Received: 16 February 2020 | Revised: 27 October 2020 | Accepted: 1 November 2020

DOI: 10.1111/eth.13112

RESEARCH ARTICLE

“Where ignorance is bliss, 'tis folly to be wise”: Indiscriminate

male care in a neotropical spider

Rafael Rios Moura1,3 | Isabella Dias Oliveira3 | João Vasconcellos-Neto2 |

Marcelo Oliveira Gonzaga3

1
Departamento de Ciências Biológicas,
Núcleo de Extensão e Pesquisa em Ecologia Abstract
e Evolução (NEPEE), Universidade do Estado Certainty of paternity is considered an important condition for the evolution and
de Minas Gerais, Ituiutaba, Brazil
2 maintenance of extended male care. In some species, males may cannibalize unrelated
Departamento de Biologia Animal,
Universidade Estadual de Campinas, offspring or abandon the progeny when the uncertainty of paternity is high, or when
Campinas, Brazil
they take over nest sites or females from other males. However, male protection of
3
Instituto de Biologia, Universidade Federal
de Uberlândia, Uberlândia, Brazil
offspring can also evolve in situations of uncertainty of paternity, especially when
males cannot recognize offspring relatedness. In such cases, males may take care of
Correspondence
Departamento de Ciências Biológicas,
all their mate's offspring, regardless of paternity. In Manogea porracea (Araneidae),
Universidade do Estado de Minas Gerais – the only known spider species where males care for offspring, males repel competi-
UEMG, R. Ver. Geraldo Moisés da Silva, s/n
- Universitário, CEP 38302-192, Ituiutaba,
tors by assuming and defending specific positions within a female's web, but females
MG, SP, Brazil. accept multiple partners during the reproductive season. Consequently, males may
Email: rafael.moura@uemg.br
care for some offspring produced with the sperm of their mate's previous partners.
Funding information If males cannot detect offspring relatedness, we expect that they will not cannibalize
Conselho Nacional de Desenvolvimento
Científico e Tecnológico, Grant/Award
progeny and will actively protect all offspring against predation. The main goal of this
Number: 306157/2014-4, 403733/2012- study was to investigate whether the extended male care depends on offspring relat-
0, 441225/2016-0, 445832/2014-2 and
465562/2014-0; Duratex S.A.; Fundação
edness recognition. Therefore, we experimentally manipulated offspring relatedness
de A mparo à Pesquisa do Estado de Minas and the presence of foster males and two egg predators usually found invading M.
Gerais, Grant/Award Number: APQ-02104-
14, APQ-02984-17, APQ-03202-13 and
porracea webs. We also compared our results with data from an experiment per-
CRA-30058/12; Fundação de Amparo à formed by Moura, Vasconcellos-Neto, & Gonzaga (2017) using the same laboratory
Pesquisa do Estado de São Paulo, Grant/
Award Number: 2017/14196-5 and
procedures, but introducing egg sacs fathered exclusively by the males. Males did
465562/2014-0 not cannibalize offspring and protected the progeny against predation regardless of

Editor: Wolfgang Goymann

offspring relatedness. In addition, all males moved the egg sacs to the center of the
web, remaining close to the progeny. We conclude that M. porracea males protect all
progeny present in their partner's web and increase offspring survivorship regardless
of relatedness. We discuss the behavioral and evolutionary implications of our find-
ings, and potential triggers of male care in M. porracea.

KEYWORDS

araneophagy, biparental care, egg predators, kin recognition, paternity assurance

[Correction added on 1 December 2020, after first online publication: the affiliation numbering has been updated.]

Ethology. 2021;127:223–230. wileyonlinelibrary.com/journal/eth© 2020 Wiley-VCH GmbH | 223


