(Phthiraptera) Infesting Crab Plover Dromas Ardeola

Acta Tropica 150 (2015) 171–175

Contents lists available at ScienceDirect

Acta Tropica

journal homepage: www.elsevier.com/locate/actatropica

Little known chewing lice (Phthiraptera) infesting crab plover Dromas

ardeola Paykull, 1805 (Charadriiformes: Dromadidae) from the Red Sea

a b a a,∗

Azzam Alahmed , Mohammed Shobrak , Salah Kheir , Mohamed Nasser

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

Saudi Arabia

Departments of Biology, Science College, Ta’if University, Ta’if, Saudi Arabia

a r t i c l e i n f o a b s t r a c t

Article history: Scanty information is available for many species of chewing lice of marine birds. Through this work we

Received 1 April 2015

investigated one of most characteristic marine bird for chewing lice. Seven individuals of crab plovers Dro-

Received in revised form 26 July 2015

mas ardeola Paykull, 1805 were trapped using standard mist nets on Humr Island in Farasan Archipelago,

Accepted 27 July 2015

Saudi Arabia. Two species of chewing lice were found to infest these birds: Actornithophilus ardeolae

Available online 29 July 2015

Timmermann, 1954 of suborder Amblycera and Quadraceps brunneus (Nitzsch in Giebel, 1866) of sub-

order Ischnocera. Diagnostic characters, data of specimens examined, high deﬁnition photos and host

Keywords:

distribution map are provided through this paper.

Chewing lice

Crab plover

Actornithophilus ardeolae

Quadraceps brunneus

Saudi Arabia

1. Introduction et al. (2013) recorded for the ﬁrst time the feather mite Zachvatkinia

(Zachvatkinia) dromae Mironov, 1992 on crab plover from the Red

The Crab plover Dromas ardeola Paykull, 1805 is a character- Sea, but no data is available for chewing lice of this bird through

istic unique sea bird and the only member of family Dromadidae the region. There are three species of chewing lice known to infest

(Jennings, 2010; Clements et al., 2014). Until recently, little was crab plover: Actornithophilus ardeolae Timmermann 1954 of sub-

known about the ecology and behavior of the crab plover, due to its order Amblycera and Lunaceps numenii numenii (Denny, 1842) and

remote and often inaccessible breeding localities (Newton and Al Quadraceps brunneus (Nitzsch in Giebel, 1866) of suborder Ischno-

Suhaibany, 1996). However, during the last few decades this species cera (Price et al., 2003; Gustafsson and Olsson 2012), but only little

has received a more comprehensive research attention throughout information is known about these interesting species of chewing

its range in the Red Sea and western Indian Ocean (Fig. 1) (Shobrak, lice. The aim of this work was to collect new material of chewing

et al., 2002; De Marchi, et al., 2006; Delany et al., 2009; Tayefeh lice from this bird for the ﬁrst time from the Red Sea population,

et al., 2011; Almalki, 2014 Delany et al., 2009; Tayefeh et al., 2011). identifying the collected samples giving clear diagnostic charac-

Crab plover is a very shy bird which rarely seen through mainland ters and high deﬁnition images for them and giving notes on how

coastal lines and urbanized shores (De Marchi et al., 2008). chewing lice invade the marine world through the bodies of sea

Through the last few years, the study of marine birds ectopara- birds.

sites have been accelerated either due to the faunistic important

of these creatures or the impact of their hosts on health of our 2. Material and methods

oceans and seas (González-Acuna˜ et al., 2011; Gomes et al., 2014;

Al-Ahmed et al., 2014; Mironov, 2014; Mironov et al., 2015). Negm As a part of large study concerning breeding distribution and

conservation of crab plover (Almalki et al., 2014), seven individu-

als of crab plover were caught during the breeding seasons from

◦

Humr Island, Farasan Archipelago, Saudi Arabia (16 47 11.56 N,

Abbreviation: HL, head length; HW, head width; HI, head index; TL, thorax ◦

42 0 23.65 E). The standard mist nets that were hung through

length; AL, abdomen length; Mg, male genitalia.

