COSEWIC Assessment and Status Report on the Unisexual Ambystoma Ambystoma laterale in Canada - 2016

Small-mouthed Salamander-dependent population
(Ambystoma laterale - texanum)

Jefferson Salamander-dependent population
(Ambystoma laterale - (2) jeffersonianum)

Blue-spotted Salamander-dependent population
(Ambystoma (2) laterale - jeffersonianum)

Unisexual Ambystoma
Photo: © J.P. Bogart., 2016

Small-mouthed Salamander dependent population - Endangered
Fefferson Salamander dependent population - Endangered
Blue-spotted Salamander dependent population - Not at risk
2016


Document information

COSEWIC
Committee on the Status
of Endangered Wildlife
in Canada

COSEWIC logo

COSEPAC
Comité sur la situation
des espèces en péril
au Canada

COSEWIC status reports are working documents used in assigning the status of wildlife species suspected of being at risk. This report may be cited as follows:

COSEWIC. 2016. COSEWIC assessment and status report on the unisexual Ambystoma, Ambystoma laterale, Small-mouthed Salamander-dependent population, Jefferson Salamander-dependent population and the Blue-spotted Salamander-dependent population, in Canada. Committee on the Status of Endangered Wildlife in Canada. Ottawa. xxii + 61 pp.

(Species at Risk Public Registry website).

Production note:

COSEWIC would like to acknowledge Jim Bogart for writing the status report on the unisexual Ambystoma in Canada. This report was prepared under contract with Environment Canada and was overseen by Kristiina Ovaska, Co-chair of the COSEWIC Amphibian and Reptile Species Specialist Subcommittee.

For additional copies contact:

COSEWIC Secretariat
c/o Canadian Wildlife Service
Environment and Climate Change Canada
Ottawa, ON
K1A 0H3

Tel.: 819-938-4125
Fax: 819-938-3984
E-mail: COSEWIC E-mail
Website: COSEWIC

Également disponible en français sous le titre Ếvaluation et Rapport de situation du COSEPAC sur L'Ambystoma unisexué (Ambystoma laterale), population dépendante de la salamandre à petite bouche, population dépendante de la salamandre de Jefferson et la population dépendante de la salamandre à points bleus, au Canada.

Cover illustration/photo:

Unisexual Ambystoma - Triploid Jefferson Salamander - dependent unisexual (LJJ) from Halton Region Ontario (10 April 2013; total length = 150 mm; snout-vent length = 80 mm). Photo by J.P. Bogart.


COSEWIC assessment summary

Assessment summary - May 2016

Common name
Unisexual Ambystoma - Small-mouthed Salamander dependent population
Scientific name
Ambystoma laterale
Status
Endangered
Reason for designation
These unusual unisexual salamanders exist only on one isolated island in Canada (Pelee Island in Lake Erie) and depend on an endangered sperm donor species, Small-mouthed Salamander (Ambystoma texanum), for recruitment. The salamander faces numerous threats that make its continued existence precarious. These include predation and habitat modification by introduced wild turkeys, drainage activities that can cause premature drying of breeding ponds, road mortality during seasonal migrations, urban development, and recreational activities.
Occurrence
Ontario
Status history
Designated Endangered in April 2016.

Assessment summary - May 2016

Common name
Unisexual Ambystoma - Jefferson Salamander dependent population
Scientific name
Ambystoma laterale
Status
Endangered
Reason for designation
These unusual unisexual salamanders occupy restricted areas within populated and highly modified areas of Ontario and depend on an endangered sperm donor species, Jefferson Salamander (Ambystoma jeffersonianum), for recruitment. The salamander faces numerous threats from human activities, leading to habitat loss and fragmentation, making its continued existence precarious.
Occurrence
Ontario
Status history
Designated Endangered in April 2016.

Assessment summary - May 2016

Common name
Unisexual Ambystoma - Blue-spotted Salamander dependent population
Scientific name
Ambystoma laterale
Status
Not at Risk
Reason for designation
These unusual unisexual salamanders depend on a sperm-donor species, Blue-spotted Salamander (Ambystoma laterale), that has an extensive distribution in Canada. It is found from Nova Scotia to Manitoba and from the Great Lakes to James Bay and Northern Quebec. Unisexuals that depend on this species have been identified in sites across this range and likely exist in many other sites that have not been subjected to genetic analyses. While declines have been observed and are expected for the Blue-spotted Salamander and unisexuals that depend on it in southwestern Ontario, threats are localized and expected to have little effect on the entire Canadian population.
Occurrence
Ontario, Quebec, New Brunswick, Nova Scotia
Status history
Designated Not at Risk in April 2016.

COSEWIC executive summary

Unisexual Ambystoma
Ambystoma laterale

Small-mouthed Salamander-dependent population
(Ambystoma laterale - texanum)

Jefferson Salamander-dependent population
(Ambystoma laterale - (2) jeffersonianum)

Blue-spotted Salamander-dependent population
(Ambystoma (2) laterale - jeffersonianum)

Wildlife species description and significance

All-female populations of Ambystoma (i.e., unisexuals) are members of the Mole Salamander family Ambystomatidae. Their morphology is variable and is determined by their nuclear genomes. Unisexuals with two or more Blue-spotted Salamander (A. laterale) chromosome complements are black with various amounts of blue flecking, and have relatively short limbs and a narrower head. Unisexuals with two or more Jefferson Salamander (A. jeffersonianum) chromosome complements are larger, grey to brown with a small amount of blue flecking, and have relatively long limbs and a broader head. Unisexuals with two or more Small-mouthed Salamander (A. texanum) chromosome complements are grey, more slender, and have narrow heads.

Unisexual Ambystoma all share a very similar mitochondrial DNA that is distinctly different from any bisexual species. They have a unique genetic system and represent a distinct, monophyletic lineage that arose 3 to 5 million years ago, making them the oldest lineage of unisexual vertebrates known. Eggs normally develop by gynogenesis. This process requires sperm, derived from sympatric bisexual species. The sperm is only used to initiate the development of the eggs and typically is not incorporated in the developing embryo. In rare cases, sperm are incorporated, and when DNA from sperm are incorporated, the ploidy of the embryos increases (i.e., triploid to tetraploid).

Distribution

Unisexual salamanders are found in association with appropriate bisexual species whose males serve as sperm donors. The geographic range of unisexual salamanders in the genus Ambystoma roughly coincides with deciduous and mixed-wood forests in northeastern North America from Nova Scotia and the New England States to Indiana. Their northern limits are in Minnesota, north-central Ontario, and southern Quebec, and they range south to Kentucky. Three designatable units are considered in this report, based on their sperm-donor species. In Canada, unisexual salamanders are found in association with the Blue-spotted Salamander in Nova Scotia, New Brunswick, Quebec, and Ontario; with the Jefferson Salamander in Ontario; and with the Small-mouthed Salamander on Pelee Island in Lake Erie, Ontario. In Canada, unisexual populations of salamanders occur in all known Jefferson Salamander and Small-mouthed Salamander populations, as well as in the majority of Blue-spotted Salamander populations that have been investigated. Unisexual Salamanders can be much more numerous than individuals of sympatric bisexual species that serve as sperm donors.

Habitat

Unisexual Salamanders have the same habitat requirements as their respective sperm-donating species. They are normally found within deciduous or mixed forests containing, or adjacent to, suitable breeding ponds. Breeding ponds are normally ephemeral, or vernal, pools that dry in late summer. Terrestrial habitat is in moist woodlands, where the salamanders find shelter from predators and desiccation under fallen trees or rocks, as well as in mammal burrows. Adults forage during humid conditions at night on the forest floor within ~1 km of the breeding pond. These salamanders also require terrestrial overwintering sites below the frost line.

Biology

In conjunction with individuals of their sperm-donating species, unisexual adults migrate to and from breeding ponds at night very early in spring. Most migration events to and from breeding ponds coincide with rain or very humid conditions. Courtship occurs with sympatric bisexual males and, within a day or two after mating, unisexual salamanders deposit several egg masses on sticks or emergent vegetation at various depths in the breeding pond. Egg deposition may occur under the ice. Duration of egg and larval development is variable and temperature-dependent. Larvae are carnivorous and eat a variety of invertebrates and are also cannibalistic. In Canada, larvae normally transform in July or early August and leave the pond. Juveniles and adults are entirely terrestrial except for the annual breeding period.

Population size and trends

Estimation of population sizes of unisexual salamanders is difficult because they are morphologically similar to females of their sympatric sperm-donating species. Most of the historical sites surveyed for the Jefferson Salamander in 1990 and 1991 no longer supported either the Jefferson Salamander or unisexual salamanders in 2003 and 2004. Furthermore, at some sites where both Jefferson Salamanders and unisexuals still existed in 2003-2004, there was a notable reduction in the number of egg masses compared to numbers found in earlier surveys. Population sizes of unisexuals vary with respect to the sperm donor and geographic area. All subpopulations of Jefferson Salamanders and Small-mouthed Salamanders also contain unisexuals that can account for ~ 85% of individuals at a site. The percent of unisexuals found in Blue-spotted Salamander breeding ponds is more variable, and some of those ponds have not yielded any unisexuals.

Threats and limiting factors

Loss of sexual sperm donors is a limiting factor unique to unisexual Ambystoma because they require the presence of diploid males of their sexual hosts for reproduction. Threats include:partial or absolute elimination of suitable habitat by development, including loss of breeding ponds, trees and ground cover;barriers (e.g., roads, silt fences) across migratory routes linked to breeding ponds; andpremature pond drying during summer.

Protection, status, and ranks

Unisexuals coexist with species some of which have a designated conservation status and are morphologically indistinguishable from those species. Connecticut lists A. jeffersonianum "complex" and A. laterale "complex" as state species of special concern. In Ontario, Jefferson Salamander dominated polyploids are unisexuals that require Jefferson Salamander males. Since 2010, these individuals have received the same habitat protection as the Jefferson Salamander under the provincial Endangered Species Act, 2007 (ESA) (see O.Reg. 242/08 s.28). So far, there is no similar regulation for Canadian unisexuals that live with the Endangered Small-mouthed Salamander (A. texanum) on Pelee Island, Ontario, or unisexuals that depend on the Blue-spotted Salamander (A. laterale).


Technical summary (DU 1)

Scientific name:
Ambystoma laterale - texanum
English name:
Unisexual Ambystoma (Small-mouthed Salamander-dependent population)
French name:
Ambystoma unisexué (population dépendante de la salamandre à petite bouche)
Range of occurrence in Canada (province/territory/ocean):
Ontario (Pelee Island, Essex County)

Demographic Information

Demographic Information
Summary itemsInformation
Generation TimeApproximately 8 years (see Life Cycle and Reproduction)
Is there an [observed, inferred, or projected] continuing decline in number of mature individuals?Yes, inferred and projected continuing decline based on the projected decline for the Small-mouthed Salamander (see COSEWIC 2004, 2014) and other identified threats.
Estimated percent of continuing decline in total number of mature individuals within [5 years or 2 generations]Unknown
[Observed, estimated, inferred, or suspected] percent [reduction or increase] in total number of mature individuals over the last [10 years, or 3 generations].Unknown
[Projected or suspected] percent [reduction or increase] in total number of mature individuals over the next [10 years, or 3 generations].Projected and suspected reduction based on the Threats Calculation that summarized the overall threat impact as "high" (10 - 70% projected decline).
[Observed, estimated, inferred, or suspected] percent [reduction or increase] in total number of mature individuals over any [10 years, or 3 generations] period, over a time period including both the past and the future.Unknown

Are the causes of the decline

  1. clearly reversible and
  2. understood and
  3. ceased?
  1. No
  2. Yes
  3. No
Are there extreme fluctuations in number of mature individuals?There are fluctuations because recruitment varies greatly from year to year, but such fluctuations are probably not extreme.

Extent and Occupancy Information

Extent and Occupancy Information
Summary itemsInformation
Estimated extent of occurrence20 km2
Index of area of occupancy (IAO) (Always report 2x2 grid value).20 km2, based on five 2 x 2 km grids superimposed on four recently occupied breeding ponds.

Is the population "severely fragmented" ie. is >50% of its total area of occupancy in habitat patches that are

  1. smaller than would be required to support a viable population, and
  2. separated from other habitat patches by a distance larger than the species can be expected to disperse?
  1. No; more than half of the occupied sites appear to support viable populations;
  2. yes; the breeding ponds are separated by > 1 km, and salamanders are unlikely to disperse among them.
Number of "locations"?
(Note: See Definitions and Abbreviations on COSEWIC website and IUCN (Feb 2014) for more information on this term.)
(use plausible range to reflect uncertainty if appropriate)
Four locations on Pelee Island. There was a loss of two historical breeding ponds (locations) between 1991 and 2000 (COSEWIC 2004).
Is there an [observed, inferred, or projected] decline in extent of occurrence?Yes, observed loss of two historical breeding ponds.
Is there an [observed, inferred, or projected] decline in index of area of occupancy?Yes, inferred decline in IAO based on loss of breeding ponds from 1991 to 2000 (COSEWIC 2004).
Is there an [observed, inferred, or projected] decline in number of subpopulations?Yes, inferred decline as each breeding pond is considered a subpopulation.
Is there an [observed, inferred, or projected] decline in number of "locations"?
(Note: See Definitions and Abbreviations on COSEWIC website and IUCN (Feb 2014) for more information on this term.)
Yes, inferred loss of breeding ponds, corresponding to locations, based on information from the Small-mouthed Salamander (COSEWIC 2004, 2014).
Is there an [observed, inferred, or projected] decline in [area, extent and/or quality] of habitat?Yes, observed and inferred loss of breeding ponds based on information from the Small-mouthed Salamander (COSEWIC 2004, 2014).
Are there extreme fluctuations in number of subpopulations?No

(Note: See Definitions and Abbreviations on COSEWIC website and IUCN (Feb 2014) for more information on this term.)?
No
Are there extreme fluctuations in extent of occurrence?No
Are there extreme fluctuations in index of area of occupancy?No

Number of Mature Individuals (in each subpopulation)

Number of Mature Individuals (in each subpopulation)
Subpopulations (give plausible ranges)Number of Mature Individuals
Fish Point (southern tip of Pelee Island)Unknown
Pond (middle of Pelee Island)Unknown
Sheridan Point (northern Tip of Pelee Island)Unknown
Stone RoadUnknown
TotalUnknown but possibly < 1000

Quantitative Analysis

Quantitative Analysis
Summary itemsInformation
Probability of extinction in the wild is at least [20% within 20 years or 5 generations, or 10% within 100 years].Not done due to lack of data

Threats (actual or imminent, to populations or habitats, from highest impact to least)

Threats (actual or imminent, to populations or habitats, from highest impact to least)
Summary itemsInformation
  1. Dams and water management/use (Threat 7.2). Drainage activities on Pelee Island can affect the breeding habitat by reducing breeding areas and cause premature drying of breeding ponds.
  2. Housing and urban areas (Threat 1.1). Decline or destruction of habitat from clearing of wooded areas.
  3. Annual and perennial non-timber crops (Threat 2.1)
  4. Roads and railroads (Threat 4.1). Barriers to breeding migrations from new roads, as well as increased road mortality.
  5. Recreational activities (Threat 6.1)
  6. Other ecosystem modifications (Threat 7.3). The introduction of Wild Turkeys on Pelee Island may pose a serious threat because Turkeys can destroy terrestrial hiding places for salamanders and may prey upon salamanders (Invasive non-native/alien species) (Threat 8.1).

Was a threats calculator completed for this species and if so, by whom?

Yes. Leslie Anthony, Jim Bogart, Joe Crowley, Yohann Dubois, Isabelle Gauthier, Bev McBride (COSEWIC secretariat), Kristiina Ovaska, Mary Sabine

Rescue Effect (immigration from outside Canada)

Rescue Effect (immigration from outside Canada)
Summary itemsInformation
Status of outside population(s) most likely to provide immigrants to Canada.Unisexual Ambystoma have no status in Ohio or Michigan. The Small-mouthed Salamander is a threatened species in Michigan owing, in large part, to loss of suitable habitat
Is immigration known or possible?No
Would immigrants be adapted to survive in Canada?Yes
Is there sufficient habitat for immigrants in Canada?No, these unisexuals depend on Small-mouthed Salamander males that, in Canada, only exist on Pelee Island, which is isolated from U.S. populations.
Are conditions deteriorating in Canada?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
Yes
Are conditions for the source population deteriorating?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
Unknown
Is the Canadian population considered to be a sink?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
No
Is rescue from outside populations likely?No

Data Sensitive Species

Data Sensitive Species
Summary itemsInformation
Is this a data sensitive species?Yes, because these unisexuals depend on, and live with, the endangered Small-mouthed Salamander, which is a data sensitive species.

Status History

Status History
Summary itemsInformation
COSEWICNot previously assessed.

Status and Reasons for Designation

Status and Reasons for Designation
Summary itemsInformation
StatusEndangered
Alpha-numeric codesB1ab(i,ii,iii,iv)+2ab(i,ii,iii,iv)
Reasons for designationThese unusual unisexual salamanders exist only on one isolated island in Canada (Pelee Island in Lake Erie) and depend on an endangered sperm donor species, Small-mouthed Salamander (Ambystoma texanum), for recruitment. The salamander faces numerous threats that make its continued existence precarious. These include predation and habitat modification by introduced wild turkeys, drainage activities that can cause premature drying of breeding ponds, road mortality during seasonal migrations, urban development, and recreational activities.

Applicability of Criteria

Applicability of Criteria
Summary itemsInformation
Criterion A (Decline in Total Number of Mature Individuals)Does not meet criteria. The magnitude of declines is unknown.
Criterion B (Small Distribution Range and Decline or Fluctuation)Meets Endangered B1ab(i,ii,iii,iv)+2ab(i,ii,iii,iv). EOO and IAO are below thresholds for Endangered. There are fewer than 5 locations (sub-criterion a), EOO has declined due to loss of 2 historical sites (b i) habitat quantity and quality are declining because of wild turkeys and other threats (b iii); there is a projected continued decline in subpopulations (locations) (b iv), which will result in a decline in IAO (b ii).
Criterion C (Small and Declining Number of Mature Individuals)Not applicable. Does not meet thresholds for Endangered.
Criterion D (Very Small or Restricted Population)Not applicable. Does not meet thresholds for Endangered.
Criterion E (Quantitative Analysis)Not done due to lack of data.

