Revisiting Parental Care in Triaenonychid Harvestmen (Opiliones)
Total Page：16
File Type：pdf, Size：1020Kb
2007. The Journal of Arachnology 35:202–204 SHORT COMMUNICATION MATERNAL OR PATERNAL EGG GUARDING? REVISITING PARENTAL CARE IN TRIAENONYCHID HARVESTMEN (OPILIONES) Glauco Machado: Departamento de Ecologia, Instituto de Biocieˆncias, Rua do Mata˜o, trav. 14, nЊ 321, Cidade Universita´ria, 05508-900, Sa˜o Paulo, SP, Brazil. E-mail:[email protected] ABSTRACT. Based on a photo published in a book on New Zealand arachnids, I propose here that the cases of maternal care described by Forster in 1954 should be considered as paternal care. Maternal care is therefore restricted to the superfamily Gonyleptoidea, while paternal care has evolved in five phylo- genetically independent lineages of Opiliones, including representatives of the superfamilies Travunioidea, Epedanoidea, and Gonyleptoidea. Keywords: Evolution, Karamea, Laniatores, Soerensenellinae In 1954, Ray Forster published a comprehensive paternal care (see Machado et al. 2004). Unfortu- study on New Zealand harvestmen in which he pro- nately no photograph or drawings were provided in vided a detailed taxonomic account of the family Forster’s paper and no voucher specimens were Triaenonychidae and also described basic aspects of mentioned for the behavioral observations; thus it the natural history of some species. As far as I is not possible to examine the individuals studied know, this work was the first record of maternal by Forster in order to determine the identity of the care in the order Opiliones. Based on field and lab- sex that provides care. oratory observations, the author stated that all New More recently, Ray and Lynn Forster published Zealand representatives of the subfamily Soeren- a book called ‘‘Spiders of New Zealand and Their senellinae lay small groups of eggs (n ϭ 10–20) on Worldwide Kin’’ (Forster & Forster 1999), which the undersurface of logs or rocks, which are guard- contains a brief description of the general biology ed by the female. Some additional information is of the New Zealand harvestmen, mostly based on presented: ‘‘At intervals of a few days or a week the data previously presented in his paper of 1954. further eggs are deposited so that in some cases egg The book provides a color photo of an individual masses of some 60–100 eggs may be found, some of Karamea sp. (Triaenonychidae, Soerensenelli- of which are hatching, while others are found at all nae) guarding an egg-batch (Figure 1). This photo stages, often including newly laid eggs’’ (Forster is highly informative since it clearly shows that the 1954). parental individual is a male and not a female. There are several differences in the behavioral Many triaenonychid males are easily recognized patterns of guarding females and guarding males in due to the size of their swollen chelicerae and, in harvestmen, which are probably a consequence of some species, also to the shape of the ocularium, the different selective pressures leading to the evo- which bends forwards while in females it is an erect lution of maternal care (via natural selection) or pa- spine (Lawrence 1937; Maury & Roig-Alsina ternal care (probably via sexual selection). Perhaps 1985). Moreover, it is also possible to recognize in the most striking difference is that females care for the photo that the eggs are in different stages of batches containing eggs in only one stage of em- embryonic development (as described by Forster bryonic development, while males care for batches 1954), which is congruent with the multiple ovi- containing eggs in several stages of embryonic de- postions observed in paternal harvestmen. Thus, velopment, likely from the result of different ovi- Figure 1 provides unequivocal evidence that at least position events (Machado et al. 2004). Therefore, in this species of the genus Karamea the guarding the behavioral pattern of oviposition described for individuals are males. However, there is no reason the New Zealand Soerensenellinae contrasts with all to believe that this case is an exception since For- other harvestman species that present maternal care ster (1954) clearly states that all New Zealand So- and is remarkably similar to the species that present erensenellinae show the same reproductive pattern. 202 MACHADO—PATERNAL CARE IN TRIAENONYCHID HARVESTMEN 203 Figure 1.