with notes on their phylogeny and ecology

1 2 3 1,4 Mohammed Shobrak & Azzam Alahmed & Ricardo Palma & Mohammed Almalki & Mohamed Gamal El-Den Nasser2

Received: 16 March 2015 /Accepted: 2 April 2015 /Published online: 30 April 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Six species of terns, which breed on the Arabian more accurate as it appeared more compatible with hosts’ phy- Peninsula, were examined for head chewing lice of the genus logeny. The trees indicate relationships between tern Saemundssonia in four different islands around the coasts of Saemundssonia and congeneric species from other marine Saudi Arabia, both in the Red Sea and in the Arabian Gulf. Four birds, especially from gulls. An ANOVA was also conducted louse species were collected: Saemundssonia laticaudata, to test the mean parasite load for each tern species studied, and Saemundssonia melanocephalus, Saemundssonia meridiana results indicate that there is a relation between louse loads and and Saemundssonia sternae,ofwhichthreearerecordedfor colonization behaviour of the hosts. Data from lice examined the first time from this region. Also, we record three new and illustrations of lice and their hosts are also included. host-louse associations for the world—Saemundssonia laticaudata and Saemundssonia sternae from white-cheeked Keywords Chewing lice . Saemundssonia spp. . Tern . terns and Saemundssonia melanocephalus from Saunders’s Gulls . Phylogeny . Saudi Arabia terns—including a host-switch event of Saemundssonia laticaudata on white-cheeked terns in the Karan Island population. Gene bank data for the COI gene from seven species of Introduction Saemundssonia that infest marine birdswereusedtopropose evolutionary trees using two different statistical methods: max- Terns (Charadriiformes: Sternidae) are common elegant sea- imum parsimony (MP) and neighbour joining (NJ). The result birds found through almost all seas and some freshwater habi- indicated that the tree which was produced by NJ is likely to be tats around the globe (Jennings 2010;LarssonandOlsen2010). Twelve species of terns have been recorded from the Arabian Electronic supplementary material The online version of this article Peninsula (Table 1): seven of them breed there, while the others (doi:10.1007/s00436-015-4463-6) contains supplementary material, which is available to authorized users. are migrant or winter visitors (Porter and Aspinall 2010) (Fig. 1). Most of the breeding species also occur in * Mohamed Gamal El-Den Nasser neighbouring countries and in the western Indian Ocean [email protected] (Shobrak et al. 2003;KasambeandDeshmukh2011). In addi- tion, terns from this region could reach the far East as one lesser 1 Department of Biology, Science College, Ta’if University, crested tern ringed in 1994 at Karan Island in the Saudi Arabian Ta’if, Saudi Arabia Gulf was found on the coast of Bali Island in Indonesia 2 Research Chair of Insect Vector Borne Diseases, Department of Plant (Shobrak, unpublished). Usually,ternsbreedonremoteislands, Protection, College of Food and Agriculture Science, King Saud where they form large noisy colonies, but in a few species, nests University, Riyadh, Saudi Arabia are located very far from each other or under the shade of low 3 Museum of New Zealand Te Papa Tongarewa, P.O. Box 467, vegetation or shrubs (Symens and Al-Suhaibany 1996; Wellington, New Zealand Shobrak and Aloufi 2014). Eggs are laid directly on the ground 4 Department of Biology and Biochemistry, University of Bath, with little or no nest materials (Martin 2004). The synchronized Bath, UK breeding behaviour of terns has many advantages for their Author's personal copy

2588 Parasitol Res (2015) 114:2587–2597

Table 1 Species of terns from the Arabian Peninsula and surrounding seas with published and new records of Saemundssonia (taken from Price et al. 2003 and this study)

