Wildlife Contraception

Purposes

  • Minimize crop damage (rat, various bird species)

    Control predators perceived to threaten livestock or game species (coyote)

    Reduce threat of exotic species to native wildlife (rabbit, fox, etc. in Australia)

    Decrease possibility of spread of disease to livestock or humans (skunk)

    Minimize damage to ecosystems by locally overabundant species (horse, deer, elephant)

    Manage zoo animal population sizes (big cats)

    *Avoid public relations repercussions of traditional culling methods

    *Lower expenses given PR needs

  • History

  • Since 1950s, when research proliferated on natural and synthetic steroids for human contraception

    Poorly organized - 1st international conference on wildlife contraception not until 1987

  • Methods

  • Separation of sexes: Useful only in captive animals; not even very effective there

    Surgical: Castration, vasectomy/tubal ligation, injecting of sclerosing agents

  • Irreversible

    Difficult in field; requires catching, performing surgery

    High attendant mortality

    Time consuming and expensive

  • Mechanical: Intra-uterine and vaginal devices, vas deferens plugs

  • Similar problems as surgical, but potentially reversible

    But also requires species-specific design and individual tailoring

  • Injectable: Chemicals, hormones, antigen preparations

  • May or may not require capture, but at minimum requires locating

    Reversible, but also has limited period of efficacy

    Persistence - especially of steroids - in tissues; passed on to 2° consumers (including humans)

  • Implantable: Mostly hormones

  • Similar to injectable, but longer acting

    Biobullet - silicone matrix rod impregnated with synthetic hormone (especially progestins or combinations), protected on entry with cellulose and calcium carbonate casing

  • Oral: Chemicals, hormones, antigen preparations

  • Similar to injectable and implantable, but does not require capture

    Frequent application of large quantities required

    May be consumed by non-target species

  • Viral: Live attenuated viruses genetically engineered to produce antigensÖ

  • Agents

  • Chemicals
  • In use since 1950s

    Often plant products, or agricultural chemicals

    Work by inhibiting gametogenesis, especially in males

    Least likely to be reversible

    Most likely to be toxic

    1959 - triethylene melamine (TEM) reduced testis size and spermatogenesis in starling, but extremely toxic

    1964 ñ Arasan ñ a fungicide/seed disinfectant ñ produced reversible inhibition of ovulation in pigeon

  • Hormones

  • In use since 1960s and 1970s (coyote, pigeon, red-winged blackbird, rat, much of modern work on white-tailed deer)

    Usually steroidal; progestins or combinations with estrogens (occasionally androgens)

    Natural or synthetic; latter generally longer-acting but less biodegradable

    MANY formulations; 25-30 different commercially available steroid contraceptives available by 1985

    Widely used because of high reversibility, low toxicity

    Broad biological action (hypothalamus, pituitary, gonads, other reproductive tissues)

    Resultant disturbance of natural behavior

    Poor biodegradability; readily available to 2° consumers

    Oral and injectable require large doses, especially of natural

    1963 ñ synthetic estrogen diethylstilbestrol (DES) used to control fertility in red fox, and many species since

    mid 1970s ñ oral progestins, especially melengestrol acetate (MGA; one of few approved for use in livestock)

  • Antigen preparationsÖ

  • Immunocontraception

  • Variety of antigens used
  • Sex hormones, especially GnRH (in both males and females)
  • Decreases FSH and LH secretion ñ atrophy of gonads - infertility

    Profound effects on behavior

    1980s - pig, rat, rabbit, horse

  • Spermatozoon (specifically sperm head) proteins

  • Sperm antibodies occasionally natural cause of human infertility

    Prevent sperm binding/penetrating ovum

    Late 1970s, early 1980s ñ being developed for use in red fox and rabbit in Australia

  • Zona pellucida (ZP) proteins

  • Solubilized porcine zona pellucida (PZP) vaccine focus of most work; proven effective in feral horses, burros

    Highly specific ZP antigens, e.g. mouse ZP3

    Prevent sperm binding/penetrating ZP, or prevent implantation if fertilization occurs

  • Placental components (e.g. riboflavin carrier protein)

  • Generally considered reversible

  • Lasts until no longer sufficient antibodies to interfere with biological activity of target antigen, usually a year or so

    Repeated treatment may result in irreversibility

  • May also require an alarm signal from stressed/damaged cells to trigger immune response; signal may be heat-shock proteins produced and released by cell surfaces in response to heat or other stressor

    Made effective by combining with adjuvant, but some adjuvants trigger localized or even systemic reactions

    May be oral if capable of involving pharyngeal or small intestinal immune cells

  • Proteins digested rapidly in stomach, so require protection to pass through to small intestine; enteric coating to slow gastric degradation

