A peer-reviewed open-access journal

NeoBiota 87: 191—212 (2023)

doi: 10.3897/neobiota.87. 108457 RESEARCH ARTICLE &) NeoBiota

https:/ / neobi ota. pen soft. net Advancing research on alien species and biological invasions

Predation risk by largemouth bass modulates feeding
functional responses of native and non-native crayfish

Larissa Faria'’, Jean R. S. Vitule', Julian D. Olden?

| Laboratorio de Ecologia e Conservacaéo, Departamento de Engenharia Ambiental, Setor de Tecnologia, Uni-
versidade Federal do Parand, Curitiba, 81531-980, Paranda, Brazil 2 School of Aquatic and Fishery Sciences,
University of Washington, Seattle, 98195, Washington, USA

Corresponding author: Larissa Faria (larissa.faria@fulbrightmail.org)

Academic editor: Jaimie T.A. Dick | Received 22 June 2023 | Accepted 1 August 2023 | Published 4 October 2023

Citation: Faria L, Vitule JRS, Olden JD (2023) Predation risk by largemouth bass modulates feeding functional
responses of native and non-native crayfish. NeoBiota 87: 191-212. https://doi.org/10.3897/neobiota.87.108457

Abstract

Context-dependency is prevalent in nature, challenging our understanding and prediction of the potential
ecological impacts of non-native species (NNS). The presence of a top predator, for example, can modify
the foraging behaviour of an intermediate consumer, by means of non-consumptive effects. This raises the
question of whether the fear of predation might modulate consumption rates of NNS, thus shaping the
magnitude of ecological impacts. Here, we quantified the functional feeding responses of three non-native
crayfish species — red swamp crayfish Procambarus clarkii, rusty crayfish Faxonius rusticus and virile crayfish
Faxonius virilis — compared to the native analogue signal crayfish Pacifastacus leniusculus, considering the
predation risk imposed by a top fish predator, the globally invasive largemouth bass Micropterus salmoides.
We applied the comparative functional response (FR) approach using snails as prey and exposing crayfish
to water containing predator and dietary chemical cues or not. All crayfish species presented a destabilising
Type I FR, regardless of the presence of chemical cues. Predation risk resulted in significantly longer han-
dling times or lower attack rates in non-native crayfish; however, no significant differences were observed
in signal crayfish. We estimated per capita impacts for each species using the functional response ratio
(FRR; attack rate divided by handling time). The FRR metric was lower for all crayfish species when ex-
posed to predation risk. Rusty crayfish demonstrated the highest FRR in the absence of chemical cues, fol-
lowed by signal crayfish, virile crayfish and red swamp crayfish. By contrast, the FRR of signal crayfish was
nearly twice that of rusty crayfish and virile crayfish and ten times greater than red swamp crayfish when
chemical cues were present. The latter result agrees with the well-recognised ecological impacts of signal
crayfish throughout its globally-introduced range. This study demonstrates the importance of consider-
ing the non-consumptive effects of predators when quantifying the ecological impacts of intermediate
non-native consumers on prey. The direction and magnitude of the modulating effects of predators have

clear implications for our understanding of NNS impacts and the prioritisation of management actions.

Copyright Larissa Faria et al. 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.

192 Larissa Faria et al. / NeoBiota 87: 191-212 (2023)

Keywords

ecology of fear, decapods, higher-order predator, kairomones, trait-mediated indirect effects

Introduction

Non-native species (NNS) are a primary driver of environmental change, with negative
impacts on individuals to entire ecosystems and severely disrupting important services
provided by nature (Ricciardi et al. 2013). Economic burdens are also concerning,
with estimated costs to prevent and control NNS impacts exceeding a hundred million
dollars per year globally (Pysek et al. 2020; Diagne et al. 2021), possibly increasing in
the future (Ahmed et al. 2022). Management and policy strategies rely on identify-
ing the most impactful species to help target prevention efforts and allocate limited
resources to control or eradicate burgeoning populations. Still, this task is challenging
due to variations in NNS impacts, based on ecosystem, geographical location, time
since establishment and individual values (Zavorka et al. 2018; Santos et al. 2019).
Considering the increasing rate of invasions, comparative studies of the context-de-
pendency of NNS impacts will help prioritise which species should be managed in the
future (Lockwood et al. 2007; Dick et al. 2017a; Seebens et al. 2017).

