2008 Vol. 25 No. 4 Pages 101 - 136 Endangered Species UPDATE Science, Policy & Emerging Issues
School of Natural Resources and Environment THE UNIVERSITY OF MICHIGAN Endangered Species UPDATE Science, Policy & Emerging Issues
Contents 2008 Vol. 25 No. 4 Protecting Climate Refugia Areas: The case of the Gaviota Megan Banka...... Editor coast in southern California ...... 103 David Faulkner...... Associate Editor Devan Rouse ...... Associate Editor Michael Vincent McGinnis Johannes Foufopoulos...... Faculty Advisor Bobbi Low...... Faculty Advisor
Population and Politics of a Plover ...... 104 Advisory Board Fritz L. Knopf Richard Block Santa Barbara Victoria J. Dreitz Zoological Gardens
Susan Haig, PhD Spatial analysis of incidental mortality as a threat for Franciscana Forest and Rangeland Ecosystem Science Center, USGS dolphins (Pontoporia blainville) ...... 115 Oregon State University Marcelo H. Cassini Patrick O’Brien, PhD Observations on the reproductive seasonality of Atlantoraja ChevronTexaco Energy Research Company platana (Günther, 1880), an intensively fished skate endemic Jack Ward Thomas, PhD to the Southwestern Atlantic Ocean ...... 122 University of Montana Maria Cristina Oddone Gonzalo Velasco Subscription Information: The Endangered Species UPDATE is published four times per year by the School Focus on Nature: Bee Creek Cave Harvestman (Texella reddel- of Natural Resources and Environment at The University li)...... 130 of Michigan. Annual rates are: $78 institution, $33 indi- vidual, $25 student/senior, and $20 electronic. Add $5 for Rochelle Mason postage outside the US, and send check or money order (payable to The University of Michigan, Endangered Spe- cies UPDATE) to: Call for Submissions...... 131 Endangered Species UPDATE Instructions to Authors...... 132 School of Natural Resources and Environment The University of Michigan 440 Church Street Endangered Species Bulletin, September 2007...... Insert Ann Arbor, MI 48109-1041 Provided by the U.S. Fish and Wildlife Service (734) 763-3243; fax (734) 936-2195 E-mail: [email protected] http://www.umich.edu/~esupdate
Cover: A swimming skate. Photo courtesy of the U.S. Fish and Wildlife Service.
The views expressed in the Endangered Species UPDATE The Endangered Species UPDATE was made may not necessarily reflect those of the U.S. Fish & Wild- life Service or The University of Michigan. possible in part by Chevron Corporation and the U.S. Fish and Wildlife Service Division of Endangered Species.
102 Endangered Species UPDATE Vol. 25 No. 4 2008 Type Protecting Climate Refugia Areas:Title The case of the Gaviota coast in southern California
Michael Vincent Abstract McGinnis The designation of “climate refuge areas” should be an important part of a more integrated, ecosystem-based approach to protect endangered species. Identifying “climate refugia” areas should be a priority as resource managers Senior Lecturer, Insitute of Policy Studies, Senior Lec- begin to develop adaptive policies. This article describes policy innovation turer, School of Government, in California that includes important strategic elements and goals that can Victoria University of Wel- support the identification and protection of climate refugia for special status lington, P.O. Box 600, Level 5, species, and offers a case study of the Gaviota coast in southern California. West Wing Railway Building, The essay concludes with general recommendations for planning and policy Bunny Street, Wellington, New Zealand, 6011 development to support better protection of endangered species, and empha- sizes the importance of better local land-use planning. [email protected] The Importance of Climate Refugia This article describes recent policy innovation in California to develop an ecosystem-based approach to endangered species protection, with particular emphasis on the importance of identifying and protecting climate refugia in areas that are known as hot spots for threatened biodiversity. Climate refugia is a term that has emerged in the conservation biology literature that refers to an area that is inhabited by plants and animals during a period of continental climatic change (as a glaciation), and remains as an important area from which a new dispersion and speciation may take place after cli- matic disturbance (Klausmeyer and Shaw 2009). Scientists have begun to describe the cumulative impacts of the multiple-use of resources, and show that these impacts will likely exacerbate an ecosystem’s ability to adapt to climate disturbance (Worm et al. 2006; Halpern et al. 2009). Large-scale cli- mate disturbance will interact with and accelerate the existing anthropogenic pressures to endangered species. Indeed, scientists show that there are syn- ergies among extinction drivers under global climate change that reflect the cumulative impacts of the multiple-use of resources and climate disturbance (Brook et al. 2008). Policy innovation is needed to begin to foster large-scale, ecosystem-based adaptive conservation strategies to better protect endan- gered species in an era of climate change. Scholarly literature has expressed concern over the lack of region- or ecosystem-specific adaptation policy that can enable ecological resilience of threatened biodiversity with respect to climate disturbance. Current strat- egies include prescriptions at the state and federal government levels that support principles of ecosystem-based planning, and the establishment of Vol. 25 No. 4 2008 Endangered Species UPDATE 103 habitat reserves that support connectiv- Case Study: California’s Mediterra- ity or migration corridors, habitat buffer nean-type Ecosystem zones, ecological core areas, the control Mediterranean-type ecosystems (MTEs) of non-native invasive species, and col- have a rich natural history that includes laboration across administrative, eco- long periods of ecosystem and climate- nomic and political jurisdictions (Yaffee related disturbance events, such as et al. 1996). Local land use planning and changes in oceanographic and climate policy can play a fundamental role in the regimes (Klausmeyer and Shaw 2009). protection of sensitive habitat areas and MTEs are far from homeostatic or stable ecosystems (Brody 2004). systems (Blondel and Aronson 1999). This article describes recent policy in- The MTEs of the world are unique novation in California that focuses on the biomes that share a common natural need to develop adaptive policy at the re- history – species of these areas have had gional and local levels to protect climate to adapt to major climate events such as refugia throughout the state. Resource flooding, earthquakes, fire, and changes managers increasingly recognize that in the available of water and food. Run- adaptive policy must occur at regional del et al. (1998) note that MTEs are not levels with local land use decisions and steady-state ecosystems. For example, management actions that can protect en- the Los Angeles River in southern Cali- dangered species dependent on climate fornia can increase its flow 3,000 fold in a refugia. Protecting endangered species 24-hour period (Davis 1998). California and their habitats on private and public has experienced significant long-term lands will become increasingly difficult droughts or extreme hydrological shifts: as plants, animals and insects adjust their 892-1112 (220 years) and 1209-1350 (141 ranges in response to climate change. years). The longest drought of the 20th More importantly, conservation effort is Century lasted 6 years during 1987-1992. needed to protect endangered species in Species adapt to these changing envi- parts of their habitat range that are rela- ronmental conditions often by relying tively stable “climate refugia” – areas on climate refugia areas. that function as important source areas Human impacts on California’s MTE from which species can expand given have led to the degradation of a range of climate disturbance. This article offers habitats that serve the needs of endan- a number of preliminary strategies that gered species: 55% of the State listed ani- should be developed at regional levels mals and 25% of the threatened plants to begin to protect endangered species depend on wetlands; 43% of the Feder- and climate refugia areas. Among the ally listed species rely directly on wet- most recent recommendations in the sci- lands for survival; estuarine wetlands entific literature is the need to identify have decline by 75-90%; riparian com- and protect climate refugia across a rap- munities have declined by 90-95%; and idly changing landscape and seascape vernal pools have declined by 90% (Noss (Barnosky 2007). Evidence is accumu- et al. 1995; McGinnis 2009). The multi- lating that emphasizes the importance ple impacts of human activities will like- of managing climate refugia that have ly exacerbate the ability of endangered historically supported ecological resil- species to adapt to climate change in ience during periods of dramatic climate California (California Resources Agency disturbance, such as long term changes 2009; Halpern et al. 2009; Halpern et al. in environmental conditions. 2008). An example of the multiple use of MTEs is coastal urbanization, the ex- traction of energy resources, such as oil