224 | MOURA et al.
1 | I NTRO D U C TI O N
Females typically invest more in parental activities than males
(Clutton-Brock, 1991; Royle et al., 2012). For males, the costs of pro-
viding parental care (e.g., reduction in mating opportunities with new
partners; increased exposure to predation; and reduction in food in-
take) usually outweigh the benefits of providing care to offspring
(Fromhage & Jennions, 2016; Queller, 1997; Requena & Alonzo, 2017).
Therefore, males usually take care of offspring when they share the
costs of parental activities with females, that is, biparental care (ver-
tebrates: Balshine, 2012; invertebrates: Machado & Trumbo, 2018). In
some cases, males can assume the parental care role in the absence of
their partners, but the care is usually provided by the female, that is,
amphisexual care (Beal & Tallamy, 2006; Buzatto & Machado, 2009).
Exclusive paternal care is rarely observed (Tallamy, 2001), except for a
few taxa (amphibians: Furness & Capellini, 2019; harvestmen: Requena
et al., 2014; fish: Reynolds et al., 2002). These cases offer good op-
portunities to investigate whether particular costs of paternal activi-
ties can be outweighed by the benefits of enhanced offspring fitness,
providing important insights into mechanisms that affect the evolution
and maintenance of parental behaviors.
Certainty of paternity is usually considered in both experimen-
tal (Safari & Goymann, 2018) and theoretical studies (Fromhage &
Jennions, 2016) as an important factor influencing the occurrence
and/or intensity of male care. Most studies have found that pater-
nal care is more likely to evolve in scenarios where certainty of pa-
ternity is high (Fromhage & Jennions, 2016; Kokko & Jennions, 2008;
Kvarnemo, 2006; Requena & Alonzo, 2017; Wright, 1998). In taxa with
external fertilization, males can often directly assess paternity, and pa-
ternal behaviors are relatively common (Smith & Wootton, 1995). On
the other hand, it is much more difficult for males to assess paternity
when fertilization is internal, and females control genetic parentage.
Under high female promiscuity, for example, males may increase fer-
tilization efforts by sperm competition and copulatory courtship be-
haviors to stimulate cryptic female choice (Eberhard, 1996; Requena
& Alonzo, 2017) and leave females just after mating (Gilbert &
Manica, 2015; Yip & Rayor, 2014). Paternity detection is particularly
complicated in many arthropods because promiscuous females can
store sperm from multiple mates in their spermathecae (Herberstein
et al., 2011; Pascini & Martins, 2017). Consequently, males have a high
chance of caring for some proportion of unrelated offspring when they
copulate with mated females. Thus, internal fertilization and high un-
certainty of paternity are thought to be barriers to the evolution of
paternal care in most arthropods (spiders: Yip & Rayor, 2014; insects:
Gilbert & Manica, 2015).
Cuckoldry is expected to reduce paternal effort when the un-
certainty of paternity is high (Griffin et al., 2013). Therefore, when
males can recognize unrelated progeny, they may cannibalize eggs
or juveniles before mating (Gonzaga & Leiner, 2013; Kondoh &
Okuda, 2002). Alternatively, males may adjust the parental care de-
pending on the presence of indicators of cuckoldry and their capacity
to detect sperm already deposited in the female spermathecae (e.g.,
Neff, 2003). Thus, offspring recognition by males may drive paternal
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protection. To minimize the risk of cuckoldry, males can use cues (e.g.,
sexual pheromones) to monitor female mating status (virgin or mated,
Gaskett, 2007) or increase fertilization success by, for example,
using mating plugs (Schulte et al., 2010) or guarding mates (Moura
& Gonzaga, 2017). Furthermore, an absence of parental recognition
may evolve in species with high risk of cuckoldry if the cost for future
reproductive success of males and for paternal care are low (Griffin
et al., 2013). Therefore, parental care can still evolve in polyandrous
mating system when males cannot discriminate offspring relatedness.
Maternal care is often observed in solitary spiders (Yip &
Rayor, 2014), while paternal care has been described in only one spe-
cies to date. Manogea porracea (C. L. Koch, 1838) (Araneidae) males
repair damage to nursery webs and actively protect egg sacs and
spiderlings against araneophagic spiders (Moura et al., 2017). Males
mature earlier than females in the breeding season and guard sub-
adult partners (Moura et al., 2020). During this period, they build a
small dome-shaped web above female's web and fight with other
males to secure a prime position. After female maturation and copu-
lation, males can continue guarding their partner or move to another
web to seek new mating opportunities (Moura & Gonzaga, 2017;
Moura et al., 2020). So, some males can copulate and guard a mated
female, even when she has already produced egg sacs and probably
holds sperm from another male in her spermathecae. In this scenario,
males may incur the risk of sperm competition during egg fertiliza-
tion and may ultimately take care of some proportion of unrelated
offspring.
The costs of protecting an unrelated progeny are high, as males
may be killed by potential egg predators and lose additional mating
opportunities, especially when several females are still available (i.e.,
in the middle of the breeding season; Moura & Gonzaga, 2017; Moura
et al., 2020). In this situation, there are two possible hypotheses: (a)
if paternity can be detected, males may practice filial cannibalism or
reduce their parental protection of unrelated offspring, increasing
the exposure of some egg sacs or juveniles to predators, or (b) if
paternity cannot be detected, males may take care of all offspring.
In this study, we tested these competing hypotheses by adopting
the same laboratory procedures proposed by Moura et al. (2017),
but introducing egg sacs collected from distinct webs to compare
offspring survival in the presence and in the absence of foster fa-
thers. We then compared the results of Moura et al. (2017) using bi-
ological fathers and those from this study to evaluate whether males
adjust their paternal protection depending on offspring relatedness.
We also evaluated whether foster males cannibalized unrelated off-
spring, and whether male are willing to assume a protective position
below the egg sac.
2 | M ATE R I A L A N D M E TH O DS
2.1 | Study area
We performed data collection at Fazenda Nova Monte Carmelo
(18°49′27ʺS, 47°51ʹ47ʺW), Estrela do Sul, Minas Gerais, Brazil. The

