Does toxic defence in Nycticebus spp. relate to ectoparasites? The lethal effects of slow loris venom on arthropods
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.
References (29)
Test systems for tick repellents
Int. J. Med. Microbiol. Suppl.
(2004)- et al.
Venomous mammals: a review
Toxicon
(2012) - et al.
Functional associations of similar MHC alleles and shared parasite species in two sympatric lemurs
Infect. Genet. Evol.
(2010) - et al.
Gastrointestinal- and ecto- parasites in wild Javan slow loris (Nycticebus javanicus)
- et al.
Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus
Am. J. Primatol.
(2012) Toxins and toothcombs: potential allospecific chemical defenses in Nycticebus and Perodicticus
Scutate Ticks, or Ixodidae, of Indonesia
(1950)- et al.
Anointing chemicals and ectoparasites: effects of benzoquinones from millipedes on the lone star tick, Amblyomma americanum
J. Chem. Ecol.
(2005) - et al.
Tick sweep: modification of the tick drag-flag method for sampling nymphs of the deer tick (Acari: Ixodidae)
J. Med. Entomol.
(1992) - et al.
A novel test system for detection of tick repellents
Entomologia Exp. Appl.
(1999)
Melyrid beetles (Choresine): a putative source for the batrachotoxin alkaloids found in poison-dart frogs and toxic passerine birds
Proc. Natl. Acad. Sci. U S A
Repellent efficacy of formic acid and the abdominal secretion of carpenter ants (Hymenoptera: Formicidae) against Amblyomma ticks (Acari: Ixodidae)
J. Med. Entomology
Talking Defensively, a Dual Use for the Brachial Gland Exudate of Slow and Pygmy Lorises
“Venom” of the slow loris: sequence similarity of prosimian skin gland protein and Fel d 1 cat allergen
Naturwissenschaften
Cited by (15)
Ecological and Evolutionary Consequences of Parasite Avoidance
2018, Trends in Ecology and EvolutionCitation Excerpt :Fourth, animals can alter their niche to avoid parasites. For example, birds incorporate volatile-containing plant material into their nests to discourage parasites [19], slow lorises apply their own venom to their bodies to repel ectoparasites [20], and termites build partitions within their nests to separate corpses from the rest of the colony [21]. Not only do these avoidance strategies benefit the host, they can also benefit its offspring.
Functional genomics analysis reveals the evolutionary adaptation and demographic history of pygmy lorises
2022, Proceedings of the National Academy of Sciences of the United States of AmericaInfection avoidance behaviors across vertebrate taxa: Patterns, processes, and future directions
2022, Animal Behavior and ParasitismShrew's venom quickly causes circulation disorder, analgesia and hypokinesia
2022, Cellular and Molecular Life Sciences