Quantifying per capita effects of NNS remains central to most frameworks evalu-
ating their ecological impacts (Parker et al. 1999; Kumschick et al. 2015; Griffen et
al. 2020). Given the challenges of estimating per capita effects, focus has shifted to
the use of experiments to quantify resource consumption rates as a proxy (Dick et al.
2017b). Non-native consumers often consume resources more efhciently than their
native counterparts (Funk and Vitousek 2007; Salo et al. 2007; Paolucci et al. 2013),
making comparative rates of consumption between native and NNS a useful currency
to anticipate negative impacts from species introductions (Dick et al. 2014).

The fundamental ecological concept of functional responses (FR) — resource use
as a function of availability — provides a measurable estimate of the per capita effect
of a consumer on a given resource (Solomon 1949; Holling 1959; Dick et al. 2014).
Type I FR describes a linear relationship between consumption and resource availabil-
ity, typical of filter-feeding species (Jeschke et al. 2004). Type II FRs are destabilising
due to high consumption rates at low resource densities, while Type III FRs promote
stabilising effects due to low consumption rates when resources are scarce (Oaten and
Murdoch 1975). The utility of FRs lies in comparing the maximum consumption rate
between NNS and native trophic analogues in the same environmental context (Dick
et al. 2014, 2017a), making this approach increasingly applied to quantify and predict
ecological impacts of NNS (Faria et al. 2023).

The comparative FR approach enables the evaluation of per capita effects in dif-
ferent contexts, allowing more realistic and practical impact assessments (Dick et al.
2017a; Dickey et al. 2020). Despite this, investigations involving trophic levels be-
yond the focal consumer-resource interaction remain limited (e.g. Barrios-O’Neill
et al. (2014); Paterson et al. (2015)). Foraging behaviour and consumption rates of

Predation risk modulates functional responses of non-native crayfish 193

consumers are sensitive to the presence of higher-order predators, which invoke trade-
offs in resource acquisition versus mortality risk by predation (Lima and Dill 1990;
Brown and Kotler 2004). Fear of predation can shape entire ecosystems through trait-
mediated indirect effects (TMIEs) on prey traits, such as behaviour and physiology
(Werner and Peacor 2003; Peckarsky et al. 2008; Laundré et al. 2010). In some cir-
cumstances, the non-consumptive effects of predators are thought to be as strong as di-
rect consumption for population dynamics, leading to greater system stability (Brown
et al. 1999) or even causing trophic cascades (Schmitz et al. 2004; Preisser et al. 2005;
Peckarsky et al. 2008).

Trait-mediated indirect effects are particularly prominent in freshwater ecosys-
tems, likely due to the effective transmission of visual and chemical cues indicating
predator presence (Preisser et al. 2005). For example, the presence of largemouth
bass (Micropterus salmoides) altered the foraging behaviour and habitat use of bluegill
sunfish (Lepomis macrochirus) prey leading to cascading changes in zooplankton com-
munities (Turner and Mittelbach 1990). In another example, rusty crayfish (Faxonius
rusticus) displayed greater consumption of macrophytes when exposed to chemical
cues from largemouth bass, suggesting a robust effect of predation risk on crayfish
foraging behaviour (Wood et al. 2018).

Despite the strong effects of non-consumptive effects in shaping communities, they
are relatively underexplored compared to consumptive effects in the context of quan-
tifying NNS impacts. Applying the comparative FR approach, we aim to test whether
the non-consumptive effects of a top predator, the non-native largemouth bass, medi-
ate the consumptive impacts of three non-native crayfish species (Procambarus clarkii,
Faxonius virilis and E rusticus) and a native analogue (Pacifastacus leniusculus) preying
on snails. We hypothesise that non-consumptive effects of a top predator will reduce
consumption rates of all crayfish species, but to a lesser extent for non-native crayfish
with a shorter evolutionary history with the predator. The differential response to pre-
dation risk imposed by the largemouth bass may explain the expected higher per capita
effects of non-native consumers compared to native analogue species.

Methods

Study system

Our study system is a three-level food chain composed by a non-native top predator,
the largemouth bass, an intermediate consumer represented by non-native or native
crayfish (Table 1) and native freshwater snails (Gastropoda, Planorbidae) as the basal
resource. Crayfish are known to be highly sensitive to different chemical cues such as
predator odour, dietary and alarm cues (Beattie and Moore 2018; Wood et al. 2018;
Wood and Moore 2020a, b) and these cues show utility in assessing TMIEs (Paterson
et al. 2013). Thus, we used a combination of predator and dietary chemical cues to
provide the biological context of predation risk in our comparative FR approach.

194 Larissa Faria et al. / NeoBiota 87: 191—212 (2023)

Table |. Crayfish species examined in this study, including scientific and common names, history of in-
troduction in the Pacific Northwest region, sampled populations (coordinates) and carapace length (CL)

and mass, presented as the mean (SD), of the individuals used in the experiments.

