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All issues No 417 (2016) Knowl. Manag. Aquat. Ecosyst., 417 (2016) 7 Full HTML
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Knowl. Manag. Aquat. Ecosyst.
Number 417, 2016
Topical Issue on Fish Ecology
Article Number 7
Number of page(s) 7
DOI https://doi.org/10.1051/kmae/2015040
Published online 18 January 2016

© L. Traversetti et al., published by EDP Sciences, 2016

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

Although scientists are aware that every singular species is the result of biological interactions with other taxa within an ecological network (e.g. Allesina and Pascual, 2009), conservation efforts still persevere in focusing on a single or a modest number of species displaying relevant roles within an ecosystem (Okey, 2004; Jordán et al., 2009). This is due to the prevailing opinion that only particular groups are expected to play an important role but ecological network interactions among the single species and the community dynamics have largely been ignored (Stouffer et al., 2012). Nowadays the current challenge is to quantify the relative importance of a single species in an ecosystem, assuming that the well-linked species are important for the whole community (Jordán, 2009). Though it is not always simple to define the sense of “important” from an ecological point of view, Kearns et al. (1998) defined important those species having the major number of links with other taxa. Theoretically this means that functionally important species could be those occupying central positions in the ecological network (Allesina and Bodini, 2004). For this reason, one approach in describing the importance of keystone species in the whole food web (Jordán et al., 2008) is to characterize the trophic aggregation of ecological groups in order to describe the interactors having a greater role within the community (Estrada, 2007; Jordán et al., 2007).

Table 1

Fish check-list of the Lake Bracciano (Gibertini et al., 2004). The years of investigation are indicated for each studied species in the last column.

Based on these premises, the main purpose of this study is to highlight the importance of the freshwater grass shrimp Palaemonetes antennarius (Milne Edwards, 1837) in the diet of fish species inhabiting the volcanic Lake Bracciano (Central Italy). This grass shrimp, recently proposed as junior synonyms of Palaemon Weber, 1795 (De Grave and Ashelby, 2013), is a caridoid body shaped southern Europe decapod belonging to the family Palaemonidae Gottstein Matoèec and Kerovec (2002) proposed it as a very rare and endangered shrimp, although the species is listed as Least Concern by the International Union for Conservation of Nature (http://www.iucnredlist.org). Although investigations on behavior (Ugolini et al., 1988, 1989; Ungherese et al., 2008) and ecology of P. antennarius are performed at local level (Dalla Via, 1983; Gottstein Matoèec et al., 2006) some ecological aspects, such as interspecific relationships with predators or other taxa of the food web remain still unclear.

To reach our goal we analysed 6120 individuals of 10 different fish species (Table 1) caught every January, April, July, and October of 1992, 1994, 1999, 2003, and 2008, for histological investigations concerning reproductive aspects (both gonado- and gametogenesis). Fish sampling was supported by professional fishermen which collocated 6 dragnets having a 2 cm mesh-size, in 6 different sites in the south-eastern lake area covering nearby 4 km2 of the 57.2 km2 water surface. Nets were fixed during sunset and drawn in the morning after. The catch per unit effort was the same in each season for the 5 years, with the exception of 2003 and 2008 when dragnets were landed using a motor-driven winch. In every sampling session, 10–15 specimens per species were selected and measured on their right body side from the mouth tip to the caudal peduncle (standard length, SL, in cm) Stomachs were collected, preserved in 85° alcohol, and sorted in laboratory. All intact or remnants of P. antennarius were divided per sampling season and year, species, and fish body size (using 5 cm SL range). We firstly calculated the grass shrimp occurrence frequency as O = (Ji/N), and the prey-specific abundance as A = (ΣSi/ΣSti), where: Ji was the stomach number containing shrimps; N the number of stomachs containing preys; Si indicated the number of shrimps in the stomachs; Sti the total preys in the stomachs containing shrimps. To assess how P. antennarius influences the fish diet strategy, both O and A (for species and year) were plotted in a series of diagrams (Amundsen et al., 1996). The analysis is based on a graphical exploration of the ingested food in relation to the predator feeding strategy, as well as the intra- and inter-individual shifts in the niche use. Specifically, in this graph data plotting follows three main directions (Supplementary Material 1): the first diagonal represents the prey abundance within the predator diet spectrum; the second, parallel to the y-axis, provides information on the predator specialization for the specific prey; the third diagonal refers to the individual resource use. The latter changing from ‘high between individuals’ (HBI, that means how many specimens of a specific predator consume shrimps, but the latter is no very abundant within each stomach) to ‘high within individuals’ (HWI, that means not many specimens of a specific predator feed on shrimps, but the latter is abundant within the stomach).

