Competitive interaction in headwaters: slow upstream migration leads to trophic competition between native and non-native amphipods

The spread of non-native species is one of the outcomes of global change, threatening many native communities through predation and competition. Freshwater ecosystems are particularly affected by species turnover with non-native species. One species that has been established in Central Europe for many decades – or even a few centuries – is the amphipod crustacean Gammarus roeselii. Although G. roeselii is nowadays widespread in major river systems, there have been recent reports of its spread into smaller streams that are typically inhabited by the native species Gammarus fossarum. Due to their leaf shredding ability, G. fossarum takes up a key position in headwater streams. This raises the important question, to what extent G. roeselii can equivalently take over this function. To answer this question, we collected both species from nine different sites in a mid-mountain river system (Kinzig catchment, Hesse, Germany) and investigated their functional similarity using a combination of stable isotope analysis, gut content and functional morphology. The species hardly differed in morphological characteristics, only females showed differences in some traits. Gut content analysis indicated a broad dietary overlap, while stable isotopes showed a higher trophic position of G. roeselii. The observed functional overlap could intensify interspecific competition and allow the larger and more predaceous G. roeselii to replace G. fossarum in the future as a headwater keystone species. However, the differentiation in the stable isotopes also shows that co-existence can occur by occupying different trophic niches. Moreover, the wide range of inhabited sites and exploited resources demonstrate the omnivorous lifestyle of G. roeselii, which is likely to help the species succeed in rapidly changing environments.

[1]  J. Oehlmann,et al.  Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipods. , 2023, Environment international.

[2]  S. Cunze,et al.  Uncovering the Grinnellian niche space of the cryptic species complex Gammarus roeselii , 2023, PeerJ.

[3]  F. Altermatt,et al.  Context‐dependent evolution of high trophic position drives functional disparity in subterranean crustaceans , 2023, Functional Ecology.

[4]  J. Oehlmann,et al.  Pesticide dynamics in three small agricultural creeks in Hesse, Germany , 2023, PeerJ.

[5]  J. Oehlmann,et al.  Flushing away the future: The effects of wastewater treatment plants on aquatic invertebrates. , 2023, Water research.

[6]  J. Oehlmann,et al.  Infection with acanthocephalans increases tolerance of Gammarus roeselii (Crustacea: Amphipoda) to pyrethroid insecticide deltamethrin , 2023, Environmental Science and Pollution Research.

[7]  A. Weigand,et al.  Small-scale population structuring results in differential susceptibility to pesticide exposure , 2022, Environmental Sciences Europe.

[8]  D. Copilaș‐Ciocianu,et al.  Morphology mirrors trophic niche in a freshwater amphipod community , 2021, Freshwater Biology.

[9]  Laurent Simon,et al.  Cave amphipods reveal co‐variation between morphology and trophic niche in a low‐productivity environment , 2021, Freshwater Biology.

[10]  T. Rewicz,et al.  Successful post-glacial colonization of Europe by single lineage of freshwater amphipod from its Pannonian Plio-Pleistocene diversification hotspot , 2020, Scientific Reports.

[11]  M. Zhai,et al.  Does predation by the omnivorous Gammarus fossarum affect small-scale distribution of macroinvertebrates? A case study from a calcareous spring fen , 2020 .

[12]  A. Weigand,et al.  Substantial differences in genetic diversity and spatial structuring among (cryptic) amphipod species in a mountainous river basin , 2020, Freshwater Biology.

[13]  D. Copilaș‐Ciocianu,et al.  Extensive variation in the morphological anti-predator defense mechanism of Gammarus roeselii Gervais, 1835 (Crustacea:Amphipoda) , 2020, Freshwater Science.

[14]  M. Zhai,et al.  Native Gammarus fossarum affects species composition of macroinvertebrate communities: evidence from laboratory, field enclosures, and natural habitat , 2020, Aquatic Ecology.

[15]  A. Weigand,et al.  Small-scale phenotypic differentiation along complex stream gradients in a non-native amphipod , 2019, Frontiers in Zoology.

[16]  Per B. Brockhoff,et al.  lmerTest Package: Tests in Linear Mixed Effects Models , 2017 .

[17]  F. Guérold,et al.  Minor food sources can play a major role in secondary production in detritus‐based ecosystems , 2017 .

[18]  C. Amsler,et al.  Gut content, fatty acid, and stable isotope analyses reveal dietary sources of macroalgal-associated amphipods along the western Antarctic Peninsula , 2017, Polar Biology.

[19]  R. Herczeg,et al.  Effects of meso‐ and microhabitat characteristics on the coexistence of two native gammarid species (Crustacea, Gammaridae) , 2017 .

[20]  Natasha P. Mothapo,et al.  Patterns of floral resource use by two dominant ant species in a biodiversity hotspot , 2017, Biological Invasions.

