Research Article |
Corresponding author: Nicolas Spilmont ( nicolas.spilmont@univ-lille.fr ) Academic editor: Frank Collas
© 2023 Nicolas Spilmont, Laurent Seuront.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Spilmont N, Seuront L (2023) Aliens eating aliens: an introduced amphipod as a potential prey of an invasive rocky shore crab in laboratory experiments. Aquatic Invasions 18(2): 163-177. https://doi.org/10.3391/ai.2023.18.2.106252
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Behavioural interactions between introduced predators and introduced prey are still largely underestimated. The present work takes advantage of the co-occurrence of two introduced species, the Asian shore crab Hemigrapsus sanguineus and the amphipod Ptilohyale littoralis, respectively first recorded on rocky shores along the French coast of the eastern English Channel in 2005 and 2016. In this context, the predation by male and female H. sanguineus on P. littoralis was examined under controlled laboratory conditions, by presenting either juveniles of the blue mussel Mytilus edulis or adult P. littoralis to H. sanguineus. We subsequently assessed the potential prey preference of the Asian shore crab for P. littoralis and M. edulis by presenting the two prey items simultaneously in the same proportion. In the absence of choice, male H. sanguineus preyed significantly more on M. edulis than P. littoralis. In contrast, females preyed significantly less on M. edulis than P. littoralis; however, male and female H. sanguineus consumed similar numbers of P. littoralis. When choice was possible between P. littoralis and M. edulis, the crab did not exhibit preference stricto sensu for any type of prey. These results suggest that the Asian shore crab cannot be considered as a naive predator when confronted to a newly introduced prey. Our results also suggest that the amphipod P. littoralis did not exhibit any effective antipredator response towards the crab. These observations nevertheless warrant further work on the effects of abiotic factors (e.g. temperature) as well as other biotic interactions (e.g. presence of other prey or predators for H. sanguineus) may have on the observed prey-predator interactions between H. sanguineus and M. edulis and P. littoralis.
Asian shore crab, Hemigrapsus sanguineus, amphipod, Ptilohyale littoralis, predation, behaviour
Behaviour is one of the most critical components in the success of introduced species to become invasive (
Based on the lack of co-evolution history between introduced species (either predator or prey) and their native counterparts, a range of evolutionary hypotheses has been introduced to describe novel predator-prey interactions; see e.g.
The nature of the abovementioned predator-prey interactions is, however, noticeably both species- and location-dependent, and may also vary along the invasion process due to a potential loss of naiveté (
Hemigrapsus sanguineus (De Haan, 1835) is a native species of the North-West Pacific coast which has been reported along the North Atlantic European coast in the late 1990’s (
The North American amphipod Ptilohyale littoralis (Stimpson, 1853) was first reported in Europe in the Port of Rotterdam in 2009, where it is believed to have been introduced through ballast water and/or hull fouling, and subsequently at the mouth of the Westerschelde estuary and in Yerseke (
Animals were collected during early spring (March-April 2016) in the mid-intertidal zone of the rocky reef “Fort de Croy” located in Wimereux, France (50°45.766'N, 1°35.962'E). Adults of H. sanguineus were collected manually, brought back to the nearby laboratory (LOG, Station Marine de Wimereux), sex determined, and males and non-ovigerous females were kept in separate tanks (52 cm × 46 cm × 35 cm) containing rocks from the sampling site, with running natural seawater at in situ temperature (11 °C) under a natural day/night cycle. Food (commercial fish pellets) was provided ad libitum but, to standardize hunger levels, crabs were starved for 24 h prior to experiments.
During the low tide preceding each experiment, sediment was collected at the same sampling site. Following Blasi & O’Connor (2016), sediment containing amphipods was placed into a bucket filled with seawater and swirled by hand to cause amphipods to swim up into the water. The water was then sieved (1 mm mesh-size) and visually inspected for the presence of Ptilohyale littoralis. Living individuals were carefully collected with forceps and checked under binoculars. Undamaged large individuals of similar sizes (10–12 mm length) were then kept in the laboratory in PVC cylinders (10 cm in diameter) with mesh bottom, suspended in aquaria with running natural seawater. Juvenile mussels (Mytilus edulis; length in the range 5–10 mm) recovered from the same sediment samples were kept in separate aquaria (same conditions as H. sanguineus). All living animals were returned to the sampling location after completion of the experiments.
For all predation trials, non-moulting adult H. sanguineus (carapace width CW = 21.02 ± 2.24 mm, mean ± SD, N = 100) with intact chelae were individually isolated in small plastic aquaria (16.0 cm × 9.5 cm × 10.5 cm) without sediment (to easily retrieve non-consumed amphipods), closed with plastic lids and immersed in larger glass aquaria (90 cm × 50 cm × 30 cm) with running natural seawater. A shelter was offered in each experimental aquarium in the form of a dark gray PVC pipe (6.5 cm long, 4 cm in diameter) longitudinally cut in half. Since H. sanguineus preferentially feeds at night due to its photophobic behaviour (
Attempts to provide a definition to food/prey ‘preference’ have a long-lasting history (see e.g.