MOURA et al.
study area is a Eucalyptus plantation, surrounded by areas of na-
tive Cerrado. Individuals of M. porracea usually build webs close to
the ground, using Eucalyptus branches and leaf litter as attachment
points for web-supporting silk threads (Moura et al., 2017). The re-
gion has a tropical savannah climate defined as Aw according to the
Köppen-Geiger classification (Peel et al., 2007) and can be separated
into two seasons, the dry (from April to October) and the rainy (from
November to March) (Aquino et al., 2007).
2.2 | Data collection and experimental design
We reproduced the same experimental protocols performed by
Moura et al. (2017) that investigated the protection of a progeny fa-
thered by the males. Individuals were collected from the same popu-
lation and in the same period of the reproductive season to make
studies comparable.
In October 2018, we collected 40 males, 58 females, and 87 egg
sacs of M. porracea. All males were found in webs with egg sacs.
We conducted data collection in this period because the sex ratio is
slight biased toward females; thus, males may be more likely to aban-
don the egg sacs and search for new mating opportunities (Moura &
Gonzaga, 2017; Moura et al., 2020). To test whether a foster male
will protect an unrelated brood from natural enemies, we collected
females of the two araneophagic species from family Theridiidae,
Faidutus caudatus (n = 10) and Agyrodes elevatus (n = 8), which are
usually found on M. porracea webs (Moura et al., 2017). All the indi-
viduals of the araneophagic species were adult females and were not
fed before the experiment. To reduce the chances of sampling egg
sacs from adjacent webs that were fathered by the collected males,
we did not sample males and eggs sacs found on webs within a 6 m
radius from the focal web. We haphazardly collected males and egg
sacs spread in an area of 1.29 km2 (4.3 × 0.3 km; length × width)
close to the trail. We carefully stored each individual and egg sac in
a separate Falcon tube and transported them to the Laboratório de
Aracnologia of the Universidade Federal de Uberlândia (Uberlândia,
Minas Gerais, Brazil). Voucher specimens are deposited in the collec-
tion of Universidade Federal de Minas Gerais (curator A. J. Santos),
Minas Gerais, Brazil.
In the laboratory, we put each female in a separate experimental
container (19 × 18 cm; depth × diameter) for at least 24 hr to build
webs. All containers had Eucalyptus branches that could be used as
attachment points during web building, and wet cotton balls to main-
tain humidity. After web construction, we carefully removed the fe-
males and placed the males and egg sacs in the containers. Males
and egg sacs were first sorted into size categories, and then, indi-
viduals within each category were randomly assigned to treatments.
For example, the first set of five heaviest egg sacs and the first set
of five largest males were sorted and distributed between the five
treatments (described below). Then, the second set of five heaviest
egg sacs and second set of five largest males were distributed ac-
cording to the same procedure and so on. Using this approach, we
avoided bias arising from distinct clutch sizes or potentially different
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| 225
abilities to repel predators related to male size. Egg sac mass is a
good proxy for the number of eggs because M. porracea eggs vary
little in size (see Moura et al., 2017).
Males were left in the containers with their adoptive egg sacs
for 24 hr before initiating the experiment. We next carefully added
predators at the edges of the web in the containers to establish the
following treatments: only the adoptive male (n = 20); adoptive male
and F. caudatus (n = 10); only F. caudatus (n = 10); adoptive male
and A. elevatus (n = 10); and only A. elevatus (n = 8). We built a con-
trol with only adoptive males and egg sacs with the largest sample
size aiming to increase our changes of detecting male aggressive be-
haviors toward unrelated offspring. Daily observation records were
made of males’ position in the webs, and any cannibalism of egg sacs
or spiderlings. Since both M. porracea and egg predators are active
during all day, we performed observations during the afternoon (be-
tween 2 and 6 p.m.). After 10 days, we removed both M. porracea
males and araneophagic predators from the experimental contain-
ers. We then waited for 20 days and counted the number of spider-
lings that emerged from the egg sacs in each treatment.
We compared our results with data from Moura et al. (2017),
which is another study conducted by our research team that per-
formed the same laboratory procedures to evaluate the protection
of egg sacs fathered by the males. We performed the following
comparisons: (a) the treatments of this study with a control in which
males remained with their own egg sacs during the experiment; (b)
the data on the presence of F. caudatus and (c) A. elevatus with the
data on protection of egg sacs by the biological and foster males. In
all models, we tested differences in the number of spiderlings that
hatched (response variable) between these treatments (predictor
variable) using generalized linear models (GLM) with Poisson error
distribution and planned comparison tests for subgroup differences.
We graphically inspected the residuals and evaluated overdisper-
sion using “AER” package (Kleiber & Zeileis, 2008). To run the mod-
els, we used “lme4” (Bates et al., 2015) and “car” packages (Fox &
Weisberg, 2019). We conducted all data analysis in R version 3.6.2
(R Development Core Team, 2020).
3 | R E S U LT S
All males moved the egg sacs to the center of the web and assumed
the protective position (Figure 1a,b). No cannibalization of egg sacs
occurred. Two samples of the control group (with male and egg sac)
were removed from analysis because spiderlings escaped from a
small opening in the experimental containers, and an egg sac was
attacked by fungi. Both araneophagic predators were observed con-
suming the egg sacs after the second day of the experiment. In treat-
ments with males, predators carefully approached the egg sacs, and
males reacted aggressively when they identified predation attempts.
Manogea porracea males killed A. elevatus in three trials, and a male
M. porracea was killed by A. elevatus in one trial. No male or preda-
tor was killed in treatments with F. caudatus. Both predator species
were observed consuming the eggs and remained close to the egg