Tern common name Tern scientific name Status Species of Saemundssonia

Gull-billed tern Gelochelidon nilotica (Gmelin, 1789) Migrant S. gelochelidoni Touleshkov, 1959 Caspian tern Hydroprogne caspia (Pallas, 1770) Breeding, resident No records Lesser crested tern Thalasseus bengalensis (Lesson, 1831) Breeding, migrant S. laticaudata (Rudow, 1869)b Swift tern Thalasseus bergii (Lichtenstein, 1823) Breeding, migrant S. laticaudata (Rudow, 1869) Sandwich tern Thalasseus sandvicensis (Latham, 1787) Breeding, migrant S. brevicornis (Giebel, 1874) S. laticaudata (Rudow, 1869)b Bridled tern Onychoprion anaethetus (Scopoli, 1786) Breeding, migrant S. lockleyi Clay, 1949 S. meridiana Timmermann, 1950a, b Common tern Sterna hirundo Linnaeus, 1758 Migrant S. sternae (Linnaeus, 1758) White-cheeked tern Sterna repressa Hartert, 1916 Breeding, migrant S. laticaudata (Rudow, 1869)b, c S. sternae (Linnaeus, 1758)a, b, c Little tern Sternula albifrons Pallas, 1764 Migrant S. melanocephalus (Burmeister, 1838) Saunders’s tern Sternula saundersi (Hume, 1877) Breeding, migrant S. melanocephalus (Burmeister, 1838)a, b, c Whiskered tern Chlidonias hybridus (Pallas, 1811) Migrant S. lobaticeps (Giebel, 1874) White-winged tern Chlidonias leucopterus (Temminck, 1815) Migrant S. lobaticeps (Giebel, 1874) a Denotes a new louse record in the Arabian Peninsula and surrounding seas b Denotes a new host-louse association in the Arabian Peninsula and surrounding seas c Denotes a new host-louse association in the world reproduction, but in turn, it also facilitates the transfer of ecto- 1758)fromSterna hirundo in Syria, Saemundssonia parasites between individuals (Welty and Baptista 1990). melanocephalus from Sternula albifrons in Egypt, Species of four genera of parasitic chewing lice are known Saemundssonia lobaticeps (Giebel, 1874) from Chlidonias to infest terns: Actornithophilus Ferris, 1916; Austromenopon leucopterus in Egypt and Saemundssonia laticaudata Bedford, 1939; Quadraceps Clay & Meinertzhagen, 1939; (Rudow, 1869) from Thalasseus bergii in the Red Sea. Also, and Saemundssonia Timmermann, 1936 (see Price et al. the gull-infesting species Saemundssonia lari (O. Fabricius, 2003, p. 293). Among these genera, Saemundssonia includes 1780) was recorded from the Middle East, collected from five over 100 species and subspecies parasitic on a wide range of species of migrant and resident Red Sea gulls (Al-Ahmed hosts from five different avian orders: Anseriformes, et al. 2014). Charadriiformes, Gruiformes, Phaethontiformes and The aim of this work is to update records and knowledge Procellariiformes (Price et al. 2003,p.232).Speciesof about the genus Saemundssonia associated with terns from the Saemundssonia have a stout round body with a large triangu- Middle East, reporting new records of species of this genus lar head and are typically found on the head and neck of the from terns that breed in the Arabian Peninsula, as well as new host (Timmermann 1936; Palma 2012). Currently, 14 species host-parasite associations for the region and the world. Also, of this genus are known to infest terns throughout the world we study the relationship between the breeding behaviour of (Table 2). Most (nine) of these species are restricted to one these birds and their louse infestations, and the phylogenetic host species, while the remainder (five) parasitize groups of relationships among some species of Saemundssonia, using related tern species, showing a possible coevolutionary rela- our and other available data. tionship with their hosts (Table 2). The morphological differentiation among species of Saemundssonia is subtle and main- ly restricted to the male genitalia (see Clay 1949; Palma 2000, Materials and methods 2012). For this reason, and because early workers did not study the male genitalia, all samples collected from terns were As part of a major project concerning the chewing louse fauna initially placed under one species name: BS. melanocephalus of wild birds in the Arabian Peninsula, some of the authors (Burmeister, 1838)^ (e.g. Harrison 1916), until Clay (1949) had a chance to visit the most important breeding habitats for clearly recognized and described other species. terns in Saudi Arabia, the largest country of the peninsula. Six Clay (1949) recorded four species of Saemundssonia from species of breeding terns were studied, as follows: Thalasseus terns in the Middle East: Saemundssonia sternae (Linnaeus, bengalensis (Lesson, 1831) (lesser crested tern), T. bergii Author's personal copy

Parasitol Res (2015) 114:2587–2597 2589

Fig. 1 Host terns: (1) white-cheeked tern on its nest in Jana Island; (2) Saunders’s tern on nest in open ground, Farasan Island; (6) Sandwich tern bridled tern over a shrub which holds its nest, Jana Island; (3) swift tern on flying over its nest, Karan Island its nest, Karan Island; (4) lesser crested tern colony, Karan Island; (5)

(Lichtenstein, 1823) (swift tern), Thalasseus sandvicensis Terns were collected alive during their breeding season (Latham, 1787) (Sandwich tern), Onychoprion anaethetus using standard mist nets (mesh, 1.8 cm×0.12 mm; size, (Scopoli, 1786) (bridled tern), Sterna repressa Hartert, 1916 2m×15 m), funnel ground traps and remote control traps. (white-cheeked tern) and Sternula saundersi (Hume, 1877) Birds were identified using the guide by Cottridge (2006) (Saunders’stern).Allcapturedternswereexaminedfor and the monograph by Porter and Aspinall (2010). We follow chewing lice and other parasites under the permission of the Del Hoyo and Collar (2014) for the scientific names of the Saudi Wildlife Authority. The breeding sites of these terns are terns. All birds were released unharmed in the same place of distributed through several protected areas and remote islands: capture. Saemundssonia lice were collected by close visual Jana (27° 22′ 10″ N, 49° 53′ 53″ E) and Kaaran (27° 43′ 5″ N, inspection of the birds’ head and neck region, and were pre- 49° 49′ 31″ E) Islands, located in the Arabian Gulf as part of served in 96 % ethyl alcohol. Some samples—representing all the Jubail Marine Wildlife Sanctuary; Farasan Islands (16° 36′ species collected—were transferred to lactic acid for clearing 7″ N, 42° 8′ 77″ E), within the Marine Protected Area near the for 2 days and then slide-mounted in Puri’s Media. The re- coast of Jazan on the southern end of the Red Sea; and some maining samples were preserved on −20 °C for further molec- scattered islands near the coast of Tabuk (25° 13′ 48″ N, 37° 8′ ular studies. Louse identifications were made using Clay 37″ E) on the northern Red Sea. (1949), Timmermann (1950) and Ward (1955). Author's personal copy

