Research Article |
Corresponding author: M. Mar Moretta-Urdiales ( mardmore@espol.edu.ec ) Academic editor: Belinda Gallardo
© 2020 M. Mar Moretta-Urdiales, Raffael Ernst, José Pontón-Cevallos, Rafael Bermúdez, Heinke Jäger.
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:
Moretta-Urdiales MM, Ernst R, Pontón-Cevallos J, Bermúdez JR, Jäger H (2020) Eat and be eaten: trophic interactions of the introduced frog Scinax quinquefasciatus in anthropogenic environments in Galápagos. NeoBiota 61: 17-31. https://doi.org/10.3897/neobiota.61.53256
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While the Galápagos Archipelago is known for its endemic flora and fauna, many introduced species have also become naturalised there, especially on the human-inhabited islands. The only amphibian species known to have established on the islands, the Fowler’s snouted treefrog (Scinax quinquefasciatus), is thought to have arrived about two decades ago. Since then, this treefrog has substantially extended its range to the islands of Santa Cruz and Isabela. Our study explores the potential influence of this introduced amphibian on native trophic systems on Santa Cruz and identifies potential antagonists likely to control larval frog populations. To understand the impact of S. quinquefasciatus as a predator of local invertebrate fauna, we performed a stomach-content analysis of 228 preserved adult specimens from seven different localities on Santa Cruz. Of the 11 macroinvertebrate orders recorded, Lepidoptera constituted more than 60% of the contents. We also identified active predators of S. quinquefasciatus tadpoles: larvae of the endemic diving beetle (Thermonectus basillarus galapagoensis). To determine the efficiency of this predator, we conducted predator-prey experiments in ex situ conditions. Tadpole predation was highest after first exposure to the predator and significantly decreased over time. Our experimental results demonstrate that although T. b. galapagoensis larvae are effective tadpole predators, their feeding saturation rates are likely inadequate for frog population control. Our findings provide the first baseline data necessary to make informed ecological impact assessments and monitoring schemes on Santa Cruz for this introduced treefrog.
amphibia, Galápagos, introduced species, island biodiversity, predator-prey interactions
Introduced species, which often transition to invasive species, are considered to be a major threat to global biodiversity (
Of the four human-inhabited islands of the Archipelago, S. quinquefasciatus is only known to occur on Santa Cruz and Isabela. It was formerly also present on San Cristóbal (
The ecology and potential impact of S. quinquefasciatus on the native ecosystems of Isabela have previously been addressed in
Invasive species often disrupt predator-prey interactions: as a new predator that consumes native prey (
Our study was conducted in the highlands of Santa Cruz, located at the centre of the Galápagos Archipelago (Fig.
The highlands of Santa Cruz support greater biodiversity and thus productivity than the lowlands, which are more extensive, but drier (
This study was conducted from April to May 2017–during the rainy season-at one ranch and six agricultural sites in the highlands of Santa Cruz (Fig.
Study area and collection sites (red dots) of Scinax quinquefasciatus specimens in the highlands of Santa Cruz, Galápagos, Ecuador. A = Rancho El Manzanillo (core locality). B – G = additional collection sites within the agricultural area (grey shading) of the island. 1.1) Larvae of the endemic diving beetle Thermonectus basillarus galapagoensis. 1.2) Adult of the introduced frog Scinax quinquefasciatus. Not to scale.
We captured adult and sub-adult individuals of S. quinquefasciatus using Visual (VES) and Acoustic Encounter Surveys (AES), as described by
For five consecutive days, we surveyed potential larval habitats, including seasonal and artificial ponds, for the presence of tadpoles and their potential aquatic predators. While we observed Anisoptera (dragonfly) larvae-known to be effective tadpole predators elsewhere-in some water bodies, they never co-occurred with S. quinquefasciatus tadpoles. Since we only observed the endemic diving beetle Thermonectus basillarus galapagoensis in the same water bodies, we chose this species as the target organism for the following predation experiments.
In order to (1) ensure that tadpole exposure to beetle predators was novel and (2) minimise ontogenetic and interpopulation differences in larval predation response (
Our experiments consisted of one treatment (predatory capacity) and two survival control experiments (tadpole survival and beetle larvae survival). For the predatory capacity experiments (N = 14), we introduced one food-deprived beetle larva into a plastic container with 20 tadpoles from our hatchery. For the tadpole survival experiments (N = 14), we transferred 20 tadpoles into one plastic container under the same conditions as the previous treatment, but without beetle larva. Finally, for the beetle survival experiments (N = 14), we added one food-deprived beetle larva to one plastic container under the same conditions, but without any tadpoles. Treatments and control experiments were run at the same time over the course of four days.
We monitored experiments and recorded data every two hours during each 12-hour period. Fourteen experiments were conducted from 12:00 am until 12:00 pm over four consecutive days (day 1 = four replicates, day 2 = three replicates, day 3 = four replicates and day 4 = three replicates), according to the number of tadpoles and beetles ready to be introduced into an experiment. We then measured mortality in tadpole survival experiments and both control treatments. Dead, but physically intact tadpoles with no signs of injury/attack were not included in the predation mortality totals. Individual beetle larvae and tadpoles were only used once.
