Successful establishment of the Asian cyclopoid copepod Thermocyclops taihokuensis in Ukrainian waters

In Ukraine, T. taihokuensis was found for the first time in the Bucha River of the Kyiv region on 15 August 2020 (Fig. 2A) and then in the Sovka River on 11 October 2020. The species, however, was initially misidentified as T. oithonoides (Svetlichny et al., 2022), as specimens from those ponds have appeared highly morphologically similar to the description of T. oithonoides in the identification key of Monchenko (1974) (see also Fig. 2). Monchenko’s monographic work on the fauna of Cyclopoida in Ukraine includes the only three species of the genus, T. oithonoides, T. crassus (Fischer, 1853), and T. dybowskii (Lande 1890), known at that time for the country. Some late faunal studies of the ponds in the Kyiv region (Gaponova, 2014, 2016) also did not report the occurrence of any non-native Thermocyclops until at least 2016.

Figure 2

Habitus of T. taihokuensis (Harada, 1931) collected in a pond of the Bucha River on 15 August 2020 (A) and on 21 June 2025 (B), and T. oithonoides collected in the Dnieper River on 21 June 2025 (C).

Detailed morphological comparisons revealed that despite superficial similarities between T. oithonoides and T. taihokuensis, the specimens of Thermocyclops found in 2020, 2021, and 2025 in Ukraine (Table 1) are conspecific with T. taihokuensis, but not with T. oithonoides. Both species differ from T. crassus and T. dybowskii by a markedly greater difference in the relative lengths of the apical spines on the third endopodite segment of leg 4 (inner spine/outer spine = 3.0–5.0) (Figs 3G and 4D,E). Those apical spines are subequal in T. dybowskii, while in T. crassus, the inner apical spine is twice as long as the outer one.

Figure 3

Diagnostic characters of T. taihokuensis (Harada, 1931), female (Nyvky pond, Kyiv, Ukraine). (A) Pediger 5, genital double-somite and urosomites 3 and 4 (ventral view)—arrow shows posteriorly curved lateral arm of the seminal receptacle. (B) Anal somite and caudal rami with caudal setae coded by Roman numerals in the text (ventral view), setulation of the caudal setae is shown only on one side of the rami—arrow shows the spinules along the posterior margin of the anal somite. (C,D). Antenna: (C) coxobasipodite (posterior view); (D) coxobasipodite and first endopodite (anterior view). (E) Leg 3 intercoxal sclerite (posterior view)—arrow shows hairs. (F,G). Leg 4: (F) protopodite, first exopodite and first endopodite (posterior view)—arrows show the morphological features (intercoxal sclerite with short hairs; coxopodite seta with plumose setulation; medial expansion of the basipodite with a row of spinules and with acute tip distally) distinguishing the species from T. oithonoides; (G) third endopodite, homonomous setulation of setae is shown only on proximal section of the lateral seta. Scale bars show 50 μm. A–B show ♀-1[MIZ CRU 001316], C–D show ♀-4 [MIZ CRU 001319], and E–G show ♀-2 [MIZ CRU 001317].

Figure 4

Photos of the diagnostic characters in Thermocyclops species. (A) Genital double-somite with seminal receptacle (shown by arrow) in T. taihokuensis. (B,C) Anal somite and caudal rami with caudal setae, note the difference in the site of the insertion of the lateral caudal (II) seta on the caudal ramus between (B) T. taihokuensis and (C) T. oithonoides. (D,E). Leg 4, note the difference in the proportional length of the inner apical spine (indicated by arrows) in relation to the length of the segment between (D) T. taihokuensis; and (E) T. oithonoides.