104 Endangered Species UPDATE Vol. 25 No. 4 2008 and gas, agricultural activity, fishing, endangered species are to be protected. and the development of irrigation sys- In response to the California tems across southern California. These Governor’s Executive Order S-13-2008, uses, including the associated multiple the 2009 California Climate Adapta- impacts have synergistic and cumula- tion Strategy Discussion Draft [hereaf- tive impacts on ecosystems, and can ex- ter, Discussion Draft] (2009) outlines a acerbate the ability of native species to wide range of strategic elements that adapt to climate disturbance (Halpern include goals and objectives for pro- et al. 2008). The native plants unique to tecting biodiversity and special status California are very vulnerable to global species in light of increasing pressures climate change such that two-thirds of from climate change. While California these “endemics” could suffer more is encouraging local governments to than an 80 percent reduction in geo- develop plans that support these adap- graphic range by the end of the century tive strategies, there has been little if (Loarie et al. 2008). Loarie et al. (2008) any formal policy developed by local point to the need for identification and governments that supports the protec- better protection of existing climate tion of climate refugia for endangered refugia given the evidence of ecosystem species beyond the regulatory require- disturbance across California’s MTE. ments set forth by the state and federal governments, such as the Endangered Adaptive Biodiversity Policy Inno- Species Act, that require critical habitat vation in California designation. However, one county in California may be on the verge of estab- California may represent the first step lishing a new era of conservation poli- toward protecting climate refugia that cymaking that may influence how we will likely be needed for endangered can protect endangered species in the species. context of climate disturbance. In light of recent evidence of climate distur- Protecting Climate Refugia: the bance, policy innovation, local initiative case of the Gaviota coast in south and leadership will be needed if endan- California gered species are to adapt to the dramat- One consequence of climate disturbance ic changes in habitats. California policy in California will be a shift of biodiver- requires that the public and private sec- sity to the north (Loarie et al. 2008). Sci- tors participate in reducing California’s entists from the US Geological Survey greenhouse gas (GHG) emissions. In developed the Coastal Vulnerability addition, the existing California policy Index (CVI) to assess the physical vul- framework includes Assembly Bill (AB) nerability of the California coast. They 32, Senate Bill (SB) 375, SB 97, as well found that from San Luis Obispo to the as a host of additional topic-specific Mexico border, communities along this bills, that require counties and cities to coastline have “high” or “very high” reduce GHG. State law requires that vulnerability to climate change. One counties and cities develop Climate Ac- area identified as climate refugia is the tion Strategies. In December 2008, the Gaviota coastal (GC), which is part of California Air Resources Board released one of the most threatened “hot spots” the state’s Climate Change Scoping for biodiversity in the world (McGinnis Plan, which describes a range of strate- et al. 2009; National Park Service 2004; gies that are necessary for the state to Stein et al. 2000). The GC extends from reduce its GHG emissions to 1990 levels Coal Oil Point to Point Sal and includes by 2020. A move beyond a focus or em- the coastal watersheds and terrestrial phasis in reducing GHG is required if foothill and mountain ecosystems as-
Vol. 25 No. 4 2008 Endangered Species UPDATE 105 sociated with the transverse Santa Ynez spatial scales, decision makers increas- Range. Map 1 depicts the GC and areas ingly recognize that implementation of high conservation value (Conception must occur at the local level with local Coast Project 2004). land use decisions. With respect to the In 2004, the National Park Ser- planning process for identification and vice (NPS) completed a feasibility study protection of climate refugia, Figure 1 that included an evaluation of the GC depicts the ideal planning process to as California’s second national sea- begin to address endangered species is- shore (the only national seashore is the sues at the county level. Map 1: Point Reyes National Seashore north of The following planning stages are Conservation Priorities San Francisco). According to the NPS recommended to begin to identify and in the Graviota Coast. Source: Conception (2004), the GC includes two of the most protect climate refugia at the local lev- Coast Project 2004. biologically diverse ecoregions in the el. world, and some of the highest concen- Stage 1 - Identification of Pressures. trations globally of important, rare spe- Climate change will have direct and in- cies in the nation. Of the approximately direct pressures and impacts on areas 1,400 plant and animal species estimat- designated as critical habitat and envi- ed to exist within GC, there are 24 fed- ronmental sensitive habitat areas (ES- erally- or state-listed threatened or en- HAs). Existing protected areas, such dangered plant and animal species and as ecological reserves, wildlife areas, another 60 considered rare or of special undesignated lands, mitigation sites, concern. The NPS concluded that the and easements will likely be impacted quality and scope of GC’s natural and by climate change. A more comprehen- cultural resources qualify it for inclu- sive, ecosystem-based and cumulative sion in the National Park system. But assessment, that includes the identifica- because of the preponderance of private tion of multiple pressures or stressors land in the area, the NPS found that it on endangered species and their habi- would not be feasible to add Gaviota to tat, should be included in local land use the National Park system at that time. planning. In March 2009, Santa Barbara Coun- Stage 2 - A comprehensive vulner- ty initiated the long-term development ability analysis should be conducted to of a Climate Action Strategy (CAS) that establish the type and extent of poten- would include or consider biodiver- tial climate changes (such as sea level sity concerns. In addition, the County rise, storm surges, and changing ocean Board of Supervisors voted to support conditions) and how these changes will a Gaviota Coast Rural Regional Plan- impact natural habitats and endan- ning (RRP) process, which may lead gered species. Smaller communities to the development of new policies in are particularly vulnerable as they lack the County’s General Plan and Local many important resources for effective Coastal Plan (LCP) that can protect en- adaptation (California Resources Agen- dangered species. The County’s CAS cy 2009). A vulnerability analysis must and RRP processes are unusual insofar include detailed mapping that contains as they include biodiversity protection “measures of physical risk,” identifica- measures, and the local effort may rep- tion of threatened habitats, among oth- resent the first local effort in California er factors. Coupled with an inventory, with regards to climate change and en- this analysis can determine the most dangered species protection. successful places that exist for ensuring While climate-related policy devel- migration of sensitive habitat, such as opment will necessarily include broad coastal wetlands, and species.
106 Endangered Species UPDATE Vol. 25 No. 4 2008 The vulnerability analysis should tect biodiversity. Such a working group be used as one foundation to develop could also include the use of a Scientific adaptation strategies (both overarching Advisory Panel to assist in the develop- and specific) to protect endangered spe- ment of guiding principles to protect cies. As much as possible, each adap- biodiversity. tive strategy should be accompanied Stage 3 - Identification of Climate by case studies that elucidate that strat- Refugia. A number of guiding princi- egy and guidance on how it should be ples should be emphasized to identify implemented. For example, changes in climate refugia including the following creek, wetland, and coastal bluff buffer goals: areas and other adaptive strategies that o Maintain healthy, connected, are needed to protect sensitive habitat genetically diverse populations areas should be incorporated in local o Improve resiliency of existing plans. In addition, the vulnerability habitats in order to maintain existing or analysis should carefully depict and de- new assemblages of species scribe information gaps. o Reduce non-climate stressors on To assist in the regional vulner- ecosystems (i.e. invasive species) ability analysis, regional interagency o Protect coastal wetlands and ac- and working groups representing gov- commodate sea level rise ernment and non-governmental organi- o Consider climate change models zations, e.g. state parks, and the private as well as historical data when making sector may be needed to discuss and projections recommend adoption of policies to pro- o Employ monitoring and adap-
Figure 1: The Planning Process for Establishing Climate Refugia.
