To date, many kinds of potential predator–prey interactions have been demonstrated between ticks and a wide range of animals, including birds, mammals, and arthropods such as beetles, spiders, and ants1,2,3. Of those, the ants were indicated to be one of the most effective tick predators4,5. More than 27 ant species of 17 genera (Anoplolepis, Aphaenogaster, Camponotus, Crematogaster, Ectatomma, Formica, Iridomyrmex, Meranoplus, Monomorium, Myrmica, Notoncus, Pheidole, Pogonomyrmex, Polyrhachis, Rhytidoponera, Solenopsis, and Tapinoma) have been reported to be effective on different tick species (Amblyomma spp., Boophilus spp., Ornithodoros spp., Ixodes spp., Argas spp., Aponomma hydrosauri, Rhipicephalus appendiculatus, Otobius megnini, and Dermacentor variabilis)2,6,7,8. It is known that ants and other predators can affect ticks in a consumptive or nonconsumptive / behavioral manner and, as a result, may reduce the abundance of ticks in the overlap ranges8,9,10. However, the effects of ants on ticks are closely related to the ant species and the species, developmental stages, and physiological status of the ticks, and as a consequence, the impact of ants on ticks can exhibit fairly high variability2,8. Furthermore, there is no sufficient data on the factors determining the tick-ant relationship11,12.
Ant predation has been examined in all developmental stages of ticks, but the proportion of the studies based on the eggs is relatively low compared to the other stages2. In an egg-based study, the eggs of O. megnini, the spinose ear tick, were supplied to five different ant species, and of those, Tapinoma melanocephalum was the only species that fed on the eggs7. Conflicting results have been reported from the studies13,14 carried out to determine the predatory effects of ant species Pheidole megacephala on the eggs of Boophilus (Rhipicephalus) microplus14. Rhipicephalus sanguineus was demonstrated to secrete an acarine allomone when attacked by fire ants, Solenopsis invicta15. This allomone-based ant deterrence is known to protect ticks from being eliminated within the sympatric range. The eggs, intact and cracked, of tick species Amblyomma americanum were not attacked by S. invicta, and it was interpreted that this deterrence might be related to the possible presence of the allomone within the eggs12.
This study was carried out to determine whether the ant species Lasius alienus (Förster, 1850) (Hymenoptera: Formicidae) has any predatory effect on the eggs of tick species Hyalomma marginatum, H. excavatum, and Rhipicephalus bursa, and if the tick egg wax has any protective properties against possible predation. Ticks lay eggs (each 50–100 µg in weight and 0.5–1 mm in length) with a wax coat 0.5–2.0 µm thick, which is secreted by the female-tick-specific glands and organs such as the Gené’s16,17. Different molecules have been detected in the wax, such as alkanes, fatty acids, steroids, alcohols, and some specific proteins and lipoproteins18,19,20. However, detailed data on the wax content, especially its bioactive components, are not yet available20,21. As for the function of the wax, it has been reported that it reduces water loss, waterproofs the eggs, ensures the proper gas exchange between the eggs and air and holds the eggs together16,18. The wax also provides protection against chemical and physical factors such as cold, heat, proteinase K and pronase, or microbial agents including bacteria, fungi, viruses, and protozoa19,20,21,22,23,24,25.
Lasius alienus is one of the most abundant ant species in the Western Palearctic26. Its distribution area can range from natural open habitats, light forests, and forest edges to urbanized areas such as wooded residential areas and gardens. The nests can be encountered mostly in the soil, under stones, or other substances, and the nest densities may reach up to 10–50 nests/100 m2 in some endemic territories. The number of workers (24 mm in length) in a colony can be more than 10,000. In the active periods in hot and warm months, workers establish foraging trails on the ground, in trees, and even in dwellings for food27,28. Lasius alienus was reported to gather plant nectar, honeydew secreted by aphids and to consume both dead and small living arthropods28,29,30. However, there is no data in the literature on whether this or any other species in the Lasius genera have a predatory interaction with ticks. Furthermore, the only definitive association of L. alienus with predation on Acarina has been established recently with Dermanyssus gallinae (poultry red mite)31.
Considering the fact that the workers of L. alienus can forage effectively in many different places within the wide range distribution area27,28,31, it seems quite possible that several tick species encounter this ant species in their habitat32. This ant can feed by scavenging and predating small insects, and it meets their protein needs by hunting large numbers of small invertebrates, especially during larval feeding periods using the central foraging strategy29. Whichever invertebrates are abundant in their environment, the ants undoubtedly tend to consume more of them, especially if they are easy to hunt and transport27,28,29. Engorged large female ixodid ticks (around 1–1.5 cm depending on the species) lay a single batch of a large number of eggs (hundreds or thousands depending on the species and feeding levels) for several days or weeks at the hiding points such as cracks, crevices, and spaces under stones or various objects on the ground21,33 that the ant can easily reach due to its small size. In ixodid ticks, the female ticks lay eggs at once and die. The next generation continues entirely through the eggs21. Referring to these data, it seems hypothetically possible that any level of predation of L. alienus on the eggs, which are immobile and easy to reach and carry for the ants, can have a direct effect on the tick community in the overlap ranges. At this point, of course, whether the natural distribution areas of the ant and tick species overlap and, potentially, whether there is a possible evolutionary background between them are of the expected determining factors in a possible predation34.
The nests of L. alienus can be seen almost everywhere in the soil in its ranging territories, however, the density increases from dry steppe, open pasture and bushlands to cultivated areas, woodlands, and gardens29. In this study, three ixodid tick species were selected that are more or less different from each other in terms of biology, ecology, and therefore the probability of encountering L. alienus in their natural habitat. Of these, H. marginatum is a two-host tick, the immature stages (larvae and nymphs) prefer rabbits, hedgehogs and birds to feed, and the adults (male and female) use particularly cattle as host. The immature stages of mostly three-host tick H. excavatum, wild rodents are the preferable host, and a wide range of large wild animals, cattle and some other domestic animals can be the host for the adults. Both species are known as arid environment ticks, however, in accordance with their different host preferences as well, H. excavatum is more prevalent in the arid open fields, steppe, and bushlands32,35. Both immature and adult stages of two-host tick R. bursa use primarily domestic ruminants to feed. Although there is no detailed data on the natural dynamics of R. bursa, this species is suspected of having a kind of peri-farm natural dynamics32.
Source: Ecology - nature.com
