Parasitism on Riparian Dragonflies (Odonata) at Biology Education and Research Forest, Universitas Andalas

Parasitism on dragonflies (Odonata) may become the least attention in most entomological studies in Indonesia, since it possesses much indirect effect to human being. The odonata parasitism is caused by the infestation of water mite larvae onto the body of adult dragonflies. In this paper we discuss the result of odonatological survey we did at two tributaries in Biology Education and Research Forest (BERF), Universitas Andalas. The survey had been conducted between August to November 2019. We recorded 17 dragonfly species bound to these tributaries, 12 Zygopterans and 5 Anispterans. Water mite infestation was observed to happen on four Zygopteran species and one Anisoptera. The highest prevalence was shown by Orthetrum testaceum (100%), followed by Euphaea variegata (16.67%), Prodasineura verticalis (14.29%), Euphaea modigliani (3.57%) and Heliocypha angusta angusta (0.85%). In overall, the prevalence on community level reached 3.29%. The parasitism case observed in the tributaries of BERF can be classified as low incident, each infested odonate only contained a single water mite except for O. testaceum with two water mites. We presume that habitat condition may contribute to the rate of dragonfly parasitism, where a good habitat help lowering the parasitism incident.


Introduction
Odonata has been reported as one among aquatic insects that is parasitized by water mites. Water mites are considered as true parasites to dragonflies and damselflies, as they exploit the odonates for food and dispersal [1]. The mites may attach to their dragonfly hosts during the period of maturity and detach when the dragonflies oviposit [2]. Despite there is a lot of sexual dimorphism observed among odonates, some previous studies indicated that there was no significant parasite infestation between sexes; it may have significant difference between dragonfly parasitism and damselfly parasitism where the latter infested more than first [3].
Parasitic water mites, although often neglected, are thought to have crucial role in the ecosystem. They serve as the limiting factor for controlling mosquito population, either as parasite during their larval stage or being predator after reaching adult stage [4]. Aside from affecting the longevity and flight performance, their attachment to certain body parts of other aquatic insects can impede the copulation or sperm transference [5,6,7]. Through its brief parasitic and phoretic association with other aquatic insects, parasitic water mites get food, transported and extend their range [8]. The larvae of Arrenurus spp. are commonly known as the ectoparasites on adult odonates [9,10]. This genus contains 800 species, with most of them act as parasites to Odonata, Diptera and Coleoptera [11,12]. The larval stages are the parasitic phase for water mites Arrenurus out of seven life cycles they have; egg, inactive prelarvae, larvae, protonymph, deutonymph, tritonymph and adult [13].
In Indonesia, despite the rampant interest in studying Odonata, the attention is paid more to the biodiversity, taxonomy and systematics, biogeography, ecology, education, ethnozoology, history and molecular [14]. Parasitology, in its association with odonata, has been neglected prior to 2020 in Indonesia despite its potential to give robust support onto the use of odonata community as environmental indicators. Two damselfly species, Euphaea variegata and Heliocypha angusta angusta, were reported on 2020 to be infested by Arrenurus spp. in Bengkulu, Indonesia [15]. No other published works regarding parasite association with Odonata after that in Indonesia. Hence, it is necessary to share equal attention toward this field. In this paper, we discuss preliminary observation of water mite parasitism on Odonata at Biology Education and Research Forest (BERF), Universitas Andalas.

Study Site and Sampling Method
The observation on Odonata had been conducted from August to November 2020 at two tributaries in Hutan Pendidikan dan Penelitian Biologi (Biology Education and Research Forest, hereinafter BERF). It is located around GPS coordinates 0° 54' 24.69" S, 100° 27' 55.76" E and at elevation 264 m above sea level ( Figure 1). The BERF area is mixed between secondary and primary forest, managed under the supervision of Biology Department, Universitas Andalas [16]. In addition to its ecological functions as water catchment area for Padang City, BERF also functions as field laboratory and biodiversity research area for Biology Department.Some text. The odonata observation was conducted through field survey along the 150-170 m line transect erected within the tributaries. All odonates that seen within and at the proximity of water body were recorded. Water mites were also visually detected from any sighted odonate and counted to determine parasite load in each infested individual. The sighting then documented using Nikon Coolpix P900, set at macro mode with fine resolution (pixellation rate 4608x3456) [17]. Species identification was guided using published materials related to the region [18,19,20].

Data Analysis
We used two indices in the descriptive analysis, which are prevalence of parasitism (percentage of infested host odonate over all counted odonate individual) and intensity of infestation that counted from number of parasites on a given odonate [21].