—Male of the triaenonychid harvestman Karamea sp. (Soerensenellinae) caring for eggs in different embryonic stages (noted by the difference in size and coloration) under a rotting log in New Zealand. Photo by Forster & Forster (1999), reproduced here with the permission of the University of Otago Press. Consequently, paternal care, and not maternal care, arachnids was reported only at the end of the 1970s is probably the rule in the subfamily. A final piece when Rodrı´guez & Guerrero (1976) described of information that can be extracted from the photo, males of the manaosbiid harvestman Zygopachylus which has never been mentioned by Forster, is that albomarginis Chamberlain 1925 guarding eggs and the debris is attached to the eggs, probably by the early hatched nymphs inside mud nests in Panama. ovipositing females. This behavior has been previ- Even if we take arthropods as a whole, the number ously described for several harvestman species of of cases of paternal care in the literature by the the families Cosmetidae and Gonyleptidae that pre- 1950s was low (see references in Tallamy 2001). sent no care or exclusive maternal care (references On the other hand, maternal care has been reported in Willemart 2001), but it is the first record of its as early as the 18th and 19th centuries for non-social existence in a paternal species. insects (e.g., Modeer 1764) and arachnids (e.g., La- Debate about the existence of paternal care has treille 1802). been commonplace in the behavioral literature (see The presence of paternal care in the New Zealand examples in Tallamy 2001), but misinterpretations triaenonychids has important implications for the about the sex of the guarding individuals are some- evolution of the forms of parental care in the order what rare. Tallamy et al. (2004) recently showed Opiliones, particularly among the Laniatores. Ma- that, with the assassin bug Atopozelus pallens, the ternal care is therefore restricted to the superfamily females and not the males are responsible for egg Gonyleptoidea, occurring in the families Cosmeti- protection. Curiously, like the case of triaenony- dae, Cranaidae, Gonyleptidae, and Stygnopsidae chids reported here, the sexual dimorphism is quite (see references in Machado & Raimundo 2001; Ma- evident and males and females can be easily rec- chado & Warfel 2006). The first real case of ma- ognized in the field. Another interesting case of ternal assistance in harvestmen belongs to the gon- mistaken parental identity is found in giant water yleptid Acanthopachylus aculeatus (Kirby 1818) bugs (Heteroptera: Belostomatidae) in which males from Uruguay (Capocasale & Bruno-Trezza 1964). of the subfamily Belostomatinae brood eggs laid by Paternal care, on the other hand, has evolved in five the females on their backs (Smith 1997). Since phylogenetically independent lineages of Opiliones: there is no clear sexual dimorphism among belos- once in Soerensenellinae triaenonychids (superfam- tomatines, the parental behavior was originally at- ily Travunioidea), once in podoctids (superfamily tributed to females (Dimmock 1887). Surprisingly Epedanoidea), once in assamiids, and at least twice the mistake was not corrected for several years in gonyleptids (superfamily Gonyleptoidea) (see (Slater 1899), despite the fact that females are clear- references in Machado et al. 2004). ly unable to lay eggs on their own dorsum. I thank Wendy Harrex from the Otago University A putative explanation for Forster’s mistake is Press for giving me the permission to reproduce the that he was influenced by the widespread occur- photo of the male Karamea, Adriano B. Kury for rence of maternal care in arthropods and the total identifying the sex of the individual in Figure 1, absence of paternal care in arachnids until that mo- Rogelio Macı´as Ordo´n˜ez, Jeffrey W. Shultz, and ment. The first case of paternal assistance in the two anonymous reviewers for comments on the 204 THE JOURNAL OF ARACHNOLOGY manuscript. GM is supported by grants from Fun- Laniatores). Journal of Arachnology 34:269– dac¸a˜o de Amparo a` Pesquisa do Estado de Sa˜o Pau- 272. lo (FAPESP, proc. #02/00381-0). Maury, E.A. & A.H. Roig-Alsina. 1985. Triaenon- ychidae sudamericanos I. El ge´nero Ceratomon- LITERATURE CITED tia Roewer, 1915 (Opiliones: Laniatores). His- Capocasale, R. & L. Bruno-Trezza. 1964. Biologı´a toria Natural 5:77–92. de Acanthopachylus aculeatus (Kirby, 1819) Modeer, A. 1764. Na˚gra ma¨rkva¨rdigheter hos in- (Opiliones: Pachylinae). Revista de la Sociedad sectet Cimex ovatus pallide griseus, abdominis Uruguaya de Entomologı´a 6:19–32. lateribus albo nigroge variis alib albis basi scu- Dimmock, G. 1887. Belostomatidae and other fish telli nigricante. Kongliga Vetenskaps Acade- destroying bugs. Zoologist 11:101–105. miens Handlingar 25:41–47. Forster, R.R. 1954. The New Zealand harvestmen Rodrı´guez, C.A. & S. Guerrero. 1976. La historia (sub-order Laniatores). Canterbury Museum Bul- natural y el comportamiento de Zygopachylus al- letin 2:1–329. bomarginis (Chamberlin) (Arachnida: Opiliones: Forster, R.R. & L. Forster. 1999. Spiders of New Gonyleptidae). Biotropica 8:242–247. Zealand and Their Worldwide Kin. Otago Uni- Slater, F.W. 1899. The egg-carrying habit of Zaitha. versity Press, Dunedin, New Zealand. 270 pp. American Naturalist 33:931–933. Latreille, P.A. 1802. Histoire Naturelle des Fourmis, Smith, R.L. 1997. Evolution of paternal care in the et Recueil de Me´moires et d’Observations sur les giant water bugs (Heteroptera: Belostomatidae). Abeilles, les Araigne´es, les Faucheurs, et Autres Pp. 116–149. In The Evolution of Social Behav- Insectes. Crapelet, Paris. 445 pp. iour in Insects and Arachnids (J.C. Choe & B.J. Lawrence, R.F. 1937. The external sexual charac- Crespi, eds.). Cambridge University Press, Cam- teristics of South African harvest-spiders.