Vol. 25 No. 4 2008 Endangered Species UPDATE 107 tive management mation becomes available. o Adopt adaptation approaches that reduce risks to species and habitats Conclusion and provide time for species evolution The long-term impacts of climate and development. change on special status species are With respect to the identifica- likely to be dramatic. In the context of tion of climate refugia, the precaution- climate change, the goal of protecting ary principle must be employed to buf- special status species is exacerbated by fer against scientific uncertainty. There the cumulative or synergistic impacts are synergistic effects and positive feed- of the multiple-use of resources and the back loops of human-induced climate expected pressures from large-scale cli- change, other anthropogenic impacts, mate disturbance. This article reviewed and natural disturbances, all of which recent policy development in California make decisions about policy solutions and offered a number of recommenda- difficult. tions for cities and counties to begin The identification of climate to develop biodiversity conservation refugia should include priority man- measures that can better protect endan- agement goals to preserve core habitat gered species and climate refugia. Pol- and migration corridors. Since cli- icy innovation that moves beyond the mate disturbance will continue to cause emphasis of reducing greenhouse gases plant communities and species’ ranges and supports the ecological resilience to shift, adaptive corridors of continu- and adaptation of species that are es- ous habitat must be preserved to enable sential to the maintenance of goods and future shifts in ranges and resiliency in services provided by a healthy, produc- ecosystems. Routes containing viable tive ecosystem is needed today. native habitats for plant pollination vectors (wind and insect) and which Acknowledgment This article is based on the report by McGinnis connect existing and predicted future et al (2009) entitled “Developing Adaptive Policy to habitat areas can be mapped and pro- Climate Disturbance in Santa Barbara County”. The tected. The identification of climate author would like to thank University of California at refugia should also include policy de- Santa Barbara Associated Students Coastal Fund for velopment that emphasizes a careful grants that supported the writing of this article. The opinions or recommendations described in this article review and assessment of existing land are those of the author, and may not represent those use plans and policies, such as Local of the University of California or UCSB’s Associated Coastal Plans, and other elements such Students Coastal Fund. as biological thresholds and environ- Literature Cited mental sensitive habitat areas. Barnosky, A.D. 2008. Climate change, refugia, Stages 4, 5 and 6 - Development of and biodiversity: where do we go from here? Adaptive Strategic Elements. City and An editorial comment. Climate Change 86: county plans should be amended to 29-32. include special conservation measures Blondel, J. and J. Aronson. 1999. Biology and Wildlife of the Mediterranean Region. Oxford that can support the ecological resil- University Press, Oxford. ience of endangered species and cli- Brody, S.D. 2004. Implementing the Principles of mate refugia. Amendment and revision Ecosystem Management Through Local Land of city and county general plans should Use Planning. Population & Environment 24, 6: 1573-1578. support an integrated, ecosystem-based California Resources Agency. August 4, 2009. approach that includes resources that California Climate Adaptation Strategy Dis- support long-term monitoring of cli- cussion Draft. http://www.climatechange. mate refugia areas, and land use ele- ca.gov/adaptation/ ments should be revised as new infor- Davis, M. 1998. Ecology of Fear. Metropolitan
108 Endangered Species UPDATE Vol. 25 No. 4 2008 Books, New York. Halpern, B.S. et al. 2009. Mapping cumulative human impacts to California Current. Conser- vation Letters. 1-11. http://www.nceas.ucsb. edu/GlobalMarine/impacts Halpern, B.S., K.L. McLeod, A.A. Rosenberg, and L.B. Crowder. 2008. Understanding cumula- tive and interactive impacts as a basis for eco- system-based management and ocean zoning. Ocean and Coastal Management 51:203-211. Klausmeyer, K.R. and M.R. Shaw. 2009. Climate Change, Habitat Loss, Protected Areas and the Climate Adaptation Potential of Species in Mediterranean Ecosystems Worldwide. PLoS ONE 4(7): e6392. doi:10.1371/journal. pone.0006392 Little, S.J., R.G. Harcourt, and A.P. Clevenger. 2002. Do wildlife passages act as prey-traps? Biological Conservation 107, 2: 135-145. Loarie, S.R., B.E. Carter, K. Hayhoe, S. McMahon, R. Moe. 2008. Climate Change and the Future of California’s Endemic Flora. PLoS ONE 3(6): e2502. doi:10.1371/journal.pone.0002502 McGinnis, M.V., W. Su, A. Willsey, and J. Tiegs. 2009. Developing Adaptive Policy to Climate Disturbance in Santa Barbara County. Ocean and Coastal Policy Center White Paper. Uni- versity of California Santa Barbara. Marine Science Institute. September. Miller, C.I., N.L. Stephenson, and S.L. Stephens. 2007. Climate change and forests of the future: managing in the face of uncertainty. Ecological Applications 17: 2145-2151. National Park Service. 2004. Final Gaviota Coast Feasibility Study. March 9. http://www.nps. gov/pwro/gaviota/ Noss, R.F., E.T. LaRoe III, and J.M. Scott. 1995. Endangered Ecosystems of the United States: A preliminary assessment of loss and degra- dation. Biological Report 28. U.S. Department of the Interior. Washington, D.C. Rundel, P.W., G. Montenegro, and F.M. Jaksic, eds. 1998. Landscape Disturbance and Bio- diversity in Mediterranean-type Ecosystems. Springer, Berlin. Worm, B. et al. 2006. Impacts of Biodiversity Loss on Ocean Ecosystem Services. Science 314: 787-790. Yaffee, S.L., A.F. Phillips, I.C. Frentz, P. Hardy, S. Maleki, and B.E. Thorpe. 1996. Ecosystem Management in the United States: An Assess- ment of Current Experience. Washington, DC: Island Press.
Vol. 25 No. 4 2008 Endangered Species UPDATE 109 Type Title
Populations and Politics of a Plover
Fritz L. Knopf1,3 The Mountain Plover (Charadrius montanus) is a species that inhabits cold, Victoria J. Dreitz2 xeric-shrub landscapes of the western United States where it breeds in low- density, scattered populations primarily in Colorado, New Mexico, and Wyo- ming. To the east of this landscape, the plover is found most predictably 1Senior Scientist, Retired, US Department of Interior, 713 on prairie-dog (Cynomys spp.) towns within western prairies from northern Boulder Circle, Fort Collins, Montana into Nuevo Leon and San Luis Potosi. These landscapes also his- CO 80524 torically supported large herds of bison (Bison bison). With near eradication of bison and decreased prairie-dog presence on the landscape, the eastern breeding range of this plover became fragmented and generally of poorer 2Avian Researcher, Colorado Division of Wildlife, 317 West quality. Thus, in contrast to westerly xeric landscapes, the current popula- Prospect, Fort Collins, CO tion of plovers in prairie landscapes is now restricted to fragments within 80526 the Oklahoma panhandle, north through the southwestern corner of Kansas, most of eastern Colorado, the southwestern corner of Nebraska, and eastern [email protected] Wyoming and Montana (Knopf and Wunder 2006). First collected by John Kirk Townsend along the Sweetwater River of Wy- oming in 1834 and subsequently named the Rocky Mountain Plover by John James Audubon, this species of relatively nondescript plumage received little conservation attention for 150 years. It was never described as historically abundant, and only scattered references to the species appeared in the litera- ture--much like comments are lacking about any non-charismatic species on the western frontier of America in the 1800s. Despite occasional collections of a few birds or clutches of eggs, one specific comment about plover occur- ring in high densities was that of an early bison hunter from the early 1870s who had killed about 200 in an hour near Dodge City, Kansas (Sandoz 1954). Those likely were from flocks of migrating birds that then flew directly south to winter in South Texas. Today, we believe that most migrants move more to the south along the Front Range of Colorado then swing west across south- ern New Mexico and Arizona to California and then north into the Central Valley of California. Historical records of migrating plovers are almost non- existent within the Great Basin (Knopf and Wunder 2006). Forty years ago, Graul and Webster (1976) estimated a continental pop- ulation of 214,200–319,220 breeding Mountain Plovers, with 20,820 in the “stronghold” of Weld Co., CO. Conservation concern for the species was first expressed when the U.S. Fish and Wildlife Service (FWS) raised questions about population declines from historic levels (Leachman and Osmundson 1990). Unpublished guesses as to the contemporary population of plovers at that time oscillated around 6,000-10,000 birds, much reduced from the his-
110 Endangered Species UPDATE Vol. 25 No. 4 2008 Mountain plover with torical estimation of Graul and Webster. birds in eastern Colorado. Personal full clutch. Photo credit: This difference reflected a severe de- communications from researchers and Fritz L. Knopf cline in the population of Weld County, FWS personnel projected an additional Colorado, used to extrapolate the earlier 2,000-5,000 plovers in Wyoming and continental projection. In 1999 the FWS 1,500 in Montana. Thus, plover breed- officially proposed listing the species ing populations in these three critical as “Threatened,” with evidence of de- states totaled ~12,800-15,800 birds, with creasing population size being statisti- additional small populations known cally supported by >3% annual decline to occur in Kansas, Nebraska, New across 30 years of Breeding Bird Survey Mexico, Oklahoma, and Utah. Since all data (USFWS 1999). populations seemed to be stable, FWS Beginning in the late 1990s, many subsequently decided to withdraw studies inventoried plover populations the proposed listing of the plover as a in major breeding areas across the spe- threatened species under The Endan- cies range. Wunder and others (2003) gered Species Act (ESA) in September estimated a population of 2,300 birds of 2003 (USFWS 2003). in the previously undescribed high-el- Additional studies following the evation population of South Park, Colo- decision to withdraw the plover list- rado. Summarizing recent inventories ing proposal confirmed, and slightly across eastern Colorado, FWS conclud- expanded, the continental population ed that there were an additional 7,000 estimate. Plumb and others (2005)
Vol. 25 No. 4 2008 Endangered Species UPDATE 111 Mountain plover on the shrubsteppe in Carbon County, Wyoming. Photo credit: Fritz L. Knopf.
