Parasitol Res DOI 10.

1007/s00436-011-2480-7

ORIGNAL PAPER

Research and increase of expertise in arachno-entomology are urgently needed

Heinz Mehlhorn & Khaled A. S. Al-Rasheid & Saleh Al-Quraishy & Fathy Abdel-Ghaffar

Received: 5 May 2011 / Accepted: 19 May 2011 # Springer-Verlag 2011

Abstract Considering the contents of international journals of parasitology dealing with broader topics inside this field show that rather a few papers appear with studies in the discipline of arachno-entomology. In the journals Journal of Parasitology, Parasitology Research and Trends in Parasitology, the relations of published papers on protozoology, helminthology and arachno-entomology showed that in all three journals, papers on protozoans were the most common, while those on helminths of any kind reached the second place being rather as common as the protozoan papers in Parasitology Research and in the Journal of Parasitology. In Trends of Parasitology, however, the papers on helminths reached only about 25% of the numbers published on protozoan topics. But in all three journalsand this is importantthe papers on arachnoentomological themes were scarce reaching less than the half of the protozoan papers in Parasitology Research, and only about 15% in the Journal of Parasitology and in the Trends of Parasitology. These disproportions between the three great subdivisions of targets in the focus of parasitological research are dangerous, since this lack exists already for several decades and thus led to a backlog of unsolved
H. Mehlhorn (*) Department of Zoology and Parasitology, Heinrich Heine University, 40225 Dsseldorf, Germany e-mail: mehlhorn@uni.duesseldorf.de K. A. S. Al-Rasheid : S. Al-Quraishy Department of Zoology, Center of Excellence, College of Science, King Saud University, Riyahd, Saudi Arabia F. Abdel-Ghaffar College of Science, Department of Zoology, Cairo University, Giza, Egypt

increasing problems that are caused by ticks, mites, insects and/or parasitic crustaceans especially in times of intensive globalization and global warming. Studies on the biology, vectorship, invasion and spreading of wanted vectors and on the control of pests and parasites belonging to the field of arachno-entomology are urgently needed.

Introduction On occasion of the publication of the excellent (in contents and pictures) book Sick Through Arthropods (Aspck 2010) which compiles in 46 chapters, many facettes of the biology, morphology and transmission activity of many important insects, mites and ticks, it became again obvious that the field of arachno-entomology is extremely important. There is no doubt that ticks, mites and insects are dangerous vectors of often deadly agents of diseases (Figs. 1, 2 and 3), which may hit as epidemics or pandemics in the increasing world population of humans and animals (Mehlhorn 2008; Brooks and Hoberg 2007; Dobler 2008; Polley and Thompson 2009). Since in times of intense globalization and global warming, arthropods have proven to be able to settle and spread at places far away from their normal environment, they are also able to transport inside their bodies agents of diseases during their migration or to become infested in their new surroundings by local parasites, bacteria and/or viruses. The sudden outbreak in the year 2006 of the Bluetongue disease in whole Central Europe and its huge death toll among infected ruminants (4% of infected cattle and up to 40% of infected sheep died) is an example, how easy it was to produce a sudden terror among Europeans, who believed to live on "a safe and blessed island" (Kiehl et al. 2009; Mehlhorn et al. 2007, 2008, 2009a, b; Carpenter et al. 2008; Conraths et al. 2008;

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Fig. 1 Micrograph of a female Dermacentor reticulatus tick, an invader into Germany coming from the South of Europe and being vector of Babesia canis

Fig. 3 Scanning electron micrograph of a female Anopheles stephensi mosquito, one of the vectors of malaria

Conraths and Mettenleiter 2011). Even today, it is not sure how this Bluetongue virus of the serotype 8 arrived in "Good old Europe". Was it included in infected midges that travelled within ship containers from Africa to The Netherlands and/or Belgium (infecting the cattle while blood sucking) or was the virus included in imported healthy appearing but silently infected antelopes finally infecting local midges (Fig. 4) during their blood meal? Similar outbreaks may occur at any time due to imported ticks, mosquitoes, sandflies, bugs, fleas, flies, tabanids, black flies, lice, ticks, mites. etc. (Dobler 2008; Aspck and Dobler 2010; Dobler and Aspck 2010a, b; Dobler 2010; Mehlhorn and Mehlhorn 2010a, b; Abdel-Ghaffar et al. 2008, 2010; Dakies 1953; Falagas et al. 2008; Kampen and Werner 2011; Lane and Crosskey 1993; Mumcuoglu and Ruffli 1983; Lscher and Burchard 2011; Martini 1946; Parola et al. 2005; Rueda 2004; Rust and Dryden 1997; Smallegange et al. 2011; Schmahl et al. 2010; Sonenshine 1991; Wenk and Schlrer 1963; Werner and Grunwald 2010; Zumpt 1965). Such an important invasion had occurred already in the USA, whenonly 12 years ago in the year 1999the West Nile virus entered New York at the Central Park (probably as result of an infection during the visit of an American in Israel) and is now spread all over the continent. Although it was found that this virus might be

