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Biodiversity of freshwater macroinvertebrates on Gökçeada Island (North Aegean Sea, Turkey)

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Introduction

Islands have been of great importance to biology and evolution since the beginning of science, and scientists have carried out research in all aspects, including biodiversity, biogeography, geology, and archaeology.

The Aegean Sea is one of the major sea basins within the Mediterranean Sea, with approximately 7500 islands and islets that have undergone different geological formation processes (Hupało et al. 2020). The Aegean Sea plays an important role as a habitat or migration route for many species (Poulakakis et al. 2014). It also has the most interesting archipelagoes in terms of biodiversity due to its high species diversity with a large percentage of endemism (Bittkau & Comes 2005; Lymberakis & Poulakakis 2010). The Aegean Islands have undergone different formation processes, including volcanic and tectonic processes, which resulted in geographic isolation and different biogeographical histories between them and the neighboring mainland (Kougioumoutzis et al. 2017). Two of the Eastern Aegean Islands, namely Gökçeada (Imbros) and Bozcaada (Tenedos), are located in the northeastern part of the Aegean Sea, which is part of the Turkish territory. The islands have a typical Mediterranean climate with dry summers and warm and rainy winters.

Gökçeada is located in the northeastern Aegean Sea, northwest of the entrance to the Dardanelles (Çanakkale Boğazı). It is the largest Turkish island with a coastline of 92 km and an area of 289 km2. Due to fairly high precipitation, Gökçeada has a great potential for freshwater resources. The average annual rainfall on the island reached 740 mm over the last thirty years (Cengiz et al. 2013), while the adjacent mainland received 574 mm per year in the last decade, which is considerably less.

Research on the freshwater macroinvertebrates of the Aegean Islands (Greece) dates back to the 19th century and has largely focused on Mollusca (Georgopoulou et al. 2016). The freshwater invertebrate fauna of the Aegean Islands, on the other hand, is poorly researched. Similar to the Aegean Islands, no complete documentation is available for freshwater invertebrates of Gökçeada and Bozcaada (the northeastern Aegean Sea). Several studies have been carried out to investigate specific taxa on Gökçeada, including Chironomidae, Ephemeroptera, Odonata, Amphipoda, Isopoda, Gastropoda, and Oligochaeta (Şahin et al. 1988; Özkan 2006; Özbek & Özkan 2017; Zeybek et al. 2017; Aslan et al. 2018; Odabaşı et al. 2019).

Most studies on Turkish freshwater macroinvertebrates have largely focused on the continental part. However, an inventory of freshwater invertebrates on freshwater-rich Gökçeada is needed from an biogeographical aspect. In this study, we aimed to explore the fauna of freshwater invertebrates on Gökçeada. To this end, some accessible groundwater fountains and surface water bodies, including ponds and streams (both temporary and permanent), were sampled.

Materials and methods

In order to study the freshwater macroinvertebrates of Gökçeada, different freshwater bodies, such as springs, fountains, brooks, and reservoirs, were surveyedbetween May 2016 and September 2018. The island has three artificial ponds and two reservoirs: Aydıncık (site 5), Şahinkaya (site 25) and Uğurlu (site 14) ponds, and Zeytinli (site 9) and Uğurlu reservoirs (site 15). In addition, some temporary streams occur on the island, such as the Marmaroz Brook (site 13) and the slow-flowing Aya Todoro Seep (site 7), which are located on the northern and eastern sides of the island, respectively. Drinking fountains are very common all over the island and provide potable water for people and wildlife. Among the sampling sites, nineteen are fountains scattered around the island and located mainly along the roadsides, while some are located in old laundries that were formerly used for washing clothes. All of these fountains provide habitat for aquatic macroinvertebrates in their concrete basins. Sampling sites selected in the streams were very shallow or even dried up in the dry season. Site 7 is an interesting aquatic habitat consisting of water seeping from a rock block located around the Aya Todoro Monastery at the eastern end of the island.

Freshwater macroinvertebrates were collected at 34 pre-selected sampling sites (e.g. St 1–34; Fig. 1) using a hand net (500 μm) and a sieve. The sampling sites are distributed throughout the island and include ponds, reservoirs, fountains, and some ephemeral water bodies such as brooks and a seep (Table 1). The fountains on the island serve as a source of drinking water for humans, whereas those for animals are generally located along the roads that are currently in use. Fountains that were formerly used for washing in old laundries are now visited only by tourists. Some of these fountains still provide habitat for macroinvertebrates. Macroinvertebrates were collected individually with forceps and fixed with 80% ethanol in plastic tubes. All material was deposited in the private collection of the author.