Crayfish Scientific Commonname_ Estimated time Sampled population CL Mass
name of introduction (mm) (g)

Pacifastacus Signal crayfish Native Skykomish River, WA 50.2 36.9

leniusculus (47.8482, -121.8403) (4.3) (10.3)

Procambarus Red swamp 1970s Pine Lake, WA 5300 wy FS 9:7

clarkii crayfish (47.5907, -122.0389) (5.7) (13.0)

Faxonius Rusty crayfish 2005 Magone Lake, OR 41.1 259

rusticus (44.5486, -118.9119) (3.1) (5.3)

x Faxonius Virile crayfish 1980s Rattlesnake Lake, WA 46.0 32.6

; virilis (47.4308, -121.7715) (3.5) (7.6)

The geographic context of the study is the Pacific Northwest region of the US,
where all species were sourced (Table 1). The apex predator largemouth bass has a
native distribution that extends from north-eastern US to northern Mexico (Brown
et al. 2009), with a long history of intentional introduction for recreational fishing
in many regions of the US and the world, including the study region dating back
to the beginning of the 20" century (Stein 1970). The non-native crayfish used in
this study have a varied history of introductions in the region (Table 1) and are
amongst the most widespread and harmful invasive crayfish species in the world
(Twardochleb et al. 2013). Signal crayfish is the most widely distributed native
crayfish species in the region (Larson and Olden 2011) and also highly invasive
outside its native range (Usio et al. 2007; Twardochleb et al. 2013; VaefSen and
Hollert 2015). All crayfish species used in this study are omnivorous and noctur-
nal, presenting maximum feeding or growth rates between 20 and 30 °C (Crandall
and Buhay 2008; Westhoff and Rosenberger 2016; Rodriguez Valido et al. 2021;
Ruokonen and Karjalainen 2022).

Predation risk modulates functional responses of non-native crayfish 195

Animal collection and maintenance

Largemouth bass were collected using electrofishing from Lake Washington, WA
(47.6469, -122.2991) in October 2022. A total of 33 fish were captured and trans-
ported to the lab facility at the University of Washington, where they were maintained
in a circular tank of approximately 800 | without shelter (hereafter stimulus tank), aer-
ated and continuously filled with water from Lake Washington, in an open circulation
system (mean total length = 194 mm, SD = 53). Fish were acclimatised to the stimulus
tank for two weeks before the beginning of the trials.

A total of 433 crayfish were sampled using baited traps deployed overnight from
lakes in Washington and Oregon States in October 2022 (Table 1). Crayfish were kept
in tanks of 256 | separated by species, with a maximum stock density of 30 individuals
per tank. Stock tanks were continuously filled with water from Lake Washington, in
an open circulation system and contained abundant structure for shelter. Crayfish were
fed daily with commercial algae pellets until satiation and were acclimatised for at least
two weeks before being used in the experiment. Snails used as prey were obtained from
various commercial pet retailers (shell length mean = 10.3 mm, SD = 2.4). Snails were
kept in a separate tank, in the same conditions as crayfish.

Functional response experiments

Native and NNS of crayfish were tested for differences in their predatory rate of snail
prey supplied in seven different initial densities (2, 4, 8, 12, 16, 24 and 40 snails)
under the presence or absence of waterborne predator and dietary chemical cues (here-
after, predator treatment and control, respectively). Experiments were conducted in
a fully-randomised design with respect to crayfish species and initial prey densities
assigned to predator treatment and control. Experimental arenas were round opaque
tanks (44.5 cm diameter, 42.5 cm height) filled with 10 | of water and no substrate or
shelter were provided (Fig. 1A). At the predator treatment, water was supplied from the
stimulus tank containing water from Lake Washington and bass (Fig. 1B), whereas un-
der the control, just water from Lake Washington was supplied (as in the stock tanks)
(Fig. 1C). Lake Washington water is piped directly from 10 m depth where largemouth
bass and other fish species are at low abundance. Water was supplied continuously by
dripping through small hoses (5 mm diameter) to ensure that chemical cues were pre-
sent throughout the experiment (Fig. 1D). Water temperature in experimental arenas
and stock tanks were similar, all demonstrating natural diel ranges of 12.5°-18.5 °C.
Fish were starved for a week and then fed every other day a diet of crayfish before
and during the experiments. Small individuals of all crayfish species were supplied
simultaneously until satiation to enhance the response of crayfish to conspecific di-
etary cues released by the fish (Beattie and Moore 2018; Wood et al. 2018). Crayfish
were starved in a separate tank for 48 h before use in experiments to standardise hun-
ger levels. After the starvation period, an individual crayfish was allocated to each

