Elsevier

Toxicon

Volume 95, 1 March 2015, Pages 1-5
Toxicon

Does toxic defence in Nycticebus spp. relate to ectoparasites? The lethal effects of slow loris venom on arthropods

https://doi.org/10.1016/j.toxicon.2014.12.005Get rights and content

Highlights

  • We conducted ectoparasite repellency tests on slow loris (Nycticebus spp.) venom.

  • Arthropods exposed to venom often were impaired or died as a result.

  • Spiders were especially susceptible to the venom, and 78% died after one hour.

  • Ectoparasites are known to transmit pathogens to hosts.

  • One function of topically anointed venom may be to repel potential ectoparasites.

Abstract

The venom produced by slow lorises (Nycticebus spp.) is toxic both intra- and inter-specifically. In this study we assessed the ecoparasite repellent properties of their venom. We tested venom from two Indonesian slow loris species: Nycticebus javanicus and Nycticebus coucang. Arthropods directly exposed to brachial gland secretions mixed with saliva from both species were immediately impaired or exhibited reduced activity (76%), and often died as a result (61%). We found no significant difference in the result of 60-min trials between N. coucang and N. javanicus [X2(1, n = 140) = 2.110, p = 0.3482]. We found evidence that the degree of lethality of the venom varies according to the arthropod taxa to which it is exposed. While most maggots (84%) were initially impaired from the venom after 10 min, maggots died after a 1 h trial 42% of the time. In contrast, at the end of 1 h trial, spiders died 78% of the time. For all arthropods, the average time to death from exposure was less than 25 min (M = 24.40, SD = 22.60). Ectoparasites including ticks, members of the arachnid order, are known to transmit pathogens to hosts and may be an intended target of the toxic secretions. Our results suggest that one function of slow loris venom is to repel parasites that affect their fitness, and that their topical anointing behaviour may be an adaptive response to ectoparasites.

Introduction

Few mammals are known to produce toxic secretions (Ligabue-Braun et al., 2012). The functions of mammal venom vary but include suppressing prey, anti-predator defence and intraspecific competition (Ligabue-Braun et al., 2012). Slow lorises (Nycticebus spp.) are unusual Southeast Asian primates; they are cryptic, nocturnal, and produce a toxic compound, which they administer topically or through their bite. Slow lorises are the only primates known to produce venom, and they do this by combining saliva with oil from a brachial gland in their mouth (Alterman, 1995), and licking their fur or biting the intended victim. Here we explore the adaptive significance of venom amongst Indonesian slow lorises in regard to its effects on invertebrates.

Nekaris et al. (2013) suggested that slow loris venom might function to repel or defend against predators, conspecifics, prey or ectoparasites in four competing, although not mutually exclusive, hypotheses. Little evidence exists to suggest that loris venom is used against prey, given that venom is not used to paralyze prey (Alterman, 1995) and the fact that lorises rapidly consume prey. Previous studies suggest that loris venom may serve as a defense against conspecifics, where bite wounds are a major cause of morbidity and mortality in captivity (Sutherland-Smith and Stalis, 2001). Further, predators may be the target of loris venom, where predators may be less likely to select prey that produces toxic compounds (Alterman, 1995, Nekaris et al., 2013). In support of this hypothesis, a female Nycticebus javanicus was witnessed anointing her offspring in venom (Nekaris et al., 2013), which could render a vulnerable infant unpalatable to potential predators.

In terms of the latter hypothesis, chemical toxicity is one feature that renders vertebrates as unsuitable hosts for ectoparasites (Weldon, 2010). Ectoparasites are important selective forces that negatively affect the fitness of their hosts (Weldon and Carroll, 2006), and they are common in the tropical Southeast Asian countries that slow lorises inhabit (Anastos, 1950). Ectoparasites are not commonly observed on both wild and captive slow lorises, and of the more than 300 wild lorises observed, representing all species, only two instances of infestation by ectoparasites have been observed (Nekaris et al., 2013, Streicher, 2004). It has been proposed that this is due to the chemicals produced by their saliva, brachial grand secretions, or a combination of the two.

We explored whether the secretions produced by slow lorises are lethal to ectoparasites by examining the physiological responses of arthropods to slow loris venom. We predicted that: a) arthropods will die more rapidly after direct exposure to slow loris secretions and b) arthropods will avoid moving to test areas that have been applied with slow loris secretions.

Section snippets

Study site

We tested the repellent effects of venom produced by adult wild Javan slow lorises (N. javanicus) in an agroforest study site in the district of Garut, West Java, Indonesia (S7°6′6 & E 107°46′5) and adult wild-born greater slow lorises (Nycticebus coucang), recently confiscated from the illegal wildlife trade in Sumatra, at Cikananga Wildlife Centre, Sukabumi District, West Java (S7°00′23.9 & E 108°33′3.9).

Sample collection and preparation

The research conducted complies with the relevant laws of Indonesia and the institutional

Direct application tests

We tested 121 subjects (Arachnida: n = 53; Siphonaptera: n = 8; Diptera: n = 35; Hymenoptera: n = 13; Lepidoptera: n = 12) in 93 venom application trials with 28 control trials. The average time to death for trials that resulted in death was 24.40 min (n = 50; SD = 22.60).

Tests using saliva or brachial oil only on fleas (n = 3), maggots (n = 3), and spiders (n = 10) did not have a significantly different outcome (α = 0.05) than the control [(X2(1,n = 16) = 1.27, p = 0.53]. These tests were

Discussion

We show here that the venom of slow lorises is toxic and often lethal to a variety of insect species. Consistent with previous findings (Alterman, 1995), we confirm that this is only the case when brachial grand secretion is combined with saliva. The degree of lethality of the venom is taxon-specific and varies according to the type of arthropod to which it is exposed. Venom was more lethal for spiders and ants than for maggots and caterpillars, suggesting its use as a deterrent against some

Acknowledgements

We thank RISTEK, BKSDA Bandung, Research Center for Biology, LIPI, KSDA Garut, and Cikananga Wildlife Centre for their support in this project. B.G. Fry, D Rustandi, A Nunur, A Zaelany, Y Nazmi, I Iryantoro, G Fuller, D Spaan, and A Palau Zango provided valuable insight and assistance. The Leverhulme Trust (RPG-084), Primate Society of Great Britain, Augsburg Zoo, Columbus Zoo, Cleveland Zoo and the Cleveland Zoo Society funded this project.

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