conducted a statewide survey within nental estimate of breeding plovers to- historical plover locales in Wyoming taling a minimum of 15,700 birds. The to estimate a minimum of 3,300 breed- true continental population is certainly ing birds. This number was within the larger by an unknown quantity given range of estimates used in the FWS deci- (1) documented small populations in sion. However, the authors emphasized contiguous states (Ellison-Manning and the “minimum” nature of the estimate White 2001, Bly et al., 2008, McConnell and it still may be well short of a true et al., 2009), (2) a potentially significant statewide population due to the inad- population in New Mexico and (3) an equate representation of private lands unknown population in Mexico (Knopf in both the historical database and con- and Wunder 2006). temporary sampling protocol. On 16 November 2006, Forest Tipton and others (2009) conducted Guardians and the Biological Conser- a systematic statewide survey of east- vation Alliance challenged the with- ern Colorado. That study defined the drawal of the proposal to list the plover Colorado population on the eastern as Threatened (Forest Guardians, et al. plains to be 8,577 birds, slightly larger v Ken Salazar et al., Case No. 3:06-cv- than the previous FWS projection of 02560-MMA-BLM). The plaintiffs and 7,000. Childers and Dinsmore (2008) the Federal defendants filed a settle- subsequently estimated 1,028 birds in ment agreement on August 8, 2009, Northeastern Montana, supportive of agreeing to reconsider the FWS 9 Sep- the earlier FWS figure of 1500 state- tember 2003, decision to withdraw the wide. The Wyoming and Colorado proposed listing of the mountain plover studies together, lead to a revised conti- (68 Federal Register 53083) and to sub-
112 Endangered Species UPDATE Vol. 25 No. 4 2008 mit to the Federal Register a notice re- plovers in prairie landscapes include opening the proposal to list the Moun- surfaces impacted by activities such as tain Plover and providing for public military maneuvers, pipeline construc- comment by July 31, 2010. Thus, the tion, petroleum development, and ag- decision to withdraw the proposed list- ricultural conversion of prairies. The ing of the species in 2003 was ‘vacated’, most attractive of these sites are those and the plover is once again proposed agricultural fields that have either been as a threatened species under the ESA. recently tilled or are crop-idle at the time The agreement calls for a final listing plovers arrive on the breeding grounds. decision by 1 May 2011. Plovers nest on those fields, and subse- The listing process for the Mountain quent tillage has been suspected to de- Plover was rather unique for the FWS. stroy nests and eggs. Recent research, Whereas most species come to be listed however, shows that nest/egg destruc- following an initial petition to FWS fol- tion by tillage practices appears to be a lowed by an FWS review, the impetus compensatory rather than an additive for increased conservation concern for constraint on reproduction; the propor- this plover came from research within tion of nests lost to tillage on relatively government research. The initial iden- predator-free croplands is comparable tification of plover declines came from to that proportion lost to predators in basic science (to 1999) within (vs. exter- contiguous, native landscapes (Dreitz nal to) the Department of Interior. FWS and Knopf 2007). biologists within Ecological Services In winter months plovers were his- pursued the review and ultimately pro- torically found in the coastal uplands posed the species for listing. The pro- and interior valleys of California. Those cess is a rather unique example of how habitats have been almost universally government science and operations converted to urban/suburban and ag- were intended to work within the De- ricultural landscapes, respectively. partment of Interior. Also, whereas the Whereas the preferred habitats on those scientific record for most species listed xeric plains near the ocean and the in- under ESA is often limited by a lack of tensely grazed sites of the San Joaquin historical and contemporary data, the and Sacramento valleys only occur in science available to the proposal deci- isolated patches on the modern land- sion for Mountain Plover in 2003 was scape, plovers are now found in large some of the best available to date for numbers mostly on agricultural fields any species. (Knopf and Rupert 1995). Favored If FWS decides to list this plover as fields include those that have been re- threatened, any plan to promote its re- cently tilled, or recently harvested and covery will be politically challenging. followed by either burning or grazing The plover is neither a montane spe- by domestic sheep to clean the field cies (as named) nor a species of shores before replanting (Wunder and Knopf and wetlands like other members of the 2003). Charadriidae. Rather, again, it is an Critics of listing the plover (includ- upland associate of xeric landscapes to ing agricultural and rural development the west of the Colorado Front Range organizations among others) note that that also occurs where disturbances al- the behavioral flexibility documented ter prairie landscapes to the east of the for the species argues strongly against Front Range. Prairie-dogs created both Mountain Plovers being limited by historical and contemporary habitats habitat. The high rate of nesting suc- for plovers (Dreitz et al., 2005). Contem- cess documented range-wide (Knopf porary sites that also attract breeding and Wunder 2006, Dinsmore et al. 2002)
Vol. 25 No. 4 2008 Endangered Species UPDATE 113 and high survival rate of breeding (Din- Movements and home ranges of Mountain smore et al. 2003) and wintering (Knopf Plovers raising broods in three Colorado land- scapes. Wilson Bulletin 117:128-132. and Rupert 1995) birds further argue Dreitz, V. J. and F. L. Knopf. 2007. Mountain that the contemporary population (al- Plovers and the politics of research on private beit historically depressed) is viable. lands. BioScience 57:681-687. Alternatively, proponents argue that the Ellison-Manning, A.E. and C.M. White. 2001. current plover population (1) is drasti- Breeding biology of Mountain Plovers (Char- adrius montanus) in the Uinta Basin. Western cally reduced from the Graul and Web- North American Naturalist 61:223-228. ster 1976 projection, (2) has experienced Graul, W.D., L.E. Webster. 1976. Breeding status widespread loss of native habitats, and of the Mountain Plover. Condor 78: 265–267. (3) is dependent upon another species Knopf, F.L. and J.R. Rupert. 1995. Habits and habitats of Mountain Plovers in California. of conservation concern (prairie-dogs). Condor 97: 743–751. Regardless of the direction of the Knopf, F.L. and M.B. Wunder. 2006. Mountain decision, the forthcoming process will Plover (Charadrius montanus). The Birds of certainly stimulate much political dia- North America Online. (A. Poole, Ed.) Ithaca: logue. If listed, however, FWS will have Cornell Laboratory of Ornithology: http://bna. birds.cornell.edu/BNA/account/Mountain to develop a plan for working with ag- Plover/. ricultural producers to manage crop- Leachman, B. and B. Osmundson. 1990. Status ping practices, which goes well beyond of the Mountain Plover: A literature review. contemporary ESA vs. private-lands U.S. Fish and Wildlife Service. Golden, Colo- rado. conflicts. The timing of agricultural McConnell, S., T.J. O’Connell, D.M. Leslie, Jr., practices is weather-driven, and inter- and J.S. Shackford. 2009. Mountain Plovers in jecting ESA considerations into daily Oklahoma: distribution, abundance, and habi- management decisions at the level of lo- tat use. Journal of Field Ornithology 80:27-34. cal farms would have a major economic Plumb, R.E., F.L. Knopf, and S.H. Anderson. 2005. Minimum population size of Mountain impact on the agricultural community. Plovers breeding in Wyoming. Wilson Bulle- Ironically, that political and administra- tin 117:15-22. tive theater will focus on a semi-desert Sandoz, M. 1954. The buffalo hunters. Hasting species that historically and currently House, New York. Tipton, H.C, P.F. Doherty, Jr., and V.J. Dreitz. occurs secondarily in altered shortgrass 2009. Abundance and density of Mountain prairie landscapes. Plover (Charadrius montanus) and Burrowing Owl (Athene cunicularia) in Eastern Colorado. Auk 126:493-499. Literature Cited U. S. Fish and Wildlife Service. 1999. Endangered Bly, B. L., L. Snyder, and T. VerCauteren. 2008. and threatened wildlife and plants: proposed Migration chronology, nesting ecology, and threatened status for the Mountain Plover. breeding distribution of Mountain Plover Federal Register: 64(30):7587-7601. (Charadrius montanus) in Nebraska. Nebraska U. S. Fish and Wildlife Service. 2003. Endan- Bird Review 76:120-128. gered and threatened wildlife and plants: Childers, T.M. and S.J. Dinsmore. 2008. Den- withdrawal of the proposed rule to list the sity and abundance of Mountain Plovers Mountain Plover as threatened. Federal Reg- in Northeastern Montana. Wilson Bulletin ister 68(174):53083-53101. 120:700-707. Wunder, M.B. and F.L. Knopf. 2003. Impe- Dinsmore, S.J., G.C. White, and F.L. Knopf. 2002. rial Valley agriculture is critical to wintering Advanced techniques for modeling avian nest Mountain Plovers. Journal of Field Ornithol- survival. Ecology 83:3476-3488. ogy 74:74-80 Dinsmore, S.J., G.C. White, and F.L. Knopf. 2003. Wunder, M.B., F.L. Knopf, and C.A. Pague. Annual survival and population estimates of 2003. The high-elevation population of Moun- Mountain Plovers in Southern Phillips Coun- tain Plovers breeding in Colorado. Condor ty, Montana. Ecol. Applications 13:1013-1026. 105:654-662. Dreitz, V.D., M.B. Wunder, and F.L. Knopf. 2005.
