To: WormMail mailing list. WormMail.2015-01-29. Hypobiosis in sheep worms in Australia? plus more…
In this issue …
Main course (worms)
Hypobiosis in sheep worms in Australia? – R B Besier
Monepantel resistant Haemonchus on sheep farms in Uruguay – first report
Do hunting dogs come onto your property? (hydatids)
Dessert, coffee, cognac (sans worms)
Richie Benaud did not Lamb alone this Australia Day
Hypobiosis in sheep worms in Australia – is it present and is it a problem ?
– Brown Besier, Department of Agriculture and Food WA (DAFWA), Albany (Jan. 2015)
“Hypobiosis in larval nematodes has been recognised as a potential feature of some ruminant worm life cycles for many years, but there has been little discussion of whether it occurs as a routine survival mechanism for sheep worm populations in Australia. However, hypobiosis (or “developmental arrest”, or “larval inhibition”) may have implications for the effectiveness of sustainable control programs, and could be important for the development of anthelmintic resistance.
Hypobiosis is common outside Australia
As classically described, hypobiosis is a characteristic of worm strains or populations that have evolved in particular environments, where the ability to survive during prolonged periods of hostile conditions for the free-living stages is essential to ensure the continuation of the population. In this form of the nematode life cycle, at times of the year time when conditions in the external environment are becoming increasingly adverse for larval survival on pasture, some of the ingested infective larvae develop only to the fourth larval stage, and enter a dormant state rather than continuing development to the fifth larval and adult stages. Sometime later – usually months – when environmental conditions are more favourable for worm eggs and larvae, the development of inhibited larvae to the later stages re-commences.
Hypobiosis has been described in a fairly wide range of nematodes of animals and man, but for livestock has been most studied in Haemonchus contortus in sheep and Ostertagia ostertagi in cattle. The latter is seen as the condition “Ostertagiosis Type 2”, where severe scouring results from massive inflammation caused by the mass emergence of inhibited larvae from the abomasal wall. This was identified in the late 1960s as a sporadically-occurring disease syndrome, at times causing large-scale cattle deaths because the anthelmintics available prior to the late 1970s did not kill the fourth larval stage. (This condition is no longer common, although the sharp decline had not been well explained – not all cattle farmers routinely use effective anthelmintics.)
Hypobiosis has also been reported in Teladorsagia (Ostertagia) circumcincta in sheep in the northern hemisphere. In Haemonchus, hypobiosis has been reported as a routine occurrence mostly from climates with periods of either extreme cold (Canada, N. USA, UK, Europe) or extreme dryness and heat (desert environments – sub-Saharan Africa, Middle East). It appears to be a hard-wired genetic mechanism, i.e., it can potentially occur every year, and is not turned on or off in relation to particular environmental conditions in any one year.
However, there can be considerable variation in the extent of its expression, as exemplified by the sporadic occurrence of Ostertagiosis Type 2 between years and on individual properties in Australia. This could be explained by differences in larval pick-up prior to the period of developmental arrest (due to pasture management and the local environment), and factors related to anthelmintic use such as the time of application and effectiveness against the inhibited larval stage. It also appears that there are strains with a greater or lesser propensity to “go hypobiotic”, certainly between environments and perhaps within regions. This is just one of many puzzles regarding hypobiosis, such as the mechanisms to trigger its onset and then the re-development of larvae: how do they “know” when to “wake up” ? – environmental cues via hormonal routes in the animal? – changes in immunological situation due to new L3 intake ? A recent study in bovine lungworm identified differences in gene expression between hypobiotic and non-inhibited strains, but no mechanistic link was postulated.
Do we see it here ?
In Australia, there has been little overt indication of whether or not hypobiosis is a routine occurrence in a particular environment. This is presumably because modern drenches are highly effective against L4s (until anthelmintic resistance occurs) and these are usually removed before they can contribute to pasture contamination and hence influence worm populations. This may change once anthelmintic resistance affects previously highly-effective anthelmintics, although as drench failure takes time to become apparent, any effect on parasite epidemiology would also take time to be noticed.
Hypobiosis in Haemonchus contortus has long been considered a routine but largely invisible phenomenon in summer rainfall regions (especially the New England region, northern NSW), presumably due to long periods of relatively cold weather, although whether hypobiosis would be essential for population survival is debateable when compared to climates with really frigid winters. Recently, Leo le Jambre (formerly of CSIRO) has commented that hypobiosis appears to be less marked than in the early 1970s, when large numbers of inhibited L4s were routinely recovered in total worm counts. Presuming that this is a real trend, is this due to sheep management, anthelmintic effects, or environment ? (climate change, anyone ?).
I don’t know about Queensland, where dry conditions may have encouraged H.contortus populations to evolve towards hypobiosis, although this would need to be where a prolonged drought period was routine in most years as part of the normal climate. In cool temperate climates (winter rainfall regions in Australia), there is less need for H.contortus to use hypobiosis to survive: my own thesis was partly on cold-temperature tolerance in Haemonchus, and it was evident that adaptation had occurred in that the eggs from cold-winter strains could develop at up to 2 C colder than those from the tropics. The conclusion was that, in an evolutionary context, hypobiosis would only be necessary for population continuance when winters were so cold that development on pasture ceased for a prolonged period, rather than an interruption of only a few weeks, as occurs in most of southern Australia.