226 | MOURA et al.
(a) (b)
(c) (d)
sacs during most experiment duration in the treatment without M.
porracea males (Figure 1c,d).
The number of spiderlings that emerged from egg sacs differed
between treatments (χ2 = 143.7; df =5; p < .001). The number of
spiderlings that hatched from the egg sacs was higher in treatments
in which males were present than in treatment in which they were
absence, regardless of offspring relatedness (Figure 2). The pres-
ence of males increased offspring survival by 2.5 folds, on average,
in treatments with A. elevatus and F. caudatus, when compared with
2
treatments containing only these predators (A. elevatus: χ = 64.6;
df = 3; p < .001; F. caudatus: χ2 = 11.5; df = 3; p < .001). Offspring
relatedness did not increase the efficiency of offspring protection
against both araneophagic species (Figure 3). Both biological and
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F I G U R E 1 Laboratory experiment with
Manogea porracea males, egg sacs with
unrelated eggs and spiderlings, and egg
predators. (a) A foster father assuming a
protective position, below the egg sac. (b)
A foster father protecting an egg sac with
recently hatched spiderlings. (c) Faiditus
caudatus and (d) Argyrodes elevatus close
to an egg sac in the treatments without
a male [Colour figure can be viewed at
wileyonlinelibrary.com]
F I G U R E 2 Number of spiderlings
that emerged from Manogea
porracea egg sacs in each treatment:
(i) biological father + egg sac; (ii)
foster father + egg sac; (iii) foster
father + Argyrodes elevatus + egg sac;
(iv) Argyrodes elevatus + egg sac; (v)
foster father + Faiditus caudatus + egg
sac; (vi) Faiditus caudatus + egg sac. The
red points show means, and bars show
standard errors. The black dots represent
the number of spiderlings that survived
in each trial. Equal letters correspond to
p > .05 and different letters to p < .05
for planned comparison tests. Data from
the treatment of related offspring (i) were
provided by Moura et al. (2017) [Colour
figure can be viewed at wileyonlinelibrary.
com]
foster fathers were similarly effective in offspring protection against
predation (see post hoc test results in Figures 2 and 3).
4 | D I S CU S S I O N
In this study, M. porracea males did not cannibalize unrelated off-
spring and engaged in protecting the progeny in all trials. All males
moved the egg sacs to the center of the web and assumed a pro-
tective position below the egg sac. Foster fathers were as effec-
tive as the biological fathers in the protection of eggs against the
two araneophagic spider species observed invading their webs in
the field. Therefore, our results support the hypothesis that males
 14390310, 2021, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/eth.13112 by UNEB - Universidade do Estado da Bahia, Wiley Online Library on [30/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MOURA et al. | 227

F I G U R E 3 Number of spiderlings that emerged from Manogea porracea egg sacs in treatments containing predators, (a) Argyrodes elevatus
and (b) Faiditus caudatus, and distinct relatedness between males and egg sacs. The red points show means, and bars show standard errors.
The black dots represent the number of spiderlings that survived in each trial. Equal letters correspond to p > .05 and different letters to
p < .05 for planned comparison tests. Data from the treatments of related offspring were provided by Moura et al. (2017) [Colour figure can
be viewed at wileyonlinelibrary.com]

