Is helping a beneficial learning experience for red-cockaded woodpecker (Picoides borealis) helpers?

Several hypotheses have been suggested to explain the evolution and maintenance of helping behavior in cooperatively breeding birds, one of which we investigated in the red-cockaded woodpecker (Picoides borealis). Helping may provide a learning experience that improves reproductive success once the helper becomes a breeder. We used data collected from a population of red-cockaded woodpeckers in the Sandhills of North Carolina to compare the reproductive success of 2-year-old breeders that were helpers at age 1 (helping experience) to those that were floaters or solitary males at age 1 (no helping experience). Reproductive success of the two groups was similar, indicating that helping provides no experience useful in reproduction. We reject the learning experience hypothesis as an explanation for the maintenance of helping behavior in red-cockaded woodpeckers. Received: 29 July 1996 / Accepted after revision: 27 April 1997     

An analysis of reciprocal exchange of helping behavior in the red-cockaded woodpecker (Picoides borealis)

We examine the frequency of reciprocal exchanges of helping behavior in three red-cockaded woodpecker populations to determine if such exchanges might constitute a significant fitness benefit of helping. Specifically, we determine how often helpers, once they become breeders, are assisted by young they previously helped raise. The estimated frequencies of reciprocal exchange of helping based on survival and status transition probabilities are low (2%). Observed frequencies of reciprocity are significantly higher than estimated frequencies in two of the three populations studied, suggesting that male fledglings more often remain on their natal territory as helpers if another helper is already present. High rates of retention of young males as helpers on high-quality territories or preferential helping of kin, as well as preferential helping of former care-givers, might explain this result. When the analysis is restricted to helpers unrelated to the young they help raise, which controls for preferential helping of kin and largely eliminates effects of territory quality, empirical estimates of the frequency of reciprocity do not differ from estimates calculated from population demography. We conclude that young males do not preferentially help former care-givers and that reciprocal exchange of help is not an important factor in the evolution of helping behavior in the red-cockaded woodpecker. In this species, all known benefits of helping behavior are indirect (i.e., derived through kin selection ) rather than direct. We discuss the occurrence of unrelated helpers in this context. Received: 10 August 1999 / Received in revised form: 13 February 2000 / Accepted: 19 February 2000     

Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker

We examined the genetic relationship among putative parents, offspring, and helpers in 224 red-cockaded woodpeckers (Picoides borealis) from the Sandhills of North Carolina. Comparison of DNA similarity with a pedigree constructed from 3,823 individually-marked birds observed from 1979 to 1992 provided verification of observed relatedness in the sampled population (R ² = 0.87,df = 14,P<0.001). In this population, breeding pairs may or may not have helpers, most of which are males that remain on their natal territory. Our sample included helpers assisting their parents, helpers assisting a related male and an unrelated female, and helpers assisting an unrelated pair. Band by band comparison and examination of similarity among DNA profiles indicated that all offspring from non-helped nests were sired by their putative parents (n = 28 families). Similarly, all but one offspring in helped nests were also sired by their putative parents (n = 16 families). In the exceptional case, the offspring evidently was sired by a male external to the group. Analysis of similarity values supported the conclusion that matings by helpers or extra-group males are rare or non-existent. Our results indicate that in this species advantages gained by individuals remaining on their natal territories as helpers do not generally include siring offspring. Correspondence to: S. Haig     

Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker

We examined the genetic relationship among putative parents, offspring, and helpers in 224 red-cock-aded woodpeckers (Picoides borealis) from the Sandhills of North Carolina. Comparison of DNA similarity with a pedigree constructed from 3,823 individually-marked birds observed from 1979 to 1992 provided verification of observed relatedness in the sampled population (R ² = 0.87, df = 14, P < 0.001). In this population, breeding pairs may or may not have helpers, most of which are males that remain on their natal territory. Our sample included helpers assisting their parents, helpers assisting a related male and an unrelated female, and helpers assisting an unrelated pair. Band by band comparison and examination of similarity among DNA profiles indicated that all offspring from non-helped nests were sired by their putative parents (n = 28 families). Similarly, all but one offspring in helped nests were also sired by their putative parents (n = 16 families). In the exceptional case, the offspring evidently was sired by a male external to the group. Analysis of similarity values supported the conclusion that matings by helpers or extra-group males are rare or non-existent. Our results indicate that in this species advantages gained by individuals remaining on their natal territories as helpers do not generally include siring offspring. Correspondence to: S. Haig     

