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1 Spatial Dispersal of Freshwater Organisms: Causes and Routes

In geological and geographical scales, freshwaters are short living and small-sized habitats. This imposes selective forces on their inhabitants and promotes both dormancy and dispersal. While these are plants that are widely recognized to use their dormant seed stage for dispersal, animal dormant eggs are functionally analogous, and routes of their dispersal are similar.

1.1 Ultimate Causes Behind Spatial Dispersal of Freshwater Organisms

Living creatures are relatively fragile structures, yet they have been present on Earth for more than 3 billion years. Their long existence is owed not to their extraordinary endurance, but to their endless replication and their spatial or temporal avoidance of unfavourable conditions (Venable and Lawlor 1980; Mc Peek and Kalisz 1998; Buoro and Carlson 2014). Organisms with effective mechanisms of dispersal may survive by shifting between habitats as long as environmental variations are not correlated between neighbouring locations. All habitat are exposed to some spatial or temporal variation in abiotic conditions. Even in relatively stable abiotic setting, biotic interactions may inevitably cause spatial or temporal fluctuations in environmental conditions. Uneven distribution of resources, interspecific competition (Holt and Barfield 2002), predation (Weisser 2002) or parasitism (Boulinier et al. 2002) may affect fitness of organisms considerably and drive spatial dispersal (Gandon and Michalakis 2002). Moreover, spatial dispersal might be beneficial even in invariable locations due to kin interactions (including sib competition or parent-offspring conflict (Hamilton and May 1977)) or inbreeding depression (Bengtsson 1978; Perrin and Mazalov 1999).

Aquatic organisms inhabiting freshwater sites need to disperse more desperately than their marine counterparts do. Most freshwater lentic habitats are highly isolated, ephemeral habitats in geological and evolutionary timescales that emerge and vanish frequently. Majority of lakes formed in the northern temperate zone after the last glaciation has disappeared within the last ten thousand years (Marszelewski 2005). Shallow temporary waters persist even shorter than large deep lakes. Thus, most if not all species inhabiting freshwater bodies need effective mechanisms of overland dispersal to thrive in time.

Environmental deteriorations may have abiotic or biotic origin, operate at local or regional scale and concern all organisms – mobile and immobile ones. While mobile organisms may seek suitable locations in the active form, the sedentary species or those living in isolated habitats frequently use their dormant forms for passive dispersal (Bohonak and Jenkins 2003; Panov et al. 2004; Panov and Cáceres 2007).

1.2 Importance of Dormant Forms in Animal Dispersal in Freshwaters

Most freshwater animals are able to move actively within aquatic habitats. Some of them may also travel between waterbodies along permanent or temporal waterway connections (Michels et al. 2001; Shurin and Havel 2002; Leuven et al. 2009). Yet, many lakes and ponds are island-like habitats, permanently isolated from each other by impenetrable terrestrial barriers. They are not lifeless, though, but inhabited by various aquatic species that colonize them quickly (Louette and de Meester 2005; Juračka et al. 2016). Some animals may actively cross short terrestrial barriers between aquatic habitats, e.g. vertebrates like reptiles, amphibians, or even fish, as well as invertebrates, e.g. most insects and some crustaceans. However, most aquatic species are incapable of moving across terrestrial zone due to sedentary lifestyle or poor moving skills or due to intolerance to overland conditions, e.g. desiccation. While passive dispersal of active forms between water habitats seems feasible on meter-wide distances, most freshwater animals are not able to survive long overland journey. Still, many of them are able to disperse passively across hostile terrestrial habitats once they suspend their development. Dormant forms of freshwater species are well suited for overland dispersal (Panov et al. 2004; Panov and Cáceres 2007). They are tolerant to various abiotic and biotic threats (Radzikowski 2013) and may possess various morphological or physiological adaptations facilitating their dispersal.

1.3 Routes of Passive Dispersal of Dormant Aquatic Organisms

Organisms producing resting stages disperse passively via different routes, often with multiple processes and vectors involved (Higgins et al. 2003; Incagnone et al. 2015). From the disperser perspective, that is, from the viewpoint of the challenges the animals encounter on route, and thus the mechanisms, or the adaptations, facilitating dispersal via these routes, dormant propagules of freshwater organisms move between habitats, mainly thanks to different processes such as (1) floating on the water surface, (2) sticking to other surfaces, (3) surviving being eaten or (4) floating in the air. The relative importance of these phenomena to effective dispersal and population establishment naturally varies both between organisms and their propagule characteristics, and between habitats. Also, the contribution of the different processes and vectors varies between studies, and is still unresolved (see Bohonak and Jenkins 2003; Cohen and Shurin 2003; Allen 2007; Vanschoenwinkel et al. 2008a; Coughlan et al. 2017).

