ORIGINAL ARTICLE /ARTÍCULO ORIGINAL

A BEHAVIORAL EXPERIMENTAL APPROACH ON THE TRANSMISSION OF

GYRODACTYLUS (MONOGENEA) OFF THE 3-SPINE STICKLEBACK

(GASTEROSTEUS ACULEATUS L.)

UN ENFOQUE EXPERIMENTAL SOBRE EL COMPORTAMIENTO EN LA

TRANSMISIÓN DE GYRODACTYLUS (MONOGENEA) FUERA DEL HOSPEDERO

'EL PEZ ESPINOSO' (GASTEROSTEUS ACULEATUS L.)

1* 2

Mayra I. Grano-Maldonado & José C. Sánchez-Ferrer

1Ecophysiology Laboratory, Faculty of Marine Sciences, Autonomous University of Sinaloa, Paseo Claussen s / n. A. P. 610.

Mazatlan, Sinaloa, Mexico, email: grano_mayra@hotmail.com

2Faculty of Sciences, National Autonomous University of Mexico México, email: sferrer@ciencia.unam.mx

Neotropical Helminthology, 2016, 10(1), ene-jun: 51-59.

ABSTRACT

Keywords: Behavior - Gyrodactylus - Gasterosteus aculeatus - Monogenea - Transmission

The aim of this study was to investigate some behavioral transmission factors of gyrodactylids

and to ascertain how maturity and reproductive status may be employed in the colonisation of

new hosts using the Gyrodactylus gasterostei Gläser, 1974 and G. arcuatus Bychowsky,

1933—Gasterosteus aculeatus L. transmission model from dead fish. Laboratory experiments

included determining the maturity (presence of male copulate organ) and reproductive (presence

of daughter) status of transmitting worms, in order to consider the behavioral factors that

influence parasite choice to migrate to a new individual of the same host species. This is the first

behavioral experimental study of the different developmental stages of two different species

gyrodactylids using the stickleback model. Indeed, the results showed the comparison between

behavioral frequencies and individuals. The analysis was elaborated among all individuals who

survived the observational period, Behavioral differences related to maturity or some other

characteristic were noted. The present work examines the initial ethological aspects of these

behavioral strategies in detached and individual gyrodactylids. It is remarkably difficult to

establish a behavioral measure of Gyrodactylus in the laboratory during most observations; data

analysis showed no behavioral differences among these monogenean species.

ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

RESUMEN

Palabras clave: Comportamiento – Gyrodactylus - Gasterosteus aculeatus – Monogenea - transmisión

El objetivo de este estudio fue investigar algunos factores en el comportamiento durante la

transmisión del monogeneo Gyrodactylus sp. y determinar si la madurez y estado reproductivo

del parásito pueden ser empleados en la colonización de nuevos hospederos. El modelo de

transmisión empleado fue Gyrodactylus gasterostei Glaser, 1974 y G. arcuatus Bychowsky 1933

- Gasterosteus aculeatus L. que migraron de peces sacrificados. Los experimentos en el

laboratorio incluyen la determinación de la madurez (presencia del órgano copulador masculino)

y reproductiva (presencia de la hija en útero), y determinar los factores de comportamiento que

influyen en la elección de los parásitos para migrar a un nuevo hospedero. Este estudio es el

primer enfoque experimental en el comportamiento con relación a diferentes etapas de desarrollo

en dos especies de Gyrodactylus utilizando el mismo modelo de hospedero. El presente trabajo

examinó los aspectos iniciales del comportamiento de las estrategias de comportamiento en

gyrodactilidos aislados de forma individual. Los resultados muestran que la comparación de las

frecuencias de comportamiento entre los individuos que sobrevivieron al registro de

observaciones y el análisis de los datos no mostró diferencias de comportamiento entre estas

especies de monogeneos.