cannot detect offspring relatedness. In the following lines, we will
briefly discuss the behavioral process that can influence male care
and trigger paternal behaviors in this species. We then discuss the
possible factors determining the absence of offspring discrimination
by males.
The rarity of paternal care in Araneae may be explained by short
male life spans and high uncertainty of paternity (Yip & Rayor, 2014).
The dome-shaped webs built by M. porracea males, directly above
the web of a female, may overcome these constraints. While spider
males usually do not feed during adulthood (Buchli, 1969), the con-
struction of these webs by M. porracea males may provide resources
during all the reproductive season, potentially increasing their lifes-
pan. In addition, the interception of prey in their own webs reduces
potential conflicts and competition for prey with their partners
(Moura et al., 2017). Finally, the web building behavior also provides
a long lasting connection between the webs of males and females,
which facilitates pre- and post-copulatory mate guarding by males
(Moura & Gonzaga, 2017; Moura et al., 2017). Therefore, the emer-
gence of longstanding male webs may have played a significant role
in determining a relatively high certainty of paternity in this species.
In M. porracea, early male maturation (protandry) and the behav-
ioral strategy of guarding subadult females before and after mating
may reduce sperm competition, minimize cuckoldry, and increase
male reproductive success (Moura et al., 2020). There is no informa-
tion on the natural frequency of male replacement in female's webs,
but it is possible that the mating system of M. porracea has a higher
proportion of monogamous partners than previously thought. If this
is true and male desertion is a relatively uncommon occurrence, the
costs associated with the incapacity of identifying unrelated prog-
eny would be low for males, and offspring recognition would not be
expected to evolve. There are some evidences supporting this “mo-
nogamy hypothesis.” Large males of M. porracea have advantages in
intrasexual competition (Moura & Gonzaga, 2017). In a promiscuous
population, they would increase their fitness by deserting fathered
offspring and searching for new mating opportunities. However, the
probability of caring for offspring is similar between males with dif-
ferent sizes in the studied population (Moura et al., 2019), mean-
ing that strong large competitors were not more prone to abandon
offspring compared to weak small competitors. Therefore, after
copulation, males are likely to remain in the web guarding the mate,
regardless their chances of obtaining new mating opportunities.
In another possible scenario, males may often abandon their
initial partners after copulation, searching for additional mating op-
portunities. This behavior would possibly generate a reproductive
advantage during the beginning of the breeding season, when sev-
eral receptive females are still available. In addition, as females are
able to protect the eggs without male assistance (Moura et al., 2017),
the impact of male desertion on offspring survival would be low in
this period due to maternal care. Late in the breeding season, how-
ever, males would acquire at least some mating opportunities with
previously mated females, which carry sperm produced by other
males or that already laid some egg sacs before their arrival. Thus,
the paternal care observed after female's death will often involve the
protection of some proportion of unrelated eggs and/or juveniles.
Our results indicate that males of M. porracea accept the significant
risks of agonistic interactions with araneophagic invaders to protect

228 | MOURA et al.
the egg sacs even in this situation of paternity uncertainty. The
maintenance of these protective behaviors by males in the absence
of females may be assured by the relative advantage of increasing
the survivorship of at least some of their offspring when receptive
females are unavailable, rare, or widely dispersed. The proportion
of eggs under alloparental care would be influenced by patterns of
sperm precedence.
We have no information on the possibility of sperm mixing within
the spermathecae or on the occurrence of cryptic female choice,
but first male sperm precedence is usually predicted for polyan-
drous Entelegynae spider species, such as M. porracea (Snow &
Andrade, 2005; Watson, 1991). However, it is important to evaluate
whether first sperm precedence is a pattern of egg fertilization in
M. porracea, because the spermathecae morphology may be a poor
predictor of sperm precedence for Araneae (Uhl, 2002), especially
when the female mate with multiple partners (Zeh & Zeh, 1994).
Considering a possible greater advantage for the first male in sperm
competition determined by sperm precedence, indiscriminate pa-
ternal care may represent a large cost for males pairing late in the
reproductive season. This would be true even for those males that
copulated before the first event of egg laying by the females. In the
situation established in our experiment, however, the costs may be
even higher. In this case, males experienced a situation in which the
egg sacs attached on the web contained only the progeny of other
males. The results indicating the protective role assumed and effi-
ciently performed by males in this situation lead to the question of
why they do not act to prevent the investment in alloparental care
by consuming the egg sacs previously laid by females or by avoiding
agonistic interactions with the araneophagic invader.
The answer to that question requires further investigation, but
there are some testable possibilities to explain the protection of un-
related progeny by foster males. The first possibility is that males
simply cannot discriminate offspring relatedness. We are assuming
that males in our experiment are aware that they are not the fathers
of the progeny because the experiment simulate the entrance in a
new web. However, it is possible that males are unable to recognize
any chemical or structural sign to differentiate the egg sacs pro-
duced by their original partners from those inserted in the vials. In
this case, they would be just extending the care provided in a situa-
tion of relative certainty of paternity to the experimental condition
with a different egg sac. Females of at least three Anelosimus species
(Theridiidae) cannot discriminate between their progeny and foreign
egg sacs, which may be a step in the evolution of alloparental care
and sociality in this group (Samuk & Avilés, 2013). More recently,
however, there has been an accumulation of evidence for parental
discrimination in spiders, but it was investigated only from the fe-
male perspective (Anthony, 2003; Clark & Jackson, 1994; Japyassú
et al., 2003; Ruch et al., 2014; Yip & Rayor, 2014). There is no evi-
dence, by now, that males of M. porracea can evaluate offspring re-
latedness (Moura et al., 2017, 2019), and our study is an additional
evidence against male parental recognition hypothesis.
A second possibility is that females may use the entire sperm stor-
age from the first male to fertilize the eggs laid in the initial egg sacs,
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especially if the copulation duration of the first partner is low or he
produces less sperm than the second one (Assis & Foellmer, 2016).
Females may also dump the sperm from their spermathecae, such
as observed in other spider species (Eberhard, 2009). In both cases,
females should be receptive to additional mating opportunities, and
the new partners may not confront intense sperm competition. To
evaluate these hypotheses, future studies may investigate whether
(a) the amount of sperm deposited within female spermathecae after
the first copulation is sufficient to fertilize all eggs produce during
her lifespan; (b) the copulation with an additional partner largely
increases the number of fertilized eggs laid by females; and (c) the
female can remove the sperm from its spermathecae.
In conclusion, we found consistent evidence that males of
M. porracea can efficiently protect egg sacs, regardless of parent-
hood, against the two most common araneophagic spider invaders
found in their webs. We have suggested some possible causes for
the investment and risk assumed by males to protect the egg sacs,
but further studies, especially on patterns of sperm precedence,
percentage of offspring fathered by the protective male, mating
system, and the frequency of male desertion, are necessary to
fully understand this exceptional evolutionary strategy adopted by
M. porracea.
AC K N OW L E D G M E N T S
The pre-title “Where ignorance is bliss, 'tis folly to be wise” is
a reference to the poem “Ode on a Distant Prospect of Eton
College” (1742) by Thomas Gray. This project was supported
by Fundação de Amparo à Pesquisa do Estado de São Paulo
(São Paulo Research Foundation, FAPESP: Proc. 2017/14196-5;
465562/2014-0), Fundação de Amparo à Pesquisa do Estado de
Minas Gerais (FAPEMIG: Proc. APQ-02984-17, APQ-02104-14,
CRA-30058/12, APQ-03202-13), Duratex S.A., Instituto Nacional
de Ciência e Tecnologia dos Hymenoptera Parasitoides da Região
Sudeste (HYMPAR/Sudeste—CNPq/CAPES/FAPESP), and Conselho
Nacional de Desenvolvimento Científico e Tecnológico (CNPq: Proc.
306157/2014-4; 403733/2012-0; 445832/2014-2; 465562/2014-
0; 441225/2016-0).
C O N FL I C T O F I N T E R E S T
The authors declare that they have no conflict of interest.
ORCID
Rafael Rios Moura https://orcid.org/0000-0002-7911-4734
REFERENCES
Anthony, C. D. (2003). Kinship influences cannibalism in the wolf spider,
Pardosa milvina. Journal of Insect Behavior, 16(1), 23–36. https://doi.
org/10.1023/A:10228​93127216
Aquino, F. D. G., Walter, B. M. T., & Ribeiro, J. F. (2007). Woody com-
munity dynamics in two fragments of “cerrado” stricto sensu over
a seven-year period (1995–2002), MA, Brazil. Revista Brasileira de
Botânica, 30(1), 113–121. https://doi.org/10.1590/S0100-84042​
00700​0100011