Reproductive suppression and inbreeding avoidance in wild populations of co-operatively breeding meerkats (Suricata suricatta)

Meerkats live in co-operatively breeding familial groups in which reproduction is monopolised by a dominant pair of breeders. Offspring of the breeders are behaviourally subordinate, and typically remain in their natal group as sexually mature, non-breeding helpers. In this study, we investigated the proximate factors limiting subordinate reproduction. Evidence for reproductive suppression by dominants was investigated by comparing life history, behaviour and hormonal profiles of dominants and subordinates. Baseline levels of plasma luteinising hormone (LH) were significantly higher in dominant than in subordinate females. However, following an exogenous injection of gonadotrophin-releasing hormone (GnRH), both categories had comparable concentrations of circulating LH. There were no significant differences in pre- or post-GnRH challenge LH levels in dominant or subordinate males. Reproduction in both dominant and subordinate females rarely occurred in the absence of unrelated males. Given that groups typically comprise parents and offspring, lack of suitable mates emerged as the primary constraint on subordinate reproduction. When this constraint was removed, subordinates typically bred but at a lower rate than dominants. This difference in reproduction may be attributed to intrasexual competition manifested through direct interference by dominant females through subordinate evictions, infanticide and the abandoning of subordinate litters. We argue that differences in reproductive regulation within mammalian co-operative breeding systems may be explained by differences in the mating strategy (inbreeding versus outbreeding) and the probability that subordinates in obligate outbreeding species will encounter unrelated opposite-sex partners. Received: 19 April 2000 / Accepted: 17 July 2000     

Plasma levels of androgens and gonadal development of breeders and helpers in the bell miner (Manorina melanophrys)

Plasma concentration of androgens and gonad development were studied in wild cooperatively breeding bell miners (Manorina melanophrys) of different age, sex and social status. Plasma levels of androgens increased with age of birds. For sexually mature (SM) bell miners, androgen levels were higher in breeders than in nonbreeding (NB) helpers (P < 0.005), and they were marginally higher in females than in males (P < 0.10). Thus female breeders showed the highest plasma levels of androgens. This pattern may be explained by an asymmetry between the sexes in the levels of competition needed to reach and defend breeding status; the degree of intra-sexual competition seems to be higher among female bell miners than among males. In general, male breeders had larger gonads than male SMNB helpers; male breeder gonads produced spermatozoa whereas most helpers' gonads did not. However, old (i.e. 34 months) SMNB male helpers had large gonads producing spermatozoa in spite of having low plasma levels of androgens. We suggest that young male bell miners may be under a voluntary mechanism of reproductive suppression perhaps favoured by inbreeding avoidance; although some aggressive interactions observed between very young helpers (about 2 months) and adult members of the breeding unit suggests that a certain degree of imposition also occurs at young ages. Older male helpers may avoid aggression with the male breeder and imposed reproductive suppression, hence the low circulating levels of androgens, but they have the potential to sneak extra-pair copulations. Gonad size decreased during the non-breeding season in both sexes.     

Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses

It is suggested that some fish of the genus Julidochromis, substrate-brooding Tanganyikan cichlids with biparental care, breed cooperatively with helpers. We studied the social system of J. ornatus in the wild and analysed genetic parentage using microsatellites. Within the studied population three patterns of social system were identified: monogamous pairs (61%, 44 of 72 groups), pairs with helpers (29%, 21), and polygamous harems with helpers (controlled by either a large female or large male owner; 10%, 7). In cooperatively breeding groups, the number of helpers at each nest ranged from 1 to 6 (median 1), and male helpers were more numerous than female helpers. In both sexes, the body size was different among individuals of different social status (harem owner > breeder > helper). Helpers and harem owners of both sexes exhibited brood defence although its frequency was low. The molecular analysis revealed that (1) the helpers were mostly unrelated to dominant breeders, (2) many helpers of both sexes contributed genetically to the next generations, (3) male helpers had high siring success (41% of young in total), and (4) large young unrelated to group members were detected at 30% of observed nests, which may be due to breeder (or helper) replacements and immigration of young. We discuss the implications of these results for understanding the complex social system of this species, especially the low reproductive skew in comparison with other cooperatively breeding cichlids.     