Here, we specifically considered preference stricto sensu as a behaviour implying an active choice between distinct food items. To be objectively and quantitatively inferred, this definition requires the comparison of food consumption when only one prey species is available with consumption when several prey species are available, as initially defined by
It has also been suggested that, in choice experiments, not only the proportions but also the order in which prey are consumed is important to determine preference (
The prey tested in the present study were either P. littoralis or M. edulis (5 individuals offered to each crab: no-choice experiments) or a mixture of both (5 individuals of each prey offered to each crab: choice experiments); in Stage 2bis, 1 individual of one type and 5 individuals of the other were offered to each crab. A batch of 10 H. sanguineus individuals was tested during each experimental night; sexes were randomly selected for each batch to attain a total of 15 males and 15 females for each type of predation trial (Table
Experimental treatments used to test for predation of female and male H. sanguineus on Mytilus edulis and Ptilohyale littoralis in no-choice experiments (Stage 1) and choice experiments (Stage 2 and Stage 2bis). Control experiments were run to test on the mortality of P. littoralis.
Experiment | Prey | Predator | replicates (N) | ||
---|---|---|---|---|---|
M. edulis | P. littoralis | female H. sanguineus | male H. sanguineus | ||
Control | 0 | 5 | 0 | 0 | 10 |
Stage 1 | 5 | 0 | 0 | 1 | 15 |
5 | 0 | 1 | 0 | 15 | |
0 | 5 | 0 | 1 | 15 | |
0 | 5 | 1 | 0 | 15 | |
Stage 2 | 5 | 5 | 0 | 1 | 15 |
5 | 5 | 1 | 0 | 15 | |
Stage 2bis | 1 | 5 | 0 | 1 | 15 |
1 | 5 | 1 | 0 | 15 | |
5 | 1 | 0 | 1 | 15 | |
5 | 1 | 1 | 0 | 15 |
To compare results obtained from the no-choice experiments, we used the non-parametric Wilcoxon-Mann-Whitney U test (WMW test hereafter).
For preference tests, we used the procedure proposed by
In no-choice experiments (Stage 1; Fig.
Number (mean ± S.D., N = 15 for each bar) of prey (Mytilus edulis, grey bars; Ptilohyale littoralis, white bars) consumed by male and female Hemigrapsus sanguineus over 12 h (nighttime) during no-choice experiments (A: Stage 1, prey presented one type at a time) and choice experiments (B: Stage, two types of prey presented simultaneously).
The consumption rate of M. edulis significantly differed between male and female H. sanguineus (WMW test: P = 4.4 10-6). Specifically, twelve females did not prey on M. edulis and the maximum number of mussels eaten by a single individual was 3. In sharp contrast, all males consumed at least one mussel and five of them did prey on the 5 individuals presented. The consumption rate of P. littoralis was non-significantly different between males and females (WMW test: P = 0.445).
The results of the choice experiments (Stage 2; Fig.
Consumed individuals of each type of prey (Mytilus edulis, M. e. and Ptilohyale littoralis, P. l.) by adult female and male Hemigrapsus sanguineus observed (Obs) during no-choice experiments (Stage 1) and choice experiments (Stage 2). Expected values (Exp) were obtained from the equations of maximal likelihood given by
Males | Stage 1 | Stage 2 | χ2 | P value | ||||
M. e. Obs | P. l. Obs | M. e. Obs | P. l. Obs | M. e. Exp | P. l. Exp | |||
Global | 55 | 32 | 47 | 20 | 43.6 | 23.4 | 0.76 | 0.385 |
1 | 3 | 4 | 2 | 3 | 2.1 | 2.8 | 0.01 | 0.916 |
2 | 5 | 3 | 5 | 2 | 4.5 | 2.5 | 0.16 | 0.693 |
3 | 4 | 4 | 3 | 2 | 2.6 | 2.4 | 0.16 | 0.691 |
4 | 3 | 2 | 5 | 3 | 4.9 | 3.1 | 0.01 | 0.937 |
5 | 3 | 2 | 3 | 0 | 2.1 | 0.9 | 1.24 | 0.266 |
6 | 4 | 3 | 5 | 1 | 3.8 | 1 | 0.99 | 0.318 |
7 | 5 | 0 | 3 | 0 | 3 | 0 | 0 | 1 |
8 | 5 | 1 | 1 | 3 | 2.8 | 1.2 | 4.03 | 0.04 |
9 | 5 | 1 | 1 | 4 | 3.4 | 1.6 | 5.43 | 0.02 |
10 | 2 | 5 | 3 | 2 | 3.3 | 1.7 | 1.46 | 0.226 |
11 | 1 | 0 | 3 | 0 | 3 | 0 | 0 | 1 |
12 | 4 | 3 | 5 | 0 | 3.4 | 1.6 | 2.40 | 0.121 |
13 | 4 | 1 | 3 | 0 | 2.6 | 0.4 | 0.47 | 0.491 |
14 | 2 | 2 | 5 | 0 | 3.7 | 1.3 | 1.78 | 0.182 |
15 | 5 | 1 | 4 | 0 | 3.6 | 0.4 | 0.49 | 0.483 |
