A neglected fish stressor: mechanical disturbance during transportation impacts susceptibility to disease in a globally important ornamental fish
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Vol. 134: 25–32, 2019 DISEASES OF AQUATIC ORGANISMS
Published online April 11
https://doi.org/10.3354/dao03362 Dis Aquat Org
A neglected fish stressor: mechanical disturbance
during transportation impacts susceptibility to
disease in a globally important ornamental fish
N. Masud, A. Ellison, J. Cable*
School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK
ABSTRACT: The transport of fish in aquaculture and the ornamental trade exposes fish to multiple
stressors that can cause mass mortalities and economic loss. Previous research on fish transport
has largely focussed on chemical stress related to deterioration in water quality. However,
mechanical disturbance during routine fish transport is unpredictable and is a neglected potential
stressor when studying fish welfare. Stress-induced immunosuppression caused by mechanical
disturbance can increase the chances of contracting infections and can significantly increase in-
fection burden. Here, using a model host−parasite system (guppy Poecilia reticulata and the
monogenean ectoparasite Gyrodactylus turnbulli) and a new method of bagging fish (Breathing
Bags™), which reduces mechanical disturbance during fish transport, we investigated how para-
site infections contracted after simulated transport impact infection trajectories on a globally
important ornamental freshwater species. Guppies exposed to mechanical transport disturbance
suffered significantly higher parasite burden compared to fish that did not experience transport
disturbance. Unfortunately, there was no significant reduction in parasite burden of fish trans-
ported in the Breathing Bags™ compared to standard polythene carrier bags. Thus, transport-
induced mechanical disturbance, hitherto neglected as a stressor, can be detrimental to disease
resistance and highlights the need for specific management procedures to reduce the impact of
infectious diseases following routine fish transport.
KEY WORDS: Animal transport · Fish welfare · Aquarium trade · Infectious disease · Guppy ·
Poecilia reticulata · Gyrodactylus turnbulli
Resale or republication not permitted without written consent of the publisher
1. INTRODUCTION 2007, Stevens et al. 2017) despite fish being the most
abundant pet in western households (American Pet
For the animal industry, transportation can lead to Products Association 2012). Indeed, with over 4500
maladaptive traits, including reduced feeding, altered freshwater and 1450 marine fish species traded glob-
immune response and mortality (cattle: Stockman et ally as pets, the ornamental trade is a lucrative busi-
al. 2013; swine: Zou et al. 2017; poultry: Matur et al. ness valued at US $800 million to $30 billion annually
2016; fish: Momoda et al. 2007, de Castro et al. 2016). (Stevens et al. 2017), and this demand for ornamentals
Although the impact of transport stress is a general is increasing with expansion of the global pet trade
animal welfare issue, priority of research has been (Saxby et al. 2010). Increased fish transport is an
placed on terrestrial livestock (Schwartzkopf-Gens- inevitable consequence of rising demands for exotic
wein et al. 2012) over aquatic species. Furthermore, species, and emphasis on meeting these demands in-
current research on transport stress in fish focusses on cludes minimising transport costs which may lead to
food fish and neglects the ornamental trade (Ashley fish being transported in sub-optimal conditions.
