Cannibalism behavior in the brown shrimp Crangon crangon
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1
Interdisciplinary Center for Marine and Environmental Research, Abel Salazar Institute of Biomedical Sciences, University of Porto, Portugal
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2
Abel Salazar Institute of Biomedical Sciences, University of Porto, Portugal
INTRODUCTION
The brown shrimp Crangon crangon is a common decapod crustacean in European estuaries and a valuable fisheries resource in the North Sea. Due to its high abundance, the species is an important component of the trophic web, both as prey and predator. Recently, a list of up to 291 prey species were identified through DNA metabarcoding of the species’ stomach contents, confirming its highly opportunistic feeding behavior (Siegenthaler et al. 2018). Yet, this list does not report cannibalism (i.e. the process of killing and consuming either all or part of a conspecific individual) which can account for up to 20% of the species’ diet in wild populations (Pihl & Rosenberg 1984, Marchand 1981, Evans 1983, Del Norte-Campos & Temming 1994, Feller 2006). Like in other crustaceans (Abdussamad & Thampy 1994, Fernandez 1999, Marshall et al 2005), both predation and cannibalism pressure are expected to vary with size and density of predator and prey, and also with food availability and temperature. Cannibalism may then contribute to control or regulate the natural recruitment (Campos & Van der Veer 2008). Additionally, cannibalism is one of the major difficulties which compromise the rearing of C. crangon (Delbare et al. 2014).
In the Dutch Wadden Sea, recent settlers of about 6mm suffer high cannibalism pressure from adults larger than 30mm (Del Norte-Campos & Temming 1994), suggesting size-selectivity. Here, we investigate the size-related susceptibility to cannibalism of C. crangon juveniles and adults. The relationship between the sizes of the cannibal-shrimp and its prey-shrimp is studied using not only live prey but also by offering a dead conspecific, in order to determine the opportunistic character of cannibalism.
MATERIAL AND METHODS
The experiments were run indoors at CIIMAR facilities. Two observational aquaria were prepared for the trials. Each aquarium was divided into 32 individual compartments (7x9cm) by a perforated acrylic structure. Water temperature (13-15ºC, mean = 14.3±1.4ºC) and salinity (26-30, mean = 29.0±2.0) were independently controlled. Photoperiod was kept at 12:12h and the food provided consisted of mussel meat.
Live juvenile and adult shrimps were collected in the Minho estuary (northern Portugal), with a 1m beam trawl, 10 days prior the start of the experiment. All animals were kept in maintenance aquaria in the same conditions and fed ad libitum. Trials were designed to favor cannibalism. Shrimps of known size (total length, TL, mm) were placed individually (in each of the 32 compartments) to act as ‘cannibal-shrimp’ (CS) and kept under starvation for 48h before the observational trials. ‘Prey-shrimps’ (PS) were kept in the maintenance aquaria up to the observational trials and fed ad libitum. After the starvation period, 5 PS (all with the same TL but smaller than the CS) were transferred into the respective CS compartment along with an extra dead shrimp of the same size as the live PS. After 24h, the animals were separated, measured and the sex of CS was identified. The number of remaining PS was registered. When ecdysis occurred during observations, these were excluded from data treatment. Shrimps used in the trials were not re-observed.
Results were tested to determine size-selectivity and to quantify the cannibal–prey length ratio, as well as possible differences between predator sex. All tests were run in R version 3.5.3 (R Core Team 2019).
RESULTS
A total of 366 observations were made, using 278 female (TL: 21 to 51mm, mean = 33.4±6.0mm) and 88 male (TL: 19 to 49mm, mean = 32.8±7.2mm) shrimps as potential cannibals.
As expected, nearly all CS showed cannibalistic behavior: 97.5% of the females and 95.5% of the males (no sex differences were found, p>0.05). Cannibalism was more common upon the dead PS (observed in 94.2% and 93.2% of the females and males, respectively; no sex differences, p>0.05) than upon live PS (observed in 61.5% and 55.7% of the females and males, respectively; no sex differences, p>0.05), while about 3% of the CS (all females) ate all the PS provided, both dead and live (Fig. 1). Only 6% of the shrimps that showed cannibalism did not eat the dead PS.
Cannibal behavior was found in all size classes, starting right at 19mm TL. Size ratio varied from 0.31 to 0.99, i.e. up to similar sizes between CS and PS (Fig. 2).
DISCUSSION
In the present work we confirmed an extremely intensive cannibalism behavior in juvenile and adult Crangon crangon. However, no size selectivity was found as feeding on conspecifics was observed in potential cannibal-shrimps over the entire size range (19-51mm), upon prey-shrimp of up to the same size of the cannibal.
Cannibalism is common in a wide range of animals, including Crustacea (Abdussamad & Thampy 1994, Fernandez 1999, Marshall et al. 2005), and has been documented both in field studies and in laboratory experiments. The evolution of cannibalism most likely resulted from a ‘tradeoff’ between its benefits (nutrition in case of food shortage, elimination of competitors) and its costs (risk of injury, acquisition of parasites and diseases, and potential detriment of a cannibal’s inclusive fitness). Cannibalistic populations may persist when food is severely scarce, whereas a non-cannibalistic but otherwise identical population would go extinct.