1.3.1 Floating on Water

Water-air interface is the first gateway out of the aquatic habitat. Floating in water – plankton-wise – distributes the propagules within and between interconnected bodies of water, and may aid encountering animate and inanimate vectors, but in itself is not effective in transporting them between the habitats where waterway connections are scarce. Temporarily entering neuston, in its turn, exposes propagules to further potential vectors of dispersal. For aquatic plants, water-mediated spread of seeds, i.e. hydrochory, is recognized as an important dispersal route (Hopfensperger and Baldwin 2009; Pollux et al. 2009), and there are no reasons to expect it to be otherwise for aquatic animals dispersing via dormant forms. As propagules float, thanks to either of the two acting forces, buoyancy (upthrust) or surface tension, water-borne dispersal is facilitated by traits harnessing either of them. Floatability is even used as a proxy for seed dispersal capacity (Kappes et al. 2014; van Leeuwen et al. 2014). For freshwater invertebrates, the dormant stage floatability has also been linked to dispersal capacity, like the increasing proportion of floatoblasts to sessoblasts produced with increasing ramet size of bryozoans (Karlson 1992), the distinction and phenotypic reversals between floaters and sinkers among resting eggs of an anostracan (Pinceel et al. 2013), or the prevalence of floating and sinking ephippia of cladocerans (Pietrzak and Ślusarczyk 2006; Cáceres et al. 2007; Ślusarczyk et al. 2017a). Furthermore, numbers of propagules attached to birds have been recorded to coincide with their availability on the water surface (Brochet et al. 2010a).

1.3.2 Sticking to Surfaces

What makes propagules trapped at the water-air phase boundary makes them also stick to other surfaces. Darwin famously noted minuscule creatures actively crawling onto duck feet immersed in water, but in fact, even surface debris, dead or alive, will stick to a resurfacing object provided both have hydrophobic surfaces. For instance, cladoceran ephippia get easily and firmly attached to hair fringes of the abdomen and legs of a heteropteran insect Notonecta sp., and thus are carried away from the water surface, with ephippium floating ability being a critical factor here (van de Meutter et al. 2008). Propagules of many aquatic species have been repeatedly found to be externally transported by vertebrates, especially waterbirds, but also mammals (Maguire Jr. 1963; Bilton et al. 2001; Figuerola and Green 2002a). Plant, fungal and protist spores were reported to disperse between aquatic environments in plumage or on feet of ducks, waders and rails (Vivian-Smith and Stiles 1994; Figuerola and Green 2002b; Brochet et al. 2010b; Raulings et al. 2011; Lewis et al. 2014; Reynolds and Cumming 2016). So were invertebrate eggs, including dormant cladocerans (Figuerola and Green 2002b; Brochet et al. 2010a; Reynolds and Cumming 2016). Finally, the omnipresent and extremely migratory species, humans, now provides a multitude of artificial surfaces frequently moved between waterbodies. Tourism, transportation and research, all these activities involve adherence and movement of dormant propagules of aquatic organisms between environments, on equipment from vehicles and vessels to boots (see Waterkeyn et al. 2010; Valls et al. 2016; Bullock et al. 2018), where even a hundred of cladoceran ephippia can adhere to a single fishing line (Jacobs and MacIsaac 2007). Indeed, animal-mediated external dispersal of propagules, i.e. ectozoochory, has been frequently evaluated as an important route, at least on local scales (see Coughlan et al. 2017; van Van Leeuwen 2018, for most recent reviews). Still, a lot, including the impact of factors affecting attachment and detachment of the propagules, like bird preening behaviour or the role of sediment type, e.g. encapsulating mud (Figuerola and Green 2002b), is still understudied (Coughlan et al. 2017).

1.3.3 Being Eaten

Even if not directly preyed upon, adherence to various organic substrates will make the dormant stages more easily an unintended prey (Green et al. 2002; Reynolds and Cumming 2016). Wherever on the tree of life, if an aquatic organism produces dormant stages, some of them are likely to survive being eaten and being defecated at another location. Chances of surviving such internal transport might be even larger than chances of surviving external one (Reynolds and Cumming 2015). Comparing to ectozoochory, dispersal involving passage through the gut, i.e. endozoochory, of aquatic invertebrate resting stages and plant seeds may play even a more important role in terms of number and diversity of propagules dispersed between water bodies (Brochet et al. 2010b; Sánchez et al. 2012; Costa et al. 2014; Lewis et al. 2014; Moreno et al. 2019). However, their relative roles may change seasonally with the availability of floating propagules (ingestion and adherence) as opposed to constant availability of sediment propagule bank (ingestion) (Brochet et al. 2010a; Reynolds and Cumming 2015). Viable organisms, from freshwater algae (Proctor 1959) to cladocerans (Brochet et al. 2010a) are found in the lower digestive tracts of migrating birds, and a meta-analysis showed that roughly one in three waterbird droppings collected in the field contains a viable propagule, of which macroinvertebrates are almost as frequent as plant seeds (van Leeuwen et al. 2012).