[21]  T. Rewicz,et al.  Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod , 2017, PeerJ.

[22]  W. Thuiller,et al.  Major drivers of invasion risks throughout the world , 2016 .

[23]  M. Oetken,et al.  Pronounced species turnover, but no functional equivalence in leaf consumption of invasive amphipods in the river Rhine , 2016, Biological Invasions.

[24]  M. Vilà,et al.  Global ecological impacts of invasive species in aquatic ecosystems , 2016, Global change biology.

[25]  F. Altermatt,et al.  Morphologically Cryptic Amphipod Species Are “Ecological Clones” at Regional but Not at Local Scale: A Case Study of Four Niphargus Species , 2015, PloS one.

[26]  S. Vizzini,et al.  Assessing anthropogenic pressures on coastal marine ecosystems using stable CNS isotopes: State of the art, knowledge gaps, and community-scale perspectives , 2015 .

[27]  B. Schwartz,et al.  Morphological and trophic specialization in a subterranean amphipod assemblage , 2014 .

[28]  K. Rothhaupt,et al.  Niche differentiation between sympatric alien aquatic crustaceans: An isotopic evidence , 2014 .

[29]  D. Richardson,et al.  Defining the Impact of Non-Native Species , 2014, Conservation biology : the journal of the Society for Conservation Biology.

[30]  R. Relyea,et al.  Phenotypically similar but ecologically distinct: differences in competitive ability and predation risk among amphipods , 2013 .

[31]  G. Velde,et al.  There is more than one ‘killer shrimp’: trophic positions and predatory abilities of invasive amphipods of Ponto-Caspian origin , 2013 .

[32]  M. Jackson,et al.  ‘Leaves and Eats Shoots’: Direct Terrestrial Feeding Can Supplement Invasive Red Swamp Crayfish in Times of Need , 2012, PloS one.

[33]  W. Walkusz,et al.  When season does not matter: summer and winter trophic ecology of Arctic amphipods , 2012, Hydrobiologia.

[34]  R. Leuven,et al.  Assessment of predatory ability of native and non-native freshwater gammaridean species: A rapid test with water fleas as prey , 2011 .

[35]  Márcio S Araújo,et al.  The ecological causes of individual specialisation. , 2011, Ecology letters.

[36]  Andrew L Jackson,et al.  Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. , 2011, The Journal of animal ecology.

[37]  C. Piscart,et al.  Effects of coexistence on habitat use and trophic ecology of interacting native and invasive amphipods. , 2011 .

[38]  P. Hendrix,et al.  Dietary flexibility aids Asian earthworm invasion in North American forests. , 2010, Ecology.

[39]  John L. Orrock,et al.  Predator-prey naïveté, antipredator behavior, and the ecology of predator invasions , 2010 .

[40]  C. Piscart,et al.  Are amphipod invaders a threat to regional biodiversity? , 2010, Biological Invasions.

[41]  Rob S. E. W. Leuven,et al.  The river Rhine: a global highway for dispersal of aquatic invasive species , 2009, Biological Invasions.

[42]  M. Huijbregts,et al.  Environmental and morphological factors influencing predatory behaviour by invasive non-indigenous gammaridean species , 2009, Biological Invasions.

[43]  A. Suarez,et al.  Trophic ecology of invasive Argentine ants in their native and introduced ranges , 2007, Proceedings of the National Academy of Sciences.

[44]  E. Angulo,et al.  Dietary shift of an invasive predator: rats, seabirds and sea turtles , 2007, The Journal of applied ecology.

[45]  M. Grabowski,et al.  How to be an invasive gammarid (Amphipoda: Gammaroidea)–comparison of life history traits , 2007, Hydrobiologia.

[46]  B. Knols,et al.  Stable isotope methods in biological and ecological studies of arthropods , 2007 .

[47]  D. Post,et al.  Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses , 2007, Oecologia.

[48]  M. Pace,et al.  Understanding the long-term effects of species invasions. , 2006, Trends in ecology & evolution.

[49]  L. Bollache,et al.  Spines and behaviour as defences against fish predators in an invasive freshwater amphipod , 2006, Animal Behaviour.

[50]  G. Velde,et al.  Trophic Relationships in the Rhine Food Web during Invasion and after Establishment of the Ponto-Caspian Invader Dikerogammarus villosus , 2006, Hydrobiologia.

[51]  J. Montoya,et al.  Flexible diet and trophic position of dreissenid mussels as inferred from stable isotopes of carbon and nitrogen , 2005 .

[52]  J. Finlay Patterns and controls of lotic algal stable carbon isotope ratios , 2004 .

[53]  C. Kendall,et al.  Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur , 2003 .

[54]  A. Dobson,et al.  Introduced species and their missing parasites , 2003, Nature.

[55]  J. Rosenfeld,et al.  Functional redundancy in ecology and conservation , 2002 .