spread by feeding (e.g. hawks eat other birds), the mosquito transmission has been proven to be most important (Smith 2008; Linke et al. 2007). In general, most invasions occur silently and speed up later as has been the case when Chikungunya fever virus occurred in Italy 4 years ago. Other examples are the findings that fleas might transmit a very wide spectrum of viruses (Mencke et al. 2008), that spiders might travel from the USA to Great Britain and bite their German hotel guests (Pippirs et al. 2009) or that travellers bring African tick bite fever as souvenir back home (Schuster et al. 2008). Such threatening invading agents of diseases and their vectors (Figs. 1, 2, 3, 4 and 5) which lurk ante portas of each continent for a chance to get in and to find there a silent place for undisturbed propagation, can only become controlled at a reasonable time, if details of their life cycles, their feeding and mating behaviour, their sensitivity to control measurements, etc. are known. However, when looking at the registers of the international journals in the field of parasitology, it becomes obvious that studies on ticks, mites and insects are neglected compared to papers on protozoans and helminths. Thus, the present paper risks a short glimpseof course not being totally representativeon the appearance of papers concerning arachno-entomology in three worldwide distributed journals: Journal of Parasitology, Parasitology Research and Trends in Parasitology.

Fig. 2 Micrograph of so called tiger mosquitoes (Aedes albopictus) invaders from Asia into Europe spreading the Chikungunya virus

Fig. 4 Micrograph of a female Culicoides obsoletusEuropean vector of the newly invaded Bluetongue virus serotype 8

Parasitol Res Fig. 5 Micrograph of a warmthloving sandfly of the genus Phlebotomus spreading northward. They are vectors of the Papataci fever and of leishmaniasis

book reviews and policy/guidelines). One hundred thirtythree papers dealt with protozoan research topics (on many disciplines). One hundred twenty-eight papers reported on leeches. The papers dealing with the different groups of arthropods were extremely scarce, reaching a total number of 19 (11 on ticks and mites, only 8 on insects). Parasitology Research In the case of this journal, recent issues starting in December 2008 reaching until April 2011 were considered. The evaluated volumes 104, 105, 106, 107 (each with six numbers) and the four numbers of volume 108 in 2011 comprised a total of 7,589 printed pages and contained a total of 998 articles (reviews, rapid and short communications, originals, errata). Four hundred eleven articles reported research results obtained in experiments with protozoans, 402 articles dealt with helminths of any kind, while 185 papers reported from research projects either on insects, ticks and/or mites. The number of papers on the field of arachno-entomology is, however, somewhat misleading, since in many studies, the insects, mites and ticks were not "the true objects", but only targets of control measurements. In these publications, they were submitted to different extracts of plants, insecticides or they were treated with various types of chemicals being enclosed (within or not) in nanoparticles or other carriers. Thus, the number of papers with respect to biology, genetics, morphology, behaviour, physiology, etc. of the different groups of arthropods was rather low. Trends in Parasitology In total, 30 monthly appeared numbers (issues) were considered after being selected from the 12 annual editions per year. Of the year 2007 (six numbers), 2008 (eight numbers), 2009 (five numbers), 2010 (seven numbers) and 2011 (four numbers) were checked. These in total 30 selected numbers comprised a total of 1,431 pages and 280 articles (updates: research focus, opinions, reviews, letters, errata, editorials). One hundred ninety-nine articles considered research results or diseases due to protozoans, while only 53 articles described various approaches in helminthological fields. The papers with topics belonging to the large field of arachno-entomology were scarce summing up to only 32 (6 on ticks and mites, 25 on insects and 1 one a crustacean ectoparasite). Eight articles dealt with several groups of parasites.

