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VIEW Open Access Long-Distance Passive Dispersal in Microscopic Aquatic Animals Diego Fontaneto

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VIEW Open Access Long-Distance Passive Dispersal in Microscopic Aquatic Animals Diego Fontaneto Fontaneto Movement Ecology (2019) 7:10 https://doi.org/10.1186/s40462-019-0155-7 REVIEW Open Access Long-distance passive dispersal in microscopic aquatic animals Diego Fontaneto Abstract Given their dormancy capability (long-term resistant stages) and their ability to colonise and reproduce, microscopic aquatic animals have been suggested having cosmopolitan distribution. Their dormant stages may be continuously moved by mobile elements through the entire planet to any suitable habitat, preventing the formation of biogeographical patterns. In this review, I will go through the evidence we have on the most common microscopic aquatic animals, namely nematodes, rotifers, and tardigrades, for each of the assumptions allowing long- distance dispersal (dormancy, viability, and reproduction) and all the evidence we have for transportation, directly from surveys of dispersing stages, and indirectly from the outcome of successful dispersal in biogeographical and phylogeographical studies. The current knowledge reveals biogeographical patterns also for microscopic organisms, with species-specific differences in ecological features that make some taxa indeed cosmopolitan with the potential for long-distance dispersal, but others with restricted geographic distributions. Keywords: Biogeography, Cosmopolitism, Dormancy, Meiofauna, Nematoda, Phylogeography, Rotifera, Tardigrada Introduction marine species [8], for which it is known as the meiofauna Microscopic animals are generally assumed to be ex- paradox: microscopic benthic organisms with little mobility tremely widespread, up to the level of not showing any seem to be cosmopolitan, contrary to their lack of dispersal biogeographical pattern: the first European expeditions ability and their lack of planktonic larval stages [9]. to remote areas brought back home surprising new The inclusion of microscopic animals in the discussion groups of plants and large animals, whereas all the on the ubiquity hypothesis makes comparisons with lar- microscopic organisms collected during the same expe- ger organisms more obvious: microscopic and macro- ditions resembled the species that were already known scopic animals have common physiology, similar in Europe [1]. Such empirical scenario of widespread ecology, and shared evolutionary trajectories [10]. Yet, distribution was found across different taxa and at differ- biogeographical patterns seem to be different between ent spatial scales. Among the different rationales that microscopic and large animals, because of the differ- tried to explain the pattern of cosmopolitism in micro- ences in size and the ecological consequences of being scopic animals the most known remains nowadays the microscopic [1, 6]. ‘everything is everywhere’ ortheubiquityhypothesis[2–5]. Three assumptions should be met in order to allow Thediscussiononthelackofbiogeography for microscopic long-distance dispersal in microscopic aquatic animals: organisms focused originally on prokaryotes and uni- dormancy capability, long-term resistance of dormant cellular eukaryotes, to then extend also to all micro- stages, and ability to colonise and reproduce quickly. scopic organisms below one or two millimetres in Here I review these assumptions and the direct and in- body length, including microscopic multicellular ani- direct evidence we have for long-distance dispersal. The mals [1, 6]. The ubiquity hypothesis for microscopic review is not meant to be exhaustive on each of the aquaticanimalsholdstrueforcontinental[7]aswellasfor topics, but is designed to introduce the subject and its relevance for our general understanding of movement Correspondence: [email protected] National Research Council of Italy, Water Research Institute, Largo Tonolli 50, 28922 Verbania Pallanza, Italy © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Fontaneto Movement Ecology (2019) 7:10 Page 2 of 10 ecology and biogeography of microscopic aquatic ani- Dormancy mals, focusing on nematodes, rotifers, and tardigrades, Nematodes, rotifers, and tardigrades independently the most notorious microscopic animals with high po- evolved adaptations to survive adverse periods without tentials for long-distance dispersal. water [16–19]: as soon as conditions are not favourable with liquid water becoming unavailable because of Review evaporation or of freezing, some animals are able to pro- Microscopic aquatic