Figure 1

Map of Gökçeada and the location of the sampling sites

Sampling sites with their coordinates in DMS (degrees minutes and seconds)

No. Local Names Coordinates
1 Bademli Çamaşırhane (laundry) 40°13′18.7″N; 25°54′27.5″E
2 Mezbaha Çeşmesi (fountain) 40°11′5.12″N; 25°55′32.9″E
3 Mezbaha Üstü Kaynak (fountain) 40°11′14.6″N; 25°55′09.0″E
4 Pınarbaşı Fountain 40°12′5.96″N; 25°49′59.6″E
5 Aydıncık Göleti (pond) 40°09′03.1″N; 25°55′40.9″E
6 Civaki Deresi (brook) 40°10′40.6″N, 25°57′32.85″E
7 Aya Todoro Manas rı (seep) 40°13′03.4″N; 25°58′03.6″E
8 Zeytinli Köy Çeşmesi (fountain) 40°11′25.5″N; 25°52′15.5″E
9 Zeytinli Baraj Gölü (dam lake) 40°10′41.4″N; 25°51′46.3″E
10 Tepeköy Çamaşırhane (laundry) 40°11′42.3″N; 25°50′17.7″E
11 Fehim Akdemir Çeşmesi (fountain) 40°08′58.2″N; 25°46′56.9″E
12 Dereköy Çamaşırhane (laundry) 40°09′03.7″N; 25°46′19.7″E
13 Marmaroz Deresi (brook) 40°10′19.7″N; 25°45′38.3″E
14 Uğurlu Göleti (pond) 40°08′21.3″N; 25°44′16.5″E
15 Uğurlu Barajı (dam lake) 40°08′16.5″N; 25°42′41.3″E
16 Karayolları Çeşmesi (fountain) 40°08′37.4″N; 25°50′45.0″E
17 Cugura Çeşmesi (fountain) 40°07′49.1″N; 25°50′35.2″E
18 Erenyurt Deresi (brook) 40°06′59.4″N; 25°49′25.9″E
19 Karakol Çeşmesi (fountain) 40°06′10.2″N; 25°49′06.6″E
20 Recep Çınar Çeşmesi (fountain) 40°07′27.9″N; 25°46′29.4″E
21 Taşoluk Çeşme (fountain) 40°08′35.0″N; 25°46′55.6″E
22 Mavisu Çeşmesi (fountain) 40°09′11.9″N; 25°45′16.8″E
23 Zeytinli Çamaşırhane (laundry) 40°11′28.3″N; 25°52′11.4″E
24 Marmaroz Şelalesi (brook) 40°10′52.3″N; 25°46′04.6″E
25 Şahinkaya Göleti (pond) 40°06′48.5″N; 25°46′23.7″E
26 Orman Kulesi Al (fountain) 40°11′07.4″N; 25°55′13.7″E
27 Orman Kulesi Al (brook) 40°11′29.5″N; 25°54′49.1″E
28 Börekçi Cafer Hayra (fountain) 40°11′38.2″N; 25°54′44.6″E
29 Aydıncık Burnu (fountain) 40°08′17.7″N; 25°58′56.7″E
30 Şahinkaya Deresi (brook) 40°08′11.7″N; 25°46′32.7″E
31 İncesu (brook) 40°07′34.33″N; 25°55′27.2″E
32 Kaymakam Rampası (brook) 40°09′40.8″N; 25°49′35.6″E
33 Nusret Bağları (brook) 40°06′47.6″N; 25°52′18.3″E
34 Recep Erden Kaynağı (fountain) 40°07′5.03″N; 25°52′31.6″E
Results

A total of 78 macroinvertebrate taxa belonging to five taxonomic classes were found in various aquatic ecosystems on Gökçeada. Aquatic Insecta were the largest group, with 50 taxa representing six orders and 25 families (some taxa were identified only to the family level). The other classes (in order of taxonomic richness) were Clitellata (10 taxa), Gastropoda (8 taxa), Malacostraca (8 taxa), and Bivalvia (2 taxa; Table 2). The highest taxonomic richness was found at site 6 (21 taxa), followed by site 34 (15 taxa), site 9 (14 taxa), and site 7 (13 taxa). At sampling sites 10, 15, 23, 24, 26, 27 and 30, no macroinvertebrates were found throughout the study period. In terms of species richness, Insecta accounted for 64% of all taxa, followed by Clitellata (13%), Gastropoda and Malacostraca (10%), and Bivalvia (3%; Fig. 2).