1.3.4 Floating in the Air

As much as for the endozoochory, the presence of dormant forms is considered a prerequisite for effective wind dispersal, i.e. anemochory, of small aquatic metazoans (Panov et al. 2004). Once at the surface, or as soon as the temporary basin dries out, they are exposed to wind. Not only the resistant dormant state gives them good chances for survival outside their aquatic medium, but also, in anhydrobiosis they are lighter, and thus more easily than the hydrated forms taken into and moving in the air (Ricci and Caprioli 2005; Ptatscheck et al. 2018). This is important, as adaptations like ballooning – using silk to fly – have evolved only on land, in spiders, mites and moths (Bell et al. 2005). Recently, nematodes have been found as an exception to the general rule, readily dispersing in the air in active form, their aquatic taxa included (Ptatscheck et al. 2018). Copepods, cladocerans, ostracods and others have been caught moving in the air (Vanschoenwinkel et al. 2008b, 2009), yet, though considered to be an important mechanism of dispersal, the actual rates of airborne transport or the distances thus covered are hardly known (Ptatscheck et al. 2018). Since the early suggestions that winds are the ‘most important means of spread’ of minute dormant stages of both animals and plants (McAtee 1917), not much has been resolved on how often and how far do aquatic animals in diapause move in reality. A century later, it is proposed that, more specifically, during the dry phase of temporary ponds, wind is the most important dispersal vector of their inhabitants (Incagnone et al. 2015). The floating of the propagules aids to the wind importance (Ślusarczyk et al. 2017a; Sirianni 2017). Not only taxa themselves differ in their ‘flying’ propensity and its dependence on environmental conditions, but their measured dispersal rates also vary greatly both between studies and methods used (Ptatscheck et al. 2018).

2 Daphnia as a Model Animal with passively Dispersing Dormant Forms

A good single crustacean taxon to study the mechanisms behind dispersal of its dormant forms will (1) rely only or mostly on the dispersal of dormant forms; (2) disperse via different routes, giving opportunities to study various adaptations; (3) be found in large numbers on at least some of these routes, enabling quantitative sampling for comparative analyses; (4) have wide distributions; and (5) have a record of recent and contemporary invasions, both proxies for effective dispersal. We focus here on the genus Daphnia, animals (1) which rarely, if ever, are found dispersing between waterbodies in active form; (2) whose resting eggs are carried over the surface of fresh waterbodies, inside and outside other animals, and in the air; (3) whose resting forms in thousands are periodically found forming near shore carpets covering the surface (Ślusarczyk and Pietrzak 2008; Kaya et al. 2014; Incagnone et al. 2015; Ślusarczyk et al. 2017a), and which together with other cladocerans have been found to be the most abundant group emerging from samples collected from waterbirds (Brochet et al. 2010a); (4) whose species have worldwide distributions (Forro et al. 2008); and (5) which are repeatedly found invading new freshwater habitats of all kinds, natural and artificial, including those experimental (see Sect. 8.2.3). Taking this all together with its being a widely used model in various fields of ecological research, from ecotoxicology to environmental genomics and evolutionary biology, Daphnia provides a well-suited model for an aquatic animal dispersing via its dormant forms.

2.1 Roles of Dormant Eggs in the life of Daphnia

Daphnia dormant eggs together with the encapsulating protective shell form an ephippium, a structure which functionally resembles a plant seed (Pietrzak and Ślusarczyk 2006): a well-protected, by default sexually produced, embryo, ready to endure both temporal challenges of the local environment and those encountered on dispersal routes outside of the native habitat. Thus, these eggs play an important role in both re-establishing local populations and colonizing new habitats.

Daphnia dormant eggs are most often, and primarily, the result of sexual reproduction. When conditions deteriorate, these animals switch from parthenogenetic production of subitaneous eggs to sexual reproduction inseparably linked with dormancy. The development of sexually produced fertilized egg is halted at the early gastrula stage (Zaffagnini 1987). Though some lineages from regions where the growing season is short, like high latitudes and altitudes, skip the sexual part and produce dormant eggs parthenogenetically (Decaestecker et al. 2009), still each genotype newly emerging after recombination first switches on the dormancy developmental program.

Dormant eggs are produced by Daphnia in anticipation of regular fluctuations and in response to direct challenges: before summer drying out and winter freezing down of shallow ponds; before winter formation of ice cover on lakes; before periods of intensive predation risk (Ślusarczyk et al. 2006); and under increasing population densities (Berg et al. 2001; Fitzsimmons and Innes 2006). This may occur once a year (Ślusarczyk 2009) after the first or the second summer in life of an individual (Pietrzak et al. 2013) or more often, and at irregular intervals (Mikulski and Grzesiuk 2019, submitted manuscript), according to the actual conditions. At a single sampling up to 80% of the females may be found carrying an ephippium (Ślusarczyk 2009), and in the laboratory up to 100% of the experimental females may produce them under certain conditions (Ślusarczyk 1995; 2004). Individuals hatching from dormancy (females exclusively) may supply overwintering active population of Daphnia or re-establish it after seasonal extinction (Cáceres 1998b).

The ephippial eggs in order to hatch need to pass through a refractory period (initial phase of suspended development when embryo remains insensitive to hatching stimuli; Ślusarczyk et al. 2019, submitted manuscript) and receive a still undefined set of environmental triggers including temperature and light (Davison 1969; Radzikowski et al. 2018; Ślusarczyk and Flis 2019).

Their resistance and other features discussed in the next section make them perfect vehicles for overland transport. Though the existence of a general and direct relationship between the ability of producing dormant forms and dispersal efficiency is still controversial (Incagnone et al. 2015), still, we can discuss many of their associated traits as – if not direct dispersal adaptions – traits effectively facilitating their spatial dispersal. Their morphology, as well as maternal life history and behaviour associated with their production and disposal, and life history of dispersing individual itself, as traits aiding the dispersal capacity, are discussed in the next section.