Table 2

Shrimp occurrence within full stomachs, divided per sampling season and year, and standard length range (SL, cm) of the 10 investigated species (au = autumn; wi = winter; sp = spring; su = summer).

Additionally we evaluated the shrimp body size by extrapolating it from the regression functions calculated for 200 specimens collected from Lake Bracciano. We performed the same measurements as Anastasiadou et al. (2009) using a digital caliper (± 0.01 mm), and considered the cephalothorax length (CTL) as the reference size. Although authors are aware that P. antennarius shows a morphometric sexual dimorphism pattern (see Anastasiadou et al., 2009), we chose to perform a series of regression for the entire sample since we were not able to sex all grass shrimp remnants within stomachs. Then we regressed shrimp size vs. fish size in order to observe eventual preferences in the choice of prey size.

thumbnail Fig. 1

Alimentary diagrams obtained plotting both freshwater shrimp abundance and occurrence for 5 selected species divided per sampling season (au = autumn; wi = winter; sp = spring; su = summer) and year, and standard length range in cm. The remaining fish species showing few data or an occasional occurrence of P. antennarius were excluded in this analysis. Since we would not evaluate fish species diet overlap, only the shrimp components found inside the stomachs were shown in the Amundsen et al. (1996) graphic outputs.

Our outputs support the hypothesis that the freshwater grass shrimp plays a relevant role in fish diet. In fact, P. antennarius occurred inside stomachs of all investigated fish species, although in different frequencies and life stages (larval, sub-adult, and adult, the latter being the most exploited by fish). Moreover, its occurrence depended on fish size and seasons as well. On the whole 4295 stomachs (70.18%) showed animal contents and 635 (15.8%) contained entire grass shrimp bodies or remnants. Shrimps occurred only as larval form in planktonfagous species such as Coregonus lavaretus (Linnaeus, 1758) and Atherina boyeri (Risso, 1810) in summer and autumn, when juvenile individuals of both fish species reside near the riparian shore of the lake (Avetrani et al., 2006). In the remaining 8 fish species, sub-adult and/or adult of shrimps were the most preyed life stage and occurred in stomachs of all size classes with the only exception of the Esox lucius 40–45 cm class . Additionally P. antennarius was easily recorded in predators (mainly in small sized specimens) such as E. lucius Linnaeus, 1758, Micropterus salmoides (Lacépède, 1802), and Perca fluviatilis Linnaeus, 1758 (see also Marinelli et al., 2007; Scalici et al., 2009a; Godinho and Ferreira, 2014). Generally, the occurrence frequency (Table 2) showed a wide value range for the entire sample having a minimum of 0.08 for the diverse species and a maximum of 0.67 for A. boyeri and M. salmoides. The Amundsen et al. (1996) method was applied only to 5 selected species (Figure 1). In several diagrams P. antennarius is under the O value of 0.5, with the exception of M. salmoides, indicating that the crustacean is preyed mostly by fish displaying a generalized feeding strategy. All fish species mainly fed on adult shrimp (Figure 2), referring to near CTL = 12 mm as size at maturity according to Gottstein Matoèec et al. (2006). Although in regressing shrimp size vs. fish size some significant outcomes emerged, overall for P. fluviatilis and M. salmoides, which always showed significant regressions (Table 3). Some regressions seemed to be casual for certain species. For example, the analysis provided significant outcomes for pike during the first sampling year, but not for the following ones. On the other hand, when the standard length of both P. fluviatilis and M. salmoides increased also the size of ingested shrimps increased.

thumbnail Fig. 2

P. antennarius cephalothorax mean length (CTL, ± standard deviation) for the 8 selected and investigated species divided per sampling year.

