Conspicuous scyphozoans have received increasing attention in recent decades owing to their ability to form large blooms in their pelagic medusae stage, typically causing adverse effects on ecosystems and human activities (Condon et al., 2012; Graham et al., 2014). One of the most common blooming medusae is Aurelia, a genus comprising multiple cryptic species living in coastal and shelf-sea environments worldwide (Lawley et al., 2021). These cosmopolitan species have also been introduced in many regions worldwide (Dawson et al., 2005; Ki et al., 2008), further potentiating their expansion. Each local population is genetically differentiated and may have different reproductive traits as an adaptation to their habitats (Schroth et al., 2002). Moreover, each ecosystem is subject to environmental changes on various spatial and temporal scales. To cope with such variability, many organisms have evolved reproductive strategies that trade off their fitness in favor of risk reduction (Schnedler-Meyer et al., 2018).

Aurelia species are characterized by a metagenetic life cycle that comprises an alternation between sessile benthic polyps (hereafter referred to as polyps) and free-living pelagic medusae (Jarms, 2010). Polyps reproduce asexually, producing and releasing ephyrae through a process known as strobilation. In contrast to most scyphozoan species, where polyps propagate through one asexual mode (mono-mode species; Schiariti et al., 2014), Aurelia species present complex reproductive strategies that include various asexual modes that can even be simultaneously displayed to produce new polyps (multi-mode species; Schiariti et al., 2014). Although the final product of these propagation modes is always a new polyp, the use of a particular mode, or a combination of more than one, might have ecological implications related to the number of released medusae, and, consequently, the frequency and magnitude of jellyfish blooms. Although observations of the asexual reproduction of Aurelia species have accumulated in recent years (Lucas et al., 2012; Wang et al., 2012; Schiariti et al., 2014, 2015), the drivers of their diverse reproduction strategies and how they promote the maintenance of the polyp populations remain unclear.

Many researchers have identified the importance of temperature and food supply for the survival of Aurelia polyps (Ishii and Watanabe, 2003; Han and Uye, 2010; Wang et al., 2015; Wang and Li, 2015; Shi et al., 2016). In general, the asexual reproduction rates (Rr) and the number of new individuals increase with temperature (Han and Uye, 2010; Lucas et al., 2012); it is also believed that abundant nutrition increases the reproduction rates of Aurelia polyps (Ishii and Watanabe, 2003; Han and Uye, 2010; Kogovšek et al., 2010; Schiariti et al., 2014; Wang et al., 2015; Wang and Li, 2015). However, these studies were mostly focused on a single population of Aurelia polyps. Different Aurelia lineages might have unique adaptations concerning their reproductive capabilities and reproduction modes according to the environmental conditions of their respective habitats (Schiariti et al., 2014; Schnedler-Meyer et al., 2018), which may result in different blooming potentials. Therefore, understanding the asexual reproduction of Aurelia lineages in a broader population range in response to current environmental changes such as global warming and eutrophication, may effectively reveal the key drivers of jellyfish blooms, thereby providing vital fundamental to predict jellyfish-related disturbances in different regions.

In this study, we explored the effects of temperature and food availability on asexual reproduction rates and strategies of five strains of Aurelia polyps of different geographical origins. The polyps were exposed to three temperatures (10, 15, and 20°C) and two food regimes (starvation and feeding ad libitum), and the corresponding effects on Rr and strategies were measured. Experimental temperatures were selected based on the species culture conditions to ensure favorable temperature ranges for all studied strains.

We observed the following asexual reproduction modes (Figure 2A): typical lateral budding (LB), lateral budding by means of stolons (LBst), reproduction from the parts of stolons/stalks (ST), motile bud-like tissue particles (MP), podocysts (POD), and strobilation (STR), which were comprehensively described by Adler and Jarms (2009) and Schiariti et al. (2014). The number of polyp-to-polyp asexual reproduction modes displayed by each strain varied between four and five; all strains produced new polyps by means of LB, LBst, ST, and POD (Figure 2B). MP was formed by A. coerulea_USA, A. coerulea_SPA and A. solida_ISR. STR was only observed in A. coerulea_USA. The survival rate of Aurelia polyps was 100% in all treatment combinations for all strains, indicating an overall tolerance to the experimental conditions.

