Will shrinking body size and increasing species diversity of crustaceans follow the warming of the Arctic littoral?

Abstract Over thirty species of littoral marine Gammaridea occur along the coasts of the North Atlantic. From one to several species can coexist in a single region. There is an evident, inverse relationship between egg incubation time and temperature (from 14 to >120 days) and consequent trends in the size of the animals on reaching maturity (from 5 mm in warmer waters to 30 mm in the coldest ones) and in lifespan (from <6 months to >5 years). Littoral gammarids are a good example of the shrinking size effect of increasing temperatures and size‐related species diversity. In large species, the annual cohorts of the population (3–5 annual size groups) functionally replace the adults of smaller species. The ongoing warming of the European Arctic seas may extend the distribution limits of boreal species so that more Gammarus species may appear on northern coasts hitherto occupied by just one or at most two species.

In the pelagic realm, the warming results in less diversified size structure of plankton (northern species mature at smaller size and small southern species arrive north). However, in the three dimensional pelagial, the competition for space or microhabitat is not crucial. In contrary, the coastal gamarids compete for the limited space on the seabed and here the size comes as an important factor.

| MATERIAL AND ME THODS
The Formalin-preserved specimens were wet-weighed after having been blotted on filter paper. The temperatures for the different localities were obtained from the cited references or meteorological data currently available on the Internet. Some of the materials collected by the first author were presented in the form of an unpublished manuscript-an MSc thesis at the University of Gdańsk (Wolska, 1983 unpublished).
Summer minimal temperature for the geographic region was taken as a critical value for marine poikilotherms (Golikov, Dolgolenko, Maximovich, & Scarlato, 1990). The occurrence of the sympatric species was assessed for the region from the literature cited, and species names were checked after Bellan-Santini and Costello (2001).

| RE SULTS AND D ISCUSS I ON
At least thirty sibling species from Gammarus and other species from closely related genera (Marinogammarus, Pontogammarus, Dikerogammarus etc.) occur in the intertidal of both the eastern and western North Atlantic (Table 1). Their size at maturity ranges from 4 to 52 mm and is related to lifespan and ambient temperature ( Figure 1, Table 1). Number of sibling gammarid species in given temperature/region corresponds inversely with the size of specimens. In low temperature, where the large species occurs, number of sympatric similar species is low, and in warmer temperatures, high number of small species coexist (Figure 2). Length frequencies in the summer samples of the Arctic population of two sympatric sibling Gammarus species indicate that there are three annual cohorts, or fourteen size groups (2 mm intervals) (Figure 3). Compared to the Arctic, the temperate water population (Baltic) of the same species in summer (after the death of the winter cohort and juvenile release in spring) has a cohort of one age (length 6-15 mm) that corresponds to five size groups (2 mm intervals). The summer length frequency of the large (40 mm) species in the Arctic spans up to twenty such size groups (G. setosus or G. wilkitzkii).