Table 3

Correlations between P. antennarius cephalothorax length (CTL) and fish standard length of the 8 selected species divided per sampling year (significant values are in bold; ns = not significant). The two planktofagous species C. lavaretus and A. boyeri were omitted from the analysis, since no data on shrimp larval size and growth were available.

Taking the double role of prey for fish and possible predator of benthic invertebrates into account (Cibinetto et al., 2005), the freshwater grass shrimp position in the food web brought to mind that it is of crucial importance as intermediate trophic species in ‘wasp-waist’ ecosystems The latter are typical for pelagic upwelling areas (Cury et al., 2000) where a large number of taxa are linked by a single or only very few species collocated in the middle of the trophic levels (Smith Jr et al., 2007). This ‘centrality’ makes P. antennarius a more imperiled taxon if we also consider the introduction and spreading of both alien invertebrates and fish species as potential competitors and/or predators This may be the case for very stressed areas such as in central Italy where diverse invasive crayfish (Chiesa et al., 2006; Nonnis et al., 2009; Scalici et al., 2010, 2009b, 2009c; Dörr and Scalici, 2013; Bissattini et al., accepted) and their unsafe parasites (Dörr et al., 2011, 2012a, 2012b; Chiesa et al., 2015) were recorded and described. Scientists are often expected to indicate the most important species which disturbance may originate the main detrimental effect on both occurrence and abundance of other taxa in a community (Jones et al., 1994). From this viewpoint, P. antennarius ought to receive the same attention recommended for other freshwater decapods (see Brusconi et al., 2008) as proposed for Austropotamobius pallipes species complex sensu Chiesa et al. (2011) and Scalici and Bravi (2012) (see http://www.iucnredlist.org) or suggested for Potamon fluviatile (Herbst, 1785) (see Jesse et al., 2009). Nevertheless, the significant role of the freshwater grass shrimp and the dynamic consequences due to its presence need to be confirmed, since understanding the dynamic implications of a species role in the food web may provide useful information when scientists have to dialogue with institutions for deciding which taxa is of main concern in conservation and managing efforts, and to focalize on those with the strongest involvement in community persistence.

thumbnail Supplementary Material 1.

Graphic representation for the interpretation of feeding strategy, niche width contribution, and prey importance, as proposed by Amundsen et al. (1996) (figure modified). HBI = high between individuals; HWI = high within individuals.