MOURA et al.
Assis, B. A., & Foellmer, M. W. (2016). One size fits all? Determinants
of sperm transfer in a highly dimorphic orb-web spider. Journal of
Evolutionary Biology, 29(6), 1106–1120. https://doi.org/10.1111/
jeb.12848
Balshine, S. (2012). Patterns of parental care in vertebrates. In N. J.
Royle, P. T. Smiseth, & M. Kölliker (Eds.), Parental care (pp. 62–75).
Oxford University Press.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear
mixed-effects models using lme4. Journal of Statistical Software,
67(1), 1–48. https://doi.org/10.18637/​jss.v067.i01
Beal, C. A., & Tallamy, D. W. (2006). A new record of amphisexual care in
an insect with exclusive paternal care: Rhynocoris tristis (Heteroptera:
Reduviidae). Journal of Ethology, 24(3), 308. https://doi.org/10.1007/
s10164-006-0212-8
Buchli, H. H. R. (1969). Hunting behavior in the Ctenizidae. American
Zoologist, 9(1), 175–193. https://doi.org/10.1093/icb/9.1.175
Buzatto, B. A., & Machado, G. (2009). Amphisexual care in Acutisoma
proximum (Arachnida, Opiliones), a neotropical harvestman with ex-
clusive maternal care. Insectes Sociaux, 56(1), 106–108. https://doi.
org/10.1007/s00040-008-1044-z
Clark, R. J., & Jackson, R. R. (1994). Portia labiata, a cannibalistic jumping
spider, discriminates between own and foreign eggsacs. International
Journal of Comparative Psychology, 7(1), 38–43.
Clutton-Brock, T. H. (1991). The evolution of parental care. Princeton
University Press.
Eberhard, W. (1996). Female control: Sexual selection by cryptic female
choice. Princeton University Press.
Eberhard, W. (2009). Why study spider sex: Special traits of spiders facil-
itate studies of sperm competition and cryptic female choice. Journal
of Arachnology, 32, 545–556.
Fox, J., & Weisberg, S. (2019). An R companion to applied regression, 2nd
ed: Sage. http://socse​r v.socsci.mcmas​ter.ca/jfox/Books/​Compa​nion
Fromhage, L., & Jennions, M. D. (2016). Coevolution of parental invest-
ment and sexually selected traits drives sex-role divergence. Nature
Communications, 7(1), e12517. https://doi.org/10.1038/ncomm​s12517
Furness, A. I., & Capellini, I. (2019). The evolution of parental care diver-
sity in amphibians. Nature Communications, 10(1), 4709. https://doi.
org/10.1038/s41467-019-12608-5
Gaskett, A. C. (2007). Spider sex pheromones: Emission, reception,
structures, and functions. Biological Reviews, 82(1), 27–48. https://
doi.org/10.1111/j.1469-185X.2006.00002.x
Gilbert, J. D. J., & Manica, A. (2015). The evolution of parental care in
insects: A test of current hypotheses. Evolution, 69(5), 1255–1270.
https://doi.org/10.1111/evo.12656
Gonzaga, M. O., & Leiner, N. O. (2013). Maternal care and infanticide by
males in Helvibis longicauda (Araneae: Theridiidae). Ethology, 119(1),
20–28. https://doi.org/10.1111/eth.12032
Griffin, A. S., Alonzo, S. H., & Cornwallis, C. K. (2013). Why do cuckolded
males provide paternal care? PLoS Biology, 11(3), e1001520. https://
doi.org/10.1371/journ​al.pbio.1001520
Herberstein, M. E., Schneider, J. M., Uhl, G., & Michalik, P. (2011). Sperm
dynamics in spiders. Behavioral Ecology, 22(4), 692–695. https://doi.
org/10.1093/behec​o/arr053
Japyassú, H. F., Macagnan, C. R., & Knysak, I. (2003). Eggsac recognition
in Loxosceles gaucho (Araneae, Sicariidae) and the evolution of mater-
nal care in spiders. Journal of Arachnology, 31(1), 90–104.
Kleiber, C., & Zeileis, A. (2008). Applied econometrics with R:
Springer-Verlag.
Kokko, H., & Jennions, M. D. (2008). Parental investment, sexual selec-
tion and sex ratios. Journal of Evolutionary Biology, 21(4), 919–948.
https://doi.org/10.1111/j.1420-9101.2008.01540.x
Kondoh, M., & Okuda, N. (2002). Mate availability influences filial can-
nibalism in fish with paternal care. Animal Behaviour, 63(2), 227–233.
https://doi.org/10.1006/anbe.2001.1915
14390310, 2021, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/eth.13112 by UNEB - Universidade do Estado da Bahia, Wiley Online Library on [30/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