∗

crab plover colony were used to trap the birds during nights. The

Corresponding author.

E-mail address: [email protected] (M. Nasser). catching of bird alive was one of most difﬁcult mission on this

http://dx.doi.org/10.1016/j.actatropica.2015.07.025

172 A. Alahmed et al. / Acta Tropica 150 (2015) 171–175

Fig. 1. Crab Plover distribution map on the western Indian Ocean (red spot indicate the place of samples collection).

study. The handling of this wild bird was done under permission

of Saudi Wildlife Commission and all the trapped individuals were

released unharmed on the same place of capturing. Lice were col-

lected manually with a forceps under strong light. Samples were

preserved in 70% alcohol and then transferred to lactic acid for two

days for clearing and mounted using Puri’s media. Lice were iden-

tiﬁed and described according to (Timmermann, 1952, 1954; Clay,

1951, 1962, 1969). Samples were photographed using Panasonic

FT2 camera 14MP over Nikon microscope eclipse 80i, while the

ﬁeld photos were taken by Canon Sx40HS bridge camera. All lice

specimens are deposited in the King Saud University Museum of

Arthropods, King Saud University, Riyadh.

3. Results

A total number of 24 lice samples were collected from seven

individuals of crab plovers. Three hosts were free of lice. The sam-

ples were representing two previously known species of chewing

lice that have been collected from this bird from tropical coasts of

Africa (Timmermann, 1952, 1954).

Species recorded:

Suborder: Amblycera

Family: Menoponidae

Actornithophilus ardeolae Timmermann 1954:837 (Fig. 2a)

Known hosts: Dromas ardeola Paykull, Crab plover (Charadri-

iformes: Dromadidae).

Head trilobed, marginal seta near the base of labial palp longer

than the palp length, temple with three very long marginal tem-

poral seta the ﬁrst one smaller than the others, gula with only two

small lateral seta, antenna completely covered by antennal fossae;

thorax well developed, prothorax without dorsal seta, meso and

meta thorax not clearly separated, mesosternal plate with 3 cen-

Fig. 2. (a) Male Actornithophilus ardeolae, (b) Head of Actornithophilus ardeolae

tral small setae, metanoutum with long anterior seta; legs stout at showing complete chaetotaxy on the left and the head out line on the right, and

base with many scattered spines especially on the margin of tibia, (c) Male genitalia.

third femur with group of (15–18) spine like seta, also it have scat-

tered marginal seta, third tibia with clear 5 separated marginal seta;

abdomen fusiform, tergite I with only marginal row of seta tergite

VI and VII with more central setae, tergum of last abdominal seg- Key characters: Head with characteristic pattern that sepa-

ment without anterior setae, black-brown pleurite are separated rated this species from any other species of the genus (Fig. 2b),

from the yellow-brown sternites by a bright zone, only the seg- ﬁrst abdominal segment with only one dorsal row of setae, the

ment IV with clear brush on ventral side; male genitalia acute on male genitalia very characteristic with its long and acute tips of

its inner tip, highly chitinized reach second segment backward. parameres (Fig. 2c).

A. Alahmed et al. / Acta Tropica 150 (2015) 171–175 173

Material examined (3): Humr Island near the coast of Farasan 2014). Throughout this work, two new records of chewing lice were

Island 17 Jul. 2012 M (2), N (1) crushed. added to Saudi Arabia and Red Sea parasitic fauna for the ﬁrst time.

Measurements in mm for male The clear diagnostic characters and high deﬁnition photos provided

in this paper are the only available for these lice in all previous.