Methods In randomly selected volumes of three "broader" parasitological journals, the titles of papers with protozoan, helminthological and arachno-entomological topics were counted in an alphabetical order; issues of the following journals were checked: 1. Journal of Parasitology (USA) Volume 91 (2005, with six numbers) 2. Parasitology Research (Germany) Volume Volume Volume Volume Volume 104: 105: 106: 107: 108: Nos. Nos. Nos. Nos. Nos. 16 16 14 16 14 (2008, 2009) plus supplement (2009) (2009, 2010) (2010) (2011)

3. Trends in Parasitology (UK) Volume Volume Volume Volume Volume 2007: 2008: 2009: 2010: 2011: Nos. Nos. Nos. Nos. Nos. 6, 4, 1, 4, 1, 7, 5, 2, 5, 2, 8, 6, 3, 6, 3, 10, 11, 12 8, 9, 10, 11, 12 5, 6 9, 10, 11, 12 4

Results Journal of Parasitology The whole volume 91 (year 2005) was considered in the present check up. Volume 91 appeared in six numbers comprising a total of 1,512 printed pages and contained a total of 289 articles (reviews, originals, research notes, errata,

Discussion The present times are characterized by a speeding up of any globalization process, reaching unbelievable dimensions.

Table 1 Transmission and propagation of agents of disease by ticks (selected examples according to many authors) Agents of disease Diseases Transmission pathway to vertebrate hosts Transmission by feces or squeezing + + + + + + + + + Saliva Saliva Saliva Saliva Saliva + + + + + Hosts

Vectors

Soft ticks Ornithodorus species Q fever, endocarditis

Tick borne relapsing fever, borreliosis

H, A A H, A H, A H, A H, A H, A H, A H, A H, A H, A H,A D H, A

Argas species Arboviruses (V) Flavivirus (V) Bunya virus (V) Borrelia burgdorferi et al. (B) Ehrlichia, Anaplasma (B) Rocky Mountains spotted fever African tick bite fever, Q fever Fivre boutonneuse Babesiosis Tularaemia Babesiosis Eshar, Tsutsugamushi fever Human ehrlichiosis Crimean Congo haemorrhagic fever Lyme disease; tick-borreliosis

Borrelia duttoni and other Borrelia species (B) Coxiella burnetii (B)

Hard ticks Ixodes species

Ixodes and Dermacentor species

Spring-summer encephalitis, Russian encephalitis (V) Omsk haemorrhagic fever

Hyalomma species Ixodes species

Ixodes species

Dermacentor species Amblyomma species

Via saliva during short biting time of 30 min Via saliva during short biting time (20 min) Via saliva starting immediately with sucking Rare: tick saliva; common: blood contact with infected animals Blood contact and tick bites (saliva) Via saliva injection starting 812 h after attachment Via saliva injection starting 812 h after attachment Saliva Saliva

Rhipicephalus species Ixodes, Dermacentor species Dermacentor Haemaphysalis, Rhipicephalus species Dermacentor reticulatus, Rhipicephalus sanguineus Mites Trombicula akamushi

Rickettsia rickettsii (R) Rickettsia africae (R) Coxiella burnetii (B) Rickettsia conori (R) Babesia species (P) Francisella tularensis (B) Babesia canis (P) Orienta tsutsugamushi

A many animals (often as reservoir hosts), B bacteria, D dogs, H humans, P protozoans, R rickettsiae, V virus, + possible

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Thus, it takes at the maximum 24 h to travel from one end of the world to the otherand this is done daily by millions of humans and also millions of tons of food or goods which also comprise plants. Inside the bodies of those travellers, but also mingled among their luggage, among the imported plants and inside of transportation containers, cars and/or planes, there is enough space for unwanted "blind" passengers such as agents of diseases and/or vectors of agents of diseases (being already infected or not). Furthermore, the possibility that birds of passage transport inside their body agents of diseases or different vectors of diseases on their body surface must not be underestimated.

