Corresponding author: James W.E. Dickey ( jdickey03@qub.ac.uk ) Academic editor: Tim Blackburn
© 2018 James W.E. Dickey, Ross N. Cuthbert, Michael Rea, Ciaran Laverty, Kate Crane, Josie South, Elizabeta Briski, Xuexiu Chang, Neil E. Coughlan, Hugh J. MacIsaac, Anthony Ricciardi, Gillian E. Riddell, Meng Xu, Jaimie T.A. Dick.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Dickey JWE, Cuthbert RN, Rea M, Laverty C, Crane K, South J, Briski E, Chang X, Coughlan NE, MacIsaac HJ, Ricciardi A, Riddell GE, Xu M, Dick JTA (2018) Assessing the relative potential ecological impacts and invasion risks of emerging and future invasive alien species. NeoBiota 40: 1-24. https://doi.org/10.3897/neobiota.40.28519
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Invasive alien species (IAS) cause myriad negative impacts, such as ecosystem disruption, human, animal and plant health issues, economic damage and species extinctions. There are many sources of emerging and future IAS, such as the poorly regulated international pet trade. However, we lack methodologies to predict the likely ecological impacts and invasion risks of such IAS which have little or no informative invasion history. This study develops the Relative Impact Potential (RIP) metric, a new measure of ecological impact that incorporates per capita functional responses (FRs) and proxies for numerical responses (NRs) associated with emerging invaders. Further, as propagule pressure is a determinant of invasion risk, we combine the new measure of Pet Propagule Pressure (PPP) with RIP to arrive at a second novel metric, Relative Invasion Risk (RIR). We present methods to calculate these metrics and to display the outputs on intuitive bi- and triplots. We apply RIP/RIR to assess the potential ecological impacts and invasion risks of four commonly traded pet turtles that represent emerging IAS: Trachemys scripta scripta, the yellow-bellied slider; T. s. troostii, the Cumberland slider; Sternotherus odoratus, the common musk turtle; and Kinosternon subrubrum, the Eastern mud turtle. The high maximum feeding rate and high attack rate of T. s. scripta, combined with its numerical response proxies of lifespan and fecundity, gave it the highest impact potential. It was also the second most readily available according to our UK surveys, indicating a high invasion risk. Despite having the lowest maximum feeding rate and attack rate, S. odoratus has a high invasion risk due to high availability and we highlight this species as requiring monitoring. The RIP/RIR metrics offer two universally applicable methods to assess potential impacts and risks associated with emerging and future invaders in the pet trade and other sources of future IAS. These metrics highlight T. s. scripta as having high impact and invasion risk, corroborating its position on the EU list of 49 IAS of Union Concern. This suggests our methodology and metrics have great potential to direct future IAS policy decisions and management. This, however, relies on collation and generation of new data on alien species functional responses, numerical responses and their proxies, and imaginative measures of propagule pressure.
ecological impacts, functional response, invasive alien species, numerical response, pet propagule pressure, relative impact potential, relative invasion risk, risk assessment
Invasive alien species (IAS), i.e. those introduced to areas outside their native range (which may or may not then have impact; see
Comparative functional responses (CFRs) have been successful in characterising damaging IAS and have proven predictive for those without invasion impact history (
RIP might prove particularly valuable for the study of IAS emerging from the pet trade, with global trade of freshwater turtles in particular a pressing problem (
Here, we utilise the RIP metric and biplots of
Trachemys scripta scripta, T. s. troostii, Sternotherus odoratus and Kinosternon subrubrum originate from North America and are sold around the world (
T. s. scripta and T. s. troostii can live for 36 years (
The four turtle species were provided by Maidenhead Aquatics, Northern Ireland (carapace lengths 35–50 mm; mixed sexes) and maintained in holding tanks containing a water heater (150W Eheim thermocontrol, Germany) and water cooler to ensure water temperature was maintained at 16 °C. Two basking platforms and basking lights created a hot spot of 23 °C, controlled by an automatic temperature controller (Habistat Classic, England). Substrate (0.8 mm grain size) was added to the bottom 30 mm of each holding tank (JBL, Germany). Nine individuals of each species were acquired for each experimental batch and each species received its own holding tank and was quarantined for one week prior to experiments. During this period, no illness or deaths were recorded and the animals were fed daily with commercial floating turtle food (JBL, Germany). Before experimental FR trials, all turtles were starved for 24 hours to standardise hunger levels. Focal prey, the amphipod crustacean Gammarus pulex (15–17mm body length; unparasitised), upon which all turtle species were observed to feed readily and represents a general prey item, were collected from the Minnowburn River, N. Ireland (N54.546, W5.594) two days before the experiments and acclimatised to the experimental temperature.
