International Journal of Acarology

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Cannibalism in Amblyseius largoensis (Muma)

(Acari: Phytoseiidae), an important natural enemy
of coconut mite pests

Jairo A. Mendes, Maria E. N. Barros, Debora B. Lima & José W. S. Melo

To cite this article: Jairo A. Mendes, Maria E. N. Barros, Debora B. Lima & José W. S. Melo
(2017) Cannibalism in Amblyseius�largoensis (Muma) (Acari: Phytoseiidae), an important
natural enemy of coconut mite pests, International Journal of Acarology, 43:5, 387-392, DOI:
10.1080/01647954.2017.1333526

To link to this article: https://doi.org/10.1080/01647954.2017.1333526

Published online: 26 May 2017.

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INTERNATIONAL JOURNAL OF ACAROLOGY, 2017
VOL. 43, NO. 5, 387–392
https://doi.org/10.1080/01647954.2017.1333526

Cannibalism in Amblyseius largoensis (Muma) (Acari: Phytoseiidae), an important

natural enemy of coconut mite pests
Jairo A. Mendesa, Maria E. N. Barrosa, Debora B. Limab and José W. S. Meloa
a
Departamento de Fitotecnia, Universidade Federal do Ceará, Fortaleza, Brazil; bDepartamento de Agronomia – Entomologia, Universidade Federal
Rural de Pernambuco, Recife, Brazil

ABSTRACT ARTICLE HISTORY

The phytoseiid mite Amblyseius largoensis (Muma) is an important natural enemy of two key coconut Received 26 March 2017
pests, the red palm mite, Raoiella indica Hirst (Acari: Tenuipalpidae), and the coconut mite, Aceria Accepted 16 May 2017
guerreronis Keifer (Acari: Eriophyidae). Amblyseius largoensis is considered a generalist due to its ability Published online 26 May
to feed on multiple food sources (e.g. phytophagous mites, small insects, plant exudates, nectar, and 2017
pollen). Specimens of A. largoensis sometimes attack each other in competitive situations. Thus, we KEYWORDS
hypothesized that intraspecific interactions, such as cannibalism, may occur when heterospecific prey Acari; phytoseiid mites;
are scarce. Experiments were conducted to determine whether, and to what extent, the availability of generalist; trophic
heterospecific prey, eggs of R. indica, influenced the tendencies of A. largoensis to cannibalise. interactions
Additionally, the oviposition of A. largoensis was measured in the presence and absence of both
conspecific nymphs and R. indica eggs. Overall, in the absence of the heterospecific prey, A. largoensis
consumed conspecific nymphs, and few eggs were produced, whereas in the presence of abundant
herbivorous prey, cannibalism decreased, and oviposition increased. These results suggest that, similar
to other phytoseiid mites, A. largoensis employs cannibalism as an adaptive survival strategy when
heterospecific prey is absent or scarce.