To estimate the overall dietary composition of S. quinquefasciatus in the agricultural areas of Santa Cruz, we calculated two indices for each taxon found in the stomach contents: (1) numerical percentage of each prey consumed and (2) frequency of occurrence. Numerical percentage estimates the quantity of ingested prey items by dividing the total stomach contents from a specific order by the total number of prey items (according to the method of
Since we sampled frogs in the breeding season, we also hypothesised that the presence of prey in the stomach (vs. an empty stomach) would differ based on sex. We conducted an analysis of variance (ANOVA) to compare the amount of stomachs with prey items amongst males and females. We previously checked for homogeneity of variances amongst groups by using a Hartley’s Fmax test.
To determine if the predation-related mortality in tadpoles was time-dependent, we used a Generalised Estimating Equation (GEE). The GEE tests for subject (trial number) and within-subject (time-interval) effects in a repeated-measure experimental design, considering these as random factors. In our model, the response variable was cumulative predation-related mortality, while the explanatory variable was time interval. We only counted the experimental units in which the predator remained alive until the end. After running the model, we used a post-hoc Bonferroni test (α = 0.05) to determine which time intervals were responsible for significant differences in cumulative predation-related mortality.
We used another GEE test to determine if cumulative non-predation-related mortality was significantly different between tadpole survival (control) and predatory capacity experiments. Since mortality was not normally distributed, we chose a negative binomial distribution with a logarithmic link function for the model. Cumulative non-predation-related mortality was selected as the response variable, while experiment type (predatory capacity vs. tadpole survival) and time intervals were set as explanatory variables. Subject and within-subject effects were the same as in the previous analysis. All statistical analyses were performed with SPSS, version 22 (
Out of the 228 captured individuals (136 males, 79 females and 13 subadults), 54 had stomach content (34 males, 18 females–16 of which were gravid-and 2 sub-adults). Of those, 36 were collected from the core locality and 18 from the additional agricultural sites (Fig.
The 54 specimens found in S. quinquefasciatus stomachs consisted mostly of Lepidopterans (numerical percentage [NP]: 30%, frequency of occurrence [FO]: 61.11%), followed by Acarina (NP: 44.38%, FO: 5.56%). In total, 160 macroinvertebrates from 11 orders were identified as prey items (Table
Description of prey items identified in Scinax quinquefasciatus individuals, classified by order. Total number of prey items represents the total number of individual invertebrates in each order consumed by collected frogs (multiple individuals could be found in the same stomach). Frequency of consumption represents the number of stomachs in which a specific order was found. Numerical percentage is the number of prey items (per order) divided by the total number of prey items (n = 160). Frequency of occurrence represents the number of stomachs that contained a specific taxon (frequency of consumption) divided by the total number of stomachs with food content (n = 54).
Order | Total number of prey items | Frequency of consumption | Numerical percentage | Frequency of occurrence |
Lepidoptera | 48 | 33 | 30 | 61.11 |
Acarina | 71 | 3 | 44.38 | 5.56 |
Araneae | 6 | 5 | 3.75 | 9.26 |
Blattodea | 1 | 1 | 0.63 | 1.85 |
Neuroptera | 2 | 2 | 1.25 | 3.70 |
Hymenoptera | 9 | 6 | 5.63 | 11.11 |
Orthoptera | 5 | 5 | 3.13 | 9.26 |
Hemiptera | 2 | 2 | 1.25 | 3.70 |
Isopoda | 9 | 2 | 5.63 | 3.70 |
Coleoptera | 5 | 4 | 3.13 | 7.41 |
Dyptera | 2 | 1 | 1.25 | 1.85 |
Nine out of the fourteen predator capacity experiments were included in the final model, since we only used the trials in which the beetle predator survived the entire experiment duration (4 days). Cumulative predation-related mortality significantly decreased over time (Wald Chi-Square = 125.92, df = 5, p = 0.001, Fig.
Results of the Bonferroni post-hoc test (α = 0.05), describing differences between time intervals in the cumulative number of Scinax quinquefasciatus tadpoles predated on by the beetle larvae Thermonectus basillarus galapagoensis during the execution of 12-hour predator capacity experiments (N = 9). Asterisks indicate significant differences between mean values of predated tadpoles with a 95% confidence level.