Technical summary (DU 2)

Scientific name:
Ambystoma laterale - (2) jeffersonianum
English name:
Unisexual Ambystoma (Jefferson Salamander-dependent population)
French name:
Ambystoma unisexué (population dépendante de la salamandre de Jefferson)
Range of occurrence in Canada (province/territory/ocean):
Ontario

Demographic Information

Demographic Information
Summary itemsInformation
Generation TimeApproximately 11 years (see Life Cycle and Reproduction)
Is there an [observed, inferred, or projected] continuing decline in number of mature individuals?Yes, observed, inferred and projected continuing decline based on the decline for the Jefferson Salamander and threats to habitat
Estimated percent of continuing decline in total number of mature individuals within [5 years or 2 generations]Unknown
[Observed, estimated, inferred, or suspected] percent [reduction or increase] in total number of mature individuals over the last [10 years, or 3 generations].Suspected decline of > 90% over the last 3 generations (33 years), based on long-term data sets for Jefferson Salamanders. Egg mass counts (index of abundance) from 1976 - 2006 show a >90% decline.
[Projected or suspected] percent [reduction or increase] in total number of mature individuals over the next [10 years, or 3 generations].Projected reduction based on the Threats Calculation that summarized the overall threat impact as "very high" (50 - 100% reduction).
[Observed, estimated, inferred, or suspected] percent [reduction or increase] in total number of mature individuals over any [10 years, or 3 generations] period, over a time period including both the past and the future.Suspected decline of > 90% based on past and projected future declines.

Are the causes of the decline

  1. clearly reversible and
  2. understood and
  3. ceased?
  1. No, habitat has been lost and road mortality is difficult to reverse.
  2. Yes
  3. No
Are there extreme fluctuations in number of mature individuals?There are fluctuations because recruitment varies greatly from year to year, but such fluctuations are probably not extreme.
Extent and Occupancy Information 

Estimated extent of occurrence

Estimated extent of occurrence
Summary itemsInformation
Index of area of occupancy (IAO) (Always report 2x2 grid value).188 km2. IAO was calculated as 728 km2, when both historical and recent localities were included using 2x2 km grids. The most recent calculation for the Jefferson Salamander is 188 km2.

Is the population "severely fragmented" ie. is >50% of its total area of occupancy in habitat patches that are

  1. smaller than would be required to support a viable population, and
  2. separated from other habitat patches by a distance larger than the species can be expected to disperse?
  1. Yes, most known subpopulations have small (< 200) numbers of adult Jefferson Salamanders and are isolated from one another. Virtually all subpopulations (breeding ponds or locations) are below estimated MVPs for long-term persistence of vertebrates in general and for other species of Ambystoma (Reed et al. 2003).
  2. Yes, there is a loss of connecting habitat between breeding ponds, most of which are separated by >1 km. This distance would be greater than expected dispersal distances for the salamanders. Salamanders have limited dispersal capability and have breeding site fidelity.
Number of "locations"
(Note: See Definitions and Abbreviations on COSEWIC website and IUCN (Feb 2014) for more information on this term.)
(use plausible range to reflect uncertainty if appropriate)
There are estimated to be ~30 geographically or ecologically distinct locations for the Jefferson Salamander. At each location, a single threatening event, such as a change in hydrology or hydroperiod from a variety of human activities, can rapidly affect all individuals.
Is there an [observed, inferred, or projected] decline in extent of occurrence?Yes, present subpopulations are more closely linked with the Niagara Escarpment. Several historical subpopulations to the east and west of the Escarpment have been lost, and there has been a 62% decline in EOO.
Is there an [observed, inferred, or projected] decline in index of area of occupancy?Yes, there is an observed and projected decline for the Jefferson Salamander that will have an impact on the unisexuals that depend on this species. Comparing 1979-2003 and 2004-2015 data for Jefferson salamanders, the decline of suitable breeding ponds in the most recent generation (2004-2015) is 74%.
Is there an [observed, inferred, or projected] decline in number of subpopulations?Yes, observed and projected declines in subpopulations (corresponding to discrete breeding ponds).
Is there an [observed, inferred, or projected] decline in number of "locations"?
(Note: See Definitions and Abbreviations on COSEWIC website and IUCN (Feb 2014) for more information on this term.)
Yes, observed and projected decline in locations (corresponding to discreet breeding ponds).
Is there an [observed, inferred, or projected] decline in [area, extent and/or quality] of habitat?Yes, observed and projected decline in area, extent, and quality of habitat.
Are there extreme fluctuations in number of subpopulations?No
Are there extreme fluctuations in number of "locations"?No
Are there extreme fluctuations in extent of occurrence?No
Are there extreme fluctuations in index of area of occupancy?No

Number of Mature Individuals (in each subpopulation)

Number of Mature Individuals (in each subpopulation)
Subpopulations (give plausible ranges)N Mature Individuals
There are estimated to be about 30 discrete breeding ponds, each of which represents a subpopulation with little or no genetic exchange expected between subpopulations.Unknown but probably < 10,000. There may be < 2500 adult Jefferson Salamanders (COSEWIC 2010). Jefferson Salamander-dependent unisexuals are more numerous than their sperm donors and, over the range of Jefferson Salamanders, constitute 60% to 95% of subpopulations with an approximate average of 80%, resulting in < 10,000 adult unisexuals.
Total< 10,000

Quantitative Analysis

Quantitative Analysis
Summary itemsInformation
Probability of extinction in the wild is at least [20% within 20 years or 5 generations, or 10% within 100 years].Not done due to lack of data

Threats (actual or imminent, to populations or habitats, from highest impact to least)

Threats (actual or imminent, to populations or habitats, from highest impact to least)
Summary itemsInformation
  1. Residential & commercial development (Threat 1), particularly from housing and urban areas (Threat 1.1).
  2. Mining & quarrying (Threat 3.2)
  3. Roads & railroads (Threat 4.1). Road mortality during breeding migrations.
  4. Agriculture (Threat 2.1) causing loss and degradation of habitats
  5. Invasive non-native/alien species
Was a threats calculator completed for this species and if so, by whom?
Yes. Leslie Anthony, Jim Bogart, Joe Crowley, Yohann Dubois, Isabelle Gauthier, Bev McBride (COSEWIC secretariat), Kristiina Ovaska, Mary Sabine.

Rescue Effect (immigration from outside Canada)

Rescue Effect (immigration from outside Canada)
Summary itemsInformation
Status of outside population(s) most likely to provide immigrants to Canada.Unisexuals have no status in adjacent states (Vermont, New York, Michigan and Ohio). The sperm donor, Jefferson Salamander, is a threatened species in Vermont and does not occur in Quebec or Michigan.
Is immigration known or possible?Unlikely, but possible from Vermont.
Would immigrants be adapted to survive in Canada?Yes
Is there sufficient habitat for immigrants in Canada?No, habitat is restricted to areas in southwestern Ontario that are diminishing.
Are conditions deteriorating in Canada?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
Yes, habitat is being lost and degraded over the range of Jefferson Salamanders in Canada.
Are conditions for the source population deteriorating?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
Unknown
Is the Canadian population considered to be a sink?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
No
Is rescue from outside populations likely?No

Data Sensitive Species

Data Sensitive Species
Summary itemsInformation
Is this a data sensitive species?Yes, because these unisexuals co-exist with the Endangered Jefferson Salamander, which is a data sensitive species.

Status History

Status History
Summary itemsInformation
COSEWICNot previously assessed.

Status and Reasons for Designation:

Status and Reasons for Designation:
Summary itemsInformation
StatusEndangered
Alpha-numeric codesA2bc+3c+4bc; B2ab(i,ii,iii,iv,v)
Reasons for designationThese unusual unisexual salamanders occupy restricted areas within populated and highly modified areas of Ontario and depend on an endangered sperm donor species, Jefferson Salamander (Ambystoma jeffersonianum), for recruitment. The salamander faces numerous threats from human activities, leading to habitat loss and fragmentation, making its continued existence precarious.

Applicability of Criteria

Applicability of Criteria
Summary itemsInformation
Criterion A (Decline in Total Number of Mature Individuals):Meets Endangered A2 because there is an observed, inferred and suspected decline of >50% in number of mature individuals over the past 3 generations (since 1982) based on a decline in index of abundance (sub-criterion b) and in IAO and quality of habitat (sub-criterion c); also meets A3 based on similar suspected future declines and A4 based on similar suspected declines that incorporate both the future and the past.
Criterion B (Small Distribution Range and Decline or Fluctuation):Meets Endangered B2 because IAO is below threshold; meets sub-criterion (a) because the population is severely fragmented; also meets sub-criterion (b) because there is a continuing inferred and projected decline in EOO (i), index of area of occupancy (ii), extent and /or quality of habitat (iii), number of locations and subpopulations (iv), and number of mature individuals (v).
Criterion C (Small and Declining Number of Mature Individuals)Not applicable. Does not meet thresholds for Endangered.
Criterion D (Very Small or Restricted Population)Does not apply. Population is not very small or restricted.
Criterion E (Quantitative Analysis)Not done due to lack of data.

Technical summary (DU 3)

Scientific name:
Ambystoma (2) laterale - jeffersonianum
English name:
Unisexual Ambystoma (Blue-spotted Salamander-dependent population)
French name:
Ambystoma unisexué (population dépendante de la salamandre à points bleus)
Range of occurrence in Canada (province/territory/ocean):
Ontario, Quebec, Nova Scotia, New Brunswick

Demographic Information

Demographic Information
Summary itemsInformation
Generation Time See Life Cycle and ReproductionApproximately 8 years (see Life Cycle and Reproduction)
Is there an [observed, inferred, or projected] continuing decline in number of mature individuals?Yes, inferred and projected decline. Although Blue-spotted Salamander-dependent unisexuals are wide-ranging and abundant in Canada, habitat and wetland loss in parts of the range of their sperm donor has resulted in a decline.
Estimated percent of continuing decline in total number of mature individuals within [5 years or 2 generations]Unknown
[Observed, estimated, inferred, or suspected] percent [reduction or increase] in total number of mature individuals over the last [10 years, or 3 generations].Unknown
[Projected or suspected] percent [reduction or increase] in total number of mature individuals over the next [10 years, or 3 generations].Unknown. Threats calculation summarized the overall threat impact as low (i.e., 0 - 10% reduction).
[Observed, estimated, inferred, or suspected] percent [reduction or increase] in total number of mature individuals over any [10 years, or 3 generations] period, over a time period including both the past and the future.Unknown

Are the causes of the decline

  1. clearly reversible and
  2. understood and
  3. ceased?
  1. Partially; known in some geographical areas but not in others.
  2. Yes
  3. No
Are there extreme fluctuations in number of mature individuals?There are fluctuations because recruitment varies greatly from year to year, but such fluctuations are probably not extreme.

Extent and Occupancy Information

Extent and Occupancy Information
Summary itemsInformation
Estimated extent of occurrence671,668 km2
Index of area of occupancy (IAO) (Always report 2x2 grid value).1,932 km2 (calculated based on documented localities; actual value is most likely larger)

Is the population "severely fragmented" ie. is >50% of its total area of occupancy in habitat patches that are

  1. smaller than would be required to support a viable population, and
  2. separated from other habitat patches by a distance larger than the species can be expected to disperse?
  1. No
  2. No
Number of "locations"
(Note: See Definitions and Abbreviations on COSEWIC website and IUCN (Feb 2014) for more information on this term.)
(use plausible range to reflect uncertainty if appropriate)
Very many >> 100 locations.
Is there an [observed, inferred, or projected] decline in extent of occurrence?No
Is there an [observed, inferred, or projected] decline in index of area of occupancy?Yes, inferred decline in some parts of the range (southern Ontario) based on habitat loss, but few data are available.
Is there an [observed, inferred, or projected] decline in number of subpopulations?Yes, observed and inferred decline in some parts of the range in southwestern Ontario and southern Quebec close to urban areas or where wetlands have been drained.
Is there an [observed, inferred, or projected] decline in number of "locations"?
(Note: See Definitions and Abbreviations on COSEWIC website and IUCN (Feb 2014) for more information on this term.)
Yes, observed and inferred decline in some parts of the range in southwestern Ontario and southern Quebec close to urban areas or where wetlands have been drained.
Is there an [observed, inferred, or projected] decline in [area, extent and/or quality] of habitat?Yes, inferred decline in area, extent and quality of habitat in parts of the range
Are there extreme fluctuations in number of subpopulations?No
Are there extreme fluctuations in number of "locations"?
(Note: See Definitions and Abbreviations on COSEWIC website and IUCN (Feb 2014) for more information on this term.)
No
Are there extreme fluctuations in extent of occurrence?No
Are there extreme fluctuations in index of area of occupancy?No

Number of Mature Individuals (in each subpopulation)

Number of Mature Individuals (in each subpopulation)
Subpopulations (give plausible ranges)N Mature Individuals
Blue-spotted Salamander-dependent unisexuals (Nova Scotia to Ontario)Likely > 1,000,000 but large parts of the range have not been surveyed
Total> 1,000,000

Quantitative Analysis

Quantitative Analysis
Summary itemsInformation
Probability of extinction in the wild is at least [20% within 20 years or 5 generations, or 10% within 100 years].Not done

Threats (actual or imminent, to populations or habitats, from highest impact to least)

Threats (actual or imminent, to populations or habitats, from highest impact to least)
Summary itemsInformation
  1. Roads & railroads (Threat 4.1) - Road mortality during breeding migrations
  2. Logging & wood harvesting (Threat 5.3) - Wetland and terrestrial habitat alteration from forestry practices, include microhabitat degradation.

Was a threats calculator completed for this species and if so, by whom?

Yes. Leslie Anthony, Jim Bogart, Joe Crowley, Yohann Dubois, Isabelle Gauthier, Bev McBride (COSEWIC secretariat), Kristiina Ovaska, Mary Sabine

Rescue Effect (immigration from outside Canada)

Rescue Effect (immigration from outside Canada)
Summary itemsInformation
Status of outside population(s) most likely to provide immigrants to Canada.Unisexual Ambystoma do not have a status in adjoining US states (Maine, Vermont, New York, Pennsylvania, Ohio, Michigan, Wisconsin and Minnesota), but the Blue-spotted Salamander is a Threatened species in Ohio.
Is immigration known or possible?Not known but possible
Would immigrants be adapted to survive in Canada?Yes
Is there sufficient habitat for immigrants in Canada?Yes
Are conditions deteriorating in Canada?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
Yes, in some parts of the range such as southwestern Ontario
Are conditions for the source population deteriorating?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
Probably. The Blue-spotted Salamander is Threatened in Ohio based on habitat loss.
Is the Canadian population considered to be a sink?
See Table 3 ( Guidelines for modifying status assessment based on rescue effect)
No
Is rescue from outside populations likely?Not likely at any meaningful scale.

Data Sensitive Species

Data Sensitive Species
Summary itemsInformation
Is this a data sensitive species?No

Status History

Status History
Summary itemsInformation
COSEWICNot previously assessed.

Status and Reasons for Designation:

Status and Reasons for Designation:
Summary itemsInformation
StatusNot At Risk
Alpha-numeric codesNot applicable
Reasons for designationThese unusual unisexual salamanders depend on a sperm-donor species, Blue-spotted Salamander (Ambystoma laterale), that has an extensive distribution in Canada. It is found from Nova Scotia to Manitoba and from the Great Lakes to James Bay and Northern Quebec. Unisexuals that depend on this species have been identified in sites across this range and likely exist in many other sites that have not been subjected to genetic analyses. While declines have been observed and are expected for the Blue-spotted Salamander and unisexuals that depend on it in southwestern Ontario, threats are localized and expected to have little effect on the entire Canadian population.

Applicability of Criteria

Applicability of Criteria
Summary itemsInformation
Criterion A (Decline in Total Number of Mature Individuals)Not met. While there is an inferred and projected decline in the number of mature adults, the magnitude of the decline is unknown.
Criterion B (Small Distribution Range and Decline or Fluctuation)Not met. Both EOO and IAO are likely above threshold values.
Criterion C (Small and Declining Number of Mature Individuals)Not met. The population is likely much larger than 10,000 mature individuals.
Criterion D (Very Small or Restricted Population)Not met. The population is not very small or restricted.
Criterion E (Quantitative Analysis)Not estimated due to lack of data.

Preface

Unisexual Ambystoma arose 3 to 5 million years ago and share a distant maternal ancestor with a Kentucky population of A. barbouri, the Streamside Salamander (Bi and Bogart 2010). Over their range, unisexual Ambystoma share nuclear genomes (chromosomes) with three distinctly different bisexual species of Ambystoma in Canada (the Jefferson salamander, the Blue-spotted Salamander, the Small-mouthed Salamander) as well asthe Streamside Salamander, and the Eastern Tiger Salamander (A. tigrinum) in the United States. Unisexual populations of Ambystoma comprise more than 20 diploid, triploid, tetraploid, and pentaploid nuclear genomic combinations (chromosomes) from two or three of these five species (Bogart 2003; Bogart et al. 2009). All unisexual individuals have at least one Blue-spotted Salamander nuclear genome (chromosome complement) and a very similar mitochondrial DNA (mtDNA) genome that distinctly differs from mitochondrial sequences in all five species whose nuclear genomes may reside in various unisexuals (Hedges et al. 1992; Bogart 2003). This eliminates the possibility that unisexual populations of Ambystoma could have arisen from contemporary or historical hybridization events that involved females of Blue-spotted, Jefferson, Small-mouthed, or Eastern Tiger salamanders.

For reproduction, all unisexuals require sperm from a co-occurring donor and would be extirpated in concert with their sperm donating host. In the case of taxa obligatorily dependent on other taxa for all or part of their life cycles, biologically appropriate values for the host taxon should be used for assessment (see definition for "population" in COSEWIC 2015a). Small-mouthed Salamander (Ambystoma texanum) was assessed as Endangered in Canada by COSEWIC in 2004 (status confirmed in 2014) and Jefferson Salamander (A. jeffersonianum) was assessed as Endangered in Canada in 2010. Blue-spotted Salamander (A. laterale) has not been assessed by COSEWIC.