The growth in two very different populations of Gammarus oceanicus from the Baltic and Arctic (summer temperatures plus 20°C
and 4°C, respectively) is similar, although the cold-water population lives longer and grows to greater lengths ( Figure 4). A cold-water individual may not reach maturity in the first year of its life, but will grow continuously for the next one or two years, ultimately attaining a large size.
If the life cycle is to be completed within a year or less, the critical phenomenon is the egg incubation time ( in less than 20 days (Jażdżewski, 1970a). The ability to shorten the egg incubation period is probably governed by temperature only (as observed in Calanus copepods- Irigoien et al., 2000or pelagic hyperids-Koszteyn, Timofeev, Węsławski, & Malinga, 1995. Other factors controlling the size of these invertebrates are the availability and quality of food and oxygen saturation (Chapelle & Peck, 1999).
Adults of Gammarus species are omnivores (Tzvetkova, 1975), and food availability is not a limiting factor in the littoral (plant detritus, meiofauna, and microorganisms are plentiful; Węsławski, Wiktor, Zajączkowski, & Swerpel, 1993). The oxygen concentration in coastal waters is always high, or even supersaturated, as there the water dynamics are the highest. Gammarus species have adequate food resources, a high level of oxygen and an appropriate range of salinity.
The only limiting factor is suitable microhabitat, that is, stones or crevices under which they can hide from predators. Gammarids are a preferred dietary constituent of coastal fish in the Baltic (MacNeil, Dick, & Elwood, 1999), and of fish, seabirds, and seals on Svalbard (Lydersen, Gjertz, & Weslawski, 1989;Węsławski & Kuliński, 1989).
The interstices among loose stones, providing adequate shelter, are quickly filled when some hundreds of animals are trying to hide beneath one of them (Węsławski, 1994). It is the occupation of this microhabitat by large, local species that is the likely factor preventing boreal, eurytopic species from successfully colonizing the North. Ca 300 large specimens (mean length 20 mm) or 2,000 small ones (mean length 5 mm) can conceal themselves under a stone 400 cm 2 in area; this corresponds with the average densities reported for Arctic localities (300-500/m 2 ) (Węsławski, 1994) and for temperate sites, where the number of small gammarid species can exceed 10,000/ m 2 (Tzvetkova, 1975).
Niche selection and competition was described as a critical factor for the new species colonization in littoral amphipods (Kotta et al., 2013;Piscart, Maazouzi, & Marmonier, 2008).
The majority of marine littoral gammarids display a very wide tolerance to salinity and temperature (Tzvetkova, 1975 Figure 1).
In the Arctic, where the two large, cold-water species (G. wilkitzkii and G. setosus) co-occur, there is almost no sympatric occurrence, as G. wilkitzkii is an ice-associated species and G. setosus is a littoral species. However, when the ice melts in coastal waters, G. wilkitzkii seeks the same shelter as its littoral congener (Poltermann, 1997(Poltermann, , 1998Węsławski, 1994 Newfoundland, the coasts of which have an extensive tidal range from three to twelve meters, G. setosus was recorded higher up on the shore and G. oceanicus lower down (Steele & Steele, 1974). On Spitsbergen, the two species coexist recently, as the G. oceanicus is colonizing the area after the glacial retreat (Grabowski et al., 2019).
In the littoral, when a species is large, there are many size groups that act as separate ecological units: Size variations in gammarids lead to differences in mobility, food, and behavior (see Węsławski et al., 2010). All the available space is occupied, and the number of true species is limited-to two, according to published observations. In areas where species are small, there are fewer size groups and more species can coexist (up to fourteen in a region like the Mediterranean Sea, Table 1).
The sympatric occurrence discussed here is considering the regional scale (gamma diversity). The co-occurrence on a small scale of one sample, alpha diversity, is difficult to assess, as there are very few data. In the Baltic, where 9 local plus four alien (man introduced) species occur, the actual occurrence of three to five species in one spot was confirmed (Jażdżewski, 1970a, own observations).
As the size of gammarids is so closely related to ambient temperature, we may speculate that with increasing coastal temperatures in the Arctic, littoral gammarids will complete their life cycle at a smaller size, which will create opportunities for the area's colonization by southern species. This will be a direct effect not of temperature (those eurytopic species are already capable of living there) but of the favorable size structure of competitors.
In summary, two phenomena are well documented in littoral Gammarus species. One is the direct relationship of temperature to lifespan and the size of an adult animal: At warmer temperatures, all known species grow faster and reach maturity at a smaller size.
The other is the low number of sympatric species in areas where large species occur, and the high number of such species where the animals are small. From these two observations, we can infer that climate change may shift the boreal species northwards, where competition from large species will be reduced as the temperature rises and the cold-water species will loose the competitive advantage of their large size.  Mechanism (Contract No Pol-Nor/201992/93/2014, project DWARF).

CO N FLI C T O F I NTE R E S T
None declared.

DATA AVA I L A B I L I T Y S TAT E M E N T
All data presented in this paper are available through the project web page ACCES https://www.iopan.pl/proje cts/Acces/ (operational since June 2020) or direct email to the first author <wesla w@ iopan.gda.pl>.