H.L. 0.33

Considering previously published records of chewing lice

H.W. 0.5

H.I 0.66 on crab plover through its range in western Indian Ocean

T.L. 0.4

(Timmermann, 1952, 1954; Clay, 1962), anyone can note that only

A.L. 1

few individuals of chewing lice usually collected from this bird. This

Total length 1.73 0.2 (M g: 0.6)

may be due to the solitary behavior that the host shows through

Suborder: Ischnocera

most duration of its life. Although, crab plover forms relatively

Family: Philopteridae

dense ﬂocks at high tide in the wintering areas, there individu-

Quadraceps brunneus (Nitzsch in Giebel, 1866):373 (Fig. 3a and

als are a way to come in direct contact except during the breeding

seasons. Also, the nature of the bird breeding behavior of using

Nirmus brunneus Nitzsch in Giebel, 1866

underground nests decreases the contact between chicks through

Docophorus antennatus Piaget, 1880:101

its breeding individuals (Newton and Al Suhaibany, 1996). Combin-

Nirmus stictochrous Nitzsch in Giebel, 1866:374

ing these facts with the very few methods that available for chewing

Known hosts: Dromas ardeola Paykull, Crab plover (Charadri-

lice to transfer from one bird to another that depend on direct con-

iformes: Dromadidae).

tact between bird individuals (Price et al., 2003), we can understand

Sexual dimorphism appear clearly in this species as male usu-

why many individuals of this bird are free of lice or have very few

ally with highly chitinized dark body while female with white color

population of this ectoparasites.

very low chitinization with small black spots decoration. Head con-

According to previous chewing lice records, the present of Actor-

ical in shape, hyaline margin well developed with small anterior

nithophilus ardeolae and Quadraceps brunneus infesting crab plover

seta, frontal part slightly expanded, clypeal notched medially with

forms a normal ectoparasite/host interaction and the two species

characteristic signature in male (Fig. 3c), the last antennal segment

could be consider endemic parasite to crab plover as they never

brown in color in male and female, antennal cavity surrounded by

recorded before from any other marine birds (Price et al., 2003).

two dark black spots (the preantennal nodi and the preocular nodi)

The third species of chewing lice that recorded from crab plover

in both sexes, temple is rounded with clear brown spots decoration

was Lunaceps numenii numenii (Denny, 1842) (Gustafsson and

in male and white in female with two strong marginal temporal

Olsson, 2012) and this species did not collected from Farasan Island

setae on each side; prothorax small, mid and meta thorax fused

population. The occurrence of Lunaceps numenii numenii on crab

with extremely dark margin, legs unequal in length with small

plover could be doubtful because this species of lice are infesting

fore legs and long hind legs; abdomen oval in shape with blackish

three unrelated host to the crab plover (Eurasian curlew Numenius

brown bordering, in female the segments 5th–7th with median yel-

arquata (L., 1758) (type host), Far Eastern Curlew Numenius mada-

low brown spots that become larger on 7th segment; the terminal

gascariensis (L., 1766) (Pilgrim and Palma, 1982) and Long-billed

segment of female forked in the middle with small yellow–brown

curlew Numenius americanus Bechstein, 1812 (Emerson, 1972)).

spot on each side, in male the tip form a semicircle outline; male

Such record of Lunaceps numenii numenii could be either due to

genitalia oblong very characteristic through the whole genus, basal

struggling or host switching of the parasite on certain restricted

plate form two connected sclerotized bars, parameres thick taper-

population of crab plover due to some ecological circumstances in

ing toward the serpentine tips that meet in the middle, endomeral

isolated islands ecosystems such as what recently recorded host

complex broad with acute lateral tips endomeres, the penis and

switching event of Saemundssonia laticaudata (Rudow, 1869) on

accompanying telomeres oval in shape and somewhat protruding.

small isolated population of white checked tern Sterna repressa

Key characters: Head with characteristic sclerotization in male,

Hartert, 1916 (Shobrak et al., 2015).

marginal temporal seta I thick and appears over small rounded

The chewing lice of marine birds form one of most interesting

tubercles protruding from the temporal margins on each said of

group of order Phthiraptera. Most of their host birds such as auk,

the head of male and female (Fig. 3c), unique genital structure of

cormorants, crab plover, gulls and pufﬁn spend their life on the

male (Fig. 3d).

