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Title: Natural History of the Salamander, Aneides hardii
Author: Johnston, Richard F., Schad, Gerhard A.
Language: English
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University of Kansas Publications
Museum of Natural History

Vol. 10, No. 8, pp. 573-585
October 8, 1959



NATURAL HISTORY OF THE SALAMANDER,
ANEIDES HARDII

BY

RICHARD F. JOHNSTON AND GERHARD A. SCHAD


University of Kansas
Lawrence
1959



University of Kansas Publications, Museum of Natural History

Editors: E. Raymond Hall, Chairman, Henry S. Fitch,
Robert W. Wilson


Volume 10, No. 8, pp. 573-585
Published October 8, 1959


University of Kansas
Lawrence, Kansas


PRINTED IN
THE STATE PRINTING PLANT
TOPEKA, KANSAS
1959

27-9040



NATURAL HISTORY OF THE SALAMANDER,
ANEIDES HARDII

BY

RICHARD F. JOHNSTON AND GERHARD A. SCHAD


The Sacramento Mountains Salamander, _Aneides hardii_ (Taylor), is a
plethodontid of relict distribution in the spruce-fir vegetational
formation from 8500 to 9600 feet elevation in Otero and Lincoln
counties, New Mexico. The salamanders on which most of this report is
based were collected three, four, and six miles northeast of Cloudcroft
in the Sacramento Mountains. Additional individuals were collected on
the eastern slope of Sierra Blanca, 1.5 miles southwest of Monjeau
Lookout, at about 9000 feet, Lincoln County, and in the vicinity of
Summit Springs and Koprian Springs, 9300 feet, Capitan Mountains,
Lincoln County. Certain details concerning the populations in Lincoln
County will be reported elsewhere (Schad, Stewart, and Harrington,
Canadian Jour. Zool., in press).

We would like to thank Mmes. Donna Schad and Lora Lee Johnston, Messrs.
Robert Stewart, Frederick Harrington and Ralph Raitt, and Dr. Robert
Selander for assistance in the field, Dr. W. Frank Blair and Dr. Marlowe
Anderson for the use of specimens in their care, and Dr. A. Byron
Leonard for the identification of the molluscan food items.

In the summer rainy season _A. hardii_ lives in and under downed timber
and under talus accumulations. Occurrence, however, seems to be partly
subterranean and always local; seemingly good habitat frequently appears
to lack the animals. Our observations and collections were made in July,
August, and September in 1956, 1957, and 1958. Two hundred seventy-seven
individuals were taken; these were measured, sexed and examined for
breeding status. The food and parasite content of the guts of a few
individuals was determined. Thirteen salamanders were kept for varying
lengths of time in captivity. The specimens are now stored in
collections at New Mexico State University, University of Texas, Museum
of Vertebrate Zoology, and the Museum of Natural History, University of
Kansas.

The primary study and collecting sites were four and six miles northeast
of Cloudcroft, Otero County, at 8600 to 8800 feet in elevation.
Vegetation was either almost pure stands of Englemann spruce (_Picea
englemanni_) or mixed stands of spruce, Douglas fir (_Pseudotsuga
taxifolia_) and white fir (_Abies_ sp.). At each locality small oaks
(_Quercus_) were present among the dominant conifers. Most of the
salamanders found were in downed Douglas fir logs; some were taken from
spruce and others from cracks in a variety of deadwood. In the less
deteriorated logs the salamanders lived under the loose bark or in small
cracks and chambers near the inner bark surface. In large fir logs in
advanced stages of decomposition, salamanders could be found to the
very centers. This kind of log was apparently highly favorable for
salamanders, for it was in such sites that we found notably large
numbers of the animals and most of the clutches of eggs that we
collected; this kind of log is not frequently found, for its wood is
saturated with water and completely punky and nearly ready for final
collapse.