2590 Parasitol Res (2015) 114:2587–2597

Table 2 List of species of Saemundssonia reported from world terns (Price et al. 2003 and this study)

Species of Saemundssonia Tern scientific name Tern common name

S. albemarlensis (Kellogg & Kuwana, 1902) Onychoprion fuscatus (Linnaeus, 1766) Sooty tern S. brevicornis (Giebel, 1874) Thalasseus sandvicensis acuflavidus (Cabot, 1848) Sandwich tern S. gelochelidoni Touleshkov, 1959 Gelochelidon nilotica (Gmelin, 1789) Gull-billed tern S. hopkinsi Clay, 1949 Sterna aurantia J.E. Gray, 1831 River tern S. laticaudata (Rudow, 1869) Thalasseus bergii (Lichtenstein, 1823) Swift tern Thalasseus bengalensis (Lesson, 1831) Lesser crested tern Thalasseus maximus (Boddaert, 1783) Royal tern Thalasseus sandvicensis (Latham, 1787) Sandwich tern Sterna repressa Hartert, 1916b White-cheeked tern S. lobaticeps (Giebel, 1874) Chlidonias hybridus (Pallas, 1811) Whiskered tern Chlidonias leucopterus (Temminck, 1815) White-winged black tern Chlidonias niger (Linnaeus, 1758) Black tern S. lockleyi Clay, 1949 Onychoprion anaethetus (Scopoli, 1786) Bridled tern Sterna paradisaea Pontoppidan, 1763 Arctic tern Sterna virgata Cabanis, 1875 Kerguelen tern Sterna vittata Gmelin, 1789 Antarctic tern S. melanocephalus (Burmeister, 1838) Sternula albifrons Pallas, 1764 Little tern Sternula nereis (Gould, 1843) Fairy tern Sternula saundersi (Hume, 1877)b Saunders’s tern S. meridiana Timmermann, 1950a Onychoprion anaethetus (Scopoli, 1786) Bridled tern S. niethammeri Eichler, 1953 Phaetusa simplex (Gmelin, 1789) Large-billed tern S. olrogi Timmermann, 1961 Sterna trudeaui Audubon, 1838 Trudeau’s tern S. parvigenitalis Ward, 1955 Sterna forsteri Nuttall, 1834 Forster’s tern S. snyderi (Kellogg & Paine, 1910) Onychoprion lunatus (Peale, 1848) Grey-backed tern S. sternae (Linnaeus, 1758) Sterna dougallii Montagu, 1813 Roseate tern Sterna hirundo Linnaeus, 1758 Common tern Sterna repressa Hartert, 1916b White-cheeked tern Sterna striata Gmelin, 1789 White-fronted tern Sterna vittata Gmelin, 1789 Antarctic tern S. gygisa Palma, 2012 Gygis alba (Sparrman, 1786) White tern a Denotes a new host-louse association due to a host-switch event b Denotes a new host-louse association

The database of the National Center for Biotechnology 1780) BAF348865.1^. The first three species are parasites of Information was used to study the phylogenetic relationships terns, while the other four species parasitize puffins, guille- among some species of Saemundssonia. A conservative gene mots, red-tailed tropicbirds and gulls, respectively. (Cytochrome Oxidase Subunit I gene=COI) was chosen to The maximum parsimony (MP) (Eck and Dayhoff 1966) study such relationships, based on the availability of se- with consistency index 0.823413 (0.684397), retention index quences of this gene from several Saemundssonia species. 0.340741 (0.340741) and composite index 0.280570 Sequences from seven species of Saemundssonia were ex- (0.233202) for all sites and parsimony-informative sites was tracted in Fasta format from the GenBank database: used to induce the final tree that was obtained using the close- Saemundssonia lockleyi Clay, 1949 BJN900114.1^, neighbour-interchange algorithm (Nei and Kumar 2000). Al- Saemundssonia meridiana Timmermann, 1950 so, neighbour joining (NJ) (Saitou and Nei 1987) was used to BAF396607.1^, Saemundssonia sternae (Linnaeus, 1758) induce another evolutionary tree that was drawn to scale, with BAF396610.1^, Saemundssonia fraterculae (Overgaard, branch lengths in the same units as those of the evolutionary 1942) BAF396601.1^, Saemundssonia grylle (O. Fabricius, distances used to infer the phylogenetic tree. The evolutionary 1780) BAF396602.1^, Saemundssonia hexagona (Giebel, distances were computed using the maximum composite like- 1874) BAF396603.1^ and Saemundssonia lari (O. Fabricius, lihood method (Tamura et al. 2004) and are in the units of the Author's personal copy