COSEWIC history

The Committee on the Status of Endangered Wildlife in Canada (COSEWIC) was created in 1977 as a result of a recommendation at the Federal-Provincial Wildlife Conference held in 1976. It arose from the need for a single, official, scientifically sound, national listing of wildlife species at risk. In 1978, COSEWIC designated its first species and produced its first list of Canadian species at risk. Species designated at meetings of the full committee are added to the list. On June 5, 2003, the Species at Risk Act (SARA) was proclaimed. SARA establishes COSEWIC as an advisory body ensuring that species will continue to be assessed under a rigorous and independent scientific process.

COSEWIC mandate

The Committee on the Status of Endangered Wildlife in Canada (COSEWIC) assesses the national status of wild species, subspecies, varieties, or other designatable units that are considered to be at risk in Canada. Designations are made on native species for the following taxonomic groups: mammals, birds, reptiles, amphibians, fishes, arthropods, molluscs, vascular plants, mosses, and lichens.

COSEWIC membership

COSEWIC comprises members from each provincial and territorial government wildlife agency, four federal entities (Canadian Wildlife Service, Parks Canada Agency, Department of Fisheries and Oceans, and the Federal Biodiversity Information Partnership, chaired by the Canadian Museum of Nature), three non-government science members and the co-chairs of the species specialist subcommittees and the Aboriginal Traditional Knowledge subcommittee. The Committee meets to consider status reports on candidate species.

Definitions (2016)

Wildlife Species
A species, subspecies, variety, or geographically or genetically distinct population of animal, plant or other organism, other than a bacterium or virus, that is wild by nature and is either native to Canada or has extended its range into Canada without human intervention and has been present in Canada for at least 50 years.
Extinct (X)
A wildlife species that no longer exists.
Extirpated (XT)
A wildlife species no longer existing in the wild in Canada, but occurring elsewhere.
Endangered (E)
A wildlife species facing imminent extirpation or extinction.
Threatened (T)
A wildlife species likely to become endangered if limiting factors are not reversed.
Special Concern (SC)
(Note: Formerly described as "Vulnerable" from 1990 to 1999, or "Rare" prior to 1990.)
A wildlife species that may become a threatened or an endangered species because of a combination of biological characteristics and identified threats.
Not at Risk (NAR)
(Note: Formerly described as "Not In Any Category", or "No Designation Required.")
A wildlife species that has been evaluated and found to be not at risk of extinction given the current circumstances.
Data Deficient (DD)
(Note: Formerly described as "Indeterminate" from 1994 to 1999 or "ISIBD" [insufficient scientific information on which to base a designation] prior to 1994. Definition of the [DD] category revised in 2006.)
A category that applies when the available information is insufficient (a) to resolve a species' eligibility for assessment or (b) to permit an assessment of the species' risk of extinction.

The Canadian Wildlife Service, Environment and Climate Change Canada, provides full administrative and financial support to the COSEWIC Secretariat.


Wildlife species description and significance

Name and classification

The taxonomic status of unisexual lineages of Ambystoma has been disputed and debated because they do not correspond to any species concept other than comprising a monophyletic mitochondrial lineage. Knowledge of their peculiarities began with Clanton (1934) who discerned, in populations that were considered to be Jefferson salamanders (A. jeffersonianum) in southern Michigan, distinctly different "dark" individuals, with a 1:1 sex ratio, and "light" individuals, all of which were females. Based on Clanton's observations and the morphological variation then thought to exist in both Blue-spotted (A. laterale) and Jefferson Salamanders, Bishop (1947) considered all these salamanders to represent a single, variable species - A. jeffersonianum. In Canada, Logier and Toner (1961) thus combined all known localities of Jefferson Salamandersand Blue-spotted Salamanders. Minton (1954) proposed that the intermediate forms were hybrids between A. laterale and A. jeffersonianum and Uzzell (1964) described the hybrids as two triploid species that were independent, self-perpetuating, clones. From the various synonyms available for A. jeffersonianum, Uzzell assigned the following species names: unisexuals with one A. laterale chromosome set and two A. jeffersonianum chromosome sets (i.e., a genomotype of LJJ) represent the Silvery Salamander (A. platineum Cope 1867) and those with two A. laterale chromosome sets and one A. jeffersonianum chromosome set (i.e., LLJ)represent Tremblay's Salamander (A. tremblayi Comeau 1943). Lowcock et al. (1987), however, demonstrated that "A. platineum" and "A. tremblayi" could not be considered valid species as many more chromosomal variants occur than just the two reciprocal triploids. A third unisexual "species," Kelleys Island Salamander, was described by Kraus (1985a) as A. nothagenes from Kelleys Island in Ohio. This species was described as a tri-hybrid Ambystoma laterale - texanum - tigrinum (i.e., LTTi), and was also believed to be a distinct evolutionary lineage (another clone). Bogart et al. (1987) demonstrated that A. nothagenus is not monophyletic and can be re-created by individual diploid A. laterale - texanum (i.e., LT) unisexuals in a single breeding season through the incorporation of A. tigrinum sperm derived from co-occurring Eastern Tiger Salamander males on Kelleys Island. Thus, unisexuals are distinct from any species of Ambystoma but are un-named. Lowcock et al. (1987) provided informal names for the known unisexuals that followed the system used by Shultz (1969) for unisexual fish of the genus Poeciliopsis. For example, a triploid unisexual possessing one Blue-spotted Salamander genome and two Jefferson Salamander genomes would be Ambystoma laterale - (2) jeffersonianum and have a moniker of LJJ.

Unisexual salamanders in the genus Ambystoma are eligible for assessment by COSEWIC because they consist of genetically distinct populations that are "wild by nature" and have been present in Canada for more than 50 years. COSEWIC requires common names for all species that are assessed. There are no official scientific and common names for the unisexual salamanders in the genus Ambystoma according to Crother (2012), the COSEWIC approved scientific authority for amphibian common names. Unisexual salamanders are mentioned in conjunction with Ambystoma jeffersonianum, "taxonomic recognition…raises complex issues dealing with discordance between cytoplasmic and nuclear genes, reticulate evolution, and genome swapping" (Crother 2012, p.23). When common names do not exist, names should be invented using protocols that are specific to the taxonomic group under consideration (COSEWIC 2015b). Although many publications include the unisexual salamanders in the Jefferson Salamander complex, some populations do not possess any Jefferson Salamander chromosomes. All of the unisexual salamanders and their sperm-donating species are included in the genus Ambystoma of the mole Salamander family Ambystomatidae. In Canada, the complex can be divided genetically and geographically into Small-mouthed Salamander-dependent, Jefferson Salamander-dependent, and Blue-spotted Salamander-dependent populations.

Morphological description

Prior to the use of genetic markers that distinguish all of the unisexual genomic combinations (i.e., genomotypes), taxonomists were frustrated by the "Jefferson Salamander complex," which, historically, included only Blue-spotted Salamanders, Jefferson Salamanders, and the unisexuals that lived with those two species. There is no distinctive unisexual morphology. The morphology of unisexual individuals reflects the genomic content of their nuclei (chromosomes from two or more species), but unisexual salamanders are morphologically variable within and between populations. Unisexuals tend to be robust, grey to blue-black salamanders with an average snout-to-vent length (SVL) of about 80 mm and with a tail that is nearly as long as the body and is laterally compressed. In breeding ponds, unisexuals are larger than Blue-spotted Salamander females but are about the same size as Jefferson Salamander females (Lowcock et al. 1992) and Small-mouthed Salamander females (Licht 1989). Their precise morphological characteristics are intermediate between the species whose chromosomes they carry. As all have at least one (haploid) set of Blue-spotted Salamander chromosomes, some degree of blue-flecking along the sides is almost always present. Unisexuals with two or more Blue-spotted Salamander chromosome complements are black with various amounts of blue flecking, and have relatively short limbs and a narrower head. Unisexuals with two or more Jefferson Salamander chromosome complements are larger, grey to brown with a small amount of blue flecking, and have relatively long limbs and a broader head. Unisexuals with two or more Small-mouthed Salamander (A. texanum) chromosome complements are grey, more slender, and have narrow heads.

Genetic identification

Both Ambystoma "platineum" and "A. tremblayi" were described as triploids by Uzzell (1964) based on finding 42 chromosomes in some Michigan unisexuals. The diploid chromosome number (2n) for bisexual species of Ambystoma is 28. Determining the ploidy of individuals was the first method that was used to distinguish bisexual and unisexual individuals. This could be accomplished by counting chromosomes and/or by estimating ploidy by comparing the sizes of erythrocytes (Wilbur 1976; Austin and Bogart 1982). More recently, genome size (and ploidy) has been estimated using flow cytometry (Lowcock et al. 1991; Lowcock and Murphy 1991; Ramsden et al. 2006). Simply knowing the ploidy, however, cannot distinguish different genomotypes. As well, diploid unisexual individuals, which were first found to exist in the complex by Bogart and Klemens (1997), would be "identified" incorrectly as belonging to bisexual species [see Ploidy reduction in Appendix 1]. Early attempts were made to identify the chromosome constituents of unisexuals by comparing the karyotypes from unisexuals with those of their sperm donors but, using standard techniques, the karyotypes are too similar and could not be used for species, or genome, identification (Taylor and Bogart 1990). Using new cytogenetic techniques, the chromosomes of each genome in a unisexual can now be identified by applying fluorescently labelled probe DNA that target species-specific chromosomes in unisexual chromosome spreads (Bi and Bogart 2006; Bogart et al. 2009).

All unisexual individuals have the same maternally inherited mitochondrial DNA (mtDNA), which is distinctly different from mtDNA sequences from any other species. Therefore, unisexuals can easily be distinguished from sympatric bisexual species by sequencing mitochondrial genes (Hedges et al. 1992; Bogart 2003; Nöel et al. 2008; Bi and Bogart 2010) or by comparing restriction fragment length polymorphisms (RFLP) of the mitochondrial genome (Spolski et al. 1992). Nuclear genetic markers must then be employed to determine the ploidy and nuclear genomes that unisexual individuals possess by reference to the genomes found in the bisexual species. For example, Jefferson Salamanders can easily be distinguished from Blue-spotted Salamanders based on the presence of alternative electrophoretic alleles (allozymes) at several isozyme loci that are mostly homozygous (p > 0.90) but have differing electrophoretic mobilities in both species. Unisexuals that co-occur with Jefferson Salamanders or Blue-spotted Salamanders have allozymes of both species and the observed staining intensity, or dosage, of the allozymes provides information on the number of Jefferson or Blue-spotted Salamander chromosomes that are present (Bogart 1982; Bogart and Klemens 1997, 2008). Isozymes have also been used to identify the genomotypes of unisexuals that possess Small-mouthed Salamander and/or Eastern Tiger Salamander genomes (Bogart et al. 1985, 1987).

Julian et al. (2003) developed primers for several microsatellite DNA loci for the Jefferson Salamander and provided fragment size ranges for loci that could also be amplified in Blue-spotted Salamanders. The primers used for amplifying nuclear genomic microsatellites at several loci amplify non-overlapping fragment sizes for the two species, and the fragments are variable enough to document the number of chromosomes in a polyploid (Ramsden et al. 2006). Using these Jefferson Salamander primers, as well as primers developed for Small-mouthed Salamander microsatellites (Williams and DeWoody 2004), it is possible to identify Jefferson, Blue-spotted, Small-mouthed and Eastern Tiger Salamanders, and all of the various unisexual genomotypes using DNA that can be extracted from a small tail tip or a toe and does not require sacrificing individuals for isozyme analyses (Bogart et al. 2007, 2009). More recently, Greenwald and Gibbs (2012) demonstrated that single nucleotide polymorphisms (SNPs) can also be used to identify bisexual and unisexual genomotypes from extracted DNA.

Population spatial structure and variability

To reproduce, all unisexual salamanders in Canada require sperm that is derived from co-occurring male Blue-spotted, Jefferson, or Small-mouthed Salamanders. Some unisexual salamanders in the United States may also obtain sperm from Eastern Tiger Salamanders (Bogart et al. 1987) or Streamside Salamanders (Bogart et al. 2009). Ambystomatids (all species in the family Ambystomatidae) are difficult to find in the terrestrial environment, so population surveys have targeted breeding ponds where adults are concentrated for a short period of time in the spring. Unisexual salamanders have been referred to as sexual parasites (Uzzell 1964; Bogart 2003) because they breed with, and derive sperm from, their bisexual hosts. In breeding ponds, unisexual salamanders typically outnumber their sexual hosts. Because unisexuals generally reproduce gynogenetically, an individual unisexual's offspring would have the same genotype as their mother and be members of the same clone (see see Appendix 1). Intra-population variability of unisexuals has been documented, however, using microsatellite multi-locus genotypes (MLGs), which identify members of the same genetic clone in populations (Bogart et al. 2007; Ramsden 2008; Nöel et al. 2011). New unisexual clones in a breeding pond may be derived from immigration, mutation, and rare genome elevation or replacement (see Appendix 1). Thus, the number of unisexual salamander MLGs vary within and between breeding ponds but is always much lower than the number of MLGs in bisexual individuals where each individual has a unique MLG.

Designatable units

Over their range, unisexual salamanders have a very similar mtDNA that is distinctly different from mtDNA sequences of all other ambystomatids (Hedges et al. 1992; Bogart 2003; Bogart et al. 2007; Bi and Bogart 2010). Therefore, unisexual salamanders cannot be considered hybrids that involve females of any contemporary species. They do, however, have chromosomal affinities with their sperm donors (Bi and Bogart 2006; Bogart et al. 2009) that can be used to distinguish three designatable units (DUs) for Canadian unisexual Ambystoma. These units correspond genetically and geographically to populations of Small-mouthed Salamander (Ambystoma texanum), Jefferson Salamander (A. jeffersonianum), and Blue-spotted Salamander (A. laterale) [see Name and Classification]. In Canada, Unisexual Ambystoma can be partitioned into a Small-mouthed Salamander-dependent population (DU1) (Figure 1), a Jefferson Salamander-dependent population (DU2) (Figure 2), and a Blue-spotted Salamander-dependent population (DU3) (Figure 3). All unisexual salamanders possess at least one Blue-spotted Salamander chromosome complement, but the other chromosome complement(s) are derived from one of the other species.

Figure 1. Small-mouthed Salamander-dependent unisexual (Ambystoma laterale - (2) texanum or LTT) from Pelee Island, Ontario. Specimen was collected as a larva by L. Licht and raised in the laboratory.
Small-mouthed Salamander-dependent unisexual
Photo: © J Bogart.
Long description for Figure 1

Photo of a Small-mouthed Salamander-dependent unisexual (Ambystoma laterale - (2) texanum or LTT) from Pelee Island, Ontario. Compared with other unisexuals, unisexuals with two or more Small-mouthed Salamander (A. texanum) chromosome complements are greyer, more slender, and have narrower heads.

Figure 2. Jefferson Salamander-dependent unisexual (Ambystoma laterale - (2) jeffersonianum or LJJ) from Hilton Falls, Ontario. Specimen collected by K. Bériault and used for radio-tracking experiments (Bériault 2005).
Jefferson Salamander-dependent unisexual
Photo: © J Bogart.
Long description for Figure 2

Photo of a Jefferson Salamander-dependent unisexual (Ambystoma laterale - (2) jeffersonianum or LJJ) from Hilton Falls, Ontario. Unisexuals with two or more Jefferson Salamander chromosome complements are grey to brown with a small amount of blue flecking. They are larger than other unisexuals and have relatively long limbs and a broader head.

Figure 3. Blue-spotted Salamander-dependent unisexual (Ambystoma (2) laterale - jeffersonianum or LLJ) from Bois de Saraguay, Montréal Island, Quebec. Specimen collected by Jean-François Desroches.
Blue-spotted Salamander-dependent unisexual
Photo: © J Bogart.
Long description for Figure 3

Photo of a Blue-spotted Salamander-dependent unisexual (Ambystoma (2) laterale - jeffersonianum or LLJ) from Bois de Saraguay, Montréal Island, Quebec. Unisexuals with two or more Blue-spotted Salamander chromosome complements are black with various amounts of blue flecking, and have relatively short limbs and a narrower head.

Recognition of DUs (see definition for "designatable unit" in COSEWIC 2015a) requires DUs to conform to criteria for discreteness and significance. The three unisexual salamander DUs are discrete and significant based on genetic characteristics that reflect deep intra-specific phylogenetic divergence and different chromosome complements. Each DU has adaptations and an ecology that is similar to that of their co-occurring sperm-donating species. Each DU is significant because it has quantitative differences in shared alleles and would suffer extirpation in concert with the extirpation of its sympatric sperm donor.

While triploid individuals are dominant, most populations also contain tetraploid unisexuals [see Ploidy Elevation in Appendix 1]. Both triploids and tetraploids would be included in their respective DUs, based on the sperm-donor species. Diploid unisexual individuals are rarely found, and where they are found, they usually exist in the same populations as triploids (Lowcock 1991; Bogart and Klemens 1997, 2008; Bogart 2003; Bogart et al. 2007). Diploid unisexuals can be included in a DU by their association with a sperm-donating species or if they are found with respective triploids. All 36 individuals sampled in one population at Mont Saint-Hilaire, in southern Quebec, were diploid LJ unisexuals (Nöel et al. 2011). No sperm donor or triploid individual was identified in the population. The Blue-spotted Salamander is the expected sperm donor in Quebec and, pending additional search effort of nearby populations, this diploid LJ population would be included in the Blue-spotted Salamander-dependent DU.

Pelee Island presents a unique situation because there are two sperm-donating species (Small-mouthed and Blue-spotted Salamanders) as well as diploid, triploid and tetraploid unisexual salamanders (Bogart et al. 1985) (Table 1). This is the only Canadian locality for the Small-mouthed Salamander-dependent population that would include LT, LTT and LTTT unisexuals that are found in sympatry with the Small-mouthed Salamander (A. texanum). Other unisexuals (LT, LLT, and LLLT) are found in the same pond with Blue-spotted Salamanders on Pelee Island but, unlike the mainland Blue-spotted Salamander-dependent DU that possesses a Jefferson salamander chromosome, all Pelee Island unisexual salamanders possess one or more Small-mouthed Salamander chromosome complements and no Jefferson Salamander chromosomes. Pelee Island also has a relatively higher frequency of diploid (LT) and symmetrical tetraploid (LLTT) unisexuals than are found elsewhere in the unisexual geographic range (see Table 1). It has been hypothesized (Bogart and Bi 2013) that the unisexuals interact with both Small-mouthed and Blue-spotted Salamanders on the island [see Ploidy Reduction and Genome Replacement in Appendix 1] and that there is no genetic discreteness or partitioning that can be applied to Pelee Island unisexuals. Including all of the Pelee Island unisexual salamanders in a single Small-mouthed Salamander-dependent DU would be consistent with the available data on the Lake Erie Island Ambystoma (Downs 1978; Bogart et al. 1985, 1987; Bogart and Licht 1986). Although Small-mouthed Salamander-dependent unisexuals also exist on mainland Ohio and extreme southern Michigan (Downs 1978; Kraus 1985b), the Canadian Small-mouthed Salamander-dependent DU is discrete because it has been isolated on Pelee Island for an extended time period.