In winter, salamanders that spent the summer at the surface presumably
move to subterranean cavities, or, at least, to sites away from winter
freezing. In December, 1957, and April, 1958, four feet of snow covered
our collecting sites, and the downed logs contained ice. A few logs were
wet at the surfaces where sunlight hit them, but just under such melt
they were icy. On May 3, 1958, snow was in isolated drifts and the
centers of the logs were still icy. On May 31, and June 22, 1958, there
was no ice anywhere, but no salamanders were evident. Late June is,
however, around the earliest time that _A. hardii_ emerges (Taylor,
1941).


Food and Foraging Behavior

We identified the contents of stomachs from 16 salamanders collected in
1956 and 1957; the items found in them are listed in Table 1. It is not
likely that this list is complete for prey species because _A. hardii_
eats a variety of food and probably takes prey almost indiscriminately
if it is of appropriate size. The kind of food most frequently eaten
was ants; they comprised almost 40 per cent of the total items.
Nevertheless, less than half the stomachs contained ants; this may mean
that salamanders do not make an effort to take ants over any other prey.
Such foraging behavior would result in random capture of ants, and it is
noteworthy that the frequency distribution of ants in stomachs suggests
a Poisson distribution, a mathematical description of one kind of random
distribution.

Table 1.--Numbers of Food Items Found in Stomachs of 16 Specimens
of Aneides hardii

=================================+==========+===========+=============
                                 |          | Percentage| Number of
                                 |Individual| of total  | stomachs in
          Items                  |animals   |  (154)    | which found
                                 |          |individuals|
---------------------------------|----------|-----------|-------------
Mollusca                         |          |           |
  _Pupilla muscorum_ }           |          |           |
  _Gastrocapta_ sp.  }           |     3    |    1.9% } |       4
  _Vallonia pulchella?_          |     4    |    2.5  } |
                                 |          |           |
Arthropoda                       |          |           |
   Arachnoida                    |          |           |
      Arachnida                  |    15    |    9.7    |       9
      Acarina                    |    13    |    8.4    |       3
                                 |          |           |
   Insecta                       |          |           |
      Orthoptera (_Ceuthophilus_)|     2    |    1.3    |       2
      Hemiptera                  |     1    |    0.6    |       1
      Coleoptera                 |          |           |
         adults (carabids and    |          |           |
            buprestids)          |     8 }  |   30.9    |       7
         larvae                  |    38 }  |           |
                                 |          |           |
      Hymenoptera                |          |           |
         ants                    |    62    |   40.2    |       7
         wasps                   |     2    |    1.3    |       2
                                 |          |           |
   Unidentified                  |     5    |    3.2    |       5
                                 +----------+-----------+-------------
             Total               |   154    |  100.0    |
---------------------------------+----------+-----------+-------------

Adult and larval beetles comprised about 28 per cent of the total items,
but were found in only seven of the stomachs. Beetles eaten were small
representatives of beetle groups likely to occur in or under logs. A
relatively large species of spider was found in nine stomachs; it
represented only ten per cent of the items taken but was one of the most
important foods when mass is considered.

Two adult salamanders not included in Table 1 were found, in the course
of examination for parasites, to have empty stomachs. One was a male,
and the other was a female taken from a chamber that held an egg
cluster. It would not be surprising regularly to find stomachs empty in
"incubating" females, but the fact is that the one other such female
collected by us had a small amount of food in the gut; probably these
individuals take anything that enters the egg chamber, but do not leave
for active pursuit of food.

Foraging behavior of captive salamanders was observed by one of us. The
salamanders were maintained in a seven-gallon aquarium, the floor of
which was covered with soil, mosses, liverworts, certain flowering
plants, and pieces of rotten fir log. The salamanders were placed in
the terrarium in September, 1956, July, 1957, and October, 1958; one
individual lived 13 months, another 14 months.

A variety of natural foods was present in the soil and plant matter
placed in the terrarium, and these were presumably eaten as found by the
salamanders. However, the great bulk of the food used by the salamanders
was introduced for them, in the form of colonies of _Drosophila
melanogaster_ in half-pint milk bottles. We tried to keep thriving
colonies of flies, primarily of the mutant vestigial-winged type,
present in the terrarium; in 1957 this was successful to the extent that
there appeared to be a surplus of food available at all times. We did
not attempt to feed the salamanders any wholly artificial food, such as
ground beef.