Parasitol Res (2015) 114:2587–2597 2591 number of base substitutions per site. All positions of the Saemundssonia laticaudata is known from terns of the ge- sequences containing gaps and missing data were eliminated nus Thalasseus (see Price et al. 2003, p. 293), which are large from the dataset, and a total of 359 positions were used to terns, and it is among the largest species of Saemundssonia- produce the final results. Mega 4 software was used for align- infesting terns. Our record of this species from white-cheeked ment and phylogenetic analysis (Tamura et al. 2004). terns is regarded as the result of a host-switching event due to To test the relation between the intensity of louse infestations some behavioural and ecological factors that are discussed and tern breeding behaviour, numbers of individuals of below. The male genitalia of this species are characterized Saemundssonia lice that parasitized each tern of the seven spe- by wide, long parameres and thick endomeres and mesosome cies were tabulated, excludingthelicefrom14white-cheeked of equal length (Fig. 3(1)). terns examined in Karan Island, which belong to a different Material examined (lice, n=291) species from that found on the other two populations of Ex T. bengalensis (n=46): 108♂,115♀, Karan Island, white-cheeked terns surveyed for lice (see BDiscussion^). The Jubail Marine Wildlife Sanctuary, Arabian Gulf, 14–17 Jun. observed variance in each particular variable is partitioned into 2012 components attributable to different sources of variation. Data Ex T. sandvicensis (n=2): 1♂,2♀, Karan Island, Jubail were first tested for homogeneity using the Levene test, and the Marine Wildlife Sanctuary, Arabian Gulf, 16 Jun. 2012 results are given as nonhomogeneous variances. So, Welch Ex T. bergii (n=9): 16♂, 18♀, Karan Island, Jubail Marine ANOVA was used to compare means of louse load on each Wildlife Sanctuary, Arabian Gulf, 16 Jun. 2012 species of tern. Due to unequal sample sizes, the post hoc Ex Sterna repressa (n=14): 10♂, 21♀, Karan Island, Jubail Games-Howell test was used to achieve more accurate results Marine Wildlife Sanctuary, Arabian Gulf, 12–13 Jun. 2012 and indicate significance of differences between means. The overall mean of louse load was 3.6 with standard error 0.26. Saemundssonia melanocephalus (Burmeister, 1838) Statistically analyses were achieved using SPSS ver. 22 IPM. Samples were photographed using a Panasonic FT2 camera (Figs. 2(2) and 3(2)) 14MP over a Nikon microscope eclipse 80i, while the bird Docophorus melanocephalus Burmeister, 1838, p. 426 photos were taken by a Canon Sx40, Sx50 bridge camera Saemundssonia melanocephalus (Burmeister, 1838); Clay and Nikon d5200. The final clear photos were produced using 1949, p. 11, figs 8, 11, 19 and 28–29 Photoshop Lightroom version 4. All collected samples were Saemundssonia melanocephalus is known from two spe- deposited in the collection of the King Saud University Mu- cies of terns: Sternula albifrons and Sternula nereis (see Price seum of Arthropods (KSMA). et al. 2003, pp. 292–293, as BSterna^), the latter being a vul- nerable endangered species. We report Saemundssonia melanocephalus for the first time from Saunders’stern Results (Sternula saundersi). This louse species is characterized by short, wide and curved parameres and strongly sclerotized Atotalof129ternindividuals were captured during 2012–2013: endomeral tips in the male genitalia (Fig. 3(2)). two Sandwich terns, seven Saunders’sterns,nineswiftterns,19 Material examined (lice, n=11) bridled terns, 46 white-cheeked terns and 46 lesser crested terns. Ex Sternula saundersi (n=7): 4♂,7♀, Farasan Island, White-cheeked terns and Saunders’sternsweresearchedforlice southern end of the Red Sea, 23–26 Mar. 2013 for the first time. The total number of Saemundssonia lice collected from all tern species was424individuals,belongingto Saemundssonia meridiana Timmermann, 1950 four species: Saemundssonia laticaudata (Rudow, 1869), Saemundssonia melanocephalus (Burmeister, 1838), (Figs. 2(3) and 3(3)) Saemundssonia meridiana Timmermann, 1950 and Saemundssonia meridiana Timmermann, 1950, p. 1, fig. 1 Saemundssonia sternae (Linnaeus, 1758). The infestation rate Saemundssonia meridiana Timmermann, 1950; Price et al. was 97.7 %, as only three terns were found free of lice. 2003, p. 235 Saemundssonia meridiana was originally described from Species recorded bridled terns (O. anaethetus), and it has not been recorded from any other host (Price et al. 2003,p.235).Itcanbedistinguished Saemundssonia laticaudata (Rudow, 1869) from other species of Saemundssonia by the male genitalia, in particular the long (over 0.33 mm) and narrow parameres and (Figs. 2(1) and 3(1)) short endomeres and mesosome (Fig. 3(3)). Docophorus laticaudatus Rudow, 1869, p. 12 Material examined (lice, n=46) Saemundssonia laticaudata (Rudow, 1869); Clay 1949, p. Ex O. anaethetus (n=19): 8♂,9♀, Umm Al-Malik Island, 14, figs 7, 18 and 26–27 northern Red Sea, 12 Nov. 2011; 6♂, 12♀, Jana Island, Jubail Author's personal copy