2.2 Adaptations Facilitating Passive Dispersal of Resting Eggs in Daphnia

Passive dispersal of dormant forms to be effective should (1) coincide in space and time with the occurrence of their vectors and (2) be based on resistance to withstand specific challenges encountered while on travel via different routes. Pinpointing particular traits as being under direct dispersal-driven selection may be difficult, though. Many traits that affect dispersal have other functions (Burgess et al. 2016). Research on plants also shows that long distance dispersal events might be rare and driven by nonstandard mechanisms, and is across adaptations (Higgins et al. 2003). Still, multiple adaptations do exist and work on shorter scales. We focus here on the challenges and the facilitating mechanisms specific to spatial dispersal of these forms, discussing still unverified hypotheses, and giving less attention to mechanisms equally facilitating dispersal both in space and in time.

In the case of Daphnia, the time of ephippia production and the place of their deposition by the mother are vital for the dispersing propagule and the dispersal vector coincidence. As for the ephippium itself, its internal and external wall structure providing toughness and aiding its floatation, its sticky appendages aiding both floatation and adherence to other structures, and its size itself are the most important traits.

2.2.1 Reaching Water Surface: Oviposition Behaviour

Few vectors of ephippial eggs operate deep in the open water, in the life zone of Daphnia, while most of them operate close to the water surface – the dangerous zone for planktonic organisms. Therefore, the resting eggs of Daphnia should appear close to the water surface in the right moment to be dispersed between water habitats. We consider two likely options of their transfer to the water surface, these linked to animal properties and not to external forces, like water current movements or air bubbles leaving the sediments, neither of which has been to our knowledge reported to bring Daphnia either in active or dormant form to the surface.

Ephippia might be either displaced to the surface due to positive buoyancy, like they are in sessile bryozoans (Karlson 1992), or due to their oviposition by mobile ephippium carrying females (Ślusarczyk and Pietrzak 2008). The first option has been proposed (e.g. by Cáceres et al. 2007), yet not proved so far. Active Daphnia are negatively buoyant and must swim constantly, otherwise they sink (Vega and Clausse 1998). Positive buoyancy of ephippia would affect overall buoyancy of ephippia carrying females and would change their swimming behaviour (e.g. hop and sink rate), which, according to our knowledge, has not been reported so far. On the contrary, experimental tests made on three common species of Daphnia (D. magna, D. pulex, D. longispina) revealed that all freshly shed ephippia were negatively buoyant, likewise active forms, and sank to the bottom when being shed by females below the water surface (Ślusarczyk and Pietrzak 2008). All ephippia that appeared at the water surface in further tests were left there by ephippial mothers during moulting, despite surface threat imposed on them during the tests (high UV radiation). While all tested ephippial females remained far from the risky water surface for most of the UV exposition period, some of them swam toward the water-air interface a few seconds ahead moulting, where they moulted shedding ephippium and dived down shortly after (Ślusarczyk and Pietrzak 2008).

Daphnia, like most other planktonic organisms, avoid surface zone of aquatic habitats (Dawidowicz and Pijanowska 2018). Close to the water surface, Daphnia may be exposed to harmful UV radiation (Alonso et al. 2004), enhanced predation risk of visual predators (Gliwicz 2003), or desiccation if being caught by surface tension and then thrown ashore (personal observation). While ephippial eggs are highly resistant to these surface threats (Radzikowski 2013), active individuals are more vulnerable. To reduce some of these threats, ephippia oviposition at the water surface might occur during night, when both fish predation and UV radiation-associated risks are negligible. Such cyclicity of ephippia deposition at the water surface would be reflected in a higher proportion of ephippial compared to non-ephippial females in subsurface zone during night vs. daytime (Fig. 8.1), or by a higher density of ephippia at the water surface at night and dawn compared to the other periods of a day at a calm weather (Fig. 8.2).

Fig. 8.1
figure 1

Vertical distribution of Daphnia pulicaria females in the deep fishless mountain lake Czarny Staw in the High Tatras, Poland (49°11′18.1″N; 20°04′33.8″E), during the period of ephippia production: top - (black bars) ephippium carrying females; bottom (grey bars) non-ephippial females of the same lineage; during the day (left, white panels) and at night (right, shaded panels). (After Ślusarczyk et al. 2017a, modified)

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Fig. 8.2
figure 2

Diurnal changes in ephippia density (mean ± 1SE) of Daphnia of the longispina group at the water surface in the middle of the small Kociołek Lake (station 5) collected in a single day of an autumn period of ephippia formation. Letters above the bars indicate homogenous groups with similar values according to ANOVA model simplification

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2.2.2 Floating on Water Surface: External Morphology

Most of the ephippia left by females at the water surface retain negative buoyancy, yet stick to the water plane thanks to weak surface tension, suggesting hydrophobic properties of their outer wall. The role of surface tension was evidenced by sinking of ephippia after water-drop-induced disruption of the water surface or by applying a detergent that reduced surface tension and lowered the proportion of floating ephippia (Ślusarczyk and Pietrzak 2008). The elongated shape (Bormashenko 2016), flattening with protruding edges and relatively small size, all aid in their surface tension-induced floating.