Special significance

The first known unisexual vertebrate species, the Amazon Molly (Poecilia formosa) from Mexico and southern Texas, was described by Hubbs and Hubbs in 1932 (they named this fish in honour of a fabled human tribe of all-female warriors, not in reference to geographical location). Since then, unisexual taxa have been discovered in various genera of fish, amphibians, and reptiles from five continents (Dawley and Bogart 1989; Vrijenhoek et al. 1989) but, collectively, unisexuals constitute only about 0.1% of all extant vertebrate species (Avise 2008). Even among unisexual vertebrates, unisexual Ambystoma are evolutionarily significant. They are the oldest known unisexual vertebrate lineage (Hedges et al. 1992; Bi and Bogart 2010) and have a unique reproductive system that is described as kleptogenetic (Bogart et al. 2007); unisexual Ambystoma may also undergo gynogenetic reproduction, which appears to be the norm. Other unisexual vertebrates have more recent evolutionary histories and are: parthenogenetic and do not require sperm for reproduction (e.g., several lizard species; Vrijenhoek et al. 1989); gynogenetic, where sperm is required but only for initiating egg development (e.g., the Amazon Molly); or hybridogenetic, where the paternal genome is eliminated during meiosis and replaced by a new male genome each generation (e.g., fish in the genus Poeciliopsis; Schultz 1977).


Distribution

Global range

The northern extent of unisexual Ambystoma is central Quebec, central Ontario, and northern Minnesota. They range south to New Jersey, and northern Kentucky. From east to west, they occur from Nova Scotia to Indiana and Minnesota (Figure 4). It is very likely that the distribution of unisexuals in Figure 4 is underestimated because genetic testing is required to distinguish unisexual individuals from the species that donate sperm, and many populations have not yet been subjected to such tests. The concentration of populations that have been examined in southern Ontario and in southern New York and New Jersey (Figure 4) is an artifact of collecting effort that targeted the endangered Jefferson Salamander in Ontario and both sperm donors of conservation concern in New Jersey [A. laterale (S1) and A. jeffersonianum (S3)]. Populations that appear to be isolated in Figure 4 result from the opportunistic collection of relatively few individuals that were genetically analyzed [see Search Effort].

Figure 4. Global range of unisexual Ambystoma that have been identified using genetic markers from 1979 to 2015. The different symbols represent unisexual populations that rely on different sperm donating species that are partitioned into three designatable units (Figures 5 - 7).
Global range of unisexual using genetic markers
Photo: © Map produced by Jenny Wu of the COSEWIC Secretariat.
Long description for Figure 4

Map of the global range of the unisexual Ambystoma, as identified using genetic markers from 1979 to 2015. Different symbols indicate the three designatable units (LJJ, LLJ, and LT). The northern extent of the unisexual Ambystoma is central Quebec, central Ontario, and northern Minnesota. They range south to New Jersey, and northern Kentucky. From east to west, they occur from Nova Scotia to Indiana and Minnesota.

Canadian range

Unisexual Ambystoma have been found from Nova Scotia to Lake Superior in Ontario (Figure 4). The ranges of unisexuals that rely on Small-mouthed Salamander (Figure 5) or Jefferson Salamander (Figure 4) are restricted to southern Ontario and are relatively well studied [see Search Effort]. Blue-spotted Salamanders have an extensive distribution in eastern Canada (Cook 1984), and comparatively few populations have been analysed for the presence of unisexual individuals, so the distribution of Blue-spotted Salamander-dependent unisexuals (Figure 7) is not well understood.

Figure 5. Global range of Small-mouthed Salamander-dependent unisexual Ambystoma that rely on the Small-mouthed Salamander (A. texanum) as a sperm donor. These populations contain individuals that possess one or more Blue-spotted Salamander, and at least one Small-mouthed Salamander chromosome complements (i.e., LT and LTT).
Global range of Small-mouthed Salamander-dependent unisexual
Photo: © Map produced by Jenny Wu of the COSEWIC Secretariat.
Long description for Figure 5

Map of the global range of the Small-mouthed Salamander-dependent unisexual Ambystoma, which rely on the Small-mouthed Salamander (A. texanum) as a sperm donor. These populations contain individuals that possess one or more Blue-spotted Salamander complements and at least one Small-mouthed Salamander chromosome complement (that is, LT and LTT). In Canada, the range of such unisexuals is restricted to southern Ontario.

Figure 6. Global range of Jefferson Salamander-dependent unisexual Ambystoma that rely on the Jefferson Salamander (A. jeffersonianum) as a sperm donor. These populations contain individuals that normally possess one Blue-spotted and two Jefferson Salamander chromosome complements (i.e., LJJ).
Global range of Jefferson Salamander-dependent unisexual
Photo: © Map produced by Jenny Wu of the COSEWIC Secretariat.
Long description for Figure 6

Map of the global range of the Jefferson Salamander-dependent unisexual Ambystoma, which rely on the Jefferson Salamander (A. jeffersonianum) as a sperm donor. These populations contain individuals that normally possess one Blue-spotted and two Jefferson Salamander chromosome complements (that is, LJJ). In Canada, the range of such unisexuals is restricted to southern Ontario.

Figure 7. Global range of Blue-spotted Salamander-dependent unisexual Ambystoma that rely on the Blue-spotted Salamander (A. laterale) as a sperm donor. These populations contain individuals that normally possess two Blue-spotted, and one Jefferson Salamander chromosome complements (i.e., LLJ).
Global range of Blue-spotted Salamander-dependent unisexual
Photo: © Map produced by Jenny Wu of the COSEWIC Secretariat
Long description for Figure 7

Map of the global range of the Blue-spotted Salamander-dependent unisexual Ambystoma, which rely on the Blue-spotted Salamander (A. laterale) as a sperm donor. These populations contain individuals that normally possess two Blue-spotted and one Jefferson salamander chromosome complements (that is, LLJ). Blue-spotted Salamanders have an extensive distribution in eastern Canada, but comparatively few populations have been analysed for the presence of unisexual individuals, so the distribution of Blue-spotted Salamander-dependent unisexuals is not well understood.

Extent of occurrence and area of occupancy

Unisexual salamanders require a sperm donor for reproduction, and unisexual salamanders are found in all Canadian ponds where Small-mouthed Salamanders or Jefferson Salamanders breed. Unisexual Ambystoma have, however, been found in ponds without a sperm donor (COSEWIC 2010) (e.g., Kitchener Site 2, Table 1). For wildlife species dependent on other species, the use of biologically appropriate values for the host taxon is recommended (Appendix C in COSEWIC 2015); for Unisexual Ambystoma, the host taxa are the sperm-donor species. The Small-mouthed Salamander (A. texanum) was calculated to have an extent of occurrence (EOO) of 43 km2 and an index of area of occupancy (IAO) of 12 km2 (COSEWIC 2014). That EOO estimate was based on the area of Pelee Island, which is ~ 43 km2, and the IAO was based on overlaying 2x2 km grid cells on sites where salamanders were found on the island (COSEWIC 2014). Using a minimum convex polygon that eliminated two historical sites, an EOO of 20 km2 was calculated by the COSEWIC Secretariat for Small-mouth Salamander-dependent unisexuals. Because the IAO cannot be greater than the EOO, the IAO must also be 20 km2.

The EOO and IAO for Jefferson Salamander were, respectively, 6,913 km2 and 196 km2 (COSEWIC 2010). The EOO and IAO for Jefferson Salamander-dependent unisexuals was calculated as 24,626 km2 and 748 km2, respectively, using both historical and recent records. Values for Jefferson Salamander and Jefferson Salamander-dependent unisexuals should be the same because the unisexuals require the presence of Jefferson Salamanders for successful reproduction. There may be some sampling bias, because it is easier to find the more abundant unisexuals, and these salamanders live a long time (~ 30 years) [see Biology - Life Cycle and Reproduction], and may exist in ponds with no chance for recruitment. Based on the fact that Jefferson Salamander-dependent unisexuals require Jefferson Salamanders to reproduce, the EOO and IAO for Jefferson Salamander-dependent unisexuals is deemed to be the same as calculated from the most recent data for Jefferson Salamander. New calculations for Jefferson Salamander, using recent data (2004 - 2015), provide estimates for an EOO of 9,457 km2 and an IAO of 188 km2.

Blue-spotted Salamander has an extensive range in Canada, and relatively few ponds have been examined for the presence of Blue-spotted Salamander-dependent unisexuals. Unisexuals have, however, been found in Blue-spotted Salamander populations across the range, providing an EOO calculation of 671,668 km2. Using 2x2 km grids, the IAO was calculated to be 1,932 km2. It is unlikely that these unisexuals would only exist in distant and isolated populations (e.g., the northern populations in Ontario and Quebec). Thus, the IAO must be considered to be an underestimate, and the known EOO might also increase when more data are obtained.

Search effort

Salamanders in the bisexual-unisexual complex are not easily distinguished without genetic analysis. Techniques for the genetic identification of these salamanders were initiated at the University of Guelph in the late 1970s. From that time, biologists from the United States and Canada have sent specimens to Guelph for genetic confirmation. At first, the identifications were curiosity-driven, and later collections were driven by need-to-know conservation concerns from areas where a sperm-donating species received a conservation status. Initially, unisexual salamanders were considered to be rare "hybrid individuals." Mitochondrial DNA sequences revealed that unisexuals are not hybrids (Hedges et al. 1992) and unisexuals were found to be more common and more numerous than the sympatric bisexual species they live with over much of their range (Bogart and Klemens 1997). In fact, very few populations were found to be devoid of unisexuals [e.g., Long Island, New York (Bogart and Klemens 1997); Prince Edward Island (Lowcock 1989); populations in central Pennsylvania and western New York (Bogart and Klemens 2008)].

In Canada, unisexuals outnumber bisexual individuals in populations of Small-mouthed Salamanders and Jefferson Salamanders(Table 1), so random surveys in breeding ponds are usually sufficient to confirm the presence of unisexuals. Sampling of Small-mouthed Salamander-dependent unisexuals on Pelee Island was mostly conducted from 1983 to 1995 by Dr. Lawrence Licht (see COSEWIC 2004) (Table 1). Most search effort in Ontario has been expended to understand the range and habitat of Jefferson Salamander and its associated unisexual because developers and aggregate companies were required to know where Jefferson Salamander, listed under SARA since 2003, exists. Biologists hired by consultant companies (e.g., Ecoservices, LGL, NRSI) and biologists from the OMNRF send tissue samples to the University of Guelph for genetic analysis of individuals that they have sampled. The identifications and localities are considered to be sensitive information by the consultants and the OMNRF but can be used for research purposes and by the Jefferson Salamander Recovery Team. The data are important for status assessments by COSEWIC and are included in Table 1 as unpublished, as well as in EOO and IAO calculations and maps. Much less effort has been expended on surveys for Blue-spotted Salamanders and associated unisexuals. In Ontario, consultants and members of the Jefferson Salamander Recovery Team collect samples from areas close to the range of Jefferson Salamander to document the "absence" of Jefferson Salamanders (e.g., Cambridge population in Table 1). The density of unisexuals that co-occur with Blue-spotted Salamanders is more variable over their range. High unisexual/bisexual ratios are found in some southern Ontario populations (Table 1) and in southern Quebec (Nöel et al. 2011). Lowcock et al. (1991) found a decrease in the proportion of unisexuals in populations of Blue-spotted Salamandersfrom south to north in central Ontario. Sampling the same population in Algonquin Provincial Park yielded only Blue-spotted Salamanders in 2010, but a small number of unisexuals were found in 2011 (Table 1).

Thus, compared with known ranges of Small-mouthed Salamander-dependent and Jefferson Salamander-dependent unisexuals, the Canadian range of Blue-spotted Salamander-dependent unisexuals is poorly understood but is not completely unknown. Blue-spotted Salamander-dependent unisexuals were reported from Nova Scotia by Gilhen (1978) and from New Brunswick by Cook and Gorham (1979). Collections were made by Les Lowcock in the Maritime Provinces, southern Quebec, and central Ontario (Lowcock 1989, 1991) and several other collections have been made by Jean-François Desroches in Quebec (see also Nöel et al. 2008, 2011). Bisexual and unisexual salamander identifications were included in a general herpetological survey in southern Ontario performed by the Hamilton Field Naturalists (Lamond 1994). That survey identified unisexual individuals and their sperm donors from a large number of populations in southern Ontario. Blue-spotted Salamanders and associated unisexuals were sampled at Rondeau Provincial Park in the Municipality of Chatham-Kent on the north shore of Lake Erie, as well as populations in Algonquin Provincial Park and the Haliburton area in Nipissing District (Table 1).


Habitat

Habitat requirements

It is assumed that unisexual Ambystoma use the same habitat as their sperm donors. These salamanders are found near or within deciduous or mixed-wood upland forests (Klemens 2000) containing suitable breeding ponds. These sites include limestone sinkhole ponds, kettle ponds, and other natural basins (Nyman 1991). Breeding ponds are devoid of predatory fish, often ephemeral, and are filled by spring runoff, groundwater, or springs. Unisexual salamandersand sympatric bisexuals spend the winter underground below the frost line. Salamander breeding ponds must contain attachment sites for eggs, and ephemeral ponds must exist for the duration of larval development. Eggs are normally attached to submerged twigs or branches, but submerged riparian vegetation or emergent grasses and sedges may also be utilized. Blue-spotted Salamanders and Small-mouthed Salamanders lay eggs singly or in small groups (Petranka 1978). Unisexuals lay eggs in masses of 20 to 50 eggs that are similar to the egg masses laid by Jefferson Salamanders (Bogart 1982). Prey items in ponds include a variety of invertebrates as well as other amphibian larvae or tadpoles.

Bériault (2005) modelled habitat quality, water quality, and micro- as well as macro-habitat used by Jefferson and Blue-spotted Salamanders. All of her study sites contained respective Jefferson Salamander-dependent unisexuals and Blue-spotted Salamander-dependent unisexuals, and no distinction was made between the bisexual and unisexual individuals. She found that ambystomatid larvae were not particularly susceptible to relatively low pH or other parameters of water chemistry, water depth, temperature, or quality in Ontario ponds. Success of larvae might be affected by reduced availability of prey items that are more susceptible to low pH than are the salamander larvae themselves (Sandinski and Dunson 1992).

Other than the few days spent in the breeding pond, adults live and forage in deciduous or mixed woodlands. Mole Salamanders are seldom seen on the forest floor except when they are migrating to or from a breeding pond. Most of the information on the terrestrial ecology of ambystomatids has been derived from experiments that employed radio transmitters that are inserted in the body cavity of tracked individuals. Faccio (2003) tracked Jefferson and Spotted Salamanders in Vermont. It is possible that some of the individuals that Faccio tracked were Jefferson Salamander-dependent unisexuals because Jefferson Salamanders and unisexuals co-occur in Vermont (Bogart and Klemens 1997), but four of the eight Jefferson Salamanders he tracked were males. Salamanders use horizontal burrows in the summer, but in winter use vertical fissures and burrows (Faccio 2003).

In Canada, Jefferson Salamander-dependent unisexuals have been radio-tracked (Bériault 2005).The habitat includes terrestrial areas 1 km or more from a breeding pond, and a "core area" with a radius of at least 300 m around the breeding pond. Microhabitats included small mammal burrows, rock fissures, tree stumps, leaf litter, logs, and woody debris on the forest floor. The tracked salamanders utilize deep rock fissures and small mammal burrows (Bériault 2005). Currently, a 1 km radius around breeding ponds is protected for Jefferson Salamander and associated unisexuals [see Protection Status and Ranks] to allow for population expansion, immigration and dispersal. Prior to 2010, planning authorities were using a 30 m "buffer" around breeding ponds, and substantial foraging and overwintering habitat has been lost. These losses are reflected in reduced population sizes and the disappearance of entire populations at some historical sites [see Fluctuations and Trends].

Habitat trends

Habitat for Jefferson and Blue-spotted Salamander-dependent unisexualsin southern Ontario is restricted to fragmented woodlands and marginal agricultural land. Development activities associated with urbanization, aggregate extraction, and resource development lead to an ongoing loss of suitable habitat, and an increase in habitat fragmentation with attendant population isolation. In addition to direct habitat loss, resource development can alter the water table or affect groundwater flow, which adversely affects moisture regimes in adjacent wetlands and soil substrates. The decline or loss of foraging and overwintering habitat of Jefferson Salamander populations is attributed to wetland draining and resource development (COSEWIC 2010). These changes can shorten the hydroperiod of ephemeral ponds and thereby lead to a loss of suitable habitat. Decline, degradation, and loss of breeding ponds have been documented for Small-mouthed Salamanders and associated unisexuals on Pelee Island (COSEWIC 2004) [see Threats].


Biology

The general biology of Small-mouthed, Jefferson, and Blue-spotted Salamandershas been summarized by Downs (1989) and Petranka (1998) and on websites (e.g., NatureServe 2014 and AmphibiaWeb 2014). Life history observations have been made in some populations where unisexuals co-occur with these species and may not even be distinguished (e.g., Weller 1980). In general,it is assumedthatunisexuals mimic the normal, observable, behaviour of female larvae, juveniles, and adults of the co-occurring sperm-donating species.

