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Contrasting Effects of the Invasive Hypogeococcus sp.
(Hemiptera: Pseudococcidae) Infestation on Seed
Germination of Pilosocereus royenii (Cactaceae), a
Puerto Rican Native Cactus
Authors: Aponte-Díaz, Laura A., Ruiz-Arocho, Jorge, Carrera-Martínez,
Roberto, and van Ee, Benjamin W.
Source: Caribbean Journal of Science, 50(2) : 212-218
Published By: University of Puerto Rico at Mayagüez
URL: https://doi.org/10.18475/cjos.v50i2.a2
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Caribbean Journal of Science (2020), 50: pp. 212–218.
© Copyright 2020 by the College of Arts and Sciences of the University of Puerto Rico, Mayagüez
212
Contrasting Effects of the Invasive Hypogeococcus sp. (Hemiptera: Pseudococcidae)
Infestation on Seed Germination of Pilosocereus royenii (Cactaceae), a Puerto Rican
Native Cactus
Laura a. aponte-Díaz1, Jorge ruiz-arocho1,2,*, roberto carrera-Martínez3, anD benJaMin W. van ee1
1Biology Department, University of Puerto Rico, Mayagüez Campus, Mayagüez, Puerto Rico
2Department of Plant and Soil Science, University of Vermont, Burlington, Vermont, U.S.A.
3Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia, U.S.A.
*Corresponding author: jruizaro@gmail.com
Communicating editor: Sean Locke
AbstrAct—We evaluated the impact of the Harrisia Cactus Mealybug (HCM), Hypogeococcus sp. (Hemiptera:
Pseudococcidae), on seed germination of Pilosocereus royenii (Cactaceae) in Puerto Rico. Mature fruits were collected
from individuals of P. royenii at various levels of HCM infestation, ranging from completely healthy plants to fruits
growing directly on HCM-induced tumors. We hypothesized that germination will be directly and negatively affected
by HCM infestation severity. After measuring germination and seedling survival for 160 days, we observed that seeds
from fruits growing on tumors had the lowest germination rate compared to the other categories, as hypothesized.
In addition, lightly infested plants germinated at a lesser rate compared to healthy plants, while seeds from severely
infested plants germinated at a greater rate, contrasting with our hypothesis. We suggest that when the infestation
is light, the host might be reallocating resources towards developing defensive responses. In contrast, when the
infestation is severe, the host might be reallocating resources toward increasing germination.
resumen—Evaluamos el impacto del Harrisia Cactus Mealybug (HCM), Hypogeococcus sp. (Hemiptera:
Pseudococcidae), sobre la germinación de semillas de Pilosocereus royenii (Cactaceae) en Puerto Rico. Frutos
maduros fueron colectados de individuos de P. royenii a varios niveles de infestación de HCM, desde completamente
sanos hasta frutos creciendo directamente de tumores inducidos por HCM. Hipotetizamos que la germinación
estaría directamente y negativamente relacionada al nivel de infestación por HCM. Después de medir germinación
y sobrevivencia durante 160 días, observamos que las semillas provenientes de frutos creciendo sobre tumores
mostraron la menor taza de germinación en comparación a las otras categorías, siguiendo nuestra hipótesis. En
adición, las semillas de plantas ligeramente infestadas germinaron a una taza menor comparado a plantas sanas,
mientras que las semillas de plantas fuertemente infestadas germinaron a una taza mayor, diriendo con nuestra
hipótesis. Sugerimos que cuando la infestación es ligera, el antrión pudiera estar reasignando recursos hacia
el desarrollo de respuestas de defensa. En contraste, cuando la infestación es severa, el antrión pudiera estar
reasignando recursos hacia el aumento en germinación.
Plants have developed multiple strategies to respond
and survive pathogenic infestations, parasites, and
herbivore damage. As a response to these attacks, plants
can reallocate resources from the damaged organ to an
undamaged organ, avoiding its consumption (Robert et
al. 2014; Zhou et al. 2015). Similarly, resources can be
reallocated by the plants to express a resistance and/or a
tolerant response (Rivera-Solís et al. 2012; Schultz et al.