Introduction Based on diet breadth, A. largoensis has been classified as a

generalist (type III) (McMurtry and Rodrigues 1987; McMurtry and
The phytoseiid mite Amblyseius largoensis (Muma) is a widespread
Croft 1997; Luh and Croft 2001; Croft et al. 2004; McMurtry et al.
species that occurs naturally in tropical and subtropical regions,
2013). Generalist phytoseiids can feed on mites of various
often in association with perennial plants (Demite et al. 2016). This
families, including eriophyids, tarsonemids, tetranychids, and
species is the most common predator encountered on coconut
tydeids, as well as on various insect species, such as thrips or
palms (Cocos nucifera L.) (Lawson-Balagbo et al. 2008; Reis et al.
whiteflies (Gerson and Weintraub 2012). Further, generalist phy-
2008; Negloh et al. 2011; Melo et al. 2015), where it resides primarily
toseiids can also feed on plant exudates (James 1989; Kreiter et al.
on the leaves or exposed fruit surface and rarely under the bracts of
2002; Nomikou et al. 2003; Gnanvossou et al. 2005), nectar (van
coconuts (Lawson-Balagbo et al. 2008; Reis et al. 2008; Negloh et al.
Rijn and Tanigoshi 1999), and pollen (Broufas and Koveos 2000;
2011; Melo et al. 2015). Amblyseius largoensis is considered a natural
Abdallah et al. 2001; Nomikou et al. 2001; Vantornhout et al.
enemy of two key coconut pests, the red palm mite, Raoiella indica
2005). Some phytoseiids not only feed on phytophagous mites,
Hirst (Acari: Tenuipalpidae), and the coconut mite, Aceria guerreronis
insects, and plant products but also attack each other in compe-
Keifer (Acari: Eriophyidae) (Carrillo et al. 2012; Melo et al. 2015).
titive situations (e.g. Yao and Chant 1989; Zhang and Croft 1995;
Amblyseius largoensis is reportedly the most abundant predator
MacRae and Croft 1997; Schausberger 1997). Cannibalism, the
associated with the red palm mite on coconut leaves in several
killing and eating of conspecifics, is a widespread phenomenon
countries (Gallego et al. 2003; Roda et al. 2008; Peña et al. 2009;
in the animal kingdom (Fox 1975; Polis 1981; Polis et al. 1989;
Bowman 2010; Ramos et al. 2011; Zannou et al. 2010; Carrillo et al.
Elgar and Crespi 1992; Rosenheim et al. 1995) and often intensi-
2011; Taylor et al. 2011; Gondim et al. 2012). Several studies have
fies when heterospecific prey are scarce (Polis 1981; Polis et al.
demonstrated that A. largoensis was able to feed, develop, and
1989; Hironori and Katsuhiro 1997; MacRae and Croft 1997;
reproduce on a diet consisting solely of the red palm mite, showing
Schausberger 1997; Lucas et al. 1998).
a strong preference for red palm mite eggs over other stages of the
Several hypotheses have been proposed to explain canni-
pest (Carrillo et al. 2010; Carrillo and Peña 2011). In addition, A.
balism, including the following: (i) nutritional benefits to the
largoensis has been observed to prey on the coconut mite in the
consumer; (ii) reduction of competition for food, physical
field (Melo et al. 2015). The coconut mite resides under the perianth
resources (e.g. egg-laying sites), and/or shelters; (iii) achieve-
of fruits, where it feeds on the meristematic tissue and is protected
ment of superiority in reproductive competition by reducing
by floral bracts (Howard and Abreu-Rodriguez 1991; Sabelis and
the fitness of other individuals of the same sex; (iv) elimination
Bruin 1996; Ambily and Mathew 2003; Fernando et al. 2003;
of a potential predator; and (v) increasing survival and repro-
Siriwardena et al. 2005; Aratchige et al. 2007; Lawson-Balagbo
duction prospects of related individuals by eliminating geneti-
et al. 2007; Silva et al. 2017). The bracts of the fruit act as a physical
cally unrelated individuals (Elgar and Crespi 1992; Hamilton
barrier, hindering access to the microhabitat occupied by the coco-
1964a, 1964b, Schausberger 2003). Nevertheless, cannibalism
nut mite (Aratchige et al. 2007; Lawson-Balagbo et al. 2007; Lima
presents the following disadvantages: (i) risk of injury and of
et al. 2012; Melo et al. 2014, 2015). Because A. largoensis cannot
transmission of disease or parasites and (ii) loss of inclusive
access the area under the bracts, it likely preys on dispersed coconut
fitness if relatives are consumed (Elgar and Crespi 1992;
mites (Melo et al. 2015).
Pfennig et al. 1998). Thus, cannibalism may affect the

CONTACT José W. S. Melo wagnermelo@ufc.br; wagnermelo@hotmail.com Universidade Federal do Ceará - Campus do Pici, Departamento de
Fitotecnia – Entomologia, Avenida Mister Hull, n 2977, Bloco 805, Sala 215, CEP 60356-000, Fortaleza, CE, Brasil
© 2017 Informa UK Limited, trading as Taylor & Francis Group