114 Endangered Species UPDATE Vol. 25 No. 4 2008 Spatial analysis of incidental mortality as a threat for Franciscana dolphins (Pontoporia blainvillei)
Marcelo Hernán Fisheries bycatch is considered one of the main threats for most large marine Cassini vertebrates, such as seabirds, marine mammals, turtles and sharks (review, among others, by Shaughnessy et al. 2003, Read et al. 2006, Zydelis et al. 2009). Incidental entanglement is a direct human threat with a straightforward ef- GEMA group, DCB and fect on species mortality. Three problems arise when results from bycatch CONICET, Universidad Nacional de Luján, Rutas 5 y research are translated into wildlife managment actions. First, predictions 7 (6700), Luján, Provincia de of population trends are normally weak because large-scale estimates of de- Buenos Aires, Argentina mographic parameters are difficult to generate (e.g., Moore and Read 2008). Second, bycatch impact is rarely compared to other threats, such as depletion [email protected] of prey base, ecosystem changes, habitat degradation or disease. The effects of these stressors are not always as conspicuous as bycatch, and may be more difficult to evaluate (Taylor et al. 2007). Third, fisheries can offer short-term benefits to some marine vertebrates that overshadow the long-term costs of this threat. An emerging method since the development of GIS and spatial statis- tics is the comparison between distributions of species and threats that are formalized in habitat suitability models or ecological-niche models. These models relate presence-absence or abundance observations based on random or stratified field sampling with stressors and other environmental variables (Guisan and Thuilier 2005, Sims et al. 2008). Franciscana dolphins (Pontoporia blainvillei) are small cetaceans restrict- ed to shallow waters of the South Atlantic Ocean, from southeastern Brazil (18º25’S) to northern Patagonia (42º10’S) (Crespo et al. 1998). It has been clas- sified as ‘vulnerable’ by the IUCN (Reeves et al 2008). There is no current abundance estimate for the species as a whole. Incidental entanglement or bycatch of Franciscana dolphins was reported repeatedly: Di Beneditto et al. (2001), Kinas (2002), Dans et al. (2003), Freitas Netto and Barbosa (2003), Secchi (2003), Bordino and Albareda (2005), Cap- pozzo et al. (in press). IUCN defines incidental mortality in gillnet -fisher ies as the main threats to this species (Reeves et al. 2008). Secchi et al. (2001) first estimated bycatch in the overall Franciscana population via population abundances based on aerial surveys. They calculated that removal by gillnets ranged between 1.1% and 3.5% per year. The Scientific Committee of the In- ternational Whaling Commission has noted that incidental mortality of 1% is sufficient for concern about the conservation future of coastal dolphins. However the various assumptions and parameters of these estimations are difficult to test. For example, Secchi et al. (2001) counted an average of 4.25
Vol. 25 No. 4 2008 Endangered Species UPDATE 115 individuals per flight and extrapolated and Rio de Janeiro states, Brazil; MU2= an overall abundance of 42,000 Francis- waters off Sao Pablo, Paraná and Santa cana dolphins (Reeves et al. 2008). It is Catarina states, Brazil; MU3= waters expected that slight changes in param- off Rio Grande Sul State (Brazil) and eters assumptions could produce sig- Uruguay; MU4= waters off Argentina. nificant changes to these results. Two studies have estimated abundance I used a spatial approach to ana- via aerial surveys for MU3 (Secchi et al. lyze the role of incidental mortality as 2001) and MU4 (Crespo et al. 2009). In a threat to Franciscana dolphins. I com- MU3, 8 flights of equal length (185.4 km pared information from different -ar except one of 129.8 km) with a single- eas of their distribution with different engine aircraft were conducted at the levels of fishery activity. I followed the end of summer 1996 and distributed main assumption of most habitat mod- equally between morning and after- els, i.e., that distribution of population noon. In MU4, 17 flights were conducted abundance is positively related to habi- of variable lengths, ranging from 185.2 tat qualities (Guisan and Thullier 2005). km to 564.9 km, with a double-engine If incidental entanglement is a main aircraft in summer 2003 and autumn mortality factor, then areas with higher 2004. On the 13th and 18th of February, incidental mortality should have lower two flights were conducted on the same population densities. day, thus afternoon flights were not Based on the genetic structure of considered in the analyses to minimize the species, Secchi et al. (2003) proposed pseudo-replicate effects and dolphin four management units (MU) (Fig. 1). behavioral response to aircraft noise of MU1= coastal waters of Espírito Santo the first daily flight. Relative abundance
Figure 1: Geographic range of Franciscana dolphins (Ponto- poria blainvillei) with four man- agement units (MU) and MU4 divided into four sectors.
116 Endangered Species UPDATE Vol. 25 No. 4 2008 Figure 2: Population abun- dances, bycatches and artisan fishery activity in the sixth areas of the distribu- tion range of Fran- ciscana dolphins. Captures per unit of effort (CPUE) = 100 x deaths x km of net-1x d-1. Fishing was aver- aged with data from 2001 to 2007. MU1 and MU2 without data on abundance.
of Pontoporia in each MU is expressed as (2004) and Cappozzo et al. (2007) from number of dolphins per km surveyed. MU4. Bycatch is expressed in ‘captures I avoided the use of absolute estima- per unit of effort’ (CPUE units), which tions of abundance to minimize er- consisted of the number of dolphins rors in parameter estimations of equa- killed in nets, divided by the km of tions. Because there are several reports fishery nets of the total float, and the from MU4 , I divided it in four sectors: number of fishing days per year. At MU4A, MU4B, MU4C (corresponding MU1, there were no comparable mea- to northern, central and southern coasts surements of bycatch effect, but Netto of Buenos Aires Province, respectively), and Barbosa (2003) counted 13 records and MU4D, corresponding to northern of Franciscana dolphins stranded along coast of Patagonia (Fig. 1). the Espirito Santo coast presenting Di Beneditto (2003) provided - sys wounds that may suggest interactions tematic data on annual incidental mor- with fisheries between 1994 and 2001. tality rate from MU2 , Secchi et al. (2001) MU1 and MU2 have similar character- from MU3, and Bordino and Albareda istics with regard to fishery activity (Di
Vol. 25 No. 4 2008 Endangered Species UPDATE 117 Beneditto and Netto 2008), therefore by- gesting that catchability depends on catch incidence at MU1 was estimated several co-varying factors, such as me- using the same fishing effort calculated teorological and economic conditions, by Di Beneditto (2003). This value of individual behavior of fishermen and CPUE was included only for illustrative social and foraging behavior of the spe- purpose, although it is well established cies (Crespo et al. 2009 ). For example, that bycatch is comparatively very if dolphins tend to be more aggregated low at MU1 (review by Di Beneditto and at the same time overlap with fish- and Netto 2008). Information on - fish ing areas, a clumped distribution pat- ing activity was obtained from official tern could be associated with predation websites of governmental agencies of for sciaenid fish in nursery areas (Cre- Brazil and Argentina (date: 09/09/09) spo et al. 2009 ). who are responsible for fishery activity Geographical differences on by- regulation: Instituto Brasileiro do Meio catch mortality did not appear to influ- Ambiente e dos Recursos Naturais Ren- ence population abundance, given that ováveis and Secretaría de Agricultura, the number of dolphins/km surveyed Ganadería, Pesca y Alimentación de la between the areas did not differ. This Argentina. unexpected result could be caused by Data on abundance, bycatch inci- various mechanisms: (1) different ini- dence and fishing activity are summa- tial population abundances between rized in Figure 2. There were no statisti- areas, (2) meta-population dynamics cal differences in the relative abundance that dilute geographical differences, (3) between MU3, MU4A, MU4B and MU4C compensation of the detrimental effects (Kruskal-Wallis ANOVA by ranks, H2 = by benefits of the use of nets, and/or (4) 1.94, P = 0.38, n = 22 with data on MU4C overestimation of the impact of bycatch and D together in a category). Howev- mortality on population growth rate. I er, there were significant differences in will briefly analyze each hypothesis. bycatch incidence, mainly due to a sub- 1) There is no information of his- stantially high value observed in MU4A torical abundances of Franciscana’s (H = 14.0, P = 0.007, n = 17) and in fish- dolphins, so it is not possible to test ery activity, due to a substantially high directly the first mechanism. An indi- value observed in MU4B (H = 40.7, P < rect approach is to project a popula- 0.0001, n = 7 yrs x 7 areas). Cappozzo et tion growth model into the past. Kinas al. (2007) provided information both on (2002) developed such model, with the Franciscana mortality and fishing effort equation: between 2002 and 2003 from 16 locali- r ties of MU4A, B and C: San Clemente N(t-1) = Nt/e (1-ht) (1) del Tuyu, Las Toninas, Santa Teresita, Mar del Tuyú, La Lucila del Mar, San Kinas (2002) used, for MU3, a Bernardo, Mar de Ajó, Villa Gesell, Mar growth rate of r = -0.053, and a fraction del Plata, Quequén - Necochea, Cla- of the population dying in year t as a
romecó, Monte Hermoso, Villa del Mar, result of entanglement ht = 0.047. Secchi Puerto Rosales - Ingeniero White. The et al. (2001) estimated total population
correlation of mortality and fishing ef- size in MU3 as Nt = 42,078 dolphins in fort among these localities was not sig- approximately 64.000 km2. At MU4A,
nificant (Spearman rank correlation,r s = estimations are: Nt = 8,279 dolphins in 0.23, P = 0.41, n = 16). approximately 22.000 km2 (Crespo et al. In summary, there was no clear 2009) and a maximal entanglement rate
positive relationship between fishery of ht = 0.097 (Bordino and Albareda, cit- activity and Franciscana mortality, sug- ed by Crespo et al. 2009). In accordance