2592 Parasitol Res (2015) 114:2587–2597

Fig. 2 Male habitus: (1) Saemundssonia laticaudata; (2) S. melanocephalus; (3) S. meridiana; (4) S. sternae

Marine Wildlife Sanctuary, Arabian Gulf, 14–15 May 2012; shorter endomeres and mesosome, and a long penis which ex- 3♂,8♀, Karan Island, Jubail Marine Wildlife Sanctuary, Ara- ceeds the length of the mesosome (Fig. 3(4)). bian Gulf, 11 Jun. 2012 Material examined (lice, n=98) Ex Sterna repressa (n=32): 21♂, 35♀ Umm Al-Malik Is- Saemundssonia sternae (Linnaeus, 1758) land, northern Red Sea, 12 Nov. 2011; 18♂, 24♀ Jana island, Jubail Marine Wildlife Sanctuary, Arabian Gulf, 16–17 (Figs. 2(4) and 3(4)) May 2012 Pediculus sternae Linnaeus, 1758, p. 612 Saemundssonia sternae (Linnaeus, 1758); Clay 1949, p. 4, Phylogeny figs 1–6, 16 and 22–23 Saemundssonia sternae is among the earliest species of Using available molecular data, we tested three species of chewing lice described from marine birds. It is currently known Saemundssonia from terns and four other species from other to infest four species of terns of the genus Sterna (see Price et al. host groups to determine their relationships and to compare 2003,p.237).Wehavecollectedthisspeciesfromthewhite- with the hosts’ relationships. cheeked tern (Sterna repressa)forthefirsttime.Themalegen- The evolutionary history was first inferred using the maxi- italia are similar to those of Saemundssonia laticaudata,but mum parsimony (MP) method. Themostparsimonioustreeis they can be distinguished by slightly narrower parameres, shown in Fig. 4.Inthistree,Saemundssonia meridiana appears Author's personal copy

Parasitol Res (2015) 114:2587–2597 2593

Fig. 3 Male genitalia: (1) Saemundssonia laticaudata; (2) S. melanocephalus; (3) S. meridiana; (4) S. sternae

as an outgroup to all the other Saemundssonia species, and very phylogeny of the lice is partially compatible with that of their far from Saemundssonia lari. In turn, Saemundssonia lari host birds. forms a clade with Saemundssonia grylle from guillemots. The unrooted tree produced by the same method (Fig. 5(2)) The remaining two species of Saemundssonia from terns shows that Saemundssonia meridiana, Saemundssonia (Saemundssonia sternae and Saemundssonia lockleyi)appear lockleyi and Saemundssonia hexagona are closely related, as a monophyletic group, but polyphyletic to the other with Saemundssonia sternae placed close to this group. Also, Saemundssonia species. This phylogeny of the lice is totally this tree indicates the relatively close relationship between incompatible with that of their host birds. Saemundssonia lari and the Saemundssonia species from Asecondphylogenetictreewasproducedusingthe terns. Although the guillemot Saemundssonia grylle is placed neighbour-joining (NJ) method. The optimal tree with the far from all other species, it is still closer to the puffin sum of branch length=8.1474 is shown in Fig. 5(1). In this Saemundssonia fraterculae than the other Saemundssonia. tree, Saemundssonia meridiana is included within a cluster together with the other two species of tern lice but, also, with Analysis of variance among parasite loads on each tern Saemundssonia hexagona from red-tailed tropicbirds. species Saemundssonia lari is a paraphyletic with the Saemundssonia cluster containing tern lice, and the remaining two species The ANOVA test indicates that there are significant differ- (Saemundssonia grylle and Saemundssonia fraterculae) are ences among means of parasite load on each tern species un- monophyletic, thus reflecting their hosts’ relationship. This der the test at a P value less than 0.05, as the P value in the test Author's personal copy

2594 Parasitol Res (2015) 114:2587–2597

and swift terns (four), but in turns, it shows a good difference from the other three species: Saunders’s terns (two), bridled terns (three) and white-cheeked terns (five). The remaining results indicated that there are no significant differences among the other five species of terns (one, two, three, four and five) (Table 3).