Thermocyclops taihokuensis can be distinguished from T. oithonoides by several qualitative and meristic characters occurring on leg 4 and the urosome. Thus, the hairs on the posterior surface of the intercoxal sclerite of leg 4 (Fig. 3F, arrow) do not reach beyond the distal margin of the sclerite in T. taihokuensis, while they are longer and reach beyond the distal margin of the intercoxal sclerite in T. oithonoides. The coxopodite seta of leg 4 is plumose (with long setules) in T. taihokuensis (Fig. 3F, arrowed), while in T. oithonoides it bears very short, hardly noticeable setules (verified in specimens from Lakes Wigry and Białe Wigierskie in Poland and Lake Storbørja in Norway). The medial expansion of leg 4 basipodite has an acute apical tip, and small spinules are present on the posterior surface (Fig. 3F, arrows), yet both the acute tip and posterior spinules are absent in T. oithonoides (Lakes Wigry and Białe Wigierskie in Poland and Lake Storbørja in Norway). Lateral arms of the seminal receptacle are strongly curved posteriorly in T. taihokuensis (Figs 3A and 4A) vs nearly straight (perpendicular to longitudinal axis) in T. oithonoides (Mirabdullayev et al., 2003). The posterior margin of the anal somite ventrally has two rows of spinules (6–8 in each row) in T. taihokuensis (Ukraine) (Fig. 3B, arrow), vs the number of spinules is less (3–5) in T. oithonoides (verified in specimens from Lakes Wigry and Białe Wigierskie, Poland, and Lake Storbørja in Norway; Mirabdullayev et al., 2003). Other distinguishing features which however may show intraspecific variation are: i. the posterior surface of the intercoxal sclerite of leg 3 (and sometimes leg 2 as well) with one (middle) or two (middle and distal) rows of hairs in T. taihokuensis (Fig. 3E), vs hairs are absent or reduced to single row (distal) on leg 3 in T. oithonoides (Lake Wigry in Poland and Lake Storbørja in Norway); and ii. caudal setae V are curved in T. taihokuensis (Fig. 3B) vs straight in T. oithonoides (Fig. 4C).

Concerning the morphometric traits, the relative length of the inner apical spine on the third endopodite of leg 4 clearly separates the species: the ratio of the spine length to the segment length is 1.1–1.2 in T. taihokuensis (Ukraine) vs 1.5–1.8 in T. oithonoides (Lakes Wigry and Białe Wigierskie Poland, and Lake Storbørja in Norway; Mirabdullayev et al., 2003; Ukrainian sites) (Figs 4D,E). Position of the lateral caudal seta (II) on the caudal ramus is also informative: the seta is inserted near posterior third in T. taihokuensis (Figs 3B and 4B) while in T. oithonoides it is inserted near middle length of the caudal ramus (Fig. 4C). The total body length in T. taihokuensis varied from 0.970 ± 0.079 mm (Bucha River, 15 August 2020) to 1.125 ± 0.054 mm (Syrets River, 5 June 2025) and it was significantly (p < 0.05) greater than in T. oithonoides (0.727 ± 0.043 mm in the Dnieper River) (Table 2). The relative length and width of the urosome also differed between the species, i.e. the urosome is shorter and wider in T. taihokuensis than in T. oithonoides (Table 2).

Setal armature of the antenna and the surface ornamentation pattern of the antennal coxobasipodite provide numerous morphological features that are successfully used in species diagnostics in the Cyclopidae (Mirabdullayev et al., 2003). Monchenko (2008) (Uzboy River, Turkmenistan) and Zhikharev et al. (2020) (Sura River in west-central Russia) described the antennal coxobasipodite having two exopodite setae in T. taihokuensis, a character state never reported in the family Cyclopidae, and interpreted by Sługocki and Hołyńska (2024) as a developmental aberrancy (atavism) in these local populations. The specimens in the Kyiv region (verified in the material from Nyvky pond) had the typical setation of the antennal coxobasipodite, i.e. two medial and one long lateral (exopodite) setae at the mediodistal and laterodistal angle of the segment, respectively (Figs 3C,D). Posterior surface ornamentation of the antennal coxobasipodite (Fig. 3C) (Nyvky pond) is the same as that in the population in southern Hungary (Égervölgyi tó, Baranya County; see Sługocki & Hołyńska, 2024). This character is rarely reported in Thermocyclops species, and its diagnostic value for species identification still needs to be verified within the genus. The only published drawing of the posterior surface ornamentation of the antennal coxobasipodite in the native range of the species known to us is that one provided by Chang (2013). In contrast to the Ukrainian/Hungarian populations, the specimens from South Korea have no spinules in the medial half of the segment.