*Corresponding author: cablej@cardiff.ac.uk © Inter-Research 2019 · www.int-res.com26 Dis Aquat Org 134: 25–32, 2019 Stressors experienced by fish during transport can bags to be completely filled with water (without the lead to immunosuppression, with the proposed mech- need to add air or oxygen), and since water is incom- anism linked to the release of catecholamines and pressible relative to air, this should provide natural glucocorticoid hormones as a stress response (Barton cushioning against mechanical stress during transport 2002, Ackerman et al. 2006), which may increase dis- (Thiagarajan et al. 2011). The impacts of other stres- ease susceptibility (Caruso et al. 2002, Ramsay et al. sors associated with fish transport have been previ- 2009). There tends to be huge variability in immune ously investigated (water quality: Ackerman et al. responses to stressors (see Tort 2011 for review), with 2006, Dhanasiri et al. 2011; capture and handling: chronic or acute stressors suppressing or enhancing Caruso et al. 2002, Thompson et al. 2016; stocking immunity (Dhabhar 2000). In Atlantic salmon Salmo densities: Ramsay et al. 2009), whereas mechanical salar, for example, chronic stress suppresses transcrip- stress has thus far remained neglected. tional immune responses to pathogenic challenge, The transport procedure for fish varies globally, whereas acute stress enhances it (Uren Webster et al. depending on local animal trading laws and whether 2018). Thus, with transport stressors that remain un- fish are transported locally or internationally. The lat- identified, we still do not know how pathogens will be ter routinely involves fish quarantine procedures affected by the host’s immune response. Further com- before transport and border inspections post-arrival plications arise when variations in susceptibility to (Portz et al. 2006). In addition, such fish will experi- disease are linked to both host and pathogen species, ence extended transport disturbance including mul- making the outcome of transportation on fish welfare tiple handlings due to inspections. Fish transporta- uncertain. Chinook salmon Oncorhynchus tshawytscha tion procedures typically lack routine screening and ayu Plecoglossus altivelis, for example, exposed procedures for parasites and therefore represent a to transport conditions showed increased susceptibil- wide-scale welfare issue (Ashley 2007, Stevens et al. ity to bacterial infections (Iguchi et al. 2003, Ackerman 2017). Ornamentals transported from the wild or et al. 2006). Channel catfish Ictalurus punctatus that local pet shops may be reservoirs of undiagnosed experienced low water crowding stress as part of sim- infections that become more pernicious due to stress- ulated transport conditions only showed increased imposed immunosuppression following transport susceptibility when exposed to Ichthyophthirius mul- (Wendelaar Bonga 1997). Due to mixing of species tifiliis, but not to inoculation with the channel catfish from different geographic regions, disease dynamics virus (Davis et al. 2002). in wholesalers, retailers and hobbyist aquaria may Typically, fingerlings, juveniles and small fish are result in parasite host switching and increased viru- transported in plastic bags filled with 25−30% water lence (Kelly et al. 2009). Accidental or intentional and 70−75% air or pure oxygen (Carneiro & Urbinati introduction of exotic species into local fish popula- 2001, Conte 2004). Presence of air pockets in poly- tions can cause transmission of highly virulent para- thene bags for fish increases the chances of mechani- sites to which native fish species may be especially cal stress due to water movement. In mechanical susceptible (Smit et al. 2017). terms, stress is defined as a force applied across a sur- Ornamental fish trade practices routinely involve face per unit area for all orientations of that surface the addition of antiparasitic chemicals into water and (Chen & Han 2007). In addition, accumulation of car- removal of weak or diseased fish, which reduces dis- bon dioxide from respiring fish can lead to displaced ease outbreaks and keeps parasite numbers to a min- available oxygen, especially if stocking densities are imum (Stevens et al. 2017). Diseases with distinctive high (Conte 2004). Thus, traditional transport carriers symptoms, such as those caused by I. multifiliis or can expose fish to multiple stressors, including cap- Saprolegnia parasitica, are relatively easy to detect ture, handling, overcrowding, abrupt changes in tem- through visual inspection of fish, leading to either perature and physical trauma (Robertson et al. 1988, quarantine or euthanizing infected individuals to halt Portz et al. 2006). A decline in water quality caused by spread of infections (Stentiford et al. 2017). Such the accumulation of ammonia (Ackerman et al. 2006) standard practice for fish farmers and hobbyists does and fluctuations in dissolved oxygen and pH (Moran reduce maintenance costs, and for legal reasons, et al. 2008, Sampaio & Freire 2016), which are known many countries only sell or display fish that appear fish stressors, is another consequence of transportation healthy (Washington & Ababouch 2011). However, (Paterson et al. 2003). Unlike traditional polythene many parasites at low levels of infection do not affect bags, micro-porous transport bags (Breathing Bags™, fish phenotype, making them undetectable to non- Kordon®) allow exchange of respired carbon dioxide specialists. Ectoparasites, such as Gyrodactylus spe- with atmospheric oxygen. Their porosity allows the cies, typically require thorough microscopic exami-
Masud et al.: Fish transport influences disease susceptibility 27
nation to determine parasite burden (Maceda-Veiga dactylus turnbulli, isolated from a Nottingham (UK)
& Cable 2019), which is not a routine procedure for aquarium shop in October 1997 and subsequently
fish at any point in the aquaculture or ornamental maintained at Cardiff University since 1999 on inbred
trade. For gyrodactylosis, there is no 100% effective guppies prior to this study. All work was approved by
treatment, and parasites can remain at low frequen- the Cardiff University Animal Ethics Committee and
cies in fish populations that are being transported; conducted under UK Home Office licence PPL 303424.
