Rearing environment influences boldness and prey acquisition behavior,and brain and lens development of bull trout

Animals reared in barren captive environments exhibit different developmental trajectories and behaviors than wild counterparts. Hence, the captive phenotypes may influence the success of reintroduction and recovery programs for threatened and endangered species. We collected wild bull trout embryos from the Metolius River Basin, Oregon and reared them in differing environments to better understand how captivity affects the bull trout Salvelinus confluentus phenotype. We compared the boldness and prey acquisition behaviors and development of the brain and eye lens of bull trout reared in conventional barren and more structurally complex captive environments with that of wild fish. Wild fish and captive reared fish from complex habitats exhibited a greater level of boldness and prey acquisition ability, than fish reared in conventional captive environments. In addition, the eye lens of conventionally reared bull trout was larger than complex reared captive fish or same age wild fish. Interestingly, we detected wild fish had a smaller relative cerebellum than either captive reared treatment. Our results suggest that rearing fish in more complex captive environments can create a more wild-like phenotype than conventional rearing practices. A better understanding of the effects of captivity on the development and behavior of bull trout can inform rearing and reintroduction programs though prediction of the performance of released individuals.     

Development of restoration techniques for Hawaiian thrushes: Collection of wild eggs,artificial incubation,hand‐rearing,captive‐breeding,and re‐introduction to the wild

From 1995 to 1999, two species of endemic Hawaiian thrushes, `Oma`o (Myadestes obscurus) and Puaiohi (M. palmeri), were captive‐reared and re‐introduced into their historic range in Hawai`i by The Peregrine Fund, in collaboration with the U.S. Geological Survey–Biological Resources Division (BRD) and the Hawai`i State Department of Land and Natural Resources. This paper describes the management techniques that were developed (collection of wild eggs, artificial incubation, hand‐rearing, captive propagation, and release) with the non‐endangered surrogate species, the `Oma`o; techniques that are now being used for recovery of the endangered Puaiohi. In 1995 and 1996, 29 viable `Oma`o eggs were collected from the wild. Of 27 chicks hatched, 25 were hand‐reared and released into Pu`u Wa`awa`a Wildlife Reserve. Using the techniques developed for the `Oma`o, a captive propagation and release program was initiated in 1996 to aid the recovery of the endangered Puaiohi. Fifteen viable Puaiohi eggs were collected from the wild (1996–1997) to establish a captive breeding flock to produce birds for re‐introduction. These Puaiohi reproduced for the first time in captivity in 1998 (total Puaiohi chicks reared in captivity 1996–1998 = 41). In 1999, 14 captive‐bred Puaiohi were re‐introduced into the Alaka`i Swamp, Kaua`i. These captive‐bred birds reproduced and fledged seven chicks in the wild after release. This is the first endangered passerine recovery program using this broad spectrum of management techniques (collection of wild eggs, artificial incubation, hand‐rearing, captive‐breeding, and release) in which re‐introduced birds survived and bred in the wild. Long‐term population monitoring will be published separately [BRD, in preparation]. Zoo Biol 19:263–277, 2000. © 2000 Wiley‐Liss, Inc.     

Captive breeding and rearing of critically endangered Mauritius fodies Foudia rubra for reintroduction

In‐situ captive rearing of endangered passerines for reintroduction has rarely been used as a conservation tool. Nests of Mauritius fodies threatened with predation by introduced mammalian predators were harvested from the wild, and chicks were reared to independence for release onto an offshore, predator‐free island. The daily probability of the survival was higher in captivity than in the wild, and 69 chicks were reared to fledging of which 47 would have been expected to fledge in the wild. Harvesting of nests probably had little impact on the wild population. Captive breeding trials on Mauritius fodies showed that large numbers of individuals could be produced for a release program from a small number of pairs if enough space was provided. Artificial incubation of passerine eggs and rearing of chicks can be used to increase the productivity of endangered taxa. Zoos can play an important role in in‐situ conservation programs through provision of avicultural expertise and training of local staff. Zoo Biol 27:255–268, 2008. © 2008 Wiley‐Liss, Inc.     