Discussion

The diversity of ectoparasites is not completely understood through different parts of the world, as many new species and new records are discovered every year (Sychra et al. 2007; Enout et al. 2012; Valim and Palma 2015). The ectoparasites of marine birds from the Arabian Peninsula are poor- ly known, with only few published reports from the region (e.g. Negm et al. 2013; Al-Ahmed et al. 2014) and scattered records of species in publications dealing with taxonomic units covering the world (e.g. Clay 1949, p. 14; Ward 1955, Fig. 4 Phylogeny tree based on maximum parsimony analysis of COI p. 88; Ryan and Price 1969, p. 821). This scarcity of data on gene alignment for seven species of genus Saemundssonia. Host birds ectoparasites is incompatible with the great diversity of marine appear as icons for each species; louse species associated with terns are marked by small red circles avifauna in this part of the world (Porter and Aspinall 2010). The position of the Arabian Peninsula between two warm water bodies and with a tropical climate makes it a very suit- is equal to 0.029. The Games-Howell test clarifies this result able place for many species of terns to breed (Shobrak et al. by giving a level of significant differences between each tern 2003). Considering the species of Saemundssonia from terns, species. The parasite load on lesser crested terns (six) shows the review by Ward (1955) is the last relatively comprehensive no significant difference from that of Sandwich terns (one) study of this group of lice.

Fig. 5 (1) Phylogeny tree based on neighbour-joining analysis of COI gene alignment for seven species of genus Saemundssonia. Host birds appear as icons for each species; louse species associated with terns are marked by small red circles. (2) Unrooted tree of the same species of Saemundssonia Author's personal copy

Parasitol Res (2015) 114:2587–2597 2595

Table 3 Parasite loads. Overall results of ANOVA test, including Host Mean Number of samples Standard error Non-significant ranges non-significant ranges Supplementary file 1 Lesser crested tern 5.265 43 0.5296 a Swift tern 3.4 10 0.636 ab Sandwich tern 3 2 1.5 ab White-cheeked tern 2.96 33 0.3183 b Bridled tern 2.3 20 0.3 b Saunders’s tern 1.5 7 0.5714 b

During this study, four species of Saemundssonia were controversial among scientists not only for chewing lice but identified. Three of them are recorded for the first time in also for other parasites (Zuo et al. 2011). the Arabian Peninsula. Also, six new host-louse associations Our study of phylogenetic relationships among some spe- have been established for this region, three of which are re- cies of Saemundssonia indicated that the tree which is pro- ported for the first time in the world: two from Sterna repressa duced by NJ is likely to be more accurate than that produced and one from Sternula saundersi (Table 1). by MP, if we accept known evolutionary relationships of the Considering previously published records of hosts and assume that host-louse cospeciation events deter- Saemundssonia from terns (Price et al. 2003, p. 293), our mined most of the present-day-tern Saemundssonia associa- collections of Saemundssonia meridiana from bridled terns tions. However, considering the large number of known spe- (O. anaethetus) and of Saemundssonia laticaudata from the cies of Saemundssonia, our sample size is too small to reach three species of terns of the genus Thalasseus breeding in our definite conclusions. However, the main aim of our phyloge- region were expected. However, our finding of netic analysis of those seven species of Saemundssonia was to Saemundssonia laticaudata on 14 white-cheeked terns (Ster- evaluate the relationship between Saemundssonia meridiana na repressa) in Karan Island was totally unexpected because from bridled terns and Saemundssonia lari from gulls, which white-cheeked terns were found parasitized by share some features in the male genitalia. The results indicate Saemundssonia sternae in two other, widely separate locali- that, although the male genitalia of Saemundssonia meridiana ties: Jana Island in the Arabian Gulf and Umm Al-Malik somewhat differ from those of other tern Saemundssonia, this Island in the Red Sea. Karan Island is an important habitat species is more closely related to them than to Saemundssonia for breeding of lesser crested terns (T. bengalensis), as lari.Also,ourphylogenetictreeshowsa paraphyletic well as swift terns and Sandwich terns, but at the same relationship between species of Saemundssonia from time, it also sustains a small population of white-cheeked terns and Saemundssonia lari,thussupportingthesep- terns. aration of gulls and terns into two families, Laridae and After eggs hatch, chicks of both lesser crested and white- Sternidae, respectively, rather than merging them into a cheeked terns move to the shore where they come in contact single family. with each other. Considering the much larger number of lesser Our statistical analysis of louse loads on each species of crested terns, the transfer of Saemundssonia laticaudata onto tern shows that lesser crested terns, which breed aggregated, white-cheeked terns is likely to occur. The white-cheeked tern have the highest mean of parasite load (Table 3). Our field population in Karan is completely isolated from other popu- observations show that Sandwich terns and swift terns also lations of this species on other islands, the closest being on have an aggregated breeding behaviour, and usually, they Jana Island, which had no Saemundssonia laticaudata but are incorporated within colonies of lesser crested terns. Con- Saemundssonia sternae, equal to the distant population on sidering that they are all parasitized by the same Umm Al-Malik Island in the Red Sea (see above). Also, we Saemundssonia species, Saemundssonia laticaudata,we found no mixed species of Saemundssonia on any of the three found no significant differences among the parasite load populations of white-cheeked terns surveyed for lice. In con- means on these three tern species. On the other hand, the clusion, we believe that the new host-louse association be- breeding ecology of the other three terns we studied is tween Saemundssonia laticaudata and white-cheeked terns completely different. Saunders’s terns breed in isolation from is most likely due to a host-switch event from Thalasseus each other, with nests separated by distances which may ex- terns, with the consequent extinction of Saemundssonia ceed 100 m. Bridled terns form colonies of a hundred birds, sternae. Further sampling of lice from white-cheeked terns is but their nests are completely separated, placed under shrubs needed to find out if Saemundssonia laticaudata is indeed and other types of vegetation. White-cheeked terns form small permanently established on this tern, thus confirming our colonies consisting of 20–30 nests, usually separated by dis- host-switching hypothesis. Finally, the host selection and the tances of at least 1 m. Parasite loads on the three terns with an ability of the parasite to differentiate between hosts are still isolated breeding behaviour show a significant difference with Author's personal copy