List of aquatic macroinvertebrates identified in freshwater habitats of Gökçeada Island with their localities and percentage frequency of occurrence (* indicates new records for the island)

Taxonomic Order Site No./% F
Phylum: Annelida
  Class: Clitellata
    Subclass: Oligochaeta
      Order: Tubificida
        Family: Naididae
          Nais barbata Müller, 1773* 7, 11/7.41
          Nais stolci Hrabe, 1981* 7/3.70
          Nais elinguis Müller, 1774* 19, 11/7.41
          Nais communis Piguet, 1906* 11/3.70
          Pristina sp.* 19, 11/7.41
          Limnodrilus udekemianus Claparède, 1862* 7, 11/7.41
          Tubifex tubifex (Müller, 1774)* 7, 19, 21, 11, 33, 34/22.22
          Psammoryctides albicola (Michaelsen, 1901) 7, 8, 19, 11, 34/18.52
          Psammoryctides barbatus (Grube, 1861)* 19/3.70
      Family: Lumbriculidae
          Stylodrilus parvus (Hrabe & Cernosvitov, 1927)* 16/3.70
Phylum: Mollusca
  Class: Bivalvia
    Order: Sphaeriida
      Family: Sphaeriidae
          Pisidium subtruncatum Malm, 1855 7, 29, 34/11.11
    Order: Myida
      Family: Dreissenidae
          Dreissena polymorpha (Pallas, 1771) 9, 25/7.41
Class: Gastropoda
  Subclass: Heterobranchia
    Superorder: Hygrophila
      Family: Planorbidae
          Ancylus fluviatilis O. F. Müller 1774 7, 34/7.41
      Family: Lymnaeidae
          Galba truncatula (O.F. Müller, 1774)* 34/3.70
      Family: Physidae
          Physella acuta (Draparnaud 1805) 9, 25/7.41
    Subclass: Caenogastropoda
      Family: Melanopsidae
          Melanopsis buccinoidea (Olivier, 1801)* 34/3.70
    Order: Littorinimorpha
      Family: Bythinellidae
          Bythinella gokceadaensis Odabaşı, 2019* 3, 4, 16, 17, 11, 12, 19/25.93
      Family: Hydrobiidae
          Pseudamnicola cirikorum Odabaşı, 2019* 8/3.70
          Pseudamnicola radea Odabaşı, 2019* 29/3.70
          Grossuana kayrae Odabaşı, 2019* 1, 16, 19/11.11
Phylum: Arthropoda
  Class: Malacostraca
    Order: Amphipoda
      Family: Gammaridae
          Gammarus komareki Schaferna, 1922 1, 3, 6, 13, 16, 33, 34/25.93
          Gammarus sp. 2, 6, 16, 21, 22, 28/22.22
          Echinogammarus sp.* 19/3.70
          Pontogammarus robustoides (Sars, 1894)* 9/3.70
      Family: Niphargidae
          Niphargus sp.* 17, 19, 20/11.11
      Family: Talitridae 19/3.70
    Order: Decapoda
      Family: Potamidae
          Potamon ibericum (Bieberstein, 1809)* 16/3.70
    Order: Isopoda
      Family: Asellidae
          Asellus aquaticus (Linnaeus, 1758) 1, 8, 12, 19, 34/18.52
Class: Insecta
    Order: Ephemeroptera
      Family: Caenidae
          Caenis sp. 6, 9, 25, 31, 33, 34/22.22
      Family: Baetidae* 6, 9, 13, 31, 34/18.52
      Family: Heptageniidae* 13, 31, 33/11.11
      Family: Ameletidae* 34/3.70
    Order: Hemiptera
      Family: Corixidae
          Arctocorisa sp.* 5, 6, 34/11.11
