Non-lethal elephant population control methods : Summary of the first workshop of the Elephant Specialist Advisory Group of South Africa

Within South Africa, private ownership of wild animals is permitted (Blackmore & Trouwborst 2018). Coupled with an improved ability to capture, transport, contain and manage large mammals, this has driven the introduction or reintroduction of elephants onto privately owned land: more than 800 elephants were translocated to existing or newly established state or privately owned fenced reserves between 1979 and 2001 as part of the efforts to reduce elephant numbers in Kruger National Park (Carruthers et al. 2008; Slotow et al. 2005). At present more than 21 000 elephants are kept on 17 state-owned, (partially) fenced reserves, with approximately 7080 elephants held on privately or community-owned fenced reserves (Pretorius, Garaï & Bates 2018).


Introduction
Within South Africa, private ownership of wild animals is permitted (Blackmore & Trouwborst 2018).Coupled with an improved ability to capture, transport, contain and manage large mammals, this has driven the introduction or reintroduction of elephants onto privately owned land: more than 800 elephants were translocated to existing or newly established state or privately owned fenced reserves between 1979 and 2001 as part of the efforts to reduce elephant numbers in Kruger National Park (Carruthers et al. 2008;Slotow et al. 2005).At present more than 21 000 elephants are kept on 17 state-owned, (partially) fenced reserves, with approximately 7080 elephants held on privately or community-owned fenced reserves (Pretorius, Garaï & Bates 2018).
Fenced wildlife reserves can be vulnerable to rapid or steep increases in elephant numbers (Mackey et al. 2006;Van Aarde et al. 2008).Management interventions are therefore often necessary to control or curb population increases, so that numbers remain within limits deemed acceptable by managers.Culling or translocation have traditionally been employed to immediately reduce elephant numbers, but these can evoke significant public criticism and/or may have significant impacts on the well-being of the remaining elephants (Dickson & Adams 2009;Lötter et al. 2008;Slotow, Whyte & Hofmeyr 2008;Van Aarde, Whyte & Pimm 1999).As an alternative, non-lethal population control methods are increasingly being utilised, namely vasectomy, immunocontraception with porcine zona pellucida (PZP) vaccine or immunocastration with gonadotropin-releasing hormone (GnRH) vaccine.These innovative methods do not directly reduce elephant numbers but can be adopted to suppress population increases by reducing reproduction rates.However, the suitability and long-term effects of these techniques on elephant physiology and behaviour are not yet fully or widely understood.Moreover, the long-term consequences of the techniques, both for the individuals who are treated and the wider social groups within the reserve, may be difficult to anticipate.Consequently, undue reliance is placed on the personal opinion and/or operational experience of individual elephant scientists, veterinarians and managers, and there appears to be considerable confusion about the function and utility of each method.There is a need, therefore, to document both scientific data and field experience, so that the collated information may direct further scientific study and form the foundation of appropriate future policy.
To this end, the Elephant Specialist Advisory Group of South Africa (ESAG) organised a workshop, the objectives of which were threefold: • Firstly, to collate the best available information on the three non-lethal population control methods, summarising both the positive and negative aspects of each and defining gaps in our knowledge so that future research efforts can be suitably targeted.
Management interventions are necessary to control elephant numbers within fenced wildlife reserves in South Africa.Use of non-lethal control methods is increasing, but information about their suitability and effects are not widely available.Three such methods are currently available: immunocontraception with porcine zona pellucida vaccine, vasectomy and gonadotropin-releasing hormone vaccine.
Here we consolidate what we know about these methods, using published sources and material shared at a workshop held in South Africa in 2016, in order to provide up-to-date information for future policy decisions concerning the use of these methods in South Africa and elsewhere.
• Secondly, to determine how owners, managers and state authorities can be best supported to use this information to make appropriate, evidence-based decisions about which non-lethal control methods they could and should employ.• And thirdly, to provide the collated information as a resource for inclusion into the National Norms and Standards for the Management of Elephants in South Africa (N&S) (Government Gazette No. 30833, 29 February 2008).
All elephants within South Africa -whether owned privately or by the state -are subject to the stipulations laid out in the N&S.However, the current document provides little guidance as to when and how to appropriately use the nonlethal methods now available.We aim to provide clear and objective guidelines on the use of these methods.Other management tools aimed at immediate population reduction (such as culling or translocation) were not addressed at the workshop.These have previously been well described (Balfour et al. 2007;Grobler et al. 2008;Slotow et al. 2008).