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

INTRODUCTION

In nature, the interaction between parasite and

host has a dual response; it is this interaction

and diverse routes that makes the study of

parasites and their infective stages a

remarkable study. Gyrodactylids are

monogenean flukes with a direct life-cycle,

and are capable of rapid multiplication. Harris

(1985) described this mode of reproduction as

being fairly unique, allowing rapid population

growth on their host and conferring an ability

to transfer to a new host at all times during their

life-cycle. As parasites, gyrodactylids are

forced to employ a range of “successful”

strategies in order to reach their target, a new

fish. During this process of transmission or

colonisation, gyrodactylids appear to display

and adapt to the behaviour of the hosts using a

wide range of behaviours in their transmission.

In particular, it was suggested that individual

gyrodactylids moved to the surface film of the

water and that therefore, as guppies are surface

feeders; detached parasites were more likely to

contact a new host (Cable & Harris, 2002), by

swimming-like behaviour in the water column

e.g. G. rysavyi (El-Naggar et al., 2004),

Ieredactylus rivuli (Schelkle et al., 2011) and

transmitting from dead hosts, suggesting that

they might provide a significant reservoir of

infection (Olstad et al., 2006) during

scavenging feeding (Grano-Maldonado,

2014b).

Behavioural flexibility in gyrodactylids may

be important in the transmission process.

Parasites that had not yet given birth for the

first time were suggested to be less likely to

transfer to a new host than worms that had

already given birth at least once (Harris, 1985).

Little is known regarding the biological basis

of gyrodactylid behavioural during host

selection and the maturity factors underlying

Grano-Maldonado & Sánchez-Ferrer

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

Source of hosts and parasites

A G. gasterostei / stickleback model was used

for the purposes of this study. Fish used for the

study were collected along specimens were

collected on previous methodology (Grano-

Maldonado 2014a, b). This experiment was

designed to examine the behaviour

characteristics of worms (n=31) moving off

dead hosts at 10°C. For this experiment we

hypothesised that host transfer might be more

favoured in those parasites having MCO (male

copulatory organ) and absence of daughter

present in uterus. Individual sticklebacks were

-1

euthanised with an overdose (0.01·L ) of

anaesthetic 2-phenoxyethanol (Merck-

Germany) and were placed in individual Petri

dishes containing clean water at 10 ± 1º C.

Dead hosts were observed under an Olympus

SZ30 stereomicroscope at different

magnifications, with the time at which each

gyrodactylid looped off the fish during 60 min

being recorded for each individual

gyrodactylid. Worms detaching naturally from

the host tissue within 60 min were then used for

analysis. Worms were carefully removed with

a 200 µl pipette and were placed individually

into 3 cm Petri dishes containing 5ml of

filtered (0.45 µm Minisart Sartorius Stedim,

Biotech) water taken from the same source as

that used for fish maintenance and incubated at

10°C. There are several observation

techniques that are used to record performance

or behaviour including i.e frequency, rate,

duration and interval recording. All of these

techniques rely on precisely identifying the

behaviours in observable and measurable

performance terms and to make the results

consequential and consistent. The target

gyrodactylid behaviour may need to be defined

in a way that it is observable and measurable, if

exist. Clearly identifying specific behaviours

being observed makes communicating and

interpreting the results of the observation more

accurate. We refer the term Frequency counts

transmission, particularly with respect to the

behavioural-mature status of gyrodactylids

moving to new hosts. The use of the sensory

and motor abilities to active and modify its

behaviour patterns allowing transmission to

new host promoting a parasite ability to

survive and reproduce. Host behavioural

changes due to parasitism have been studied

(Levri, 1999) and are often assumed to be

adaptations of the parasite. However,

behavioural aspects of parasites as

gyrodactylid may be a general response

biological characteristic for parasite

transmission. For this reason, alternatives

behavioural studies which consider the stage

development hypothesis should be tested. As

Gyrodactylus has no specific transmission

stage in its life-cycle, movement between hosts

must be achieved by strategies employed by

the adult. Species employ to interpret both

their host and ambient environments

employing structural features, such

information may assist in the interpretation of

transmission behaviours, like in this particular

case. This transfer may be facilitated by the

response of mechanoreceptors present on the

tegument, detecting the aquatic turbulence

(Grano-Maldonado, 2011a) or their responses

to chemical stimili (ie. fish) or the presence of a

photoreceptor, which register the shadow

produced by a passing fish could increase the

chances of a successful transmission which

gyrodactylids employ in host location during

the transmission process (Grano-Maldonado

2014a).