      Family: Micronectidae
          Micronecta sp.* 5, 6, 9, 14/14.81
      Family: Notonectidae
          Notonecta sp.* 2, 6, 13/11.11
    Order: Coleoptera
      Family: Dytiscidae* 6, 13, 16, 29, 34/18.52
      Family: Hydrophilidae* 6, 28/7.41
      Family: Curculionidae* 9/3.70
      Family: Elmidae* 9/3.70
    Order: Diptera
      Family: Chironomidae
          Clinotanypus pinguis (Loew, 1861) 5/3.70
          Procladius (Holotanypus) sp. Roback, 1982 6, 7, 9/11.11
          Paramerina cingulata (Walker, 1856)* 7/3.70
          Krenopelopia binotata (Wiedemann, 1817)* 7/3.70
          Krenopelopia sp. 6/3.70
          Natarsia punctata (Fabricius, 1805)* 6/3.70
          Rheocricotopus (Rheocricotopus) fuscipes (Kieffer, 1909) 31, 34/7.41
          Halocladius fucicola (Edwards, 1926)* 22/3.70
          Cricotopus (Cricotopus) tremulus (Linnaeus, 1758)* 6, 20, 28/11.11
          Cricotopus (Cricotopus) triannulatus (Macquart, 1826)* 6/3.70
          Cryptochironomus defectus (Kieffer, 1913) 9/3.70
          Einfeldia pagana (Meigen, 1838) 2, 7/7.41
          Chironomus tentans Fabricius, 1805 7/3.70
          Chironomus thummi (Kieffer 1911) 2, 19, 11, 34/14.81
          Chironomus anthracinus Zetterstedt, 1860 5, 4, 19, 28/14.81
          Chironomus viridicollis (van der Wulp, 1877) 11, 28/7.41
          Polypedilum (Pentapedilum) exsectum (Kieffer, 1916) 5/3.70
          Polypedilum (Polypedilum) nubeculosum (Meigen, 1804)* 9/3.70
          Polypedilum (Tripodura) scalaenum (Schrank, 1803) 1, 3, 9, 16/14.81
          Stictochironomus yalvacii Şahin, 1971 5, 31/7.41
          Microtendipes pedellus (De Geer, 1776)* 3, 34/7.41
          Paratanytarsus lauterborni (Kieffer, 1909) 6, 9/7.41
          Rheotanytarsus exiguus (Johannsen, 1905) 6/3.70
          Cladotanytarsus mancus (Walker, 1856) 9/3.70
      Family: Simuliidae
          Simulium sp.* 31, 34/7.41
      Family: Stratiomyidae* 7, 13/7.41
      Family: Tabanidae
          Tabanus sp.* 6, 13/7.41
      Family: Ephydridae* 6/3.70
      Family: Dolichopodidae* 6/3.70
    Order: Odonata
      Family: Cordulegasteridae
          Cordulegaster sp.* 6, 28/7.41
      Family: Libellulidae
          Brachythemis leucosticta (Burmeister, 1839)* 6/3.70
          Crocothemis erytraea (Brullé, 1832) 29/3.70
      Family: Aeshnidae
          Boyeria irene (Boyer de Fonscolombe, 1838)* 33/3.70
Family: Gomphidae
          Onychogomphus forcipatus (Linnaeus, 1758)* 13/3.70
      Family: Coenagrionidae
          Erythromma viridulum Charpentier, 1840* 25/3.70
    Order: Trichoptera
      Family: Hydropsychidae
          Hydropsyche instabilis (Curtis, 1834)* 13, 32/7.41
          Hydropsyche bulbifera McLachlan, 1878* 18/3.70
      Family: Polycentropodidae
          Cyrnus sp.* 29/3.70
      Family: Ecnomidae
          Ecnomus tenellus (Rambur, 1842)* 25/3.70