Some ephippia left by Daphnia at the water surface gain positive buoyancy due to atmospheric air absorption. Anatomical analysis of the outer structure of the ephippium revealed possible way of air absorption (Bernatowicz et al. 2018). The ephippium of Daphnia is made of two concave chitinuous shells that enclose the resting eggs. Each shell is made of double walls (Hiruta and Tochinai 2014) interconnected by cellular integuments of various shapes (Bernatowicz et al. 2018). In Ctenodaphnia (D. magna, D. lumholtzi), the integument has sponge-like structure that hardly absorbs air unless ephippium dries completely. In other Daphnidae (longispina or pulex group), the wall has a honeycomb structure with hollow cells that readily absorb air after even brief contact with the atmosphere, what makes them positively buoyant. Air probably does not penetrate through external wall, which seems impermeable, but most likely enters integuments through a ventral gap then hollows in the internal wall. The surface of the external wall differs considerably between species, which might translate into differences in floating ability: in some species, the wall is dotted with convexities (e.g. D. rosea) or with concavities (D. pulex, D. longispina) or is covered by scaly shaped structures (e.g. D. magna) in others (Fig. 8.3).

Fig. 8.3
figure 3

Divergent morphology of the ephippium surface in different groups of Daphnia revealed by scanning microscopy. (a) D. magna, (b) D. pulex, (c) D. rosea

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2.2.3 Sticking to Other Surfaces: External Morphology Continued

What makes them hydrophobic and easily caught at the water-air phase boundary makes them also stick to other surfaces. Daphnia magna, which hardly ever sheds ephippia at the water surface and is expected to use other mechanisms aiding dispersal, has ephippia that are equipped with tacky filaments, remnants of the moulted carapace which are not seen in other species (Mergeay et al. 2006a), that stay with the ephippium and act as hooks, sticking readily to solid objects (personal observations).

2.2.4 Time of Reaching Water Surface: Timing of Life History Events

Ephippia appearance at the water surface was reported not only in laboratory studies but also in the field. Mass occurrence of ephippia at the water surface reaching thousands per square meter in the middle of the lake (Ślusarczyk and Pietrzak 2008) or getting even higher densities on the downwind shore of the waterbodies (Fig. 8.4). It would be tempting to associate seasonal occurrence of ephippia at the water surface with timing of operation of their putative vectors, e.g. with bird migrations period, which seem to us the most effective vectors of ephippial eggs dispersal. However, this would need to be disentangled from the effect of the timing of the environmental deterioration, which might be a stronger selection force than dispersal vector availability.

Fig. 8.4
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Floating ephippia accumulating in high densities on a downwind shore within foam or debris

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2.2.5 Harsh Physical Conditions: Resistance

While the structure of the wall of the ephippia varies greatly between species (Bernatowicz et al. 2018), it invariably gives them toughness and endurance. Also, unlike the subitaneous egg, the dormant embryo invariably has a yet another protective layer: the inelastic and highly impermeable outermost egg shell (chorion). The embryo also contains high concentrations of the heat shock protein Hsp60, and cryoprotective glycerol (Pauwels et al. 2007) and possibly trehalose (Smirnov 2014).

Dormant embryo enclosed in the protective ephippial case of some species of Daphnia may withstand prolonged desiccation, extremely high or low temperature, anoxic conditions and passage through the gut of fish or birds (for review, see Radzikowski 2013). For instance, ephippia from northern Daphnia from Greenland hatched with success after being keep at –18°C for 18 years (Meijering 2003).

We might expect some differences between resident and dispersal ephippial eggs in their resistance to environmental extremes since different selective forces may shape properties of the two groups. The ephippial eggs of the individuals predestined for passive overland dispersal might be expected to be more resistant to extreme abiotic threats than the resident ones. The latter remain at the bottom of the native habitats where they may never face desiccation nor extreme thermal conditions, which dispersion forms have to cope with. Indeed, ephippial eggs collected at the water surface (dispersing) revealed higher tolerance to elevated temperature and desiccation compared to the resident ones collected at the bottom of some deep lakes in Poland (see Radzikowski 2019 for more details).

Risk of mechanical damage of the resting eggs is relatively low in “soft” aquatic lentic habitats. Unlike, overland dispersing resting eggs are exposed to abrasion and much greater mechanical forces not balanced by water buoyancy or viscosity. Therefore, the ephippial case seems redundant for resident resting eggs residing in deep permanent lakes, more useful in temporarily drying habitats, while vital for those passively dispersing. In this light, the ephippial case could be viewed as a structural adaptation for overland dispersal. Indeed, cladocerans which possess well-developed ephippial case are among the first invaders to newly formed isolated waterbodies (Louette and de Meester 2005). The most advanced ephippial structures may be found in Daphnidae (including Moinidae), while poorly developed cases are found in other Anomopoda (e.g. Bosminidae, Chydoridae, Macrothricidae) and non-existent in other Cladocera: Ctenopoda, Haplopoda or Onychopoda (Fryer 1996).