animals, smaller than one or two duce dormant stages to allow the following generation millimetres [5], are small by definition: they cannot be to recover a viable population when liquid water be- easily seen with a naked eye and they are considered comes available again [16]. Such dormant stages are known ecologically different from the large, macroscopic or- asrestingeggsinrotifersandintardigrades[20, 21], and ganisms that we see around us [1, 9]. One of the main eggs in nematodes [22]. They are dormant embryos and consequences of being microscopic for aquatic animals not actual eggs [23], and they are produced both by par- is that the ratio between volume and surface of the or- thenogenesis and by sexual reproduction. There is an ample ganism is so small that when the animal is taken out of literature on the triggers that drive the production of rest- water it may be unable to retain its internal liquids, ing stages, and also on the mechanisms that are put in which would evaporate very quickly unless some sort of place to maximise the efficacy of such stages to maintain protection is present [11]. The volume to surface ratio viable populations through bet-hedging strategies, especially may not usually be a problem for an unprotected for microscopic zooplankton animals [24]. The production microscopic animal that lives in osmotically and of dormant stages that accumulate at the bottom of chemically stable, permanently hydrated habitats, such an ephemeral water body is also considered the main as large lakes and open oceans. Such animal will have mechanism that structures community and population very small or almost no probability of encountering dynamics for microscopic animals with high genetic desiccation problems. Moreover, some animals, espe- differentiation at the local and landscape level [25], in cially arthropods, have protective integuments to con- what was named monopolisation hypothesis [26]. trast such rapid desiccation. Yet, several microscopic These communities, structured by the interplay be- animals with no thick protective integuments live in tween the buffering effect of dormant stages acting temporary water bodies that desiccate frequently, for against new colonisers and the dispersal of dormant example shallow ponds, bogs, small puddles, intermit- propagules from other populations [27, 28], are one tent rivers, cryoconites, rock pools, salt marshes, etc. of the most studied examples within the metacommu- Some microscopic aquatic animals even adapted to live in nity framework [29, 30]. The research output of com- the thin and ephemeral water layers surrounding mosses, munity ecology connected to dispersal in microscopic lichens, and soils, in what is called a limno-terrestrial habi- aquatic animals is highly productive, but will be only tat: an aquatic microscopic environment (the ‘limno’ part) marginally considered in this review, given that it in- in an otherwise terrestrial ecosystem. The most common volves local or landscape-level settings, and not and abundant animals living in these habitats, especially in proper long-distance dispersal across continents. continental freshwater settings, are nematodes, rotifers, Microscopic animals can withstand lack of liquid water and tardigrades, a community of microscopic animals col- through other mechanisms, not only through the pro- lectively known as meiofauna [8, 9]. Other microscopic duction of dormant embryos: bdelloid rotifers and tardi- aquatic animals exist and are part of the meiofauna, e.g. grades can simply contract into a ‘tun’ shape and gastrotrichs, loriciferans, kinorhynchs, etc., but they do nematodes can coil, losing most if not all of their in- not have the dormancy capabilities of nematodes, rotifers, ternal water, halting any metabolic activity, and and tardigrades that make them suitable candidates for remaining in this dormant condition until water be- long-distance transportation, dispersal and cosmopolitan comes available again [31, 32]. The physiological mecha- distribution [12]. nisms allowing these animals to remain viable while The three animal groups included in this review be- desiccated during dormancy are still under study, and long to different evolutionary lineages in the meta- are thought to involve protecting molecules such as zoan tree of life [10], but they all share small body sugars, late embryogenesis abundant proteins, antioxi- size, usually much less than 1 mm, together with the abil- dants, etc. [33–35], in addition to the ability to recover ity to survive lack of water through dormancy [13, 14]and their broken DNA when rehydrated [36]. Two main
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