Time intervals | Cumulative # of predated tadpoles | Difference in predated tadpoles between time intervals | Significance | |
---|---|---|---|---|
(mean value across trials) | ||||
1st | 4.89 | 0–2 h vs. 2–4 h | -2.44 | |
0 h – 2 h | ||||
2nd | 7.33 | 0–2 h vs. 4–6 h | -4.89 | * |
2 h – 4 h | ||||
3rd | 9.78 | 0–2 h vs. 6–8 h | -5.11 | * |
4 h – 6 h | ||||
4th | 10 | 0–2 h vs. 8–10 h | -6 | * |
6 h – 8 h | ||||
5th | 10.89 | 0–2 h vs. 10–12 h | -6.67 | * |
8 h – 10 h | ||||
6th | 11.56 | |||
10 h – 12 h |
Boxplots depicting comparisons of cumulative mortality rates in predator-prey experiments over time (predator = Thermonectus basillarus galapagoensis larvae; prey = Scinax quinquefasciatus tadpoles) A cumulative non-predation-related mortality of tadpoles in predatory capacity experiments B cumulative predation-related mortality of tadpoles in predatory capacity experiments C cumulative larvae mortality in survival control experiments D cumulative non-predation-related mortality in tadpole survival experiments. Empty circles outside boxplots represent outlier values (1.5 times higher than box height). Asterisks represent extreme outlier values (3 times higher than box height).
There was no significant difference in tadpole mortality between the non-predation deaths that occurred in the predatory capacity experiments versus those that occurred without the presence of a predator (Wald Chi-Square = 1.61, df = 1, p = 0.20, Fig.
One way to determine the trophic effect of an introduced species is to carry out a stomach-content analysis. In this study, Scinax quinquefasciatus in the highlands of Santa Cruz are shown to have a diet that consists mostly of Lepidopterans, followed by Acarina (Table
This apparent preference for Lepidopterans is likely due to their availability in the environment. Anurans are typically diet generalists (
Sex did not influence the likelihood that a frog’s stomach contained prey: 22.8% of females and 25% of males had prey items in their stomachs. This may be related to the fact that we sampled during the S. quinquefasciatus mating season (rainy season, December-May), when both sexes are expending energy on breeding. In many frog species, males invest more energy in behaviour related to reproduction than foraging during the breeding period (
Even though most studies on introduced species focus on their effect on native prey communities (
If the feeding behaviour of T. b. galapagoensis larvae were selective (i.e. showing a strong preference for tadpoles) and/or if their populations were highly abundant, this endemic beetle could serve as a biological control for S. quinquefasciatus. However, our predator-prey experiments showed that the endemic beetle larvae stopped feeding before the tadpole resource was depleted, predating on a total mean value of 11.6 tadpoles after the 12-hour period. This ‘feeding saturation’ has direct implications for S. quinquefasciatus population control, suggesting that the predator-to-prey ratio is too skewed for the beetle to diminish populations of the invasive frog. This mirrors our observations in nature: there were far more tadpoles than beetle larvae in each surveyed water body on Santa Cruz. T. b. galapagoensis larvae presumably preyed on other animals prior to the arrival of S. quinquefasciatus to the island, but our finding also suggests that the beetle larvae have not developed a tadpole specialisation-decreasing its potential as a natural control agent. A recent study showed that an introduced bird, the smooth-billed ani (Crotophaga ani), feeds on S. quinquefasciatus adults in Galápagos, but predation rates are also too low to have an effect on the frog’s population size (
Population dynamics of introduced and invasive species depend on biological parameters (e.g. fecundity, growth, survival;
Due to rapid development and the increasing human population, Santa Cruz is prone to invasive species events. Scinax quinquefasciatus is the first successfully invasive amphibian on the island; furthering our understanding of its ecological effect(s) is crucial for management, especially in such a fragile and unique ecosystem. As reproduction for both frogs and beetles in the highlands is apparently restricted to water sources provided in the rainy season and/or anthropogenic structures, we recommend that long- term research be conducted to investigate the frog’s ontogeny, especially in relation to beetle presence/absence.
This diet composition study was limited to higher taxonomic identification levels due to the nature of digested stomach contents (exoskeletons, wings etc.) and economic constraints that prevented us from testing with molecular methods. Further research should address the selection of native, endemic and introduced prey item ratios using DNA-metabarcoding approaches.
Our findings strongly suggest that Scinax quinquefasciatus population growth is likely to remain stable or increase on Santa Cruz. The dietary preferences and predation rates by natural predators on this introduced frog should be taken into account when considering management strategies in the Galápagos Islands.
This project was supported by the Charles Darwin Foundation, Rancho El Manzanillo, the Dean of Research at Escuela Superior Politécnica del Litoral and the Galápagos National Park Directorate (GNPD, permit PC-35-17). This study was financially supported by the Basler Stiftung für Biologische Forschung and Galápagos Conservancy. We also thank Jacqueline Rodríguez at CDF for her continuous support in laboratory training, the Zoology Museum at the Pontifical Catholic University of Ecuador (QCAZ) for field training and support, the El Manzanillo family for their hospitality and Rebecca M. Brunner for professional edits to the manuscript. R. Ernst would particularly like to thank Marcelo Loyola and Hilla for their support during field work. Thanks to Rolf Sievers for providing the long-term weather data and to Clare Peabody for compiling these. The International Atomic Energy Agency is grateful for the support provided to its Environment Laboratories by the Government of the Principality of Monaco. This publication is contribution number 2227 of the Charles Darwin Foundation for the Galápagos Islands.