Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Six species of terns, which breed on the Arabian Peninsula, were examined for head chewing lice of the genus Saemundssonia in four different islands around the coasts of Saudi Arabia, both in the Red Sea and in the Arabian Gulf. Four louse species were collected: Saemundssonia laticaudata, Saemundssonia melanocephalus, Saemundssonia meridiana and Saemundssonia sternae, of which three are recorded for the first time from this region. Also, we record three new host-louse associations for the world—Saemundssonia laticaudata and Saemundssonia sternae from white-cheeked terns and Saemundssonia melanocephalus from Saunders’s 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 Saemundssonia that infest marine birds were used to propose evolutionary trees using two different statistical methods: maximum parsimony (MP) and neighbour joining (NJ). The result indicated that the tree which was produced by NJ is likely to be more accurate as it appeared more compatible with hosts’ phylogeny. The trees indicate relationships between tern Saemundssonia and congeneric species from other marine birds, especially from gulls. An ANOVA was also conducted to test the mean parasite load for each tern species studied, and results indicate that there is a relation between louse loads and colonization behaviour of the hosts. Data from lice examined and illustrations of lice and their hosts are also included.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Al-Ahmed A, Shobrak M, El-D NMG (2014) Chewing lice (Phthiraptera: Amblycera, Ischnocera) from Red Sea gulls with new host-parasite records. Zootaxa 3790(4):567–576

    Article  PubMed  Google Scholar 

  • Burmeister H (1838) Mallophaga. In: Handbuch der Entomologie. 2(1), 418–443. Enslin, Berlin

  • Clay T (1949) Species of the genus Saemundssonia (Mallophaga) from the Sterninae. Am Mus Novit 1409:1–25

    Google Scholar 

  • Cottridge D (2006) A photographic guide to birds of the Middle East. New Holland Publishers, United Kingdom, p 63

    Google Scholar 

  • Del Hoyo J, Collar N (2014) HBW and Birdlife International illustrated checklist of the birds of the world. Volume 1: Non-passerines. Lynx Edicions in association with BirdLife International, Barcelona. 904

  • Eck RV, Dayhoff MO (1966) Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Springs, Maryland

  • Eichler W (1953) Mallophagen. In: niethammer, G., Zur vogelwelt boliviens. Bonn zool Beitr 4(3–4):195–303

    Google Scholar 

  • Enout AMJ, Lobato DNC, Diniz FC, Antonini Y (2012) Chewing lice (Insecta, Phthiraptera) and feather mites (Acari, Astigmata) associated with birds of the Cerrado in Central Brazil. Parasitol Res 111:1731–1742

    Article  PubMed  Google Scholar 

  • Giebel CGA (1874) Insecta epizoa. Die auf Säugetieren und Vögeln schmarotzenden Insecten nach Chr. L. Nitzsch’s Nachlass bearbeitet. Leipzig: Otto Wigand. xvi + 308 pp., 20 pls

  • Harrison LJS (1916) The genera and species of Mallophaga. Parasitology 9(1):1–156

  • Jennings MC (2010) Atlas of the breeding birds in the Arabia Peninsula. Fauna of Arabia 25. 751 pp

  • Kasambe R, Deshmukh V (2011) Ring recoveries of lesser crested tern Thalasseus benghalensis along the Maharashtra coast, India. Indian BIRDS 7(3):88–89

    Google Scholar 

  • Kellogg VL, Kuwana SI (1902) Papers from the Hopkins Stanford Galapagos expedition, 1898–1899. X. Entomological results (8). Mallophaga from birds. J Wash Acad Sci 4:457–499, 4 pls

    Google Scholar 

  • Kellogg VL, Paine JH (1910) Mallophaga from the birds of Laysan Island. Entomol News 21(3):124–125

    Google Scholar 

  • Larsson H, Olsen KM (2010) Terns of Europe and North America. Helm identification guides. Bloomsbury Publishing, London, p 224

    Google Scholar 

  • Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tenth Edition. Volume 1. Holmiae: Laurentii Salvii. 824 pp

  • Martin G (2004) Birds of the world. Harry N. Abrams, Inc, U.S.A, 294 pp

    Google Scholar 

  • Negm MW, Nasser MG, Alatawi FJ, Al Ahmad AM, Shobrak M (2013) Feather mites of the genus Zachvatkinia Dubinin, 1949 (Astigmata: Analgoidea: Avenzoariidae) from Saudi Arabia: a new species and two new records. Zootaxa 3710(1):61–71

    Article  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York, p 128

    Google Scholar 

  • Palma RL (2000) The species of Saemundssonia (Insecta: Phthiraptera: Philopteridae) from skuas (Aves: Stercorariidae). N Z J Zool 27(2):121–128

    Article  Google Scholar 

  • Palma RL (2012) Three new species of the louse genus Saemundssonia (Insecta: Phthiraptera: Philopteridae). Zootaxa 3478:38–48

    Google Scholar 

  • Porter R, Aspinall S (2010) Birds of the Middle East, 2nd edn. Princeton University Press, Princeton, p 400

    Google Scholar 

  • Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (2003) The chewing lice: world checklist and biological overview. Illinois Natural History Survey, 24, x + 501 pp

  • 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

    Article  Google Scholar 

  • Rudow F (1869) Beitrag zur Kenntniss der Mallophagen oder Pelzfresser. Neue exotische Arten der Familie Philopterus. Inaugural—Dissertation, Universität zu Leipzig. Druck von Wilh. Plötz, Halle. 47

  • Ryan SO, Price RD (1969) A review of the genus Eidmanniella (Mallophaga: Menoponidae) from the Pelecaniformes. Ann Entomol Soc Am 62(4):817–823