Published online 26 May 2017

388 J. A. MENDES ET AL.
distribution and abundance of populations and species (Sih
et al. 1985; Hurd and Eisenberg 1990; Moran et al. 1996;
Walzer et al. 2001).
Although cannibalism has been reported and studied in
many phytoseiid species (see Schausberger 2003 for a review
of the evidence), it has not yet been explored in A. largoensis, a
species that is valued for its contribution to the biological
control of mite pests on coconut plants in tropical and sub-
tropical regions. According to Schausberger (1999, 2003), phy-
toseiids that are classified as generalists can discriminate
between conspecifics and heterospecifics and prefer to prey
upon the latter when given the choice. Herein, we investigated
the effects of the availability of R. indica eggs, the heterospe-
cific prey of A. largoensis, on the tendency of A. largoensis to
engage in cannibalism. Additionally, oviposition was measured
in the presence and/or absence of both juvenile predators and
herbivorous prey.
Materials and methods
Mite collection and rearing
Individuals of A. largoensis were obtained from coconut leaflets
in Fortaleza, Ceará State. Approximately 100 adults were trans-
ferred from leaflets to rearing units. Each rearing unit consisted
of a black PVC square (side length: 15 cm; 1 mm thick) laid onto
a disc-shaped foam mat placed in a plastic tray. The margin of
the PVC square was covered with a band of hydrophilic cotton,
and both the foam mat and the cotton band were saturated
with water on a daily basis via the addition of distilled water
into the tray. A tuft of cotton wool covered by a piece of
transparent plastic was placed in the centre of each rearing
unit, serving as the oviposition site for the predators. In each
unit, the predators were provided with fresh surplus amounts
of coconut pollen + pieces of leaflets (approximately 5 cm2)
containing nearly 300 individuals of all developmental stages
(immature stages and adults) of R. indica. Coconut pollen was
obtained from flowers collected from the field every month
and preserved in a sealed container at approximately 10°C.
Food was replenished every 3 days. The rearing units were
maintained in the laboratory at 27.0 ± 1.0°C and 70 ± 10%
Relative humidity (RH) with a 12:12 LD photoperiod.
Experimental procedures
The study was conducted under the same environmental con-
ditions as those maintained in the rearing units. Each experi-
mental unit was similar to a rearing unit, except that a 2.0 ×
2.0 cm square of jack bean (Canavalia ensiformes L.) leaf was
used instead of a PVC square. Gravid females (10–14 days after
egg hatching) were used as cannibals, and nymphs (2–3 days
after egg hatching) were used as conspecific prey. To obtain
the nymphs used as conspecific prey in the experiments, eggs
were collected from cohorts of gravid females and were trans-
ferred to experimental units prior to the experiment. To start
the experiment, eggs of predators were collected from estab-
lished colonies of 100–150 gravid females and placed on a new
unit. After 72 h, 10 nymphs were placed on each experimental
unit, with or without R. indica eggs (heterospecific prey), which
were collected from coconut leaflets. Adult A. largoensis females
were randomly withdrawn from the rearing units, starved for
~4 h prior to testing, and then singly introduced onto experi-
mental units. The following experimental conditions were eval-
uated: (i) a single female (adult predator, hereafter) placed in
the experimental arena with 60 R. indica eggs (prey, hereafter);
(ii) 10 predator nymphs (juvenile predators, hereafter) with 60
prey eggs; (iii) one adult predator with 10 juvenile predators
and 60 prey eggs; (iv) 10 juvenile predators; (v) 1 adult predator
with 10 juvenile predators; and (vi) 1 adult predator. Each
