Extended male care in Manogea porracea (Araneae: Araneidae): the exceptional case of a spider with amphisexual care

doi:10.1016/j.anbehav.2016.09.018

Animal Behaviour

Volume 123, January 2017, Pages 1-9

https://doi.org/10.1016/j.anbehav.2016.09.018 Get rights and content

Highlights

•
The first description of amphisexual and paternal care in a solitary spider.
•
Male Manogea porracea protected their offspring against araneophagic spiders.
•
Web maintenance by males, in the absence of females, increased offspring survival.
•
OSR became increasingly biased towards males throughout the reproductive season.
•
Paternal care occurred more often at the end of the reproductive season.

Paternal care is less common than maternal care because male fitness usually depends on the number of mating opportunities with distinct females. Yet, males also invest in parental care when offspring survival depends on paternal contribution for protection and/or brood nutrition and mating opportunities with new females are scarce. Although the second condition is common in spiders, male contribution to the survival of spiderlings is very rare. However, males of Manogea porracea build their webs above female webs, where they capture prey throughout the reproductive period. In addition, both sexes may have contact with eggsacs and attack predators that approach them. This unusual extended period of co-occurrence between males and their offspring may favour the establishment of paternal care. Here, we investigated (1) the mortality factors influencing offspring survival, (2) how the presence of parents affects offspring survival, (3) how males affect web integrity and protect eggs against predation and (4) variations in operational sex ratio (OSR) during the reproductive season, along with the proportion of eggsacs in webs occupied by males alone before the dispersal of spiderlings. We found that (1) four kleptoparasitic/araneophagic spider species invaded webs and attacked eggsacs, (2) parental care significantly improved offspring survival, (3) males maintained web integrity and protected offspring against the attacks of two araneophagic species and (4) the OSR became quickly biased towards males, and that these remaining males assumed exclusive care of 68% of the eggsacs produced during the season. The ability of males to protect the offspring and the reduced availability of receptive females at the end of the reproductive season might represent the possible causes of male care in M. porracea. We propose that web building by males and their rapid access to the eggsacs create unique conditions that may favour the evolution of paternal care in Cyrtophorinae.

Section snippets

Study Site

This study was carried out between 2013 and 2015 in a Eucalyptus plantation in Fazenda Nova Monte Carmelo, property of Duratex S.A., located in the municipality of Estrela do Sul, Minas Gerais, Brazil (18°49′27″S, 47°51′47″W). Areas covered by Eucalyptus are interspersed with fragments of native Cerrado vegetation. However, all webs of M. porracea were located within the Eucalyptus plantation.

Study Species

Manogea porracea is a widespread Neotropical spider that occurs from Panama to Argentina (Levi, 1997,

Male Behaviours and Mortality Factors Influencing Offspring Survival

We observed four spider species attacking the eggsacs and the adults of M. porracea: Faiditus caudatus (Theridiidae), A. elevatus (Theridiidae), Gelanor zonatus (Mimetidae) and Mimetus sp. (Mimetidae) (Fig. 2). However, both mimetid species were found attacking eggsacs only during eventual observations. Gelanor zonatus was often observed attacking adults of M. porracea, and Mimetus sp. was found only once attacking a M. porracea female. In December 2013, during standard inspections, we only

Discussion

All described cases of parental care in spiders are restricted to the efforts of mothers to protect and/or feed their offspring, including sharing prey items, regurgitation, production of trophic eggs and matriphagy (Yip & Rayor, 2014). The only exception seems to be the case of the social African species S. dumicola. Kürpick (2002) observed that some males of S. dumicola react aggressively to ants and other intruders that attempt to remove eggsacs from colonies, even when females are absent.

