Biota Neotrop., vol. 12, no. 3
Upstream guppies (Poecilia reticulata, Peters, 1859) go against the low
Ryan Simon Mohammed1,2,5, Cock van Oosterhout3, Bettina Schelkle4,
Joanne Cable4 & Mark McMullan3
1
Department of Life Sciences, The University of the West Indies, St Augustine, Trinidad, West Indies
2
Aquaculture Association of Trinidad and Tobago, West Indies
3
School of Environmental Sciences, University of East Anglia, Norwich Research Park,
Norwich NR4 7TJ, United Kingdom
4
School of Biosciences, Cardiff University, Cardiff CF10 3AX, United Kingdom
5
Corresponding author: Ryan Simon Mohammed, e-mail: rmohammed@gmail.com
MOHAMMED, R.S., VAN OOSTERHOUT, C., SCHELKLE, B., CABLE, J. & MCMULLAN, M. Upstream
guppies (Poecilia reticulata, Peters, 1859) go against the low. Biota Neotrop. 12(3): http://www.biotaneotropica.
org.br/v12n3/en/abstract?article+bn01512032012
Abstract: Guppies (Poecilia reticulata Peters 1859) in lakes and from captive-bred populations are predicted
to show little rheotaxis compared to conspeciics in a stream environment that are regularly exposed to lash
loods associated with involuntary downstream migration. Here we test this hypothesis using an artiicial stream,
examining guppies of two wild riverine populations, one lake population, and one ornamental strain. Guppies
from the most upstream riverine habitat show the most pronounced rheotaxis and are less likely to be swept
downstream during looding events. However, there is no signiicant difference between guppies from the lowland
riverine habitat, the Pitch Lake and ornamental strain. We propose that station-keeping behaviours are most
strongly selected in the upstream population because large spatial differences exist in ecology and environment
between up- and downstream habitats. Given that these sites are separated by barrier waterfalls that prevent
compensatory upstream migration, natural selection operates particularly strong against upstream guppies that
have been displaced downstream during looding events.
Keywords: Guppy (Poecilia reticulata), rheotaxis, swimming behaviour, migration, natural selection.
MOHAMMED, R.S., VAN OOSTERHOUT, C., SCHELKLE, B., CABLE, J. & MCMULLAN, M. Gupies
(Poecilia reticulata, Peters, 1859) de áreas de cabeceira se posicionam contra a corrente. Biota Neotrop.
12(3): http://www.biotaneotropica.org.br/v12n3/pt/abstract?article+bn01512032012
Resumo: Populações de guppies (Poecilia reticulata Peters) que vivem em lagos e em cativeiro podem demonstrar
menos reotaxia em comparação com populações que habitam rios e que estão frequentemente expostas a enchentes
e que provocam a migração involuntária para jusante. Neste trabalho, vamos testar esta hipótese num rio artiicial
utilizando guppies de duas populações selvagens que habitam em rios, uma população que habita em lagos, e uma
linhagem ornamental. Os resultados demonstram que os guppies de rios que provêm de localidades a montante
demonstram maior reotaxia, diminuindo assim probabilidade de serem arrastados para jusante em períodos de
enchentes. No entanto, não foram encontradas diferenças signiicativas entre guppies de localidades a jusante, do
lago Pitch ou ornamentais. Este resultado pode dever-se ao facto de existirem grandes diferenças ecológicas entre
os habitats localizados a jusante e a montante dos rios. Devido ao facto de estas localidades estarem separadas
por cachoeiras, impossibilitando a migração rio-acima, a seleção natural poderá estar a actuar contra guppies que
sejam arrastados rio abaixo durantes os períodos de cheias
Palavras-chave: Guppy (Poeciliareticulata), reotaxia, piscina comportamento, migração, seleção natural.
http://www.biotaneotropica.org.br
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69
Biota Neotrop., vol. 12, no. 3
Rheotaxis in Trindadian guppies
Introduction
Many freshwater ish species have an innate response to orientate
their bodies in water currents, a phenomenon known as positive
rheotaxis (Northcutt 1997). Unlike species without active swimming
abilities or other station-keeping adaptations (e.g. Blake et al. 2007),
this innate swimming response prevents the inevitable extinction of
closed populations subject to dominant downstream migration (cf.
Müller 1954 ‘drift paradox’). Rheotaxis also maximizes perception of
chemical cues, interception of prey, and minimizes energy expenditure
(Montgomery et al. 1999). From an evolutionary perspective,
rheotaxis allows animals to maintain a position within a stream
(station-keeping) which avoids potential itness costs involved with
emigration (McCormick et al.1998).
