Research Article |
Corresponding author: Péter Borza ( borza.peter@ecolres.hu ) Academic editor: Adam Petrusek
© 2024 Katalin Patonai, Anna Bessenyei, Csaba F. Vad, Péter Borza.
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:
Patonai K, Bessenyei A, Vad CF, Borza P (2024) Functional responses correspond to stable isotope-based trophic positions among four invasive Ponto-Caspian mysid species (Crustacea, Mysida). NeoBiota 93: 187-201. https://doi.org/10.3897/neobiota.93.121346
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Determining the consumptive effects of non-native predators, for which several direct and indirect methods have been applied, is a common goal in invasion biology. Functional responses and stable isotope analysis are among the most widely used approaches; however, they are rarely used in combination. In this study, we used these two complementary methods to compare the predatory impacts of four invasive Ponto-Caspian mysids on zooplankton in a habitat (Danube River) where all four species coexist. The order of the species based on the attack rates of the functional response models matched with their mean δ15N values, indicating a correspondence between their predatory potentials and trophic positions in their invaded habitat. Hemimysis anomala had the highest attack rate on zooplankton presumably due to its higher degree of specialization linked to its pelagic lifestyle. Contrary to our expectations, the largest species, Paramysis lacustris, had an intermediate predatory efficiency and trophic position, similar to those of Limnomysis benedeni but higher than those of the smallest species, Katamysis warpachowskyi. Nevertheless, all of the four species exhibited a considerable predatory potential, suggesting that any of them can contribute significantly to their combined predatory impact depending on their densities. The congruence between the results of the two methods shows that the species can realize their different predatory potentials in their invaded environment, indicating favorable conditions (i.e., food availability and spatial heterogeneity) which allowed dietary differentiation. We recommend the combined use of functional responses and stable isotope analysis, which might allow robust conclusions to be drawn on the trophic ecology of the species and also provide further insights into the studied ecosystem.
Hemimysis anomala, Katamysis warpachowskyi, Limnomysis benedeni, Paramysis lacustris, predatory impact
Many of the most notorious cases of biological invasions are related to predatory impacts causing drastic declines or even extinctions of native prey populations (
Determining the consumptive effects of non-native predators is a common goal in invasion biology. Since the direct visual analysis of stomach contents is often problematic (especially in small animals with masticatory organs) and burdened heavily with spatiotemporal variation, several indirect methods have been developed (
Although both methods are widely used, they are rarely combined (
Owing to its highly diverse endemic euryhaline fauna, the Ponto-Caspian region (i.e., the Black, Azov, Caspian, and Aral seas and the lower sections of the rivers running into them) is one of the most important sources of aquatic invasive species in Europe and in North America (
Previous studies suggest that the predatory impacts of the four species might be different. The most widespread species, Hemimysis anomala G. O. Sars, 1907 is the most notorious for its partially predatory diet causing substantial changes in the zooplankton community, thereby altering pelagic trophic pathways (
These dietary profiles are based mainly on single-species studies (with the exception of
The specimens of the four mysid species used for the experimental test of functional responses were collected on 29.10.2019 in a semi-enclosed inlet of the Danube River) within the city of Budapest, Hungary (’Lágymányosi-öböl’; 47°27.9'N, 19°03.6'E) by a hand net. The populations of the species at the time of the sampling consisted mainly of relatively large (i.e., similarly-sized as the adults of the summer generations) but sexually immature specimens of the overwintering generation with a few mature individuals originating from the last summer generation (
The setup of the functional response experiment. The body length and dry weight values represent the means and ranges (in brackets).