References

  • Allesina S. and Bodini A., 2004. Who dominates whom in the ecosystem? Energy flow bottlenecks and cascading extinctions. J. Theor. Biol., 230, 351–358. [CrossRef] [PubMed] [Google Scholar]
  • Allesina S. and Pascual M., 2009. Food web models: a plea for groups. Ecol. Lett., 12, 652–662. [CrossRef] [PubMed] [Google Scholar]
  • Amundsen P.A., Gabler H.M. and Staldvik F.J., 1996. A new approach to graphical analysis of feeding strategy from stomach contents data – modification of the Costello method. J. Fish Biol., 48, 607–614. [Google Scholar]
  • Anastasiadou C., Liasko R. and Leonardos I.D., 2009. Biometric analysis of lacustrine and riverine populations of Palemonetes antennarius (H. Milne-Edwards, 1837) (Crustacea, Decapoda, Palaemonidae) from north-western Greece. Limnologica, 39, 244–254. [CrossRef] [Google Scholar]
  • Avetrani P., Gibertini G., Scalici M. and Moccia G., 2006. Studio della popolazione di Coregonus lavaretus (L., 1758) nel Lago di Bracciano (Lazio). Biol. Ambientale, 20, 231–235. [Google Scholar]
  • Bissattini A.M., Traversetti L., Bellavia G. and Scalici M., 2015. Tolerance of increasing water salinity in the red swamp crayfish Procambarus clarkii (Girard, 1852). J. Crustacean Biol., 35, 682–685. [Google Scholar]
  • Brusconi S., Bertocchi S., Renai B., Scalici M., Souty-Grosset C. and Gherardi F., 2008. Conserving indigenous crayfish: stock assessment and habitat requirements in the threatened Austropotamobius italicus. Aquat. Conserv., 18, 1227–1239. [Google Scholar]
  • Chiesa S., Scalici M. and Gibertini G., 2006. Occurrence of allochthonous freshwater crayfishes in Latium (Central Italy). Knowl. Manag. Aquat. Ecosyst., 380-381, 883–902. [CrossRef] [EDP Sciences] [Google Scholar]
  • Chiesa S., Scalici M., Negrini R., Gibertini G. and Nonnis Marzano F. 2011. Fine-scale genetic structure, phylogeny and systematics of threatened crayfish species complex. Mol. Phylogenet. Evol., 61, 1–11. [Google Scholar]
  • Chiesa S., Scalici M., Lucentini L. and NonnisMarzano F., 2015. Molecular identification of an alien temnocephalan crayfish parasite in Italian freshwaters. Aquat. Inv., 10, 209–216. [Google Scholar]
  • Cibinetto T., Castaldelli G., Mantovani S. and Fano E.A., 2005. Valutazione della nicchia trofica potenziale di Palaemonetes antennarius (Crustacea: Palaemonidae) e di Diamysis mesohaobia (Crustacea: Mysidacea). 15° Meeting of the Italian Society of the Ecology, 6 p. [Google Scholar]
  • Cury P., Bakun A., Crawford R.J.M., Jarre A., Quiñones R.A., Shannon L.J. and Verheye H.M., 2000. Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. J. Mar. Sci., 57, 603–618. [Google Scholar]
  • Dalla Via J., 1983. Ecological-studies on the fresh-water shrimp Palaemonetes antennarius of Laguna di Lesina (Gargano, south Italy). Archiv Hydrobiol., 97, 227–239. [Google Scholar]
  • De Grave S. and Ashelby C.W., 2013. A re-appraisal of the systematic status of selected genera in Palaemoninae (Crustacea: Decapoda: Palaemonidae). Zootaxa, 3734, 331–344. [CrossRef] [PubMed] [Google Scholar]
  • Dörr A.J.M. and Scalici, M., 2013. Revisiting reproduction and population structure and dynamics of Procambarus clarkii eight years after its introduction into Lake Trasimeno (Central Italy). Knowl. Manag. Aquat. Ecosyst., 408, 10. [CrossRef] [EDP Sciences] [Google Scholar]
  • Dörr A.J.M., Rodolfi M., Scalici M., Elia A.C., Garzoli L. and Picco A.M., 2011. Phoma glomerata, a potential new threat to Italian inland waters. J. Nat. Conserv., 19, 370–373. [Google Scholar]
  • Dörr A.J.M., Rodolfi M., Elia A.C., Scalici M., Garzoli L. and Picco A.M., 2012a. Mycoflora on the cuticle of the invasive crayfish Procambarus clarkii. Fund. Appl. Limnol., 180, 77–84. [Google Scholar]
  • Dörr A.J.M., Elia A.C., Rodolfi M., Garzoli L., Picco A.M., D’Amen M. and Scalici M., 2012b. A model of co-occurrence: segregation and aggregation patterns in the mycoflora of the crayfish Procambarus clarkii in Lake Trasimeno (central Italy). J. Limnol., 71, 135–143. [Google Scholar]
  • Estrada E., 2007. Characterisation of topological keystone species: local, global and “meso-scale” centralities in food webs. Ecol. Complex., 4, 48–57. [CrossRef] [Google Scholar]
  • Gibertini G., Scalici M., Vignoli L., Moccia G. and Mattina F., 2004. I pesci del Lago di Bracciano. La comunità ittica, la pesca e il ripopolamento. Provincia di Roma. Assessorato alle Politiche dell’Agricoltura, Ambiente e Protezione Civile. [Google Scholar]
  • Godinho F.N. and Ferreira M.T., 2014. Feeding ecology of non-native centrarchids (Actinopterygii: Perciformes: Centrarchidae) in two Iberian reservoirs with contrasting food resources. Acta Ichthyologica et Piscatoria, 44, 23–35. [CrossRef] [Google Scholar]