The effect of helpers on artificially increased brood size in sociable weavers (Philetairus socius)

In cooperatively breeding birds, the presence of helpers is expected to increase the reproductive success of the breeding pair. However, some studies fail to find this effect. A positive effect of helpers may be restricted to cases in which a breeding pair has a poor likelihood of raising the entire brood on its own, as would be the case under stressful environmental conditions or with enlarged brood sizes. We conducted brood size manipulations in a cooperative breeder, the sociable weaver, Philetairus socius, to investigate the relationship between the difficulty of raising nestlings and the effort and impact of helpers. Overall, sociable weavers did not work harder to raise the enlarged broods. However, the presence of helpers significantly increased the feeding rates at enlarged nests, but not controls. This was insufficient to prevent generalised brood reduction in enlarged broods, whether attended by pairs alone or with helpers. Nonetheless, the presence of helpers was associated with decreased nestling mortality and an increase in the numbers of young fledged. Our results suggest that groups are better able to respond to the needs of enlarged broods than pairs alone and that the presence of helpers has a beneficial effect on overall reproductive success.Communicated by J. Dickinson     

Delayed breeding in the cooperatively breeding Florida scrub-jay (Aphelocoma coerulescens): inhibition or the absence of stimulation?

To determine whether fundamental differences exist in the reproductive physiology of breeder and nonbreeder Florida scrub-jays (Aphelocoma coerulescens), we compared plasma levels of testosterone (T) and luteinizing hormone (LH) in males, and estradiol (E₂) and LH in females. Although male breeders had higher overall T and larger testes, nonbreeders’ T paralleled that of breeders, and their testes were more than an order of magnitude larger than regressed testes. Breeder and nonbreeder males had equivalent baseline LH, and equivalent changes in LH following a gonadotropin-releasing hormone (cGnRH-I) challenge. The T, LH and GnRH challenge data indicate that nonbreeder males have functional hypothalamo-pituitary-gonadal (HPG) axes. We found no hormonal evidence of inbreeding suppression in males: nonbreeders that did not live with their mothers and those that did had similar T. Male nonbreeders that were exposed to E₂-implanted females had higher T than did controls, suggesting that the lack of within-pair stimulation is a key factor in whether an individual delays breeding. Female nonbreeders had E₂ titres equal to or higher than breeders and neither basal LH nor LH following GnRH challenge differed by breeding status. Nonbreeders’ ovarian follicles were smaller than breeders’, but were larger than they would be during the non-breeding season. These data suggest that nonbreeders were primed for breeding and were simply waiting for an opportunity or a required stimulus. Female nonbreeders that lived in a territory with an unrelated male breeder had significantly higher E₂ than those that remained with their fathers. Similarly, nonbreeders that were captured away from their home territories had elevated E₂. However, nonbreeders that lived with their fathers had E₂ that was equivalent to breeding females, suggesting that inbreeding avoidance may not be the primary factor leading to delayed breeding in females. Received: 13 June 1995 /Accepted after revision: 27 April 1996     

Effects of temperature on morphological landmarks critical to growth and survival in larval Atlantic cod (Gadus morhua)