2013; Robert et al. 2014; Zhou et al. 2015). Resistance
is dened here as plant traits that limit the capacity,
degree, or probability of its enemies to damage it, while
tolerance, on the other hand, is the ability to limit the
impact of enemies’ damage to the plant tness (Agrawal
2000b; Agrawal and Fishbein 2006; Heil 2010; Pagán
and García-Arenal 2018; Garcia and Eubanks 2019).
Therefore, a tolerant plant is able to reproduce and
potentially develop as if it were unaffected when it
falls victim of an herbivore, pathogen, or a parasite
(Agrawal 2000b; Heil 2010); limiting such impacts
by compensation (Agrawal 2000b; Heil 2010; Garcia
and Eubanks 2019). In some cases, tolerance could be
manifested by an increase in biomass (Katayama et al.
2015; Poveda et al. 2018), germination rate (Liu et al.
2017), or ower, fruit, and seed production (Salvaudon
et al. 2008; Garcia and Eubanks 2019). On occasions,
compensatory responses through resources reallocation
can be manifested as tradeoff between plants functions,
as for example, growth and reproduction (Mabry and
Wayne 1997; Agrawal 2000a; Pratt et al. 2005; Shukla
et al. 2018).
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213 caribbean JournaL of Science [Volume 50
A newly introduced enemy in Puerto Rico, the
Harrisia Cactus Mealybug (HCM), Hypogeococcus
sp. (Hemiptera: Pseudococcidae), has become a major
invasive species and a threat to native and endemic
columnar cacti species on the island (Carrera-Martínez
et al. 2015, 2019). HCM promotes abnormal growth
in infested cacti, including deformed owers and
possibly unviable fruits (Carrera-Martínez et al.
2015). Furthermore, it has decreased fruit and ower
production and increased cactus mortality (Carrera-
Martínez et al. 2019). These antagonistic effects on
the survival and reproduction of infested cacti make
Hypogeococcus spp. an ideal biological control agent
for invasive cacti species. For example, a reduction in
the population density, reproduction, and survival of
the invasive Harrisia spp. in South Africa and Australia
(McFadyen and Tomley 1978, 1980; Paterson et al.
2011; Houston and Elder 2019) and Cereus jamacae in
South Africa (Paterson et al. 2011; Sutton et al. 2018)
were observed under exposure to Hypogeococcus spp.
Understanding the effects of HCM on their host’s
reproduction and seed germination is crucial for the
conservation of Caribbean native cacti. Among the
species affected by HCM is Pilosocereus royenii (L.)
Byles & G.D.Rowley, which is the most common and
widespread columnar cactus in Puerto Rico (Liogier
1994; Carrera-Martínez et al. 2018). As a species
that depends on cross-pollination (Rivera-Marchand
and Ackerman 2006), a decline in the proportion of
reproductively-active individuals could potentially
have lasting effects on the species. Therefore, the
objective of this study was to determine the effects of
HCM infestation on seed germination in P. royenii.
Furthermore, because some cacti species may benet
from seed scarication (Rodrigues da Luz and Ferreira-
Nunes 2013), we scaried half of the seeds used in the
experiment in order to determine if there is any effect of
seed mechanical scarication on their germination rate.
We hypothesized that germination would be affected
by HCM infestation, where infested cacti would have
a lower germination rate relative to healthy cacti. We
also hypothesized that scarication would signicantly
increase seed germination.
MethoDS
Fruit Selection
Mature and unbroken fruits over 10 g were randomly
selected from individuals of P. royenii growing in the
Wildlife and Fisheries Refuge at Cabo Rojo, Puerto
Rico (sites CR1, CR2, and CR3 in Carrera-Martínez et
al. 2018, 2019). Fruit selection was conducted between
September and November of 2016, which coincides
with the peak of fruiting reported by Rivera-Marchand
and Ackerman (2006). Maturation was determined by a
high proportion of the fruit showing the characteristic
dark-pink color. One to six fruits were selected from
four cacti infestation categories: 1) Healthy, 2) Lightly
Infested, and 3) Severely Infested, based on the HCM
infestation index published in Carrera-Martínez et al.
