Predation of Adult Large Diving Beetles Dytiscus Marginalis (Linnaeus

Oceanological and Hydrobiological Studies International Journal of Oceanography and Hydrobiology

Volume 43, Issue 4

ISSN 1730-413X (360–365) eISSN 1897-3191 2014

DOI: 10.2478/s13545-014-0153-8 Received: July 29, 2014 Original research paper Accepted: October 13, 2014

INTRODUCTION Predation of adult large diving beetles (Linnaeus, 1758), The problem of the presence of fish in the diet of Dytiscus marginalis diving beetles from the family Dytiscidae has not Dytiscus circumcinctus (Ahrens, 1811) and been sufficiently explored. There are only a few Cybister lateralimarginalis (De Geer, 1774) observations conducted by some authors who (Coleoptera: Dytiscidae) on fish fry reported that adult beetles feed on fish and that they may cause damage in fish farms (Wesenberg-Lund 1912, Kiriejczuk 2001, Erman&Erman 2008,

* Ohiba&Takagi 2010, Miller 2013). According to Anna Frelik other authors, imagines of Dytiscidae do not harm adult fish but only feed on their eggs and fry (Walker 1901, Galewski 1978). Some also argue that they feed Department of Ecology and Environmental Protection, only on dead fish (Nilsson&Holmen 1995). General University of Warmia and Mazury, studies on the predation of diving beetles have been Pl. Łódzki 3, 10-727 Olsztyn, Poland dominated by laboratory experiments, largely devoted to the larval phases of their development (Johansson&Nilsson 1992, Young 1967, Key words: diving beetles, predation, fish, lake, small Young&Sperling 1986, Pearman 1995, Le water body Louarn&Cloarec 1997, Inoda 2012). Unfortunately, due to different feeding patterns of Dytiscidae larvae and imagines, it is not possible to directly relate the Abstract results of experiments from juvenile forms to adult beetles. Experimental studies of imagines of those The presented study describes the presence of fish fry in the insects have been less thorough (Gautam&Goutam diet of imagines of large Dytiscidae. The study was conducted between March and September in 2012 and 2013. A total of 163 2006, Cobbaert et al. 2010). large, aquatic, diving beetles were caught, which represented the Field observations of the predatory behavior of following species: Dytiscus marginalis, Dytiscus circumcinctus, Cybister diving beetles have been carried out by, for example, lateralimarginalis. Fish were identified by scales, bones, vertebrae, Sailer&Lienk (1954); Kuhlhorn (1961); James (1965); pharyngeal teeth. Insects were identified by epicrania, mandibles, hooks, limbs, body segments, eyes and wings. Crustaceans were Lee (1967); Roberts et al. (1967) and Young (1967). identified by limbs and Oligochaeta by bristles. Seeds and eggs of Results of studies based on the analysis of digestive invertebrates were found whole and intact. Fragments of fish fry tract content are also available. Unfortunately, studies were found in the digestive tracts of all three species collected in based on analysis of proventriculi content were three studied ponds. The alimentary canals of the studied beetles conducted on small- and medium-sized insects contained also fragments of insects, detritus, plant tissue, Crustacea, Arachnida, other invertebrates, Oligochaeta, and (Dettner et al. 1986, Deding 1988, Hicks 1994, Bosi Gastropoda. 2001, Kehl&Dettner 2003, Frelik 2014). The objective of this study is to determine the prevalence of fish fry in the diet of imagines of large Dytiscidae in relation to other elements of the diet, * [email protected]

Predation of adult large diving beetles on fish fry| 361 based on the contents of digestive tracts of insects living in the natural environment. One hypothesis was put forward: the amount of beetles feeding on fish is different at each of the three sites.