then, under favourable conditions, they can increase
exponentially until stock survival is severely affected
(Cable 2011). Thus, even if species harbour low-level 2.2. Experimental design
infections due to the presence of anti-parasitic chem-
icals, stressful transport conditions can sufficiently To test the impact of traditional polythene bags ver-
weaken the immune system, allowing large infection sus Breathing Bags™ on fish susceptibility to disease,
sources to be established in healthy stocks. guppies (20 per experimental treatment) were exper-
Amongst the most popular tropical fish species is imentally infected after experiencing simulated trans-
the guppy Poecilia reticulata (see Maceda-Veiga et al. port. All guppies were netted carefully from breeding
2016), which has been transported worldwide as an tanks to minimise handling stress and transferred to
ornamental and biological control agent, with 41 re- separate tanks for a 24 h holding period. Fish were
corded introductions outside its native habitat (Magur- not fed during the holding period to ensure a post-
ran 2005). The most common parasites of wild and or- absorptive stage and to minimise build-up of nitro-
namental guppies are the viviparous monogeneans genous waste, as per standard aquacultural practice
Gyrodactylus spp., known for their ‘Russian doll’ re- (Berka 1986). To simulate transport stress, fish were
production and direct transmission (Cable 2011). This randomly assigned to either 48 × 21 cm polythene
makes them capable of rapidly colonising a fish popu- bag treatments (provided by Aquatic World, Cardiff)
lation, affecting the behaviour of the fish, including or 36 × 19 cm Breathing Bags™ treatments. The poly-
courtship, feeding and shoaling (Kennedy et al. 1987, thene bags were filled with one-third dechlorinated
Kolluru et al. 2009, Hockley et al. 2014) and survival water to two-thirds air, which is the most common
(Cable & van Oosterhout 2007, Yamin et al. 2017). method of transporting small fish in aquaculture
Here we investigated the impact of simulated (Conte 2004). Air was not added to the Breathing
transportation on fish infection dynamics. Specifi- Bags™ as per supplier instructions to reduce mechan-
cally, we assessed how mechanical disturbance asso- ical disturbance due to sloshing (Thiagarajan et al.
ciated with traditional polythene carrier material im- 2011). Fish stocking density was 4 fish l−1 for both bag
pacts susceptibility to disease in fish exposed to treatments, which falls within approved guidelines
parasites after simulated transport. In addition, we for tropical freshwater species stocking densities
tested the efficacy of Breathing Bags™ in helping (OATA 2008), and each bag contained water volumes
alleviate mechanical disturbance-induced elevated of up to 1.5 l. To prevent handling fish with nets, they
disease susceptibility and mortality. were placed into bags while fully submerged. Bagged
fish were then contained in an insulated sealed ther-
mal box (dimensions: 30 × 24 × 19 cm, 24 ± 1°C) and
2. MATERIALS AND METHODS placed onto an orbital shaker (Stuart®) for 24 h at
50 rpm to simulate transport motion. The rotator al-
2.1. Host and parasite species maintenance lowed for orbital movement on a horizontal platform,
similar to any flat surface fish would be placed on in
Male guppies (standard length: 12.1−17.4 mm) bred a transport vehicle or aircraft (Portz et al. 2006). Con-
from a stock originating in the Lower Aripo River in trol fish (n = 20) were kept in bags without turning on
Trinidad, were initially housed at Exeter University, the orbital rotator, adjacent to an operating rotator to
UK, before being transferred to Cardiff University, UK, ensure fish were exposed to the same noise levels.