(2019; healthy with no infestation, lighlty with indexes
1–2, and severly, 3–5). The fourth treatment consisted of
fruits growing directly on HCM-induced tumors. Each
treatment had six individual cacti replicates, except that
of fruits growing directly on tumors as only two fruits
from two cacti were selected (n = 4). The low number
of fruits obtained from tumors (see Figure 4 in Carrera-
Martínez et al. 2015) was due to their low occurrence
in the eld, and most failed to comply with the size
criteria for fruit selection (Aponte-Díaz pers. obs.). In
total, 39 fruits were collected and used in this study.
Seed Selection and Scarication
From each fruit, 200 fully developed seeds were
randomly selected using sterilized tools in an aseptic
environment. Half of the seeds were randomly selected
to undergo mechanical scarication by placing them
inside a small paper bag half full of commercially
available all-purpose sand and rubbing them for
approximately one minute. Although numerical data
were not recorded, we observed a high proportion of
undeveloped or empty seed coats in fruits from the
HCM-induced tumors.
Seed Planting and Germination
Seeds were planted, and germination was recorded,
at the greenhouse facility of the Biology Department
at the University of Puerto Rico, Mayagüez. A potting
mixture was prepared using a proportion of 50%
potting soil, 25% all-purpose rocks, 12.5% all-purpose
sand, and 12.5% peat moss, all commercially available.
After mixing, the potting mixture went through a
dry oven at 200°C for 30 minutes to neutralize any
undesired plant materials. The mixture was placed
in commercial seedling trays with cells of 4.4 cm
square by 5.7 cm deep. Seeds were planted in groups
of ve in each cell, and different trays were allocated
to the scaried and unscaried treatments. Trays were
watered approximately once per week, to maintain a
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2020] aponte-Díaz et aL.: effectS of hypogeococcuS on piLoSocereuS cactuS 214
moisture level similar to their natural environment and
were covered with plastic wrap to avoid rapid water
desiccation. To ensure that all seeds received similar
sunlight, trays were rotated daily on their own axis, and
around the greenhouse. Finally, the number of newly
germinated seeds was recorded starting two weeks
after planting and were followed for seven weeks at
different time intervals (starting in Wk 3: at days 14–
16; Wk 4: 19–23 after planting; Wk 5 and Wk 6: at
days 25, 27, 29, and 31 after planting; Wks 7–9 at days
31, 34, 38, 41, and 48 after planting) with a nal count
done six months after the beginning of the experiment
(160 days after planting, for a total of 17 observation
dates). For each observation date we recorded seed
germination success of fruits in two ways. First, we
estimated the seeds’ germination capacity (expressed
as the cumulative percentage of germinated seeds) by
dividing the number of germinated seeds by the total
number of seeds planted and multiplying that number
by 100 at each observation day. Second, we calculated
the seed germination speed (expressed as the rate of
new recruitment for each time interval) as the number
of newly germinated seedlings for a time interval minus
the number of seedlings of the previous time interval.
The values for both seed germination capacity and speed
of fruits were averaged for each individual cactus.
Statistical Analyses
To test the hypothesis that HCM infestation severity
has an effect on seed viability (capacity to germinate)
and germination speed, we performed a Factorial
Repeated Measures ANOVA, with scarication and
percentage of germinated seeds as factors. Later,
scarication was eliminated as a factor since it did not
hold a signicant interaction with HCM infestation
severity on seed germination (see results), but we
conserved it as a block in the model. Differences
between HCM infestation levels were determined with
a t-test pairwise comparisons between groups. All
statistical analyses were performed in R ver. 3.6.1 (R
Core Team 2019).
reSuLtS
Our analyses found a signicant effect of HCM
infestation on seed germination capacity (P < 0.001, F3,
35 = 7.40, Fig. 1A). These differences reside primarily in
seeds obtained from fruits growing on tumors having a
much lower germination rate and speed of germination
throughout the experiment, with a maximum
germination of 19%, and a minimum of 1% by the
end of the experiment. Similarly, seeds from healthy
cacti had signicantly higher germination compared to
seeds from lightly infested cacti and those from tumors
during the rst week of observations (on days 14 to
16) but from day 19 on, seeds from severely-infested
cacti had a consistently higher cumulative germination
percentage than seeds from healthy cacti, becoming
signicant on days 38, 41, 48, and 160 (Fig. 1A).