196 Larissa Faria et al. / NeoBiota 87: 191-212 (2023)

Figure |. Experimental setup used in the functional response trials A experimental arena with a signal

crayfish and snail prey during a trial B water from the tank containing largemouth bass (left) was pumped
to a head tank (upper right) and C distributed to the experimental arenas in the predator treatment
(upper-left row) or water was supplied directly from Lake Washington to the control arenas (lower-right
row). Blue tanks in the background were stock and starvation tanks where crayfish were kept before being
used in trials D the water from both treatments was supplied to each experimental arena via individually

controlled hoses.

experimental arena containing one of the seven initial densities of prey and allowed to
forage for 24 h. The number of remaining prey was recorded at the end of the trials,
along with the number of attacked, but uneaten prey. Crayfish sex, carapace length
(CL) and mass were recorded, as well as the water temperature at the end of the trial.
There were seven replicates for each combination of crayfish species, initial density
of prey and treatment. At least five replicates of each combination were performed in
the absence of crayfish to account for any background mortality of prey. Prey survi-
vorship in these replicates was 99.9%, thus all prey deaths during experiments were
attributed to crayfish predation. Crayfish were not reused in the experimental trials
and replicates where crayfish moulted during the trial or one week after were repeated.

Data analysis

All statistical analyses were carried out in R version 4.1.2 (R Core Team 2021). Func-
tional response analyses were conducted using the number of prey consumed as the
response variable, under the frair package (Pritchard et al. 2017). For each crayfish
species x treatment combination, FR type was determined by logistic regression of
the proportion of prey consumed against initial prey density (Juliano 2001). If the
proportion of prey consumed decreases with increasing prey density, it produces a
significantly negative first-order term, indicating a Type II FR; if otherwise, a signifi-
cantly positive first-order term is obtained then it indicates a Type III FR (Juliano
2001). When the results of the logistic regression were not conclusive, different FR

Predation risk modulates functional responses of non-native crayfish 197

models were fitted directly and compared using Akaike’s Information Criterion (AIC)
(Pritchard et al. 2017).

Based on these analyses, all FRs were then modelled as Type H. Maximum Like-
lihood model fitting was used to fit data to the Rogers’ random predator equation
(Rogers 1972) that accounts for the depletion of prey along the experimental duration:

N,=N (1 —exp(a(Nh- T)))

where WV is the number of prey consumed, J, is the initial density of prey, a is the at-
tack rate, / is the handling time and 7 is the time available for predation in days (i.e.
experimental duration). As NV. is obtained experimentally, the estimated FR parameters
are attack rate and handling time, representing a measure of successful attacks and the
time needed for a predator to handle and ingest a prey item, respectively. The Lambert
W function is implemented to solve the fact that V appears on both sides of the equa-
tion (Bolker 2008).

To compare FR parameters a and / between predator treatment and control, we
used the indicator variables method (Juliano 2001; Pritchard et al. 2017), as:

0 =Ny—Noexpi[a + D,(/) [p+ DAW) |(N.)- TH-N,

where j is an indicator variable that takes value 0 for control and 1 for predator treat-
ment. The parameters Da and D/ estimate the differences between treatments in the
value of the parameters a and /, respectively. If Da and Df are significantly different
from zero, then the estimated FR parameters differ between treatment and control
(Juliano 2001). The maximum feeding rate of each crayfish species x treatment com-
bination was calculated as 1/(/T) indicating the maximum number of prey that one
crayfish can consume in one day (T = 1 day). Additionally, the functional response
ratio (FRR) was calculated, as a comparative metric of the ecological impact of NNS
(Cuthbert et al. 2019), dividing the attack rate parameter by the handling time (a/A).
High values of FRR are indicative of strong per capita impacts, while low values indi-
cate less impactful predators (Cuthbert et al. 2019).

Potential differences in the trial’s water temperature amongst species and initial
densities of prey were evaluated through Kruskal-Wallis tests, as well as differences
in crayfish weight and carapace length (CL) amongst species and initial densities
of prey. Water temperature in trials did not vary amongst species (Kruskal—Wallis
X?(3) = 7.366, p = 0.06) nor in association with the initial densities of prey tested
(Kruskal-Wallis X7(6) = 11.339, p = 0.08). Crayfish mass and carapace length varied
amongst species (Mass: Kruskal-Wallis X°(3) = 96.73, p < 0.001; CL: Kruskal—Wal-
lis X°(3) = 224.73, p < 0.001). The effect of crayfish size and sex on the proportion
of prey consumed was investigated with Spearman’s correlation and Mann-Whitney
tests, respectively. Crayfish size (Mass: r = 0.01, p = 0.84; CL: r = -0.08, p = 0.12)
and sex (Mann-Whitney U = 14828, p = 0.74) had no relation to the proportion of
prey consumed.