Predator | Prey density (replicates) | ||||
---|---|---|---|---|---|
Species | No. of specimens | Body length, mm | Dry weight, mg | Sex | |
Hemimysis anomala | 24 | 6.0 (5.0–8.0) | 1.2 (0.6–1.7) | 1 male, 23 juv. | 2(3), 4(3), 6(3), 8(3), 10(3), 15(3), 20(3), 30(3) |
Katamysis warpachowskyi | 10 | 4.5 (3.5–5.0) | 0.4 (0.2–0.6) | 4 females, 6 juv. | 2(1), 4(1), 6(2), 8(3), 10(3) |
Limnomysis benedeni | 12 | 6.25 (5.5–7.0) | 1.1 (0.8–1.3) | 12 juv. | 2(1), 4(1), 8(1), 10(3), 15(3), 20(3) |
Paramysis lacustris | 24 | 9.5 (7.0–11.0) | 2.65 (1.6–4.4) | 3 males, 21 juv. | 2(3), 4(3), 6(3), 8(3), 10(3), 15(3), 20(3), 30(3) |
None (control) | 2(1), 4(1), 6(1), 8(1), 10(1), 15(1), 20(1), 30(1) |
At the start of the experiment, commercially available Daphnia pulex Leydig, 1860 (body length: 1.5–2 mm) were added to the jars as prey corresponding to the experimental prey density levels (Table
The samples for stable isotope analysis were collected in the same location as mentioned above between 29.-30.08.2022. In total, samples for seven different food web components were obtained: four mysid species, Copepoda, Cladocera, and detritus. The four mysid species were collected using a hand net and sorted by species into separate containers in the field. Zooplankton samples were collected using a 70 μm-mesh-sized plankton tow net, rinsed with distilled water, and stored in plastic containers. Pieces of decomposing willow leaves (i.e., detritus) were picked from the sediment material caught up in the hand net during the collection of the mysids. Zooplankton and detritus samples were stored on dry ice until returning to the laboratory where they were stored at −20 °C until further processing. In the laboratory, the mysid specimens were kept in filtered tap water over gauze for 24 hours to allow their gut contents to empty before freezing (
For each stable isotope sample of animals, entire individuals belonging to the same taxonomic group were processed as a batch, yielding 4–6 sample replicates per group. Mysid samples contained 4–5 (P. lacustris) or 8–11 (the other three species) adult individuals of both sexes distributed evenly (corresponding to the sex ratio of the collected material). Cladocera and Copepoda (copepodites and adults of calanoids and cyclopoids, excluding nauplii) samples contained several specimens sorted using a fine tweezer. All samples were placed in 2 ml cryovials covered with lint-free tissue paper held by rubber bands and freeze-dried for 24 hours.
Lipids are more depleted in 13C compared to carbohydrates and proteins (
Functional response models were fitted using the ‘frair’ package (
Our aquatic invertebrate samples had high C:N ratio (>3.5), thus lipid correction was applied using the equation for aquatic animals (δ13Ccorr = δ13Craw −3.32 + 0.99 × C:N;
Three of the four studied species – H. anomala, L. benedeni, and P. lacustris – showed density dependent consumption of D. pulex during the experiment (Fig.
Functional responses of the four invasive Ponto-Caspian mysid species. The solid lines correspond to the fitted Type II curves with the 95% confidence intervals indicated by the dashed areas. The dashed line indicates the consumption of all prey items (slope = 1).
Estimates of the parameters of the Type II functional response curves (a: attack rate, h: handling time). The units of the parameters correspond to the experimental setup (a: 1/200 ml/12 hours; h: 12 hours).
Species | Parameter | Estimate | Lower CI | Upper CI |
---|---|---|---|---|
Hemimysis anomala | a | 1.459 | 1.029 | 2.198 |
h | 0.02 | 0 | 0.052 | |
Limnomysis benedeni | a | 0.515 | 0.335 | 0.703 |
h | 0 | 0 | 0.139 | |
Paramysis lacustris | a | 0.693 | 0.517 | 1.074 |
h | 0.027 | 0 | 0.075 |
Estimates of the interspecific differences between the parameters of the Type II functional response curves (a: attack rate, h: handling time). The units of the parameters correspond to the experimental setup (a: 1/200 ml/12 hours; h: 12 hours).
Compared species | Parameter | Estimate | SE | Z | p |
---|---|---|---|---|---|
H. anomala – L. benedeni | ∆a | 0.946 | 0.352 | 2.687 | 0.0072** |
∆h | 0.020 | 0.071 | 0.287 | 0.7742 | |
H. anomala – P. lacustris | ∆a | 0.766 | 0.308 | 2.487 | 0.0129* |
∆h | −0.007 | 0.025 | 0.287 | 0.7744 | |
P. lacustris – L. benedeni | ∆a | 0.180 | 0.276 | 0.653 | 0.5139 |
∆h | 0.028 | 0.074 | 0.373 | 0.7090 |
In the case of K. warpachowskyi, only 1–2 D. pulex specimens were consumed in eight out of the ten jars independently of prey density (Fig.