We observed a signicant effect of HCM infestation
on seed germination rate (number of new seedlings for
each observation) (P < 0.001, F3, 35 = 3.72, Fig. 1B).
This difference was found in the rst eight intervals and
in the nal time interval. In general, seeds from severely
infested cacti germinated faster than those from lightly
infested cacti or from tumors during the rst four
intervals, while seeds from healthy cacti maintained
a steady germination rate. Seeds from lightly infested
cacti had a higher germination rate during intervals ve
and eight compared to all other groups, and in interval
seven compared to severely infested cacti. On the other
hand, seeds from lightly infested cacti had a lower
germination rate than those from severely infested cacti
and healthy cacti in interval six and compared to all
treatments in the last interval. In both cases, lightly
infested cacti had a negative germination rate as a result
of mortality. In general, seeds from healthy cacti had a
more consistent and stable germination rate compared
to all other treatments, with relatively low mortality
or negative germination rate. In contrast, germination
rates from lightly- and severely-infested cacti uctuated
throughout the experiment, while seeds obtained
from fruits growing on tumors had low germination,
increasing only at the end of the experiment (Fig. 1B).
Seed scarication had no signicant interaction with
HCM infestation category when testing germination
capacity (P = 0.998, F3, 32 = 0.14) or germination rate
(P = 0.997, F3, 32 = 0.26), nor was it found to have a
signicant effect on germination capacity (P = 0.724,
F1, 35 = 0.43), nor rate (P = 0.754, F1, 35 = 0.52).
DiScuSSion
Seeds of Pilosocereus royenii obtained from fruits
growing on tumors germinated at a signicantly lower
rate than those obtained from fruits growing on healthy,
lightly- and severely infested specimens. Contrasting
with this result, fruits obtained from severely infested
cacti germinated at a signicantly much higher
frequency than those from lightly infested and healthy
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215 caribbean JournaL of Science [Volume 50
fig. 1. Seed germination from fruits of Pilosocereus royenii that are uninfested (and healthy), lightly infested, and
severely infested by Hypogeococcus sp. and from fruits growing on tumors caused by Hypogeococcus sp. A. Average
cumulative percentage of germinated seeds per plant by observation day. B. Seed germination rates expressed as number of
new seedlings between sampling intervals; negative numbers indicate higher seedling mortality compared to germination
(or negative germination rate), positive numbers indicate a net germination rate growth, and 0’s represent no net growth in
the number of seedlings (either there was no mortality and no germination, or they cancel each other).
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cacti. Further, lightly infested cacti had a lower
germination and seedling survival rate at the end of the
experiment than both healthy and severely infested cacti,
but higher than fruits from HCM-induced tumors. Such
disproportionate decrease in reproductive success may
be in response to the plant’s reallocation of resources
to generate defenses against the HCM infestation.
The development of such defenses is assumed to be
energetically costly for the plant (Agrawal 2000a). Our
results together suggest that while the HCM infestation
progresses and the host health degrades, the host may
undergo a trade-off between combating the infestation
towards increasing the production of viable seeds (or
offspring). Thus, the plant must reallocate resources
to develop such resistances or tolerant traits, such as
trading growth and/or reproduction (Agrawal 2000a;
Pratt et al. 2005; Salvaudon et al. 2005; Miler and
Straile 2010; Shukla et al. 2018).
Seeds extracted from fruits growing directly on
tumors had the lowest germination rate of all treatments,
with a mean difference greater than 30% to all other
treatments. The frequency of fruits growing on HCM-
induced tumors in nature has not been documented, but
eld observations suggest that their frequency is low
and likely restricted to severely infested cacti (Aponte-
Díaz et al. pers. obs.). Therefore, natural recruitment
of seedlings from fruits growing on tumors is expected
to be minimal, if not trivial. Low seed viability may be
the result of these fruits growing in an area of the plant
that is deeply depleted of resources by the mealybug,
as previously suggested in different systems (Ruiz
et al. 2006; Faghihi et al. 2011). These observations
combined with those of the other treatments suggests
that reproductive success of P. royenii will depend
on the severity and changes of HCM infestation, and
whether the fruits are associated with tumors or not.