2596 Parasitol Res (2015) 114:2587–2597 that of the highly aggregated lesser crested tern (Table 3). This associated with birds of the Cerrado in Central Brazil. Parasitol result agrees with the conclusions reached by Rózsa et al. Res 111:1731–1742 Giebel CGA (1874) Insecta epizoa. Die auf Säugetieren und Vögeln (1996) from an analysis of louse loads on rooks and crows schmarotzenden Insecten nach Chr. L. Nitzsch’s Nachlass bearbeitet. (Corvidae). However, the absence of significant differences Leipzig: Otto Wigand. xvi+308 pp., 20 pls that we found between parasite loads on Saunders’s, bridled Harrison LJS (1916) The genera and species of Mallophaga. Parasitology and white-cheeked terns on one hand and those of the other 9(1):1–156 Jennings MC (2010) Atlas of the breeding birds in the Arabia Peninsula. two aggregated terns (Sandwich and swift terns) may be due Fauna of Arabia 25. 751 pp to the small sample size of the latter two species. Kasambe R, Deshmukh V (2011) Ring recoveries of lesser crested tern More work is needed to achieve a better understanding of Thalasseus benghalensis along the Maharashtra coast, India. Indian interactions between terns and their Saemundssonia lice, es- BIRDS 7(3):88–89 Kellogg VL, Kuwana SI (1902) Papers from the Hopkins Stanford pecially obtaining molecular data of more species of Galapagos expedition, 1898–1899. X. Entomological results (8). Saemundssonia. Also, knowledge of the diversity of chewing Mallophaga from birds. J Wash Acad Sci 4:457–499, 4 pls lice from wild birds in the Middle East is still very sparse and Kellogg VL, Paine JH (1910) Mallophaga from the birds of Laysan in great need of further study. Island. Entomol News 21(3):124–125 Larsson H, Olsen KM (2010) Terns of Europe and North America. Helm identification guides. Bloomsbury Publishing, London, p 224 Acknowledgments This work is part of a Ph.D. study of the last author Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum concerning the diversity of chewing lice associated with the bird fauna of classes, ordines, genera, species, cum characteribus, differentiis, Saudi Arabia. The authors extend their appreciation to the Deanship of synonymis, locis. Tenth Edition. Volume 1. Holmiae: Laurentii Scientific Research at King Saud University for funding this work Salvii. 824 pp through research group named BInsect Vector Borne Diseases^. Great Martin G (2004) Birds of the world. Harry N. Abrams, Inc, U.S.A, 294 pp appreciations are also due to HH Prince Bander Bin Saud Bin Negm MW, Nasser MG, Alatawi FJ, Al Ahmad AM, Shobrak M (2013) Mohammad, the president of Saudi Wildlife Authority, for his sponsor- Feather mites of the genus Zachvatkinia Dubinin, 1949 (Astigmata: ship of the study of ectoparasites of wild birds in the kingdom. Also, we Analgoidea: Avenzoariidae) from Saudi Arabia: a new species and would like to thank the Saudi Wildlife Committee for supporting this two new records. Zootaxa 3710(1):61–71 study during field survey trips to protected areas, especially Dr. Ahmed Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford Mansy and Mr. Anas Sambas. Also, we appreciate the suggestions of University Press, New York, p 128 Prof. Boris Kondratieff from Colorado State University, USA, during Palma RL (2000) The species of Saemundssonia (Insecta: Phthiraptera: the preparation of this manuscript. Eslam M. Abdel-Salam, Walid Ben Philopteridae) from skuas (Aves: Stercorariidae). N Z J Zool 27(2): Romdhane and Eid Ibrahim Plant Production Department, College of 121–128 Food and Agricultural Sciences, King Saud University, are appreciated Palma RL (2012) Three new species of the louse genus Saemundssonia for their help in statistical analysis. (Insecta: Phthiraptera: Philopteridae). Zootaxa 3478:38–48 Porter R, Aspinall S (2010) Birds of the Middle East, 2nd edn. Princeton Ethical statement The authors declare that the present study followed University Press, Princeton, p 400 the ethical standards and the ethical rules applicable for this journal and Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (2003) no conflict of interest. The handling of wild birds was done under per- The chewing lice: world checklist and biological overview. Illinois mission of the Saud Wildlife Committee and according to international Natural History Survey, 24, x+501 pp standards. Rózsa L, Rékási J, Reiczigel J (1996) Relationship of host coloniality to the population ecology of avian lice (Insecta: Phthiraptera). J Anim Ecol 65:242–248 Rudow F (1869) Beitrag zur Kenntniss der Mallophagen oder Pelzfresser. References Neue exotische Arten der Familie Philopterus. Inaugural— Dissertation, Universität zu Leipzig. Druck von Wilh. Plötz, Halle. Al-Ahmed A, Shobrak M, El-D NMG (2014) Chewing lice (Phthiraptera: 47 Amblycera, Ischnocera) from Red Sea gulls with new host-parasite Ryan SO, Price RD (1969) A review of the genus Eidmanniella records. Zootaxa 3790(4):567–576 (Mallophaga: Menoponidae) fromthePelecaniformes.Ann Burmeister H (1838) Mallophaga. In: Handbuch der Entomologie. 2(1), Entomol Soc Am 62(4):817–823 418–443. Enslin, Berlin Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425 Clay T (1949) Species of the genus Saemundssonia (Mallophaga) from Shobrak MY, Aloufi AA (2014) Status of breeding seabirds on the the Sterninae. Am Mus Novit 1409:1–25 Northern Islands of the Red Sea, Saudi Arabia. Saudi J Biol Sci Cottridge D (2006) A photographic guide to birds of the Middle East. 21:238–249 New Holland Publishers, United Kingdom, p 63 Shobrak M, Alsuhaibany A, Al-Sagheir O (2003) The Regional Del Hoyo J, Collar N (2014) HBW and Birdlife International illustrated Organization for the Conservation of the Environment of the Red checklist of the birds of the world. Volume 1: Non-passerines. Lynx Sea and Gulf of Aden. Status of breeding seabirds in the Red Sea Edicions in association with BirdLife International, Barcelona. 904 and Gulf of Aden. PERSGA Technical Series 8:1–70 Eck RV, Dayhoff MO (1966) Atlas of protein sequence and structure. Sychra O, Naz S, Rizvi SA (2007) New record of Afrimenopon waar National Biomedical Research Foundation, Silver Springs, (Eichler) (Phthiraptera: Menoponidae) from budgerigar Maryland Melopsittacus undulates (Psittaciformes: Psittacidae) from Eichler W (1953) Mallophagen. In: niethammer, G., Zur vogelwelt Karachi. Pakistan Parasitol Res 101:505–509 boliviens. Bonn zool Beitr 4(3–4):195–303 Symens P, Al-Suhaibany A (1996) Status of the breeding populations of Enout AMJ, Lobato DNC, Diniz FC, Antonini Y (2012) Chewing lice terns (Sternidae) along the eastern coast of Saudi Arabia following (Insecta, Phthiraptera) and feather mites (Acari, Astigmata) the 1991 Gulf War. In: A marine wildlife sanctuary for the Arabian Author's personal copy