Acknowledgments

We thank Paulo Enrique Cardoso Peixoto for comments on a first draft of this manuscript, Giancarlo Ângelo Ferreira and Yuri Lima Vasconcelos Ferreira for providing transport to study area on several occasions and Duratex S.A. for allowing our work in Fazenda Nova Monte Carmelo. This project was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (research grant to R.R.M.), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Proc. APQ-02104-14, CRA-30058/12), Instituto

References (75)

S. Balshine et al.
Parental care in fishes
L.S. Fink
Cost and benefits of maternal behavior in the green lynx spider (Oxyopidae, Peucetia viridians)
Animal Behaviour
(1986)
A.I. Houston et al.
The parental investment models of Maynard Smith: A retrospective and prospective view
Animal Behaviour
(2013)
M. Itzkowitz et al.
Parental division of labour and the shift from minimal to maximal role specializations: An examination using a biparental fish
Animal Behaviour
(2001)
J. Lehtonen et al.
The many costs of sex
Trends in Ecology & Evolution
(2012)
M.J. Magrath et al.
Is male care compromised by additional mating opportunity?
Trends in Ecology & Evolution
(2003)
D. Mayntz et al.
Balancing of protein and lipid intake by a mammalian carnivore, the mink, Mustela vison
Animal Behaviour
(2009)
T.M. Nazareth et al.
Mating system and exclusive extended paternal care in a Neotropical harvestman (Arachnida: Opiliones)
Animal Behaviour
(2010)
A. Qvarnström et al.
Maternal effects, paternal effects and sexual selection
Trends in Ecology & Evolution
(2001)
G.S. Requena et al.
Efficiency of uniparental male and female care against egg predators in two closely related syntopic harvestmen
Animal Behaviour
(2009)

M. Ridley

Paternal care

Animal Behaviour

(1978)

R. Rios Moura et al.

The effect of operational sex ratio on the opportunity for sexual selection: A meta-analysis

Animal Behaviour

(2013)

J.M. Schneider et al.

Infanticide by males in a spider with suicidal maternal care, Stegodyphus lineatus (Eresidae)

Animal Behaviour

(1997)

M. Anderson

Sexual selection

(1994)

M.A. Benamú et al.

Postembryonic development and population parameters of Alpaida veniliae (Araneae, Araneidae), reared in the laboratory

Journal of Natural History

(2011)

H.H. Buchli

Hunting behavior in the Ctenizidae

American Zoologist

(1969)

B.A. Buzatto et al.

Amphisexual care in Acutisoma proximum (Arachnida, Opiliones), a neotropical harvestman with exclusive maternal care

Insect Sociaux

(2009)

T.H. Clutton-Brock

The evolution of parental care

(1991)

T. Clutton-Brock

Sexual selection in males and females

Science

(2007)

M.A. Elgar

Sperm competition and sexual selection in spiders and other arachnids

S.T. Emlen et al.

Ecology, sexual selection, and the evolution of mating systems

Science

(1977)

R.F. Foelix

Biology of spiders

(2011)

M.O. Gonzaga et al.

Maternal care and infanticide by males in Helvibis longicauda (Araneae: Theridiidae)

Ethology

(2013)

M.E. Herberstein et al.

Costs of courtship and mating in a sexually cannibalistic orb-web spider: Female mating strategies and their consequences for males

Behavioral Ecology and Sociobiology

(2002)

C.S. Hieber

The hole of spider cocoons in controlling desiccation

Oecology

(1992)

A. Horel et al.

Egg sac guarding by the funnel-web spider Coelotes terrestris: Function and development

Behavioural Processes

(1992)

R.R. Jackson

The life history of Phidippus johnsoni (Araneae:Salticidae)

Journal of Arachnology

(1978)

R.R. Jackson et al.

The biology of New Zealand and Queensland pirate spiders (Araneae, Mimetidae): Aggressive mimicry, araneophagy and prey specialization

Journal of Zoology

(1986)

A.T. Kahn et al.

Paternity protection can provide a kick-start for the evolution of male-only parental care

Evolution

(2013)

M.M. Kasumovic et al.