When considering the incubation period (first occurrence of symptoms of disease after an infection) and when looking at the prepatent period (time of appearance of newly transmittable agents of diseases after an infection), it becomes clear that the described short travel (or transportation) times will support an easy invasion process of agents of diseases into new countries and help to propagate there especially the agents of emerging infectious diseases (EID) besides the numerous already known diseases that are transmitted by vectors from the field of arachno-entomology (Tables 1 and 2). Since the importance of many of these actually spreading agents of diseases is often underestimated, they are also

Table 2 Transmission and propagation of agents of disease transmitted by various groups of insects Vectors Agents of disease Diseases Transmission pathway Transmission by Hosts feces or squeezing + + + + + + H, H, H, H, H, H A A A A A

Fleas (Siphonaptera) (many species)

Body lice (Pediculus humanus corporis) Raptor bugs (Triatomidae)

Rickettsia felis (R) Rickettsia typhi (R) Dipylidium caninum (T) Yersinia pestis (B) Viruses (V) Rickettsia prowazekii (R)

Flea borne spotted fever Murine spotted fever Plaque Dipylidiasis Virosis (various) Louse borne spotted fever

Trypanosoma cruzi (P)

Chagas disease Leishmaniasis Pappataci fever West Nile fever Nairobi disease Oropouche fever Bluetongue Filariasis Filariasis Virosis/fever Encephalitis Malaria Filariasis Japanese encephalitis Rift Valley virus West Nile fever Filariasis Chikungunya fever Dengue fever Yellow fever Filariasis Bacteriosis Sleeping disease Bacteriosis Loiasis

Sand flies (Phlebotomidae) Leishmania species (P) Bunyavirus (V) Midges (Ceratopogonidae) West Nile virus (V) Bunyavirus (V) Oropouche virus (V) Bluetongue virus (V) Filariae (N) Black flies (Simulidae) Filariae (N), e.g. Onchocerca Mosquitoes (Culidae), Arboviruses (V) Anopheles Bunya virus (V) Plasmodium (P) Filariae (N) Mosquitoes, Culex Flavivirus (V) Bunyavirus (V) Arbovirus (V) Filariae (N) Chikungunga virus (TO) Dengue virus (FL) Yellow fever virus (FL) Filariae (N) Bacteria (B), many species Trypanosomes (P) Bacteria (B) Filariae (N)

Intestinal contents Intestinal contents Intestinal contents Oral uptake Blood meal Mechanical input of rickettsiae into bite sites of lice Scratching in of parasites into bite sites Blood meal Blood meal Blood meal Blood meal Blood meal Blood meal Blood meal Blood meal Saliva Saliva Saliva Blood meal Saliva Saliva Saliva Blood meal Saliva Saliva Saliva Blood meal Mechanical contamination of mouth parts Blood meal Mechanical contamination Blood meal

+ + + + + + + + + + + + + + + + + + + + + + + +

H, A H, H, H, H, H A H, H, H, H, H, H, H, H, H, H, H, H, H, H, H, A A A A

A A A A A A A A A A A A A A A

Mosquitoes, Aedes

Flies, Muscidae Flies, Glossinidae Flies, Tabanidae

H, A H, A H, A

A animals (often as reservoir hosts), B bacteria, FL flavirus, H humans, N nematodes, P protozoans, T tapeworm, TO togavirus, V virus, + possible

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described as neglected diseases or neglected tropical diseases (Claczinski et al. 2007) or positive as EID. Therefore, knowledge in arachno-entomology is highly needed but actually neglected. And it will take time to increase the number of scientists working in this field so that knowledge and experience become lost worldwide every day by retirement of entomologists and acarologists. Especially more studies are needed on the following fields: Knowledge on the existence of species in local regions Observation of invading species Life cycles and current situation of invading and of local species Propagation of species in different biotopes and adaption to unfavourable conditions Food supply and benefits Modes of the development of resistances of vectors Recent sensitivity to insecticides/acaricides Development of new insecticides and acaricides, respectively new modes of application Host selection and host specification Modes how vectors find their hosts Uptake and propagation of agents of diseases by blood sucking or licking vectors Factors that are need for a successful transmission Molecular biological and genetic investigations on the relations of vector species (complexes) Importance of mechanical transmissions Biological control methods Methods to exclude or minimize long distance transportations of potentially infected vectors, etc.

These and many related other fields have to be studied intensively in order to avoid outbreaks of pandemics with potentially uncontrollable consequences on earth, which become more and more crowded and the distances of which shrink daily.
Acknowledgement We are grateful to the Center of Excellence of the College of Science of the King Saud University at Riyahd (Saudi Arabia).

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