Guppies (Poecilia reticulata Peters, 1859) can be found in a wide
range of habitats, from riverine environments to lakes (Deacon et al.
2011).This species is also common in the aquarium trade; they have
been bred and kept in captivity since the 1920s (Deacon et al. 2011).
The hydrodynamic environment the ish in wild populations encounter
is dramatically different. In the mountainous region of the Caroni
Drainage in Trinidad, the ish are exposed to seasonal lash-looding
events, coinciding with the wet-season rains (van Oosterhout et al.
2007a). In contrast, the guppies from ornamental strains in
aquaculture and those occurring in natural lakes never encounter
high water velocities or lash-looding. For example, the Pitch Lake
in Trinidad is a lat crater with pitch and asphalt folds that create
several freshwater pools. It is approximately 0.8 km2 and guppies in
this habitat experience little or no water currents. Here we hypothesize
that guppies have adapted to the hydrodynamic conditions typical for
their habitat. In particular, we predict that the guppies in the Pitch Lake
may have lost their innate rheotaxic behaviours. Similarly, we predict
that due to relaxed natural selection in captivity (van Oosterhout et al.
2007b) ornamental strain guppies will show little station-keeping
behaviour. In contrast, guppies from a riverine habitat are predicted
to show more pronounced rheotaxis and station-keeping.
Materials and Methods
1. Experimental animals and procedure
The behaviour of 60 adult guppies from three populations in
Trinidad were studied: the Upper Naranjo (UN: Grid Ref. UTM 20P
693443, 1183935), the Lower Aripo (LA: 694432, 1178141) and the
Pitch Lake (PL: 650459, 1131727). Additionally, ornamental strain
guppies (OS, n = 20) belonging to the Istanbul strain were tested for
their rheotactic or station-keeping behaviours. The UN is a small
upstream tributary of the Aripo River. The mean water low rate of
upstream sites is signiicantly higher than in the downstream sites
(upstream ≈8.7 cm.s–1; downstream ≈5.5 cm.s–1, see Reznick et al.
2001). This set of populations was chosen to test the hypothesis that
riverine ish populations that experience seasonal loods in the wild
(i.e. the UN and LA populations) display stronger station-keeping
behaviours than guppies from a natural or captive environment with
little or no natural water currents (i.e. the PL and the OS guppies). All
ish were collected at the end of the dry season (March-June) in 2009
where the water depth and low rate was comparable to Reznick et al.
(2001) observations.
In total, 20 guppies per population with approximately
equal sex ratio and similar size range were used: standard length
SL = 12-25 mm, (mean (±SD): SL = 18.3 (±1.2) mm). Guppies were
maintained in four 80 L aquaria in groups of 35-60 ish per tank.
They were screened for parasites following the protocol described in
van Oosterhout et al. (2003) and Schelkle et al. (2009). These screens
http://www.biotaneotropica.org.br/v12n3/en/abstract?article+bn01512032012
were conducted because guppies infected with Gyrodactylus spp. are
more likely to be swept downstream than uninfected counterparts van
(van Oosterhout et al. 2007a). Briely, guppies were anaesthetised
with 0.02% MS222 and using a stereo-microscope and ibre optic
illumination, gyrodactylids were removed with watchmaker’s
tweezers. Fish were clean of all ectoparasites and showed no
symptoms of disease in the two weeks prior to the experiment.
The behaviour of guppies was recorded in an artiicial stream
(length × width × depth = 112.2 × 12 × 4.0 cm3). The water low rate
was 15.4 (±1.2) cm.s–1, comparable to their mean critical swimming
speed (Syriatowicz & Brooks 2004). The artiicial stream was divided
into 11 segments of 10.2 cm each, with a downstream weir which led
to a small pool. The focal ish was released into the sixth segment
in the middle of the stream. Its position was recorded at 5 seconds
intervals over a period of 240 seconds. The experiment was terminated
after 240 seconds or when the focal ish went across the weir into the
pool (i.e. swept downstream). Post release, all monitoring was done
via video to avoid disturbance to the ish.
The incidence of guppies being swept downstream was noted,
and the average position of a guppy in the river and its mobility (i.e.
average distance swum in 5 seconds intervals) during its time in the
stream was calculated. A previous study using an artiicial stream
showed that guppies were not attracted to conspeciic chemosensory
cues (Archard et al. 2008). Hence, we used tank water that was
recycled throughout the experiment. The water temperature was 27.0
(±1.0) °C and recordings were made between 0700-1700 h under
indirect natural daylight in June 2009.