Life cycle and reproduction

The courtship of unisexual salamanders with Small-mouthed and Blue-spotted Salamander males on Pelee Island has been described (Licht 1989; Licht and Bogart 1990). Courtship of Jefferson Salamanders was described by Mohr (1931). Once in the ponds, males will court females and then deposit spermatophores on the substrate (e.g., leaves, sticks) on the bottom of the pond. The female will pick up a spermatophore with her cloacal "lips" and, within 1-2 days, will lay several clutches of approximately 30 eggs each on stems or submerged vegetation near the periphery of the pond (Brodman 1995). Although male Jefferson Salamanders will court both Jefferson and unisexual females, Dawley and Dawley (1986) showed that Jefferson Salamander males can discriminate between Jefferson Salamander females and unisexual females and that the males used in their experiments preferred Jefferson Salamander females. Blue-spotted and Jefferson Salamander males amplex females during courtship, but amplexus is not part of the courtship of Small-mouthed Salamander males on Pelee Island (Licht and Bogart 1990).

The persistence of unisexuals with their sperm donors could be related to an ambystomatid breeding strategy that involves sperm competition. Male ambystomatids are generally more common than females in breeding ponds that do not have unisexuals and they produce many more spermatophores than would be required to sustain the population. In some species (e.g., the Spotted Salamander), spermatophore fields that contain several hundred spermatophores can be observed in breeding ponds and males deposit spermatophores on top of rival males' spermatophores (Petranka 1998). Small-mouthed Salamanders deposit spermatophores relatively randomly when males and females are in proximity (Licht and Bogart 1990). Jefferson Salamander and Blue-spotted Salamander males engage in courtships that allocate spermatophores to courted females, but males still produce many more spermatophores than are required (~20 per courted female) and twice as many spermatophores when they are courting conspecific females as they do when they court unisexuals (Uzzell 1969). It has been proposed that unisexual Ambystoma might affect population densities of their sperm donors. Clanton (1934) hypothesized that spermatophores could be limiting in unisexual dominated populations and that females of the sperm-donor species might lose out to unisexual females, which would continually reduce the population of the sperm donor until there was no longer any recruitment. Because the salamanders on Pelee Island have been isolated on that Island for about 5,000 years (Calkin and Feenstra 1985), they likely represent an equilibrium condition for unisexual salamanders that live with bisexual sperm donors. The percentage of bisexual and unisexual salamanders on Pelee Island (Table 1) is similar to that found in mixed bisexual/unisexual populations on the mainland.

Based on growth rates and sizes of first-time breeders in a southern Ontario pond, Weller (1980) estimated that male Jefferson Salamanders return to the breeding pond 22 months after metamorphosis. Female Jefferson Salamanders and unisexuals, however, required 34 months or more before returning. There is also evidence that Small-mouth Salamander-dependent unisexuals generally take longer to reach sexual maturity than do Small-mouthed Salamander females (Licht and Bogart 1989). Triploid Blue-spotted Salamander-dependent unisexuals also take a longer time to reach sexual maturity than Blue-spotted Salamanders; tetraploid unisexuals require an additional year (Lowcock et al. 1992). Weller (1980) found that the breeding frequency varied among individual salamanders. Of 26 male Jefferson Salamanders that arrived at and left the breeding pond in the first year of his study, 12% returned in each of the next four years, 4% did not return until 4 years later, and the remainder returned to the pond and skipped years in various combinations. Females, including both Jefferson Salamanders and Jefferson Salamander-dependent unisexuals, followed a similar pattern with 10% of 206 females returning each year, 6% not returning until four years later, with the remaining females returning or skipping years in various combinations.

High egg mortality, observed in many egg masses in a breeding pond, often signifies the presence of unisexual Ambystoma (Petranka 1998). Piersol (1910) observed high egg mass mortality in a Toronto, Ontario, pond that was probably a Jefferson Salamander population with a high frequency of unisexual individuals, and Clanton (1934) mentioned egg mortality in southern Michigan where bisexual and unisexual salamanders co-occurred. The embryonic period from egg deposition to hatching varies from 3 to 14 weeks in the unisexual/bisexual complex and is dependent on the seasonal time of egg deposition and water temperature (Smith 1983), with an average of about 28 days (Brodman 1995) in a northern Ohio population of Jefferson Salamanders and associated unisexuals. An embryonic survival rate of 60-88% was reported for the Jefferson Salamander by Cook (1983) from five Massachusetts ponds. In contrast, Small-mouthed Salamander-dependent unisexual eggs typically have a very low embryonic survival rate (16%) (Bogart and Licht 1986).

When hatched, larvae feed on zooplankton until they are large enough to feed on larger invertebrates that include nematodes, water mites, cladocerans, copepods, collembolans, mosquito larvae, chironomid larvae, snails, and assorted insects (Smith and Petranka 1987). Larvae are often cannibalistic and will also feed on larvae of sympatric species of Ambystoma (Brandon 1961; Smith and Petranka 1987). The larval period varies from 2 to 4 months and is likely related to water temperature, available food, and hydroperiod (Downs 1989). In Ontario, transformation has been observed from mid-July to mid-September (Bogart pers. obs.). By early November, juveniles have an average total length of 62 mm (Downs 1989). Based on studies in Maryland (Thompson et al. 1980), Ohio (Downs 1989), and Illinois (Mullen and Klueh 2009), pre-metamorphic survival rates and recruitment rates are believed to be very low (0 to 0.7%) and little is known about the ecology of juveniles. Downs (1989) reported that juveniles could be found as far as 92 m from the breeding pond in a 10-day period.

In a mark-recapture study, Downs (1989) estimated that 10-18% of adults survive a 3-year period. Weller (1980) estimated an extremely high, annual adult survivorship (0.981 for females (including unisexuals) and 0.883 for male A. jeffersonianum). Using skeletochronology, Flageole and Leclair (1992) documented that most of the salamanders in the population under study were between 2 and 18 years of age but some live as long as 32 years. Evidence for longevity of unisexual salamanders comes from the following observation of L. Licht: "An individual salamander (presumably LJJ) which was collected from a breeding pond near Hamilton, Ontario in spring of 1988 is still alive as of this writing. Assuming an age of 3 years to reach sexual maturity and breed, this salamander is now at least 30 years old" (Licht pers. comm. 2015).

Generation time was calculated for the Jefferson Salamanders as 11 years based on the formula: age at maturity + 1/mortality, where mortality = annual rate of mortality of adults (Downs 1989). The mortality rate was estimated from data provided for Jefferson Salamanders and its associated unisexuals (Weller 1980; Downs 1989) as the mean of 2, 12 and 27% = 14%. Thus, generation time = 4 + 1/0.14 = 11 years. Mortality rates have not been calculated for populations of Small-mouthed Salamander-dependent or Blue-spotted Salamander-dependent unisexuals and must vary with respect to different threats to adult survival (e.g., roads and road traffic close to breeding ponds). Small-mouthed salamanders were estimated to have a generation time of 3 years (COSEWIC 2004) based only on the estimated average age of breeding adults and no mortality. Small-mouthed Salamander-dependent and Blue-spotted Salamander-dependent unisexuals take a longer time to reach sexual maturity than the bisexuals (Licht and Bogart 1989; Lowcock et al. 1992), and adults are expected to have some unknown mortality rate. A generation time of approximately 8 years would be more realistic for these unisexuals.

Physiology and adaptability

Similar to most amphibians, unisexual Ambystoma have skin that is permeable to water and oxygen. To avoid desiccation and anoxia, juveniles and adults normally occur in cool, damp environments and surface movement is restricted to rainy, or humid, nights. Over their range, unisexual Ambystoma time their breeding activities to coincide with their sperm donors, which are often the earliest seasonal breeders among salamanders (Petranka 1998) and are active at < 1oC (Feder et al. 1982). Migration and breeding often occur when ponds are ice-covered and before the ground has completely thawed (Bogart pers. obs.). Unisexuals are not known to possess cryoprotectants. Frozen adults and eggs normally die (Pisapio and Bogart unpubl. data).

Although the poison that is present in the skin of bisexual or unisexual Ambystoma species has not been analyzed, it is suspected of being important as an anti-predator defence. Poison glands are especially concentrated in the skin on the dorsal surface of the tail. When confronted with a possible predator or during manipulation by a human, a salamander will present and elevate its tail towards the threat. Waving the tail and oozing poison are typical responses to a predator (Ducey and Brodie 1983; Brodie 1989).

Dispersal and migration

In southern Ontario, there are two periods of movement for unisexual salamanders and their sperm donors: dispersal of newly metamorphosed juveniles from ponds to surrounding forest, which normally takes place in July and August, and migration of adults from overwintering sites to and from breeding ponds that takes place each spring (late March to mid-April).

Migratory distance from the breeding pond to surrounding terrestrial habitat for Jefferson Salamander-dependent unisexuals can exceed 1 km (Bériault 2005), but the distance travelled varies among individuals and populations. Ninety percent of radio-tracked adults reside in suitable habitat within 300 m of the breeding pond (Bériault 2005). During migratory movements, salamanders may traverse terrestrial habitat that would not be considered suitable habitat, such as agricultural fields, plantations, and roads. Because unisexual adults and juveniles move only on rainy or humid nights, they may be found in such habitats when conditions are not suitable to complete their migration. Pond fidelity, where individuals continually return annually to the same pond for breeding, has not been studied for unisexual Ambystoma but has been confirmed for several species of Ambystoma, such as Spotted Salamanders (Schoop 1965), Jefferson Salamanders (Douglas and Monroe 1981), and Mole Salamanders (A. talpoideum; Raymond and Hardy 1990).

Interspecific interactions

Over the range of unisexual Ambystoma, the co-occurring sperm-donating species of Ambystoma have similar attributes and share similar habitats. Larval ambystomatids eat other larval ambystomatids, but it is not known if unisexuals can choose their prey or distinguish between bisexual and unisexual larvae. Predation by larval Marbled Salamanders (A. opacum) on bisexual and unisexual larvae may significantly reduce survivorship (Cortwright 1988). Marbled Salamander larvae are larger because they are fall, rather than spring breeders. They do not occur in Canada but co-exist with unisexuals in mainland Ohio and on Kelleys Island, Ohio. Spotted Salamanders co-occur with unisexual salamanders in many Quebec and mainland Ontario populations. Nyman (1991) observed ecological partitioning of Spotted Salamander and unisexual larvae in New Jersey.Eastern Newts (Notopthalmus viridescens) are also commonly found breeding in the same ponds over the range of unisexuals. There is no indication that these species have a serious impact on unisexual salamanders, but data that address possible competition are not available.


Population sizes and trends

Sampling effort and methods

Populations of ambystomatid salamanders are sampled effectively using drift fences combined with pit fall traps in spring, when the adults enter breeding ponds (Heyer et al. 1994); they can also be trapped in the breeding ponds with minnow traps (Figure 8) (Table 1). Small tissue samples are taken for DNA extractions, and the salamanders are set free. Prior to 2004, before DNA methods were employed, a pond was designated as a breeding pond for members of the bisexual/unisexual complex if at least a few individuals were genetically confirmed, using isozymes (Bogart 1982). Individuals had to be sacrificed for isozyme analyses so it was not acceptable to determine the absolute frequencies of bisexual and unisexual individuals in populations or to estimate trends over time. Estimates of bisexual/unisexual frequencies were obtained for a few populations of Blue-spotted and Blue-spotted Salamander-dependent unisexuals based on ploidy that was determined with a small blood sample using flow cytometry (Lowcock et al. 1991, 1992) (Table 1). Since 2004, microsatellite DNA loci have provided a better method for genetic testing (Ramsden et al. 2006; Bogart et al. 2007) because many individuals can be safely genotyped in a relatively short period [see Genetic Identification], but trends have only been estimated for very few populations based on observed numbers of egg masses over time. Continual effort by Jefferson Salamander Recovery Team members have resulted in surveys of new and historical breeding ponds in Ontario to find new occupied ponds [see Search Effort] and to estimate population trends over time.

Figure 8. Salamanders are collected using minnow traps at Hilton Falls Conservation Area in late March when the ice recedes from the margin of the pond. This trap contains Jefferson Salamanders, Jefferson Salamander-dependent unisexuals, and Spotted Salamanders (A. maculatum).
Salamanders are  collected using minnow traps
Photo: © J Bogart.
Long description for Figure 8

Photo of a minnow trap being inspected for salamanders at Hilton Falls Conservation Area in late March (the ice has receded from the margin of the pond).

Table 1. Genomotype frequencies found in ontario subpopulations of unisexual Ambystoma where adequate sample sizes are available to estimate frequency distributions of bisexuals and diploid or polyploid unisexuals. frequencies are provided in numbers of individuals of each genomotype and the percentage in the subpopulation (in parentheses). all unisexual genomotypes have at least one A. laterale (l) chromosome complement and one or more A. jeffersonianum (j) or A. texanum (t) complements or genomes. diploids have 2, triploids have 3, tetraploids have 4, and pentaploids have 5 chromosome complements.

Table 1a. Small-mouthed Salamander-dependent unisexual
Population(n)LLTTLTLLTLTTLLLTLTTTLLTTSource
Pelee Island Table Footnote a128783 (6.4)191 (14.8)272 (21.1)474 (36.8)209 (16.2)22 (1.7)19 (1.5)17 (1.3)COSEWIC (2004)
Table 1b. Jefferson Salamander-dependent unisexual
Subpopulation(n)JJLJJLJJJLLJJLLJJJSource
Kitchener (site 1) Table Footnote b14212 (8.45)111 (78.17)19 (13.38)00LGL 2007 (unpubl. data)
Kitchener (site 1) Table Footnote b19115 (7.85)139 (72.77)36 (18.85)00LGL 2008 (unpubl. data)
Kitchener (site 2) Table Footnote b46038 (82.6)5 (10.87)2 (4.35)1 (2.17)NRSI 2009 (unpubl. data)
Kitchener (site 2) Table Footnote b16020 (95.24)01 (4.76)0NRSI 2015 (unpubl. data)
Hilton Falls Conservation Area Table Footnote b520168 (32.3)337 (64.8)15 (2.88)00Ramsden (2004)
Waterdown Table Footnoteb11811 (9.32)103 (87.29)4 (3.39)00OMNR 2007 (unpubl. data)
Erindale Table Footnote c2865426 (14.9)2439 (85.13)   Weller (1980)
Table 1c. Blue-spotted Salamander-dependent unisexual
Subpopulation(n)LLLJLLJLLLJLLLLJSource
Cambridge Table Footnote d12417 (13.7)6 (4.8)99 (79.8)2 (1.61)0Ecoservices 2007 (unpubl. data)
Rondeau Provincial Park Table Footnote e7225 (34.7)8 (11.11)37 (51.39)2 (2.78)0S. Dobbyn, 2004 (unpubl. data)
Algonquin Provincial Park Table Footnote d6363 (100.0)0000Wildlife Research Station, 2010 (unpubl. data)
Algonquin Provincial Park Table Footnote d131121 (92.4)010 (7.63)00Wildlife Research Station, 2011 (unpubl. data)
Haliburton Beaver Pond Table Footnote b2646650 (24.6)01714 (64.78)279 (10.54)3 (0.1)Lowcock (1991)

Table Footnote

Footnote 1

On Pelee Island, adults and larvae were dip-netted from breeding ponds and larvae were raised. Larvae were also raised from egg masses collected in the breeding ponds.

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Footnote 2

Salamanders were collected using minnow traps placed in the breeding pond as well as drift fences with pit-fall traps that surrounded the breeding pond.

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Footnote 3

Salamanders were collected using drift fences around the breeding pond. This study only distinguished males and females. The number of Jefferson Salamanders (JJ) were derived by doubling the number of males and assumed a 1:1 sex ratio.

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Footnote 4

Only minnow traps were used to collect salamanders.

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Footnote 5

Salamanders were found using cover board arrays.

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Abundance

Because of the difficulty distinguishing unisexual salamanders from their co-occurring sperm-donating species, only a few studies have genetically identified large numbers of individuals in subpopulations to estimate comparative abundance of bisexual and unisexual individuals (Table 1). About 80% of 1287 salamanders sampled on Pelee Island were Small-mouthed Salamander-dependent unisexuals. Jefferson Salamander-dependent unisexuals outnumber Jefferson Salamanders in all known Ontario populations, and there are populations where only unisexual individuals have been found. The lack of Jefferson Salamanders in these populations is likely a reflection of sampling effort and the much higher density of unisexual salamanders. In three separate studies that involved sample sizes > 100 individuals, the percentage of Jefferson Salamander-dependent unisexuals ranged from ~67 to 92% of sampled individuals. Blue-spotted Salamander-dependent unisexuals made up 75% of 2646 salamanders from a pond in the Haliburton area, Ontario, but were not found in some other Ontario populations.

There are no robust estimates of the number of adults in any of the three DUs. The Small-mouthed Salamander-dependent population is probably very small, possibly less than 1000 adults, based on the low number of breeding ponds and limited capture data. There may be < 2500 adult Jefferson Salamanders (COSEWIC 2010). Jefferson Salamander-dependent unisexuals are more numerous than their sperm donors and constitute 60% to 95% of subpopulations, resulting in < 10,000 adult unisexuals. There is much uncertainty associated with the population size of Blue-spotted Salamander-dependent unisexuals, but the population is undoubtedly very large, possibly > 100,000 adults.

Fluctuations and trends

In general, Mole Salamanders (Ambystoma sp.) are assumed to be fairly long-lived (~ 30 yrs) [see Life Cycle and Reproduction]. Therefore, unisexuals likely have several breeding opportunities over their lifetime that may compensate for extrinsic factors such as a cold snap that freezes eggs or a dry spring and summer that evaporates vernal pools and kills larvae. Fluctuations in the number of breeding adults in any year could be related to the cohorts of previous "good" and "bad" years for recruitment. Trends in population density and inferences on presence/not detected data can only be estimated through repeated yearly surveys of the same ponds combined with surveying several ponds in the same year.

From repeated surveys within about a 15-year time frame (1990 to 2005) in Ontario, no population of Jefferson Salamanders was estimated to be larger than originally found. Most populations were declining and some are probably extirpated. There are now fewer than 33 known extant subpopulations (defined here as equivalent to number of known, extant breeding ponds) that still maintain Jefferson Salamanders and their associated unisexuals. A few new subpopulations have been found since 2000, but the continued existence of about 25 historical subpopulations cannot be confirmed. There are few or no egg masses in many ponds that formerly had many egg masses. Some historical ponds have been stocked with predatory fish, some no longer hold water for the required time for larval development, and some have been lost to development (COSEWIC 2010).