198 Larissa Faria et al. / NeoBiota 87: 191-212 (2023)

Results

All crayfish species presented a destabilising Type II FR towards snail prey, regardless of
the presence of chemical cues (Fig. 2). This was confirmed by the significantly negative
first-order term of the logistic regression, except for red swamp crayfish under predator
treatment and rusty crayfish under control, where the estimates were non-significant
(Table 2). For these two specific cases, the FR type was determined by comparing the
AIC of different model fittings. For red swamp crayfish, Type I had a lower AIC (AAIC
= 0.8), while for rusty crayfish, Type II presented a better fit (AAIC = 1.1) compared
to other models (generalised FR model, Type I and Type HI).

Non-consumptive effects were observed for all non-native crayfish species, except
for native signal crayfish (Fig. 2). Predation risk lowered the magnitude of the FR,
which reflects reduced maximum consumption rates estimated in the predator treat-
ment compared to the control (Table 2). These differences were driven by significantly
longer handling time of snails for virile crayfish (Dh = -0.03 = 0.008, p < 0.001) and
rusty crayfish (D/ = -0.02 + 0.008, p = 0.01) (Fig. 3A) and significantly lower attack
rate displayed by red swamp crayfish (Da = 0.25 + 0.09, p = 0.006) (Fig. 3B) in the
presence of chemical cues. No significant differences in handling time or attack rates
were evidenced for signal crayfish between treatment and control.

Native signal crayfish demonstrated a greater consumption rate when exposed to
predation risk compared to non-native crayfish (Fig. 2). Per capita effects of signal
crayfish on snails, according to the FRR, was nearly twice that of rusty crayfish and
virile crayfish and ten times greater than red swamp crayfish (Fig. 4, Table 2). By con-
trast, rusty crayfish demonstrated the highest FRR in the control, followed by signal
crayfish, virile crayfish and red swamp crayfish (Fig. 4, Table 2).

Discussion

Predators can exert non-consumptive effects on prey that are comparable in magni-
tude to consumptive effects (Werner and Peacor 2003; Preisser et al. 2005). Despite
that, non-consumptive effects remain largely under-studied in evaluations of ecologi-
cal impacts of NNS (Sih et al. 2010). Here, we quantified rates of snail predation by
multiple non-native and a native crayfish species in the presence or absence of chemical
and dietary cues from a higher-order predator. We found that predation risk reduced
maximum consumption rates of snails due to longer handling times or lower attack
rates, but did not alter the shape of the FR curve. Reduced foraging activity is a com-
mon antipredator behavioural response of crayfish when exposed to predation risk
(Gherardi et al. 2011b; Beattie and Moore 2018; Kenison et al. 2018). For example,
red swamp crayfish significantly reduces the time spent feeding by adopting a lowered
posture after being exposed to largemouth bass cues (Gherardi et al. 201 1b).

Native signal crayfish was the only study species demonstrating little evidence for
the effect of predation risk on the FR magnitude. This outcome is supported by a body

Predation risk modulates functional responses of non-native crayfish 199

A) Signal crayfish (native) B) Red swamp crayfish
=) oO
t t

—e— Predator

--@-- Control

30
30

j=)
™N
ra
2 -
—
>
~ °
oO bs ye
—
O
=
xe)
cb) © Se eh Ce
= 0 8 16 24 32 40
Cc C) Rusty crayfish D) Virile crayfish
8 io) =) \
ay + + \
oO ‘
—
oO.
6
= 8 @
a “r
= 0
= A.
Zz oO a ; i=)
N a NI
=
()

0 8 16 24 32 40

Initial density of prey (snails)

Figure 2. Functional responses of native and non-native crayfish feeding on snails under predator treat-
ment and control A native signal crayfish B non-native red swamp crayfish C non-native rusty crayfish
and D non-native virile crayfish. Lines represent model fit (solid line: predator treatment, dashed line:
control). Points represent mean consumption and error bars represent + SE per density (filled circles:

predator treatment, open circles: control; n = 7 per initial density x treatment combination).

of literature suggesting that the response of signal crayfish to predation risk is highly var-
iable and context-dependent (Stebbing et al. 2010; Gherardi et al. 2011b; Beattie and
Moore 2018; Wood and Moore 2020b). For instance, Stebbing et al. (2010) observed
altered behaviour as raised posture in signal crayfish exposed to the chemical cues of
European eels (Anguilla anguilla), but not to European perch (Perca fluviatilis), whereas
Hirvonen et al. (2007) reported crayfish reduced shelter use when exposed to eel odour.