Resources reallocation that may secure reproductive
success could be considered as compensating or
defensive plant responses (Schultz et al. 2013; Zhou
et al. 2015). Compensation, by denition, is the ability
of the host to reduce or mitigate the effects of the
parasite or pathogen on its tness (Agrawal 2000b;
Heil 2010). We observed a 10–15% greater germination
rate and seedling survival from severely infested cacti
compared to healthy cacti and lightly infested cacti, and
of almost 50% more than those from fruits growing on
tumors. However, HCM infestation still considerably
decreases the reproductive success of P. royenii through
a dramatic reduction of ower and fruit production
(Carrera-Martínez et al. 2019). Furthermore, the
HCM-P. royenii infestation differs from most known
examples of compensation and infestation-tolerant
systems in that HCM represents a recent invasion in the
area (<30 years since its rst record; Segarra-Carmona
et al. 2010). Most well-studied systems showing
compensation are mostly examples of longer-term
coevolutionary adaptations (Agrawal 2000a, 2000b;
Heil 2010; Faghihi et al. 2011; Liu et al. 2017; Pagán
and García-Arenal 2018). Moreover, higher severities
of HCM infestation lead to a higher rate of mortality in
P. royenii (Carrera-Martínez et al. 2019). Therefore, we
can only suggest a partial compensating response of the
HCM-infested cactus through resources reallocation.
Whether (and how) plants will reallocate resources,
have a resistance or compensating response, or a
combination, to a natural enemy depends on the
resources available, environmental conditions, the cost
of the tradeoff (Salvaudon et al. 2005, 2008; Ruiz et
al. 2006; Montes et al. 2020), life history (Boege and
Marquis 2005; Montes et al. 2020), and on the severity
of the infestation, infection, or herbivore damage
(Huhta et al. 2000; Vergés et al. 2008). Thus, it is to
be expected that plants will reallocate (or combine)
resources as these are used or made available, to express
a response to infestation. Therefore, we hypothesize that
when HCM infestation on P. royenii is light, P. royenii
will reallocate growth and reproductive resources
toward developing defensive responses to ght the
infestation. Furthermore, we hypothesize that as the
infestation advances, severely infested cacti could be
reallocating resources toward increasing germination
success and rate. Nonetheless, because of the limited
fruits collected from more severely infested cacti, we
were not able to utilize the complete HCM infestation
index as described by Carrera-Martínez et al. (2019),
limiting our understanding of P. royenii response
patterns to HCM infestation at a ner severity scale.
Further, resources reallocation in response to herbivore
or parasitic attacks on plants is in general poorly
understood (Schultz et al. 2013), and further sampling
and longer-term experiments are needed to test these
hypotheses. Finally, we cannot discard the inuence
of other P. royenii responses to herbivore damage, as
these are not necessary mutually exclusive, and are
commonly found to co-occur (Restif and Koella 2004;
Pagán and García-Arenal 2018).
2020] aponte-Díaz et aL.: effectS of hypogeococcuS on piLoSocereuS cactuS 216
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217 caribbean JournaL of Science [Volume 50
Acknowledgements—We are grateful to the Wildlife
and Fisheries Refuge at Cabo Rojo for granting access
to the site, to Barbara Sánchez for granting access to
the UPRM greenhouse, and to Sandra L. Maldonado-
Ramírez for providing lab space used to store and
process fruits. Assistance on the processing of fruits
and planting of the seeds was provided by Héctor J.
River-Jiménez, Kiara L. Pérez-Medina, and students
of the Biology Student Association (Asociación de
Estudiantes de Biología, AEB) and of the Ecological
Society of America’s Strategies for Ecology Education,
Development and Sustainability (SEEDS) Lewe
Chapter, both of the UPRM Department of Biology.
Finally, we appreciate assistance from Carlos J. Santos-
Flores on early development of the experimental design,
and from two anonymous reviewers whose comments
signicantly improved the manuscript.
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