Programme
To achieve the primary objective of the workshop, leading researchers in each of the non-lethal techniques were invited to present their latest data, with the following presentations: 'PZP immunocontraception and lack of behavioural responses' (Delsink 2016); 'Use and effects of GnRH vaccine on bulls' (Lueders 2016); and 'Effects of vasectomy on behaviour of bulls' (Zitzer 2016).These were followed by a final presentation, 'Anecdotes on possible behavioural implications of the three population control methods' (Pretorius 2016), introducing questions raised from a literature search and oral reports.This final presentation was intended to stimulate the subsequent discussions.
After the presentations, Professor Rob Slotow facilitated a discussion session, aimed at meeting the second and third objectives.All delegates were encouraged to consider two key questions: (1) what do you want to know about non-lethal control methods and ( 2) what is your primary motivation?Motivation is important because individual aims influence the perceived advantages and disadvantages of each method, and a method can only be deemed appropriate if its intended outcome is clear (e.g.aiming to preserve the habitat whilst avoiding lethal control).Delegates initially discussed these questions in small groups for 30 min, with each group subsequently presenting their thoughts to the entire workshop, with time for questions and comments during and after each group's summary.The facilitator made notes during each summary and discussion using a flip chart, and the entire workshop was recorded using a Sony Dictaphone.The information from the presentations, published material and discussions were collated in Table 1, with recommendations for the use of each method summarised in Table 2.

Results and discussion
Objective 1: Collate available scientific information summarising each method and define the remaining gaps in our evidence-based knowledge Porcine zona pellucida is an immunocontraceptive vaccine that is delivered by intramuscular injection to female elephants, usually via remote darting.The non-hormonal vaccine works to prevent pregnancy by stimulating antibodies against proteins vital for fertilisation (Kirkpatrick et al. 2012).It does not affect the hormone balance of the elephant (Delsink & Kirkpatrick 2012).Studies have been measuring the efficiency and effects of PZP on elephant families and populations since 2000 (Delsink & Kirkpatrick 2012), and success rates of at least 95% have been reported.The effects have been shown to be reversible over the current 16-year study period (Delsink 2016), with no side effects on pathology, histology or elephant behaviour so far having been noted (Delsink & Kirkpatrick 2012;Delsink et al. 2013).Based on knowledge derived from this ongoing study (Bertschinger et al., submitted), this method can be considered an effective and safe way to limit elephant population growth, when it is part of a long-term, predefined management plan.-Treatment of all males is necessary as soon as they reach sexual maturity, if zero population increases are to be maintained.

Is it reversible at any time?
Medium-term studies show reversibility.
No studies yet available on reversibility after more than a decade of treatment.
Veterinary advances could make reversibility plausible in the future, but it is unlikely.Four males stopped treatment after 3 years.
One has reversed and come into musth and has normal semen.No pathological studies of treated individuals yet conducted.
Viable sperm production decreases and may cease totally after a year.
There may be variation caused by age and time frame of administration, but little data is available.
Feminisation may occur if treatment is carried out prepubertally.Growth and size of treated captive males appears normal.
It will affect size of the penis and other reproductive organs.
It is unclear how old a male must be before treatment to avoid damage or alteration of sexual organs.No change evident.
-No change evident yet.
Long-term effects currently unknown. -Unknown.
What are the long-term effects of the vaccine or procedure?None evident from the longest running study (established in 2000 and ongoing).
Lifetime effects currently unknown.None evident from the only running study (established in 2009 and ongoing).
Long-term effects currently unknown.
Possible permanent infertility. Unknown.

Source:
Collated from references cited in text, including the oral presentations made at the workshop and the subsequent discussion sessions

TABLE 2:
Scenarios for the most appropriate use of the non-lethal fertility control methods.

Notes
Reduced population expansion rate (some births allowed with extended interbirth intervals).

Porcine zona pellucida
Small population where all adult females individually known.Rotate use between units every few years to allow some births.
--Large populations with distinct and separate cow-calf units.Large populations where females not individually identifiable.All adult females with at least one offspring are treated, or percentage of females are treated based on population demographic projection and reserve specific objectives.
No breeding at all.

Porcine zona pellucida
Small or large populations.
Treat all females continuously.
Lifelong treatment.
Preventing all breeding on a permanent basis is not recommended as this could change elephant behaviour with unknown consequences.

Vasectomy
Very small captive populations.
Vasectomise all currently sexually mature males in reserve and/or continue to vasectomise all maturing males if maintenance of zero birth rate is required.
Populations with a large number of sexually mature bulls and/or situations where breeding will be desired again in the future as this method is currently irreversible.It is not recommended to continue vasectomising in the medium to long term, as not allowing any breeding will change elephant behaviour with unknown consequences.
Wild populations where all sexually mature males are identifiable.
Short-term reduction in aggression.Gonadotropin-releasing hormone vaccine In captive setting with males showing androgen-related aggression.Short-term use only, or acceptance of possible 'feminisation' and physiological and behavioural changes with long-term use.
Use on young males that may be required for breeding in the future, as reversibility not guaranteed.
-In wild settings with only one or two males on reserve showing androgenrelated aggression.
Not appropriate as a contraceptive method in wild populations.