200 Larissa Faria et al. / NeoBiota 87: 191-212 (2023)

Table 2. Functional response estimates of native and non-native crayfish species under predator treat-
ment and control. The 1* order term of the logistic regression (see Methods), the functional response (FR)

type, estimated parameters attack rate (a) and handling time (/), the maximum feeding rate (1//T) and

the functional response ratio (FRR). * = significant results.

Treatment/ Species 1 order term FR at SE (p-value) 4+ SE (p-value) 1/AT FRR
(p-value) type
Predator
Signal crayfish (native) -0.0617 II 2.26 + 0.23 0.04 + 0.004 28.02 63.5
(> 0.001)* (> 0.001)* (> 0.001)*
Red swamp crayfish -0.0078 i 0.25 + 0.05 0.04 + 0.037 24.81 6.1
(0.29) (> 0.001)* (0.271)
Rusty crayfish -0.0283 II 1.16 +0.14 0.03 + 0.006 31,37 36.3
(> 0.001)* (> 0.001)* (> 0.001)*
Virile crayfish -0.0411 II 1.64 + 0.23 0.05 + 0.006 19.81 32.5
(> 0.001)* (> 0.001)* (> 0.001)*
Control
Signal crayfish (native) -0.0358 II 2.08 + 0.24 0.03 = 0.004 37.53 78.2
(> 0.001)* (> 0.001)* (> 0.001)*
Red swamp crayfish -0.0142 a 0.50 + 0.08 0.04 + 0.015 2 14.3
(0.022) (> 0.001)* (0.021)*
Rusty crayfish -0.0101 Ul 1.14 + 0.13 0.01 + 0.006 94.99 108.0
(0.086) (> 0.001)* (0.061)
Virile crayfish -0.0252 II 1.43 + 0.15 0.02 + 0.005 47.95 68.8
(> 0.001)* (> 0.001)* (> 0.001)*

"Despite being categorised as Type I using AIC, we fitted data to the Type II model to allow comparison of parameters
between treatment and control.

‘These studies were performed in the invaded range of signal crayfish; thus, unexpected
behavioural responses were attributed to naive juvenile individuals with a lack of evo-
lutionary history with these predators (Hirvonen et al. 2007; Stebbing et al. 2010).
However, this may not be the case in our study where signal crayfish is native and has
experience with largemouth bass in the region for over a hundred years. ‘This suggests
that signal crayfish may better assess the risk posed by a familiar predator using both
chemical and visual cues (Blake and Hart 1993), whereas all three non-native crayfish
species responded in a more conservative manner to the presence of chemical cues
alone in a novel environment (Gherardi et al. 2002; Hazlett et al. 2003). Another
possible mechanism is related to the larger body sizes of signal crayfish compared to
other species (both in the wild and individuals used in this experiment: Table 1). There
is evidence that crayfish can assess predator size through chemical cues (Wood and
Moore 2020a; Wagner and Moore 2022); thus, the size of the largemouth bass in the
experiment may have been too small relative to signal crayfish to elicit an antipredator
behaviour resulting in reduced foraging rates.

All crayfish species presented a Type II FR, which is deemed to destabilise re-
source populations. This result aligns with the known impacts of these species on bio-
mass and abundance of benthic invertebrates, particularly snails (Twardochleb et al.
2013). Moreover, when applying an FR-based metric to evaluate impacts, our native

Predation risk modulates functional responses of non-native crayfish 201

@® Predator

© Control

0.06

0.04

0.02

Handling time (day/prey)

0.00

Kk

Attack rate (arena/day)

0.5 p
é
Signal Red Rusty Virile

crayfish swamp. crayfish crayfish
(native) crayfish

Figure 3. Estimated functional response parameters of native and non-native crayfish species under
predator treatment and control A handling time parameter / and B attack rate parameter a. Points rep-
resent the mean estimate of the model (filled circles: predator treatment, open circles: control) and error
bars represent + SE. *p < 0.1 and **p < 0.05.