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Shobrak MY, Aloufi AA (2014) Status of breeding seabirds on the Northern Islands of the Red Sea, Saudi Arabia. Saudi J Biol Sci 21:238–249

    Article  PubMed Central  PubMed  Google Scholar 

  • Shobrak M, Alsuhaibany A, Al-Sagheir O (2003) The Regional Organization for the Conservation of the Environment of the Red Sea and Gulf of Aden. Status of breeding seabirds in the Red Sea and Gulf of Aden. PERSGA Technical Series 8:1–70

    Article  Google Scholar 

  • Sychra O, Naz S, Rizvi SA (2007) New record of Afrimenopon waar (Eichler) (Phthiraptera: Menoponidae) from budgerigar Melopsittacus undulates (Psittaciformes: Psittacidae) from Karachi. Pakistan Parasitol Res 101:505–509

    Article  Google Scholar 

  • Symens P, Al-Suhaibany A (1996) Status of the breeding populations of terns (Sternidae) along the eastern coast of Saudi Arabia following the 1991 Gulf War. In: A marine wildlife sanctuary for the Arabian Gulf. Environmental Research and Conservation Following the 1991 Gulf War Oil Spill. F. Krupp, A. H. Abuzinada and I. A. Nader (eds) 1996. NCWCD, Riyadh and Senckenberg Research Institute. Frankfurt and Main

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Timmermann G (1936) Saemundssonia nov. gen., ein neues Mallophagengenus, aufgestellt für Philopterus gonothorax (Giebel) und verwandte Arten. Zool Anz 114(3–4):97–100

    Google Scholar 

  • Timmermann G (1950) Saemundssonia meridiana n. sp., eine bemerkenswerte neue Mallophagenart von Sterna anaethetus Scopoli. Parasitol News 1(1):1–4

    Google Scholar 

  • Timmermann G (1961) Ein neuer Seeschwalbenkneifer (Mallophaga, Philopteridae) aus Argentinien. Bonn zool Beitr 12(1/2):65–67

    Google Scholar 

  • Touleshkov K (1959) Two new mallophag [sic] species on the species of the larine family. C R Acad Bulg Sci 12(6):557–559

    Google Scholar 

  • Valim MP, Palma RL (2015) A new genus and two new species of feather lice (Phthiraptera: Ischnocera: Philopteridae) from New Zealand endemic passerines (Aves: Passeriformes). Zootaxa 3926:480–498

    Article  PubMed  Google Scholar 

  • Ward RA (1955) Biting lice of the genus Saemundssonia (Mallophaga: Philopteridae) occurring on terns. Proc U S Nat Mus 105(3353):83–100

    Article  Google Scholar 

  • Welty JC, Baptista L (1990) The life of birds, 4th edn. Harcourt Brace Jovanovich College Publishers, Fort Worth, p 398

    Google Scholar 

  • Zuo XH, Guo XG, Zhan YZ, Wu D, Yang ZH, Dong WG, Huang LQ, Ren TG, Jing YG, Wang QH, Sun XM, Lin SJ (2011) Host selection and niche differentiation in sucking lice (Insecta: Anoplura) among small mammals in southwestern China. Parasitol Res 108:1243–1251

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work is part of a Ph.D. study of the last author concerning the diversity of chewing lice associated with the bird fauna of Saudi Arabia. The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group named “Insect Vector Borne Diseases”. Great appreciations are also due to HH Prince Bander Bin Saud Bin Mohammad, the president of Saudi Wildlife Authority, for his sponsorship of the study of ectoparasites of wild birds in the kingdom. Also, we would like to thank the Saudi Wildlife Committee for supporting this study during field survey trips to protected areas, especially Dr. Ahmed Mansy and Mr. Anas Sambas. Also, we appreciate the suggestions of Prof. Boris Kondratieff from Colorado State University, USA, during the preparation of this manuscript. Eslam M. Abdel-Salam, Walid Ben Romdhane and Eid Ibrahim Plant Production Department, College of Food and Agricultural Sciences, King Saud University, are appreciated for their help in statistical analysis.

Ethical statement

The authors declare that the present study followed the ethical standards and the ethical rules applicable for this journal and no conflict of interest. The handling of wild birds was done under permission of the Saud Wildlife Committee and according to international standards.

Author information

Authors and Affiliations

  1. Department of Biology, Science College, Ta’if University, Ta’if, Saudi Arabia

    Mohammed Shobrak & Mohammed Almalki

  2. Research Chair of Insect Vector Borne Diseases, Department of Plant Protection, College of Food and Agriculture Science, King Saud University, Riyadh, Saudi Arabia

    Azzam Alahmed & Mohamed Gamal El-Den Nasser

  3. Museum of New Zealand Te Papa Tongarewa, P.O. Box 467, Wellington, New Zealand

    Ricardo Palma

  4. Department of Biology and Biochemistry, University of Bath, Bath, UK

    Mohammed Almalki

Authors
  1. Mohammed Shobrak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Azzam Alahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricardo Palma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohammed Almalki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohamed Gamal El-Den Nasser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohamed Gamal El-Den Nasser.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(25.9 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shobrak, M., Alahmed, A., Palma, R. et al. New records of species of Saemundssonia (Insecta: Phthiraptera: Philopteridae) infesting breeding terns in the Arabian Peninsula, with notes on their phylogeny and ecology. Parasitol Res 114, 2587–2597 (2015). https://doi.org/10.1007/s00436-015-4463-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4463-6

Keywords

Search

Navigation