Corresponding author: Josie South ( josiesouth93@gmail.com ) Academic editor: Anthony Ricciardi
© 2019 Josie South, Monica McCard, Dumisani Khosa, Lubabalo Mofu , Takudzwa C. Madzivanzira, Jaimie T. A. Dick, Olaf L. F. Weyl.
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:
South J, McCard M, Khosa D, Mofu L, Madzivanzira TC, Dick JTA, Weyl OLF (2019) The effect of prey identity and substrate type on the functional response of a globally invasive crayfish. NeoBiota 52: 9-24. https://doi.org/10.3897/neobiota.52.39245
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Biological invasions threaten biodiversity on a global scale, therefore, developing predictive methods to understand variation in ecological change conferred is essential. Trophic interaction strength underpins community dynamics, however, these interactions can be profoundly affected by abiotic context, such as substrate type. The red swamp crayfish (Procambarus clarkii) has successfully invaded a number of freshwater ecosystems. We experimentally derive the Functional Response (FR) (density dependent predation) of the red swamp crayfish preying upon both a benthic prey; chironomid larvae, and a pelagic prey; Daphnia magna, on a no substrate control, sand, and gravel substrates to determine whether (1) there is a higher impact on prey that are benthic, and (2) whether the presence of different substrate types can dampen the interaction strength. We apply and demonstrate the utility of the Functional Response Ratio (FRR) metric in unravelling differences in ecological impact not obvious from traditional FR curves. Procambarus clarkii is capable of constantly utilising high numbers of both benthic and pelagic prey items, showing a Type II functional response under all scenarios. The presence of gravel and sand substrate each independently decreased the magnitude FR upon D. magna. Though, with regards to chironomid larvae the FR curves showed no difference in magnitude FR, the FRR reveals that the highest impact is conferred when foraging on sand substrate. This reinforces the need for impact assessments to be contextually relevant.
Aquatic invasions, functional response ratio, invader impact, macroinvertebrates, Procambarus clarkii, substrate
Aquatic biological invasions are increasing at an alarming rate driven by increased connectivity due to new trade routes and ongoing climatic change (
Invasive species are often characterised by their efficiency of resource consumption, whereby they generally show a higher per capita effect towards a focal resource in comparison to a native analogue (
Species usually form habitat associations depending on their specific life history needs or due to optimal foraging theory, wherein the most productive habitat is selected (
The red swamp crayfish, Procambarus clarkii (Girard, 1852), is a widespread invasive species due to its wide thermal tolerance, high trait plasticity ,and popularity in aquaculture and the pet trade (
Specimens of sub-adult P. clarkii (mean ± SD: 21.62 ± 2.6 mm carapace length, n = 25) were supplied by Seahorse Aquariums (Republic of Ireland) and maintained at the Queen’s University Marine Laboratory in a continuously aerated 600 L holding tank, with shelters made of drainpipe halves, supplied with dechlorinated tap water held at 23 ± 1.0 °C using aquarium heaters and subject to natural light regime. During the experimental period there was no cannibalism. Procambarus clarkii were maintained on commercial sinking fish food (JBL, Germany) to avoid conditioning to experimental prey items. As this species breeds at small sizes and because they are controlled species within the United Kingdom and Northern Ireland non-reproductive sub-adult crayfish were used in this experiment. Two live prey species, chironomid larvae (3.0 ± 0.6 SD mm total length) (Chironomidae) and Daphnia magna (0.3 ± 0.01 SD mm) (Daphnia magna; Daphniidae), were supplied, also from Seahorse Aquariums. Appropriate ethical approval for the use of these animals in research was obtained from the QUB Ethics Committee (School of Biological Sciences) and National Research Foundation – South African Institute for Aquatic Biodiversity (NRF–SAIAB ethics boards (25/4/1/5_2018-06).