  • Gottstein Matoèec S. and Kerovec M., 2002. Atyaephyra desmaresti and Palaemonetes antennarius (Crustacea: Decapoda, Caridea) in the delta of the Neretva River (Croatia). Biol. Bratislava, 57, 181–189. [Google Scholar]
  • Gottstein Matoèec S.G., Kuzman A. and Kerovec M., 2006. Life history traits of the grass shrimp Palaemonetes antennarius (Decapoda, Palaemonidae) in the delta of the Neretva River, Croatia. Limnologica, 36, 42–53. [CrossRef] [Google Scholar]
  • Jesse R., Pfenninger M., Fratini S., Scalici M., Streit B. and Schubart C.D., 2009. Disjunct distribution of the Mediterranean freshwater crab Potamon fluviatile – natural expansion or human introduction? Biol. Invasions, 11, 2209–2221. [CrossRef] [Google Scholar]
  • Jones C.G., Lawton J.H. and Shachak M., 1994. Organisms as ecosystem engineers. Oikos, 69, 373–386. [CrossRef] [Google Scholar]
  • Jordán F., 2009. Keystone species and food webs. Phil. Trans. R. Soc. B., 364, 1733–1741. [CrossRef] [Google Scholar]
  • Jordán F., Benedek Zs. and Podani J., 2007. Quantifying positional importance in food webs: a comparison of centrality indices. Ecol. Model., 205, 270–275. [CrossRef] [Google Scholar]
  • Jordán F., Okey T.A., Bauer B. and Libralato S., 2008. Identifying important species: Linking structure and function in ecological networks. Ecol. Model., 216, 75–80. [CrossRef] [Google Scholar]
  • Jordán F., Liud W.C. and Mike A., 2009. Trophic field overlap: A new approach to quantify keystone species. Ecol. Model., 220, 2899–2907. [CrossRef] [Google Scholar]
  • Kearns C.A., Inouye D.W. and Waser N.M., 1998. Endangered mutualisms: the conservation of plant pollinator interactions. Annu. Rev. Ecol. Syst., 29, 83–112. [CrossRef] [Google Scholar]
  • Marinelli A., Scalici M. and Gibertini G., 2007. Diet and reproduction of the largemouth bass in a recently introduced population, Lake Bracciano (central Italy). Knowl. Manag. Aquat. Ecosyst., 385, 53–68. [CrossRef] [EDP Sciences] [Google Scholar]
  • NonnisMarzano F., Scalici M., Chiesa S., Gherardi F. and Gibertini G., 2009. The first record of the marbled crayfish adds further threats to fresh water in Italy. Aquat. Invasions, 4, 401–404. [Google Scholar]
  • Okey T.A., 2004. Shifted community states in four marine ecosystems: some potential mechanisms. Ph.D. thesis, University of British Columbia, Vancouver. [Google Scholar]
  • Scalici M. and Bravi R., 2012. Solving alpha-diversity by morphological markers contributes to arranging the systematic status of a crayfish species complex (Crustacea, Decapoda). J. Zool. Syst. Evol. Res., 50, 89–98. [CrossRef] [Google Scholar]
  • Scalici M., Schiavone F., Marinelli A. and Gibertini G., 2009a. Growth, longevity, and mortality of the largemouth bass Micropterus salmoides (Lacépède, 1802) in a Mediterranean lake (Rome, Italy). Rev. Écol.-Terre Vie, 64, 51–60. [Google Scholar]
  • Scalici M., Chiesa S., Gherardi F., Gibertini G. and Nonnis Marzano F., 2009b. The new threat to Italian inland waters from the alien crayfish “gang”: the Australian Cherax destructor Clark, 1936. Hydrobiologia, 632, 341–345. [CrossRef] [Google Scholar]
  • Scalici M., Pitzalis M. and Gibertini G., 2009c. Crayfish distribution updating in central Italy. Knowl. Manag. Aquat. Ecosyst., 394-395, 1–8. [Google Scholar]
  • Scalici M., Chiesa S., Scuderi S., Celauro D. and Gibertini G., 2010. Population structure and dynamics of Procambarus clarkii (Girard, 1852) in a Mediterranean brackish wetland (Central Italy). Biol. Invasions, 12, 1415–1425. [Google Scholar]
  • Smith Jr W.O., Ainley D.G. and Cattaneo-Vietti R., 2007. Trophic interactions within the Ross Sea continental shelf ecosystem. Phil. Trans. R. Soc. B., 362, 95–112. [CrossRef] [Google Scholar]
  • Stouffer D.B., Sales-Pardo M., Sirer M.I. and Bascompte J., 2012. Evolutionary Conservation of Species’ Roles in Food Webs. Science, 335, 1489–1492. [CrossRef] [MathSciNet] [PubMed] [Google Scholar]
  • Ugolini A., Beugnon G. and Vannini M., 1988. Orientation and escape reaction in Palaemonetes antennarius (Milne Edwards) (Natantia: Palaemonidae). Monitor. Zool. Ital., 22, 105–109. [Google Scholar]
  • Ugolini A., Talluri P. and Vannini M., 1989. Astronomical orientation and learning in the shrimp Palaemonetes antennarius. Mar. Biol., 103, 489–493. [CrossRef] [Google Scholar]
  • Ungherese G., Boddi V. and Ugolini A., 2008. Eco-physiology of Palaemonetes antennarius (Crustacea, Decapoda): the influence of temperature and salinity on cardiac frequency. Physiol. Entomol., 33, 155–161. [CrossRef] [Google Scholar]