118 Endangered Species UPDATE Vol. 25 No. 4 2008 to these estimations, present abundance brates develop foraging strategies that proportion of MU3: MU4A is almost are designed to maximize food-search- 5:1. Assuming the same value of r, con- ing strategies. Fishery gillnets facilitate stant impact of entanglements and lack finding prey locationand bycatch can of density-dependency, it is possible to occur when predators are attracted to apply equation (1) to predict popula- these overabundant and fixed patches tion densities at MU3 and MU4A in the of food. This phenomenon is evident past. Applying this equation suggests for seabirds for which gillnets do not that abundances in MU3 and MU4A normally represent a risk of passive en- could have been equalized 30 years be- tanglement, however, they may drown fore. At that time, population density in when they actively attempt to snatch MU4A should have been almost triple baited hooks deployed by longline fish- that in MU3. There are no obvious rea- ing vessels (Gales 1997). sons to expect such spatial differences Díaz López (2006) described how in population densities between Brazil gillnet fishing appeared to benefit the and Argentina when stranding effect Mediterranean bottlenose dolphin (Tur- is eliminated or substantially reduced siops truncatus) in Sardinia, Italy. These from calculations. dolphins were frequently observed 2) Another possibility is that those feeding near the location of nets, sug- populations exposed to a high bycatch gesting dolphins try to exploit a concen- incidence retain high levels of popula- trated food source at gillnets. Interviews tion density due to immigration pro- of fishermen in Argentina revealed that cesses, as in a typical source-sink system they frequently observe Franciscana (Pulliam 1988). However, recent studies dolphins near the boats when they in- using tracking devices on Franciscana stall gillnets (Negri, unpubl. data). It dolphins showed that animals did not appears that, like Tursiops sp., Francis- tend to disperse significantly from the cana dolphins also approach gillnet target location, which suggests a clear areas, although there is no evidence resident pattern for the studied animals that they increase foraging efficiency (Bordino and Wells 2005, Bordino et al. by doing so. If the benefit in terms of 2008). A new series of genetic studies survival and breeding success provided that identified several genetic stocks by this alternative source of food equals along the relatively small geographic the cost due to incidental mortality, no range of this species confirms low lev- apparent effect will be measured in the els of interaction between populations short term until the population collaps- (Secchi et al. 2003, Mendez et al. 2008). es. These results do not support the source- 4) The final consideration is that the sink model. effect of incidental mortality rates have 3) Another possible mechanism is been overestimated due to biases in es- that Franciscanas receive some kind of timations of abundance. Equations for benefit from artisan fishing that com- calculating population abundance and pensates the cost of entanglement. The overall impact of entanglement require main potential benefit is facilitation of the use of several parameters. Poten- food patch detection. Foraging theory tial error terms of these parameters are has investigated the effect of food dis- difficult to calculate. Field data are re- tribution on foraging behavior and its stricted to a small fraction of the coast- population consequences (Sutherland line representing only approximately 1996). Fish schools are typically charac- 0.7% of the possible range in the MU3 terized as rich food patches with an un- subpopulation (Reeve et al. 2008). Thus, predictable distribution. Marine verte- final numbers frequently contain un-
Vol. 25 No. 4 2008 Endangered Species UPDATE 119 controlled and large error terms that re- Mamıferos Acuaticos de America del Sur. Monte- duce reliability of conclusions. Reeve et video, Uruguay. Cappozzo, H. L., M. F. Negri, J. E. Pérez, F. al. (2008) stated that estimates of Fran- Monzón, D. Albareda and J. F. Corcuera. 2007. ciscana abundance and, consequently, Incidental mortality of Franciscana dolphin of density or entanglement, need to be (Pontoporia blainville) in Argentina. Latino treated cautiously. American Journal of Aquatic Mammals 6: in This paper provides the first ap- press, ISSN 1676-7497. Crespo, E. A., G. Harris and R. González. 1998. plication of a spatial approach to the Group size and distributional range of the analysis of anthropogenic threats to franciscana, Pontoporia blainvillei. Marine Franciscana dolphin survival. Bycatch Mammal Science 14(4): 845-849. does not produce the expected spatial Crespo, E. A., S. N. Pedraza, F. M. Grandi, L. S. Dans and G. Garaffo. 2009. Abundance pattern in population abundance if in- estimation of Franciscana dolphins, Ponto- cidental entanglement is a main threat poria blainvillei, in Buenos Aires province, to this species. Franciscana dolphins Argentina, from aerial surveys. Marine are threatened by several human im- Mammal Science on line, DOI, 10.1111/j.1748- pacts, other than bycatch, mainly: (1) 7692.2009.00313.x. Dans, S., M. K. Alonso, S. N. Pedraza and E. A. water pollution, (2) human depletion Crespo. 2003. Incidental catch of dolphins in of dolphin food, and (3) marine debris trawling fisheries off Patagonia, Argentina, swallowed by the dolphins. Conserva- Can populations persist? Ecological Applica- tion agencies do not have resources to tions 13: 754-762. Di Beneditto, A. P. M. 2003. Interaction between solve all these problems at once, thus gillnet fisheries and small cetaceans in north- criteria to define priorities is essential. ern Rio de Janeiro, Brazil: 2001–2002. Latin It is urgently required that research on American Journal of Aquatic Mammals 2: Franciscana dolphins provides clues to 79-86. evaluate the precise impact of inciden- Di Beneditto, A. P., R. Ramos and N. R. W. Lima. 2001. Sightings of Pontoporia blainvillei (Ger- tal bycatch on their conservation. vais & D’Orbigny, 1844) and Sotalia fluviatilis (Gervais, 1853) (Cetacea) in South-eastern Bra- Acknowledgements zil. Brazilian Archives of Biology and Technol- M. F. Negri kindly provided information on ogy 44: 291-296. Franciscana dolphins. M. H. C is researcher of the Díaz Lopez, B. 2006. Interactions between Medi- the Argentinean Research Council (CONICET). terranean bottlenose dolphins (Tursiops trunca- GEMA group is supported by the Department of tus) and gillnets off Sardinia, Italy. ICES Jour- Basic Sciences from the University of Lujan and nal of Marine Science 63: 946-951. CONICET. Freitas Netto, R. F. and L. A. Barbosa. 2003. Ce- taceans and fishery interactions along the Espírito Santo State, Southeastern Brazil dur- LITERATURE CITED ing 1994-2001. The Latin American Journal of Bordino, P. and D. Albareda. 2004. Incidental Aquatic Mammals 2: 57-60. Gales, R. 1997. Al- mortality of Franciscana dolphin Pontoporia batross populations: status and threats. Pages blainvillei in coastal gillnet fisheries in north- 20-45 in G. Robertson and R. Gales, eds. Alba- ern Buenos Aires, Argentina. Technical Paper tross biology and conservation. Surrey Beatty SC/56/SM11 presented at the International and Sons, Chipping Norton. Whaling Commission Meeting. Sorrento, Ita- Guisan, A. and W. Thuiller. 2005. Predicting spe- ly. cies distribution: offering more than simple Bordino, P. and R. S. Wells. 2005. Radiotracking habitat models. Ecology Letters 8: 993-1009. of Franciscana Dolphins (Pontoporia blainvillei) Kinas, P. G. 2002. The impact of incidental kills in Bahia Samborombon, Buenos Aires, Argen- by gillnets on the franciscana dolphin (Ponto- tina. 16th Biennial Conference on the Biology poria blainvillei) in southern Brazil. Journal of of Marine Mammals. San Diego, California. Marine Science 70: 409-421. Bordino, P., R. S. Wells and M. A. Stamper. 2008. Mendez, M., H. C. Rosenbaum and P. Bordino. Satellite tracking of Franciscana dolphins (Pon- 2008. Conservation genetics of the francis- toporia blainvillei) in Argentina. Preliminary cana dolphin in Northern Argentina, popula- information on ranging, diving and social pat- tion structure, bycatch impacts, and manage- terns. 130 Reunion de Trabajo de Especialistas en ment implications. Conservation Genetics 9: 419-435.
120 Endangered Species UPDATE Vol. 25 No. 4 2008 Moore, J. E. and A. J. Read. 2008. A Bayesian of Cetacean Research and Management 3: uncertainty analysis of cetacean demography 95-100. and bycatch mortality using age-at-death data. Secchi, E. R., J. Y. Wang, B. Murray, C. C. Roccha- Ecological Applications 18: 1914-1931. Campos and B. N. White. 1998. Populational Netto, R. F. and L. A. Barbosa. 2003. Cetaceans differences between Franciscanas, Pontoporia and fishery interactions along the Espírito San- blainvillei, from two geographical locations as to State, southeastern Brazil during 1994–2001. indicated by sequences of mtDNA control re- Latin American Journal of Aquatic Mammals gion. Canadian Journal of Zoology 76: 1-6. 2: 57-60. Shaughnessy, P. D., R. J. Kirkwood, M. Caw- Pulliam, H. R. 1988. Sources, sinks, and popu- thorn, C. Kemper and D. Pemberton. 2003. lation regulation. American Naturalist 132: Pinnipeds, cetaceans and fisheries in Austra- 652-661. lia: a review of operational interactions. Pp. Read, A. J., P. Drinker and S. Northridge. 2006. 135-156, in N. J. Gales, M. A. Hindell and R. Bycatch of marine mammals in the US and Kirkwood, R, eds. Marine mammals: fisheries, global fisheries. Conservation Biology 20: tourism and management issues. CSIRO Pub- 163-169. lishing, Washington, D.C. Reeves, R. R., M. L. Dalebout, T. A. Jefferson, L. Sims, M., T. Cox and R. Lewison. 2008. Identify- Karczmarski, K. Laidre, G. O’Corry-Crowe, ing spatial patterns in fisheries bycatch: using L. Rojas-Bracho, E. R. Secchi, E. Slooten, B. D. models to improve the stability of bycatch esti- Smith, J. Y. Wang, A. N. Zerbini and K. Zhou. mates and aid fisheries management. Ecologi- 2008. Pontoporia blainvillei. In: IUCN 2009. cal Applications 18: 649-661. IUCN Red List of Threatened Species. Version Sutherland, W. J. 1996. From individual behav- 2009.1.