MATERIALS AND METHODS

Study area

Samples were collected in three water bodies. Site no. 1 was located in the North-East of Poland, near the town of Bartoszyce (54°12’18’’N; 20°56’47’’E) (Fig. 1). It is a small eutrophic field water body with an area of 0.4 ha. The pH of water was about 8.0, the oxygen level − about 50% and salinity − about 650 Cl- mg l-1 at 25°C. The pond is exposed to surface run-off from nearby fields. The inflow of pesticides and fertilizers into the pond has resulted in a rapid decrease in the population of vertebrates, such as frogs. The pond is inhabited by Carassius auratusi, Carassius carassius, Tinca tinca and Cyprinus carpio. Samples were collected at sites overgrown with Typha Fig. 1. Study area and study sites (1, 2, 3) latifolia and Phragmites australis at a depth of 20 cm. Site no. 2 was located in the North-East of Poland, in the city of Olsztyn (53°44’89’’N; taken out intact due to stress and rapid death of 20°20’65’’E) (Fig. 1). It is a small forest pond with a predators. No fish were found in the traps. large amount of organic matter accumulated at the The oxygen level, temperature and salinity of bottom and with brown water. The pH of water was water in the studied water bodies were measured with about 6.0, the oxygen level − about 22% and salinity a CC0-401 conductivity meter/oxygen meter. The − about 30 Cl- mg l-1 at 25°C. Ichthyofauna was pH level was measured with an SP 300 pH-meter. represented by Carassius carassius, which occurs in the Three species of diving beetles were analyzed, pond in large numbers. Samples were collected at which belonged to the insect size category of 27 to sites overgrown with Phragmite saustralis and Juncus sp. 37 mm. These species were selected because of the at a depth of 20 cm. fish found in their alimentary canals, namely: Site no. 3 − eutrophic Lake Skanda, situated in the North-East of Poland, in the city of Olsztyn Dytiscus marginalis – the body length of these insects (53°45’39’’N; 20°31’76’’E) (Fig. 1). The pH of water ranges from 27 to 35 mm. A ubiquist species, was about 7.0, the oxygen level − about 80% and occurring in varied types of waters; it is frequently salinity − about 200 Cl- mg l-1 at 25°C. The found both in natural and artificial water bodies ichthyofauna was represented by typical lacustrine (Galewski 1978); taxa. Samples were collected at sites overgrown with Phragmites australis, Typha sp. and Carex sp. at a depth Dytiscus circumcinctus – the body length of these insects of 20 cm. ranges from 32 to 36 mm. They occur mainly in The material was collected by means of bottle small water bodies, considerably overgrown with traps and a sampling net Volkova et al. (2013) in vegetation (Galewski 1978); 2012-2013, in monthly intervals from April to September. The traps were submerged in water, Cybister lateralimarginalis – the body length of these leaving the gathered insects without access to air. The insects ranges from 30 to 37 mm. They occur in material was retrieved 24 hours after the traps had deeper water bodies (ponds, large clay pit ponds, been set (Volkova et al. 2013). Apart from beetles, dead arms of rivers), overgrown with grass (Galewski there were also some invertebrates, but they were 1978).