Figure 2

Species richness of taxonomic classes

Several studies have been carried out on benthic macroinvertebrates in freshwater ecosystems of Gökçeada (i.e. Şahin et al. 1988; Balık & Ustaoğlu 1993; Özkan 2006; Çamur-Elipek & Aslan 2007; Özbek & Özkan 2017; Zeybek et al. 2017; Aslan et al. 2018; Odabaşı et al. 2019). In addition to the records of benthic macroinvertebrates reported in the above studies, 51 taxa were recorded for the first time during this study.

The list of invertebrate taxa identified on Gökçeada along with their localities is provided in Table 2. New records for the island are marked with asterisks.

The most frequent taxa in this study are G. komareki and B. gokceadaensis with a frequency of 25.93%, followed by T. tubifex, Gammarus sp., and Caenis sp. with a frequency of 22.22% (Table 2).

Discussion

In the present study, four taxa of Gastropods were recently described and are endemic to Gökçeada (Odabaşı et al. 2019). In addition, some invasive species were also recorded in this study. Physella acuta is the only invasive and alien species that was recorded at two sampling sites, site 9 and site 25, i.e. Zeytinli Dam Lake and Şahinkaya Pond, respectively. It is a globally invasive freshwater snail, native to North America and found in a wide variety of aquatic habitats due to its resistance to organic pollution. It is a pioneer species that easily establishes a population in a new habitat and spreads via aquatic birds (Taylor 2003; Ebbs et al. 2018). Dreissena polymorpha is an invasive bivalve species, but unlike P. acuta, it is native to Eastern Europe and the Black Sea catchment area. Similarly, this species was found at sampling sites where P. acuta occurs with large colonies on all hard substrates. The main route of the species introduction may be associated with some vehicles or equipment such as boats and fishing gear that bear D. polymorpha clumps (Benson et al. 2020). P. acuta and D. polymorpha, which were recorded in some freshwater habitats of Gökçeada, were not mentioned in previous studies except Odabaşı et al. (2019). However, according to the field observations in this study, D. polymorpha had probably entered the ecosystem before the year it was found.

There are several studies dedicated to freshwater macroinvertebrates on Aegean Islands. Taxa belonging to the families Hemerobiidae, Chrysopidae and Myrmeleontidae found in Samothraki (Dvořák & Georgiev 2018), the island closest to Gökçeada, were not found in freshwater bodies of Gökçeada. Eidinger et al. (2016) also reported the occurrence of taxa representing several families of macroinvertebrates, including Gammaridae, Baetidae, Chironomidae, and Hydropsychidae, which are similar to those of Gökçeada. Moreover, Reischults (1988) reported six freshwater Mollusca species: Theodoxus fluviatilis euxinus, Islamia bendidis, Bythinella carpentieri cabirius, Ferrissia wautieri, Ancylus fluviatilis, and Pisidium casertanum. These species, with the exception of A. fluviatilis, are different from those found on Gökçeada.

Freshwater mollusks are one of the most studied taxa in the Aegean Sea archipelago. For example, researchers such as Schütt (1980), Bank (2004), Radea et al. (2016), Falniowski (2016), Georgopoulou et al. (2016), Szarowska et al. (2016), Glöer et al. (2018), Glöer & Hirschfelder (2019), Szarowska et al. (2014) reported the presence of taxa belonging to the families of Hydrobiidae, Bythinellidae, Planorbidae, Neritidae, Melanopsidae, Physidae, and Sphaeriidae. Most of the taxa listed by the above authors are local endemics, except Melanopsidae and Sphaeriidae. According to the study by Georgopoulou et al. (2016), eight freshwater Mollusca taxa occur on Andros Island located in the Northern Cyclades. When comparing taxa between the islands of Andros and Gökçeada, four of the ten gastropods are common, while Bythinella and Pseudamnicola species are local endemics for both islands.

Seven species of aquatic Heteroptera belong to the families Corixidae, Gerridae, Hydrometridae, Notonectidae, and Micronectidae known from Rhodes Island (Csabai et al. 2017), while only two species belong to Micronectidae and Notonectidae found in freshwater ecosystems of Gökçeada. According to the studies carried out on Gökçeada so far, the Chironomidae family is represented by 68 species, while 34 species belonging to this taxon were identified on Rhodes (Mora & Csabai 2008). Of the Chironomidae found on both Aegean islands, only two are common, i.e. Procladius (Holotanypus) sp. and Cricotopus triannulatus.

While one species belonging to the Gammarid family was recorded on the islands of Samothraki and Lesbos of the Aegean Islands (Hupalo et al. 2020), four taxa – Gammarus sp., G. komareki, Echinogammrus sp., and Pontogammarus robustoides – were found in this study. Considering the occurrence of species belonging to the Gammaridae family, it is clear that Gökçeada is characterized by high taxonomic diversity compared to other islands with the same geography.

Regarding freshwater macroinvertebrates, several authors have reported the occurrence of 80 taxa on Gökçeada. In addition to the taxa reported in previous studies, 46 taxa were identified in the present study for the first time. Thus, a total of 126 taxa of freshwater macroinvertebrates occur on Gökçeada. In conclusion, the taxonomic analysis shows that Gökçeada Island is very diverse in terms of freshwater macroinvertebrate fauna.

Considering all taxonomic studies on freshwater macroinvertebrates on the Aegean Islands, Gökçeada Island was found to occupy a prominent place among them in terms of macroinvertebrate diversity. It was hypothesized that habitat diversity (ponds, reservoirs, streams, and springs), geographical location and relief (Sarı et al. 2015) were the main driving factors that increase the aquatic biodiversity of Gökçeada.

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