A full factorial experimental design was employed to test differences in FR with regards to factors: “prey species” (2 levels), “density” (9 levels), and “substrate” (3 levels). Experimental arenas (W: 20 × L: 30 × H: 14 cm, 8 L) were held at 23 ± 1.0 °C and experiments were completed in a fully randomised design. Three substrate treatments were supplied: no substrate, commercial aquarium sand supplied at a depth of 4 mm in the experimental arena, and gravel (grain size: 8 × 4 mm) positioned using one 4 mm layer at the bottom of the experimental arena. Arenas were covered from the top and sides to avoid any synergistic or antagonistic conspecific effects. Individual predators were added per arena and allowed to acclimate for one hour before adding prey items. Each prey species was supplied at 9 densities (2, 7, 15, 40, 60, 90, 120, 200, 300 individuals per arena, n = 5 for each treatment), crayfish were allowed to feed for 1 h, after which the predators were removed, and number of prey items consumed were enumerated.
Control trials were carried out in experimental tanks at identical environmental conditions, wherein each prey species was supplied at the highest density in the absence of predators (n = 3 per substrate treatment) to determine potential background mortality. Each crayfish was re-used multiple times, but experienced each density of each prey type only once. Crayfish were given at least 3 days between use and were not fed for 24 h prior to experimental procedure to standardise hunger levels.
All analyses were undertaken using the R Statistical Software (v. 3.4.3). A generalised linear model (GLM) with a quasi-Poisson error distribution was used to determine differences in prey consumption with regards to factors “prey species”, “prey density”, and “substrate complexity”, using a Type 3 Anova and χ2 to report the effect size of a factor on the dependent variable. Tukey’s HSD was used to generate pairwise estimates with Holm-Bonferroni adjustment of P values post-hoc.
The R package ‘frair’ (
wherein, Ne represents the number of prey eaten, N0 is the initial density of prey, a is the attack parameter, h is the handling parameter, and T is the total time available. The Lambert W function was implemented to fit the model to the data (
The FRR (
where a is the attack parameter and h is the handling parameter derived from the FR curve. In this case the FRR is used as a diagnostic tool to determine whether there were differences that can not be observed from the usual FR outputs. Therefore, the higher the FRR value the higher the inferred impact (
Prey survival was >99% under all control treatments and thus any mortality was due to predation by P. clarkii, which was also frequently observed. Procambarus clarkii were observed in pilot experiments to feed upon chrinomid larvae by searching with their antennae and maxillipeds, contrastingly they fed upon D. magna in a filter feeding fashion by generating a flow via tail flicking behaviours.
All model terms significantly affected prey consumption by P. clarkii (Table
Model terms for all factors from GLM with a quasi-Poisson error distribution used to determine differences in prey consumption with regards to factors “prey species”, “density”, and “substrate”, using a Type 3 Anova and χ2 to report the effect size of a factor on the dependent variable.
Model term | Chisq | df | p-value |
---|---|---|---|
Prey species | 14 | 1 | <0.001 |
Density | 207713 | 8 | <0.001 |
Substrate | 78 | 2 | <0.001 |
Prey species * Density | 607 | 8 | <0.001 |
Prey species* Substrate | 112 | 2 | <0.001 |
Density * Substrate | 1556 | 16 | <0.001 |
Prey species * Density * Substrate | 1681 | 16 | <0.001 |
All prey species and substrate treatments resulted in a significant Type II FR by P. clarkii (Table
The FRR shows that when predating on chironomid larvae the impact of P. clarkii is highest on sand substrate compared to gravel or no substrate (Fig.
Functional responses of Procambarus clarkii preying on chironomid larvae and Daphnia magna under different substrate treatments; no substrate (solid line), sand (dashed line), gravel (dotted line). Points indicate raw data distributions; no substrate (green), sand (blue), gravel (brown). Shaded areas are bootstrapped (n = 2000) 95% confidence intervals.
Functional response ratio (FRR) (a/h) of Procambarus clarkii preying on chironomid larvae and Daphnia magna under different substrate treatments; no substrate (green), sand (blue), gravel (brown).