Adaptations to Captivity in the Butterfly Pieris brassicae (L.) and the Implications for Ex situ Conservation

Captive breeding has been suggested as a method of conserving many threatened vertebrates, and is increasingly being proposed as a valuable conservation strategy for invertebrates. Potential genetic problems associated with ex situ conservation are widely recognized, but a further issue has received less attention: the possibility that populations will undergo adaptation to the captive environment, rendering them less well adapted to survival in the wild. We investigated six traits related to dispersal and reproduction in a culture of the large white butterfly Pieris brassicae (L.), that had been captive for c. 100–150 generations, and in recently wild stock reared simultaneously in a common environment. Individuals in the captive culture were heavier, with smaller wings and lower wing aspect ratios. Females from the captive culture laid many more eggs in cage experiments, and had higher ovary mass at the time of peak egg production. These differences are consistent with adaptation to captive conditions. Over time, similar evolutionary changes may affect invertebrates reared in ex situ conservation programmes, decreasing the likelihood that these species can be re-established in the wild. Although the timescale over which most vertebrates are likely to adapt to captivity is longer, and the traits involved will be different, invertebrates like P. brassicae may also provide a model of potential problems in long-term ex situ conservation programmes for both invertebrates and vertebrates. We suggest that measures to reduce or slow adaptation to captivity should be introduced alongside measures to reduce deleterious genetic effects in captive populations.     

Genetic diversity in wild and reared populations of the Japanese bitterling <Emphasis Type="Italic">Tanakia tanago</Emphasis> (Cyprinidae)

 The Japanese bitterling Tanakia tanago is an endangered cyprinid species; thus, captive breeding programs are being conducted in various facilities as ex situ conservation. To examine the genetic diversity in one wild and three reared populations, and its changes during the process of captive breeding, sequences of the mitochondrial cytochrome b gene and control region were determined. The wild population, collected in 1993, was monomorphic. Although the reared population that originated from the wild population was almost monomorphic, a rare haplotype, distinct from all others by a relatively large sequence divergence, was also observed. In the other reared populations, some degree of genetic diversity had been maintained. A reared hybrid population, which originated from a mixture of three distinct populations, showed the greatest genetic diversity. These results suggest considerable genetic diversity within and among populations of T. tanago in the past. Although a loss of genetic diversity was observed in some year-classes of reared populations, there was no tendency for genetic diversity to decrease as a result of captive breeding, probably because offspring were obtained from multi-year-class parents in the captive breeding program. Accordingly, this breeding method should be appropriate for conserving the genetic diversity of T. tanago. Received: June 12, 2002 / Revised: December 3, 2002 / Accepted: December 16, 2002     

Seasonal butterfly design: morphological plasticity among three developmental pathways relative to sex,flight and thermoregulation

The temperate‐zone butterfly Pararge aegeria can use three developmental pathways corresponding to different seasonal cohorts: (1) development with a pupal winter diapause resulting in early spring adults; (2) development with a larval winter diapause resulting in late‐spring adults and (3) direct development resulting in summer or second generation adults. In order to test adaptive predictions, we compared variation in flight‐ and thermoregulation‐related morphology among adult males and females from the three pathways using both field data (i.e. wild‐caught butterflies) and experimental breeding data (i.e. reared under different photoperiod regimes). Morphological patterns among the pathways were largely similar in the field and rearing data. Seasonal patterns differed between the sexes for most traits, including (relative) size measures and wing colour. Our results suggest sex‐related, adaptive seasonal plasticity for morphological traits related to flight behaviour in a multivoltine insect.     