    Attraction and attachment to mucosal surfaces important; a bacterial lectin coat is useful for this, making it mimic a pathogenic bacterium; liposomes (phospholipid and cholesterol membranes)

    Oral delivery requires larger dose of vaccine, and has less predictable result

  • Proteinaceous in nature ñ breaks down when eaten by 2° consumer, so presumably safe for environment

    Behavioral effects minimized (but note continued cycling in unfertilized polyestrous females)

    Species- and individual-specific response in antibody development

  • In antibody titer achieved

    In time until effective titer reached

    In time until titer no longer effective

    In whether antibody titer has contraceptive effect (e.g. for some species, PZP is too dissimilar structurally to their own ZP)

  • May genetically engineer harmless virus (e.g. vaccinia virus, ectromelia virus - mousepox) with ability to produce desired antigen like mouse ZP3

  • Would be exceptionally effective, economic large-scale strategy

    Species-specificity and attenuation would be VERY important

  • Not yet used outside of controlled situation

  • Conclusions

  • Still largely ineffective after 4 decades; most methods not feasible for free-ranging animals

    None effective in reducing populations already too large ñ traditional culling still necessary (reproduction not only factor affecting population size, compensatory survivorship important too)

    Effects on non-target species, including humans, still largely unknown

     

  • Assisted Breeding of Wildlife

    Purpose

  • Proliferation of human species
  • Direct killing of wildlife (guns, poisons, automobiles)

    *Habitat destruction

  • Loss of much suitable area

    Fragmentation of remaining suitable area

  • Areas too small to harbor viable populations of various species, because of genetic considerations

  • inbreeding depression; resultant infertility, susceptibility to disease, inability to adapt to changing conditions

    genetic drift with unpredictable results ñ esp. fixation of deleterious alleles (FL panther cryptorchidism)

  • Populations require assistance to survive in long-term; management of wild lands as parks ñ "zoos without fences"

    Translocation is a low tech, relatively low cost strategy, but

  • Danger to animals during shipping

    Translocated animals often disperse or are killed before reproducing

    Animals may be too valuable to their original population to remove

  • Zoos also interested because of problems breeding captive animals (mate too distant, behavioral problems, incompatibility, health or age)

  • History

  • Experimentation on exposure of horse semen to "winter conditions" in 1776!

    Strong (eutherian) mammalian bias

    Externally-fertilizing Fish

  • Hormonally primed to force gamete development and maturation using GnRHs, or extracted pituitaries, or OvaPrim ñ commercial preparation of Salmon GnRH and a dopamine blocker (dopamine is a GnRH blocker)

    Subsequent hatchery-style combination of gametes and rearing of embryos for later stocking

  • Same methods being applied to endangered amphibians; sure to increase because they are under global threat

    Birds ñ little real work done

    Reptiles ñ virtually no work done

  • Preparative techniques

  • Estrus synchronization ñ to manipulate femaleís reproductive state to time readiness for techniques
  • PGF2a in ruminants: destruction of CL and decrease in circulating P4 ñ> initiates sequence of endocrine events resulting in ovulation

    Exogenous gonadotrophins, e.g. PMSG and HCG in felids (induced ovulators): stimulates LH surge by pituitary ñ> LH induces follicle rupture

  • Superovulation ñ (ultimately) to obtain largest number of viable embryos for use

  • Quite a range of potentially viable oocytes produced by species in nature - plains viscacha produces several thousand oocytes each cycle, and eventual litter size is result of subsequent death of oocytes and embryos (remember the most common fate of a follicle is atresia)

    Exogenous gonadotrophins, e.g. PMSG, FSH

    Tip development in favor of ovulation instead of atresia

  • Semen collection ñ to obtain sperm capable of fertilizing ova

  • Artificial vagina ñ requires tame animals, risks to handler

    Electroejaculation ñ variable results, generally requires anesthesia, and so must develop proper protocol to avoid urine contamination, retrograde ejaculation

    Biopsy or postmortem ñ mature sperm from cauda epididymis; now also having some success with immature sperm from head of epididymis; maybe even sperm precursors

    Special note ñ sperm precursor cells transferred into testes of immunodeficient mice ñ have obtained viable rat sperm; this technique would only require single biopsy from donor to produce large # of sperm

  • Genetic transfer

  • Artificial insemination (AI)
  • Very old technique, still most commonly and widely used

    Anterior vagina ñ most often used because least invasive, but also least effective

    Cervix

    Uterine ñ often laparoscopic intrauterine insemination works best

  • Embryo transfer (ET)

  • Widely applicable in ungulates (cervids, bovids, camelids, ovids); limited application elsewhere

    Allows recovery of more of donor females genome

    Keeps donor female donating, rather than busy in gestation and lactation of young