Experiments were performed 22 February–27 April 2016. Experimental tanks (250 mm × 120 mm × 90 mm) with 30 mm of substrate at 16 °C were supplied with prey 15 minutes prior to the turtles being introduced. Prey densities were 2, 4, 8, 16, 32, 64, 128, 256 (n = 6 per experimental group). For each turtle species, individuals were randomly selected and assigned to a random prey density and allowed to feed for thirty minutes. Controls were performed for each prey density (n = 3 each) with the same experimental conditions but in the absence of turtle predators, to quantify prey mortality for any other reasons.
Data were analysed using R version 3.2.3. (R Core Team 2015). Logistic regression of the proportion of prey killed as a function of prey density was used to discern functional response types (see
Ne=N0 (1–exp (a (Neh–T))) (1)
where Ne is the number of prey eaten, N0 is the initial density of prey, h is the handling time, a is the attack constant and T is the total experimental period. Model fitting used the Lambert W function (
Relative Impact Potential (RIP) was originally developed using population abundance/density/biomass as a proxy for the consumer numerical response (NR:
(1) Lifespan (L). With temperatures in many temperate regions high enough for turtles to survive in the wild for many years, but as yet too low to facilitate reproduction (
IPL = FR × L (2)
where FR is the functional response (estimated maximum feeding rate, 1/h, from equation 1) and L is maximum lifespan (Table
Numerical response proxies of lifespan, fecundity and lifetime fecundity, plus Pet Propagule Pressure (PPP; see Text and Table
Turtle | Lifespan (L) (maximum years) | Ref. | Fecundity (F) (eggs per year) | Ref. | Lifetime fecundity (LxF) | Pet Prop. Press. (PPPNI) | Pet Prop. Press. (PPPGB) |
---|---|---|---|---|---|---|---|
T. s. scripta | 36 |
|
115 |
|
4140 | 0.05 | 0.1 |
T. s. troostii | 36 |
|
115 |
|
4140 | 0.00 | 0.05 |
S. odoratus | 30 |
|
36 |
|
1080 | 0.30 | 0.39 |
K. subrubrum | 46 | Frazer et al. 1991 | 18 |
|
828 | 0.05 | 0.02 |
(2) Fecundity (F). Where reproduction of the turtles occurs or may occur in future, fecundity offers another proxy multiplier of per capita effects, since reproductive output is clearly an element of the true numerical response. Thus, Impact Potential utilising fecundity data (IPF) is:
IPF = FR × F (3)
where FR is as above and F is the product of clutch size and number of clutches per annum (Table
(3) Lifespan fecundity (LF). Where suitable data are available, a third proxy for the numerical response may be constructed as the product of maximum lifespan and fecundity, that is lifetime fecundity (LF), as this captures both reproductive output per bout and over time and thus Impact Potential is:
IPLF = FR × LF (4)
The RIP calculations of
IPL = a × L (5)
and with fecundity data is:
IPF = a × F (6)
and with lifetime fecundity:
IPLF = a × LF (7)
In addition, to enter the propagule pressure argument to measure overall invasion risk, we qualify each IP equation with Pet Propagule Pressure (PPP). We propose two PPP methods. First, we quantified the availability of the four species on a local (i.e. Northern Ireland, NI) level via a survey of twenty pet shops between the 31 January and 1 March 2017 (Suppl. material 1: Table S1; PPP values as per Table
PPP (NI) = Np/Tp (8)
where Pet Propagule Pressure (Northern Ireland, NI) is a function of the proportional availability of each species across pet shops (Np) and the total number of pet shops surveyed (Tp).