in October 2014. Guppies were kept in 70 l breeding
tanks, containing artificial plants and refugia. They
were maintained under a 12:12 h light:dark photo- 2.3. Experimental infections
period (lights on from 07:00−19:00 h) at 24 ± 1°C and
fed daily on dry food flakes (Aquarium®) and every To perform controlled infections, guppies were
alternate day on live freshly hatched Artemia nauplii. lightly anaesthetised with 0.02% MS-222, and each
Experimental infections used the Gt3 strain of Gyro- fish was infected with 2 gyrodactylid worms. Parasite28 Dis Aquat Org 134: 25–32, 2019
transfer was conducted using a dissection micro- model but was removed because the size range
scope with fibre optic illumination following standard did not explain significant variation (Thomas et al.
methods of King & Cable (2007). Briefly, 2 worms from 2013). The area under the curve (AUC) is a statistical
heavily infected donor fish were transferred to the parameter that provides a measure for analysing
caudal fin of recipient hosts by placing the anaes- infection trajectories over time using the trapezoid
thetised donor fish in close proximity to an anaes- rule (White 2011). AUC was analysed using a second
thetised naïve host with the transfer monitored con- GLMM with a negative binomial error family. Finally,
tinuously using the dissecting microscope. Parasite we used a generalised linear model (GLM) to analyse
infections were then monitored every 48 h by anaes- how peak parasite day and maximum parasite count
thetising fish and counting the total number of gyro- varied with treatment. For analysing maximum para-
dactylids over the first 17 d of infection. On Day 17, site count, we used a negative binomial error family
all fish that survived were treated with Levamisole with a log link function and a Gaussian error family
(Norbrook®) according to Schelkle et al. (2009), and with an identity link function for peak parasite day.
their post-treatment recovery and any further mortal- All error families were determined based on the low-
ities were monitored for 3 wk. est Akaike’s information criterion (AIC) value. A logis-
tic regression was used to analyse mortality between
transported and control fish and between bag types.
2.4. Water quality
As water quality can impact disease susceptibility 3. RESULTS
(Ackerman et al. 2006), we measured water ammonia
(freshwater master test kit, API®), pH (battery pow- Parasite dynamics were influenced by simulated
ered checker HANNA®) and oxygen saturation (dis- transport of fish, with guppies that were transported
solved oxygen meter, Lutron Electric Enterprise) to suffering significantly higher mean parasite intensity
ensure this did not vary between treatment and con- than untransported control fish (GLMM: Z = 2.51,
trol groups (n = 5 bags per experiment). All water SE = 0.16, p = 0.009; Fig. 1). The carrier type used to
quality levels within the polythene bags and Breath- simulate transport (polythene bags or Breathing
ing Bags™ post-transport were within normal ranges Bags™), however, did not affect the mean intensity
(ammonia levels: undetectable for both bag treat-
ments; pH: 7.1−7.8; oxygen saturation: 20.4−21.4%)
and were consistent between treatments (Fisher’s
exact test: oxygen, p = 0.958, pH, p = 0.909).