In winter rainfall regions in Australia, presumably the widely-used “summer drenching” program would remove inhibited worms, provided anthelmintic resistance was not severe. However, there are recent indications that Teladorsagia, at least, employs hypobiosis to survive over the hot dry WA summers, to emerge in mid-autumn once milder conditions occur. This was seen in work by Rob Woodgate (formerly DAFWA, now CSU Wagga Wagga) that led to the current “summer-autumn drench” program in WA, by which drenching adult sheep is delayed until March or April, to provide refugia for non-resistant worms. Although worm egg counts were almost always low in early summer, they had often increased to significant levels by mid-autumn. This could not be explained by over-summer pick up or faecal concentration, although the variation in occurrence between properties may be explained by differences in larval exposure in the late spring period when L3s would start to become seasonally inhibited ahead of a long period of no egg development on pasture.
Does it matter ?
There are two main potential issues of consequence if indeed hypobiosis does occur routinely in some environments.
– Sustainable worm control programs. These are generally based on the refugia concept for populations of worms not recently exposed to drenches, and in some winter rainfall regions insufficient refugia is provided by over-summering larvae. The general response is to leave some sheep untreated in summer, whether as a “targeted treatment” strategy (avoiding drenching of a proportion of the best-condition sheep) or in WA, the “summer-autumn drench” program. If worm egg counts sharply increase in autumn as inhibited larvae become adult worms, recommendations will need to allow for potential increases in pasture contamination, through additional monitoring or treatments.
– Drench resistance development. It has long been suspected that the presence of inhibited L4s may have assisted in the development of anthelmintic resistance. The L4 stage is harder to kill than adult worms, as shown by experimental data during anthelmintic development (assumed to be due to lower metabolic rate – presumably lowest for inhibited larvae – or for some species, in tissues with less blood supply than at the gut surface). For large populations of these, there will be a greater chance that some individuals would receive a sub-lethal anthelmintic dose. If this occurred when drenches were given for a strategic effect, typically ahead of periods when pasture development is minimal, these surviving (resistant) worms would have a survival advantage once the L4s reached the egg-laying adult stage.
It is intriguing to speculate that the early detection of ivermectin resistance in Teladorsagia in WA (4 years after release) may in part be related to this effect in invisible and unsuspected hypobiotic worms. Of more immediate concern, we know that many sheep owners routinely used anthelmintics that are not fully effective against adult worms – what would this mean for worms we can’t detect in resistance tests, but are even more resistant to drenches ?
Plenty of puzzles
Apart from the fundamental queries over the cues that trigger the commencement and end of hypobiosis, there are many other unanswered questions – presuming that it does indeed occur more commonly than we suspect.
– Where does it occur – only or mostly in environments where there is seasonally poor survival of the free-living stages ?
– What ages of sheep are involved, or can all be affected similarly ?
– Why is there apparent variation between seasons and properties ? – reasons and extent.
– When does pick-up occur for hypobiotic-prone larvae, and when do they re-emerge ?
– Which species are affected ?
– How should we detect and manage this ? – if it is really of consequence.
Of interest, if there are real differences between the occurrence of hypobiosis in sheep worms in response to different environments around Australia, this must have developed (or been lost if initially present) in only 200 years or so, which is very swift in evolutionary terms.”
First report of monepantel Haemonchus contortus resistance on sheep farms in Uruguay
Parasit Vectors. 2014 Dec 17;7(1):598. [Epub ahead of print]
First report of monepantel Haemonchus contortus resistance on sheep farms in Uruguay.
http://www.ncbi.nlm.nih.gov/pubmed/25515711 (Thanks John K).
Do hunting dogs come onto your property?
This from SheepConnect Tasmania:
“T. Eliot, top bard, notes putrid tang emanating, is sad. I’d assign it a name: gnat dirt upset on drab pot toilet”.
I first came across this while reading a book by Alexander McCall Smith (“Sunshine on Scotland Street” (p148 hardcover edition that I am reading)).
Richie Benaud did not Lamb alone this Australia Day
The characters (for the benefit of overseas readers): http://en.wikipedia.org/wiki/Richie_Benaud ; http://en.wikipedia.org/wiki/James_Cook ; http://en.wikipedia.org/wiki/Ned_Kelly (with gluten intolerance (disputed by Burke and Wills)); http://en.wikipedia.org/wiki/The_Twelfth_Man (not invited, due to parodies of Bernaud); http://en.wikipedia.org/wiki/Donald_Bradman (no answer); http://en.wikipedia.org/wiki/Ita_Buttrose (in limo, thinking ‘lamingtons’); http://en.wikipedia.org/wiki/Burke_and_Wills_expedition (in extremis) ; http://en.wikipedia.org/wiki/Sam_Kekovich (on jet ski); http://en.wikipedia.org/wiki/Lamb_chop .