    Eliminates chance of death due to pregnancy or parturition

    Can even use different species

  • So far used in closely related species, such as mouflon to sheep, gaur to domestic cattle

    For extremely rare species, where every female is important

    Problematic

  • Embryos might not secrete correct factors, or at right times to prevent luteolysis

    Physiological mismatch possible: endocrine, immunological problems (rejection by female), formation of inadequate placenta

  • One solution ñ chimaeric embryos

  • Outermost layer of placenta (in direct apposition to maternal tissues) derived from trophectoderm, which differentiates from the embryoís inner cell mass at the blastocyst stage, and so does NOT form any part of the fetus

    So, transplant inner cell mass of endangered species into trophectoderm from recipient species

    May not solve all problems, as other major constituents of placenta are formed by inner cell mass cells at later stages

  • Transfer embryos under laparoscopy rather than general anesthesia and surgery

  •  

    In vitro fertilization (IVF)

  • Recent adaptation of human procedures to animals

    4 phases

  • oocyte maturation ñ complex nuclear, cytoplasmic and cytoskeletal processes leading to ovulation

    sperm capacitation ñ complex changes in cell membrane constituents to prepare sperm to penetrate egg

    fertilization ñ combination of sperm and egg

    (note problems with capacitation and fertilization being overcome by direct intracytoplasmic (ICSI) and subzonal (SUZI) sperm injection)

    embryo culture ñ fostering pre-implantation development

  • Demanding, expensive, sometimes low pregnancy rates for high-tech methods:

  • Natural reproduction ñ approximately 80% pregnancy rate (near 100% in captive species)

    AI ñ 50%

    ET ñ 65%

    IVF - 20%

  • Genome banking

  • Cryopreservation ñ the "Frozen Zoo"
  • Zoos found new purpose in conservation of endangered species
  • Some captive species now extinct in wild

    But what good is a captive species? ("The California Condor vs. National Audubon Society")

    Still, in general successful reintroduction is highly unlikely (whooping cranes in FL, red wolves in NC)Ö

    ÖAnd impossible if no habitat remains

    Zoos have too little space and other resources to maintain genetically viable populations for more than a handful of species

    Number of endangered species increasing at exponential rate

    Idea that gametes and/or embryos of endangered species could be cryopreserved in lieu of keeping large population

    Goal to maintain frozen zoo until human population passes some "demographic winter"

    Then wild lands can be rededicated and endangered species will be "reborn" (some criticize as fantasy)

  • Accidental discovery in 1949 that glycerol protects sperm during freezing

    Cryobiological research on erythrocytes, tissue culture cells, stem and yeast cells in 1950s

    Now used in many species

    Very long-term storage possible (some mouse embryos already stored >> decade), estimated longevity in THOUSANDS of years

    Cryoprotectants were key

  • Physiochemistry - Heat and water transport between intra- and extracellular environment (mammalian embryos approximately 80% water)

    Phase change from liquid to solid especially important

    Cryoprotectants lower temperature at eutectic point (upper limit of salt solubility) and freezing point

    Temperature decrease -> Extracellular water removed as ice -> Osmotic pressure gradient develops between concentrated extracellular solution and dilute intracellular solution -> Efflux of water from embryo -> Influx of cryoprotectant

  • Permeating cryoprotectants: glycerol, dimethyl sulfoxide (DMSO)

  • Stabilize membrane phospholipids and protein macromolecules

    Act as solvent for solutes and electrolytes

    Reduce onset of ice formation

    *Increase viscosity of intracellular compartments, promoting VITRIFICATION (production of solid, laminar "glass" phase) instead of crystallization

  • Non-permeating cryoprotectants ñ sucrose, dextrose, albumin

  • Dehydrate embryonic blastomeres during cooling, thereby decreasing risk of intracellular ice
  • High molarity cryoprotectants best for vitrification

    At least one, VS3a, can be used at room temperature

    Need to avoid osmotic trauma or cryoprotectant toxicity

  • The major problem ñ failure of embryo-maternal signaling

  • Asynchronous development ñ embryo death (recall maternal recognition of pregnancy ñ embryo prevents destruction of CL; CL IMPERATIVE to embryoís early survival)

    Primates ñ placenta releases luteotrophic gonadotrophin

    Ruminants ñ embryo releases interferon before implantation, suppressing luteolysis

    Luteal lifespan supplementation with interferon successful in some ungulates

    Still much work needed

  • But not the only problem

  • Complex and still poorly understood interplay between intra-, inter- and extraovarian regulatory mechanisms

    Many adverse treatment (especially anesthetic) effects, on essentially every stage of development: follicular, oocyte, embryo

  • All techniques still only with sporadic successes, often not replicated despite effort