Annual observations document a severe reduction in number of egg masses from hundreds in 1979 to fewer than ten in 2006, suggesting a population decline of over 90% over this period for the Jefferson Salamander and its associated unisexuals; the majority of known sites (over 20 ponds) were sampled (Bogart pers. obs.). Weller (1980) estimated that the population at his study site in Peel Region contained 80 breeding males and about 838 breeding females (mostly unisexuals). His study recorded the actual number of individuals captured while migrating to the breeding pond. The numbers diminished over the three years of his study from 624 in 1975 to 513 in 1976 to 324 in 1977. In 2003 and 2004, researchers surveyed historically known breeding sites along the Niagara Escarpment that were documented in 1990 and 1991. Eighteen sites were searched for Jefferson Salamander and Jefferson Salamander-dependent unisexual egg masses by staff from Ontario's Niagara Escarpment (ONE) Monitoring Program. Only three sites were confirmed to have Jefferson Salamanders and Jefferson Salamander-dependent unisexuals (COSEWIC 2010). Only a few of the documented subpopulations of Jefferson Salamanders and their associated unisexuals in Ontario that have been repeatedly surveyed have been stable over a relatively long period based on surveys performed in 1979, 1981, 1990 (NHIC 1998), and 2003-2005 (Bériault 2005; Ramsden 2008).

Similar survey data are not available for Small-mouthed Salamanders or Blue-spotted Salamanders and their associated unisexuals. Habitat for the Blue-spotted Salamanders has been lost in developed areas and in areas where wetlands have been drained in Ontario and Quebec but documentation of the presence or abundance of this salamander over time are not available. The last surveys that assessed Small-mouthed Salamanders and associated unisexuals on Pelee Island were done in the 1980s (COSEWIC 2004), but a survey is currently (2015) underway on the island by Dr. Dennis Murray and his students from Trent University.

Rescue effect

The Pelee Island Small-mouthed Salamander-dependent unisexuals exist on an isolated island with no chance for rescue from Ohio or Michigan where Small-mouthed Salamander-dependent unisexuals exist in small isolated populations (Figure 5). The closest U.S. populations of Jefferson Salamanders and Jefferson Salamander-dependent unisexuals are in Cattaraugus and Wayne counties in New York (Bogart and Klemens 2008) (Figure 6). Considering the limited movements of these salamanders, current distribution, and barriers to dispersal, rescue from the U.S. is highly improbable. Most Blue-spotted Salamander-dependent unisexuals likely occur in Canada (Figure 4), but these salamanders are also present in US states that border Canada from Maine to Minnesota, so there are several areas where dispersal into Canada from the US is possible.


Threats and limiting factors

Limiting factors

The presence of unisexual Ambystoma populations is limited by the presence of an acceptable sperm donor that co-occurs in the same breeding pond.

Threats

The threat classification below is based on the IUCN-CMP (World Conservation Union-Conservation Measures Partnership) unified threats classification system (see Master et al. 2009 and CMP 2010 for details). Threats may be observed, inferred, or projected to occur in the near term. Threats are characterized in terms of scope (usually within the next 10 years), severity (within next 10 years or 3 generations, whichever is longer), and timing (ongoing or predicted). Threat "impact" is calculated from scope and severity. Impact ratings for the three DUs of unisexual salamanders are shown in Table 2; see Appendices 2 - 4 for full spreadsheets). The threats for each DU are described below in their approximate perceived order of importance.

Table 2. Summary of threat impact ratings for three designatable units of unisexual Ambystoma, according to assessment conducted on 2 February 2015. See Appendices 2 - 4 for full threat calculator spreadsheets.
ThreatThreatSmall-mouthed Salamander-dependent DUJefferson Salamander-dependent DUBlue-spotted Salamander-dependent DU
1Residential & commercial developmentLowHighNegligible
1.1Housing & urban areasLowHighNegligible
1.2Commercial & industrial areasNot scoredLowNegligible
1.3Tourism & recreation areasNot scoredLowNegligible
2Agriculture & aquacultureLowLowNegligible
2.1Annual & perennial non-timber cropsLowLowNegligible
2.3Livestock farming & ranchingNot scoredLowNegligible
3Energy production & miningNot calculated (unknown timing)HighNot scored
3.2Mining & quarryingNot calculated (unknown timing)HighNot scored
4Transportation & service corridorsLowHigh - MediumLow
4.1Roads & railroadsLowHigh - MediumLow
5Biological resource useNot scoredNegligibleLow
5.3Logging & wood harvestingNot scoredNegligibleLow
6Human intrusions & disturbanceLowNot scoredNot scored
6.1Recreational activitiesLowNot scoredNot scored
7Natural system modificationsHighNot scoredNegligible
7.2Dams & water management/useHighNot scoredNegligible
7.3Other ecosystem modificationsLowNot scoredNot scored
8Invasive & other problematic species & genesUnknownLowNegligible
8.1Invasive non-native/alien speciesUnknownLowNegligible
9PollutionUnknownUnknownNegligible
9.1Household sewage & urban waste waterNot scoredUnknownNegligible
9.3Agricultural & forestry effluentsUnknownUnknownNot scored
11Climate change & severe weatherNot Calculated (outside assessment timeframe)Not scoredNot scored
11.2DroughtsNot Calculated (outside assessment timeframe)Not scoredNot scored
Calculated Overall Threat Impact:Calculated Overall Threat Impact:HighVery HighLow

DU 1: Small-mouthed Salamander-dependent unisexuals (calculated overall threat impact = high)

Natural system modifications (impact "high")

Draining of wetlands is probably the greatest threat to Small-mouthed Salamanders and Small-mouthed Salamander-dependent unisexuals. Drainage ditches alter water levels in salamander breeding ponds. Canal/ditch dredging right by the road at Fish Point (one of occupied sites on Pelee Island) sucks out water from breeding ponds. Dredging may happen throughout the island and the only population that is not affected is in the abandoned quarry at Sheridan Point. Water levels in Lake Erie fluctuate, and salamanders do better at higher water levels. Clearing of wood and removal of coarse woody debris, mostly at the Fish Point area, can detrimentally affect juveniles (adults use burrows).

Transportation and service corridors (impact "low")

Salamander breeding ponds on Pelee Island are situated close to roads, and salamanders frequently cross roads during migration and dispersal. Road-kill is a threat to migrating and dispersing salamanders. Although traffic is relatively light during the early spring breeding season, tourist traffic on the island has increased, especially during the summer when juveniles are leaving ponds.

Human intrusions and disturbance (impact "low")

Human disturbance occurs at the Fish Point area, which is heavily used by tourists. Inadvertent trampling of salamanders and their habitat may occur from visitors photographing and looking for salamanders in the woods and ponds. Other visitors also frequent salamander habitats while bird viewing or hiking.

Residential and commercial development (impact "low")

Some residential expansion is taking place on Pelee Island. While no developments are known in salamander habitat, it remains a possibility. Because of the small size of the salamander population, even one development would be an issue. The severity of impact depends on whether the breeding pond is drained (extreme) or whether only the terrestrial habitat is affected (less severe).

Agriculture (impact "low")

One breeding pond is near an agricultural field, containing approximately 5% of the population. Further agricultural development or expansion at this site is a possibility, but no plans are known.

Introduced species (impact "unknown")

The introduction of Wild Turkeys (Meleagris gallopavo) poses a potential threat to Small-mouthed Salamanders and their associated unisexuals on Pelee Island (Hamill 2014; COSEWIC 2014). From about 25 breeding pairs released in 2002, a large population now exists on the Island. Turkeys can change forest floor conditions to the detriment of (especially juvenile) salamanders, and turkeys possibly eat salamanders.

DU 2: Jefferson Salamander-dependent unisexuals (calculated overall threat impact = very high)

Residential and commercial development (impact "high")

The Carolinian forest with its associated fauna reaches the northern limit of its distribution in southern Ontario, but the vast majority of this habitat in Ontario has been cleared, initially for agriculture and subsequently for urban development. Habitat continues to be lost as a result of housing development, especially in the Hamilton area and along the Niagara Escarpment. When breeding ponds are filled or drained, local extirpations will occur. Migratory paths between a breeding pond and terrestrial habitat may be blocked by development (e.g., silt fencing). The most probable cause of low numbers of Jefferson Salamanders and their associated unisexuals in Canada is the limited amount of suitable habitat, both terrestrial habitat and breeding ponds.

Energy production and mining (impact "high")

Aggregate mining and quarrying pose an important problem for Jefferson Salamanders and their unisexual associates on the Niagara Escarpment. In addition to the loss of breeding ponds and terrestrial habitat, hydrological alterations from quarrying below the water table can reduce the hydroperiod of a breeding pond so that the pond consistently dries up before the larvae transform.

Transportation and service corridors (impact "high - medium")

Southern Ontario has a dense network of roads. Salamanders are frequently killed on roads by vehicles while migrating to or from a breeding pond (Beebee 2013). Using data from 500 Spotted Salamander breeding ponds in Massachusetts, Gibbs and Shriver (2005) modelled the demographic significance of road mortality. He found that an annual risk of road mortality > 10% can lead to local population extirpation and with a salamander road mortality of 20 to 30%, the population would be extirpated within 25 years. Curbs and catch basins can act as barriers or traps, respectively. Road-kill is substantial in some areas in southern Ontario despite mitigation attempts (e.g., road closures close to some breeding sites). Road-kill is expected to have severe impacts on local populations of Jefferson Salamanders and their associated unisexuals.

Invasive and problematic species (impact "low")

Introduced fish, invasive zooplankton, and invasive aquatic plants (Phragmites australis) were considered in this category. Ambystomatid salamanders do not thrive with predatory fish, and many Jefferson Salamander breeding sites where the species no longer exists have been stocked with fish. Introduced zooplankton is becoming an ecosystem-level problem in southern Ontario, as native arthropods are reluctant to feed on them, and the salamander prey base could potentially be affected. Other than the introduction of predatory fish, there is no information on whether or not these other threats are a problem for these salamanders.

Pollution (impact unknown)

Roads are often a source of chemical pollution (e.g., salt, metals, and products of combustion) that degrade adjacent aquatic and terrestrial habitat. Toxic effects of salts applied for road de-icing can extend considerable distances into wetlands and have been demonstrated to be detrimental to Spotted Salamanders (Turtle 2000; Karraker et al. 2008; Collins and Russell 2009).

DU 3: Blue-spotted Salamander-dependent unisexuals (calculated overall threat impact = low)

Although Blue-spotted Salamander-dependent unisexuals experience most of the same threats as Jefferson Salamander-dependent unisexuals in southern Ontario, those populations represent a small percentage (5 - 10%) of the range of Blue-spotted salamanders. Because of their large range and occurrence of a substantial proportion of the range in areas away from human activities and developments, the scope of the threats is considerably less than for the Jefferson Salamander-dependent unisexuals, therefore resulting in lower threat impacts.

Number of locations

It is assumed that each breeding pond, or pond complex if ponds are within a 1 km area, qualifies as a "location" as per the COSEWIC definition as a geographically or ecologically distinct area in which a single threatening event can rapidly affect all individuals of the taxon present. In most cases, the threatening event would be the loss of a suitable breeding pond, as a result of changes to hydrology or draining associated with development or other human activities.

There are very few populations of Small-mouthed Salamander-dependent unisexuals in Canada. Pelee Island had six historical breeding ponds (Bogart and Licht 1991), and each can be considered a location, but two of those ponds were probably lost between 1990 and 2003 (COSEWIC 2004). Similarly, the number of locations for the Jefferson Salamander (~ 33) (COSEWIC 2010) would appear to be fewer than the number of locations for Jefferson Salamander-dependent unisexuals because historical and recent populations are included in Figure 6 and only Jefferson Salamander-dependent unisexuals have been found in some ponds (COSEWIC 2010). It was assumed that there was no longer any recruitment of Jefferson Salamanders or Jefferson Salamander-dependent unisexuals in ponds that were found to have only unisexual salamanders in recent surveys. The number of locations for Jefferson Salamanders (~33) or 30 recent locations would be the same for the Jefferson Salamander-dependent unisexuals (COSEWIC 2015; Appendix C). The large number of locations that are estimated for the Blue-spotted Salamander-dependent unisexuals reflect the extensive distribution of Blue-spotted Salamanders in Canada (Figure 7).


Protection, status and ranks

Legal protection and status

Jefferson, Blue-spotted, and Small-mouthed Salamanders present problems for conservation and management decisions because they coexist with unisexual individuals that usually do not have a conservation status (Kraus 1995). Connecticut lists A. jeffersonianum "complex" and A. laterale "complex" as state species of special concern because it is difficult to distinguish the unisexuals from the bisexual species, A. jeffersonianum and A. laterale (Klemens 2000). Connecticut also lists pure diploid populations of A. laterale in the eastern portion of the state as a threatened species, but there is no status given for A. jeffersonianum (only A. jeffersonianum "complex") (Klemens 2000).

A federal recovery strategy has been proposed (Environment Canada 2015) but is yet to be approved. In Ontario, "Jefferson dominated polyploids" are unisexuals that require Jefferson Salamander males, which is equivalent to Jefferson Salamander-dependent unisexuals. These unisexuals receive the same habitat protection as Jefferson Salamander under the provincial Endangered Species Act, 2007 (ESA) (Government of Ontario 2007) in the form of a habitat regulation, which came into force February 18, 2010 (ESA 2007, Regulation 242/08 s. 28). Protection includes an area of 300 m around breeding ponds and an area of 1 km from a breeding pond to connected breeding ponds or potential breeding ponds that would allow for dispersal. So far, there is no similar habitat regulation for Canadian unisexuals that live with the endangered Small-mouthed Salamander on Pelee Island or for unisexuals that depend on the Blue-spotted Salamander. Unisexual salamanders receive additional legal protection under various fish and wildlife legislation in several provinces. For example, the New Brunswick Fish & Wildlife Act defines "wildlife" as any vertebrate, and it is an offence to capture or take into captivity, keep in captivity, or release from captivity any wildlife. The Ontario Fish and Wildlife Conservation Act provides similar protection for wildlife in Ontario. Under the FWCA, the Jefferson, Blue-spotted, Spotted and Small-mouthed Salamanders are also listed as "Specially Protected", and the additional protection that those species receive would also apply to unisexual Ambystoma.

Non-legal status and ranks

Unisexual Ambystoma are not listed in IUCN or NatureServe databases. The Ontario National Heritage Information Centre (NHIC) assigns sub-national conservation status ranks to two categories of Unisexual Ambystoma: Jefferson X Blue-spotted Salamander, Jefferson genome dominates (Ambystoma hybrid pop. 1), which would be equivalent to Jefferson Salamander-dependent unisexuals, are ranked S2 (and tracked by NHIC) and Jefferson X Blue-spotted Salamander, Blue-spotted genome dominates (Ambystoma hybrid pop. 2), which is equivalent to Blue-spotted Salamander-dependent unisexuals, are ranked S4 (and not tracked by NHIC).

Habitat protection and ownership

Most of the unisexuals that rely on Small-mouthed Salamanders on Pelee Island exist in habitat that has natural heritage protection that is owned by the OMNRF, Essex Region Conservation Authority, or the Nature Conservancy of Canada. About one third of the known populations of Jefferson Salamander-dependent unisexuals are found in suitable habitat (forests with small ponds) within provincial parks along the Niagara Escarpment, within the Ontario Greenbelt, and on lands held by conservation authorities. The inclusion of suitable habitat within a provincial park, conservation area, or along the Niagara Escarpment does not necessarily guarantee protection of that habitat for the salamanders because these areas serve multiple recreational uses. Some small permanent ponds on private lands and within conservation areas have been stocked with predatory fish to provide recreational fishing opportunities (Bogart and Cook 1991). Blue-spotted Salamander-dependent unisexuals may receive general protection by residing in provincial parks or conservation areas in Ontario, New Brunswick, Nova Scotia, and Quebec. In Ontario, the Provincial Policy Statement under the Planning Act provides some protection for significant wildlife habitat, which can include salamander breeding ponds.


Acknowledgements and authorities contacted

The report writer thanks the members of the Jefferson Salamander Recovery Strategy Development Team, who have worked hard to find salamanders in historical populations and in new areas in Ontario. He especially thanks Emma Followes, the former recovery team coordinator, John Pisapio who has collaborated in research efforts, and Melinda Thompson who collates the collection data for the Recovery Team. The report writer has been fortunate to have worked with many interested and dedicated students at the University of Guelph, both in the field and in the laboratory as well as several colleagues in the United States who have sent specimens and tissue samples that have been instrumental to improve our understanding of unisexuals. Several biological consultants have worked closely with the OMNRF and the Jefferson Salamander Recovery Team to provide important data. The report writer especially thanks Alison Featherstone, Christen Harrison, Karl Konze, Jessica Linton, Al Sandilands, and Gwendolyn Weeks. Ecologists working for various conservation authorities have provided data from historical populations and have found new sites. Many serve on the Recovery Team and the report writer would like especially to thank Brenda Van Ryswyk from Halton Region Conservation Authority. Francis Cook (Canadian Museum of Nature), Ross MacCulloch and Amy Lathrop (Royal Ontario Museum) maintain collections of voucher specimens and are continual sources of encouragement and assistance. A very special thanks to Jenny Wu of the COSEWIC Secretariat who constructed the maps and calculated the areas for this report.

Funding for this report was provided by the Canadian Wildlife Service, Environment Canada.

Authorities consulted

  • Ruben Boles, Species Populations and Standards Management (SPASM), Canadian Wildlife Service, Environment Canada.
  • Michael J. Oldham, Ontario Natural Heritage Information Centre (NHIC), Ministry of Natural Resources.

Jefferson Salamander Recovery Team Members

  • Karine Bériault, Species at Risk Biologist, Ministry of Natural Resources, Vineland Area Office.
  • Kim Barrett, Senior Ecologist, Conservation Halton
  • Emma Followes, District Ecologist, Ontario Ministry of Natural Resources, Aurora District.
  • Ron Gould, Species at Risk Biologist, Ontario Ministry of Natural Resources, Aylmer District.
  • Lisa Grbinicek, Environmental Planner, Ecological Monitoring Specialist, Ontario's Niagara Escarpment (ONE) Monitoring Program, Niagara Escarpment Commission.
  • Sue Hayes, Project Coordinator, Terrestrial Field Inventories, Toronto and Region Conservation Authority.
  • Anne Marie Laurence, Ecological Monitoring Specialist, Ontario's Niagara Escarpment (ONE) Monitoring Program, Niagara Escarpment Commission.
  • Heather Lynn, Natural Heritage Ecologist, Credit Valley Conservation.
  • Bob Murphy, Senior Curator, Centre for Biodiversity and Conservation Biology, Royal Ontario Museum.
  • John Pisapio, Wildlife Biologist, Ontario Ministry of Natural Resources, Aurora District.
  • Tony Zammit, Ecologist, Grand River Conservation Authority.