The morphology and function of structures important to energy acquisition were studied from spawning to the stage of transformation of larva to pelagic juvenile in Atlantic cod, Gadus morhua L., from December 1991 to July 1992. Fertilized eggs produced by adult fish from two genetically discrete populations (Newfoundland and Scotian Shelf) were raised under similar conditions in the laboratory at temperatures of 5 and 10°C. Subsamples of larvae were removed from cultures daily for 10 d, and then less frequently, and fixed for light microscopy and scanning electron microscopy. Nine functional morphological landmarks important to feeding, respiration and locomotion were chosen from observation of 280 ind. These landmarks defined 12 major developmental stages, from hatching to the pelagic juvenile stage. One of the feeding landmarks, intestinal stage, varied as a function of age and size and the variance in development was higher at 10°C than at 5°C; Newfoundland larvae developed more complex intestines than did Scotian Shelf larvae. In addition, Newfoundland larvae had significantly higher growth rates than those of Scotian Shelf larvae. Despite the higher growth rates and greater structural complexity of the intestine in Newfoundland larvae, the rate of yolk utilization was not significantly different between Newfoundland and Scotian Shelf larvae. Staging of respiratory landmarks showed that the gill arches were probably used preferentially in feeding while respiration was cutaneous. The gills, operculum and gill rakers developed late in larval life and accompanied the transition from cutaneous to branchial respiration. In the yolk-sac period, development of feeding and respiratory structures may be largely genetically controlled. During exogenous feeding, extrinsic factors also become important, as shown by the size and age-independent variation in intestinal development of larval cod raised at different temperatures.     

Effects of temporary starvation on the survival,and on subsequent feeding and growth,of oyster (Crassostrea gigas) larvae

Larvae of oysters, Crassostrea gigas, were maintained without food for 1 to 8 d after fertilization, and fed daily thereafter. There was little difference in survival and growth between controls and larvae kept without food for 2 or 3 d. Survival and growth rates were depressed in larvae starved for 4 or 5 d. For larvae starved for 6 to 8 d, survival was negligible or nil; even those larvae which survived the starvation period died later in the presence of food, apparently because of impaired digestion. Therefore, food availability in the first few days after spawning appears to be of paramount importance to the successful recruitment of Pacific oysters.     

Effects of autotomy on long-term survival and growth of painted spiny lobster (Panulirus versicolor) on the Great Barrier Reef, Australia

The effects of autotomy (shedding of appendages) on survival and growth rates of painted spiny lobster were investigated at Northwest Island (23^° 18?? S, 152^° 43?? E) during the period 2003?C2006. Adult lobsters were captured, tagged, and classified as either uninjured (n?=?68), minimally injured (n?=?39) or moderately injured (n?=?19) depending on the number and type of appendages that were autotomized during capture and handling. Six to thirty-six months after release, 86 lobsters were recaptured (mean time at large?=?305?days). Recapture rates of uninjured (64.7%), minimally injured (71.8%), and moderately injured lobsters (73.7%) were not significantly different. Similarly, mean annualized growth rates of uninjured, minimally injured, and moderately injured lobsters were not significantly different. This suggests that the energetic cost of a single episode of autotomy is either negligible or exists as a trade-off with some other life history trait, such as reduced reproductive performance. These results support the use of certain management tools (e.g., size limits) that prescribe release of non-legal lobsters, regardless of their injury status.     

Effects of chytrid fungus and a glyphosate-based herbicide on survival and growth of wood frogs (Lithobates sylvaticus)

Anthropogenic-derived stressors in the environment, such as contaminants, are increasingly considered important cofactors that may decrease the immune response of amphibians to pathogens. Few studies, however, have integrated amphibian disease and contaminants to test this multiple-stressor hypothesis for amphibian declines. We examined whether exposure to sublethal concentrations of a glyphosate-based herbicide and two strains of the pathogenic chytrid fungus, Batrachochrytrium dendrobatidis (Bd) could: (1) sublethally affect wood frogs (Lithobates sylvaticus) by altering the time to and size at metamorphosis, and (2) directly affect survivability of wood frogs after metamorphosis. Neither Bd strain nor herbicide exposure alone significantly altered growth or time to metamorphosis. The two Bd strains did not differ in their pathogenicity, and both caused mortality in post-metamorphic wood frogs. There was no evidence of an interaction between treatments, indicating a lack of herbicide-induced susceptibility to Bd. However, the trends in our data suggest that exposure of wood frogs to a high concentration of glyphosate-based herbicide may reduce Bd-caused mortality compared to animals exposed to Bd alone. These results exemplify the complexities inherent when populations are coping with multiple stressors. In this case, the perceived stressor, glyphosate-based herbicide, appeared to affect the pathogen more than the host's immune system, relieving the host from disease-caused effects. This suggests caution when invoking multiple stressors as a cause for increased disease susceptibility and indicates that the effects of multiple stressors on disease outcome depend on the interrelationships of stressors to both the pathogen and the host.     