The aim of this study is to assess the

behavioural flexibility concerning maturity

and reproductive stage employed the

Gyrodactylus gasterostei Gläser, 1974 and G.

arcuatus /Gasterosteus aculeatus L. infection

model to examine these questions, concerning

transmission process off the host. The present

work examines the ethological initial aspects

of these behavioural strategies in detached and

individual gyrodactylids.

Behavioural transmission in gyrodactylids

MATERIALS AND METHODS

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Grano-Maldonado & Sánchez-Ferrer

magnification. Additionally, parasites were

identified to species through morphological

and morphometric analysis of the

opisthaptoral hard parts as described in Grano-

Maldonado (2014a,b).

Data analysis

All data were analysed by comparing

behavioural frequencies and developed status

among all the individuals (G. gasterostei and

G. arcuatus) which survived the observational

record. Also, to determinate the behavioural

differences between them not parametrical

statistical tests, Kruskal-Wallis and Mann-

Whitney, were employed. All statistical

analyses were performed using the software

SPSS version 20.

These experiments were carried out with a

view to gaining some insight into the

transmission strategies of gyrodactylids and

individual behaviour during transmission off

the fish host. During 31 h of observation of 31

individuals of recorded video, from 12

conducts originally described, just 8 conducts

were used and identified these behaviours

being described in this study in terms of

possible transmission. The comparison of the

behavioural frequencies between all

individuals (G. gasterostei and G. arcuatus)

showed there are not statistically significant

differences (Kruskal-Wallis Test; χ=25.36;

df=30, p=0.70). The average of the twelve

behaviours recorded in G. gasterostei and G.

arcuatus during the observation period shown

in Table 1. Comparative analysis showed that

there were no statistically significant

differences between the behavioural pattern of

both species (U = 62.0, p = 0.56).

(a record of the number of times a specific

behaviour occurs within a specific period of

time). Frequency counts are useful for

recording behaviours which have; a clear

beginning and ending, are of relatively short

duration, and tend to occur a number of times

during the specified time period (Martin &

Bateson, 1993; Lehner, 1998).

Twelve basic behaviours were observed and

evaluated; each specimen was observed every

minute by the method denominated “scan

sampling” according with Martin & Bateson

(1993). The behavioural record elaborated for

this study was based in gyrodactylid individual

activities under the microscope every minute

during 60 min. The data obtained of the

occurrence of each behaviour was recorded: A.

motionless - attached only by their haptor

(worm static); B. Haptor attached and

exploring surroundings; C. Looping “worm

moving” across the dish; D. Haptor detached

from dish (no twitching); E. Haptor attached

from dish and twitching; F. Haptor detached

and twitching; G. Erratic movements (moving

in a way that is not regular twitching); H.

Haptor detached but head attached to bottom;

I. Keeping a “C” body shape and no twitching;

J. Keeping a “C” body shape and twitching; K.

Motionless (no moving but non dead); L. Mom

Gives birth. Worms were considered dead

when no movement were noticed after a gentle

touch within a needle. Following observation,

each worms were fixed in 10% neutral

buffered formalin (NBF), each specimen was

then mounted on a glass slide in a drop of

distilled water ensuring that the haptoral hooks

were flat, stained and fixed in situ by the

addition of a drop (~3 µl) of Malmberg's

fixative (ammonium picrate glycerine, APG;

saturated picric acid and 100% glycerin) to the

edge of the coverslip which was drawn under

the coverslip by capillary action. The coverslip

was then sealed with transparent nail vanish.

The maturity and reproductive status of worms

were recorded using a compound microscope

(Olympus BX51) at 100× / oil immersion

RESULTS

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

who gave birth, regardless of the species. The

analysis showed no statistically significant

differences in the condition of presence or

absence of a daughter (χ =0.37, df=2, p=0.85).