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Petranka, J.W. 1998. Salamanders of the United States and Canada. Smithsonian Institution Press. 587pp.

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Taylor, A.S., and J.P. Bogart, 1990. Karyotypic analyses of four species of Ambystoma (Amphibia, Caudata) which have been implicated in the production of all-female hybrids. Genome 33:837-844.

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Turtle, S.L. 2000. Embryonic survivorship of the spotted salamander (Ambystoma maculatum) in roadside and woodland vernal pools in southeastern New Hampshire. Journal of Herpetology 34:60-67.

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Vrijenhoek R.C., R.M. Dawley, C.J. Cole, and J.P. Bogart. 1989. A list of the known unisexual vertebrates. Pp. 19-23, in R. Dawley and J.P. Bogart (eds.). Evolution and Ecology of Unisexual Vertebrates. New York State Museum Bull. 466. Albany, New York.

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Williams, R.N., and J.A. DeWoody. 2004. Fluorescent dUTP helps characterize 10 novel tetranucleotide microsatellites from an enriched salamander (Ambystoma texanum) genomic library. Molecular Ecology Notes 4:17-19.


Biographical summary of report writer(s)

James (Jim) Bogart is Professor Emeritus in the Department of Integrative Biology at the University of Guelph. His research examines evolution at the species level and involves molecular biology, cytogenetics, ecology and evolution with a focus on polyploid amphibians. His studies on unisexual Ambystoma and their sperm donors were initiated in 1975 and have continued to the present time. He has advised several graduate students who have studied various aspects of these salamanders in Canada and in the United States.


Collections examined

Most unisexual salamanders and their sperm-donating species that were examined from the eastern United States are deposited in the American Museum of Natural History (AMNH). Data and catalogue numbers for these specimens are included in Bogart and Klemens (1997, 2008). Specimens from Ohio are in collections at the University of Dayton and Ohio State University. Specimens from Indiana are under the care of Dr. R. Brodman, Saint Joseph's College, Rensselaer, Indiana. Michigan samples are deposited in the Museum of Vertebrate Zoology at the University of Michigan. Canadian voucher specimens are deposited at the Royal Ontario Museum (ROM) or the Canadian Museum of Nature (CMN). A frozen collection of tissues and DNA extractions is catalogued and stored at the University of Guelph.


Appendix 1. Ploidy elevation and reduction.

Ploidy elevation

The modal ploidy level in unisexual Ambystoma is triploid, but diploid, tetraploid and pentaploid individuals have been encountered over the extensive range of unisexual Ambystoma. Pentaploids are very rare (Lowcock and Murphy 1991), and tetraploids are more common than diploid unisexuals (Phillips et al. 1997; Bogart and Klemens 1997, 2008) (Table 1). In laboratory crosses (Bogart et al. 1989), triploid females produced triploid and tetraploid offspring, and tetraploid females produced tetraploid and pentaploid offspring. There was a significant increase in the number of tetraploid offspring from triploid mothers if the temperature was increased to 15° C from 6° C. These data show that ploidy elevation is a fairly common phenomenon in unisexual Ambystoma and may be related to extrinsic factors, such as temperature. When offspring from a unisexual female are sampled for several microsatellite loci, gynogenetic offspring have the same multi-locus genotype (MLG) as their mother (e.g., clones). Ploidy-elevated offspring have an additional allele at loci where the sperm-derived genome possesses alternate alleles. It is possible to genotype a male sperm donor of a unisexual triploid female from the tetraploid offspring that are produced (Bogart and Bi 2013).

Genes residing in bisexual individuals should have been sorted over many generations of natural selection and in theory may represent the 'best' genes for the contemporary environment. Theoretically, by stealing such genes (and chromosomes), co-occurring unisexuals could bypass long periods of natural selection and are better able to successfully compete with bisexuals. Subsequent gynogenetic reproduction would avoid the expected 50% loss of 'good genes' that would be expected to occur during normal meiosis. Although empirical data show that genome elevation exists in most unisexual salamander populations (Bogart 2003), ploidy elevation probably has an upper limit that is likely pentaploid (Lowcock and Murphy 1991).

Ploidy reduction and genome replacement

The problem of ever increasing ploidy levels through ploidy elevation could be alleviated if genomes can be discarded as well as added. From an evolutionary perspective, it would be advantageous for a unisexual to keep a genome that confers a selective advantage in a contemporary population and discard a genome that would confer a lower fitness. Microsatellite data (Bogart et al. 2007, 2009; Ramsden 2008; Nöel et al. 2011) show that diploid, triploid, and tetraploid unisexuals share microsatellite DNA alleles with available sympatric sperm donors. It is of interest, and perhaps significant, that all of the more than 20 unisexual genomotypes (Bogart 2003; Bogart et al. 2009) contain at least one Blue-spotted Salamander (A. laterale)genome. The A. laterale genome was targeted by Bi et al. (2008), who constructed a genealogy of that genome using sequences from an A. laterale - specific, variable, nuclear DNA marker (L-G1C12). They found that unisexuals invariably shared the same haplotype with A. laterale in sympatric populations over much of the unisexual range. An alternate hypothesis, that an 'ancient' Ambystoma laterale genome persists in all of the various unisexual genome combinations was rejected.

Bogart and Bi (2013) believe that ploidy reduction and genome replacement are linked. Such linkage requires the (sometimes) sympatric occurrence of Blue-spotted Salamanders and another sperm donor species that enable ploidy-elevated symmetrical tetraploids to be produced. The possible events are illustrated in Figure 9. These conditions and biotypes are found on Pelee Island (Table 1). Theoretically, the formation of ploidy-reduced diploid LT unisexuals from a symmetrical tetraploid LLTT would simply involve skipping the pre-meiotic endoduplication step that is a prerequisite for triploid meiosis (Bogart 2003). Sperm incorporation in an unreduced LT egg elevates the ploidy to a triploid level and explains genome replacement. One L genome (from a level A female) is replaced with a new L or a new T genome in level D individuals. Such a scenario could also be used to explain ploidy reduction and genome replacement in unisexuals that co-occur with Blue-spotted and Jefferson Salamanders on the mainland.

Genome replacement has implications with respect to designatable units (DUs). It could be argued that the unisexual Ambystoma represent a single DU and individuals randomly gain and lose genomes across their range. Using simulation models, Charney (2012) tracked the expected outcome of unisexuals that engaged in ploidy elevation and genome replacement over time. He concluded that nuclear genomes would eventually be indistinguishable from their hosts over a relatively short period of time, which corresponded with the frequency of genome replacement that he considered to be equal to the frequency of ploidy elevation. The logical outcome would be diploid or triploid Jefferson or Blue-spotted Salamanders that possessed a unisexual mtDNA. That such individuals have never been found is, according to Charney, the result of inadequate sampling effort.

It is true that the DNA that is extracted for identifying bisexual and unisexual genomotypes is not always used for mtDNA sequences, but such sequence data are available over the range of unisexual salamanders and their bisexual hosts (Hedges et al., 1992; Bogart 2003; Bogart et al., 2007, 2009; Nöel et al., 2008, 2011; Bi and Bogart 2010; Greenwald and Gibbs 2012; Bi and Bogart, unpublished data). If the mechanism for genome replacement requires symmetrical tetraploids, as hypothesized by Bogart and Bi (2013) (see Figure 9), a unisexual individual would use the "wrong" sperm donor. For example, an LJJ unisexual, which typically used A. jeffersonianum as a sperm donor, was inseminated with sperm from A. laterale. Gynogenetic offspring would still be LJJ but ploidy-elevated offspring would be LLJJ. If Jefferson Salamanders were extirpated and Blue-spotted Salamanders persisted, the frequency of LLJ/LJJ would be expected to rise but it would probably take a very long time for LLJ to displace LJJ. In Ontario, there are very few areas where Blue-spotted and Jefferson Salamanders are sympatric or parapatric and it is in such, generally disturbed, areas that LLJJ and LJ unisexuals are rarely encountered. Jefferson and Blue-spotted Salamanders have different habitat preferences (Petranka 1998), which probably explains why these species are rarely found together and this would probably extend to their associated unisexual DUs that are also very rarely found together.

Figure 9. Hypothetical events to explain genome reduction and genome replacement used by unisexual salamanders on Pelee Island. Blue-spotted Salamanders (Ambystoma laterale orLL) and Small-mouthed salamanders (A. texanum orTT) are bothfound on the island. A triploid LLT unisexual (level A) lays unreduced LLT eggs that can produce LLT larvae by gynogenesis (sperm is rejected). If the sperm from an A. laterale male is incorporated, the offspring are tetraploid LLLT, and if a sperm cell from A. texanum is incorporated, the offspring are symmetrical tetraploid LLTT (level B). Eggs from a symmetrical tetraploid could be unreduced and develop by gynogenesis or undergo reductional meiosis to produce LT eggs (level C). Diploid LT eggs can develop by gynogenesis or be fertilized by A. laterale sperm to produce LLT or by A. texanum sperm to produce LTT (level D). All these biotypes are found on Pelee Island (Table 1), and such a system could explain the formation of diploid LT unisexuals. Sperm incorporation elevates the ploidy to a triploid level and explains genome replacement. One L genome (in a level A unisexual) is replaced with a new L or a new T genome in level D unisexuals.
Hypothetical  events to explain genome reduction and genome replacement
Photo: © From Bogart and Bi 2013
Long description for Figure 9

Diagram illustrating hypothetical events that could explain genome reduction and genome replacement used by unisexual salamanders on Pelee Island, Ontario.


Appendix 2. Threats calculator spreadsheet, including notes, for the Small-mouthed Salamander-dependent unisexual Ambystoma (DU1).

Threats assessment worksheet

Species or Ecosystem Scientific Name:
Unisexual Ambystoma, A. texanum-dependent population
Date:
2/2/2015
Assessor(s):
Jim Bogart (report writer), Kristiina Ovaska (facilitator), Bev McBride (COSEWIC Secretariat), Mary Sabine, Leslie Anthony, Isabelle Gauthier, Yohann Dubois, Joe Crowley
References:
COSEWIC status report (2015 draft)
Overall reat Impact Calculation Help:
Threat ImpactThreat Impact (descriptions)Level 1 Threat Impact Counts:
high range
Level 1 Threat Impact Counts:
low range
AVery High00
BHigh11
CMedium00
DLow44
-Calculated Overall Threat Impact:HighHigh
Assigned Overall Threat Impact:
High
Overall Threat Comments
Generation time - 8 years (24 years for 3 generations); ca. 1000 adults; EOO & IAO = 20 km2
Threats Assessment Worksheet Table (DU1)
ThreatThreatImpact (calculated)Impact (calculated)Scope (next 10 Yrs)Severity (10 Yrs or 3 Gen.)TimingComments
1Residential & commercial developmentDLowSmall (1-10%)Serious (31-70%)Moderate (Possibly in the short term, < 10 yrs/3 gen)-
1.1Housing & urban areasDLowSmall (1-10%)Serious (31-70%)Moderate (Possibly in the short term, < 10 yrs/3 gen)Some residential expansion is taking place on Pelee Island. While currently none known in salamander habitat, the possibility remains. Because the population is so small, even one development in salamander habitat would be an issue (scope >1%). Severity of effects depend on whether the breeding pond is drained (extreme) or whether terrestrial habitat is affected (less severe).
1.2Commercial & industrial areas------
1.3Tourism & recreation areas-----A new trail development is possible (Lighthouse Point), but other expansion is unlikely.
2Agriculture & aquacultureDLowSmall (1-10%)Extreme (71-100%)Moderate (Possibly in the short term, < 10 yrs/3 gen)-
2.1Annual & perennial non-timber cropsDLowSmall (1-10%)Extreme (71-100%)Moderate (Possibly in the short term, < 10 yrs/3 gen)Middle Pond in the centre of the island is near an agricultural field (rich pond & probably has 5% of the salamander population on the island). Further agricultural development is a possibility.
2.2Wood & pulp plantations------
2.3Livestock farming & ranching------
2.4Marine & freshwater aquaculture------
3Energy production & mining-Not calculated (unknown timing)Small (1-10%)Extreme (71-100%)Unknown-
3.1Oil & gas drilling------
3.2Mining & quarrying-Not calculated (unknown timing)Small (1-10%)Extreme (71-100%)UnknownThere is an old quarry with salamanders (North Pond), which could potentially be activated in the future, but there is no knowledge of such plans.
3.3Renewable energy------
4Transportation & service corridorsDLowSmall (1-10%)Serious (31-70%)High (Continuing)-
4.1Roads & railroadsDLowSmall (1-10%)Serious (31-70%)High (Continuing)Most salamander ponds are in the interior of the island rather than on the periphery where most roads are. Impacts of roads include barriers to breeding migrations, and from roadkill. There are ponds on each side of road in the south of the island where salamanders do cross and get killed (~ 5% of the population use these ponds). There is uncertainty about impacts on the population but it could be serious. There is relatively little traffic during the breeding season on Pelee Island.
4.2Utility & service lines------
4.3Shipping lanes------
4.4Flight paths------
5Biological resource use------
5.1Hunting & collecting terrestrial animals-----There is no evidence of targeted collecting; see Recreation
5.2Gathering terrestrial plants------
5.3Logging & wood harvesting------
5.4Fishing & harvesting aquatic resources------
6Human intrusions & disturbanceDLowSmall (1-10%)Slight (1-10%)High (Continuing)-
6.1Recreational activitiesDLowSmall (1-10%)Slight (1-10%)High (Continuing)Only an issue in the Fish Point area where tourists visit, and these areas are heavily used but maybe not in breeding season when salamanders are most vulnerable. Disturbance (trampling of salamanders and their habitat) occurs from people occasionally photographing and looking for salamanders in the woods and ponds; birders & other recreational tourists also go into salamander habitats.
6.2War, civil unrest & military exercises------
6.3Work & other activities------
7Natural system modificationsBHighLarge (31-70%)Serious (31-70%)High (Continuing)-
7.1Fire & fire suppression------
7.2Dams & water management/useBHighLarge (31-70%)Serious (31-70%)High (Continuing)This probably poses the greatest threat to this population. Drainage ditches alter water levels in salamander ponds: e.g., canal dredging is occurring right by the road at Fish Point that sucks out water from breeding ponds, and it may also happen throughout the island (the only population not affected is in the northern quarry pond). Water level in Lake Erie fluctuates greatly, and salamanders do better at higher water levels. The habitat is not legally protected from dredging and drainage alteration in Ontario except from the Ontario Endangered Species Act in relation to the endangered Ambystoma texanum.
7.3Other ecosystem modificationsDLowSmall (1-10%)Moderate (11-30%)High (Continuing)Clearing of wood and removal of coarse woody debris occurs mostly at Fish Point area. It is mostly expected to affect juveniles (adults use burrows). Also introduced turkeys are changing forest floor conditions with largely unknown effects (predation by turkeys dealt with under Introduced Species). Note: loss of sperm-donor populations through stochastic events is not scored here; this would most likely happen together due to other threats that affect both unisexuals and sperm-donors.
8Invasive & other problematic species & genes-UnknownPervasive (71-100%)UnknownHigh (Continuing)-
8.1Invasive non-native/alien species-UnknownPervasive (71-100%)UnknownHigh (Continuing)Possible predation by introduced Wild Turkeys is of concern. There is no information on chytrid fungus or other disease. Invasive aquatic reeds (Phragmites australis) are unlikely to affect these salamanders.
8.2Problematic native species------
8.3Introduced genetic material------
9Pollution-UnknownRestricted (11-30%)UnknownHigh (Continuing)-
9.1Household sewage & urban waste water------
9.2Industrial & military effluents------
9.3Agricultural & forestry effluents-UnknownRestricted (11-30%)UnknownHigh (Continuing)Run-off from vineyards and from agricultural (pasture?) fields, especially around Middle Pond. Scope and severity are both uncertain. There is also uncertainty of chemicals and the quantities that are used.
9.4Garbage & solid waste------
9.5Air-borne pollutants------
9.6Excess energy------
10Geological events------
10.1Volcanoes------
10.2Earthquakes/tsunamis------
10.3Avalanches/ landslides------
11Climate change & severe weather-Not Calculated (outside assessment timeframe)Pervasive (71-100%)Serious (31-70%)Low (Possibly in the long term, >10 yrs/3 gen)-
11.1Habitat shifting & alteration------
11.2Droughts-Not Calculated (outside assessment timeframe)Pervasive (71-100%)Serious (31-70%)Low (Possibly in the long term, >10 yrs/3 gen)Premature drying of breeding ponds is of concern, exacerbating impacts of human water withdrawal. Lake Erie (see Water Management) has fluctuating water levels from unknown causes. All but one of the salamander breeding sites are temporary ponds and would be affected by climate change. Unsure whether there are specific predictions for this area.
11.3Temperature extremes------
11.4Storms & flooding------

Classification of Threats adopted from IUCN-CMP, Salafsky et al. (2008).

Glossary

Impact
The degree to which a species is observed, inferred, or suspected to be directly or indirectly threatened in the area of interest. The impact of each threat is based on Severity and Scope rating and considers only present and future threats. Threat impact reflects a reduction of a species population or decline/degradation of the area of an ecosystem. The median rate of population reduction or area decline for each combination of scope and severity corresponds to the following classes of threat impact: Very High (75% declines), High (40%), Medium (15%), and Low (3%). Unknown: used when impact cannot be determined (e.g., if values for either scope or severity are unknown); Not Calculated: impact not calculated as threat is outside the assessment timeframe (e.g., timing is insignificant/negligible or low as threat is only considered to be in the past); Negligible: when scope or severity is negligible; Not a Threat: when severity is scored as neutral or potential benefit.
Scope
Proportion of the species that can reasonably be expected to be affected by the threat within 10 years. Usually measured as a proportion of the species' population in the area of interest. (Pervasive = 71-100%; Large = 31-70%; Restricted = 11-30%; Small = 1-10%; Negligible < 1%).
Severity
Within the scope, the level of damage to the species from the threat that can reasonably be expected to be affected by the threat within a 10-year or three-generation timeframe. Usually measured as the degree of reduction of the species' population. (Extreme = 71-100%; Serious = 31-70%; Moderate = 11-30%; Slight = 1-10%; Negligible < 1%; Neutral or Potential Benefit > 0%).
Timing
High = continuing; Moderate = only in the future (could happen in the short term [< 10 years or 3 generations]) or now suspended (could come back in the short term); Low = only in the future (could happen in the long term) or now suspended (could come back in the long term); Insignificant/Negligible = only in the past and unlikely to return, or no direct effect but limiting.