2.2.6 Unknown Hatching Habitat: Sensitivity and Hatching Phenology

The resident and dispersal ephippial eggs might also differ in some other features related to their distinct functions, like hatching phenology or longevity, which has not been probably tested so far. According to Venable and Levin (1985), who compared hatching phenology of dispersal and resident seeds of some terrestrial plants inhabiting unpredictably changing desert habitats, the dispersal seeds equipped with morphological adaptations for spatial dispersal germinated readily and synchronously while the resident seeds germinated more gradually. Some proportion of resident seeds postponed germination until a further favourable occasion as if they hedged against risk of unpredictable environmental deterioration (Venable and Lawlor 1980; Venable and Levin 1985). Diversified revival from the periodic rest (asynchronous germination or hatching) is considered the adaptive mechanism reducing risk of failed decision to resume development at uncertain conditions (Cohen 1966; Seger and Brockmann 1987; Ślusarczyk et al. 2017b).

It is hard to guess which ephippial eggs, either dispersal (shed at the water surface) or resident (released in the water column), should reveal higher longevity since both of them may be exposed to unpredictable environmental fluctuations. The dispersal hitchhikers may be displaced into unpredictable sites before they luckily reach some suitable location. Yet, the fate of the resident ephippia might not be defined either, once most of them may be buried for indefinite time in lake sediments before some external force (burrowing animal, gas bubbles, etc.) bring them back to the sediment surface, only where their development is feasible (Radzikowski et al. 2016). Large quantities of ephippia reside deep in lake sediments (Carvalho and Wolf 1989; Cáceres 1998a; Kerfoot et al. 2004) and may never hatch. For the above reasons, both dispersal and resident ephippial eggs might feature long viability, helping them to survive to a rare occasion for reactivation. While dispersal ephippia might possibly hatch at first favourable occasion (as it might be the last one), the resident should be more careful and reveal bet-hedging way of reactivation to cope with temporal variability of environmental conditions. The uncertainty receives now a new dimension under increasing intensity and scope of anthropogenic hydrological disturbances in the freshwater habitats (Brendonck et al. 2017).

So far we know little about Daphnia hatching phenology, length of latency included. We are aware that ephippial eggs of some lake Daphnia have very long dormancy periods reaching decades (Cáceres 1998a) or even centuries (Frisch et al. 2014), while those from temporary ponds reveal bet-hedging way of reactivation (Radzikowski 2019) which may prevent coincident resurrection off all resting eggs and diversify the risk of the failed choice in unpredictably changing habitats. We do not know, however, the hatching phenology of ephippial eggs of the lake Daphnia nor longevity of ephippial eggs in temporary waters, not mentioning the differences between resident and dispersing ones in that field.

2.2.7 More Challenges and Mechanisms

Many more potentially important selective forces can be identified and adaptive mechanisms speculated on. Surviving gut passage demands particular chemical and mechanical resistance. Anemochory and ectozoochory are facilitated by small size of the propagule (van de Meutter et al. 2008), which in case of Daphnia is directly linked to mother body size, and female-size-corrected variation in ephippium size has not been shown so far. Lethal effect of ultraviolet light is a vital factor not only for airborne propagules (Maguire Jr. 1963) but also to all exposed for longer periods to direct sunlight. Hydrophobic ephippial case offers enhanced protection against desiccation, and honeycomb-like structure offers enhanced protection against mechanical damage (Bernatowicz et al. 2018) and – when incrusted with black protective pigments – to UV radiation (Shan 1970). Indeed, pigmentation of the shell varies between ephippia (Gerrish and Cáceres 2003), and its association with dispersal versus resident phenotype has neither been shown yet.

2.3 Effectiveness of Passive Dispersal

For a long time, it was thought that plankton organisms producing resting stages have high dispersal capacities, enabling them to successfully colonize waterbodies and be widespread in ponds and lakes across large-scale extent (Mayr 1970; Cohen and Shurin 2003). The wide geographical ranges of many freshwater taxa are testimony that passive dispersal by resting stages can be effective for dispersal-gene flow and make many aquatic taxa essentially cosmopolitan and genetically similar.

This assumption was questioned following detailed morphological studies (Frey 1982) and molecular work (Lynch and Spitze 1994; Colbourne and Hebert 1996; De Meester 1996a; Schwenk et al. 1998; Gómez et al. 2000, 2002). Comparison of patterns in gene flow in freshwater taxa with different life cycles support the scenario that high dispersal of organisms favour an effective monopolization of waterbody resources by newly invading species (and genotypes), yielding a strong priority effect (De Meester et al. 2002). This founder effect increases genetic differentiation among zooplankton populations inhabiting nearby ponds and reduces gene flow among populations and waterbodies. Boileau et al. (1992) proposed that the high levels of genetic differentiation in cyclic parthenogenetic species such as Daphnia reflect their potential to colonize habitats from a few resting eggs that are resistant to decay for dozens of generations, and their capacity for rapid population growth upon hatching. Such founder effects were illustrated by the persistence of non-indigenous species (Daphnia exilis and D. lumhotzi in USA; D. ambigua and D. parvula in Europe) as resting eggs in sediments and their rapid colonization only promoted by human disturbances (Hairston et al. 1999; Havel et al. 1995; Maier 1996).