Behavioural averages frequencies are

presented in Table 2.

Because no significant differences between the

behavioural pattern of individuals and species

were observed, we compared using the

Kruskal-Wallis test, behavioural patterns

among individuals with presence of a

daughter, without the presence of daughter and

Behavioural transmission in gyrodactylids

Table 1. Behavioural pattern displayed by Gyrodacylus arcuatus and G. gasterostei off the host. Values express the

average frequencies ± SD.

Table 2. Behavioural pattern exhibited by individuals who gave birth, with a daughter without daughter. Values

express the averages frequencies ± SD.

G. arcuatus G. gasterostei

Behaviour Average SD Average SD

A 38.50 29.99 30.07 19.89

B 33.25

24.42

26.26 19.08

C 23.25

21.50

17.44 19.20

D 47.25

24.12

32.33 22.46

E 7.75

8.30

1.67 3.49

F 39.25

30.43

30.70 20.27

G 15.75

18.55

5.93 13.13

H 0.75

0.96

4.00 5.51

I 5.75 6.24 6.63 9.64

J 0.00 0.00 0.19 0.40

K 6.00 5.48 8.30 9.24

L 1.00 2.00 0.59 3.08

Gave birth With a daughter Without daughter

Behaviour Average SD Average SD Average SD

A 22.25

6.85

32.69

20.63

32.29 24.21

B 19.50

10.41

27.15

20.48

29.36 21.06

C 14.25

13.74

17.85

21.00

19.64 19.89

D 36.00

20.72

32.31 23.59

35.57 24.15

E 0.50

1.00

1.85 4.41

3.57 5.39

F 29.50

9.85

28.46 20.32

35.57 24.96

G 1.00

2.00

7.31 15.80

8.86 14.27

H 4.25

2.22

2.38 4.74

4.50 6.28

I 6.75

7.89

6.46

12.23

6.50 6.53

J 1.00 0.00 0.08 0.28 0.00 0.00

K 13.50 7.77 3.85 5.37 10.29 10.32

L 0.00 0.00 1.54 4.48 0.00 0.00

showed that the behaviour is not affected by

the presence of a MCO (U=66.0, p=0.73).

Behavioural averages frequencies are

presented in Table 3.

We conducted a second analysis by Mann-

Whitney test to compare the behavioural

pattern with respect to the presence or absence

of the male copulatory organ (MCO) in

individuals regardless of species. This analysis

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Grano-Maldonado & Sánchez-Ferrer

Table 3. Behavioural pattern exhibited by individuals with MCO and without MCO. Values express the averages

frequencies ± SD.

With MCO Without MCO

Behaviour Average SD Average SD

A 29.44 19.19 33.54 23.88

B 25.61 19.35 29.31 20.33

C 15.39

16.37

22.08 22.72

D 30.44

22.33

39.54 23.32

E 0.78

1.77

4.77 6.31

F 30.06

18.77

34.23 25.16

G 5.11

11.17

10.08 17.18

H 3.78

4.31

3.31 6.54

I 6.06 7.21 7.15 11.70

J 0.28 0.46 0.00 0.00

K 9.61 10.44 5.77 5.51

L 1.11 3.83 0.00 0.00

DISCUSSION

This study suggests that there are no

significant differences between the

behavioural pattern in G. gasterostei and G.

arcuatus concerning the presence of a daughter

in uterus or the presence of MCO. These

factors did not affect the host-seeking

behaviour, and potentially the transmission

success may affect in a similar manner. The

observed host-seeking behaviour of

gyrodactylids during this study may increase

transmission success of gyrodactylids species.

Decreased host-seeking behaviour during this

time may also result in reduced movements

towards the end of the observation; this may be

for a possible temperature raise, thus also

affecting the fitness of the worm parasite.

However, every 5 min 5ml of cold water were

add to keep the outside Petri dish cool;

additional effects of infection by species

remain to be elucidated and further studies

could include measures of fitness, such as

longevity under the same experimental

circumstances.