| 229
Kvarnemo, C. (2006). Evolution and maintenance of male care: Is in-
creased paternity a neglected benefit of care? Behavioral Ecology,
17(1), 144–148. https://doi.org/10.1093/behec​o/ari097
Machado, G., & Trumbo, S. T. (2018). Parental care. In A. Córdoba-
Aguilar, D. González-Tokman, & I. González-Santoyo (Eds.), Insect be-
havior: From mechanisms to ecological and evolutionary consequences
(pp. 203–218). Oxford University Press.
Moura, R. R., & Gonzaga, M. O. (2017). Temporal variation in size-as-
sortative mating and male mate choice in a spider with amphisex-
ual care. The Science of Nature, 104, 3–4. https://doi.org/10.1007/
s00114-017-1448-6
Moura, R. R., Pinto, N. S., Vasconcellos-Neto, J., & Gonzaga, M. O. (2019).
Does body size influence male care? Investigating an alternative re-
productive tactic in Manogea porracea (Araneae: Araneidae), a spider
with amphisexual care. Journal of Insect Behavior, 32(3), 201–206.
https://doi.org/10.1007/s10905-019-09725-w
Moura, R. R., Vasconcellos-Neto, J., & Gonzaga, M. O. (2017). Extended
male care in Manogea porracea (Araneae: Araneidae): The exceptional
case of a spider with amphisexual care. Animal Behaviour, 123, 1–9.
https://doi.org/10.1016/j.anbeh​av.2016.09.018
Moura, R. R., Vasconcellos-Neto, J., & Gonzaga, M. O. (2020). Female
sexual maturity as a determining factor of size-assortative pairing
in the protandrous spider Manogea porracea (Araneae, Araneidae).
Zoologischer Anzeiger, 284, 1–6. https://doi.org/10.1016/j.
jcz.2019.11.003
Neff, B. D. (2003). Decisions about parental care in response to perceived
paternity. Nature, 422(6933), 716–719. https://doi.org/10.1038/
natur​e 01528
Pascini, T. V., & Martins, G. F. (2017). The insect spermatheca: An overview.
Zoology, 121, 56–71. https://doi.org/10.1016/j.zool.2016.12.001
Peel, M. C., Finlayson, B. L., & McMahon, T. A. (2007). Updated world
map of the Köppen-Geiger climate classification. Hydrology and
Earth System Sciences, 11(5), 1633–1644. https://doi.org/10.5194/
hess-11-1633-2007
Queller, D. C. (1997). Why do females care more than males? Proceedings
of the Royal Society B: Biological Sciences, 264(1388), 1555–1557.
https://doi.org/10.1098/rspb.1997.0216
R Development Core Team (2020). R: A language and environment for sta-
tistical computing (p. 3.6.2). https://www.r-proje​c t.org/ .
Requena, G. S., & Alonzo, S. H. (2017). Sperm competition games when
males invest in paternal care. Proceedings of the Royal Society B:
Biological Sciences, 284(1860), e20171266. https://doi.org/10.1098/
rspb.2017.1266
Requena, G. S., Munguía-Steyer, R., & Machado, G. (2014). Paternal care
and sexual selection in arthropods. In Sexual Selection: Perspectives
and models from the Neotropics (pp. 201–233). Elsevier. https://doi.
org/10.1016/B978-0-12-416028-6.00008-6
Reynolds, J. D., Goodwin, N. B., & Freckleton, R. P. (2002). Evolutionary
transitions in parental care and live bearing in vertebrates.
Philosophical Transactions of the Royal Society of London. Series B:
Biological Sciences, 357(1419), 269–281. https://doi.org/10.1098/
rstb.2001.0930
Royle, N. J., Smiseth, P. T., & Kölliker, M. (2012). The evolution of parental
care. Oxford University Press.
Ruch, J., Herberstein, M. E., & Schneider, J. M. (2014). Offspring dynamics
affect food provisioning, growth and mortality in a brood-caring spi-
der. Proceedings of the Royal Society B: Biological Sciences, 281(1779),
e20132180. https://doi.org/10.1098/rspb.2013.2180
Safari, I., & Goymann, W. (2018). Certainty of paternity in two coucal
species with divergent sex roles: The devil takes the hindmost.
BMC Evolutionary Biology, 18(1), 110. https://doi.org/10.1186/
s12862-018-1225-y
Samuk, K., & Avilés, L. (2013). Indiscriminate care of offspring predates
the evolution of sociality in alloparenting social spiders. Behavioral

