Diptera: Ceratopogonidae) F Arné Verhoef1*, Gert J Venter2 and Christopher W Weldon1
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Verhoef et al. Parasites & Vectors 2014, 7:384 http://www.parasitesandvectors.com/content/7/1/384 RESEARCH Open Access Thermal limits of two biting midges, Culicoides imicola Kieffer and C. bolitinos Meiswinkel (Diptera: Ceratopogonidae) F Arné Verhoef1*, Gert J Venter2 and Christopher W Weldon1 Abstract Background: Culicoides imicola Kieffer and Culicoides bolitinos Meiswinkel (Diptera: Ceratopogonidae) are both of veterinary importance, being vectors of Schmallenberg, bluetongue and African horse sickness (AHS) viruses. Within South Africa, these Culicoides species show a marked difference in their abundances according to altitude, with C. imicola highly abundant in lower altitudes, but being replaced as the dominant species by C. bolitinos in cooler, high-altitude regions. Methods: The thermal physiology of field collected adults of each species was determined to evaluate whether it could account for differences in their distribution and abundance. Critical thermal maxima (CTmax) and minima (CTmin), as well as upper and lower lethal temperatures (ULT and LLT) were assessed after acclimation temperatures of 19°C, 24°C and 29°C. Critical thermal limits were determined using an ecologically relevant rate of temperature change of 0.06°C.min−1. Results: Significant differences in CTmin and CTmax were found between acclimation temperatures for C. imicola and C. bolitinos. In C. bolitinos, the LLT of individuals acclimated at 24°C was significantly improved (LLT50 = −6.01°C) compared with those acclimated at the other temperatures (LLT50 = −4°C). Acclimation had a weak (difference in LLT50 of only 1°C) but significant effect on the LLT of C. imicola. When CTmin,CTmax, LLT and ULT were superimposed on daily maximum and minimum temperature records from locations where each tested Culicoides species is dominant, it was found that temperatures frequently declined below the CTmin and LLT of C. imicola at the location where C. bolitinos was dominant. Conclusions: The distribution and abundance of C. imicola is likely directly constrained by their relatively poor tolerance of lower temperatures. Results for C. bolitinos suggest that the adult phase is hardy, and it is hypothesised that the thermal biology of other life stages could determine their range. Keywords: Bluetongue, African horse sickness, Orbiviruses, Phenotypic plasticity, Thermal biology, Tolerance limits Background all belonging within the genus Orbivirus (Reoviridae), Biting midges in the genus Culicoides (Diptera: Ceratopo- cause diseases of such international significance in live- gonidae) are incredibly abundant, small flies (ranging from stock that they have been classified as notifiable to the 1–4 mm). Female biting midges feed on vertebrate blood, World Organisation for Animal Health (OIE). The rapid and in so doing, act as vectors of up to 66 viruses that spread of BTV in Europe, outbreaks of AHSV in Spain affect animals including humans [1,2]. At least three of since 1987 [3], and recent outbreaks of a novel orthobu- these viruses, namely bluetongue (BTV), epizootic haemor- nyavirus, Schmallenberg virus [4,5], has demonstrated the rhagic disease, and African horse sickness (AHSV) viruses, devastating effect of these viruses on naïve livestock popu- lations. Due to the emergence and over-wintering poten- * Correspondence: [email protected] tial of these viruses in Europe, whereby novel European 1Flies of Economic Significance Research Group, Department of Zoology and Entomology, University of Pretoria, Private Bag X20, Hatfield 0028, South Culicoides species have been incriminated as the vector Africa [6], there is an increased interest in the vector competence Full list of author information is available at the end of the article © 2014 Verhoef et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Verhoef et al. Parasites & Vectors 2014, 7:384 Page 2 of 9 http://www.parasitesandvectors.com/content/7/1/384 and ecology of Culicoides species [7]. Similarly, in sub- marked differences in abundance, seemingly according to Saharan Africa where AHS is endemic and widespread, regional climate. It is likely, therefore, that thermal physi- long term economic losses have resulted from export em- ology may be a determining factor in their distribution and bargoes on horses as well as direct loss of livestock [8]. abundance. Most of the physiological processes of insects The population dynamics of Culicoides species are mark- are temperature-dependent [24] and thermal limits are sig- edly influenced by environmental conditions [9]. On ac- nificant for fitness because they determine the ability of an count of these factors, there is a need to understand the organism to remain active and survive during extreme con- biotic and abiotic drivers of Culicoides distribution and ditions [25]. Extending from