2.5. Statistical analyses
All statistical analyses were conducted using RStu-
dio v2.1 (R Development Core Team 2015). G. turn-
bulli mean intensity for all experiments was defined
as the average number of worms on infected hosts
(Bush et al. 1997). A generalised linear mixed model
(GLMM) with a negative binomial error family in the
‘MASS’ R package was used to analyse the relation-
ship between transport treatments (polythene bags
and Breathing Bags™) and mean parasite intensity.
Host standard length, bag type (polythene bags and
Breathing Bags™) and treatment (transport and no-
transport) were treated as fixed factors. As parasite
intensity was recorded for each individual fish on dif- Fig. 1. Mechanical disturbance significantly impacted sus-
ferent days, ‘Fish ID’ and ‘days since initial infection’ ceptibility to disease in Poecilia reticulata exposed to Gyro-
dactylus turnbulli infections after experiencing 24 h of simu-
were included as random effects in the GLMM to lated transport in both types of transport bags (Breathing
avoid pseudoreplication by incorporating repeated BagsTM and polythene bags). Standard error bars are slightly
measures. Fish length was included in the initial transposed to one side to prevent overlapMasud et al.: Fish transport influences disease susceptibility 29
between transported and untransported fish (GLMM: cortisol levels, increased disease susceptibility and
Z = 2.51, SE = 0.15, p = 0.19). Total infection trajec- significant mortality levels (Robertson et al. 1988,
tory over 17 d, as measured by AUC, was signifi- Caruso et al. 2002, Iguchi et al. 2003, Cho et al. 2009).
cantly greater in fish that experienced simulated However, in the current study, fluctuating water qual-
transport versus controls (GLMM: Z = 2.42, SE = 0.17, ity, temperature, lighting, noise, netting and stocking
p = 0.01). Similarly, peak parasite day (t = 2.24, SE = densities were controlled, leaving mechanical distur-
0.25, p = 0.02) and the associated maximum parasite bance as the major stressor. While we are unaware of
count (Z = 6.73, SE = 0.06, p < 0.001) were signifi- how long a stress response would last in guppies post-
cantly different between transported and control fish, transport, as there is likely a species-level difference
with maximum parasite count on peak days having in cortisol production (Honryo et al. 2018), mechanical
approximately 51% greater parasite load compared disturbance in our transported guppies could have
to controls in both carrier types (Breathing Bags™ = caused elevated cortisol production during a stress
50.9% greater, polythene bags = 51.2% greater). response leading to immunosuppression. Surprisingly,
There was no significant difference in mortality be- guppies exposed to gyrodactylid infection immedi-
tween simulated transport and control fish within the ately prior to experiencing mechanical transport dis-
same bags or between Breathing Bags™ and poly- turbance did not show a significant effect of trans-
thene bags (between bags, GLM: Z = 0.18, SE = 0.35, portation on total infection trajectories or mean parasite
p = 0.85; within same bags, GLM: Z = 0.89, SE = 0.36, intensity compared to untransported fish (see the Ap-
p = 0.371). pendix), which indicates that immune status at the
time of initial infection is the most important factor de-
termining disease outcome.
4. DISCUSSION Undiagnosed infections of imported fish are a major
biosecurity risk in the ornamental trade (Maceda-
Simulated transport significantly affected guppy Veiga & Cable 2019), particularly as they may intro-
susceptibility to infections with Gyrodactylus turn- duce novel parasite species to which local hosts have
bulli, showing for the first time the impact of mechan- no immunity (Paterson et al. 2012). Our study empha-
ical disturbance on disease dynamics. Unfortunately, sises the need for stricter screening procedures after
increased parasite burdens were not ameliorated transport, as diseases such as gyrodactylosis are diffi-
following use of specialized Breathing Bags™, even cult to diagnose without thorough microscopic screen-
though these bags did reduce the level of water ing and can cause an explosion in parasite burden
sloshing during mechanical disturbance. However, it due to transport stress. Application of anesthetic
should be noted that there could be additional bene- agents, like clove oil and MS-222, into water prior to
fits of these bags that were not tested here, for exam- transport has shown limited efficacy in reducing
ple in terms of maintaining higher water quality. stress and mortality in transported fish (Rubec et al.