While our records are supported by detailed morphological comparison, future molecular analyses would provide valuable additional confirmation of the identity of T. taihokuensis across its introduced range and help to assess genetic divergence between native and invasive populations.

In Europe, T. taihokuenis was first found in the early 2010s in the southern part of European Russia and Hungary (Lazareva et al., 2022; Sługocki & Hołyńska, 2024), which may suggest that the species was present but overlooked at that time in Ukraine. A geographically broad-scale study and verification of Thermocyclops samples collected before 2020 could test this hypothesis. The Dnieper River is artificially connected to the Don River basin via water-transfer channels, which may facilitate the spread of T. taihokuensis. Zooplankton studies conducted in the Dnieper–Donbas Channel in the spring of 2020 reported the presence of T. oithonoides (Novitskyi et al., 2020), a species common in northern Ukraine and morphologically highly similar to T. taihokuensis. Therefore, revising the identification of those specimens may correct the occurrence records.

Nevertheless, the rate of expansion and certain occurrence records outside the major waterways suggest additional vectors, such as unintentional introductions through fish aquaculture, ballast water, and potentially birds. Passive dispersal by migratory waterbirds has been documented for copepods and other invertebrates, as eggs or cysts can be transported on feathers, feet, or via gut passage (Bilton et al., 2001; Hessen et al., 2019).

The high abundance of T. taihokuensis in 2020 in the ponds in the Bucha and Sovka Rivers, located about 30 km apart, may indicate that this Asian species had by then successfully established itself in the ponds of the right-bank tributaries of the Dnieper River. Thermocyclops taihokuensis co-occurs with other congeners (T. oithonoides and T. crassus) in the large river systems such as the Volga, Don, and Oder (Lazareva, 2022; Lazareva et al., 2022; Sługocki & Hołyńska, 2024), but it was the only representative of the genus in smaller water bodies around Kyiv. Thermocyclops taihokuensis was the dominant species in the zooplankton of all studied sites of the right-bank tributaries of the Dnieper River with an abundance varied between 430 and 12 600 ind. · m⁻³, but T. oithonoides was found only in the Dnieper riverbed, where calanoid copepods were dominant (Table 2).

Experimental studies on the thermal biology of T. taihokuensis (adult female) collected from the Bucha River in August 2020 and initially misidentified as T. oithonoides (Svetlichny et al., 2022) showed that under new conditions, this species exhibits a warm-water but eurythermal response to temperature changes. Thermocyclops taihokuensis females entered a lethargic state after 24 h at a temperature around 4°C. Their activity resumed between 7 and 27°C, and the recorded swimming speed increased synchronic with temperature, consistent with the linear temperature dependence of activity, a characteristic of the eurytherms. Field observations of the long breeding period of the species, lasting until October in the Shat Reservoir (Oka River basin, 54° N) in Russia, also confirm the eurythermic character of T. taihokuensis (Lazareva, 2021). Although the surface of most water bodies in Kyiv freezes in winter, the temperature in the lower layers does not fall below zero. Thermocyclops taihokuensis may have adapted its life cycle to low temperatures through diapause in bottom sediments.