One of the first descriptions of a specific

migratory behaviour that facilitates

transmission of a gyrodactylid from dead hosts

was detailed by Cable & Harris (2002). These

latter authors described the method by which

Gyrodactylus turnbulli Harris, 1986 and its

hosts, guppies Poecilia reticulata (Peters),

come into close contact. After death, guppies

float at the water's surface, its burden of G.

turnbulli parasites move off these fish into the

water film, hanging motionless with the haptor

held by surface tension. Since guppies are

surface feeders, detached parasites in the water

film are using this host's behaviour to increase

the likelihood of contacting a new host.

However, the majority of gyrodactylid species,

if they are dislodged from the host's skin host,

they sink until they reach a solid surface (Cable

& Harris, 2002). Another interesting case of

gyrodactylid behaviour was reported by El-

Naggar et al. (2004). These authors suggested

that Gyrodactylus rysavyi Ergens, 1973 was

capable of directional swimming by flexing its

body, this involving ~4-8 per sec looping

contractions in any direction with a speed of

~1.7-5mm/sec and a range of ~15cm distance.

This motility was suggested to be an

exceptionally efficient infection mechanism

with respect to the Nile catfish Clarias

gariepinus (Burchell) host. By comparison,

these authors reported that the closely related

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

approach concerning different developmental

stages on two different species gyrodactylids

using the stickleback model. These results

showed that the behaviour is not affected by

the presence of daughter o penis (MCO) and

behavioural sequences are very similar

between species (they perform singular

movements in the same way). However,

Grano-Maldonado (2011, 2014b) showed that

the presence of the MCO favoured migration

to a new fish host of the same species. Thus,

those individuals with MCO present will

colonise sooner and consequently have more

time available to find a new host once detached

(Grano-Maldonado, 2011, 2014b). The present

study was a part of an experimental section

from an extensive previous research (Grano-

Maldonado, 2011a; Grano-Maldonado et al.,

2011; Grano-Maldonado 2014a,b; Grano-

Maldonado & Palaiokostas, 2015). The

maturity and reproductive status of parasites

that transferred to live hosts was recorded and

it was found that 65.6% of the parasites had a

MCO present whilst 54.2% had a daughter in

utero (Grano-Maldonado 2014b) during this

research resulting that parasites with MCO

presence (p<0.05) showed a significantly

higher probability of transmission. However,

there are no significant differences between

Gyrodactylus species and behavioural

conduct.

We attempted to link the previous research

which developed from the same fish

model/parasite and similar experimentation set

up. In previous research, it was identified the

presence of structures: ciliated photoreceptor

located sub-surface, localised in close

proximity to the spike sensilla in monogeneans

as reported by Watson & Rohde (1994) and

sense organs were conducted on the works of

Lyons (1969, 1973). It is possible that parasites

may initially detect water movements

associated with an approaching host and then

prepare themselves for attachment employing

mechano-chemical and photo receptors

(Grano-Maldonado, 2014a). To date, few

Macrogyrodactylus congolensis (Prudhoe,

1957) Yamaguti 1963 and M. clarii Gusev

1961 does not possess the ability to swim, even

though they parasitized the same Nile catfish

host. Another clear example, Schelkle et al.

(2011) suggested a swimming-like behaviour

for the gyrodactylid Ieredactylus rivuli from

Rivulus hartii (Boulenger, 1890) in Trinidad.

Gyrodactylids use a variety of different

strategies to infect new hosts (Bakke et al.,

2002), but robust experimentation to test these

possible strategies is lacking.

One observation suggests gyrodactylids can

transmit from dead hosts when live fish

cannibalise the carcass of an infected one

(Olstad et al., 2006). This behaviour would

increase the chances of parasites contacting a

new fish host, particularly if potential hosts are

either scavengers or benthophagous feeders.