Risky mate search and mate preference in the golden orb-web spider (Nephila plumipes)

Behavioral Ecology

(2007)

C.T. Kloock

Diet and insectivory in the ‘araneophagic’ spider, Mimetus notius (Araneae: Mimetidae)

American Midland Naturalist

(2001)

C.T. Kloock

Natural history of the pirate spider Mimetus hesperus (Araneae; Mimetidae) in Kern County, California

Southwestern Naturalist

(2012)

H. Klug et al.

Theoretical foundations of parental

H. Klug et al.

Sex differences in life history drive evolutionary transitions among maternal, paternal, and bi-parental care

Ecology and Evolution

(2013)

S.M. Kürpick

Cocoon care in the social spider Stegodyphus dumicola (Eresidae)

R.M. Lehtinen et al.

Impacts of paternal care and seasonal change on offspring survival: A multiseason experimental study of a Caribbean frog

Ethology

(2014)

H.W. Levi

The American orb weavers of the genera Mecynogea, Manogea, Kapogea and Cyrtophora (Araneae: Araneidae)

Bulletin of the Museum of Comparative Zoology

(1997)

Cited by (14)

Unrevealing components of risk assessment: escape behaviour and refuge use in a web-building spider
2024, Animal Behaviour
Optimal escape models assume that decisions to escape after a predation attempt depend on the initial risk assessment. However, few studies have explored animals' decisions to return to normal activities after their first escape and how the ecological context influences these behaviours. To address these gaps, we investigated the influence of substrate type on escape behaviour and refuge use in the spider Aglaoctenus castaneus. Individuals forage on sheet webs but hide in funnels after detecting potential threats. Spiders from two populations build webs either on injurious substrates that can harm predators or on noninjurious substrates. The dominant injurious substrates include a large thorny palm species in the ‘thorny palm’ population and a razor grass in the ‘razor grass’ population. We hypothesized that spiders constructing webs on injurious substrates would (1) display reduced sensitivity to approaching predators by hiding in their funnels and (2) would return to their sheet web more quickly after detecting a predator. We also assessed whether these behaviours were correlated across and within populations and whether they were affected by the social context (couples or solitary individuals). Spiders inhabiting injurious substrates exhibited shorter flight initiation distances (FIDs) compared to those inhabiting noninjurious substrates. Interpopulation variation was observed, with spiders from the thorny palm population displaying shorter FID and lower hiding time than those from the razor grass population. However, there was no correlation between FID and hiding time. Spiders from the thorny palm population showed less sensitivity to predators, probably because thorny palm location was safer than the razor grass location. In conclusion, A. castaneus can adjust risk-taking behaviours depending on the damaging potential of the substrate for predators. We propose new hypotheses with the aim of improving risk assessment research.
Don't put all your eggs in small baskets: Ineffective guardians, incidence of parasitoids and clutch size of Latrodectus geometricus (Araneae, Theridiidae) along an urban gradient
2021, Zoologischer Anzeiger
Maternal care is common in spiders, but the effects of egg protection by mothers on offspring survival remains understudied for most species, especially against parasitoids. Parasitoid incidence can also be modulated by host clutch size (since larger egg masses provide the opportunity of producing larger clutches for the parasitoids) and urbanization (by creating conditions that may restrict the occurrence of less tolerant species). In this study, we conducted field experiments with the brown widow spider Latrodectus geometricus to investigate the following hypothesis: (1) females are effective in the defense of eggs against parasitoids; (2) large clutch sizes are attacked more often by parasitoids than the smaller ones; and (3) the incidence of parasitoids in egg sacs decreases in a gradient from a preserved area to an urbanized one. The presence of caring females reduced by three times the incidence of two parasitoids, Baeus latrodecti (Hymenoptera, Scelionidae) and an unidentified Eulophidae wasp, compared to unattended egg sacs, but this distinction did not differ from a random distribution. Parasitoids were most often found in egg sacs containing few eggs. The incidence of B. latrodecti in egg sacs was highest in the area with an intermediate degree of urbanization, but Eulophidae wasps were unaffected by the urbanization gradient. We concluded that (1) females are generally ineffective at protecting their egg sacs against parasitoids, that (2) egg sacs containing small clutch sizes are usually more vunerable to parasitoid attacks, and that (3) urbanization does not reduce the incidence of the egg parasitoids identified here. Our study provides an important step towards our understanding of the interactions between spiders with parental care and egg parasitoids, suggesting new aspects to be investigated in future studies.
Araneophagy as an alternative foraging tactic to kleptoparasitism in two Argyrodinae (Araneae: Theridiidae) species
2021, Behavioural Processes
Citation Excerpt :
Host spiders can aggressively attack kleptoparasites if they represent a risk for eggs or spiderlings (Moura et al., 2021, 2017). In the absence of females, males protect their offspring regardless of body size (which is positively correlated with mating success) and kinship and may kill the invaders while protecting egg sacs (Moura et al., 2021, 2019, 2017). Therefore, the presence of one or both adults represent a high risk for the invaders when kleptoparasites try to consume eggs, spiderlings or adults (Fig. 1B–D).