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The collected material was preserved in 70% In order to analyze how the natural environment alcohol and ether solution. The proventriculi of affects the predatory feeding of Dytiscidae on insects was dissected under a binocular microscope ichthyofauna, Fisher’s exact test was conducted using (MST 132 EDU BK). The contents of each specimen the software Statistica 2010. The species D. marginalis were immersed in a droplet of glycerin, placed on a and D. circumcinctus, collected in all three water bodies, microscope slide, enclosed with a cover glass and were compared. C. lateralimarginalis was not analyzed analyzed under a XJS 400 microscope. The because fragments of fish bodies were only found in photographic documentation of fish fragments was the proventriculi of insects caught in one of the prepared using a camera connected to a microscope. ponds. The results were analyzed at the significance In order to precisely determine the composition level of 0.05. of the diet of predatory beetles, reference The contents of proventriculi of insects in three preparations were made. To this end, aquatic size groups were analyzed. No fragments of fish invertebrates as well as adult amphibious beetles, and skeletons were found in the digestive tracts of beetles flying terrestrial insects were collected. Subsequently, with a size of 2.3-5.0 mm and 13-15 mm. they were pre-digested in a KOH solution and then No protected species were used in the study. digested so they resembled the chyme of insects under study. The digested corpses were immersed in RESULTS a drop of Faure’s liquid on a microscope slide and enclosed with a cover glass. The reference The study material included 163 specimens of preparations were subsequently compared to the diving beetles of three species: Dytiscus marginalis, chyme preparations. Dytiscus circumcinctus, Cybister lateralimarginalis (Table 1). Fish were identified by scales, bones, vertebrae, Organisms included in the diet of beetles belonged to pharyngeal teeth (Fig. 2). Insects were identified by 9 taxonomic groups (Table 1). epicrania, mandibles, hooks, limbs, body segments, The most frequently-consumed prey were insects, eyes and wings. Crustaceans were identified by limbs including: Odonata, Ephemeroptera, Diptera, aquatic and Oligochaeta by bristles. Seeds and eggs of and terrestrial Coleoptera, Heteroptera, Trichoptera invertebrates were found whole and intact. and Lepidoptera (Table 1). Other groups were found less frequently. Protista were represented only by Bacillariophyta. Crustaceans were represented by Cladocera, Copepoda and Ostracoda. Some Arachnida were also consumed, including: Hydrchnidia, other Acari and Araneae. Gastropoda were represented by Planorbidae. Other invertebrates included Nematoda, Rotifera and Tricladida (Table 1). Plant material included seeds, pollen, leaves of

Table 1

The number of diving beetles with different types of food in their foreguts (A − Dytiscus marginalis; B – Dytiscus circumcinctus; C − Cybister lateralimarginalis; n – number of individuals) Sampling site no. 1 Sampling site no. 2 Sampling site no. 3 A B C A B C A B C n - 27 n - 32 n - 2 n - 34 n - 22 n - 2 n - 6 n - 6 n - 32 Protista - 1 ------Oligochaeta 2 - - 1 - - - - - Crustacea 2 4 - 1 1 - 2 - 1 Insects 21 30 2 31 22 2 6 6 31 Arachnida 2 1 - - 1 - 1 - - Gastropoda - - - 1 - - - - - Other invertebrates 1 1 ------1 Fig. 2. Fragments of the fish body in foreguts of Pisces 3 5 - 6 6 - 2 1 5 Plants 9 10 - 5 8 2 1 3 4 predaceous diving beetles: a − shell; b − pharyngeal Detritus 13 18 2 16 9 1 5 2 16 teeth; c-d − vertebra; e − coccyx; f − bone Empty guts - 2 - 3 - - - - 1

Predation of adult large diving beetles on fish fry| 363 moss and other plants, as well as filamentous algae (Table 1). In terms of general composition of the diet, fragments of fish were found in the proventriculi of large Dytiscidae, accounting for 17.8% of all beetles. As much as 96.1% of the beetles consumed insects, 52.2% − detritus and 26.7% − plant tissue. Few of them consumed Crustacea (7.6%), Arachnida (3.2%), Oligochaeta and other invertebrates (1.9%), Gastropoda and Protista (0.63%). Fragments of fish were usually found in the proventriculi of beetles of the species D. circumcinctus, Fig. 3. Beetles containing fish in their foreguts slightly less frequently in D. marginalis and the least frequently in C. lateralimarginalis (Fig. 3). Fragments of fish were usually found in proventriculi of beetles collected in pond no. 2. Slightly fewer fish were found in the digestive tracts of beetles collected in Lake Skanda and the smallest amounts − in beetles caught in pond no. 1 (Fig. 4). Among beetles caught in pond no. 1, fragments of fish bodies were found only in proventriculi of Dytiscus marginalis and Dytiscus circumcinctus. They were found in the diet of D. circumcinctus more frequently than in other beetles. They were not found in Cybister lateralimarginalis. This pattern was similar to that Fig. 4. Beetles feeding on fish at the study sites observed for large beetles collected in pond no. 2. Fragments of fish bodies were found in proventriculi of all three species of beetles caught in Lake Skanda. They were most frequently found in D. marginalis, less frequently in D. circumcinctus and C. lateralimarginalis. The frequency of their occurrence in the latter two species was similar (Fig. 5). The results of Fisher’s exact test for the sites under analysis based on two beetle species are as follows: site no. 1 and site no. 2 − p = 0.67; no. 2 and 3 − p =1.0; 1 and 3 − p = 0.54. Fig. 5. D. circumcinctus, D. marginalis, C. lateralimarginalis containing fish in their foreguts DISCUSSION 1,2,3 − site number

