Harvest-Ironman: Heavy Armature, and Not Its Defensive Secretions, Protects a Harvestman Against a Spider
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Animal Behaviour 81 (2011) 127 e133 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Harvest-ironman: heavy armature, and not its defensive secretions, protects a harvestman against a spider Elene da Silva Souza, Rodrigo H. Willemart * Escola de Artes, Ciências e Humanidades, Universidade de São Paulo article info Natural selection has caused prey species to evolve distinct defensive mechanisms. One of such mech- Article history: anisms was the evolution of noxious or distasteful chemicals, which have appeared independently in Received 3 July 2010 a number of vertebrates and invertebrates. In detailed analyses of arthropod behaviour, scent gland Initial acceptance 31 August 2010 secretions have consistently been shown to be responsible for repelling speci fic predators. Because using Final acceptance 20 September 2010 such chemicals is costly, animals with alternative cheaper defences are expected not to release such Available online 18 October 2010 secretions when alternative options exist. In this study, we sought to determine the defensive mecha- MS. number: A10-00462 nisms of the harvestman Discocyrtus invalidus , a heavy bodied species that bears a pair of repugnatorial glands. The spider Enoploctenus cyclothorax was used as the predator, and the cricket Gryllus sp. was used Keywords: as a control. In a first set of experiments, the harvestmen were preyed upon signi ficantly less than the Araneae crickets. In two other experiments, we found that harvestmen did not use their scent gland secretions to defensive behaviour deter the predator. Moreover, results of a fourth experiment revealed that these spiders are not repelled foraging Discocyrtus invalidus multiple defences by defensive secretions. has a thick cuticle on the entire body: scanning electron Opiliones micrographs revealed that only the mouth, the articulations of appendages and the tips of the legs are prey capture not covered by a hard integument. In a fifth experiment, we found that these spiders had dif ficulty scent gland piercing the harvestmen body. This is the first experimental evidence that a chemically defended sclerotization arachnid does not use its scent gland secretions to repel a much larger predator but instead relies on its tegument heavily built body. Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Selective pressures caused by predators on prey species have led Arthropods have a particularly interesting array of repellent to the appearance of distinct defensive mechanisms that favour chemicals ( Roth & Eisner 1962 ). The identi fication of their scent greater survival and consequently a greater probability of gener- gland secretions and their repelling effects on predators have been ating offspring ( Lind & Cresswell 2005 ). In chemical defence, studied in different taxa, including Myriapoda, Insecta and Arach- noxious or distasteful chemicals have appeared independently nida ( Eisner 1970, 2005 ). Arachnids often release their prey and several times within metazoans, having evolved among sponges, may even autotomize their own legs in an attempt to get rid of the cnidarians, molluscans, annelids, arthropods, echinoderms, ascid- secretions ( Eisner 2005; Eisner et al. 2006 ). However, the costly ians and vertebrates such as amphibians, reptiles, mammals and production of defensive chemicals ( McCormick & Larson 2008 ) birds ( McClintock & Baker 1997; Dumbacher et al. 2000; Pisut & could affect development, resulting in a reduction in adult size Pawlik 2002; Wood et al. 2002; Brizzi & Corti 2007; Hutchinson (Cohen 1985; Rowell-Rahier & Pasteels 1986; Dobler & Rowell- et al. 2007; Meredith et al. 2007; Hani fin et al. 2008; Fleury et al. Rahier 1994; Zalucki et al. 2001 ) and lower mating success 2008; Tschuch et al. 2008; Peters et al. 2009; Sheybani et al. (Andersson 1994 ). Therefore, animals with defences that would not 2009 ). Such chemicals can cause the predator to simply release require the costly replenishment of scent glands are expected to the prey but in some cases may even cause temporary paralysis or avoid using their secretions unless it is absolutely necessary. death (e.g. Carrel & Eisner 1984; Hagman et al. 2009; Hayes et al. Harvestmen (Arachnida, Opiliones) have defensive mecha- 2009 ). nisms such as fleeing, feigning death, pinching with chelicerae, pedipalps or leg spines and autotomizing legs ( Gnaspini & Hara 2007 ). They also possess a pair of scent glands that open in the lateral regions of the cephalothorax ( Gnaspini & Hara 2007 ). When * Correspondence: R. H. Willemart, Escola de Artes, Ciências e Humanidades, disturbed, harvestmen may release water from their mouth that Universidade de São Paulo, Rua Arlindo Béttio,1000, Ermelino Matarazzo 03828-000, São Paulo, SP, Brazil. eventually mixes with the scent gland secretions (see Eisner et al. E-mail address: [email protected] (R.H. Willemart). 