The second version of PPP involved a survey of online classified advertisements (Suppl. material 2: Table S2; PPP values as per Table
PPP (GB) = Na/Ta (9)
where PPP (Great Britain, GB) is the proportional availability of the four species based on online classified advertisements (Na) and the total number of online advertisements surveyed (Ta).
By incorporating these two measures of propagule pressure, the Impact Potential (IP) equations (equations 2–7) can incorporate both risk of introduction and its ecological consequences to become Invasion Risk (IR):
IRL = FR × L × PPP (10)
IRF = FR × F × PPP (11)
IRLF = FR × LF × PPP (12)
IRL = a × L × PPP (13)
IRF = a × F × PPP (14)
IRLF = a × LF × PPP (15)
We present biplots to illustrate Relative Impact Potential (equations 2–7) and triplots for Relative Invasion Risk (equations 10–15) of the four turtle species to give visual representations of relative ecological impact and invasion risk (see Suppl. material 3, 4 for R scripts, and Suppl. material 5 for associated .csv file).
Prey survival in control treatments was 98–100%, therefore mortality during FR experiments was attributed to predation, which was also directly observed. Type II functional responses were observed for all turtle species (Table
First order terms calculated from logistic regression to denote functional response type across all predator treatments. The significant negative first order term values across all four turtles indicate Type II functional responses for each predator. Handling time (h), maximum feeding rate (1/h) and attack rate (a) parameter mean estimates (bootstrapped, n = 30), derived using Rogers’ random predator equation (eqn 1).
Predator | First term, P | Handlingtime, h | Maximum feeding rate, 1/h (G. pulex consumed per 30 mins) | Attack rate, a |
---|---|---|---|---|
T. s. scripta | -0.011, <0.001 | 0.027 | 37.036 | 2.678 |
T. s. troostii | -0.011, <0.001 | 0.028 | 35.405 | 2.038 |
S. odoratus | -0.011, <0.001 | 0.039 | 25.468 | 1.847 |
K. subrubrum | -0.012, <0.001 | 0.037 | 27.142 | 2.314 |
Functional responses of T. s. scripta, T. s. troostii, S. odoratus and K. subrubrum towards G. pulex prey. Values are mean ±SE.
Parameter estimates (±SE) of: a handling time h b maximum feeding rate 1/h c attack rate a, for bootstrapped (n = 30) Type II functional response curves of T. s. scripta (Tss), T. s. troostii (Tst), S. odoratus (So) and K. subrubrum (Ks) towards G. pulex prey.
The numerical response proxy values are given in Table
Impact Potential (IP) and Invasion Risk (IR) calculations, whereby: IP(FR) = Maximum feeding rate (FR) × NRproxy i.e. lifespan (L), fecundity (F) or lifetime fecundity (LF); IP(a) = Attack rate (a) × NRproxy; IR(FR) = IP(FR) × Pet Propagule Pressure (PPP); IR(a) = IP(a) × PPP. PPPNI (Northern Ireland) is a function of the proportional availability of each species across pet shops and the total number of pet shops surveyed and PPPGB (Great Britain) is the proportional availability of the four species based on online advertisements and the total number of advertisements surveyed.
IPL(FR) | IPF(FR) | IPLF(FR) | IPL(a) | IPF(a) | IPLF(a) | |
T. s. scripta | 1,333.30 | 4,259.14 | 153,329.04 | 96.41 | 307.97 | 11,086.92 |
T. s. troostii | 1,274.76 | 4,072.15 | 146,597.40 | 73.37 | 234.37 | 8,437.32 |
S. odoratus | 764.04 | 916.85 | 27,505.44 | 55.41 | 66.49 | 1,994.76 |
K. subrubrum | 1,248.53 | 488.56 | 22,473.58 | 106.44 | 41.65 | 1,915.99 |
Using PPPNI | IRL(FR) | IRF(FR) | IRLF(FR) | IRL(a) | IRF(a) | IRLF(a) |
T. s. scripta | 66.66 | 212.96 | 7,666.45 | 4.82 | 15.40 | 554.35 |
T. s. troostii | 0 | 0 | 0 | 0 | 0 | 0 |
S. odoratus | 229.21 | 275.05 | 8,251.63 | 16.62 | 19.95 | 598.43 |
K. subrubrum | 62.43 | 24.43 | 1,123.68 | 5.32 | 2.08 | 95.80 |
Using PPGB | IRL(FR) | IRF(FR) | IRLF(FR) | IRL(a) | IRF(a) | IRLF(a) |
T. s. scripta | 133.33 | 425.91 | 15,332.90 | 9.64 | 30.80 | 1,108.69 |
T. s. troostii | 63.74 | 203.61 | 7,329.87 | 3.67 | 11.72 | 421.87 |
S. odoratus | 297.98 | 357.57 | 10,727.12 | 21.61 | 25.93 | 777.96 |
K. subrubrum | 24.97 | 9.77 | 449.47 | 2.13 | 0.83 | 38.32 |
Biplots showing Relative Impact Potential of T. s. scripta, T. s. troostii, S. odoratus and K. subrubrum towards G. pulex prey. Impact potential calculated as a product of maximum feeding rate and lifespan (a), fecundity (b) and lifetime fecundity (c); then attack rate and lifespan (d), fecundity (e) and lifetime fecundity (f). Impact increases from bottom left to top right.