2. Statistical analyses
A binary logistic regression analysis (logit) with a dichotomous
dependent variable (“swept downstream” or “kept station”) was used
to test whether the incidence that a guppy was swept downstream
was explained by the origin of population, sex and SL. The model
had three predictors: ‘Population’ and ‘Sex’ as ixed factors, and ‘SL’
as covariate. The model was itted using an iterative re-weighted
least squares algorithm to obtain maximum-likelihood estimates
of all parameters. The log-likelihood was used to test whether the
coeficients of the predictors were signiicantly different from zero.
A logit link function was used to calculate the odds ratio and its
95% conidence interval (CI). Differences in the mean position
of guppies in the stream between populations, sexes and SL were
tested using a General Linear Model (GLM). We also used a GLM
to compare the mobility of guppies among populations, sexes and
SL. In these models, Population and Sex were ixed factors, and SL
was the covariate. We checked whether the data were appropriate
for parametric analysis and conirmed homogeneity of variances
and normal distributions of residuals. All tests were conducted in
Minitab 12.1.
Results
Guppies from the UN were signiicantly less likely to be swept
downstream than their LA counterparts (Binary Logistic Regression:
Z = –2.47, p = 0.014), mean and 5-95%CI odds ratio = 0.11 (0.020.64). However, there was no signiicant difference in the likelihood
of ish being displaced downstream between the other populations
(OS guppies: Z = –1.83, p = 0.068; PL guppies: Z = –1.25, p = 0.212)
(Figure 1). The Sex and SL of guppies did not explain variation in
the probability being swept downstream (Z = 0.47, p = 0.636 and
Z = 0.17, p = 0.862, respectively).
There was a signiicant difference in the mean position of ish
among populations (F3,74 = 4.32, p = 0.007), with the UN being on
average most upstream, and the OS the furthest downstream (see
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70
Mohammed, R.S. et al.
Figure 2). Fish size (SL) and Sex did not affect the position of ish
within the artiicial river (F1,74 = 0.16, p = 0.692, and F1,74 = 1.87,
p = 0.161). There were signiicant differences in mobility between the
ish of the four populations (GLM: F3,74 = 3.71, p = 0.015) without the
inclusion of Sex and SL data. However, SL did not explain variation
in mobility between the ish (GLM: F1,74 = 0.61, p = 0.438), and there
was no difference between the Sexes (GLM: F1,74 = 0.89, p = 0.414).
The UN ish were signiicantly less mobile than ish of the other three
populations, moving on average 6.0 cm per 5s, compared to 11.4,
9.1 and 9.3 cm per 5s for the LA, PL and OS guppies, respectively.
Discussion
Guppies from the upstream population, the Upper Naranjo (UN)
were signiicantly less likely to be lushed downstream than Lower
Figure 1. Number of ish that remained stationary and retained their position in
the artiicial stream (grey bars) and ish swept downstream over the weir into
the pool (black bars) in the four populations. UN guppies were signiicantly
less likely to be swept downstream than LA guppies (see text).
Figure 2. Box plot showing the average position of guppies in the artiicial
stream. Dots represent outliers, bars show the lower and upper limits and the
box represents the irst and third quartile value with the median. There was a
signiicant difference between the mean positions of ish among populations
(see text).
http://www.biotaneotropica.org.br
Aripo (LA), Pitch Lake (PL) and ornamental strain (OS) guppies.
We hypothesised that wild ish, experiencing seasonal loods (i.e.
the UN and LA populations) should display stronger rheotaxis or
station-keeping behaviours than guppies in habitats with little or no
natural water currents (i.e. the PL and the OS guppies). The results
are inconsistent with our hypothesis, and suggest that the level of
rheotaxis of guppies in populations that are not subjected to seasonal
looding is similar to that of guppies occurring in (lowland) rivers
which are regularly in spate-conditions.
First, we consider the hypothesis that the relatively reduced level
of station-keeping observed in the high-predation LA guppies can be
explained by a trade-off between escape-response versus swimming
endurance. The UN guppies live a low predation environment,
whereas the LA has high predator pressure on the guppies
(van Oosterhout et al. 2007). Selection favours enhanced escaperesponse in high predation sites, a behaviour known as fast-start
evasion response or c-start (Ghalambor et al. 2004). Could adaptations
favouring the c-start compromise rheotaxis and swimming endurance
in the high-predation LA? To answer this question we need to consider
the station-keeping behaviour of the Pitch Lake and the ornamental
guppies, which originate from habitats with little or no predation.
Similar to the low-predation UN guppies, these populations do not
experience strong selection for c-start. Nevertheless, Pitch Lake and
ornamental guppies are equally prone to being swept downstream as
the LA guppies. This suggests that the hypothesised trade-off between
escape-response versus swimming endurance in the LA cannot be
held responsible for reduced station-keeping performance in all three
populations (i.e. LA, PL and OS).