Captive breeding for reintroduction: influence of management practices and biological factors on survival of captive kaki (black stilt)

An important component of the restoration strategy for the critically endangered kaki or black stilt (Himantopus novaezelandiae) is captive breeding for release. Since 1981 1,879 eggs were collected from wild and captive pairs, with birds laying up to four clutches. Eggs were incubated artificially and most chicks reared by hand until released as juveniles (about 60 days) or sub‐adults (9–10 months). Because survival in captivity is a significant determinant of the number of birds available for release, we wished to identify sources of variation in mortality to assess potential impacts of management on productivity. Hatchability was 78% for captive‐laid eggs and 91% for wild‐laid eggs. Survival of hatched eggs was 82% by 10 months of age for both wild and captive birds. Most egg mortality occurred early in incubation and around hatching: the timing of mortality was unaffected by whether birds were captive or wild, hybrid or pure kaki, or when eggs were laid. Heavier hatchlings showed higher initial survival, as did chicks from wild parents. Hatchlings from fourth‐laid eggs showed lowest survival, even though hatchling mass tended to increase with hatch order. Survival of chicks subjected to major health interventions was 69% after 4 months. No differences in survival were found between different genders, hybrids and pure kaki, hand‐reared or parent‐reared birds, chicks hatching early or late in the season, different seasons, different‐sized groups of chicks, chicks reared in different brooders, juveniles kept in different aviaries, and chicks from subsequent clutches. Birds subjected to minor health interventions were equally likely to survive as healthy chicks (82%). Survival was high despite aggressive management (quadruple clutching and collecting late in the season). Differences between captive and wild birds suggest further improvements could be made to captive diet. Wide variation in hatchability between parent pairs substantiates the practice of breaking up poorly performing pairs. Zoo Biol 0:1–16, 2005. © 2005 Wiley‐Liss, Inc.     

POPULATIONS OF MONARCH BUTTERFLIES WITH DIFFERENT MIGRATORY BEHAVIORS SHOW DIVERGENCE IN WING MORPHOLOGY

The demands of long‐distance flight represent an important evolutionary force operating on the traits of migratory species. Monarchs are widespread butterflies known for their annual migrations in North America. We examined divergence in wing morphology among migratory monarchs from eastern and western N. America, and nonmigratory monarchs in S. Florida, Puerto Rico, Costa Rica, and Hawaii. For the three N. American populations, we also examined monarchs reared in four common environment experiments. We used image analysis to measure multiple traits including forewing area and aspect ratio; for laboratory‐reared monarchs we also quantified body area and wing loading. Results showed wild monarchs from all nonmigratory populations were smaller than those from migratory populations. Wild and captive‐reared eastern monarchs had the largest and most elongated forewings, whereas monarchs from Puerto Rico and Costa Rica had the smallest and roundest forewings. Eastern monarchs also had the largest bodies and high measures of wing loading, whereas western and S. Florida monarchs had less elongated forewings and smaller bodies. Among captive‐reared butterflies, family‐level effects provided evidence that genetic factors contributed to variation in wing traits. Collectively, these results support evolutionary responses to long‐distance flight in monarchs, with implications for the conservation of phenotypically distinct wild populations.     

Induction of diapause egg production in Eurytemora affinis by their own metabolites

Chemically mediated crowding effect on induction of diapause egg production in the calanoid copepod Eurytemora affinis was investigated. Two types of eggs, i.e. subitaneous and diapause eggs, produced by females that were reared in crowded culture conditions or the water from crowded culture under excess food supply were examined. 2.3% of the females that were reared at a population density of 5 or 6 animals per 10 ml of filtered lake water (FLW) produced diapause eggs. Females that were reared individually in 2-ml containers with FLW did not produce diapause eggs while 72.7% of females that were individually reared in 2-ml containers, but with water from a crowded culture (500 ind. l^–1, culture medium was changed once a week), produced diapause eggs. These results demonstrate that accumulation of their own metabolic products in the medium induces diapause egg production by E. affinis.     

Nature versus nurture? Consequences of short captivity in early stages

Biological changes occurring as a consequence of domestication and/or captivity are not still deeply known. In Atlantic salmon (Salmo salar), endangered (Southern Europe) populations are enhanced by supportive breeding, which involves only 6 months of captive rearing following artificial spawning of wild‐collected adults. In this work, we assess whether several fitness‐correlated life‐history traits (migratory behavior, straying rate, age at maturity, and growth) are affected by early exposure to the captive environment within a generation, before reproduction thus before genetic selection. Results showed significant differences in growth and migratory behavior (including straying), associated with this very short period of captivity in natural fish populations, changing even genetic variability (decreased in hatchery‐reared adults) and the native population structure within and between rivers of the species. These changes appeared within a single generation, suggesting very short time of captivity is enough for initiating changes normally attributed to domestication. These results may have potential implications for the long‐term population stability/viability of species subjected to restoration and enhancement processes and could be also considered for the management of zoo populations.     