Pet Propagule Pressure (PPP) of each species was similar in both the Northern Ireland (NI) and Great Britain (GB) surveys, with respective orders of S. odoratus > T. s. scripta = K. subrubrum > T. s. troostii and S. odoratus > T. s. scripta > T. s. troostii > K. subrubrum (see Table
For all six of the NI Relative Invasion Risk (RIR) triplots, values were highest for S. odoratus, with the order S. odoratus > T. s. scripta > K. subrubrum > T. s. troostii across all derivations of RIR (equations 10–15; Table
Triplots showing Relative Invasion Risk of T. s. scripta, T. s. troostii, S. odoratus and K. subrubrum in a Northern Irish context. Invasion Risk calculated as a product of maximum feeding rate and Pet Propagule Pressure (PPP) with lifespan (a), with fecundity (b) and with lifetime fecundity (c); then attack rate and PPP with lifespan (d), with fecundity (e) and with lifetime fecundity (f). PPP for each species calculated by surveying 20 local pet shops and determining proportions of each species sold. Invasion Risk increases from bottom left to top right of each plot, with species ranked 1–4.
Triplots showing Relative Invasion Risk of T. s. scripta, T. s. troostii, S. odoratus and K. subrubrum in a Great British context. Invasion Risk is calculated as a product of maximum feeding rate, lifespan and Pet Propagule Pressure (PPP) (a), with fecundity (b) and with lifetime fecundity (c); then attack rate, lifespan and PPP (d), with fecundity (e) and with lifetime fecundity (f). PPP for each species calculated by surveying classified advertisements online and finding what proportion were selling the species in question. Invasion Risk increases from bottom left to top right of each plot, with species ranked 1–4.
Invasion ecology has long lacked a unifying methodology that predicts ecological impacts and overall invasion risks of invasive species (
While FR analyses have been used mainly to determine the impacts of alien predators (see
The Impact Potential (IP) and Invasion Risk (IR) metrics, plus our illustrative bi- and triplots giving Relative IP and Relative IR, retain the benefits of CFR, but bolster these per capita measures with proxies for the numerical response (NR), that is, the consumer population response. Emerging invaders may lack NR data and have no data for their abundances/densities/biomass in potential invasion regions. With these latter NR proxies not available, we hence require alternatives and use lifespan, fecundity and lifetime fecundity as comparative multipliers of per capita effects. The resulting impact potentials were subsequently combined with values for our two versions of Pet Propagule Pressure (PPP) to give Invasion Risk (IR), which assesses which species are currently the most likely candidates for introduction, combined with potential impact. Using these approaches, we determined that T. s. scripta and T. s. troostii have the highest RIP, but the more commonly traded S. odoratus has the greatest RIR and thus should be of great concern. Our approach illustrates the potential use of combinatorial metrics to guide policy and intervention and exploits inherent life-history traits of invaders with their feeding impacts and their likelihood of introduction.