Reduced predator fauna has been shown to increase the
number of guppies that occupy the fast lowing regions of the river
(Kodric-Brown & Nicoletto 2005). Flow rates in upstream sites
are, on average, greater than in downstream sites (Reznick et al.
2001). Furthermore, upstream guppies that are not discouraged
(by piscivorous predators) from deeper or faster lowing regions of
the river are presumably more likely to develop peduncle muscle
in response to exposure to high low rates (e.g. Nicoletto 1996).
Therefore, increased rheotactic behaviour in the UN may be a plastic
response to reduced predator fauna in a fast lowing river. Darden &
Croft (2008) found that in high predation (lowland) sites, predation
risk is greater in the deeper regions of a river. Interestingly, the authors
also found that, in response to male presence, females will move into
deeper waters, thereby increasing their predation risk (Darden & Croft
2008). The authors argue that this behaviour may increase the risk
of female predation, but that this cost is balanced by a reduced level
of harassment from males. It is conservable that in low predation
(upstream) sites males do not suffer such increased predation risk
in high low regions and therefore only those males able to display
and maintain their position in faster lowing regions of the river pass
on their genes (e.g. Kodric-Brown & Nicoletto 2005). The indings
in the present study and those in previous studies (Kodric-Brown &
Nicoletto 2005, Darden & Croft 2008) suggest that a reduction in
predator fauna in upstream sites may drive both phenotypic plasticity
(in development of peduncle muscle) and selection toward increased
rheotactic behaviour in the UN guppies.
Fish that are displaced from the UN during seasonal lood events
may be prevented from returning upstream by barriers to gene low
such as waterfalls (Crispo et al. 2006, van Oosterhout et al. 2007a).
Compensatory upstream migration in the lowlands may allow the
return of displaced ish that have not been swept over such barriers
(see Barson et al. 2009, Willing et al. 2010). In addition, distinct
differences exist in predator and parasite faunas between upland
and lowland habitats (Endler 1980, Reznick et al. 2001, Cable &
van Oosterhout 2007). Several translocation experiments have
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Rheotaxis in Trindadian guppies
shown that guppies are particularly well-adapted to cope with the
local biotic and abiotic environmental conditions (e.g. Gordon et al.
2009). For example, guppies that evolved in a low-predation upland
habitat have reduced anti-predator responses such as shoaling
behaviour (Huizinga et al. 2009). Furthermore, the males tend to
be more colourful, which make them vulnerable to visually-hunting
predators that are common in the lowland environment (Endler
1995). Consequently, selection will favour behavioural responses that
increase site idelity (Winker et al. 1995, Aparicio & De Sostoa 1999).
It is therefore likely that in the low-predation upland population of the
UN, natural selection has promoted lush avoidance behaviour and
positive rheotaxis. In contrast, even after downstream displacements
during floods, lowland guppies of the LA population will find
themselves in a similar, high-predation habitat to which they are
adapted. We propose that the combination of a larger low rate in the
upland habitats in combination with the dramatic itness consequences
for upland guppies that are unable to resist lash-looding has resulted
in strong selection for station-keeping in the UN. This could explain
why the UN guppies show the highest level of rheotaxis.
Croft et al. (2003) showed sex-biased dispersal in guppies,
demonstrating a signiicant bias for upstream movement by males but
not females. In addition, they found a positive correlation between
body length and distance moved in females. van Oosterhout et al.
(2007a), on the other hand, showed that males with parasite infections
were more likely to be swept downstream during wet-season loods
than females. The current study did not detect differences in rheotaxic
behaviour between the sexes, and the size of ish did not explain
differences in this behaviour. Instead, most variation was explained
by the population origin of the ish.
Although our data can be explained by differences in selection
pressures between populations, we cannot rule out that these results
can be explained also by proximate (mechanistic) differences between
populations. Future anatomical, behavioural and genetic studies into
rheotaxis of guppies seem warranted, as due to the strong gradient
in selection pressure the expression of this behaviour should vary
predictably across the environment.
Acknowledgements
We thank Mr and Mrs Rasheed Mohammed for their support,
Gabrielle Archard and Thomas Breithaupt for comments on the MS
and Raquel S. Xavier for Portuguese translations. This work was
supported by a Natural Environment Research Council studentship
to MM (NER/S/A/2005/13362A), a Biotechnology and Biological
Sciences Research Council CASE studentship to BS (BB/D526137/1)
and a European Community Framework Programme 6 (MTKDCT-2005-030018).
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Received 05/04/2012
Revised 02/08/2012
Accepted 06/08/2012
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