Vol. 25 No. 4 2008 Endangered Species UPDATE 121 Observations on the reproductive seasonality of Atlantoraja platana (Günther, 1880), an intensively fished skate endemic to the Southwestern Atlantic Ocean
Maria Cristina Abstract Oddone1,2 Specimens of the La Plata skate (Atlantoraja platana) were collected Gonzalo Velasco1 monthly from commercial fishing landings at Guarujá, São Paulo State, Brazil, from March of 2005 to April of 2006. One hundred males rang- 1Instituto de Oceanografia, ing from 13.1 to 70.0 cm and 88 females ranging from 12.5 to 76.0 cm Universidade Federal do Rio of total length were collected and their gonads analysed to determine Grande, Caixa Postal 474, CEP maturity stages. Gonadosomatic and hepatosomatic indexes did not 96201-900, Rio Grande-RS, Brazil. significantly vary among seasons between the sexes. Ovulation and egg-laying were continuous throughout the year. These observations suggest an annual cycle with eventual -though not well delimited- [email protected] peaks in the reproductive activity. This pattern has been reported for skates of the same genus and for other species. Atlantoraja platana is intensely exploited, though as a non-target species, and retained for exportation over the South and Southeast Brazilian coast. For these reasons the species is already considered ‘vulnerable’ by the IUCN Red list of Threatened Species. Present data may be the base for future studies in order to protect the populations of A. platana from��������������� local dis- appearance.
Introduction Genus Atlantoraja Menni, 1972, is endemic to the Southwestern Atlantic Ocean (McEachran and Aschliman 2004). The La Plata skate’s (Atlantoraja platana) (Günther 1880) distribution ranges from São Paulo’s littoral area to Argenti- na, and is common in Rio Grande do Sul State in Southern Brazil (Figueiredo 1977). In Southern Brazil, it is found at depths of 40-100 m (Vooren 1997), though Marçal (2003) recorded its occurrence at up to 231 m deep. In the Southeastern Brazilian continental shelf, A. platana is commonly caught in the range of 20-120 m deep (Oddone and Amorim 2007). The assessment of chondrichthyan populations requires a quantitative approach to the study of reproduction (Walker 2005). Oddone and Amorim (2007) reported the size at maturity of male and female A. platana in South- eastern Brazil. Data on the reproduction of A. platana were also provided by Marçal (2003), Oddone et al. (2008) and Oddone and Vooren (2008). How- ever, so far, the trend in the seasonality of the reproduction of this species is unknown. But Vooren and Klippel (2005) demonstrated that intensive fisher-
122 Endangered Species UPDATE Vol. 25 No. 4 2008 ies in the South-western Atlantic have known in order to make decisions on led to overexploitation of several spe- stock management of chondrichthyan Figure 1: cies of demersal elasmobranchs, such as fishes. Map of the study area, southeast Brazil, south- the congeneric Atlantoraja castelnaui and The conservation status of A. pla- western Atlantic Ocean. A. cyclophora, already ‘endangered’ and tana is considered ‘vulnerable’ by the Symbols represent the to- ‘vulnerable’ species according to the IUCN Red list of Threatened Species tal number of fishing hauls IUCN Red list of Threatened Species. (San Martin et al. 2007). This is a matter (when registered by fish- ermen) in the area where (Hozbor et al. 2004, Massa et al. 2006 ). of concern for a commercially exploited samples of Atlantoraja plat- Over the past thirty years, catches species because when life history char- ana were collected. of rajoids (skates) have increased in the acteristics are coupled with the selective
western Atlantic, mainly as a by-catch of removal of large individuals (as is the bony-fish target fisheries, yet, sustaina- case for this species) of a given popu- ble catch rates are completely unknown lation subjected to intense fishery pres- (Frisk et al. 2002). This situation is also sure, such a population may become valid for the Brazilian continental shelf, highly susceptible to overexploitation where bottom trawling fisheries affect and even disappearance, as has been populations of A. Platana, which is in- the case for several rajoids (Brander cidentally captured. Thus, the knowl- 1981; Hoenig and Gruber 1990). Speci- edge of all the events compounding the mens of Atlantoraja spp. are commonly reproduction of a species needs to be landed and sold in Santos and Guarujá
Vol. 25 No. 4 2008 Endangered Species UPDATE 123 (São Paulo state, Brazil), especially the larg- 1.0 g, a precision scale was used. Classifica- est individuals (Oddone, unpublished data). tion of the specimens by maturity stage was In the present paper, we aim to analyze the done according to criteria defined by Odd- trend of the reproductive variables for A. one et al. (2007) for Rioraja agassizi (Müller platana on an annual basis for this species in and Henle, 1841). The presence of sperm in southeastern Brazil , which is critical infor- the males’ seminal vesicle was noted. mation for developing a successful conser- To compare the reproductive activity in vation program. males and females among seasons, the gona- dosomatic and hepatosomatic indexes were Materials and Methods calculated as: GSI=(gonad weight/M )*100 Specimens of Atlantoraja platana were col- G and HSI=(liver weight/MG)*100, respective- lected monthly from commercial fishing ly. To use parametric/non-parametric tests, landings at Guarujá, São Paulo State, Brazil, normality and homoscedasticity of the vari- from March of 2005 to April of 2006 by eight ables were tested by Lilliefors’ and Levene’s fishing vessels regularly bringing (once or tests, respectively. Parametric comparisons twice a month) samples of this species. The were performed using a Student t-test. study area was situated between latitudes Comparisons among monthly HSI and GSI 23°37’S and 27°40’S, at depths between 10 were performed using Kruskal-Wallis’ H- and 120 m (Fig. 1). test (Sokal and Rohlf 1995). Variables range Specimens were measured to the near- was expressed along with the mean value est millimetre below in total length (TL) and and the standard deviation, as ‘range (mean weighted as gutted (M ) mass (g). Gonad G ±SD)’. Significance level considered in all and liver weight (g) were recorded for both cases was 0.05. sexes. Electric scales used had 1 and 5 g pre- cision. For weighting material of less than
Figure 2: Seasonal variation of hepatosomatic (HSI) for males and females of At- lantoraja platana, from March 2005 to March 2006. Whiskers represent the non-outlier minimum and maximum (whiskers’ middle point represents the median).
124 Endangered Species UPDATE Vol. 25 No. 4 2008 Figure 3: Seasonal variation of go- nadosomatic index (GSI) for males and females of Atlantoraja platana, from March 2005 to March 2006. Whiskers represent the non-outlier minimum and maximum (whiskers’ middle point represents the median).
Results Discussion In all, 100 males ranging from 13.1 to We are aware that much more data 70.0 cm of total length (TL) were collect- should be obtained in order to infer the ed for analysis. Regarding the females, reproductive cycle of this species. How- a total of 88 specimens ranging from ever, this species occurs less frequently 12.5 to 76.0 cm TL were recorded. than other rajoids in the SE Brazil trawl The HSI peaked in summer for fisheries’ catches, as shown by Oddone the females, while it was lowest for (2007). Nevertheless, according to the the males. However, it did not signifi- observations presented in this paper cantly vary among seasons in males and information about this species in
(H(3,10)=6.67, p=0.0830) nor females other regions, and even other related
(H(3,10)=1.34, p=0.7184) (Fig. 7a). Just the species in the same region, we inferred opposite pattern was observed for the that female A. platana undergo an annu- GSI, which showed a trend to be low- al cycle, with continuous reproduction est in summer for the females, when throughout the year, and eventual sea- was highest for the males. This varia- sonal variation (though not statistically tion of the GSI was neither significant significant). Marçal (2003) analysed the for males (H(3,10)=3.37, p=0.3515) nor for reproductive trends of A. platana for females (H(3,9)=2.84; p=0.4162, Fig. 7b). summer and winter in Southern Brazil, Egg-bearing females were observed recording the GSI and HSI of egg-bear- in spring (n=2), summer (n=2) and win- ing females in both seasons and found ter (n=1). Males with sperm in the semi- no seasonal variation. nal vesicle were caught in spring (n=2) Our �������������������������������hypothesis of lack of seasonal- and summer (n=3). ity in the reproduction of A. platana is,
Vol. 25 No. 4 2008 Endangered Species UPDATE 125 R. agassizi has an annual cycle, also with year long ovulation that peaks twice a A 128.0 cm total length year (during Sep- and 410 g total weight tember and De- immature female of cember, austral Atlantoraja platana, Spring) (Oddone captured in Novem- ber 2005 off southeast et al., 2007). In Brazil. Black bar rep- Argentinean and resents 3.0 cm. Photo Uruguayan wa- credit: Maria Cristina ters, Colonello et Oddone al. (2007) also re- corded continu- ous reproduction for R. agassizi, with a peak in the reproductive activity of males during late spring and summer and evidence of a par- tially defined an- nual cycle with two peaks for the as stated above, reinforced by observa- females, one from tions done in other species inhabiting November (Spring) to February (Sum- the Southwestern Atlantic, including mer) and another in July (Winter). We those belonging to the genus Atlantoraja infer that this presumably occurs in A. Menni, 1972, i.e., A. castelnaui (Ribeiro, platana as well. Braccini and Chiara- 1907) and A. cyclophora (Regan, 1903). monte (2002) reported a continuous re- Oddone and Vooren (2005) proposed productive cycle during the year, with a that A. cyclophora in Southern Brazil maximum number of females carrying have an annual cycle with continued re- egg-cases in summer, for Psammobatis productive activity, but with no peaks; extenta Garman , 1913 . or an annual cycle with at least one Examples of these patterns observed peak in reproductive activity in spring in species of other areas can be seen in and/or autumn. Oddone et al. (2008), Raja ‘pulchra’ Liu, 1932 in the Yellow Sea, with a large data set for the same spe- which undergo egg-laying throughout cies elsewhere, demonstrated that the the year except in August and Septem- second hypothesis was correct. A simi- ber, peaking from April to June and lar pattern, with a peak in the GSI and during November and December (Yeon HSI detected in autumn was reported et al. 1997). Annual reproductive cycles for female A. castelnaui for the area in have been also described for Raja clava- question (Oddone et al., 2008). ta Linnaeus, 1758 in British waters and For other sympatric genera, as Rio- Dipturus chilensis (Guichenot, 1848) in raja Whitley, 1939 (also endemic to the the Chilean coast ��������������������(Holden 1975; Fuent- southwestern Atlantic), it was observed ealba and Leible 1990). that for the southeastern Brazilian area, The observations carried out for all
126 Endangered Species UPDATE Vol. 25 No. 4 2008 A 70.0 cm total length and 2490 g total weight mature male of At- lantoraja platana, captured in No- vember 2005 off southeast Brazil. Black bar represents 2.0 cm. Photo credit: Maria Cristina Oddone.