Mechanical stress is a broad term that encompasses 2001) and is actually associated with the risk of respi-
aspects of physical forces such as pressure and ratory failure (Wagner et al. 2003, Pramod et al. 2010).
impulse (Thiagarajan et al. 2011), and reduced slosh In contrast, addition of compounds such as salt prior to
does not rule out the possibility of such forces acting fish transportation can reduce transport-related mor-
on fish within Breathing BagsTM during the transport tality (Oyoo-Okoth et al. 2011); however, they have
simulation. Thus, fish transported in Breathing BagsTM variable efficacy on diseases such as gyrodactylosis,
may indeed have experienced a form of mechanical as treatment is often time-, concentration- and species-
stress despite reduced water sloshing, leading to dependent (Schelkle et al. 2011). Studies of parasite
increased susceptibility to disease. diversity in the ornamental trade (pet shops, retailers
The link between stressors and susceptibility to dis- and home aquaria) highlight Gyrodactylus spp. as one
ease in fish is influenced by the production of cortisol, of the most common groups of parasites detected dur-
an immunosuppressant (Tort et al. 2003, Tort 2011). ing screening procedures (Trujillo-González et al.
While the relationship between a stress event and im- 2018, Maceda-Veiga & Cable 2019). Thus, the impact
munosuppression is far from clear (reviewed by Tort of this monogenean infection remains a serious wel-
2011), the transport process for fish is associated with fare issue for the global ornamental fish trade. For the
multiple stressors including handling and netting, first time, our investigation highlights that even when
with water quality deterioration considered the major water quality, stocking density and temperature are
stressor linked to high stocking density (see Braun & stable, mechanical disturbance during transport, hith-
Nuñer 2014), which has been implicated in elevated erto neglected as a potential stressor, significantly im-30 Dis Aquat Org 134: 25–32, 2019
pacts susceptibility to infections in fish. With disease tatus to Ichthyophthirius multifiliis and channel catfish
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32 Dis Aquat Org 134: 25–32, 2019
Appendix. Transport-induced mechanical stress impact on infection trajectories of guppies with pre-existing infections
Here, we investigated how mechanical disturbance dur- Results. Mean parasite intensity and total infection tra-
ing simulated transport impacted pre-existing high burden jectories over 17 d as measured by the area under the
infections in guppies Poecilia reticulata. curve (AUC) were not significantly different between
Materials and Methods. Each guppy (n = 20 per treat- transported guppies and controls (mean parasite intensity:
ment) was experimentally infected with 30 Gyrodactylus GLMM: Z = 1.64, SE = 0.1, p = 0.1; AUC: GLM: Z = 0.6, SE =
turnbulli worms, packaged in standard polythene bags 0.38, p = 0.54; Fig. A1). Peak parasite burden, however,
and then exposed to simulated transport (as described in was significantly higher in guppies that experienced simu-
Section 2.2 of the main text) or left as untransported con- lated transport (GLM: Z = 2.72, SE = 0.05, p = 0.006) and
trols. After 24 h of simulated transport, all fish (transport timing of peak parasite burden was also earlier in these
and control) were individually isolated in 1 l pots and guppies compared to controls (GLM: t = −3.83, SE = 0.03,
screened every 48 h over 17 d to monitor their infection tra- p = 0.0001).
jectories. Data were analysed as described in Section 2.5 of
the main text.
Fig. A1. Infection trajectory with standard error
bars showing that Poecilia reticulata exposed to a
starting point Gyrodactylus turnbulli infection of
30 worms prior to transport did not suffer signifi-
cantly elevated mean parasite intensity compared
to controls
Editorial responsibility: Stephen Feist, Submitted: November 27, 2018; Accepted: February 17, 2019
Weymouth, UK Proofs received from author(s): March 29, 2019You can also read