Deep littoral habitats where the study material was collected are perfect places for both fish and understated due to beetles flying between various large predatory diving beetles. Therefore, a predator water bodies. According to Buczyńska et al. (2008) or and its prey will meet there frequently. This makes it Serajuddin et al. (2013), adult Dytiscidae (including easy for large Dytiscidae to catch fish fry. It is Dytiscus sp. and Cybister sp.) inhabit fish ponds and noteworthy that during an extensive study of occur there in large numbers of specimens. It should predatory feeding habits of Dytiscidae, when material be known that their high predation on fish fry and a was collected in water bodies with no fish present, large number may cause damage in fish farms. And the contents of digestive tracts of some insects while adult diving beetles are predators in fish ponds caught in such water bodies were indicative of all year, their larval stages feed on prey only during a previous consumption of fish. Even 30% of diving short period of time. So the importance of predation beetles contained a fish in their proventriculi. of Dytiscidae larval stages is smaller than predation Therefore, the results of those studies may be of adult diving beetles.

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Interestingly, while the intensity of predation in Buczyńska E., Buczyński P., Lachowski L. & Stryjecki R. (2008). two of the water bodies is similar, it is much lower in Fish pond as refugia of aquatic invertebrates (Odonata, Coleoptera, Heteroptera, Trichoptera, Hydrachnidia): a case the field pond. This may be caused by pollution, study of the pond complex in Zalesie Kańskie (Central-East which probably resulted in the decreased fish Poland). Nature Conservation 64: 39-55. population. Cobbaert, D., Bayley. S. E. & Greter J.L. (2010). Effects of a top According to Sih (1986) and Johansson (1992), invertebrate predator (Dytiscus alaskanus; Coleoptera: Dytiscidae) on fishless pond ecosystems. Hydrobiologia the intensity of predation of large Dytiscidae on fish 644:103–114. DOI: 10.1007/s10750-010-0100-7 fry results from the fact that the prey which moves Deding, J. (1988). Gut content analysis of diving beetles more quickly (e.g. fish) is more easily spotted by (Coleoptera: Dytiscidae). Natura Jutlandica 22: 177-184 predatory Dytiscidae, which affects the frequency of Dettner, K., Hübner M. & Classen R. (1986). Age Structure, their consumption. However, according to Phenology and Prey of Some Rheophilic Dytiscidae (Coleoptera). Entomologica Basiliensia 11: 343-370. McArthur&Pianka’s (1966) optimal foraging theory, Erman, O. K, &. Erman O. (2008). Dytisicidae Coleoptera the slowest prey should be caught most easily. The species in Artvin and Rize Provinces of northeastern Turkey. frequency of fish catching may be affected by the fact Munis Enomology and Zoology 3(2): 582-593. that fry swim in shoals and by hunting tactics of a Frelik, A. (2014). Food of adult diving beetles Colymbetes fuscus (Linnaeus, 1758) and C. striatus (Linnaeus, 1758) predatory insect, which catches its prey by surprise. 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