De Meester et al. (2002) examined the potential mechanisms causing a discrepancy between high dispersal rates and reduced level of gene flow (the monopolization hypothesis and dispersal-gene flow paradox) in cyclical parthenogens such as Daphnia. Founder events upon colonization of waterbodies followed by rapid population growth and local adaptation of daphnids as well as buffering effect of resting eggs banks result in an effective monopolization of resources and a strong priority effect, creating high genetic differentiation among nearby populations (see also Boileau et al. 1992; Jenkins and Buikema 1998; Palsson 2000). Pronounced genetic differentiation among daphnid populations was detected for neutral markers as well as ecological relevant traits (De Meester 1996a, b). Thus, patterns of regional genetic differentiation in daphnid populations may often reflect historical colonization of new habitats via dispersal and priority effect rather than contemporary gene flow. In addition, strong local selection also favours genetic divergence among nearby populations even if dispersal rates are high (Michels et al. 2001; De Meester et al. 2002).

Effectiveness of passive dispersal in freshwater organisms is still debated because it varies among species due to specific differences in functional traits such as body size, resting egg features, resistance to environmental threats during dispersal and adaptation to local habitat (Cohen and Shurin 2003). There is now a substantial amount of evidence that daphnids exhibit significant potential for passive dispersal via long distance transport through wind (Michels et al. 2001; Cáceres and Soluk 2002), direct water flow among connected waterbodies (van de Meutter et al. 2006) or animal vectors such as waterfowl (Proctor and Malone 1965; Figuerola et al. 2003, 2005; Moreno et al. 2019) or aquatic insects (van de Meutter et al. 2008). However, several studies have suggested that aquatic microcrustaceans are relatively efficient dispersers in a variety of landscapes, whereas others have indicated dispersal limitation at large and small spatial scales or under specific circumstances (Juračka et al. 2016; Horváth et al. 2016).

Supporters of effective dispersal have shown that species of cladocerans can disperse effectively over short distance (<1 km) and colonize suitable habitats quickly depending on their ability to tolerate local conditions, such as water acidity and the presence of fish. Louette and De Meester (2005) monitored cladoceran colonization in 25 newly created waterbodies and isolated pools over a wide geographic area. They found high effectiveness of passive dispersal via transport of dormant stages. Daphnids (D. obtusa, Ceriodaphnia spp., Simocephalus vetulus and Scapholeberis mucronata) were the most frequently found, representing almost 50% of the colonization events. Experimental studies also gave strong evidence of high dispersal and colonization effectiveness of cladoceran zooplankton, as 60–75% of the regional species pool can be captured in mesocosms after between less than two months and two years depending on the distance to the nearest pond (Cáceres and Soluk 2002; Cohen and Shurin 2003; Lopes et al. 2016). Recently, dispersal limitation was suggested not important in the Arctic young freshwater habitats, where the structure of asexual Daphnia populations reflected environmental gradients and differences in clonal ecology (Haileselasie et al. 2016). In another study conducted in Ethiopian reservoirs, these were the founder effects again suggested to structure regional population (Haileselasie et al. 2018).

Effectiveness of passive dispersal of cladocerans has also been evaluated by quantifying the build-up of the dormant egg bank in the sediment during the first six months in newly created egg-free pools over Flanders, Belgium (Vandekerkhove et al. 2005). High densities (60–10000 eggs per m2) of cladoceran egg banks were observed in the new pools. In parallel, the temporal dormant egg bank on the water surface, reaching densities of hundreds to thousands of ephippia per m2, has been suggested as another proxy for this high potential (Ślusarczyk et al. 2017a). The high prevalence of floating ephippia in Daphnia may make it a more effective disperser than some other cladocerans (Sirianni 2017).

Supporters of dispersal limitation found multiple indications of dispersal limitation affecting the community assembly of microcrustacean communities. On a large-scale survey, spatial patterns in zooplankton community composition were better explained by the geomorphological structure of the landscape than by mere geographic distances between waterbodies (Juračka et al. 2016), suggesting that ridges separating the network of valleys act as dispersal barriers and may channel the dispersal routes of the taxa. Furthermore, dispersal limitation was reflected by a strong positive relationship between species richness and the number of neighbouring waterbodies. On a small-scale extent, although the effect of wind lessen dispersal limitation along its prevailing direction, it persists that dispersal limitation may constraint community assembly in highly mobile organisms even at spatial scale below 5 km (Horváth et al. 2016). Most probably, different processes dominate at different spatial and temporal scales. Heino et al. (2015) suggested dispersal limitation to be increasing with distances between habitats, contrary to the importance of mass effects, and the spatial extents of different processes to be affected by the dispersal ability of organisms. More recently, the need of using novel tools to assess the role of dispersal in shaping communities has been proposed (Heino et al. 2017).

2.4 Consequences of Dispersal of Dormant Eggs

Several phenomena associated with the passive dispersal of ephippial eggs may have far reaching non-adaptive implications for these organisms.