Cite this article as: L. Traversetti, A.J.M. Dörr and M. Scalici, 2016. The freshwater grass shrimp Palaemonetes antennarius in the diet of fish in Lake Bracciano (Central Italy). Knowl. Manag. Aquat. Ecosyst., 417, 7.

All Tables

Table 1

Fish check-list of the Lake Bracciano (Gibertini et al., 2004). The years of investigation are indicated for each studied species in the last column.

In the text
Table 2

Shrimp occurrence within full stomachs, divided per sampling season and year, and standard length range (SL, cm) of the 10 investigated species (au = autumn; wi = winter; sp = spring; su = summer).

In the text
Table 3

Correlations between P. antennarius cephalothorax length (CTL) and fish standard length of the 8 selected species divided per sampling year (significant values are in bold; ns = not significant). The two planktofagous species C. lavaretus and A. boyeri were omitted from the analysis, since no data on shrimp larval size and growth were available.

In the text

All Figures

thumbnail Fig. 1

Alimentary diagrams obtained plotting both freshwater shrimp abundance and occurrence for 5 selected species divided per sampling season (au = autumn; wi = winter; sp = spring; su = summer) and year, and standard length range in cm. The remaining fish species showing few data or an occasional occurrence of P. antennarius were excluded in this analysis. Since we would not evaluate fish species diet overlap, only the shrimp components found inside the stomachs were shown in the Amundsen et al. (1996) graphic outputs.
In the text
thumbnail Fig. 2

P. antennarius cephalothorax mean length (CTL, ± standard deviation) for the 8 selected and investigated species divided per sampling year.
In the text
thumbnail Supplementary Material 1.

Graphic representation for the interpretation of feeding strategy, niche width contribution, and prey importance, as proposed by Amundsen et al. (1996) (figure modified). HBI = high between individuals; HWI = high within individuals.
In the text

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