The results of this study suggest that temperature and food supply seem to be the environmental factors that influence the Rr of Aurelia polyps, which determine the potential number of medusae released into the pelagic realm. The different responses of each strain may serve as the indicators of their potential to cause outbreaks. The highest Rr under sufficient food conditions regardless of temperature was observed in the United States strain, suggesting that jellyfish blooms are more likely to occur in this area than in any other tested areas; the Israel strain is the least likely to cause a jellyfish bloom, as it had the lowest Rr. Several laboratory experiments have investigated the effects of these factors on polyp reproduction by exposing polyps to different conditions, and most studies have revealed accelerated and increased production of new polyps in response to warm temperatures and high food availability (e.g., Purcell, 2007; Lucas et al., 2012; Schiariti et al., 2014), which are consistent with the results obtained in our study.

Food supply had the most significant effect on Rr, with starved polyps producing considerably few new polyps (or none). The importance of food supply in Aurelia polyp reproduction has been previously observed for different species and locations, indicating that higher food concentration promotes Rr (Lucas et al., 2012 and references therein). The contrasting feeding conditions used in this study did not allow for testing the gradual effects of food concentration but confirmed that a certain nutritional state is required for polyp reproduction. Nevertheless, mortality was null in all experiments, suggesting a high tolerance of these strains to unfavorable conditions. Although reproduction was minimal or null, 100% survival indicated that Aurelia polyps could tolerate starvation for 7 weeks within the studied temperature range. The ability to tolerate hunger has been observed in Aurelia polyps, even for considerably longer periods (up to 60 days; Spangenberg, 1967; Shick, 1975; Sun et al., 2017). However, the water that was filtered through a 0.45 μm mixed membrane might contain a certain concentration of picoplankton and bacteria that seeped through, providing nutrition for the livelihood of polyps (Kamiyama, 2011).

Without food limitations, the effect of temperature on Rr was clearly observed, with higher Rr being observed at warmer temperatures (Figure 3). This trend has been confirmed in several Aurelia species (most of them identified in the literature as A. aurita) both in the laboratory (Kakinuma, 1975 Keen, 1991; Han and Uye, 2010; Schiariti et al., 2014) and in field conditions (Gröndahl, 1988; Watanabe and Ishii, 2001; Willcox et al., 2008), with only few studies have reported the opposing trend, where fewer polyps were observed at warmer temperatures (Purcell, 2007; Winans and Purcell, 2010). These contrasting patterns have been attributed to the adaptations of Aurelia spp. to specific environments (Widmer et al., 2016). However, the lower budding rates at warmer temperatures reported by Purcell (2007), and Winans and Purcell (2010), corresponded to treatments where higher strobilation rates were observed. Therefore, although several species can simultaneously strobilate and produce new polyps, the available energy would have been utilized for ephyrae production at the expense of polyp production. In our study strobilation was only observed in A. coerulea_USA at low rates, and therefore, the effect on the response of Rr could be neglected.

The positive effects of temperature and food supply (as a proxy for nutritional state) on asexual Rr of polyps are common not only in Aurelia but also in different species of Scyphozoa. When food is sufficient, Aurelia uses excess energy to expand the polyp population rather than support individual livelihood (Lucas, 2001). However, when the stimulus for strobilation is present, polyps might start producing ephyrae at the expense of polyp Rr. Temperature changes (mostly a decrease in temperature) can trigger strobilation in several Aurelia species/strains (Kroiher et al., 2000; Fuchs et al., 2014; Sukhoputova and Kraus, 2017). In our study, all polyps were kept at 15°C during the acclimation period before the experiment, and one-third of them then suffered a 5°C temperature decrease when kept at 10°C. The strobilation observed in A. coerulea_USA was likely triggered by this stimulus. However, the formation of ephyrae is not only induced by temperature changes but also by particular combinations of environmental factors specific to each strain (Berrill, 1949; Russell, 1970). The presence of only one of these factors alone is not sufficient to induce strobilation.