Females | Stage 1 | Stage 2 | χ2 | P value | ||||
M. e. Obs | P. l. Obs | M. e. Obs | P. l. Obs | M. e. Exp | P. l. Exp | |||
Global | 5 | 38 | 4 | 34 | 0.2 | 33.8 | 0.01 | 0.904 |
1 | 0 | 1 | 0 | 5 | 0 | 5 | 0 | 1 |
2 | 1 | 3 | 1 | 4 | 1 | 4 | 0 | 1 |
3 | 0 | 3 | 0 | 3 | 0 | 3 | 0 | 1 |
4 | 0 | 3 | 0 | 1 | 0 | 1 | 0 | 1 |
5 | 0 | 3 | 0 | 1 | 0 | 1 | 0 | 1 |
6 | 3 | 4 | 0 | 2 | 1 | 1 | 2.2 | 0.136 |
7 | 0 | 3 | 0 | 2 | 0 | 2 | 0 | 1 |
8 | 0 | 5 | 0 | 2 | 0 | 2 | 0 | 1 |
9 | 0 | 4 | 0 | 4 | 0 | 4 | 0 | 1 |
10 | 0 | 3 | 0 | 5 | 0 | 5 | 0 | 1 |
11 | 1 | 2 | 0 | 0 | 0 | 0 | 0 | 1 |
12 | 0 | 4 | 1 | 2 | 0.4 | 2.6 | 1.2 | 0.277 |
13 | 0 | 3 | 1 | 0 | 0.2 | 0.8 | 3.8 | 0.05 |
14 | 1 | 4 | 1 | 1 | 0.5 | 1.5 | 0.6 | 0.434 |
15 | 1 | 2 | 0 | 2 | 0.4 | 1.6 | 0.6 | 0.457 |
The present study provides evidence, under laboratory-controlled conditions, for the existence of predator-prey interactions between two introduced crustaceans, the Asian shore crab Hemigrapsus sanguineus and the North American amphipod Ptilohyale littoralis, co-occurring outside their distinct native ranges in the intertidal zone of the eastern English Channel. Specifically, in no-choice experiments, both male and female H. sanguineus actively selected both M. edulis and P. littoralis, with females exhibiting a significantly lower consumption rate (i) on M. edulis than males, but not on P. littoralis, and (ii) on the native M. edulis than on the non-native P. littoralis. These results are consistent with previous studies showing a stronger predation pressure of males H. sanguineus on M. edulis than females due to differences in claw morphology and strength (
In two-prey choice experiments, H. sanguineus consistently did not exhibit any preference stricto sensu for either native or non-native prey though significant differences in the consumption rates of both types of prey were observed. This result seems to diverge from previous evidence that the Asian shore crab preferred mussels over other animal prey (
We, however, unambiguously showed that H. sanguineus is able to detect and consume P. littoralis although the latter was putatively introduced a decade later (i.e. circa 2016;
Since H. sanguineus did not exhibit any preference stricto sensu for either the indigenous (M. edulis) or the introduced (P. littoralis) prey, none of the evolutionary hypotheses of novel prey-predator interactions (see
The fact that a motile prey such as P. littoralis was consumed in high proportion, especially by female H. sanguineus, implicitly suggests, that P. littoralis either did not exhibit any, or expressed inappropriate/uneffective, antipredator response, which would support the ‘naive prey’ hypothesis (
Our results are relevant in an experimental context and, though controlled experiments remain a stepping stone in the understanding of prey-predator interactions, the extrapolation of laboratory observations to field events remains uncertain (
Though being part of the diet of the Asian shore crab in both its native and north-American invaded ranges, amphipods usually constitute only a small proportion of the overall food use (
This work is a contribution to the CPER research project CLIMIBIO. The authors thank the French Ministère de l’Enseignement Supérieur et de la Recherche, the Hauts de France Région and the European Funds for Regional Economical Development for their financial support for this project. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
N.S.: research conceptualization, sample design and methodology, investigation and data collection, data analysis and interpretation, original draft; writing
L.S.: research conceptualization, sample design and methodology, data interpretation, original draft; review & editing
The authors thank the organizing committee of the ICAIS 2022 conference and especially H. Verreycken for handling the ICAIS 2022 species issue of Aquatic Invasions as lead guest editor. We also thank anonymous reviewers for their constructive comments and suggestions which improved this paper.