The use of maximum lifespan as a numerical response proxy offers a readily available multiplier of per capita effects. With reproduction by these turtles not yet possible in most temperate regions, the longer the species survive in the wild, the greater the ecological impact that will accrue. One caveat is the combination of unfamiliar climate, flora and fauna, combined with invader naiveté, which could alter the estimations of lifespan should these species be released into the wild. A caveat exists for lifetime fecundity too, as fecundity does not remain constant over the course of a lifetime. However, as our metric is comparative and all species should be equally affected, such reductions may not affect predictions of relative ecological impact. Here, using lifespan, we find that T. s. scripta and T. s. troostii had the highest impact potentials on the maximum feeding rate biplot, while K. subrubrum and T. s. scripta had the highest and second highest impacts on the attack rate biplot. However, as illustrated by
Our second NR proxy, fecundity, defined as the number of offspring born over a given period of time (
Our novel Relative Invasion Risk (RIR) triplots used Pet Propagule Pressure (PPP) to give a third dimension for invasion risk assessment. The first PPP calculations are based on a survey of 20 pet shops, ranging from small independent traders to UK-wide chains across Northern Ireland (NI). This offered vital data on which species are currently being sold in the NI pet trade and, by proxy, which species are likely candidates for future release and escape (
The second measure of PPP was derived from online classified advertisements for unwanted pet turtles in GB and showed a similar result to that of the NI pet shop survey, with S. odoratus again found to be much more available than the other three turtle species. S. odoratus had the highest RIR for the lifespan calculations, but T. s. scripta, found to be twice as common in GB as it was in NI, had the highest RIR when fecundity and lifetime fecundity were taken into account. Trachemys scripta troostii was also more available than in the prior NI survey and, as a result, poses a greater risk in GB. Monitoring needs to occur in the future as changes in supply and demand will lead to the study species shifting their relative availabilities (
Assessing potential for long-term impact requires information on which species will likely establish. Temperature is crucial for embryonic development and offspring phenotype (
The Relative Impact Potential metric, in its original form (
Using our impact potential metric, the turtle warranting management priority is Trachemys scripta scripta. While uncertainty surrounds the ability and timeframe of all four turtles to adapt to more temperate climates, the potential for high relative clutch size, high feeding rate on a locally abundant prey, large body size and aggression to ward off potential competitors and predators, mean the likelihood of establishment and ecological impact of T. s. scripta is high. However, the widespread availability of S. odoratus, combined with a wide range of habitats, TSDII reproduction and the same population destabilising Type II functional response as T. s. scripta, mean the Relative Invasion Risk (RIR) triplots highlight this as a species that would otherwise have been overlooked solely on the basis of Comparative Functional Response (CFR) and Relative Impact Potential (RIP) studies.
With the pet trade likely to continue to be the main driver of any turtle species arriving, either by release or escape, knowing the species being imported into local pet shops and being sold by owners, is of vital importance. For that reason, the RIR triplots, which combine IP data with a measure of propagule pressure (i.e. PPP), offer an informative way of prioritising potential invasive species for management interventions. Going forward, there is vital need for regular surveys and for assessing the potential impact and risks of newly arrived specimens. With some turtle species encountered in both PPP surveys that were not investigated in this study, what we have provided is an avenue for further research and a starting point for the compilation of a user-friendly database of potential pet shop invaders to help decision-makers worldwide to assess IAS impact and invasion risk. More broadly, in terms of future research and management directions, there is a need for compilation of data on alien species functional responses, that is, existing and new data similar to those collated for biocontrol agents. We also need better estimates of numerical responses, as this latter measure is the gold standard for providing the total response and hence impact of invaders (see
JTAD, MR, CL, KC, JS and GR conceived the study, performed the experiments and produced initial results; JWED and RNC conducted statistical analyses; JWED, RNC and JTAD prepared the initial manuscript, led by JWED. AR, HJM, NEC, MX, XC and EB contributed vital input to the development of concepts. All contributed to production of final manuscript and gave approval for publication. JWED supported by Inland Fisheries Ireland (IFI), RNC by Department for the Economy Northern Ireland, NEC by Environmental Protection Agency (EPA), EB by Alexander von Humboldt Sofja Kovalevskaja Award and HJM and TR by NSERC Discovery grants. Thanks also to the Natural Environment Research Council (NERC). The authors would like to give credit to Pablo García-Díaz for insightful, constructive comments that improved the quality of the manuscript.