Based on δ13C, all investigated animal groups (range: −30.52 to −32.76‰) separated clearly from detritus (−28.76 to −29.83‰; Fig.
Stable isotope ratios of the studied food web components A all groups with means ± SD (empty symbols and error bars) B the isotopic niche overlap of the four invasive Ponto-Caspian mysid species illustrated by Stable Isotope Bayesian Ellipses corrected for small sample size (SEAc). The inner ellipses correspond to the 40%, the outer ones to the 95% credible intervals. CLA: Cladocera, COP: Copepoda, HA: Hemimysis anomala, KW: Katamysis warpachowskyi, LB: Limnomysis benedeni, PL: Paramysis lacustris.
Results of the post hoc Dunn’s test on the stable isotope ratios and isotopic niche overlaps of the four invasive Ponto-Caspian mysid species.
Compared species | δ13C | δ15N | Overlap (95% SEAc ellipses) | ||
---|---|---|---|---|---|
z | padj | z | padj | ||
H. anomala – K. warpachowskyi | −2.650 | 0.040* | 3.112 | 0.011* | 0% |
H. anomala – L. benedeni | 0.102 | 0.919 | 1.020 | 0.923 | 32% |
K. warpachowskyi – L. benedeni | 2.752 | 0.036* | −2.092 | 0.146 | 13% |
H. anomala – P. lacustris | −1.322 | 0.372 | 0.786 | 0.864 | 19% |
K. warpachowskyi – P. lacustris | 1.446 | 0.593 | −2.464 | 0.069 | 28% |
L. benedeni – P. lacustris | −1.428 | 0.460 | −0.280 | 0.780 | 23% |
The δ15N values were the lowest in the detritus samples (3.92 to 5.89‰), followed by cladocerans (10.13 to 10.42‰), copepods (11.33 to 14.23‰), and mysids (14.24 to 17.36‰; Fig.
The 95% Bayesian ellipses overlapped between all species pairs except for K. warpachowskyi and H. anomala (Fig.
The two methods applied in our study yielded congruent results, providing a consistent picture about the predatory impacts of the four invasive Ponto-Caspian mysid species. Specifically, the order of the species based on the attack rates of the functional response curves matched with their mean δ15N values, indicating a correspondence between their predatory potentials and trophic positions in their natural habitat. Contrary to our expectations, both approaches indicated H. anomala as the most predatory species, whereas the largest species, P. lacustris, had an intermediate attack rate and trophic position similar to those of L. benedeni. The smallest species, K. warpachowskyi, showed the lowest predatory activity in both tests which matched our a priori assumptions. The δ13C values indicated further differences in the diet of the species corresponding to their habitat preferences (benthic or pelagic) which were also reflected in the isotopic overlaps.
The higher attack rate of H. anomala indicates that it is more effective at capturing zooplankton than the other species, presumably due to its higher degree of specialization in connection to its pelagic lifestyle. The constant swimming might imply a higher encounter rate which in itself could potentially explain the differences; however, other behavioral, physiological, or morphological adaptations related to prey capture might also be involved (e.g., longer setae on the thoracic endopods; pers. obs.). On the other hand, the active lifestyle of H. anomala might also result in a higher metabolic rate, implying that the high ratio of nutritious animal prey in its diet is an energetic necessity in this species. Body size proved to be irrelevant in this context, suggesting that its role in intraspecific diet shifts might be related to prey size limitations that are not relevant at the size of adults. Although we did not test it, it is reasonable to assume that P. lacustris is in turn more effective at capturing benthic prey and indeed consumes more of them as indicated by its higher δ13C values, implying a somewhat stronger association with detritus-based food sources. Nevertheless, the congruence between the results of the two methods suggests that its attack rate on zooplankton reflects its overall trophic position. Unfortunately, our data did not allow the estimation of handling times which could be used to calculate the maximum feeding rates of the species. However, the higher trophic position and the presumably higher metabolic rate of H. anomala suggest that it might potentially have a higher per capita predatory impact than P. lacustris despite the larger body size of the latter.