Odonate Species in BERF Tributaries and the Prevalence of Water Mite Parasitism
Our observation resulted in the inventory of seventeen odonates that bound to the aquatic body of tributary. These species consisted of 12 Zygoptera or damselflies (species 1-12 in Table 1) and 5 Anisoptera or dragonflies (species 13-17 in Table 1). Some of these recorded species were not in the previous record for Universitas Andalas campus complex, i.e. Drepanosticta draco (Platystictidae), Euphaea aspasia, E. modigliani (Euphaeidae), Devadatta argyoides (Devadattidae), Vestalis luctuosa, Neurobasis chinensis (Calopterygidae) and Zygonyx ida (Libellulidae) [17,24]. Heliocypha angusta angusta (Chlorocyphidae) was counted as species with most individuals, followed by Euphaea modigliani (Euphaeidae) and Libellago hyalina (Chlorocyphidae). These dominant species were observed at open stream area. These dominant species are damselflies with metallic color in their wings, prefer environment with direct exposure from the sunlight, used not only to warm themselves but also to increase their sexual performance during reproduction [22]. A male-on-male agonistic competition over mating site was also observed on Euphaea aspasia from this area [23].
Odonata species with most infested was Heliocypha angusta angusta with three individuals observed carrying water mite larval in their body. The prevalence for this species, however, is the lowest among other infested species (2.54%); it was apparently due to the sheer abundance of this species at the survey area. Similar to Euphaea modigliani which recorded with two infested individuals, its prevalence rate is as low as 3.57%, in consequence of its abundance population. In contrary, Orthetrum testaceum became odonate species with the highest prevalence (100%), as only a single individual encountered during the survey, in which the parasites observed. This species is indicated as common in the vicinity of Universitas Andalas [17], yet its proximity to stream or other moving water bodies is not well defined. Other infested species are Euphaea variegata (16.67%) and Prodasineura verticalis (14.29%). These two species were known at the survey area from a handful of individuals. The overall prevalence for water mite parasitism on odonates at BERF's tributaries was 3.29%. The parasitism prevalence in our study area fall between the range of prevalence observed in many previous studies, however, the infested species are not listed [25].
From the Table 1, we can also see that Zygopterans are more parasitized than Anisopterans at our survey area. Parasitic water mites are known to parasitize more common insects in a certain habitat rather than the rare ones, as it increases their opportunity to get their host [26]. Heliocypha angusta angusta and Euphaea modigliani are from the families that known to be living around aquatic body in most of their time, hence improves the possibility for water mites to return to water as soon as their parasitic phase ended [1,2]. Albeit there is common thought that parasite will choose large host as it provides better resources and habitat for them, it is still unclear on the case of parasitic water mites as they have been observed infesting various sizes of odonates [27,28]. Since the size of odonate species will affect their density in a habitat, it is understandable that the smaller an odonate, the more their population therein [29]. Hence, the preference on common but small odonates rather than on big but rare ones can be thought as a tradeoff made by the water mites to carry on their live.

Detail on Odonate Parasitism
As previously implied, there is lack of publications for parasitic water mites in Indonesia [15], while what currently available mostly came from the works in central and eastern parts of the country [30]. During fieldwork, following the documentation on infested odonates, our attempt to collect the water mites failed to yield any result as the mites always escaped whenever their host insects captured. Their small and inconspicuous body made it difficult to follow as soon as their detachment from host body. Tentatively, we identified the parasitic water mites infested the odonates observed at BERF's tributaries as Arrenurus spp. by account that this genus is more widespread in tropical affinities and contains numerous species [2,31]. In Table 2 below, we summarized our observation on infested odonates. Female odonates seemed to be more prone for water mite infestation than the males. Major assumption thinks that mites prefer female dragonflies as they tend to have more robust body and broader distribution which help the feeding and dispersal of mites [32]. Nevertheless, more studies in this matter revealed that male and female odonates can be equally parasitized [33,34]. Meanwhile, the load of parasite in each infested odonata was only one, except for Orthetrum testaceum with two parasites. This number was much lower than what observed at Protected Forest Management Unit Seluma in Bengkulu, where an individual of Heliocypha angusta angusta was observed with 10 mites  [15]. It still needs further study regarding what factors driving the infestation of water mites onto dragonflies, however we presume that environmental conditions could contribute. The tributaries in BERF are clean running water bodies, while in the observation in Bengkulu, the stream was slow, turbid and surrounded with agricultural area that affect water condition. Many accounts on parasitic water mites are without description on their environmental preference, as it is probably referred to habitat of odonates they infest on. Arrenurus mites in North America were reported to prefer temporary or permanent lentic or slow lotic water bodies [34,35], which included turbid or unclean water bodies. On further observation on mite load on odonate body, we found that mites attach more onto abdominal segments than the thoracical area of odonates. As it needs to be confirmed with more observation, mites' preference for attachment may be derived by the accessibility and sufficiency of food source. Abdominal parts of odonata mainly house digestive and reproductive apparatus, which govern sufficient flow of body fluid and nutrition into this body part.