Appendix 3. Threats calculator spreadsheet, including notes, for the Jefferson Salamander-dependent unisexual Ambystoma (DU2).

Threats assessment worksheet

Species or Ecosystem Scientific Name:
Unisexual Ambystoma, A. jeffersonianum-dependent population
Date:
2/2/2015
Assessor(s):
Jim Bogart (report writer), Kristiina Ovaska (facilitator), Bev McBride (COSEWIC Secretariat), Mary Sabine, Leslie Anthony, Isabelle Gauthier, Yohann Dubois, Joe Crowley
References:
COSEWIC status report (2015 draft)
Overall reat Impact Calculation Help:
Threat ImpactThreat Impact (descriptions)Level 1 Threat Impact Counts:
high range
Level 1 Threat Impact Counts:
low range
AVery High00
BHigh32
CMedium01
DLow22
-Calculated Overall Threat Impact:Very HighVery High
Assigned Overall Threat Impact:
Very High
Overall Threat Comments
Generation time - 11 years (33 years for 3 generations); < 10,000 adults
Threats Assessment Worksheet Table (DU2)
Threat #ThreatImpact (calculated)Impact (calculated)Scope (next 10 Yrs)Severity (10 Yrs or 3 Gen.)TimingComments
1Residential & commercial developmentBHighLarge (31-70%)Serious (31-70%)High (Continuing)-
1.1Housing & urban areasBHighLarge (31-70%)Serious (31-70%)High (Continuing)Habitat loss from housing development, especially in the Hamilton area and along the Niagara escarpment is an issue. It is challenging to protect habitat in these areas. Average impact is serious (terrestrial or aquatic habitat affected). If breeding ponds are drained, local extirpations will occur.
1.2Commercial & industrial areasDLowSmall (1-10%)Extreme (71-100%)High (Continuing)The group didn't know of any imminent areas slated for this activity, but industrial development is a possibility.
1.3Tourism & recreation areasDLowSmall (1-10%)Moderate (11-30%)Moderate (Possibly in the short term, < 10 yrs/3 gen)There is likely some development, but no examples were available. Impacts are from habitat loss. Golf courses, park infrastructure and similar developments would likely have lower impacts than housing because regulations apply (e.g., in terms of their placement; riparian protection etc.), and habitat modification is often less intense as for housing (e.g., ponds may be included in golf courses; however, herbicides and pesticides may accumulate in these ponds reducing their suitability).
2Agriculture & aquacultureDLowSmall (1-10%)Extreme (71-100%)High (Continuing)-
2.1Annual & perennial non-timber cropsDLowSmall (1-10%)Extreme (71-100%)High (Continuing)Current rates of land conversion into agriculture are low in southern Ontario. Where it happens, however, impacts are severe because ponds are usually drained and turned into agricultural fields such as for corn and soy beans.
2.2Wood & pulp plantations-----Conversion of hardwoods to soft woods may occur after logging and reduce available habitat but is not considered a threat at this point due to very low scope.
2.3Livestock farming & ranchingDLowSmall (1-10%)Moderate (11-30%)High (Continuing)Scope is similar to other agriculture uses, but severity is lower. Free range livestock can impact salamanders and their habitat by using ponds as a water source and trampling shoreline vegetation, salamanders and eggs.
2.4Marine & freshwater aquaculture------
3Energy production & miningBHighPervasive - Large (31-100%)Serious (31-70%)High (Continuing)-
3.1Oil & gas drilling------
3.2Mining & quarryingBHighPervasive - Large (31-100%)Serious (31-70%)High (Continuing)Aggregate mining: quarrying is a big problem on Niagara escarpment
3.3Renewable energy------
4Transportation & service corridorsBCHigh - MediumLarge (31-70%)Serious - Moderate (11-70%)High (Continuing)-
4.1Roads & railroadsBCHigh - MediumLarge (31-70%)Serious - Moderate (11-70%)High (Continuing)Southern Ontario has a dense road networks, and the vast majority of sub-populations are exposed to roads. Impacts are from road mortality during breeding migrations and, to a lesser extent, from barriers to movements. Roadkill is known from some areas in southern Ontario despite mitigation attempts, such as road closures by some sites. Roadkill can have severe impacts on local populations.
4.2Utility & service lines------
4.3Shipping lanes------
4.4Flight paths------
5Biological resource use-NegligibleNegligible (<1%)Serious (31-70%)High (Continuing)-
5.1Hunting & collecting terrestrial animals------
5.2Gathering terrestrial plants------
5.3Logging & wood harvesting-NegligibleNegligible (<1%)Serious (31-70%)High (Continuing)In southwest Ontario, there are some small woodlots on private lands. Habitat is unsuitable after logs are taken out (at least one population disappeared after logging). However, there is not much logging along the Niagara escarpment where most salamander populations exist.
5.4Fishing & harvesting aquatic resources------
6Human intrusions & disturbance------
6.1Recreational activities-----ATVs sometimes damage ponds, usually later in the summer. They do not necessarily target vernal pools but can kill newly transformed salamanders.
6.2War, civil unrest & military exercises------
6.3Work & other activities-----No killing anymore as part of research
7Natural system modifications------
7.1Fire & fire suppression------
7.2Dams & water management/use-----Not considered to be an issue for these salamanders (apart from pond draining due to development, which is addressed under Threat 1)
7.3Other ecosystem modifications-----Note: loss of sperm-donor populations through stochastic events is not scored here; this would most likely happen together due to other threats that affect both unisexuals and sperm-donors.
8Invasive & other problematic species & genesDLowSmall (1-10%)Extreme (71-100%)High (Continuing)-
8.1Invasive non-native/alien speciesDLowSmall (1-10%)Extreme (71-100%)High (Continuing)Introduced fish, invasive zooplankton (introduced with fish), emerging diseases, invasive aquatic plants (Phragmites australis) were considered. Salamanders don't do well with predatory fish. Introduced zooplankton is becoming a big ecosystem-level problem in southern Ontario (native arthropods don't eat them). Other than the introduction of predatory fish, there is no information whether or not these other threats are a problem for these salamanders.
8.2Problematic native species------
8.3Introduced genetic material------
9Pollution-UnknownSmall (1-10%)UnknownHigh (Continuing)-
9.1Household sewage & urban waste water-UnknownSmall (1-10%)UnknownHigh (Continuing)Run-off from roads (e.g., salts) is included here. Natural habitats are buffered to some degree, but some ponds are right by roads. We have no data on effects on salamanders, and hence severity is scored as unknown.
9.2Industrial & military effluents------
9.3Agricultural & forestry effluents-UnknownSmall (1-10%)UnknownHigh (Continuing)Runoff from agricultural chemicals (pesticides, herbicides, fertilizers) were considered. We have no information on what is used and how they might affect salamanders.
9.4Garbage & solid waste------
9.5Air-borne pollutants------
9.6Excess energy------
10Geological events------
10.1Volcanoes------
10.2Earthquakes/tsunamis------
10.3Avalanches/landslides------
11Climate change & severe weather------
11.1Habitat shifting & alteration------
11.2Droughts-----Occasional early drying of vernal pools from prolonged droughts is probably not a big problem for these salamanders that potentially have several breeding seasons and are long lived; however, several years of drought would impact populations. It is unlikely that this issue will become a problem for the salamanders over next 10 years but might be more important in the future.
11.3Temperature extremes-----Temperature fluctuations - warm springs followed by freezing conditions can kill salamanders in breeding ponds.
11.4Storms & flooding------

Classification of Threats adopted from IUCN-CMP, Salafsky et al. (2008).

Glossary

Impact
The degree to which a species is observed, inferred, or suspected to be directly or indirectly threatened in the area of interest. The impact of each threat is based on Severity and Scope rating and considers only present and future threats. Threat impact reflects a reduction of a species population or decline/degradation of the area of an ecosystem. The median rate of population reduction or area decline for each combination of scope and severity corresponds to the following classes of threat impact: Very High (75% declines), High (40%), Medium (15%), and Low (3%). Unknown: used when impact cannot be determined (e.g., if values for either scope or severity are unknown); Not Calculated: impact not calculated as threat is outside the assessment timeframe (e.g., timing is insignificant/negligible or low as threat is only considered to be in the past); Negligible: when scope or severity is negligible; Not a Threat: when severity is scored as neutral or potential benefit.
Scope
Proportion of the species that can reasonably be expected to be affected by the threat within 10 years. Usually measured as a proportion of the species' population in the area of interest. (Pervasive = 71-100%; Large = 31-70%; Restricted = 11-30%; Small = 1-10%; Negligible < 1%).
Severity
Within the scope, the level of damage to the species from the threat that can reasonably be expected to be affected by the threat within a 10-year or three-generation timeframe. Usually measured as the degree of reduction of the species' population. (Extreme = 71-100%; Serious = 31-70%; Moderate = 11-30%; Slight = 1-10%; Negligible < 1%; Neutral or Potential Benefit > 0%).
Timing
High = continuing; Moderate = only in the future (could happen in the short term [< 10 years or 3 generations]) or now suspended (could come back in the short term); Low = only in the future (could happen in the long term) or now suspended (could come back in the long term); Insignificant/Negligible = only in the past and unlikely to return, or no direct effect but limiting.

Appendix 4. Threats calculator spreadsheet, including notes, for the Blue-spotted Salamander-dependent unisexual Ambystoma (DU3).

Threats assessment worksheet

Species or Ecosystem Scientific Name:
Unisexual Ambystoma, A. laterale-dependent population
Date:
2/2/2015
Assessor(s):
Jim Bogart (report writer), Kristiina Ovaska (facilitator), Bev McBride (COSEWIC Secretariat), Mary Sabine, Leslie Anthony, Isabelle Gauthier, Yohann Dubois, Joe Crowley
References:
COSEWIC status report (2015 draft)
Overall reat Impact Calculation Help:
Threat ImpactThreat Impact (descriptions)Level 1 Threat Impact Counts:
high range
Level 1 Threat Impact Counts:
low range
AVery High00
BHigh00
CMedium00
DLow22
-Calculated Overall Threat Impact:LowLow
Assigned Overall Threat Impact:
Low
Overall Threat Comments
Generation time - 11 years (33 years for 3 generations); >1000,000 adults; EOO: 671,668 km2; IAO: 1,932 km2 (from draft COSEWIC status report)
Threats Assessment Worksheet Table (DU3)
Threat #ThreatImpact (calculated)Impact (calculated)Scope (next 10 Yrs)Severity (10 Yrs or 3 Gen.)TimingComments
1Residential & commercial development-NegligibleNegligible (<1%)Serious (31-70%)High (Continuing)-
1.1Housing & urban areas-NegligibleNegligible (<1%)Serious (31-70%)High (Continuing)Wide range, and most areas are not affected by housing developments; this is only an issue in southern Ontario and southern Québec.
1.2Commercial & industrial areas-NegligibleNegligible (<1%)Extreme (71-100%)High (Continuing)The group did not know specific examples, but development is likely; again a very small proportion of the wide range would be affected.
1.3Tourism & recreation areas-NegligibleNegligible (<1%)Moderate (11-30%)Moderate (Possibly in the short term, < 10 yrs/3 gen)Habitat loss from development of golf courses, park facilities, and campgrounds may take place, but there are no specific examples.
2Agriculture & aquaculture-NegligibleNegligible (<1%)Extreme (71-100%)High (Continuing)-
2.1Annual & perennial non-timber crops-NegligibleNegligible (<1%)Extreme (71-100%)High (Continuing)Northern parts of range have no agricultural activity. The scope is very small considering the wide range of this DU.
2.2Wood & pulp plantations------
2.3Livestock farming & ranching-NegligibleNegligible (<1%)Moderate (11-30%)High (Continuing)Possible, but not an issue for much of the extensive habitat. There are some dairy farms in NB, but no significant expansion is likely. Also true for QC.
2.4Marine & freshwater aquaculture------
3Energy production & mining-NegligibleNegligible (<1%)Serious (31-70%)High (Continuing)-
3.1Oil & gas drilling------
3.2Mining & quarrying-NegligibleNegligible (<1%)Serious (31-70%)High (Continuing)Aggregate mining is an issue mostly in southern Ontario but is not considered to be an issue across the rest of the range.
3.3Renewable energy------
4Transportation & service corridorsDLowSmall (1-10%)Serious - Moderate (11-70%)High (Continuing)-
4.1Roads & railroadsDLowSmall (1-10%)Serious - Moderate (11-70%)High (Continuing)Impacts are from road mortality during breeding migrations and from barriers to movements. Mostly a problem in southern Ontario (probably 5-10% of the distribution of this DU); otherwise scope would be negligible.
4.2Utility & service lines-NegligibleNegligible (<1%)Moderate (11-30%)High (Continuing)Pipeline from St. John through NB is proposed and might be built within the next 10 years; clearcuts for hydrolines are continuing, fragmenting habitats and affecting hydrology of ponds). Only a very small proportion of the wide range is affected.
4.3Shipping lanes------
4.4Flight paths------
5Biological resource useDLowRestricted (11-30%)Moderate (11-30%)High (Continuing)-
5.1Hunting & collecting terrestrial animals------
5.2Gathering terrestrial plants------
5.3Logging & wood harvestingDLowRestricted (11-30%)Moderate (11-30%)High (Continuing)Most populations on Canadian Shield or northward are on active forestry lands, but it is uncertain how much will be logged in the next 10 years, as forestry operates on long-term cycles. In Ontario, logging usually doesn't involve large clearcuts, but some type of selective logging is used. Water features are normally protected. Depending on the scale and type of logging. logging is not necessarily detrimental to salamanders.
5.4Fishing & harvesting aquatic resources-----Use of salamanders as fish bait is illegal, not considered an issue.
6Human intrusions & disturbance------
6.1Recreational activities------
6.2War, civil unrest & military exercises------
6.3Work & other activities------
7Natural system modifications-NegligibleNegligible (<1%)Serious (31-70%)High (Continuing)-
7.1Fire & fire suppression------
7.2Dams & water management/use-NegligibleNegligible (<1%)Serious (31-70%)High (Continuing)Many of the bigger ponds are old beaver ponds that have been there for decades or longer. Removal of beaver dams either drain a pond or change pond characteristics to the detriment of salamanders. While beaver dam removal can have a severe local impact, spread across the whole population the scope is likely negligible.
7.3Other ecosystem modifications-----Note: loss of sperm-donor populations through stochastic events is not scored here; this would most likely happen together due to other threats that affect both unisexuals and sperm-donors.
8Invasive & other problematic species & genes-NegligibleNegligible (<1%)Extreme (71-100%)High (Continuing)-
8.1Invasive non-native/alien species-NegligibleNegligible (<1%)Extreme (71-100%)High (Continuing)Introduced fish, invasive zooplankton (introduced with fish), emerging diseases, introduced aquatic plants (Phragmites australis) are included. In general, there are fewer introductions in northern areas than in the south. Fish stocking occurs mostly in larger water bodies (with no salamanders), but illegal introductions to salamander ponds may occur occasionally (but no data). Salamanders don't do well with predatory fish. Introduced zooplankton is becoming a big ecosystem-level problem in southern Ontario (native arthropods don't eat them). We have no information whether zooplankton or emerging diseases are a problem for this population.
8.2Problematic native species------
8.3Introduced genetic material------
9Pollution-NegligibleNegligible (<1%)UnknownHigh (Continuing)-
9.1Household sewage & urban waste water-NegligibleNegligible (<1%)UnknownHigh (Continuing)-
9.2Industrial & military effluents------
9.3Agricultural & forestry effluents-NegligibleNegligible (<1%)UnknownHigh (Continuing)-
9.4Garbage & solid waste------
9.5Air-borne pollutants------
9.6Excess energy------
10Geological events------
10.1Volcanoes------
10.2Earthquakes/tsunamis------
10.3Avalanches/landslides------
11Climate change & severe weather------
11.1Habitat shifting & alteration------
11.2Droughts-----Not considered an issue over the next 10 years.
11.3Temperature extremes------

Glossary

Impact
The degree to which a species is observed, inferred, or suspected to be directly or indirectly threatened in the area of interest. The impact of each threat is based on Severity and Scope rating and considers only present and future threats. Threat impact reflects a reduction of a species population or decline/degradation of the area of an ecosystem. The median rate of population reduction or area decline for each combination of scope and severity corresponds to the following classes of threat impact: Very High (75% declines), High (40%), Medium (15%), and Low (3%). Unknown: used when impact cannot be determined (e.g., if values for either scope or severity are unknown); Not Calculated: impact not calculated as threat is outside the assessment timeframe (e.g., timing is insignificant/negligible or low as threat is only considered to be in the past); Negligible: when scope or severity is negligible; Not a Threat: when severity is scored as neutral or potential benefit.
Scope
Proportion of the species that can reasonably be expected to be affected by the threat within 10 years. Usually measured as a proportion of the species' population in the area of interest. (Pervasive = 71-100%; Large = 31-70%; Restricted = 11-30%; Small = 1-10%; Negligible < 1%).
Severity
Within the scope, the level of damage to the species from the threat that can reasonably be expected to be affected by the threat within a 10-year or three-generation timeframe. Usually measured as the degree of reduction of the species' population. (Extreme = 71-100%; Serious = 31-70%; Moderate = 11-30%; Slight = 1-10%; Negligible < 1%; Neutral or Potential Benefit > 0%).
Timing
High = continuing; Moderate = only in the future (could happen in the short term [< 10 years or 3 generations]) or now suspended (could come back in the short term); Low = only in the future (could happen in the long term) or now suspended (could come back in the long term); Insignificant/Negligible = only in the past and unlikely to return, or no direct effect but limiting.