[56]  G. van der Velde,et al.  Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe , 2002 .

[57]  J. Finlay,et al.  STABLE‐CARBON‐ISOTOPE RATIOS OF RIVER BIOTA:IMPLICATIONS FOR ENERGY FLOW IN LOTIC FOOD WEBS , 2001 .

[58]  P. Chesson Mechanisms of Maintenance of Species Diversity , 2000 .

[59]  M. Pace,et al.  Ecosystem size determines food-chain length in lakes , 2000, Nature.

[60]  J. Casselman,et al.  Stable isotope evidence for the food web consequences of species invasions in lakes , 1999, Nature.

[61]  M. Dobson,et al.  A perspective on leaf litter breakdown in streams , 1999 .

[62]  M. Delong,et al.  ONTOGENETIC AND TEMPORAL SHIFTS IN THE DIET OF THE AMPHIPOD GAMMARUS FASCIATUS, IN THE OHIO RIVER , 1997 .

[63]  J. Dick Post-invasion amphipod communities of Lough Neagh, Northern Ireland : influences of habitat selection and mutual predation , 1996 .

[64]  J. Dick,et al.  Intraguild predation and species exclusions in amphipods: the interaction of behaviour, physiology and environment. , 1996 .

[65]  J. Rasmussen,et al.  Comparison of aquatic food chains using nitrogen isotopes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Nelson G. Hairston,et al.  Cause-Effect Relationships in Energy Flow, Trophic Structure, and Interspecific Interactions , 1993, The American Naturalist.

[67]  M. Delong,et al.  Influence of Food Type on the Growth of a Riverine Amphipod, Gammarus fasciatus , 1993 .

[68]  M. Pöckl Reproductive potential and lifetime potential fecundity of the freshwater amphipods Gammarus fossarunt and G. roeseli in Austrian streams and rivers , 1993 .

[69]  M. Pöckl Effects of temperature, age and body size on moulting and growth in the freshwater amphipods Gammarus fossarum and G. roeseli , 1992 .

[70]  U. Humpesch,et al.  Intra‐ and inter‐specific variations in egg survival and brood development time for Austrian populations of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda) , 1990 .

[71]  P. Ward Sexual Selection, Natural Selection, and Body Size in Gammarus pulex (Amphipoda) , 1988, The American Naturalist.

[72]  R. Howarth,et al.  Sulfur and Carbon Isotopes as Tracers of Salt‐Marsh Organic Matter Flow , 1986 .

[73]  M. Winterbourn,et al.  Stable Carbon Isotopes and Carbon Flow in EcosystemsMeasuring 13C to 12C ratios can help trace carbon pathways , 1986 .

[74]  M. Minagawa,et al.  Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age , 1984 .

[75]  K. Cummins,et al.  Influences of Diet on the Life Histories of Aquatic Insects , 1979 .

[76]  M. J. Deniro,et al.  Influence of Diet On the Distribtion of Nitrogen Isotopes in Animals , 1978 .

[77]  Thomas W. Schoener,et al.  Resource Partitioning in Ecological Communities , 1974, Science.

[78]  W. Bock,et al.  ADAPTATION AND THE FORM–FUNCTION COMPLEX , 1965 .

[79]  D. Richardson,et al.  Ecological Impacts of Alien Species: Quantification, Scope, Caveats, and Recommendations , 2015 .

[80]  J. Guerra-García,et al.  Dietary analysis of the marine Amphipoda (Crustacea: Peracarida) from the Iberian Peninsula , 2014 .

[81]  A. Ortmann-Ajkai,et al.  Niche segregation between two closely similar gammarids (Peracarida, Amphipoda) — native vs. naturalized non-native species , 2014 .

[82]  Marc Kenis,et al.  Ecological effects of invasive alien insects , 2008, Biological Invasions.

[83]  K. Young ASYMMETRIC COMPETITION, HABITAT SELECTION, AND NICHE OVERLAP IN JUVENILE SALMONIDS , 2004 .

[84]  D. Sutcliffe,et al.  Life history and reproductive capacity of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda) under naturally fluctuating water temperatures: a simulation study , 2003 .

[85]  O Hammer-Muntz,et al.  PAST: paleontological statistics software package for education and data analysis version 2.09 , 2001 .

[86]  J. Dick,et al.  Replacement of the indigenous amphipod Gammarus duebeni celticus by the introduced G. pulex: differential cannibalism and mutual predation. , 1993 .

[87]  B. Peterson,et al.  STABLE ISOTOPES IN ECOSYSTEM STUDIES , 1987 .

[88]  G. Minshall,et al.  The River Continuum Concept , 1980 .

[89]  M. Klug,et al.  Feeding Ecology of Stream Invertebrates , 1979 .

[90]  R. Meldola Sexual Selection , 1871, Nature.