Survival at higher latitudes may also be facilitated by the rising winter temperatures due to global warming, as indicated by the spread of other warm-water Thermocyclops species to the northern regions in Europe (Nowakowski & Sługocki, 2024) and Canada (Campbell et al., 2024). It should be noted that in the same year, we discovered another non-native Asian copepod, Sinodiaptomus sarsi (Rylov, 1923) in the Nyvky Park (Syrets River) (Svetlichny & Samchyshyna, 2021). In the warm season, T. taihokuensis and S. sarsi dominated the zooplankton in the Nyvky pond, and on 21 June 2025 S. sarsi was present in high numbers in the Borshchahivka River (unpublished). Interestingly, another invader Eucyclops roseus Ishida, 1997 was discovered in the Holosiivski and Orekhovatski ponds of Kyiv in 2020 (Gaponova & Hołyńska, 2022; Kostenko et al., 2021). All three newcomers in Ukraine, T. taihokuensis, E. roseus, and S. sarsi are thermophilic species with native distribution in Eastern and Central Asia.

In its native range, T. taihokuensis inhabits diverse water bodies, including ditches, small pools, fish ponds, rice fields, rivers, reservoirs, lakes, and water bodies in highly urbanized areas (Chen et al., 2012; Dela Paz et al., 2018; Guo et al., 2013; Li et al., 2010; Xie & Takamura, 1997). It occurs in both continental and island water bodies, such as those on Hainan Island (Li et al., 2011). The species primarily lives in freshwater environments, but was also found as a dominant component of the zooplankton in saline–alkaline ponds with a salinity ranging from 1.36 g · L⁻¹ to 20 g · L⁻¹ (Zhao et al., 2001). In Asia, T. taihokuensis often co-occurs with other Thermocyclops and Mesocyclops species and is a frequent and abundant taxon of the copepod communities (Wei et al., 2024; Zhao et al., 2007). The species was also found in water bodies of diverse trophic conditions, varying from oligotrophic to eutrophic (Li et al., 2010; Wei et al., 2024). Some authors suggest that T. taihokuensis may serve as an indicator for a high level of nutrients in the water (Dela Paz et al., 2018). Furthermore, Wu et al. (2018) reported a strong relationship (R = 0.87, Pearson correlation) between its abundance and chlorophyll a concentration in the Huangpu River, indicating a close link with the primary productivity. Along with the observations from turbid habitats such as the Huaihe River (transparency 0.40–0.43 m; Deng et al., 2013) and Chinese soft-shelled turtle (Trionyx sinensis) aquaculture ponds (Secchi depth 0.13–0.50 m, oxygen 1.36–7.06 mg/L; Wei et al., 2020), these findings suggest that T. taihokuensis is particularly well adapted to eutrophic and environmentally dynamic waters.

As a warm-adapted species, T. taihokuensis reaches its highest abundance in the warmest months. In the zooplankton communities of rivers and lakes in China, the highest densities were observed from June to August (Deng et al., 2013; Wu et al., 2018; Zhao et al., 2007). Its development rate is strongly temperature-dependent, with a total development time (egg to adult) ranging from 16.4 days (females) and 13.2 days (males) at 20°C to 9.3 days (females) and 6.8 days (males) at 30°C (Chen, 1985). The species exhibits marked sexual dimorphism in the rate of development, with males consistently reaching maturity faster than females, primarily due to the shorter copepodid stages. At lower temperatures (~20°C), the development slows significantly, more than doubling the maturation time compared to the summer peak. This slower development limits the population turnover in spring and autumn, while the very rapid development during warmer periods allows the species to exploit the seasonal productivity peaks. These traits indicate strong adaptation to eutrophic and thermally dynamic environments, with a high reproductive potential during summer and reduced growth activity in the cooler months. We speculate that the higher reproductive rate of T. taihokuensis compared to native species (Maier, 1989) may facilitate its competitive advantage in warm, food-rich environments, which are especially common in small water bodies during the summer.

Long-term studies also indicate its opportunistic strategy. Lu and Xie (2002) reported that in Lake Donghu (China), between the 1960s and 1990s, substantial changes occurred in the zooplankton community structure, following the introduction of filter-feeding fishes. As a consequence, the large-bodied Daphnia and calanoid copepods became rare, while T. taihokuensis and Diaphanosoma brachyurum (Liévin, 1848) increased in dominance. This demonstrates the capacity of T. taihokuensis to take advantage of altered community structures or newly constructed water bodies.