Effects of photoperiod, temperature, and host plant age on induction of reproductive diapause and development time in Danaus plexippus

Abstract 1. Diapause induction in monarch butterflies Danaus plexippus was studied using adults captured from the wild in Minnesota and Wisconsin, and individuals reared under outdoor and controlled conditions.
2. Oocyte presence in females and ejaculatory duct mass in males were used to indicate reproductive status.
3. Some wild individuals were in diapause in mid-August, and all males and females were in diapause by late August and early September respectively.
4. Individuals reared under decreasing day lengths and fluctuating temperatures were more likely to be in diapause than were individuals reared under long or short day lengths or constant temperatures.
5. Individuals fed potted old Asclepias curassavica plants were more likely to be in diapause than were those fed potted young host plants; when cuttings of Asclepias syriaca plants from the field or greenhouse pots were used, there was no effect of host plant age.
6. Extremely high temperatures increased the number of day-degrees required for development from egg to adult, while decreasing day lengths and older host plants tended to decrease the number of day-degrees required for development.
7. There appears to be a continuum of reproductive development in monarchs, with gradual declines in mean ejaculatory duct mass and oocyte production during the late summer.
8. None of the experimental treatments led to 100% diapause, and diapause was more likely to occur in monarchs subjected to more than one diapause-inducing cue.     

Reduction in antipredator response detected between first and second generations of endangered juvenile Atlantic salmon Salmo salar in a captive breeding and rearing programme

Behaviour trials determining antipredator response were conducted on first and second generation juveniles from a captive breeding and rearing programme for endangered Inner Bay of Fundy Atlantic salmon Salmo salar. Second generation captive fry displayed significantly higher levels of risk‐taking behaviour before and after exposure to a simulated avian predator. Because the first and second generation fry were reared under the same environmental conditions and differed only in the number of generations spent in captivity, these results suggest that rapid genetic changes, possibly due to domestication selection, may have occurred. Antipredator response was also assessed in fully wild and highly domesticated experimental groups: wild fry displayed the greatest antipredator response and domesticated fry displayed the highest levels of risk‐taking behaviour. These results add to the growing evidence documenting rapid genetic change in response to rearing in a captive environment.     

Hypoxia and life‐history traits in a eurytopic African cichlid

This study quantified variation in key life‐history traits of the widespread African mouth‐brooding cichlid Pseudocrenilabrus multicolor victoriae. Egg size, number, batch reproductive effort, size at maturity and brooding efficiency were compared among field populations across a wide range of dissolved oxygen (DO) concentrations from extreme hypoxia to normoxia. In the laboratory, a similar suite of characters was quantified in F1 of low‐ and high‐DO origin reared under low or high DO. In general, females from low‐DO habitats and females reared under low DO were characterized by a smaller size at maturity and no difference in batch reproductive effort when compared with females from high‐DO habitats or females reared under normoxia. A trade‐off between egg size and number was evident in the field and in the laboratory‐rearing experiment, but the direction of the trade‐off differed. Egg size was negatively correlated with egg number across field populations; females collected from low‐DO sites generally had more, smaller eggs relative to females from high‐DO sites. In the laboratory‐rearing experiment, F1 females of high‐DO origin produced larger, fewer eggs than F1 females of low‐DO origin, lending support to the field results and suggesting a heritable component to these traits. There was also an element of developmental plasticity, F1 females raised under low DO produced larger, fewer eggs compared with F1 females raised under high DO (regardless of population) suggesting that DO may interact with other variables to determine egg size in the field.     