Elevated temperature elicits greater effects than decreased pH on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae

Climate models predict that the average temperature in the North Sea could increase 3–5 °C and surface-waters pH could decrease 0.3–0.5 pH units by the end of this century. Consequently, we investigated the combined effect of decreased pH (control pH 8.1; decreased pH 7.6) and temperature (control 6.7 °C; elevated 9.5 °C) on the hatching timing and success, and the zoeal development, survival, feeding, respiration and growth (up to stage IV zoea) of the northern shrimp, Pandalus borealis. At elevated temperature, embryos hatched 3 days earlier, but experienced 2–4 % reduced survival. Larvae developed 9 days faster until stage IV zoea under elevated temperature and exhibited an increase in metabolic rates (ca 20 %) and an increase in feeding rates (ca 15–20 %). Decreased pH increased the development time, but only at the low temperature. We conclude that warming will likely exert a greater effect on shrimp larval development than ocean acidification manifesting itself as accelerated developmental rates with greater maintenance costs and decreased recruitment in terms of number and size.     

Effects of salinity and two food regimes on survival, fecundity and sex ratio in two groups of Dinophilus gyrociliatus (Polychaeta: Dinophilidae)

The effects of salinity on survival, fecundity and sex ratio were studied in Dinophilus gyrociliatus; a small polychaete with a short lifespan, semicontinuous reproduction and progamic sex determination. The experiment was performed on two groups, originally collected as one sample, from the port of Genoa in November 1995. The specimens were separated into two groups, differing only in their diet: the first was fed with frozen spinach and the other with Tetramin Mikromin. The experiment was performed in 1998 after numerous generations had been maintained under laboratory conditions. The maximum expectation of life at birth varied with salinity level, and both groups showed a better tolerance towards a salinity below 35 psu than above 35 psu. The influence of both salinity and diet on fecundity had statistical significance even though the greatest differences were due to diet; animals fed with Tetramin had a two- or even threefold higher fecundity than those fed with spinach. Diet and salinity also had a statistically significant influence on the sex ratio. These results, as well as all the experimental observations carried out up to date, indicate that in D. gyrociliatus the determination of the sex ratio has a strong phenotypic component. Received: 9 September 1999 / Accepted: 9 May 2000     

Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamesus) on recruitment and survival of two species of kelp (Macrocystis pyrifera and Pterygophora californica)

We studied the effects of grazing by two species of sea urchins on two species of kelp (Macrocystis pyrifera and Pterygophora californica) in the San Onofre kelp bed in southern California from 1978 through 1981. Both red sea urchins, Strongylocentrotus franciscanus, and white sea urchins, Lytechinus anamesus, were abundant and lived in aggregations. The purple sea urchin (S. purpuratus) was rare at the study site and was not studied. The aggregations of red urchins were either relatively small and stationary (for over 3 yr) or relatively large and motile (advancing at about 2 m mo^–1). Both stationary and moving aggregations were observed at the same time, and within 100 m of one another. Stationary aggregations of red urchins probably subsisted mainly on drift kelp and had no effect on kelp recruitment or on adult kelp abundance. In contrast, red sea urchins in large, motile aggregations or fronts ate almost all the macroalgae in their path. The condition of their gonalds indicated that red urchins in fronts were starved relative to red urchins in the small, stationary aggregations. Large, motile aggregations developed after 2 yr of declining kelp abundance (probably due largely to storms). We propose that a scarcity of drift algae for food results in a change in the behavior pattern of the red urchins and thus leads to the formation of large, motile aggregations. The aggregations of white urchins, which occurred along the offshore margin of the kelp bed, were large, but relatively stationary. The white urchins rarely ate adult kelps, but grazed extensively on early developmental stages of kelps and evidently prevented seaward expansion of the bed. The spatial distribution of both types of red urchin aggregations appeared to be unrelated to predation pressure from fishes or lobsters.Please address all requests for reprints to the senior author at his present address.     