In crustaceans, cannibalism is often a response to a stressor such as limited food availability, high population densities (Abdussamad & Thampy 1994), limited refuge accessibility for vulnerable prey (Luppi et al. 2001) and low habitat complexity (Marshal et al. 2005). Prey vulnerability to predation is also relevant and is influenced by prey size (Fernandez 1999, Marshall et al. 2005), developmental stage and moult stage (Marshall et al. 2005). Favorable conditions to feed on conspecifics in this study included prior starvation, the lack of alternative prey, the relatively high densities and the absence of refuges for the prey-shrimp, including bottom sand.
As a form of density-dependent mortality, cannibalism functions as a self-regulating mechanism in many populations under natural settings, though the role of cannibalism in the recruitment control or regulation of C. crangon’s natural populations is not entirely clear (Campos & Van der Veer 2008). The stocking densities used in this study (11.1 ind m-2) were much lower than the highest reported for juvenile shrimps in their natural areas (about 80 ind m-2) (Bodekke et al. 1986). Under controlled settings, even higher densities of up to 582 ind m-2 have been used, and the resulting increased mortality (up to 66%) was attributed to cannibalism (Regnault 1976).
Feeding on conspecifics is associated with size heterogeneity between the cannibal and its prey (Marshall et al. 2005). The handling time of prey is expected to decrease with increasing size differences between cannibal and prey, resulting in higher profitability. Surprisingly, size disparity (ratio between the total length of cannibal and prey-shrimps) did not influence the results, as cannibalism was found in all size classes and upon prey-shrimps of up to similar size of the cannibal-shrimp. In other animals, cannibalism occurs between different life stages (and hence differing sizes): adults cannibalize their own eggs, larvae, juveniles, or other adults, and juveniles consuming eggs or other juveniles. Already during larval stages, food unpalatability or insufficient quantity can condition the brown shrimp’s cannibalistic behavior. During settlement, extreme cannibalism of C. crangon juveniles causes very high mortalities (Dalley 1980). The starving condition must then be a strong trigger for cannibalism in C. crangon, even at relatively low densities.
Cannibalism in crustaceans is often considered an opportunistic behavior associated with moulting (Marshal et al. 2005, Romano & Zeng 2017). During ecdysis, crustaceans are particularly vulnerable to predation and hence to cannibalism, because they must remain immobile and soft up to the end of the hardening process of the new carapace. It is still unknown which factors trigger the cannibalistic behavior, i.e. the release of signal products during molting or simply the presence of newly molted individuals (soft carapace). In the present work, the effect of molt stage was not investigated. Yet, the higher impact of cannibalistic behavior upon the dead prey-shrimp suggests that it is an opportunistic behavior. Nevertheless, active cannibalism upon the live prey-shrimp, which required agonist encounters, occurred in more than half of the observations.
Besides density-dependent, cannibalism is always a direct cause of mortality. Therefore, cannibalism by brown shrimp should be carefully considered when rearing brown shrimp under controlled conditions. In the rearing of other crustaceans, cannibalism poses similar problems. In Penaeus monodon, the cannibalism rate increases with stocking densities and decreases with increasing feeding frequency (Abdussamad & Thampy 1994), while in Litopenaeus vannamei higher mortalities are associated with cannibalism upon molting shrimps (Romano & Zeng 2017).
Future research should compare cannibalism for different population densities. Multiple-choice studies with alternative prey can clarify the preference for other prey. The impact of other factors requiring further investigation include: the shrimp molt cycle, the nutritional state, and the availability of refuges (sand, vegetation, shell, crevices).
List of figures
Figure 1. Proportion of female (F) and male (M) shrimps which displayed cannibalism behavior upon live (active) and upon dead (opportunistic) prey-shrimp.
Figure 2. Relationship between the total length (TL) of the cannibal-shrimp and the total length of its prey. The black line represents the size of the cannibal-shrimp.
Acknowledgements
The present study was supported by the Strategic Funding UID/Multi/04423/2019 (J Campos and A Bio) through national funds provided by FCT – Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020, Project RecBio - Operation MAR-01.04.02-FEAMP-0025 (S Costa-Dias) and SFRH/BD/111133/2015 (C Moreira) by NORTE-01-0145-FEDER-000035 (MARINFO).
References
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Keywords:
Cannibalism,
size-selectivity,
Opportunistic feeding,
Trophic relationship,
predator/prey
Conference:
XX Iberian Symposium on Marine Biology Studies (SIEBM XX) , Braga, Portugal, 9 Sep - 12 Sep, 2019.
Presentation Type:
Poster Presentation
Topic:
Ecology, Biodiversity and Vulnerable Ecosystems
Citation:
Moreira
C,
Reis
JT,
Costa-Dias
SC,
Bio
A and
Campos
J
(2019). Cannibalism behavior in the brown shrimp Crangon crangon.
Front. Mar. Sci.
Conference Abstract:
XX Iberian Symposium on Marine Biology Studies (SIEBM XX) .
doi: 10.3389/conf.fmars.2019.08.00107
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Received:
14 May 2019;
Published Online:
27 Sep 2019.
*
Correspondence:
Mx. Joana Campos, Interdisciplinary Center for Marine and Environmental Research, Abel Salazar Institute of Biomedical Sciences, University of Porto, Matosinhos, 4450-208, Portugal, jcampos@ciimar.up.pt