Captive rearing for Chinook salmon (Oncorhynchus tshawytscha) and Atlantic salmon (Salmo salar): the Idaho and Maine experiences

Captive rearing is a conservation strategy where juveniles are collected from the natural environment, reared to maturity in a hatchery environment, and then released back into the natural environment at maturity for volitional spawning. This strategy has been used to produce adult outplants for stock enhancement where natural escapement is poor or capture of adults is difficult. In both Idaho (Chinook salmon, Oncorhynchus tshawytscha) and Maine (Atlantic salmon, Salmo salar), captive rearing programs have been initiated as an experimental strategy to prevent cohort collapse and conserve genetic integrity of select depressed populations. In this paper, we provide an overview of these programs and describe some of the methods used to evaluate the effectiveness of this approach. Behaviors such as habitat selection, courting, and spawn timing were monitored. Data collected for both programs indicate that the captive fish display similar behaviors as their wild conspecifics in terms of habitat selection and spawning, although there were some differences in spawn timing. Evaluations of egg and fry production also indicate that captive-reared adults are successfully spawning and producing offspring. Each program is still waiting on final evaluations of reproductive success through genetic analyses of returning adults, but results so far indicate that this could be an additional captive propagation strategy for depressed populations.     

EFFECTS OF PHOTOPERIOD ON EMBRYONIC DIAPAUSE AND REPRODUCTION IN THE MIGRATORY LOCUST IN THREE GEOGRAPHIC POPULATIONS1

Abstract The three investigated populations of migratory locust, Locusta migratoria L. (Orthoptera, Acrididae), reported in this paper show significant variation in diapause characteristics. The insects of the Heshuo Xinjiang population show diapause in egg stage regardless of the photoperiod of rearing condition, while the adults of the Beidagang Tianjin and the Hami Xinjiang populations produce diapause or nondiapause eggs according to the short or long photoperiod. From this research, we infer altitude plays an important role in inducing diapause. The long photoperiod which extends the duration of pre-oviposition period and reduces the oviposition frequency in the Beidagang and Hami populations shows no effect on those features of the Heshuo population. The duration at low temperature to end diapause in the Heshuo population is longer than that in the other two populations.     

Life history of Bicyclus anynana mutants: Can they serve as internal controls?

Correction for environmental effects in quantitative genetics experiments is often achieved by use of separate control populations. However, this method may not always correct accurately for environmental fluctuations in rearing conditions. A more suitable approach could be rearing mutants together with experimental groups, provided that these mutants are clearly distinguishable phenotypically and have similar life histories. We tested whether two mutants (yellow and Spotty) available for the tropical butterfly Bicyclus anynana could serve as such true internal controls. The yellow butterflies had lower survival and longer development time than the wild type animals they were reared with, whereas Spotty individuals were equivalent in those respects to their wild type counterparts. Moreover, heritability estimates for development time in the Spotty stock were mostly significantly different from zero and fell within the range found for wild type butterflies. Therefore, we conclude that a backcrossed stock homozygous for the Spotty mutant of B. anynana can reliably serve as an internal control in life-history studies and we discuss potential advantages of this method.     

Unravelling first-generation pedigrees in wild endangered salmon populations using molecular genetic markers

There is increasing interest in the use of molecular genetic data to infer genealogical relationships among individuals in the absence of parental information. Such analyses can provide insight into mating systems and estimations of heritability in the wild. In addition, accurate pedigree reconstruction among the founders of endangered populations being reared in captivity would be invaluable. Many breeding programs for endangered species attempt to minimize loss of genetic variation and inbreeding through strategies designed to minimize global co-ancestry, but they assume a lack of relatedness among the founders. Yet populations that are the target of such programs are generally in serious demographic decline, and many of the available founders may be closely related. Here we demonstrate determination of full and half-sib relationships among the wild founders of a captive breeding program involving two endangered Atlantic salmon populations using two different approaches and associated software, pedigree and colony. A large portion of the juveniles collected in these two rivers appear to be derived from surprisingly few females mating with a large number of males, probably small precocious parr. Another group of potential founders, obtained from a local hatchery, clearly originated from a small number of full-sib crosses. These results allowed us to prioritize individuals on the basis of conservation value, and are expected to help minimize loss of genetic variation through time. In addition, insight is provided into the number of contributing parents and the mating systems that produced this last generation of endangered wild Atlantic salmon.     