wing in open seas away from the main land (Alderton, 2008). As per-

Material examined (21): Humr Island near the coast of Farasan

manent ectoparasites, chewing lice travel with their marina hosts

Island 17 Jul. 2012, F (11), M (9).

through oceans and open seas of the world. This shows how the

Measurements in mm for female Measurements in mm for male

ancestors of such very small insects adapted themselves to invade

H.L. 0.6 0.55 the marine ecosystem through the body of these hosts millions of

H.W. 0.48 0.44

years ago before many insect groups dominate the terrestrial habi-

H.I 1.25 1.25

tats. Such kind of interesting phenomena need more investigations

T.L. 0.35 0.4

to discover the complete picture of these charismatic parasites, how

A.L. 1.11 0.86

± ±

Total length 2 0.2 1.8 0.2 (M g: 0.26) they complete their life cycle? How they can with stand the long

dive of cormorants and grebes? How they can transfer from one

bird to another in cases such as appear in crab plover? And many

4. Discussion more questions that wait to be answered about this characteristic

strife between host and parasite in their race for survival.

The data available for the ectoparasites of marine birds of the

Red Sea and the Middle East is minimal (Clay, 1949; Ward, 1955;

Ryan and Price, 1969; Hafez and Madbouly, 1968; Negm et al., Acknowledgements

2013). This may be due to difﬁculties that face anyone trying

to catch this kind of birds alive without harming their breeding This work is a small part of PhD study of the last author which

colonies. This study forms the ﬁrst ﬁeld investigation for the chew- concerning the diversity of chewing lice associated with bird fauna

ing lice fauna of such kind of restrictedly distributed marine bird of Saudi Arabia. This project was funded by the National Plan For

of the region except that concerning the endemic white eyed gull Science, Technology and Innovation (MAARIFAH), King Abdulaziz

Ichthyaetus leucophthalmus (Temminck, 1825) (Al-Ahmed et al., City for Science and Technology, Kingdome Saudi Arabia, Award

174 A. Alahmed et al. / Acta Tropica 150 (2015) 171–175

Fig. 3. (a) Male Quadraceps brunneus, (b) Female Quadraceps brunneus, (c) Head of male Quadraceps brunneus showing complete chaetotaxy the black arrow indicate to

characteristic marginal temporal seta I, and (d) Male genitalia.

Number (11-ENV-1960-02). Great appreciations are also due to De Marchi, G., Chiozzi, G., Fasola, M., 2008. Solar incubation cuts down parental

care in a burrow nesting tropical shorebird, the crab plover Dromas ardeola. J.

HH Prince Bander Bin Saud Bin Mohammad, the president of Saudi

Avian. Biol. 39, 484–486.

Wildlife Commission for his acceptance of the study of ectopara-

Emerson, K.C., 1972. Checklist of Mallophaga of North America (North of Mexico).

sites of wild birds in the kingdom. Also, we would like to thank Part 1, suborder Ischnocera. Deseret Test Centre, 94.

Gomes, S.N., Pesenti, T.C., Cirne, M.P., Müller, G., 2014. Chewing lice (Phthiraptera)

Mohammed Almalki from Department of Biology and Biochemistry,

from Calidris fuscicollis (Aves: Scolopacidae) in Southern Brazil. Acta Trop. 136,

University of Bath, Bath, UK for his help during survey trips. Finally, 101–103.

we thank the anonymous reviewers for their comments and notes González-Acuna,˜ D., Corvalan, F., Barrientos, C., Doussang, D., Mathieu, C., Nilsson,

L., Casanueva, M.E., Palma, R.L., 2011. Community structure of lice (Insecta:

that help in improving our manuscript.

Phthiraptera) from two sympatric gull species: kelp gull (Larus dominicanus)

and Franklin’s gull (Larus pipixcan) in Talcahuano, Chile. Neotrop. Entomol. 40, 300–304.

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