Initially, the salamanders, although seemingly healthy and well-fed,
were not fat. Those that we maintained on a presumably minimal diet
remained slender and did not grow in length. Two individuals captured
in 1957, however, were maintained on food in excess, and these grew in
length and in girth; from an initial size of about 37 mm. snout-vent
length (a subadult size) they attained about 45 mm. snout-vent length
(an adult size) in a period of five months. The observations on foraging
behavior were made primarily on these latter individuals.

The salamanders captured prey by pursuit. A salamander would pursue a
fly until it was caught, or until it moved out of the field of action.
The salamanders were attracted by movements of flies, and ignored those
that were completely quiet; predation was oriented almost wholly on a
visual basis. Once they were within 2 to 4 mm. of a fly they would snap
out the tongue to secure the fly; they were successful in capturing
vestigial-winged flies in about 75 per cent of all tries. The relative
success of capture was greater when the animals were fresh from the
field and less after they had become fattened. The vigor of their
pursuit also decreased noticeably once they became fat. About two days
after any new fly colony was placed in the terrarium, a salamander would
take up a position just inside the lip of the milk bottle, which was
placed on its side. From this vantage point the salamanders took heavy
toll of the fly populations, eating both adults and larvae.

Initially the salamanders foraged indiscriminately in daylight or in
darkness. Later, as they became fat, they avoided high light intensity
and were active only at night or under artificial light of low
intensity. The latter pattern of activity is probably typical of the
pattern they maintain under natural conditions. Certainly we never saw
individuals abroad in daylight at Cloudcroft, yet under favorable
environmental conditions they were to be found in sites that required
considerable movement over open areas of the ground surface.

For several months two individuals of _Eurycea longicauda_ were kept in
with _A. hardii_. Foraging of these two plethodontids is nearly
identical, but the tongue of an adult _Eurycea_ can be extended somewhat
more than one-half inch in capturing flies; for _A. hardii_ this
distance is usually less than one-quarter inch. The relatively short
tongue of _A. hardii_ can be correlated with its life in restricted,
subsurface chambers, where prey most frequently is close to salamanders;
_E. longicauda_ inhabits significantly more open sites.


Parasites

Thirty of the adult _Aneides_ collected were examined for parasites;
most were parasitized by two species of nematodes, _Oswaldocruzia_ sp.
and _Thelandros_ sp. The former is found in the anterior part of the
small intestine and occasionally in the stomach, and the latter occurs
in the rectum. There were no gross intestinal pathological changes in
the salamanders resulting from parasitism. In fact, no pathological or
structural abnormalities were noted in any of the salamanders examined.
We believe the two nematodes are well-tolerated by the salamander.

Table 2.--Occurrence of Parasitic Nematodes in Aneides hardii

=========================+=============+==============+===================
                         |             |              |
                         |             |  Number of   |   Per cent of
                         |             |  nematodes   |  nematodes that
                         | Per cent of |   per host   |  were immature
                         | salamanders +-------+------+-------+-----------
                         |  infected   |       |      |       |
                         |             | range | mean | July  | Aug.-Sept.
-------------------------+-------------+-------+------+-------+-----------
                         |             |       |      |       |
_Oswaldocruzia_ sp.      |      83     |  2-15 |  3.6 | 100   |    20
                         |             |       |      |       |
_Thelandros_ sp.         |      90     |  1-17 |  3.3 |  64.6 |     5.7
-------------------------+-------------+-------+------+-------+-----------

The numerical and temporal occurrence of the nematodes is summarized in
Table 2. It should be noted that of the 17 worms constituting the
maximum infection by _Thelandros_, only one was an adult worm; the
maximum number of adult _Thelandros_ in any one host was five.
Similarly, the heaviest _Oswaldocruzia_ infection, 15 worms, consisted
of immature individuals; the maximum number of adult worms in any one
host was ten.