these rajoid species agree with one of year. the three reproductive cycles proposed The same data set as the present by Wourms, continuous reproduction data was reported for sexually resting with eventual peaks in reproductive females of A. platana by Oddone and activity, (1977) for elasmobranch fishes Amorim (2008) . A sexual resting period and would also apply to A. platana. So for the females to the ovary level was far, this is surely the case of the females. noted in several rajoid species (Holden For the males, reproductive activity et al. 1971; Capapé 1974, 1976; Capapé probably takes place continuously dur- and Quignard 1974; Oddone and Voo- ing the year with no apparent peaks. ren 2005; Ebert 2005, Oddone et al. This affirmation should be confirmed 2007). However, as in other species, the through histological examinations of temporal length of that period is very the testicular tissues throughout the difficult to assess, especially because it
Vol. 25 No. 4 2008 Endangered Species UPDATE 127 is not synchronized to the population 48–49 level, but occurring at the species level, Capapé, C. 1974. Contribution à la biologie des Rajidae des côtes tunisiennes. 2. Raja radula. as it was observed in A. cyclophora (Odd- Archives de I’nstitut Pasteur Tunis 51: 211-228. one and Vooren 2005). For determining Capapé, C. 1976. Contribution à la biologie des more details on this phenomenon, more Rajidae des côtes tunisiennes. 3. Raja clavata, observations should be done on a larger Linné, 1758: répartition géographique et ba- number of specimens and over a longer thymétrique, sexualité, reproduction, fécon- dité. Bulletin du Museum national d’Historie time period. naturelle 393: 907–922. Even when taken as by-catch, skates Capapé, C. and Quignard, J. P. 1974. Contribution are often subjected to high fishing mor- à la biologie des Rajidae des côtes tunisiennes. tality and as a consequence, some spe- 1. Raja miraletus, Linné, 1758: répartition géo- graphique et bathymétrique, sexualité, repro- cies have been extirpated from large duction, fécondité. Archives de I’nstitut Pasteur regions (Stevens et al., 2000) and at least Tunis 51: 39-60 nine skate species have already disap- Colonello, J. H., García, M. L. and Lasta, C. A. peared from their distribution range 2007. Reproductive biology of Rioraja agassizi (Brander 1981; Dulvy and Reynolds from the coastal southwestern Atlantic eco- system between northern Uruguay (34ºS) and 2002). Our deeper concern is that data northern Argentina (42ºS). Environmental����������������� Bi- presented here may be the base for fu- ology of Fishes DOI 10.1007/s10641-007-9239-0, ture studies on this species that may 2007. contribute to its conservation status and Dulvy, N. K. and Reynolds, J. D. 2002. Predicting extinction vulnerability in skates. Conserva- also support rational fisheries manage- tion Biology 16, 440-450 ment in order to protect the populations Ebert, D. A. 2005. Reproductive biology of skates, of Atlantoraja spp. from disappearance. Bathyraja (Ishiyama), along the eastern Bering Population information such as repro- Sea Continental Slope. Journal of Fish Biology ductive season and area, altogether 66: 618-649 Figueiredo, J. L. 1977. Manual de Peixes Marin- with other crucial reproductive param- hos do Sudeste do Brasil. Introdução, cações, eters as size-at-maturity (provided for raias e quimeras. Museu de Zoologia da Uni- this species by Oddone and Amorim, versidade de São Paulo 2008) and reproductive potential are es- Frisk, M. G., Miller, T. J, Fogarty, M. J. 2002. The population dynamics of little skate Leucoraja sential for developing management and erinacea, winter skate Leucoraja ocellata, and conservation plans. barndoor skate Dipturus laevis: predicting ex- ploitation limits using matrix analyses. ICES Acknowledgements Journal of Marine Science 59: 576-586 Special thanks to P. L. Mancini, W. A. Nor- Fuentealba, M. and Leible, D. 1990. Perspectivas bis, P. G. Kinas, skippers G. A. do Nascimento de la pesquería de la raya volantín Raja (Dip- and P. Silva (CV ‘Cigano do Mar’ II and III); A. turus) flavirostris: estudio de edad, crecimiento Faria and J. dos Santos (CV ‘Antares I’ and ‘Po- y algunos aspectos reproductivos. In: Barbieri lares III’); A. de Oliveira Neto (CV Franzese III); MA (ed) Perspectivas de la Actividad Pesquera O. Vicente (CV ‘São Paulo IV’); W. da Silva (CV en Chile pp. 227-236 ‘São Paulo II’); E. Nascimento dos Santos (CV Hoenig, J. M. and Gruber, S.H. 1990. Life-history ‘Dourado e Araguaia’); G. A. do Nascimento patterns in the elasmobranchs: implications (CV ‘São Paulo’ VI and XI) and J. da Silva (CV for fisheries management. Pratt H., Gruber S. ‘Jangadeiro XV’). The first author had a FAPESP H., Taniuchi, T. (eds) Elasmobranchs as living (Fundação de Amparo à Pesquisa do Estado de resources: advances in the biology, ecology, São Paulo, Brazil) PhD grant during the develop- systematics, and the status of the fisheries. ment of this research. U.S. Department of Commerce. National Oce- anic and Atmospheric Administration Techi- Literature cited cal Report NMFS, 90: 1-16 Braccini, J. M. and G. E., Chiaramonte. 2002. Holden, M. J. D., Rout, W. and Humphreys, C. N. Reproductive Biology of Psammobatis extenta. 1971. The rate of egg laying by three species of Journal of Fish Biology, 61, 272-288 ray. Journal du Conseil - Conseil International Brander, K. 1981. Disappearance of common pour l’Exploration de la Mer 33: 335-339 skate Raia batis from Irish Sea. Nature 290: Holden, M. J. D. 1975. The fecundity of Raja clavata in British waters. Journal du Conseil -
128 Endangered Species UPDATE Vol. 25 No. 4 2008 Conseil International pour l’Exploration de la (Müller and Henle, 1841) (Chondrichthyes, Mer 36: 110-118 Rajidae), in southeast Brazil, SW Atlantic Hozbor, N, Massa A. and Vooren, C. M. 2004. Ocean. Scientia Marina 71(3): 593-604 Atlantoraja castelnaui, http:// www.iucnredlist. Oddone, M. C & Amorim, A. F. 2008. Size at ma- org. Cited 12 Feb 2007 turity of Atlantoraja platana (Günther, 1880) Marçal, A. S. 2003. Biologia reprodutiva de Atlan- (Chondrichthyes: Rajidae: Arhynchobatinae) toraja platana (Günther 1880) (Elasmobranchii: in the SW Atlantic Ocean. Journal of Fish Biol- Rajidae) no Sul do Brasil. MSc. Dissertation, ogy, 72, 1515–1519 Universidade Federal de Rio Grande. San Martín, J. M., Stehmann, M. F. W. & Kyne, P. Massa, A., Hozbor, N. & Vooren, C.M. 2006. At- M. 2007. Atlantoraja platana. In: IUCN 2009. lantoraja cyclophora. In: IUCN 2009. IUCN Red IUCN Red List of Threatened Species. Version List of Threatened Species. Version 2009.2. 2009.2.
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