comparator species generally showed a higher FRR than non-natives, which con-
tradicts the pattern of invaders being more impactful than their native counterparts
(Cuthbert et al. 2019). Nevertheless, signal crayfish is itself highly invasive in Europe,
Japan and the south-western United States, usually reaching higher abundances than
those observed in its native range (Larson and Olden 2013) and causing significant
impact through their omnivorous feeding habits (Usio et al. 2009; Twardochleb et
al. 2013; VaefSen and Hollert 2015). Our results also align with a previous study that

202 Larissa Faria et al. / NeoBiota 87: 191-212 (2023)

160 B® Signal crayfish (native)
NM) Red swamp crayfish
|| Rusty crayfish
BW Virile crayfish

120

80

Functional response ratio (FRR)

Predator Control

Figure 4. The functional response ratio (FRR) of native and non-native crayfish species under predator
treatment and control. The calculated FRR (a/h) is represented as bars (solid bars: predator treatment,
shadowed bars: control) and error bars represent propagated standard errors of original estimates of pa-
rameters attack rate a and handling time /.

experimentally compared the predation rate of signal crayfish and non-native crayfish
towards Chinese mystery snail (Bellamya chinensis), where native signal crayfish con-
sumed significantly more snails of all size classes than did non-native crayfish (Olden
et al. 2009). Indeed, previous studies that used the comparative FR approach to assess
the impacts of signal crayfish where it is non-native found that the species generally
present higher FR magnitude when compared to European native analogues, such as
white-clawed crayfish (Austropotamobius pallipes) and noble crayfish (Astacus astacus),
although impact varied with prey type (Haddaway et al. 2012; Rosewarne et al. 2016;
Taylor and Dunn 2018; Chucholl and Chucholl 2021). Differences in experimental
systems, such as diverse prey types and arena sizes, preclude us from comparing the na-
tive signal crayfish findings here to those of invasive populations of the species. Future
comparative studies of the FRs of native and non-native populations are recommended.

We found significant differences amongst NNS predatory impacts towards prey.
Rusty crayfish and virile crayfish showed consumption rates similar to those of native
signal crayfish, whereas red swamp crayfish demonstrated the lowest feeding rate, despite
the latter species being considered one of the most impactful invasive crayfish in the
world (Lodge et al. 2012; Twardochleb et al. 2013). Even though all crayfish are con-
sidered omnivorous or polytrophic, there are marked differences in their predominant
trophic ecology (Reynolds et al. 2013). For instance, red swamp crayfish has a lower
trophic position than signal crayfish, which is consistent with the perceived impact on
macrophyte communities of the former species (Matsuzaki et al. 2009; Larson et al.
2017). Similarly, Madzivanzira et al. (2021) also reported a lower FR magnitude of red
swamp crayfish preying on catfish fry compared to a native analogue crab. Despite this, it

Predation risk modulates functional responses of non-native crayfish 203

has been demonstrated that invasive populations of red swamp crayfish in Europe present
ontogenetic niche shifts and have opportunistic feeding habits, adjusting its diet to differ-
ent biotic and abiotic contexts, which further explains its success as an invader (Correia
2002, 2003; Carreira et al. 2017; Jackson et al. 2017). Additionally, red swamp crayfish
has weaker chelae closing force compared to other decapods, which helps explain its
preference for feeding on softer resources (South et al. 2020). Our findings support previ-
ously observed impacts of rusty crayfish and virile crayfish on snail communities where
they are invasive (Dorn and Wojdak 2004; McCarthy et al. 2006; Kreps et al. 2012). The
greater consumption rate of invasive crayfish is likely associated with selected traits, such
as boldness and foraging voracity in NNS populations, which are known to differ from
their native range (Pintor and Sih 2009; Reisinger et al. 2017; Glon et al. 2018).

Previous studies that investigated TMIEs using the FR approach reported mixed
outcomes. Considering simple habitats, the presence of predator cues reduced con-
sumption rates of the amphipod Echinogammarus marinus, an intermediate predator,
towards isopod prey (Alexander et al. 2013). By contrast, fish cues did not influence the
FR’s magnitude of two amphipod species (the native Gammarus duebeni and the inva-
sive Gammarus pulex) towards three different invertebrate preys (Paterson et al. 2015).
Our study reinforces the need for considering the wider biological context of ecological
interactions when quantifying the impacts of NNS. Moving forward, we suggest three
primary ways that future studies could further explore context-dependencies.