this tenet, thermal limits form abundance. a fundamental part of mechanistic niche modelling [26] Two Culicoides species have been implicated in the that aid in the generation of distribution maps and risk transmission of BTV and AHSV in southern Africa, management strategies. These distribution models are in- namely C. imicola and C. bolitinos. Culicoides (Avaritia) creasingly important with a changing climate, in order to imicola Kieffer is one of the most widely distributed mem- assist in predicting future outbreaks or range expansions bers of Culicoides in the world, extending over the African or to assess local changes in dominance of species [27]. continent into southern Europe and eastwards to south Some work has been done on the role of temperature on China [10,11]. Based on its wide geographical distribution the geographical distribution of Culicoides species [28], in- and host preference for larger mammals, as indicated by cluding C. imicola [29-32], mainly through the use of cli- the high numbers collected near livestock, C. imicola is mate envelope models. The effect of temperature on BTV considered the principal vector of AHSV, equine encepha- replication within both C. imicola and C. bolitinos has also losis virus and BTV in South Africa [12,13] and BTV in been investigated [33,34]. However, the tolerance of these southern Europe [14,15]. Often found in great densities, species to temperature extremes has never been estab- with single trap captures able to reach 106 individuals lished, and spatial models are coarse [23]. Knowledge of [16], they may make up 99% of all Culicoides species col- the thermal biology of these species may aid in under- lected near livestock in areas where they are abundant standing their population dynamics, particularly their dis- [10,17]. The larvae develop in moist soils rich in organic tribution and abundance, and may even provide insight matter, often in full sun. In years with above-average rain- into the epidemiology of the arboviruses they transmit. fall, a 200-fold increase in abundance may be observed This study determined the thermal limits of adult C. [16] due to increased availability of breeding sites. In con- imicola and C. bolitinos. Phenotypic plasticity in measured trast, C. bolitinos Meiswinkel occurs in low numbers thermal tolerance traits was also determined. Results were across sub-Saharan Africa, but can become the dominant related to the temperature conditions of locations within species in cooler, high altitude regions [16,18] such as the the known geographical distribution of these two livestock Free State province of South Africa, and Lesotho. In South associated species. Africa, Culicoides bolitinos was also shown to be abundant in the winter rainfall region of the Western Cape province Methods [19,20], and the dominant Culicoides species, in the ab- Collections and study animals sence of C. imicola, in the sandy dunefields adjoining Port Rearing Culicoides in the laboratory is extremely difficult Elizabeth in the Eastern Cape Province [21]. The absence [10], and due to unsuccessful rearing attempts during pilot of C. imicola at Port Elizabeth in light trap collections studies, only the thermal limits of adult, field collected in- made at Struisbaai and Alexander Bay on the southern dividuals were investigated in this study. All midges were and western coastline was attributed to the sandiness of collected using Onderstepoort light traps during March, the soil [22]. Described in 1989 [11], C. bolitinos was iden- April and October, 2013. Trap catches of both species tified as a potential vector of AHSV as recently as 1998 are highly female biased, so all individuals tested using [16]. The larval cycle is completed in bovid dung (buffalo, the methods outlined below were female. All C. imicola domestic cattle and blue wildebeest) [11]. The abundance were trapped at ARC-Onderstepoort Veterinary Institute, of C. bolitinos is thus affected by the availability of suitable Gauteng, South Africa (ARC-OVI; 25° 39’ 2.58” S28°11’ dung, with the decomposition of dung potentially acting 8.58” E; 1219 m a.s.l.). The Onderstepoort area is relatively to incubate C. bolitinos larvae. frost-free with only a few days where the minimum Despite the role of Culicoides species as potential vec- temperature will fall below 0°C. Culicoides bolitinos were tors and their increased relevance to epidemiological re- trapped on Koeberg farm near the Clarens Valley, Free search [23] little is known about their basic physiology. State, South Africa (28° 0’ 0” S, 28° 31’ 0.12” E, 1631 m a.s. This is most likely due to their small size, nocturnal be- l.). Clarens regularly experiences minimum daily tempera- haviour as well as ease of injury during handling, which tures below freezing, with occasional snow in winter. Both has discouraged or hampered experimental manipulation species were transported in cool boxes to the Hatfield [10]. As noted above, C.