The monthly variation in the relative occurrence of young stages
_versus_ adult in both nematodes (Table 2) suggests that the parasites
are eliminated from hosts sometime in the long period, late September
to early June, when _A. hardii_ exists subterraneously; the worms thus
would be reacquired annually when the salamanders resumed living on the
"surface" or near the surface. Table 2 shows that the majority of the
worms are immature (100 per cent, in _Oswaldocruzia_) in samples taken
in July. Additionally, all but one individual of those constituting the
20 per cent occurring as immature _Oswaldocruzia_ in the period August
to September were actually collected in early August. These were found
in one salamander, and this constituted the heaviest infection for the
period; crowding effects may have led to retardation of development of
the worms.

If it is true that parasites are reacquired each spring--we assume that
no temperature factors or immune reactions are delaying development of
the worms, and no unusually long external ovic or free-living phase is a
necessary part of their life-history--then the host-parasite data can
be used as a basis for hypothesizing about the winter life of the
salamander. During "surface" life the incidence of parasitism is high
(90 per cent and 83 per cent: see Table 2), indicating that salamanders
are readily invaded in times of activity. Salamanders examined in
September were all parasitized and probably carried nematodes with
them into their winter retreats. This part of their habitat should thus
be contaminated with infective stages of both parasites. Yet the
salamanders seem to become re-infected when the period of summer
activity starts (note the high incidence of immature parasites in
salamanders taken in July); therefore, the salamanders lose their worms
in winter. This suggests that during their subterranean life salamanders
are inactive, and avoid ingestion of infective stages of the parasites.
A fairly complete hibernation such as we suppose they undergo has been
reported by Szymanski (1914) for _Salamandra_ on the basis of
kymographic records of movement.


Characteristics of Breeding


_Sex-ratio_

Tables 3 and 4 show the distribution of sexes for two subsections of
our sample. The ratio of males to females in the total sample was
nearly 1:1. There were differences in ratios between the three general
localities: the two northerly sites had fewer females than males, when
compared with the Cloudcroft samples. This is true for the samples of
adults, but not for the juveniles, where in each instance the females
predominated. We cannot absolutely explain these differences in ratios.
Possibly the data on adults reflect different patterns of activity among
the sexes so that adult females are simply not present in numbers where
we looked for them. They could be located underground, in connection
with "incubating" duties; if this is true it would account for the fact
that so few egg-clusters have been found in logs.

Table 3.--Sex Ratios in Aneides hardii, Total Sample

===================================================
                     | Number | Number  | Ratio of
      Locality       |   of   |   of    | males to
                     |  males | females | females
---------------------+--------+---------+----------
Capitan Mountains    |   35   |    31   |  100:87
Sierra Blanca        |   28   |    21   |  100:75
Sacramentos, 1958    |   23   |    20   |  100:121
Sacramentos, '56-'57 |   34   |    43   |  100:126
                     +--------+---------+----------
    All              |  120   |   123   |    1:1
---------------------+--------+---------+----------

Table 4.--Sex Ratios in Aneides hardii, Adults

===================================================
                     | Number | Number  | Ratio of
      Locality       |   of   |   of    | males to
                     |  males | females | females
---------------------+--------+---------+----------
Capitan Mountains    |   35   |    19   |  100:54
Sierra Blanca        |   22   |     7   |  100:32
Sacramentos, 1958    |   15   |    14   |  100:93
Sacramentos, '56-'57 |   22   |    16   |  100:73
---------------------+--------+---------+----------


_Age-ratio_

The data in Table 5 show adult salamanders to outnumber young at each
collecting locality. This is probably not an accurate reflection of
actual age composition in this species. Yet, we obtained the same
general result in all three years of the study. We assume, therefore,
that young were located where we could not catch many of them; probably
they were underground. Sites of hatching and of the activities of early
life would thus occur where we think the bulk of eggs are laid.