Source:
Collated from references cited in text, including the oral presentations made at the workshop and the subsequent discussion sessions affecting testosterone production or musth cycling.The procedure has been performed on male elephants in several reserves across South Africa, but to date only one long-term (≥ 10 years) monitoring and research programme exists, at the Pongola Game Reserve.Based on observations at this site, vasectomies do not appear to have any behavioural consequences for treated males (Zitzer & Boult, in press).However, the effects on testosterone levels in younger males are not yet known and continuation of behavioural studies is required to identify any longer-term implications.This method of population control has not been tested for reversibility (D.Hendrickson [Colorado State University] pers.comm., 24 August 2017).
GnRH is a vaccine that is commercially available under prescription in South Africa, being currently registered for use in pigs.It neutralises endogenous GnRH and therefore reduces production of all androgen hormones, including testosterone (Bertschinger & Scott Sills 2013).It has been studied in captive elephants, where males show a significant reduction of testosterone after the second booster (or third vaccination) (Lueders et al. 2014) and significant decrease of testicular and accessory sex gland sizes (Lueders et al. 2017).
Reports from captive studies suggest it can reduce musth-(testosterone-) related aggression (Bertschinger & Scott Sills 2013), but further studies specifically measuring changes in musth aggression are required.Furthermore, its effects on wild (non-captive) elephants are not known.It is unclear if this method is reversible, or what duration of treatment is optimal if reversal may subsequently be required, but feminisation of males has occurred in those treated prepubertally (Lueders et al. 2014(Lueders et al. , 2017)).Moreover, by altering musth and aggressive behaviour, this method could have direct impacts on the male dominance hierarchy and male behaviour (Doughty et al. 2014), although, again, detailed behavioural studies are lacking.
The information gained from the workshop presentations, discussions and published data were collated and summarised in Table 1.It was apparent from the workshop discussions that there were some key questions and concerns common to all three methods, specifically: (1) How is each method applied and what is the dosage?(2) What is the likelihood of success with each method?(3) Do the methods have any effects on elephant behaviour?(4) What are the (unintended) consequences of each method, in the short and long term?And (5) is the method appropriate for large populations?Table 1 at least partly answers most of these questions and clearly shows where more information is required.
Objective 2: Determine how owners, managers and state authorities can be best supported to use this information When discussing the three methods, broader issues were also examined, principally concerning the benefits of each, in both the short and long term, to the environment and to the elephant population; their effects on the welfare of the elephant population; the economic implications of the control methods over both the short and long term; and how to best maintain the integrity of the whole ecological system, including maintaining or mimicking 'natural' gene flow.It was noted that all of these issues must be considered by individual properties before a method is adopted, and these are considered in Table 2, which summarises when each method might be most appropriately employed, based on current knowledge.
When asking the delegates to consider what they wanted to know about the methods, and what their motivation was, the facilitator directly asked participants how they could be helped to use the information that was being shared.
One overwhelmingly popular suggestion was to develop a toolbox that could be used as a checklist by managers and state authorities to help them make appropriate decisions that take account of both the motivation (desired outcome) and available knowledge of the methods.The Trustees of ESAG agreed to take the lead in the process, and the toolbox will be based on the information set out in Tables 1 and 2.

Objective 3: Inform revisions of the relevant sections of the National Norms and Standards for the Management of Elephants in South Africa
A short summary of the relevant points discussed, along with expanded copies of Tables 1 and 2 and all supporting documentation, were submitted to the DEA for inclusion in the N&S revision process.

Conclusion
Following consideration of the information presented and the workshop discussions, the following recommendations are made: (1) PZP is the best studied and understood population control method.It has been shown to work effectively and studies so far indicate that it is reversible after medium-term use.We conclude it is the best method currently available to control increases in free-ranging elephant populations.
(2) Vasectomy is an effective yet invasive and currently non-reversible method and therefore should only be adopted for use in free-ranging elephant populations after careful consideration.
(3) GnRH vaccine should only be used on captive elephants, and only to reduce androgen-related aggression.Until further controlled scientific studies have been conducted, utilisation for reducing androgen-related aggression in free-ranging males should remain cautious and be temporary, following due consideration of all the potential side effects.Behavioural problems that are not related to androgens cannot be effectively treated with GnRH.The use of GnRH as a contraceptive should be discouraged and/or halted until controlled studies have been conducted.

TABLE 1 :
Summary of current knowledge about the available non-lethal fertility control methods.

TABLE 1 (
Continues...):Summary of current knowledge about the available non-lethal fertility control methods.