Our results on L. benedeni confirmed its considerable predatory potential observed previously under artificial conditions (
K. warpachowskyi did not show density dependent consumption in our functional response experiment which might indicate that the size of the offered prey items was close to the upper limit of its potential prey size range. Nonetheless, the significantly higher mortality of D. pulex in the presence of the species compared to the control jars suggests that K. warpachowskyi was able to actively hunt down at least some of the prey instead of merely consuming the dead ones. The stable isotope data also confirmed that predation can have a considerable contribution to the diet of the species, as its trophic position – although the lowest among the four mysid species – was still somewhat higher than that of copepods. This suggests that K. warpachowskyi may still be an effective predator of smaller zooplankton and zoobenthos.
Overall, our results indicate that H. anomala is the most effective predator of the four invasive Ponto-Caspian mysids. However, all of the other three species also have a considerable predatory potential, suggesting that their combined effect might be even stronger when occurring in syntopy. The densities of each mysid species might be highly dependent on local environmental conditions (e.g., habitat availability), implying that any of them may become the most impactful in certain areas regardless of their per capita effects. We also would like to point out that animal prey is only one component of the diet of these omnivorous species, and other food sources such as phytoplankton, phytobenthos or detritus (
Beyond the characterization of the species, the combination of the two methods also allows certain conclusions to be drawn on the studied ecological system. The differences in predatory effectiveness among the species revealed by their functional responses can be interpreted as a result of coevolution which can contribute to their niche differentiation. The congruence between the results of the two methods indicates that the species can realize their different predatory potentials in their natural environment. The favorable conditions of the studied water body (e.g., availability of alternative food sources and sufficient habitat diversity) could have allowed the diversification of the diets among the species, indicating a stable coexistence. The differentiation in carbon source between the benthic and pelagic species resulting in lower isotopic overlaps also points in this direction. Alternatively, it can also be presumed that the species are subject to top-down control (by e.g. fish) resulting in relatively low population densities, in which case the food is not a limiting factor for them in the studied system.
Due to the low number of studies applying both methods in parallel, our understanding of the factors determining the connection between functional responses and stable isotope-based trophic positions is still rather limited. It seems likely that the congruent results in our case are not exceptional and similar outcomes can be expected in systems in a near-equilibrium state (i.e., after the establishment and stabilization of invasive populations, as in the present case). However, we expect that discrepancies are possible also among species with coevolved differences in predatory efficiency under certain conditions. For example, predation risks or low food availability might prevent a more effective predator from realizing its potential. Anomalies might be more frequent in cases involving native and invasive species, or multiple invasives with different origins. For instance, one of two species might be competitively superior and therefore more successful at capturing the preferred prey even if their predatory potentials are similar. The study of
In summary, combining functional responses and stable isotope analysis allowed us to draw robust conclusions on the trophic ecology of the species and also provided further insights into the trophic structure of the studied ecosystem. We recommend the use of this approach in further studies which might also shed more light on the factors determining how predatory potentials are realized in natural environments.
The authors wish to thank Martin Kainz, Samuel-Karl Kämmer, and Leonard Wassenaar for conducting the stable isotope measurements.
The authors have declared that no competing interests exist.
No ethical statement was reported.
KP was supported by the ÚNKP-22-4 New National Excellence Program of the Ministry for Cul-ture and Innovation from the source of the National Research, Development and Innovation Fund. KP and PB was supported by the project FK_19 132605 of the National Research, Development and Innovation Fund of Hungary.
Conceptualization: PB, KP, CFV. Formal analysis: KP, AB, PB. Funding acquisition: PB. Investigation: KP, PB, AB. Methodology: AB, PB, KP, CFV. Visualization: PB, CFV, KP. Writing - original draft: PB, KP. Writing - review and editing: AB, CFV.
Katalin Patonai https://orcid.org/0000-0002-7248-7394
Csaba F. Vad https://orcid.org/0000-0003-4744-0698
Péter Borza https://orcid.org/0000-0002-8555-8235
All of the data that support the findings of this study are available at: https://figshare.com/projects/Functional_responses_and_stable_isotope_analysis_of_invasive_Ponto-Caspian_mysids/177159.
Estimates of the differences between the parameters of the Type II functional response curves with and without mature specimens (a: attack rate, h: handling time)
Data type: docx