Gyrodactylus species usually have preferred

sites on their host which, depending on the

transmission strategy to facilitate their

transmission to new host (Grano-Maldonado,

2011; 2014b). Gyrodactylids disperse

effectively using a variety of mechanisms, but

the most common is most likely through

contact between living hosts. The transmission

could be by direct host contact, via dead fish

(scavenging or food items), transmission also

occurs by contact with dead hosts, parasites

attached to the substratum and worms drifting

in the water column (Bakke et al., 1992;

Soleng et al., 1999, Cable & Harris, 2002;

Grano-Maldonado, 2011, 2014b). In benthic

species, such as the 3-spine stickleback,

transmission via the substrate is noticeable and

can be one of the most important routes of

transmission. Some gyrodactylids are capable

of reproducing on several hosts, whilst on

others they are unable to reproduce.

Nevertheless, the colonisation of a host on

which reproduction cannot occur may still play

a role in the transmission of the parasite

towards its final host (Bakke et al., 1992).

This study is the first behavioural experimental

Behavioural transmission in gyrodactylids

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Grano-Maldonado & Sánchez-Ferrer

swimmin g perform ance at every

developmental fish stage i.e. larvae or adult.

Unfortunately, in our study, we did not

consider the possible effect of formaldehyde in

the sticklebacks-host, when it was employed to

reduce in some cases the parasite load. In the

best of our knowledge, all fish used in the

experiments did not present any erratic

behaviour or skin disorder. The G. gasterostei,

G. arcuatus / Gasterosteus model is a simple

and successful system to examine aspects of

transmission of parasites from fish. Future

studies to evaluate the tolerance to

formaldehyde including possible gill and skin

epithelium damage which may affect

gyrodactylid transmission in sticklebacks

warrant further investigation. Thus, further

studies, such as power analysis to determine if

any effect would emerge with a higher sample

size, would likely reveal useful information;

also, considering that gyrodactylids may not be

comparable with other behavioural patterns

from more evolved organisms.

studies have explored the effect of some

chemical compounds on the behaviour

transmission of Gyrodactylus species on both

their vertebrate hosts (Brooker et al., 2011).

This study provides the first example of a

measurable behavioural approach to

Gyrodactylus species during migration off the

host.

A significant difference was not observed

between numbers of parasites with daughter or

MCO; however, it is likely that results for

Gyrodactylus species were confounded by

temperature, which may inhibit host-seeking

behaviour. Gyrodactylids become less active

as physiological age increases or experience

environmental responses of receptors that may

signal the presence of a fish close by, and they

may be more susceptible to infection (Grano-

Maldonado, 2014a). Indeed, the results show

the comparison in behavioural frequencies

between individuals; this analysis was

elaborated among all individuals who survived

the record, and if whether there behavioral

differences between them life status (i.e

presence of daughter or MCO), or some other

characteristic.

Regarding the data analysis no behavioural

differences are among species. Taking into

consideration, other possible factors affecting

transmission in gyrodactylids, we may

consider that skin and gills are in contact with

the external environment and may be subject to

morphological, histopathological and

behavioural changes when exposed to

substances which may 'damage' tissues or

'affect' gyrodactylid transmission, i.e

anaesthetic (Grano-Maldonado &

Palaiokostas, 2015) did not have an effect on

gyrodactylid transmission. However,

formaldehyde (Pahor-Filho et al., 2014)

caused mild to severe hyperplasia and

detachment of respiratory epithelium in the

gills of juvenile Mugil liza (Valenciennes,

1836). The tolerance to formaldehyde may be

fish species-specific; also may affect

Bakke, T, Harris, P, Jansen P & Hansen, L.

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Bakke, T, Harris, P & Cable, J. 2002.

Brooker, AJ, Grano-Maldonado, MI, Irving, S,

Bron, J, Longshaw, M & Shinn AP. 2011.

Cable, J & Harris, P. 2002.

Host specificity and dispersal

strategy in gyrodactylid monogeneans

with particular reference to

Gyrodactylus salaris (Platyhelminthes,

Monogenea). Diseases of Aquatic

Organisms, vol. 13, pp. 63-74. Host

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gyrodactylid monogenean. International

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308.

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Gyrodactylus. Parasite Vectors, vol. 4,

pp. 207. Gyrodactylids

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Received February 22, 2016.

Accepted March 24, 2016.