Influence of photoperiod on the overwintering induction of Galerucella calmariensis L

Understanding thephenology of biological control agents iscritical for developing effective rearingmethods. In the case of Galerucellacalmariensis L, a biological control agentintroduced against purple loosestrife (Lythrum salicaria), the presence of anobligatory diapause affects successful rearing.G. calmariensis individuals were rearedfrom egg to adult under four differentcombinations of long and short photoperiods.Two weeks after adult emergence, individualsfrom each treatment were dissected to check forovary development and presence of developedeggs as indicators of overwintering induction.Individuals treated under short photoperiodthroughout their lifetime were found to havesmaller ovaries and few developed eggs,indicating an effective overwinteringinduction. The adult stage of G.calmariensis was determined to be the stagesensitive to photoperiod, as evidenced byreduction in ovary size, decreasedoverwintering mortality and increasedpost-overwintering fecundity in individualstreated as adults with short daylength. Increased post-overwintering fecundity whendiapause was effectively induced can increasethe efficiency of rearing programs for G. calmariensis and other weed biological controlagents with a reproductive diapause.     

Use of genetic tags to identify captive-bred pallid sturgeon (<Emphasis Type="Italic">Scaphirhynchus albus</Emphasis>) in the wild: improving abundance estimates for an endangered species

The ability to distinguish captive-bred and natural-origin individuals in the wild is critical for evaluating the impact of captive breeding programs on natural populations. Continued persistence of endangered pallid sturgeon (Scaphirhynchus albus) in the Missouri River is largely dependent on captive breeding efforts that spawn natural-origin adults in fish hatcheries and release their progeny into the wild. Prior to release, hatchery-origin individuals are physically marked so they can be distinguished from natural-origin individuals when recaptured. During the years 2004–2006, 24 unmarked juvenile pallid sturgeon tissue samples were collected in the Missouri River downstream of Gavins Point Dam, South Dakota, USA that were presumed natural-origin. However, these individuals were similar in size to hatchery-origin fish released in this area raising concerns that these individuals were actually hatchery-origin fish with lost or malfunctioning tags. We used microsatellite based parentage analysis to determine if the unmarked fish were members of hatchery families that had been released in this area. This retrospective genetic tagging approach revealed that 23 of 24 unmarked fish were indeed hatchery-origin. The origin of the remaining individual remains unknown because genetic samples were not available from all of the families released below the dam and the unassigned fish may have originated from one of these un-sampled families. These results provide important insight into the conservation status of endangered pallid sturgeon as well as provide data important for guiding management decisions. Our results also demonstrate the efficacy of using genetic tags as an alternative or complimentary approach to physically marking individuals.     

Alarm responses are maintained during captive rearing in chicks of endangered kaki

The maintenance of species-specific behavioural repertoires and traditions is an important but often implicit goal of conservation efforts. When captive rearing is used as a conservation practice, it becomes critical to address its possible implications for the social and behavioural traits of developing individuals. In particular, animals must retain or acquire many of their behavioural abilities to increase the likelihood of survival upon release into the wild. This study investigated the behavioural development of critically endangered kaki (black stilt: Himantopus novaezelandiae ) chicks reared without live adult conspecifics. The captive rearing programme included playbacks of adult kaki alarm calls during cleaning and handling of precocial chicks housed as groups. We used videotaped observations and playback experiments to address the following questions: do kaki chicks respond differentially to (1) familiar versus unfamiliar adult kaki alarm calls and (2) conspecific alarm versus heterospecific control vocalizations. Adult-naïve kaki chicks exhibited a varied behavioural repertoire over their early development. In multivariate analyses, when age was statistically controlled, chicks showed responses to familiar and unfamiliar alarm calls that were similar in magnitude. In contrast, following conspecific alarm calls chicks had longer average latencies to resume pre-playback activities than following heterospecific vocalizations. Although the generality of these conclusions is limited by experimental constraints stemming from working with an endangered species, the findings suggest that current management techniques produce captive-reared kaki for release into the wild that possess many of the behavioural and auditory recognition skills that are required for survival.