230 | MOURA et al.
Ecology and Sociobiology, 67(8), 1275–1284. https://doi.org/10.1007/
s00265-013-1555-0
Schulte, K. F., Uhl, G., & Schneider, J. M. (2010). Mate choice in males
with one-shot genitalia: Limited importance of female fecundity.
Animal Behaviour, 80(4), 699–706. https://doi.org/10.1016/j.anbeh​
av.2010.07.005
Smith, C., & Wootton, R. J. (1995). The costs of parental care in teleost
fishes. Reviews in Fish Biology and Fisheries, 5(1), 7–22. https://doi.
org/10.1007/BF011​03363
Snow, L. S., & Andrade, M. C. (2005). Multiple sperm storage organs fa-
cilitate female control of paternity. Proceedings of the Royal Society B:
Biological Sciences, 272(1568), 1139–1144. https://doi.org/10.1098/
rspb.2005.3088
Tallamy, D. W. (2001). Evolution of exclusive paternal care in arthro-
pods. Annual Review of Entomology, 46(1), 139–165. https://doi.
org/10.1146/annur​ev.ento.46.1.139
Uhl, G. (2002). Female genital morphology and sperm priority patterns in
spiders (Araneae). In S. Toft, & N. Scharff (Eds.), European Arachnology
2000 (pp. 145–156). Aarhus University Press.
Watson, P. J. (1991). Multiple paternity and first mate sperm precedence
in the sierra dome spider, Linyphia litigiosa Keyserling (Linyphiidae).
14390310, 2021, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/eth.13112 by UNEB - Universidade do Estado da Bahia, Wiley Online Library on [30/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Animal Behaviour, 41(1), 135–148. https://doi.org/10.1016/
S0003-3472(05)80509-3
Wright, J. (1998). Paternity and paternal care. In T. R. Birkhead, & A. P.
Moller (Eds.), Sperm Competition and Sexual Selection (pp. 117–145).
Academic Press.
Yip, E. C., & Rayor, L. S. (2014). Maternal care and subsocial behaviour in
spiders. Biological Reviews, 89(2), 427–449. https://doi.org/10.1111/
brv.12060
Zeh, J. A., & Zeh, D. W. (1994). Last-male sperm precedence breaks down
when females mate with three males. Proceedings of the Royal Society
of London. Series B: Biological Sciences, 257(1350), 287–292. https://
doi.org/10.1098/rspb.1994.0127
How to cite this article: Moura RR, Oliveira ID, Vasconcellos-
Neto J, Gonzaga MO. “Where ignorance is bliss, 'tis folly to be
wise”: Indiscriminate male care in a neotropical spider. Ethology.
2021;127:223–230. https://doi.org/10.1111/eth.13112