2.4.1 Ephippia Exploitation

During periods of intense ephippia formation, high quantities of ephippia may accumulate along the downwind shore of the waterbodies (Figs. 8.4 and 8.5). This supra- and meso-littoral aggregation of resting eggs constitutes an underestimated bank of Daphnia resting forms in freshwater habitats. The accumulation of the resting eggs of Daphnia may be intense enough to exploit it commercially in aquacultures likewise floating eggs of the brine shrimps Artemia franciscana and has already been suggested as a source for exploitation for chitin extraction (Kaya et al. 2014).

Fig. 8.5
figure 5

Mean densities of ephippia of Daphnia of the longispina group at the water surface of the small eutrophic Lake Kociołek (54°03′01″N 22°19′54″E), collected with half-submerged neuston net kept in front of cruising boat at noon at five sampling stations located along prevailing wind directions reported week ahead of sampling period. Letters below the density values indicate homogenous groups with values similar according to ANOVA model simplification

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2.4.2 Trap More Than Shelter

Ephippia accumulate in deep locations. The resident ephippia which are shed below the water surface, and those oviposited at the water surface that sink with time become unevenly distributed over the lake bottom. The highest densities of ephippia frequently occurs in the deepest zones of lakes (Carvalho and Wolf 1989; Jankowski 2003; Kerfoot et al. 2004) either because of the higher number of females shedding ephippia in cumulated volume of water above those places or, what is more likely, due to their slipway from shallower locations along the bottom slopes. Controversy exists if bottom sediments are shelter for the resting eggs or rather a trap that disable their hatching (Cáceres and Hairston 1998). Dormant forms of aquatic species may reside in lake sediments for long time not deliberately, but due to their burrowing by lake sediments. According to Radzikowski et al. (2016), even a thin sediment layer (less than 2.5 mm) may hamper development of resting eggs of Daphnia. This might provoke a significant question on the ultimate function of ephippia deposition at the water surface: is it dispersion between, or rather within aquatic habitats? Daphnia could shed ephippia at the water surface not to colonize other waterbodies, but to let them be rafted toward the shallow littoral zone and try to escape the sediment trap of the profundal zone. Higher proportion of ephippia left by Daphnidae at the water surface in shallow lakes with frequently mixed sediments than deep ones with stagnant bottom (Ślusarczyk et al. 2017a) indicate, however, that between-lake dispersal is the more likely selective force behind this phenomenon.

2.4.3 Anthropogenic Invasions

Local mass aggregations of ephippia, together with their clinginess to different surface, and with carelessness on the human part, has led to unprecedented dispersal events. Intensified transport of dormant forms by anthropogenic vectors (e.g. by regional and global trades) broke existing intercontinental barriers and facilitated colonization of freshwater habitats by invasive species. This includes encroachment of alien species of Daphnia originating from remote locations in a recent time (Havel and Shurin 2004; Panov et al. 2004; Panov and Cáceres 2007), e.g. ongoing invasion of D. lumholtzi in North America (Havel et al. 2002) or D. pulex in Africa (Mergeay et al. 2006b).

2.4.4 Enhanced Biotic Diver sity and Slower Evolutionary changes

The spatial dispersal of dormant forms may enhance biotic diversity on a local (alfa diversity) and regional scale (gamma diversity) due to immigration of novel or recolonization of exterminated genotypes from neighbourhood locations (Chesson 2000) and reduce biotic dissimilarities between habitats within a region (i.e. lower beta diversity). The immigration of dormant forms from neighbourhood locations, like resurrection from the native bank of resting eggs, may slow down competitive exclusion of suboptimal competitors by superior ones and slow down evolutionary changes within genetic pool and species sorting within local habitats (Hairston and de Stasio 1988).

3 Conclusions

While the old paradigm of panmictic occurrence of planktonic species due to their easy colonization of aquatic habitats has eroded, the frequent spread of aquatic organisms has not yet been seriously questioned. What stops their successful invasions seems abiotic and biotic filters rather than dispersal barriers (Shurin 2000; De Meester et al. 2002; Incagnone et al. 2015). Frequent overland dispersal may be attributed to dormant forms used not only for temporal but also for spatial dispersal. Freshwater dormant forms can survive long voyage across hostile terrestrial zone and may hitchhike using various animate or inanimate vectors, especially when aided by behavioural or morphological adaptations. Planktonic crustaceans of the genus Daphnia are among the first colonizers of newly founded waterbodies (Louette and de Meester 2005). Ephippial case of resting eggs may boost their spatial dispersal by offering positive buoyancy facilitating their hitchhiking by surface vectors and enhanced protection against mechanical damages or UV radiation. During periods of intense ephippia formation, high quantities of ephippia often accumulate along the downwind shore, where the wind blows them to. The supra-littoral and meso-littoral banks of resting eggs may be an underestimated source not only for passive dispersal between waterbodies but possibly also as a refuge preventing their dislocation to the deep trap of profundal sediments.

Daphnia is undoubtedly the best-studied cladoceran species. The question remains, how effective is dispersal of other cladocerans with poorly developed ephippia or no ephippia at all, and what mechanisms of dispersal they utilize instead. An open question remains also, if dormant eggs used for only temporal dispersal differ structurally or physiologically from ones used for spatial dispersal.