Table 5.--Age Ratios, Adults-juveniles

======================================================
                     | Number |  Number   | Ratio of
      Locality       |   of   |    of     | adults to
                     | adults | juveniles | juveniles
---------------------+--------+-----------+----------
Capitan Mountains    |   57   |     15    |  100:26
Sierra Blanca        |   30   |     22    |  100:73
Sacramentos, 1958    |   42   |     30    |  100:71
Sacramentos, '56-'57 |   46   |     35    |  100:76
                     +--------+-----------+----------
    All              |  175   |    102    |  100:58
---------------------+--------+-----------+----------

For purposes of this study we had only to age the individuals into adult
and subadult classes. The criterion for adult status was breeding
capability. A five-millimeter testis was the smallest size found in
individuals that probably bred, and all of these were 40 mm. or more in
snout-vent length. We arbitrarily considered individuals smaller than 40
mm. to be subadult. This probably does injustice to reality (females
were treated the same way), but it should be noted that any error
introduced in this way was almost certain to have increased the number
of "subadults" in the samples. Thus, the hypothesis above based on
age-ratios is not automatically invalid because of improper aging.


_Timing of the breeding season_

The time in which egg-clusters are deposited is a good rough index to
events in the breeding cycle. We found four egg-clusters, one on July
14, 1957, and three on July 27, 1957; the only other eggs taken to date
were found in late August (Lowe, 1950:94). Thus, courtship could occur
in June, oviposition in July and August, and hatching from August to
September. Actually, it is likely that the season is more restricted in
time for any one year. Lowe's find was made in a year in which the
summer rains were late, beginning in late July (Stebbins, 1951:137),
whereas ours were made in a year having abundant and relatively early
rainfall, beginning in late June. Microclimatic humidity is of extreme
importance to both the salamanders and their food.

We suppose a great deal of breeding activity takes place underground;
the chronology of events in such sites may bear no close relationship to
those occurring at the surface, yet it is likely that a close parallel
would be found. Breeding activities are ordinarily associated in time
with greatest food abundance.


_Clutch-size_

By clutch-size we refer to the number of eggs in laid clusters. We
collected clutches of six, four, four and one; adding one more of three
(Lowe, _op. cit._) gives an average of 3.6 eggs per cluster; the average
is 4.2 eggs if our clutch of one is discarded on the grounds it was
incomplete.

For comparison we have listed (Table 6) clutch-sizes for some other
plethodontids. It should be noted that these numbers refer only to eggs
deposited in clusters, and not to large ovarian eggs. Thus, _Aneides
hardii_ has the lowest range in clutch-size of any North American
plethodontid on record. It has been noted in other species that low
clutch-size is correlated with low productivity, slow population
turnover, and long average life-expectancy (Lack, 1954:103-105; Pitelka
and Johnston, MS). If this is the case with this salamander, several
other features in its environment and habits would tend to reinforce
such population structure: the animals are exceedingly well-concealed
(they were first described only 17 years ago [Taylor, 1941]), apparently
have few natural enemies (one garter snake [_Thamnophis_] was collected
within the habitat of the salamander in three years), apparently have
few and benign parasites, and abundant and readily available food.

Table 6.--Ranges and Mean Values of Clutch-sizes in Salamanders of
the North American Plethodontidae[1]

==========================================
                           | Range | Mean
---------------------------+-------+------
_Desmognathus_ spp.[2]     | 11-40 | 20
_Leurognathus marmorata_   |  28   |
_Plethodon cinereus_       |  3-13 |  9
_Plethodon_ spp.           |  8-18 | 13
_Ensatina eschscholtzii_   | 12-14 | 13
_Hemidactylium scutatum_   |  30   |
_Batrachoseps_ spp.        |  7-74 |
_Aneides hardii_[3]        |  1-6  |  3.6
_Aneides_ spp.             |  7-19 | 13
_Stereochilus marginatus_  |       | 57
_Pseudotriton ruber_       |  72   |
_Manculus quadridigitatus_ |  3-48 |
---------------------------+-------+------

[1] From Bishop (1947) and Stebbins (1951).