Kleptoparasitism is assumed to be the main foraging strategy in some animal groups, such as the spiders of the subfamily Argyrodinae (Theridiidae). However, some species may also feed on silk threads, egg sacs, or even their hosts. The conditions determining these alternative foraging tactics remain unknown for most species. We performed field observations, stable isotope analysis and laboratory experiments to investigate kleptoparasitism and araneophagy of Argyrodes elevatus and Faiditus caudatus in webs of Manogea porracea (Araneidae). We evaluated the following hypotheses: (1) both species exhibit higher trophic positions than their hosts and closest to an araneophagic sympatric species; (2) host web selection is influenced by the presence of alternative resources (adult male and female, and egg sacs); and (3) they preferentially consume egg sacs instead of stored prey items. Both argyrodines showed higher trophic positions than their female hosts and closest to an araneophagic spider species. The invaders were found mainly on host webs with one adult and egg sacs and with egg sacs only. Finally, A. elevatus preferred to feed on prey captured by the host spider instead of egg sacs. We discussed the factors that can potentially determine the choices between foraging exclusively as kleptoparasites and consuming the hosts.
Female sexual maturity as a determining factor of size-assortative pairing in the protandrous spider Manogea porracea (Araneae, Araneidae)
2020, Zoologischer Anzeiger
Citation Excerpt :
After maturation and copulation, females lay their fertilized eggs inside egg sacs and protect offspring until the development of the first instars. In the absence of females, males can assume the parental activities until egg hatching and spiderling dispersion (Moura et al. 2017). We collected all couples visually located within a 1620 m2 (90 × 18 m) area of the Eucalyptus plantation at the beginning of the breeding season (August and September 2012; Fig. 2).
Protandry occurs when males mature prior to females in the breeding season. There may be a fitness benefit for males if they are able to copulate and defend virgin and more fecund females. Therefore, fitness benefits can be investigated by studying assortative mating during mate guarding of virgin females before and after female sexual maturation. The asynchrony of female development in the protandrous spider Manogea porracea (Araneidae) provides an opportunity to investigate how female sexual maturity (subadult and adult females) influence size-assortative pairing. We investigated size differences between couples composed of males and subadult females, and of males and adult females. We hypothesized that size-assortative pairing is stronger in couples with adult females. Adult females were larger than subadults, but the size of males paired with females from both groups was similar. We found assortative pairing within all couples involving an adult female. However, this pattern was not observed among couples with subadult females. It is possible that the production of sexual pheromones by adult females after their last molt intensifies male intrasexual competition, promoting positive assortative pairing. We discuss the potential mechanisms affecting male mate choice and mate competition during pairings in M. porracea.
Flexible compensation of uniparental care in an arachnid species: things are not always what they seem
2018, Animal Behaviour
Flexible compensatory parental care takes place when one parent increases its parental effort in response to its mate's reduction or absence. Although this behavioural response is well known in species with biparental care, the few cases attributed to species with uniparental care are usually based on descriptive observations of apparent compensation without a proper examination of its effects on offspring fitness. In the harvestman Serracutisoma proximum, a species with female uniparental care, harem-owning males stand on unattended clutches when the egg-tending females desert or die. Here, we experimentally investigated under field conditions whether this behaviour constitutes an example of true parental compensation. We evaluated the effects of ecological and life history factors on males' proximity to unattended clutches. We also presented egg predators to the harem-owning males and parental females when they were standing on their clutches and compared their aggressive responses. Finally, we compared egg survival between three manipulation groups: in the absence of both adults; in the presence of only the harem-owning males; and in the presence of the parental females. We observed that males spent considerably less time standing on clutches than parental females, rarely attacked potential egg predators (in contrast to parental females which commonly exhibited aggressive behaviours) and, ultimately, had no effect on offspring survival. Our results do not support the existence of paternal compensation in S. proximum. Instead, we hypothesize that males' behaviour comprises a tactic that increases: (1) fertilization success of unfertilized eggs retained by egg-tending females that temporarily abandon the clutch; and/or (2) mating success with newcomer mates that trade copulations for the opportunity to cannibalize the unattended offspring. This study demonstrates that it is imperative to formally test adaptive assumptions before deriving conclusions on the evolution of complex traits and their implications, as an apparently adaptive behaviour is not always what it seems.
Beyond classical theories: An integrative mathematical model of mating dynamics and parental care
2023, Journal of Evolutionary Biology