First order terms and significance levels from logistic regression of the proportion of prey consumed against initial prey density, with FR Type, functional parameters (a, h, and 1/h), associated significance levels from Rogers’ random predator equation, bias accelerated and corrected 95% confidence intervals for a and h, and the functional response ratio (a/h) with regards to Procambarus clarkii predating upon chironomid larvae and Daphnia magna under different substrate types. a = attack rate; h = handling time; 1/h = maximum feeding estimate.
Prey | Substrate | First order term (p-value) | FR type | a (p-value) | a 95% BCa CI | h (p-value) | h 95% BCa CI | Maximum Feeding Estimate (1/h) | Functional Response Ratio (a/h) |
---|---|---|---|---|---|---|---|---|---|
Chironomid larvae | None | -0.016, <0.001 | II | 9.51, <0.001 | 6.79 – 3.53 | 0.007, <0.001 | 0.007–0.008 | 136.9 | 3102.7 |
Sand | -0.016, <0.001 | II | 14.54, <0.001 | 9.30 – 28.8 | 0.007, <0.001 | 0.007–0.008 | 129.8 | 1888.3 | |
Gravel | -0.016, <0.001 | II | 12.40, <0001 | 8.79 – 19.08 | 0.007, <0.001 | 0.007–0.008 | 131.5 | 1631.5 | |
D. magna | None | -0.022, <0.001 | II | 8.37, <0.001 | 6.43 – 12.09 | 0.003, <0.001 | 0.003–0.004 | 263.1 | 2202.6 |
Sand | -0.017, <0.001 | II | 14.50, <0.001 | 8.60 – 28.58 | 0.006, <0.001 | 0.006–0.007 | 144.9 | 2101.4 | |
Gravel | -0.014, <0.001 | II | 9.63, <0.001 | 6.58 – 15.31 | 0.009, <0.001 | 0.008–0.009 | 111.1 | 1070.9 |
Management of invasive species depends upon generating contextually relevant and accurate estimates of potential impact conveyed upon a recipient ecosystem (
Through the comparison of FR curves, it was possible to parameterise attack rate and handling time of a consumer upon a resource. Further, by comparing the FR curves for each prey species, we were able to distinguish whether one species may have higher pressures exerted upon it by an invasive species. Our results corroborate that P. clarkii indeed utilises both benthic and pelagic resources (
The presence of different substrata affects the predation efficiency of crayfish towards each prey type. Compared to the control treatment of no substrate, both sand, and gravel substrate caused a slight reduction in the attack parameter (or search efficiency) of P. clarkii upon the benthic chironomid prey rather than altering the handling time. This suggests that the presence of both sand and gravel can offer a refuge for benthic prey species as the crayfish is not able to access the meiofauna as readily. Similar trends are seen in benthic invasive gobiids, where gravel substrate reduces magnitude FR compared to sand substrates (
Daphnia magna is an important prey species for larval and adult crayfish (
Crayfish were able to generate a flow wherein the prey items were drawn closer, perhaps facilitating the low handling time demonstrated and indicating that filter feeding efficiency by adults is comparable to benthic foraging and thus warrants further investigation. Plasticity in feeding mode and flexible omnivory have been identified in other crustacean invaders (
Procambarus clarkii is a global polytrophic keystone consumer which has facilitated its spread and pervasion into numerous systems (
In the context of furthering approaches to impact prediction in invasion science, we establish here how the application of FR and FRR methods can be used to powerfully predict impact where traditional assessment methods would not have identified a difference between contexts. Furthermore, we discern that there is high potential for crayfish to differentially consume both benthic and pelagic macroinvertebrate species which has implications for nutrient cycling and resource provisioning for native species. In a destructive and spreading species like P. clarkii it is imperative to continue to determine scenarios wherein its predatory effect can be dampened in order to implement mitigation strategies as removal of crayfish once established is unfeasible.
We acknowledge the infrastructure and equipment provided by the NRF-SAIAB Research Platform and the funding channelled through the NRF-SAIAB Institutional Support system as well as the support received through the National Research Foundation – South African Research Chairs Initiative of the Department of Science and Technology (Inland Fisheries and Freshwater Ecology, Grant No. 110507). We thank the Queen’s University Marine Laboratory for use of laboratory facilities and a running grant.