Effect of the spionid polychaeteBoccardia syrtis on the distribution and survival of juvenileMacomona liliana (Bivalvia: Tellinacea)

The tellinid bivalveMacomona liliana (Iredale) occurs at relatively low densities on a sandbank (Te Tau bank) in Manukau Harbour, New Zealand. Te Tau bank is dominated by polychaetes, including the tube-building spionidBoccardia syrtis (Rainer). JuvenileM. liliana are known to disperse as post-settlement juveniles by byssus-drifting. Laboratory experiments were conducted to assess whether the low abundance ofM. liliana on Te Tau bank was due to the presence ofB. syrtis, or to some reaction to the sediment itself. In particular, we, examined how juvenileM. liliana survived after exposure to Te Tau bank sediments with and without the spionid tube-mat for 1 mo in still-water conditions, and how they responded when given a choice of different sediment/tube-mat treatments in moving water. JuvenileM. liliana did not appear to have a strong aversion to settling and burrowing in sediments from Te Tau bank. Sediments without the tube-mat did not adversely affect the survivorship of the bivalves, but survival was significantly lower amongst theB. syrtis tube-mat. In the presence of a current, the juvenile bivalves settled in Te Tau bank sediments without a tube-mat, but avoided settling amongst liveB. syrtis. An artificial tube-mat enhanced settlement. Avoidance of liveB. syrtis appears to be an avoidance of the worms themselves rather than a response to the physical presence of their tubes.     

Effects of temperature and salinity acclimation of adults on larval survival,physiology, and early development of Lytechinus variegatus (Echinodermata: Echinoidea)

Larval survival and developmental rates of Lytechinus variegatus (Lamarck) were determined as a function of temperature and salinity in two experiments by: (1) directly transferring fertilized eggs to 35, 30, 27.5, 25, 20, 15, and 10S seawater at 18 and 23°C, and (2) acclimation of adult sea urchins to the conditions described above for 1 to 4 wk prior to spawning. Developmental rates and percent survival of larvae prior to metamorphosis decreased at salinities below 35 (Q₁₀ values for metamorphosis=0.380 to 0.384). Temperature and salinity significantly (P<0.05) affected metabolic rates of L. variegatus plutei. These results show that L. variegatus larvae are stenohaline when compared to larvae of other echinoderm species. LC₅₀ values (S), developmental rates, and survival to metamorphosis indicate that acclimation of adult sea urchins to lower salinity prior to spawing and fertilization does not enhance development or survival of embryos exposed to low salinity.     

Effects of foundress number on brood raids and queen survival in the fire ant Solenopsis invicta

In several ant species, colonies are founded by small groups of queens (pleometrosis), which coexist until the first workers eclose, after which all but one queen is killed. It has been hypothesized that, by producing a larger cohort of workers, cooperating queens may increase colony success during brood raids, a form of competition in which brood and workers from losing nests are absorbed into winning colonies. To test whether this benefit is sufficient to favor pleometrosis, newly mated queens of the fire ant Solenopsis invicta were assembled in groups of one, two, three, or four, reared in the laboratory until the first workers eclosed, then planted in the field in replicated assemblages. The proportion of colonies engaging in brood raids increased with average foundress number per nest and with colony density but was unaffected by variance in foundress number among interacting colonies. Within mixed assemblages of single-queen and multiple-queen colonies, queen number had no effect on the likelihood of engaging in raids or the probability of nest survival through the brood raiding period. However, following nearly 30% of raids, queens moved to new nests and displaced the resident queens. When queen relocation and subsequent mortality were accounted for, it was found that the survival of queens from four-queen groups was substantially higher than that of solitary queens. By contrast, the survival of queens from two-queen colonies was no greater than that of solitary queens. These results show that the competitive advantages of multiple-queen colonies are sufficient to counterbalance the increased mortality of queens within groups only when the number of foundresses is greater than two and when colonies are founded at high density. When colonies lose brood raids, the workers appear to abandon their mothers to join surviving colonies. However, in laboratory experiments, queens attempting to enter foreign nests were significantly more likely to displace the resident queen if their own daughters were present within the invaded nest. Thus, workers may be able to bias the probability that their mother rejoins them and displaces competing queens.