2004 ). This increases the amount of liquid used as a repellent. Not 0003-3472/$38.00 Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi: 10.1016/j.anbehav.2010.09.023 128 E.S. Souza, R.H. Willemart / Animal Behaviour 81 (2011) 127 e133 only are harvestmen chemically defended, but they also have Experiments a hard integument that could be protective just like the carapaces that have convergently evolved among mammals (armadillos and We ran the trials of experiments 1 e4, from April to October pangolins; Nowak 1999 ), reptiles (turtles; Pritchard 1979 ) and 2009, under dim light, at room temperature (20 e25 C). Data from other arthropods (beetles and mites; Sanders & Norton 2004; experiments 2 e4 were collected between 1800 and 2400 hours. Majerus et al. 2007 ). Although several harvestmen species, such Experiment 5 was conducted in March 2010, at room temperature, as cyphophthalmids and laniatorids, and some Dyspnoi ( van der normal light, and between 2200 and 0200 hours. We used a Sony Hammen 1985; Shultz & Pinto-da-Rocha 2007 ) have a strong Handycam DCR-TRV361 ‘nightshot ’. For experiments 1 e4, the cuticle, it is unknown whether this cuticle offers protection against proportion of subadults (last stage before adulthood) and adults predators. and of males and females were equally distributed among treat- In the present study, we conducted a detailed behavioural ments. Only three adult males of E. cyclothorax were used. Adult analysis of the interaction between the harvestman Discocyrtus females are usually slightly larger than subadults. Adult males have invalidus (Opiliones, Gonyleptidae) and the syntopic generalist longer legs. Except for this criterion, the animals were randomly spider Enoploctenus cyclothorax (Araneae, Ctenidae). We first tested distributed among treatments. whether the spider preyed upon the harvestmen, then explored the details of their behaviour. Next, we experimentally tested whether Experiment 1 the release of small amounts of scent gland secretions, invisible to To verify whether E. cyclothorax prey on D. invalidus , one indi- the human eye, could play a role in protecting the harvestmen. We vidual of each species was left for 5 days in the same arena then experimentally tested the effect of the scent gland secretions (20 cm diameter  8 cm height) ( N ¼ 16). As a control, another 16 per se on the spider, and finally tested the possible role of the spiders were left with crickets for 5 days. All 32 spiders were heavily built body of the harvestman in defence. Taken together, we starved for 25 e30 days before day 1 of the experiment to ensure present a case in which, in accordance with the notion of the that they would be hungry and therefore motivated to eat. We economical use of costly resources such as gland secretions (see e.g. monitored all containers for predation daily between 1200 and Nolen & Johnson 2001; Radwan et al. 2006 ), the scent gland 1300 hours and then compared the predation rate between control secretions are not used to repel a predator even after an attack: and experimental treatments after the fifth day. D. invalidus instead seems to rely on its strong cuticle for protection against the much larger E. cyclothorax . Experiment 2 In experiment 2, we were interested in observing the details of the predatory interaction. Thirty two spiders were exposed to METHODS either a harvestman or a cricket ( N ¼ 16). All 32 spiders were starved for 25 e30 days before day 1 of the experiment. The circular Species Studied arena used for the tests (20 cm diameter  8 cm height) had humid soil on the bottom. The spider was introduced into this arena 8 h The harvestman Discocyrtus invalidus (Piza 1938) (Laniatores, before the trial to minimize stress, and the harvestman was intro- Gonyleptidae) is found in forests, where it hides under logs during duced in a vial as far as possible from the spider, allowed to accli- the day and wanders on tree trunks, on the ground or on bushes at mate for 2 min and then released. By digitally recording the trials, night. The scent gland secretions of these animals are composed we recorded behaviours related to the approach between the two mainly of highly volatile 2,3-dimetil-1,4-benzoquinone ( Hara et al. animals, the physical interaction and subsequent 10 s, which was 2005 ). Their natural predators are not known. suf ficient to detect whether the spider would start eating the prey. The spider Enoploctenus cyclothorax (Bertkau 1880) (Ctenidae) is From the videos, we created and quanti fied behavioural categories a large spider that hides beneath palm sheats and in natural holes and compared their occurrences across treatments. in forests during the day and sits and waits for prey at night. They feed on a variety of arthropods, such as large roaches and crickets, Experiment 3 other spiders (including conspeci fics) and isopods ( Willemart & In experiment 3, we tested the hypothesis that harvestmen can Kaneto 2004 ). Prior to this study, it was unknown whether secrete small amounts of defensive secretions, invisible to the E. cyclothorax preys on D. invalidus . human eye. This would form a chemical shield that would explain why E.