treatment unit constituted a single replicate, and each treat-
ment was replicated 20 times. The number of prey killed (juve-
nile predators and/or prey) and the number of eggs laid by
each predator were determined after 24 h. A previous bioassay
with R. indica eggs and without predator revealed that egg
mortality due to egg handling was very low (<5%), and thus,
no correction for performed.
Data analysis
All analyses were performed using SAS (SAS Institute 2001).
Prey egg consumption was normalized via square-root transfor-
mation, submitted to analysis of variance, and compared using
Tukey’s test. Juvenile predator mortality and oviposition were
analysed using 2-factor generalized linear models with a normal
distribution of errors. To analyse the juvenile predator mortality,
only data obtained from treatments with juvenile predators (ii,
iii, iv, and v) were included in the models, and the explanatory
variables were “presence of adult predators” (YES or NO) and
“presence of prey” (YES or NO). To analyse oviposition, only
data from treatments with an adult predator were included in
the models (i, iii, v, and vi), and the explanatory variables were
“presence of juvenile predators” (YES or NO) and “presence of
prey” (YES or NO). When necessary, post hoc comparisons were
performed using the Bonferroni test. The statistical procedures
were performed following those published by Guzman et al.
(2016).
Results
Prey egg consumption differed among treatments (F2,57 = 41.53;
P < 0.0001). It was higher in the presence of both adult pre-
dators and juvenile predator, lower in the presence of the adult
predator without the juvenile predators, and intermediate in the
presence of the juvenile predators without the adult predator
(Figure 1).
Juvenile predator mortality was affected by the presence of
adult predators (Wald stat. = 177.85; df = 47; P < 0.0001), the
presence of prey (Wald stat. = 29.81; df = 47; P < 0.0001), and
their interaction (Wald stat. = 14.41; df = 47; P < 0.0001).
Juvenile predator mortality was higher in the presence of can-
nibalistic female (Figure 2, compare treatments ii and iii or iv
and v) and lower in the presence of prey (Figure 2, compare
treatments ii and iv or iii and v). The significant interaction here
indicated that juvenile predator mortality was similar in the
presence and absence of both cannibalistic female and prey
(Figure 2, compare treatments iii and iv), whereas juvenile pre-
dator mortality was higher in the presence of cannibalistic
female and the absence of prey than in the absence of canni-
balistic female and the presence of prey (Figure 2, compare
treatments iii and v).
Few cannibalistic females laid eggs when neither juvenile
predators nor prey were present (treatment “vi”, see Figure 3),
likely due to cannibalism among females during the starvation
period (since tested females were not isolated) or due to the
previous feeding (since tested females were deprived of food
for less than 24 h). Oviposition was influenced by the presence
of prey (Wald stat. = 4.07; df = 76; P = 0.0435) but not by
juvenile predators (Wald stat. = 2.14; df = 76; P = 0.2743), and
their interaction was significant (Wald stat. = 4.85; df = 76;
P = 0.0760). Despite the significant effect of prey, differences
were only observed when the juvenile predators were absent:
females produced more eggs in the presence of prey than in
the absence of prey (Figure 3, compare treatments i and vi).
The significant interaction here indicated that females pro-
duced more eggs in the presence of both the adult predator
and the prey than when both the adult predator and the prey
were absent (Figure 3, compare treatments iii and vi), and egg
production was higher in the presence of prey and the absence
 INTERNATIONAL JOURNAL OF ACAROLOGY 389