View all citing articles on Scopus

View full text

Extended male care in Manogea porracea (Araneae: Araneidae): the exceptional case of a spider with amphisexual care

Highlights

Section snippets

Study Site

Study Species

Male Behaviours and Mortality Factors Influencing Offspring Survival

Discussion

Acknowledgments

Animal Behaviour

Animal Behaviour

Animal Behaviour

Trends in Ecology & Evolution

Trends in Ecology & Evolution

Animal Behaviour

Animal Behaviour

Trends in Ecology & Evolution

Animal Behaviour

Animal Behaviour

Animal Behaviour

Animal Behaviour

Sexual selection

Postembryonic development and population parameters of Alpaida veniliae (Araneae, Araneidae), reared in the laboratory

Journal of Natural History

Hunting behavior in the Ctenizidae

American Zoologist

Amphisexual care in Acutisoma proximum (Arachnida, Opiliones), a neotropical harvestman with exclusive maternal care

Insect Sociaux

The evolution of parental care

Sexual selection in males and females

Science

Sperm competition and sexual selection in spiders and other arachnids

Ecology, sexual selection, and the evolution of mating systems

Science

Biology of spiders

Maternal care and infanticide by males in Helvibis longicauda (Araneae: Theridiidae)

Ethology

Costs of courtship and mating in a sexually cannibalistic orb-web spider: Female mating strategies and their consequences for males

Behavioral Ecology and Sociobiology

The hole of spider cocoons in controlling desiccation

Oecology

Egg sac guarding by the funnel-web spider Coelotes terrestris: Function and development

Behavioural Processes

The life history of Phidippus johnsoni (Araneae:Salticidae)

Journal of Arachnology

The biology of New Zealand and Queensland pirate spiders (Araneae, Mimetidae): Aggressive mimicry, araneophagy and prey specialization

Journal of Zoology

Paternity protection can provide a kick-start for the evolution of male-only parental care

Evolution

Risky mate search and mate preference in the golden orb-web spider (Nephila plumipes)

Behavioral Ecology

Diet and insectivory in the ‘araneophagic’ spider, Mimetus notius (Araneae: Mimetidae)

American Midland Naturalist

Natural history of the pirate spider Mimetus hesperus (Araneae; Mimetidae) in Kern County, California

Southwestern Naturalist

Theoretical foundations of parental

Sex differences in life history drive evolutionary transitions among maternal, paternal, and bi-parental care

Ecology and Evolution

Cocoon care in the social spider Stegodyphus dumicola (Eresidae)

Impacts of paternal care and seasonal change on offspring survival: A multiseason experimental study of a Caribbean frog

Ethology

The American orb weavers of the genera Mecynogea, Manogea, Kapogea and Cyrtophora (Araneae: Araneidae)

Bulletin of the Museum of Comparative Zoology