First, the effect of abiotic contexts, such as habitat complexity and presence of
shelter, continues to be a research need. The Type II FR curves reported here align with
general expectations from the broader literature (Jeschke et al. 2004); however, the
lack of habitat complexity in experimental arenas may prevent the observation of more
stabilising Type III responses (Alexander et al. 2012; Griffen 2021). Likewise, gravel
substrate has been reported to reduce crayfish consumption of pelagic, but not benthic
prey (Vollmer and Gall 2014; South et al. 2019). Additionally, shelter use is a common
behavioural response of crayfish to predator cues (Blake and Hart 1993; Garvey et al.
1994) and could have further magnified the observed differences between the predator
treatment and control reported in our study.

Second, it would be valuable to evaluate additional biotic contexts, such as alter-
native resource availability, the presence of intra- and inter-specific competitors and
effects of visual predator cues. For instance, prey preference for different resources,
such as macrophyte or detritus, could have a significant effect on FRs for omnivorous
crayfish (Cuthbert et al. 2018; Médoc et al. 2018), ultimately defining their ecologi-
cal impacts when invasive (South et al. 2019; Chucholl and Chucholl 2021). Better
incorporating the effects of competitive interactions in FR experiments are also fun-
damental to more realistic scaling of NNS per capita effects in the wild (Dickey et al.
2020; Latombe et al. 2022). As crayfish can respond to predation risk using a variety of
different cues, the relative importance of visual and alarm cues can also be investigated
using FRs (Blake and Hart 1993; Ramberg-Pihl and Yurewicz 2020). Third, future
research investigations discussed above would benefit from the linking of mesocosms
experiments with in-situ field studies to ensure robust scaling of our understanding
(Iacarella et al. 2018).

204 Larissa Faria et al. / NeoBiota 87: 191-212 (2023)

Conclusions

Ecological impacts of NNS are notoriously challenging to anticipate given a myriad
of biotic and abiotic context-dependencies that can affect the organismal performance
in nature. The comparative FR approach has been used to incorporate these context-
dependencies to predict the impact of NNS, through relative comparisons of per capita
effects (Dick et al. 2014; Cuthbert et al. 2019; Faria et al. 2023). Here we showed that
the presence of a higher-order predator can alter important parameters of FR, with
direct effects on maximum consumption rates and predicted impact of intermediate
non-native consumers. These findings suggest that the broader biological context in
which consumer activities take place should not be overlooked if we aim to understand
the ecological impacts of NNS. Likewise, biogeographic origin alone is not the sole
indicator of impact, as we found that native signal crayfish demonstrated the highest
estimated impact on prey in the presence of predation risk by a fish predator.

The ecology of fear predicts that the cost of anti-predator behaviour is associated
with reduced offspring, thus modulating consumer abundance (Zanette and Clinchy
2019). Given the immense challenges in eradicating and controlling invasive crayfish
populations (Gherardi et al. 2011a; Manfrin et al. 2019), this raises the interesting
question of whether chemical cues could be used as an additional management tool
to reduce their short-term ecological impacts, while other control strategies are being
implemented. We encourage more research on which and how chemical components
of predator and dietary cues trigger behavioural responses in crayfish, as these are not
entirely elucidated (Mitchell et al. 2017), but have potential management applications.

Acknowledgements

Assistance in the collection of fish provided by the Washington Department of Fish
and Wildlife and the collection of crayfish by the Oregon Department of Fish and
Wildlife, the Washington Crawfish Company and Dwayne Lamb. We thank Alexan-
dre Bee Amaral, Jon Wittouck and lab-mates in the Freshwater Ecology & Conserva-
tion Lab for their help in assembling the mesocosms. We are grateful to Fulbright Bra-
zil, the Fulbright Scholarship Board and the Bureau of the Educational and Cultural
Affairs of the United States Department of State for the scholarship granted to LF as
part of the Doctoral Dissertation Research Award programme. JRSV was supported by
Conselho Nacional de Desenvolvimento Cientifico e Tecnolégico (CNPq) — Process
Numbers 02367/2018-7 and 303776/2015-3. JDO was supported by the Richard
C. and Lois M. Worthington Endowed Professor in Fisheries Management from the
School of Aquatic and Fishery Sciences, University of Washington. ‘This study was also
supported by Coordenacao de Aperfeigoamento de Pessoal do Nivel Superior (CAPES)
— Finance Code 001. All experiments were approved by the University of Washington
Institutional Animal Care and Use Committee (permit 4172-12).

Predation risk modulates functional responses of non-native crayfish 205

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Supplementary material |

Data from functional response trials

Authors: Larissa Faria, Jean R. S. Vitule, Julian D. Olden

Data type: xls

Explanation note: Data from functional response trials for each crayfish species under
predator treatment and control.

Copyright notice: This dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License
(ODDbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.

Link: https://doi.org/10.3897/neobiota.87.108457.suppl1