Our results confirmed previous experimental observations, indicating that Aurelia polyps can display most of the asexual reproduction modes described for Scyphozoa (Adler and Jarms, 2009). We also found that Aurelia strains produced new polyps mostly via non-motile buds (LB + LBst) and ST. Within optimal temperature and food availability ranges, Aurelia polyps propagate almost exclusively through these modes, colonizing substrates very rapidly (Han and Uye, 2010; Schiariti et al., 2014, 2015). However, room for expansion soon reaches a limit, and available substrate becomes a limiting factor that controls population size, reproductive output, and survival of polyps, similar to many other sessile marine invertebrates (Müller and Leitz, 2002; Purcell, 2007; Schiariti et al., 2015).

Utilization of these modes (mostly the budding types) allows rapid colonization of available substrates, reaching an average of 4 (A. solida_ISR)-8 (A. coerulea_USA) polyps per day. As described by Schiariti et al. (2014), the formation of a new polyp takes between 3 and 5 days from the first signs of the bud to its detachment. A new bud develops its tentacles and starts feeding before detachment, becoming a double-headed polyp with elevated feeding rates, allowing increased energy storage for reproductive and somatic growth. The same pattern was described by Han and Uye (2010) for A. aurita s.l. These rapid reproduction modes are utilized by all Aurelia species described so far when there is room for the attachment of new polyps (A. coerulea, A. solida, A. aurita, A. limbata, and A. labiata; Coyne, 1973; Keen and Gong, 1989; Han and Uye, 2010; Schiariti et al., 2014, 2015). However, Aurelia starts developing MP after a certain threshold of density is achieved (carrying capacity; Melica et al., 2014); therefore, the permanent low-density population during our experiment would explain the low rates of MP production observed for all strains. Thus, the multi-mode reproduction strategy allows Aurelia to rapidly colonize the available substrate rapidly in favorable conditions, encyst and withstand adverse conditions, and develop motile buds or detach to facilitate dispersion and avoid the negative effects of inter-or intraspecific competition for space and food.

In summary, temperature and nutrition play vital roles in regulating asexual reproduction of Aurelia strains. Starvation appeared to be a common limiting factor for reproduction at all experimental temperature values. However, temperature also affected Rr, with a higher number of produced polyps at higher temperatures. Therefore, the combined effects of temperature and food supply may synergistically affect polyp reproduction and density, both positively and negatively. Furthermore, the multi-mode reproduction strategy allows Aurelia to adapt to the changes in the environment. The capability to switch reproductive strategies in response to environmental cues gives Aurelia high adaptability (Schiariti et al., 2014, 2015). These features, in addition to the high tolerance of Aurelia polyps and medusae to changing environmental conditions (Lucas, 2001; Lucas et al., 2012), describe the high frequency of blooming events of the cosmopolitan Aurelia lineages.

The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding author.

The authors declare that sampling of specimens was performed in the respect of ethical rules and Chinese laws. No approval of research ethics committees was required to accomplish the goals of this study because experimental work was conducted with an unregulated invertebrate species.

ZD, AS, and JZ contributed to the experimental designs of the manuscript. SX and FW conducted the experiment. FW, AS, SX, YM, TS, LW, and ZD contributed to the analysis of the data and writing of the manuscript. All authors contributed to the article and approved the submitted version.

This work was supported by grants from the National Natural Science Foundation of China (No. 41876138), Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA23050301), the National Science and Technology Fundamental Resources Investigation Program of China (2022FY100603), the Key Project of NSFC-Shandong Joint Fund (U2106208), Instrument Developing Project of the Chinese Academy of Sciences (No. YJKYYQ20180047), the Taishan Scholars Program, and FONCyT PICT 2018–03872.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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