Figure 1. Daily consumption of Raoiella indica (mean ± SE) by Amblyseius largoensis adult females (i), Amblyseius largoensis nymphs (ii) or Amblyseius largoensis
adult females and nymphs (iii). Different letters indicate significant differences among treatments (P < 0.05).

Figure 2. Daily predation/mortality (mean ± SE) of juvenile predators (Amblyseius largoensis nymphs) in the presence and/or absence of both adult predators
(Amblyseius largoensis adult females) and prey (Raoiella indica eggs). Asterisks indicate significant differences between treatments (P < 0.05). ns: not significant.

of juvenile predators than in the absence of prey and the
presence of juvenile predators (Figure 3, compare treatments i
and v).
Discussion
In the present study, we investigated whether cannibalism
occurred in A. largoensis. This trophic interaction was modulated
by the absence/presence of the prey, R. indica eggs. Overall, the
presence of prey decreased cannibalism, and few eggs were pro-
duced when predators consumed only conspecific prey (nymphs).
Cannibalism occurs in various contexts across the animal king-
dom and can enable a population to remain viable when it would
otherwise become extinct (Elgar and Crespi 1992). When food
resources are absent or too scarce to support a population, adults
may exploit cannibalism to maintain egg production or to survive
periods of low resource availability (Elgar and Crespi 1992).
Therefore, it is possible that adult A. largoensis females prey on
conspecifics in order to survive and ensure reproduction. Several
authors have suggested that cannibalism among phytoseiid mites
occurs due to low prey densities (e.g. Yao and Chant 1989; Zhang
and Croft 1995; Croft and Croft 1993, Croft et al. 1996;
Schausberger 1997; present study). However, we observed that A.
largoensis engaged in cannibalism despite sufficient supplies of
heterospecific prey, R. indica eggs. When the heterospecific prey
was available, predation on conspecific prey (nymphs) by A. lar-
goensis females occurred only occasionally and may have resulted
from random encounters. In the present study, space was limited,
and dispersal was not allowed; therefore, the rate of cannibalism is
likely lower in the field than in the current experiments.
390 J. A. MENDES ET AL.
Figure 3. Daily oviposition (mean ± SE) of adult predators (Amblyseius largoensis adult females) in the presence and/or absence of both juvenile predators
(Amblyseius largoensis nymphs) and Raoiella indica eggs. Asterisks indicate significant differences between treatments (P < 0.05). ns: not significant.
The presence of heterospecific prey decreased A. largoensis
cannibalism, as observed for other phytoseiid species (see
Schausberger 2003 for a review of the evidence). When the
heterospecific prey are present in abundant supply, the predator
is expected to spend more time and energy on that prey, thereby
decreasing the consumption of conspecifics (Schausberger 2003;
Zannou et al. 2005). In addition, there is risk of injury or death
when attacking other predators, even juvenile predators
(Montserrat et al. 2006).
Amblyseius largoensis was able to reproduce when fed only
conspecifics prey; however, a low number of eggs were observed.
Several studies have demonstrated that the quality of conspecific
prey is often lower than the quality of heterospecific prey (Polis
1981; Polis et al. 1989). However, a recent study showed that
conspecific prey may be a similar or even better food source
than heterospecific prey (thrips) for the phytoseiid mites
Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) and
Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae)
(Buitenhuis et al. 2010). In the present study, heterospecific prey
appeared to be a more suitable food source than conspecific prey
for A. largoensis. Similar results were reported by Cavalcante et al.
(2017) for A. swirskii when larvae were offered as conspecific prey
and larvae of Euseius concordis (Chant) (Phytoseiidae) as hetero-
specific prey. Another possible explanation for these results is
that females may have eaten their own eggs, since it is not
known if they can discriminate between own and conspecific
eggs. Kin recognition in the order Acari has received less atten-
tion. However, some phytoseiid species, such as Phytoseiulus
persimilis Athias-Henriot and Phytoseiulus macropilis Banks, were
able to discriminate between their own and non-kin immature
forms and preferentially ate non-kin when given a choice
(Schausberger and Croft 2001). Further investigations are
required to determine (1) whether the greater oviposition on
heterospecifics resulted from more and/or qualitatively superior
nutrients or less energy investment in handling prey and (2)
whether A. largoensis possesses the ability to distinguish related
and non-related eggs and this ability may as well be used to
avoid cannibalism on related forms.
The results described herein suggest that, similar to other
phytoseiid mites, A. largoensis employs cannibalism as an adap-
tive survival strategy when heterospecific prey is absent or scarce.
Nevertheless, the persistence of A. largoensis and ultimately its
role in the biological control of R. indica will likely depend on the
intensity of cannibalism and on interactions with other predators
(e.g. Euseius alatus DeLeon (Acari: Phytoseiidae) or Neoseiulus
recifensis Gondim Jr and Moraes (Acari: Phytoseiidae), phytoseiid
mites often encountered on coconut leaves (Gondim and Moraes
2001; Lawson-Balagbo et al. 2008; Melo et al. 2009a, 2009b,
2015)). Both of these factors will be affected by the availability
of food sources such as phytophagous mites, pollen, and coconut
exudates as well as the degree of spatial and temporal overlap in
the distribution of phytoseiids on coconut plants and within
coconut fields.
Acknowledgments
The research reported in this manuscript was supported by a
grant of the Conselho Nacional de Desenvolvimento Científico e
Tecnológico [CNPq—MCTI/CNPQ/Universal 14/2014 (Proc.:
447458/2014-0)] from the Brazilian government.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the Conselho Nacional de
Desenvolvimento Científico e Tecnológico [CNPq—MCTI/CNPQ/
Universal 14/2014 (Proc.: 447458/] from the Brazilian government.
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