Parasitol Res (2015) 114:2587–2597 2597

Gulf. Environmental Research and Conservation Following the Touleshkov K (1959) Two new mallophag [sic] species on the species of 1991 Gulf War Oil Spill. F. Krupp, A. H. Abuzinada and I. A. the larine family. C R Acad Bulg Sci 12(6):557–559 Nader (eds) 1996. NCWCD, Riyadh and Senckenberg Research Valim MP, Palma RL (2015) A new genus and two new species of feather Institute. Frankfurt and Main lice (Phthiraptera: Ischnocera: Philopteridae) from New Zealand en- Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large demic passerines (Aves: Passeriformes). Zootaxa 3926:480–498 phylogenies by using the neighbor-joining method. Proc Natl Ward RA (1955) Biting lice of the genus Saemundssonia (Mallophaga: Acad Sci U S A 101:11030–11035 Philopteridae) occurring on terns. Proc U S Nat Mus 105(3353):83– Timmermann G (1936) Saemundssonia nov. gen., ein neues 100 Mallophagengenus, aufgestellt für Philopterus gonothorax (Giebel) Welty JC, Baptista L (1990) The life of birds, 4th edn. Harcourt Brace und verwandte Arten. Zool Anz 114(3–4):97–100 Jovanovich College Publishers, Fort Worth, p 398 Timmermann G (1950) Saemundssonia meridiana n. sp., eine Zuo XH, Guo XG, Zhan YZ, Wu D, Yang ZH, Dong WG, Huang LQ, bemerkenswerte neue Mallophagenart von Sterna anaethetus Ren TG, Jing YG, Wang QH, Sun XM, Lin SJ (2011) Host selection Scopoli. Parasitol News 1(1):1–4 and niche differentiation in sucking lice (Insecta: Anoplura) among Timmermann G (1961) Ein neuer Seeschwalbenkneifer (Mallophaga, small mammals in southwestern China. Parasitol Res 108:1243– Philopteridae) aus Argentinien. Bonn zool Beitr 12(1/2):65–67 1251