[2] Clusters of one and two occasionally found in _D. ochrophaeus_.

[3] This study, and from Lowe (1950).


_Eggs and "incubation"_

Our information concerning eggs essentially duplicates that already
reported (see Stebbins, 1951). All egg clusters that we found were in
small chambers within decomposing fir logs. In each instance the eggs
were suspended from the roofs of the chambers. The clutch of six eggs
was a compact mass, and the individual suspensory cables of the eggs
were intertwined and fused with one another. The clutches of four eggs,
although they too were compact clusters, had each suspensory pedicel
distinct from the others. The surface of the eggs was lightly moist, but
did not glisten with water, and each egg was completely free of the
others. The outer coat of jelly of the fresh eggs measured about 6.4 by
5.7 mm. as they hung suspended; sizes were uniform and no egg was
notably smaller or larger than the others.

We attempted to keep eggs artificially, but mold destroyed them after 12
days. We had difficulty keeping them wet without inundating them, for
the climate at Las Cruces, New Mexico, where we kept the eggs, is
exceedingly dry in summer. Until death, embryos were active and
responsive to disturbances around them. This was at a time when the limb
buds could not be detected and when the external gills were evident only
under close scrutiny.

Two times we found adult female salamanders in the chambers with the egg
clusters. The other two egg clutches seemingly had no attendant adult,
but our method of going through a log was such that we could easily have
alarmed any attendant animal well before we found the eggs, allowing
time for the adult to move away from the eggs. We presume that
incubation, so-called, in _A. hardii_ is similar to that found in other
plethodontids (see, for example, Gordon, 1952:683). Our findings on the
conditions of the stomachs of these attendant adults have been outlined
above ("Food and Foraging"). Our limited data suggest that only females
are found in chambers with eggs.


Summary

The montane relict plethodontid _Aneides hardii_ was studied in the
field and laboratory in 1956-1958. Food items detected in a small sample
of stomachs are listed tabularly. Two roundworms were found to
parasitize the guts of the salamanders; the parasitism looks to be
benign. Subterranean winter inactivity is thought to be an integral part
of the salamanders' lives, and is suggested in part by the life cycles
of the worms. Summer activity appears to occur at the ground surface in
logs and talus, and underground; the latter site is suggested by certain
ratios obtained in the samples, showing adults to outnumber young and
males to outnumber females. The season for egg deposition seems to be in
July and August. Clutch-size is lower than for any other plethodontid on
record. "Incubation" of eggs apparently parallels that characteristic of
other plethodontids.


Literature Cited

Bishop, S. C.
  1947. Handbook of salamanders. Ithaca, Comstock. xiv + 555 pp.

Gordon, R. E.
  1952. A contribution to the life history and ecology of the plethodontid
    salamander _Aneides aeneus_ (Cope and Packard). Amer. Midl. Nat.,
    47:666-701.

Lack, D.
  1954. The natural regulation of animal numbers. Oxford, Clarendon,
    viii + 343 pp.

Lowe, C. H., Jr.
  1950. The systematic status of the salamander _Plethodon hardii_, with
    a discussion of biogeographic problems in _Aneides_. Copeia,
    1950(2):92-99.

Stebbins, R. C.
  1951. Amphibians of western North America. Berkeley, Univ. Calif,
    xviii + 539 pp.

Szymanski, J. S.
  1914. Eine Methode zur Untersuchung der Ruhe- und Aktivitätsperioden
    bei Tieren. Arch. ges. Physiol., 158:343-385.

Taylor, E. H.
  1941. A new plethodont salamander from New Mexico. Proc. Biol. Soc.
    Wash., 54:77-79.


_Transmitted May 11, 1959._

27-9040



Transcriber's Notes:

Changed "vestigal" to "vestigial" on page 578: vestigal-winged flies.

Changed "inmature" to "immature" in Table 2: nematodes that were inmature.

Changed "auomatically" to "automatically" on page 582: not auomatically
invalid.

Changed "Syzmanski" to "Szymanski" in Literature Cited on page 585.





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